CRANIAL SHAPE CORRELATES WITH DIET SPECIALIZATION IN NORTHEAST PACIFIC KILLER WHALE (ORCINUS ORCA) ECOTYPES. by Charissa W. Fung B.Sc., The University of Calgary, 1999 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Zoology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) August 2016 © Charissa W. Fung, 2016 1 Abstract Resident, transient (Bigg’s), and offshore killer whales (Orcinus orca) live in sympatric and parapatric ranges in the northeast Pacific Ocean. These ecotypes have different vocal repertoires (Ford and Fisher, 1982; Ford, 1991; Yurk, 2002), echolocation use (Barrett-Lennard et al., 1996), foraging strategies (Bigg et al., 1987; Ford et al., 1998; Baird et al., 1992; Deecke et al., 2002; Ford et al., 2011), and sociobiology (Ford and Fisher, 1982; Bigg et al., 1987; Deecke et al., 2000; Baird and Whitehead, 2000; Riesch et al., 2012). Genetic studies corroborate the behavioural evidence that the resident and transient (Bigg’s) populations are reproductively isolated despite the absence of any geographic or temporal barrier (Stevens et al., 1989; Barrett-Lennard, 2000; Hoelzel and Dover, 1991; Morin et al., 2010). The behavioural segregation between the sympatric ecotypes is apparently maintained by cultural mechanisms alone, which is extremely unusual among non-human mammalian species (Barrett-Lennard, 2000; Riesch et al., 2012). These ecotypes also exhibit dramatic resource polymorphisms: resident killer whales feed exclusively on fish, transient (Bigg’s) killer whales primarily hunt marine mammals (Bigg, 1982; Baird et al., 1992, Ford et al., 1998) and offshore killer whales are thought to feed on fishes including Pacific sleeper shark (Somniosus pacificus) (Ford et al., 2011). We do not know if cranial features related to capturing and processing prey have evolved to reflect the dramatic dietary specializations observed in these three ecotypes. The goal of this research was to determine whether there has been divergence of cranial morphology among the three ecotypes. To this end, I measured and compared cranial shape using traditional and geometric morphometrics techniques. I found that transient (Bigg’s) killer whales that bite and tear apart large mammals have more robust cranial skeletons than the piscivorous resident and offshore killer whales that handle smaller prey items. I found that resident and transient (Bigg’s) killer whales are distinguishable based on skull width, rostral width, and mandibular shape, and that offshore killer whales have a more variable morphology that precludes identification based on cranial shape alone. ii Preface Charissa Fung developed this research project under the guidance of Dr. William K. Milsom and Dr. Lance Barrett- Lennard. All of the morphological data were collected and analyzed by C. Fung, with statistical advice from Dr. Douglas Altshuler and Dr. Roslyn Dakin, and R programming assistance from Shannon Obradovich. Dr. Lance Barrett-Lennard and Allyson Miscampbell provided genetic identification of skeletal material. iii Table of contents Abstract ................................................................................................................................................. ii Preface .................................................................................................................................................. iii Table of contents................................................................................................................................... iv List of figures ........................................................................................................................................ ix List of abbreviations: museums and institutions ................................................................................ xii List of abbreviations: data collection ................................................................................................. xiii List of abbreviations: data analysis .................................................................................................... xv Acknowledgements ............................................................................................................................. xvi Dedication ......................................................................................................................................... xviii Chapter 1: General introduction .......................................................................................................... 1 1.1 Killer whale (Orcinus orca) diversification and taxonomic uncertainty .................................. 1 1.2 Resident, transient (Bigg’s), and offshore killer whale ecotypes of the northeast Pacific Ocean .....................................................................................................................................................1 1.2.1 Distribution and movement patterns of northeast Pacific ecotypes................................... 2 1.2.2 Behavioural differences between ecotypes ...................................................................... 4 1.2.3 Field observations of morphological differences in ecotypes ........................................... 5 1.2.4 Dietary differences/trophic level differences among ecotypes ......................................... 6 1.2.4.1 Resident killer whales hunt salmonids ..................................................................... 6 1.2.4.2 Offshore killer whales feed on fishes (e.g., Pacific sleeper shark) ............................ 7 1.2.4.3 Transient (Bigg’s) killer whales hunt marine mammals............................................ 7 1.2.5 Dentition differences between ecotypes .......................................................................... 9 1.2.6 Inference of jaw function from simplified lever system and muscle attachment ............. 10 1.3 Summary................................................................................................................................. 10 iv Chapter 2: Comparison of cranial shape among northeast Pacific killer whale ecotypes ................. 11 2.1 Introduction ......................................................................................................................... 11 2.2 Materials and methods ......................................................................................................... 12 2.2.1 Measuring cranial morphology: geometric morphometrics and traditional morphometrics ............................................................................................................................................12 2.2.2 Cranial skeleton anatomy.............................................................................................. 13 2.2.3 Materials ...................................................................................................................... 18 2.2.3.1 Specimens ............................................................................................................. 18 2.2.3.2 Ecotype assignment ............................................................................................... 19 2.2.4 Traditional morphometrics measurements ..................................................................... 22 2.2.4.1 Linear measurements............................................................................................. 22 2.2.4.2 Traditional morphometrics - analysis ..................................................................... 22 2.2.5 Geometric morphometrics ............................................................................................ 26 2.2.5.1 Standardized photography protocol ....................................................................... 26 2.2.5.2 Landmark digitization from standardized photographs and analyses of landmark coordinates ........................................................................................................................... 28 2.2.5.3 Geometric morphometrics - analysis ...................................................................... 28 2.3 Results................................................................................................................................. 30 2.3.1 Total body length and condylobasal length measurements............................................. 30 2.3.2 Results from traditional morphometrics of cranium and dentary bone ........................... 30 2.3.2.1 Overall skull width and height across the vault and occipital regions ..................... 33 2.3.2.2 Rostrum (facial bones and the palate) .................................................................... 33 2.3.2.3 Bones associated with jaw adductor muscles (temporalis) ...................................... 33 2.3.2.4 Length of tooth-bearing alveolar bones on maxilla and dentary .............................. 44 2.3.2.5 Dentary bone shape ............................................................................................... 44 v 2.3.2.6 The foramen magnum, occipital condyles, and internal nares ................................. 44 2.3.3 Results from geometric morphometrics ......................................................................... 50 2.3.3.1 Cranium, dorsal view ............................................................................................ 50 2.3.3.1.1 PCA of Procrustes coordinates, dorsal view of cranium .................................