Research methods and Comparative examination of pinniped craniofacial musculature and its role in aquatic feeding
Description
Secondarily aquatic tetrapods have many unique morphological adaptations for life underwater compared to their terrestrial counterparts. A key innovation during the land-to-water transition was feeding. Pinnipeds, a clade of air-breathing marine carnivorans that includes seals, sea lions, and walruses, have evolved multiple strategies for aquatic feeding (e.g., biting, suction feeding). Numerous studies have examined pinniped skull and dental specializations for underwater feeding. However, data on the pinniped craniofacial musculoskeletal system and its role in aquatic feeding are rare. Therefore, the objectives of this study were to conduct a comparative analysis of pinniped craniofacial musculature and examine the function of the craniofacial musculature in facilitating different aquatic feeding strategies. We performed anatomical dissections of 35 specimens across six pinniped species. We describe 32 pinniped craniofacial muscles—including facial expression, mastication, tongue, hyoid, and soft palate muscles. Pinnipeds broadly conform to mammalian patterns of craniofacial muscle morphology. Pinnipeds also exhibit unique musculoskeletal morphologies—in muscle position, attachments, and size—that likely represent adaptations for different aquatic feeding strategies. Suction feeding specialists (bearded and northern elephant seals) have a significantly larger masseter than biters. Further, northern elephant seals have large and unique tongue and hyoid muscle morphologies compared with other pinniped species. These morphological changes likely help generate and withstand suction pressures necessary for drawing water and prey into the mouth. In contrast, biting taxa (California sea lions, harbor, ringed, and Weddell seals) do not exhibit consistent craniofacial musculoskeletal adaptations that differentiate them from suction feeders. Generally, we discover that all pinnipeds have well-developed and robust craniofacial musculature. Pinniped head musculature plays an important role in facilitating different aquatic feeding strategies. Together with behavioral and kinematic studies, our data suggest that pinnipeds' robust facial morphology allows animals to switch feeding strategies depending on the environmental context—a critical skill in a heterogeneous and rapidly changing underwater habitat.
Notes
In situ measurements—maximum length (straight rostral-caudal distance from rostral tip of skull to caudal edge of occipital condyles), width (straight medio-lateral distance from lateral edges of zygomatic arch), and depth (straight dorso-ventral distance from sagittal crest to auditory bullae)—were measured for each muscle when possible. We used scaled photographs to take ex situ measurements of the maximum length and width of each muscle in two-dimensions in ImageJ. Muscle area was calculated from tracing the perimeter of the muscle in scaled photographs. We then calculated the muscle-to-skull area ratio (MSR) for each muscle, which was obtained by dividing each muscle area by the skull area to standardize for head size. We calculated mean MSR for each craniofacial muscle group within each species (e.g., facial expression, mastication, tongue, hyoid, and soft palate) for interspecific comparisons.
We ran linear models to compare the relationship between relative muscle size (MSR), species, and feeding strategy and determined significance using ANOVAs (car package; Fox & Weisberg 2011; Bates et al. 2015). We examined the relationship between muscle size and species with species as the predictor variable and between muscle size and feeding strategy with feeding strategy as the predictor variable. We used least-square means to perform Tukey post-hoc pairwise contrasts between each significant predictor variable (lsmeans package; Lenth, 2016). Residual plots for each model were examined for deviations from normality and homoscedasticity. When heteroscedasticity was observed, data were log-transformed.
Additionally, we examined variability in MSR for each muscle and species by quantifying the coefficient of variation [CV, standard deviation (s.d.)/mean] for each muscle. The CV measures variation in a trait. A low CV (values close to 0) indicates stereotypy, while a high CV (values close to 1) indicates high variability (Gerhardt, 1991; Wainwright et al., 2008). All statistical analyses were conducted in R v. 3.5.3 (R Core Team, 2019).
Funding provided by: National Oceanic and Atmospheric Administration
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000192
Award Number: Dr. Nancy Foster Scholarship Program
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- 10.5281/zenodo.6585360 (DOI)