ORIGINAL PAPER
Spawning, egg development and early ontogenesis in rock codPatagonotothen ramsayi (Regan, 1913) caught on the PatagonianShelf and maintained in captivity
Alexander Arkhipkin • Elena Jurgens •
Paul Nicholas Howes
Received: 7 March 2013 / Revised: 1 May 2013 / Accepted: 2 May 2013
� Springer-Verlag Berlin Heidelberg 2013
Abstract Rock cod Patagonotothen ramsayi (Regan,
1913) is one of the most abundant fish of the family Noto-
theniidae inhabiting the Patagonian Shelf and upper Slope in
the southwest Atlantic. Recently, P. ramsayi became an
important commercial species around the Falkland Islands
with annual catch of 60,000–75,000 t. The present study
aimed to reveal previously unknown aspects of reproductive
biology of P. ramsayi during the first successful maintenance
of adults for more than a year in an aquaculture facility with
running seawater. The fish spawned at the end of austral
winter. During spawning, males changed their coloration
dramatically, occupied artificial shelters on the bottom and
showed aggressive territorial behaviour. Egg masses were
light-yellow to light-orange irregular spongiform. They were
negatively buoyant, but located outside shelters and were
ignored by males. Egg diameters varied between 2.1 and
2.3 mm, and the number of eggs per egg mass ranged from
26,800 to 123,400. Embryogenesis lasted 28–32 days. Total
lengths of newly hatched larvae ranged from 6.2 to 6.7 mm.
The yolk sac feeding period lasted approximately 11 days,
during which the larvae showed negative phototaxis. One-
month-old larvae attained 8.8–9.0 mm in length. This study
confirms that P. ramsayi exhibit the reproductive strategy
typical for nototheniid species occupying low-latitude
peripheries of their distributional range, characterised by a
combination of r-features (small eggs and larvae, high
fecundity) and K-features (territorial behaviour and possible
nest guarding).
Keywords Patagonotothen ramsayi � Spawning �Egg mass � Embryogenesis � Southwest Atlantic
Introduction
Fish of the family Nototheniidae exhibit variations in
reproductive behaviour throughout Antarctica and the
Southern Ocean. Although they occupy a wide range of
ecospace from pelagic to intertidal rock pools (Eastman
2000), their reproductive strategies generally change with
latitude. At low latitudes, fish species are more fecund,
have relatively small eggs and small pelagic larvae and
spawn in winter, while at high latitudes, fish are less
fecund, have larger eggs and larvae and spawn in summer
(Kock and Kellermann 1991; Rae and Calvo 1995). Spe-
cies belonging to the latter group may also have nest
guarding behaviour protecting their egg masses until
hatching, especially in species that spawn relatively few
eggs (Kock and Kellermann 1991).
Patagonian rock cod, Patagonotothen ramsayi (Regan
1913), occur at the northern periphery of the nototheniid
distribution in the southwest Atlantic. This fish inhabits
mixed Subantarctic and temperate shelf waters of the Pat-
agonian Shelf at depths between 50 and 400 m, from
Burdwood Bank in the south to the shelf as far north as
36�S. P. ramsayi is a medium-sized fish attaining 46 cm
total length (TL). It is one of the most abundant species on
the outer Patagonian Shelf and preyed upon by a variety of
large nektonic fish (Arkhipkin et al. 2012). The abundance
of P. ramsayi has increased in recent years, and it is now an
important target in the commercial fishery, with catches
A. Arkhipkin (&) � E. Jurgens
Falkland Islands Government Fisheries Department,
P.O. Box 598, Stanley FIQQ 1ZZ, Falkland Islands
e-mail: [email protected]
P. N. Howes
Falklands Fish Farming Limited, The Chandlery, Airport Road,
Stanley FIQQ 1ZZ, Falkland Islands
123
Polar Biol
DOI 10.1007/s00300-013-1339-z
reaching *70,000 t per year only around the Falkland
Islands (Falkland Islands Government 2012).
The main aspects of P. ramsayi reproductive strategy
are similar to other low-latitude nototheniid fishes. This
species is a total spawner with potential fecundity ranging
between 24,300 and 76,700 small eggs. Observations of P.
ramsayi with mature gonads indicated that spawning
occurs on the shelf edge and upper continental slope
(250–400 m depths) during austral winter (Brickle et al.
2006b). Changes in length frequency and sex ratios
throughout the year showed a prevalence of mature females
during spawning season, which may indicate nesting and
nest guarding behaviour by males similar to congeneric
shallow water Patagonotothen tessellata from the Beagle
Channel (Rae and Calvo 1995).
Other aspects of the reproductive biology of P. ramsayi
remain unknown, probably because of its relatively deep-
water spawning. The shape, size and number of eggs in
their egg masses, existence of brooding behaviour,
embryogenesis and early larvae are not yet described. The
first successful live maintenance of P. ramsayi for more
than a year in an onshore aquaculture facility provided the
opportunity to address previously unknown aspects of
spawning and early development of this abundant and
commercially important fish.
Materials and methods
Fifty live, healthy-looking specimens of P. ramsayi
(22.1–37.4 cm TL) were collected from one commercial-
size trawl at 245 m depth, on the eastern Falkland Shelf
(51�450S, 57�250W), on 14 July 2011. Immediately after
hauling, the fish were transferred from the fish bin into
25-litre plastic tanks with running sea water. The vessel
returned to port within 5 h, and just before disembark,
thirty-eight fish with visually intact skin and fins were put
into large plastic bags containing 5–6 l of sea water and
brought ashore.
The fish were placed into the 7,216-litre circular tank
located in the Fisheries Aquaculture Facility in Port Stan-
ley. The tank has a bottom area of approximately 7.2 m2
and 1 m water depth. The bottom was kept bare of sand or
rocks for easy cleaning. Sea water was pumped in from
Stanley Harbour at a constant rate of 83 l/min and filtered.
Water turnover in the tank took approximately 87 min.
Temperature and salinity were measured daily using a
Valeport mini-CTD and kept similar to those in Stanley
Harbour. Additionally, oceanographic parameters were
recorded at 200 m depths near the bottom in presumed
spawning grounds of P. ramsayi to the east of Port Stanley.
Temperature and salinity data were acquired during
monthly oceanographic transects carried out onboard
Falkland Islands Patrol Vessel Protegat using a CTD
sealogger SBE-25 (Sea-Bird Electronics Inc., Bellevue,
USA). Temperature was measured directly, whereas
salinity was calculated using Seasoft v. 4.326 software
(Sea-Bird Electronics Inc.). All sensors of the CTD were
calibrated annually at Sea-Bird Electronics Inc. (Bellevue
USA).
The room with the fish tank was kept in ‘twilight’
conditions during daytime by covering the room window
with semi-transparent black plastic. Fluorescent lighting
was used only when feeding the fish and cleaning the tank.
During the course of the experiment, 10 terracotta plant
pots were cut in half longitudinally and placed on the
bottom to create shelters for the fish.
After 3 days of acclimatisation, the fish were placed in a
50-l tank and slightly anesthetised with AQUI-S water-
dispersible liquid anaesthetic and then measured for total
length (to the nearest mm) and weighed (to the nearest
1 g). Immediately after measurements, the fish were
returned to the tank and did not show any ‘post-traumatic’
disturbance. P. ramsayi were fed every second day with
small pieces of defrosted squid Doryteuthis gahi, juvenile
fish discards from commercial by-catch (mostly Patagonian
toothfish Dissostichus eleginoides and icefish Champso-
cephalus esox), and 13-mm ‘Skretting—select marine’
halibut pellets. Only two fishes died during the whole
experiment.
During July–August of 2011 and 2012 (spawning
months for P. ramsayi; Brickle et al. 2006b), fish behaviour
was observed through the water surface every second day
for about 20–30 min. Additionally, fish were photographed
by a diver within the tank using a Nikon D90 digital
camera with underwater housing and flash.
Several egg masses were found on the bottom of the
reservoir in August–September 2011 and 2012 (Table 1).
After several hours of observations of egg masses and fish
behaviour in the tank, egg masses were removed and
weighed. A subsample of 0.15–0.44 g was taken from
each egg mass. The number of eggs was counted in each
subsample to estimate average individual egg weight and
extrapolate the total number of eggs in each egg mass.
Each egg mass was placed in an individual 100-l incu-
bation tank supplied by a REDOX re-circulation system
with a separately pumped TMC System 5000 reservoir-
based filtration unit. Incubation tanks had two complete
water exchanges per hour during incubation, and the rate
was increased to 2.5 exchanges per hour during hatching
and larvae rearing. The water was aerated and chilled
using a Teco TR 60 chiller unit to maintain constant
temperatures close to what rock cod experience in their
natural environment (5–6 �C). The entire incubation sys-
tem was sheltered by a poly-tunnel with a reflective
cover.
Polar Biol
123
Samples of 10–15 eggs were taken daily from each egg
mass and examined under a zoom microscope Olympus
SZX12 to identify stages of embryonic development
according to Kimmel et al. (1995). Various stages were
measured and photographed using an Olympus DP70 dig-
ital camera attached to the zoom microscope.
After hatching, several P. ramsayi larvae were taken
from each tank for examination. Upon disappearance of the
yolk sac, the larvae were fed with Otohime B1 Diet larval
feeds (Japan), of 200–360 microns particle size. Unfortu-
nately, P. ramsayi rearing experiments in 2011 and 2012
were terminated by power cuts of the incubation system
that led to complete loss of all larvae.
Results
Environmental parameters
Temperature in the circular tank varied from 3 to 6.2 �C
(mean 4.3 �C between 22 August and 12 September and
5.1 �C until 24 October). One time the temperature reached
8 �C, but did not appear to affect the fish (Fig. 1a). Salinity
varied from 33.1 to 33.5 between 22 August and 12 Sep-
tember. Between 12 September and 30 October, salinity
varied stronger due to freshening of the surface water in
Stanley Harbour because of precipitation (Fig. 1b). In the
incubation tanks, temperature and salinity were near-con-
stant at 5 �C and 33.4 in August–September 2011 and
2012.
In presumed spawning grounds of P. ramsayi at 200 m
depths near the bottom to the east of Port Stanley, water
temperatures increased from 5 to 5.8 �C, salinity slightly
dropped from 34.07 to 33.63 between 14 August and 23
October 2011 (Fig. 1).
Fish behaviour in reservoir
During the first 2 weeks, the bottom of the reservoir was
kept bare, and the fish moved around slowly near-bottom,
preferring to swim against the current created by the flow
from the filter pipe. Initially, the food was offered every
day, but the fish did not take it actively. After a week, the
fish was fed every second day. During feeding, P. ramsayi
ascended to the surface and in several days got used to
taking the food. The pellets were consumed only when
being pre-soaked in water.
After 2 weeks, eight halves of terracotta pots were dis-
tributed evenly around the bottom of the tank. Almost
Table 1 Features of egg
masses in P. ramsayiNumber of
egg mass
Spawning
date
Egg mass
weight, g
Subsamples
weight, g
Egg
weight, g
Number of eggs
in each egg mass
Hatching
date
Year 2011
1 22/08 384.9 1.52 0.0031 123,404 19/09
2 31/08 204.8 0.16 0.0030 67,107 29/09
3 31/08 71.4 0.27 0.0027 26,812 29/09
4 5/09 154.4 0.43 0.0027 56,210 5/10
5 6/09 92.2 0.15 0.0026 35,323 7/10
6 7/09 142.8 0.16 0.0031 44,813 7/10
7 8/09 223.1 0.45 0.0032 70,117 9/10
Year 2012
1 9/09 176.5 2.15 78,982
2 10/09 324.5 0.73 111,896
3 10/09 135.6 0.86 69,894
4 10/09 71.5 0.44 28,744
Fig. 1 Temperature (a) and salinity (b) profiles in the maintenance
reservoir (line with rhombuses) and in situ (triangles) near-bottom at
200 m depth on the shelf east of Port Stanley (Falkland Islands)
Polar Biol
123
immediately, males started to react to these shelters, with
one fish occupying each shelter. Out of 16 males, eight
occupied shelters, while the rest were swimming with
females. All males changed their coloration dramatically
independent of whether they occupied the shelters or not
(Fig. 2a, b). The body became darker with the head, throat
and pelvic fins becoming almost black. The anal and dorsal
fins became dark brown with a white stripe along the edge.
Females kept their common coloration; however, white
edges on the dorsal, caudal and anal fins became more
distinct. Females developed distended abdomens possibly
showing egg maturation in their gonads (Fig. 2c).
Males that occupied the shelters showed aggressive
territorial behaviour, leaving the shelters only for a short
time and charging other males that tried to approach. All
males stopped feeding during this period, but females did
not. Our observations did not reveal any spawning and
courting behaviour between sexes.
Egg masses
Seven egg masses were found in the reservoir between 22
August and 8 September 2011 and four egg masses were
found between 9 and 10 September 2012 (Table 1). Egg
masses were negatively buoyant and laid on the bottom.
None of the egg masses was located inside or near shelters.
The fish ignored the egg masses completely, neither
guarding nor preying on them.
The egg masses appeared as irregularly shaped light-
yellow to light-orange sponges (Fig. 2d), of wet weight
ranging from 71.4 to 384.9 g (Table 1). Eggs in each mass
were clustered in a honeycomb pattern (Fig. 3) leaving
gaps to allow water circulation to the eggs inside.
Approximately 2–3 % of eggs were unfertilised and opa-
que milky in colour (Fig. 2d). Egg diameters varied
between 2.1 and 2.3 mm; the individual mean egg weight
was estimated to be 0.0029 g. Total numbers of eggs per
mass varied from 26,800 to 123,400 in 2011 and from
28,700 to 111,900 in 2012.
Fig. 2 P. ramsayi: male in breeding coloration occupying artificial shelter in the reservoir (a); male (left) and female (right) in their breeding
coloration near the bottom of the reservoir (b); female in breeding coloration (c) and egg mass located on the bottom (d)
Fig. 3 Honeycomb cluster of P. ramsayi eggs with gaps that allow
water circulation through the egg mass. Scale bar 1 mm
Polar Biol
123
Embryogenesis
Stages of the embryonic development are summarised in
Table 2. After fertilisation, the outer protective layers of
zygote formed the fertilisation membrane. The discoid
cleavage developed within 24 h and the embryo entered the
blastula period. The blastodisc grew in height and formed
the multicellular dome-shaped blastula by the second day
of post-fertilisation. At this stage, epiboly covers about
30 % of the egg from the animal pole. With the further
development of epiboly, the germ ring becomes visible on
the animal pole, indicating that the egg has entered the
gastrula period. Formation of the embryonic shield was
observed with approximately 50 % of epiboly. With
completion of epiboly, the embryo had brain and notochord
rudiments, as well as a prominent tail bud. Segmentation
period and formation of various organs and systems of the
embryo are presented in Table 2 and Figs. 4, 5, 6 and 7.
Early larval period
The larvae started to hatch in mass between 28 and 32 days
after fertilisation. Total length of newly hatched larvae
ranged from 6.2 to 6.7 mm, with the diameter of the yolk
sac attaining 1.2 mm. At this stage, the primordial larval
fin runs the length of the body from head to anus. The snout
is flat. Two rows of melanophores are present: one row
along the ventral part of the body from anus to tail and the
second row along the midline. Several melanophores are
scattered over the yolk sac. The head and snout are free of
pigmentation (Fig. 8a).
After hatching, larvae were distributed throughout the
whole water column. They were negatively phototactic
forming aggregations over the bottom of the incubation
tank when the fluorescent light was turned on.
The yolk sac feeding period lasted approximately
11 days. Then, different types of food were given. De-
capsulated eggs and newly hatched nauplii of Artemia
salina were too big for the early larvae, but they started to
consume pellet particles. The larvae were reared and fed
on pellet food until they were about 1 month old. At this
age, they had attained 8.8–9.0 mm TL. The general body
morphology did not change much compared to hatchlings
(Fig. 8b), but the snout had become more elongated and
the jaws more compressed dorso-laterally. Melanophores
in the ventral part of the body became more numerous
and less branched. Pectoral fins became larger and oval
shaped.
Table 2 Stages of embryonic development in P. ramsayi
Stage Days Description
Zygote period (Fig. 4a) 1 cell 1 (dpf)
Cleavage period (Fig. 4b–d) 2, 4 and 8
cells
Cleavage
2 distinct cells formed, 2 9 2 array, 2 9 4 array
Blastula period (Fig. 5) 2 (dpf)
Spherical ball (Fig. 5a,b) The blastodisc looks like a spherical ball
Dome shape (Fig. 5c) The cleaving cells begin to take a dome shape and the yolk cells grow
inwards
25 % of epiboly (Fig. 5d) The blastoderm growing around the yolk (epiboly) towards the vegetal pole
(25 % of epiboly)
Gastrula Period (Fig. 6) 4 (dpf) The blastoderm continues swelling around the yolk producing the primary
germ layers and the embryonic axis
50 %-epiboly (Fig. 6a) Germ ring visible and embryonic shield visible from animal pole
75 %-epiboly (Fig. 6b) Dorsal side is distinguishably thicker, accumulation of cells along the germ
ring
100 %-epiboly (Fig. 6c) Formation of the embryonic axis and primordia becoming apparent
Segmentation period (Fig. 7) 5 (dpf) First somites formed and optical vesicle becoming visible
10 (dpf) Two otoliths are formed in the auditory vesicles; first movement of the
embryo observed
15 (dpf) First heart beat noticed, eye pigmentation began
16 (dpf) Melanophores appeared on the yolk suck, pigmentation of the eyes continued
17 (dpf) Pelvic fins became visible
24 (dpf) Beginning of hatching
28 (dbf) Massive hatching
Polar Biol
123
Discussion
The results of the present study confirmed several previous
assumptions about the reproductive strategy of one of the
most abundant nototheniids of the Southern Ocean, P.
ramsayi (Brickle et al. 2006b). During the maintenance
experiment which lasted for 1.5 years, the fish spawned at
the end of each winter season (end of August—beginning
of September) in 2011 and 2012, corroborating seasonal
trends in gonado-somatic indices and proportions of mature
animals that have been observed in catches on the Pata-
gonian Shelf (Brickle et al. 2006b). Timing of spawning in
both years coincided with the minimum water temperatures
observed on the shelf at depths between 100 and 300 m
(Arkhipkin et al. 2004).
Patagonotothen ramsayi have relatively small eggs
(1.3–1.4 mm in diameter) that have been measured from the
gonad of mature females (Brickle et al. 2006b). These were
similar in size to those of another nototheniid species living
near the Subantarctic periphery of distribution, especially
South Georgian P. guntheri (1–1.4 mm; Lisovenko 1987).
After fertilisation, perivitelline space in P. ramsayi eggs
increased, and they attained 2.1–2.3 mm in diameter. The
egg masses were demersal, as in another species of Pata-
gonotothen—P. tessellata (Rae and Calvo 1995). The
number of eggs per egg mass was consistent with the total
fecundity observed in maturing and mature female P.
ramsayi (21,000–130,000 eggs depending on the size of the
female; Brickle et al. 2006b). This confirms the total
spawning reproductive strategy of this species, whereby one
portion of the eggs develops and matures in the gonad and
then is spawned as one egg mass.
In our study, the egg masses were always found in the
reservoir in the morning, suggesting that spawning took
place at night or early morning. In all egg masses, the most
developed eggs were at either 2 or 4 cells cleavages,
indicating that fertilisation had occurred just a few hours
earlier (Hall et al. 2004; Gorodilov and Melnikova 2006;
our data). Brickle et al. (2006b) observed P. ramsayi
females with hydrated oocytes in the gonads at night
between 22.00 and 08.00. Thus, it is likely that P. ramsayi
spawns at night and early morning.
Fig. 4 Early embryogenesis in P. ramsayi: zygote (a); cleavage period with two (b), four (c) and eight (d) cells. Scale bar 1 mm
Polar Biol
123
Nest guarding behaviour and parental care of egg mas-
ses is a common feature in the family Nototheniidae.
Chaenocephalus aceratus build nests and remain in close
contact with the egg masses during embryonic develop-
ment (Detrich et al. 2005). Naked dragonfish Gymnodraco
acuticeps show parental care of eggs masses by both sexes
(Evans et al. 2005). Icefish Chionobathyscus dewitti have
developed a special feature where females carry their
fertilised eggs around pelvic fins (Kock et al. 2006).
Male P. ramsayi displayed territorial behaviour by
occupying artificial shelters and defending the shelters and
adjacent bottom areas. Male P. tessellata (Rae and Calvo
Fig. 5 Blastula period of embryogenesis in P. ramsayi: spherical ball (a, b); dome shaped (c) and 25 % of epiboly (d). Scale bar 1 mm
Fig. 6 Gastrula period of embryogenesis in P. ramsayi: 50 %-epiboly (a); 75 %-epiboly (b); 100 %-epiboly (c). Scale bar 1 mm
Polar Biol
123
1995) and Nototheniops nudifrons (Hourigan and Radtke
1989) have also been observed protecting their nests during
the spawning period. However, in our experiment P.
ramsayi males were never observed guarding egg masses,
which were located out of the shelters. This is in contrast to
P. tessellata males that were observed to fertilise and guard
one or several egg masses, and keep them within their nest
(Rae and Calvo 1995). As P. ramsayi males guarded their
shelters for 3–4 weeks after fertilisation without eating the
eggs, it cannot be ruled out that they would guard the egg
masses in nature. Possibly, the artificial conditions within
the tank with non-typical substrate and shelters inhibited
guarding behaviour by the males.
Our data confirm sexual dimorphism in body coloration
in P. ramsayi during their spawning period (Ekau 1982),
when males acquire almost black coloration of the pelvic
and anal fins, head and throat. Change in body coloration of
males has also been observed in other nototheniids such as
C. dewitti and P. tesselleta (Rae and Calvo 1995; Kock
et al. 2006).
Duration of embryogenesis varies to a great extent in
nototheniids, from 28 days in P. tessellata (Rae and Calvo
Fig. 7 Segmentation period of
embryogenesis in P. ramsayi:development of first somites and
optical vesicle (a); formation of
otoliths in the auditory vesicles
and first movement of the
embryo (b); first heart beat and
pigmentation of eye balls (c);
appearance of melanophores on
the yolk sac (d); developed
pelvic fins (e); start of hatching
(f). Scale bar 1 mm
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123
1995) to approximately 310 days in G. acuticeps (Evans
et al. 2005). The observed duration of embryogenesis in P.
ramsayi is close to the short end of the range (28–32 days).
Duration of the yolk stage in P. ramsayi larvae is longer
than in Subantarctic P. tessellata (5 days, Rae et al. 1999),
but shorter than in the Antarctic G. acuticeps (15 days) and
N. nudifrons (up to 18 days, Hourigan and Radtke 1989).
Pigmentation patterns of the body are quite specific in
nototheniid larvae and used for species identification
(Stevens et al. 1984). Unlike larvae of Dissostichus elegi-
noides and Pleuragramma antarcticum (Evseenko et al.
1995; Vacchi et al. 2004), early larvae of P. ramsayi lack
head pigmentation, but have scattered melanophores on the
yolk sac and dense row of melanophores above the
urostyle.
The combination of r-features (small eggs and larvae,
high fecundity) and K-features (territorial behaviour and
possible nest guarding) in the reproductive strategy of P.
ramsayi is characteristic for nototheniid species occupying
low-latitude peripheries of their distribution (Rae and
Calvo 1995). Winter spawning and spring development of
the early larvae coincide with spring bloom of zooplankton
in the southwest Atlantic (Boltovskoy 1999). Summer
warming of shelf waters enhances growth rates of pelagic
fry which reach 6–8 cm TL by autumn and settle to the
bottom (Brickle et al. 2006a). At that size, they are suffi-
ciently large to exploit the demersal gammarid and isopod
resources (Laptikhovsky and Arkhipkin 2003). This suc-
cessful reproductive strategy of P. ramsayi contributed to
dominate the ecological niche of medium-sized nektonic
predators (trophic level 3–4) on the Patagonian Shelf and
upper Slope in the southwest Atlantic.
Acknowledgments We are grateful to L. Jurgens and Z. Shcherbich
for collecting and transporting live fish to the aquaculture facility and
to scientific observers from the Falkland Islands Fisheries Depart-
ment, especially D. Davidson and A. Monllor, who helped in main-
taining the fish tank and looking after the fish. We are thankful to S.
Brown (Shallow Water Marine Group, Stanley, Falkland Islands) for
photographing live fish in the tank. We thank our colleagues Drs A.
Winter, P. Brewin and V. Laptikhovsky for their comments and
suggestions that helped to improve the manuscript. We also thank the
Director of Natural Resources John Barton for supporting this work.
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