Antarctic krill Euphausia superba is a predominant species in the Southern Ocean, it is very sensitive to climate change, and it supports large stocks of fishes, seabirds, seals and whales in Antarctic marine ecosystems. Modern krill stocks have been estimated directly by net hauls and acoustic surveys; the historical krill density especially the long-term one in the Southern Ocean, however, is unknown. Here we inferred the relative krill population changes along the West Antarctic Peninsula (WAP) over the 20th century from the trophic level change of Antarctic fur seal Arctocephalus gazella using stable carbon (δ13C) and nitrogen (δ15N) isotopes of archival seal hairs. Since Antarctic fur seals feed preferentially on krill, the variation of δ15N in seal hair indicates a change in the proportion of krill in the seal's diets and thus the krill availability in local seawater. For the past century, enriching fur seal δ15N values indicated decreasing krill availability. This is agreement with direct observation for the past ∼30 years and suggests that the recently documented decline in krill populations began in the early parts of the 20th century. This novel method makes it possible to infer past krill population changes from ancient tissues of krill predators.
Citation: Huang T, Sun L, Stark J, Wang Y, Cheng Z, Yang Q, et al. (2011) Relative Changes in Krill Abundance Inferred from Antarctic Fur Seal. PLoS ONE 6(11): e27331. https://doi.org/10.1371/journal.pone.0027331
Editor: Yan Ropert-Coudert, Institut Pluridisciplinaire Hubert Curien, France
Received: June 30, 2011; Accepted: October 14, 2011; Published: November 7, 2011
Copyright: © 2011 Huang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Funding for this work was provided by the National Natural Science Foundation of China (No. 40730107 and No. 41106162). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Over the past 50 years, the West Antarctic Peninsula (WAP) has experienced rapid regional warming associated with significant sea-ice and krill stock reductions –. More importantly, Antarctic krill is a key species in Southern Ocean food webs that supports large amounts of fishes, seabirds and marine mammals in Antarctic marine ecosystems –. Environmental variability throughout the WAP could lead to cascading trophic level changes , particularly for krill predators such as the Antarctic fur seal. From a predator's perspective, trophic level and dietary change of krill predators is a reflection of relative krill population changes . Therefore, past relative krill abundance, which is difficult to obtain, could be inferred from the paleodiet of krill predators.
Stable isotope analyses of animal tissues are increasingly recognized as a powerful tool for quantifying animal's foraging habitat and trophic level . For example, stable carbon (δ13C) and nitrogen (δ15N) isotope signatures of hair and whisker have been used to infer animal diets , . Keratinous tissues can preserve dietary information for long time periods , particularly in Antarctica, and archival keratinous hairs are ideal material for studying the dietary history of krill predators. Well-preserved hairs and droppings in lake sediments have also been used to infer past populations of seals and penguins –.
In this study, we propose a novel stable isotope methodology for deducing long-term relative krill population dynamics based upon the trophic level of krill predators, and inferred the relative krill population change of the 20th century using the δ15N of Antarctic fur seal hair. Since Antarctic fur seals feed preferentially on krill , and their trophic level (indicated by δ15N) is controlled by their dietary compositions. Therefore, a shift in δ15N of seal hair indicates a change in the proportion of krill in the seal's diet, and such a change should be a reflection of the availability of krill in local seawater.
Materials and Methods
The authors have declared that there is no ethics problem because our samples were extracted from lake sediment.
Sampling area and chronology
Field study was carried out on Fildes Peninsula, King George Island, South Shetland Islands (62°02′S, 58°21′W). The sediment core HN1, 35.5 cm long, was retrieved from a lake catchment near a large fur seal colony. Usually, there are many female fur seals and only one male seal in the colony in summer, and seal remains such as excrements and hairs were shed to the lake and deposited into the sediments. The top 25.5-cm layer of HN1 contains seal excrement and seal hairs and is identified as seal excrement deposition; the section below 25.5 cm is littoral deposition with black basaltic sand. Here we focus on the top 25.5 cm. The chronology of HN1 was established by 137Cs dating on sediments, which was verified as a reliable dating method in previous studies , . Based on the 137Cs signal in sediments, we determined the depth of 15.5 cm corresponds to 1954 AD, the beginning of the 137Cs sedimentation. The 137Cs peaks at depths of 11.5, 8.5, and 4.5 cm correspond to 1965 AD, 1977 AD and 1988 AD, respectively (Fig 1a). The bottom (25.5 cm) of the seal excrement deposition section was inferred corresponds to the early 20th century (approximately 1924 AD), based on the average sedimentation rate in the top 15.5 cm of the core (Fig 1b). These results are described in Yang et al. (2010) . The hairs in the present study from the same sections were assumed to be from the same date.
Stable isotope analyses
HN1 was sectioned at 0.5-cm intervals. Seal hairs were hand picked, cleaned using 2∶1 chloroform: methanol solution, dried at 40°C, and then weighed accurately into tin capsules. Seal hairs were analyzed for δ13C and δ15N by continuous-flow direct combustion and mass spectrometry using a Europa 20/20 SL isotope-ratio mass spectrometer at Utah State University. Precision is ±0.15‰ for δ15N and ±0.10‰ for δ13C. δ15N in sediments were determined by Finnigan-MAT-251 mass spectrometer at Institute of Soil Science, Chinese Academy of Sciences, and the precision is ±0.20‰. Results are presented in δ (‰) and expressed relative to air for δ15N and Vienna Pee Dee Belemnite (VPDB) for δ13C according to the equation: δ (‰) = [(Rsample−Rstandard)/Rstandard] ×103, where δ (‰) represents the δ15N or δ13C value, Rsample is the isotopic ratio of the sample, and Rstandard of the air and VPDB.
The δ13C values of seal hairs range from −22.87‰ to −20.17‰ with a mean of −21.18‰ (Fig 2a) and show equivocal trends (t = −1.196, p = 0.238). The δ15N values of seal excrement sediments range from 7.64‰ to 19.37‰ with a mean of 14.67‰ (Fig 2b). The δ15N values of seal hairs range from 10.26‰ to 11.94‰ with a mean of 11.24‰ (Fig 2c); There is an obvious difference in the rates of change between 1924–1957 and after 1957, that is the amplitude of variation in hair δ15N in 1924–1957 (10.30‰–11.78‰, a 1.48‰ difference) is larger than that in 1958–1997 (11.12‰–11.94‰, a 0.82‰ difference). The δ15N values of sediments are as enriched as 19.37‰, exceeding the normal δ15N values of marine mammals; the abnormally enriched δ15N values of sediments could be the result of large fractionation effects during ammonia volatilization from seal excrement . The δ15N signature in hair, however, is not subject to this fractionation effect because hair is keratinized. The δ15N signatures of both sediments and hairs become significantly enriched over time (sediments: t = 13.47, p<0.001; hairs: t = 11.04, p<0.001). The 1.68‰ enrichment of δ15N in seal hairs indicates an obvious change of fur seal diets over time.
Due to the different metabolic rates of various tissues, stable isotope values reflect trophic levels at different time scales, from days for plasma and excrement to weeks and months for feathers and hairs , . So the stable isotope values in archival hairs in HN1 reflect the average diets of fur seals during summer in their breeding seasons. In the Southern Ocean, δ13C values vary with latitudes and along an inshore/offshore gradient, and typical values for Antarctica fur seal are −23‰ ∼ −19‰ in Antarctica and −19‰ ∼ −16‰ in subantarctica . The depleted δ13C values in HN1 clearly indicate foraging of fur seal in Antarctica during breeding seasons in the study area although we cannot rule out possible inshore/offshore influence.
Fecal analysis showed that Antarctic fur seals in South Shetland Islands feed mainly on krill and various fish species . We estimated the range of δ15N values in seal hair with various percentages of krill vs. fish in seal diet using endmember bulk nitrogen isotope values, and the result shows that seal δ15N becomes enriched as krill proportion in seal diet decreases (Table 1). Krill availability affects predator's foraging behavior. In Scotia Sea, when krill is abundant, seals prey primarily on krill; and when krill is scarce, seals feed on krill and fish . In Ross Sea, Adélie penguins eat more fish when krill availability is low, and vice versa . The recent significant depletion of δ15N in Adélie penguin is ascribed to the ‘krill surplus’ in the Southern Ocean . Dietary change of predators reflects relative abundance of their prey items. Therefore, the δ15N signature in seal hairs is linked to and thus could be used to infer krill availability and population.
The significantly enriching trend of the δ15N signature in HN1 for the last century indicates rising seal trophic levels and decreasing proportion of krill in seal diets, and this strongly suggests that local krill populations could have been in decline since the early 20th century. Two independent evidences support this inference. First, although there are no complete krill density databases for the past century, the decreasing krill stock in this region since 1970 s is well documented  and consistent with our results in overall trend. Second, krill abundance is closely linked with the sea ice extent and duration , , . In this region for the past decades, the sea ice shows a decline trend  (Fig 2d), and this is in coincidence with the decline trend in krill populations  (Fig 2e). Like the seal δ15N values, the sea surface temperature (SST) anomaly in Southern Ocean (50°S) also shows an obvious increasing trend for the 20th century  (Fig 2f), and the significant correlation between them (r2 = 0.82, p<0.001) suggests that the inferred decreasing krill population is linked with warming ocean and declining sea ice extent.
Two other plausible explanations for the enriching δ15N values in the sediment core HN1 could be excluded. First, an enriching baseline (δ15N of the primary producer) may have contributed to the enriching seal δ15N values. The δ15N values of the Southern Ocean primary producer (diatom) are enriched during cold periods and depleted during warm periods . Over the last 50 years, the present study site experienced a rapid air and ocean warming , , and the δ15N values of local primary producer were expected to be depleted. Therefore, the enriching baseline explanation seems unlikely. Second, an increasing intra-specific competition could also have led to the rising trophic level of seal in this study. The seal populations inferred from HN1 show rapid increase between 1955 and 1965 due to the ban of sealing , but the seal δ15N values do not show corresponding ‘rapid’ enrichment, indicating that the intra-specific competition is not responsible for seal dietary changes. Or it is also possible that the increases in seal populations might still have been too low during that time for krill stocks to be limited. Thus, the rising fur seal trophic levels are caused mainly by reduced krill availability and dietary changes.
Krill is the major consumer of diatom primary producers, the major food source for upper trophic predators, and the major fishery resource in the Southern Ocean. Krill density is of critical importance for the apex predator, and its massive biomass underpins the entire Southern Ocean ecosystems. Therefore finding a potential method for inferring krill populations change would be highly beneficial for research and management purposes. We could provide only a single core (HN1) for stable isotope analyses at present due to the limits of logistics. Further core analysis in other areas in Antarctica could be performed in future by international collaborations in field. Nevertheless, the results from HN1 do show that δ15N values in Antarctic fur seal hair can be used as an indicator for seal trophic level changes and the potential relative krill population dynamics. And long-term δ15N series from krill predators could provide vital information about the relative krill abundance in the Holocece epoch and its responses to abrupt or transitional climatic and environmental changes.
We thank the Chinese Arctic and Antarctic Administration and Polar Research Institute of China for support in field, and all the people who provided help in field.
Conceived and designed the experiments: LS. Performed the experiments: TH JS ZC QY. Analyzed the data: LS TH. Wrote the paper: TH LS. Provided help in the data interpretation: YW. Provided insight to the krill ecology: SS.
- 1. Vaughan DG, Marshall GJ, Connolley WM, Parkinson C, Mulvaney R, et al. (2003) Recent rapid climate warming on the Antarctic Peninsula. Climate Change 60: 243–274.
- 2. Ducklow HW, Baker K, Martinson DG, Quetin LB, Ross RM, et al. (2007) Marine pelagic ecosystems: the West Antarctic Peninsula. Philosophical Transactions Royal Society Series B 362: 67–94.
- 3. Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432: 100–103.
- 4. Marr JWS (1962) The natural history and geography of the Antarctic krill (Euphausia superba Dana). Discovery Research 32: 33–464.
- 5. Miller DG, Hampton I (1989) Biology and Ecology of the Antarctic Krill (Euphausia superba Dana): a review. BIOMASS Science Series 9: 1–166.
- 6. Hofmann EE, Murphy EJ (2004) Advection, krill, and Antarctic marine ecosystems. Antarctic Science 16: 487–499.
- 7. Schofield O, Ducklow HW, Martinson DG, Meredith MP, Moline MA, et al. (2010) How Do Polar Marine Ecosystems Respond to Rapid Climate Change? Science 328: 1520–1523.
- 8. Reid K, Watkins JL, Croxall JP, Murphy EJ (1999) Krill population dynamics at South Georgia 1991-1997, based on data from predators and nets. Marine Ecology Progress Series 177: 103–114.
- 9. Hobson KA, Piatt JF, Pitocchelli J (1994) Using Stable Isotopes to Determine Seabird Trophic Relationships. Journal of Animal Ecology 63: 786–798.
- 10. Cerling TE, Wittemyer G, Rasmussen HB, Vollrath Fritz, Cerling CE, et al. (2006) Stable isotopes in elephant hair document migration patterns and diet changes. Proceedings of the National Academy of Sciences USA 103: 371–373.
- 11. Cherel Y, Kernaleguen L, Richard P, Guinet C (2009) Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biology Letter 5: 830–832.
- 12. Hodgson DA, Johnston NM (1997) Inferring seal populations from lake sediments. Nature 387: 30–31.
- 13. Sun LG, Xie ZQ, Zhao JL (2000) Palaeoecology - A 3,000-year record of penguin populations. Nature 407: 858–858.
- 14. Sun LG, Liu XD, Yin XB, Zhu RB, Xie ZQ, et al. (2004) A 1,500-year record of Antarctic seal populations in response to climate change. Polar Biology 27: 495–501.
- 15. Murphy EJ, Watkins JL, Trathan PN, Reid K, Meredith MP, et al. (2007) Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web. Philosophical Transactions Royal Society Series B 362: 113–148.
- 16. Appleby PG, Jones VJ, Ellis-Evans JC (1995) Radiometric dating of lake sediments from Signy Island (maritime Antarctic): evidence of recent climatic change. Journal of Paleolimnology 13: 179–191.
- 17. Yang QC, Sun LG, Kong DM, Huang T, Wang YH (2010) Variation of Antarctic seal population in response to human activities in 20th century. Chinese Science Bulletin 55: 1084–1088.
- 18. Liu XD, Sun LG, Yin XB, Zhu RB (2004) Paleoecological implications of the nitrogen isotope signatures in the sediments amended by Antarctic seal excrements. Progress in Nature Science 14: 786–792.
- 19. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiological and Biochemical Zoology 75: 451–458.
- 20. Casaux R, Baroni A, Carlini A (1998) The diet of the Antarctic fur seal Arctocephalus gazella at Harmony Point, Nelson Island, South Shetland Islands. Polar Biology 20: 424–428.
- 21. Ainley DG, Ballard G, Barton KJ, Karl BJ, Rau GH, et al. (2003) Spatial and temporal variation of diet within a presumed metapopulation of Adelie Penguins. Condor 105: 95–106.
- 22. Emslie SD, Patterson WP (2007) Abrupt recent shift in delta C-13 and delta N-15 values in Adelie penguin eggshell in Antarctica. Proceedings of the National Academy of Sciences USA 104: 11666–11669.
- 23. Loeb V, Siegel V, HolmHansen O, Hewitt R, Fraser W, et al. (1997) Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387: 897–900.
- 24. Nicol S, Pauly T, Bindoff NL, Wright S, Thiele D, et al. (2000) Ocean circulation off east Antarctica affects ecosystem structure and sea-ice extent. Nature 406: 504–507.
- 25. Rayner NA, Parker DE, Horton EB, Folland CK, Alexander LV, et al. (2003) Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. Journal of Geophysical Research 108: NO. D14, 4407.
- 26. Crosta X, Shemesh A (2002) Reconciling down core anticorrelation of diatom carbon and nitrogen isotopic ratios from the Southern Ocean. Paleoceanography 17: 10.1029/2000PA000565.
- 27. Whitehouse MJ, Meredith MP, Rothery P, Atkinson A, Ward P, et al. (2008) Rapid warming of the ocean around South Georgia, Southern Ocean, during the 20th century: Forcings, characteristics and implications for lower trophic levels. Deep-Sea Research Part I 55: 1218–1228.
- 28. Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: Implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences 53: 528–533.
- 29. Cherel Y, Fontaine C, Richard P, Labat JP (2010) Isotopic niches and trophic levels ofmyctophid fishes and their predators in the Southern Ocean. Limnology & Oceanography 55: 324–332.