The Diet of Antarctic Fur Seals Arctocephalus Gazella During the Breeding Season at South Georgia

Polar Biol (1996) 16: 105—114 ( Springer-Verlag 1996

ORIGINALPAPER

Keith Reid · John P.Y. Arnould The diet of Antarctic fur seals Arctocephalus gazella during the breeding season at South Georgia

Received: 15 March 1995/Accepted: 13 May 1995

Abstract The diet of lactating female Antarctic fur seals Introduction Arctocephalus gazella at South Georgia was investi- gated during the pup-rearing period (January/March) of 1991—1994. Antarctic krill Euphausia superba was the It is generally reported that the diet of female Antarctic main prey item, occurring in 88% of all scats (n"497), fur seals Arctocephalus gazella at South Georgia during whereas fish occurred in 47% and squid in 5% of all the breeding season is predominantly Antarctic krill scats. There was considerable intra- and inter-annual Euphausia superba (Doidge and Croxall 1985; Croxall variation in the characteristics of krill taken by fur and Pilcher 1984; North et al. 1983; Boyd et al. 1991). seals. The distribution of krill sizes taken suggests that However, the data available suggest that there is some fur seals are not actively selecting particular sizes of variability in the appearance of other taxa along with krill and, therefore, that the krill in the diet reflects the krill. For example, indications of krill were found in krill available around South Georgia. The absence most of the 97 stomachs collected from adult female fur of group 3 krill (44—48 mm in length) in the South seals in 1971—1973, while fish and squid remains occur- Georgia area, as indicated by their absence in the red in 10% and 8% of specimens respectively (M.R. diet of seals, is suggested as a possible reason for Payne unpublished data, in Doidge and Croxall 1985). low availability of krill and the subsequent reproduc- In contrast, during 1983, very few remains of other taxa tive failure among krill predators. The frequency were found in 238 stomachs collected from adult fe- of occurrence of fish was much higher than in previous males (1 squid beak and no fish otoliths) (Doidge and studies; the pattern of fish consumption showed a Croxall 1985) and only krill remains were found in 300 consistent seasonal pattern in 3 of the 4 years scats collected between November 1982 and March studied. Of the total number of the myctophid Proto- 1983 (North et al. 1983). Similarly, of 11 faecal samples myctophum choriodon, the most numerous fish taxon, collected in 1988, 2 contained non-specified remains 98% were taken between early February and the other than krill whereas 24 of 36 faecal samples collected middle of March. Champsocephalus gunnari and in 1989 contained non-krill remains (Boyd et al. 1991). ¸epidonotothen larseni agg., which both feed on The distribution and abundance of krill in the South krill, dominated the fish component of the diet outside Georgia area are likely to be dependent on a number this period and together constituted 94% of the total of oceanographic and biological characteristics and estimated biomass of fish consumed. The intra- and events operating both in the immediate vicinity of inter-annual variability in the diet of Antarctic fur South Georgia and on a larger scale in the Scotia Sea seals emphasise the need for diet studies to be conduc- and beyond. Small-scale local changes in either or both ted during the entire pup-rearing periods of several of these may result in short-term changes in prey avail- years. ability around South Georgia and therefore contribute to intra-annual variations in the diet of predators. Larger perturbations of this system may have more serious implications for the reproductive success of krill-feeding higher predators (Croxall et al. K. Reid ( ) · J.P.Y. Arnould British Antarctic Survey, 1988; Priddle et al. 1988). Several species of higher Natural Environment Research Council, High Cross, predators at South Georgia are known periodically to Madingley Road, Cambridge CB3 OET, UK suffer from low reproductive success as a result of poor 106 krill availability (Croxall et al. 1988), most recently in Where possible, otoliths were identified to species level using 1991 and 1994. In 1991 analysis of stomach samples of the keys in Hecht (1987) and Williams and McEldowney (1990). Champsocephalus gunnari, a krill-feeding fish, suggested Partially eroded otoliths from some species, particularly the Nototheniidae, are often impossible to identify and these otoliths were that krill availability during January and February assigned to species groups or to family. Thus the ¸epidonotothen 1991 was the lowest for 28 years (Kock et al. 1994). This larseni aggregation may include a small number of ¸. kempi, ¸. low availability had a severe detrimental effect on the nudifrons and Patagonotothen guntheri; however, the majority of this reproductive success of krill-feeding predators such as group were specifically identified as ¸. larseni. Any unidentified black-browed albatrosses Diomedea melanophris and notothenioid otoliths that did not belong to this group were recorded as Nototheniidae spp. Each otolith was then assigned to one Antarctic fur seals (Prince et al. 1994; Boyd et al. 1994; of the three following groups according to the degree of erosion: Lunn and Boyd 1993). Prey availability in 1994 appeared to be lower than in 1991, and the mortality rate 1. Good — little or no erosion, still with intact margins and medial of Antarctic fur seal pups was the highest recorded relief. 2. Fair — some signs of smoothing of margins and medial sculptur- in over 10 years of continuous monitoring (Boyd et al. ing. 1995). 3. Poor — heavily eroded with little or no medial relief and margins Since the biological composition both within and generally rounded. between krill swarms is known to vary considerably When assigning otoliths to these groups, consideration was given to (Watkins et al. 1986) and the distribution and abund- the characteristics of otoliths from different fish families, in partic- ance of krill also varies, there is considerable scope for ular otoliths from myctophids, which have characteristically small intra- and inter-annual variations in the characteristics amounts of medial relief. of krill taken and also the frequency of occurrence of The length of the otoliths in groups 1 and 2 was measured by other, particularly krill-feeding, taxa in the diet of fur means of a microscope eye-piece graticule, following the method of Williams and McEldowney (1990) and a correction factor was ap- seals. The aim of this study was: (1) to examine the plied to compensate for erosion (10% for group 1 and 20% for inter- and intra-annual variations in the diet of lactat- group 2 based on comparison with intact otoliths). (Reid, in press). ing female Antarctic fur seals during the pup-rearing Total length (TL) and mass (M) of the fish eaten were estimated from period in four consecutive summers at South Georgia; the corrected otolith length (OL) using standard log-linear regres- sion equations (Hecht 1987; Williams and McEldowney 1990; Ada- and (2) to examine the size frequency of prey items in ms and Klages 1987). The proportional frequency distirbution of the diet to determine if any differences exist in the a fish taxon was calculated in terms of absolute frequency (the characteristics of prey taken during years of contrasting number of otoliths of a taxon/total number of otoliths of all taxa prey availability. recovered), the proportional frequency of occurrence (the number of scats containing a taxon/total number of scats containing otoliths) and estimated biomass (the estimated biomass of a taxon/ total calculated biomass of all taxa). Each fish taxon was ranked according to its relative importance in each of these three categories; Materials and methods these ranks were then scored and summed to produce an index of relative importance (see Bigg and Perez 1985). Krill carapaces were All scats were collected on, or in the immediate vicinity of, Fresh- measured using a microscope and eyepiece graticule; krill total water Beach, Bird Island (54°00S, 38°02W) during the austral length was estimated using the general equation for krill whose sex summers of 1990/1991—1993/1994 (since most of these scats were and maturity stage are unknown (Hill 1990). collected during the latter part of the summer, 1990/1991 is referred During January 1993 stomach contents were collected by lavaging to as 1991 etc.). Up to ten scats were collected each week between female fur seals immediately after they came ashore. These samples late December/early January and the end of March, when pups were were processed using the same method as for scats except that the weaned. Each scat was individually bagged and, where immediate maturity stage and sex of up to 50 krill in each sample was assessed processing was not possible, stored frozen (!20°C). Collection of where possible (Makarov and Denys 1981), and the total length of scats was concentrated in areas used predominantly by lactating the krill was calculated using the equations in Hill (1990) for specific female seals and care was taken only to collect whole fresh scats. maturity stage and sex. The scats collected during 1991 and 1992 were broken up in All cephalopod mandibles were identified by Dr. P.G. Rodhouse. a sorting tray containing water and then thoroughly searched for any identifiable prey remains. In 1993 and 1994 this method was modified by suspending the scat in a solution of detergent (1%) and Results disinfectant (1%) in a glass beaker. The scat was gently disinteg- rated, whereupon the differential settling rates of components of the scats allowed denser objects to settle out. The supernatant fluid was Krill was the most frequently occurring prey item, then decanted into a sorting tray and the beaker topped up with occurring in 88% (range across years 71—100%) of scats solution. This process of gentle agitation, partial decanting and containing identifiable remains (n"497), fish occurred re-suspension was continued until no further remains passed over into the sorting tray. The residue in the beaker was then sorted in 47% (range across years 10—67%) and squid in 5% under a binocular microscope (;6). (range across years 0—10%). Krill occurred in 100% Remains of prey items such as fish otoliths and cephalopod of scats in both 1992 and 1993 and in 85% and 71% mandibles were collected for identification and measurement. The in 1991 and 1994 respectively, when there was also the presence of prey remains such as fish vertebrae and eyes, and highest incidence of fish (1991"62%, 1994"67%). cephalopod eyes, from which specific identification is usually impossible, was recorded when no otoliths or mandibles were found. There was a significant difference in the frequency Where present, a sample of up to 20 intact krill carapaces was of occurrence of krill, fish and squid between years " ( collected from the sorting tray for subsequent measurement. (s 73.4, P 0.001). 107

Table 1 The diﬀerence between observed and expected numbers of homogeneous between years. Values are given where the individual each size class of krill in the diet of Antartic fur seals. Based on the chi-square contributed more than 10% of the total chi-square for the Ho that the proportional frequency of krill in ecah size class is year

Year Chi-square Krill length (mm)

34—36 36—38 38—40 40—42 42—44 44—46 46—48 48—50 50—52 52—54 54—56 56—58 58—60 1990/1991 118 94 1991/1992 69 1992/1993 341 !87 !115 64 44 57 1993/1994 647 57 120 107 !107 !78 !62 !51 72 31 1175

Fig. 1 The length-frequency distributions of krill during the early, Georgia mid and later periods of the breeding seasons of 1991—1994 at South

The modal size class of krill taken was 42 mm (range Table 2 Chi-square values for the length-class frequency distribu- 32—66 mm). There were significant differences in the tion of krill in the diet of Antarctic fur seals during the early, mid and length-frequency distribution of krill between years late periods of the breeding season (degrees of freedom are given in " ( parentheses). Based on the Ho that the length-class frequencies of (s 1175.9, P 0.001). Examination of the contri- krill are homogeneous within and between years bution of each year to the chi-square value shows that 1994 contributed 55% of the total variation from ex- Year Early-mid Early-late Mid-late Overall pected (Table 1). The largest differences between observed and expected values for 1994 were in the 34- to 1990/1991 88.7 (13) 155.8 (13) 63.1 (13) 210.8 (26) 1991/1992 23.6 (13) 20.5 (13) 30.7 (13) 52.7 (22) 40-mm range (observed greater than expected), in the 1992/1993 196.2 (11) 156 (11)! 59.7 (11) 336.7 (22) 44- to 50-mm range (observed lower than expected) and 1993/1994 657.3 (13) 992.3 (13) 38.1 (10)! 1185.8 (26) in the 58- to 60-mm range (observed higher than expected). Figure 1 shows the length-frequency distri- ! Values presented had expected counts less than 5 butions of krill during the early (late December/late January), mid (February) and late (March) periods of the summer. The length-frequency distributions for All regurgitated samples contained krill alone, of these three periods show significant differences within which 43% (n"92) were juvenile, 37% (n"79) were " ( " " each year (1991, s 208.1, P 0.001; 1992, s adult female and 20% (n 42) were adult male. There ( " ( 50.1, P 0.001; 1993, s 228.5, P 0.0001; 1994, was no difference in the lengths of krill from the stom- " ( s 1085.8, P 0.0001). The largest difference was ach contents and from scats collected during the same in 1994 when large krill (total length greater than time period when using either the maturity stage and " " 50 mm) predominated in the early part of the season sex-specific equations (F 2.1, P 0.147), or the " " but were almost completely absent in the mid and general equation (F 1.1, P 0.297) to estimate late periods (Table 2). A similar pattern for krill the total length of krill from the stomach samples. greater than 50 mm in length, of abundance in the early period followed by under-representation during the mid and late periods, was seen in 1991, although Fish less pronounced. In the late periods of each year the krill taken were smaller than in the early periods, A total of 2037 otoliths from 21 taxa were recovered with the modal length class of krill in the range during this study, 458 (22%) in 1991, 17 (1%) in 1992, 38—46 mm. 624 (31%) in 1993 and 943 (46%) in 1994. The most 108 numerous taxon overall was Protomyctophum chor- being almost completely replaced by P. choriodon iodon (absolute frequency"37%), followed by Cham- (Fig. 2). Between the sampling dates of 5 February psocephalus gunnari (29%) (Table 3). ¸epidonotothen and 15 March (1991, 1993 and 1994 combined) my- larseni agg. was the only other taxon to contribute ctophids constituted 75% of all fish taken, and 98% more than 10% of the total number of otoliths (24%). of all P. choriodon otoliths were recovered during It was, however, the most frequently occurring taxon this period. In both 1993 and 1994 there was a shift (frequency of occurrence"85%), with C. gunnari back to C. gunnari and ¸. larseni agg. by the end (72%) P. choriodon (53%), Krefftichthys anderssoni of March. (25%) and Gymnoscopelus nicholsi (16%) also making The number of C. gunnari taken increased during the substantial contributions in terms of frequency of period of this study from 22 in 1991 (only 1 in 1992) to occurrence (Table 4). However, only C. gunnari (78%) 167 in 1993 and then 390 in 1994. The length-frequency and ¸. larseni agg. (16%) contributed more than distributions of C. gunnari (Fig. 3) for 1991, 1993 and 10% of the total estimated biomass (Table 5). Despite 1994 indicate that a different element of the fish popula- being the most numerous taxon, P. choriodon contrib- tion was being eaten by seals in 1994. In 1993 there uted only 3% of the estimated biomass. Using the were distinct peaks between 140 and 200 mm, repres- index of relative importance (see Methods), C. gunnari, enting 1-year-old fish, and a smaller peak between 320 ¸. larseni agg. and P. choriodon were shown to be and 400 mm representing 3-year-old and older fish; the the three most important species (in that order) small sample in 1991 all appear to fall within the range (Table 6). of this second peak although there were no 1-year-old A shift occurred in the species composition of fish. In 1994 there was a single peak between 260 and fish taken during February and March of 1991, 1993 360 mm, probably representing 2-year-old fish (Parkes and 1994, with C. gunnari and ¸. larseni agg. 1993).

Table 3 The absolute frequency distribution of ﬁsh taxa in the diet of 1991—1994. The absolute freqeuncy is given as the number of of Antarctic fur seals at South Georgia during the breeding seasons otoliths of a taxon/total number of otoliths of all taxa

Taxa 1991 1992 1993 1994 Total n % n % n % n %%

Myctophidae Electrona antarctica 4 0.9 14 2.2 8 0.8 26 1.3 E. carlsbergi 3 0.7 8 0.8 11 0.5 E. subaspera 1 0.1 1 0.0 Gymnoscopelus braueri 1 0.2 1 0.0 G. fraseri 8 0.8 8 0.4 G. nicholsi 4 0.9 4 23.5 1 0.2 30 3.2 39 1.9 Gymnoscopelus sp. 2 0.2 2 0.1 Kreﬀtichthys anderssoni 22 4.8 36 5.8 20 2.1 78 3.9 Protomyctophum bollni 1 0.2 14 1.5 15 0.7 P. choriodon 262 57.2 245 39.3 245 26.0 752 37.2 P. tenisoni 2 0.4 2 0.1 Myctophiform sp. 7 1.1 13 1.4 22 1.1 Muraenolepidae Muraenolepis microps 1 0.1 1 0.0 Nototheniidae Gobionotothen gibberifrons 1 0.2 1 0.0 ¸epidonoitothen larseni agg. 132 28.8 11 64.7 144 23.1 195 20.7 482 23.8 Notothenidae sp. 4 0.6 4 0.2 Bathydraconidae Parachaenichthys georgianus 4 0.9 4 0.2 Channichthyidae Chaenocephalus aceratus 1 0.2 2 0.3 3 0.1 Champsocephalus gunnari 22 4.8 1 5.9 167 26.8 390 41.4 580 28.7 Pseudochaenichthys georgianus 2 0.3 4 0.4 6 0.3 Gempylidae Paradiplospinus gracillis 1 0.1 1 0.0 Unknown 1 0.2 1 5.9 3 0.3 5 0.2 Total 458 17 624 943 2042 109

Table 4 The proportional frequency of occurrence of the ﬁsh taxa in given as the number of scats containing of a taxon/total number of the diet of Antarctic fur seals at South Georgia during the breeding scats containing otoliths seasons of 1991—1994. The proportional frequency of occurrence is

Taxa 1991 1992 1993 1994 Total f % f % f % f % Total %

Myctophidae Electrona antarctica 1 2.0 5 10.4 3 3.8 9 8.7 E. carlsbergi 2 4.0 4 5.1 6 5.8 E. subaspera 1 1.3 1 1.0 Gymnoscopelus braueri 1 2.1 1 1.0 G. fraseri 3 3.8 3 2.9 G. nicholsi 4 8.0 3 60.0 1 2.1 8 10.3 16 15.5 Gymnoscopelus sp. 2 2.6 2 1.9 Kreﬃchthys anderssoni 9 18.0 10 20.8 7 9.0 26 25.2 Protomyctophum bolini 1 2.1 2 2.6 3 2.9 P. choriodon 19 38.0 16 33.3 20 25.6 55 53.4 P. tenisoni 2 0.4 2 1.9 Myctophiform spp. 2 4.2 5 6.4 7 6.8 Muraenolepidae Muraenolepis microps 1 1.3 1 1.0 Nototheniidae Gobionotothen gibberifrons 1 0 1 1.0 ¸epidonoitothen larseni agg. 29 58.0 1 20.0 24 45.8 36 46.2 88 85.4 Notothenidae spp. 3 6.3 0 0.0 3 2.9 Bathydraconidae Parachaenichthys georgianus 2 4.0 0 0.0 2 1.9 Channichthyidae Chaenocephalus aceratus 1 2.0 2 4.2 0 0.0 3 2.9 Champsocephalus gunnari 10 20.0 1 20.0 19 39.6 44 56.4 74 71.8 Pseudochaenichthys georgianus 1 2.1 2 2.6 3 2.9 Gempylidae Paradiplospinus gracillis 1 1.3 1 1.0 Unknown 1 2.0 1 20.0 3 3.8 5 4.9 Total 50 5 48 78 103

Unlike C. gunnari, the number and length-frequency relatively common in the sub-Antarctic (Rodhouse distribution of P. choriodon were similar between the et al. 1992). years in which it occurred, with the modal length classes for 1991, 1993 and 1994 being in the range 84—86 mm (Fig. 4). The overall length-frequency distribution for ¸. larseni agg. appears to show three Discussion separate age classes (Fig. 5); however, there were marked differences in the size classes taken between One of the major assumptions associated with using years. faecal analysis to study the diet of marine mammals is that prey remains in the faeces appear in the same proportions as they were ingested. In practice, however, Cephalopods selective retention or regurgitation and differential digestion rates of various prey taxa may bias results Squid remains occurred in only 5% of scats (n"24). (Jobling and Breiby 1986). The slow rate of digestion of Fourteen of these samples contained beaks and eyes krill, due to its hard chitinous exoskeleton (Jackson while ten contained only eyes. Of the 14 mandibles and Ryan 1986; Martensson et al. 1994), is one factor recovered, 7 were lower mandibles from which identi- that could introduce biases. In the present study, only fication was possible. The species recorded were the intact krill carapaces were used to estimate krill total squid Alluoroteuthis antarcticus (n"1), Brachioteuthis? lengths, and therefore a systematic bias due to partial picta (n"2), Moroteuthis knipovitchi (n"3) and the digestion is unlikely to occur. In addition, the length octopus Pareledone turgueti (n"1), all of which are distribution of krill from faeces was not significantly 110

Table 5 The proportional estimated biomass of ﬁsh taxa in the diet of 1991—1994. The proportional estimated biomass is given as the of Antarctic fur seals at South Georgia during the breeding seasons estimated biomass of a taxon/total estimated biomass of all taxa

Taxa 1991 1992 1993 1994 Total g % g % g % g % g %

Myctophidae Electrona antarctica 17.6 0.0 41.4 0.2 11.9 0.0 70.9 0.1 E. carlsbergi 40.9 0.1 74.5 0.1 115.4 0.1 E. subaspera 44.0 0.1 44.0 0.0 Gymnoscopelus braueri 8.9 0.0 8.9 0.0 G. fraseri 31.1 0.0 31.1 0.0 G. nicholsi 83.2 0.2 64.7 10.419 8.9 0.0 551.0 0.8 707.8 0.7 Gymnoscopelus sp. 0.0 0.0 Kreﬀtichthys anderssoni 51.5 0.1 81.8 0.4 49.6 0.1 182.9 0.2 Protomyctophum bolni 2.1 0.0 13.4 0.0 15.5 0.0 P. choriodon 872.4 1.6 979.6 5.4 917.6 1.3 2769.6 2.7 P. tenisoni 7.0 0.0 7.0 0.0 Myctophiform spp. 12.4 0.1 12.4 0.0 Muraenolepidae Muraenolepis microps 93.0 0.1 93.0 0.1 Nototheniidae Gobionotothen gibberifrons 470.6 0.9 470.6 0.5 ¸epidonotothen larseni agg. 2809.7 5.2 453.8 73.076 2526.6 14.0 11025.3 15.4 16815.4 16.4 Notothenidae spp. 0.0 0.0 Bathydraconidae Parachaenichthys georgianus 0.0 0.0 Channichthyidae Chaenocephlus aceratus 436.7 0.8 208.5 1.2 645.2 0.6 Champsocephalus gunnari 7267.8 13.3 101.9 16.409 14139.2 78.5 58079.5 81.1 79588.4 77.8 Pseudochaenichtys georgianus 2.0 0.0 711.0 1.0 713.0 0.7 Gempylidae Paradiplospinus gracillis 0.0 0.0 Unknown 0.0 0.0 Total 12050.4 620.5 18011.4 71601.7 102291

Table 6 The composition of the ﬁsh component of the diet of data for 1991—1994). Taxa are arranged according to their relative Antarctic fur seals at South Georgia during the breeding season (all importance

Taxa Number % Frequency % Biomass %

Champsocephalus gunnari 580 28.7 74 71.8 79588.4 77.8 ¸epidonotothen larseni agg. 482 23.8 88 85.4 16815.4 16.4 Protomyctophum choriodon 752 37.2 55 53.4 2769.6 2.7 Gymnoscopelus nicholsi 39 1.9 16 15.5 707.8 0.7 Kreﬀtichthys anderssoni 78 3.9 26 25.2 182.9 0.2 Electrona antarctica 26 1.3 9 8.7 70.9 0.1 E. carlsbergi 11 0.5 6 5.8 115.4 0.1 Pseudochaenichthys georgianus 6 0.3 3 2.9 713.0 0.7 Myctophidae spp. 22 1.1 8 7.8 12.4 0.0 Chaenocephalus aceratus 3 0.1 3 2.9 645.2 0.6 Protomyctophum bolini 15 0.7 3 2.9 15.5 0.0 Gymnoscopelus fraseri 8 0.4 3 2.9 31.1 0.0 Nototheniidae spp. 4 0.2 3 2.9 0.0 0.0 Gobionotothen gibberifrons 1 0.0 1 1.0 470.6 0.5 Muraenolepis microps 1 0.0 2 1.9 93.0 0.1 Parachaenichthys georgianus 4 0.2 1 1.0 0.0 0.0 Gymnoscopelus spp. 2 0.1 1 1.0 0.0 0.0 Electrona subaspera 1 0.0 1 1.0 8.9 0.0 Gymnoscopelus braueri 1 0.0 1 1.0 8.9 0.0 Paradiplospinus gracilis 1 0.0 1 1.0 0.0 0.0 Total 2037 103 102239.83 111

Fig. 2 The percentage composition by number of Champsocephalus combined (1992 contributed less than 1% of all otoliths and is gunnari, ¸epidonotothen larseni agg. and Protomyctophum choriodon therefore excluded). A solid line indicating the frequency of scats in the diet of Antarctic fur seals. Data from 1991, 1993 and 1994 are containing ﬁsh is superimposed

Fig. 3a–c The length-frequency distribution of the icefish Cham- Fig. 4a–c The length-frequency distribution of the myctophid psocephalus gunnari in a 1991, b 1993 and c 1994 (1992 contributed fish Protomyctophum choriodon in a 1991, b 1993 and c 1994 less than 1% of all C. gunnari otoliths and is therefore excluded). (no P. choriodon were recorded in 1992) Note alternative scaling in a 112 occurrence of fish in 1993 compared to 1992 was not related to a difference in the frequency of occurrence of krill, as krill occurred in all scats in both years. This would suggest that, while krill availability is important, it is not the only factor affecting the incidence of fish in the diet. In addition to being the most important prey type, krill may also influence the consumption of other prey taxa. For example, C. gunnari and ¸. larseni agg, the two fish taxa that together make up 94% of the estimated biomass of fish taken, are both krill-feeding fish and are probably taken by seals in the vicinity of krill swarms. Despite being the most important prey type in each year, there were temporal differences in the sizes of krill taken within each year. The length-frequency distributions of krill taken in 1992 and 1993 appeared to show more similarity to each other than with either 1991 or 1994; furthermore, 1991 and 1994 showed more similarity to each other than to either of the other 2 years. In general, years of low or reduced krill availability are defined by the response of krill predators in the absence of an independent measure of krill availability. Since there appear to be similarities in the distribution of krill in 1992 and 1993, both apparently good years for krill Fig. 5a–c The length-frequency distribution of the nototheniid fish predators, and in 1991 and 1994, both poor years for ¸epidonotothen larseni agg. in a 1991, b 1993 and c 1994 (1992 contributed only 2% of ¸. larseni agg. otoliths and is therefore predators, then perhaps the characteristics of the krill excluded) taken can provide additional information about the krill available to predators. The only other krill-feeding predators at South different to that from stomach samples, suggesting that Georgia, for which published data exist on the length- the size of krill estimated from faecal analysis accu- frequency distribution of krill taken at different times rately reflects the size of krill consumed. The use of fish of year, are the baleen whales (Mackintosh 1974). Al- otoliths to estimate the fish component of the diet can though there is a large amount of inter-annual vari- lead to an under-estimate of both frequency and size of ation in the characteristics of krill taken by both baleen fish taken (Dellinger and Trillmich 1988). The amount whales and fur seals, both show a similar overall of partial erosion of otoliths during digestion may well length-frequency distribution, with a major peak be- vary between fish taxa, particularly between pelagic tween 40 and 42 mm and a second smaller peak around fish such as myctophids, which have relatively less 52 to 54 mm (Mackintosh 1974). This suggest that fur dense skeletal structures, and benthic fish such as chan- seals are either selecting particular size classes of krill in nichthyids, where skeletal structures are generally more the same way as baleen whales, although selectivity dense (Eastman 1993). Another limitation of faecal within krill swarms by whales seems unlikely, or that analysis in determining the diet of Antarctic fur seals is both seals and whales are taking whatever krill is that while it is possible to determine the relative pro- available. If this is the case, then the length-frequency portions of fish species in the fish component of the distribution of krill in the diet of fur seals should reflect diet, it is not possible to determine what proportion of the krill available in the South Georgia area at the time the overall diet fish represent. To determine these pro- of sampling. Mackintosh (1974) showed that whales portions requires a quantitative analysis of the diet, take mainly large krill (50—60 mm) in October and using the methods other than faecal analysis. November; during December smaller krill (35—40 mm) As previous studies have indicated (Doidge and begin to appear and then form the major peak of the Croxall 1985; Croxall and Pilcher 1984; North et al. distribution from January to March. Again, assuming 1983; Boyd et al. 1991), krill is the main prey item of whales are not being selective, this should reflect the lactating Antarctic fur seals at South Georgia. In the krill available and could indicate recruitment of smaller present study it was the most common prey type in krill into the South Georgia population during late all 4 years. In 1991 and 1994, when the frequency December and January. of occurrence of krill was reduced, there was the Using the model in Priddle et al. (1988), an absence of highest occurrence of fish, suggesting that at times of these smaller krill [group 3 (mean length, 45 mm) and low or reduced krill availability fish may form an im- group 4 (mean length, 50 mm) in the model] would portant component of the diet. However, the increased result in an 87% reduction in the total biomass of krill. 113 In the present study, the lower-than-expected number to recover otoliths in that season, as the otoliths of this of krill in the range 44—48 mm (group 3) and the size class of fish are very small and were only recovered higher-than-expected number of krill between 36 and under a binocular microscope in 1993 and 1994. The 40 mm (group 2 in the model) suggest that fur seals temporal and biological similarities in the myctophids were taking group 2 krill in the absence of group 3 krill. taken, compared to the variability of C. gunnari and ¸. Thus the predominance of large krill during the early larseni agg., again suggest that the factors influencing part of the lactation period and the absence of group the availability of myctophids are acting independently 3 krill during the mid and late periods of 1994 would of those factors affecting krill and krill-feeding fish. The suggest that the absence of group 3 krill in the South differences in the length-frequency distributions of the Georgia area was a possible cause of the low krill two krill-feeding taxa, C. gunnari and ¸. larseni agg., in availability in 1994. 1994 compared to the preceding years, could result The highly seasonal pattern of consumption of fish from different spatial distributions of fish around South taxa, particularly myctophids, has also been recorded Georgia or from fur seals foraging in different areas as in Antarctic fur seals at Heard Island (Green et al. a result of changes in krill distribution. Since eu- 1989), where it was attributed to changes in the popula- phausiids and myctophids are the commonest prey tion structure of seals ashore. However, in the present items in the diet of Antarctic squid (Kear 1992; Rod- study, no change in the population structure of seals house et al. 1992), squid might be expected to occur ashore occurred during the period in question. regularly in the diet of fur seals. However, the very low Monitoring of adult female foraging behaviour at Bird frequency of occurrence of squid in this study (5%) is Island during the lactation period in all 4 years in- similar to the low incidence in stomach samples (8% in dicated no changing parameters to which the switch to Payne 1977) and confirms the very small contribution different fish taxa could be attributed (Boyd et al. 1994; made by squid to the diet. Only one of the four species BAS unpublished data). It is possible that the period of squid recorded in this study, Alluroteuthis antarc- when myctophids are taken could be attributed to ticus, has not previously been recorded in the diet of oceanographic changes that bring large shoals of Pro- Antarctic fur seals of South Georgia (Reid, in press; tomyctophum choriodon and other myctophids into the Doidge and Croxall 1985). foraging range of female fur seals rearing pups at South This study confirms the importance of krill in the Georgia. Myctophids such as Protomyctophum chor- diet of lactating Antarctic fur seals at South Georgia iodon, and Electrona carlsbergi are associated with the and also suggests that scat analysis is a suitable tool to water of the Antarctic Polar Front (APF) (Sabouren- monitor fur seal diet, from which important informa- kov 1991), the position of which is known to vary tion about the distribution and abundance of this seasonally and under the influence of weather systems patchy prey may be obtained. In addition, the first (Priddle et al. 1988). Dense concentrations of E. car- evidence is presented to show that fish, in particular lsbergi and smaller numbers of Protomyctophum chor- C. gunnari, ¸. larseni agg. and myctophids, are taken in iodon have been found in the southernmost part of the appreciable numbers and there is a distinct seasonality APF, particularly in areas of thermohaline disturbance in the consumption of fish by fur seals during the (Filin et al. 1990). The current level of information on pup-rearing period at South Georgia. The dynamic the factors influencing the distribution and aggregation system governing the availability of prey within the of Protomyctophum choriodon, however, is inadequate foraging range of fur seals, both within years, such as to explain why it should be the most common my- the seasonal occurrence of myctophids, and between ctophid in the summer diet of fur seals. years, such as the variability in abundance and charac- Priddle et al. (1988) suggested that a southerly dis- teristics of krill taken, emphasises the requirement for placement of the APF could be responsible for the diet studies to be conducted over several complete periodic absence of krill from the South Georgia area. breeding seasons. However, despite the difference in the characteristics of krill taken and the varying reproductive success of krill Acknowledgements We would like to thank Drs. I.L. Boyd and predators, in 1991, 1993 and 1994 the pattern of fish J.P. Croxall for their encouragement and invaluable advice during consumption, in particular those fish associated with this study, Dr. I. Everson for his helpful advice, Dr. A.W. North for the APF, was remarkably consistent. In all 3 years the assistance with otolith identification, Dr. P.G. Rodhouse for cephalopod identification and to T.R. Walker for his help in collect- same seasonal switch to myctophids occurred, sugges- ing and sorting scats. Dr. F. Trillmich and an anonymous referee ting that the factors influencing the choice of fish prey provided critical comments on the manuscript. may well be acting independently of the factors affecting krill availability. The length-frequency distributions of Protomyctophum choriodon were similar in each year, References whereas the length-frequency distributions of C. gun- ¸ nari and . larseni agg. were both different in 1994 from Adams NJ, Klages NT (1987) Seasonal variation in the diet of king preceding years. The apparent absence of 1-year-old C. penguin Aptenodytes patagonicus at sub-Antarctic Marion gunnari in 1991 may be an artefact of the method used Island. J Zool London 212:303—324 114

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