Cranial ontogeny in Steller sea lions: Relationships between cranial morphology and suction feeding

Cranial ontogeny in Steller sea lions: Relationships between cranial morphology and suction feeding | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Cranial ontogeny in Steller sea lions: Relationships between cranial morphology and suction feeding Ryunosuke Yuge, Yumi Kobayashi, Takeomi Isono, Orio Yamamura This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3872222/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Suction feeding is a specific behavior in pinnipeds such as the Steller sea lion ( Eumetopias jubatus ), whereas the phylogenetically related brown bear ( Ursus arctos ) ingests by masticatory feeding. Because these feeding modes use different organs, the morphology and ontogeny of the cranial bones of these species may be related to differences in their feeding behavior. In this study, we performed multiple regression analyses to compare the ontogeny of Steller sea lion and brown bear cranial morphology by species and sex, using age, species, and the age × species interaction as explanatory variables and site measurements standardized by cranial length as response variables. The results showed that the palatine bone in both sexes widened with age in Steller sea lions compared to brown bears, whereas the width of the zygomatic arch was less developed in female Steller sea lions than in brown bears. This result may reflect the fact that the masticatory muscles are used less during suction feeding, whereas the tongue is used to perform force-intensive tasks. These results are consistent with previous studies on Carnivora and suggest that the development of the palatine bone and underdevelopment of the zygomatic arch represent characteristics of suction feeding. Figures Figure 1 Figure 2 Figure 3 Figure 4 Introduction Cranial morphology can reveal the ecological characteristics of an animal from various perspectives (Dumont et al. 2009 ; Roston and Roth 2019 ; Santana et al. 2012 ), including muscles and sensory organs (Hanken and Hall 1993 ). The cranium also reflects behavioral characteristics, particularly related to feeding. For example, dolphins feed by swallowing whole prey, whereas terrestrial carnivores chew their food. Therefore, the masticatory muscles of dolphins are less developed than those of terrestrial carnivores, and the zygomatic bone containing the masticatory muscles is thin (Wuersig et al. 2017 ). Furthermore, because the noses of dolphins are located on the top of their heads for efficient breathing, the anterior maxillary bone extends over the head, whereas the nose of a terrestrial carnivore is located at the tip of the rostrum (Roston and Roth 2019 ). Cranial morphology changes with age, representing ontogenetic changes in the ecological characteristics of animals (Abdala et al. 2001 ; Brunner et al. 2004 ; Flores et al. 2010 ; Giannini et al. 2010 ). Cranial ontogeny in terrestrial carnivores reflects increasing dependence on masticatory feeding with growth (Giannini et al. 2010 ; Segura and Prevosti 2012 ; Tanner et al. 2010 ). In terrestrial carnivores, the zygomatic bone develops significantly with age, and the width of the palatal bone relative to cranial length decreases with age. The zygomatic bone houses the masticatory muscles and the palatal bone houses the tongue, and the developmental pattern of these bones represents the development of the respective muscles. Among mammals, pups suckle the mother’s milk until weaning, when they begin to chew food using their masticatory muscles. Terrestrial animals use their tongues for suckling during breastfeeding (Bosma et al. 1990 ; German et al. 1992 ), but do not use them for force-intensive tasks during chewing and feeding (Crompton 1989 ; Liu et al. 2008 ). Therefore, the development of the zygomatic bone and underdevelopment of the palate bone observed in terrestrial carnivores indicate masticatory feeding. Whereas terrestrial carnivores generally feed primarily by mastication, some pinnipeds exhibit a unique feeding mode called suction feeding (Hocking et al. 2015 ). Based on their cranial morphology, various pinnipeds suction feed, in which underwater prey is sucked into the mouth by negative pressure (Adam and Berta 2002 ). Suction feeding uses an organ system different from that used for masticatory feeding. The tongue is pulled back into the throat to create negative pressure in the oral cavity, which is used to suck in food (Bloodworth and Marshall 2005 ; Kane and Marshall 2009 ; Marshall et al. 2008 , 2014 , 2015 ). Thus, the ontogeny of cranial morphology in pinnipeds is expected to be substantially different from that of terrestrial carnivores. Studying the ontogeny of cranial morphology in pinnipeds would provide an opportunity to understand the relationship between suction feeding and cranial morphology, which is unique to marine mammals. Previous studies on the cranial morphology of carnivores have included pinnipeds (Brunner et al. 2004 ; Isono 1998 ; Tarnawski et al. 2014b , 2014a , 2015 ); however, few have mentioned feeding behavior (e.g., Tarnawski et al. 2015 ). Because these studies employed different methods to assess cranial ontogeny, including bivariate and multivariate analyses, it is impossible to compare cranial ontogeny between terrestrial carnivores and pinnipeds. Therefore, in this study, the cranial ontogeny of pinnipeds and terrestrial carnivores were compared using the same method. As the pinniped species, we examined the Steller sea lion Eumetopias jubatus , which is among the few species whose suction feeding has been confirmed in an experimental setting (Marshall et al. 2015 ). The brown bear Ursus arctos was selected as the terrestrial carnivore for comparison because it is closely phylogenetically related to sea lions (Eizirik et al. 2010 ; Sato et al. 2009 ) and has comparable body size and life span (Bischof et al. 2018 ; Loughlin 2009 ; Swenson et al. 2007 ). Most previous studies on the Steller sea lion have examined sexual dimorphism (e.g., Brunner et al. 2004 ; Isono 1998 ). Steller sea lion is polygamous; males form harems at age 9 or older, when they reach social maturity. The males engage in fierce competition while forming a harem. Multiple studies have specifically investigated sexual dimorphism in Steller sea lion cranial ontogeny (Brunner et al. 2004 ; Fiscus 1961 ; Isono 1998 ). Although some studies have described its developmental patterns, no study has described age-related changes in its cranial morphology. One reason for this paucity is that conventional analyses use allometry, which excludes age as a factor. Brunner (2000) plotted the value of the cranial length divided by the braincase width for different age groups and showed that this value decreased with age, suggesting that the development of sensory organs including the brain is completed during the juvenile period. In this study, we evaluated the ontogeny of cranial morphology in the Steller sea lion by plotting measurements for each body part standardized by cranial length (CL) in age-determined specimens. This approach allowed us to identify the age at which specific morphological changes occurred, such that they could be related to behavior and life history. The objective of this study was to identify cranial morphology related to suction feeding and sexual dimorphism in the Steller sea lion by analyzing a wide range of ages and comparing male and female cranial ontogeny in Steller sea lions and brown bears. Materials and Methods Specimens We used 104 Steller sea lion craniums stored at the Faculty of Fisheries Science, Hokkaido University, Japan. These animals were captured by shooting to mitigate fishing damage or bycaught off the Hokkaido Island coast. The samples consisted of 46 females and 45 males. All craniums were age-assessed or of known age. Age was estimated by counting the annual rings on sections of canine teeth. The accuracy of the age assessment was 83% correct for the 2005-2011 sample (Isono et al. 2019). Thirty-nine females and 38 males were age-assessed and seven females and males were of known ages. The specimens were marked at age 0 on their rookeries, and their exact ages were determined by counting backward from the date of cranium sampling (Burkanov et al. 2011; Permyakov et al. 2015). Thus, the ages within the entire sample ranged from 0 to 10 years for females and 0 to 11 years for males (Table 1). The craniums of brown bears were used for comparison with those of the Steller sea lion. We used 33 female and 53 male specimens of known age from the collection at the Hokkaido University Museum. The ages of brown bear specimens ranged from 0 to 15 years for females and 0 to 16 years for males (Table 1). Measurements A total of 13 Steller sea lion sites were measured using electronic calipers (± 0.01 mm; Fig. 1). These sites were selected based on Brunner (2003) and Segura and Prevosti (2012) and were assumed to be related to feeding behavior and fighting between males. First, we measured eight sites that were assumed to be related to feeding behavior. Palate length (LP) and breadth (BP) were assumed to be related to tongue development, and zygomatic breadth (ZB) was related to the development of masticatory muscles (Segura and Prevosti 2012). Because other sensory organs, including the eyes and ears, are also used for feeding (Debey and Pyenson 2013; Kastak and Schusterman 1998; Schusterman et al. 2000), related sites were measured. Next, we measured sites assumed to be related to fighting between males. Cranial width (CW) and breadth of the mastoid process (BM) are related to neck muscle development (Diogo et al. 2012; Hasan 2011). In brown bear specimens, the three sites related to feeding (i.e., LP, BP, and ZB) were measured for development comparisons. Data analyses The measurements for each region were standardized by CL and plotted against age to describe cranial ontogenetic development (Brunner et al. 2004). Then, differences in ontogeny by sex and species were examined for each cranial region utilizing multiple regression analyses (‘lm’ function in R v4.2.1; R Core Team, Vienna, Austria). The explanatory variables were age, sex, and the age × sex interaction for sex differences, and age, species, and the age × sex interaction for species differences. Finally, analysis of variance (ANOVA) was performed, with p < 0.05 indicating significantly different slopes in interaction analyses or significant differences from age 0 among sexes or species for a given site. Because Steller sea lions exhibit substantial sexual dimorphism, analyses of species differences were conducted separately for each sex. Results Sexual comparison within Steller sea lions The length of the upper postcanine row (Upr), breadth of the auditory bulla (BBu), length of the auditory bulla (LBu), and breadth of the orbit (BO) showed no growth trend, whereas LP and BP (orbit length [LO] and cranium height [HC]) tended toward longer (shorter) length relative to cranial length with growth in both sexes (Appendix 3). These trends were confirmed in multiple regression analyses (Table 3). Among these eight sites, four sites (BBu, BP, LO, and HC) revealed significant sexual differences in the slopes of regression analyses including the age × sex interaction as an explanatory variable. Four sites (ZB, CW, BM, and height of the cranium at the supraorbital processes [HCS]) exhibited apparent sexual differences in plots against age (Fig. 3). Females showed no ontogenetic trend, whereas males exhibited remarkable development in these sites after 4–6 years of age. Multiple regression analyses confirmed sexual differences in the slopes of regression lines for the four sites, whereas no significant difference in the intercepts was found between the sexes, indicating that there were no sexual differences in morphology at age 0. Interspecific comparison The relative length of the palate relative to cranial length (LP) remained constant with age in both sexes of brown bears, but it increased with age in both sexes of Steller sea lions (Appendix 4). BP became relatively narrower with age in both sexes, whereas the opposite trend was observed in Steller sea lions (Fig. 4). Multiple regression analyses confirmed these interspecific differences; the slopes of the LP and BP regression lines vs. age were significantly steeper in Steller sea lions, indicating that they exhibit more pronounced development than brown bears (Table 4). The slope of the regression line for brown bear BP was negative and became relatively narrower with growth. No interspecific difference in the ZB of males was observed, and both values increased with growth (Fig. 4). However, the zygomatic bone of female brown bears grew wider with age compared with that of the Steller sea lion. These results were confirmed by multiple regression analysis (Table 4). Discussion CW, HCS, BM, and HC No sex differences in CW, HCS, MB, or HC of SSLs were detected at age 0, whereas these sites exhibited more conspicuous growth in males after 5–6 years of age. This sex difference in development reflected polygamy; the CW, HCS, BM, and HC differed between the sexes in this study, and these are the sites that reflect enlargement of the face and neck. CW, BM, and HC are attachment sites for the neck muscles, such that development in these areas indicates neck muscle development (Diogo et al. 2012; Hasan 2011). Furthermore, HCS represents the size of the face as it appears relative to other individuals. As mentioned above, males form harems at age 9 or older, and males fight fiercely (Thorsteinson and Lensink 1962) and need to appear large in a fight (Brunner et al. 2004; Campagna and Boeuf 1988; Isono 1998; Schusterman and Gentry 1971). Therefore, we infer that these regions, which develop significantly before harem formation, are important for fights. Similarly, the more pronounced development of CW, HCS, BM, and HC in males compared to females may reflect the importance of neck and face size during fights between males. BP The BP decreased with age in brown bears, and increased with age in SSLs. This difference reflects a difference in feeding behavior. The palatine bone houses the tongue, and the development of this bone is thought to represent tongue development (Segura and Prevosti 2012). The relative size of the brown bear tongue decreases with the size of the head with age, whereas the tongue develops considerably with age in the Steller sea lion. Mammalian pups suckle milk using their tongues (Bosma et al. 1990; German et al. 1992). As adults, they masticate their food and the tongue is used less frequently (Segura and Prevosti 2012; Tanner et al. 2010). Brown bears also follow this ontogenetic pattern, as the tongue is less important for food ingestion in adults (Kadosaki 1983; Mealey 1980). Conversely, the Steller sea lion uses its tongue for suction feeding, which requires negative pressure in the mouth to ingest food. They then collect the food by pulling the tongue down into the back of the throat (Marshall et al. 2015). Therefore, the tongue plays a more important role in food acquisition in the Steller sea lion than in the brown bear, and the development of BP in the Steller sea lion may reflect the importance of the tongue in its feeding behavior. ZB The ZB was less developed in female Steller sea lions than in brown bears, which may reflect differences in feeding behavior. The zygomatic arch is a bone that houses the masticatory muscles, and an increase in ZB represents masticatory muscle development (Giannini et al. 2010; Segura and Prevosti 2012; Tanner et al. 2010). As mentioned above, bears engage in feeding behavior that requires the use of masticatory muscles, whereas Steller sea lions engage in feeding behavior that requires less frequent use of masticatory muscles (Kadosaki 1983; Marshall et al. 2015; Mealey 1980). Underdevelopment of the zygomatic arch in female Steller sea lions compared to female brown bears may reflect the lower importance of the masticatory muscles in the feeding behavior of the sea lion. Male Steller sea lions had a well-developed zygomatic arch, whereas females did not, suggesting that the development of this bone reflects fighting between males, as do CW, HCS, BM, and HC development. The ZB of males also developed significantly between 4 and 6 years of age, a few years before harems are formed, suggesting a relationship between this site and male fighting. Steller sea lion males have been suggested to use their masticatory muscles, which are housed in the zygomatic arch, to bite their opponents vigorously during fighting (Pitcher and Calkins 1981). Therefore, larger masticatory muscles are expected to be more advantageous for breeding in males. In conclusion, the comparable development of the zygomatic arch in males between the Steller sea lion and brown bear may reflect the fact that more developed masticatory muscles are a reproductive advantage in male sea lions. Future studies The present study highlighted differences in cranial morphology related to feeding behavior between a terrestrial carnivore and a pinniped. Future comparisons with other otariids and phocids may provide further insight into the evolution of suction feeding. For example, the northern fur seal, the earliest differentiated otariid, engages in biting feeding rather than suction feeding (Marshall et al. 2015), and other otariids such as Otaria and Zalophus species, which are thought to have differentiated later than the Steller sea lion, are presumed to engage in suction feeding (Adam and Berta 2002). The evolution of suction feeding and cranial morphology could be further elucidated by comparing otariids that do not engage in suction feeding with those that differentiated later than the Steller sea lion and engage in suction feeding. Among pinnipeds, seals are more likely than sea lions to have cranial morphology characterized by suction feeding (Adam and Berta 2002). Studies that have analyzed the feeding behavior of harbor seals from a kinematic perspective have reported that harbor seals engage in both suction and bite feeding (Marshall et al. 2014). Therefore, cranial ontogeny in seals may show characteristics of both suction and bite feeding modes. Identifying the relationship between cranial morphology and suction feeding in extant species will allow inferences about the lives of fossil species. If fossil species have surviving bones and the relationship between cranial morphology and behavior is known in greater detail, it will be possible to examine whether cranial morphology expresses behavioral characteristics (Adam and Berta 2002). Further research on extant species and the application of the findings to fossil species will help us to speculate on the feeding behavior of fossil species. Conclusion The present study showed less development of the ZB in female Steller sea lions compared to female brown bears and greater development of the BP in Steller sea lions compared to brown bears of both sexes. Both of these results reflected differences in feeding behavior and were consistent with previous studies in other carnivores (Giannini et al. 2010 ; Segura and Prevosti 2012 ; Tarnawski et al. 2014a , 2014b , 2015 ). In conclusion, we propose the following relationships between cranial ontogeny and behavior: sexual differences in cranial ontogeny in CW, HCS, BM, HC, and ZB reflect fighting between males; ZB underdevelopment reflects feeding by swallowing; and BP development reflects suction feeding. Declarations Author Contribution R.Y. : Conceptualization, Formal Analysis, Methodology, Visualization, Main writing – original draft. Y. K.: Investigation, Writing – review & editing.T. I. : Investigation, Writing – review & editing. O.Y. : Supervision, Writing – review & editing. Acknowledgments In this study, we partly used the specimens collected under the Comprehensive Project to Mitigate Fisheries Damages by Harmful Animals conducted by the Fishing Industry/Communities Promotion Organization. We thank all those who engaged in collecting and preparing Steller sea lion specimens, M. Eda at Hokkaido University Museum for kindly providing the opportunity to measure brown bear specimens, Y Watanuki and M Harunari for constructive comments. References Abdala, F., Flores, D. A., & Giannini, N. P. (2001). Postweaning Ontogeny of the Skull of Didelphis Albiventris. Journal of Mammalogy, 82(1), 190–200. https://doi.org/10.1644/1545-1542(2001)0822.0.CO;2 Adam, P. J., & Berta, A. (2002). Evolution of prey capture strategies and diet in the Pinnipedimorpha (Mammalia, Carnivora). Oryctos, 4(3–8), 3–27. Bischof, R., Bonenfant, C., Rivrud, I. M., Zedrosser, A., Friebe, A., Coulson, T., Mysterud, A., & Swenson, J. E. (2018). 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Allometry of the postnatal cranial ontogeny and sexual dimorphism in Otaria byronia (Otariidae). Acta Theriologica, 59, 81–97. Tarnawski, B. A., Cassini, G. H., & Flores, D. A. (2014b). Skull allometry and sexual dimorphism in the ontogeny of the southern elephant seal (Mirounga leonina). Canadian Journal of Zoology, 92(1), 19–31. Tarnawski, B. A., Flores, D., Cassini, G., & Cappozzo, L. H. (2015). A comparative analysis on cranial ontogeny of South American fur seals (Otariidae: Arctocephalus). Zoological Journal of the Linnean Society, 173(1), 249–269. Thorsteinson, F. V., & Lensink, C. J. (1962). Biological Observations of Steller Sea Lions Taken during an Experimental Harvest. The Journal of Wildlife Management, 26(4), 353–359. https://doi.org/10.2307/3798011 Wuersig, B., Thewissen, J. G. M., & Kovacs, K. M. (2017). Encyclopedia of Marine Mammals. Academic Press. Tables Tables 1 to 4 are available in the Supplementary Files section. Additional Declarations No competing interests reported. Supplementary Files Appendix.docx Table1.png Table2..png Table3.png Table4.png Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3872222","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":267801659,"identity":"a35d0654-09f2-41b5-9971-eb594265008f","order_by":0,"name":"Ryunosuke Yuge","email":"","orcid":"","institution":"Hokkaido University","correspondingAuthor":false,"prefix":"","firstName":"Ryunosuke","middleName":"","lastName":"Yuge","suffix":""},{"id":267801660,"identity":"f81e3800-e5cf-4439-a7bb-1e3192aa8ce7","order_by":1,"name":"Yumi Kobayashi","email":"","orcid":"","institution":"Hokkaido University","correspondingAuthor":false,"prefix":"","firstName":"Yumi","middleName":"","lastName":"Kobayashi","suffix":""},{"id":267801661,"identity":"d1c2b2b2-10a1-467a-b54e-f6eabf13bf65","order_by":2,"name":"Takeomi Isono","email":"","orcid":"","institution":"Fisheries Research Agency","correspondingAuthor":false,"prefix":"","firstName":"Takeomi","middleName":"","lastName":"Isono","suffix":""},{"id":267801662,"identity":"08805bbd-d72c-49fd-820e-6e8393c4f0fc","order_by":3,"name":"Orio Yamamura","email":"data:image/png;base64,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","orcid":"","institution":"Hokkaido University","correspondingAuthor":true,"prefix":"","firstName":"Orio","middleName":"","lastName":"Yamamura","suffix":""}],"badges":[],"createdAt":"2024-01-17 07:59:13","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3872222/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3872222/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":49862060,"identity":"cfed1167-0c94-42a7-a27f-0841492a4c54","added_by":"auto","created_at":"2024-01-19 09:05:47","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":726714,"visible":true,"origin":"","legend":"\u003cp\u003eVentral (a), lateral (b), and occipital views of the cranium and measurements sites for the Steller sea lion. \u003cem\u003eBBu\u003c/em\u003e breadth of auditory bulla (1–2), \u003cem\u003eBM\u003c/em\u003e breadth of mastoid process, \u003cem\u003eBO\u003c/em\u003e breadth of orbit,\u003cem\u003e BP\u003c/em\u003e breadth of palate,\u003cem\u003e CL\u003c/em\u003ecranial length,\u003cem\u003e CW\u003c/em\u003e cranial width, \u003cem\u003eHC\u003c/em\u003e height of cranium,\u003cem\u003e HCS\u003c/em\u003e height of cranium at supraorbital processes,\u003cem\u003e LBu\u003c/em\u003e length of auditory bulla (3–4), \u003cem\u003eLO\u003c/em\u003e length of orbit,\u003cem\u003e LP\u003c/em\u003e length of palate,\u003cem\u003e Upr\u003c/em\u003elength of upper postcanine row,\u003cem\u003e ZB\u003c/em\u003ezygomatic breadth.\u003c/p\u003e","description":"","filename":"Fig.1.png","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/d8c80f49a6702b226f146cc7.png"},{"id":49861180,"identity":"49c38e25-d4d0-4bf5-a6ab-0d9358a25e7f","added_by":"auto","created_at":"2024-01-19 08:57:49","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":340581,"visible":true,"origin":"","legend":"\u003cp\u003eVentral view of the cranium and brown bear measurement sites. \u003cem\u003eBP\u003c/em\u003e breadth of palate, \u003cem\u003eCL\u003c/em\u003ecranial length, \u003cem\u003eLP\u003c/em\u003e length of palate, \u003cem\u003eZB\u003c/em\u003e zygomatic breadth.\u003c/p\u003e","description":"","filename":"Fig.2.png","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/1999a77f2ae94374025d6663.png"},{"id":49861175,"identity":"39255814-bc6a-4864-8348-5da88820200c","added_by":"auto","created_at":"2024-01-19 08:57:47","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":234132,"visible":true,"origin":"","legend":"\u003cp\u003eChanges in measurements relative to cranial length with age in Steller sea lions. a: Zygomatic breadth, b: cranial width c: height of cranium at supraorbital processes, d: breadth of mastoid process. 〇: female (age-estimated individuals), ●: male (age-estimated individuals), ◇: female (branding-marked individuals), ◆: male (branding-marked) individuals). Solid and dotted lines indicate linear regression curvesfor males\u003cstrong\u003e \u003c/strong\u003eand females, respectively.\u003c/p\u003e","description":"","filename":"Fig.3.png","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/357f8f058bed57f2f47a39a9.png"},{"id":49861181,"identity":"f19759b3-6350-4a0d-b778-3ff7269a3221","added_by":"auto","created_at":"2024-01-19 08:57:51","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":241525,"visible":true,"origin":"","legend":"\u003cp\u003eChanges in measurements relative to cranial length with age. a: Female breadth of the palate, b: male breadth of the palate, c: female zygomatic breadth, d: male zygomatic breadth. ●: Steller sea lion (age-estimated individuals), 〇: Brown bear, ◆: Steller sea lion (branding-marked individuals). Solid and dotted lines indicate linear regression curves for the Steller sea lion\u003cstrong\u003e \u003c/strong\u003eand brown bear, respectively.\u003c/p\u003e","description":"","filename":"Fig.4.png","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/7a384137807743001c3269a0.png"},{"id":50225027,"identity":"afaf1998-d441-4ec9-8efa-9d814b97fc79","added_by":"auto","created_at":"2024-01-26 17:37:22","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1038909,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/20dd934f-29d1-47ef-82fa-dc2e8f17711f.pdf"},{"id":49862061,"identity":"0ff5e1c8-22eb-4c89-a9ab-acf23c470f51","added_by":"auto","created_at":"2024-01-19 09:05:48","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":2460401,"visible":true,"origin":"","legend":"","description":"","filename":"Appendix.docx","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/01b596be2dd55519b548d533.docx"},{"id":49861173,"identity":"3383b012-6df0-4eb5-8a65-136ffcc5b233","added_by":"auto","created_at":"2024-01-19 08:57:47","extension":"png","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":258908,"visible":true,"origin":"","legend":"","description":"","filename":"Table1.png","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/3dde95981e08cef55a78eb1f.png"},{"id":49861176,"identity":"05bc4989-602d-4599-a3f8-64a610a14134","added_by":"auto","created_at":"2024-01-19 08:57:48","extension":"png","order_by":3,"title":"","display":"","copyAsset":false,"role":"supplement","size":858438,"visible":true,"origin":"","legend":"","description":"","filename":"Table2..png","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/7c34de4652df0d5c0cda58af.png"},{"id":49861179,"identity":"3364932b-1285-48eb-82c7-776a7bd9fd4a","added_by":"auto","created_at":"2024-01-19 08:57:48","extension":"png","order_by":4,"title":"","display":"","copyAsset":false,"role":"supplement","size":674172,"visible":true,"origin":"","legend":"","description":"","filename":"Table3.png","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/b7a7ea6b7875a5ce50348452.png"},{"id":49861178,"identity":"41ad0fcb-7688-4b97-8783-aaee2a807220","added_by":"auto","created_at":"2024-01-19 08:57:48","extension":"png","order_by":5,"title":"","display":"","copyAsset":false,"role":"supplement","size":492373,"visible":true,"origin":"","legend":"","description":"","filename":"Table4.png","url":"https://assets-eu.researchsquare.com/files/rs-3872222/v1/eab5db9f1974b4fbd5549df5.png"}],"financialInterests":"No competing interests reported.","formattedTitle":"Cranial ontogeny in Steller sea lions: Relationships between cranial morphology and suction feeding","fulltext":[{"header":"Introduction","content":"\u003cp\u003eCranial morphology can reveal the ecological characteristics of an animal from various perspectives (Dumont et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Roston and Roth \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Santana et al. \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2012\u003c/span\u003e), including muscles and sensory organs (Hanken and Hall \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e1993\u003c/span\u003e). The cranium also reflects behavioral characteristics, particularly related to feeding. For example, dolphins feed by swallowing whole prey, whereas terrestrial carnivores chew their food. Therefore, the masticatory muscles of dolphins are less developed than those of terrestrial carnivores, and the zygomatic bone containing the masticatory muscles is thin (Wuersig et al. \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Furthermore, because the noses of dolphins are located on the top of their heads for efficient breathing, the anterior maxillary bone extends over the head, whereas the nose of a terrestrial carnivore is located at the tip of the rostrum (Roston and Roth \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2019\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eCranial morphology changes with age, representing ontogenetic changes in the ecological characteristics of animals (Abdala et al. \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Brunner et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Flores et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Giannini et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). Cranial ontogeny in terrestrial carnivores reflects increasing dependence on masticatory feeding with growth (Giannini et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Segura and Prevosti \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Tanner et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). In terrestrial carnivores, the zygomatic bone develops significantly with age, and the width of the palatal bone relative to cranial length decreases with age. The zygomatic bone houses the masticatory muscles and the palatal bone houses the tongue, and the developmental pattern of these bones represents the development of the respective muscles. Among mammals, pups suckle the mother\u0026rsquo;s milk until weaning, when they begin to chew food using their masticatory muscles. Terrestrial animals use their tongues for suckling during breastfeeding (Bosma et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e1990\u003c/span\u003e; German et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e1992\u003c/span\u003e), but do not use them for force-intensive tasks during chewing and feeding (Crompton \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e1989\u003c/span\u003e; Liu et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). Therefore, the development of the zygomatic bone and underdevelopment of the palate bone observed in terrestrial carnivores indicate masticatory feeding.\u003c/p\u003e \u003cp\u003eWhereas terrestrial carnivores generally feed primarily by mastication, some pinnipeds exhibit a unique feeding mode called suction feeding (Hocking et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Based on their cranial morphology, various pinnipeds suction feed, in which underwater prey is sucked into the mouth by negative pressure (Adam and Berta \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2002\u003c/span\u003e). Suction feeding uses an organ system different from that used for masticatory feeding. The tongue is pulled back into the throat to create negative pressure in the oral cavity, which is used to suck in food (Bloodworth and Marshall \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Kane and Marshall \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Marshall et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2008\u003c/span\u003e, \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2014\u003c/span\u003e, \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Thus, the ontogeny of cranial morphology in pinnipeds is expected to be substantially different from that of terrestrial carnivores. Studying the ontogeny of cranial morphology in pinnipeds would provide an opportunity to understand the relationship between suction feeding and cranial morphology, which is unique to marine mammals.\u003c/p\u003e \u003cp\u003ePrevious studies on the cranial morphology of carnivores have included pinnipeds (Brunner et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Isono \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e1998\u003c/span\u003e; Tarnawski et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2014b\u003c/span\u003e, \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2014a\u003c/span\u003e, \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2015\u003c/span\u003e); however, few have mentioned feeding behavior (e.g., Tarnawski et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Because these studies employed different methods to assess cranial ontogeny, including bivariate and multivariate analyses, it is impossible to compare cranial ontogeny between terrestrial carnivores and pinnipeds. Therefore, in this study, the cranial ontogeny of pinnipeds and terrestrial carnivores were compared using the same method. As the pinniped species, we examined the Steller sea lion \u003cem\u003eEumetopias jubatus\u003c/em\u003e, which is among the few species whose suction feeding has been confirmed in an experimental setting (Marshall et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). The brown bear \u003cem\u003eUrsus arctos\u003c/em\u003e was selected as the terrestrial carnivore for comparison because it is closely phylogenetically related to sea lions (Eizirik et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Sato et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2009\u003c/span\u003e) and has comparable body size and life span (Bischof et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Loughlin \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Swenson et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2007\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eMost previous studies on the Steller sea lion have examined sexual dimorphism (e.g., Brunner et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Isono \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e1998\u003c/span\u003e). Steller sea lion is polygamous; males form harems at age 9 or older, when they reach social maturity. The males engage in fierce competition while forming a harem. Multiple studies have specifically investigated sexual dimorphism in Steller sea lion cranial ontogeny (Brunner et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Fiscus \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e1961\u003c/span\u003e; Isono \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e1998\u003c/span\u003e). Although some studies have described its developmental patterns, no study has described age-related changes in its cranial morphology. One reason for this paucity is that conventional analyses use allometry, which excludes age as a factor. Brunner (2000) plotted the value of the cranial length divided by the braincase width for different age groups and showed that this value decreased with age, suggesting that the development of sensory organs including the brain is completed during the juvenile period. In this study, we evaluated the ontogeny of cranial morphology in the Steller sea lion by plotting measurements for each body part standardized by cranial length (CL) in age-determined specimens. This approach allowed us to identify the age at which specific morphological changes occurred, such that they could be related to behavior and life history.\u003c/p\u003e \u003cp\u003eThe objective of this study was to identify cranial morphology related to suction feeding and sexual dimorphism in the Steller sea lion by analyzing a wide range of ages and comparing male and female cranial ontogeny in Steller sea lions and brown bears.\u003c/p\u003e"},{"header":"Materials and Methods","content":"\u003cp\u003e\u003cstrong\u003eSpecimens\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe used 104 Steller sea lion craniums stored at the Faculty of Fisheries Science, Hokkaido University, Japan. These animals were captured by shooting to mitigate fishing damage or bycaught off the Hokkaido Island coast. The samples consisted of 46 females and 45 males. All craniums were age-assessed or of known age. Age was estimated by counting the annual rings on sections of canine teeth. The accuracy of the age assessment was 83% correct for the 2005-2011 sample (Isono et al. 2019). Thirty-nine females and 38 males were age-assessed and seven females and males were of known ages. The specimens were marked at age 0 on their rookeries, and their exact ages were determined by counting backward from the date of cranium sampling (Burkanov et al. 2011; Permyakov et al. 2015). Thus, the ages within the entire sample ranged from 0 to 10 years for females and 0 to 11 years for males (Table 1). The craniums of brown bears were used for comparison with those of the Steller sea lion. We used 33 female and 53 male specimens of known age from the collection at the Hokkaido University Museum. The ages of brown bear specimens ranged from 0 to 15 years for females and 0 to 16 years for males (Table 1).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMeasurements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eA total of 13 Steller sea lion sites were measured using electronic calipers (\u0026plusmn; 0.01 mm; Fig. 1). These sites were selected based on Brunner (2003) and Segura and Prevosti (2012) and were assumed to be related to feeding behavior and fighting between males. First, we measured eight sites that were assumed to be related to feeding behavior. Palate length (LP) and breadth (BP) were assumed to be related to tongue development, and zygomatic breadth (ZB) was related to the development of masticatory muscles (Segura and Prevosti 2012). Because other sensory organs, including the eyes and ears, are also used for feeding (Debey and Pyenson 2013; Kastak and Schusterman 1998; Schusterman et al. 2000), related sites were measured. Next, we measured sites assumed to be related to fighting between males. Cranial width (CW) and breadth of the mastoid process (BM) are related to neck muscle development (Diogo et al. 2012; Hasan 2011). In brown bear specimens, the three sites related to feeding (i.e., LP, BP, and ZB) were measured for development comparisons.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData analyses\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe\u0026nbsp;measurements for each region were standardized by CL and plotted against age\u0026nbsp;to describe cranial ontogenetic development\u0026nbsp;(Brunner et al.\u0026nbsp;2004). Then, differences in ontogeny by sex and species were examined for each cranial region\u0026nbsp;utilizing\u0026nbsp;multiple regression analyses\u0026nbsp;(\u0026lsquo;lm\u0026rsquo;\u0026nbsp;function in R\u0026nbsp;v4.2.1; R\u0026nbsp;Core Team,\u0026nbsp;Vienna, Austria).\u0026nbsp;The explanatory variables were age, sex, and the\u0026nbsp;age \u0026times; sex\u0026nbsp;interaction for sex\u0026nbsp;differences, and\u0026nbsp;age, species,\u0026nbsp;and the\u0026nbsp;age \u0026times; sex\u0026nbsp;interaction for species\u0026nbsp;differences. Finally, analysis of variance\u0026nbsp;(ANOVA)\u0026nbsp;was performed, with\u0026nbsp;\u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05 indicating significantly different slopes in interaction analyses or significant differences from age 0 among sexes or species for a given site. Because Steller sea lions exhibit substantial sexual dimorphism, analyses of species differences were conducted separately for each sex.\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003e\u003cstrong\u003eSexual comparison\u003c/strong\u003e \u003cstrong\u003ewithin\u003c/strong\u003e\u003cstrong\u003e\u0026nbsp;Steller sea\u0026nbsp;\u003c/strong\u003e\u003cstrong\u003elions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe length of the upper postcanine row (Upr), breadth of the auditory bulla (BBu), length of the auditory bulla (LBu), and breadth of the orbit (BO) showed no growth trend, whereas LP and BP (orbit length [LO] and cranium height [HC]) tended toward longer (shorter) length relative to cranial length with growth in both sexes (Appendix 3). These trends were confirmed in multiple regression analyses (Table 3). Among these eight sites, four sites (BBu, BP, LO, and HC) revealed significant sexual differences in the slopes of regression analyses including the age \u0026times; sex interaction as an explanatory variable. Four sites (ZB, CW, BM, and height of the cranium at the supraorbital processes [HCS]) exhibited apparent sexual differences in plots against age (Fig. 3). Females showed no ontogenetic trend, whereas males exhibited remarkable development in these sites after 4\u0026ndash;6 years of age. Multiple regression analyses confirmed sexual differences in the slopes of regression lines for the four sites, whereas no significant difference in the intercepts was found between the sexes, indicating that there were no sexual differences in morphology at age 0.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eInterspecific comparison\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThe relative length of the palate relative to cranial length (LP) remained constant with age in both sexes of brown bears, but it increased with age in both sexes of Steller sea lions (Appendix 4). BP became relatively narrower with age in both sexes, whereas the opposite trend was observed in Steller sea lions (Fig. 4). Multiple regression analyses confirmed these interspecific differences; the slopes of the LP and BP regression lines vs. age were significantly steeper in Steller sea lions, indicating that they exhibit more pronounced development than brown bears (Table 4). The slope of the regression line for brown bear BP was negative and became relatively narrower with growth. No interspecific difference in the ZB of males was observed, and both values increased with growth (Fig. 4). However, the zygomatic bone of female brown bears grew wider with age compared with that of the Steller sea lion. These results were confirmed by multiple regression analysis (Table 4).\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003e\u003cstrong\u003eCW, HCS, BM,\u0026nbsp;\u003c/strong\u003e\u003cstrong\u003eand\u0026nbsp;\u003c/strong\u003e\u003cstrong\u003eHC\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNo sex differences in CW, HCS, MB, or HC of SSLs were detected at age 0, whereas these sites exhibited more conspicuous growth in males after 5\u0026ndash;6 years of age. This sex difference in development reflected polygamy; the CW, HCS, BM, and HC differed between the sexes in this study, and these are the sites that reflect enlargement of the face and neck. CW, BM, and HC are attachment sites for the neck muscles, such that development in these areas indicates neck muscle development (Diogo et al. 2012; Hasan 2011). Furthermore, HCS represents the size of the face as it appears relative to other individuals. As mentioned above, males form harems at age 9 or older, and males fight fiercely (Thorsteinson and Lensink 1962) and need to appear large in a fight (Brunner et al. 2004; Campagna and Boeuf 1988; Isono 1998; Schusterman and Gentry 1971). Therefore, we infer that these regions, which develop significantly before harem formation, are important for fights. Similarly, the more pronounced development of CW, HCS, BM, and HC in males compared to females may reflect the importance of neck and face size during fights between males.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eBP\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe BP decreased with age in brown bears, and increased with age in SSLs. This difference reflects a difference in feeding behavior. The palatine bone houses the tongue, and the development of this bone is thought to represent tongue development (Segura and Prevosti 2012). The relative size of the brown bear tongue decreases with the size of the head with age, whereas the tongue develops considerably with age in the Steller sea lion. Mammalian pups suckle milk using their tongues (Bosma et al. 1990; German et al. 1992). As adults, they masticate their food and the tongue is used less frequently (Segura and Prevosti 2012; Tanner et al. 2010). Brown bears also follow this ontogenetic pattern, as the tongue is less important for food ingestion in adults (Kadosaki 1983; Mealey 1980). Conversely, the Steller sea lion uses its tongue for suction feeding, which requires negative pressure in the mouth to ingest food. They then collect the food by pulling the tongue down into the back of the throat (Marshall et al. 2015). Therefore, the tongue plays a more important role in food acquisition in the Steller sea lion than in the brown bear, and the development of BP in the Steller sea lion may reflect the importance of the tongue in its feeding behavior.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eZB\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe\u0026nbsp;ZB was less developed in\u0026nbsp;female Steller sea lions\u0026nbsp;than in brown bears, which\u0026nbsp;may reflect\u0026nbsp;differences\u0026nbsp;in feeding behavior. The zygomatic arch is a bone that houses the masticatory muscles, and\u0026nbsp;an\u0026nbsp;increase\u0026nbsp;in\u0026nbsp;ZB represents\u0026nbsp;masticatory muscle\u0026nbsp;development\u0026nbsp;(Giannini et al.\u0026nbsp;2010; Segura\u0026nbsp;and\u0026nbsp;Prevosti 2012; Tanner et al.\u0026nbsp;2010). As mentioned above, bears engage in feeding behavior that requires the use of masticatory muscles,\u0026nbsp;whereas Steller sea lions\u0026nbsp;engage in feeding behavior that requires less frequent use of masticatory muscles\u0026nbsp;(Kadosaki 1983; Marshall et al.\u0026nbsp;2015; Mealey 1980).\u0026nbsp;Underdevelopment of the zygomatic arch in\u0026nbsp;female Steller\u0026nbsp;sea lions compared to\u0026nbsp;female\u0026nbsp;brown bears may reflect the\u0026nbsp;lower importance\u0026nbsp;of\u0026nbsp;the\u0026nbsp;masticatory muscles in the feeding behavior of\u0026nbsp;the\u0026nbsp;sea\u0026nbsp;lion. \u003c/p\u003e\n\u003cp\u003eMale Steller sea lions had a well-developed zygomatic arch, whereas females did not, suggesting that the development of this bone reflects fighting between males, as do CW, HCS, BM, and HC development. The ZB of males also developed significantly between 4 and 6 years of age, a few years before harems are formed, suggesting a relationship between this site and male fighting. Steller sea lion males have been suggested to use their masticatory muscles, which are housed in the zygomatic arch, to bite their opponents vigorously during fighting (Pitcher and Calkins 1981). Therefore, larger masticatory muscles are expected to be more advantageous for breeding in males. In conclusion, the comparable development of the zygomatic arch in males between the Steller sea lion and brown bear may reflect the fact that more developed masticatory muscles are a reproductive advantage in male sea lions.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFuture studies\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe present study\u0026nbsp;highlighted differences\u0026nbsp;in cranial morphology\u0026nbsp;related\u0026nbsp;to feeding behavior\u0026nbsp;between a terrestrial carnivore and a pinniped.\u0026nbsp;Future comparisons with other otariids and phocids may provide\u0026nbsp;further\u0026nbsp;insight into the evolution of suction feeding.\u0026nbsp;For example, the\u0026nbsp;northern fur seal, the earliest differentiated\u0026nbsp;otariid, engages in biting feeding rather than suction feeding (Marshall et al.\u0026nbsp;2015), and other otariids\u0026nbsp;such as\u0026nbsp;\u003cem\u003eOtaria\u0026nbsp;\u003c/em\u003eand \u003cem\u003eZalophus\u003c/em\u003e species, which are thought to have differentiated later than the Steller sea lion, are presumed to engage in suction feeding (Adam and Berta 2002). The evolution of suction feeding and cranial morphology could be further elucidated by comparing otariids that do not engage in suction feeding with those that differentiated later than the Steller sea lion and engage in suction feeding. Among pinnipeds, seals are more likely than sea lions to have cranial morphology characterized by suction feeding (Adam and Berta 2002). Studies that have analyzed the feeding behavior of harbor seals from a kinematic perspective have reported that harbor seals engage in both suction and bite feeding (Marshall et al. 2014). Therefore, cranial ontogeny in seals may show characteristics of both suction and bite feeding modes. Identifying the relationship between cranial morphology and suction feeding in extant species will allow inferences about the lives of fossil species. If fossil species have surviving bones and the relationship between cranial morphology and behavior is known in greater detail, it will be possible to examine whether cranial morphology expresses behavioral characteristics (Adam and Berta 2002). Further research on extant species and the application of the findings to fossil species will help us to speculate on the feeding behavior of fossil species.\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eThe present study showed less development of the ZB in female Steller sea lions compared to female brown bears and greater development of the BP in Steller sea lions compared to brown bears of both sexes. Both of these results reflected differences in feeding behavior and were consistent with previous studies in other carnivores (Giannini et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Segura and Prevosti \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Tarnawski et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2014a\u003c/span\u003e, \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2014b\u003c/span\u003e, \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). In conclusion, we propose the following relationships between cranial ontogeny and behavior: sexual differences in cranial ontogeny in CW, HCS, BM, HC, and ZB reflect fighting between males; ZB underdevelopment reflects feeding by swallowing; and BP development reflects suction feeding.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\u003cp\u003eR.Y. : Conceptualization, Formal Analysis, Methodology, Visualization, Main writing \u0026ndash; original draft. Y. K.: Investigation, Writing \u0026ndash; review \u0026amp; editing.T. I. : Investigation, Writing \u0026ndash; review \u0026amp; editing. O.Y. : Supervision, Writing \u0026ndash; review \u0026amp; editing.\u003c/p\u003e\u003ch2\u003eAcknowledgments\u003c/h2\u003e \u003cp\u003eIn this study, we partly used the specimens collected under the Comprehensive Project to Mitigate Fisheries Damages by Harmful Animals conducted by the Fishing Industry/Communities Promotion Organization. We thank all those who engaged in collecting and preparing Steller sea lion specimens, M. Eda at Hokkaido University Museum for kindly providing the opportunity to measure brown bear specimens, Y Watanuki and M Harunari for constructive comments.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n \u003cli\u003eAbdala, F., Flores, D. A., \u0026amp; Giannini, N. P. (2001). Postweaning Ontogeny of the Skull of Didelphis Albiventris. Journal of Mammalogy, 82(1), 190\u0026ndash;200. https://doi.org/10.1644/1545-1542(2001)082\u0026lt;0190:POOTSO\u0026gt;2.0.CO;2\u003c/li\u003e\n \u003cli\u003eAdam, P. J., \u0026amp; Berta, A. (2002). Evolution of prey capture strategies and diet in the Pinnipedimorpha (Mammalia, Carnivora). Oryctos, 4(3\u0026ndash;8), 3\u0026ndash;27.\u003c/li\u003e\n \u003cli\u003eBischof, R., Bonenfant, C., Rivrud, I. M., Zedrosser, A., Friebe, A., Coulson, T., Mysterud, A., \u0026amp; Swenson, J. E. (2018). 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Development of a fatted male phenomenon in California sea lions. Developmental Psychobiology, 4(4), 333\u0026ndash;338. https://doi.org/10.1002/dev.420040406\u003c/li\u003e\n \u003cli\u003eSegura, V., \u0026amp; Prevosti, F. (2012). A quantitative approach to the cranial ontogeny of Lycalopex culpaeus (Carnivora: Canidae). Zoomorphology, 131(1), 79\u0026ndash;92.\u003c/li\u003e\n \u003cli\u003eSwenson, J. E., Adamič, M., Huber, D., \u0026amp; Stokke, S. (2007). Brown bear body mass and growth in northern and southern Europe. Oecologia, 153(1), 37\u0026ndash;47. https://doi.org/10.1007/s00442-007-0715-1\u003c/li\u003e\n \u003cli\u003eTanner, J. B., Zelditch, M. L., Lundrigan, B. L., \u0026amp; Holekamp, K. E. (2010). Ontogenetic change in skull morphology and mechanical advantage in the spotted hyena (Crocuta crocuta). Journal of Morphology, 271(3), 353\u0026ndash;365.\u003c/li\u003e\n \u003cli\u003eTarnawski, B. A., Cassini, G. H., \u0026amp; Flores, D. A. (2014a). Allometry of the postnatal cranial ontogeny and sexual dimorphism in Otaria byronia (Otariidae). Acta Theriologica, 59, 81\u0026ndash;97.\u003c/li\u003e\n \u003cli\u003eTarnawski, B. A., Cassini, G. H., \u0026amp; Flores, D. A. (2014b). Skull allometry and sexual dimorphism in the ontogeny of the southern elephant seal (Mirounga leonina). Canadian Journal of Zoology, 92(1), 19\u0026ndash;31.\u003c/li\u003e\n \u003cli\u003eTarnawski, B. A., Flores, D., Cassini, G., \u0026amp; Cappozzo, L. H. (2015). A comparative analysis on cranial ontogeny of South American fur seals (Otariidae: Arctocephalus). Zoological Journal of the Linnean Society, 173(1), 249\u0026ndash;269.\u003c/li\u003e\n \u003cli\u003eThorsteinson, F. V., \u0026amp; Lensink, C. J. (1962). Biological Observations of Steller Sea Lions Taken during an Experimental Harvest. The Journal of Wildlife Management, 26(4), 353\u0026ndash;359. https://doi.org/10.2307/3798011\u003c/li\u003e\n \u003cli\u003eWuersig, B., Thewissen, J. G. M., \u0026amp; Kovacs, K. M. (2017). Encyclopedia of Marine Mammals. Academic Press.\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables 1 to 4 are available in the Supplementary Files section.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-3872222/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3872222/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eSuction feeding is a specific behavior in pinnipeds such as the Steller sea lion (\u003cem\u003eEumetopias jubatus\u003c/em\u003e), whereas the phylogenetically related brown bear (\u003cem\u003eUrsus arctos\u003c/em\u003e) ingests by masticatory feeding. Because these feeding modes use different organs, the morphology and ontogeny of the cranial bones of these species may be related to differences in their feeding behavior. In this study, we performed multiple regression analyses to compare the ontogeny of Steller sea lion and brown bear cranial morphology by species and sex, using age, species, and the age \u0026times; species interaction as explanatory variables and site measurements standardized by cranial length as response variables. The results showed that the palatine bone in both sexes widened with age in Steller sea lions compared to brown bears, whereas the width of the zygomatic arch was less developed in female Steller sea lions than in brown bears. This result may reflect the fact that the masticatory muscles are used less during suction feeding, whereas the tongue is used to perform force-intensive tasks. These results are consistent with previous studies on Carnivora and suggest that the development of the palatine bone and underdevelopment of the zygomatic arch represent characteristics of suction feeding.\u003c/p\u003e","manuscriptTitle":"Cranial ontogeny in Steller sea lions: Relationships between cranial morphology and suction feeding","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-01-19 08:57:42","doi":"10.21203/rs.3.rs-3872222/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"50b40b54-16d0-450e-bf0e-33a663a19380","owner":[],"postedDate":"January 19th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2025-05-20T04:53:10+00:00","versionOfRecord":[],"versionCreatedAt":"2024-01-19 08:57:42","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3872222","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3872222","identity":"rs-3872222","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}