THE ANATOMICAL RECORD 298:643–647 (2015)

Introduction to the Anatomy of the Head of a Neonate Gray Whale (Mysticeti, Eschrichtius robustus)  E,  2 ANNALISA BERTA,1* ERIC G. EKDALE,1 THOMAS A. DEMER 3 AND JOY S. REIDENBERG 1 Department of Biology, San Diego State University, San Diego, California 2 Department of Paleontology, San Diego Natural History Museum, San Diego, California 3 Center for Anatomy and Functional Morphology, Mount Sinai School of Medicine, New York, New York

ABSTRACT The gray whale (Eschrichtius robustus) is the sole living representative of the mysticete (baleen whale) family Eschrichtiidae. Previous anatomical work on gray whales has been limited owing, in part, to difficulties of specimen access. These contributions to the anatomy of the gray whale head based on dissection of a stranded specimen from northern California include detailed investigation of internal and external features that confirm existing information and provide new evidence for their functional roles, particularly in thermoregulation and feeding. Anat C 2015 Wiley Periodicals, Inc. Rec, 298:643–647, 2015. V

Key words: Gray whale; head anatomy; musculature

The research presented in this Thematic Papers issue of The Anatomical Record is based on a series of dissections of the head of a neonate gray whale, Eschrichtius robustus, that were conducted during 2012 and 2013 at San Diego State University (SDSU) in San Diego, California, USA. The goal of this collection of papers is to provide detailed observations of the external morphology, cranial anatomy, and musculature of the gray whale head. The baleen whale suborder, Mysticeti, is composed of four extant families: Eschrichtiidae (gray whales), Balaenopteridae (rorquals), Balaenidae (right whales), and Neobalaenidae (pygmy right whales). Eschrichtiidae is currently composed of a single extant species, Eschrichtius robustus, although several extinct taxa are known (e.g. Bisconti, 2003, 2005). The gray whale has often been phylogenetically placed as sister to the rorq ual clade, Balaenopteridae (e.g., Arnason et al., 2004; Rychel et al., 2004; Demere et al., 2008). Although most morphological and combined data studies unite Eschrichtiidae and Balaenopteridae into the more inclusive superfamily Balaenopteroidea (e.g. Demere et al., 2005, 2008; McGowen et al., 2009), many molecular studies position gray whales as nested within a paraphyletic Balaenopteridae (Fig. 1; McGowen et al., 2009; Gatesy et al., 2013). C 2015 WILEY PERIODICALS, INC. V

Gray whales differ both anatomically and ecologically from other extant mysticetes. In general, Eschrichtius is externally characterized by having a nearly uniform mottled gray skin, broad paddle-shaped flippers, a dorsal hump followed by a row of knobs (often referred to as “knuckles”) that extend onto the peduncle, dorsoventrally short, yellowish-white baleen, a slightly arched and transversely narrow rostrum, several short throat grooves, and a distinctly triangular head in cross section (Jefferson et al., 2008; Jones and Schwartz, 1984; Demere et al., 2005). Eschrichtius robustus differs from other mysticetes in its highly specialized benthic suction feeding strategy (Goldbogen et al., 2011; Nerini, 1984). During feeding, E. robustus will dive to muddy portions of the floor of the continental shelf, roll to one side, and engulf prey-laden sediment, laterally, into the oral cavity. Sediment and water is then pumped out of the

*Correspondence to: Annalisa Berta, Department of Biology, San Diego State University, San Diego, CA 92182. Fax: 5945676. E-mail: [email protected] Received 28 October 2013; Revised 10 February 2014; Accepted 2 September 2014. DOI 10.1002/ar.23110 Published online 3 March 2015 in Wiley Online Library (wileyonlinelibrary.com).

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Fig. 1. Phylogenetic position of mysticetes among cetartiodactyls (following Gatesy et al., 2013) and differing hypotheses for the position of Eschrichtius robustus (gray whale) among extant mysticetes based  re  et al., 2005; Marx, 2011) and molecular data on the right on morphological data on the left (e.g., Deme (e.g., McGowen et al., 2009; Gatesy et al., 2013). Artwork by Carl Buell.

mouth and through the baleen sieve, which separates the target prey from the matrix slurry (Jones and Swartz, 2009). The gray whale, once commercially hunted nearly to extinction, has made a remarkable comeback in population size from only a few thousand individuals prior to 1946 to more than 20,000 individuals today (Rugh et al., 2005). Although gray whales essentially are restricted to the North Pacific, they formerly occurred on both sides of the North Atlantic as well, but were extirpated from that ocean basin by the 1700s (Mead and Mitchell, 1984). The May 2010 report of a gray whale in the Mediterranean Sea suggests a recent dispersal event through the Arctic Ocean and into the North Atlantic

(Scheinin et al., 2011). This dramatic recovery in population size and the apparent beginnings of re-colonization of once occupied territory makes the gray whale arguably the best example of a successful conservation effort for a great whale. In large part because of the nearly fatal impact of commercial whaling on gray whales in the 19th and early 20th centuries, scientific studies of this species were extremely limited in the past. The earliest detailed anatomical work on the gray whale was that of Andrews (1914) which included an account of the natural history, external morphology, and skeletal anatomy of the species. Subsequent reports have focused more on the migratory behavior and conservation of gray whales and

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Fig. 2. Participants in the gray whale dissection at San Diego State University April, 2012. From left: J.  re , E. Martin, T. Cranford, K. Albertine (editor Anatomical Record), A. Berta (inserted), A. Martiny, T. Deme Ekdale, J. El Adli, J. Reidenberg (Mt. Sinai Medical School), W. Ary, L. Witmer (Ohio University Medical School), N. Zellmer, A. Zumwalt, J. Organ, and S. Kienle.

include the comprehensive volume on gray whale natural history (including some anatomy) by Jones et al. (1984) and several summary species accounts in larger edited volumes (e.g., Perrin et al., 2009). The recent description of selected features of the musculoskeletal anatomy of the head of a yearling male gray whale (Johnston et al., 2010) marks a return to more basic anatomical research. Given this limited amount of previous anatomical work on gray whales, many questions remain concerning the functional anatomy of Eschrichtius robustus. Access to specimens is a major factor hampering anatomical studies of mysticete whales, which is why the live stranding in January 2012 of a female gray whale calf on the beach in Moss Landing, Monterey County, California, USA was viewed as such an important event. The stranding report indicated that the calf (Moss Landing Marine Lab 2501) measured 394 cm in body length and weighed 225–320 kg. The calf was inferred to be a neonate based on the presence of fetal folds and an unhealed umbilicus. Total length data included in Sumich (1986) indicate that the calf falls within the size range of individuals of less than one month of age. Upon

consultation with a veterinarian, it was determined that the live-stranded calf would not survive if returned to the ocean, and was therefore humanely euthanized. Once deceased, the head of MLML 2501 was removed from the body by slicing through the joint between the occipital condyles and the atlas vertebra. Graduate students in Annalisa Berta’s lab at SDSU (Will Ary, Sarah Kienle, Jessica Martin, Samantha Young, and Nick Zellmer) travelled from San Diego to Moss Landing to retrieve the specimen and were assisted by Stephanie Hughes, Elizabeth McHuron, and Gary Adams of the Moss Landing Marine Lab. The head was then transferred to the San Diego Natural History Museum (SDNHM) where it was kept frozen until the time of initial dissection and in between the subsequent dissection sessions. Initial dissection of the head of the neonate gray whale took place on April 25–27, 2012, with several subsequent dissection sessions occurring in late 2012 and early 2013 in the SDSU Department of Biology. In addition to students in the Berta lab, local scientists involved with the dissection were Drs. Eric Ekdale (SDSU), Ted Cranford (SDSU), and Tom Demere

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(SDNHM). Other participants in the initial dissection session were Drs. Joy Reidenberg (Mt. Sinai School of Medicine), Larry Witmer (Ohio University), Kurt Albertine (University of Utah; editor of The Anatomical Record), Mr. Joseph El Adli (San Diego Natural History Museum), and several SDSU undergraduates: Daniel Silva, Meghan Smallcomb, and Mary Alice Chocas (Fig. 2). Upon completion of all dissections at SDSU, the skull, dentaries and right baleen rack were accessioned into the Mammal Collection at the San Diego Natural History Museum under catalogue number SDNHM 25307. In December 2012, a block of tissue containing the right ear region of the neonate was removed from the skull at the San Diego zoo’s necropsy lab with the assistance of Dr. Rebecca Papendick and April Gorow for future study. Additional tissue samples, including both eyeballs, were sent to other scientific institutions for independent research. The results of this research are not incorporated into this Thematic Papers issue. After the initial dissections, the head was CT scanned at the UCSD Hospital CT facility in La Jolla, California. On February 12 and 13, 2013, the blood vessels of the rostrum of SDNHM 25307 were injected with liquid latex mixed with a barium solution following preestablished protocols (Holliday et al., 2006). Barium is radio-opaque and registers on CT scans. This process allowed digital reconstruction of the course of the palatal blood vessels in situ and aided in the identification of specific arteries to the baleen and surrounding epithelium.The entire injected skull was then re-scanned at the UCSD –Medical Center in Hillcrest in San Diego with the assistance of Matt Costa and Diane Connelly. A final round of dissections focused on examination and removal of the right and left baleen racks, the gross anatomy of the blowhole region, the myology of the basicranial region, and the musculature and vascular anatomy of the tongue (originally removed from the skull in April 2012). The contributions to gray whale head anatomy compiled within this Thematic Papers issue include detailed investigations of external and internal features. Berta et al. (this issue) discuss the external morphology of the head, including sensory hairs, blowholes, throat grooves, the eye, and the first ever report of a vomeronasal organ in gray whales. Histological examination of sensory hairs on the rostrum were found to be of the follicle sinus type, which have been similarly documented in other mysticetes, but previously have been unstudied in gray whales where they, have an apparent tactile function. Kienle et al. (this issue) describe the tongue, hyoid apparatus, and associated musculature. They report the presence of taste buds for the first time in mysticetes, as well as a unique position and fiber orientation of the genioglossus muscle that is hypothesized to be related to suction feeding. Ekdale and Kienle (this issue) confirm the presence of lingual retia in the tongue and discuss the hypothesis that the structures serve a thermoregulatory function in the species. The anatomy of the temporomandibular joint and its associated musculature are described for the first time by El Adli and Demere (this issue). They report a unique configuration of the temporomandibular joint, and discuss the temporomandibular musculature as it relates to feeding and as it compares to that of rorquals. Palate

vasculature and its implications for the origin and evolution of baleen were investigated using dissection, latex injection, and CT scanning by Ekdale et al. (this issue). They confirmed that baleen epithelium receives blood from branches of the superior alveolar artery and that these vessels are transmitted to the maxilla via the lateral palatal foramina. These results are consistent with the hypothesis that homologous lateral palatal foramina observed in fossil mysticetes are bony correlates for the presence of baleen in extinct taxa (Demere et al., 2008). Furthermore, a thermoregulatory hypothesis is proposed here in addition to a previous suggestion that an increase in palate vascularization may be related to rostral expansion. A final paper by Young et al. (this issue) incorporates measurements of the baleen of SDNHM 25307 in addition to other young gray whale baleen racks in one of the first morphometric studies of the baleen apparatus. Features of the baleen including variation in the laminae, plate and bristle morphology and structure are discussed as they relate to both feeding and baleen evolution. The research presented within this Thematic Papers issue of the Anatomical Record provide some of the first comprehensive studies of the gross anatomy of the gray whale, Eschrichtius robustus. These detailed descriptions elucidate the complex morphology of the gray whale, and contribute to an understanding of the overall poorly-known anatomy of mysticetes. Though much is still to be learned about the anatomy of the gray whale and its implications for evolutionary history and ecology, it is the hope of the authors that this research provides the foundation for an in depth understanding of this exemplary mysticete, and for mysticetes as a whole.

LITERATURE CITED Andrews RC. 1914. The California gray whale (Rhacianectes glaucus Cope): its history, habits, external anatomy, osteology and relationship. Monographs of the Pacific Cetacea. Mem Am Museum Nat Hist 1:227–287.  Arnason U, Gullberg A, Janke A. 2004. Mitogenomic analyses provide new insights into cetacean origin and evolution. Gene 333: 27–34. Bisconti M. 2003. Evolutionary history of Balaenidae. Cranium 20: 9–50. Bisconti M. 2005. Skull morphology and phylogenetic relationship of a new diminutive balaenid form the lower Pliocene of Belgium. Palaeo 48:793–816. Dem er e TA, Berta A, McGowen MR. 2005. The taxonomic and evolutionary history of fossil and modern balaenopteroid mysticetes. J Mamm Evol 12:99–143. Dem er e TA, McGowen MR, Berta A, Gatesy J. 2008. Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Syst Biol 57:15–37. Gatesy J, Geisler JH, Chang J, Buell C, Berta A, Springer MS, McGowen MR. 2013. A phylogenetic blueprint for a modern whale. Mol Phylogenet Evol 6: 479–506. Goldbogen J, Calambokidis J, Oleson E, Potvin J, Pyenson ND, Schorr G, Shadwick R. 2011. Mechanics, hydrodynamics and energetics of blue whale lunge feeding: efficiency dependence on krill density. J Exp Biol 214:131–146. Holliday CM, Ridgely RC, Balanoff A, Witmer LG. 2006. Cephalic vascular anatomy in flamingos (Phoenicopterus ruber) based on novel vascular injection and computed tomographic imaging analyses. Anat Rec 288A:1031–1041.

ANATOMY OF THE HEAD OF A NEONATE GRAY WHALE Jefferson TA, Webber M, Pitman RL. 2008. Marine mammals of the world. San Diego, CA: Academic Press. Johnston C, Dem er e TA, Berta A, Yonas J, St. Leger J. 2010. Observations on the musculoskeletal anatomy of the head of a neonate gray whale (Eschrichtius robustus). Mar Mamm Sci 26: 186–194. Jones ML, Swartz SL, Leatherwood S, editors. 1984. The Gray Whale, Eschrichtius robustus. San Diego: Academic Press. Jones LJ, Swartz SL. 2009. Gray Whale, Eschrichtius robustus. In: Perrin WF, Wursig B, Thewissen JGM, editors. Encyclopedia of marine mammals. 2nd ed. San Diego: Academic Press. p 503–511. Mead JG, Mitchell ED. 1984. Atlantic gray whales. In: Jones ML, Swartz SL, Leatherwood S, Folkens PA, editors. The gray whale: Eschrichtius robustus. San Diego, CA: Academic Press. p 33–53. Marx F. 2011. The more the merrier: a large cladistic analysis of mysticetes, and comments on the transition from teeth to baleen. J Mamm Evol 18:77–100. McGowen M, Spaulding M, Gatesy J. 2009. Divergence estimation and a comprehensive molecular tree of extant cetaceans. Mol Phylogenet Evol 53:891–906.

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Nerini M. 1984. A review of gray whale feeding ecology. In: Jones ML, Swartz SL, Leatherwood S, Folkens PA, editors. The gray whale: Eschrichtius robustus. Orlando, FL: Academic Press. p. 423–450. Perrin WF, Wursig B, and Thewissen JGM, editors. 2009. Encyclopedia of Marine Mammals. 2nd ed. San Diego: Academic Press. Rugh DJ, Hobbs RC, Lerczak JA, Breiwick JM. 2005. Estimates of abundance of the eastern Pacific stock of gray whales (Eschrictius robustus) 1997–2002. J Cetacean Res Manag 7:1–12. Rychel AL, Reeder TW, Berta A. 2004. Phylogeny of mysticete whales based on mitochondrial and nuclear data. Mol Phylogenet Evol 32:892–901. Scheinin AP, Kerem D, MacLeod CD, Gazo M, Chicote CA, Castellote M. 2011. Gray whale (Eschrichtius robustus) in the Mediterranean Sea: anomalous event or early sign of climatedriven distribution change? Mar Biodiv Rec 4:e28. Sumich JL. 1986. Growth in young gray whales (Eschrichtius robustus). Mar Mamm Sci 2:145–152.

Introduction to the anatomy of the head of a neonate gray whale (Mysticeti, Eschrichtius robustus).

The gray whale (Eschrichtius robustus) is the sole living representative of the mysticete (baleen whale) family Eschrichtiidae. Previous anatomical wo...
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