Journal of Mammalogy,83(2):370-380, 2002 GEOGRAPHIC VARIATION IN THE SKULL OF THE RINGED SEAL, PUSA HISPIDA MASAO AMANO,* AZUSA HAYANO, AND NOBUYUKIMIYAZAKI Otsuchi Marine Research Center, Ocean Research Institute, The Universityof Tokyo, Otsuchi, Iwate 028-1102, Japan (MA, NM) Departmentof Zoology, GraduateSchool of Science, Kyoto University,Kitashirakawa, Sakyo, Kyoto 606-8502, Japan (AH) A sample of 244 ringed seal (Pusa hispida) skulls from 7 localities was examined mor- phometrically to describe the pattern of geographic variation and to assess subspecies-level taxonomy. Analyses of covariance revealed significant differences among specimens from Lake Saimaa, Lake Ladoga, and other areas. Saimaa seals are robust and short in the skull portion related to feeding, whereas Ladoga seals have narrower skulls and smaller bulla. On scatter plots of canonical discriminant scores obtained using size-free scores, Ladoga and Saimaa specimens were almost separated, but other specimens overlapped and could not be distinguished. Saimaa seals were the most distant, followed by Ladoga seals in the unweighted pair-group method using arithmetic average clustering and neighbor-joining phenograms. These results showed that although ringed seals from Lake Ladoga and Saimaa were considerably differentiated, specimens from other localities were not distinguishable from each other, suggesting similar selection pressure or extensive gene flow especially in the Arctic basin. Further recognition of subspecies for the Arctic seals was not supported. Key words: geographicvariation, Pusa hispida, ringed seals, skull morphometry,subspecies Ringed seals, Pusa hispida, are small ry 1997; Mouchaty et al. 1995; Perry et al. seals adapted to life on ice. They have a 1995). On the basis of these results, Carr circumpolar distribution, which is the larg- and Perry (1997) and Rice (1998) conclud- est range among the northern pinnipeds ed that genus Pusa should be retained, if (Fig. 1), and are the most numerous seals we preserve the widely recognized Hali- in the northern hemisphere (Frost and Low- choerus. ry 1981). They are considered to be the Many subspecies have been described in closest relative to the Baikal (P. sibirica) the ringed seal, including P. hispida hispi- and Caspian (P. caspica) seals (Frost and da, coast of Greenland and Labrador; P. h. Lowry 1981). In the traditional taxonomy beaufortiana, Beaufort Sea; P. h. birulai, these seals were included in genus Phoca northern coast of Siberia; P. h. botnica, (Frost and Lowry 1981; Wozencraft 1993). Baltic Sea; P. h. krascheninikovi, Bering However, recent molecular studies reveal Sea; P. h. ladogensis, Lake Ladoga; P. h. that genus Phoca (sensu lato) includes spe- ochotensis, Okhotsk Sea; P. h. pomororum, cies from 2 distinct clades (tribes Phocinii White Sea and the southern and eastern and Cystophorini) and 3 clades in Phoci- coasts of Barents Sea; P. h. saimensis, Lake nii-Phoca (sensu stricto), Pusa, and Hal- Saimaa; and P. h. soperi, west coast of Baf- fin Island. ichoerus, which are closely related to one another (Arnason et al. 1995; Carr and Per- Although some subspecies descriptions include a comparison of skull morphology, * Correspondent: [email protected] they are based on a small number of spec- 370 May 2002 AMANO ET AL.-GEOGRAPHIC VARIATIONOF RINGED SEALS 371 1601WISO. IW~E 140"E (Frost and Lowry 1981; Rice 1998; Fig. 1). 140-WL However, the overall geographic variation .....E in P. h. hispida and across other subspecies Southern Okhotsk Sea 12 has not been studied. We examined skulls Alaska 95 P. h. ochotensis of ringed seals from several localities IWEthroughout their range to describe the geo- h variation and assess the SP.h. lsp ia graphic validity of gO 6 "~~North+ Pol Russian Arctic 20 subspecies-level taxonomy. MATERIALSAND METHODS <D1 601W LakeSaimaa16 We examined 244 skulls (Appendix I), in- P. h. saimensis skulls collected at Dikson, Russia, in the anadianArctic Lake Ladoga 23 cluding Ph.ladogensis research Western Greenland Japanese-Russian joint expedition pro- Baltic Sea 57 20P' gram for ringed seals in 1995 and now deposited in the National Science Museum, Tokyo, Japan. P..h.-,ica We divided the specimens into 7 geographic 0W_"j 20'W 0. 20'E WE samples: Alaskan coast, eastern area of Cana- dian Arctic, Baltic Lake Lake La- FIG. 1.-Polar view showing geographic rang- Sea, Saimaa, Russian and Okhotsk Sea es of P. hispida subspecies, and localities and doga, Arctic, (Fig. 1). We did not Alaskan into numbers of the specimens used in the present separate specimens those from the Arctic and from the Sea study. Localities of Alaskan and Canadian Arc- Bering because their localities were and Fe- tic specimens are indicated by the hatched area, continuous, doseev and Nazarenko no dif- and Dikson, where Russian Arctic sample was (1970) reported ferences between the and the Arctic obtained, is indicated by a star. Bering seals. Canadian Arctic sample included speci- mens from Baffin Island through the Labrador imens, and intersubspecific differences are coast and also 1 from western Greenland and 1 not clearly addressed (Andersen 1943; Nau- stranded on the Massachusetts coast. We made 30 measurements on each mov and Smirnov 1936; Nordquist 1899; specimen with to the nearest 0.1 mm, Smirnov 1929). On the basis of geographic calipers following Burns et al. (1984; Appendix II; Fig. 2). All separation of the range, King (1964) and specimens were measured by 1 person (M. Ama- Scheffer (1958) reduced the number of sub- no) to avoid interobserver errors. species to 6, lumping Arctic subspecies un- Sample size and size range varied among lo- der P. h. Further hispida. morphological calities. For example, Alaskan samples included of skulls were carried out but comparisons a wide range of specimens from small to large, represented limited geographic sampling. but Okhotsk samples were seriously biased to- Fedoseev and Nazarenko (1970) found no ward smaller seals (Fig. 3). Further, the size of morphological differences between skulls seals varies with ice conditions (e.g., seals that from the Barents and Bering seas, and breed on fast ice, or ice attached to land, tend Youngman (1975) reported no significant to be larger than those that breed on pack ice- differences between skulls from the Beau- McLaren 1958). fort Sea and the eastern Canadian Arctic. Therefore, we used statistical methods that re- duce the effect of size. First, we applied an anal- On the other hand, comparisons among ysis of covariance (ANCOVA) with the common specimens from Lake Saimaa and Lake La- slope model, assuming that slopes for all sam- doga, and those from the Baltic and White ples are the same, using condylobasal length as seas revealed considerable differentiation a covariate and post hoc pairwise comparisons and Nieminen (Hyvairinen 1990; Mtiller- with the Tukey method (Zar 1996). We disre- Wille 1969). Five subspecies, including the garded the differences in slope because slopes Bering Sea P. h. krascheninikovi to P. h. of regression lines should be affected by the bi- hispida, are generally recognized now ased range of the covariate variable. Second, 372 JOURNALOF MAMMALOGY Vol. 83, No. 2 TABLE1.-Summary of descriptive statistics on cranial measurements for geographic samples of P. hispida. Measurements (in mm) are shown as adjusted means of log-transformed values based on ANCOVAs. For measurement numbers and abbreviations, see Fig. 2 and Appendix II. Alaska Canada Measure- Baltic ments n X SD n X SD n X SD 2. PL 94 1.823 0.017 57 1.821 0.017 19 1.815 0.022 3. LUTR 95 1.711 0.014 56 1.706 0.014 19 1.712 0.011 4. GWM 95 1.989 0.013 57 1.999 0.016 19 2.001 0.020 5. GWC 95 1.921 0.015 57 1.924 0.015 19 1.929 0.016 6. ZW 94 1.980 0.014 57 1.983 0.018 19 1.976 0.014 8. LM 79 1.996 0.009 55 1.992 0.010 14 1.993 0.009 9. HMC 82 1.595 0.027 55 1.603 0.026 16 1.588 0.027 10. LLTR 78 1.635 0.018 55 1.626 0.015 14 1.634 0.016 12. LNAS 91 1.541 0.045 56 1.554 0.040 19 1.525 0.038 13. LMFN 92 1.352 0.042 56 1.356 0.038 19 1.341 0.045 14. WNAS 93 0.769 0.072 57 0.787 0.075 19 0.774 0.076 15. WEN 94 1.315 0.024 57 1.325 0.027 18 1.322 0.027 17. IOW 94 0.738 0.076 57 0.835 0.068 19 0.804 0.074 18. LPM 91 0.776 0.040 53 0.795 0.043 19 0.808 0.044 19. WPL 95 1.510 0.023 56 1.524 0.027 19 1.529 0.021 20. WPH 92 1.397 0.029 56 1.397 0.027 19 1.408 0.030 21. WB 93 1.436 0.027 55 1.448 0.021 19 1.463 0.027 22. LB 92 1.538 0.022 57 1.529 0.022 19 1.553 0.018 23. WCD 93 1.722 0.020 57 1.731 0.018 19 1.734 0.021 24. WFM 92 1.465 0.034 57 1.474 0.031 19 1.467 0.042 25. HFM 89 1.357 0.047 55 1.354 0.042 19 1.364 0.043 26. LSN 93 1.340 0.032 57 1.281 0.044 19 1.324 0.041 27. DMP 94 1.257 0.062 56 1.268 0.073 19 1.238 0.064 28.