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- MATERIALS AND METHODS
- LITERATURE CITED
- Supporting Information
Pinnipeds (seals, sea lions, and walruses) underwent a shift in jaw function away from typical carnivoran mastication to more novel marine behaviors during the terrestrial-aquatic transition. Here we test the effect of aquatic prey capture and male-male combat on the morphological evolution of a mammal jaw that does not masticate. Nine three-dimensional landmarks were taken along the mandible for 25 species (N = 83), and corpus and symphysis external and cortical breadths for a subset of five species (N = 33). Principal components analysis was performed on size-corrected landmark data to assess variation in overall jaw morphology across pinnipeds. Corpus breadths were input to a beam model to calculate strength properties and estimated bite force of specific species with contrasting behaviors (filter feeding, suction feeding, grip-and-tear feeding, and male-male combat). Results indicate that, although phylogenetic signal in jaw shape is strong, function is also important in determining morphology. Filter feeders display an elongate symphysis and a long toothrow that may play a role in filtering krill. Grip-and-tear feeders have a long jaw and large estimated bite force relative to non-biting species. However, the largest estimated bite forces were observed in males of male-male combative species, likely due to the high selection pressure associated with male success in highly polygynous species. The suction feeding jaw is weak in biting but has a different morphology in the two suction feeding taxa. In conclusion, familial patterns of pinniped jaw shape due to phylogenetic relatedness have been modified by adaptations to specialized behavior of individual taxa. Anat Rec, 296:1049–1063, 2013. © 2013 Wiley Periodicals, Inc.
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
- Supporting Information
The evolution of pinnipeds from a terrestrial ancestor to a fully aquatic mammal has involved numerous morphological and behavioral adaptations (Adam and Berta, 2002; Berta et al., 2006). While the postcrania have become specialized for swimming, the cranio-mandibular complex has assumed increased importance in prey-acquisition and reproduction, with the development of novel feeding strategies, facial displays and combative behaviors (Adam and Berta, 2002); Jones and Goswami, 2010a). Simultaneously, the role of oral processing of food has decreased, leading to simplification of the dentition and loss of unilateral mastication (Berta et al., 2006). All these factors make pinnipeds a fascinating model for the study of cranio-mandibular functional morphology.
The Pinnipedia is made up of phocids (18 species), otariids (14 species), and odobenids (1 species) that diverged around 33 million years ago (Ma) (Arnason, 2006) and have undergone independent morphological evolution of both the cranium (Jones and Goswami, 2010a) and post-cranium (Berta et al., 2006). Within the Phocidae there are two subfamilies: phocines (10 species) and monachines (8 species) (Higdon, 2007). Phocines split from monachines about 22 Ma ago (Arnason, 2006) and have mostly adopted an ice-breeding habit. Pinnipeds make a particularly interesting mammalian model for testing non-masticatory adaptation of the jaw as they display a wide range of novel behaviors including marine prey-capture and extreme male-male combat. The majority of both phocids and otariids share a generalist “pierce-feeding” technique, catching squid and fish using sharp, homodont teeth, and swallowing them whole (Table 1). Phocid and otariid pierce feeders do not have systematic differences in diet though feeding is opportunistic and may vary depending on the season or locality (Tollit et al., 1998; Dellinger and Trillmich, 1999). However, a number of species have evolved novel prey acquisition methods (Klages and Cockcroft, 1990; Bonner, 1999; Adam and Berta, 2002; Reeves et al., 2002; Berta et al., 2006). Specialized suction feeding on bivalve mollusks is found in both the walrus and in one species of phocid (Erignathus barbatus) (Kastelein, 1994; Adam and Berta, 2002; Marshall, 2008). However, it is utilized to a lesser extent in other species to draw the prey toward the mouth before biting (Klages and Cockcroft, 1990; Marshall, 2013). In the walrus and bearded seal, soft-bodied mollusks are removed from their shells by powerful suction forces (up to 120 mpa in walrus) created by the rapid retraction of the tongue (Kastelein, 1994). A study examining evolution of discrete cranio-dental traits with different feeding strategies related suction feeding to a modified palate and fused mandibular symphysis in odobenids (Adam and Berta, 2002). The crabeater seal (Lobodon carcinophagus) uses filter feeding to extract prey by gulping water then sieving out krill (King, 1961; Klages and Cockcroft, 1990; Berta et al., 2006). Filter feeding has been associated with the unusual shape and positioning (cuspate and interdigitate) of the teeth of L. carcinophagus (Klages and Cockcroft, 1990; Adam and Berta, 2002). Further, qualitative links have been made between filter feeding and elongation of the mandibular symphysis in this species, possibly relating this to modified insertions of the intrinsic tongue muscles (King, 1961). The leopard seal (Hydrurga leptonyx), has two disparate feeding modes (Hocking et al., 2013). It is well known for using its enlarged canines for grip-and-tear feeding, in which it holds large warm-blooded prey such as seal pups and penguins in its sharp teeth then shakes its head violently to rip off pieces of flesh that can be swallowed whole (Adam and Berta, 2002). In captivity, they have also been observed sucking prey into the mouth and using heavily cusped postcanine teeth for filtering, in a similar manner to the crabeater seal. This combination of feeding techniques allows the leopard seal to access a bimodal diet of prey both at the top (large vertebrates) and bottom (krill) of the marine food web (Hocking et al., 2013).
Table 1. Species sampling and ecological information
|Family||Genus||Species||Morph, n||Biomech, n||Prey type||Technique||SSD||Harem size|
|Odobenid||Odobenus||rosmarus||3|| ||Bivalve mollusks||Suctiona||1.52||7.2|
|Phocid||Hydruga||leptonyx||4||7||Vertebrates/crustaceans||Grip and tear/filtera||0.88||1|
Polygyny involving extreme male combat behavior has evolved convergently in both phocid and otariid pinnipeds, and involves males defending their harems through violent clashes in which they rear up and bite each other's head and neck (Bartholomew, 1970; Berta et al., 2006). Included in this group are the elephant seals, in which males are on average six times larger in mass than females, representing amongst the largest known dimorphism in mammals (Reeves et al., 2002; Ferguson, 2006). Female elephant seals also interact aggressively although biting is rarer and less damaging than during male-male combat (Christenson and Le boeuf, 1978). Other pinnipeds are monogamous or display the less violent “resource-defense polygyny” (Berta et al., 2006).
Previous studies (Jones and Goswami, 2010a, 2010b) used three-dimensional geometric morphometrics to assess the influence of phylogeny, ecology, and sexual dimorphism on cranial morphology in a large sample of extant pinnipeds. We showed that pinniped cranial morphology is very strongly influenced by phylogenetic history, with the three pinniped families, Phocidae (seals), Otariidae (fur seals and sea lions), and monospecific Odobenidae (walrus), occupying distinct regions of cranial morphospace. Superimposed on this phylogenetic pattern were possible functional signals relating to modification of the crania for facial displays and feeding behavior. Specifically, the grip-and-tear feeder (H. leptonyx) has a more elongate skull and greater interorbital breadth than other phocids, possibly relating to a more aggressive feeding strategy. Suction feeding (E. barbatus) and sediment feeding (Halichoerus grypus) phocids have broader, flatter snouts with larger nasal openings than most other phocids, which may relate to feeding at the sediment-water interface. Dimorphism of the cranium is very large in species with male facial displays. Male Cystophora cristata have a nasal bladder and Mirounga leonina have a proboscis, and males of both species display an enlarged nasal opening. Otaria byronia exhibits more cranial dimorphism than the other otariids studied.
Here, we apply this same method to the mandible to determine whether similar factors are influencing the evolution of both the cranium and the mandible. The analysis is further extended by assessing biomechanical parameters of the mandibular corpus. Whereas the cranium represents a very functionally complex unit that may be constrained by multiple requirements, including brain protection, sensory perception, and feeding (Cheverud, 1981; Hallgrimsson et al., 2007), the mandible has a direct link to the production of bite force and oral processing of food (Hylander and Johnson, 1994). Many studies have supported this interpretation of the mandible and thus used mandibular morphology to directly infer function (Hylander, 1979; Daegling and Grine, 1991; Biknevicius and Ruff, 1992a; Therrien, 2005b). Hence, when examining the pinniped jaw, more directly assessing its functional capabilities can enrich and refine our interpretation of the purely morphological data. Therefore, the original morphological dataset is augmented with additional biomechanical measures from species characterized by a variety of behaviors involving the jaw. Specifically, measures of strength of the mandibular corpus are calculated using cross-sectional properties and mechanical beam theory (Biknevicius and Ruff, 1992a, 1992b; Therrien, 2005a, 2005b).
Though many previous studies have examined mandibular function using biomechanical beam modeling, the primary emphasis has been on mastication and unilateral biting (Hylander, 1979; Daegling and Grine, 1991). A limited number of studies have considered biomechanical influences resulting from non-masticatory behavior, for example, sanguinivory and roost-excavating in bats (Davis et al., 2010; Santana and Dumont, 2011). Beam model analysis indicated that non-masticatory gouging behavior has not influenced cross-sectional properties of the primate mandible (Vinyard and Ryan, 2006), whereas cross-sectional data from humpback whale jaws indicated that they are optimized for resisting forces involved in lunge feeding in the absence of mastication (Field et al., 2010). Both jaw length and toothrow length are examined using landmark data. Jaw length has previously been related to diet and bite force production in primate taxa (Hylander, 1985; Ravosa, 2000) and gape in carnivores (Greaves, 1985, 2001). Toothrow length is shortened in pinnipeds, possibly relating to a release from the requirement of large bite force at the posterior teeth due to the lack of mastication (Greaves, 1983, 1988; Adam and Berta, 2002), though variation within the pinnipeds has not been examined.
Finally, morphology of the mandibular symphysis will be considered. The nature of the articulation between the two hemimandibles is highly variable in mammals. They may be linked by bone, strong cruciate ligaments, or looser fibrocartilagenous pads (Scapino, 1981). In masticating mammals, a fused symphysis transfers balancing side muscle forces to the working side and tends to be correlated with processing hard foodstuffs (Hylander et al., 2000, 2004; Scott et al., 2012). In primates, symphyses that are deeper superoinferiorly are thought to be strengthened against dorsoventral bending during anterior biting. Whereas, anteroposteriorly long symphyses may be resisting lateral forces during wishboning of the hemimandibles (Hylander, 1988; Daegling, 1989, 2001). These shape changes may be accomplished by both changing dimensions and orientation of the symphysis relative to the long axis of the jaw (Daegling, 1989, 2001). Pinniped symphyses are generally unfused (Adam and Berta, 2002; Scott et al., 2012), but, depending on the nature of stiffness of the joint, shape may still reflect function. An elongate symphysis in L. carcinophagus has been suggested as a filter feeding adaptation (King, 1961); however, very little is known about pinniped symphyses compared to terrestrial carnivores (Scapino, 1981; Scott et al., 2012).
Morphometric data for 25 of 36 extant pinniped species are presented, representing all families and a wide range of ecologies. More detailed biomechanical data were collected for a subset of five of these species. Specifically, two species with male-male combat, an otariid (O. byronia) and a phocid (M. angustirostris) were selected due to their size dimorphism, aggressive behavior and to examine convergent instances of sexual selection (Bartholomew, 1970; Berta et al., 2006; Sanvito et al., 2007). Three species with specialized feeding behavior were also selected. Direct observations of feeding behavior are rare in this group; however, these three species are relatively well studied and have been previously highlighted for their unique feeding behavior in the literature. E. barbatus is one of two highly specialized suction feeding pinnipeds (Marshall, 2008). (The other, the walrus, we were unable to measure because the fused mandibles ruled out X-raying, see below.) H. leptonyx is the only pinniped to feed on large vertebrates using the grip-and-tear technique but also filter feeds, like L. carcinophagus (Hocking et al., 2013). Hence, the species included in this subset were chosen to best encompass the extremes of feeding and reproductive modes found in pinnipeds and to provide additional functional information relevant for understanding these unusual ecologies.
We hypothesize that variation in mandibular morphology between groups will show some similarities to that observed in the cranium (Jones and Goswami, 2010a, 2010b). Specifically:
- There should be strong contrasts between the morphology of the three pinniped families as observed in the cranium. Pierce feeding phocids and otariids may have distinctive morphology reflecting phylogenetic differences, despite strongly overlapping feeding habits. However, the correlation between phylogeny and morphology may be slightly weaker and function might play a larger role in the jaw than in the cranium due to its simpler structure and direct role in feeding.
- H. leptonyx, which has a cranial morphology that diverges from the rest of the phocids, likely due to its grip-and-tear feeding technique, should also show distinctive jaw morphology. Specifically, H. leptonyx should have an enlarged coronoid for attachment of the temporalis muscle to produce a posteriorly directed muscle vector for resisting struggling prey (Smith and Savage, 1959; Weijs, 1980; Greaves, 1995), as well as a large gape for grasping large prey items. We expect morphological evidence of higher bite force production in this species than in those that do not utilize biting to capture prey (suction or filter feeding). Hence, dorsoventral mandibular strength relative to length will be increased in H. leptonyx relative to suction or filter feeders.
- Previous qualitative observations of an elongated mandibular symphysis in L. carcinophagus that has been related to filter feeding will be tested (King, 1961). Since it has been suggested that toothrow length is shortened in pinnipeds, related to the loss of mastication at posterior teeth (Adam and Berta, 2002), the secondary lengthening of the toothrow due to use of the posterior teeth in filtering krill will also be tested.
- Similarities in jaw morphology between phocid and odobenid suction feeders due to their shared feeding ecology will be examined since this pattern is observed in the cranium. Suction feeding relieves the necessity for biting, and so adaptations might include reduced dorsoventral bite force and temporalis muscle attachment size.
- We hypothesize that species using male combat will have more dimorphism in jaw shape than monogamous species, and that combative males will have jaws with large muscle attachment sites. Bite force (relative mandibular corpus strength) dimorphism between males and females will be greater in those species with combative male selection than in those with monogamous strategies.