Polar Biol (2004) 27: 368–373 DOI 10.1007/s00300-004-0598-0
O R I GI N A L P A P E R
Liying Zhao Æ Michael A. Castellini Æ Tamara L. Mau Stephen J. Trumble
Trophic interactions of Antarctic seals as determined by stable isotope signatures
Received: 15 October 2003 / Accepted: 26 January 2004 / Published online: 28 February 2004 Springer-Verlag 2004
Abstract The diets and trophic interactions among Weddell, crabeater, Ross, and leopard seals in the eastern Ross Sea, Antarctica, were investigated by the use of stable isotope techniques during the 1999–2000 summer seasons. The d13C and d15N values in seal serum clearly distinguished the three Antarctic pack-ice seal species at different trophic positions (Weddell>Ross>crabeater). These patterns appeared to reflect a close linkage to their known foraging ecology and diving behaviors, and agreed well with their presumed dietary diversity. The more enriched d13C and d15N values in male Weddell seals than those in females suggested differences in foraging preferences between them. Significant differences in d15N were also found among different age groups of Weddell seals. A strong correlation between the C:N ratios and serum cholesterol was probably due to extremely high cholesterol levels in phocids. Comparisons of isotope data with harbor seals revealed distinct differences between Antarctic phocids and the northern seal species.
Introduction The knowledge of trophic interactions is essential to a better understanding of the foraging ecology of the four phocid species in the Antarctic ecosystem. Dietary diversity has been documented among Weddell (Lepthonychotes weddellii), crabeater (Lobodon carcinophagus), Ross (Omatophoca rossii), and leopard (Hydrurga leptonyx) seals, mostly by direct field observation (Laws
L. Zhao (&) Æ M. A. Castellini Æ T. L. Mau Æ S. J. Trumble Institute of Marine Science, School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, P.O. Box 757220, Fairbanks, AK 99775-7220, USA E-mail:
[email protected] Tel.: +1-907-4745926 Fax: +1-907-4747204
1984; Castellini et al. 1992; Rau et al. 1992). The diet of Weddell seals has been further derived from a combination of scat analyses and stable isotope approaches (Burns et al. 1998). Stable isotope techniques have become a powerful tool in ecosystem studies and have proven very useful in defining trophic relationships and food sources. A stepwise trophic enrichment of 3–5& in d15N has been observed from plants to herbivores to carnivores in all ecosystems (DeNiro and Epstein 1978, 1981; Minagawa and Wada 1984; Michener and Schell 1994). The preferential excretion of 14N via amino acid metabolism and urine nitrogen disposal has made d15N in a consumer’s tissues a natural tracer of both feeding sources and trophic relationships in an ecosystem. In contrast, the relatively conservative transfer of carbon isotope ratios up the trophic ladder allows d13C to be used to distinguish distinct food sources and track the energy flow from the base of ecosystems (Fry and Sherr 1984). This paper presents the carbon and nitrogen stable isotope data from 109 Antarctic seals captured during the 1999–2000 summer seasons, including 41 crabeater, 33 Ross, 33 Weddell and 2 leopard seals. The data indicate that the four species are easily distinguished based on blood isotope patterns. Stable isotope patterns reveal trophic relationships for Weddell, Ross, and crabeater seals that have never been tested in all three species simultaneously and from the same region. Comparisons of isotope data with harbor seals from the northern oceans reveal distinct isotopic differences between the Antarctic phocids and the northern seal species. Moreover, data from Ross seals provide new insights into the biology of this rarely handled species.
Materials and methods Blood samples from four Antarctic phocid species were collected within a 6-week period as part of the National Science Foundation Antarctic Pack Ice Seals (APIS) cruise in the Ross Sea in late 1999 and early 2000. The APIS cruise moved throughout the eastern Ross Sea and into the western Amundsen Sea in a series of
369 transects up to 500 km off shore (Ackley et al. 2003). Seals were observed from the deck of the RVIB Nathanial B. Palmer and captured on the pack ice using either manual restraint or sedation methods. Venous blood samples were collected from the extradural intravertebral vein directly into vacuumed serum collection tubes (Vacutainer) or into syringes for immediate transfer to plain serum tubes (no additive in these tubes), following approved Marine Mammal Protection Act (permit no. 495-1524) and UAF Institutional Animal Care and Use Committee Protocols. The blood samples were returned to the ship, serum separated by clinical centrifugation and then frozen at 80C. The samples were shipped on dry-ice to Fairbanks at the conclusion of the cruise. Blood samples from northern phocids included harbor seals captured in the Gulf of Alaska in 1994, and Atlantic harbor seals captured during a March 2000 field study located in coastal waters of Maine. In both cases, serum was separated immediately after the blood collection and stored at 80C. Serum cholesterol was analyzed at the Sea World San Diego Animal Care Laboratory. Lipid-free serum samples were obtained using an extraction procedure adapted from Bligh and Dyer (1959). Carbon and nitrogen isotope ratios of freeze-dried and homogenized whole serum and lipid-free serum samples were measured with a Europa 20/20 continuous-flow isotope ratio mass spectrometer. Analytical precision of peptone standards was ±0.1& for carbon and ±0.2& for nitrogen. Results are reported using standard d notation in parts per thousand (&) relative to Pee Dee Belemnite (PDB) for d13C and atmospheric N2 for d15N as follows: dX=[(Rsamples/Rstandard) 1]·1000, where dX is d13C or d15N, and R is the ratio of 13C/12C or 15N/14N. Analysis of variance (one-way ANOVA, Tukey-Kramer pairwise comparisons) was conducted to compare the means of carbon and nitrogen isotope ratios among the three seal species and age groups. The leopard seals were excluded from statistical analysis due to the small sample size. Student’s t-test was conducted to compare gender-specific differences. Paired Student’s t-test was used to determine if differences existed in carbon and nitrogen isotope ratios between lipid-free serum and whole serum.
produced three distinct groups for both d13C and d15N (Fig. 2). The highest d13C and d15N values were found in Weddell seals, with intermediate values in Ross seals. Crabeater seals had the lowest d13C and d15N means (ANOVA,F2, 104=88.87, Pcrabeater. The isotope data of two leopard seals overlapped with those of Weddell seals, but the limited number of leopard seal samples did not allow further statistical analysis. Comparisons of isotope data with harbor seals from the Gulf of Alaska and the northern Atlantic revealed significantly different isotopic signatures between the Antarctic phocids and the northern seals (Fig. 3). Intraspecific variations in carbon and nitrogen isotope data were tested in relation to sex and age (Table 1). No age or sex differences in d13C and d15N values existed in crabeater and Ross seals. However, significant differences in d13C (Student t-test, P=0.015) and d15N (Student t-test, P=0.023) were found between male and female Weddell seals. Both d13C and d15N in male Weddell seals were more enriched than those in females,
Results Figure 1 shows the distribution of d13C and d15N values of 109 seals (41 crabeater, 33 Ross, 33 Weddell, and 2 leopard seals). Serum d13C values in crabeater seals spanned a much wider range from 28.60 to 24.54 & than those in Weddell and Ross seals, whereas d15N values were less variable in crabeater seals than in Weddell seals. Statistical analysis of the isotope data
Fig. 1 The d13C and d15N distribution in blood serum of the four Antarctic seal species
Fig. 2 The means±SD of d13C and d15N in blood serum of the four Antarctic seal species
Fig. 3 Comparisons of d13C and d15N values of the four Antarctic seal species with harbor seals captured from the northern oceans
370 Table 1 Summary of carbon and nitrogen isotope ratios (mean±SD) based on sex and age
Species
Sex/Age
No. of samples
d15N (&)
Crabeater
Male Female Adult Subadult Juvenile Pup Male Female Male Female Adult Subadult Juvenile Pup Male/adult
26 15 30 4 3 4 21 12 17 16 22 4 6 1 2
8.18±0.54 8.43±0.44 8.36±0.55 8.38±0.31 7.98±0.08 7.74±0.06 10.59±0.55 9.98±0.52 13.28±0.84 12.46±1.12 13.04±0.92 11.51±1.14 13.11±1.04 13.44 12.27±0.51
Ross Weddell
Leopard
Fig. 4 Comparisons of d13C values between whole and lipid-free serum samples in the three subgroups of Antarctic seal species: upper crabeater; lower Ross and Weddell
implying sex-specific feeding differences. Age-group comparisons among adult, subadult, and juvenile Weddell seals, as well as pups, showed significant differences in d15N between adults and subadults (ANOVA, F3, 29=3.09, PRoss>crabeater seals. The low carbon and nitrogen isotope ratios in Antarctic phocids most likely reflect similar differences in isotope ratios in phytoplankton between the southern and the northern oceans. The intraspecific variations in d13C and d15N values with gender and age indicate the possible differences in feeding ecology. Further studies combining dive records and physiological condition with stable isotope data should allow a better understanding of the foraging and diving behaviors among different sex and age groups. Acknowledgements This research was supported by grant OPP 9815176 from the National Science Foundation to M.A. Castellini. Blood samples from Antarctic seal species were collected under MMPA permit no. 495-1524 with University of Alaska Fairbanks Institutional Animal Care and Use Committee (IACUC) approval. Archived harbor-seal blood samples were collected under EVOS project no. 97001. Blood samples from Atlantic harbor seals were collected under permits issued to G.T. Waring (NMFS-NEFSC)
and J. Gilbert (The University of Maine, Orono). Cholesterol analysis was conducted by Drs. P.K. Yochem and B.S. Stewart.
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