Variation and Integration of the Simple Mandibular Postcanine Dentition in Two Species of Phocid Seal

Journal of Mammalogy, 88(5):1325–1334, 2007

VARIATION AND INTEGRATION OF THE SIMPLE MANDIBULAR POSTCANINE DENTITION IN TWO SPECIES OF PHOCID SEAL

EDWARD H. MILLER,* HA-CHEOL SUNG,VALERIE D. MOULTON,GARY W. MILLER, J. KERRY FINLEY, AND GARRY B. STENSON Biology Department, Memorial University, St. John’s, Newfoundland and Labrador A1B 3X9, Canada (EHM, H-CS, VDM) LGL Ltd., Environmental Research Associates, 22 Fisher Street, P.O. Box 280, King City, Ontario L7B 1A6, Canada (GWM, JKF) Department of Fisheries and Oceans, P.O. Box 5667, St. John’s, Newfoundland and Labrador A1C 5X1, Canada (GBS) Present address of H-CS: Department of Biology Education, Korean National University of Education, Chungbuk 363-791, Korea Present address of VDM: LGL Ltd., Environmental Research Associates, P.O. Box 13248, Stn. A, St. John’s, Newfoundland and Labrador A1B 4A5, Canada Present address of JKF: Finley Research Associates, 10232 Summerset Place, Sidney, British Columbia V8L 4X2, Canada

Pinnipeds generally swallow prey whole, and most have simple, homodont, nonoccluding cheek teeth. We investigated whether cheek teeth in seals are more variable and weakly integrated than in terrestrial Carnivora. We measured mandibular length and crown length of mandibular postcanines (PCs) in ringed seals (Pusa hispida; n ¼ 912) from the Canadian Arctic, and harp seals (Pagophilus groenlandicus; n ¼ 636) from Newfoundland and Labrador. PC size was uncorrelated or only weakly correlated with adult mandibular length. PC length and mandibular length were strongly bilaterally symmetrical (r 0.8 between left and right sides). PC size was moderately variable (coefficients of variation [CVs] ; 7–10%), and CV varied with position in the toothrow. Adjacent PCs were correlated more strongly in size (to r . 0.8) than PCs more distant from one another. In summary, PC size in ringed and harp seals was slightly more variable than cheek teeth in complex dentitions of fissipeds, and the 2 seals were similar to fissipeds in strong bilateral symmetry in mandibular and PC size, patterned variation along the toothrow, and correlated size between adjacent PCs.

Key words: bilateral symmetry, Canadian Arctic, dental variation, dentition, harp seal, Labrador, morphometrics, Newfoundland, ringed seal

Functional, developmental, and evolutionary interdepen- mastication or tooth sharpening, and is shown morphologically dence of teeth within mammalian dentition has long been in dental orientation, surface features, wear patterns, or size appreciated (Butler 1937, 1939). Tight integration serves (Crompton and Hiiemae 1970; Evans 2005; Every et al. 1998; diverse functions, including food procurement, mastication, Popowics 2003). For example, teeth that interact in occlusion tooth sharpening, or social activities such as fighting or display or mastication, neighboring teeth, and corresponding teeth on (Evans and Sanson 2003, 2006; Every et al. 1998; Ewer 1973). left and right sides often vary little and are morphologically Integration is reflected in specific movements used in complementary and similar in size (Gingerich and Schoeninger 1979; Gingerich and Winkler 1979; Kurteń 1953, 1967; Pengilly 1984; Prevosti and Lamas 2006). Teeth that are not * Correspondent: [email protected] integrated within the dentition for food processing may be Deceased. variably present or variable in morphology or size; examples are the anteriormost premolars of some ursids and m2 Ó 2007 American Society of Mammalogists (lowercase letters signify lower teeth) of Eurasian lynx (Lynx www.mammalogy.org lynx—Kurteń 1953, 1963, 1964; Lanyon and Sanson 2006; 1325 1326 JOURNAL OF MAMMALOGY Vol. 88, No. 5

and Garwood 1969; Tague 1997). Scattered observations suggest that these characteristics apply to the dentition of pinnipeds; for example, supernumerary PCs are fairly common (Odobenidae—Fay 1982; Otariidae—Braunn and Ferigolo 2004; Drehmer et al. 2004; Drehmer and Ferigolo 1996; Tedman 2003; Phocidae—Eastman and Coalson 1974; Ko¨nemann and Van Bree 1997; Stewart and Stewart 1987a; Suzuki et al. 1990). Variation in number of PCs is highest in northern elephant seals (Mirounga angustirostris, .30% of specimens are bilaterally asymmetric—Briggs 1974), and bearded seals (Erignathus barbatus—Chapskii 1955; Manning 1974). How- ever, few supernumerary teeth have been reported in the complex specialized filter-feeding PC dentition of crabeater seals (Lobodon carcinophagus—Adam 2005; Eastman and Coalson 1974). Fine-scale dental variation also has been detailed for several pinniped species (Briggs 1974; Briggs and Morejohn 1976; Burns and Fay 1970; Chapskii 1955; Jernvall 2000; Scheffer 1960; Scheffer and Kraus 1964). Mensural dental variation and the correlation structure of tooth size within the dentition have been investigated in detail for a number of fissipeds and other mammal species (Polly 1998b; Meiri et al. 2005; Szuma 2000). We use those studies as a basis for comparison, while acknowledging fissiped para- phyly and the superficial nature of many differences between pinnipeds and their terrestrial relatives (Bininda-Emonds and FIG.1.—Mandibular postcanines of phocid seals vary in size and Gittleman 2000; Bininda-Emonds et al. 2001). In this paper we complexity: mandibles and lower teeth of some Northern Hemisphere present the 1st analysis of mensural variation in tooth size for phocids (right lateral view). The scale bar is based on a mean mandibular length (as defined in this paper) of 130 mm, for harp seals pinnipeds, based on collections of lower jaws from animals of (Pagophilus groenlandicus) 8 years of age (after Chapskii known sex and age for 2 species of Phocidae that fall within the 1955:162, figure 1). ‘‘pierce-feeding’’ marine mammal guild recognized by Adam and Berta (2002) and Deme´re´ and Berta (2005): ringed seals (Pusa hispida) and harp seals (Pagophilus groenlandicus). Rui and Drehmer 2004; however, nonoccluding teeth occa- Members of the pierce-feeding guild use a piercing bite, with sionally are positively correlated in size—Szuma 2000). Apart prey captured in the mouth and held in place by small sharp from functional requirements operated on by natural selection, teeth. In pinnipeds, this guild is characterized morphologically intraspecific morphological variability in teeth also may reflect by nonoccluding upper and lower cheek teeth with lack of tooth-specific levels of variability or underlying developmental occlusal wear facets, m1 approximately midway along dentary, processes (Evans and Sanson 2003; Gingerich 1974; Jernvall and homodonty with morphologically similar premolars and 2000; Kangas et al. 2004; Pengilly 1984; Polly 1998a). molars (Adams and Berta 2002). Many prey of these species Pinnipeds evolved from carnivores with complex dentition, are small and are swallowed whole; for example, pelagic and the postcanine (hereafter, PC) dentition of pinnipeds amphipods and other crustaceans (particularly by young seals became secondarily simplified in several ways (as in aquatic and adults in parts of the range, e.g., the offshore population of mammals generally), because little preparation of food takes Canadian Arctic ringed seals—Finley et al. 1983) and small place orally aside from holding and puncturing (the widespread fish such as Arctic cod (Boreogadus saida), capelin (Mallotus and generalized phases of shearing and grinding do not occur— villosus), polar cod (Arctogadus glacialis), and sand lance Gingerich 1973): the PC dentition is homodont; PCs do not (Ammodytes species—Chapskii 1955; Frost and Lowry occlude; and PCs are anatomically simple in most species, 1981; Holst et al. 2001; McLaren 1958; Svetocheva 2004; often being just more-or-less pointed for grasping active Vikingsson and Kapel 2000; Wallace and Lawson 1997). How- slippery prey (Adam and Berta 2002; Chapskii 1955; Eastman ever, both species take large prey in some parts of the range and Coalson 1974; Frechkop 1955; Howell 1930; King 1983; or at some seasons (Lowry et al. 1980; Wallace and Lawson Wang et al. 2005). The mandibular PCs of phocids represent p1 1997), and these must require use of the dentition for gripping, to p4 plus m1 (Eastman and Coalson 1974; Meyer and Matzke subduing, or dismembering. Some interspecific differences 2004; Stewart and Stewart 1987b; Stewart et al. 1998; Weber in size and complexity of PCs reflect gross dietary differences, 1928). Secondarily simplified structures often are phenotypi- but the trophic significance of most interspecific variation is cally variable (e.g., in presence, morphology, or size—Dayan unknown (Chapskii 1955; Fig. 1). et al. 2002; Fong et al. 1995; West-Eberhard 2003; Yablokov We hypothesized that lower jaws would be bilaterally 1974) and exhibit weakened morphological integration (Gould symmetrical in size for general functional purposes (Chapskii October 2007 MILLER ET AL.—PHOCID SEAL DENTAL VARIATION 1327

1955), although less so than in fissipeds, and that size of the Most specimens were suitable for measurement, although relatively simple mandibular PCs would be fairly variable and many had been damaged by shooting. The final sample with weaker levels of intercorrelation than the more morpho- contained 520 males and 392 females. Males ranged up to 23 logically complex, functionally integrated PCs of many years in age, and females to 20 years, though the sample of fissipeds and other mammals. males had a slightly lower median age (5.38 versus 6.23 years, respectively). Harp seals.—Seals were shot with high-powered rifles by MATERIALS AND METHODS professional sealers or by employees of the Department of Ringed seals.—Lower jaws (mandibles) were purchased Fisheries and Oceans around the island of Newfoundland in from Inuit hunters in Grise Fiord, Pond Inlet, and Clyde River, September 1994, November 1994–July 1995, and November Nunavut, Canada, from June 1978 to September 1980, by LGL 1995–June 1996. Lower jaws were removed and frozen until Ltd., Environmental Research Associates. Specimens were processing. After thawing, jaws were boiled for about 1 h, and frozen until processing. Jaws were boiled for about 1 h until a canine was removed for ageing, then jaws were cleaned of the canines could be extracted easily by hand, and then were tissue and dried at room temperature. They were measured refrozen. After thawing, jaws were soaked in tap water at room about 1 year later. Variables and measurement protocols temperature for a day or so, until the central PC (i.e., PC3) followed those for ringed seals, except all mandibular PCs could be removed by hand from left and right sides. Jaws then (i.e., PC1–PC5) were available for measurement, and teeth were cleaned of tissue and dried at room temperature. Jaws were not removed from jaws for measurement. We removed were measured approximately 1 year later. Only PC3 was and remeasured 10 teeth 3 times to determine whether the dif- available for study. ferent measurement procedure affected our estimates; measure- The technique of ageing ring seals by counting dentinal ments were identical (all differences , 1%). This results from annuli was described by McLaren (1958) and Smith (1973). the wide spacing of the cheek teeth of seals (unlike terrestrial Thin (0.3-mm) cross sections of both lower canines were cut on Carnivora—Dayan et al. 2002), which permits ready measure- a rotating saw approximately one-third of the distance from the ment of teeth. Some of these specimens were used by Miller root end to the crown. Extracted teeth and the thin sections et al. (1998) and Miller and Burton (2001). were stored in a mixture of equal parts of tap water, absolute As for ringed seals, many specimens had been damaged by ethanol, and 10% glycerin. Tooth sections were examined shooting, so data were not complete for all specimens. The final under transmitted light with a dissecting microscope (magni- sample contained 323 males and 313 females. Males ranged up fication 20–30). Each section was read in blind replicates to 28 years in age and females to 31 years; age distributions until 2 identical readings, or a maximum of 3 readings, were were similar between the sexes and were dominated by young completed. When no 2 readings were identical, the mean of the age classes (median ages 2.80 versus 3.05 years, respectively). 3 readings was calculated and rounded to the nearest integer. Sampling of both species accorded with guidelines of the Seals were aged relative to their month of birth, which was American Society of Mammalogists (Animal Care and Use assumed to be April in the study area. This technique slightly Committee 1998). underestimates age up to about 15 years of age; underestimates can be substantial for seals of that age or older (Stewart et al. 1996). Therefore, data on seals 15 years of age were RESULTS combined. Tooth size in relation to position, sex, age, and jaw size.— Information on body size was not available, so we used The PCs of Pagophilus differed in size according to position in size of the lower jaw as a proxy for body size. Greatest length the toothrow, with PC1 being the smallest, PC2 about 40% (or ‘‘size’’) of the lower jaw (mandible) was measured to larger, and PC3–PC5 about 7% larger again (Table 1; Fig. 2). 0.1 mm with calipers, from the anteriormost point on the jaw to For seals 8 years old, males were ;2–3% larger than females the posteriormost point on the articular condyle. Length of in jaw size in both species, and were relatively larger in PC toothrow was measured (to 0.1 mm) from the anterior margin size: ;8% in male Pusa and 5% in male Pagophilus (Table 1). of the PC1 alveolus to the posterior margin of the PC5 When age classes were pooled, PC3 was ;8% larger for male alveolus. Mesiodistal extent (‘‘length’’ or ‘‘size’’) of PC3 was Pusa and ;3% larger for male Pagophilus. Other PCs of measured in lingual aspect to 0.124 mm, using a dissecting Pagophilus differed less between the sexes: PC2 and PC4 were microscope with an ocular micrometer (measurement precision ;2% larger in males, and PC1 plus PC5 were only ;1% larger reflects the micrometer’s scale). Measurement error was in males. assessed by measuring variables 10 times for 10 seals, blind Jaw length increased in size up to about 8 years of age in and in a random sequence over several days. The coefficient of both species; toothrow length reached an asymptote slightly variation (CV) for these repeated measurements was very small earlier (E. H. Miller, in litt.). In contrast, PC length did not vary (,0.5% for jaw length and ;0% for PC length), so we ignored with age in either sex of either species (slopes in simple linear measurement error in statistical analyses (Bailey and Byrnes regression ranged from positive to negative, all were 1990; Polly 1998b). For analyses, we used mean values of left statistically inseparable from 0, and all had extremely low r2 and right jaws and teeth for complete specimens, unless values [maximum, 3%]). All estimates of r between jaw length indicated otherwise. and PC length were slightly positive but only 1 was significant 1328 JOURNAL OF MAMMALOGY Vol. 88, No. 5

TABLE 1.—Size (mesiodistal length in mm) of mandibular postcanines (PCs) differed between sexes in ringed seals (Pusa hispida) from the Canadian Arctic, and between sexes and with position in the toothrow in harp seals (Pagophilus groenlandicus) from Newfoundland and Labrador. Mean 6 SD are shown with sample size in parentheses. See Fig. 2.

Species and sex PC1 PC2 PC3a PC4 PC5 Ringed seal Males 5.26 6 0.52 (509) Females 4.87 6 0.45 (361) Harp seal Males 4.75 6 0.40 (311) 7.12 6 0.51 (317) 7.74 6 0.50 (319) 7.67 6 0.49 (320) 7.80 6 0.58 (313) Females 4.69 6 0.38 (304) 6.97 6 0.48 (306) 7.55 6 0.53 (306) 7.51 6 0.53 (303) 7.70 6 0.61 (301)

a For seals 8 years old, jaw and PC3 length means were: male Pusa, 103.8 6 5.1 mm (103) and 5.21 6 0.52 mm (167); female Pusa, 102.3 6 4.9 mm (97) and 4.84 6 0.44 mm (161); male Pagophilus, 133.3 6 4.4 mm (19) and 7.80 6 0.49 mm (39); and female Pagophilus, 128.8 6 4.0 mm (29) and 7.43 6 0.60 mm (65).

(for female Pusa 8 years old; r2 ¼ 12%) after a was In Pusa, CVs for length of PC3 (left side, for purposes of corrected for multiple tests (Table 2). Several other relation- exposition) were 9.9% (males) and 9.5% (females). Slightly ships (PC2, PC3, and PC5 of male Pagophilus 8 years old; lower variation occurred across the toothrow of Pagophilus r2 ¼ 20–22%) were signiﬁcant at an uncorrected a ¼ 0.05; (left PC1–PC5): 7.4%, 6.6%, 8.8%, 6.8%, and 7.4% in males; however, these 3 relationships were based on the same sample and 7.4%, 7.4%, 8.4%, 7.1%, and 8.0% in females. In this of males so were not independent of one another. In summary, species, CVs had a fairly small range (6.4–8.9% across all teeth PC size was unrelated to or correlated with mandibular size and between the sexes); nevertheless, teeth in different only very weakly within species. positions had characteristically different levels of variation. Character variation and correlations.—Left and right sides The evidence for this is 2-fold; 1st, CVs of corresponding teeth were similar in size, with bilateral differences within seals on left and right sides within sexes were correlated (males: r ¼ averaging ;2–4% for teeth, ;1% for toothrow length, and 0.988, n ¼ 5, P , 0.002; females: r ¼ 0.978, n ¼ 5, P ¼ ,1% for mandibular length (Table 3). High correlations 0.004). Second, CVs of corresponding teeth in males and between sides also were found for mandibular length (r ¼ females were correlated: r ¼ 0.881 (left teeth only; N ¼ 5, P , 0.995 for Pagophilus and r ¼ 0.944 for Pusa) and PC size 0.05), 0.937 (right teeth only; n ¼ 5, P ¼ 0.02), and 0.906 (all (mean r ¼ 0.876 for Pagophilus and mean r ¼ 0.944 for Pusa; teeth; n ¼ 10, P , 0.001): PC2 varied least (between sexes, Table 3). mean CV ¼ 7.0%); PC1 and PC3 varied most (mean CVs ¼ 8.1% and 8.2%, respectively); and PC4 and PC5 varied at intermediate levels (mean CVs ¼ 7.1% and 7.3%, respectively). The PC size was not correlated with mandibular size in either species (Fig. 3). In Pagophilus, tooth size was correlated most strongly between adjacent PCs, and strength of correlations weakened with the distance between teeth (Table 4; Fig. 4). In both sexes, PC3 size was correlated most strongly with size of adjacent teeth, and PC1 size was correlated most weakly with size of other teeth.

DISCUSSION Tooth size in relation to position, sex, age, and jaw size.— The PC size varied with position in the toothrow in the harp seal, with PC3 being (slightly) the largest tooth, as in the ringed seal (Belobdorov 1975; Chapskii 1955; Doutt 1942). Size ordering of PCs is ubiquitous in pinnipeds (e.g., Phocidae— Briggs and Morejohn 1976; Burns and Fay 1970; Doutt 1942; Scheffer 1960). Sexual size differences in pinnipeds have been investigated extensively (mainly in relation to social systems), but most analyses pertain to overall body size (Alexander et al. 1979; Lindenfors et al. 2002). Yablokov and Sergeant (1963) quantiﬁed

FIG.2.—Size (mesiodistal length) of mandibular postcanines varied cranial sexual size differences in adult harp seals similar to levels with position in the toothrow and between sexes in harp seals we observed: ;5% in mandibular length and ;7% in distance (Pagophilus groenlandicus) from Newfoundland and Labrador. between PC5 and anterior extreme of cranium or mandible Mean 6 95% conﬁdence intervals (¼ 61.96 SE) are shown. (Yablokov and Sergeant 1963:1859–1860, tables 1 and 2). October 2007 MILLER ET AL.—PHOCID SEAL DENTAL VARIATION 1329

TABLE 2.—Size (mesiodistal length in mm) of mandibular postcanines did not vary with mandibular length in ringed seals (Pusa hispida) 8 years old from the Canadian Arctic, or harp seals (Pagophilus groenlandicus) 8 years old from Newfoundland and Labrador. Values for Pearson’s product-moment correlation coefficient (r) are shown; P (uncorrected) and sample size are given in parentheses. Significant correlations at an uncorrected significance level of a ¼ 0.05 are in bold (following Sidak’s correction to a ¼ 0.05 for multiple tests [2 for ringed seal and 5 for each sex of harp seal]; only the value for female ringed seals was significant).

Species and sex PC1 PC2 PC3 PC4 PC5 Ringed seal Males 0.119 (0.23; 102) Females 0.343 (0.001; 89) Harp seal Males 0.042 (0.86; 21) 0.448 (0.04; 21) 0.468 (0.03; 21) 0.221 (0.35; 20) 0.468 (0.04; 20) Females 0.107 (0.59; 28) 0.038 (0.85; 29) 0.130 (0.50; 29) 0.084 (0.67; 28) 0.122 (0.54; 28)

Ringed seals show extensive ecogeographic variation in size and were ;9–10% in ringed seal and ;7–9% in harp seal, very sexual size differences (Amano et al. 2002; Fedoseev 1975; close to estimates for M2 of the polar bear (Ursus maritimus)— Finley et al. 1983; Hyva¨rinen and Nieminen 1990; McLaren a reduced structure in this species that would be expected to be 1993; Reeves 1998), so we do not discuss our limited findings more variable than in other bears (CVs ¼ 7.2–9.6%—Kurteń further, aside from suggesting that the apparently greater sexual 1964). Reported values for carnassials in other fissipeds size difference in PC3 than mandibular length merits further invariably are lower than those values. Some examples of study. CVs for P4 and m1 (respectively) are 4.7% and 4.3–4.8% for The PC toothrow lengthens substantially with age in red foxes (Vulpes vulpes—Szuma 2000, 2003); 4.1% and 4.3% phocids, because PCs are crowded in young animals and for Arctic foxes (Vulpes lagopus—Pengilly 1984); 6.4% and become less crowded with growth (Belkin et al. 1969; Doutt 5.1% for cave bears (Ursus spelaeus—Baryshnikov et al. 2003; 1942; Harington and Sergeant 1972; Ooe and Esaka 1981); computed from weighted means of data in their tables 3 and 4); however, PC size does not change with age because of wear and 6.1% and 5.4% for Eurasian badgers (Meles meles— after full eruption of the crown in ringed or harp seals. Baryshnikov et al. 2002; computed for ‘‘cluster 1’’ in their Therefore, sample size can be increased in future studies by tables 4 and 5). Other cheek teeth are similarly or slightly more pooling samples across ages within sexes. In ringed seals, other variable (Kurteń 1964; Wolsan et al. 1985). Similarly low measurement variables on PC3 decline with age, indicating wear over time (E. H. Miller, in litt.). Tooth wear, breakage, and associated problems occur in all pinniped species but with different patterns, according to diet, intraspecific strife, and TABLE 3.—Size (mesiodistal length in mm) of mandibular postcanines and mandibular length were similar, and were closely other factors (Braunn and Ferigolo 2004; Chapskii 1955; correlated between right and left sides in ringed seals (Pusa hispida) Drehmer and Ferigolo 1996; Fay 1982; Stirling 1969). from the Canadian Arctic and harp seals (Pagophilus groenlandicus) Tooth size has been used widely to predict body size from Newfoundland and Labrador. Values for percent left–right interspecifically, especially in paleobiology (Creighton 1980; differencesa are shown as mean 6 SD and (below), Pearson’s product- Gingerich et al. 1982; Pan and Oxnard 2003; Van Valkenburgh moment correlation coefficient (r) between left- and right-side 1990). Some significant intraspecific correlations between size measurements (sample size is given in parentheses). All correlations of lower cheek teeth and cranial or mandibular size also have were highly significant (P , 0.001). been reported for terrestrial Carnivora (Kurteń 1953, 1967; Meiri et al. 2005). Significant relationships occur in other taxa, Ringed seal Harp seal including rodents and primates (Dayan et al. 2002; Gould and Variable Male Female Male Female Garwood 1969; Moyer et al. 1985; Olson and Miller 1958), but Jaw length 0.71 6 0.55 0.57 6 0.49 0.74 6 0.65 0.79 6 0.64 are not universal even within Carnivora (e.g., brown bear 0.991 (160) 0.994 (109) 0.995 (50) 0.995 (70) [Ursus arctos]—Kurteń 1953; jaguar [Panthera onca]—Turner Toothrow length 1.3 6 1.9 1.2 6 1.0 1.2 6 1.1 1.0 6 0.91 and O’Regan 2002), and we detected little or no relationship of 0.983 (370) 0.960 (306) 0.982 (152) 0.986 (172) PC1 length 4.0 6 3.4 4.3 6 3.8 tooth size to mandibular size in our study. 0.821 (290) 0.772 (286) Character variation.—Carnassial dentition has evolved PC2 length 2.8 6 2.3 3.2 6 2.9 independently several times in mammals (Butler 1946). In 0.883 (300) 0.828 (299) Carnivora, carnassial teeth are P4 (uppercase letters signify PC3 length 2.2 6 2.4 2.3 6 2.6 2.6 6 2.2 2.5 6 2.4 upper teeth) and m1, and these have been reported to vary little 0.950 (449) 0.937 (323) 0.883 (289) 0.894 (292) PC4 length 2.1 6 1.8 2.4 6 2.2 intraspecifically in species with complex dentition, presumably 0.920 (292) 0.905 (285) because of high morphological complexity related to precise PC5 length 2.5 6 2.1 2.7 6 2.2 integrated functions in food processing. Hence, CV estimates 0.931 (282) 0.918 (275) for mesiodistal length in carnassials provide a basis for a Percent difference between left (L) and right (R) sides computed per specimen as comparison with our results. In our study, CVs for PC size 100(L R)/[2(L þ R)]. 1330 JOURNAL OF MAMMALOGY Vol. 88, No. 5

FIG.3.—Size (mesiodistal length) of the central lower postcanine tooth (PC3) was not correlated with mandibular size (length) in ringed seals (Pusa hispida) from the Canadian Arctic or harp seals (Pagophilus groenlandicus) from Newfoundland and Labrador. The 95% confidence ellipses are shown for specimens of all ages (for data on seals 8 years old; see Table 2). levels of variation characterize complex cheek teeth in other 0.98) for mandibular length and toothrow length; r was 0.77– fissipeds as well as primates (Gingerich 1974; Polly 1998b). 0.95 for PCs. In the complex dentition of pine martens (Martes High variation in dental traits has been related to martes), r between linear dental measurements on left and right evolutionary factors and processes other than the weakening sides was similarly high, averaging 0.88 (maximum, 0.92— of stabilizing selection, including directional selection and Wolsan et al. 1985). geographic isolation of small populations (Juste and Ibań˜ez We predicted relatively weak size correlations among teeth, 1993; Tomow et al. 2006). We interpret high CVs for PC size but again our estimates were fairly high (e.g., for Pagophilus, in ringed and harp seals to indicate increased variation due to r averaged ;0.60 with maxima . 0.82). These values are evolutionary simplification of morphology via selective release, surprisingly similar to some for lower cheek teeth of fissipeds; in connection with evolution from complex specialized to for example, r averaged 0.57–0.65 (maxima, 0.81–0.87) for simple generalized food-processing (Adam and Berta 2002; mesiodistal tooth lengths in several studies on red foxes Briggs 1974; Chapskii 1955; Gould and Garwood 1969). (Szuma 2003), and 0.47 (maximum, 0.78) for the same Character correlations.—Close functional relationships variables in Arctic foxes (Pengilly 1984). Correlations are between neighboring or occluding teeth, or between corre- similar or weaker in other mammals with complex integrated sponding teeth on left or right sides, are reflected in dentitions (cuscuses [Ailurops ursinus]—Kurteń 1953; wild complementary size and morphology (Gould and Garwood house mice [Mus musculus]—Wallace 1968; and white-footed 1969; Kurteń 1953, 1967; Prevosti and Lamas 2006). High mice [Peromyscus leucopus]—Van Valen 1962). bilateral symmetry is expressed jointly through similarity in We conclude that evolutionary simplification of the PC size and high correlations, and we found both in our study. dentition of ringed and harp seals was not accompanied by Similarity in size between left- and right-side measurements marked weakening of bilateral asymmetry or of size correla- was strong overall, but particularly for mandibular length (left– tions among mandibular PCs. Our observations may be ex- right differences averaged ,1%) and toothrow length (differ- plained by evolutionarily conserved developmental programs ences ;1%); differences averaged ;2–4% for PCs. Similarly, for mammalian dentition (Butler 1937, 1939, 1946; Kangas bilateral correlations were high overall but especially (r . et al. 2004). Other observations that support this possibility for

TABLE 4.—Size (mesiodistal length in mm) of mandibular postcanines (PCs) was correlated most strongly between PCs closest to one another, in both sexes of harp seals (Pagophilus groenlandicus) from Newfoundland and Labrador (see Fig. 3). Estimates for Pearson’s product-moment correlation coefﬁcient (r; using means of left and right PC measurements) are shown (sample size is given in parentheses; males above diagonal, females below diagonal). All correlations were highly signiﬁcant (P , 0.0001).

PC1 PC2 PC3 PC4 PC5 PC1 0.557 (310) 0.464 (309) 0.470 (310) 0.346 (305) PC2 0.549 (304) 0.789 (316) 0.677 (316) 0.479 (310) PC3 0.453 (303) 0.758 (305) 0.821 (318) 0.590 (311) PC4 0.447 (300) 0.696 (302) 0.855 (303) 0.632 (312) PC5 0.426 (298) 0.488 (300) 0.590 (301) 0.661 (299) October 2007 MILLER ET AL.—PHOCID SEAL DENTAL VARIATION 1331

FIG.4.—Size (mesiodistal length) of postcanine teeth was correlated most strongly between adjacent teeth, and declined with distance between teeth, in harp seals (Pagophilus groenlandicus) from Newfoundland and Labrador (see Table 4). pinnipeds concern the nature of dental variation, which can be was the driving force behind this program; R. Davis and B. Koski high but is bounded. For example, occasionally teeth of ribbon managed the project on behalf of LGL Ltd., Environmental Research seals (Histriophoca fasciata) are indistinguishable from those Associates. G. Glazier, G. Koening, W. Speller, and B. Veldhoen of of ringed or harp seals, or common seals (Phoca vitulina— Petro-Canada gave invaluable assistance and support to the work. The Burns and Fay 1970). Furthermore, dental variants often are study could not have been accomplished without the assistance of Pond Inlet hunters, particularly P. Aglak. G. Sleno of the former expressed bilaterally in ribbon seals and in otariids (Drehmer Department of Fisheries and Oceans Arctic Biological Station (Ste. et al. 2004; Tedman 2003). Other observations along these Anne de Bellevue, Quebec, Canada) assisted in preparation of tooth lines are reported by Bateson (1894), Briggs (1974), Briggs and sections of ringed seals. Collections of harp seals were made as part of Morejohn (1976), Burns and Fay (1970), Chapskii (1955), the research program of the Marine Mammal Section, Department of Drehmer et al. (2004), Fay (1982), Ko¨nemann and Van Bree Fisheries and Oceans (St. John’s, Newfoundland and Labrador, (1997), and Scheffer and Kraus (1964). Canada); we thank D. Wakeham and D. McKinnon for dissecting Concluding comments.—Quantitative aspects of variation out harp seal jaws, extracting teeth, and entering data, and W. Penney and integration of pinniped dentition have not been reported for ageing teeth. A. Beltane, L. Burton, J. Hamilton, J. Hinchey, and previously. Compared with complex cheek teeth of most A. Hussey helped to clean and organize specimens and data. For ﬁssiped carnivores, PCs of ringed and harp seals express commenting on manuscript drafts, we thank P. J. Adam (Department slightly higher variation in size, but similar levels and patterns of Ecology and Evolutionary Biology, University of California Los Angeles), C. J. Drehmer (Universidade Federal de Pelotas, Pelotas, of size correlations and bilateral symmetry. Whether the same Brazil), J. M. Lawson (Department of Fisheries and Oceans, St. patterns occur in other pinnipeds is an open question, because John’s), and W. J. Richardson (LGL Ltd., Environmental Research no other studies have been conducted. Yet PCs of phocids, in Associates). Financial support speciﬁcally for costs related to this particular, vary greatly across species in size, morphology, research project was provided to EHM by York University (Toronto, and spacing (Bininda-Emonds and Russell 1996; Burns and Ontario, Canada), Memorial University, and the Natural Sciences and Fay 1970; Chapskii 1955; Doutt 1942; Eastman and Coalson Engineering Research Council (Discovery Grant to EHM). 1974; King 1983; Fig. 1). Cranial and masticatory anatomy of phocids varies in relation to diet (Endo et al. 1998a, 1998b, LITERATURE CITED 2002; Howell 1929; King 1972; Kosygin and Shustov 1971), ADAM, P. J. 2005. Lobodon carcinophaga. Mammalian Species and geographic variation in PCs and mandibles is known 772:1–14. (Chapskii 1955; Doutt 1942). Therefore, this group seems to ADAM, P. J., AND A. BERTA. 2002. Evolution of prey capture strategies and provide many opportunities for morphometric studies, to com- diet in Pinnipedimorpha (Mammalia, Carnivora). Oryctos 4:83–107. plement the extensive work that has been carried out on ter- ALEXANDER, R. D., J. L. HOOGLAND,R.D.HOWARD,K.M.NOONAN, restrial Carnivora. AND P. W. SHERMAN. 1979. Sexual dimorphism and breeding systems in pinnipeds, ungulates, primates and humans. Pp. 402–435 in Evolutionary biology and human social behavior: an anthropo- ACKNOWLEDGMENTS logical perspective (N. Chagnon and W. Irons, eds.). Duxbury, Research on ringed seals was funded by Petro-Canada Explorations North Scituate, Massachusetts. Inc. (Calgary, Alberta, Canada) as part of the Eastern Arctic Marine AMANO, M., A. HAYANO, AND N. MIYAZAKI. 2002. Geographic Environmental Studies research program. N. Snow (then of De- variation in the skull of the ringed seal, Pusa hispida. Journal of partment of Indian and Northern Affairs, Ottawa, Ontario, Canada) Mammalogy 83:370–380. 1332 JOURNAL OF MAMMALOGY Vol. 88, No. 5

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