The Environment InstituteWhere ideas grow
Assoc. Prof. Bronwyn Gillanders
Giant Australian cuttlefish: a globally unique species under threat?
Bronwyn Gillanders
Population structure Melita de Vries
Steve Donnellan
Mike Gardner
PhD/Hons students Jackie Dupavillon
Nick Payne
Leanne Trott
Giant Australian cuttlefish & the issues
Population structure
Potential impacts of desalination brine
Photo: Kaufmann Productions
Weighs up to 13 kgGrows up to 1 mLives 1-2 years
Ningaloo ReefMoreton Bay
Adelaide
8 km of coastlineWinter – May to August
8 km of coastlineWinter – May to August
Habitat map: SA DEH
Rocky reef
Males larger than females
High male:female sex ratio
Males ‘battle’ for females
Females may or may not mate with a male
Small males have other strategies (e.g. sneakers)
Shear numbers impressive
Photos: Fred Bavendam
Skewed towards males (4:1) based on counts of each sex
Assumes individuals on breeding aggregation similar amounts of time
Population sex ratio may be 1:1 with sexes spending different amounts of time on the breeding aggregation
Predict males spend more time than females
Males n = 13Females n = 6
Payne, PhD project
Male:Female = 3.7 : 1
Residence time
Male:Female = 4.6 : 1
Residence period
0
10
20
30
40
50
60
Males FemalesM
ean
Res
iden
ce P
erio
d (
da
ys ±SE
)
*
0
5
10
15
20
25
30
35
Males Females
Mea
n R
esid
ence
Tim
e (d
ay
s ±
SE
)
*
Payne, PhD project
Population composed of equal numbers of males & females
0
30
60
90
120
150
180
210
240
270
300Ca
tch (to
nnes
)
1984
1985
1986
1987
1988
1993
1989
1990
1991
1992
1994
1995
1999
1998
1997
1996
2000
2001
2002
2003
2004
2005
2006
2007
Renewable moratorium on fishing introduced in 1998
Now permanently closed to taking of cuttlefish
Need to establish long-term scientific based management plan
From: SARDI Catch Data
BHP Olympic Dam expansion Preferred option: coastal desalination plant in USG
Point Lowly preferred location (18 ha site)
Bulk commodities export facility Feasibility study by Spencer Gulf Port Link Consortium
(SGPLC), led by Flinders Ports
7-13 million tonnes of ore could be exported through new facility
Need to understand population structure for appropriate spatial management
Demographic processes & population dynamics may vary
From: Keough & Swearer (2007)
Strongest inferences use a suite of techniques
Genetic & phenotypic approaches
Might not necessarily expect concordance among approaches
Evolutionary history vs. environmental variation
Spatial resolution varies by technique
Genetic approaches may be more conservative
Marine populations
Genetic homogeneity over large distances
High dispersal life history characteristics
Squid
High levels of gene flow among populations
Cuttlefish
Sepia officinalis – extensive population structuring
Determine population structure of giant Australian cuttlefish using a multidisciplinary approach Molecular (microsatellite DNA markers)
Morphometrics
Statolith chemistry
Investigate spatial & temporal variation in population structure
Microsatellite genotyping
12 microsatellite loci screened per individual Kassahn et al. (2006) Marine Biology
Wheaton et al. (2007) Molecular Ecology Notes
Temporal variation South Australia
Five yrs between 1998 & 2006
Spatial variation 18 sites across Australia
18
WA
SA
QLD
NSW
VIC23
4 56
Whyalla
13 14
151617
Breeding aggregation
Spencer
GulfGSV
Ningaloo
Bass Strait
Moreton
Bay
Wallaroo
Glenelg
Aldinga
Cape
Jervis
Edithburg
19982000200420052006
20042005
19982005
20052006
1998
2005
1
Bayesian clustering approach
Triplicate runs for 1 (panmixia) to 6 populations
Used admixture model
Assumed correlated alleles across populations
Examined each of K populations further to detect sub-population structure
STRUCTURE
1 2 3 4 5 6K, number of populations
-24500
-23500
-22500
-21500
-20500
Ln P
r(X |
K)
Shows overall population structure & individual assignmentLength of each line proportional to estimated membership in each group
1.00
0.80
0.60
0.40
0.20
0.00
Why
alla
199
8
Why
alla
200
0
Why
alla
200
4
Why
alla
200
5
Why
alla
200
6
Wal
laro
o 19
98
Wal
laro
o 20
05
Edith
burg
200
5
Cap
e Je
rvis
200
5
Cap
e Je
rvis
200
6
Ald
inga
/Myp
onga
19
98
Ald
inga
/Myp
onga
20
05
Gle
nelg
199
8
wes
tern
AU
S 19
98-2
006
VIC
200
2
NSW
20
02/2
003
Q
Breeding aggregationWhyalla
NSWWallarooSpencer Gulf
Gulf St Vincent WA
Vic
Est
imat
ed m
emb
ersh
ip c
oef
fici
ents
1.00
0.80
0.60
0.40
0.20
0.00
Q
Wol
long
ong
Jerv
is B
ay
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Cof
fs H
arbo
ur
Jerv
is B
ay
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
Wol
long
ong
New
cast
le
New
cast
le
New
cast
le
New
cast
le
JervisBay
Wollongong Newcastle Coffs Harbour
Northern NSWCentral & Southern NSW
Est
imat
ed m
emb
ersh
ip c
oef
fici
ents
Spatial information – sampling location 1 to 10 populations (n=5 replicate runs)
Fixed K at modal value to estimate assignment of individuals to populations (n=10)
Continued hierarchical analyses to detect subpopulation structure
GENELAND
Population 2Population 1 Population 4
Population 3
Population 5
Population 4
Population 5
Contact zone
Breeding aggregation
100 km
South Australia
28 measurements per individual
Removed allometric effects of body size
Sexually dimorphic sexes analysed separately (n= 173 females & 342 males)
No difference in size among years pooled years
-5 -3 -1 1 3 55
3
1
1
3
5 Breeding aggregationGSV & Southern SGWestern SA
Discriminant function 1
Dis
crim
inan
t fu
nct
ion
2
90% correctly classified
3 variables used for classification
3 variables important: cuttlebone width & 2 beak parameters
LRL UHL
-5.0 -2.8 -0.6 1.6 3.8 6.0-5
-1
3
7 Breeding aggregationGSV & Southern SGWestern SA
Discriminant function 1
Dis
crim
inan
t fu
nct
ion
2
90% correctly classified
8 variables used for classification
3 beak parameters contribute to differences
Dissolved traceelements
Uptake bycephalopod
Statolithincorporation
Sr:Ca prehatchling seawater (mmol mol-1
)
0 5 10 15 20 25 30 35
Sr:
Ca
pre
hat
chli
ng s
tato
lith
(m
mol
mol-1
)
0
5
10
15
20
25
30
35
Sr:Ca hatchling seawater (mmol mol-1
)
0 5 10 15 20 25 30 35
Sr:
Ca h
atc
hli
ng
sta
toli
th (
mm
ol
mo
l-1)
0
5
10
15
20
25
30
35
Sr:Ca seawater (mmol mol-1) Sr:Ca seawater (mmol mol-1)
Sr:C
ast
atol
ith(m
mol
mol
-1)
Sr:C
ast
atol
ith(m
mol
mol
-1)Prehatchling Hatchling
Trott, Hons thesis
-7 -3 1 5-5
-3
-1
1
3
5
Discriminant function 1
Dis
crim
inan
t fu
nct
ion
2
Mg:Ca, Sr:Ca & Ba:Ca
Discriminant Function AnalysisAll years – 77% correctly classified2004 – 78% correct2005 – 79% correct2006 – 83% correct
Breeding aggregationGSV & Southern SGWestern SA
Not one panmictic population Evidence for 5 populations across species range Breeding aggregation differs from elsewhere
Evolutionary & ecological implications
Possibly incipient species
Adaptive divergence along an environmental
gradient
Recent & rapid differentiation
Ocean again at ~ 7KYA
From: Andrew Hugall
Mating behaviour differs Physiological tolerance & condition in relation to
temperature & salinity▪ Two populations may be prevented from significant overlap due to
differing tolerances
Are individuals from two populations able to mate, are eggs viable, are offspring fertile▪ Testing degree of reproductive isolation
Determine degree of genetic isolation – genome wide screening
Ecological implications of morphological differences
Breeding area
Intake pipe
Out take pipe320 ML SW/day
from USG;Salinity >40 ppt
200 ML SW/dayreturned in more
concentrated form;Salinity 78 ppt
120 ML FW/day via 320 km pipeline
From: Olympic Dam EIS website
Proposed locations
Discharge of large volumes of highly concentrated brine back to ocean
Elevated salt concentration & contaminants
Elevated temperature & turbidity levels
Decreased oxygen levels
Brine high specific density sinks to bottom
Could impact adult mating behaviours, & benthic life history stages
Salinity effects embryonic development Resources diffuse across membrane Solubility of gases (e.g. O2) decreased in
hyper-saline water Increased salinity causes a diffusion limitation
Control39ppt 40ppt 45ppt 50ppt
Brine55ppt
n =12
Dupavillon, Hons thesis
Treatment
Brine: Increased Sr, Ca, K & Mg
High Mg causes mortality and reduced mobility
High concentrations found in 45, 50 and 55‰.
Mean field concentration
Dupavillon & Gillanders (2009)Treatment - salinity
Increase 1‰ = ~7%
decrease in survival
Total mortality
Treatment - salinity
Dupavillon & Gillanders (2009)
Treatment - salinity
Smaller size at higher salinitySmaller individuals less well developed for feeding & swimming
Dupavillon & Gillanders (2009)
If brine disperses & background salinity levels reached close to discharge outfall May be little impact on eggs
But USG already hypersaline environment
Strong tidal currents, but are USG waters flushed & mixed with ocean waters given bathymetry?
Also, dodge tides
Potential for major impact on GAC
Mating behaviour highly visual Inbound migratory routes of cuttlefish
Will adults move up and over high salinity, benthic plumes?
Will adults migrate around benthic plume to reach breeding sites?
Only known breeding aggregation of cuttlefish in world!
Population at Point Lowly likely a different species
Little if any input from SSG population
Potential for brine to impact early life history stage
Unsure about impacts on adult behaviour & migration
Species can’t move elsewhere to lay eggs
Cephalopods short lived (1-2 years)
No storage effect in population
Need to be more cautious cf. managing finfish
Recent ABC Catalyst story:http://www.abc.net.au/catalyst/stories/2695601.htm
Photos: Fred Bavendam, Sean Connell, Jackie Dupavillon, Kaufman Productions, Nick Payne, Tim Rogers
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Assoc. Prof. Veronica Soebarto
Environmentally-sensitive design