Variation in standing stock of the mackerel ice®sh

Champsocephalus gunnari at South Georgia

INIGO EVERSON, GRAEME PARKES*, KARL-HERMANN KOCK{and IAN L. BOYD

British Antarctic Survey, Madingley Road, Cambridge CB3 0ET, UK; *Marine Resources Assessment Group

Ltd, 47 Prince's Gate, London SW7 2QA, UK; and {Bundesforschungsanstalt fuÈr Fischerei, Institut fuÈrSee®scherei, Hamburg, Germany

Summary

1. Bottom trawl surveys on the South Georgia shelf indicate episodic declines in

the abundance of the mackerel ice®sh Champsocephalus gunnari that, since 1990,

are not directly attributable to commercial ®shing.

2. The greatest e�ect has been observed in years when krill are known to have

been scarce on the South Georgia shelf.

3. It is thought that C. gunnari survivorship is closely related to, but indirectly

in¯uenced by, krill availability.

4. Examination of food chain relationships indicates that predation by fur seals is

likely to play a major role in the observed changes in C. gunnari abundance.

5. Periodic shifts in food chain relationships, involving krill, C. gunnari and fur

seals, are postulated that could explain the episodic declines in the abundance of

C. gunnari in the absence of ®shing.

6. The study demonstrates how a key predator can have an over-riding impact on

a commercial ®sh species, highlighting the importance of the ecosystem approach

to ®sheries management.

Key-words: Antarctic, CCAMLR, ecosystem management, fur seal, krill.

Journal of Applied Ecology (1999) 36, 591±603

Introduction

The Antarctic mackerel ice®sh Champsocephalus

gunnari LoÈ nnberg is a member of the

Channichthyidae, a unique family lacking haemo-

globin (Kock & Everson 1997) that has an interest-

ing and unusual stock structure at South Georgia, a

sub-Antarctic island centred on approximately 54�S,37�W. Even before the onset of commercial ®shing

most of the stock consisted of 2±4-year-old ®sh, 20±

37 cm in total length, although the species can grow

to more than 60 cm and live for 12±14 years

(Permitin 1973). Champsocephalus gunnari is one of

several species of ®n®sh taken commercially in the

region.

Commercial ®shing for ®n®sh around South

Georgia began in the late 1960s, and catches have

been reported to the Commission for the

Conservation of Antarctic Marine Living Resources

(CCAMLR) since 1982, going back to the 1970 sea-

son (seasons are designated by split year, thus the

period 1 July 1969 to 30 June 1970 is referred to as

1970) (CCAMLR 1990a,b; CCAMLR 1996).

Mackerel ice®sh was one of the most important spe-

cies caught. Maximum catches yielded 80 000 tonnes

in 1977, 128 000 tonnes in 1983 and 71 000 tonnes in

1987 (Fig. 1). The ®shery ceased after 1990. During

the 1970s and 1980s the large variation in catches

from year to year was attributed primarily to the

di�erences in ®shing between years and variation in

year-class strength. Little attention was paid to

other substantial sources of natural variation that

might be present in the stock. Since the late 1980s

the standing stock of C. gunnari has been monitored

by ®shery-independent ground®sh surveys.

Even though there has been no commercial ®shing

since 1990, the stock has continued to ¯uctuate sub-

stantially, with dramatic episodic declines in abun-

dance. In seeking an explanation for these declines,

we have investigated the status of krill Euphausia

superba Dana, a key prey item, and predators such

as the fur seal Arctocephalus gazella Peters, follow-Correspondence: Inigo Everson (fax 01223 362616).

e-mail: iev@pcmail.nerc-bas.ac.uk

Journal of

Applied Ecology

1999, 36,

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# 1999 British

Ecological Society

ing on from suggestions made by Parkes (1993) and

Everson et al. (1994a).

Materials and methods

GROUNDFISH SURVEYS

A series of seven ground®sh surveys was carried out

on the shelf around South Georgia between 1986

and 1994. The ®rst two surveys were undertaken as

part of the United States Antarctic Marine Living

Resources Programme (AMLR). The third was

jointly by the UK and Poland, and the remainder

by the Government of South Georgia and the South

Sandwich Islands. The sampling periods for the

seven surveys are set out in Table 1.

The principal aim of the surveys was to provide

estimates of the relative abundance of demersal ®sh

species of commercial interest within CCAMLR

subarea 48.3, with particular reference to C. gunnari.

Other species sampled included two other ice®sh,

Chaenocephalus aceratus LoÈ nnberg and

Pseudochaenichthys georgianus Norman, and the

humphead notothen Gobionotothen gibberifrons

LoÈ nnberg. The survey area was divided into three

depth strata, 50±149m, 150±249m and 250±500m.

The sampling design was a series of randomly prelo-

cated sampling stations with the net ®shing on the

bottom for 30min at each. (In practice, due to pro-

blems with the uneven seabed around South

Georgia, the track of each station was surveyed

before each tow and adjustments made to the exact

location of the haul as necessary.) All the surveys

covered the South Georgia shelf, with the exception

of an area o� the south-west coast between

Fig. 1. Catches of the dominant ®sh species around South Georgia reported to CCAMLR in recent years. ANI,

Champsocephalus gunnari; SSI, Chaenocephalus aceratus; SGI, Pseudochaenichthys georgianus; NOG, Gobionotothen gibberi-

frons.

Table 1. Timing of the surveys

Year Vessel Period of survey

1987 Profesor Siedlecki 29 November 1986±17 December 1986

1988 Profesor Siedlecki 19 December 1987±10 January 1988

1989 Profesor Siedlecki 1±14 February 1989

1990 Hill Cove 6±26 January 1990

1991 Falklands Protector 22 January ± 11 February 1991

1992 Falklands Protector 3±26 January 1992

1994 Cordella 4 January ± 6 February 1994

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Annenkov Island and Cape Disappointment, where

the ground is very rough and unsuited to bottom

trawling. All except one survey covered the much

smaller Shag Rocks shelf. Figure 2 provides an

example chart showing the haul locations from the

1991 survey. Sampling e�ort was allocated in rela-

tion to the area of seabed and the expected density

of C. gunnari in the three strata. Sampling locations

were distributed around the islands using a grid of

rectangles 0´5 degree of latitude by 1 degree of long-

itude. Details of the seven surveys are given in

Gabriel (1988), McKenna & Saila (1989), Parkes

et al. (1989, 1990) and Everson et al. (1991, 1992,

1994b).

The catch from each haul was sorted by species

and the number and total mass of each were mea-

sured. Samples were taken for length, individual

mass and age determination. Length-to-mass rela-

tionships and age±length keys were prepared and

reported to CCAMLR for use in stock assessments.

Age determination using otoliths was undertaken on

samples of C. gunnari by the Sea Fisheries Institute,

Gdynia, Poland. Diet composition and feeding

intensity of ice®sh were recorded in 1991, 1992 and

1994 using the frequency of occurrence method

(Kock et al. 1994).

ESTIMATION OF RELATIVE ABUNDANCE OF

GROUNDFISH

Studies on ground®sh surveys have shown that

catchability is potentially in¯uenced by a number of

factors, including three major components of the

survey equipment: the vessel, the trawl doors (otter

boards) and the trawl itself (Anonymous 1991;

J.R.S. Forrester, personal communication). Changes

in equipment during the course of a survey series

are therefore seen as undesirable, due to the poten-

tial for the introduction of bias in abundance

indices. Every attempt was made to standardize the

personnel, vessel and sampling gear during the sur-

vey series.

The team of scientists undertaking the surveys

remained more or less constant over the study per-

iod and the ®shing master changed only twice. The

same design of trawl doors was used throughout the

series. The trawl warp-to-water depth ratio was 3 : 1

for all surveys and the towing speed was 3´5 knots

with the net on the bottom. Unfortunately, however,

logistics and costs meant that changes in equipment

were unavoidable and four di�erent vessels, whose

details are shown in Table 2, were used. Three di�er-

ent variants of the same bottom trawl design were

used, all of which had a 40-mm liner in the cod end.

The di�erences between the trawls are set out in

Table 3. Similar headline length and the same design

of trawl doors provided for a similar wingspread,

and thus ®shing area, on all the nets. Even so, it was

only possible to measure the geometry of the trawl

in situ during one of the surveys (Pilling & Parkes

1995). In the absence of additional experimental evi-

dence, the surveys were treated as a time series from

which indices of stock abundance of ground®sh

could be generated. The unknown bias between sur-

veys resulting from vessel and gear changes was

treated as a random factor in the time series.

Fish density for each sample was estimated from

the mass of the catch, distance trawled and horizon-

Fig. 2. Map of South Georgia shelf showing the sampling locations on the 1991 survey. The same basic pattern was used

on all the surveys reported in this paper.

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tal opening (wingspread) of the net. Estimates of

relative abundance were ®rst made by the swept

area method (Gulland 1975; Saville 1977), assuming

normal distribution of densities. Areas of seabed

were taken from Everson & Campbell (1991). Due

to concerns over the application of this method to

species with patchy distributions, such as C. gunnari,

the density estimates were also analysed using a

computer program TRAWLCI (de la Mare 1994).

This uses Aitchison's delta distribution (Aitchison

1955; Pennington 1983) to model the underlying sta-

tistical distribution of trawl survey densities, and

generates unbiased estimates of abundance with

con®dence intervals that give the correct coverage

probability (de la Mare 1994). In both cases, esti-

mates of relative abundance and variance by stra-

tum were calculated and combined over strata to

give an overall relative abundance estimate.

THE POPULATION MODEL

Where the age composition of the catches is known,

the survey estimates of year class strength can be

used directly to predict relative abundance in subse-

quent years, assuming growth, natural mortality M

and catch C are known approximately. At meetings

of the CCAMLR Working Group on Fish Stock

Assessment, cohort analysis (Pope 1972) has been

used to project abundance in the terminal (most

recent) year of the Virtual Population Analysis

(VPA) and/or the relative abundance estimates from

surveys forward in time to examine the possible

e�ects of di�erent levels of future catch. For num-

bers N at age a and time t:

Nt�1;a�1 � NtaeÿM ÿ Ctae

ÿM=2: eqn 1

Throughout the analyses, M was assumed to be con-

stant both across ages and years.

Parkes (1993) and Anonymous (1993) used a time

series of abundance estimates for the South Georgia

shelf, derived from trawl surveys, as a relative index

of absolute abundance to tune VPA using both

Laurec±Shepherd tuning (Pope & Shepherd 1985)

and the ADAPT program (Gavaris 1993). The results

of these VPA demonstrated several important

points. The abundance of C. gunnari went through

major ¯uctuations during the active period of the

®shery in the 1970s and 1980s. Several surveys were

conducted during this period and they track the

changes in abundance reasonably well. However, in

the period after the cessation of commercial ®shing,

the VPA results did not correspond well to changes

in both abundance and age structure shown by sur-

veys between 1990 and 1991 (Anonymous 1993;

Parkes 1993).

To investigate population changes between adja-

cent surveys, we used cohort analysis to project

numbers at age estimated from one survey forwards

to the time of the following survey. When catches

are involved, this type of analysis su�ers from the

fact that surveys are regarded as a relative measure

of abundance, while the catches are taken to be

absolute. However, since the end of February 1990

the catch at South Georgia has been very small (the

reported catch between the times of the 1990 and

1991 surveys was 3828 tonnes, all taken in February

and March 1990). For simplicity, the catch compo-

nent of equation 1 was therefore omitted from the

cohort analyses.

Table 2. Details of vessels used in the surveys

Vessel name Profesor Siedlecki Hill Cove Falklands Protector Cordella

Port of registry Gdynia, Poland Stanley, Falkland Islands Hull, UK Hull, UK

Surveys 1987, 1988, 1989 1990 1991, 1992 1994

LOA 89´3 60 69´15

Horsepower 2800 2200 2500 2700

Tonnage 997´27 NRT 1591 GRT 1500 GRT

Trawl used P32/36 HC-120 FP-120 FP-120

LOA = length overall; GRT = gross registered tonnage; NRT = net registered tonnage.

Table 3. Characteristics of bottom trawl nets used in the surveys

P32/36 HC-120 FP-120

Headline length (m) 36 36´6 36´6

Measured headline height (m) (Pilling & Parkes 1995) 3´25±5

Measured wingspread (m) (Pilling & Parkes 1995) 14´5±22´3

Lower wings Absent Present Absent

Doors Polyvalent Polyvalent 1200 kg Polyvalent 1200 kg

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Observed abundance at age was estimated from

the total biomass (this study); age distributions and

mean weight at age were derived separately from

each survey data set (Parkes 1993). These values

were projected stochastically to the time of the fol-

lowing survey. Ninety-®ve per cent con®dence inter-

vals (CI) for observed abundances at age were

simulated, using a bootstrap method, from the over-

all coe�cients of variation (CV) (assumed to be con-

stant across ages) provided by the TRAWLCI

program, assuming log-normally distributed resi-

duals. The 95% CI for the projected values was

derived from 2000 individual evaluations for each

age class. M was assumed to be constant (0´42)

across ages and years. Values for South Georgia

only were used in the projections due to the incom-

plete time series and small number of hauls from

Shag Rocks. The projection periods and age class

comparisons are shown in Table 4.

Results

SURVEYS

Throughout the survey series, the total catch of C.

gunnari in each haul was generally between 1 and

100 kg for a standard 30-min haul. All surveys

included a small proportion (about 5±10%) of larger

hauls, generally in the region of 0´2±1´0 tonnes. The

most extreme case was the 1990 survey, which con-

tained three hauls from South Georgia of between 2

and 8 tonnes each, two hauls at Shag Rocks of

between 3 and 5 tonnes, and a further haul at Shag

Rocks of about 55 tonnes, each for a standard half-

hour tow. Owing to the relatively small number of

hauls from Shag Rocks, this last catch had a great

e�ect on the estimates of both biomass and variance

for that year. Indices of relative abundance for C.

gunnari at Shag Rocks and South Georgia are set

out in Table 5.

Table 4. Projected means and con®dence intervals of relative abundance compared with the observed values from the sur-

veys

Projection

Period of

projection Comparison

2- and 3-year-old ®sh observed in 1989 to

3- and 4-year-old ®sh in 1990

1 year Predicted and observed 3- and 4-year-old ®sh in 1990

2- and 3-year-old ®sh observed in 1990 to

3- and 4-year-old ®sh in 1991

1 year Predicted and observed 3- and 4-year-old ®sh in 1991

2- and 3-year-old ®sh observed in 1991 to

3- and 4-year-old ®sh in 1992

1 year Predicted and observed 3- and 4-year-old ®sh in 1992

2- and 3-year-old ®sh observed in 1992 to

4- and 5-year-old ®sh in 1994

2 years Predicted and observed 4- and 5-year-old ®sh in 1994

Table 5. Estimated standing stock of Champsocephalus gunnari at South Georgia and Shag Rocks from trawl surveys. Note

that the 1990 survey around Shag Rocks included one exceptionally large haul of 40 tonnes in 22min

South Georgia Shag Rocks

Year Biomass (tonnes)

(lower CI±upper CI)

N

CV(%)

Biomass (tonnes)

(lower CI±upper CI)

N

CV(%)

1987 48 452 94 11 254 9

(31 839±85 567) 22´4 (2445±29 191) 63´2

1988 17 326 113 1386 3

(10 687±35 086) 36´8 (77±2´6� 1011) 76´7

1989 24 290

(12 201±76 002)

55

38´1

No sample

1990 67 620 59 305 889 8

(18 289±605 485) 64´2 (25 287±2´3� 1010) 78´7

1991 27 160 66 3855 10

(17 196±55 599) 25´9 (925±242 113) 68´6

1992 41 449 67 4659 11

(27 347±123 349) 21´6 (990±273 453) 72´7

1994 16 572 71 5275 13

(10 704±39 336) 23´5 (3134±15 049) 26´4

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The point estimates of biomass and associated

lower con®dence limits ¯uctuated substantially but

it is di�cult to interpret these because of the extre-

mely large upper con®dence limits. These latter we

believe to be overestimated by the TRAWLCI pro-

gram. The CV of the mean values of relative abun-

dance around South Georgia were, with one

exception, in the region of 21±38%. The lower num-

ber of sample stations and patchy distributions of

®sh at Shag Rocks resulted in high CV (60±80%)

for all except the 1994 survey.

COHORT ANALYSIS

The results of the cohort projections are shown in

Table 6. In both 1990 and 1992, observed abun-

dances were reasonably close to, and not signi®-

cantly di�erent from, those expected from previous

surveys. However, in 1991 and 1994 there were

anomalies indicating major departures from the

population model. In both these years, the observed

abundances were signi®cantly below those expected

on the basis of assumed levels of growth and M.

The incomplete time series and small number of

hauls from Shag Rocks means that estimates for

this area are subject to a much greater uncertainty

than those from South Georgia. In spite of this,

there is good evidence for a substantial decline in

standing stock at Shag Rocks between the 1990 and

1991 surveys (Table 5).

Discussion

The level of uncertainty around survey biomass esti-

mates and projections based on them is very often

high. Despite this, the anomalies shown by the ana-

lysis presented here show signi®cant departures

from the population model. However, the purpose

of this paper is not to examine the magnitude of

these anomalies in detail, beyond noting that they

are substantial, but rather to suggest mechanisms

that might be responsible for their existence.

The natural mortality coe�cient, M, prior to the

start of commercial ®shing was thought to be

around 0´42 (Everson 1998). This would mean that

under normal circumstances only around 5% of 1-

year-old ®sh would live to 7 years or more.

Although ®sh up to age 14 have been observed

(Permitin 1973), the older ®sh made up only a very

small proportion of the population prior to exploita-

tion (Kock & KoÈ ster 1989). Thus even prior to the

onset of commercial ®shing the population would

have been dominated by younger ®sh and the great-

est changes in biomass would have been associated

with 2, 3 and 4 year olds. Increase in the preponder-

ance of younger ®sh in the stock is a typical result

of the impact of commercial ®shing and has been

reported for ice®sh (Kock 1992). Following the ces-

sation of commercial ®shing in 1990 one would rea-

sonably expect to have seen a corresponding

increase in the proportion of older ®sh in the stock

and an associated reduction in the interannual varia-

bility in abundance. The survey estimates and

cohort projections indicate that this has not

occurred.

Evidence from surveys at South Georgia indicates

that the biomass of the dominant year classes was

signi®cantly less than expected in 1991 and 1994.

We conclude that these deviations from the popula-

tion model genuinely demonstrate two major

declines in adult abundance of C. gunnari in the

region in the absence of ®shing. These declines

occurred during seasons when the krill abundance

was low. In seasons when the krill abundance

appeared normal, 1990 and 1992, the cohort projec-

tions fell within the con®dence intervals of the sur-

vey results.

Table 6. Observed abundance of age classes compared with abundance predicted from cohort projections. The krill density

for each year from Brierley et al. (1999) is shown for comparison

Survey and projection results Mean Lower CI Upper CI Predicted/observed Krill density (gm±2)

Observed 2+3 year olds 1989 14 047 5569 30 112

Predicted 3+4 year olds 1990 14 297 5659 30 003

Observed 3+4 year olds 1990 27 979 8787 69 092 Within CI 45±75

Observed 2+3 year olds 1990 65 736 25 467 145 686

Predicted 3+4 year olds 1991 89 697 33 243 210 209

Observed 3+4 year olds 1991 15 805 10 821 22 296 5´7 6

Observed 2+3 year olds 1991 15 578 10 643 22 271

Predicted 3+4 year olds 1992 17 999 12 312 25 355

Observed 3+4 year olds 1992 21 236 14 942 29 736 Within CI 95

Observed 2+3 year olds 1992 35 477 26 248 46 854

Predicted 3+4 year olds 1993 43 735 32 086 58 103 66

Predicted 4+5 year olds 1994 41 618 30 598 55 201

Observed 4+5 year olds 1994 1383 913 2020 30´1 7

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The remainder of this paper is devoted to consid-

ering possible explanations for these observations,

posed as a series of questions.

ARE THE ANOMALIES SIMPLY AN

EXPERIMENTAL ARTEFACT?

There are two main issues to be considered when

assessing whether the observed anomalies in 1991

and 1994 are genuine. These are, ®rst, that some

aspect of the survey design was inappropriate for

the distribution of the target species, and secondly,

that the e�ciency of the sampling gear varied

between surveys due to changes in equipment speci-

®cation or some aspect of the behaviour of the ®sh

associated with the timing of the surveys.

The random strati®ed design of the ground®sh

survey is a well-established methodology, used

around the world (Sissenwine, Azarovitz & Suomala

1983; Anonymous 1992a, b) that has been examined

and approved for surveying of C. gunnari by the

CCAMLR Working Group on Fish Stock

Assessment on a number of occasions (Anonymous

1992c). Therefore there is not thought to be any

inherent problem with the basic experimental meth-

odology used for the surveys.

As stated earlier, inter-vessel calibration studies

were not possible for a variety of reasons. The e�ect

of changing the survey vessel during the course of

the series is therefore unknown. Other studies have

shown that both vessel and trawl door e�ects are

potentially signi®cant. For example, using data from

the 35-year trawl survey series conducted by the US

NMFS North-east Fisheries Science Centre and its

predecessors, calculated vessel coe�cients (catch

ratio of two vessels ®shing simultaneously) in the

region of 0´8 for cod and haddock (95% CI 0´69±

0´94) and door coe�cients (catch ratio of polyvalent

to BMV doors) in the region of 1´49±1´56 (95% CI

1´18±1´88) were obtained (Anonymous 1991). The

reason that larger vessel di�erences were not

observed may be due, at least in part, to the fact

that both of the NMFS research vessels are much

oversized with regard to weight and horsepower for

the size of the trawl employed (C. Byrne, personal

communication). The same can be said of the vessels

used in the South Georgia survey series, all of which

were large stern trawlers more than capable of hand-

ling the small bottom trawl used throughout. In the

absence of any other information, the possible

e�ects resulting from changes in vessels were treated

as negligible. In contrast, it was concluded from the

NMFS study that changes in the trawl doors were

the most signi®cant intervention in the survey series.

There were no changes in the design of polyvalent

trawl doors used during the South Georgia series.

With respect to the three trawls, a comparison of

the characteristics of the nets is given in Parkes

(1993). The most notable di�erence between them is

the presence of lower wings in the HC-120 (1989/90

survey), which were not included in the other two

nets (the P32/36, 1986/87±1988/89, and the FP-120,

1990/91±1993/94). While it is possible that the pre-

sence of the lower wings increased the catching e�-

ciency of the HC-120 trawl compared to the others,

there is no way of knowing the extent to which this

is true. The ®shing master who worked with both

the HC-120 and the FP-120 trawls thought that the

e�ect was probably small on the rough trawling

ground around South Georgia. It should also be

noted that the two surveys that indicated the decline

in abundance between 1992 and 1994 used the same

trawl (the FP-120).

Champsocephalus gunnari are known to spend

daylight hours very close to the seabed and migrate

up into the water column at night (Frolkina &

Shlibanov 1991). Since the 1991 season, sampling on

the South Georgia ground®sh survey has been

restricted to daylight hours to prevent under-repre-

sentation of ®sh in the catch at night. Abundance

estimates prior to this time may therefore be nega-

tively biased compared with later estimates. If true,

this would make the discrepancy between expected

and observed abundance in 1991 even greater.

All of the surveys were undertaken at approxi-

mately the same time of year, during the summer

period, several months prior to the main spawning

season. The ®sh are known to aggregate prior to

spawning (Kock & Everson 1997); however, we do

not feel that this e�ect could have in¯uenced the

abundance estimates to the extent that we have

found.

COULD THE ANOMALIES BE THE RESULT

OF UNREPORTED FISHING?

The ®shing that took place up to the 1989/90 season

(Fig. 1) will have had an e�ect on the variability in

abundance and age structure of the population. This

e�ect would have continued as the population

recovered. Even allowing for this e�ect, the dra-

matic and abrupt declines in abundance in 1991 and

1994 cannot be explained by the reported catches.

The cohort analysis assumes that the reported

catches are a true re¯ection of the biological

removals from the C. gunnari stocks around South

Georgia, i.e. that there was negligible ®shing mortal-

ity after January 1990. In 1991 the reported com-

mercial catch was only 41 tonnes (SC-CAMLR

1991), against a total allowable catch of 26 000

tonnes (CCAMLR 1990c). Fishing vessels were

known to have been operating in the area, but left

due to the extremely poor catch rates (SC-CAMLR

1991), which tends to con®rm the gross reduction in

abundance at that time. It is unlikely that misreport-

ing has occurred given the low catch rates.

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Subsequent to 1990, we know of no commercial ®sh-

ing that could account for the discrepancies in the

standing stock estimates.

COULD THE FISH BE MIGRATING AWAY

FROM THE SURVEY AREA?

The distribution of C. gunnari is restricted to the

shelf area, and most ®sh were caught in water less

than 300m deep. South Georgia is an island, sepa-

rated from other major island groups by several

hundred miles and by waters over 2000m deep. A

survey at the South Orkney Islands, 300 miles away

from South Georgia, in January and February 1991

(Balguerias 1991) did not indicate a dramatic

increase in abundance over previous estimates, as

might be expected if a migration to that area, of the

scale necessary to account for the observed change,

had taken place.

Shag Rocks are close to South Georgia but are

separated from it by water deeper than 1000m for

approximately 10 nautical miles. If the decline on

the South Georgia shelf were a result of ®sh having

migrated across this gap, then a negative correlation

would be expected between the standing stock on

the South Georgia shelf and that around Shag

Rocks. This correlation is positive (R=0´764, d.f.

4, 0´1<P<0´05), indicating that the changes in

biomass at the two locations are moving in the same

direction and consequently discounting migration

between Shag Rocks and South Georgia as a viable

explanation.

Information from analysis of genetic variability

between di�erent localities has indicated that move-

ment of individuals between the South Orkneys and

South Georgia does occur (Carvalho & Lloyd-Evans

1990; Carvalho & Warren 1991). However, the

amount of mixing of ®sh required to produce these

results is almost certainly very much smaller than

would be required to explain the substantial reduc-

tions in standing stock around South Georgia.

Consequently we consider it unlikely that the

e�ect is due to local migration and also that, due to

the large expanse of deep water separating the

South Georgia and Shag Rocks region from other

suitable areas of shelf such as South Orkneys and

South Shetlands, the probability of such a large-

scale migration over such a distance is extremely

small.

COULD THE ANOMALIES BE THE RESULT

OF DEPARTURES FROM THE ASSUMPTIONS

IN THE POPULATION MODEL?

In 1990 and 1992, when the krill density was high,

the cohort projections in Table 6 fell within the con-

®dence intervals of the survey values, but when the

krill density was low, 1991 and 1994, the cohort pro-

jections were substantially above the survey values.

This is indicative of an ecological e�ect whereby

some of the assumptions in the population model

may no longer be valid.

Departures from the assumptions about growth

and M in the population model could give rise to

the observed anomalies. M was assumed to be con-

stant across years and ages. Growth was assumed to

be well represented by the mean weights at age cal-

culated from samples taken during the surveys. Of

these two possibilities, the single most plausible

explanation for these observations that has emerged

from discussions within the CCAMLR Working

Group on Fish Stock Assessment, is that periodi-

cally there is a dramatic increase in M considerably

in excess of the normally assumed level

(Anonymous 1994) of 0´42 (Everson 1998). We envi-

sage three situations under which natural mortality

could have dramatically increased to account for the

apparent changes in 1991 and 1994: zoonosis, star-

vation and increased predation.

In spite of examining over 10 000 ®sh during the

course of the surveys we have found no indication

that would point to disease as being the cause of

declines in numbers. The only evidence of disease

observed during the surveys was very small numbers

of ®sh, less than ®ve ®sh on any survey, that

appeared to have lesions, similar to the `X cell'

lesions reported by Bucke & Everson (1992) from

Lepidonotothen squamifrons.

Information on the diet of ice®sh, obtained during

most of the surveys, has been published (Kock et al.

1994). This indicates that the preferred food of C.

gunnari is Antarctic krill Euphausia superba, but that

periodically, when this is scarce, there is a greater

proportion of mysids and the hyperiid amphipod

Themisto gaudichaudii in their diet (Kock et al.

1994).

In years when krill are scarce, more of the sto-

machs of C. gunnari examined were empty com-

pared with years when krill were abundant. Even so,

when krill were scarce, the ®sh were apparently able

to feed successfully on alternative prey. Condition

indices have also been examined, which indicate

that, when krill were scarce, the ®sh were in poorer

condition. However, the reduction in condition is

thought to be insu�cient to cause death (Everson,

Kock & Parkes 1997). We therefore consider that

feeding conditions are unlikely to be the major

direct cause of the year-to-year di�erences in survi-

vorship.

The CCAMLR Ecosystem Monitoring

Programme (CEMP) uses data that provide indices

of krill availability on a variety of time and space

scales (Anonymous 1995). All four indicator species

monitored at South Georgia (fur seals Arctocephalus

gazella, gentoo penguin Pygoscelis papua Brandt,

macaroni penguin Eudyptes chrsolophus Forster and

598Variation in

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black browed albatross Diomedea melanophris

Temminick) provided indices (e.g. reproductive per-

formance) indicating that from 1988 to 1997 there

have been two periods when the availability of krill

around South Georgia was low. These were immedi-

ately prior to 1991 and 1994 (Table 7). These years

coincide with the years of unexpectedly low abun-

dance of C. gunnari and also krill at South Georgia

(Table 6).

In considering possible e�ects due to predation on

C. gunnari it is necessary to note the size spectrum

of ®sh in the diet and the amount that each predator

is likely to consume. Table 8 lists the dominant ®sh-

eating predators known to forage on the South

Georgia shelf.

Gentoo penguins at South Georgia are estimated

to consume about 28 000 tonnes of ®sh each year

(Croxall, Prince & Ricketts 1984), around 27% of

which is estimated to be C. gunnari. In an average

year, therefore, gentoo penguins are likely to con-

sume around 7500 tonnes. There would need to be a

substantial increase in this amount to account for

the observed discrepancies in C. gunnari abundance,

which seems unlikely.

At South Georgia the fur seal population has

been increasing over the past several decades to its

present level of more than 4 million (Boyd 1993).

Models based on the energetic requirements of seals

using estimated pup production, age-speci®c annual

survival (Boyd et al. 1995), growth (Payne 1979) and

an average ®eld metabolic rate, which is four times

the basal metabolic rate (Costa, Croxall & Duck

1988), indicate that the current population would

consume about 5 or 6 million tonnes of krill each

year.

During the breeding season, the period of greatest

food consumption, lactating female fur seals are

land-based predators, with a median foraging range

in the region of 80 km from shore. Consequently

they rely on a high local abundance of food, prefer-

ably krill, to meet their energetic requirements at

this critical time of year (Reid & Arnould 1996;

Iverson, Arnould & Boyd 1997). They also feed on

®sh, particularly C. gunnari (Reid 1995), although

their ability to take large amounts of that species

may be constrained by their restricted diving depth

relative to the main depth range of the ®sh, 150±

250m. Dives tend to be no deeper than the mixed

Table 7. South Georgia krill density from acoustic surveys (Brierley et al. 1999) and CEMP indices for four species depen-

dent on krill. GEPE, gentoo penguin; MAPE, macaroni penguin; BBAL, black browed albatross; FUSE, fur seal

Year Krill (g m±2)

GEPE

Breeding

success Krill in diet

MAPE

Breeding

success Krill in diet

BBAL

Breeding

success

FUSE

Foraging

trip Pup growth

1988 M M L VL S M

1989 M H H M M M M

1990 45±75 L-M M H M M S L±M

1991 6 VL L H L VL VL M

1992 95 H M M H M M M

1993 66 H H M-H H H M±L M±H

1994 7 VL VL M VL VL VVL M

For indices of breeding success, diet and growth: M = medium, L-M=low to medium, H = high, VL = very low, M±H

= medium to high.

In addition, for indices of foraging trip duration: S = short, VL = very long, VVL = very very long, M±-L = medium to

long.

Table 8. Diet information on dominant ®sh eating predators known to forage on the South Georgia shelf

Predator Diet

Gentoo penguin Pygoscelis papua Diet varies but in some seasons includes signi®cant amounts of ®sh

Take ®sh up to 26 cm total length. C. gunnari forms a signi®cant component of

the diet (Croxall, Prince & Reid 1997)

Fur seal Arctocephalus gazella Diet varies. Appears to feed preferentially on krill but is known to take signi®cant

amounts of ®sh particularly when krill are scarce

Diet includes C. gunnari but in some seasons myctophids and nototheniids

predominate in the ®sh component of the diet

Able to feed on C. gunnari of all size classes (Reid 1995)

Blue-eyed shag

Phalacrocorax georgianus

Known to feed on ®sh but no evidence of signi®cant amounts of C. gunnari in the diet

Elephant seals Mirounga leonina Known to feed on ®sh but no evidence of C. gunnari in the diet at South Georgia

599I. Everson et al.

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layer, with 95% of dives being less than 50m,

although they are known to dive deeper than 100m

(Boyd & Croxall 1992; Boyd, McCa�erty & Walker

1997).

We suggest that if krill were scarce at this time of

year then fur seals are likely to feed to a greater

extent on ®sh, including C. gunnari, within their

foraging range. The magnitude of this prey shift

could be su�cient to result in a signi®cant increase

in M on C. gunnari. A brief study of the relative

energy densities of krill and ®sh provides a ®rst

approximation of the possible quantities involved:

assuming energy densities for krill and ®sh of 3´5

and 4´0 MJ kg±1, respectively (Clarke 1980; Cherel

& Ridoux 1992), the total dietary requirement, if the

diet was totally of ®sh, would be over 4´5 million

tonnes. If the increased consumption of C. gunnari

by fur seals in times of krill scarcity amounted to

only 5% of this total requirement, this would be in

the same order of magnitude as the observed unex-

plained declines in the abundance of C. gunnari.

Is there evidence for such shifts occurring? Reid &

Arnould (1996) studied the diet of breeding fur seals

during the period from January to March from 1991

to 1994. They found that during this time, although

krill was the most frequently occurring prey item,

present in 88% of all scats examined, ®sh were pre-

sent in 47% of scats. Protomyctophum choriodon,

Lepidonotothen larseni and C. gunnari were the

dominant ®sh species present. They also found that

in the two seasons when krill were known to be

scarce, 1991 and 1994, the occurrence of ®sh was

highest; ®sh occurring in 62% and 67% of scats,

respectively. However, the proportion of C. gunneri

in fur seal diet was very much lower in 1991 than in

1994, and they appeared to be eating older ®sh (3+

years) than in 1994, when they ate 2-year-old ®sh

(Reid & Arnould 1996). Thus, while there is sub-

stantial evidence for increased consumption of ice-

®sh by fur seals in years of low krill abundance, the

interaction between the two species is obviously also

dependent upon other factors, such as the timing of

krill scarcity and year-class strength of the ice®sh

population itself.

This scenario leads to a relatively straightforward

series of food chain relationships involving ®sh, krill

and fur seals, illustrated schematically in Fig. 3. We

envisage a situation whereby when krill are plentiful

around South Georgia (the left hand side), fur seals

and C. gunnari feed preferentially on krill. When

krill are scarce (the right hand side), fur seals feed to

a greater extent on ®sh, including myctophids and

C. gunnari. Under these circumstances C. gunnari

feed to a greater extent on non-krill components of

the zooplankton such as Themisto. Such a periodic

shift in the food web dynamics in response to occa-

sional scarcity of krill in the vicinity of South

Georgia, and thus increased predation by the huge

fur seal population, could be responsible for the two

anomalies in the abundance of C. gunnari observed

in 1991 and 1994.

Although there were ground®sh surveys con-

ducted around South Georgia and Shag Rocks prior

to the 1986/87 season, these were not conducted

with su�cient frequency to enable reliable partition-

ing on a year-by-year basis of ®shery and ®shery-

independent e�ects on abundance. Even a slight

increase in the predation of C. gunnari by just 5%

could have a signi®cant e�ect on the size of the

stock. The extent to which the mechanism postu-

lated here was responsible for ¯uctuations in the

abundance of C. gunnari in the 1970s and 1980s is

therefore unclear, although the fur seal population

was also increasing rapidly over that period (Boyd

1993).

The results demonstrate that it is not appropriate

to consider management of the ice®sh around South

Georgia by the traditional single species methods.

Careful consideration needs to be given to the incor-

poration of key elements of food web dynamics, spe-

Fig. 3. Food chain relationships involving Champsocephalus gunnari, krill and fur seals. The thickness of the arrows indi-

cates a hypothesized strength of the interactions in years when krill are scarce and in years when krill are abundant.

600Variation in

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# 1999 British

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ci®cally those interactions involving krill, Themisto,

myctophids and fur seals into a management regime.

This is central to the mechanism for precautionary

management that is currently being developed and is

based on the assumption that M may increase dra-

matically in some years due to changes in predation

pressures (Agnew et al. 1998).

Viewed in a wider context, this study demon-

strates how a key predator can have an over-riding

impact on a commercial ®sh species. Furthermore,

through the interaction between environmental

variability and a large population of predators, it

highlights the importance of the ecosystem approach

to management of the Convention for the

Conservation of Antarctic Marine Living Resources,

the only international ®sheries convention to have

such an approach as its central pillar (Anonymous

1981).

Acknowledgements

We gratefully acknowledge all the o�cers, crew and

scienti®c teams on the various research cruises. We

also thank David Agnew, Geo� Kirkwood, John

Croxall and Keith Reid for their contributions to

various discussions leading up to completion of this

paper. Two anonymous referees made several useful

comments on an earlier draft of the manuscript that

served to strengthen the paper and this is gratefully

acknowledged.

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