Growth and survival of hatchling saltwater crocodiles
(Crocodylus porosus) in captivity: the role of agonistic
and thermal behaviour
Matthew Lindsay Brien
BSc. Hons. (University of Queensland)
Submitted in fulfilment of the requirements for the degree of Doctor of
Philosophy
Research Institute for the Environment and Livelihoods
Charles Darwin University
March 2015
ii
Hatchling saltwater crocodile (Crocodylus porosus) emerges from egg (photo credit:
Jemeema Brien).
iii
Declaration
This work contains no material which has been accepted for the award of any other
degree or diploma in any university or other tertiary institution and, to the best of my
knowledge and belief, contains no material previously published or written by another
person, except where due reference has been made in the text.
I give consent to this copy of my thesis, when deposited in the University Library,
being made available for loan and photocopying online via the University’s Open
Access repository eSpace.
Matthew L Brien
September 2014
iv
Acknowledgements
First and foremost, I would like to thank my wife, Jemeema, and my family for their
amazing love, support, and understanding throughout the last few years. It is a rare
and amazing thing to have a partner that not only shares the same love and passion for
all things scaly, but has also willingly been by my side in the bug infested swamps
and marshes all over the world for the best part of 10 years. Her knowledge and
understanding of crocodiles, and in particular hatchling saltwater crocodiles, has been
invaluable during this research. I have been very fortunate to also have a family that,
even though they may find it hard at times to comprehend what it is I do, why, and for
such little money, they have always supported me unconditionally in pursuit of my
dreams. My Nan died shortly before I finished my thesis, but I know she was proud.
This research would not have been possible without the logistical, technical, financial,
and intellectual support of Grahame Webb and Charlie Manolis through Wildlife
Management International (WMI). I have benefited from their amazing generosity
and support of student research, and have witnessed first hand the vast number of
students throughout the world who they have also helped, often at a financial cost to
WMI. I am greatly appreciative, and it is this generosity and insistence on high quality
research that I will take with me. I am also grateful to all WMI staff that have assisted
and supported with the research in various capacities over the years. These include
John Pomeroy, Steve Coulson, Dave Ottway, Tate Chambers, and the many hatchery
staff: Sally Sibley, Tanya Bradley, Jodi Cox, Sharon Harlock, and Olivia Plume. My
supervisors have been a great source of knowledge, guidance, and support throughout,
and have been incredibly generous with their time and efforts. To me they have been
v
the perfect balance of the practical and dependable (Keith Christian), innovative and
inspiring (Grahame Webb), statistical and clinical (Keith McGuinness), and the
crocodile behavioural guru (Jeff Lang). It has been a privilege and an honour to work
with all four. However, I am fortunate to have had someone like Keith (Christian) as
my primary supervisor. His calm and composed nature often belies his brilliance, and
he has been a great source of guidance, balance and support throughout. I would like
to make special mention of Chris Gienger, who as a recently graduated PhD student
and post-doctoral at Charles Darwin University, provided critical mentorship,
guidance and advice early on that I am indebted to. I would also like to thank the two
Dutch veterinary students, Elize and Evelyn, for their help, and Steve Garnett for
advice and guidance early on. Cathy Shilton from Berrimah Veterinary labs is
brilliant, and I enjoyed working with her on the Valium and Tryptophan chapter.
Funding through WMI from the Rural Industries Research and Development
Corporation is gratefully acknowledged, as is the funding provided through
Holsworth Wildlife Research Endowment (ANZ Trustees Foundation), Northern
Territory Research and Innovation Board student grants, IUCN Crocodile Specialist
Group student grant, and Charles Darwin University student grants. Last but not least,
I will be forever grateful to the object of my passion and inspiration, the crocodile.
But for crocodiles, I would never have considered myself capable of doing Honours,
much less a PhD.
vi
Abstract
Agonistic and thermal behaviour was studied in hatchling Crocodylus porosus under
captive conditions using CCTV cameras. The results guided the design of experiments
aimed at improving growth and survival of this species in captivity. C. porosus are
born with a repertoire of 16 distinctive agonistic behaviours, and most interactions
occur in the morning and evening in open, shallow water. There are clutch-specific
differences in the frequency of agonistic interactions, and older hatchlings display
fewer behaviours based on dominance status. A comparison of eight crocodilian
species revealed differences in behaviours displayed and the level of conspecific
tolerance, with C. porosus being the most aggressive. Hatchling C. porosus preferred
body temperatures (Tbs) between 29.4ºC and 32.6ºC, and the mean (30.9±2.3ºC SD)
was not influenced by social situation or feeding status. During the day, hatchlings
had higher Tbs and were less active than at night. Growth of C. porosus during the
first 24 days can be used to predict ‘failure to thrive’ (FTT) affliction up to 300 days.
Hatchlings fed short chopped meat had higher growth than those fed standard mince
or long chopped meat. Although visual barriers and deeper water reduced agonistic
behaviour among hatchlings, these factors did not result in improved growth.
Hatchling growth was highest at a density of 6.7/m2, and was lower at higher
densities. The frequency of agonistic interactions was higher at lower densities
(3.3/m2; 6.7/m
2) than at higher densities (13.3/m
2; 20.0/m
2). Although hatchlings
given Valium in their food had fewer agonistic interactions, they had reduced growth.
Hatchlings raised under constant warm temperatures (32-34ºC), a gradient of
temperatures, or warmer night time temperatures had higher growth than hatchlings
vii
with warm temperatures during the day only. Hatchlings afflicted with FTT and
placed in a semi-natural enclosure had almost double the growth of those in standard
raising pens.
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Publications arising from this Thesis
Each chapter has been formatted as a journal article, so there is a lot of repetition
throughout the thesis. Sections of the thesis that were published in peer reviewed
journals during the candidature (2.1, 3.1, 3.2, 3.3, 4.1, and 5.1) are formatted
according to the journal’s specifications. For each published manuscript, supervisors
were included as co-authors. Chris Gienger was also a co-author on two papers (2.1,
5.1). All co-authors consented to the publication of these manuscripts in each of the
journals, as well as in this thesis. Chapters that had not been submitted for publication
prior to the submission of this thesis are formatted in the same way.
List of publications:
Brien, M.L., Webb, G.J., Gienger, C.M., Lang, J.W., Christian, K.A., 2012.
Thermal preferences of hatchling saltwater crocodiles (Crocodylus porosus) in
response to time of day, social aggregation and feeding. Journal of Thermal Biology
37, 625–630.
(Chapter 4.)
Brien, M.L., Webb, G.J., Lang, J.W., McGuinness, K.A., Christian, K.A., 2013.
Born to be bad: agonistic behaviour in hatchling saltwater crocodiles (Crocodylus
porosus). Behaviour 150: 737–762.
(Chapter 3.1)
ix
Brien, M.L., Webb, G.J., Lang, J.W., McGuinness, K.A., Christian, K.A. 2013.
Intra- and interspecific agonistic behaviour in hatchling Australian freshwater
crocodiles (Crocodylus johnstoni) and saltwater crocodiles (Crocodylus porosus).
Australian Journal of Zoology 61: 196-205. Won ‘Best Student Paper Award 2013’
with the Australian Journal of Zoology.
(Chapter 3.2)
Brien, M.L., Lang, J.W., Webb, G.W., Stevenson, C., Christian, K.A. 2013. The
good, the bad, and the ugly: agonistic behaviour in juvenile crocodilians. PloS one
8: DOI: 10.1371/journal.pone.0080872.
(Chapter 3.3)
Brien, M.L., Webb, G.J., McGuinness, K.A., Christian, K.A. 2014. The relationship
between early growth and survival of hatchling saltwater crocodiles (Crocodylus
porosus) in captivity. PloS ONE 9: e100276. doi:10.1371/journal.pone.0100276.
(Chapter 2.1)
Brien, M.L., Gienger, C.M., Webb, G.J., McGuinness, K.A., Christian, K.A., 2014.
Out of sight or in too deep: effect of visual barriers and water depth on agonistic
behaviour and growth in hatchling saltwater crocodiles (Crocodylus porosus).
Applied Animal Behaviour Science – in press.
(Chapter 5.1)
In each publication, Grahame Webb and Keith Christian were primarily involved in
x
developing study design and methodology, as well as reviewing early drafts of the
manuscript. Keith McGuinness reviewed experimental design, provided statistical
advice and ran some of the analyses, and also reviewed early drafts. Jeff Lang and
Chris Gienger provided advice on study design and reviewed early drafts of the
manuscripts that they co-authored.
xi
Table of Contents
CHAPTER 1. GENERAL INTRODUCTION ....................................... 1
Conservation and management of C. porosus ...................................................................................... 1
Survivorship and population dynamics of C. porosus ......................................................................... 2
Crocodylus porosus in the Northern Territory ..................................................................................... 9
Failure to thrive syndrome .................................................................................................................. 10
Addressing FTT: factors that may influence growth and survivorship of hatchling C. porosus ... 14
Limitations of previous research ......................................................................................................... 20
Intended aims and goals of this thesis ................................................................................................. 22
Literature Cited .................................................................................................................................... 24
CHAPTER 2. THE RELATIONSHIP BETWEEN EARLY
GROWTH AND SURVIVAL OF HATCHLING SALTWATER
CROCODILES (CROCODYLUS POROSUS) IN CAPTIVITY ......... 39
Abstract ................................................................................................................................................. 39
Introduction .......................................................................................................................................... 40
Materials and Methods ........................................................................................................................ 42
Results ................................................................................................................................................... 47
Discussion .............................................................................................................................................. 61
Acknowledgements ............................................................................................................................... 65
References ............................................................................................................................................. 66
CHAPTER 3.1. BORN TO BE BAD: AGONISTIC BEHAVIOUR IN
HATCHLING SALTWATER CROCODILES (CROCODYLUS
POROSUS) ............................................................................................... 79
Summary ............................................................................................................................................... 79
Introduction .......................................................................................................................................... 80
Materials and methods ......................................................................................................................... 83
Results ................................................................................................................................................... 89
Discussion ............................................................................................................................................ 100
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Acknowledgements ............................................................................................................................. 108
References ........................................................................................................................................... 108
CHAPTER 3.2. INTRA- AND INTERSPECIFIC AGONISTIC
BEHAVIOUR IN HATCHLING AUSTRALIAN FRESHWATER
CROCODILES (CROCODYLUS JOHNSTONI) AND SALTWATER
CROCODILES (CROCODYLUS POROSUS) .................................... 119
Abstract ............................................................................................................................................... 119
Introduction ........................................................................................................................................ 120
Materials and methods ....................................................................................................................... 122
Results ................................................................................................................................................. 127
Discussion ............................................................................................................................................ 138
Acknowledgements ............................................................................................................................. 147
References ........................................................................................................................................... 148
CHAPTER 3.3. THE GOOD, THE BAD, AND THE UGLY:
AGONISTIC BEHAVIOUR IN JUVENILE CROCODILIANS .... 157
Abstract ............................................................................................................................................... 157
Introduction ........................................................................................................................................ 158
Materials and Methods ...................................................................................................................... 160
Results ................................................................................................................................................. 168
Discussion ............................................................................................................................................ 190
Acknowledgements ............................................................................................................................. 204
References ........................................................................................................................................... 205
CHAPTER 4. THERMAL PREFERENCES OF HATCHLING
SALTWATER CROCODILES (CROCODYLUS POROSUS) IN
RESPONSE TO TIME OF DAY, SOCIAL AGGREGATION AND
FEEDING .............................................................................................. 217
Abstract ............................................................................................................................................... 217
1. Introduction .................................................................................................................................... 218
2. Materials and Methods .................................................................................................................. 221
3. Results ............................................................................................................................................. 225
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4. Discussion ........................................................................................................................................ 233
Acknowledgements ............................................................................................................................. 237
References ........................................................................................................................................... 238
CHAPTER 5.1. OUT OF SIGHT OR IN TOO DEEP: EFFECT OF
VISUAL BARRIERS AND WATER DEPTH ON AGONISTIC
BEHAVIOUR AND GROWTH IN HATCHLING SALTWATER
CROCODILES (CROCODYLUS POROSUS) .................................... 246
Abstract ............................................................................................................................................... 246
1. Introduction .................................................................................................................................... 247
2. Animals, materials, and methods .................................................................................................. 250
3. Results ............................................................................................................................................. 257
4. Discussion ........................................................................................................................................ 260
5. Conclusion ....................................................................................................................................... 263
Acknowledgements ............................................................................................................................. 263
References ........................................................................................................................................... 264
CHAPTER 5.2. EFFECT OF DENSITY ON GROWTH,
AGONISTIC BEHAVIOUR, AND ACTIVITY IN HATCHLING
SALTWATER CROCODILES (CROCODYLUS POROSUS) ......... 268
Abstract ............................................................................................................................................... 268
Introduction ........................................................................................................................................ 269
Methods ............................................................................................................................................... 271
Results ................................................................................................................................................. 275
Discussion ............................................................................................................................................ 282
Acknowledgements ............................................................................................................................. 288
Literature Cited .................................................................................................................................. 289
CHAPTER 5.3. FACTORS AFFECTING INITIAL GROWTH
RATES OF CAPTIVE SALTWATER CROCODILES
(CROCODYLUS POROSUS) HATCHLINGS IN CAPTIVITY:
FOOD FORM AND TEMPERATURE CYCLE ............................... 298
Abstract ............................................................................................................................................... 298
xiv
Introduction ........................................................................................................................................ 299
Methods ............................................................................................................................................... 302
Results ................................................................................................................................................. 307
Discussion ............................................................................................................................................ 313
Acknowledgements ............................................................................................................................. 317
Literature Cited .................................................................................................................................. 317
CHAPTER 5.4. USE OF DIAZEPAM AND TRYPTOPHAN TO
REDUCE STRESS AND INCREASE GROWTH AND SURVIVAL
OF HATCHLING SALTWATER CROCODILES (CROCODYLUS
POROSUS) IN CAPTIVITY ................................................................ 327
Abstract ............................................................................................................................................... 327
Introduction ........................................................................................................................................ 328
Methods ............................................................................................................................................... 330
Results ................................................................................................................................................. 335
Discussion ............................................................................................................................................ 341
Acknowledgements ............................................................................................................................. 344
Literature Cited .................................................................................................................................. 345
CHAPTER 6. IMPROVING GROWTH AND SURVIVAL IN
HATCHLING C. POROSUS: SUMMARY, OUTDOOR
ENCLOSURES, AND CONCLUSIONS ............................................ 352
Agonistic behaviour ............................................................................................................................ 352
Thermal behaviour ............................................................................................................................. 354
Growth and survival........................................................................................................................... 355
Understanding agonistic behaviour .................................................................................................. 356
Optimal thermal regime ..................................................................................................................... 358
The raising environment: a case study ............................................................................................. 359
Methods ............................................................................................................................................... 360
Results ................................................................................................................................................. 362
Discussion ............................................................................................................................................ 366
Conclusions and Recommendations .................................................................................................. 368
xv
Acknowledgements ............................................................................................................................. 369
Literature Cited .................................................................................................................................. 369
1
Chapter 1. General Introduction
Conservation and management of C. porosus
Saltwater crocodiles (Crocodylus porosus) are one of the largest and most widely
distributed of living crocodilians, ranging from Sri Lanka and India in the north-west,
across south-east Asia to the Phillipines and some Pacific Islands in the north east,
and down through Indonesia, Papua New Guinea and Australia to the south (Ross
1998; Webb et al. 2010). The skins of C. porosus are also the most commercially
valuable of any of the 23 species of extant crocodilians, because they have relatively
small scales and no osteoderms in the scales of the ventral skin, the ‘belly’ skin,
which is the most prized for high quality fashion leather (Webb and Manolis 1989;
Fuchs 2006).
Historically (<1960s), all wild C. porosus populations were greatly reduced through
eradication as pests, particularly as predators on people and livestock, loss of habitat
and through hunting for skins (Ross 1998; Webb et al. 2010). Throughout much of the
former range of C. porosus, wild populations are either highly depleted, extinct, or
represented by small remnants in some protected areas (Ross 1998; Webb et al. 2010).
In contrast, countries such as Australia, Brunei, Papua New Guinea, Sarawak, Sabah,
and the Solomon Islands have implemented successful management programs to
encourage wild populations to recover (Webb et al. 2010).
National priorities with C. porosus since the 1960’s have varied from country to
2
country (Ross 1998). However, it has proven virtually impossible to rebuild wild
populations of C. porosus in areas with high density human populations that are
vulnerable to crocodile attacks because people use rivers and wetlands continually
(Ross 1998; Webb et al. 2010).
Crocodile farms and ranches are intimately linked to the success of programs in parts
of Australia, Indonesia and Papua New Guinea, where the commercial benefits
derived from using wild C. porosus populations, provide incentives for people to
tolerate large and expanding wild populations of C. porosus (Hutton and Webb 1992;
Webb et al. 2010). Underlying such programs are various assumptions concerning
how the population dynamics of wild C. porosus populations will respond to
interventions (Webb and Smith 1987).
Survivorship and population dynamics of C. porosus
The balance of population dynamics that determine whether a population increases,
decreases, or remains stable is dependent on rates of reproduction, mortality,
immigration and emigration (Hutchinson 1978). The same is true in captive
populations, but here the parameters are largely controlled to get particular outcomes.
The success or failure of both wild and captive populations of C. porous is based on
assumptions about population dynamics, with age-specific survival rates being of
critical importance (Webb and Smith 1987; Hutton and Webb 1992). Indeed, the
whole theoretical basis of ranching programs in Australia, Indonesia and Papua New
3
Guinea is based on assumptions about age-specific survival rates.
Rates of survival are known to vary within and among species and populations
depending on habitat, food, weather, and the size structure of the population (Webb
and Smith 1987). Regardless, survival rates for C. porosus are typically lowest in the
early life stages (eggs and hatchlings), when predators and environmental problems
are greatest, and increase with increasing size and age (Webb et al. 1983). However, if
eggs and juveniles are collected and raised on farms, many of the animals that would
be destined to die in the wild are assumed to have ‘high survival rates’ in captivity
(Webb and Smith 1987; Hutton and Webb 1992). The ecological impact of collecting
eggs and juveniles should thus theoretically be minimal, and if necessary, can be
compensated for by a release back to the wild of some captive raised juveniles (Elsey
et al. 1992).
Eggs
Female C. porosus build mound nests primarily out of vegetation near water, which
they are known to actively and aggressively defend in the wild and in captivity (Webb
et al. 1977; 1983). Egg-laying occurs mainly during the wet season, with low egg
survivorship (as low as 25% in some areas) in the wild due to flooding (Webb et al.
1977). Predation on C. porosus nests, outside of ranching programs, is considered to
be very low (<2%) (Webb et al. 1984; 1987). In captivity, populations of C. porosus
experience high egg survivorship (80-95%) from viable eggs either ranched from the
wild or collected from captive bred stock, and incubated artificially (Hutton and Webb
4
1992).
Previous studies suggest that genetics and the nature of embryonic development are
two of the most important factors determining overall growth and survival of
crocodiles, with differences in the performance of individuals often directly related to
the clutch of origin and the environmental conditions experienced during incubation
(Webb and Cooper-Preston 1989; Deeming and Ferguson 2009). This is referred to as
the ‘clutch affect’, and while this influence can sometimes be physically apparent, in
the form of abnormalities, degree of yolk absorption, sex determination, and size at
hatching, it can also have important physiological and behavioural implications for
survival that are less obvious and still poorly understood (Webb et al. 1987; Webb and
Cooper-Preston 1989; Riese 1991). For example, parameters such as dietary and
thermal preferences, along with social tolerance may already be determined before
hatching (Webb and Cooper-Preston 1989; Sneddon et al. 2000). The ‘clutch’ affect
among hatchling crocodilians is so strong that the results of many studies have been
compromised because they have failed to recognise and adjust for this affect when
designing experiments.
Temperature during incubation is critical in determining the rate of embryonic
development, degree of yolk absorption and size at hatching (Ferguson and Joanen
1982; 1983; Webb et al. 1987). Although the size of an individual at hatching is
determined by the size of the egg (Webb et al. 1983), it is unknown whether larger
body size in hatchling crocodilians is related to increased growth and survival (Webb
and Cooper-Preston 1989) as is the case with a number of other reptiles (Congdon and
5
Gibbons 1985; Sinervo 1990; Stearns 1992; Janzen 1993).
For C. porosus, ideal conditions for artificial incubation are considered to be a
constant 32ºC and 90-95% relative humidity, which result in mostly male (85%)
hatchlings emerging after 80 days (Webb and Cooper-Preston 1989; Richardson et al.
2002). At temperatures higher or lower than 32ºC, the sex ratio will be split between
males and females and overall survival is generally lower (Webb and Cooper-Preston
1989; Whitehead et al. 1989). At higher temperatures (>32ºC), hatchling C. porosus
develop more rapidly and show trends toward neotony, where they hasten
development and tend to hatch with small body size and abundant yolk (Webb and
Cooper-Preston 1989; Whitehead et al. 1989). At lower temperatures (<32ºC)
incubation times are extended, and more of the yolk is used in embryonic growth,
although at very low temperatures (~28ºC), development is so compromised that
internalisation of yolk itself becomes problematic (Webb and Cooper-Preston 1989;
Whitehead et al. 1989). Once hatched, individual C. porosus have higher growth rates
when raised at a temperature similar to that experienced during incubation (Webb and
Cooper-Preston 1989).
Hatchlings
After the female has uncovered the nest and transported the hatchlings to the water,
she usually remains within the vicinity of the clutch anywhere from 1-8 weeks (Webb
et al. 1977; 1983). Whether survival of hatchling C. porosus is dependent upon the
degree of protection provided by the female and if it decreases after the crèche of
6
hatchlings disperses is not known. It is possible that female C. porosus may be
important in keeping the crèche together (Webb et al. 1977; Magnusson 1979) and in
the provisioning of food, as has been demonstrated for other species of crocodilians in
captivity (Whitaker 2007).
In the wild, approximately 54% of hatchling C. porosus successfully survive to one
year, with most mortality through predation (Webb et al. 1987). There are a wide
range of species (bird, fish, crustacean, reptile) reported to consume hatchling C.
porosus and this is considered to be the primary cause of mortality in the wild.
Species that are believed to predate hatchling C. porosus in Australia include goannas
(eg. Varanus indicus), fish (eg. Lates calcarifer, Scleropages leichardti), sharks
(Glyphis spp.), kites (eg. Milvus and Haliastur spp.), sea eagles (Haliaeetus
leucogaster), herons (eg. Nycticorax caledonicus), turtles (eg. Chelonea rugosa),
crabs (Scylla serrata), and larger C. porosus (Messel and Vorlicek 1989; Webb and
Manolis 1998; Somaweera et al. 2013). While it is widely accepted that predation is a
significant cause of mortality among hatchling C. porosus, actual predation events are
rarely seen due to the cryptic and aquatic nature of hatchlings and a number of the
species that prey upon them (Magnusson 1984). In captivity, predation is largely
controlled, and in most cases is non-existent for hatchling C. porosus raised in
appropriate facilities.
For C. porosus, hatchling survivorship to one-year-of-age in the wild is correlated
with the total number of hatchlings in the population (Webb and Manolis 2001).
Lower survival rates have been reported in years when more hatchlings are produced
7
in at least some rivers (Messel et al. 1981; Webb and Manolis 2001). The number of
adults in the population appears to have limited influence on hatchling survivorship,
suggesting cannibalism may be of minor significance with this life stage (Magnusson
1984; Webb and Manolis 2001). However, cannabilism is considered to have a
significant influence on survivorship in several other species of crocodilian (Cott
1961; Staton and Dixon 1975; Rootes and Chabreck 1993; Delaney et al. 2011;
Somaweera et al. 2013). Hatchling survivorship to one year in captivity is
considerably higher, with the majority of mortalities due to runtism or a failure to
thrive (FTT) syndrome (Mayer 1998; Isberg et al. 2009).
Sub-adults
After the first year, crocodiles are larger and the threat of predation is reduced
resulting in higher survivorship (up to 70%) between one and two years of age in the
wild (Webb et al. 1984; 1987). Between two and four years of age, survival depends
on adult density. In wild populations with fewer adults, average survival from 2-4
years is around 66%, while in populations with more adults, survival can be as low as
30% (Messel et al. 1981; Webb et al. 1984; 1987). In comparison, rates of survival
after one year of age in captivity are typically greater than 95% until slaughter at 3-5
years of age (Mayer 1998; Isberg et al. 2009).
In the wild, cannibalism of juveniles between 1 and 2 years of age is highly correlated
with the number of larger crocodiles present (>2m total length), suggesting
cannibalism may become more important with size (Messel et al. 1981; Webb and
8
Manolis 2001). Beyond two years of age, cannibalism and social exclusion (perhaps
linked with lower survival rates) increase in importance (Messel et al. 1981; Webb
and Manolis 2001).
Adults
Adult C. porosus have few predators other than humans and other crocodiles (Messel
et al. 1981; Webb and Manolis 2001). Once individuals reach adulthood survivorship
is generally high, at least for females. However, males are known to kill rivals in
disputes over territories and mates during the breeding season (Webb and Manolis
2001).
Population dynamics
Knowledge of survival rates is thus critical for understanding population dynamics
when trying to predict how a wild population of C. porosus is likely to respond to
management interventions, or explain how they have responded where interventions
have already taken place (Webb and Smith 1987; Hutton and Webb 1992). Survival
rates, particularly amongst hatchlings, are also important for understanding the
dynamics of captive populations of C. porosus on farms and ranches, and the
biological and commercial viability of such enterprises (Webb and Smith 1987;
Hutton and Webb 1992).
9
Crocodylus porosus in the Northern Territory
Although two species of crocodilian occur in northern Australia, C. porosus and the
freshwater crocodile (Crocodylus johnstoni), farming is largely restricted to C.
porosus due to the slow growing nature and smaller size of C. johnstoni, and the
poorer quality skin it produces (Hutton and Webb 1992; Webb et al. 2010). While
farming of C. porosus is restricted to captive breeding in Queensland, the industry in
the Northern Territory and Western Australia is now based on both captive breeding
and a ranching program, in which eggs are collected from the wild and incubated
artificially (Letnic 2004; Webb et al. 2010). Ranched eggs from the Northern
Territory are also used to stock farms in Queensland (Webb et al. 2010).
In the Northern Territory, where severely depleted wild populations of C. porosus
were protected in 1971, the wild populations have now almost fully recovered
(Fukuda et al. 2011). Current management programs for C. porosus allow strictly
controlled commercial use, through both ranching of wild eggs and captive breeding
(Letnic 2004; Webb et al. 2010). Eggs are artificially incubated and the resultant
hatchlings raised on crocodile farms (Letnic 2004; Webb et al. 2010). This program
is one mechanism through which C. porosus have been made economically beneficial
to the people of the Northern Territory, and so between 1971 and 2010 they have
tolerated a 20 times increase in C. porosus abundance and a 100 times increase in C.
porosus biomass (Fukuda et al. 2011).
In commercial captive raising facilities within the Northern Territory, average
10
survival rates of C. porosus between hatching and one-year-of-age are generally
reported to be 80-90% (Isberg et al. 2004; Department of Resources - DoR).
However, this figure is based on self reporting by farms and a mandatory hatchling
audit undertaken by the DoR each year during October-November. As C. porosus
hatch out late December through early July, with the majority between February and
April, this survival rate is for animals ranging between 3-10 months old. A study on
one farm reported that only 51% of hatchlings produced from captive stock survived
to 400 days old (Isberg et al. 2006; 2009). Therefore, the figure of 80-90% annual
survivorship of hatchling C. porosus to one year is considered an overestimate.
Regardless, these survival rates are still significantly lower than the 95-99%
survivorship to one-year-of-age reported for American alligators (Alligator
mississippiensis) hatched in artificial incubators and raised under similar conditions
(Joanen and McNease 1976).
Failure to thrive syndrome
In captive raising facilities for C. porosus, losses due to predation are rarely
encountered. The mortality that does occur appears to be the consequence of a ‘failure
to thrive syndrome (FTT)’ or ‘runtism’ (Mayer 1998; Isberg et al. 2004). For reasons
that are not clear, 15-40% of C. porosus hatchlings eat and grow little relative to
others, including siblings, and become vulnerable to mortality through reduced
immunity to disease and/or voluntary starvation (Onions 1987; Webb et al. 1987;
Mayer 1998; Isberg et al. 2009). These individuals become emaciated and usually die
between 70-200 days, or need to be culled (Huchzermeyer 2003; Isberg et al. 2009).
11
Whether or not wild C. porosus hatchlings are as afflicted by FTT as their captive
raised counterparts is unclear. In the wild, individual growth rates are highly variable
(Webb et al. 1978), yet amongst hatchlings caught or sighted in surveys, FTT or
anorexic animals are rarely reported (Webb pers. com.). However, as hatchlings in the
wild suffering from FTT would be more susceptible to predation, accurately
determining its prevalence would not be possible. Also, hatchlings of other
crocodilians (A. mississippiensis, C. acutus) suffering from FTT have been observed
in the wild.
FTT is the leading cause of hatchling C. porosus mortality up to one year old on
Australian farms each year (Hibberd et al. 1996; Mayer 1998; Isberg et al. 2009).
Total losses attributable to FTT are probably higher, with some animals that suffer
from FTT often surviving until the second year before they either die or need to be
culled due to stunted growth (Isberg et al. 2009). There are no known infectious
diseases that cause FTT, although animals suffering FTT usually succumb to
opportunistic infections due to their compromised state (Isberg et al. 2009).
Although FTT may be more prevalent in the wild than currently accepted, it is
common in captivity, which clearly constrains production efficiency on farms, and
equally important, confounds the ability to test and experiment (Mayer 1998; Isberg et
al. 2009). One consequence of FTT is that the size distribution of hatchlings in
captivity rapidly becomes bimodal which increases variability. A problem
exacerbated by the experimental treatment resulting in the largest hatchlings, also
12
providing the smallest ones (the largest number of animals with FTT).
FTT in captive raised C. porosus may be a product of the raising environment and
raising protocols used for hatchlings (Hutton and Webb 1992; Buenviaje 1994).
Although pens and procedures vary from farm to farm, and are continually being
adapted and modified by crocodile farmers, they all seem to be variants of the same
basic approach to raising based on the same assumptions – the C. porosus raising
paradigm (Hutton and Webb 1992).
The possibility that this raising paradigm, instigated some 30 years ago, is
fundamentally compromised for C. porosus hatchlings cannot be rejected. When
crocodile farming started in Australia, particularly during the 1970’s, survival and
growth rates of hatchlings were problematic (Garnett and Murray 1986; Onions 1987;
Webb et al. 1987; Mayer 1998). The same occurred with Nile crocodiles (Crocodylus
niloticus) when farming started (Hutton and Webb 1992). In both cases, it was
considered that ‘outdoor’ pens would provide a more natural raising environment, and
that problems could be overcome by trial, error, innovation and research in captivity
(Riese 1995; Mayer 1998; Davis 2001)
However, the raising paradigm implemented with American alligators (Alligator
mississippiensis) was based on ‘indoor’ raising in controlled environments
(particularly temperature) and the results in terms of survival and growth rates were
by comparison exceptionally good (Joanen and McNease 1976). This led to a shift
towards controlled environment raising of both C. porosus and C. niloticus, which
13
improved both survival and growth rates (Hutton and Webb 1992). However, with C.
porosus at least, the problem of FTT remained. At that time the possibility of species-
specific traits affecting the ideal raising environment had not been explored. Although
little information exists, substantially higher rates of growth and survival to one year
of age have been reported for A. mississippiensis when raised under identical
conditions to C. porosus (Webb et al. 1994).
In any overview, the raising strategies implemented for C. porosus are the result of
adaptive management: corrected error to corrected error. The starting point was not
based on a sound understanding of how hatchling C. porosus behave, feed, grow,
thermoregulate or function because this information was not available at the time. Nor
did it take into account the possibility that significant species-specific traits may be
involved: technologies that work well with one species may not be automatically
transferable to others.
That FTT is common in captive raised crocodiles suggests that the general raising
environment used for C. porosus may be inadequate (Onions 1987; Hutton and Webb
1992). This crocodilian has long been regarded as a species least tolerant of
conspecifics (Lang 1987), so it seems possible that social behaviour may be
implicated in FTT. The possibility that behavioural ‘bullying’ promotes fast growth
rates in dominant hatchlings, and FTT in sub-dominant ones, has rarely been
considered because social interactions such as this in the first few weeks have not
been reported. Information on hatchling C. porosus in the wild may provide valuable
insights into the causes of FTT and potential options for managing it in captivity.
14
Addressing FTT: factors that may influence growth and survivorship of
hatchling C. porosus
Along with genetics, embryonic development, parental care, and predation, other
factors that can potentially influence survival of hatchling C. porosus in both the wild
and captivity include diet, movement and habitat use, thermoregulation, social
dynamics, and size and age. The following sections examine what is currently known
about hatchling C. porosus in the wild and in captivity. Information from the wild is
critical to understanding hatchling C. porosus survivorship and may provide clues to
improving captive management and therefore reducing the incidence of FTT.
Diet
Hatchling C. porosus in the wild feed intermittently on a diet of small crustaceans
(predominantly crabs), insects, and occasionally fish, usually captured in shallow
water near the land water interface during the night (Taylor 1979; Webb et al. 1991).
Wild hatchling C. porosus appear to be far more efficient at converting food in to
increased body mass, compared with individuals raised in captivity (Garnett and
Murray 1986; Webb et al. 1991). In general, hatchling C. porosus are attracted to
movement and readily consume live food (Webb et al. 1991; Hutton and Webb 1992).
However, while providing live food to hatchlings in captivity is rarely economically
practical (Hutton and Webb 1992), if the shape or form of the food is too different
from that of prey then it may negatively impact consumption and result in FTT.
15
A number of studies have been dedicated to dietary preference and feeding regimes of
hatchling C. porosus in captivity (Garnett and Murray 1986; Mayer et al. 1997; Davis
2001). Hatchling C. porosus are typically fed a red meat based diet in combination
with multivitamin and calcium supplements five to six days a week (Hutton and Webb
1992; Mayer et al. 1997; Davis 2001). This regime achieves superior growth for the
large majority of hatchling C. porosus (80-85%) compared to diets based on fish, or
pelletized food (Hutton and Webb 1992). However, there appears to be clutch and
individual specific dietary preferences, and so providing a mixture of different protein
sources may be important for achieving higher rates of growth and survival (Garnett
and Murray 1986; Manolis et al. 1990; Hutton and Webb 1992).
It has been argued that the odor of a food source may affect consumption, and that
hatchling C. porosus may be inherently wary of piles of meat, as in the wild this
would generally attract larger crocodiles and other scavengers that could feed on
small hatchlings (Manolis et al. 1990). In comparison, alligators achieve high rates of
growth and survival (>90%) when raised on any number of different food types,
including red meat, fish or pelletized food containing vegetable protein (Staton et al.
1990; Hutton and Webb 1992). Alligators are also far more adaptable when it comes
to changing between different feed types (Hutton and Webb 1992).
Movement and habitat use
Despite differences between habitats, hatchling C. porosus in the wild make few if
16
any large scale movements during the first year, with individuals often found within
several kilometres of the nest site (Webb and Messel 1978; Webb et al. 1978).
Hatchling crocodiles spend the majority of the day hidden in cover among vegetation,
branches and logs near the water’s edge (Platt and Thorbjarnarson 2000; Mazzotti et
al. 2007). This cryptic behaviour enables them to not only avoid predators but may
also allow them to thermo-regulate more effectively (Bolton 1990; Pooley 1990;
Riese 1991). It is unknown how movement patterns and habitat use change in
response to different weather patterns and season. In captivity, hatchling C. porosus
that are not provided with some form of shelter tend to pile on top of each other and
grow less, compared with those in which shelter is provided (Riese 1991; Mayer
1998; Davis 2001). Hatchling C. porosus are prey to a wide range of predators and so
the amount and type of cover provided could have important implications for FTT.
Thermal relations
Crocodilians are largely dependent upon their environment for heat, and have the
ability to warm up twice as fast as they can cool (Boland and Bell 1980; Lang 1987;
Hutton and Webb 1992). However, the rate of heat exchange with the environment is
directly related to the mass of the individual, with adults heating and cooling at a
slower rate than hatchlings due to greater thermal inertia (Lang 1979; Boland and Bell
1980). Hatchling crocodilians operate over a wider range of temperatures, achieving
preferred body temperatures through behavioural means (Lang 1987; Seebacher et al.
2003). However, the way in which they achieve preferred body temperatures differs
between species (Grigg and Seebacher 2000; Seebacher et al. 2003). While adults are
17
less sensitive to changes in temperature, smaller individuals are more adaptable to
prolonged shifts in environmental temperatures as they can utilize microhabitat to heat
and cool more rapidly (McNease and Joanen 1974; Pooley and Gans 1976).
Many species of crocodilian are maintained on farms at relatively constant high
temperatures (30-33ºC) (Hutton and Webb 1992). However, research suggests that
this approach may be inappropriate for optimal physiological functioning, due to the
need for individuals to vary their body temperature according to their physiological
state, with higher temperatures often sought after feeding or during illness, and lower
temperatures sought during fasting (Hutton and Webb 1992; Lang 1987). It is also
important to note that the large majority of reptile species raised in captivity are
provided with a range of thermal options within their enclosure, and that the
importance of this has long been recognised (Peaker 1969). Despite the success of
raising A. mississippiensis at constant high temperatures (30-33ºC), providing a
thermal gradient may be important for those species that inhabit year round warm
climates such as C. porosus that need the ability to cool down (Lang 1979; 1981;
1987).
Optimal temperatures (air and water) for hatchling C. porosus in captivity are
currently believed to be between 32ºC and 34ºC, with some studies reporting higher
rates of growth and survival at a constant 32ºC and others at 34ºC (Webb et al. 1990;
Mayer 1998; Davis 2001). Hatchling C. porosus maintained at either low (<26ºC) or
high temperatures (>34ºC) for long periods do poorly in terms of growth and survival
(Webb et al. 1990; Mayer 1998; Davis 2001), as do those in which only a localised
18
source of heat is provided (eg. heat lamp, hot water tap) that can not be accessed by
all individuals (Lang 1987; Webb and Manolis 1990; Riese 1991). As individuals get
larger, they are less reliant on an artificial source of heat and can be raised outdoors
under ambient conditions (Webb and Manolis 1990; Riese 1991).
There are almost no studies that have examined thermoregulatory behaviour of
hatchling C. porosus in the wild or in captivity. Lang (1981) provided some
information regarding thermal preference of hatchling C. novaeguineae in a natural
enclosure, and found that hatchlings selected higher temperatures (33.4-33.9ºC)
during the first two weeks than when they were between two and five weeks old
(31.8-32.2ºC), and that this was similar for hatchling C. porosus (Lang 1981). Just as
the provision of a varied diet may allow for clutch-specific dietary preferences,
providing a thermal gradient may allow for clutch-specific thermal preferences.
Understanding thermal relations of hatchling C. porosus in captive and wild settings is
important for improving captive management and reducing the incidence of FTT.
Social dynamics
Social interactions among crocodiles are known to have a strong influence over
almost all other behaviours (thermoregulatory, feeding, movement, habitat use etc)
(Lang 1987). As the natural inclination for young hatchlings of most species is to
group together in crèches, this will usually override normal thermoregulatory
behaviour (Lang 1987). Hatchlings in these groups will emit a high pitched call which
is believed to be important in keeping the crèche together, as well as to alert others of
19
danger (Magnusson 1979; Britton 2000). However, as hatchlings get older and grow
larger, dominance hierarchies begin to establish and individuals of low social status
can often be excluded from a resource (food, water, cover, etc.) (Riese 1991).
There is almost no information regarding the social interactions and behaviour of
hatchling C. porosus. In one study that examined hatchling C. porosus in the wild, a
recording of a hatchling played on the opposite bank to a crèche resulted in the whole
crèche relocating to the other side of the river (Magnusson 1979). However, whether
this grouping behaviour is simply for protection against predators, or whether there
are other social or thermoregulatory reasons that are important is unknown.
Hatchling C. porosus tend to disperse from the crèche after two months (Webb et al.
1977), while hatchling A. mississippiensis will remain together in some areas for up to
several years (Hunt 1982). The reason for earlier dispersal among hatchling C.
porosus may be due to an increasing intolerance of conspecifics (Webb and Messel
1978). However, it is unknown how early aggressive or dominant behaviours occur
and how important they are for survival.
In captivity, hatchling C. porosus appear to perform better at lower densities or group
sizes of around 10-15 individuals, with overcrowding (>30 individuals) causing lower
rates of growth and survival (Riese 1991; Webb et al. 1992; Mayer 1998). As
individuals grow, it is believed by some that larger group sizes may be preferable as it
may dilute the affect of social dominance (Mayer 1998). Regular sorting or grading of
animals by size is an effective strategy for breaking any dominance effects within a
20
group (Riese 1991). As with thermal relations, understanding social dynamics of
hatchling C. porosus in wild and captive settings is important for improving captive
management and reducing FTT.
Our understanding of these factors and how they interact to ultimately influence
survival of hatchling C. porosus remains poorly understood. As there is almost no
information regarding the social and thermal behaviour of hatchling C. porosus, this
research will provide new information that, combined with existing knowledge, will
be important for addressing the issues of survival and FTT.
Limitations of previous research
The dramatic increase in size that a hatchling crocodilian will go through to reach
adulthood, which in some cases can be an increase of more than five orders of
magnitude (Grigg and Seebacher 2000), is unmatched by most other vertebrate
species. As a result, hatchling and adult crocodilians have such different physiological
and behavioural requirements, that they could almost be considered separate species.
Hatchling crocodilians are small ‘prey’ species that group together, occupy sheltered
habitat, and shuffle between sun and shelter in order to avoid predators (Lang 1987;
Webb and Manolis 1989). In contrast, adults as ‘apex predators’ have very few
predators other than humans and larger crocodiles, and as a result are generally not
restricted to sheltered habitat or nocturnal feeding (Lang 1987; Webb and Manolis
1989). Adults are more solitary with individuals coming together only during the
21
breeding season or because drought has restricted the amount of water available
(Webb and Manolis 1989).
Therefore, results from studies that have examined sub-adult and adult C. porosus are
not necessarily applicable to hatchlings. As the majority of studies involving C.
porosus have focused on larger size classes, there is limited information on hatchling
C. porosus. Because growth of hatchling C. porosus within the first year is rapid
(double in size), this will result in changes to their requirements both in the wild and
in captivity. Thus, what is ideal for a new hatchling may not be so for an animal that
is two months, six months, or 12 months of age.
Many of the studies involving hatchling C. porosus in captivity have been
compromised by inadequate temperature control, clutch affects, use of individuals of
different ages and sizes, poor husbandry, and a superficial approach (Garnett and
Murray 1986; Webb et al. 1992; Riese 1991; Mayer 1998; Davis 2001). Subsequently,
results have often been inconclusive or conflicting. This is why there is still no
standard way of raising C. porosus hatchlings (Riese 1991; Davis 2001). A variety of
different methods (pen types, feeding etc) are now being used to raise hatchling C.
porosus, with most farms experimenting with new approaches (Mayer 1998; Davis
2001). However, many of these new practices are often based on assumptions or
anecdotal beliefs not proven by science (Riese 1991; Davis 2001). As the industry has
developed, so to has the commercial confidentiality associated with in-house research,
especially with regard to raising hatchlings (Webb pers. com.). The prevalence of FTT
among captive raised hatchling C. porosus highlights our relative lack of knowledge
22
regarding the requirements of the species at this early developmental stage.
The few studies on wild hatchling C. porosus in Australia occurred in the years
following protection (1977-1991) when the population of C. porosus in Australia was
in a state of recovery (Webb et al. 2000; Letnic 2004). These studies were limited by
low numbers of hatchlings available due to past hunting. In the Northern Territory, the
population is now considered to be approaching pre-exploitation levels, with the
overall size structure now biased towards larger animals which has occurred despite
high levels of egg harvest (Webb et al. 2000; Letnic 2004). The overall change in the
population dynamics, with a shift towards larger individuals, is likely to result in
changes at the hatchling level in terms of growth and survival.
Intended aims and goals of this thesis
It is clear that the hatchling life stage is an important but little understood one, in both
wild and captive conditions. There is a broad range of interrelated factors that are
known or suspected to influence hatchling potential and ultimately fitness, particularly
survival rates, for example egg and thus hatchling size, incubation environment,
absence or presence of parental care, thermoregulation, predation, diet, social
behaviour, movement and dispersal, growth, size-related changes, density, habitat
contexts and more. The degree of importance and overlap of such factors between
wild and captive environments is sometimes obvious (eg. predation), but at other
times obscure (eg. behaviour). A series of these factors is investigated in this study,
the main focus being the poorly understood role of hatchling behaviours. This
23
research provides new information that, combined with existing knowledge, provides
importance guidance about the factors known or likely to affect the survival rates of
hatchling C. porosus. In this study these results were used to guide the design of
experiments aimed at improving growth and survival of this species in captivity and
reducing FTT.
Specific questions addressed through research are:
What are the thermal requirements of hatchling C. porosus, and how are these
influenced by feeding, group size and density, time of day, change in weather
or season, age and size?
What is the nature of agonistic interactions between hatchling C. porosus, how
early do they start and how do they change with age and size, time of day,
feeding, group size and density, distribution of resources, clutch?
Does the nature of agonistic interactions differ between species during this
early life stage?
Can the raising environment be modified based on this information in order to
improve rates of growth and survival of hatchling C. porosus in captivity.
The results of this research will improve our understanding of the thermal and social
requirements of hatchling C. porosus in captivity, and will have broader application to
24
reintroduction and head starting programs involving C. porosus in other countries
where the species is considered threatened or endangered. This study will also provide
the farming industry with information that may improve raising conditions and reduce
the level of mortality.
The thesis is set out as follows. In Chapter 2 the relationship between early growth
and survival of hatchling C. porosus in captivity is examined, Chapter 3.1-3.3 details
the nature of agonistic behaviour and Chapter 4 the nature of thermal behaviour in
hatchling C. porosus. Chapter 5.1-5.4 examines factors affecting growth and survival
of hatchling C. porous in captivity with a focus on agonistic and thermal behaviour,
and Chapter 6 provides a summary, examines the raising environment itself and then
provides conclusions.
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38
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39
Chapter 2. The relationship between early growth and survival of
hatchling saltwater crocodiles (Crocodylus porosus) in captivity
Published as: ‘Brien, M.L., Webb, G.J., McGuinness, K.A., Christian, K.A., 2014.
The relationship between early growth and survival of hatchling saltwater crocodiles
(Crocodylus porosus) in captivity. PloS ONE 9: e100276.
doi:10.1371/journal.pone.0100276’. Formatted according to author guidelines for
journal.
Abstract
Hatchling fitness in crocodilians is affected by ‘runtism’ or failure to thrive syndrome
(FTT) in captivity. In this study, 300 hatchling C. porosus, artificially incubated at
32oC
for most of their embryonic development, were raised in semi-controlled
conditions, with growth criteria derived for the early detection of FTT (within 24
days). Body mass, four days after hatching (BM4d), was correlated with egg size and
was highly clutch specific, while snout-vent length (SVL4d) was much more variable
within and between clutches. Growth trajectories within the first 24 days continued to
90 days and could be used to predict FTT affliction up to 300 days, highlighting the
importance of early growth. Growth and survival of hatchling C. porosus in captivity
was not influenced by initial size (BM4d), with a slight tendency for smaller hatchlings
to grow faster in the immediate post-hatching period. Strong clutch effects (12
clutches) on affliction with FTT were apparent, but could not be explained by
measured clutch variables or other factors. Among individuals not afflicted by FTT (N
= 245), mean growth was highly clutch specific, and the variation could be explained
by an interaction between clutch and season. The results of this study highlight the
40
importance of early growth in hatchling C. porosus, which has implications for the
captive management of this species.
Introduction
Initial offspring size in the wild and in captivity can be expected to confer short to
long term fitness advantages if it improves the ability to forage or capture food, avoid
predation, compete with conspecifics, survive adverse environmental conditions [1]
[2] [3] [4] [5] and ultimately produce more offspring [6] [5]. This has been
demonstrated in a wide range of mammals [7] [8], birds [9] [10], reptiles [11] [12],
amphibians [13] [14], fish [15] [16], and arthropods [17] [18] [4].
Large variation in offspring size and early growth rates are common within and
between species [2] [5], between different populations of the same species [14] [19]
[3], and between siblings from the same clutch [5]. Maternal size and condition [20]
[21] genetic effects [22], multiple paternity, and conditions experienced prior to and
after birth or hatching [22] may all be involved. With several species of mammals
[23], snakes [22], fish [24], and frogs [25], the early nutritional environment is
reportedly just as important as genetic influences in creating irreversible changes in
growth rate and survival which affect long-term fitness [26] [27] [28] [22].
Despite larger offspring size often being correlated with higher rates of initial growth
and survival (‘bigger is better’) [1] [16] [3] [22] [29], there are many exceptions.
There can be small or no effects of initial size on fitness [30] [2] [31], skewed effects
41
in which intermediate sized individuals are the most fit [32], or negative effects in
which initial high growth rates are detrimental to fitness [33] [34]. Among reptiles,
the ‘bigger is better’ hypothesis appears to be generally supported [1] [35] [12] [22],
but there are few data available for crocodilians in the wild or in captivity.
This study examines growth and survival in captive raised hatchling saltwater
crocodiles (Crocodylus porosus), mostly from wild collected eggs (10 of 12 clutches).
Average clutch size for C. porosus in Australia is around 50 eggs (range 2-78; 65.4 to
147.0 g eggs) producing hatchlings from 41.4 to 93.6 g [36] [37]. In the wild an
estimated 54% of hatchlings survive to 1-year-of-age [36] [38], whereas in captivity
survival rates are higher, but vary greatly between establishments using different
raising techniques [39]. The primary cause of mortality in captivity (49% of all
hatchling deaths in captivity) is ‘runtism’ [40] [41] [39] [42], which is in essence a
failure to thrive syndrome (FTT) involving voluntary starvation, which reduces
immunity to disease and causes death between 70 and 200 days post-hatching [40]
[41] [39], with time to death dependent upon initial weight [43]. The root causes of
FTT in hatchlings remain poorly understood, but genetic [39] and incubation effects
[37], elevated corticosterone levels [44], agonistic social interactions [45], and various
aspects of the raising environment (temperature, noise, visual stimuli) and
management protocols (density, size disparity, disturbance) have all been implicated
[46] [40] [41] [39].
Central aims of the present study were to determine the degree to which growth
trajectories established within the first three weeks post-hatching could be used as
42
indices of short-term fitness.. The degree to which size and body condition at hatching
influences post-hatching growth is examined. Particular attention is focussed on
clutch effects on both growth rates and the incidence of FTT. The FTT phenomenon
in C. porosus and its implications on short-term fitness in captivity and in the wild are
discussed.
Materials and Methods
This project was conducted under the approval of the Animal Ethics Committee of
Charles Darwin University (permit no. A11003).
Clutches, eggs and incubation
Saltwater crocodile eggs and hatchlings used in these experiments were provided by
Wildlife Management International (WMI; Darwin, Australia). There were effectively
two groups of hatchlings, those clutches that hatched early in the year (16 - 24
January; 5 clutches; N = 120) when ambient conditions were warmer, and those that
hatched later in the year (Late: 29 March-22 May 2011; 7 clutches; N = 180) when
conditions were cooler. Eggs came from wild nests (N = 10) collected 1 - 50 days
after laying and captive nests (N = 2), collected 1 - 2 days after laying. Egg
temperature within the nest (Tnest) was measured at the time of collection with
calibrated thermometers, 2 - 3 eggs deep in the clutch. Daily fluctuations in Tnest are
reasonably modest but peak at 19:00h to 21:00h [47]. Measured Tnest and the time of
measurement were used as a clutch-specific index for aligning what the mean (Tn.mean)
43
and maximum (Tn.max) nest temperatures may have been up to the time of collection.
Variation in egg size within clutches of C. porosus is low [38], and so mean egg size
(mass, length, width) was measured from only 10 eggs per clutch. All eggs are carried
within the oviducts of females prior to laying, and thus total clutch mass or volume is
the best clutch-specific indicator of female size [38]. The age of each clutch at the
time of collection and the number of infertile eggs and eggs with dead embryos were
estimated using methods described previously [36] [49].
Incubation to hatching (6th
April to 10th
August 2011) was completed for all eggs at
constant 32ºC (± 0.2ºC) and 98-100% humidity, which produces hatchlings with the
highest rates of growth and survival [37]. Eggs were inspected regularly and the
embryos of any dead eggs were used to determine whether death had occurred during
incubation or prior to collection. Hatching typically occurred on the same day for each
clutch. Hatchlings with deformities or which appeared to have excessive abdominal
yolk were excluded from the experiment. Sex was not determined, but 32ºC is a male
producing temperature, and the sensitive period for sex determination for the majority
of eggs (10 of 12 clutches) occurred in the incubator [49] [50] [51]. For the two oldest
clutches, sex may have been determined in the field. One (Tn.mean = 28.6ºC at 50 days)
was probably 100% female, whereas the other (Tn.mean = 33.3ºC at 36 days) may have
contained males and high temperature females [49] [50] [51] [37]. All hatchings were
held in the incubator (32ºC) in crates for three days after hatching before release into
their raising enclosures (day 4) and being fed.
Experimental enclosures
44
Two types of experimental enclosures (initial and final) were used. Hatchlings were
housed between days 4 and 24 in sibling-only groups of 7-10 individuals in the initial
enclosures. They were box shaped (170 x 100 x 50 cm high) fibreglass enclosures
with a land area (70 x 100 cm) that gradually sloped down to a water area (100 x 100
cm; < 8cm deep). At 24 days, hatchlings were transferred into the final enclosures, in
mixed clutch groups of twenty individual hatchlings of similar size. The final
enclosures were 3 m2 box-shaped concrete pens (150 x 200 x 150 cm high), with a
land area (150 x 80 cm) that gradually sloped to a water area (150 x 120 cm; < 19 cm
deep). Each enclosure had a basking cage (100 x 120 cm) attached to the outside and
accessible through an opening (20 x 10 cm) in the wall, which effectively increased
the enclosure area from 3 to 4.2 m2. The cage increased the range of thermal options
available to hatchlings. Hatchlings remained in the final enclosures up until a
maximum of 8 months of age (300 days), but were sorted on the basis of size every 3-
4 weeks [52] [53] [54]. Hence, density remained the same but the individuals in each
final enclosure did not.
A ‘hide area’ [52] [53] [54] was provided in all initial and final enclosures. Each was
80 x 90 cm, constructed of eight lengths (80 cm long) of 10 cm (diameter) PVC pipe
strapped together in the horizontal plane and mounted on legs (5 cm). Hides were
centrally positioned in the water (partly immersed) and overhung the land. One hide
area was provided in the initial fibreglass enclosures, and two in each final enclosure.
All hatchlings were subjected to a natural light cycle. Water temperature (Tw) was
maintained at 31-32°C with thermostatically controlled injection of warm water
45
(initial enclosures) or submerged heating pipes (final enclosures). Air temperature
(Ta) averaged around 32-34°C but varied from 26-36°C at different times of the day
depending on ambient temperatures. All animals were fed chopped red meat
supplemented with di-calcium phosphate (4% by weight) and a multivitamin
supplement (1%) at 16:00-17:00 h six days a week, with waste removed the following
morning (08:00-09:00 h) when the water was changed. Equilibration of Tw after water
changes took 0.5 to 1.5 hours.
Identification and measurements
A uniquely numbered metal webbing tag (Small animal tag 1005-3, National Band
and Tag Co.) was attached to the rear back right foot at the time of hatching. Snout-
vent length (SVL in mm to the anterior of the cloaca) and body mass (BM in grams)
were measured when the animals were introduced into the initial enclosures at 4 days
of age, at 24 days of age when transferred to the final enclosures, and again at 70 to
194 days of age (depending on hatch date). All hatchlings were fasted the day prior to
measurements being taken. Fasting for 48 hours prior to measurement does not affect
growth rates but longer periods of fasting do [43]. These data allowed a size-age curve
to be constructed for each individual, from which, size at 90 days could be predicted,
which avoided problems associated with the different real ages of individuals. These
measurement intervals reflect previous indications that growth patterns established in
the first few weeks and months are an important index of growth and survival after
that time in crocodilians [55]. Hatchling C. porosus that are afflicted by FTT can be
expected to succumb to mortality from 70-200 days post-hatching [39], so although
46
measurements were not taken after 70-194 days, mortalities were recorded up 300
days (10 months) after which survival rates tend to be 95-97% [39].
Statistical analyses
All statistical analyses were performed using JMP 8.0 statistical software [56]. Where
appropriate, data were checked for normality (Shapiro-Wilk’s test) and
homoscedasticity (Cochran’s test) prior to statistical analysis. Morphometric
relationships between egg length (EL) and egg mass (EM) of each clutch with SVL4d
and BM4d; SVL, BM, and body condition (BC = BM /SVL g/mm) at 4 (SVL4d;
BM4d), 24 (SVL24d; BM24d), and 90 (SVL90d; BM90d) days of age, and growth in BM
between 4 and 24 days of age (GBM4-24d) and 24 and 90 days of age (GBM24-90d) were
examined using regression analyses. Size at 90 days was predicted from the size-age
relationship for each individual at 4, 24 and 70 to 194 days (dependent on actual age).
As a check on biases associated with prediction, the actual BM90d and SVL90d of a
sample of animals measured at 90 days (N = 48) were compared with the predicted
values using paired t-tests. No significant difference was detected for the actual and
predicted values of either BM90d (t=0.26; df=94; P=0.79) or SVL90d (t=0.56; df=94;
P=0.58). We examined the effect of season (early: 16-24 January, N = 5; late: 29
March – 22 May, N = 7) on egg mass, hatchling size and growth (SVL and BM) at 4,
24, and 90 days, and %FTT using a PERMANOVA with clutch as a random factor
nested within season. In PERMANOVA, probabilities that treatments are significantly
different from each other are generated by permutation, which requires only limited
assumptions about the distribution of the data: in particular, normality of the data is
47
neither assumed nor required [57]. The analysis was conducted with 1000
permutations in the PERMANOVA+ add-in for PRIMER [57]. Regression analyses
were also used to predict the probability of %FTT affliction up to 300 days from
GBM4-24d and BC24d, and BM24d, using progress means (N = 20 animals). Unequal t-
tests were used to examine differences in BM4d between hatchlings that became
afflicted with FTT (N = 55) and those that survived (N = 245). A Pearson’s chi-square
test was used to examine the effect of clutch on the proportion of individuals that died
from FTT affliction. The effect of clutch on size and growth of non FTT animals (N =
245) was analysed with an ANOVA. All means are reported ± one standard error with
sample sizes.
Results
Clutch, incubation and hatchling characteristics
The wild and captive laid clutches had different numbers of different sized eggs,
which produced different sized hatchlings, came from different sized and aged
females (indicated by total clutch mass). Clutches were collected at different embryo
ages from nests with different temperatures that were laid at different times. Clutches
also had different rates of infertility and embryo mortality before and during
incubation, ultimately producing different proportions of apparently normal hatchlings
(Table 1). The raising experiments also occurred at different times of year, and despite
Tw being constant, Ta varied with the prevailing ambient temperatures.
48
Table 1. Clutch-specific details associated with the hatchlings used in the raising trials and their incubation. ‘30°C days’ is the age an
embryo would be had it been incubated at 30°C [47] [48] [49]. Spot nest temperature (Tn) was measured at the time of collection whereas mean
(Tn.mean) and maximum (Tn.max) nest temperatures are crude estimates [49] [50] [51]. Lay and hatch days: January 1 = day 1. Hatchling sizes were
measured 4 days after hatching, before feeding started. The mean seasonal maximum (Tmax: 13:00h) and minimum (Tmin: 09:00h) air
temperatures during the 21 days of raising for the hatchlings from each clutch (Australian Bureau of Meteorology: Darwin airport). A = wild
nests from the Adelaide River mainstream; BP/CB = captive bred; M = wild nest from Melacca swamp on Adelaide River floodplain.
Clutch ID
Characteristic A20 A44 A70 A71 A75 A77 BP4 CB5 M28 M43 M55 M62
Grand
means
±SD
Age at collection 1 4 24 12 1 1 0 0 16 24 46 42 12.9±15.6
Lay day of year 10 82 125 132 141 141 22 22 15 6 91 114 75.1±56.0
Actual Tn (oC) 29.8 29.8 27.2 28.4 31.9 27.2 30.7 29.5 32.4 32.9 33.2 28 30.1±2.2
Tn.mean (oC) 29.9 31 28.2 29.2 32.2 27.5 31.5 31.4 32.7 33 33.3 28.6 30.7±2.0
Tn.max (oC) 31.8 28.8 31.1 31.4 32.1 32.1 31.8 31.8 31.8 31.8 31.1 31.2 31.4±0.9
Hatch day of year 90 163 198 210 221 221 103 103 98 90 178 182 154.8±51.7
Clutch size (N) 57 45 50 70 50 63 38 47 58 53 53 72 54.7±10.0
Clutch mass (kg) 6.61 4.64 4.52 7.6 5.58 7.21 4.45 5.65 6.7 6.12 6.06 8.09 6.1±1.2
Mean egg mass
(g) 115.9 103.2 90.3 108.6 111.5 114.4 117.2 120.2 115.5 115.5 114.4 112.4 111.6±8.0
Mean egg length
(mm) 78.3 76.8 71.5 79.3 78.8 78.9 80.6 82.4 80.8 81.4 77.9 75.8 78.5±2.9
Mean egg width
(mm) 50.3 48.3 47.1 48.5 50.2 50.2 50.2 49.6 50.2 49.9 50.7 48.9 49.5±1.1
49
Infertile (N) 0 2 2 5 2 4 1 9 14 15 0 0 4.5±5.3
Dead before
collection (N) 1 16 27 17 7 0 0 0 2 0 0 0 5.8±9.1
Dead during
incubation (N) 3 3 0 4 4 4 7 10 4 3 4 1 3.9±2.6
Total dead before
hatching (N) 4 19 27 21 11 4 7 10 6 3 4 1 9.8±8.3
Live remaining
(LR) eggs (N) 53 24 21 44 37 55 30 28 38 35 49 71 40.4±14.6
Abnormal
hatchlings (N) 0 0 0 0 0 0 0 0 0 0 0 1 0.10±0.3
Abundant yolk
hatchlings (N) 0 0 0 1 3 2 0 0 0 0 0 0 0.50±1.0
External yolk
hatchlings (N) 4 1 2 1 5 0 0 4 4 4 0 0 2.1±2.0
Normal
hatchlings (NH) 49 23 19 42 29 53 30 24 34 31 49 70 37.8±15.1
No. NH used in
study 39 19 15 30 15 37 20 17 25 19 25 39 (25.0±9.2)
NH of LR eggs
(%) 92.5 95.8 90.5 95.5 78.4 96.4 100 85.7 89.5 88.6 100 98.6 92.6±6.5
Seasonal Tmin
(ºC)
23.6 17.1 18.7 18.6 19.8 19.8 21.8 21.8 22.7 23.6 19.7 19.3 20.5±0.61
Seasonal Tmax
(ºC) 31.8 28.8 31.1 31.4 32.1 32.1 31.8 31.8 31.8 31.8 31.1 31.2 31.4±0.26
50
Size
Mean EM was highly clutch specific (Table 1), which in turn affected BM4d which is
comprised of hatchling tissue plus the internalised residual yolk mass. Overall, there
was a strong positive linear relationship between mean EM and EL of each clutch and
BM4d but not with SVL4d (Table 2). However, mean clutch EM differed significantly
between seasons (Table 2), with clutches of larger eggs laid earlier in the year (EM
early = 116.86 ± 3.05 g; late = 107.83 ± 2.58 g).
51
Table 2. Relationships between egg length, egg mass, size and growth at 4, 24 and
90 days of age, and % afflicted by Failure to thrive syndrome.
To predict From Formulae
Size and
Growth
BM4d EM
BM4d = 11.677 + 0.541EM + 2.05g; R2 = 0.83; F = 48.74;
P<0.0001
EL
BM4d = -41.856 + 1.445EL + 2.25g; R2 = 0.79; F = 38.78;
P<0.0001
SVL4d EM R2 = 0.10; F = 1.13; P = 0.310
EL R2 = 0.07; F = 0.78; P = 0.400
SVL4d
BM4d
(<70g) R2 = 0.003; F = 0.242; P = 0.620
BM4d
(>70g)
SVL4d = 76.775 + 0.915BM4d + 2.85 mm; R2 = 0.44; F =
164.28; P<0.0001
SVL24d BM24d
SVL24d = -85.632 + 1.290BM24d – (0.00497BM24d)2 ± 4.13 mm;
R2 = 0.60; F = 449.5; P<0.0001
SVL90d BM90d
SVL90d = 147.611 + 0.240BM90d ± 8.82 mm; R2 = 0.94; F =
3865.0; P<0.0001
BM24d BM4d R2 = 0.01; F = 3.14; P = 0.081
BM90d BM4d R2 = 0.01; F = 2.16; P = 0.143
BM90d BM24d
BM90d = -214.090 + 4.179BM24d - 0.0252(BM24d-89.34)2 +
48.69g; R2 = 0.62; F = 241.11; P<0.0001
SVL90d SVL24d
SVL90d = -144.76 + 2.057SVL24d ± 16.29 mm; R2 = 0.44; F =
234.41; P<0.0001
GBM24-90d BM4d R2 = 0.01; F = 2.03; P = 0.161
GBM4-24d BM4d
GBM4-24d = 65.470 - 0.669BM4d ± 15.70 g; R2 = 0.04; F = 12.81;
P = 0.0004
GBM24-90d GBM4-24d
GBM24-90d = 19.146 + 3.147GBM4-24d - 0.0377(GBM4-24d -17.21) ±
50.57g; R2 = 0.44; F = 114.38; P<0.0001
FTT
affliction
%FTT GBM4-24d %FTT = 63.9 - 7.79 GBM4-24d + 10.52; R2 = 0.94; P = 0.0013
BC24d %FTT = 411.8 - 759.12 BC24d + 8.06; R2 = 0.93; P<0.0001
BM24d %FTT = 446.4 - 5.35 BM24d + 6.86; R2 = 0.96; P = 0.0005
Overall mean BM4d of C. porosus (N = 300) was 72.1 ± 4.9 g (55.4-80.8 g), SVL4d
was 144.5 ± 3.8 mm (135-153 mm), and BC4d was 0.50 ± 0.03 g/mm (0.39-0.50
g/mm). However, clutches of eggs laid early in the year produced hatchlings with
52
significantly larger BM4d (75.09 ± 0.38 g) than those produced later in the year (70.15
± 0.31 g; Table 3). However, this was not the case with SVL at 4 days. To examine
the relationship between SVL4d and BM4d the data set was subdivided into <70g (N =
86) and >70g (N = 214) BM4d. There was no relationship between SVL4d and BM4d
for hatchlings with a BM4d <70g, while for hatchlings with BM4d <70g the
relationship was linear (Table 2; Fig. 1a).
Figure 1. Relationship between BM and SVL of hatchling C. porosus (N = 300) at
different ages. Relationship at a) 4d, b) 24d, and c) 90d for hatchlings born early (N
= 120; blue) and late (N = 180; grey) in the year. BM90d was predicted from the size-
age relationship for each individual at 4, 24 and 70 to 194 days.
At 24 days of age, the overall mean BM24d of C. porosus (N = 300) was 89.3 ± 15.8 g
(60-142 g), SVL24d was 159.6 ± 7.0 mm (143-178 mm), and BC24d was 0.55 ± 0.08
g/mm (0.41-0.80 g/mm). Clutches of hatchlings born later in the season were not
significantly heavier at 24 days than those born early in the year (Table 3). In contrast
to the highly variable relationship between SVL and BM at 4 days, there was a much
stronger relationship between BM and SVL at 24 days (Table 2; Fig. 1b).
53
Based on predictions at 90 days of age (N = 300), mean BM90d was 162.7 ± 75.9 g
(37-409 g), SVL90d was 187.7 ± 24.8 mm (147-250 mm), and BC90d was 0.80 ± 0.33
mm (range 0.25 to 1.62 g/mm). There were no significant seasonal differences in
SVL90d or BM90d (Table 3). The relationship between SVL and BM at 90 days of age
was strongly linear (Table 2; Fig. 1c).
Growth
Given the relatively uniform size of hatchling BM at 4 days (SD of BM4d = ±4.9 g)
the individual variation in size by 24 days (SD of BM24d = ± 15.8 g) and 90 days (SD
of BM90d = ± 78.6 g) was extreme and was reflected in BC. Mean GBM4-24d was 17.2 ±
16.0 g but the range (-6.9 to 70.1 g) was already extreme with some individuals
increasing by 70 g (+97.5%BM4d) while others had lost 7 g (-9.3%BM4d). Mean
GSVL4-24d was 15.4 ± 6.9 mm (range 1 to 30 mm). Mean GBM24-90d (63.7 ± 67.1 g;
range -40.2-278.6 g) and GSVL24-90d (24.2 ± 17.91 mm; range -3 to 77) both increased
substantially relative to the 4-24 day period, but variation remained extreme. There
were no seasonal differences in SVL or BM growth (Table 3).
54
Table 3. Seasonal differences in size, growth and %FTT between clutches laid
early in the year (16-24 January 2011; 5 clutches) and clutches laid late in the
year (29 March-22 May 2011; 7 clutches) using PERMANOVA with d.f. as 1 and
10.06.
Early vs late clutches Pseudo-F P(Perm)
EM 5.11 0.04
BM4d 8.09 0.02
SVL4d 1.70 0.23
BM24d 0.01 0.76
SVL24d 4.64 0.06
BM90d 0.79 0.43
SVL90d 1.06 0.33
GSVL4-24d 1.30 0.27
GBM4-24d 2.50 0.14
GSVL24-90d 0.11 0.77
GBM24-90d 1.25 0.33
%FTT 1.71 0.22
There was no significant relationship between BM4d and either BM24d, BM90d, or
GBM24-90d (Table 2). However, BM4d did have a slightly significant but highly variable
relationship with GBM4-24d (Table 2), with higher growth among the smallest
hatchlings born. Growth trajectories in BM and SVL established within the first 24
days were largely continued up to 90 days (Fig. 2; Table 2). A high proportion of
individuals with the lowest GBM4-24d and GSVL4-24d and smallest BM24d and SVL24d
failed to recover by 90 days (Fig. 2).
55
Figure 2. Relationship between size and growth of hatchling C. porosus (N = 300)
at different ages. Relationship at 24 and 90 days: a) BM24d and BM90d, b) SVL24d and
SVL90d, c) GBM4-24d and GBM24-90d, and d) GSVL4-24d and GSVL24-90d for hatchlings born
early (N = 120; blue) and late (N = 180; grey) in the year.
Survival - FTT affliction
All animals which died during and after the study (<300 days post-hatching) were
recorded. Of these, 55 (72% of mortalities) were seriously afflicted by FTT, did not
respond to efforts to stimulate feeding, and died or were euthanized [31 (56.4%) at
70-100 days 15 (27.3%) at 100-130 days; 9 (16.4%) at 130-202 days]. The remainder
included animals (N = 17) that were otherwise healthy that died for other reasons
between 90 and 300 days post-hatching. The proportion of individuals that died from
FTT was not significantly different between seasons (Table 2).
56
BM4d was not significantly different between those hatchling afflicted by FTT (N =
55) and those that survived (N = 245; unequal t-test: t=-0.429; df=298; P=0.668).
However, the probability of affliction with FTT was clearly indicated within the first
24 days, by the extent of growth in body mass (Table 2; Fig. 3a), body condition
(Table 2; Fig. 3b), and body mass (Table 2; Fig. 3c). No affliction by FTT (0%FTT)
was detected in animals that grew more than 8.2 g, achieved a BC24d of 0.55 g/mm
SVL or a BM24d of 81.7 g in the first 24 days post-hatching. However, there were a
total of 55 hatchlings that grew less than 8.2 g after 24 days and survived. These
hatchlings grew significantly less (44.43 ± 4.59g; Welch’s t-test: t = 7.49; df = 243;
P<0.0001) between 24 and 90 days and were significantly smaller at 90 days (122.48
± 4.67g; Welch’s t-test: t = 9.82; df = 243; P<0.0001) compared with other hatchlings
(GBM24-90d= 92.03 ± 4.40; BM90d= 189.28 ± 4.95).
57
Figure 3. Probability of avoiding FTT and surviving to 300 days for hatchling C. porosus (N = 300) in relation to a) GBM4-24d, b) BC24d,
and c) BM24d. Points are means for progress intervals (N = 20).
58
Clutch effects
Among the non-FTT individuals (N = 245), clutch had a significant effect on BM4d,
GBM4-24d, and BM24d (Table 4). As growth trajectories established within the first 24
days are continued to 90 days, clutch effects were also apparent in GBM24-and BM90d
(Table 4). However, if the variance due to GBM4-24d is removed, no remaining clutch
variation occurred in BM24d, GBM24-90d, or BM90d. This confirms that the clutch
variation detected was mainly due to variation in GBM4-24d.
59
Table 4. BM4d, BM24d, BM90d, GBM4-24d, GBM24-90d, and for non-FTT animals (N = 245) and the percentage of FTT animals (N=55)
according to clutch.
Variable ANOVA Clutch ID
A20 A44 A70 A71 A75 A77 BP4 CB5 M28 M43 M55 M62
BM4d (g) R2=0.68; F=45.14; P<0.0001
Mean 73.9 67.6 61 72.2 71.6 71.9 77.3 77.7 74.5 73.9 76.2 67.8
SD 3.3 1.9 3.4 2.2 3.7 3.6 1.8 2.4 2.7 2.2 2.6 3.1
BM24d (g) R2=0.24; F=6.62; P<0.0001
Mean 85.6 99.2 82.6 101.6 88.6 102.4 92.9 98.7 84.8 83.2 92.6 97.3
SD 7.1 16.2 10.5 17.1 3.7 18.9 13.1 12.6 10.9 5.5 8.5 13.5
BM90d (g) R2=0.23; F=6.23; P<0.0001
Mean 142.2 181.1 125.3 185.6 123.1 215.3 158.6 260.9 152.6 111.5 96.9 178.8
SD 56.9 73.3 70.9 64.5 18.6 86.0 88.4 61.4 60.8 53.2 54.2 53.0
60
GBM4-24d
(g) R2=0.32; F=10.01; P<0.0001
Mean 11.7 31.6 21.6 29.4 16.9 30.5 15.6 20.9 10.3 9.3 16.4 29.5
SD 6.3 15.9 9.3 16.9 4.1 18.4 12.3 12.4 9.6 5.3 9 13.2
GBM24-90d
(g) R2=0.23; F=6.23; P<0.0001
Mean 68.0 81.9 58.9 82.1 34.5 112.9 83.7 162.3 72.5 52.7 42.9 84.3
SD 43.8 61.9 62.8 59.1 18.6 74.5 68.7 50.5 49.6 34.7 42.3 41.7
%FTT 10.3 0 20 23.3 53.3 27 15 0 8 26.3 48 2.6
61
Across clutches, the mean incidence of FTT was 19.5 + 4.99% of hatchlings, but the
range varied from 0% to 53.3%, demonstrating highly significant clutch effects (X2 =
48.36, df = 11, P < 0.0001; Table 4). None of the clutch-specific variation in %FTT
could be explained by the mean clutch and incubation characteristics (Table 1),
although it was a relatively small sample (N = 12) and none of these variables were
controlled.
Discussion
Our results suggest that under similar experimental conditions, growth trajectories for
the majority of C. porosus hatchlings established within the first 24 days post-
hatching extend to 90 days and beyond. Similarly, individuals with a high probability
of affliction by FTT up to 300 days post-hatching can be identified within the first 24
days by reduced growth. Therefore, instead of conforming to the ‘bigger is better’
hypothesis, hatchling C. porosus under these conditions appear to benefit from rapid
early growth. However, whether this is the situation in the wild, where the
environment is vastly different to that in captivity, is unknown.
While insights into the fitness of animals can be gained from both captive and wild
animals, results need to be merged and assessed carefully. Growth and survival of
neonate snakes (Thamnophis sirtalis) under captive conditions were similar to those in
the field [12] [58]. Yet other animals held in captivity can experience either greater or
less fitness than their wild counterparts. Species which suffer high levels of stress [59]
in captivity generally appear to be less fit, and this has been reported in certain species
62
of lemur [60] [61], dolphin [62] [63], parrot [64] [65], and raptor [66], and predictably
so if their ecology and response to humans is considered [67] [59].
For hatchling C. porosus under captive conditions, resources such as temperature,
cover and food are abundant and there is no risk of predation [55]. However,
individuals are confined and forced to live at higher than natural densities, and are
subject to human disturbance [55]. In the wild, the availability of resources can often
be limited or can fluctuate while the threat of predation is high and hatchling C.
porosus must contend with larger crocodiles [36] [49]. Female C. porosus also protect
their offspring for the first few weeks and months post hatching [36] [49]. As such,
differences may exist in terms of which traits (size etc) may be selected for in
captivity and in the wild, and this in turn may vary according to location and habitat.
For C. porosus, and many other crocodilians, there may be advantages in attaining a
large size rapidly, in terms of the ability to avoid predation, compete with
conspecifics, survive adverse environmental conditions, and reach sexual maturity
[68]. In the majority of cases, aggressive encounters between crocodilians favour the
larger animal [45] [69] [70], which then enables greater access to resources and
subsequently improved long-term fitness both in the wild and in captivity [68] [55].
Crocodylus porosus is considered the most aggressive and intolerant of conspecifics
of all crocodilians [70], and agonistic behaviour begins within two days of hatching
[45]. Such behaviours are known to affect growth and survival in several species of
reptile [71] [72] [73] [74], and this also appears to be the case in C. porosus under
captive conditions [55] [75] [39].
63
Clutch of origin and the incubation environment have been widely reported to affect
post-hatching growth and survival in crocodilians [42] [76] [77] [37] [78] [39].
Therefore, we tried to quantify sources of variation within the clutch, egg and
incubation variables that may have biased our results (Table 1). None explained the
variation in growth or affliction with FTT. However, the results highlight the inherent
complexity of potential variables that may influence growth and survival, and the
importance of assumptions about the homogeneity of neonates used for such raising
trials [42] [39].
That FTT can be predicted after 24 days, suggests that the first few weeks post-
hatching are crucial to short-term fitness of C. porosus under captive conditions with
survival increasing up to 90% in individuals that increased in mass by 4-7g during this
period. While this has been suggested for crocodilians by previous authors [37] [55],
it has never been accurately quantified for any species. Regardless of whether this is
the situation in the wild it does suggest that if early conditions are unfavourable,
short-term growth and survival can be compromised. This has been found in water
pythons [22] in which different rates of growth and survival occur between years
based on prey abundance during the early post-hatching stage.
The occurrence of FTT among captive-raised crocodilians is widespread, although
because weakened animals are vulnerable to secondary illnesses, FTT may be under-
reported [41]. Regardless, C. porosus appear particularly prone to FTT affliction [40]
[42] [39]. FTT is generally considered to result from an inadequate raising
64
environment, but what constitutes an adequate raising environment for each species
remains poorly understood and may be more species-specific than previously realised.
For example, Alligator mississippiensis have substantially higher rates of growth and
survival to one year of age when raised under identical conditions to C. porosus [82]
[73]. Hatchling A. mississippiensis are reported to initiate feeding more rapidly and on
a wider range of food types, and as a species are considered far more tolerant of
conspecifics with no or little aggression reported among juveniles in captivity [79]
[68] [55] [70]. Therefore, it is possible that the current approach to raising C. porosus
in captivity, which was originally based on the model used for A. mississippiensis [79]
[68], may be inadequate.
The extent to which FTT occurs in wild populations of C. porosus is not well
understood, and would be difficult to quantify due to (presumably) an increased
vulnerability of these weakened animals to predation. However, while emaciated or
malnourished hatchling C. acutus [80], A. mississippiensis, and C. johnstoni (M.
Brien pers. observation) have been observed in the wild on a number of occasions,
hatchling C. porosus in an emaciated state have rarely been encountered in the wild
[81] [82]. Hence FTT may not occur in wild C. porosus at anything like the rates
reported in captivity [39]. If so, genetic predispositions to FTT, which could be
complicated by multiple paternity [83], may be a response to threats that can be
avoided by appropriate behaviour in the wild, but not in captivity.
Factors that affect survival rates in hatchling C. porosus under captive conditions have
clear implications on future growth and survival. However, it is not really clear that
65
enhanced growth trajectories in the hatchling stage, forewarned in the first 24 days,
will ultimately influence ‘fitness’ of individuals in the long-term. It is unlikely that
measured variation in growth within a time scale of 24 days will ultimately be
correlated with variation in reproductive performance after a time scale of up to 20+
years depending on species [38] [84]. This is because a completely different suite of
factors dictate progress and outcomes during this time [85].
Variation in the survival and growth rates of C. porosus hatchlings in controlled
environments are intimately connected to each other, particularly through FTT.
Absolute growth, independent of hatchling size, is perhaps the best index of
individual performance, which has implications for survival within captive
environments, where the goal is often to enhance both survival and the early
attainment of large juvenile size. However, it is important to realise that some
hatchlings can recover from poor growth rates within the first 24 days (<8.2 g).
Identifying and understanding the causes of FTT among hatchling crocodilians is
essential for improving conservation and management programs aimed at raising
crocodilians that are threatened or endangered for purposes such as head starting, in
which individuals are released back to the wild at a size that ensures greater survival.
Acknowledgements
We thank Jemeema Brien and Charlie Manolis for their help in different phases of the
project. We would also like to thank Wildlife Management International for the
supply of animals, use of facilities, logistical support and major funding for this
66
project. WMI funding through the Rural Industries Research and Development
Corporation is gratefully acknowledged. Funding was provided through a Holsworth
Wildlife Research Endowment (ANZ Trustees Foundation), Northern Territory
Research and Innovation Board student grant, and Charles Darwin University.
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Chapter 3.1. Born to be bad: agonistic behaviour in hatchling
saltwater crocodiles (Crocodylus porosus)
Published as: ‘Brien, M.L., Webb, G.J., Lang, J.W., McGuinness, K.A., Christian,
K.A., 2013. Born to be bad: agonistic behaviour in hatchling saltwater crocodiles
(Crocodylus porosus). Behaviour 150: 737–762’. Formatted according to author
guidelines for journal.
Summary
Detailed observations on groups of captive saltwater crocodile (Crocodylus porosus)
hatchlings revealed sporadic periods of intense agonistic interactions, with 16 highly
distinctive behaviours, in the morning (0600-0800 h) and evening (1700-2000 h) in
shallow water. Ontogenetic changes in agonistic behaviour were quantified by
examining 18 different groups of hatchlings, six groups each at 1-week, 13-weeks,
and 40 weeks after hatching. Agonistic interactions between hatchlings at 1 week of
age (mean: 7.3 ± 0.65/night) were not well-defined and varied in intensity (low,
medium, high), number of individuals that were aggressive, and the outcome, while
most interactions involved contact (94.5%). There were also clutch specific
differences in the frequency of agonistic interactions. At 13 and 40 weeks, a more
hierarchal dominance relationship appeared to be established which primarily
involved aggression-submission interactions. Agonistic interactions were more
frequent (13 weeks: 9.7 ± 0.61/night; 40 weeks: 22.2 ± 0.61/night) and intense
(medium, high), but shorter in duration, in which the subordinate individual fled in
response to an approach by a dominant animal that often gave chase but did not make
80
contact. While the full repertoire of behaviour was displayed by hatchlings at 1 week
of age, a smaller subset based on dominance status was displayed among 13 and 40
week old hatchlings. Agonistic behaviour occurs in C. porosus shortly after hatching
and is important in establishing and maintaining dominance hierarchies that are
characterised by aggression-submission interactions. This type of interaction appears
typical for C. porosus both in the wild and in captivity, and may be important in
preventing serious injury in a species equipped with formidable armoury. Dispersal by
hatchling C. porosus at around 13 weeks of age appears to be driven by a growing
intolerance of conspecifics, while territoriality is apparent at an early age.
Consequently, agonistic behaviour and social status may be major contributors to the
observed differences in growth rates and survival in captivity.
Keywords: agonistic behaviour, Crocodylus porosus, dominance, hatchling crocodiles,
ontogenetic change
Introduction
Agonistic behaviour is defined as any behaviour related to aggression and includes
displays, threats, physical contact, submission, and retreats (Schenkel, 1967; Hinde,
1971; Wilson, 1975). Agonistic behaviour has been widely reported in many taxa,
including birds (Drummond, 2001; Dickinson et al., 2009), fish (Bergman, 1968;
Genner et al., 1999), mammals (Bekoff et al., 1981; Smale et al., 1995), amphibians
(Wells, 1980; Staub, 1993), crustaceans (Huber & Kravitz, 1995), and reptiles
(Stamps, 1977; Phillips et al., 1993), and is known to affect access to resources, which
81
in turn influences rates of growth and survival (Drummond, 2006).
Agonistic behaviour is an integral part of establishing and maintaining dominance
hierarchies in a range of taxa that coexist in groups for at least part of their life
(Krause & Ruxton, 2002; Drummond 2006). The establishment of a dominance
hierarchy can often reduce the frequency of actual physical contact, and thus injury
(Carpenter & Ferguson 1977; Lumsden & Holldobler 1983), which can be especially
important among species equipped with dangerous weaponry (Huber & Kravitz,
1995). Therefore, understanding the onset and ontogeny of agonistic behaviour, and
the nature of dominance, is relevant to the species’ ecology in nature and in captivity.
Although social behaviour among newly hatched or born reptiles has seldom been
studied, agonistic behaviour is believed to start early, reach maximum intensity
quickly (Drummond, 2006), and become involved in the early establishment of
dominance hierarchies in some lizards (Phillips et al., 1993; Goetz & Thomas, 1994;
Worner, 2009), snakes (Barker et al., 1979; Carpenter, 1984) and possibly turtles
(Froese & Burghardt, 1974). Agonistic behaviour and social dominance are also
linked to variation in juvenile growth and survival rates in some reptiles (Carpenter &
Ferguson, 1977; Stamps & Tanaka, 1981; Castanet et al., 1988; Phillips et al., 1993;
Goetz & Thomas, 1994; Worner, 2009).
Crocodilians are behaviourally complex reptiles (Garrick & Lang, 1977; Garrick et
al., 1978; Lang, 1987; Vliet, 1989; Thorbjarnarson & Hernandez, 1993), in which
agonistic behaviour is well established and interacts in complex ways with other
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behaviour (e.g. thermoregulation, feeding, movements and habitat use) (Lang, 1987;
Seebacher & Grigg, 2000). However, detailed studies of social behaviour are limited
to adults of only a few of the 23 extant species, most notably the American alligator
(Alligator mississippiensis) (Garrick & Lang, 1977; Garrick et al., 1978; Vliet, 1989),
Nile crocodile (Crocodylus niloticus) (Cott, 1961; Modha, 1967; Pooley, 1969), and
American crocodile (Crocodylus acutus) (Garrick & Lang, 1977; Thorbjarnarson,
1991). Agonistic behaviour has been opportunistically reported among juvenile
Crocodylus johnstoni (Webb et al., 1982), C. niloticus (Morpurgo et al., 1993),
Crocodylus porosus (Messel et al., 1981; Bustard & Maharana, 1983) and A.
mississippiensis (Joanen & McNease, 1987), but has not been documented or
examined thoroughly early in life in any crocodilian species.
Of the extant crocodilians, saltwater crocodiles (C. porosus) are considered the
most aggressive and least tolerant of conspecifics (Lang, 1987). Yet in the immediate
post-hatching period (first few weeks), hatchling C. porosus exist in nest-specific
crèches, that may be joined by hatchlings from other nearby crèches (Webb et al.,
1977). They undertake group activities, such as crossing rivers together, and
hatchlings appear to exhibit high levels of tolerance to each other (Webb et al., 1977).
Agonistic behaviour and social dominance may be responsible for hatchling C.
porosus eventually dispersing from crèches by 2-3 months (8-12 weeks) of age in the
wild (Webb & Messel, 1978). If so, in captive situations, where the ability of
hatchlings to disperse is limited, agonistic behaviour may be implicated in social
structuring within a group, creating the high variability in individual growth rates
reported (Onions, 1987; Webb et al., 1987; Webb & Smith, 1987; Mayer, 1998;
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Isberg et al., 2009). This in turn has been implicated in the 10-40 % of C. porosus
hatchlings that do not survive (Webb et al., 1987; Isberg et al., 2009). By 1-2 years of
age, agonistic behaviour in C. porosus is reportedly well established both in the wild
(Messel et al., 1981) and in captivity (Bustard & Maharana, 1983; Lang, 1987).
However, the situation that exists within the first year of life is largely unknown, with
only one unpublished study (Riese, 1991) reporting agonistic behaviour among
hatchling C. porosus in captivity.
In this study, we examined agonistic behaviour among captive C. porosus at three
important life history stages: 1 week (crèche together), 13 weeks (dispersal occurs),
and 40 weeks (solitary and much larger size) after hatching, with the following
objectives:
a. Determine the extent to which hatchling C. porosus engage in agonistic
interactions from the first week of life onward;
b. Describe and quantify agonistic behaviour that may be used by hatchling C.
porosus to elicit and respond to aggression;
c. Quantify any ontogenetic changes in agonistic interactions (1, 13 and 40 weeks)
in terms of frequency, timing, duration, intensity of interaction and the types of
behaviour used; and,
d. Discuss the implications of agonistic behaviour and dominance in C. porosus
hatchlings in the field and in captivity, and in relation to other taxa.
Materials and methods
84
Subjects and Housing
In August-December of 2011, 90 captive-born hatchling saltwater crocodiles
(Crocodylus porosus), in three age cohorts, were provided by Wildlife Management
International (WMI; Darwin, Australia). The first cohort (N = 30) contained
individuals from six different clutches, one week after hatching, while the second (13
weeks after hatching; N = 30) and third (40 weeks after hatching; N = 30) cohorts
contained hatchlings from a further five and seven different clutches respectively, that
were of similar size and age. These age cohorts were based on the early life history of
C. porosus (see Introduction), along with previous observations of behaviour. Using
the same crocodiles throughout the study was initially considered but not feasible, due
to the highly variable nature of growth within and between different clutches for this
species. Because some individuals can be almost 2-3 times the size of others by 1-2
months of age, this can lead to the death of smaller animals. In most cases, using the
same animals would simply not have been possible as 10-40% of hatchling C. porosus
in captivity die during the first 3-8 months of life (despite best practices), and this can
be higher (80-100%) for certain clutches (Webb et al., 1987; Isberg et al., 2009).
All crocodiles originated from eggs collected from wild nests in the Northern
Territory of Australia, between December and February shortly after they were laid
(10-25 days old). These eggs were then artificially incubated at a constant 32ºC and
100% humidity until they hatched (March-May). After hatching, all crocodiles were
held in the incubator for three days to assist the assimilation of residual yolk before
85
they were released as sibling only groups into the same type of enclosure (day 4).
Only crocodiles that had experienced similar environmental conditions during
incubation, and were considered ‘normal’ (healthy size and weight, no deformities)
were used in experiments. All hatchlings were subject to the same raising conditions
(enclosure, temperature, and husbandry) prior to, and during the experiments. For the
one week old cohort, 5 individuals from 6 separate clutches that hatched on the same
day (N = 30) were used, whereas the 13 and 40 week hatchlings came from clutches
of different origin, and were placed into the same experimental enclosures, at the
same density (5 per pen) and on the same day.
For each animal, snout-vent length (SVL - mm), total length (TL - mm), and body
mass (g) were measured and a uniquely numbered metal webbing tag (Small animal
tag 1005-3, National Band and Tag Co.) was attached to the rear right foot. Mean size
of 1-week olds (N = 30) was 144.7 ± 0.31 mm (SE) SVL, 308.8 ± 1.2 mm TL, and
71.1 ± 0.43 g mass. Mean size of 13-week olds (N = 30) was 209.0 ± 1.6 mm SVL,
442.4 ± 2.7 mm TL, and 254.5 ± 5.6 g mass, while the mean size of 40 week olds was
345.3 ± 1.6 mm SVL, 704.2 ± 2.5 mm TL, and 836.0 ± 4.28 g. Sex was determined by
manually probing the cloaca. The majority of crocodiles in all age cohorts were male
(3-5 in each group), and this was attributed to the incubation temperature (32ºC)
(Webb et al., 1987).
The fibreglass enclosures used to house all experimental groups were box shaped
(170 × 100 × 50 cm), with a land area (70 × 100 cm) that gradually sloped down to a
water area (100 × 100 cm; < 8cm deep). Therefore, all hatchlings were at a density of
86
2.9 animals per m2 which was considered very low based on previous studies (Garnett
and Murray 1986; Riese, 1991; Mayer, 1998). These studies determined that the
optimal density for raising hatchling C. porosus, in terms of growth and survival, was
10-15 animals per m2. A ‘hide area’ (Riese, 1991; Mayer, 1998; Davis, 2001) was
provided in each enclosure, and was constructed with 8 lengths (80cm long) of 10 cm
PVC pipe strapped together and on legs, centrally positioned in the water (partly
immersed) and overhanging the land. Water temperatures were maintained at 30-
32°C, air temperatures varied from 26-32°C, and there was a natural light cycle. All
animals were fed on chopped red meat supplemented with di-calcium phosphate (4%)
and a multivitamin and mineral supplement (1%), which is the standard diet, fed to
hatchling C. porosus in captivity. Enough food for each individual was made
available throughout the night (1600-0900h), which is when hatchling C. porosus are
known to feed in captivity and in the wild (Lang, 1987). Waste removal and cleaning
occurred the following morning (0900 h) when the water was changed.
Recording Behaviour
Wide angle infrared CCTV cameras (Signet, 92.6º) in each enclosure were used to
record all behaviour on digital video recorders (Signet 4CH DVR QV-8104). The
recording period lasted 15 hours (1700 to 0800 h) and was conducted on 3
consecutive nights for each group (45 hours per group). This daily sampling period
was based on previous recordings (100’s of hours) that revealed no agonistic
behaviour occurring between 0800 and 1700 h, with hatchlings spending the majority
of the day inactive and hiding under cover. The recordings were taken 4-5 days after
87
the crocodiles were placed in the new experimental enclosures. The only exception
were the 1-week groups in which some recordings were taken immediately after
release (when individuals were 4-5 days of age) to determine whether agonistic
behaviour or behaviour patterns were already present, and then again at 6-8 days.
Agonistic Interactions
An agonistic interaction was defined as any interaction between individuals in which
aggression and intolerance was signalled by postures or actions by one or both
individuals. An aggressive individual was one that made aggressive advances toward
another and/or made physical contact with another. Each agonistic interaction was
examined to quantify whether one or both contestants engaged in aggression. The
intensity of agonistic interactions was characterised as: low, medium or high. Low
intensity interactions were accidental, occurring when individuals lying together
appeared to disturb each other when moving, or if one swam into another underwater.
Medium and high intensity interactions appeared deliberate, with one individual
approaching another with the goal of initiating an agonistic interaction. High intensity
interactions were distinguished from medium intensity interactions by the display of
more intense contact behaviour. The behaviour exhibited, the intensity of interaction
(low, medium, high), the location (water, hide, land), the time, duration of interaction
and outcome were all quantified from the tapes.
Classification of Behaviour
88
Behavioural observations recorded during these experiments were used to create an
inventory of agonistic behaviour for C. porosus hatchlings. The descriptions are based
on a series of basic postures, modified by movement of body parts, or of the whole
animal, and whether visual signals or actual contact was involved. Some of these
behaviours have been described in other studies with adult crocodilians (Garrick &
Lang, 1977; Lang, 1987).
Statistical Analyses
All statistical analyses were performed using JMP 8.0 statistical software (SAS
Institute Inc., 2010). Where appropriate, data were checked for normality (Shapiro-
Wilk’s test) and homoscedasticity (Cochran’s test) prior to statistical analysis. A
repeated-measures ANOVA was used for comparison of means between 1 week, 13
week, and 40 week old hatchlings, with night of recording (N = 3) as the repeated
measure. A Pearsons’ Chi-square test was used to compare intensity, outcome, contact
made, number of individuals aggressive, and how often the instigator won, where
sample sizes were adequate. To test whether variation in the frequency of interactions
could be explained by time of day, the results were grouped into one of three periods:
dusk 1700-2000 h; night 2000-0600 h; and dawn 0600-0800 h. A significance level of
P<0.05 was used for all statistical tests. All means are reported ± one standard error
with sample sizes.
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Results
All agonistic interactions were in open water with none occurring on the land or near
the food on land. Some interactions were initiated accidentally, when individuals
lying together appeared to disturb each other when moving, or if one swam into
another underwater. All agonistic interactions between hatchling C. porosus involved
only two individuals at any one time. Most interactions were initiated by one or both
individuals moving deliberately toward each other, in a rapid advance (RA),
consisting of a series of short, rapid movements (Table 1). In response to RA, one or
both individuals would adopt a series of other agonistic behaviour. These involved the
adoption of some discrete postures, which often varied in the intensity of expression
(Table 1; Figure 1).
The adoption of such postures could be abandoned at any time by either slow (SF)
or rapid flight (RF), ending the agonistic interaction. Alternatively, the signals
emanating from the postures could be intensified with body movements, such as light
jaw claps (LJC) or tail wagging (TW), which were displays, not involving physical
contact with combatants. If the agonistic interaction was still not terminated by flight
of one or both animals, the behaviour intensified further, with contact movements
such as head pushing (HP), biting (B) or side head striking (SHS), often combined in
different ways with intense tail wagging (Table 1; Figure 1), until one or both
individuals took flight.
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Table 1. Classification of the behaviour used by hatchling C. porosus during
agonistic interactions. Responses to aggression can be graded, involving the adoption
of static postures, followed by non-contact movements followed again by contact
movements.
Abbreviation Definition
Initiation
Rapid advance RA Series of short rapid advance movements towards another
individual while LIW.
Termination
Slow flight SF Slow movement away from another individual in a LIW
posture.
Rapid flight RF Rapid movement away from another individual in a LIW
posture.
Chase C Rapid movement toward another individual in a LIW
posture.
Posture
Low in water LIW Immobile with only the top of the head and back above the
water surface (Figure 1a).
Inflated posture IP* Immobile with upward extension of either the front two or
all four limbs, with neck and back arched high and head and
tail angled downward (Figure 1b).
Head and tail raised HTR* Immobile with head and tail raised out of water while back
remains low. Head is usually parallel to the water but can
also be angled upwards (Figure 1c).
Head raised high
HRH*
Immobile with upward extension of the front two limbs
pushing the head and chest high out of the water on a ~45º
angle while tail remains low (Figure 1d).
Mouth agape MA* Immobile with mouth opened wide (in combination with
postures LIW, IP, HTR or HRH; Figure 1e).
Non-contact
movements
Light jaw-clap LJC* Rapid opening and closing of the jaws at the water surface,
often repeated several times (LIW or IP posture; Figure 1f).
Tail-wagging TW* Undulation of the tail from side to side in either a gentle
sweeping motion or rapid twitching, often repeated several
times (all postures; Figure 1g).
Contact movement
Head push HP Head is pushed in to an opponent, usually with mouth closed
(LIW or IP posture).
Bite B Jaws closed shut on an opponent (all postures).
Side head-strike SHS Head is thrust sideways in to an opponent while the mouth is
either open or closed (all postures).
Tail-wag side head
strike
TWSHS Tail wagging occurs prior to a side head strike, increasing
the force of the impact (all postures; Figure 1h).
Tail-wag bite TWB Tail wagging occurs prior to a bite which propels the
individual in to an opponent with force (LIW posture; Figure
1i).
91
*behaviour previously described by Garrick & Lang (1977) and Lang (1987)
Figure 1. Postures, non-contact and contact movements, described in Table 1,
displayed by hatchling C. porosus during agonistic interactions at 1, 13 and 40 weeks
of age.
Ontogenetic Changes
1. Aggression
An aggressive individual was defined as one that made aggressive advances toward
92
another and, or which made physical contact with another animal. Each agonistic
interaction was examined to quantify whether one or both contestants engaged in
aggression, and whether this differed across age classes. The number of interactions in
which both individuals were aggressive was highest at 1 week of age (37.9% of
interactions involved both individuals displaying aggression) and decreased
significantly with age. At 13 and 40 weeks, only 2.3% and 0.0% of interactions
respectively involved both individuals being aggressive. The number of separate
movements or steps in the RA increased significantly with age (F2,15 = 4.63, P <
0.05), from a mean of 1.61 ± 0.18 (mean of means; range 0-7; N = 6) per interaction at
1 week to 3.62 ± 0.11 steps (range 0-12; N = 6) at 40 weeks.
2. Frequency
Filming during the first two nights in the enclosure (hatchlings 4-5 days old)
confirmed agonistic interactions were already occurring. Frequency of agonistic
interactions was determined from film records for days 6-8 in the 1 week old cohort.
In all six groups of 5 hatchlings, the mean number of agonistic interactions per group
per night was 7.3 ± 0.65 (mean of means; N = 6, range 3-13). The frequency of
agonistic interactions was significantly higher among the older age cohorts (F2,15 =
6.75, P < 0.05), with 9.7 ± 0.61 (N = 6, range 6-14) at 13 weeks old, and 22.2 ± 0.61
(N = 6, range 12-34) at 40 weeks old.
3. Timing
93
For all three age cohorts combined, the frequency of agonistic interactions at dusk
(1700-2000 h), night (2000-0600 h) and dawn (0600-0800 h) varied significantly
(F2,14 = 13.46, P < 0.05). The majority of agonistic interactions occurred in the early
evening (1700-2000 h), with about half as many in the early morning (0600-0800 h)
(Figure 2). Agonistic interactions were rare during the night (2000 to 0500 h), when
the 1 week old hatchlings would often lie together in contact, in the water, in groups
of 2-5 individuals. The 13 and 40 week old hatchlings were non-aggressive during the
same period, but were rarely observed lying in contact with each other.
Figure 2. Percentage of agonistic interactions (%) as a function of hour (1700-0800
h) for C. porosus housed in groups of 5 at three different ages (1, 13 and 40 weeks).
4. Postures
The postures displayed in agonistic interactions, as deemed to be aggressive and non-
aggressive, varied across the three age cohorts (Table 2). When both individuals were
94
aggressive, they typically aligned head to head, usually parallel to each other before
assuming a HTR, IP, or HRH posture (Table 1; Figure 1). At one week old, aggressive
hatchlings were more likely to assume a range of postures during an agonistic
interaction than hatchlings at 13 or 40 weeks, when aggressive individuals adopted
mainly a LIW (83.9-100%) posture. Non-aggressive individuals at 1 week of age
assumed a more diverse range of postures than hatchlings at 13 or 40 weeks, when
HRH, and MA were the most common (Table 2).
Table 2. The percentage of agonistic interactions containing specific postures for
aggressive and non-aggressive hatchling C. porosus at 1, 13, and 40 weeks of age. As
MA can be displayed in conjunction with other postures during an agonistic
interaction, columns do not add to 100%. LIW = low in water; HTR = head and tail
raised; IP = Inflated posture; HRH = head raised high; MA = mouth agape.
1 week 13 weeks 40 weeks
aggressive
non
aggressive aggressive non aggressive aggressive
non
aggressive
Posture
LIW 50.0 40.2 83.9 32.8 100 43.8
HTR 16.7 17.4 1.7 1.7 0 0.0
IP 26.5 16.7 12.1 3.6 0 0.8
HRH 6.8 25.7 2.3 61.9 0 55.4
MA 3.8 0.8 1.1 25.3 0 38.3
5. Non-contact and Contact Movements
After assuming a posture, hatchlings often graduated to non-contact movements by
displaying a series of light jaw claps (LJC) with or without tail wagging (TW). LJCs
were used to indicate aggressive intent, while TW was also displayed by aggressive
individuals to forewarn (threaten) an impending contact movement. Non-aggressive
95
individuals also engaged in TW in anticipation of an attack by an approaching
individual. TW often occurred after LJC, and increased in intensity as an interaction
escalated. The frequency of LJC displayed by aggressive individuals during an
interaction was highest among one week olds (F2,15 = 18.78, P < 0.05; Table 3). The
frequency of tail wagging (TW) was higher for aggressive (F2,15 = 4.01, P < 0.05) and
non aggressive (F2,15 = 4.98, P < 0.05) hatchlings at 1 week of age, and was not
displayed by aggressive individuals at 13 or 40 weeks of age (Table 3).
Contact movements were often adopted after non-contact movements, with TWB
and TWSHS (Figure 1h) being the most aggressive and intense forms. The frequency
of HP’s and B’s was significantly higher among 1 week olds (HP: F2,15 = 21.35, P <
0.05; B: F2,15 = 9.39, P < 0.05), as was the frequency of SHS’s and TWSHS’s (SHS:
F2,15 = 15.79, P < 0.05; TWSHS: F2,15 = 3.76, P < 0.05; Table 3). The frequency of
TWB’s was significantly lower among 1 week olds (F2,15 = 10.63, P < 0.05; Table 3).
The number of agonistic interactions in which contact was made was also lower
among 13 (66.2%) and 40 week old (45.5%) hatchlings (X2 = 106.06, df = 2, P <
0.05), compared with 1 week olds (94.5%). In many cases, the aggressive individual
made an unsuccessful attempt to bite the other animal that fled rapidly, thus avoiding
contact.
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Table 3. The number of different non-contact and contact movements incorporated
into the average agonistic interaction, by aggressive and non-aggressive C. porosus
hatchlings of different ages (1, 13 and 40 weeks). Any one agonistic interaction can
include multiple incidents of each type of movement. LJC = light jaw clap; TW = tail
wag; HP = head push; B = bite; TWB = tail wag bite; SHS = side head strike;
TWSHS = tail wag-side head strike.
1 week 13 weeks 40 weeks
aggressive
non
aggressive aggressive
non
aggressive aggressive
non
aggressive
mean ± se
Non contact
movements
LJC 0.75 ± 0.11 - 0.22 ± 0.04 - 0.02 ± 0.01 -
TW 0.14 ± 0.05 0.50 ± 0.09 0 0.54 ± 0.08 0 0.2 ± 0.02
Contact
movements
HP 0.49 ± 0.07 - 0.06 ± 0.01 - 0.11 ± 0.02 -
B 0.59 ± 0.06 - 0.25 ± 0.04 - 0.31 ± 0.05 -
TWB 0.18 ± 0.04 - 0.77 ± 0.09 - 0.83 ± 0.17 -
SHS 0.09 ± 0.04 - 0.06 ± 0.03 - 0.04 ± 0.01 -
TWSHS 0.40 ± 0.05 - 0.34 ± 0.07 - 0.03 ± 0.01 -
6. Intensity
While low intensity interactions appeared accidental, both medium and high intensity
interactions appeared deliberate. High intensity interactions were distinguished from
medium intensity interactions by the display of more intense contact movements, in
the form of TWB or TWSHS. The intensity of interactions differed among the age
cohorts (X2 = 166.66, df = 4, P < 0.05), with a decrease in low intensity interactions
among 13 and 40 week old hatchlings (Figure 3). There was also more high intensity
interactions at 13 weeks of age compared to 40 weeks of age. The majority of high
97
intensity interactions occurred at dusk (1700-2000 h) and dawn (0600-0800h), while
low intensity interactions predominantly occurred during the night.
Figure 3. The overall percentage of agonistic interactions deemed to be low, medium
or high intensity, over a three night period (1700-0800 h), for C. porosus at 1 week
(a), 13 weeks (b) and 40 weeks (c) of age. All were housed in groups of 5 individuals
with 6 groups for each age class.
7. Duration and Outcome
The mean duration of an agonistic interaction was significantly longer among 1 week
old hatchlings (42.4 ± 2.60, 3 - 149 s; F2,15 = 1.97, P < 0.05) compared with 13 week
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old (22.1 ± 0.90 s, 6 - 59 s) and 40 week old hatchlings (17.6 ± 0.44 s, 5 - 41 s). In the
majority of interactions, the instigator was the winner, although this differed among
age cohorts. At 1 week 25% of instigators lost, whereas at 13 and 40 weeks only 0.6%
and 0.0% lost respectively.
The outcome of an agonistic interaction differed among the different age cohorts.
At 1 week, 56.8% of losers, defined as the least aggressive individual and the first to
back down, took flight slowly (SF; Figure 4), whereas by 13 and 40 weeks, 81.6%
and 100% of losers took flight rapidly (RF), and usually with the aggressive
individual giving chase (C) until the loser left the water (Figure 4).
99
Figure 4. Percentage of C. porosus hatchlings involved in agonistic interactions that
ended in different outcomes at 1 week (a), 13 weeks (b) and 40 weeks (c) of age. All
were housed in groups of 5 individuals with 6 groups for each age cohort.
8. Clutch Specific Differences
A closer look at the ‘sibling only’ groups at one week of age revealed clutch specific
differences in the number of agonistic interactions (F5,12 = 4.0, P < 0.05) with a higher
frequency among groups 1, 3, and 4 compared with those in 5 and 6 (Figure 5).
Groups 1 and 3 also had a higher proportion of high intensity interactions (55%)
100
compared with the other four groups (high intensity: < 25%; X2 = 25.44, df = 10, P <
0.05). While groups 3, 4, 5 all consisted of 4 male and 1 female, groups 1 and 6 had
no females. Consequently, the composition of each group with respect to sexes
present/absent does not correlate with the proportion of high intensity interactions
observed.
Figure 5. Mean number of agonistic interactions between hatchling C. porosus (N=5)
at one week of age in each of the six sibling only groups. Symbols distinguish
different sibling only groups.
Discussion
Within a few days of hatching, captive C. porosus hatchlings tolerate high levels of
close contact with each other, with little aggression, for most of the night. Yet at dusk
(1700-2000 h) and dawn (0600-0800 h), sporadic periods of agonistic interactions
occur between two individuals at any one time. Agonistic behaviour has never been
reported before among crocodiles of this age. During these interactions, hatchlings
101
exhibited a diverse range of behaviour in the form of postures (N=5), non-contact
(N=6), and contact (N=5) movements, and often in combination (Table 1; Figure 1).
No specific vocalizations were noted to accompany these various behaviours, nor
were any sex specific differences apparent. However, the frequency and nature of
agonistic interactions, along with the type and pattern of behaviour displayed, differed
between the three age groups.
1. Agonistic Interactions
Among hatchling C. porosus at 1 week of age, agonistic interactions were not well-
defined, with a higher number of both low intensity interactions (Fig. 3), and
interactions in which both individuals engaged in aggression. These interactions were
longer in duration and more often involved physical contact and resulted in the
instigator losing. The full repertoire of behaviour (Table 1) was displayed by
hatchling C. porosus at this age, while there were also clutch specific differences in
the frequency of agonistic interactions, suggesting a genetic and, or maternal
component. A similar undefined pattern of behaviour, characterised by unstructured
interactions in which all individuals often display both aggressive and submissive
behaviour has also been reported in several species of birds (Drummond, 2001),
mammals (Bekoff et al., 1981; Smale et al., 1995), and other reptiles (Burghardt,
1977; Drummond, 2006) that exist in social groups shortly after birth.
Among hatchlings at 13 and 40 weeks of age, agonistic interactions were an
‘aggression-submission’ form of dominance relationship (Drummond, 2006), with a
102
more defined pattern of behaviour, in which individuals had a distinct role as either a
dominant or a subordinate. Interactions were of a medium to high intensity and more
frequent, especially among 40 week old hatchlings, although the duration was shorter.
A number of the behaviours initially displayed among hatchlings at 1 week of age
were either rarely displayed, or no longer present among hatchlings at 13 and 40
weeks of age. Instead, most interactions were characterised by a dominant individual
approaching another in a series of rapid advances (RA) while remaining low in the
water (LIW), almost as if stalking prey. In response, the subordinate individual often
adopted a head raised high (HRH) posture, combined with mouth agape (MA) to
indicate submission before taking flight rapidly (RF). The dominant animal would
then chase (C) the subordinate, while attempting a bite (B), until the subordinate left
the water area. In contrast with one week old hatchlings, individuals at 13 and 40
weeks of age were also rarely observed lying together at any time. These results
support the theory that dispersal by hatchling C. porosus may be driven by a growing
intolerance of conspecifics (Webb & Messel, 1978).
2. Dominance Hierarchy
This study suggests that agonistic interactions between C. porosus immediately post-
hatching, when hatchlings would naturally exist together in crèches (Webb & Messel,
1978), may be important in the initial establishment of dominance. This pattern
appears to be a common strategy for many reptiles that exist in social groups for a
short period after birth (Burghardt, 1977; Stamps & Tanaka, 1981; Phillips et al.,
1993). Hatchling C. porosus are clearly born with the ability to display a wide range
103
of agonistic behaviour, but as they grow, these are replaced by a simpler subset of
behavioural interactions based on social status. When C. porosus in the wild would
naturally disperse around 13 weeks of age, subordinate individuals clearly recognise
aggression displayed by dominant individuals, and have learnt to avoid physical
contact (and thus potential injury) by indicating submission and by promptly fleeing.
At 40 weeks of age, C. porosus are much larger in size, and in the wild would be
largely solitary.
The development of agonistic interactions in hatchling C. porosus is indicative of
an increasingly well-defined dominance hierarchy in this species, characterised by a
clearly recognisable, asymmetrical pattern of aggression-submission interaction
(Drummond, 2006). This pattern of dominance, in which an aggressive display by one
individual elicits a submissive response without aggression in the other, has also been
reported in birds (Drummond, 2001), mammals (Smale et al., 1995; Bekoff et al.,
1981), and fish (Bergman, 1968), and appears typical for C. porosus in general based
on the limited information available (Messel et al., 1981; Lang, 1987; Riese, 1991;
Brien pers. observation).
Both Riese (1991) and Messel et al. (1981) report an almost identical dominance
pattern among hatchling C. porosus (3-50 weeks post hatch) in captivity and juvenile
and subadult C. porosus (90-240 cm total length) in the wild respectively, with most
interactions occurring in shallow water near the bank. In the majority of cases, the
dominant animal would approach low in the water, while the subordinate would
respond by raising the head up high, before fleeing rapidly with the dominant animal
104
giving chase. To escape, the subordinate individual often ran up on land, which
caused the dominant animal to cease chasing.
Although a number of species are equipped with the ability to inflict serious
damage and even death in conspecifics (eg. teeth, horns), this rarely occurs because
the majority have evolved strategies to minimize the chance of injury, which in most
cases takes the form of a dominance hierarchy (Carpenter & Ferguson, 1977;
Lumsden & Holldobler, 1983). This also appears to be the case in C. porosus, a
species with a formidable armoury that has long been regarded as the most aggressive
of all crocodilians (Lang, 1987). After hatchling C. porosus have dispersed from the
crèche (<13 weeks; Webb & Messel, 1978), they tend to be largely solitary and
nomadic as juveniles and sub-adults, and may only encounter other crocodiles
infrequently (Webb & Messel, 1978). As has been reported in lobsters (Huber &
Kravitz, 1995) and mice (Terranova et al., 1998), the early development of a defined
and clearly recognisable pattern of aggressive-submissive behaviour seems to enable
older C. porosus to resolve conflict rapidly and without injury when they do
encounter a conspecific.
The nature and ontogeny of agonistic behaviour and dominance hierarchies can
vary greatly both within and between taxa (Lovern & Jennssen, 2001; Drummond,
2006). Although little is known regarding agonistic behaviour and dominance in
crocodilians, a similar behavioural study involving captive Australian freshwater
crocodiles (C. johnstoni), a species regarded as gregarious and highly tolerant of
conspecifics, was recently undertaken (Brien et al., unpublished). In contrast to C.
105
porosus, no such dominance hierarchy was present among C. johnstoni at 13 or 50
weeks of age. Typically, aggressive interactions between hatchling C. johnstoni were
also less frequent and intense, and less one-sided than in hatchling C. porosus, while
grouping was also common among C. johnstoni at 50 weeks of age. These differences
are likely due to distinct morphological and ecological differences between these
species, and further studies with other crocodilian species will likely demonstrate
further variation.
3. Territoriality
Sub-adult and adult C. porosus are known to be highly territorial, with larger
crocodiles often preventing smaller ones from accessing particular resources such as
basking sites, food, shelter and water (Lang, 1987; Grigg & Seebacher, 2000). While
agonistic interactions between hatchling C. porosus in this study often resulted in
temporary displacement, this did not result in hatchlings of any age being permanently
excluded from any area or resource (eg. food) within the enclosure. However, among
hatchling C. porosus at 13 and 40 weeks of age, shallow, open water areas appear to
be an important resource, with dominant individuals clearly attempting to exclude
others from it during periods of aggression (dusk and dawn).
Messel et al., 1981 also reported resident juvenile (90-240 cm total length) C. porosus
in the wild chasing conspecifics from areas of shallow water near the bank. Although
dependent largely upon the availability of resources, which can often be limited in
captivity, taken together, this indicates that territoriality may occur early in juvenile C.
porosus (Bustard and Maharana, 1983). It also suggests that shallow water near the
106
bank may be a critical resource, at least for smaller C. porosus, which is where they
tend to feed and would be less vulnerable to aquatic predators (Lang, 1987).
4. Agonistic Behaviour
The range of postures, non-contact, and contact movements displayed by hatchling C.
porosus is similar to those observed for juveniles and adults of other species of
crocodilian (Garrick & Lang, 1977; Vliet, 1989; Lang, 1987), including C. porosus
(Webb & Manolis, 1989; Brien pers. obs). This suggests that C. porosus, and possibly
most species of crocodilian, may have a pattern of signal or behavioural ontogeny
commonly seen in some lizards (Cooper, 1971; Stamps, 1978; Lovern & Jenssen,
2001), in which individuals are born with almost the full repertoire of agonistic
behaviour. While conditions experienced in captivity might expedite the onset and
development of agonistic behaviour in hatchling C. porosus, the results still illustrate
the potentially innate nature of agonistic behaviour in this species.
While a number of the behaviours displayed by hatchling C. porosus appear to be
standard forms of communication during agonistic interactions among crocodilians in
general, several also appear common in other taxa. The raising of the head up high on
an angle (HRH), or snout lifting (Garrick & Lang, 1977), is a clear indication of
submission in crocodilians, while raising or inflating the whole body (HTR, IP)
signals aggression (Garrick & Lang, 1977; Vliet, 1989; Senter, 2008). Raising or
inflating the body is commonly used by many taxa to indicate aggressive intent,
including lizards (Burghardt, 1977; Stamps, 1983), salamanders (Staub, 1993), and
107
crustaceans (Huber & Kravitz, 1995).
The clapping of the jaws together by crocodilians either lightly, in the case of
hatchling C. porosus, or as an intense event producing a loud noise in adults, is also
used to signal aggression (Garrick & Lang, 1977; Lang, 1987), while tail wagging
(TW) is often performed by subordinates and indicates stress or high agitation
(Garrick & Lang, 1977). In all crocodilians studied to date, both behaviours appear to
be graded signals, indicating differing degress of intensity, from low to high. Jaw
clapping, or snapping, also occurs in Plethodontid salamanders to signal aggressive
intent (Staub, 1993), while rapid twitching of the tail from side to side has been
reported in lizards (Carpenter et al., 1970; Torr & Shine, 1994), mice (Terranova et
al., 1998), and salamanders (Staub, 1993), to indicate high agitation or stress rather
than a ritualised social signal.
5. Management Implications
The presence of agonistic behaviour involving physical contact among hatchling C.
porosus at one week of age, along with clutch specific differences, has potentially
important implications for raising hatchling C. porosus in captivity. As with a number
of other species of reptiles (Carpenter & Ferguson, 1977; Phillips et al., 1993; Goetz
& Thomas, 1994; Worner, 2009), high levels of aggression may be responsible for
divergent patterns of growth among hatchling C. porosus in captivity, and may be
linked to lower survivorship among slow-growing animals (Bustard and Maharana,
1983; Isberg et al., 2009). If so, husbandry techniques that reduce the frequency of
108
agonistic interactions may improve growth and survival of hatchling C. porosus raised
for farming or conservation purposes.
Acknowledgements
We thank Chris Gienger, Jemeema Brien, and Charlie Manolis for their help in
different phases of the project. We would also like to thank Wildlife Management
International for the supply of animals, use of facilities, logistical support and major
funding for this project. WMI funding through the Rural Industries Research and
Development Corporation is gratefully acknowledged. Funding for cameras and
digital video recorders was provided through a Holsworth Wildlife Research
Endowment (ANZ Trustees Foundation), Northern Territory Research and Innovation
Board student grant, IUCN-SSC Crocodile Specialist Group Student Research
Assistance Scheme grant, and Charles Darwin University. Experimental protocols
were approved by the Charles Darwin University Animal Ethics Committee (Animal
ethics permit number A11003).
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Chapter 3.2. Intra- and interspecific agonistic behaviour in hatchling
Australian freshwater crocodiles (Crocodylus johnstoni) and
saltwater crocodiles (Crocodylus porosus)
Published as: ‘Brien, M.L., Webb, G.J., Lang, J.W., McGuinness, K.A., Christian,
K.A. 2013. Intra- and interspecific agonistic behaviour in hatchling Australian
freshwater crocodiles (Crocodylus johnstoni) and saltwater crocodiles (Crocodylus
porosus). Australian Journal of Zoology 61: 196-205’. Formatted according to author
guidelines for journal.
Abstract
We examined agonistic behaviour in hatchling Australian freshwater crocodiles
(Crocodylus johnstoni) at 2-weeks, 13-weeks, and 50 weeks after hatching, and
between C. johnstoni and saltwater crocodiles (Crocodylus porosus) at 40–50 weeks
of age. Among C. johnstoni, agonistic interactions (15–23 seconds duration) were
well established by two weeks old and typically involved two and occasionally three
individuals, mostly between 17:00–24:00 h in open water areas of enclosures. A range
of discrete postures, non-contact and contact movements are described. The head is
rarely targeted in contact movements with C. johnstoni because they exhibit a unique
‘head raised high’ posture, and engage in ‘push downs’. In contrast with C. porosus of
a similar age, agonistic interactions between C. johnstoni were conducted with
relatively low intensity, showed limited ontogenetic change, and there was no
evidence of a dominance hierarchy among hatchlings by 50 weeks of age, when the
frequency of agonistic interactions was lowest. Agonistic interactions between C.
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johnstoni and C. porosus at 40–50 weeks of age were mostly low level, with no real
exclusion or dominance observed. However, smaller individuals of both species
moved slowly out of the way when a larger individual of either species approached.
When medium or high level interspecific interactions did occur, it was between
similar-sized individuals, and each displayed species-specific behaviours that
appeared difficult for contestants to interpret: there was no clear winner of loser. The
nature of agonistic interactions between the two species suggests that dominance may
be governed more strongly by size rather than species-specific aggressiveness.
Introduction
Agonistic behaviour is any behaviour relating to aggression including threat, display,
attack, submission and flight (Tinbergen 1952; 1953; Wilson 1975). Agonistic
behaviour plays a crucial role in determining access to resources such as food, shelter
and mates in many species of bird (Drummond 2001), reptile (Phillips et al. 1993),
crustacean (Huber and Kravitz 1995), fish (Genner et al. 1999), and amphibian (Staub
1993). For many of these species, agonistic behaviour starts shortly after birth and is
important in the formation of dominance hierarchies and in determining future rates of
growth and survival (Tinbergen 1953; de Waal and Luttrell 1989; Drummond 2006).
Therefore, studies of agonistic behaviour during early development can greatly
improve our understanding of the social structuring and population dynamics of a
species.
The role of agonistic behaviour in interspecific competition is not as well
understood. It can be expected to occur between species that exist in sympatry and
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utilise similar resources (Brown and Wilson 1956; Ricklefs 1990), and may well
contribute to divergence in morphology, behaviour and ultimately niche partitioning
(Brown and Wilson 1956; Adams 2004), as proposed for mammals (Stoecker 1972;
Pereira and Kappeler 1997; Aguirre et al. 2002), birds (Schoener 1965; Murray 1971;
Smith 1990), salamanders (Jaeger 1972; Adams 2004), fish (Newman 1956) and
crustaceans (Bovbjerg 1970).
Knowledge of agonistic behaviour in crocodilians is mostly associated with adults
and breeding biology, in wild and captive situations (Cott 1961; Pooley 1969; Garrick
and Lang 1977; Garrick et al. 1978; Vliet 1989; Thorbjarnarson 1991). With
saltwater crocodiles (Crocodylus porosus), which are considered the most aggressive
of extant crocodilian species (Lang 1987), they begin life in hatchling crèches and
dominance hierarchies become established within the first three weeks of life (Brien
et al. 2013). Intolerance of conspecifics has long been implicated in their dispersal
from crèches after a few months, and in the later spatial separation of juveniles and
adults (Webb et al. 1977; Messel et al. 1981; Lang 1987). The degree to which
agonistic behaviour occurs in less aggressive crocodilian species is unknown.
Australian freshwater crocodiles (Crocodylus johnstoni) are regarded as one of the
least aggressive crocodilians (Lang 1987). Like C. porosus, they exist in crèches after
hatching, but unlike C. porosus, juvenile and adult C. johnstoni often congregate at
high densities during the annual dry season (Webb et al. 1983a; Kennett and Christian
1993). They thus appear much more tolerant of conspecifics, although some discrete
behaviours such as tail raking, are implicated in dominance hierarchies (Webb et al.
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1983c). Although C. johnstoni and C. porosus have largely allopatric distributions in
northern Australia, they also coexist within zones of sympatry in some rivers and
wetlands (Webb et al. 1983a). Despite the larger size of adult C. porosus, and the
strong possibility that adult C. porosus may control C. johnstoni populations in such
zones (Webb et al. 1983a), juveniles of each species live together with similar size-
specific morphology, diet and spatial needs (Messel et al. 1981; Webb et al. 1983a),
which is reasonably uncommon in situations where crocodilian distributions overlap
(Ouboter 1996; Thorbjarnarson et al. 2006).
The present study was undertaken with two primary aims. Firstly, to describe
agonistic behaviour in hatchling C. johnstoni, and determine whether the nature and
ontogeny is similar to that observed in hatchling C. porosus (Brien et al. 2013).
Secondly, to examine how C. johnstoni and C. porosus respond during agonistic
interactions involving both species.
Materials and methods
Subjects and housing
In December 2011, 70 hatchling Australian freshwater crocodiles (Crocodylus
johnstoni), in three age cohorts, were provided by Wildlife Management International
(WMI; Darwin, Australia). All had been captured in the wild from crèches when <1
week post-hatching (based on size and extent of yolk scar healing), and were almost
certainly siblings. The first cohort (n = 25) contained individuals from five different
clutches (20 males, 5 females), two weeks after hatching, while the second (13 weeks
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after hatching; n = 25; 19 males, 6 females) and third (50 weeks after hatching; n =
25; 20 males, 5 females) cohorts contained hatchlings from a further six and seven
different clutches respectively, that were of similar size and age. These age cohorts
were based on the early life history of C. johnstoni which is similar to that described
for C. porosus (Brien et al. 2013). This also enabled direct comparisons. Using the
same crocodiles throughout the study was initially considered but not feasible, due to
the highly variable nature of growth within and between different clutches for this
species and crocodilians in general, which can lead to significant differences in size
and high rates of mortality during the first year of life under captive conditions (Webb
et al. 1983b; Brien et al. 2013).
Hatchling C. johnstoni of different ages were transferred to experimental
enclosures and housed in groups of five individuals for the duration of the study. For
each animal, snout-vent length (SVL to the front of the cloaca - mm), total length (TL
in mm), and body mass (BM in g) were measured and a uniquely numbered metal
webbing tag (Small animal tag 1005-3, National Band and Tag Co.) was attached to
the rear back right foot. Mean size of crocodiles at the initiation of observations were:
2-week olds, 110.5 ± 0.5 mm SVL, 245.3 ± 1.1 mm TL, and 42.7 ± 0.8 g mass; 13-
week olds, 147.0 ± 1.7 mm SVL, 316.8 ± 2.8 mm TL and 76.3 ± 1.8 g mass; 50 week
olds, 305.5 ± 1.7 mm SVL, 618.8 ± 2.3 mm TL, and 628.2 ± 14.5 g mass.
In February 2012, 12 hatchling C. porosus at 40 weeks after hatching (10 male, 2
female) and 12 hatchling C. johnstoni of a similar size and age (50 week after
hatching, 9 male, 3 female) were also provided by WMI. However, while the three
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age cohorts of C. johnstoni were all captured from the wild, the 40 week old C.
porosus were from seven different clutches of eggs artificially incubated in captivity
(see Brien et al. 2013). In the wild, this is the age and, or size at which C. johnstoni
and C. porosus are naturally found occupying similar habitat (Webb et al. 1983a).
Hatchlings of both species were transferred to experimental enclosures and housed in
six groups of four individuals (2 C. porosus and 2 C. johnstoni), each containing two
similar size ‘large’ crocodiles of each species (CJ: 345.2 ± 3.7 mm SVL, 700.5 ± 7.4
mm TL, 957.2 ± 34.7 g mass; CP: 348.8 ± 3.1 mm SVL, 709.7 ± 6.7 mm TL, 952.2 ±
24.8 g mass) and two similar size ‘small’ crocodiles of each species (CJ: 305.5 ± 1.7
mm SVL, 618.8 ± 2.3 mm TL, 628.2 ± 14.5 g mass; CP: 300.3 ± 2.8 mm SVL, 624.0
± 3.9 mm TL, 632.2 ± 10.8 g mass).
The fibreglass enclosures in which the experimental groups (C. johnstoni only, C.
johnstoni and C. porosus combined) were housed were box shaped (170 x 100 x 50
cm), with a land area (70 x 100 cm) that gradually sloped down to a water area (100 x
100 cm; < 8 cm deep). Therefore, all hatchlings were at a density of 2.9 animals per
m2 which was considered very low based on previous studies (Riese 1991; Mayer
1998). A ‘hide area’ (Riese 1991; Mayer 1998; Davis 2001) was provided in each
enclosure, and was constructed with eight lengths of PVC pipe (80 cm long; 10 cm
diameter) strapped together and on legs, centrally positioned in the water (partly
immersed) and overhanging the land. Water temperatures were maintained at 30–
32°C, and air temperatures varied from 26–32°C, with a natural light cycle. All
animals were fed chopped red meat supplemented with di-calcium phosphate (4%)
and a multivitamin supplement (1%), which is the standard diet fed to hatchling C.
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johnstoni and C. porosus in captivity. Enough food for each individual was made
available throughout the night (16:00–17:00 h), which is when hatchling C. johnstoni
and C. porosus are known to feed in captivity and in the wild (Lang 1987; Brien et al.
2013). Waste removal and cleaning occurred the following morning (08:00–09:00 h)
when the water was changed. Hatchlings of both species were subject to the same
raising conditions (enclosure, temperature, density, and husbandry) prior to, and
during the experiments.
Recording behaviour
Wide angle infrared CCTV cameras (Signet, 92.6º) in each enclosure were used to
record all behaviour on digital video recorders (Signet 4CH QV–8104). For the three
cohorts of C. johnstoni, a recording period lasted 15 hours (17:00–08:00 h), and was
conducted on three consecutive nights for each group (45 h per group). To allow for
settling, the recordings were taken 4–5 days after the crocodiles were placed in the
new experimental enclosures. This night-time sampling period was based on previous
recordings (100’s of hours) that revealed no agonistic behaviour in C. johnstoni
hatchlings between 08:00 and 17:00 h, when they were inactive and under cover. For
the mixed species groups, recordings were only taken during the first two nights
(17:00–08:00 h) when, from previous experience, the level of aggression and
frequency of interactions is typically high. Despite the documented importance of
vocalisations during crocodilian communication at all life stages (Lang 1987),
especially among hatchlings and juveniles, no audio was recorded during this study
due to limitations of the recording equipment.
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Agonistic interactions
An agonistic interaction was defined as any interaction between individuals in which
aggression and intolerance appeared to be signalled by postures or actions by one or
more individuals. An aggressive individual was one that made deliberate advances
toward another, or that made physical contact with another. Each agonistic interaction
was described in terms of whether one or both contestants engaged in aggression, and
the intensity (low, medium, high) demonstrated. Low intensity interactions appeared
accidental, occurring when individuals lying together disturbed each other when
moving, or if one swam into another underwater. Medium and high intensity
interactions appeared deliberate, with one individual approaching another with the
apparent goal of initiating an agonistic interaction. High intensity interactions were
distinguished from medium intensity interactions by the display of more intense
contact behaviours. The behaviour exhibited, the intensity of interaction (low,
medium, high), the location (water, hide, land), the time, duration of interaction and
outcome were all obtained from the videos, as previously described for C. porosus
(Brien et al. 2013).
Classification of behaviour
Behavioural observations recorded during these experiments were used to create an
inventory of agonistic behaviours for C. johnstoni hatchlings, similar to that described
for hatchling C. porosus (Brien et al. 2013). The descriptions are based on a series of
basic postures, modified by movement of body parts, or of the whole animal, and
whether visual signals or actual contact was involved. Some of these behaviours have
been described in studies with adult crocodilians (Garrick and Lang 1977; Lang
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1987).
Statistical analyses
All statistical analyses were performed using JMP 8.0 statistical software (SAS
Institute Inc. 2010). Where appropriate, data were checked for normality (Shapiro–
Wilk’s test) and homoscedasticity (Cochran’s test) prior to statistical analysis. A
repeated-measures ANOVA was used for comparison of means between 2-, 13-, and
50-week-old hatchlings, with consecutive night of recording (N = 3) as the repeated
measure. A Pearsons’ Chi-square test was used to compare intensity, outcome, contact
made, number of individuals being aggressive, and how often the instigator won,
where sample sizes were adequate. To test whether variation in the frequency of
interactions could be explained by time of day, the results were grouped into one of
three periods: dusk 17:00–20:00 h; night 20:00–06:00 h; and dawn 06:00–08:00 h. A
significance level of P < 0.05 was used for all statistical tests. All means are reported
± one standard error with sample sizes.
Results
The majority of agonistic interactions between hatchling C. johnstoni involved two
individuals in open water, with none observed on the land or near food (on land).
However, there were two interactions at 13 weeks and three at 50 weeks in which 3–4
individuals were involved in an agonistic interaction. Some interactions appeared to
occur accidentally when individuals lying together disturbed each other when moving
off, or if one swam into another underwater. However, interactions were also initiated
either by one or both individuals moving toward each other in a series of short, rapid,
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deliberate advance movements (RA). In response to RA, one or both individuals
would adopt a series of other agonistic behaviours that involved the adoption of some
discrete postures that varied in the intensity of expression (Table 1; Fig. 1).
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Table 1. Classification of the behaviour used by hatchling C. johnstoni during
agonistic interactions. Responses to aggression can be graded, involving the adoption
of static postures, followed by non-contact movements followed again by contact
movements. This table has been adapted from Brien et al. 2013. * = has not been
previously described, or is different in some way.
Abbreviation Definition
Initiation
Rapid advance RA Series of short rapid advance movements towards
another individual while LIW.
Termination
Slow flight SF Slow movement away from another individual in a
LIW posture.
Rapid flight RF Rapid movement away from another individual in a
LIW posture.
Posture
Low in water LIW Immobile with only the top of the head and back
above the water surface.
Head raised high HRH* Immobile with upward extension of the head high
out of the water on a ~45º angle while tail remains
low. However, unlike C. porosus, body remains low
in water.
Mouth agape MA Immobile with mouth opened wide (in combination
with postures LIW, IP, HTR or HRH).
Non-contact movement
Light jaw–clap LJC Rapid opening and closing of the jaws at the water
surface, often repeated several times (LIW posture).
Tail–wagging TW Undulation of the tail from side to side in either a
gentle sweeping motion or rapid twitching, often
repeated several times (all postures).
Contact movement
Head push HP Head is pushed in to an opponent, usually with
mouth closed (LIW posture).
Push down PD* Chest and neck of individual pushed down on the
upper neck or back of an opponent (HRH posture).
Bite B Jaws closed shut on an opponent (all postures).
Side head-strike SHS Head is thrust sideways in to an opponent while the
mouth is either open or closed (all postures).
Tail–wag bite TWB Tail wagging occurs prior to a bite and propels the
individual into an opponent with force (LIW
posture).
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Figure 1. Push down (PD) contact movement (a) displayed exclusively by hatchling
C. johnstoni during agonistic interactions and head raised while resting (non-
aggressive) (b) at 2 weeks, 13 weeks and 50 weeks of age, described in Table 1.
The adoption of such postures could be abandoned at any time by either slow (SF)
or rapid flight (RF), ending the agonistic interaction. Alternatively, the signals
emanating from the postures could be intensified with body movements, such as light
jaw claps (LJC) or tail wagging (TW), which were displays not involving physical
contact with combatants. If the interaction was still not terminated by flight of one or
both animals, the behaviour intensified further, with contact movements such as head
pushing (HP), or biting (B), occasionally combined in different ways with intense tail
wagging (TWB), or side head striking (SHS), until one or both individuals took flight.
Another contact movement unique to C. johnstoni was a push down (PD) (Fig. 1).
When crocodiles were not engaged in aggression and were at rest, they typically lay
with their head raised up on an angle, appearing as if on look out (Fig. 1).
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Aggression
An aggressive individual was defined as one that made deliberate advances toward
another and, or which made physical contact with another animal. Each agonistic
interaction was examined to quantify whether one or both contestants engaged in
aggression, and whether this differed across age classes. The number of interactions in
which both individuals appeared aggressive was similar for all age classes (X2 = 2.48,
df = 2, P > 0.05), with 31.7% at 2 weeks, 41.2% at 13 weeks and 40% at 50 weeks.
The number of separate movements or steps in the RA did not change significantly
with age (F2,12 = 1.04, P > 0.05), with a mean of 1.9 ± 0.10 steps (mean of means;
range 0–4; n = 15) per interaction.
Frequency
The mean number of agonistic interactions per group per night at two weeks of age
was 6.9 ± 0.42 (mean of means; n = 5, range 5–10). The frequency of agonistic
interactions was significantly lower among the older age cohorts (F2,10 = 20.55, P <
0.05), with 5.7 ± 0.35 (n = 5, range 4-9) at 13 weeks, and 2.8 ± 0.86 (n = 5, range 2–5)
at 50 weeks.
Timing
For all three age cohorts combined, the frequency of agonistic interactions at dusk
(17:00–20:00 h), night (20:00–06:00 h) and dawn (06:00–08:00 h) varied significantly
(F2,11 = 6.99, P < 0.05). The majority of agonistic interactions occurred throughout the
night (17:00–02:00 h), and were lower during the early morning (Fig. 2). Outside of
agonistic interactions, hatchlings of all ages would often lie together in contact, in the
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water, in groups of 2–5 individuals. The 2- and 13-week-old hatchlings would retreat
under the hide and were rarely visible after 06:00 h.
Figure 2. Percentage of agonistic interactions (%) as a function of hour (17:00–08:00 h) for
C. johnstoni housed in groups of 5 at three different ages (2, 13 and 50 weeks).
Postures
The postures displayed in agonistic interactions, as deemed to be aggressive and non-
aggressive, varied among the three age cohorts (Table 2). At two weeks old, all
hatchlings typically remained LIW (~80%) during an interaction (Table 2). The
number of aggressive hatchlings observed in an HRH posture during an agonistic
interaction was significantly higher among the older age cohorts (X2 = 29.06, df = 2, P
< 0.05), while the number of non-aggressive individuals observed in an HRH posture
during an interaction was highest among 50-week-olds (X2 = 10.39, df = 2, P < 0.05;
Table 2). The number of hatchlings with MA was higher among the older age cohorts
for both aggressive and non-aggressive individuals (Table 2).
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Table 2. The percentage of agonistic interactions containing specific postures for
hatchling C. johnstoni at 2, 13 and 50 weeks of age deemed aggressive and non-
aggressive. As MA can be displayed in conjunction with other postures during an
agonistic interaction, columns do not add up to 100%. LIW, low in water; HRH, head
raised high; MA, mouth agape.
Posture 2 weeks 13 weeks 50 weeks
Aggressive Non-
aggressive
Aggressive Non-
aggressive
Aggressive Non-
aggressive
LIW 82.5 80.3 63.3 88.8 45.0 56.0
HRH 17.5 19.7 36.7 12.0 55.0 44.0
MA 0 1.4 2.5 8 8.3 12.0
Non-contact and contact movements
After assuming a posture, hatchlings often graduated to non-contact movements by
displaying a series of LJC’s with or without TW. LJCs appeared to indicate
aggressive intent, while TW was also displayed by aggressive individuals and
appeared to forewarn (threaten) of an impending contact movement. Non-aggressive
individuals also engaged in TW which appeared to signal anticipation of an attack by
an approaching individual. TW often occurred after LJC, and increased in intensity as
an interaction escalated. LJC’s were only displayed by aggressive individuals at two
weeks of age, while the display of TW by aggressive and non-aggressive individuals,
despite being infrequent, was displayed at both two weeks and 50 weeks of age (Table
3).
Contact movements were often adopted after non-contact movements. The
frequency of HP’s was significantly higher at two weeks of age (F2,12 = 3.60, P <
0.05), while the frequency of PD’s was slightly higher at 13 and 50 weeks of age
(F2,12 = 0.76, P < 0.05; Table 3). The frequency of B’s was similar for all age cohorts
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(F2,12 = 0.34, P > 0.05), while SHS’s were infrequent (Table 3). The number of
agonistic interactions in which contact was made did not change significantly with
age (X2 = 0.70, df = 2, P > 0.05), with an average of 90% for all three age groups (2
weeks: 92.7%; 13 weeks: 92.5%; 50 weeks: 90.3%).
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Table 3. The number of different non-contact and contact movements incorporated into the average agonistic interaction, by aggressive and non-
aggressive C. johnstoni hatchlings of different ages (2-, 13-, 50-weeks-old). Any one agonistic interaction can include multiple incidents of each
type of movement. LJC, light jaw clap; TW, tail wag; HP, head push; B, bite; PD, push down; SHS, side head strike. For each measure mean ±
SE is presented.
Movement 2 weeks 13 weeks 50 weeks
Aggressive Non-
aggressive
Aggressive Non-
aggressive
Aggressive Non-
aggressive
Non contact movements
LJC 0.30 ± 0.06 - 0 - 0 -
TW 0.03 ± 0.02 0.05 ± 0.03 0 0.04 ± 0.03 0.03 ± 0.03 0.07 ± 0.07
Contact movements
HP 0.91 ± 0.09 - 0.30 ± 0.03 - 0.20 ± 0.06 -
PD 0.07 ± 0.02 - 0.23 ± 0.03 - 0.55 ± 0.19 -
B 0.91 ± 0.12 - 0.61 ± 0.05 - 0.88 ± 0.15 -
SHS 0.07 ± 0.03 - 0.02 ± 0.01 - 0.07 ± 0.05 -
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Intensity
While low intensity interactions appeared accidental by definition, both medium and
high intensity interactions appeared deliberate. High intensity interactions were
distinguished from medium intensity interactions by the display of more intense
contact movements, in the form of TWB. The majority of interactions between
hatchlings of all ages were mostly low or medium intensity, with only two high level
interactions observed between hatchlings at 50-weeks-old. The proportion of low and
medium level interactions did not differ with age (X2 = 2.98, df = 2, P > 0.05).
Duration and outcome
The mean duration of an agonistic interaction was similar between two week (16.1 ±
1.32 s, 5–120 s) 13 week (15.6 ± 0.97 s, 5–50 s) and 50-week-old hatchlings (23.0 ±
3.3 s, 6–88 s) (F2,12 = 0.31, P > 0.05). The instigator in the majority of agonistic
interactions was usually the winner, and this did not change with age (X2 = 2.14, df =
2, P > 0.05).
The outcome of an agonistic interaction did not differ between the three age groups
(X2 = 19.85, df = 8, P > 0.05). The most common outcome was that both individuals
stood their ground (37.7%), or the loser, defined as the least aggressive individual and
the first to back down, took flight slowly (SF: 27.7%). Very few interactions (4.5%)
resulted in the loser taking flight rapidly (RF).
Interspecific agonistic interactions
Among groups containing hatchling C. johnstoni (1 small, 1 large) and C. porosus (1
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small, 1 large) of a similar size and age, a mean of 11.2 ± 1.2 (mean of means, range
8-16) agonistic interactions was observed mostly (46.3%) around dusk (17:00-20:00
h). The majority of these interactions (74%) were low intensity and involved both
species and sizes, with biting the most common behaviour (92.4%). Individuals of
both species were commonly observed lying together or near each other, with no
obvious partitioning, exclusion or dominance observed. However, size did vary within
groups and if a larger animal approached a smaller one, regardless of species, the
smaller individual would move slowly out of the way in response. There was also a
clear distinction between the two species while at rest, with C. porosus remaining
LIW and C. johnstoni lying with the head raised (Fig. 1).
The few medium and high intensity agonistic interactions observed occurred
between individuals of the same size (different species). During these interactions,
individuals displayed a species-specific pattern of behaviour, described for C.
johnstoni at 50-weeks-old in this study, and for C. porosus at 40-weeks-old in Brien et
al (2013). The typical pattern involved C. porosus rapidly advancing (RA) towards C.
johnstoni. However, unlike agonistic interactions between two C. porosus, where this
behaviour clearly signals dominance and elicits rapid flight (RF) in the other animal,
C. johnstoni would stand its ground and appeared unclear about the intended message.
In some cases, due to the lack of response in C. johnstoni, the interaction would end.
However, if C. porosus continued to RA, C. johnstoni would respond by lifting its
head high in the air (HRH). The interaction would then escalate with C. porosus
remaining low in the water (LIW), biting (B) and side head striking (SHS), while C.
johnstoni would push down (PD) on the top of C. porosus and occasionally bite (B).
138
This resulted in the two individuals moving together in a circular motion and
becoming entangled. Both individuals appeared confused by this species–specific
behaviour, and the interaction would end with both lying together, often entangled, or
swimming away slowly with no clear winner.
Discussion
Within two weeks post–hatching, captive C. johnstoni hatchlings tolerated high levels
of close contact with each other with little evidence of aggression. C. johnstoni at all
ages (2-, 13-, and 50-weeks-old) regularly grouped together throughout the evening.
Agonistic interactions typically involved contact between two or more individuals, but
were of low intensity, and halved in frequency by the end of the first year. Clear
dominance or submissive outcomes from an interaction were infrequent, and there
was no evidence of a dominance hierarchy within groups by 50 weeks of age.
Agonistic behaviour
Hatchling C. johnstoni exhibited a diverse repertoire of postures (n = 3), non-contact
movements (n = 5) and contact movements (n = 6) that were utilized in agonistic
interactions. All of these behaviours were displayed by individuals at two weeks of
age, and most were utilized in similar contexts, with few ontogenetic changes during
the first year of life. None of the behaviours appeared to be sex specific, and while
vocalisations may play an important role in agonistic interactions, audio was not
recorded in this study. One behaviour, a push-down contact movement (=PD) in C.
johnstoni has never been observed in C. porosus hatchlings under the same
conditions. The other 13 behaviour components listed in Table 4 were shared between
139
the two species.
140
Table 4. Comparison of the behavioural repertoire of hatchling C. johnstoni and C. porosus during agonistic interactions at various stages (in
weeks) to illustrate shared and species-specific behaviours, and ontogenetic changes. N: neutral, behaviour equally likely to be aggressive or
submissive; A: aggressive, behaviour by aggressive animal; S: submissive, behaviour by submissive individual; ( ): parentheses indicate
behaviour performed at low frequency or rarely observed.
C. porosus C. johnstoni
Agonistic
behaviour
Present
in both
species
Hatchling age
Change in
behaviour
with age
Hatchling age
Change in
behaviour with
age
1
week
13
weeks
40
weeks
2
weeks
13
weeks
50
weeks
Posture
LIW Yes N A A increase N N N decrease
IP No N A absent decrease
HTR No N (N) absent decrease
HRH Yes (S) S S increase N (A) N increase
MA Yes A S S increase N (S) N increase
Non-contact movement
RA Yes A A A increase A A A same
SF Yes N S (S) decrease N N S same
141
RF Yes N (S) S increase (N) (N) (N) same
LJC Yes A A (A) decrease (A) absent absent decrease
TW Yes N S (S) decrease (N) (N) (N) same
Contact movement
HP Yes A A A decrease A A (A) decrease
PD No (A) A A increase
B Yes A A A decrease A A A same
SHS Yes (A) (A) (A) same (A) (A) (A) same
TWSHS No A A (A) decrease
TWB Yes A A A increase (A) (A) (A) increase
142
Lying either on land or in water with the head raised up at an angle (approx. 30º)
was commonly observed among C. johnstoni. This posture, not associated with
agonistic behaviour, makes them appear as if they are on ‘look out’. This behaviour
has been observed for C. johnstoni hatchlings in the wild (Somaweera pers. comm.),
and may indicate a heightened vigilance in a species that remains small and more
vulnerable to predation and inter-specific competition for an extended period. It was
not observed in C. porosus which tend to remain low in the water (LIW) while at rest
(Brien et al. 2013).
Push downs (PD) were displayed by either one or both C. johnstoni during an
agonistic interaction with a head raised high (HRH) posture, with hatchlings often
moving together in a circling motion as they attempted to push each other down. This
behaviour increased in frequency by 13 and 50 weeks of age and is very similar to
what has been reported for several species of salamander (Staub 1993; Davis 2002)
and snakes (Carpenter 1977), with the apparent aim of pinning the other individual
down in a ritualized display of dominance (Staub 1993; Davis 2002).
Raising the head, or ‘snout lifting’, has been reported among larger sub-adults and
adults of several crocodilian species, including C. johnstoni and C. porosus (Webb
and Manolis 1989), as a typical submissive response common to most species studied
to date (Lang 1987). It appears that the raising of the head and, or trunk may also
initially be an attempt at bluffing an opponent, but with age, signals submission. The
transition appears to occur more rapidly in hatchling C. porosus than in C. johnstoni
143
(Brien et al. 2013).
C. johnstoni rarely targeted the head of another individual during an interaction,
and often raised the head out of the way (HRH posture), especially when both
individuals were aggressive. This tendency to avoid contact with the head and the
prevalence of less injurious forms of contact (HP and PD) among C. johnstoni,
especially as they get older, may be linked to skull morphology. During the initial
post-hatching period, the shape of the snout in C. johnstoni is not noticeably different
to that of C. porosus, and the frequency of agonistic interactions and behaviours used
is similar (Brien et al. 2013). However, as C. johnstoni grow, the snout becomes
considerably narrower which coincides with a decrease in the frequency of agonistic
interactions and an increase in the frequency of push downs (PD) and head pushes
(HP).
As the long, narrow snouts of crocodilian species such as C. johnstoni are
structurally weaker than those of species with broader snouts (e.g. C. porosus)
(McHenry et al. 2006; Pierce et al. 2008), this makes them more vulnerable to broken
or damaged jaws during conflict (Huchzermeyer 2003), which can impair or prevent
their ability to feed or even be fatal (Webb et al. 1983c). The use of less invasive
contact behaviours and avoidance of the head may both have an adaptive evolutionary
significance in C. johnstoni, and perhaps with other slender-snouted species of
crocodilian which are often specialist fish eaters (Lang 1987).
Intraspecific agonistic interactions
144
The frequency and nature of agonistic interactions between C. johnstoni at two weeks
of age was similar to those seen between C. porosus hatchlings at 1 week of age,
when both species were maintained in captivity under comparable conditions (Brien et
al. 2013). In C. johnstoni, agonistic interactions decreased in frequency slightly by 13
weeks, and were reduced to less than one half of the initial frequency by 50 weeks.
Agonistic interactions involved contact (>90%) occurred at all ages, but were
typically two-sided and symmetrical, with each individual engaging in the same
behaviour, e.g., push-downs (=PD).
Interactions between hatchling C. johnstoni occurred largely between 17:00–
24:00h, with individuals at two and 13 weeks of age retreating under the hide boards
by 06:00h and not being seen again. In comparison, hatchling C. porosus of all ages
(1, 13, 40 weeks), had a characteristic dusk (17:00–20:00 h) and dawn (06:00–08:00
h) pattern of agonistic interactions and were regularly observed out in open areas <
08:00h. That hatchling C. johnstoni would retreat under the hide almost an hour
before sunrise, may again be linked to the greater vulnerability of hatchling C.
johnstoni to predation due to their smaller size.
Agonistic interactions between hatchling C. johnstoni typically involved two
individuals, and on occasion even up to three or four at 13 and 50 weeks of age. The
number of interactions in which both individuals were aggressive increased slightly
with age (30–40 % of interactions), as did the duration of an interaction, while the
number of times contact was actually made did not change (90% of interactions).
Almost all interactions between hatchling C. johnstoni were a low to medium
145
intensity, while the outcome varied, often resulting in either both individuals standing
their ground or the loser taking flight slowly. While the majority of interactions
resulted in the instigator winning (76.4%), this was far lower than for hatchling C.
porosus older than one week old (Brien et al. 2013).
The formation of dominance hierarchies is often important in limiting the cost of
interactions in species that exist together in social groups, while in more solitary
species, dominance is usually absent and individuals will engage in higher levels of
aggression (Bekoff 1974; 1977; Huntington and Turner 1987; Krause and Ruxton
2002). Although C. johnstoni in the wild are generally solitary, in some habitats they
are often forced to live together at higher densities during certain times of the year due
to lower water levels (Webb et al. 1983a), while they also show a high degree of site
fidelity and communal nesting (Webb et al. 1983a; Tucker et al. 1997).
While there was no evidence of a dominance hierarchy among C. johnstoni by 50
weeks of age in this study, agonistic interactions were relatively infrequent and of a
lower intensity, which may reflect a different social strategy enabling them to coexist
at certain times of the year. In comparison, C. porosus under captive conditions had
well-defined dominance hierarchies despite being largely solitary in the wild. While it
is possible that these results are a consequence of captivity, and that dominance may
develop at a later stage in C. johnstoni, it does indicate that juveniles of these two
species employ very different social strategies.
Interspecific agonistic interactions
146
Agonistic interactions between C. johnstoni and C. porosus in this study involved
only two individuals and were mostly low level, with no real exclusion or dominance
observed. However, smaller individuals of both species moved slowly out of the way
when a larger individual approached. Occasional medium or high level interactions
occurred between the same sized (different species) individuals in a group, and
involved both individuals displaying a species–specific pattern of behaviour with no
clear winner of the contest.
These results were unexpected, as observations of intraspecific aggression
suggested that C. porosus would dominate C. johnstoni due to a higher level of
aggression, and the use of more injurious forms of contact. Instead, it suggests that
interspecific interactions between these two species may be governed largely by size,
which has also been found among different species of crayfish (Vorburger and Ribi
2001) and trout (Newman 1956) during staged interactions. Given that C. porosus
reaches a much larger adult size, it is likely that C. johnstoni may avoid C. porosus in
the wild.
Since the recovery of the saltwater crocodile population in the Northern Territory
from hunting (Fukuda et al. 2011), there appears to have been displacement of C.
johnstoni by C. porosus from areas they previously occupied (Messel et al. 1981;
Webb et al. 1983a). Increased numbers of C. porosus were found to be negatively
correlated with C. johnstoni abundance, suggesting competitive exclusion (Messel et
al. 1981; Webb et al. 1983a). This situation has also been described in a number of
sympatric species of lizards (Jenssen 1973), salamanders (Jaeger 1972; Keen and
147
Sharp 1984), birds (Williams and Batzli 1979) and mammals (Terman 1974), with
removal of the competitively superior species resulting in increased habitat use by the
inferior one.
This study describes agonistic behaviour in C. johnstoni for the first time and
provides new insights into the nature of agonistic behaviour between C. porosus and
C. johnstoni at one year of age, a time at which they would naturally start occurring
together in the wild. Several clear differences exist in morphology, resource use, and
behaviour, between C. porosus and C. johnstoni, which may have been shaped by
interspecific agonistic interactions. As the larger, more dominant species, C. porosus
may have played a significant role in this divergent evolution.
Acknowledgements
We thank Charlie Manolis, Ruchira Somaweera, and Jemeema Brien for their help in
different phases of the project. We would also like to thank Wildlife Management
International for the supply of animals, use of facilities and logistical support. WMI
funding through the Rural Industries Research and Development Corporation is
gratefully acknowledged. Funding for equipment (cameras, digital video recorders)
was provided through a Holsworth Wildlife Research Endowment (ANZ Trustees
Foundation), a Northern Territory Research and Innovation Board student grant, an
IUCN Crocodile Specialist Group student grant, and Charles Darwin University.
Experimental protocols were approved by the Charles Darwin University Animal
Ethics Committee (Animal ethics permit number A11003).
148
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Chapter 3.3. The good, the bad, and the ugly: agonistic behaviour in
juvenile crocodilians
Published as: ‘Brien, M.L., Lang, J.W., Webb, G.W., Stevenson, C., Christian, K.A.
2013. The good, the bad, and the ugly: agonistic behaviour in juvenile crocodilians.
PloS one 8: DOI: 10.1371/journal.pone.0080872’. Formatted according to author
guidelines for journal.
Abstract
We examined agonistic behaviour in seven species of hatchling and juvenile
crocodilians held in small groups (N = 4) under similar laboratory conditions.
Agonistic interactions occurred in all seven species, typically involved two
individuals, were short in duration (5-15 seconds), and occurred between 1600-2200 h
in open water. The nature and extent of agonistic interactions, the behaviours
displayed, and the level of conspecific tolerance varied among species. Discrete
postures, non-contact and contact movements are described. Three of these were
species-specific: push downs by C. johnstoni; inflated tail sweeping by C.
novaeguineae; and, side head striking combined with tail wagging by C. porosus. The
two long-snouted species (C. johnstoni and G. gangeticus) avoided contact involving
the head and often raised the head up out of the way during agonistic interactions.
Several behaviours not associated with aggression are also described, including snout
rubbing, raising the head up high while at rest, and the use of vocalizations. The two
most aggressive species (C. porosus, C. novaeguineae) appeared to form dominance
158
hierarchies, whereas the less aggressive species did not. Interspecific differences in
agonistic behaviour may reflect evolutionary divergence associated with morphology,
ecology, general life history and responses to interspecific conflict in areas where
multiple species have co-existed. Understanding species-specific traits in agonistic
behaviour and social tolerance has implications for the controlled raising of different
species of hatchlings for conservation, management or production purposes.
Introduction
Agonistic behaviour plays an important role in determining access to resources such
as food, shelter and mates, and in establishing dominance status in a wide range of
mammals [1] [2], birds [3] [4], fish [5] [6], reptiles [7] [8], amphibians [9] [10], and
invertebrates [11] [12]. Agonistic behaviour is often present shortly after birth or
hatching, and can vary widely in terms of the nature and ontogeny, both within and
among species [13]. This variability is often associated with differences in the
ecology, morphology, or general life history of a particular species or population,
which can have an evolutionary or adaptive significance [14] [15].
Among reptiles, many behaviours are largely considered ‘hard wired’ from birth,
because they are stereotypical in many species of lizard [8] [16], snake [7] [17],
crocodilian [18] [19] and possibly chelonian [20]. However, detailed information on
agonistic behaviour among hatchling and juvenile reptiles is limited, due to the often
small, cryptic and secretive nature of many species during this early life stage [21].
159
For crocodilians, detailed information on agonistic behaviour is available for the
adults of three species (Crocodylus acutus, Crocodylus niloticus, and Alligator
mississippiensis; [22] [23] [24], and recently, for hatchlings and juveniles of two
species (Crocodylus porosus; Crocodylus johnstoni) [25] [26]. The results suggest
that some agonistic behaviours are shared by different species whereas others are
species-specific. However, all appear subject to species-specific variation in the way
they are expressed in different contexts and the way they change ontogenetically.
Comprehensive studies of hatchling and juvenile C. porosus and C. johnstoni under
captive conditions have recently revealed that a full repertoire of species-specific
agonistic behaviours are displayed during the first few weeks and months post-
hatching [25] [26]. For both species, clutch specific differences were observed in the
frequency and intensity of agonistic interactions, but importantly not in the range of
behaviours displayed [25] [26]. However, a wide range of other factors (eg. size, sex,
age, habitat type and complexity, density, parental care, wild vs captivity) can also
potentially influence the nature and expression of agonistic interactions, even within a
species. While this makes comparative studies difficult, detailed behavioural
observations are still informative, given the significant gap in knowledge about
agonistic behaviours for most species, for all life stages.
In this study, we observed and compared agonistic behaviour of four species of
hatchling and seven species of juvenile crocodilians representing all three crocodilian
lineages (Crocodylidae, Alligatoridae, and Gavialidae). The work was carried out in
captive conditions, because it was a practical approach that allowed control over
160
many, but not all variables.
The aims of the research were:
a. To determine whether all species engaged in agonistic interactions, and for
those that did, to describe and quantify the behaviours used to elicit and
respond to aggression.
b. To quantify inter-specific differences in types of behaviour and in the
frequency, timing, duration, intensity and outcome of an interaction, and
where possible, ontogenetic shifts in these parameters between hatchlings and
juveniles.
c. To discuss species-specific differences in agonistic behaviour among the seven
species examined and the ecological and evolutionary significance of these
differences and their relevance to conservation, management, and/or
production.
Materials and Methods
This project was conducted under the approval of the Animal Ethics Committee of
Charles Darwin University (permit no. A11003).
Subjects and housing
161
Hatchling and juvenile saltwater crocodiles (Crocodylus porosus - CPO), Australian
freshwater crocodiles (Crocodylus johnstoni - CJ), American alligators (Alligator
mississippiensis - AM), and juvenile New Guinea freshwater crocodiles (Crocodylus
novaeguineae - CNG) were provided by Wildlife Management International (WMI)
and were examined in Darwin, Australia, 27 December 2011 to 27 March 2013 (Table
1). Hatchling and juvenile Gharials (Gavialis gangeticus - GG), and juvenile Siamese
crocodiles (Crocodylus siamensis - CS), and dwarf caimans (Paleosuchus
palpebrosus - PP) were provided by the Madras Crocodile Bank Trust (MCBT) and
were examined in Chennai, India in September 2012 (Table 1).
162
Table 1. Groups of hatchling (10-21 days of age) and juvenile (10-18 months of age) crocodilians used in behavioural experiments. H:
hatchling; J: juvenile.
Species Location Date
Age
class Age
Groups
(animals)
No.
clutches TL (mm) BM (g)
Sex
ratio
A. mississippiensis
(AM) WMI 27-Mar-13 H 10-14 days 2(4) 2 234.6 ± 12.7 45.3 ± 6.9 -
WMI 27-Mar-13 J 12 months 1(4) 1 357.3 ± 7.0 118.8 ± 6.3 2M:2F
P. palpebrosus (PP) MCBT 14-Sep-12 J 12 months 3(12) 1 450.1 ± 7.9 361.4 ± 21.8 9M:3F
G. gangeticus (GG) MCBT 13-Sep-12 H 21 days 2(8) 1 504.7 ± 38.9 172.4 ± 34.6 -
MCBT 13-Sep-12 J 12 months 3(12) 2 718.5 ± 25.4 566.5 ± 76.3 8M:4F
C. porosus (CPO) WMI 16-Mar-12 H 10-14 days 3(12) 3 288.8 ± 4.9 74.2 ± 6.2 9M:3F
WMI 12-Jun-12 J 12-18 months 3(12) 3 679.6 ± 11.2 794.8 ± 38.1 10M:2F
C. johnstoni (CJ) WMI 27-Dec-11 H 10-14 days 3(12) 3 245.3 ± 5.3 42.7 ± 4.8 8M:4F
WMI 14-May-12 J 12-18 months 3(12) 3 605.4 ± 19.9 631.0 ± 67.6 9M:3F
C. novaeguineae
(CNG) WMI 18-Jan-12 J 14 months 3(12) 1 558.7 ± 15.6 491.8 ± 39.3 8M:4F
C. siamensis (CS) MCBT 11-Sep-12 J 14 months 4(16) 1 545.2 ± 13.5 475.5 ± 35.7 11M:5F
163
Each species varied in general morphology, particularly snout shape, and had different
ecological and natural history traits in the wild (Table 2). The family Alligatoridae
(AM, PP) has been separated from other extant crocodilians by 85-90 million years,
and the Gavialidae (GG) and Crocodylidae (CJ, CNG, CPO, CS), separated from
each other by 55-60 million years [27]. Snout shape categories used here are derived
from [28] which were a modification of the categories determined by [29] based on
cross-sectional dimensions and the ratio of rostral length to skull length. Several
authors have argued that snout shape in crocodilians is more closely related to
ecological habit than to phylogeny [28] [30].
164
Table 2. General characteristics of the seven species of crocodilian examined [31]. Snout shape is defined as long, generalised, or blunt
according to [28]. Species information was derived from [32] and [33].
Mean max. size
Species
Geographical
location Snout shape Primary habitat type Male Female
Nesting
strategy
Clutch
size
A. mississippiensis (AM) south eastern USA Generalised
Freshwater swamps, marshes,
and lakes 4m 3m Mound 20-50
P. palpebrosus (PP) South America Blunt
Heavily forested freshwater
rivers, creeks and flood plain 1.5m 1.2m Mound 10-20
G. gangeticus (GG) Indian subcontinent Long Freshwater rivers 5m 3.5m Hole 30-50
C. porosus (CP) south east Asia Generalised
Widespread in waterways
from coastal to far inland 5m 3m Mound 30-60
C. johnstoni (CJ) northern Australia Long
Freshwater swamps,
billabongs, rivers and creeks 3m 2m Hole 10-20
C. novaeguinea (CN)
Papua New
Guinea; Indonesia Generalised
Freshwater swamps, marshes,
and lakes 3.5m 2.5m Mound 20-45
C. siamensis (CS) south east Asia Generalised
Freshwater swamps, marshes,
and lakes 4m 3m Mound 20-50
165
All animals had been raised in captivity since hatching in relatively small groups (3-
15) in enclosures of various shapes and designs containing land and water areas. Four
species involved individuals from multiple clutches (AMh, CJ, CPO, and GGj), while
all others were siblings from single clutches. Clutch differences have been reported in
the frequency and intensity of agonistic interactions [25] [26], but not in the repertoire
of behaviours displayed.
From earlier studies with CPO and CJ hatchings and juveniles it was known that
reorganizing crocodiles into small groups (3-5 individuals) increased the probability
that agonistic interactions would occur, and that the various species-specific
behaviours would be displayed, as members adjusted to their new social setting.
Hence the crocodiles here were transferred to experimental enclosures (WMI and
MCBT) in groups of 4 individuals at the same time (1200 h). Total length (TL - mm)
and body mass (g) of each animal was recorded and sex determined where possible.
Groups contained individuals of a similar size and with a similar sex ratio, which was
male biased (Table 1).
Enclosures at WMI were fibreglass and rectangular (170 x 100 x 50 cm high), with a
land area (40 %) that gradually sloped down to a water area (60 %; < 8cm deep). At
MCBT, circular plastic enclosures were used (120 x 120 x 80 cm high), with a land
area (40 %) that gradually sloped down to a water area (60 %; < 8cm deep). While the
amount of space per individual differed between both locations, our previous studies
on agonistic behaviour of hatchling and juvenile C. porosus [25] and C. johnstoni
[26], involving groups of 5 (0.34 individuals/m2) in the same enclosures used here
166
with groups of 4 (0.43 individuals/m2), revealed very similar results in terms of the
frequency, intensity, and behaviours displayed. Water temperatures were maintained
at 30-32°C (WMI) or 29-31°C (MCBT), while air temperatures varied from 26-32°C,
with a natural light cycle. These temperatures are within the range either preferred by
most crocodilians under captive conditions [34], or within the range that results in
optimal rates of growth and survival. The thermal regime that crocodilians were
exposed to prior to the study was also similar. Animals were not fed for the duration
of the observations (48 hours). No form of cover was provided which enabled clear
viewing of interactions.
Recording behaviour
Wide angle infrared CCTV cameras (Signet, 92.6º) in each enclosure recorded
behaviour on digital video recorders (Signet 4CH QV-8104). A recording period
lasted 16 hours (1600 to 0800 h), and was conducted on two consecutive nights for
each group (32 h per group). The recordings were started four hours after the
crocodiles were placed in the new experimental enclosures. This sampling period was
based on previous recordings (100’s of hours) of the hatchlings and juveniles of
several species (CPO, CJ, CNG, GG, CS, AM) that revealed no agonistic behaviour
occurring between 0800 and 1600 h. For all these species, agonistic interactions
corresponded with periods of increased activity, mostly occurring at dusk and early
evening (1600-2200h). No audio was recorded during this study, but some species did
vocalize. Vocalization produced distinctive ripples in the water, which were visible on
the film, allowing some but not all vocalizations to be detected.
167
Agonistic interactions
An agonistic interaction was defined as any interaction between individuals in which
aggression and intolerance appeared to be signalled by postures or actions by one or
both individuals [25] [26]. An aggressive individual was one that made deliberate
advances toward another, or that made physical contact with another. Each agonistic
interaction was examined to quantify whether one or both contestants engaged in
aggression. The intensity of agonistic interactions was characterised as: low or high.
Low intensity interactions appeared accidental, when individuals lying together
disturbed each other when moving, or if one swam into another underwater. High
intensity interactions appeared deliberate, with one individual approaching another
with the apparent goal of initiating an agonistic interaction. The behaviour exhibited,
the intensity of interaction (low or high), the location (water, land), the time, duration
of interaction and outcome (displacement or no displacement) were all quantified, as
previously described for hatchling CPO and CJ under similar conditions [25] [26].
Classification of behaviour
Behavioural observations recorded during these experiments were used to create an
inventory of agonistic behaviour, similar to that described for hatchling and juvenile
CPO and CJ [25] [26]. The descriptions are based on a series of basic postures,
modified by movement of body parts or of the whole animal, and whether visual
signals or actual contact was involved [25] [26]. Some of these behaviours have been
168
described in other studies with juvenile and adult crocodilians [22] [18] [25] [26].
Statistical analyses
All statistical analyses were performed using JMP 8.0 statistical software [35]. Where
appropriate, data were checked for normality (Shapiro-Wilk’s test) and
homoscedasticity (Cochran’s test) prior to statistical analysis. Due to the potential
influence of clutch on the frequency, intensity, duration, and outcome of agonistic
interactions, statistical analyses were limited to species with more than one clutch
(AMh, CJ, CPO, GGj). However, the data is still presented for other species because
there are so few data of this sort in the literature. Frequency and duration of
interactions was compared among species using a Kruskal-Wallis test with Wilcoxon
pair-wise comparisons to account for small and unequal sample sizes. A Pearson’s
chi-square test was used to compare the intensity and outcome of an interaction
among species. Hatchlings and juveniles were compared separately in all species. A
significance level of P<0.05 was used for all statistical tests. All means are reported ±
one standard error with sample sizes.
Results
Agonistic behaviour
In 960 h of observation of 120 individuals of seven species, we observed a total of
462 agonistic interactions. Observed agonistic interactions occurred in open water,
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with none observed on land. All interactions involved only two animals, with the
single exception of three juvenile. For most species, interactions appeared to occur
accidentally when individuals lying together disturbed each other when moving off, or
if one swam into another. However, interactions were also initiated by one individual
moving deliberately toward another in either a single movement or in a series of short,
rapid advance (RA) movements. In response to an approach, an animal displayed a
series of other agonistic behaviours (Table 3).
Table 3. Description of the various postures, non-contact and contact movements
displayed by hatchling and juvenile crocodilians during agonistic interactions
[30] [31]. *= has not been previously described, or is different in some way.
Abbreviation Definition
Initiation
Rapid advance RA
Series of short rapid advance movements towards another
individual while low in water
Termination
Slow flight SF
Slow movement away from another individual in a low in
water posture.
Rapid flight RF
Rapid movement away from another individual in a low in
water posture.
Posture
Low in water LIW
Immobile with only the top of the head and back above the
water surface.
Inflated posture IP
Immobile with upward extension of either the front two or all
four limbs, with neck and back arched high and head and tail
angled downward.
Head and tail
raised HTR
Immobile with head and tail raised out of water while back
remains low. Head is usually parallel to the water but can also
be angled upwards.
Head raised high HRH
Immobile with upward extension of the front two limbs
pushing the head and chest high out of the water on a ~45º
angle while tail remains low.
Mouth agape MA Immobile with mouth opened wide (all postures).
Non-contact movements
Light jaw-clap LJC
Rapid opening and closing of the jaws at the water surface,
often repeated several times while low in the water or inflated.
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Tail-wagging TW
Undulation of the tail from side to side in either a gentle
sweeping motion or rapid twitching, often repeated several
times (all postures).
Inflated tail sweep ITS*
In an inflated posture, the whole tail is swept side to side in a
slow deliberate fashion as the individual approaches another.
This becomes more rapid and the tail is thrashed from side to
side.
Vocalization V* Vocalization observed and confirmed from body movement.
Contact movement
Head push HP
Head is pushed in to an opponent, usually with mouth closed
while low in water or inflated.
Push down PD
Chest and neck of individual pushed down on the upper neck
or back of an opponent while head is raised high.
Bite B Jaws closed shut on an opponent (all postures).
Side head-strike SHS
Head is thrust sideways in to an opponent while the mouth is
either open or closed (all postures).
Tail-wag side
head strike TWSHS
Tail wagging occurs prior to a side head strike, increasing the
force of the impact (all postures).
Tail-wag bite TWB
Tail wagging occurs prior to a bite and it propels the individual
in to an opponent with force while low in water.
Agonistic behaviours involved the adoption of some discrete postures that varied in
the intensity of expression (Table 3). The adoption of such postures could be
abandoned at any time by either slow (SF) or rapid flight (RF), ending the interaction.
Alternatively, the signals emanating from the postures could be intensified with body
movements, such as mouth agape (MA), light jaw claps (LJC), or tail wagging (TW),
which were signalling displays that did not involve physical contact between
combatants. If the agonistic interaction was not terminated by flight (SF or RF) by one
or both animals, the behaviours intensified, with contact movements such as head
pushing (HP), push downs (PD), biting (B), or side head striking (SHS), occasionally
combined in different ways with intense tail wagging (Table 3), until one or both
individuals took flight. While several behaviours were common across the majority of
species, other behaviours were often specific to only one or a couple of species, varied
in the frequency with which it was exhibited (common or rare), and in some cases
appeared to be used to signal different intentions (Table 4).
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When not involved in agonistic interactions, individuals of most species would lie
close together in the water. CS was observed rubbing the sides of their snouts against
each other while lying together in what appeared to be some form of non-aggressive
communication. In contrast, close contact rarely occurred among juvenile CPO, CNG
and PP, which tended to separate from each other.
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Table 4. Presence or absence of the various postures, non-contact and contact
movements displayed by hatchling (H) and juvenile (J) crocodilians during
agonistic interactions [25] [26]. AM: A. mississippiensis, PP: P. palpebrosus, GG:
G. gangeticus, CPO: C. porosus, CJ: C. johnstoni, CNG: C. novaeguineae, CS: C.
siamensis.
Species
AM PP GG CPO CJ CNG CS
Initiation H J J H J H J H J J J
Rapid advance (RA) X X X X X
Termination
Slow flight (SF) X X X X X X X X
Rapid flight (RF) X X X X
Posture
Low in water (LIW) X X X X X X X X X X X
Inflated posture (IP) X X X
Head and tail raised (HTR) X
Head raised high (HRH) X X X X X X X
Mouth agape (MA) X X X X X X X X
Non-contact movements
Light jaw-clap (LJC) X X X
Tail-wagging (TW) X X X X X X
Inflated tail sweep (ITS) X
Contact movement
Head push (HP) X X X X X X X X X X X
Push down (PD) X X
Bite (B) X X X X X X X X X X
Side head-strike (SHS) X X X X X
Tail-wag side head strike
(TWSHS) X X
Tail-wag bite (TWB) X X X X X X
Postures
Crocodilians of all species and ages most commonly remained low in the water (LIW)
during an agonistic interaction and while at rest (Table 4; Fig. 1). However, GG and
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CJ adopted postures with their heads raised ~40º to the body, while PP lay with its
head raised up but parallel to the water surface (Fig. 1). In most cases, remaining LIW
did not signal aggressive intent, unless used by aggressive individuals during an
approach, which was commonly observed among juvenile CPO, CNG, and PP.
Figure 1. Agonistic behaviours displayed by young crocodilians. Postures, non-
contact and contact movements (described in Table 3) displayed by hatchling (h) and
juvenile (j) crocodilians. Crocodilians in the figure include G. gangeticus - h (a); P.
palpebrosus (b); C. siamensis; (c); C. porosus - h (d,e,f,g,h); C. novaeguineae (i); C.
johnstoni - j (j); C. porosus - h (k,l).
The head raised high (HRH: ~45º) posture was observed in five species (CJ, CNG,
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CPO, GG, PP; Table 4) where it appeared to signal aggressive intent, submission or
avoidance. In juvenile CNG and CPO, HRH clearly signalled submission, while in PP
and hatchling CPO it signalled readiness to give or receive contact. In CJ and GG,
HRH generally signalled avoidance and was more common among juvenile than
hatchling CJ.
The inflated posture (IP) was only observed in two species (CNG, CPO; Table 4) and
in CNG was a common and clear display of aggressive intent. The head and tail raised
(HTR) posture was only observed in hatchling CPO (Table 4) and while rarely
displayed, signalled aggressive intent. Mouth agape (MA) was observed in all but
three species (hatchling AM and CJ; juvenile CS; Table 4) and was displayed by
aggressive individuals as a threat or by submissive individuals when approached by
an attacker. While hatchling CPO utilised a wide range of postures, juvenile CPO
most commonly assumed a LIW posture if aggressive, non-aggressive individuals
were either in a LIW or HRH posture that signalled submission.
Non-contact movements
Light jaw claps (LJC) were only observed in CPO and CJ (Table 4), and clearly
signalled aggressive intent in hatchlings, and were absent (CJ) or rare (CPO) in
juveniles. Tail wagging (TW) signalled high agitation and was displayed by
aggressive individuals as forewarning of a contact movement, and by non-aggressive
individuals in anticipation of an attack by an approaching individual. Tail wagging
often increased in intensity as an interaction escalated. Inflated tail sweeping (ITS)
175
was only observed in CNG and was a highly aggressive non-contact movement that
increased in intensity as an interaction escalated (Fig. 1). It differed from TW in that
the whole tail was involved, sweeping from side to side.
Vocalizations that created ripples in the water were observed in juvenile CS, CNG,
and hatchling and juvenile AM. In CS and AM, vocalizations did not appear to be
associated with aggression. While the initial reason for vocalizing was often unclear,
if one individual vocalized between 1 and 3 of the others often responded. On one
occasion, a juvenile AM vocalization resulted in the other three individuals swimming
over from their place of rest towards the vocalizing individual. Then all four AM
juveniles initiated foraging behaviour. In contrast, vocalizations by CNG occasionally
preceded the initiation of an agonistic interaction.
Contact movements
Contact was made during the majority of agonistic interactions (88-100%) in all but
juvenile CPO (42.2%), hatchling and juvenile GG (H=20%; J=36%), and juvenile PP
(45.7%). For juvenile CPO, PP, and CNG (70.7%), an attempt at contact was usually
made, but the individual under attack often took flight (RF, SF) and avoided actual
contact. In contrast, in hatchling and juvenile GG contact was rarely even attempted.
Head pushes (HP) and bites (B) were the most common form of contact used by all
species of crocodilian. HP was the least aggressive form of contact, usually directed at
the body. Bites were mostly directed at the head or body or at the tail if an animal fled
176
(common in CPO and CNG). AM commonly grabbed hold of another individuals’
snout, while bites by CS, GG and CJ juveniles were only very light. In general, GG
and CJ juveniles avoided physical contact involving the head. Push downs (PD) were
low intensity and only observed in CJ, more frequently among juveniles than
hatchlings (Fig. 1). Side head strikes (SHS) and SHS and bites accompanied by tail
wagging (TWB) were a highly aggressive form of contact displayed by only a few
species [(SHS: CNG, PP, CJ(h), CPO (h,j); TWB: CNG, CS, CPO (h,j); Table 4].
Side head strikes accompanied by tail wagging (TWSHS) were another highly
aggressive form of contact only observed in CPO hatchlings and juveniles (Fig. 1).
While hatchling CPO displayed a range of contact movements, juveniles mostly
displayed TWBs.
Agonistic interactions
Aggression
An aggressive individual was defined as any individual that made deliberate advances
toward another and, or which made deliberate physical contact with another [30] [31].
Each agonistic interaction was examined to quantify whether one or both contestants
engaged in aggression, and whether this differed among species. For most species,
only one individual appeared aggressive during an agonistic interaction. However,
both individuals appeared aggressive during interactions between hatchling (51.9%)
but not juvenile CPO (0%), in both hatchling (27.8%) and juvenile (35.7%) CJ, and in
a few of interactions between juvenile CNG (8.6%).
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Frequency and duration
Agonistic interactions for most species occurred sporadically throughout the night and
early morning with the majority between 1600-2200h. However, in CPO there was a
more defined pattern, with the majority occurring predominantly at dusk (1700-
1900h) and dawn (0600-0800h). The mean number of agonistic interactions (X2 =
30.80, df = 5, P < 0.05) and mean duration of interactions (X2 = 142.88, df = 5, P <
0.05) observed per group per night among the four species from multiple clutches
varied significantly (Table 5). The frequency and duration of agonistic interactions
was highest for CPO juveniles and hatchlings, while the frequency of agonistic
interactions was lower in juvenile CJ compared with hatchling CJ (>2 times), and was
highest among juvenile CPO compared with hatchlings (>2 times).
188
Table 5. The frequency, duration, intensity, and outcome of agonistic interactions between young crocodilians. Different letters indicate
significant difference.
Species Age
class
No.
interactions
Frequency
per night
Mean
duration
Intensity
(%high)
Outcome
(% displacement)
Multiple clutches
C. porosus J 147 24.7 + 3.53A
19.1 + 0.77B
95.9A
100A
C. porosus H 52 8.7 + 0.88B
49.3 + 4.89A
75B
63.5B
C. johnstoni H 36 6.0 + 0.63B,C
13.4 + 1.30B,C
38.9C
30.6C
C. johnstoni J 13 2.3 + 0.21C
13.0 + 2.44B,C
30.8D
38.5C
A. mississippiensis H 24 4.2 + 0.31C
8.5 + 0.57C
0E
0D
G. gangeticus J 25 4.2 +0.60C
5.6 + 0.21C
0E
36C
Single clutches
C. novaeguineae J 56 9.3 + 0.71 18.6 + 1.88 67.9 60.7
P. palpebrosus J 32 5.3 + 0.42 8.9 + 0.82 55.2 43.8
C. siamensis J 64 8.1 +0.67 6.05 + 0.25 7.8 9.4
A. mississippiensis J 8 4.0 + 0.0 9.3 + 1.03 12.5 0
G. gangeticus H 5 1.3 + 0.5 3.6 + 0.40 0 0
189
The duration of agonistic interactions was longer among hatchling CPO compared
with juveniles, but was similar between juvenile and hatchling CJ. Between juvenile
CS and hatchling AM, two individuals grabbed each other and did not let go for an
extended period (CS: 484 s; AM: 42 s) in which they rolled around together. In the
only interaction to involve more than two individuals, three juvenile CJ came together
with their snouts raised up high and then began a series of PDs while biting. As they
did this, they moved in a circular motion and this continued for 51 seconds.
Intensity and outcome
The intensity of interactions differed among the four species with multiple clutches
(X2 = 176.27, df = 5, P < 0.05; Table 5). The frequency of high-intensity interactions
was highest for hatchling and juvenile CPO, followed by hatchling and juvenile CJ.
None of the interactions between hatchling AM and juvenile GG were high intensity.
The instigator was usually the winner of interactions between juvenile CPO (100%),
but for most species it was generally unclear whether either individual had won (0-
36%) due to the predominance of low intensity interactions. The outcome of
interactions differed among species from multiple clutches (X2 = 163.55, df = 5, P <
0.05; Table 5). In contrast to the other species (hatchling and juveniles), the majority
of interactions between juvenile CPO resulted in the loser being displaced.
190
Discussion
Agonistic behaviour
Many of the behaviours observed during agonistic interactions among juvenile
crocodilians in this study have also been reported among adults [22] [18] [24], which
suggests that agonistic behaviour, as with other behaviours in crocodilians [19], may
be hard wired from birth and stereotypical for most species. However, for a particular
species, certain behaviours may be present or absent at different life stages, or only
used when the prevailing social context requires. However, behaviours shared by
different species often varied in frequency and intensity (eg. tail wagging) and could
be used to signal different intentions (eg. head raised high).
Of the behaviours displayed by juveniles in this study, three were common to all
seven species (Low in water; head push; bite), and three were specific to only one
species (Push down: CJ; Inflated tail sweeping: CNG; Tail wag side head strike:
CPO), while the other behaviours were displayed by some and not others (Table 4).
Of the behaviours displayed by hatchlings in this study, two were common to all four
species (low in water; head push). Five were shared by CJ and CPO hatchlings (RA,
TWB, SHS, LJC, TW). Four behaviours were unique to CPO (RF, IP, HTR,
TWSHS), and one to CJ (PD) (Table 4). Among hatchlings compared, only AM
hatchlings were observed to vocalize.
Individuals of most species remained low in the water during agonistic interactions
191
that did not signal aggressive intent, while inflating the body or raising the head and
tail combined with mouth agape was a clear sign of aggression. However, among
species with a more defined pattern of dominance (CPO, CNG) aggressive individuals
would remain low in the water when approaching a subordinate. The head raised high
posture was most commonly used to signal submission, while tail wagging indicated
high agitation.
Inflating the body and opening the mouth to signal aggressive intent and raising the
head high to indicate submission are postures used by several species of sub-adult and
adult crocodilian [22] [18]. Many species of birds [36], mammals [1] [2], and fish [37]
[38] will also raise or inflate their body and open their mouth wide during agonistic
interactions in an attempt to intimidate their opponent.
In most cases, this type of display enables both individuals to assess the potential
combative ability of the other and is often sufficient to prevent physical contact
through causing one individual to retreat [39] [40]. The use of tail wagging to signal
high agitation has also been observed in sub-adult and adult crocodilians [22], along
with certain species of lizards [41], mice [42] and salamanders [9].
The main forms of contact during interactions for most species in this study were head
pushes and bites. Bites could range in severity from light mouthing (CS) or grabbing
and letting go, which were most common, to bites in which the aggressor either
propelled itself into another individual, or bites in which the individual grabbed and
shook before letting go. On the extreme end of the scale, a few interactions between
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individuals from less aggressive species (CJ, AM, CS) resulted in two individuals
grabbing each other and rolling around with neither letting go for an extended period.
Biting is the most common form of contact used during agonistic interactions in other
reptiles [43], birds [3], mammals [1] [2], and fish [44] [45].
There were essentially three agonistic behaviours observed that appeared to be
specific to only one species: push down by CJ; inflated tail sweep by CNG; and, the
side head strike combined with tail wagging by CPO. The push down by CJ may have
evolved in response to its elongated snout that is presumably more vulnerable to
damage by contact such as bites or side head strikes. The inflated tail sweeping by
aggressive CNG provided subordinates with a clear warning of aggressive intent,
giving them time to take flight and avoid an attack. A similar behaviour has also been
observed in skinks, and is described as ‘tail lashing’, which precedes biting and
chasing [41] [46].
Tail wag side head striking by CPO was the most aggressive contact movement
observed in any species of crocodilian, and is similar to that observed between rival
adult male CPO during the breeding season [47]. While infrequent, tail wag side head
striking was more common among hatchlings and occurred when both individuals
were aggressive. One or both individuals would typically align head to head and raise
themselves up with the head raised high, before swinging the head violently into the
head or body of the other individual. The object of this contact movement appeared to
be to inflict maximum damage and may be an important behaviour, along with tail
wag biting, in establishing dominance in this species.
193
Most animals avoid the use of severe or injurious forms of contact during interactions,
unless the stakes are high enough to justify the risk, such as during the acquisition of
mates, food, shelter or territory [48]. However, the use of such intense agonistic
behaviours may also be important in establishing dominance, as the loser of these
interactions may be less likely to challenge again in the future and become
subordinate [13]. Many species typically engage in intense forms of agonistic
interactions involving more highly aggressive behaviours during the juvenile stage
until a dominance hierarchy is formed [49] [13].
In terms of snout morphology, crocodilians have been broadly categorised as blunt-
snouted, generalised, or long-snouted, [28], in which the potential for the snout to be
damaged during interactions increases respectively [50]. In this study, two
crocodilians were long-snouted (GG and CJ), four were generalised (AM, CPO, CS,
CNG) and one was blunt-snouted (PP). During agonistic interactions the two long-
snouted species (CJ, GG) raised the head and generally avoided contact involving the
head, while the generalised and blunt-snouted species often made contact with the
head. Species of salamander that have morphologically more vulnerable head shapes
are also known to employ less injurious forms of contact than those with more robust
shapes [9].
Non-aggressive behaviour
Several behaviours were observed that were not involved in agonistic interactions.
194
Juvenile CS would often lie close together in the water, and were often observed
rubbing the sides of their snouts together. This behaviour was not associated with
aggression and appeared to be some form of social recognition or communication
which has also been observed among males and females during the breeding season
[51] [52]. In crocodilians, the side of the snout contain numerous integumentary
sensory organs that are highly sensitive to external stimuli [18] [53] [54], and may
play an important role in communication. Chemoreception in crocodilians is also
acute, and has been implicated in behavioural responses of juveniles and adults to skin
gland secretions [55] [56].
While the majority of species remained low in the water while at rest, CJ, GG, and PP
lie with their heads raised up on an angle. However, while CJ and GG angled their
head up high, the head of PP remained parallel to the water in a ‘dog-like’ pose
commonly observed in caiman species. While the significance of these raised postures
remains unclear, it is possible that they have evolved in response to a need to keep
vigilant for predators, including larger crocodiles, given that these species either
remain quite small (CJ, PP) for an extended period of time, or are physically more
vulnerable (CJ and GG).
Vocalizations of sufficient intensity to ripple the water were made by juvenile CS and
CNG, and by hatchling and juvenile AM. For CS and AM, they did not appear to
signal aggression but did result in a response from other individuals. For CS and AM,
the other individuals often responded by vocalizing themselves, while on one
occasion a series of vocalizations by one AM resulted in the commencement of
195
foraging behaviour by three pen mates. In contrast, vocalizations by CNG did appear
to be linked to aggression, and were observed on one occasion preceding an
aggressive advance, and on another occasion resulting in a nearby subordinate taking
flight rapidly.
Vocal communication has been widely reported among crocodilians, especially during
the hatchling stage when crèches are maintained, and among adults during the
breeding season [24] [57]. As we did not record sound during these experiments it is
likely that vocalizations were more common than reported here. Nevertheless, the
three species observed vocalising here are all known to occupy densely vegetated
habitats such as freshwater swamps and lagoons, where vocalization may play a larger
role in communication than with species that live mainly in open water areas [18]
[58]. Previous studies have suggested that juvenile vocalizations serve two primary
functions: (1) contact calls localize individuals and facilitate grouping, and (2) distress
calls signal potential predators and promote defence by larger individuals [59] [60].
Vocalizations related to aggression in young crocodilians have not previously been
reported, and would constitute a possible third, and new, functional category of
juvenile vocalizations.
Aggression and dominance
The large majority of interactions among the less aggressive species of juvenile
crocodilian appeared accidental. Despite a similar or higher frequency of agonistic
interactions between CS compared with CNG and PP, interactions were generally low
196
intensity with individuals often observed lying together. While biting occurred during
interactions, it was mostly light mouthing.
Agonistic interactions between juvenile CJ, AM, and GG were infrequent and
considered very low level with individuals highly tolerant of others. The frequency of
agonistic interactions in AM and GG were similar in hatchlings and juveniles, while
the frequency of agonistic interactions between hatchling CJ was almost twice that of
juveniles, although in both age classes there was limited contact with the head and a
high frequency of push downs on their opponent.
Behaviour suggesting dominance hierarchies was observed among juvenile CPO,
CNG, and to a lesser extent PP. Agonistic interactions among these species were
characterised by an aggressive individual advancing towards another, either low in the
water (CPO, PP, CNG) or while inflated and tail thrashing (CNG), and the
subordinate individual responding by remaining low in the water or rising with the
head raised high before taking flight. In CPO and CNG, the aggressor often gave
chase and attempted to bite or tail wag bite, while PP struck sideways with the head.
However, with CPO, these behaviours were most obvious in juveniles rather than
hatchlings.
Dominance hierarchies appear common in crocodilians in the wild and in captivity
[18], and the formidable morphological armour crocodilians are endowed with could
be important for preventing serious injury or death during agonistic interactions linked
to establishing dominance [48]. The nature and extent of dominance varies across
197
species [18] and appeared to be correlated with the general level of aggressive
behaviour in adults.
While the formation of a dominance hierarchy may be more rapid under captive
conditions, the results of this study demonstrate that dominance and agonistic
behaviour develops early in highly aggressive species of crocodilian, and may
ultimately be a strategy for the early honing of avoidance skills that minimise the
potential for injury. In contrast, dominance appeared less important among the other
five species, which displayed low levels of aggression and a higher tolerance of
conspecifics at this early life stage. These less aggressive species also displayed fewer
types of behaviours than the more aggressive ones. This absence or loss of behaviours
has previously been reported in other animals in which dominance is considered less
important [14].
Hatchlings of almost all crocodilian species studied to date will form tight-knit
crèches in the immediate post-hatching period before dispersing anywhere from a few
days to several years later. While information on crèche formation and dispersal is
lacking for most species of crocodilian, it may help explain the species-specific
variation in agonistic behaviour and social tolerance between hatchlings and juveniles
in certain species. For AM and CS (low aggression), hatchlings within swamp or
marsh habitats are known to remain together accompanied by the female and older or
younger siblings for up to several years [18] [61]. Hatchling GG (low aggression)
from multiple clutches form large creches of 100-1000 individuals which remain
together for 2+ months, typically accompanied by adult females and a defensive male
198
[62].
In contrast, hatchling CPO (high aggression) remain together in crèches anywhere
from one week up to two months at which point dispersal is considered to occur due
to a growing intolerance of each other [63]. However, hatchling PP, that were
considered relatively aggressive in this study, were recently found to crèche together
in small groups accompanied by a female up to 12 months post-hatching [64]. During
this time, the size of the crèche steadily decreased, which could be due to mortality
(eg. predation) or a growing intolerance of each other. The relatively high level of
aggression among 12 month old PP in this study would suggest that agonistic
behaviour may at least play a role in dispersal.
While adult crocodilians are often less tolerant of conspecifics than hatchlings or
juveniles, insome species, large numbers of adults group together in large numbers at
different times throughout the year [18]. Among the less aggressive species in this
study, CJ, CS, and AM are all known to congregate together seasonally in large
numbers due to lower water levels in the dry season [18] [65], while CJ, GG, and AM
are also known to congregate together during the breeding and nesting season [18]. In
comparison, CPO and PP have rarely been observed together at any time of the year
outside of the breeding season when they form only male-female pairs [32] [33].
Suspension or reduction in agonistic behaviour may itself be an important strategy
enabling certain species of crocodilian to coexist in high numbers without sustaining
serious injuries [18]. That high density of conspecifics can reduce levels of aggression
has been found in certain species of trout [37].
199
Interspecific aggression
In areas where species of crocodilian exist in sympatry, there may be a competitive
advantage to being the more aggressive species, as this may result in greater access to
resources. However, while some studies of crayfish have found that the level of
intraspecific aggressiveness observed in the laboratory is often consistent with the
competitive ability of species in the wild [66] [67], others have found the opposite
[15].
In crocodilians, the nature and extent of agonistic behaviour among sympatric species
is poorly known. A recent study that examined interspecific aggression between
juvenile CPO and CJ under laboratory conditions found that despite the higher level
of aggressiveness observed during intraspecific interactions between CPO, CPO did
not dominate CJ in any way [25] [26]. Instead, dominance appeared to be related to
body size, with smaller individuals avoiding larger ones regardless of species.
Agonistic interactions were only observed between similar sized individuals of both
species, with no clear winner in the interactions observed due to the different
strategies employed. Hence the much larger size that adult CPO attains relative to
adult CJ may give it the competitive ability, forcing CJ to adapt and evolve
morphologically, behaviourally and ecologically. Larger body size rather than
intraspecific aggression is also a greater determinant of competitive ability among
several species of crayfish [68] [69], and fish [37].
200
Species comparisons
Based on our studies of four species at WMI, we are able to construct a relative
ranking of high to low aggression of CPO>CNG>CJ>AM. The relative ranking of the
species studied at MCBT on the same scale is PP>CS>GG. If we then collate our
findings at WMI with three additional species at MCBT, the relative ranking on a high
to low aggression scale for the seven species studied is:
CPO>CNG>PP>CS>CJ>AM>GG. Although we only focused on hatchlings and
juveniles of seven species in this study, the relative ranking of these seven species
provides new information that can be integrated with other more recent data into an
updated version of Lang’s [18] original scaling of species according to high to low
aggression and its reciprocal, tolerance vs. intolerance of conspecifics (Fig. 2). This
remains a subjective assessment, because genetics, sex, age and the environment
(captive vs wild) may all be implicated, but nevertheless updating it with additional
qualitative and quantitative new information is useful. Based on the results of our
observations reported here, we propose that slender snouted species may be far more
tolerant of each other, or at least avoid agonistic interactions involving more
damaging behaviours.
201
Figure 2. Tolerance of conspecifics in crocodilian species – updated assessment
[18]. Tolerance of conspecifics (low-high) and level of aggression (high-low) in
crocodilian species based largely on behavioural observations of social interactions
between adults and juveniles in captivity and in the wild. Information has been
sourced from published and unpublished reports, papers, theses and anecdotal
accounts. Boxes highlight species involved in this study; ? indicates minimal
information; arrows indicate direction of update.
The most significant changes are that CS, originally considered a fairly aggressive
species with a low tolerance of conspecifics, may not be so. Adults have recently been
reported as sharing burrows in the wild [70], while another study reported animals of
different ages and sizes existing in close proximity within a lake environment [61]. In
areas where CS and CPO are farmed, CS is usually the favoured species despite its
less valuable skin [71], because the greater tolerance of conspecifics is more amenable
to captive raising. We also consider GG to be far more tolerant than first thought,
202
based on the results of this study and that juveniles and sub-adults of various sizes
have been observed together in captivity without any agonistic behaviour, injuries or
voluntary spatial segregation (M. Brien pers. observation).
C. mindorensis was not originally involved in Lang’s [18] original comparison, but is
considered by many as one of the most aggressive species of crocodilian, which has
led to difficulties in breeding this species in captivity [72]. Intraspecific aggression
among juveniles and sub adults is also reportedly high in the wild and in captivity
[72]. While C. rhombifer was originally considered less aggressive and tolerant, more
recent reports from captivity suggest that C. rhombifer may be far more aggressive
[73] and they are even known to dominate larger crocodilian species [74]. Based on
the results of this study and on observations by one of the authors (JL), we also
consider that CNG is also far more aggressive than originally thought.
Phylogenetic relationships, based on recent analyses using morphological and
molecular features, do not provide robust explanations for the differences we
observed in agonistic behaviours of young in the seven species we examined,
representing the three major lineages. A close examination of the groupings in Figure
2 indicates that representatives of the Alligatoridae (PP,AM) and of the Crocodylidae
(CPO, CNG, CS, CJ) span the continuum from high to low aggression, and
intolerance to tolerance of conspecifics. The seemingly larger suite of behaviours
documented in CPO and CJ, relative to the other species studied here (Table 4) likely
reflects the detailed investigations focused on ontogenetic changes, and the many
variables influencing the full expression of the species-specific behavioural
203
repertoires [25] [26].
Conclusions
Variation in the nature and extent of agonistic behaviour in crocodilians may reflect
evolutionary divergence associated with differences in morphology, ecology, and
general life history. In areas where more than one species exists, this divergence may
have even been shaped by the more dominant species of crocodilian. Understanding
interspecific differences in the level of aggression and social tolerance has
implications for conservation and management programs that involve captive
breeding and reintroduction. For example, how aggressive a species is towards
conspecifics at a particular life stage will influence not only how they are raised in
captivity but also how reintroductions need to be undertaken to be successful. In areas
where more than one species coexists, either naturally or through artificial
introductions, an understanding of interspecific aggression can also be used to assess
the competitive ability of each species and the potential of an invasive species to
displace a native one.
This study indicates that many behaviours displayed by crocodilians are evident early
in life, and that hatchlings do exhibit a wide range of behaviours that may change or
disappear with age, but are similar to the behavioural repertoires known to
characterize adults. Although the seven species studied here included representatives
of the three major crocodilian lineages alive today, the New World caiman species are
underrepresented, as well as species of New World crocodiles, and the other
204
representative of Gavialidae, the genus Tomistoma. Cataloguing the behavioural
repertoires of young in these unstudied species will be of value in advancing species
comparisons.
The diverse and complex nature of crocodilian behaviour and communication is
similar to that observed in birds and mammals [18] [19]. In this study we focussed on
visual displays of hatchlings and juveniles during agonistic interactions. However,
crocodilians are also capable of vocal and chemical communication, which will likely
be productive for further studies. Future research on agonistic behaviour in
crocodilians should focus not only on the visual components, but also the role of
vocalizations and chemical cues, and how these may develop with age. Future
research will also be important for determining whether species-specific behaviours
reported here are in fact consistent for the species as a whole, and whether this may
differ in the wild.
Acknowledgements
We thank Charlie Manolis, Jemeema Brien, Elize Dorrestein from WMI for their help
in different phases of the project; Toody from Melanesia (Green Island, QLD) for the
supply of C. novaeguineae; Tim Faulkner, Julie Mendozona, and staff at the
Australian Reptile Park (Gosford, NSW) for help and supply of A. mississippiensis;
and Rom Whitaker, Gowri Mallapur, Nikhil Whitaker, Gayathri Selvaraj, and Josh
Van Lier from Madras Crocodile Bank (Chennai, India) for use of crocodilians and
facilities and general help and support. We would also like to thank Wildlife
205
Management International for the supply of animals, use of facilities and logistical
support.
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Chapter 4. Thermal preferences of hatchling saltwater crocodiles
(Crocodylus porosus) in response to time of day, social aggregation
and feeding
Published as: ‘Brien, M.L., Webb, G.J., Gienger, C.M., Lang, J.W., Christian, K.A.,
2012. Thermal preferences of hatchling saltwater crocodiles (Crocodylus porosus) in
response to time of day, social aggregation and feeding. Journal of Thermal Biology
37, 625–630’. Formatted according to author guidelines of journal.
Abstract
Three month old hatchling C. porosus with data loggers in their stomachs were placed
in thermal gradients, in isolation (N=16) and in groups of 4 (N=8 groups; 32
individuals). Mean Tb and variation in Tb (SD) was not different whether individual
crocodiles in isolation were fasted or fed, or if individuals were housed in isolation (I)
or in groups (G). However, individuals in isolation (N=16) maintained slightly lower
Tbs than those in groups (N=32) during the early morning (0600-1100h). The overall
mean Tb recorded for fasted individuals in the isolated and group treatments (N=48)
was 30.9 ± 2.3 ºC SD, with 50% of Tbs (Tset) between 29.4 ºC and 32.6 ºC, and a
voluntary maximum and minimum of 37.6 ºC and 23.2 ºC respectively. During the
day (1100-1700h), individuals in isolation and in groups selected the warmer parts of
the gradient on land, where they moved little. Outside of this quiescent period (QP),
activity levels were much higher and they used the water more. There was a strong
diurnal cycle for fasted individuals in isolation and in groups, with Tb during the QP
(31.9 ± 2.09ºC; N=48) significantly higher than during the non-quiescent period
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(NQP: 30.6 ± 2.31ºC). Thermal variation (SD) in Tb was relatively stable throughout
the day, with the highest variation at around dusk and early evening (1800-2000h),
which coincided with a period of highest activity. The diurnal activity cycle appears
innate, and may reflect the need to engage in feeding activity at the water’s edge in
the early evening, despite ambient temperatures being cooler, with reduced activity
and basking during the day. If so, preferred Tb may be more accurately defined as the
mean Tb during the QP rather than the NQP. Implications for the thermal environment
best suited for captive C. porosus hatchlings are discussed.
Key words: Thermal preference; diurnal cycle; feeding; social aggregation;
Crocodylus porosus
1. Introduction
Many ectotherms maintain body temperatures (Tb) within a preferred range through
behavioral means, namely shuttling between warm and cool parts of their
microhabitat (Heath, 1970; Heatwole, 1977; Seebacher, 1999; Tattersall et al., 2006).
The preferred Tb range can vary throughout the day due to endogenous circadian
rhythms (Ellis et al., 2006), but it is also subject to variation by stochastic
environmental events (changed availability of warm and cool sites), the physiological
state of an individual, the social landscape in which it exists, the extent of nocturnal
versus diurnal activity, and various other factors (Heatwole et al., 1975, Huey, 1982;
Lang, 1987; Yang et al., 2008).
219
Feeding is often followed by the selection of elevated Tbs (Blouin-Demers and
Weatherhead, 2001; Gatten, 1974; Slip and Shine, 1988), but it can also be associated
with reduced or stable Tbs (Brown and Brooks, 1991; Brown and Weatherhead, 2000;
Knight et al., 1990). The response to feeding may depend on whether feeding is
nocturnal or diurnal, or the Tb experienced during feeding versus the optimal Tb for
digestive processes (Huey, 1982). Effects of feeding on Tb vary in species with highly
seasonal influences on food intake (Webb et al., 1982), and in species in which
juveniles eat small amounts of food regularly (Webb et al., 1991), versus larger adults
with a boom and bust feeding cycle and empty stomachs most of the time (Cott,
1961).
Crocodilians use both the land (sun, shade) and water (warm, cool) to regulate their Tb
(Grigg and Seebacher, 2000; Lang, 1987). As predicted by Spotila et al. (1972),
hatchlings and juveniles maintain Tbs within a narrower range than adults, which
spend relatively more time either heating or cooling their larger body mass (Grigg and
Seebacher, 2000; Lang, 1987). However, social interchange between individuals can
also interfere with, and take precedence over, behaviors aimed specifically at fulfilling
thermoregulatory needs in highly territorial species (Dewitt, 1967; Grigg and
Seebacher, 2000; Khan et al., 2010; Lang, 1987), and social status may itself co-vary
with body size and feeding strategy. The Tbs (mean and variation) that individual
crocodilians maintain in a particular thermal, social and ecological context can be
inherently complex.
The importance of thermoregulation is well recognised in crocodile farming contexts
220
(Hutton and Webb, 1992), where providing an ‘adequate’ thermal environment is
critical to survival, growth and well-being. However, studies of thermoregulation in
hatchling saltwater crocodiles (Crocodylus porosus) have been limited (Lang, 1981).
American alligators (Alligator mississippiensis) exist in climates limited by short
warm seasons, and maintaining them in captivity with high and constant temperatures
(31-32 ºC) improves health and growth rates (Joanen and McNease, 1976). A similar
high and constant thermal regime was assumed to apply equally to Crocodylus species
(Hutton and Webb, 1992), and has been applied in captive situations for C. porosus
(Davis, 2001; Mayer, 1998), Crocodylus niloticus (Hutton and Van Jaarsveldt, 1987)
and Crocodylus siamensis (Lang, 1987). However, there have long been concerns that
some fundamental differences may occur between A. mississippiensis and other
species, and that a more variable thermal environment may be more appropriate for
some crocodilians (Lang, 1987). Captive Alligator sinensis, despite being genetically
close to A. mississippiensis, have poor survival and growth rates at constant
temperature and need to experience winter cooling to maintain good health (Herbert et
al., 2002).
In this study we describe the thermal preferences that hatchling C. porosus exhibit
under controlled laboratory conditions in a thermal gradient and test the hypotheses
that the temperatures selected by hatchlings are not subject to a daily rhythm, and are
not affected by state of feeding or social aggregation (being in a group).
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2. Materials and Methods
2.1 Animals and husbandry
In July-August of 2011, 48 captive-born C. porosus hatchlings, 3-4 months of age,
were obtained from Wildlife Management International (WMI), Darwin, Australia.
Hatchlings originated from 19 clutches collected from the wild (2-30 days old when
collected), and from captive bred stock, and had been artificially incubated at 32 ºC
and 95-100 % humidity. All were raised in the same conditions, with constant water
temperature (32 ºC), and air temperature fluctuating a few degrees higher during the
day than at night. The mean size of hatchlings, when released into the laboratory
gradients at Charles Darwin University, was 214.0 ± 10.0 mm SVL (SD; 190 to 230
mm), 456.6 ± 20.6 mm TL (SD; 410 to 490 mm) and 263.3 ± 35.3 g body mass (SD;
201 to 321 g). Individuals were housed in isolation (N=16) or in groups of four
individuals (N=8 groups). Given that all animals had been subjected to the same
thermal environment from hatching, no period of acclimation at a constant
temperature was considered necessary to counter effects of the previous thermal
history on preferred temperatures (Heatwole et al., 1975).
Experimental enclosures which served as thermal gradients were comprised of glass
tanks (115 cm x 65 cm x 50 cm high) propped up on one end (10 cm high) to create
an area of land (32.5 cm x 57.5 cm) that gradually sloped down to an area of water
(32.5 cm x 57.5 cm x 5 cm deep). They were in a temperature controlled room (22 ± 1
ºC) with a 12:12 h light:dark cycle (light 0700 to 1900h). Two ceramic heating
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elements (150 W and 250 W, Oz Black URS®) were arranged at different heights in
each enclosure to establish an approximately linear temperature gradient on the land
(22-45 ºC). Air and water temperatures were measured throughout the experiment
using temperature data loggers (Thermocron iButtons®) and remained stable at 22 ±
0.5 ºC with no daily fluctuations. This range of temperatures is that what hatchling C.
porosus in northern Australia are exposed to in the wild (Webb et al., 1978), and is
similar to the range used in the thermal gradient studies of Lang (1987). To ensure
hatchlings were not simply using the heating ceramics as cover, several other
ceramics, not connected to power, were placed throughout the tank. The use of
ceramic heat sources, rather than heat lamps, allowed shuttling between land and
water (Grigg and Seebacher, 2000; Seebacher and Grigg, 1997) without
compromising the diurnal light cycle.
The sides of each tank were covered in thin black plastic to restrict visual contact
between adjacent tanks. Preliminary observations, using infrared CCTV cameras
(Signet® IR wide angle) prior to the experiment revealed that individuals settled and
began shuttling between warm and cooler areas within 24-35 hours. Observations of
behavior were collected during the experiment using cameras mounted in the pens and
connected to a digital video recorder (Signet® 4 CH-DVR, model QV-3020).
2. 2 Procedure and protocol
All 48 hatchlings were force-fed temperature data loggers (Thermocron iButtons®).
Each iButton® (12 x 4 mm) was coated with a thin layer of inert liquid plastic
223
(Performix® Plasti dip). The package weighed 3 g and constituted < 1.5% of
hatchling body mass. Each iButton® was calibrated against a mercury-in-glass-
thermometer traceable to a standard, before and after each experiment. Loggers were
programmed to record body temperature at hourly intervals. Crocodilians typically
retain hard objects in their stomach (e.g. gastroliths) and all iButtons® remained in
place until removed at the end of the experiment by stomach flushing (Taylor et al.,
1978). Force-feeding and removal of the iButton® took less than 30 s and appeared to
cause minimal distress to the animals.
To ensure individuals were in a post-absorptive state when the experiments started,
they were fasted for 24 h before release into the pen and allowed 48 additional hours
to settle. For several species of crocodilians, digestion is essentially complete within
48 h of feeding at or near optimal Tb (Coulson and Hernandez, 1979; Garnett and
Murray 1986). Body temperature data over 24 hours (day 3: 0900 h - day 4: 0900 h)
was used to establish initial baseline thermal preferences for each individual, while
fasted, in both isolated (N=16) and group treatments (N=32).
On day 4 (1000 h), randomly chosen hatchlings from the isolated treatment (N=8)
were force-fed a meal of minced red meat, equivalent to 7% of each individual’s body
mass (mean: 18 g), which was considered a satiation meal (Davenport et al., 1990).
The interference involved in force-feeding was undesirable but considered essential to
ensure ‘fed’ animals had all eaten a similar amount of food, and that the amount of
food eaten was considerably greater than the mass of the loggers (3 g). To account for
the potential affect of handling, fasted individuals in the isolated treatments (N=8)
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were subjected to the same force-feeding procedure, but the food was withheld (sham
feeding). Body temperatures from 1100 h on day 4 through to 1100 h on day 5, were
used to test differences in Tb between fasted and fed individuals in the isolated
treatment. All experiments were then terminated. Three of the hatchlings in isolation
(fasted) and three groups of hatchlings were filmed during the 24 h period from 0900
h on day 3 to 0900 h on day 4 to quantify activity cycles. The number of times each
individual moved between land and water was recorded. For the group treatments, the
total number of movements observed in an hour was divided by the number of
animals (N=4). Animals in the social groups were neither fed nor subjected to sham
feeding.
2.3 Statistical analyses
The majority of results are presented as mean Tb with one standard deviation (SD) to
indicate thermoregulatory precision (Khan et al., 2010), and N is provided to allow
calculation of standard errors. Where appropriate, thermoregulatory set point range
(Tset: central 50% of Tbs recorded) and the voluntary thermal minimum (VTmin) and
maximum (VTmax) temperature (Hertz et al., 1993; Huey, 1982) are reported.
Distributions of Tb for individuals and groups showed a high degree of normality
(Shapiro-Wilk’s test) and homoscedasticity (Cochran’s test). A paired t-test (Sokal
and Rohlf, 1995) was used to compare mean Tb and variation (SD) on the same
individuals in isolation before and after feeding (and sham feeding). A repeated
measures ANOVA (mean Tb) and an ANOVA (variation: SD) was used in
comparisons between individuals in isolation that were force fed and sham fed, and
225
between individuals in the isolated and group treatments. An ANOVA was used to
compare mean Tb and variation between active (1100-1700 h) and less active (1800-
1000 h) periods for the same individuals. A significance level of α = 0.05 was used
for all statistical tests. Statistical analyses were performed using JMP 8.0 statistical
software (SAS Institute Inc., 2010).
3. Results
3.1 Behavior
Hatchlings in the gradients displayed classic thermoregulatory behavior, shuttling
between the warm (land) and cooler (land and water) sections of the gradient. When
on land, they were rather inactive, tending to lie flat on the ground in one place, and
then after a time, move to another site (warmer or cooler) and settle. This inactivity
was particularly obvious between 1100 to 1700 h (quiescent period, QP), and
independent of whether individuals were housed in isolation or in groups. Activity
levels were higher at other times (see below; non-quiescent period, NQP), and
markedly so at dusk and early evening. When in water, which was cool (22 ºC),
hatchlings were constantly active and moving before returning to the land.
When on land, individuals that approached the radiant ceramic heaters oriented their
head and anterior trunk towards the heat source. After a period they re-adjusted their
position so the tail and lower trunk were closest to the heater. If positioned in a less
extreme part of the heated area (32-34 °C), they often moved to a cooler section of the
226
land surface (26-28 °C) or adopted a position with part of the body on land and part in
the water. If lying in the warmest section (42-45 °C) of the gradient, or orienting close
to the heat source for a prolonged period, they typically moved directly into the water.
In the group treatments, individuals often lay together, in contact with each other on
parts of the land surface (warm or cool), particularly during the QP. Despite some
aggressive interactions, mainly around dusk and dawn (head strikes and assertive
displays), no individuals appeared to be actively or aggressively excluded from any
section of the gradient by other individuals, as judged by viewing the videos.
3.2 Mean Body Temperatures
The same individual C. porosus in isolation had similar mean Tb’s with similar
variation (SD) the day before force feeding (FF-1: day 3) or sham feeding (SF-1: day3),
and after FF and SF (day 4), and there were no significant differences between FF and
SF treatments (day 4) (N=8 each; Table 1 and 2). There was no significant difference
in mean Tb or variation between the treatment in which individuals were housed in
isolation (N=16) and the treatment in which individuals were housed in groups
(N=32) (Table 1 and 2).
227
Table 1. Mean of mean body temperatures (Tb) (SD and N), set point range
(Tset), and voluntary maximum (VTmax) and minimum (VTmin) for individual C.
porosus in isolation in the force fed (FF-1, FF) and sham fed (SF-1, SF)
treatments, and individuals housed in isolation (fasted; N=16) and individuals
housed in groups (fasted: N=32) in a thermal gradient (22-45 ºC).
Treatment Mean Tb SD N Tset VTmax VTmin
FF-1 30.9 2.2 8 29.2-32.6 37.1 25.1
FF 30.8 2.3 8 29.5-32.4 37.4 24.5
SF-1 30.5 2.3 8 28.7-32.2 36.5 24.7
SF 30.5 2.5 8 28.9-32.2 38.3 23.7
I 30.7 2.3 16 29.1-32.2 37.1 24.7
G 31.1 2.3 32 29.6-32.6 37.6 23.2
FF = force fed, SF = sham fed, FF-1 and SF-1 indicates the FF and SF animals
in isolation 1 day before feeding. I = individuals housed in isolation (fasted),
G = individuals housed in groups (fasted).
228
Table 2. Comparisons of mean (paired t-test or repeated measures ANOVA) and
variation (paired t-test or ANOVA) in Tb between individual C. porosus in isolation
in the force fed (FF-1, FF; N=8) and sham fed (SF-1, SF; N=8) treatments, and
individuals housed in isolation (fasted; N=16) and housed in groups (fasted; N=32),
in a thermal gradient (22-45 ºC).
Treatments Mean Variation
FF-1 and FF t = 0.67, df = 191, P = 0.50 t = -1.04, df = 7, P = 0.33
SF-1 and SF t = -0.59, df = 191, P = 0.56 t = 0.23, df = 7, P = 0.82
FF and SF F1,14 = 0.73, P = 0.41 F1,14 = 0.49, P = 0.50
I and G F1,46 = 1.84, P = 0.18 F1,46 = 0.01, P = 0.94
FF = force fed, SF = sham fed, FF-1 and SF-1 indicates the FF and SF animals
in isolation 1 day before feeding. I = individuals in isolation (fasted), G =
individuals in groups (fasted).
As there was no statistical differences between treatments, Tbs from individuals in a
post absorptive state (day 3) from both the isolated (N=16) and group (N=32)
treatments were combined to give an overall mean Tb of 30.9 ± 2.3 ºC (SD; N=1152).
Fifty percent of Tbs (Tset) were between 29.4 ºC and 32.6 ºC, and the voluntary
maximum (VTmax) and minimum (VTmin) temperatures were 37.6 ºC and 23.2 ºC
respectively.
3.3 Cyclic Body Temperatures
Although mean Tb (Tables 1 and 2) provides a general index of preferred temperature
229
and the effects of feeding and social aggregation on it, at a finer level of resolution the
situation is more complicated. In the thermal environment provided, Tbs of individual
C. porosus fluctuated on a pronounced diurnal cycle (Fig. 1a,b) with significantly
higher Tbs during the QP (1100-1700 h) compared with the NQP (I: F1,382 = 35.42, P
< 0.5; G: F1,766 = 45.22, P < 0.5), with the lowest hourly Tbs during the early morning
(0600-0700 h). Mean Tb was similar during the QP and NQP regardless of treatment
(Table 3).
Fig. 1. Mean Tb (±SE) as a function of time of day, for individual C. porosus housed
in (a) isolation (N=16) and in (b) groups (N=32) in a post-absorptive state in a
thermal gradient. The thin horizontal line is the mean value across all hours and the
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heavy bar indicates the quiescent period (QP).
Table 3. Comparisons of mean Tb (paired t-test or repeated measures ANOVA)
during the QP and NQP between individual C. porosus in isolation in the force fed
(FF-1, FF; N=8) and sham fed (SF-1, SF; N=8) treatments, and individuals housed in
isolation (fasted; N=16) and individuals housed in groups (fasted; N=32) in a thermal
gradient (22-45 ºC).
Mean Tb
Treatment groups Quiescent period Non quiescent period
FF-1 and FF t = 0.48, df = 55, P = 0.64 t = -1.48, df = 135, P = 0.14
SF-1 and SF t = -0.28, df = 55, P = 0.79 t = -0.45, df = 135, P = 0.65
FF and SF F1,46 = 0.16, P = 0.70 F1,46 = 0.81, P = 0.38
I and G F1,46 = 0.18, P = 0.67 F1,46 = 2.8, P = 0.10
As there was no statistical differences between treatments, Tbs from individuals in a
post absorptive state (day 3) from both the isolated (N=16) and group (N=32)
treatments were combined to give a mean Tb of 31.9 ± 2.09ºC during the QP and a
mean Tb of 30.6 ± 2.31ºC during the NQP. However, upon further inspection there
was a significant difference in Tbs (F1,46 = 9.52, P < 0.05) between individuals in the
isolated and group treatments just prior to the QP (0600-1100 h). During this period,
individuals in groups maintained Tbs slightly higher (1.2°C) than individuals in
isolation (Fig 1a,b).
Variation in Tb (SD) was not significantly different between the QP and NQP for
231
individuals housed in isolation (F1,22 = 0.04; P = 0.85) or individuals housed in
groups (F1,22 = 1.91; P = 0.19), although Tbs were more variable at dusk and early
evening (Fig. 2a,b).
Fig. 2. Variation in Tb (SD) as a function of time of day, for individual C. porosus
housed in (a) isolation (N=16) and in (b) groups (N=32) in a post-absorptive state in a
thermal gradient. The thin horizontal line is the mean value across all hours and the
heavy bar indicates the quiescent period (QP).
During the QP individual C. porosus in the isolated (N=16) and group (N=32)
treatments were relatively inactive (I: 2.3 ± 1.46 movements/h; G: 2.0 ± 1.53
232
movements/h) and on land thermoregulating (Fig. 3a,b) whereas during the NQP
individuals were more active (I: 6.2 ± 2.39 movements/h; G: 5.0 ± 2.40 movements/h;
Fig. 3a,b). Activity increased rapidly for individual C. porosus housed in the isolated
(N=16) and group (N=32) treatments immediately after the QP, at dusk and early
evening (1800-2000 h; Fig. 3a,b), when mean Tb declined and variation (SD) was
highest (Fig. 1a,b; 2a,b). The variability in Tb and activity (movements/h) throughout
the day could not be explained by any changes in ambient temperature, which
remained constant across the 24 h period (22.0 ± 0.5 ºC).
Fig. 3. Activity (mean movements per hour ±SE) as a function of time of day,
observed for three individual C. porosus housed in (a) isolation and for three (b)
233
groups of four individuals in a post-absorptive state in a thermal gradient. For the
groups of individuals, the total number of movements in an hour was divided by the
number of animals (N=4). The thin horizontal line is the mean value across all hours
and the heavy bar indicates the quiescent period (QP).
4. Discussion
The Tbs of hatchling C. porosus in this study were broadly similar to those reported
for other species of crocodilian (30-34 ºC) of similar size, measured in thermal
gradients, including C. novaeguineae (Lang, 1981), C. crocodilus (Diefenbach, 1975),
C. siamensis (Lang, 1987), and A. mississippiensis (Lang, 1976). Alligator
mississippiensis is a temperate species of crocodilian that sometimes operates at lower
ambient temperatures than most other crocodilians (Brandt and Mazzotti, 1990). The
mean preferred body temperatures sought by crocodilians appear similar across
species, despite the ability to sustain those temperatures no doubt being affected by
prevailing thermal conditions as affected by season, time of day and geographic
location (Andrews, 1998; Bury et al., 2000; Tracy and Christian, 1986). Hence,
performance in a thermal gradient is likely to provide different insights into preferred
Tb than those obtained by measuring Tb of crocodilians in the wild.
Hatchling C. porosus in this study maintained similar Tbs and thermal precision
regardless of whether they were fasted or fed, as reported for C. crocodilus
(Diefenbach, 1975) and C. novaeguineae (Lang, 1981). We could not reject the
possibility that the data loggers (3 g) could have triggered a feeding response in all
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animals, even though the fed animals received 18 g of food. Alligator mississippiensis
and C. acutus selected higher and less variable Tbs after feeding, although the
response was less pronounced in C. acutus (Lang, 1979). It has been suggested that
the postprandial thermophilic response may be more important for species, such as A.
mississippiensis, that inhabit temperate climates with more variable seasonal
fluctuations in ambient conditions (Lang, 1979; 1987). For crocodilian such as C.
porosus that inhabit tropical climates with relatively constant, year-round warm
temperatures, the need to increase Tb in response to feeding may be unnecessary,
given that ambient conditions can generally be expected to be suitable for digestion
(Lang, 1979; 1987).
In our study, just prior to the QP (0600-1100 h), animals in groups maintained Tbs
slightly higher than individuals in isolation. This difference was minor, and may
reflect grouped animals, with their lateral surfaces often in contact with each other,
heating and cooling more slowly due to changes in the exposed surface area to mass
ratio and its affects on relative insulation. Little biological significance is attached to
this finding.
Individuals in a group basked together, and although aggression was observed, it was
never intense enough to exclude individuals from any section of the gradient. This
suggests that thermoregulation in hatchling C. porosus may not be affected by
agonistic behavior to the same degree as reported for juveniles and adults of several
species, where less dominant individuals were actively excluded (eg. chased) from
optimal thermal habitat by larger animals, and as a consequence had lower and more
235
variable Tbs (Grigg et al., 1998; Johnson et al., 1976; Lang, 1987; Seebacher and
Grigg, 1997). While aggression among hatchling C. porosus may lead to temporary
displacement, hatchlings appear to be largely tolerant of each other when
thermoregulation appears to be a priority for all individuals (basking during the QP).
The general daily cycle of body temperatures reported here, although less pronounced,
is similar to that reported for sub-adults and adults of several crocodilian species
studied in semi-natural enclosures, or in nature (Downs et al., 2008; Grigg et al.,
1998; Seebacher, 1999). In those studies, diurnal variation in ambient temperatures
was an obvious cause of the observed changes in Tb. In our study, Tbs of hatchling C.
porosus were 1-2 ºC higher during the day than at night with over 3 ºC separating the
peak high temperatures (1100-1700 h) from the peak low temperatures (0600-0700 h).
Lower body temperatures at night were correlated with increased activity and time
spent in the water, but activity alone could not explain the peak trough in Tb in the
early morning (0600-0700 h), when for some reason, hatchling C. porosus prefer
lower Tbs.
Because hatchling C. porosus have a behavioral tendency to be in the water at night,
the constant low water temperature (22 ºC) provided in our gradient may have
encouraged lower preferred Tbs than would be adopted if a higher water temperature
had been available. Other gradient studies with hatchling and juvenile crocodilian
species have not reported any clear daily cycle in thermal preference to date (Lang,
1979; 1981). However, these studies involved a temperature gradient in both the water
and on land (Lang, 1979) which could dampen any variation that did exist. Juvenile A.
236
mississippiensis within a gradient preferred to remain in the heated water during the
day, rather than basking on land, despite land basking being a normal and common
behavior in the wild (Lang, 1979). Wild juvenile C. porosus have appreciably higher
food conversion rates than their captive counterparts, which could also be partly
explained by reducing Tb (and maintenance costs) when possible (Webb et al., 1991).
Voluntary night time hypothermia has been observed in some lizards, perhaps for the
same reason (Christian, 1986; Huey, 1982; Regal, 1967).
The increase in activity around dusk and early evening (1800-2000 h), which
introduced more variability in Tb, has also been reported in several crocodilian species
(Lang, 1987). It appears to reflect obligations to forage, but if the risk of predation on
hatchlings by diurnal predators is high, it may also reflect predator avoidance.
The overall mean Tb (31.0 ± 0.07 °C) of three month old hatchling C. porosus in this
study was slightly lower than that reported for both hatchlings less than 10 days old
(33.2 ± 0.3 °C; N=6) within an indoor enclosure (Lang, 1981), and for free-ranging
adults and sub-adults in a natural enclosure during the summer (28.4-33.6 °C, N=11;
Grigg et al., 1998; 32-33.1 °C, N=14, Johnson et al., 1976). However, the differences
were less if only Tb during the QP (31.9 ± 2.09 ºC) is considered as the best index of
preferred Tb. Thus, while thermoregulatory behavior of C. porosus no doubt changes
with increasing size (Spotila et al., 1972), altering the time taken to heat and cool,
preferred temperature does not appear to vary greatly with increasing size, as found
for C. niloticus, A. mississippiensis, and C. novaeguineae (Lang, 1987). Similar
preferred temperatures across sizes is also found in other large reptiles, such as
237
Komodo dragons (Varanus komodoensis), in which body size changes dramatically
between hatching and adulthood (Harlow et al., 2010).
In captivity, hatchling C. porosus exhibited higher growth and survival rates when
raised at a temperature experienced during incubation (Webb and Cooper-Preston,
1989; Webb et al., 1991), relative to either lower or higher constant temperatures
(Davis, 2001; Mayer, 1998; Webb et al., 1991). However, the current common
practice of raising hatchling C. porosus at constant warm temperatures (32-34 ºC air
and, or water) may not be optimising body temperature regulation and could be
constraining growth and survival rates (Licht, 1973; Wilhoft, 1958). Experimentation
with more variable thermal regimes, in the form of gradients or fixed temperature
cycling within the Tset range would seem warranted.
Acknowledgements
We thank Charlie Manolis and Jemeema Brien for their help in different phases of the
project. We would also like to thank Wildlife Management International for the
supply of animals, and for logistical support. WMI funding through the Rural
Industries Research and Development Corporation is gratefully acknowledged.
Funding for equipment was provided through a Holsworth Wildlife Research
Endowment (ANZ Trustees Foundation), Charles Darwin University, and a Northern
Territory Research and Innovation student grant. Experimental protocols were
approved by the Charles Darwin University Animal Ethics Committee, Darwin
(Animal ethics permit number A11003).
238
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Chapter 5.1. Out of sight or in too deep: effect of visual barriers and
water depth on agonistic behaviour and growth in hatchling
saltwater crocodiles (Crocodylus porosus)
Published as: ‘Brien, M.L., Gienger, C.M., Webb, G.J., McGuinness, K.A., Christian,
K.A., 2014.Out of sight or in too deep: effect of visual barriers and water depth on
agonistic behaviour and growth in hatchling saltwater crocodiles (Crocodylus
porosus)’. Animal Behaviour Science: in press. Formatted according to author
guidelines for journal.
Abstract
This study tests the role of visual barriers and water depth on levels of agonistic
behaviour and growth in hatchling Crocodylus porosus within the first 3 weeks of life.
Ninety-six individuals from four separate clutches hatched over 2 days were divided
across three treatments containing two groups with 16 individuals each: shallow water
with no visual barrier (SW), shallow water with visual barriers (VB), and deep water
with no visual barrier (DW). Body mass (BM-g) was measured at introduction and
after 21 days, and was used as an index of growth. Behaviour was described and
quantified in the night (17:00-8:00 h), when there is an innate peak in behavioural
interactions, for three consecutive nights on two occasions (days 9-11 and 18-20 post-
hatch). Visual barriers in open shallow water (VB: mean 0.7 interactions/night) nearly
eliminated agonistic behaviour relative to SW (mean 10.8 interactions/night; P <
0.05). DW did not reduce the frequency of agonistic interactions relative to SW, but
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did affect the outcome of interactions (P < 0.05), with both individuals swimming off
slowly. The distribution of hatchling growth after 21 days was highly bimodal
regardless of treatment, with a group of slow growing (-3.6 to <6 g change in BM)
and fast growing hatchlings (6-15 g increase in BM). Although this made statistical
comparisons difficult, there was no clear effect of any treatment (P < 0.05) on mean
growth rates. The results of this study suggest that there may be utility in providing
hatchling and juvenile C. porosus in captivity with a more complex raising
environment in order to reduce negative social interactions, but it is not clear whether
this improves growth and survival.
Keywords: Crocodylus porosus, hatchlings, agonistic behaviour, growth, visual
barriers, water depth.
1. Introduction
Many species in captivity face a range of environmental and social challenges
which can cause stress and lead to a reduction in survivorship (Kristiansen et al.,
2004; Morgan and Tromborg, 2007). In farming situations, individuals often have to
contend with restricted space, higher than natural densities, and insufficient cover or
places to hide (Morgan and Tromborg, 2007). How well a species is able to adapt to
captivity is dependent upon the level of intraspecific aggression and tolerance to
conspecifics, and the complexity of the raising environment itself (Price, 1999;
Kristiansen et al., 2004).
The structure and complexity of the habitat has a strong influence on the social
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behaviour of many animals, especially in captivity (Petren and Case, 1998; Price,
1999). The use of artificial cover objects, dividers, and barriers have been successful
in reducing the frequency and intensity of agonistic interactions in several groups of
captive animals, including fish (Kadry and Bareto, 2010), pigs (McGlone and Curtis,
1985), red deer (Whittington and Chamove, 1995), chickens (Estevez et al., 1998;
Cornetto et al., 2002), goats (Aschwanden et al., 2009), and macaques (Estep and
Baker, 1991). Cover objects and barriers enable less dominant individuals to escape or
avoid such interactions (Price, 1999), which can in turn result in improved rates of
growth and survival.
In the wild, hatchling crocodilians typically occupy habitat at the water’s edge that
provides a high degree of protective cover in the form of vegetation, logs, and
branches (Mazzotti et al., 2007). Hatchlings use the complexity of their environment
to hide from predators, locate prey, regulate body temperature, and to possibly avoid
negative social interactions, as has been suggested for other species of animal (Estep
and Baker, 1991; Cornetto et al., 2002). However, in captivity, hatchling crocodilians
have fewer options for protective cover, and are often forced together in smaller
spaces at higher densities than would be encountered in the wild (Hutton and Webb,
1992).
Agonistic behaviour among juvenile crocodilians, along with clutch of origin, has
been implicated in highly variable growth and survival rates in captivity
(Huchzermeyer, 2003), and this variation in growth is established within a few weeks
post-hatching (Hutton and Webb, 1992; Brien et al., 2013). Regular size grading is a
common strategy used by farmers to manage agonistic behaviour which alleviates the
stress placed on smaller crocodiles by removing larger more dominant ones (Riese,
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1991; Hutton and Webb, 1992). Another strategy is the provision of a hide or shelter
that covers a section (15-60%) of the raising enclosure which provides refuge and
may also reduce agonistic behaviour (Hutton and Webb, 1992; Huchzermeyer, 2003).
Although few published studies have examined the effectiveness of these strategies, it
is widely acknowledged that they are important in reducing stress and improving
growth and survivorship in juvenile crocodilians (Riese, 1991; Mayer, 1998;
Huchzermeyer, 2003).
The saltwater crocodile (Crocodylus porosus) is considered the most aggressive
and least tolerant of conspecifics, which affects their captive management (Lang,
1987; Brien et al., 2013a, 2013b, 2013c). In captivity, agonistic behaviour is present
shortly after hatching (within 2 days) and has been implicated in reduced rates of
growth and subsequent mortality of hatchling C. porosus through ‘runtism’ or ‘failure
to thrive syndrome (FTT)’ on crocodile farms in Australia (Onions, 1987; Isberg et
al., 2009; Brien et al., 2014). Agonistic interactions occur primarily between two
individuals during defined activity periods (dusk and dawn) in shallow, open water
areas of the pen (<8 cm), which also coincides with feeding (Brien et al., 2013a).
In this study, we test the hypotheses that the frequency and type of agonistic
interaction between hatchling C. porosus would not be affected by: (a) increasing the
environmental complexity in a way that restricts visual contact between individuals;
and (b) increasing water depth. We also used absolute growth (body mass - BM) of
hatchling C. porosus after the first few weeks post-hatching as a predictor of longer
term growth and survival (Brien et al., 2014).
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2. Animals, materials, and methods
2.1. Animals and housing conditions
In March of 2012, 96 captive-born hatchling saltwater crocodiles (C. porosus)
were obtained from Wildlife Management International (WMI; Darwin, Australia).
They originated from four clutches collected from the wild (embryo age at collection
for each clutch ranged between 2-30 days) that had been artificially incubated at 32º C
and 95-100% humidity. After hatching (16-17th March 2012), individuals remained in
the incubator (32º C) for 3 to 4 days which allows early detection of compromised
individuals (none found here).
On the 20th of March 2012, 24 hatchlings from each of the four clutches (N = 96)
were divided into six groups of 16, each group consisting of four individuals
randomly selected from each clutch. The groups were allocated randomly to six tanks,
two of which contained a ‘visual barrier’ with shallow water (VB), two had ‘deep
water’ without visual barriers (DW), and two had ‘shallow water’ without visual
barriers (SW), regarded as normal practice controls. For each animal, snout-vent
length (SVL - mm), and body mass (BM - g) were measured and a uniquely numbered
metal tag (Small animal tag 1005-3, National Band and Tag Co., Newport, Kentucky,
USA) was attached between the webbing on the rear right foot prior to release into the
tank.
Hatchlings remained in these treatments for 21 days, before recapture and
measurement on day 22 (11th April 2012), with change in body mass (g) for each
individual used as an index of growth. Food was withheld for 24 h prior to this second
set of BM measurements.
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Treatment groups were fed chopped red meat supplemented with di-calcium
phosphate (4%) and a multivitamin supplement (1%) at 16:00-17:00 h each day ad
libitum, with waste removed the following morning (8:00-9:00 h) when the water was
changed. Water temperature was 24-28° C when changed, but was heated and
maintained at 32-34° C by two aquarium heaters (300 W Hydor Theo®, Just
Hydroponics, Melbourne, Victoria, Australia) thereafter. Ambient air temperatures
varied from 26-34° C, which are within the preferred range for this species at this life
stage (Brien et al., 2012). There was a 9:15 h light:dark cycle, with treatment groups
exposed to low levels of natural light during the day (light: 08:00-17:00 h), and
complete darkness from late afternoon (17:00 h) through to early morning (08:00 h).
The plastic tanks used to house treatment groups were oval shaped (220 x 110 x 50
cm), with a land area (approx. 75 x 110 cm) that gradually sloped down to a water
area (approx. 145 x 110 cm) (1000 L Oval Water Tub, Reln Pty. Ltd., Ingleburn, New
South Wales, Australia; Fig. 1). In the SW and VB tanks, the water level ranged from
4-8 cm, while in the DW tanks it ranged from 8-18 cm which was achieved by
elevating the front of the tank. At this greater depth, hatchlings either could not stand
or had difficulty touching the bottom comfortably. A ‘hide area’ (Riese, 1991; Mayer,
1998) was provided in each enclosure, and was constructed with eight lengths (50 cm
long) of 10 cm PVC pipe strapped together and on legs, positioned so that it covered
equal portions of land and water (Fig. 1).
In the VB tanks, the visual barrier was a square frame (110 cm long x 100 cm
wide) constructed with lengths of 2.5 cm diameter PVC pipe on legs also made from
PVC pipe (15 cm high). A total of 14 interlocking sheets of 1 mm thick, black, high-
density polyethylene film (HDPE) (110 cm long x 10 cm tall) were suspended from
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underneath the frame so that they hung down at the waters’ surface. Seven sheets
were suspended length ways with slits in the top so that the other seven sheets could
slot in and run perpendicular forming a more or less evenly spaced pattern of 6 x 6
grids across the water surface (Fig. 1). The sheets were also extended to form a further
six half open spaces on each side of the frame (Fig. 1). From preliminary trials, these
visual barriers did not restrict movement with individuals able to swim underneath the
suspended sheets with ease. This setup also allowed a clear view from above for
filming.
Agonistic behaviour among hatchling C. porosus of this age, under captive
conditions, occurs almost exclusively in areas of open water (Brien et al., 2013).
Therefore, the barrier structure was placed in the water adjacent to the hide area of
PVC pipes in order to eliminate open water. The intention of the visual barrier
structure was to replicate conditions experienced in the wild, in which hatchling C.
porosus exist at the waters’ edge in amongst vegetation, logs, and branches that
provide both visual and physical separation from conspecifics.
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Fig. 1. Top view (a) of the shallow water and deep water (left side) and visual barrier
tanks (right side) and side view (b) of the shallow water and deep water (top) and
visual barrier tanks (bottom).
2.2. Behaviour
A wide angle infrared CCTV camera (96º angle QV-8104, Signet, Brisbane,
Queensland, Australia) was used in each tank to record behaviour on digital video
recorders (4CH DVR QV-8104, 25 frames/s, Quad Mode, Signet, Brisbane,
Queensland, Australia). A recording period lasted 15 h (17:00-8:00 h), and was
conducted on three consecutive nights for each treatment group (45 h each) under
complete darkness with infrared cameras enabling clear viewing. This time period is
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when the majority of agonistic interactions among hatchling C. porosus occur under
captive conditions (Brien et al., 2012; 2013). The recordings were taken 9 (8-10) and
18 (17-19) days after the crocodiles were placed in the treatment tanks and were
viewed and assessed the following day by the same single observer. For each
recording period (17:00-8:00 h) all agonistic interactions that occurred were recorded.
An agonistic interaction was any interaction in which aggression was signalled by
postures or actions by one or both individuals (Table 1; Fig. 2). For each interaction,
the behaviours exhibited, number of individuals involved and displaying aggression,
the intensity of interaction (low, medium, high), the location (water, hide, land), the
time, duration of interaction, and outcome were also recorded (Table 1; Fig. 2).
Table 1. Ethogram of behaviours used by hatchling C. porosus during agonistic
interactions (derived from Brien et al., 2013a).
Abbreviation Definition
Initiation
Rapid advance RA Series of short rapid advance movements
towards another individual while LIW.
Chase C Rapid movement toward another individual in a
LIW posture.
Posture
Low in water LIW Immobile with only the top of the head and back
above the water surface (Fig. 2a).
Inflated posture IP Immobile with upward extension of either the
front two or all four limbs, with neck and back
arched high and head and tail angled downward
(Fig. 2b).
Head and tail raised HTR Immobile with head and tail raised out of water
while back remains low. Head is usually parallel
to the water but can also be angled upwards
(Fig. 2c).
Head raised high
HRH
Immobile with upward extension of the front
two limbs pushing the head and chest high out
of the water on a ~45º angle while tail remains
low (Fig. 2d).
Mouth agape MA Immobile with mouth opened wide (in
combination with postures LIW, IP, HTR or
HRH; Fig. 2e).
Non-contact
movements
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Light jaw-clap LJC Rapid opening and closing of the jaws at the
water surface, often repeated several times (LIW
or IP posture; Fig. 2f).
Tail-wagging TW Undulation of the tail from side to side in either
a gentle sweeping motion or rapid twitching,
often repeated several times (all postures; Fig.
2g).
Contact movement
Head push HP Head is pushed in to an opponent, usually with
mouth closed (LIW or IP posture).
Bite B Jaws closed shut on an opponent (all postures).
Side head-strike SHS Head is thrust sideways in to an opponent while
the mouth is either open or closed (all postures).
Tail-wag side head
strike
TWSHS Tail wagging occurs prior to a side head strike,
increasing the force of the impact (all postures;
Fig. 2h).
Tail-wag bite TWB Tail wagging occurs prior to a bite which
propels the individual in to an opponent with
force (LIW posture; Fig. 2i).
Aggressive
individual
One that advances toward another and, or that
makes physical contact with another.
Duration of
interaction
Measured from when an individual advances
rapidly toward another or makes contact,
whichever comes first, until agonistic
behaviours cease or an individual moves away.
Intensity of
interactions
Low Contact is made after individuals lying together
disturb each other when moving, or after one
swims into another underwater.
Medium One individual approaches another and initiates
an agonistic interaction.
High One individual approaches another and initiates
an agonistic interaction. High intensity
interactions are distinguished from medium
intensity interactions by the display of more
intense contact behaviours, either TWB or
TWSHS.
Outcome
Both stand ground Both individuals remain in the vicinity of each
other in LIW posture.
One swims off
slowly
One individual swims slowly away from the
other in a LIW posture.
Both swim off
slowly
Both individuals move slowly away from each
other in LIW posture.
One swims off
rapidly
One individual moves rapidly away from the
other individual in a LIW posture.
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Fig. 2. Postures, non-contact and contact movements, described in Table 1, displayed
by hatchling Crocodylus porosus during agonistic interactions (derived from Brien et
al., 2013).
2.3. Statistical analyses
Statistical analyses were performed using GenStat 12.2 statistical software (VSN
International Ltd, Hemel Hempstead, Hertfordshire, United Kingdom). For each
analysis the effect of treatment was examined as a three treatment x two replicate,
completely random design. For some count data diagnostic tests on residuals from an
ANOVA indicated that a square-root (of X+0.5) transformation on the counts was
appropriate before analysis. In such a case, treatment means were back transformed to
257
original units. A split-plot ANOVA of growth data examined the effect of clutch.
Because the analysis of treatment was based on tank average data, the fact that
animals within tanks displayed bi-modal patterns in growth did not violate
assumptions of normality in the ANOVA. As there was a consistent behavioural
response by each treatment across all nights, the behavioural data from the two
recording periods (days 7-9 and 17-19) was combined for analysis. To account for
lack of independence over time, repeated measures ANOVA’s were used to examine
the effect of treatment on the mean number of agonistic interactions, number of
contacts per interaction, duration of an interaction, number of individuals displaying
aggression per interaction, and intensity (low: 1; medium: 2; high: 3). Pair-wise
comparisons were done using a protected Fisher's LSD procedure. A Chi-square test
was used to analyse the effect of treatment on the outcome of an interaction. Due to
insufficient data (total: 9 interactions), this analysis did not include the Barrier
treatment. Back transformed means are presented in each case, with transformed
means (±SE) also presented for significant results. A significance level of P < 0.05
was used for all statistical tests.
3. Results
3.1. Growth
There was no significant effect of clutch (F3,9 = 1.81; P = 0.22) or treatment x clutch
interaction (F6,9 = 0.21; P = 0.97) on hatchling growth of the animals. There was also
no significant effect of treatment on hatchling growth in BM (F2,3 = 1.17, P = 0.42).
Back-transformed mean growths for the VB, SW, and DW groups were 4.0, 4.0, and
258
4.2 g respectively. In fact growth of animals in all six tanks was similar (Fig. 3), and
appeared to demonstrate two distinct patterns of growth: animals that lost weight or
grew little (slow growing: -3.6 to <6 g change in BM), and those that grew rapidly (fast
growing: 6-15 g increase in BM; Fig. 3).
Fig. 3. Initial body mass and change in body mass after 21 days for hatchling
Crocodylus porosus in each of the six treatment groups (shallow water; visual barrier;
deep water). Individual dots represent individual animals.
3.2. Behaviour
Hatchlings in all three treatments were primarily active at dusk and dawn, which
coincided with feeding in which individuals would grab food from where it was
placed on land and retreat to the water to eat. In most cases, the frequency of agonistic
259
interactions was also higher during these times. Agonistic interactions involved only
two individuals at any one time. A square-root transformation was applied to the
number of agonistic interactions per night before analysis. The number was
significantly lower (F2,3 = 460.16, P < 0.05) among hatchlings in the VB treatment
(0.7) than among those in the SW (10.8) and DW (9.3) treatments. Transformed
means for VB, SW, and DW groups were 1.1 ± 0.10 SE, 3.4 ± 0.03 SE, and 3.1 ± 0.06
SE respectively.
The mean duration of an agonistic interaction did not differ significantly (F2,3 =
5.24, P = 0.11) across treatments in the analysis of square-root transformed data.
Back-transformed means were 12.6, 24.6, and 9.0 for treatments VB, SW and DW
respectively.
The mean number of individuals displaying aggression during an interaction (one
or both) did not differ significantly with treatment (F2,3 = 0.08, P = 0.92), with only
one individual displaying aggression in 56.6 % of interactions. Back-transformed
means for VB, SW and DW were 1.5, 1.4, and 1.4 respectively.
The mean number of contact movements made by an individual during an
interaction did not differ significantly across treatments (F2,3 = 8.33, P = 0.06), with
back-transformed means of 1.3, 1.9 and 0.9 for VB, SW and DW respectively.
The mean intensity of interactions did not differ significantly between treatments
(F2,3 = 2.43, P = 0.24), with 28.9% low, 27.7% medium, and 43.5% high intensity
interactions over all tanks. However, the outcome of an interaction differed
significantly between the SW and DW treatments (X2 = 196, df = 4, P < 0.05). The
majority of interactions in the SW treatments resulted in both individuals standing
their ground, while in the DW treatments most interactions resulted in both
260
individuals swimming off with some also resulting in one individual swimming off
rapidly (Fig. 4).
Fig. 4. Outcome of agonistic interactions between hatchling Crocodylus porosus
in the shallow water (N = 32) and deep water (N = 32) treatments over three
consecutive nights (17:00-8:00 h) at 9 days and 18 days post-hatching. Mean
percentages and SE.
4. Discussion
The results of this study demonstrate that the provision of a visual barrier in open
water areas reduced, and nearly eliminated (~90% reduction), agonistic interactions
among hatchling C. porosus in captivity during the first few weeks post-hatch.
Significant reductions in the frequency of agonistic interactions due to the provision
of visual barriers or cover have also been reported in captive populations of deer (60%
reduction; Whittington and Chamove, 1995), pigs (40% reduction; McGlone and
Curtis, 1985), bulls (87% reduction; Chamove and Grimmer, 1993), and macaque
monkeys (30-50% reduction; Estep and Baker, 1991).
261
In all of these studies, the barrier effectively increased the complexity of the
environment, making it difficult for individuals to view or encounter each other while
also providing escape options. In hatchling crocodilians, this situation is similar to
what they encounter in the wild, where they tend to occupy vegetation, branches, or
logs at or near the waters’ edge (Mazzotti et al., 2007). While this type of habitat is
important in providing shelter and prey (eg. shrimp, fish, insects) it would also
influence social interactions, as has been reported in lizards (Petren and Case, 1998).
While increased water depth did not reduce the frequency of agonistic interactions
between hatchling C. porosus, it did affect the outcome with one or both individuals
forced to swim off in the majority of interactions. Deeper water made it difficult for
hatchlings to engage in agonistic behaviour, as they were unable to touch the ground
and were forced to expend energy maintaining their position at the water’s surface. In
comparison, hatchling C. porosus in shallow water (<8 cm) were able to stand their
ground during encounters with less effort.
Despite the effect of visual barriers and deep water on the frequency and nature of
agonistic interactions, this was not associated with any difference in mean growth
between the three treatments. This suggests that visual forms of agonistic behaviour
may be unimportant in influencing rates of growth at this early life stage. However,
previous research has demonstrated that visual forms of agonistic behaviour in
hatchling C. porosus in captivity develop shortly after hatching and are important in
the formation of dominance hierarchies within the first year of life (Brien et al., 2013).
As a consequence, dominant individuals grow rapidly, while subdominants have
lower rates of growth and survival. Therefore, the effect of visual barriers and deeper
water levels on agonistic behaviour and rates of growth and survival may be either
262
delayed, or are more important among older hatchling and juvenile C. porosus in
which the frequency of agonistic interactions is higher (Brien et al., 2013).
Although the importance of visual displays during agonistic interactions has been
widely reported, many animals also employ chemical and vocal forms of
communication (Lang, 1987; Mason and Parker, 2010). Chemical signalling plays a
significant role in communication among many animals (Mason and Parker, 2010),
including several species of lizard (Duvall et al., 1979; Burghardt, 1977) and snakes
(Carpenter and Ferguson, 1977), which begins shortly after hatching. Although
chemical communication is poorly understood in crocodilians, they possess two sets
of semio-chemical glands (throat and cloaca) (Mason and Parker, 2010) that are
believed to be used by adult males in marking territories and deterring rivals (Herzog
and Burghardt, 1977). As chemical signals can be detected by the receiver in the
absence of the signaller (Gosling and Roberts, 2001), it is possible that chemical
signals may be used by hatchling C. porosus to communicate, among other things,
aggressive intent.
Vocalisations are considered to be important forms of communication among
crocodilians (Herzog and Burghardt, 1977; Lang, 1987), especially among hatchlings
which vocalise with each other and the mother to signal danger, and keep the crèche
together (Lang, 1987). As adult crocodilians use vocalisations during agonistic
interactions (Herzog and Burghardt, 1977; Lang, 1987), it is possible that hatchlings
may do the same. However, we did not record audio during this study.
Regardless of whether other forms of social communication are employed by
hatchling C. porosus, they may simply be a consequence of the factors driving
variation in growth trajectories, rather than their proximate cause. For instance,
263
genetics and conditions experienced during incubation (ie. the clutch affect) have long
been known to have a strong underlying affect on growth and survival in crocodilians
and may be the ultimate driver (Webb and Cooper-Preston, 1989). However, there
may also potentially be a wide range of other variables responsible that are associated
with the raising environment itself.
5. Conclusion
Although the provision of a more complex raising environment did not result in
improved rates of growth among hatchling C. porosus, it did reduce the frequency of
agonistic interactions which would reduce the incidence and severity of injuries
among hatchling and juvenile C. porosus in captive settings. However, the provision
of a more complex raising environment may be more important in improving growth
rates among C. porosus at higher densities or at a later age and size when agonistic
interactions are more frequent and intense.
Acknowledgements
We would like to thank Wildlife Management International for the supply of
animals, use of facilities and logistical support. WMI funding through the Rural
Industries Research and Development Corporation is gratefully acknowledged.
Funding for equipment (cameras, digital video recorders) was provided through a
Holsworth Wildlife Research Endowment (ANZ Trustees Foundation), a Northern
Territory Research and Innovation Board student grant, IUCN Crocodile Specialist
Group student grant, and Charles Darwin University. Funding was also provided
264
through ARC Linkage grant LP0882478 awarded to authors KAC, CMG, and
GJW. We would like to thank one of the reviewers, Bob Mayer, for his very generous
assistance with the statistical analyses. Experimental protocols were approved by the
Charles Darwin University Animal Ethics Committee (Animal ethics permit number
A11003).
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Chapter 5.2. Effect of density on growth, agonistic behaviour, and
activity in hatchling saltwater crocodiles (Crocodylus porosus)
Abstract
Hatchling C. porosus were raised (two replicates) in identical enclosures (1.5m2), in
different group sizes (5, 10, 20 and 30) giving four densities (3.3, 6.7, 13.3 and 20.0
hatchlings/m2; or 0.30, 0.15, 0.08 and 0.05m
2/hatchling respectively). Hatchlings
came from five different clutches, hatched on the same day, spread evenly between
treatments. Growth was assessed between 4 and 25 days of age, which is a reliable
indicator of post-hatching growth trajectories for this species. Clutch and initial body
mass (BM) had a strong influence on growth, with lower growth among the largest
hatchlings born. The highest mean growth in body mass occurred at 6.7/m2
(6.12±1.24g) and was lowest at the highest density (20.0/m2: -2.33±0.63g).
Behavioural observations taken every 10 minutes on day 19 (24 h period) confirmed
that hatchlings remained relatively inactive and hidden under cover for most of the
day, and were more active at night, with peaks at dusk and dawn. However, the level
of hourly activity (mean movements per individual per hour) was highest at densities
of 13.3/m2 (0.44±0.10) and 20.0/m
2 (0.43±0.09), compared with densities of 3.3/m
2
(0.15±0.07) and 6.7/m2
(0.12±0.07). Behavioural observations at 17:00-08:00h over
three days (days 17-19) revealed that the frequency of agonistic interactions (mean
per animal per night) was highest at the lower densities (3.3/m2: 1.70±0.16; 6.7/m
2:
1.20±0.06) and decreased with increased density (13.3/m2: 0.71±0.04; 20.0/m
2:
0.49±0.03). The results suggest that as density increases above 6.7/m2, growth in
hatchling C. porosus during the first three weeks begins to decline as activity
269
increases. However, at the lowest density (and group size: 5), one or two individuals
become dominant and grow large at the expense of the remaining hatchlings.
Management implications are discussed.
Introduction
Animals in captivity are subject to a range of environmental and social challenges
which can impact the well-being and fitness of individuals (Kristiansen et al. 2004;
Morgan and Tromborg 2007). How a species responds to changes in population
density under captive conditions is dependent upon the level of intraspecific
aggression and social tolerance (Browns and Orians 1970; Kristiansen et al. 2004).
Understanding the role of density in shaping behaviour, growth, and survival of a
species is essential for optimising production and improving animal welfare in captive
situations (Estevez et al. 2007; Rodenburg and Koene 2007).
Growth and survival of many animals (eg. fish, poultry, pigs, cattle) under captive
conditions is often reduced when raised at unnaturally high densities or group sizes
(Weng et al. 1998; Kristiansen et al. 2004; Estevez et al. 2007). However, how social
interactions and activity are affected by density or group size is inconsistent (Estevez
et al. 2007). Increasing group size can result in higher (Estevez et al. 1997; Fisher et
al. 1997), lower (Hughes et al. 1997; Estevez et al. 1997), or no change (Schmolke et
al. 2003) in the frequency of agonistic interactions in different species. A few studies
have examined the effect of group size or density on activity patterns, with lower
activity observed at higher densities in chickens (Estevez et al. 1997) and rabbits
270
(Morrise and Maurice 1997), but higher activity at higher densities reported in fish
(Holm et al. 1998; Kristiansen et al. 2004).
Stocking density is an important consideration when raising crocodilians in captive
situations, with low rates of growth and survival and high rates of injury and illness
associated with high densities (Webb et al. 1983; Elsey et al. 1990; Hutton and Webb
1992). However, most studies have tended to report no significant effects of density
on mean rates of growth or survival (Zilber et al. 1992; Webb et al. 1983; Garnett and
Murray 1986), but this is partly a result of extreme variation in individual growth
rates. These studies have also been confounded by different pen types, land to water
ratios, level and type of cover, group sizes, densities, species, sizes and ages, and
degree of temperature control (Riese 1991; Mayer 1998). Furthermore, clutch effects
have not always been adequately accounted for, despite their significant influence on
individual performance (Webb and Cooper-Preston 1989). In virtually none of these
studies has behaviour been considered.
The saltwater crocodile (Crocodylus porosus) is the largest species of crocodilian and
produces the most commercially valuable skin (Webb and Manolis 1989; Fuchs
2006). In the wild, most hatchling C. porosus exist in crèches of 30-80 individuals
with the parental female for the first two months of their lives (Webb et al. 1977),
although there are exceptions (Magnusson, 1979). After this they disperse, which is
generally considered a response to growing intolerance of each other (Webb and
Messel 1978). In captivity, hatchlings also have a strong tendency to group together
(Webb et al. 1994), despite agonistic behaviour, the frequency and intensity of which
271
is affected by clutch and increases with age during at least the first year of life (Brien
et al. 2013a). Agonistic behaviour has been implicated in reduced rates of growth and
increased mortality of hatchling C. porosus on crocodile farms in Australia (Riese
1991; Isberg et al. 2009).
The recommended density guideline for raising hatchling C. porosus during the first
few months of life is 10-15/m2 (Australian COP 2009), but this is based on general
experience rather than experimental results. Therefore, the objective of this research
was to quantify the effect of density on growth, behaviour, and activity in the
immediate post-hatching period, which is considered crucial in determining long term
patterns of growth and survival in C. porosus (Webb and Cooper-Preston 1989;
Hutton and Webb 1992; Brien et al. 2014).
Methods
Subjects and housing
In April of 2012, 129 captive-born hatchling C. porosus were obtained from Wildlife
Management International (WMI; Darwin, Australia). Hatchlings originated from five
clutches of eggs collected from the wild (embryo age: 2-30 days) that had been
artificially incubated at 32ºC and 95-100% humidity. After hatching, individuals
remained in the incubator (32ºC) for three days to assist in the assimilation of residual
yolk. On day four, hatchlings from each of the five clutches were randomly assigned
and transferred to experimental enclosures where they were assigned to one of four
272
densities (Table 1). In this experiment we did not separate density from group size,
with the same enclosure (size and shape) used to house different numbers of hatchling
C. porosus.
Table 1. Group size and density of hatchling C. porosus with and without
basking cage included.
Group
size
Number of
groups
Density
(hatchling per m2)
Density
(m2 per hatchling)
5 2 3.3 0.30
10 2 6.7 0.15
20 2 13.3 0.08
30 2 20 0.05
Experimental groups were housed in box-shaped concrete enclosures with a core pen
area of 1.5m2
(75 x 200 cm; walls 150 cm high), comprising a land area (0.6m2; 75 x
80 cm) that gradually sloped to a water area (0.9m2; 75 x 120 cm x < 19 cm deep).
Five lengths (80 cm long) of 10 cm PVC pipe strapped together and on legs were used
as a ‘hide area’ centrally positioned in the water (partly immersed) but overhanging
the land. To increase thermal options, an outdoor ‘basking cage’ (100 x 120 x 150 cm
high), accessible through a hole in the wall (10 x 20 cm), was attached to each
enclosure. The results confirmed that most time was spent in the core area of each
enclosure (1.5m2), which is used for all density analyses, and the extra area provided
by the basking cages was ignored.
Hatchling groups were fed chopped red meat supplemented with di-calcium
phosphate (4%) and a multivitamin supplement (1%) at 16:00-17:00 h ad libitum each
273
day, with waste removed the following morning (08:00-09:00 h) when the water was
changed. Water temperature was 24-28°C when changed (total 1h), but was heated
and maintained at 32-34°C by a gas hot water system. Ambient air temperatures
varied from 26-34°C throughout the day, and there was a natural light cycle. These
temperatures are within the preferred range for this species at this life stage (Brien et
al. 2012).
For each animal, snout-vent length (SVL - mm), and body mass (BM - g) were
measured and a uniquely numbered metal tag (Small animal tag 1005-3, National
Band and Tag Co.) was attached between the webbing on the rear right foot prior to
release into the enclosures. The increase in body mass (BM-g) for each individual was
used as an index of growth. Hatchlings remained in these treatment groups for a
period of 21 days, before they were captured and re-measured on day 22. Food was
withheld for 24 h prior to the second BM measurements on day 22. This initial post-
hatching period is critical in determining rates of growth and survival after 300 days
(Brien et al. 2014), and after several years in this species (Webb and Cooper-Preston
1989).
Behaviour
Wide angle infrared CCTV cameras (Signet, 92.6º) in each enclosure were used to
record behaviour on digital video recorders (Signet 4CH DVR QV-8104). A recording
period lasted 15 hours (17:00-08:00 h), and was conducted on two consecutive days
for each group (30 h per group). The recordings were taken 18 and 19 days after the
274
crocodiles were placed in the new experimental enclosures. When scoring the
observations, an agonistic interaction was defined as any interaction between
individuals in which intolerance was signalled by postures or actions by one or both
individuals (Brien et al. 2013a). The total number of agonistic interactions observed
and the total number of agonistic interactions divided by the number of animals was
calculated.
For each agonistic interaction, the duration and intensity was also recorded. The
intensity of an interaction was characterised as: low, medium or high (Brien et al.
2013a). Low intensity interactions appeared accidental, occurring when individuals
lying together appeared to disturb each other when moving, or if one swam into
another underwater. Medium and high intensity interactions appeared deliberate, with
one individual approaching another with the goal of initiating an agonistic interaction.
High intensity interactions were distinguished from medium intensity interactions by
the display of more intense contact behaviour (Brien et al. 2013a).
One group of hatchlings from each of the four densities was filmed during the 24h
period from 17:00 h on day 18 to 17:00 h on day 19 to quantify habitat use and rates
of activity. The number of animals that were observed moving (swimming or
walking) along with the position of each individual in the enclosure (land: exposed;
water: exposed; under hide: covering equal parts land and water; at entrance to
outdoor cage; inside outdoor cage) was recorded every 10 minutes. The total number
of movements observed in an hour and the total number of movements in an hour
divided by the number of animals was calculated.
275
Statistical Analyses
All statistical analyses were performed using JMP 8.0 statistical software (SAS
Institute Inc. 2010). Where appropriate, data were checked for normality (Shapiro-
Wilk’s test) and homoscedasticity (Cochran’s test) prior to statistical analysis. A
linear regression was used to examine the effect of initial BM on growth. An ANOVA
was used to examine the effect of density on growth with replicate (replicate
enclosure) and clutch as factors, and initial BM as a covariate. Significant effects were
investigated by Tukey’s pair-wise comparisons. A repeated measures ANOVA was
used to examine the effect of density on the mean number of agonistic interactions in
a night, and mean number of interactions per animal in a night, with replicate and the
number of nights as factors. A repeated measures ANOVA with replicate and number
of nights as factors was also used to examine the effect of density on the duration of
an agonistic interaction, and on the mean number of movements per hour and per
animal per hour. A Pearsons’ chi square test was used to compare the intensity of
agonistic interactions. A significance level of P < 0.05 was used for all statistical
tests. All means are reported ± one standard error (SE) with sample sizes (N).
Results
1. Habitat use
Hatchling C. porosus had a similar pattern of habitat use regardless of density and
276
used the basking cages rarely (Fig. 1). The majority of the time (44.0-56.9%)
hatchlings were concealed under the hide-boards which covered equal parts of both
land and water, and this was highest during the day (10:00-15:00 h; Fig. 1). As
density increased, the percentage of animals under the hide-board decreased slightly
(Fig. 1). Hatchlings spent more time on land (25.8-31.9%) than they did in water
(15.2-26.7%), except for those at a density of 20.0/m2 in which it was similar (Fig. 1).
The use of land and water was highest between dusk and dawn (16:00-09:00 h), with
few animals venturing out from underneath the hide-board during the day. Hatchlings
rarely used the outdoor cages (0-1.3%), but lay at the entrance (0.9-2.2%) between
dusk and dawn (16:00-09:00 h). However, the percentage of crocodiles that utilised
the cages or lay at the entrance was slightly higher at 13.3/m2 and 20.0/m
2 compared
with those at 3.3/m2 and 6.7/m
2 (Fig. 1).
277
Figure 1. Percentage of the time hatchling C. porosus in each density utilised each of
the five habitat types as a function of time of day (dawn: 06:00-09:00 h; day: 10:00-
15:00 h; dusk: 16:00-20:00 h; night: 21:00-05:00 h) as determined by locations of
hatchling C. porosus each 10 minutes. For each density only one replicate group was
observed for a 24 h period.
2. Growth
Initial BM had a significant effect on growth (linear regression: R2
=0.27; F=47.26;
P<0.05; N=129), which decreased with increasing BM, and this pattern was consistent
across all but the lowest density (Fig. 2).
278
Figure 2. The effect of density (3.3, 6.7, 13.3, 20.0/m2) and initial BM on growth in
BM (g) after 21 days.
Most hatchling C. porosus either lost weight (N=63; 49%) or put on little weight
(<5g; N=40; 31%) after 21 days (Fig. 2). Density had a significant effect on growth
(F2,4=19.55; P<0.05), which was highest among hatchlings at a density of 6.7/m2, and
lowest at a density of 20/m2 (Table 3).
279
Table 3. Mean growth in BM (±SE) of hatchling C. porosus according to density (3.3,
6.7, 13.3, 20.0/m2) after 21 days. Levels are based on the results of pair wise
comparisons: those with the same letter are not significantly different.
Density (per m2) N Mean SD Range Levels
3.3 10 1.34±2.22 7.02 -5.6-14.7 A
6.7 20 6.12±1.24 5.56 -2.2-17.8 A
13.3 39 2.60±0.86 5.37 -7.2-16.5 A
20 60 -2.33±0.63 4.87 -12.2-11.8 B
3. Agonistic interactions
Frequency
The overall mean number of agonistic interactions in a night increased significantly as
density increased (F2,4=22.37, P<0.05; Fig. 3a), while the mean number of
interactions per animal in a night decreased significantly with increasing density
(F2,4=183.23, P<0.05; Fig. 3). At the lowest density, the frequency of agonistic
interactions per night was lowest, while the frequency per animal in a night was
highest. The frequency in a night and per animal in a night was similar at densities of
13.3 and 20.0/m2.
280
Figure 3. Mean (±SE) number of agonistic interactions per animal in a night for
hatchling C. porosus raised under the same conditions at different densities with two
replicates for each density.
Intensity
The intensity of agonistic interactions decreased significantly as density increased
(X2=87.56, df=6, P<0.05), with fewer medium and high level interactions among
hatchlings at 13.3/m2 and 20.0/m
2 (Fig. 4). In the majority of cases, these higher
intensity interactions involved and were instigated by the largest hatchlings in the
group.
281
Figure 4. Percentage of agonistic interactions at different intensities (low, medium,
high) between hatchling C. porosus raised under the same conditions at different
densities with two replicates for each density.
Duration
The duration of agonistic interactions also decreased significantly with increased
density (F2,4=46.95, P<0.05), with the duration of interactions at 13.3/m2 (mean:
16.86±0.70 s, range: 3-31) and 20/m2 (mean: 11.88±0.57 s, range: 3-30) significantly
shorter compared with those at 3.3/m2 (mean: 28.98±1.4 s, range: 10-55) and 6.7/m
2
(mean: 35.35±1.3s; range: 12-62).
4. Activity
The mean number of movements/h increased with density (F2,4 =37.50, P<0.05; Fig.
5a), as did the mean number of movements/h per animal (F2,4=12.36, P<0.05; Fig.
5b). Activity (mean movements) was similar between hatchlings at 3.3/m2
and 6.7/m2,
282
and between hatchlings at 13.3/m2 and 20.0/m
2.
Figure 5. Mean (±SE) movements per animal per hour for hatchling C. porosus
raised under the same conditions at different densities with two replicates for each
density.
Activity was highest among hatchlings across all densities at around dusk (16:00-
20:00 h) and dawn (06:00-09:00 h), coinciding with increased use of land and water.
Hatchlings at the two highest densities (13.3, 20.0/m2) were observed during the night
moving around the perimeter and appeared to be looking for a way out, often pushing
into the corners of the pen. This ‘escape/circling’ behaviour was rarely observed
among hatchlings at the lower densities (3.3, 6.7/m2).
Discussion
The results of this study suggest that density has a strong influence on growth,
agonistic behaviour and activity in hatchling C. porosus in a captive situation during
283
the first few weeks post-hatching. Although there was a strong effect of clutch on
initial size and growth of hatchling C. porosus, mean growth was highest at 6.7/m2
and was lower at the highest density (20.0/m2). Based on predictions of hatchling C.
porosus survivorship to 300 days of age from growth in BM (g) 24 days post-hatching
made by Brien et al. (2014), this would result in survival probabilities of 70% at
6.7/m2, 48% at 13.3/m
2, 45% at 20/m
2, and 40% at 3.3/m
2.
Higher densities are often associated with lower rates of growth in hatchling and
juvenile crocodilians raised in captivity, despite several studies reporting no
significant effect of density (Garnett and Murray 1976). For C. porosus, one study
reported higher growth rates after five weeks (post-hatch) at a density of 10/m2
compared with 20/m2 (Riese 1991), and another involving 8-10.5 month old hatchling
C. porosus reported lower growth rates among smaller animals as density increased
from 1/m2 to 10/m
2 (Mayer 1998). Studies involving juvenile (>5 months old)
American alligators (Alligator mississippiensis; Elsey et al. 1990) and Broad-snouted
caiman (Caiman latirostris; Poletta et al. 2008) also found lower rates of growth at
higher densities. However, while these lower rates of growth at high densities have
been attributed to higher levels of stress; it is unclear as to the social mechanisms
associated with this response in crocodilians.
The saltwater crocodile is considered the most aggressive species of crocodilian, with
a very low tolerance of conspecifics (Lang 1987; Brien et al. 2013b,c). Agonistic
behaviour starts as early as two days post-hatch, with the frequency of agonistic
interactions increasing and the development of a well-defined dominance hierarchy
284
within the first year of life (Brien et al. 2013a). In this study, the highest frequency of
agonistic interactions per individual occurred among hatchling C. porosus raised at
the lowest density (3.3/m2). In these smaller groups, one individual grew large and
dominated resources such as food and water, while the other four remained small.
These larger animals were the most dominant and were almost always involved in
agonistic interactions, which were often deliberate and of a medium to high intensity.
As density increased, the frequency of agonistic interactions (per individual) between
hatchling C. porosus decreased. Interactions were less focussed and intense (low
intensity) and were resolved more rapidly (shorter duration) as most individuals that
were nearby would react to the altercation by fleeing which caused the combatants to
stop. Unlike at the lowest density, dominant individuals were unable to target others
aggressively, as there appeared to be too many animals in close proximity for
sustained, intense encounters to occur. This suggests that for hatchling C. porosus at
very low densities, agonistic behaviour may be responsible for reduced growth in less
aggressive or subdominant individuals, while at higher densities, the effect of
agonistic behaviour appears to be less important.
Although the results were not significant, another study involving hatchling C.
porosus reported slightly lower growth rates among hatchlings raised at the lowest
(2.5/m2) and highest (10/m
2) densities (Garnett and Murray 1986), with the highest
growth at 5/m2, similar to this study. Lower rates of growth at both the highest and
lowest densities have also been reported in lobsters (Chittleborough 1975; Ryther et
al. 1988), poultry (Estevez et al. 1997; 2002; 2003), pigs (Andersen et al. 2004), trout
285
and Arctic charr (Alanara and Brannas 1996), and mice (Davis 1958). This pattern of
behaviour is similar to that described in the ‘tolerance hypothesis’ model proposed by
Estevez et al. 1997, in which lower levels of agonistic behaviour are predicted at
higher densities as individuals are unable to dominate others as they would in low
density situations.
Although the gregarious nature of crocodilians during the initial post-hatching stage
makes them good candidates for high density farming situations, there appears to be
important species-specific differences. For example, rates of growth and survival of A.
mississippiensis are much higher than for C. porosus, even when they are raised under
identical conditions (Joanen and McNease 1976; Webb et al. 1994), and this has been
attributed to the higher levels of aggression and lower tolerance of conspecifics in C.
porosus compared with A. mississippiensis (Lang 1987; Hutton and Webb 1992;
Brien et al. 2013c). Studies with lobsters under captive conditions have also found
lower rates of growth and survival in species that are highly aggressive and have a
low tolerance of conspecifics (James et al. 2001). This suggests that highly aggressive
and intolerant species may not be suited to captivity. In order to improve growth and
survival in these species, it may be necessary to provide a more complex raising
environment (eg. cover, barriers, escape routes) and ensure optimal stocking densities
are maintained and adjusted as individuals increase in size in order to mitigate
negative social interactions.
The level of activity among hatchling C. porosus (per individual) increased at the
higher densities (≥13.3/m2) while growth rates declined. This increased activity
286
coincided with the display of a circling or escape behaviour that was not observed at
the lower densities (≤6.67/m2). Individuals would move around the perimeter of the
enclosure, primarily at dusk and dawn. This circling behaviour is usually only
observed among hatchling C. porosus during the first few days after individuals have
been introduced into a new enclosure (MB personal observation), and is considered
exploratory or stress-related. However, hatchlings at the higher densities in this study
continued to display this behaviour after 18 days, suggesting a sustained level of
stress. The lower growth at higher densities may reflect the energetic consequences of
increased activity. While increased activity at higher densities has also been observed
in captive raised fish (Kristiansen et al. 2004), activity levels are often reduced in
chickens at higher densities or group sizes (Estevez et al. 1997) and this is due to a
barrier effect created by the animals themselves (Newberry and Hall 1990).
Higher than optimal densities can cause increased levels of plasma corticosterone,
increased incidence of disease, and lower levels of growth among juvenile
crocodilians raised in captivity (Elsey et al. 1990; Huchzermeyer 2003). However,
while agonistic behaviour has often been implicated, especially in C. porosus, the
results of this study suggest that hatchling C. porosus may respond to higher than
optimal densities by increasing the level of activity and demonstrating escape
behaviour. This may also be the case for other species such as A. mississippiensis that
exhibit increased corticosterone levels at higher densities which is not associated with
an increase in agonistic behaviour (Elsey et al. 1990). In rats, higher densities are also
associated with increased levels of activity and escape behaviour, which has been
linked to elevated corticosterone (indicating stress), organ pathology and
287
immunodepression (Hurst et al. 1999).
Garnett and Murray (1986) reported that densities for hatchling C. porosus should be
based on available land area only, as they observed that this is where hatchlings spend
the majority of the time. However, observations were only made during the day and
experimental enclosures did not contain any cover for animals to hide under, which
resulted in individuals piling on top of each other in the corners of the pen. This issue
of piling has been reported in other earlier studies involving hatchling crocodilians
(Webb et al. 1983; Webb et al. 1994; Huchzermeyer 2003), before the importance of
providing cover was recognised (Huchzermeyer 2003).
Hatchling C. porosus in this study spent the majority of the time during the day
inactive and under cover (hide board), or basking on land near cover. However,
activity levels increased between dusk and dawn and this coincided with increased use
of exposed water and land areas in which individuals engaged in other important
behaviours such as feeding and social interaction. Therefore, we argue that
considerations of density involving hatchling C. porous should incorporate land and
water areas.
In this experiment we did not separate density from group size, with the same
enclosure (size and shape) used to house different numbers of hatchling C. porosus.
However, group size and density are often adjusted simultaneously in studies of farm
animals (Estevez et al. 1997; Morisse and Maurice 1997; Nicol et al. 1999; Dumont
and Boissy 2000), including those undertaken with crocodilians (Garnett and Murray
288
1986; Elsey et al. 1990). Although studies should aim to examine either density or
group size in isolation, there are inherent difficulties associated with this (eg.
adjusting pen shape and size) which have only recently been fully appreciated
(Christman and Leone 2007; Estevez et al. 2007). Because growth rates of hatchling
C. porosus within the first 3-4 weeks post hatch are known to influence long term
patterns of growth and survival (Webb and Cooper Preston 1989; Brien et al. 2014),
these results also have important implications for management.
Despite a large number of confounding variables, it appears that the optimal density
for housing hatchling C. porosus during the initial post hatching stage is around 10-
15/m2 which is in agreement with the current Australian code of practice (COP 2009).
However, just as there appears to be a maximum optimal density at which to raise
hatchling C. porosus of this age, there also appears to be a minimum, or at least a
minimum group size. Based on the results of our study, we would argue that a group
size of less than 10 animals encourages higher levels of aggression and dominance
which results in highly variable rates of growth and lower survivorship.
Acknowledgements
We thank Wildlife Management International for the supply of animals, use of
facilities and logistical support. WMI funding through the Rural Industries Research
and Development Corporation is gratefully acknowledged. Funding for equipment
(cameras, digital video recorders) was provided through a Holsworth Wildlife
Research Endowment (ANZ Trustees Foundation), Northern Territory Research and
289
Innovation Board student grant, IUCN-SSC Crocodile Specialist Group Student
Research Assistance Scheme grant, and Charles Darwin University. Experimental
protocols were approved by the Charles Darwin University Animal Ethics Committee
(Animal ethics permit number A11003).
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Chapter 5.3. Factors affecting initial growth rates of captive
saltwater crocodiles (Crocodylus porosus) hatchlings in captivity:
food form and temperature cycle
Abstract
Growth trajectories of hatchling C. porosus established in the first few weeks of life
are key determinants of survival rates and thus of fitness. This study examines
whether this initial growth, at a constant temperature regime, is affected by food form
(minced red meat, long- and short-chopped red meat, and a variety of short copped
meat). It also tests within the same experimental enclosures whether the temperature
regime (constant: 32-34ºC, gradient: 28-34ºC, warm night: 32-34ºC, warm day: 32-
34ºC), when fed short-chopped red meat, significantly influences early growth.
Hatchling C. porosus were from several clutches (Feed: 3; Temperature: 5) and raised
(two replicates) in identical enclosures (1.5m2) in groups of 10 hatchlings (6.7
hatchlings/m2). Body mass (BM-g) was measured at introduction and after 21 days,
while behaviour (Food form: feeding; Temperature regime: habitat use) was observed
on days 18-20. Hatchling C. porosus fed a short chopped form of either red meat
(15.2±2.3 g) or a variety of meats (12.3±2.1 g) had higher growth in BM than those
fed the standard minced (8.4±2.4 g) form or long chopped form of red meat (3.5±1.9
g). Hatchlings appeared to be more efficient at consuming short chopped pieces of
meat than they were at consuming either mince, which they frequently lost in the
water, or long chopped pieces, which were dropped after some effort trying to
consume. Hatchlings provided with a temperature regime of constant warm
299
temperatures (constant: 6.4±2.0 g), a gradient of temperatures (gradient: 5.3±2.2 g), or
warmer night time temperatures (warm night: 7.8±2.2 g), had higher growth than
hatchlings provided with warm temperatures during the day only (warm day: -1.2±1.1
g). Hatchlings in the Warm day temperature treatment had access to temperatures
within the Tset (measured as the central 50% of Tbs voluntarily selected in a thermal
gradient) for only 16 hours of the day, compared with 24 hours a day for all other
treatments. The results of this study suggest that growth of hatchling C. porosus in
captivity can be improved by providing ‘bite’ sized pieces of meat instead of mince
and a thermal regime that enables 24 h access to temperatures within the Tset for this
species.
Introduction
Hatchling C. porosus in captivity are particularly sensitive to failure to thrive syndrome
(FTT) up until one year of age, which results in low rates of growth and survival
(Huchzermeyer 2003; Isberg et al. 2009; Brien et al. 2014). Mortality through FTT
during the first year of life is generally reported as 10-20% but can be as high as 50%
(Isberg et al. 2009). Despite a large number of unreported on-farm attention and trials,
in addition to formal research (eg. Garnett and Murray 1986; Riese 1991; Webb et al.
1992; Davis 2001; Mayer 1998; Isberg et al. 2009; Brien et al. 2012; 2013; 2014), the
cause of this syndrome remains largely unknown.
In captive environments, new born hatchling C. porosus are sensitive to the structural,
functional and management characteristics of their raising environment. There are
300
pronounced clutch effects in that sensitivity, which appear to be an interaction between
genetic predispositions and incubation history (Webb and Cooper-Preston 1989). The
success or otherwise of a raising strategy is largely reflected in the proportion of
hatchlings afflicted by FTT, which once started is difficult to reverse (Brien et al.
2014). This syndrome is apparent by the extent of individual growth in the first 24 days
post hatching, which is a good predictor of later growth and survival probabilities
(Brien et al. 2014).
In the wild, C. porosus live in communal groups (crèches) for at least the first two
months of life (Webb et al. 1991), and feed on a wide range of prey items, such as
crustaceans and arthropods, that are alive and moving (Taylor 1979; Webb et al.
1991). They crush, manipulate and swallow them whole, obtaining a reasonably large
amount of food for each unit of capture effort. The majority of feeding occurs around
the waters’ edge. In captivity, a number of studies have been dedicated to dietary
preference and feeding regimes of hatchling C. porosus (Garnett and Murray 1986;
Davis 2001). Hatchlings are typically fed a diet of red meat mince combined with
multivitamin and calcium supplements five to six days a week, in order to maximize
growth (Hutton and Webb 1992; Davis 2001).
The current temperature regime used for raising hatchling C. porosus on commercial
farms involves air and water temperatures being maintained at a constant 32-34ºC
(Webb and Manolis 1990; Mayer 1998). This was originally based on the American
alligator (Alligator mississippiensis) farm model and the optimal temperature used for
incubating C. porosus eggs (32ºC: Webb and Cooper-Preston 1989). However, the
301
merits of a constant thermal environment for hatchling C. porosus as used with A.
mississippiensis, relative to a cyclic or variable one, have not been examined and
remain unclear. It is important to note that the large majority of reptiles in captivity
are provided with some form of thermal gradient, and the importance of this variable
regime is widely recognised (Peaker 1969; Pough 1991).
In a recent study of hatchling C. porosus within a thermal gradient, preferred Tb’s
were not constant but cycled throughout the day (Brien et al. 2012). Warmer more
stable Tb’s were maintained during the day (11:00-17:00 h: 31.2ºC) when hatchlings
were less active and basking on land, with slightly cooler and more variable Tb’s
(18:00-10:00 h: 30.6ºC) during the night and early morning when hatchlings were
more active and in the water (Brien et al. 2012). While engaging in thermoregulatory
behaviour within a variable thermal regime may not be essential for maintaining
preferred temperatures per se in hatchling C. porosus, it could still play a role in
influencing rates of growth and survival.
Hatchling C. porosus that initiate feeding rapidly, and thus start to grow quickly, are the
least likely to suffer from FTT (Brien et al. 2014). So while the interactive causes of
FTT may still be unknown, manipulating food form or the temperature regime may be
ways of reducing this problem. The present study examines the effects of a) four
different thermal regimes (constant, gradient, diurnal heating, nocturnal heating) and b)
three different food forms (minced, short chop, long chop): on growth of new-born
hatchling C. porosus after 24 days, raised in otherwise identical enclosures, using the
same management and husbandry procedures and protocols.
302
Methods
Clutches, eggs and incubation
Eggs and hatchlings used in these experiments were provided by Wildlife
Management International (WMI; Darwin, Australia). Eggs came from both captive
(collected 1-2 days after laying) and wild nests (collected 1-25 days old after laying)
in the Northern Territory of Australia. Incubation was carried out (or completed)
artificially at constant 32ºC (±0.2ºC) and 98-100% humidity until hatching. Eighty
hatchling C. porosus from five clutches (4 wild; 1 captive bred) were used in the
thermal experiment, and a further eighty five from three clutches (1 wild; 2 captive
bred) were used in the feeding experiment. Clutches within each experiment hatched
within 1 day of each other (Thermal: 8-10th March 2012; Feeding: 19-21st March
2012), with those hatchlings that had deformities or obviously excessive yolk
excluded from experiments. Hatchling sex was not determined, but 32ºC is a male
producing temperature and the majority of eggs were incubated at this temperature
through the sensitive period for sex determination (Webb et al. 1987).
All hatchings were held in the incubator in crates for three days, which is thought to
assist the assimilation of residual yolk, before release into their raising enclosures on
day four. For each hatchling, a uniquely numbered metal webbing tag (Small animal
tag 1005-3, National Band and Tag Co.) was attached to the rear back right foot at the
time of hatching. Snout-vent length (SVL in mm to the anterior of the cloaca) and
303
body mass (BM in g) were also measured at four days of age when the animals were
introduced into the enclosures and again at 24 days of age. However, we used only
growth in BM as an index of performance, as previous studies involving hatchling C.
porosus have found this to be the most effective measure (Brien et al. 2014).
Experimental enclosures
Hatchlings in both experiments were raised in mixed clutch groups of 10-11
individuals under identical conditions from day four until day 24 post-hatching. The
enclosures were box shaped (170 x 100 x 50 cm high) and constructed of fibreglass
with a land area (70 x 100 cm) that gradually sloped down to a water area (100 x 100
cm; <8 cm deep). A ‘hide area’ (Riese 1991; Mayer 1998; Davis 2001) was provided
that was constructed of eight lengths (80 cm long) of 10 cm (diameter) PVC pipe
strapped together in the horizontal plane and mounted on legs (5 cm). Hides were
centrally positioned in the water (partly immersed) and overhung the land.
Feeding
In both experiments, feeding occurred at 16:00-17:00 h six days a week, with waste
removed the following morning (08:00-09:00 h) when the water was changed. In the
thermal experiment, all animals were fed chopped red meat supplemented with di-
calcium phosphate (4% by weight) and a multivitamin supplement (1%). In the
feeding experiment, two groups of approximately 10-11 hatchlings were used to test
each of the four feeding treatments:
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1. Standard mince: red meat (horse) minced through a 10 mm plate. This is the
standard diet currently provided to hatchling C. porosus in captivity (Mayer
1998; Davis 2001).
2. Short chop: red meat (horse) chopped in small pieces (8 long x 8 wide x 4 mm
thick). Prey items in the wild are captured whole and broken into pieces of
various sizes before consumption.
3. Long chop: red meat (horse) chopped in long pieces (35 long x 5 wide x 4 mm
thick). Prey items in the wild are captured whole and broken into pieces of
various sizes before consumption.
4. Variety short chop: a variety of red meat (horse), fish (white bait), prawns, pork,
and chicken meat chopped in small pieces (8 long x 8 wide x 4 mm thick).
Hatchling C. porosus in the wild consume a range of different prey types.
All four diets also contained di-calcium phosphate (4% by weight) and a multivitamin
supplement (1% by weight).
Temperature regime
In the feeding experiment, water temperature (Tw) was maintained at 31-32°C with
thermostatically controlled injection of warm water. Air temperature (Ta) varied on a
daily cycle from 26-35°C and there was a natural light cycle. In the thermal
experiment, Tw was maintained with two thermostatically controlled aquarium heaters
(200 W, Hydor Theo®
), while Ta was maintained with two thermostatically controlled
305
ceramic heaters (250 W, Oz Black URS®) positioned 40 cm above the land surface.
Temperature data-loggers (Thermocron iButtons®
) were used to measure hourly Tw,
and Ta at two sites, one at hatchling level (Ta(5)) 5 cm above the land surface, and the
other (Ta(20)) 20 cm above the land surface. In the thermal experiment, two groups of
approximately 10 hatchlings were used to test each of the four temperature treatments:
1. Constant Temperature: Tw and Ta heated constantly at 32-34ºC. This is the
standard thermal regime currently provided to hatchling C. porosus in
captivity (Mayer 1998; Davis 2001).
2. Warm Night: Tw and Ta heated during the night only (21:00-04:00 h: 7 hours
total) at 32-34ºC. While Ta increased with ambient conditions during the day,
Tw did not. This treatment provided heat at night, a time when hatchling C.
porosus are most active and use the water more frequently (Brien et al. 2012).
3. Warm Day: Tw and Ta heated during the day only (10:00-17:00 h: 7 hours
total) at 32-34ºC. This treatment provided heat during the day when hatchling
C. porosus spend the majority of time inactive under cover and prefer to
maintain a higher Tb (Brien et al. 2012).
4. Gradient: Tw not heated at all, and maintained at 28-30ºC. Ta heated constantly
at 32-34ºC. The treatment created a thermal gradient from the water (cool) to
the land (warm), providing a constant range of thermal options within the Tset.
Most reptiles housed in captivity are provided with a thermal gradient that
enables them to thermoregulate (Peaker 1969; Pough 1991).
In all four treatments, an attempt was made to maintain Ta and Tw close to the thermal
306
set point range (Tset) of Tb’s preferred by hatchling C. porosus: 29.4-32.6ºC (Brien et
al. 2012).
Behaviour
Wide angle infrared CCTV cameras (Signet, 92.6º) in each enclosure were used to
record general feeding and thermoregulatory behaviour on a digital video recorder
(Signet 4CH QV-8104). Observations were made over three days prior to recapturing of
animals at the end of the experimental period (18-20 days).
Statistical analyses
Statistical analyses were performed using JMP 8.0 statistical software (SAS Institute
Inc., 2010). Where appropriate, data were checked for normality (Shapiro-Wilk’s test)
and homoscedasticity (Cochran’s test) prior to statistical analysis. The relationship
between initial BM and Growth in BM was examined using regression analyses. An
ANOVA with pair-wise comparisons was used to examine the effect of feed treatment
(Minced, Short chop, Variety chop, Long chop) and temperature treatment (Constant,
Warm Day, Warm Night, Gradient) on growth in BM (grams), with initial BM,
replicate and clutch as factors. A significance level of P<0.05 was used for all statistical
tests.
307
Results
Feeding
The majority of feeding (70-90%) occurred during the first few hours after food was
placed in the pen (16:30-21:00 h), but a little occurred in the early morning (07:00-
08:00 h) just prior to cleaning. Most of the food (>90%) was consumed in water with
very little (<10%) consumed on land at or near where the food was provided. During
feeding the jaws were clapped together repeatedly, just under the waters’ surface,
combined with intermittent sideways shaking of the head. Both behaviours appeared to
be attempts at manoeuvring food to the back of the throat while lubricating it with
water. While swallowing, hatchlings would tilt their head up at a 45-90° angle to the
substrate.
Feeding effort, behaviour and consequences varied between treatments. In the
hatchlings fed mince, a significant amount of food was lost from the sides of the mouth
as they attempted to manoeuvre the food under the waters’ surface. Individuals fed long
chopped meat often dropped the meat, after a relatively long period (15-30 s)
attempting to manoeuvre and swallow it. After the meat was dropped, individuals rarely
attempted to recover the same piece. By way of contrast, the small chopped food
appeared easier to grasp, manoeuvre and swallow, and resulted in less waste. It was
noteworthy during cleaning that waste chopped pieces in the water (short or long
chopped) created less pollution than waste mince.
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Initial BM had a significant effect on growth (R2=0.17; F=16.48, P<0.05), which
increased with initial BM. Growth in BM differed significantly with treatment
(F2,4=5.29, P<0.05) and was highest in the short chop treatments (red meat and
variety) which achieved similar growth, and was lowest in the long chopped treatment
(Fig. 1).
Figure 1. Mean (±SE) growth in BM of hatchlings fed standard red meat in minced,
short chopped and long chopped forms, and a variety of meats in small chopped form
(two groups in each), over 21 days. Survivorship of hatchlings is based on growth in
BM predicted by Brien et al. 2014. Red lines represent the mean (central) and standard
error (top and bottom).
Animals which failed to put on BM during the trials were largely restricted to the long
chopped (43%) and minced (32%) treatments, whereas only one individual in the short
chopped treatments (red meat and variety) lost weight (Fig. 1). Based on the survival
309
probabilities predicted from growth after 24 days post-hatch for hatchling C. porosus in
captivity (Brien et al. 2013), the number of individuals expected to survive was highest
in the short chopped treatments (Short chopped: 87%; Variety short chopped: 81%),
and lowest in the Minced (59%) and Long chopped treatments (47.7%; Fig. 1).
Temperature regime
Although the prevailing temperatures were not controlled precisely due to warmer
ambient conditions during the day, the mean hourly Ta and Tw measured over 21 days
of the experiment confirmed the temperature treatments were different (Fig. 2).
Hatchlings within the Constant, Gradient, and Warm Night treatments had access to
temperatures (Ta and Tw) within the Tset for 24 hours, while those in the Warm Day
treatment only had access to temperatures (Ta and Tw) within the Tset for 16 hours.
Figure 2. The mean water temperature (Tw), air temperature at hatchling level 5cm
above land surface (Ta(5)), and air temperature 20cm above land surface Ta(20) in each
of the four different types of temperature regimes (Constant, Warm Night, Warm Day,
310
and Gradient) over 21 days.
Hatchling C. porosus in all treatments remained inactive and under the hide-board for
the majority of the day (08:00-18:00 h: 65-80%). Activity increased at dusk (17:00-
20:00 h) as hatchlings moved from under the hide-board into open areas of land and
water, and this coincided with feeding behaviour. Throughout the evening (20:00-
05:00 h) hatchlings were more commonly observed in open areas of land and water
than during the day, while there was another peak of activity at dawn (06:00-08:00 h)
which also coincided with feeding behaviour.
Habitat use by hatchlings was similar in the Constant and Gradient treatments
(Exposed on land: 35%; Exposed in water: 15%; Under hide: 50%), but differed
slightly in the Warm Night and Warm Day treatments (On land: 30%; In water: 25%;
Under hide: 45%) with hatchlings spending more time in the water at night, especially
in the Warm Night treatment (Fig. 3).
311
Figure 3. Percentage habitat use by hatchling C. porosus over a 24 h period raised
under the same conditions at different densities with two replicates for each density.
For all hatchlings, there was no significant relationship between initial BM and growth
in BM (R2=0.010; F=0.77, P=0.38). Growth in BM was significantly lower (F2,4=5.08,
P<0.05) in the Warm Day treatment (Fig. 4).
312
Figure 4. Mean growth in BM (±SE) of hatchlings raised with four different
temperature treatments: Constant, Warm Night, Gradient, and Warm Day (two groups
in each), over 21 days. Survivorship of hatchlings is based on growth in BM predicted
by Brien et al. 2013.
Based on the survival probabilities predicted from growth after 24 days post-hatch for
hatchling C. porosus in captivity (Brien et al. 2013), the number of individuals
expected to survive was highest in the Warm night (66.5%), Constant (61.5%), and
Gradient (56.5%) treatments, and was lowest in the Warm day treatment (23.5%; Fig.
4).
313
Discussion
Feeding
Hatchling C. porosus fed a short chopped form of either red meat or a variety of meats
had higher growth rates during the first three weeks post hatching than those fed the
standard minced or long chopped forms of red meat. Hatchlings appeared to be more
efficient at consuming short chopped pieces of meat than they were at consuming either
mince, which they frequently lost in the water, or long chopped pieces, which were
dropped after some effort trying to consume.
Hatchling C. porosus in the wild typically consume small prey which they break off
into pieces that they are better able to consume (Webb et al. 1991). Therefore,
providing small ‘bite’ sized pieces of meat to hatchling C. porosus may be more
suitable for maximising feeding effort and subsequent growth under captive conditions.
However, the optimal size of these pieces is still not clear.
Physical form of the food can have a significant effect on the growth of other animals,
such as chickens (Plavnik et al. 1997; Quentin et al. 2004; Zang et al. 2009) and pigs
(Bayley and Carlson 1970). In chickens, higher growth and efficiency of gain is
achieved with a pelleted form of food rather than a mash (Plavnik et al. 1997;
Wahlström et al. 1999; Preston et al. 2000; Quentin et al. 2004), and this has been
attributed to better nutrient availability (Wahlström et al. 1999; Kilburn and Edwards
2001) and an increase in daily nutrient intake (Hamilton and Proudfoot 1995).
314
In a recent study, growth of sub-adult C. porosus in captivity was improved when
individuals were fed minced chicken heads in a sausage form compared with whole
chicken heads (Webb et al. 2013), which was explained by the reduced metabolic
costs of digesting mince (Gienger et al. 2012). Although this result appears to be in
contrast with the findings of our study, lower growth of hatchlings fed mince was
attributed to the inability of individuals to consume mince efficiently. These results
highlight the importance of feed form for optimal growth in crocodilians, which is an
area that has received little attention.
Hatchling crocodilians have traditionally been fed a minced diet of fish, poultry, pig,
or red meat, based largely upon local availability and price (Hutton and Webb 1992;
Huchzermeyer 2003). While studies with hatchling C. porosus have found higher
rates of growth on a red meat diet (Hutton and Webb 1992; Davis 2001), there also
appears to be clutch specific dietary preferences, which suggests a mixture of different
protein sources may be important for growth (Manolis et al. 1990; Hutton and Webb
1992). There may also be individual differences in dietary preference as reported
found in snakes (Burghardt 1975). However, in this study there was no significant
difference between the red meat and mixed meat diets.
Temperature regime
The temperature regime to which new born hatchling crocodilians are exposed has
long been recognised as a fundamental or overriding variable in determining rates of
315
growth (Hutton and Webb 1992; Lang 1987). As a generalisation, hatchlings need to
attain preferred body temperatures (Tb=29-33ºC), while avoiding short-term exposure
to lethal high temperatures (>38ºC) and prolonged exposure to suboptimal low
temperatures (<27ºC) (Lang 1987; Brien et al. 2012). This can be achieved technically
by controlling water temperature (Tw) and air temperature (Ta) in various ways, with
or without radiant heat sources. However, differences in preferred Tb exist both within
and between species due to clutch, body size, and incubation conditions (Lang 1987;
Webb and Cooper-Preston 1989).
In this study, hatchling C. porosus provided with a thermal regime of constant warm
temperatures (Constant: 32-34ºC), a gradient of temperatures (Gradient: 28-34ºC), or
warmer night time temperatures (Warm Night), had higher growth than hatchlings
provided with warm temperatures during the day only (Warm Day). Hatchlings in the
Warm day temperature treatment had access to temperatures within the Tset for only 16
hours of the day, compared with 24 hours a day for all other treatments. Therefore, we
attribute lower growth in the Warm day treatment to reduced access to temperatures
within the Tset that may not have allowed individuals to maximise digestion and energy
absorption.
Environmental temperatures have an important influence on the physiology, growth and
survival of ectotherms, with most species operating efficiently within an optimal range
(Pelletier et al. 1995; Rhen and Lang 1999). Lower rates of growth and survival have
been reported in abalone (Britz et al. 1997), lobster (Lellis and Russell 1990), fish
(Meeuwig et al. 2004), lizard (Waldschmidt et al. 1986), and other crocodilians (Lang
316
1987; Pina and Larreira 2002) when held under captive conditions with limited or no
access to optimal temperatures (Panov and McQueen 1998; Rhen and Lang 1999).
However, even when optimal temperatures are provided, the nature of the thermal
regime can also have a strong influence on growth and survival (Peterson and
Robichaud 1989; Dong et al. 2006).
In this study, growth of hatchling C. porosus was lowest in the fluctuating regime
(Warm Day) that best replicated the diel cycle of preferred Tbs recorded for hatchling
C. porosus in a thermal gradient (Brien et al. 2012). As with other species of reptile
(Christian 1986), hatchling C. porosus prefer cooler Tbs at night. Therefore, this
fluctuating regime, which allowed ambient conditions to drop just below the Tset over
night (28ºC), was expected to achieve similar, if not improved rates of growth in this
study. However, unlike in the wild where the availability of food is limited (Webb et al.
1991), hatchling C. porosus in captivity are provided with food every day which may
necessitate higher Tbs throughout a 24h period for digestion.
A thermal regime fluctuating or alternating on a diel cycle has been found to improve
growth and survival relative to constant temperatures in species of shrimp (Miao and
Tu 1996), sea star (Sanford 2002), and fish (Sierra et al. 1999). However, other
studies with crayfish (Thorp and Wineriter 1981), fish (Lyytikainen and Jobling
1999), and crocodiles (Kanui et al. 1991) have found no difference between a constant
and fluctuating temperature regime. While the underlying mechanism for these
different responses is unknown, it is likely related to the specific ecology of a species
and the nature of food conversion and energy allocation (Brett 1971; Diana 1984;
317
Dong et al. 2006).
Management implications
Growth and survival of ectotherms in captivity is strongly influenced by the feeding
and thermal regime provided. The results of this study suggest that growth, and thus
survival, of hatchling C. porosus in captivity can be improved by providing ‘bite’
sized pieces of meat instead of mince and a thermal regime that enables 24h access to
temperatures within the Tset for this species. However, further research is required to
establish the optimal size of the food and nature of the thermal regime.
Acknowledgements
We thank Wildlife Management International for the supply of animals, use of
facilities and logistical support. WMI funding through the Rural Industries Research
and Development Corporation is gratefully acknowledged. Funding for equipment
(cameras, digital video recorders) was provided through a Holsworth Wildlife
Research Endowment (ANZ Trustees Foundation), Northern Territory Research and
Innovation Board student grant, IUCN-SSC Crocodile Specialist Group Student
Research Assistance Scheme grant, and Charles Darwin University. Experimental
protocols were approved by the Charles Darwin University Animal Ethics Committee
(Animal ethics permit number A11003).
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porosus). In S.C. Manolis and C. Stevenson (Eds.). Crocodiles, Status Survey and
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Webb, G.J.W., Manolis, S.C., Otley, B. and Heyward, A. 1992. Crocodile
management and research in the Northern Territory: 1990-1992. In: Proceedings of
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Webb, G.J.W., Reynolds, S., Brien, M.L., Manolis, S.C., Brien, J.J., and Christian, K.
2012. Improving Australia’s crocodile industry. Nutritional requirements, feed
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327
Chapter 5.4. Use of diazepam and tryptophan to reduce stress and
increase growth and survival of hatchling saltwater crocodiles
(Crocodylus porosus) in captivity
Abstract
In this study, 120 hatchling saltwater crocodiles (C. porosus) from four separate
clutches were divided randomly into 12 sibling only groups (N=10), with four groups
fed chopped red meat (RM), four fed chopped red meat with Valium® (VRM: 0.2-
0.8mg/kg body mass), and four fed chopped red meat with L-Tryptophan (TRM: 2%
wet weight of food). All hatchlings were raised in the same enclosures under semi-
controlled conditions for 21 days, with daily estimates of food eaten recorded and the
increase in individual body mass (g) used as an index of growth. Behaviour was
described and quantified (infrared CCTV cameras) in the evenings (17:00-08:00h) for
five consecutive nights (days 15-19). In clutch 1, hatchlings in the VRM treatment
(0.8mg/kg; -1.18±1.39 g) had significantly lower growth in BM (g) after 22 days than
those from either the TRM (2% wet weight; 13.05±4.82 g) or RM (25.29±3.8 g)
groups and this was reflected in the amount of food eaten. The mean number of
agonistic interactions observed per night (days 15-19; 17:00-08:00h) was lowest in the
VRM group (1.0±0.32 per night) compared to the TRM group (10.2±1.32 per night;
P<0.05) and RM group (15.0±1.61 per night; P<0.05). Based on lower growth and
food consumption observed in the VRM group from clutch 1, it was decided to lower
the dosage of valium provided to the VRM groups in clutches 2-4 to 0.2mg/kg.
However, after 10 days, the trend in food consumption in the VRM groups (clutches
2-4) appeared similar to that observed in clutch 1 at the higher dosage (0.8mg/kg).
328
Due to welfare concerns, experimental treatments were discontinued at day 10, with
all hatchlings fed RM until 22 days post-hatching. Differences between treatments in
growth, food consumption after 21 days and the frequency of agonistic behaviour
(days 7-9) in clutches 2-4 followed a similar pattern to that observed in clutch 1. The
results of this study suggest that while the provision of Valium® in the food may
reduce the frequency of agonistic interactions among hatchling C. porosus it can also
lead to reduced growth at dosages between 0.2-0.8mg/kg body mass.
Introduction
Stress in animals can be caused by a wide range of stimuli and conditions, causing an
elevation in the glucocortiod hormone, corticosterone, which has important
behavioural and physiological implications for survival (Romero and Wikelski 2001;
Overli et al. 2002). Prolonged or chronic elevation in corticosterone due to stress can
result in decreased growth, lower activity, and a depressed immune system relative to
conspecifics (Overli et al. 1999; 2002). Animals in production situations are
particularly susceptible to high levels of stress through social aggression and the
nature of the captive-rearing environment itself (Boissy 1995; Andersen et al. 2000;
Forkman et al. 2007).
Lower rates of growth and survival correlated with high levels of corticosterone have
been reported in hatchling and juvenile crocodilians under farm conditions (Elsey et
al. 1990; Turton et al. 1997; Isberg et al. 2009). For hatchling C. porosus, this is
known as ‘failure to thrive syndrome (FTT)’ or ‘runtism’ (Mayer 1998; Isberg et al.
329
2009; Brien et al. 2014). For reasons that are not clear, 15-40% of C. porosus
hatchlings eat and grow little relative to others, including siblings, and become
vulnerable to mortality through reduced immunity to disease or voluntary starvation
or both (Onions 1987; Mayer 1998; Isberg et al. 2009). These individuals typically
have high levels of corticosterone and usually die between 70-200 days, or need to be
culled for both efficient production and welfare considerations (Turton et al. 1997;
Huchzermeyer 2003; Isberg et al. 2009).
The saltwater crocodile has long been regarded as a species least tolerant of
conspecifics (Lang 1987; Brien et al. 2013a). Studies of agonistic behaviour in
hatchlings have revealed that social aggression among C. porosus occurs immediately
after hatching and involves actual fighting (Brien et al. 2013a). Furthermore, the
amount of growth within the first few weeks post-hatching can determine future rates
of growth and survival (Brien et al. 2014). Therefore, it is possible that social
aggression among hatchling C. porosus may promote fast growth rates in dominant
animals, and be responsible for FTT in submissive individuals.
Diazepam (Valium®) is a powerful anxiolytic benzodiazepine which is used as a
muscle-relaxant, sedative, and anti-convulsant in humans and animals (Jarvik 1970;
Andersen et al. 2000, Plumb 2002), while tryptophan is an essential amino acid, found
in most protein-based foods that can increase production of the calming
neurotransmitter serotonin (5-HT) and nictotinic acid in the central nervous system
(Grimmett and Silence 2005).
330
Diazepam and tryptophan have both been used successfully to treat aggression, fear
and anxiety in a number of animal species (rats, horses, goats, fish, and chickens)
under production conditions (Wise and Dawson 1974; Brown et al. 1976; Anika 1985;
Wongwitdecha and Marsden 1996; Warner et al. 1998; DeNapoli et al. 2000; Janczak
et al. 2001; Winberg et al. 2001; Hoglund et al. 2005). Diazepam has also been found
to increase food consumption in rats (Wise and Dawson 1974), and pigs (Dantzer
1978), while tryptophan increased food consumption in chickens (Laycock and Ball
1990). Diazepam has been used extensively as a premedicant and mild sedative in
various species of animals, establishing the safety of this drug in a wide variety of
species and resulting in established dosage ranges for various reptile species,
including crocodilians (Lloyd 1999, Schumacher and Yelen 2006).
In this study we examined the effect of diazepam and tryptophan on hatchling C.
porosus under captive conditions in reducing aggression and ultimately improving
growth and survival in the early post-hatching period. It is anticipated that if these
treatments are efficacious at reducing stress and aggression in the first few weeks
post-hatching, the resultant improved learned adaptation and adjustment to the captive
environment while on the treatment will continue once the crocodiles are weaned off
of them.
Methods
Animals and housing
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In February and March of 2012, 120 captive-born hatchling saltwater crocodiles (C.
porosus) were obtained from Wildlife Management International (WMI; Darwin,
Australia). They originated from 4 clutches collected from the wild (10-20 days old)
that had been artificially incubated at 32ºC and 95-100% humidity. After hatching
(clutch 1: 1st February; clutches 2-4: 24th February 2012), individuals remained in the
incubator (32ºC) for 3 days, which allows early detection of compromised individuals
(none found here). After three days in the incubator, 30 hatchlings from each of the
four clutches (N = 120) were divided into twelve groups of 10, each group housed
separately and consisting of ten individuals from the same clutch. For each animal,
snout-vent length (SVL - mm), and body mass (BM - g) were measured and a
uniquely numbered metal tag (Small animal tag 1005-3, National Band and Tag Co.)
was attached between the webbing on the rear right foot prior to release into the
enclosures (clutch 1: 4th February; clutches 2-4: 27th
February).
Enclosures were box shaped (170x100x50cm high) and constructed of fiberglass with
a land area (70x100cm) that gradually sloped down to a water area (100x100cm;
<8cm deep). A ‘hide area’ (Riese 1991; Mayer 1998; Davis 2001) was provided that
was constructed of eight lengths (80cm long) of 10cm (diameter) PVC pipe strapped
together in the horizontal plane and mounted on legs (5cm). Hides were centrally
positioned in the water (partly immersed) and overhung the land. Water temperature
(Tw) was maintained at 31-32°C with thermostatically controlled injection of warm
water. Air temperature (Ta) averaged around 32-34°C but varied from 26-36°C at
different times of the day depending on ambient temperatures.
332
Treatment groups
All hatchling groups were fed chopped red meat supplemented with di-calcium
phosphate (4%) at 16:00-17:00 h each day ad libitum with waste removed the
following morning (08:00-09:00 h) when the water was changed. However, of the
twelve groups, four were fed just chopped red meat (RM), four were fed chopped red
meat with Diazepam (Valium®: oral form) mixed through (VRM), and four were fed
chopped red meat with tryptophan (L-Tryptophan reagent grade: Sigma-Aldrich,
USA) mixed through (TRM). Food was placed on the land and the amount left over
the next day was weighed and recorded for each group as a crude estimate of feeding
rate. Uneaten food in the water was not accounted for.
In the VRM treatment, 0.8mg/kg body mass (clutch 1) of valium was mixed in the
food. The treatment of the early clutch (clutch 1) with 0.8mg/kg of valium was
undertaken as a trial to enable improvement and refinement for the following clutches
(2-4). These dosages of diazepam are remarkably consistent among animals of various
taxa and of a wide range in body sizes, from small mammals to birds and large adult
crocodilians (Plumb 2002, Lloyd 1999). The selected range for this study was based
on a range of 0.5-2.0 mg/kg body mass used for mild sedation/calming pre-
anaesthesia in a wide variety of reptiles, including snakes and lizards, which are of a
similar body size to hatchling crocodiles (and thus likely similar in terms of metabolic
scaling of drug dosages) (Schumacher and Yelen 2006).
Diazepam has low toxicity and a relative lack of side-effects (Baldwin et al. 1990,
333
Plumb 2002), and is currently approved for use with Crocodylus porosus as a sedative
according to the ‘Code of Practice on the Humane Treatment of Wild and Farmed
Australian Crocodiles 2009’ (pp. 11. section 60, 71). However, dosage rates used
were lower than what is required for sedation. The half-life for diazepam in small
animals ranges from a few to several hours, therefore if mild sedation occurs, the
effect should wear in less than a day (Plumb 2002). The reversal agent (Flumazenil -
Anexate) was on hand to be administered in case severe sedation or any other adverse
signs occur (eg. muscle fasciculations, excitement).
In the TRM treatment, tryptophan was mixed in with the standard diet at 2% of wet
mass, in accordance with previous studies (Laycock and Ball 1990; Winberg et al.
2001; Hoglund et al. 2005). Tryptophan is readily available for use by humans and
animals. No adverse side effects have been substantiated in humans or animals from
long-term use and sudden withdrawal of relatively high tryptophan from the feed has
not been noted as having adverse consequences (Leathwood 1987; Laycock and Ball
1990; Bellisle et al. 1998).
Hatchlings remained in these treatment groups for 21 days, before recapture and
measurement on day 22 (clutch 1: 26th
February 2012; clutches 2-4: 20th
March 2012),
with increase in body mass (g) for each individual used as an index of growth. Food
was withheld for 24 h prior to the second BM measurements. This time period was
selected because absolute growth of C. porosus after 24 days post-hatching in
captivity is crucial in determining future rates of growth and survival (Hutton and
Webb 1992; Brien et al. 2014). Following the experiment, all animals were returned
334
to regular raising facilities where both their behavior and food consumption was
monitored for the next two weeks to ensure no ill effect of the treatments. At the
conclusion of the experiment, in order to minimize any potential withdrawal
symptoms from abrupt cessation of the diazepam, the oral treatment was administered
at one-half the dosage for a week, then at one-half the dosage on every other day for a
week prior to cessation.
Behavior
Wide angle infrared CCTV cameras (Signet, 92.6º) in each enclosure were used to
record the total number of agonistic interactions on a digital video recorder (Signet
4CH QV-8104) over a five day period (days 15-19) between the hours of 17:00-
08:00h. This time period is when the majority of agonistic interactions among
hatchling C. porosus occur under captive conditions (Brien et al. 2012; 2013a). An
agonistic interaction was defined as any interaction between individuals in which
intolerance was signaled by postures or actions by one or both individuals (Brien et al.
2013a).
Statistical analyses
All statistical analyses were performed using JMP 8.0 statistical software (SAS
Institute Inc. 2010). Where appropriate, data were checked for normality (Shapiro-
Wilk’s test) and homoscedasticity (Cochran’s test) prior to statistical analysis. To
examine differences in growth in BM (g) between treatment groups, a t-test was used
335
or a Welch’s t-test when variances were unequal. To examine differences in the
frequency of agonistic interactions between treatment groups, a Kruskal Wallis test
with Wilcoxon pair wise comparisons was used to account for small sample sizes. A
significance level of P<0.05 was used for all statistical tests. All means are reported ±
one standard error (SE).
Results
In clutch 1, hatchlings in the VRM treatment (-1.18±1.39 g) had significantly lower
growth in BM (g) after 22 days than those from either the TRM (13.05±4.82 g;
Welch’s t-test: t=2.84, df=18, P<0.05) or RM (25.29±3.8 g; Welch’s t-test: t=42.35,
df=18, P=0.0001) groups (Fig. 1), which did not differ significantly from each other
(t-test: t=-1.99, df=19, P=0.06).
Figure 1. Hatchling growth in BM (grams) after 22 days for hatchling C. porosus
from clutch 1 fed chopped red meat (RM), chopped red meat with tryptophan (TRM)
336
and chopped red meat with valium (VRM). Red lines indicate the mean (central) and
the standard error (top and bottom).
Differences in BM growth (grams) between each group were reflected in crude
estimates of food consumption, which was much lower in the VRM group (total
eaten: 255 g) compared with those from the TRM (total eaten: 700 g) and RM (total
eaten: 830 g) groups (Fig. 2).
Figure 2. Crude estimate of food eaten (grams) per treatment group over 22 days for
hatchling C. porosus fed chopped red meat (RM), chopped red meat with tryptophan
(TRM) and chopped red meat with valium (VRM).
Based on lower growth and food consumption observed in the VRM group from
clutch 1, it was decided to lower the dosage of valium provided to the VRM groups in
clutches 2-4 to 0.2mg/kg. However, after 10 days, the trend in food consumption in
the VRM groups (clutches 2-4) appeared similar to that observed in clutch 1 at the
337
higher dosage (0.8mg/kg). Due to welfare concerns, experimental treatments were
discontinued at day 10, with all hatchlings fed RM until 22 days post-hatching (Fig.
3).
Figure 3. Crude estimate of food eaten (grams) per treatment group for a) clutch 2; b)
clutch 3; c) clutch 4, over 22 days for hatchling C. porosus fed chopped red meat (RM
- blue), chopped red meat with tryptophan (TRM - black) and chopped red meat with
valium (VRM - grey).
Growth in BM was still measured after 22 days for hatchlings in clutches 2, 3, and 4.
In all instances, growth in BM followed a similar pattern to what was observed in
clutch 1, with highest growth among those in the RM treatment, followed by TRM
338
and VRM (Fig. 4). However, these differences were not significant in the majority of
cases (Table 1).
Figure 4. Hatchling growth in BM (grams) after 22 days for hatchling C. porosus
from a) clutch 2, b) clutch 3, and c) clutch 4, fed chopped red meat (RM), chopped red
meat with tryptophan (TRM) and chopped red meat with valium (VRM). Red lines
indicate the mean (central) and the standard error (top and bottom).
339
Table 1. Growth in BM (grams) differences between treatment groups for clutches 2, 3, and 4. *indicates statistical difference.
Clutch 2 Clutch 3 Clutch 4
Treatment
groups Test Result (df=18) Test Result (df=18) Test Result (df=18)
RM and TRM Welch’s t-test t=2.74, P=0.02* t-test t=-0.47, P=0.65 t-test t =-0.85, P=0.41
RM and VRM Welch’s t-test t=2.14, P=0.06 t-test t =-0.58, P=0.57 t-test t =-2.53, P=0.02*
TRM and VRM t-test t=1.47, P=0.16 t-test t = -0.12, P=0.91 t-test t =-0.66, P=0.52
340
Agonistic behavior
The mean number of agonistic interactions observed per night (days 15-19; 17:00-
08:00h) differed significantly between treatment groups from clutch 1 (X2= 11.11,
df=2, P<0.05) with fewer observed in the VRM group (1.0±0.32 per night) compared
to the TRM group (10.2±1.32 per night; P<0.05) and RM group (15.0±1.61 per night;
P<0.05) which were similar (P=0.07; Fig 5).
Figure 5. Mean number of agonistic interactions observed between hatchlings from
clutch 1 in each treatment group (RM: red meat, TRM: tryptophan and red meat,
VRM: valium and red meat) over a three night period (15-19 days) between 17:00-
08:00h. Red lines indicate the mean (central) and the standard error (top and bottom).
For hatchlings in clutches 2-4, behavioral observations were undertaken over three
nights (7-9 days post hatching; 17:00-08:00 h) prior to termination of experimental
341
treatments (VRM and TRM) on day 10. While the sample sizes were too small for
accurate statistical analyses, the mean number of agonistic interactions observed per
night followed a similar pattern to those in clutch 1, with a lower number of agonistic
interactions observed among the VRM groups (Fig. 6).
Figure 6. Mean number of agonistic interactions observed between hatchlings from a)
clutch 2 b) clutch 3, and c) clutch 4 in each treatment group (RM, TRM, VRM) over a
three night period (7-9 days) between 17:00-08:00h. Red lines indicate the mean
(central) and the standard error (top and bottom).
Discussion
While the provision of valium in the food generally appeared to reduce the frequency
342
of agonistic interactions among hatchling C. porosus, it did not coincide with an
increase in growth. Based on the survival probabilities predicted from growth of
hatchling C. porosus in captivity after 24 days post-hatch (Brien et al. 2014), in the
first clutch, only 25% of animals in the valium group would be expected to survive to
200 days compared with 70% in the tryptophan group and 99% in the red meat group.
While estimates of daily and overall food consumption in this study were considered
crude, they did appear to provide a general index of growth performance. Based on
these estimates, it appeared that all hatchling groups initiated feeding regardless of
treatment, and that consumption was similar across treatments for the first four days.
This suggests that hatchlings were not initially deterred by the presence of tryptophan
(powder – no smell) or valium (liquid – sweet smell) in the food. However, after 4-5
days, food consumption by hatchlings in the valium treatment groups declined, while
the other groups continued to feed.
The benefit of oral administration in the food is that it is more practical to administer
in a production system and is less stressful on hatchlings since handling is not
required. However, a significant disadvantage of the oral form is that the actual
dosage taken in by the hatchling depends on whether, and how much, the hatchling
eats. Therefore, it is possible that the more dominant individuals within the valium
groups ate more than the intended amount and were subsequently sedated. As the
frequency of agonistic interactions between hatchling C. porosus can be used as an
index of overall activity (Brien et al. 2012), the lower frequency of agonistic
interactions among hatchlings in the valium groups would support this idea.
343
Food supplemented with tryptophan has been found to reduce aggression and size
heterogeneity and improve growth in pigs, poultry and fish (Grimmett and Silence
2005). While there was a general trend for groups of hatchling C. porosus fed
tryptophan in this study to engage in slightly fewer agonistic interactions than groups
fed just red meat, growth was also slightly lower.
As one of the most aggressive species of crocodilian, social aggression is considered
one of the primary causes of FTT in hatchling C. porosus raised in captivity (Isberg et
al. 2009; Brien et al. 2013a, b). However, a recent study that examined the effect of
barriers and water levels on agonistic behaviour and growth in groups (N=10) of
hatchling C. porosus found that, while the frequency and intensity of agonistic
interactions could be reduced substantially by the provision of complex visual barriers
or deeper water, it did not coincide with improved growth (Brien et al. 2014).
Fear and anxiety in animals can be caused by situations that are unpredictable,
unfamiliar, or sudden, in which individuals feel threatened, such as a predatory attack
(Boissy 1995; Andersen et al. 2000; Forkman et al. 2007). The majority of farming
practices involve handling, size-sorting, cleaning, maintenance, and culling, which
can all induce fear and anxiety (Boissy 1995; Andersen et al. 2000; Forkman et al.
2007). As a result, fear and anxiety is common for a number of species in production
situations and is associated with elevated levels of corticosterone (Boissy 1995;
Forkman et al. 2007).
344
As a small ‘prey’ species that groups together, occupies sheltered habitat, and that
spends most of the time avoiding predators, hatchling C. porosus may be susceptible
to high levels of fear and anxiety in production situations (Lang 1987; Webb and
Manolis 1989). Hatchling C. porosus on farms will rapidly and consistently flee for
cover (eg. water, hide) in response to any form of disturbance (pers. obs). When
raised without any form of cover, hatchling C. porosus will pile together in the corner,
which is interpreted as a stress response, and will invariably grow poorly (Riese 1991;
Mayer 1998; Davis 2001). Therefore, FTT in hatchling C. porosus may be caused by
high levels of fear and anxiety induced by the raising environment itself, rather than
as a product of agonistic behaviour.
Acknowledgements
I would like to thank Wildlife Management International for the supply of animals,
use of facilities and logistical support. Thank you to my supervisors, Keith Christian,
Grahame Webb, Keith McGuinness, Jeff Lang, and Cathy Shilton from Berrimah
Veterinary laboratories in Darwin for their help with experimental design and edits.
WMI funding through the Rural Industries Research and Development Corporation is
gratefully acknowledged. Funding for equipment (cameras, digital video recorders)
was provided through a Holsworth Wildlife Research Endowment (ANZ Trustees
Foundation), a Northern Territory Research and Innovation Board student grant,
IUCN Crocodile Specialist Group student grant, and Charles Darwin University.
Experimental protocols were approved by the Charles Darwin University Animal
Ethics Committee (Animal ethics permit number A11042).
345
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Chapter 6. Improving growth and survival in hatchling C. porosus:
summary, outdoor enclosures, and conclusions
The central focus of this thesis was to examine two poorly understood aspects of
hatchling behaviour in saltwater crocodiles (Crocodylus porosus), agonistic and
thermoregulatory behaviour, and to gain insights through experimentation into the
roles they may play in various factors influencing hatchling growth and survival rates
in captive raising facilities. The majority of studies relied on the use of infrared CCTV
cameras positioned within experimental enclosures to observe behavioural
interactions, and temperature data-loggers were used to monitor body temperatures in
relation to the environment.
Agonistic behaviour
After reviewing the first video recordings, it was clear that C. porosus are born with
the repertoire of agonistic behaviours. Sixteen distinctive behaviours were described
which are similar to those observed in adults. The majority of agonistic interactions
were observed between two individuals in the morning (06:00–08:00 h) and evening
(17:00–20:00 h) in open areas of shallow water. There were clutch specific
differences in the frequency of agonistic interactions. However, ontogenetic changes
occurred, with a smaller subset of behaviours based on dominance status displayed by
13 and 40 weeks.
It was concluded that agonistic behaviour is important in establishing and maintaining
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dominance hierarchies in C. porosus, characterised by aggression–submission
interactions. This type of interaction appears typical for C. porosus both in the wild
and in captivity, and may be important in preventing serious injury in a species
equipped with formidable armoury. Dispersal by hatchling C. porosus at around 13
weeks of age appears to be driven by a growing intolerance of conspecifics, while
territoriality is apparent at an early age.
To test whether the repertoire of behaviours described in hatchling C. porosus was
ubiquitous across all crocodilians, agonistic behaviour was also examined in seven
other species of crocodilian with an initial comparison made with C. johnstoni. In
contrast with C. porosus of a similar age, agonistic interactions between C. johnstoni
were conducted with relatively low intensity, showed limited ontogenetic change, and
there was no evidence of a dominance hierarchy among hatchlings by 50 weeks of
age, when the frequency of agonistic interactions was lowest. The head was also
rarely targeted in contact movements with C. johnstoni because they exhibit a unique
‘head raised high’ posture, and engage in ‘push downs’. Agonistic interactions
between C. johnstoni and C. porosus at 40–50 weeks of age were mostly low level,
with no real exclusion or dominance observed. The nature of agonistic interactions
between the two species suggests that dominance may be governed more strongly by
size rather than species-specific aggressiveness.
Comparisons of agonistic behaviour between the seven other species of crocodilian
(Australian freshwater crocodiles (Crocodylus johnstoni), American alligators
(Alligator mississippiensis), New Guinea freshwater crocodiles (Crocodylus
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novaeguineae), Gharials (Gavialis gangeticus), Siamese crocodiles (Crocodylus
siamensis), dwarf caimans (Paleosuchus palpebrosus) and Morelet’s crocodiles
(Crocodylus moreletti), and C. porosus revealed that the nature and extent of agonistic
interactions, the behaviours displayed (3 species-specific), and the level of conspecific
tolerance varied among species. The saltwater crocodile was considered the most
aggressive species, followed by C. novaeguineae, both of which appeared to form
dominance hierarchies, whereas the less aggressive species did not. It was concluded
that interspecific differences in agonistic behaviour may reflect evolutionary
divergence associated with morphology, ecology, general life history and responses to
interspecific conflict in areas where multiple species have co-existed.
Thermal behaviour
To examine thermoregulation we force-fed hatchling C. porosus (400 mm TL and 250
g BM) small temperature data loggers (Thermocron iButtons®). Data loggers were
recovered at the end of the experiments and the temperature data collected and
analysed. As very little information existed on thermoregulation in hatchling C.
porosus, the temperature range at which they chose to operate when given the
complete range of thermal options was determined. This was undertaken in a thermal
gradient where environmental temperatures were thermostatically controlled and
maintained.
It was found that hatchling C. porosus preferred temperatures between 29.4ºC and
32.6ºC (50% of Tbs (Tset), with a mean Tb of 30.9±2.3ºC SD which was not influenced
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by social situation (isolated, group) or whether individuals had been fed or not.
However, there was a strong daily cycle in temperature selection and activity, with
hatchlings maintaining higher Tbs during the day (11:00-17:00 h: 31.9±2.09ºC) and
moving little, compared to the evening when activity was higher and Tbs were lower
(18:00-10:00 h: 30.6±2.31ºC).
Based on the results of these earlier experiments, and previous studies involving C.
porosus, it was considered that agonistic and thermal behaviour may play a major role
in the observed differences in growth rates and survival in captivity, and as a
consequence, the high incidence of FTT in captivity. Therefore, ways of minimising
or reducing the level of agonistic behaviour and its effect on growth and survival was
investigated. The optimal thermal regime for growth and survival was also examined.
Growth and survival
Individual hatchlings have growth trajectories in body weight over time that ideally
follow a positive exponential curve, as more and more body mass accumulates per
unit length. Variation in these trajectories results in some individuals being longer and
heavier than others after the same time post-hatching time interval. It also results in
some individuals failing to thrive (FTT), losing weight, and eventually dying. A
central question addressed in this study was the degree to which individual growth, in
raising conditions considered ‘standard’ for hatchling C. porosus in the Australian
Code of Practice, could be used as indicators of later performance, and particularly of
the probability of succumbing to FTT. It was found that growth in the first 24 days
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post-hatching was a highly significant predictor of growth to 90 days and the
incidence of FTT. Hence a series of trials were undertaken testing the effects of a
range of variables considered potentially important (independent variables) in
predicting growth to 24 days of age (dependent variable).
The effect of food form (minced red meat, long- and short-chopped red meat, and a
variety of short copped meat) on initial growth at a constant temperature regime was
examined. The results determined that hatchling C. porosus fed a short chopped form
of either red meat or a variety of meats had higher growth in BM than those fed the
standard minced form or long chopped form of red meat. Hatchlings appeared to be
more efficient at consuming short chopped or ‘bite-sized’ pieces of meat than they
were at consuming either mince, which they frequently lost in the water, or long
chopped pieces, which were dropped after some effort trying to consume.
Understanding agonistic behaviour
Because agonistic interactions occurred between hatchlings in areas of shallow, open
water shortly after hatching, the effect of visual barriers and deeper water on the level
and nature of agonistic behaviour and growth was examined. However, while visual
barriers almost eliminated agonistic behaviour and deeper water reduced the duration,
intensity and outcome of interactions, it did not result in improved rates of growth.
The effect of density (3.3/m2, 6.7/m
2, 13.3 m
2, 20.0/m
2) on agonistic behaviour and
growth rates was investigated. It was found that as density increased above 6.7/m2,
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growth in hatchling C. porosus began to decline as activity increased. Hatchlings at
these higher densities were more often in contact with others and were more active,
especially at night when they were observed circling the perimeter and appeared to be
searching for a way out. The frequency of agonistic interactions (mean per animal per
night) was highest at the lower densities (3.3/m2;6.7/m
2) and decreased with increased
density (13.3/m2; 20.0/m
2). At the lowest density (and group size: 5), one or two
individuals became dominant and grew large at the expense of the remaining
hatchlings.
In another attempt to reduce the level of agonistic behaviour and possibly increase
growth in hatchling C. porosus, the effect of supplementing food with Valium® (0.2-
0.8mg/kg) or L-Tryptophan (2% wet weight) was examined. While hatchlings in the
initial group fed Valium (0.8mg/kg) had a far lower frequency of agonistic
interactions compared with the control and L-Tryptophan groups, they also had the
lowest overall rate of growth. While the experiment was replicated again (4 more
groups) at a lower dosage of Valium® (0.2mg/kg), the trend in food consumption
suggested lower growth would again occur in the Valium® groups and so the decision
was made to discontinue the experiment after 10 days. The results of this study
suggest that while the provision of Valium® in the food may reduce the frequency of
agonistic interactions among hatchling C. porosus it can also lead to reduced growth
at dosages between 0.2-0.8mg/kg.
These studies were focussed on visual displays of agonistic behaviour, and there is no
doubt that this species is capable of communicating through vocal or chemical means.
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Hatchlings were detected vocalising (ripples made in water as gular pouch fluttered)
on different occasions, which often elicited a response from one if not more
individuals in the enclosure. While this has been reported previously (Britton 2001;
Verne et al. 2012), chemical communication has received very little if any attention in
crocodilians let alone C. porosus. The presence of semio-chemical glands in the
cloaca and in the gular pouch of C. porosus, suggests that chemical communication
may play an important role and is an area of study that deserves further attention. In
any instance, it is likely that C. porosus communicate and interact through a
combination of visual, vocal, and chemical means, and that understanding this
relationship may hold the key to identifying and managing the primary causes of FTT.
Optimal thermal regime
Given the clear diurnal pattern of thermoregulation among hatchling C. porosus, the
effect of adjusting the thermal regime on initial rates of growth and survival was
examined. We created four thermal regimes within enclosures (constant: 32-34ºC,
gradient: 28-34ºC, warm night: 32-34ºC, warm day: 32-34ºC) using the results of the
earlier thermal regime study (Tb, Tset) as a guide. Hatchlings under constant warm
temperatures, a gradient of temperatures, or warmer night time temperatures, had
higher growth than hatchlings provided with warm temperatures during the day only.
This result was unexpected, given that the warm day treatment best replicated the
diurnal pattern observed in earlier studies. However, when examined in the context of
the Tset, hatchlings in the warm day temperature treatment had access to temperatures
within the Tset for only 16 h of the day, compared with 24 h a day for all other
359
treatments. Therefore, constant access to temperatures within the Tset appears to be
important for optimal growth and survival of hatchling C. porosus under captive
conditions.
It is clear that hatchling C. porosus have a range of temperatures at which they prefer
to function, and that they have a diurnal pattern of activity and thermoregulatory
behaviour. The results of our studies suggest that hatchlings under captive conditions
require constant access to this preferred range of temperatures within their
environment. However, it does not seem necessary to maintain constant air and water
temperatures, as long as a section of the environment is maintained within this range.
The raising environment: a case study
While the results of these studies have shed some light on previously unknown
aspects of thermal and agonistic behaviour in hatchling C. porosus and the influence
on growth and survival, the question of what causes FTT and how it can be reversed
or prevented remains unknown. By the end of these experiments, it was decided that
perhaps the actual raising environment itself may be contributing to the high levels of
stress experienced by hatchlings leading to FTT. Therefore, it was decided to examine
how hatchlings afflicted by FTT to varying degrees, and likely to deteriorate much
further unless provided with special care, may respond when placed into a semi-
natural enclosure as opposed to remaining in standard raising pens. Standard pens are
those described in the density experiment: comprising land and water areas, constant
warm temperatures (32ºC: air, water), hide-boards, and low densities (<15 crocodiles
360
per m2).
Methods
A total of 505 hatchling C. porosus (24-57 days old) of a similar size (332.9±0.61 mm
TL range 300-374 mm; 69.7±0.43 g BM range 47-89 g) and considered to be afflicted
by FTT were obtained from Wildlife Management International (WMI), Darwin
(Australia). Hatchling C. porosus originated from clutches of eggs collected from the
wild (2-30 days old when collected) and from captive bred stock that had been
artificially incubated at 32ºC and 95-100% humidity. All had been raised in the same
standard raising pens, with constant water temperature (32-34ºC), and air temperature
fluctuating a few degrees higher during the day (34-38ºC) than at night (17-22ºC).
On 13 April 2012, 405 hatchlings were captured and redistributed back into the
standard raising pens in three groups of 5 (2m2), 10 (4m
2), 20 (6m
2), 40 (12m
2), 60
(18m2) at a density of 2.5-3.3 crocodiles per m
2. The other 100 hatchlings were
released into a semi-natural enclosure (202m2; 0.5 crocodiles per m
2; Fig. 1) that was
designed to replicate conditions in the wild. The enclosure was largely earthen and
specifically designed to replicate conditions experienced by hatchling C. porosus in
the wild in the Northern Territory.
The enclosure was rectangular (36m long x 10m wide) and enclosed by a 1-1.5m high
wire mesh fence with bird netting over the top to prevent access by predators. It had a
centrally located channel of water (36m long x 5.6m wide x 1.3m deep) with land on
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each side. The land on one side (36m x 3.2m) sloped down on a 40º angle (approx.),
and the other bank was flat (36m x 1.3m). Land was densely covered with grass and
small bushes, except for a section of black high density polyurethane plastic (10m x
1.3m) designed to replicate mud banks commonly found in the wild and used by
crocodiles for basking.
Figure 1. Semi-natural enclosure replicating conditions naturally occurring in the
wild.
A single uniquely numbered metal webbing tag (Small animal tag 1005-3, National
Band and Tag Co.) was attached to the rear back right foot at the time of release into
the enclosures. Body mass (BM in g) was measured when the animals were
introduced into the initial enclosures, and again after 27 days (10th
May 2012). All
hatchlings were fasted the day prior to measurements being taken. All animals were
fed chopped or minced red meat supplemented with di-calcium phosphate (4%) and a
multivitamin and mineral supplement (1%). Feeding occurred at 16:00-17:00 h each
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day throughout the study, with food placed on the edge of the bank near the water and
the waste removed the following morning (08:00-09:00 h).
Statistical Analyses
Statistical analyses were performed using JMP 8.0 statistical software (SAS Institute
Inc., 2010). Regression analyses were used to examine the relationship between initial
BM and final BM and Growth in BM. An ANOVA with Tukeys pairwise
comparisons was used to examine initial BM between groups. An ANOVA with
replicate and clutch as factors, and initial BM as a covariate was used to examine
differences between groups in final BM and growth in BM. Tukeys pairwise
comparisons were used to examine differences between individual groups.
Results
While environmental temperatures within the semi-natural enclosure fluctuated during
the day, temperatures within the standard raising pen were thermostatically controlled
and maintained at a more or less constant temperature (Fig. 2).
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Figure 2. Environmental temperatures in the a) semi-natural enclosure: air
temperature at 1.5m, water temperature 5cm below the surface, soil surface in the
shade, soil surface in the sun; and within the b) standard raising pen: air temperature
measured at 1.5m above the ground and just above the ground at crocodile height, and
water temperature.
There was a stronger positive linear relationship between initial BM and final BM
among hatchlings in the standard raising pens (R2=0.47, F=352.14, P<0.05) compared
with those in the semi-natural enclosure (R2=0.14, F=15.49, P<0.05; Fig. 3a). While
there was also a strong linear relationship between initial BM and growth in BM in
the standard pens (R2=0.16, F=74.69, P<0.05), there was no such relationship among
hatchlings in the semi-natural enclosure (R2=0.03, F=2.65, P=0.11; Fig. 3b).
364
Figure 3. Relationship between initial BM and a) final BM and b) growth in BM of
hatchling C. porosus suspected of suffering from FTT within standard raising pens
(grey: 5, 10, 20, 40, 60), and within a semi-natural enclosure (blue: 100).
Initial BM differed significantly between groups (F3,6 = 8.75, P<0.05) and was lowest
among groups of 5, 60, and also 100: which was the semi-natural enclosure (Fig. 4a).
Final BM (F2,13 = 7.50, P<0.05) and growth in BM (F2,13 = 7.45, P<0.05) also differed
significantly between enclosure types and was highest in the group of 100 hatchlings
in the semi-natural enclosure (Fig. 4b,c).
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Figure 4. Mean size and growth in BM (grams; ±SD and SE) of hatchling C. porosus
suspected of suffering from FTT after 27 days within standard raising pens (5, 10, 20,
40, 60), and within a semi-natural enclosure (N=100).
The number and percentage of hathlings that lost weight during the study period was
lowest in the semi-natural enclosure (100: 4%) and highest among those in the
standard raising enclosures (5: 80.0±11.6%; 10: 30.0±5.8%; 20: 51.7±11.7%; 40:
50.8±14.3%; 60: 61.1±12.3%).
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Discussion
In this study, mean growth in BM (grams) of hatchlings in the semi-natural enclosure
was more than double that of hatchlings in the standard raising pens after 27 days.
This suggests that captive raised hatchling C. porosus suffering from FTT may benefit
from being moved into a more natural enclosure. While it is not exactly clear why this
may be the case, there are a broad range of interrelated factors that could potentially
explain this result. For instance, there was an abundance of live prey (eg. tadpoles,
fish, insects) in the semi-natural enclosure, which hatchling crocodilians are known to
instinctively chase and consume, even those afflicted by FTT (Webb et al. 1991;
Hutton and Webb 1992). It has also previously been reported that the provision of live
food to hatchling C. porosus afflicted by FTT can improve growth and survival under
captive conditions (Garnett 1986; Mayer 1998).
There was a strong positive relationship between initial BM and growth BM among
hatchlings within the standard pens. However, there was no such relationship among
hatchlings in the semi-natural enclosure. As the most aggressive and intolerant species
of crocodilian (Lang 1987), in which agonistic behaviour begins shortly after hatching
(Brien et al. 2013), hatchling C. porosus may require more space per individual and a
more complex environment to mitigate against negative social interactions. The
ability of hatchlings to avoid or escape negative social interactions would have been
far greater within the semi-natural enclosure and may have resulted in the higher
growth rates regardless of initial size.
367
The level of disturbance experienced by hatchling C. porosus was considerably lower
in the semi-natural enclosure. As part of the cleaning regime in the standard pens each
morning, all the water was drained, hide-boards were lifted, and the leftover food
hosed out. This process involved two people getting within 1m of the hatchlings, and
took up to an hour before the water was then refilled at a cooler temperature. In
comparison, the leftover food in the semi-natural enclosure was removed each
morning by one person, which took less than 10 minutes and did not require draining
of the water. During this time, hatchlings remained hidden in the dense vegetation on
the opposite bank, which was a distance of more than 5m.
As a small ‘prey’ species that groups together, occupies sheltered habitat, and that
spends most of the time avoiding predators, hatchling C. porosus may be susceptible
to high levels of fear and anxiety in production situations (Lang 1987; Webb and
Manolis 1989). Hatchling C. porosus on farms will rapidly and consistently flee for
cover (e.g. water, hide) in response to any form of disturbance (pers. obs). When
raised without any form of cover, hatchling C. porosus will pile together in the corner,
which is interpreted as a stress response, and will invariably grow poorly (Riese 1991;
Mayer 1998; Davis 2001). Hatchling C. porosus in the semi-natural enclosure were
rarely sighted and likely experienced lower levels of stress than hatchlings in the
standard pens.
Environmental temperatures in the semi-natural enclosure were high enough
throughout most of the day to enable hatchling C. porosus to maintain Tb’s within the
preferred range (Tset). Hatchling C. porosus were originally raised on commercial
368
farms in outdoor earthen enclosures (Hutton and Webb 1992). However, in many
cases, while rates of growth and survival were reportedly high during the summer,
they were comparatively very low during the winter and this was attributed to
temperatures below optimal for the species (Riese 1991; Isberg et al. 2009). This
resulted in a shift to indoor enclosures where environmental temperatures were
constant and warm (30-33ºC), which resulted in improved rates of growth and
survival (Webb and Manolis 1990; Hutton and Webb 1992). However, rates of FTT
affliction remained high.
Conclusions and Recommendations
The possibility that the current ‘indoor’ raising paradigm for hatchling C. porosus,
instigated some 30 years ago based on the alligator model (Hutton and Webb 1992), is
fundamentally compromised cannot be rejected. While it was initially considered that
‘outdoor’ enclosures would provide a more natural and suitable raising environment
(Hutton and Webb 1992), it seems that the inability to efficiently overcome lower
winter temperatures may have led to the abandonment of outdoor enclosures
altogether. However, in doing so the ‘baby may have been thrown out with the bath
water’.
Based on these results, it could be argued that raising hatchling C. porosus in outdoor
enclosures may lead to improved rates of growth and survival as long as
environmental temperatures can be maintained within the Tset throughout the year.
This could be achieved by covering sections of the enclosure which may provide
369
hatchlings with a range of thermal options within the Tset. This has been achieved with
juvenile Nile crocodiles (Huchzermeyer 2003) and may enable higher rates of growth
and survival throughout the year. In any case, future studies involving C. porosus may
benefit from experimentation in outdoor enclosures.
Acknowledgements
I thank Jemeema Brien and Charlie Manolis for their help in different phases of the
project. We would also like to thank Wildlife Management International for the
supply of animals, use of facilities, logistical support and major funding for this
project. WMI funding through the Rural Industries Research and Development
Corporation is gratefully acknowledged. Funding was provided through a Holsworth
Wildlife Research Endowment (ANZ Trustees Foundation), Northern Territory
Research and Innovation Board student grant, and Charles Darwin University.
Experimental protocols were approved by the Charles Darwin University Animal
Ethics Committee (Animal ethics permit number A11003).
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I have learned that the line between success and failure is often very thin and comes
down, not so much to skill or intelligence, but to what extent you are willing to stick it
out even when things get tough.