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: aarkhipkin@fisheries.gov.fk

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.

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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

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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

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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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