Predicting changes in the Antarctic krill, Euphausia superba, population at South Georgia

Transcription

1 Marine Biology (1999) 135: 647±652 Ó Springer-Verlag 1999 K. Reid á K. E. Barlow á J. P. Croxall á R. I. Taylor Predicting changes in the Antarctic krill, Euphausia superba, population at South Georgia Received: 6 March 1999 / Accepted: 3 September 1999 Abstract Variability in the Southern Ocean is frequently re ected in changes in the abundance of Antarctic krill Euphausia superba and subsequent e ects on dependent predators. However, the nature and consequences of changes in krill population dynamics that accompany uctuations in its abundance are essentially unknown. A conceptual model, developed from quantitative measures of krill length in the diet of predators at South Georgia from 1991 to 1997, allowed predictions to be made about the abundance and population structure of krill in 1998 and the consequences for predators. Consistent with model predictions, in 1998 there was a serial change in krill population structure, low krill biomass and low reproductive performance of predators. The change in the modal size of krill, from 56 mm in December to 42 mm in March, was apparently a result of the transport of krill into the region. This is the rst occasion when the future status and structure of the krill population at South Georgia has been successfully predicted. By representing local krill population dynamics, which may also re ect large-scale physical and biological processes, predators have a potential key role as indicators of environmental variation in the Southern Ocean at a range of spatial scales. Introduction Many aspects of the variability in the Southern Ocean marine system have been described and documented (e.g. Sahrhage 1988). Despite this system having short food Communicated by J.P. Thorpe, Port Erin K. Reid (&) á K.E. Barlow á J.P. Croxall á R.I. Taylor British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, England Fax: 0044 (0) k.reid@bas.ac.uk chains, reduced complexity of trophic interactions and pronounced yet regular seasonality (all nominally contributing to simplicity), the causes and consequences of variability are poorly understood. In reality, variability within the Southern Ocean is exempli ed by a complex set of interactions between large-scale physical and biological processes at a range of scales and trophic levels. Strong direct and indirect e ects of cycles in sea-ice duration and extent on the distribution and abundance of the Antarctic krill Euphausia superba (Loeb et al. 1997) and on the abundance and reproductive performance of dependent predators (Mackintosh 1974; Croxall et al. 1988, 1999; Murphy et al. 1998) have been suggested. At South Georgia, the reproductive performance of a range of marine predators shows a relationship to the abundance of krill, particularly in years when krill is scarce (Croxall et al. 1988, 1999; Boyd et al. 1994). Long-term monitoring of this reproductive performance has provided an indirect method of describing the variability in the local ecosystem (Fraser et al. 1992; Boyd et al. 1994). However, the nature and consequences of changes in krill population dynamics that accompany uctuations in its abundance are essentially unknown. This is primarily because of the di culty of obtaining serial samples of krill at appropriate temporal and spatial scales across a series of consecutive years. Consequently it has been impossible hitherto to make predictions as to the future status and dynamics of krill populations. Reid et al. (1996) showed that krill in the diet of predators provided a reliable and consistent representation of the structure of the krill population at scales of at least 100s of kilometers. Using weekly samples of krill from the diet of the Antarctic fur seal Arctocephalus gazella during the breeding season at South Georgia between 1991 and 1997, Reid et al. (1999) found a consistent pattern of change in the krill population structure, especially during years of low krill abundance, with data from March giving the most consistent and representative comparison between years. Three modal size/age classes of krill (28, 42 and 56 mm) were identi ed, and the presence/absence of each class resulted in changes in the overall mean length of

2 Krill length (mm) 648 krill in the diet of the Antarctic fur seal. We can summarise the data and conclusions of Reid et al. (1999) in terms of a conceptual model based on quantitative measures of krill size (see Fig. 1) as follows: when only the smallest size class of krill is present this is re ected in a mean krill length of 38 mm, as a result of Antarctic fur seals selecting krill from the upper size range in this class. In the following year, these Class 1 krill become Class 2 and are themselves replaced by the incoming Class 1; thus, the overall mean length increases. By the next year the original Class 1 krill have become part of the Class 3 krill (which also includes older krill not separable on the basis of length); the presence of all three classes produces an overall increased mean length of 42 to 46 mm. If there is a failure of the Class 1 krill to enter the population, i.e. only Class 2 and 3 krill are present, then the mean increases to 48 mm. At the beginning of the summer following such a recruitment failure (i.e. a failure of a cohort to enter the population), Class 3 krill are present, Class 2 are absent, and the new incoming Class 1 appear gradually during the course of the summer. By the end of the predator breeding season (March), the new Class 1 krill are the dominant component of the population, resulting in a small overall mean length. Over such a cycle there is a serial change from large to small krill and a resulting overall bimodality in the krill length-frequency distribution. Based on 7 yr data from 1991 to 1997 (Fig. 1), our conceptual model can be used to make a number of predictions about the state and nature of the krill population at South Georgia in We used data on krill population structure, and the reproductive performance of predators from October 1997 to February 1998, together with results from krill biomass surveys in October 1997 and January 1998 to test the following predictions: (1) The length-frequency distribution of krill would change markedly during the summer from krill mostly of a modal length of 56 mm during December/January to krill mainly of a modal length of 42 mm in February/ March; (2) Krill-dependent predators would show poor reproductive performance [based on potentially analogous years in the past, predator indices might be at or below the lower 95% con dence interval of the long-term (20 yr) mean]; (3) The acoustic estimate of krill biomass would be low (i.e the upper 95% con dence interval would be <15 g m )2, as de ned by Brierley et al. 1999). Materials and methods Krill population structure Length-frequency distributions of Euphausia superba were constructed from the diet of Antarctic fur seals (Arctocephalus gazella) and macaroni penguins (Eudyptes chrysolophus) following the methods of Reid et al. (1996), from samples collected weekly over the period December 1997 to March 1998 from Bird Island, South Georgia. The gradual appearance of Class 1 krill during the course of the summer could re ect either resident krill growing into the size range exploited by Antarctic fur seals or an in ux of new krill into their foraging area. Krill of <38 mm are generally not represented in the diet of Antarctic fur seals, although they are taken by macaroni penguins; sampling both species simultaneously reveals the full size range of krill present (Reid et al. 1999). Therefore, resident krill growing into the size range exploited by predators would rst appear in the diet of macaroni penguins and subsequently, after further growth, in the diet of Antarctic fur seals. However, the simultaneous appearance in the diet of both species would indicate an in ux of new krill into the region. Predator performance To assess the reproductive performance of krill-dependent predators, we used parameters which have been measured annually as part of long-term studies of Antarctic fur seals, macaroni penguins, and gentoo penguins (Pygoscelis papua) on Bird Island, South Georgia (Croxall et al. 1988, 1999). Breeding success for fur seals was the number of pups surviving to 6±8 wk of age as a proportion of the total number of pups born; for penguins it was the number of chicks raised to independence per breeding pair. Foraging success was represented by the duration of the foraging trips of Antarctic fur seals, which increases in years of low krill abundance (Boyd et al. 1994; McCa erty et al. 1998) and by the mass of meals delivered to penguin chicks, since penguins maintain feeding Fig. 1 Euphausia superba. Mean length of krill in diet of Antarctic fur seals (Arctocephalus gazella) at South Georgia during March of each year (1991±1997). Right hand graph shows how mean length relates to structure of the population, and should be read from bottom to top (arrows indicate in ux of smallest size class into a population consisting of a maximum of three size classes of krill; dotted arrow with bar across indicates no in ux; see ``Introduction'' for details) Year Krill length (mm)

3 649 frequency at the expense of meal mass in years of low prey availability (Croxall et al. 1999). Krill biomass The British Antarctic Survey conducts annual acoustic surveys of krill density at South Georgia (Brierley et al. 1999), in a 100 km 80 km area to the northwest of South Georgia that lies within the main foraging ranges of lactating female Antarctic fur seals and macaroni penguins breeding at Bird Island (Hunt et al. 1992; Boyd et al. 1998; Trathan et al. 1998). In the 1997/1998 austral summer, acoustic estimates of krill biomass were available from October 1997 and January Results Krill population structure Both species of predator exhibited signi cant di erences in the length-frequency distribution of Euphausia superba taken during December and March (Kolmogorov±Smirnov two-sample test: Antarctic fur seal D max ˆ 0.805, P < 0.01; macaroni penguin D max ˆ 0.836, P < 0.01). The length-frequency distribution of krill in the diet of Antarctic fur seals and macaroni penguins in mid-december had modal sizes of 52 and 56 mm, respectively, with an almost complete absence of krill <44 mm (Fig. 2a). Between early January and early February, the dominant mode changed from 52 to 42 mm in Antarctic fur seals and 56 to 40 mm in macaroni penguins (Fig. 2b). By mid-march, krill of >50 mm represented <5% of the krill taken by either species (Fig. 2c). The mean length of krill taken by Antarctic fur seals in March was 42.3 mm (0.3 SE). Predator performance All but one of the indices of reproductive success were below the 95% con dence limit of the long-term mean in all three species (Fig. 3.) The foraging trips of Antarctic fur seals lasted 157 h (0.9 h SE), 25% more than the long-term (17 yr) average of 118 h (10 h SE); fur seals achieved 72% pup survival compared to a long-term (17 yr) mean of 79% (1.6% SE). The average mass of meals delivered to chicks of macaroni penguin was 292 g (22 g SE), 26% less than the long-term (13 yr) mean of 394 g (41 g SE). However, their breeding success (45%) was very similar to the overall long-term (20 yr) mean of 47% (3% SE). Gentoo penguins delivered meals to chicks of 382 g (36 g SE), 40% less than the long-term (15 yr ) mean of 642 g (62 g SE). They failed to rear any chicks to independence compared to the long-term (20 yr) mean of 40% (5% SE) breeding success. Krill biomass The estimated biomass of krill during October/November 1997 was 1.8 g m )2 (95% con dence interval, CI ˆ 0.7), with a modal size of krill taken in scienti c nets of 46 mm; in January/February 1998 the biomass was 21.4 g m )2 (95% CI ˆ 8.3), with a modal krill size of 36 mm. Discussion The changes in the Euphausia superba population structure in the diet of both predator species, speci cally the progressive switch from 52±56 mm in December to 40±42 mm in March, were highly consistent with the predictions of the model. The simultaneous appearance of the smallest size class of krill in the diet of both predator species, despite the di erence in their size selectivities, suggests that these krill were transported into the South Georgia region. The very low provisioning rate and reproductive output of predators was also consistent with our predictions, especially in the case of Antarctic fur seals and gentoo penguins. As in most earlier years of reduced krill availability, macaroni penguins maintained breeding success by switching their diet from krill to the amphipod Themisto gaudichaudii (Croxall et al. 1999). The upper 95% CI of the acoustic estimate of krill biomass in October (2.5 g m )2 ) was well below the ``low'' threshold of 15 g m )2, consistent with our prediction. Although the upper 95% CI in January (29.7 g m )2 ) was above the threshold, the mean biomass was 54% lower than the long-term mean reported by Brierley et al. (1999). The mean length of krill taken by Antarctic fur seals in March 1998 (Fig. 4) decreased sharply from the 1997 value, a similar situation to that in both 1991 and 1994, when krill abundance was low (Boyd et al. 1994; Brierley and Watkins 1996; Croxall et al. 1999). While there is considerable variability in the krill population structure both within and between years, the greatest changes are consistently associated with periods of low krill abundance (Reid et al. 1999). The ability to predict the nature and consequences of changes in the krill population, especially krill ux into the South Georgia region, is potentially crucial in understanding the responses of predators to environmental variability. However, while we were able to make good predictions over a period of relatively rapid and marked change, it may be more di cult to make predictions for all years. These di culties may be exacerbated by di erences in the timing of sampling of krill and predator populations, and the heterogeneity in the spatial scales that such sampling re ects. It is therefore important that parameters used to examine this relationship integrate variability over similar spatio±temporal scales (Murphy et al. 1988; Rose and Leggett 1990; Boyd 1996). The distinct sequence of change during years of low krill biomass suggests that the period of lowest krill abundance will normally occur in the early part of the summer; thus, predators will be most a ected at the onset of breeding. However, most biomass estimates

4 650

5 651 b Fig. 2 Euphausia superba. Length-frequency distribution in diet of Antarctic fur seals (Arctocephalus gazella) and macaroni penguins (Eudyptes chrysolophus) on Bird Island, South Georgia, during December 1997 (a), weeks beginning 10, 17, 24 and 31 January, and rst two weeks in February (b) and March 1998 (c) come from later in the summer, typically January or February (Brierley et al. 1999) by which time, depending on the timing and magnitude of the incoming year-class of krill, the biomass might well have changed considerably. There are similar problems with the most common index of krill population structure. The proportional recruitment index is the number of krill in the smallest size class as a proportion of the overall population (Siegel and Loeb 1995). However, given the changes observed in the length-frequency distribution of krill during the course of some summers at South Georgia (Reid et al. 1999), the recruitment index could vary by two orders of magnitude between December and March. Comparison of predator reproductive success (which typically integrates a period of several months) with estimates of prey abundance and population structure (which may re ect shorter time periods) may be misleading, particularly in years when conditions change rapidly. Establishing the representativeness of shortterm estimates of prey availability is important not only Fig. 3 Antarctic fur seal (Arctocephalus gazella), macaroni penguin (Eudyptes chrysolophus) and gentoo penguin (Pygoscelis papua). Foraging and reproductive performance at South Georgia between 1976 and Upper and lower 95% con dence intervals for long-term mean are shown for each series (see ``Materials and methods±predator performance'' for de nitions of parameters)

6 Mean krill length (mm) Year Fig. 4 Euphausia superba. Mean length (error bars 1 SE) in diet of Antarctic fur seals (Arctocephalus gazella) at South Georgia during March of each year from 1990 to (Data from 1990 are from limited pilot study that ended in rst week of March) when examining short-term predator/prey interactions but also for long-term, inter-annual comparisons. Differences between annual, near-instantaneous, point measures of prey availability re ect some combination of a large-scale, year-speci c signal as well as small-scale di erences generated by di erences in timing of intraannual processes. Separating these two components may require scaling the point estimates of krill biomass and simultaneous population structure such that subsequent changes in the population structure, determined from serial samples from predators, can be used to model changes in the krill biomass. Developing such a model would reveal the representativeness of point estimates of krill biomass, as well as allowing comparison of predator performance indices with prey availability indices over appropriate timespans. Although there is some evidence that cyclicity in patterns of sea-ice distribution and abundance can e ect krill productivity and recruitment (Siegel and Loeb 1995; Stammerjohn and Smith 1996), there has so far been no attempt to predict future patterns of krill abundance. Our study shows that such predictions are feasible, even though a much better understanding of the relationship between physical and biological processes will be required to extend the predictions for more than one year ahead. While krill in the diets of predators represents local population processes and e ects, these re ect the in uence of larger-scale environmental in uences. Therefore, predators, in addition to re ecting small-scale local process, also have the potential to play a key role as indicators of larger-scale environmental variability. Acknowledgements We thank Professor I.L. Boyd, Dr A.S. Brierley, Dr E.J. Murphy and three anonymous referees for helpful discussion and comments on the manuscript, Dr I.J. Staniland for help in processing Antarctic fur seal diet data, and all of our colleagues who have contributed to the long-term data collection at Bird Island. References Boyd IL (1996) Temporal scales of foraging in a marine predator. Ecology 77: 426±434 Boyd IL, Arnould JPY, Barton T, Croxall JP (1994) Foraging behaviour of Antarctic fur seals during periods of contrasting prey abundance. J Anim Ecol 63: 703±713 Boyd IL, McCa erty DJ, Reid K, Taylor R, Walker TR (1998) Dispersion of male and female Antarctic fur seals Arctocephalus gazella. Can J Fish aquat Sciences 55: 845±852 Brierley AS, Watkins JL (1996) Acoustic targets at South Georgia and the South Orkney Islands during a season of krill scarcity. Mar Ecol Prog Ser 138: 51±61 Brierley AS, Watkins JL, Goss C, Wilkinson MT, Everson I (1999) Acoustic estimates of krill density at South Georgia 1981±1998. CCAMLR Sci (In press) Croxall JP, McCann TS, Prince PA, Rothery P (1988) Reproductive performance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976±1987: implications for Southern Ocean monitoring studies. In: Sahrhage D (ed) Antarctic ocean and resources variability. Springer-Verlag, Berlin, pp 261±285 Croxall JP, Reid K, Prince P (1999) Diet, provisioning and productivity responses of predators to di erences in availability of Antarctic krill. Mar Ecol Prog Ser 177: 115±131 Fraser WR, Trivelpiece WZ, Ainley DG, Trivelpiece SG (1992) Increases in Antarctic penguin populations: reduced competition with whales or a loss of sea ice due to environmental warming? Polar Biol 11: 525±531 Hunt GL, Heinemann D, Everson I (1992) Distributions and predator±prey interactions of macaroni penguins, Antarctic fur seals, and Antarctic krill near Bird Island, South Georgia. Mar Ecol Prog Ser 86: 15±30 Loeb V, Siegel V, Holm-Hansen O, Hewitt R, Fraser W, Trivelpiece W, Trivelpiece S (1997) E ects of sea-ice extent and krill or salp dominance on the Antarctic food-web. Nature, Lond 387: 897±900 Mackintosh NA (1974) Sizes of krill eaten by whales in Antarctica `Discovery' Rep 36: 157±178 McCa erty DJ, Boyd IL, Walker TR, Taylor RI (1998) Foraging responses of Antarctic fur seals to changes in the marine environment. Mar Ecol Prog Ser 166: 285±299 Murphy EJ, Morris DJ, Watkins JL, Priddle J (1988) Scales of interaction between Antarctic krill and the environment. In: Sahrhage D (ed) Antarctic ocean and resources variability. Springer-Verlag, Berlin, pp 120±130 Murphy EJ, Watkins JL, Reid K, Trathan PN, Everson E, Croxall JP, Priddle J, Brandon MA, Brierley AS, Ho mann E (1998) Interannual variability of the South Georgia marine ecosystem: biological and physical sources of variation in the abundance of krill. Fish Oceanogr 7: 381±390 Reid K, Trathan PN, Croxall JP, Hill HJ (1996) Krill caught by predators and nets: di erences between species and techniques. Mar Ecol Prog Ser 140: 13±20 Reid K, Watkins JL, Croxall JP, Murphy EJ (1999) Krill population dynamics at South Georgia 1991±1997, based on data from predators and nets. Mar Ecol Prog Ser 177: 103±114 Rose GA, Leggett WC (1990) The importance of scale to predator± prey spatial correlations: An example of Atlantic shes. Ecology 71: 33±43 Sahrhage D (1988) Antarctic ocean and resources variability. Springer-Verlag, Berlin Siegel V, Loeb V (1995) Recruitment of Antarctic krill Euphausia superba and possible causes for its variability. Mar Ecol Prog Ser 123: 45±56 Stammerjohn SE, Smith RC (1996) Spatial and temporal variability in west Antarctic sea ice coverage. Antarctic Res Ser 70: 81±104 Trathan PN, Croxall JP, Murphy EJ, Everson I (1998) Use of at-sea data to derive potential foraging ranges of macaroni penguins during the breeding season. Mar Ecol Prog Ser 169: 263±275