1 Quantifying the Link Between Craniodental Morphology and Diet

Home , Myosorex, Myosoricinae, Nectogalini, Notiosorex, Notiosoricini, Scutisorex

Quantifying the link between craniodental morphology and diet in Soricidae using

geometric morphometrics

Thesis

Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in

the Graduate School of The Ohio State University

Yuen Ting Tse

Graduate Program in Evolution, Ecology and Organismal Biology

The Ohio State University

2020

Thesis Committee

Jonathan Calede, Advisor

Andreas Chavez

John Hunter

Copyrighted by

Yuen Ting Tse

2020

Abstract

The family Soricidae is one of the most species-rich mammalian families and much attention has been given to studying population-level variation in morphology and genetics, systematics, and morphological disparity within soricids. However, little work has been undertaken on the ecomorphology of shrews. Here, I seek to determine if the variation in craniodental morphology observed among shrew species reflects adaptations to diet, specifically to the hardness of the food consumed. I use geometric morphometrics to capture the variation in skull and dentary morphology within a sample of 136 shrew specimens representing 42 species spanning all three sub-families of Soricidae. My analyses demonstrate that morphology is associated with dietary ecology. Specifically, species that consume hard food items have specific morphological adaptions including an anteroposteriorly expanded parietal, an anteroposteriorly short and dorsoventrally tall rostrum, a mediolaterally wide palate, buccolingually wide cheek teeth, a large coronoid process, and a dorsoventrally short jaw joint. The m. masseter does not play an important role in the strong bite force of shrews. The dentary is a better indicator of ecology than the skull. The results of my analyses also support a role of size in the ability of shrews to capture and process hard preys. A phylogenetic flexible discriminant function analysis suggests that the evolutionary history of shrews has shaped their morphology canalizing dietary adaptations and enabling functional equivalence whereby different morphologies

ii achieve similar dietary performances. My results would enable additional studies of niche partitioning among sympatric species; it may also be used to investigate the diet of extinct Soricidae.

iii

Acknowledgments

I thank the following people for access to the specimens in their care: John Wible and

Suzanne McLaren (CM), Roberta Muehlheim (CMNH), Tamaki Yuri and Meg Daly

(OSU), Jim Dines (LACM), and Darrin Lunde (USNM). I thank my committee members,

Dr. Jonathan Calede, Dr. John Hunter, and Dr. Andreas Chavez, for providing me with tremendous feedbacks, recommendations, and/or access to their laboratory resources. I also want to acknowledge Stephanie Smith for providing constructive feedbacks on my analyses. Funding for this research was provided by The Ohio State University to J.

Calede. Silhouette images used in the figures were uploaded to Phylopic

(http://phylopic.org/) by Birgit Lang, Javier Luque, Maxime Dahirel, Michael Keesey, and Scott Hartman.

Vita

2014...... Skagit Valley College

2016...... B.S. in General Biology, University of

Washington

2015 to 2017 ...... Research Assistance in Paleontology, Sidor

Lab and Wilson Lab, University of

Washington

August 2018 to August 2020 ...... Graduate Teaching Associate, Department

of Evolution, Ecology, and Organismal

Biology, The Ohio State University

Publications

Whitney, M. R., Y. Tse, and C. A. Sidor. 2019. Histological evidence of trauma in tusks of southern African dicynodonts. Palaeontologia Africana 53:75-80.

Fields of Study

Major Field: Evolution, Ecology and Organismal Biology

Table of Contents

Abstract ...... ii Acknowledgments...... iv Vita ...... v List of Tables ...... viii List of Figures ...... ix Introduction ...... 1 Materials and Methods ...... 7 Sampling ...... 7 Landmarking ...... 8 Food hardness data ...... 18 Analyses ...... 19 Analyses of functional units of the skull ...... 20 Analyses of centroid size ...... 21 Analysis of coronoid-mandibular articulation distance ...... 22 Phylogenetic flexible discriminant function analysis (pFDA) ...... 22 Institutional abbreviations ...... 23 Results ...... 24 Centroid size distribution ...... 24 Principal component analyses ...... 26 Lateral skull ...... 26 Ventral skull ...... 28 Lateral dentary ...... 29 Canonical variate analyses ...... 31 Temporalis, masseter, and dental units ...... 35 Phylogenetic flexible discriminant function analysis (pFDA) ...... 35 vi

Discussion ...... 37 Bibliography ...... 45 Appendix A. List of all shrew species included in the analyses, their diet category, and supporting diet data ...... 57 Appendix B. References for diet data in Appendix A...... 64 Appendix C. Figures showing cranial musculature of dissected Sorex trowbridgii...... 69

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List of Tables

Table 1. List of all of the Soricidae species included in the analyses and their diet category...... 9

Table 2. Landmarks (L) and semi-landmarks (SL) of the lateral skull analysis and the biological variables they characterize ...... 12

Table 3. Landmarks (L) and semi-landmarks (SL) of the ventral skull analysis and the biological variables they characterize ...... 13

Table 4. Landmarks (L) and semi-landmarks (SL) of the lateral dentary analysis and the biological variables they characterize...... 14

Table 5. Origin, insertion, and action of muscles associated with food processing by the jaw apparatus ...... 16

Table 6. Hardness categorization for major invertebrate prey items of Soricidae ...... 19

Table 7. Overall classification accuracy (%) for the individual craniodental orientations

(lateral skull, ventral skull, lateral dentary), the three craniodental units (temporalis, masseter, dental), CVA when all craniodental orientations are considered, and pDFA when all craniodental orientations are considered...... 32

viii

List of Figures

Figure 1. Landmarking scheme shown on Blarina brevicauda (lateral skull, ventral skull) and Suncus murinus (lateral dentary) ...... 11

Figure 2. Box plot showing the centroid sizes of the (a) lateral skull, (b) ventral skull, and

Figure 3. Results of the PCA of the lateral skull when all landmarks are included in the analysis ...... 27

Figure 4. Results of the PCA for the ventral skull when all landmarks are included in the analysis ...... 29

Figure 5. Results of the PCA for the lateral dentary when all landmarks are included in the analysis ...... 31

Figure 6. Overall percent classification accuracy when all three craniodental orientations are included in the analysis for both (a) CVA and (b) pFDA ...... 33

Figure 7. Lateral view of skull of dissected Sorex trowbridgii. Colors: blue circle, temporalis; red circle, masseter...... 69

Figure 8. Dorsal view of skull of dissected Sorex trowbridgii ...... 70

Figure 9. Ventral view of skull of dissected Sorex trowbridgii ...... 71

Introduction

Many ecomorphological studies have investigated the link between morphological diversity, dietary specialization, and evolutionary success (e.g., Dumont et al. 2012; Price et al. 2012; Monteiro and Nogueira 2011; Santana and Dumont 2009; Rossoni et al.

2017). Such work has shown that dietary specializations and niche diversifications associated with morphological adaptations have enabled the radiations of several mammalian clades (Arbour et al. 2019; Freeman 2000; Samuels 2009; Monteiro and

Nogueira 2011; Santana and Dumont 2009; Rossoni et al. 2017). Most of this work has focused on taxa with very different diets (e.g., Nogueira et al. 2009; Verde Arregoitia et al. 2017) and diverse skull morphologies, sometimes dramatically so (e.g., Lazagabaster et al. 2016; Hedrick and Dumont 2018). These analyses have shed light on the evolution of the most diverse mammalian orders: rodents, bats, and artiodactyls. Other studies have also investigated the roles of morphological adaptations and diet in the evolution of carnivores (Slater and Friscia 2019) and primates (Aristide et al. 2018; Marroig and

Cheverud 2005). One of the mammalian orders that conspicuously remains to be studied is the order Eulipotyphla. It is the fourth most-species rich order within Mammalia

(Burgin et al. 2018) and has the potential to shed light on evolutionary processes associated with radiation in a clade with a narrower range of diets and cranial

1 morphologies. Within Eulipotyphla, shrews are the most species-rich family; they represent over 83% of the species richness of the order.

The family Soricidae includes 440 species, more species in fact than all but three of the 167 families of mammals (Burgin et al. 2018). Although the family is relatively more homogenous ecologically than many other mammalian families (e.g.,

Phyllostomidae [Santana and Dumont 2009], Cricetidae and Muridae [Verde Arregoitia et al. 2017]), shrews feed on a wide range of invertebrates and other foods (e.g.,

Churchfield et al. 1999; Hamilton 1941; McCay and Storm 1997; Whitaker and Mumford

1972; Whitaker 1974). Some shrews feed mostly on softer foods including annelids; others prefer hard gastropods and arthropods (Hamilton 1941; Whitaker and Mumford

1972; McCay and Storm 1997; Churchfield et al. 1999). There are several species that partially feed on vertebrates or vegetation (Hamilton 1941; Whitaker and Mumford 1972;

McCay and Storm 1997; Whitaker and Ruckdeschel 2006), and some shrews are among the few venomous mammals (Pournelle 1968; Martin 1981; Dufton 1992; Lopez-Jurado and Mateo 1996).

The dietary range of animals is determined in large part by the biomechanical capabilities of their jaws (Herrel and O’Reilly 2006; Verwaijen et al. 2002; Wilson et al.

2016). Consequently, craniodental morphology is a powerful predictor of diet (e.g.,

Dumont et al. 2016; Maestri et al. 2016; Hedrick & Dumont 2018) and is often used to determine the feeding preferences of many extant and extinct taxa (e.g., Mendoza et al.

2002; Samuels 2009; Casanovas-Vilar and van Dam 2013). Such analyses have, for example, inferred the broad levels of carnivory of fossil dogs (Van Valkenburgh and

Koepfli 1993; Van Valkenburgh 2007; Friscia et al. 2007) and distinguished browsing from grazing ungulates (Mendoza et al. 2002).

One of the determinants of dietary range is bite force (Gignac and Erickson 2016;

Herrel and O’Reilly 2006; Verwaijen et al. 2002). The ability to generate a strong bite force enables an animal to access a large number of food resources (e.g., Herrel and

O’Reilly 2006; Verwaijen et al. 2002; Cornette et al. 2015; Wilson et al. 2016; Maestri et al. 2016; Monteiro and Nogueira 2011; Santana and Dumont 2009). It is also associated with morphological adaptation in skull height, rostrum length, and coronoid height, among others, that can be quantified (e.g., Pérez-Barbería and Gordon 1999; Herrel et al.

2002; Herrel and Holanova 2008; Nogueira et al. 2009; Slater et al. 2009). Numerous studies have therefore focused on assessing the bite force of both modern and extinct mammals to better understand their dietary ecology (e.g., Calede et al. 2018; Pérez-

Barbería and Gordon 1999; Wilson et al. 2016; Wroe et al. 2005, Young et al. 2007).

In this study, I explore the relationship between dietary specializations and craniodental morphology across a broad sample of shrew species focusing on bite force. I test the hypothesis that the craniodental morphology of shrews modulates their dietary ecology through biomechanical adaptations. This hypothesis is grounded in the strong potential for selection of dietary adaptations in Soricidae. Indeed, shrews have a very high metabolism, and therefore a very high demand for food (Vogel 1976; Hanski 1984).

Their ability to feed efficiently is paramount to their survival (Vogel 1980; Crowford

1954). I therefore expect the morphology of their feeding apparatus to be optimized for their food intake. Additionally, bite force has been specifically mentioned to likely be

3 under strong selection in shrews (Cornette et al. 2015). I predict that species that process different levels of food hardness have distinct morphologies that reflect an increase in bite force in hard food consumers relative to soft food consumers. I also expect that the evolutionary history of shrews has contributed to the observed morphologies. In other words, shrew species that are closely related to each other would have similar morphologies even if they differ in their dietary habits as a result of their shared ancestry.

This pattern is widespread across analyses of animal morphology (e.g., Close and

Rayfield 2012; Felice and O’Connor 2014; Hall et al. 2012; Smith et al. 2018; Tarquini et al. 2018; Verde Arregoitia et al. 2017).

Prior studies of the dietary adaptations of the cranial osteology and myology of shrews have focused on the genus Sorex (Young et al. 2007, 2010). These studies used linear measurements, dissections of muscles, bite force estimations, and geometric morphometric analyses of the dentary to explore the roles of individual muscles, mandible size, and mandible shape in dietary adaptations. The results of this work support a pattern of functional equivalence whereby similar diets are achieved by distinct mandibular morphologies (Young et al. 2007) and mandibular musculatures (Young et al.

2010). Additionally, Sorex species from distinct dietary hardness categories exhibit morphologies characteristic of their diets. Thus, the distance between the coronoid and condyloid processes as well as the force angle are particularly indicative of mechanical potential and diet in this genus (Young et al. 2007). In the genus Crocidura, geometric morphometric analyses and calculations of mechanical potential have shown that bite force likely played an important role in the distribution of the genus across western

Europe and the Atlantic islands (Cornette et al. 2015). Higher bite forces would enable access to a broader dietary range and provide a competitive advantage in interspecific aggressions (Cornette et al. 2015). The same analysis does also suggest, however, that species might not be benefiting from high mechanical potential if they are highly variable in morphology intraspecifically (Cornette et al. 2015). The myology and feeding behavior of select species within both Crocidura and Sorex has also been studied (Pernetta 1977).

Only limited analyses have been undertaken outside of the genera Sorex and Crocidura; they have been limited to muscle dissections and comparative analyses of jaw movement during feeding on preys of different sizes by Suncus murinus (Dötsch 1986).

Within Sorex, other analyses have informed the relationship between morphology and dietary ecology by focusing on the development of shrew mandibles (Badyaev and

Foresman 2000; Badyaev and Foresman 2004; Badyaev et al. 2005). This work revealed that morphological integration plays a big role in shaping the dentary and drives development in Sorex (Badyaev and Foresman 2004; Badyaev et al. 2005). Additionally, changes in environments, which could affect prey availability, are associated with an increase in morphological variability in between the integrated regions of the mandible

(Badyaev and Foresman 2000); the highest levels of morphological variation are associated to areas of muscle attachments (Badyaev and Foresman 2004).

Several studies have already used geometric morphometrics to investigate the variation in craniomandibular morphology within species (e.g., Cornette et al. 2012;

Jacquet et al. 2013; Rychlik et al. 2006; White and Searle 2009; Shchipanov et al. 2014;

Shchipanov et al. 2016) or genera of shrews (e.g., Polly 2007; Polly et al. 2013; Zidarova

5 and Popov 2018). However, these analyses mostly explored morphological disparity, intraspecific as well as interspecific variation and systematics; few addressed ecological issues (but see Rey et al. 2019). Here, I use geometric morphometrics to undertake an analysis of the size and shape of the craniomandibular apparatus of shrews to explore ecomorphology. My analyses differ from prior studies in their broad taxonomic sampling.

By incorporating 42 different shrew species, I attempt to uncover patterns of morphological adaptations to a hard diet across the entire shrew family and test the hypotheses developed and tested solely in Sorex and Crocidura before.

The majority of studies of shrew morphology have focused on the dentary (e.g.,

Cornette et al. 2015; Young et al. 2007); only a few have included skull morphology

(e.g., Polly 2007; Polly et al. 2013). Here, I specifically include data from both skull and dentary to explore the convergence of patterns between these two units of the feeding apparatus. I also assess the differences among morphological regions of the craniodental apparatus to explore their relative adaptations to a hard diet. Finally, I explicitly consider the evolutionary history of Soricidae in my analyses by incorporating a phylogenetic framework. The geometric morphometric analysis of the dietary adaptations of shrews I present herein will help shed light on the ecomorphology of shrews and their evolutionary trajectory. My work is the first step towards the investigation of the evolutionary processes at play in the rise of this species-rich mammalian family.

Materials and Methods

Sampling

I included 136 specimens representing 42 different species from all three subfamilies within Soricidae in my analyses (Table 1; Appendix A). My dataset is dominated by the most diverse subfamily, Soricinae (four tribes, five genera, 27 species), but I do include a large phylogenetic diversity with 13 species from three genera within the subfamily Crocidurinae, and two species of Myosoricinae (genus Myosorex). Most species are represented by more than two specimens (mean: 3.26, median: 3). I used specimens that come from a large portion of the range of the family. Specifically, I sampled specimens from 17 different countries. 73 specimens were collected across 20 states and provinces of the United States and Canada. 25 specimens were collected from six European countries (Austria, Belgium, Finland, Portugal, Russia, and Spain); another

31 specimens were collected in seven African countries (Democratic Republic of the

Congo, Ethiopia, Ghana, Kenya, Nigeria, Sierra Leone, South Africa, and Zimbabwe); and 7 specimens come from four Asian countries (China, India, Israel, and Korea). I included species with a wide range of body sizes. The smallest species in the dataset is

Sorex minutus (mean body mass: 3.9 g, mean skull length: 15.37 mm; Ochocińska and

Taylor 2003). The largest species I included is Scutisorex somereni (mean body weight:

60.1 g; Lavrenchenko et al. 2009). I only used complete skulls and dentaries of adult 7 specimens bearing a full dentition. Although many shrew species do not exhibit apparent sexual dimorphism (Meegaskumbura et al. 2007; Stanley and Esselstyn 2010; Woodman and Timm 1993; Zidarova 2015), a few have been reported to display low levels of sexual dimorphism (Zidarova 2015). As a consequence, I included both males and females in my dataset whenever possible. I photographed the lateral and ventral view of the skulls and the lateral view of the dentary using a Nikon D300 and a Canon EOS

Rebel SL2 camera.

Landmarking

I used two-dimensional geometric morphometrics (GM) to quantify variation in cranial and dentary shape (Figure 1, Table 2, 3, 4). I chose landmarks and semi- landmarks for each of the orientation of the skull (lateral, ventral) and dentary (lateral) that reflect the anatomy of the musculoskeletal apparatus involved in food capture and processing (Dötsch 1986). I focused on features of the skull and dentary that are associated with prey capture, feeding performance, bite force, muscle attachment surfaces, lever inputs and outputs, and jaw movements (Badyaev and Foresman 2000;

Badyaev et al. 2005; Young et al. 2007, 2010; Cornette et al. 2015).

Label Subfamily Tribe Genus Species Diet N 1 Soricinae Blarinini Blarina hylophaga Hard 5 2 Crocidurinae - Crocidura lasiura Hard 3 3 Crocidurinae - Crocidura montis Hard 5 4 Myosoricinae - Myosorex cafer Hard 4 5 Myosoricinae - Myosorex varius Hard 4 6 Soricinae Nectogalini Neomys fodiens Hard 4 7 Crocidurinae - Scutisorex somereni Hard 2 8 Crocidurinae - Crocidura buettikoferi Intermediate 1 9 Crocidurinae - Crocidura douceti Intermediate 1 10 Crocidurinae - Crocidura nimbae Intermediate 1 11 Crocidurinae - Crocidura russula Intermediate 5 12 Crocidurinae - Crocidura suaveolens Intermediate 1 13 Soricinae Notiosoricini Notiosorex crawfordi Intermediate 2 14 Soricinae Soricini Sorex alpinus Intermediate 3 15 Soricinae Soricini Sorex araneus Intermediate 4 16 Soricinae Soricini Sorex arcticus Intermediate 3 17 Soricinae Soricini Sorex bendirii Intermediate 2 18 Soricinae Soricini Sorex dispar Intermediate 3 19 Soricinae Soricini Sorex gracillimus Intermediate 1 20 Soricinae Soricini Sorex merriami Intermediate 2 21 Soricinae Soricini Sorex pacificus Intermediate 4 22 Soricinae Soricini Sorex tundrensis Intermediate 4 23 Crocidurinae - Suncus murinus Intermediate 3 24 Soricinae Blarinini Blarina brevicauda Soft 7

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Table 1. List of all of the Soricidae species included in the analyses and their diet category.

Table 1 Continue

Label Subfamily Tribe Genus Species Diet N 26 Crocidurinae - Crocidura cyanea Soft 3 27 Crocidurinae - Crocidura fuscomurina Soft 2 31 Soricinae Nectogalini Neomys anomalus Soft 3 32 Soricinae Soricini Sorex cinereus Soft 5 33 Soricinae Soricini Sorex coronatus Soft 2 34 Soricinae Soricini Sorex fumeus Soft 3 35 Soricinae Soricini Sorex hoyi Soft 4 36 Soricinae Soricini Sorex isodon Soft 1 37 Soricinae Soricini Sorex longirostris Soft 4 38 Soricinae Soricini Sorex minutus Soft 2 39 Soricinae Soricini Sorex monticolus Soft 5 40 Soricinae Soricini Sorex palustris Soft 4 41 Soricinae Soricini Sorex trowbridgii Soft 4 42 Soricinae Soricini Sorex vagrans Soft 4

Figure 1. Landmarking scheme shown on Blarina brevicauda (lateral skull, ventral skull) and Suncus murinus (lateral dentary). Black dots represent semi-landmarks, red dots represent landmarks. (a. Ventral view of skull; b. Lateral view of skull; c. Lateral view of dentary) See Table 2, 3, and 4 for descriptions. Abbreviations: L = landmarks, SL = semi- landmarks, D = dentary unit, M = masseter unit, T = temporalis unit. 11

Biological variable Landmark and semi-landmarks characterized L1. Anterior end of premaxilla Length of skull L2. Tip of first incisor Length of incisor L3. Posterior end of first incisor Length of incisor L4. Junction of P4 and M1 Length of M1; Depth of maxilla L5. Junction of M1 and M2 Length of M1; Depth of maxilla L6. Junction of M2 and M3 Length of M2; Depth of maxilla Length of M3; Length of L7. Posterior end of upper toothrow toothrow L8. Posterior extension of jugal Origin of masseter L9. Ventral edge of pterygoid Origin of pterygoid muscles L10. Ventral-most point of auditory bulla Depth of skull Length of skull; Size of L11. Distal end of occipital condyle temporalis L12. Suture between interparietal and occipital Depth of skull Curvature of skull; Size of L13. Fronto-parietal suture temporalis L14. Dorsal end of rostrum corresponding to Depth of maxilla M2/M3 junction L15. Dorsal end of rostrum corresponding to Depth of maxilla M1/M2 junction L16. Dorsal end of rostrum corresponding to P4/M1 Depth of maxilla junction

SL1: From L11 to L12 (SL = 8) Size of temporalis SL2: From L12 to L13 (SL = 8) Size of temporalis

Table 2. Landmarks (L) and semi-landmarks (SL) of the lateral skull analysis and the biological variables they characterize.

Landmark and semi-landmarks Biological variable characterized L1. Tip of first incisor Width of incisor L2. Anterior end of premaxilla Length of skull L3. Posterior end of incisor on buccal side Width of incisor L4. Posterior end of premaxilla Length of premaxilla L5. Anterior end of P4 on buccal side Width of P4 L6. Lingual edge of protocone of P4 Width of P4 L7. P4/M1 junction on buccal side Length of P4; Length of M1 L8. Lingual edge of protocone of M1 Width of M1 L9. M1/M2 junction on buccal side Length of M1; Length of M2 L10. Lingual edge of protocone of M2 Width of M2 L11. Junction of jugal and maxilla Width of jugal; Origin of masseter L12. Lateral end of jugal Width of jugal; Origin of masseter L13. M2/M3 junction on buccal side Length of M2; Length of M3 L14. Lingual edge of protocone of M3 Width of M3 L15. Lateral end of pterygoid-palatine junction Length and width of pterygoid; Origin of pterygoid muscle L16. Posterior end of maxilla Length of maxilla L17. Posterior end of palatine Length of palatine L18. Medial end of pterygoid Length and width of pterygoid; Origin of pterygoid muscle L19. Postero-lateral end of pterygoid Length and width of pterygoid; Origin of pterygoid muscle L20.Lateral edge of mastoid process Width of the skull L21. Posterior end of paroccipital process Origin of digastric L22.Distal end of occipital condyle Total length of skull; Length/size of foramen magnum L23. Posterior end of basioccipital Length/size of foramen magnum

Table 3. Landmarks (L) and semi-landmarks (SL) of the ventral skull analysis and the biological variables they characterize.

Landmark and semi-landmarks Biological variable characterized L1. Tip of first incisor Length of incisor L2. Base of first incisor, at alveolus Length of incisor L3. p4/m1 junction Length of m1 L4. m1/m2 junction Length m1 and m2 L5. m2/m3 junction Length of m2 and m3 L6. Posterior end of toothrow Length of toothrow L7. Based of anterior end of coronoid process Insertion for temporalis; Relative size of temporalis L8. Dorsal most point of coronoid process Insertion for temporalis; Relative size of temporalis L9. Most ventral point between coronoid and Shape of condyloid process; Jaw condyloid process joint movement L10. Dorsal end of double mandibular Shape of condyloid process; Jaw articulation joint movement L11. Ventral end of double mandibular Shape of condyloid process; Jaw articulation joint movement L12. Most dorsal point between condyloid and Shape of condyloid process; Jaw angular process joint movement L13. Antero-dorsal end of angular process Insertion for masseter; Shape and length of angular process L14. Posterior end of angular process Insertion for masseter; Shape and length of angular process L15. Junction between ventral side of angular Insertion for masseter; Shape and process and ramus of the dentary length of angular process; Length and shape of ramus of dentary L16. Ventral end of dentary corresponding to Length and shape of ramus of the junction between p4 and m1 dentary

Table 4. Landmarks (L) and semi-landmarks (SL) of the lateral dentary analysis and the biological variables they characterize.

Bite force is a crucial factor in determining the hardest food a species can process because the maximum range of prey that a species can process is linked to the strength of the bite force produced (e.g., Gignac and Erickson 2016; Herrel and O’Reilly 2006;

Verwaijen et al. 2002); the ability to generate greater bite force is usually associated with a larger range of food and prey items (Herrel and O’Reilly 2006; Verwaijen et al. 2002;

Wilson et al. 2016). Previous studies on the biomechanical capabilities of vertebrates, including bats (Dumont et al. 2009; Herrel et al. 2008; Nogueira et al. 2009; Santana et al. 2010; Santana 2016), reptiles (Herrel et al. 2001a; Herrel et al. 2002; Herrel and

Holanova 2008), and carnivorans (Slater et al. 2009; Tseng and Stynder 2011; Tseng and

Flynn 2015) as well as data on select shrew taxa (Young et al. 2007, 2010) show that bite force is linked to a number of morphological characteristics including height and shape of the cranium, length of the rostrum, gape size, physiological cross-sectional area of the temporalis, masseter, and digastric muscles, and location of bite point. Specifically, increase in skull height (Herrel et al. 2002; Herrel and Holanova 2008; Nogueira et al.

2009), decrease in rostrum length (Nogueira et al. 2009; Slater et al. 2009), increase in height or size of the coronoid and angular processes (Hedrick and Dumont 2018;

Nogueira et al. 2009; Young et al. 2007), and greater jaw muscle mass (Greaves 2000;

Herrel et al. 2008) are associated with increased bite force. I placed landmarks and semi- landmarks to capture the relative size and shape of these anatomical features (Tables 2-4).

Additional landmarks and semi-landmarks were placed based on prior morphofunctional analyses of shrew skulls and dentaries and dissections of the musculature (Cornette et al.

2015; Dötsch 1986; Young et al. 2007, 2010). I also performed dissections of two

15 specimens of Sorex trowbridgii to further verify the origins and insertions of the m. temporalis, m. masseter, and m. digastricus suggested in previous publications. This work enabled me to validate my choices of landmarks (Table 3, Appendix C).

Muscle Origin Insertion Action Temporalis Parietal Coronoid process Closing the and fossa jaw temporalis Masseter Lateral side of maxilla (above M1 Lateral side of Closing the to the end of zygomatic process angular process jaw of maxilla) Digastric Posterolateral side of the Mandibular ramus Opens the jaw paraoccipital process below m2 Pterygoid Wing of pterygoid process, lateral Medial edge of Pulls mandible edge of pterygoid bone and mandibular dorso-medially palatal bone nearby condyle

Table 5. Origin, insertion, and action of muscles associated with food processing by the jaw apparatus (Dotch 1986; Young et al. 2010).

I used 14 traditional landmarks (five type 1 landmarks and nine type 2 landmarks) to capture the overall shape of the lateral skull (Figure 1a). I used 16 semi-landmarks

(two curves of eight semi-landmarks) to quantify the curvature of the temporal region of the skull. Critically, the landmarks and semi-landmarks I placed enable me to estimate the areas of origin of the m. temporalis and m. masseter (Dötsch 1986; Table 5). I also 16 used landmarks to estimate the size and proportions of the dental apparatus and its distance from the double temporomandibular joint (TMJ) (Cornette et al. 2015; Young et al. 2007, 2010).

I used 21 traditional landmarks (10 type 1 landmarks and 11 type 2 landmarks) to represent the shape of the ventral skull (Figure 1b). Once again, I included landmarks that help characterize the size and proportions of the dental apparatus. For the lateral view of the dentary (Figure 1c).

I used 16 traditional landmarks (three type 1 landmarks and 13 type 2 landmarks) to represent the overall shape of the dentary in lateral view. I used 16 semi-landmarks

(two curves of eight semi-landmarks) to quantify the shape of the coronoid process and eight semi-landmarks to characterize the curvature of the ventral edge of the ramus of the dentary. I used landmarks and semi-landmarks to estimate the area of insertion of the m. temporalis and m. masseter (Dötsch 1986; Table 5). I also used landmarks to estimate the size and proportions of the dental apparatus and its distance from the jaw joint (Young et al. 2007).

For all views studied, I used tpsUtil v.1.58 (Rohlf 2013) to create a TPS file, which was then input into tpsDig 2 v.2.16 (Rohlf 2010) to digitize landmarks. The number of semi-landmarks was chosen following a sensitivity analysis involving successive subsampling of a curve of 16 semi-landmarks aiming to minimize the number of semi-landmarks while accurately representing the shape of the osteological material in the relative warp plots (see below). Each set of landmarks was size-calibrated using the scale included in the specimen photos.

Food hardness data

I classified all 42 shrew species in my sample into one of three food hardness categories: soft, intermediate, or hard (Table 1) based on diet information from previous publications documenting the gut and fecal pellet contents of shrew species (Appendix A,

B). The hardness of the prey items was determined based on their taxonomic identity

(Table 6) and prior experimental work on the crushing force required to process various invertebrate prey items (Dollion et al. 2017; Measey et al. 2011; Vanhooydonck et al.

2007). For each shrew species, I used the following criteria: (1) If the prey is found in at least 50% of the sampled individuals or the prey represents at least 50% of the food ingested by the sampled individuals on average, the prey type is considered to be a major food source. (2) The major food items of a species could be composed of prey from a mix of hardness categories. Since the hardest common prey of each species likely reflects its maximum biomechanical performance, species are assigned to a hardness category based on the hardest major prey item eaten by the species. (3) If the data from different publications suggest very different diet composition for the same shrew species, possibly reflecting variation in food availability across the range of the species or seasons, the food hardness category is assigned based on the hardest major food items recorded. (4) If the data from different publications suggest very different diet composition for the same shrew species without clear information about the differences in percentage or proportion, the species would be assigned to “intermediate” hardness category to avoid over- or underestimation of its biomechanical capability. 18

Soft Intermediate Hard Insect larvae Isopoda Adult Coleoptera Araneae Orthoptera Hymenoptera Diptera Coleoptera pupa Gastropoda Hemiptera Lepidoptera pupa Isoptera Lepidoptera Myriapoda Oligochaeta Oplione

Table 6. Hardness categorization for major invertebrate prey items of Soricidae (Dollion et al. 2017; Measey et al. 2011; Vanhooydonck et al. 2007).

Analyses

I analyzed the geometric morphometric data I collected in R 3.6.0. using R Studio

1.2.1335 and the packages geomorph 3.1.3 (Adams and Oarola-Castillo 2013), MASS 7.3

– 51.4, Morpho 2.7 (Schlager 2017), shapes 1.2.4 (Dryden 2018), vegan 2.5-6 (Oksanen et al. 2019), and lmodel2 1.7-3 (Legendre 2018). I used generalized Procrustes superimposition (Rohlf and Slice 1990; Zelditch et al. 2012) to translate, scale, and rotate the digitized landmarks for all three views I studied (i.e. lateral view of the skull, ventral 19 view of the skull, and lateral view of the dentary) and all specimens. I used all 136 specimens in the initial relative warp analysis and then input the species means of the warp scores into subsequent analyses. I analyzed the data using principal component analyses (PCA) to explore morphospace occupation and the relationship between morphology and food hardness. I quantified the potential for morphology to predict food hardness using jackknifed canonical variate analyses (CVA) incorporating information from all three views studied. I assessed the significance of relative warps using a broken- stick distribution and only retained significant axes in my analyses.

Analyses of functional units of the skull

In order to investigate the relative roles of the m. temporalis, m. masseter, and dental apparatus in the processing of hard foods in shrews, I subset the landmarks and semi-landmarks into three different units (Figure 1), which I analyzed independently. I focused on exploring the potential of the morphological correlates of both jaw-closing muscles and the dentition to accurately classify species into the food hardness category they belong in as a measure of the role of this unit in the adaptation to hard food processing in shrews.

The m. masseter and m. temporalis enable crushing of hard foods because the size of these muscles is associated to bite force production. Greater muscle mass is related to the production of a greater bite force (Greaves 2000; Herrel et al. 2008), which could potentially be achieved by having larger areas for the origin and insertion of the muscles

(Becerra et al. 2014; Law et al. 2018; Nogueira et al. 2009; Table 5). The position of the

20 origin and insertion of these muscles may also be important because it could affect the lengths of the in-levers involved in the biomechanics of biting (Dumont et al. 2005;

Greaves 2000; Lappin and Jones 2014; Santana et al. 2010; Slater and Van Valkenburgh

2009).

The relative position of the bite point as well as the length and location of the toothrow also affect the bite force produced by an animal. For instance, a decrease in distance between the TMJ and the bite point leads to increased bite force (Campbell and

Santana 2017; Ellis et al. 2009; Lappin and Husak 2005; Lappin and Jones 2014; Young et al. 2007). In shrews, this would be linked to a decreased distance between the double mandibular jaw joint and the fourth upper premolar as well as the first lower molar

(Cornette et al. 2015; Dötsch 1986; Young et al. 2007, 2009). A decrease in rostrum length, which is associated with increased bite force (Goswami et al. 2011; Nogueira et al. 2009; Wroe and Milne 2007), may be linked to the compression of the toothrow an its decreased relative length.

Analyses of centroid size

In order to investigate whether or not the hardness of the food consumed is associated with the size of the shrew predator, I also quantified cranium size and dentary size using centroid size. Larger mammal species can produce a stronger bite force than smaller species (Ellis et al. 2009; Maestri et al. 2016; Nogueira et al. 2009; Tseng and

Flynn 2015; Verwaijen et al. 2002). As such, there is the possibility that larger shrew species consume harder prey. Additionally, the hardness of many invertebrate prey items

21 tends to increase with their body sizes (Aguirre et al. 2003; Herrel et al. 2001b). The consumption of harder preys could therefore be linked to increased prey and predator sizes. I compared the centroid sizes of shrew species across food hardness categories using ANOVAs followed by post-hoc comparisons using Tukey Honest Significant

Differences tests when the ANOVA was significant.

Analysis of coronoid-mandibular articulation distance

The distance between the tip of the coronoid process and the ventral end of the double mandibular articulation (the jaw joint of shrews; Fearnhead et al. 1955) has previously been shown to reflect dietary specialization; this distance is significantly higher in species with a hard diet than other shrew taxa (Young et al. 2007). I calculated the coronoid-mandibular articulation distances of all the shrew species included by in my dataset. I used landmarks eight and 11 to determine the average Euclidean distance for each taxon and an ANOVA to test for significant differences in distances among dietary categories.

Phylogenetic flexible discriminant function analysis (pFDA)

I used a phylogenetically informed flexible discriminant function analysis (pFDA) to examine the relationship between craniodental morphology and food hardness while accounting for the shared evolutionary history between soricid taxa (Close and Rayfield

2012; Felice and O’Connor 2014; Hall et al. 2012; Hastie et al. 1994). I modeled my work after prior studies implementing pFDA (Kohli and Rowe 2019; Schmitz and Motani

2011; Smith et al. 2018; Verde Arregoitia et al. 2017) in R using the packages ape

(Paradis et al. 2004) and mda (Hastie et al. 2009). I calculated Pagel’s lambda to estimate the importance of phylogeny in the analysis using the phylo.fda.R script published by

Schmitz and Motani (2011) subsequently updated by Verde Arregoitia et al. (2017). I used 100 trees drawn out of the 1,000 species-level trees of mammals published by

Faurby and Svenning (2015) pruned to only retain the species included in my dataset. A lambda value of zero indicates that the phylogenetic relatedness of the species studied is not important to the model (i.e. equals to when no phylogenetic information has been included to the analysis), while a lambda value of one indicates that phylogenetic relationships are important to the model (Hall et al. 2012; Revell 2010). I used the lambda values recovered, together with the PC scores from the geometric morphometric analysis to perform the pFDA.

Institutional abbreviations

CMNH, Cleveland Museum of Natural History, Cleveland, Ohio; OSU MBD, The Ohio

State University Museum of Biological Diversity, Columbus, Ohio; CM, Carnegie

Museum of Natural History, Pittsburgh, Pennsylvania; LACM, Natural History Museum of Los Angeles County, Los Angeles, California; USNM, United States National

Museum of Natural History, Smithsonian Institution, Washington DC.

Results

Centroid size distribution

The analysis of the centroid size of the lateral view of the skulls demonstrates a significant difference in size among the different food hardness categories (F = 4.27, p =

0.02) (Figure 2a). The post-hoc Tukey HSD test shows that this difference stems from that between hard and soft diet species, which are significantly different from each other

(p = 0.02) (Figure 2a). There are no other significant differences in centroid sizes among the categories studied. A similar pattern is recovered from the analysis of the centroid sizes of the ventral view of the skulls (ANOVA: F = 3.93, p = 0.0279; Post-hoc Tukey

HSD test: p = 0.02) (Figure 2b) and the lateral view of the dentaries (ANOVA: F = 4.72, p = 0.0146; Post-hoc Tukey HSD test : p= 0.01) (Figure 2c).

p = 0.02

a ANOVA 5

5 f = 4.27

p = 0.0211

5 2

p = 0.02 ANOVA f = 3.93

b p = 0.0279

0 2

p = 0.01 ANOVA f = 4.72

c p = 0.0146

5 1

Soft Intermediate Hard Hardness

Figure 2. Box plot showing the centroid sizes of the (a) lateral skull, (b) ventral skull, and

(c) lateral dentary of shrew species across diet categories. The dark line in each box represents the median.; open circles represent outliers. The bracket and p-value in each boxplot represents the groups that are significantly different from each other (p < 0.05) in the THSD tests. 25

Principal component analyses

Lateral skull

Together, PC1 and PC2 explain 50.3% of the variation in craniodental morphology (PC1: 32%; PC2: 18.3%) (Figure 3). PC1 scores are not significantly different among the three hardness categories (ANOVA: F = 0.963, p = 0.384). Positive

PC1 scores are associated with a dorsoventrally flat parietal, an angular transition from occipital to parietal (as opposed to curved), and a dorsoventrally shallow and straight occipital. Negative PC1 scores are associated with a convex parietal-interparietal- occipital portion of the skull and a dorsoventrally deep and curved occipital. In contrast, the PC2 scores are significantly different between the three categories (ANOVA: F =

12.97, p ~0), with hard diet species being distinct from both soft (Post-hoc Tukey HSD test: p~0) and intermediate diet species (Post-hoc Tukey HSD test: p~0). Soft and intermediate diet species are not significantly different (Post-hoc Tukey HSD test: p =

0.996). Species with a hard diet tend to have more negative PC2 scores whereas most species with a soft diet have positive PC2 scores; species with an intermediate hardness diet show a wide distribution along PC2 but their scores are not significantly different from soft diet species (Post-hoc Tukey HSD test: p~1). Positive PC2 scores are associated with an anteroposteriorly elongated and dorsoventrally compressed rostrum and dorsoventrally shallow parietal region. Negative PC2 scores are associated with an

26 anteroposteriorly short and dorsoventrally expanded rostrum and dorsoventrally deep parietal.

Figure 3. Results of the PCA of the lateral skull when all landmarks are included in the analysis. Species numbers detailed in Table 1. Colors: blue square, hard diet; black triangle, intermediate hardness diet; red circle, soft diet.

Ventral skull

PC1 and PC2 explain 58.4% of the craniodental variations (PC1: 38.2%; PC2:

20.2%) (Figure 4). PC1 scores are significantly different among the three hardness categories (ANOVA: F = 9.6, p~0). Hard diet species can be differentiated from both soft

(Post-hoc Tukey HSD test: p~0) and intermediate hardness species (Post-hoc Tukey HSD test: p~0). Soft and intermediate diet species are not significantly different from each other (Post-hoc Tukey HSD test: p = 0.999). Along PC1, more positive PC1 scores are associated with hard diet species whereas intermediate and soft diet species mostly have negative PC1 scores. Positive PC1 scores correspond to a V-shaped palatine with a buccolingually expanded posterior end and buccolingually broad P4 and M1. Negative

PC1 scores correspond to a buccolingually compressed posterior end of the palatine and buccolingually narrow P4 and M1. There are no significant differences in PC2 scores among food hardness categories (ANOVA: F = 2.395, p = 0.095). Positive PC2 scores are associated with mediolaterally broad basicranium and pterygoid. Negative PC2 scores are associated with a mediolaterally compressed basicranium and pterygoid.

Figure 4. Results of the PCA for the ventral skull when all landmarks are included in the analysis. Species numbers detailed in Table 1. Colors: blue square, hard diet; black triangle, intermediate hardness diet; red circle, soft diet.

Lateral dentary

PC1 and PC2 explain 55.1% of the craniodental variations (PC1: 36.5%; PC2:

18.6%) (Figure 5). There are no significant differences in PC1 scores among food hardness categories (ANOVA: F = 2.87, p = 0.06). Positive PC1 scores are associated with an anteroposteriorly compressed dorsal end of the coronoid process, a posteroventrally elongated angular process, and the anteroventral edge of the condyloid 29 process far dorsal of the angular process. Negative PC1 scores are associated with an anteroposteriorly expanded dorsal end of the coronoid process, a short angular process, and the anteroventral edge of the condyloid process abutting the angular process. PC2 scores are significantly different among the three hardness categories (ANOVA: F =

15.97, p~0). Soft (Post-hoc Tukey HSD test: p~0) and intermediate hardness species

(Post-hoc Tukey HSD test: p~0) can be distinguished from hard feeders along PC2, whereas soft and intermediate species are not different from each other (Post-hoc Tukey

HSD test: p = 0.5). Hard food consumers tend to have negative PC2 scores whereas soft food eaters tend to have positive PC2 scores; intermediate species show a wide distribution of PC2 scores. More positive PC2 scores are associated with coronoid process with concave anterior and posterior edges, and a large distance between the dorsal and ventral end of the double mandibular articulation. Negative PC2 scores are associated with straight anterior and posterior edges of the coronoid process and a short distance between the dorsal and ventral ends of the double mandibular articulation. There is no significant difference in coronoid-mandibular articulation distance among the dietary categories studied (ANOVA: F = 1.25, p = 0.298).

Figure 5. Results of the PCA for the lateral dentary when all landmarks are included in the analysis. Species numbers detailed in Table 1. Colors: blue square, hard diet; black triangle, intermediate hardness diet; red circle, soft diet.

Canonical variate analyses

Among the three views studied (lateral skull, ventral skull, and lateral dentary), the lateral dentary shows the highest a posteriori classification accuracy of species into their hardness category (59.5%); the lateral view of the skull (54.8%) and the ventral view of the skull (52.4%) show lower values (Table 7). Soft food consumers are most

31 accurately classified using the shape of the lateral view of the dentary (78.9%); the same is true for intermediate hardness feeders (50%). Hard food consumers are most accurately classified using the shape of the lateral view of the skull (71.4%) (Table 7). When considering all three craniodental orientations together, the overall classification accuracy is 66.7%, higher than for any individual orientation (Figure 6a, Table 7).

Soft Intermediate Hard Overall Lateral skull 57.9% 43.8% 71.4% 54.8% Ventral skull 68.4% 43.8% 28.6% 52.4% Lateral dentary 78.9% 50% 28.6% 59.5% Temporalis unit 47.4% 18.8% 42.9% 35.7% Masseter unit 68.4% 0% 0% 31% Dental unit 57.9% 43.8% 42.9% 50%

All views and 63.2% 43.8% 42.9% 66.7% landmarks pFDA 94.7% 68.8% 85.7% 83.3%

Table 7. Overall classification accuracy (%) for the individual craniodental orientations

6 a

7 5 Hard

1 6

9 17 0 11 19 10

16 15

42 8 Intermediate Soft 18

0 CV1 (56.6%) b

Soft 40

35 25 30 42 28 24 34 27 38 31 23 37 32 36 29 18 33 16 26 41 11 15 8 39 2 13 14 6 20 9 10 22 5 17 1 3 21 19 Hard 12 7

Intermediate 4

Figure 6. Overall percent classification accuracy when all three craniodental orientations are included in the analysis for both (a) CVA and (b) pFDA. The percent classification accuracy for each diet hardness is shown in brackets below the hardness category labels.

Species numbers detailed in Table 1. Colors: blue square, hard diet; black triangle, intermediate hardness diet; red circle, soft diet. (Silhouettes from Phylopic; see acknowledgements). Major correlates of the x-axis and y-axis of the CVA are labeled. (LS: lateral skull; VS: ventral skull; LD: lateral dentary)

CV1 explains 56.6% of the variation (Figure 6a). Species with a soft diet and those with an intermediate hardness diet are segregated from one another along CV1

(Figure 6a); soft diet species have negative CV1 scores whereas intermediate diet species have positive CV1 scores. Morphological variation along CV1 is primarily driven by

PC1, PC2, PC4, and PC7 of the lateral dentary and PC2 and PC3 of the ventral skull

(Figure 6a). From positive to negative CV1 scores, there is a gradual anteroposterior narrowing of the coronoid process. The coronoid process also shifts from having straight anterior and posterior edges to having concave edges. The double mandibular articulation changes from being more dorsoventrally expanded to compressed. The basicranium and posterior end of palatine narrow mediolaterally. The angular process is elongated.

CV2 explains 43.4% of the variations (Figure 6a). It explains the partition between hard food consumers and soft/intermediate food eaters (Figure 6a). Hard diet species have positive CV2 scores; soft and intermediate diet species mostly have negative

CV2 scores. Morphological variation along CV2 is primarily driven by the PC1 of the ventral skull, PC2 and PC3 of the lateral skull, and PC1, PC2 and PC3 of the lateral dentary (Figure 6a). From positive to negative CV2 scores, there is a gradual narrowing 34 of the palatine, P4, and M1. The rostrum changes from anteroposteriorly short and dorsoventrally deep to anteroposteriorly elongated and dorsoventrally shallow. The parietal region shifts from dorsoventrally flattened to dome-shaped. The angular process is elongated. The coronoid process changes from having straight anterior and posterior edges to having concave edges. The coronoid also narrows anteroposteriorly. The double mandibular process is enlarged.

Temporalis, masseter, and dental units

Among the three units analyzed (temporalis, masseter, and dental units), the dental unit shows the highest a posteriori classification rate (50%) (Table 7). The accuracies of the classification when using the temporalis unit (35.7%) and the masseter unit (31%) are much lower. Soft food consumers are most accurately classified using the masseter unit (68.4%), intermediate hardness feeders are most accurately classified using the dental unit (25%), and hard food eaters are most accurately classified using the temporalis unit (42.9%). The masseter unit cannot accurately classify any species with intermediate and hard diet (Table 7).

Phylogenetic flexible discriminant function analysis (pFDA)

The optimal lambda value is 0.266, indicating a weak to moderate phylogenetic signal in the craniodental morphology of shrews (Hall, et al. 2012; Smith et al. 2018;

Verde Arregoitia et al. 2017; Figure 6b). The three food hardness categories form three

35 separate clusters in the pFDA (Figure 6b). pFDA1 explains 60.1% of the variation; pFDA2 explains 39.9% of the variation. Hard food eaters cluster at the positive end of pFDA1 whereas intermediate food eaters cluster at the negative end of pFDA1. Along pFDA2, both hard food and intermediate food consumers have negative scores whereas soft food eaters have positive scores. The overall classification rate is higher for the pFDA (83.3%) than the CVA (66.7%) (Table 7). The classification accuracy is higher for all three food hardness categories. The accuracy percentage increases from 63.2% in the

CVA to 94.7% in the pFDA for the soft diet, from 43.8% to 68.8% for the intermediate diet, and from 42.9% to 85.7% for the hard diet.

Discussion

The objectives of this study were to investigate (1) whether the cranial morphology of shrews modulates their dietary ecology through biomechanical adaptation and (2) whether the evolutionary history of shrews contributed to their craniodental morphology independently of food acquisition and processing. Overall, my results provide evidence that craniomandibular morphology is indeed associated with the differences in prey hardness observed among shrew species. In fact, skull shape alone can accurately identify the hardness of prey consumed for 66.7% of the 42 species I studied

(Table 7).

My analyses enable the characterization of the morphology associated to a specialized hard food diet. Hard food consumers have an anteroposteriorly expanded parietal region and an anteroposteriorly short but dorsoventrally tall rostrum. They also have a mediolaterally wide palate as well as a buccolingually wide P4 and M1. Their coronoid processes have anterior and posterior edges that are straight, rather than concave, and the distance between the dorsal and ventral end of the double mandibular articulation is short. Although the distance from the tip of the coronoid process to the double mandibular articulation has been shown to be significantly higher in hard food consuming Sorex than in other Sorex species (Young et al. 2007), I do not find such a pattern across my broader taxonomic sample. My results suggest that having a greater

37 area for muscle insertion, a greater dental surface area for crushing food, and a reduced distance of jaw out-lever are most important for processing hard food items. Soft food consumers are characterized by an anteroposteriorly compressed parietal region, dorsoventrally shallow rostrum, mediolaterally narrow palatine, and buccolingually narrow P4 and M1. Their coronoid processes have concave anterior and posterior edges.

They also have a dorsoventrally expanded double mandibular articulation of the dentary.

Intermediate species display a morphology that is a mix of the characteristics of both hard and soft food consumers.

The morphological characteristic of shrews that eat hard foods are associated with strong mechanical capabilities to generate high bite forces. Indeed, a wide parietal region and a tall rostrum would enable a large area for the origin of the temporalis muscle and a broad coronoid process provides a large area for the insertion of the m. temporalis

(Becerra et al. 2014; Law et al. 2018; Nogueira et al. 2009). A large area of muscle origin or insertion enables increased muscle mass and, as such, the generation of greater bite force (Becerra et al. 2014; Greaves 2000; Herrel et al. 2008; Law et al. 2018; Nogueira et al. 2009). A short rostrum length reduces the distance between the TMJ and the bite point, decreasing the out-lever of the jaw, and increasing bite force (Campbell and

Santana 2017; Ellis et al. 2009; Lappin and Husak 2005; Lappin and Jones 2014). A wider palatine enables better stress transmission under greater amount of load when feeding on hard objects (Dumont et al. 2005; Thomason and Russell 1986). Large P4 and

M1 provide an increased crushing and shearing surface, enhancing crushing ability and the processing of invertebrates with hard cuticles or shells (Daegling et al. 2011;

Popowics 2003; Wilson et al. 2016). The double mandibular articulation of shrews is a morphological adaption to the change in stress experienced by jaw joint (Fearnhead et al.

1955). The change in shape of this articulation in hard-food consumers is likely associated with changes in mechanical advantage. Past work has suggested that bite force played an important role in shaping the evolution of the shrew dentary because adaptations to greater bite force provides competitive advantages in food acquisitions and interspecific aggressions (Cornette et al. 2015). My work does not specifically speak to selection but provides the framework for future investigations of the evolution of morphology in shrews, including fossils (Gunnell et al. 2008) and the test of the hypothesis of Cornette and colleagues (2015) in a phylogenetic framework through a phylomorphospace.

Among the three functional units of the craniodental apparatus studied, the dental unit shows the greatest classification accuracy (50%; Table 7). This suggests that tooth size and shape play a more important role in the processing of hard objects than muscles.

Despite a lower classification accuracy (35.7%; Table 7), the size and location of origin and insertion of the temporalis muscle appear to contribute to the ability of shrews to feed on hard food. The masseter unit shows the lowest classification accuracy (Table 7). In particular, it does not accurately classify any hard food and intermediate food consumers

(Table 7). This suggests that the size of the masseter muscle does not play a big role in facilitating hard food consumption in shrews. This result is consistent with the findings of

Young et al. (2010) from two populations of two species of Sorex that there was no

39 significant difference in masseter physiological cross-section area between shrews with different bite forces.

My analyses demonstrate that the morphology of the lateral dentary enables a more accurate classification of shrew species in dietary hardness categories than skull morphology (Table 7). This suggests that dentary morphology may better reflect morphological adaptations to hard food processing in shrews. The dentary has been extensively used in prior studies of Soricidae morphology, taxonomy, and ecology (e.g.,

Badyaev and Foresman 2004; Cornette et al. 2012, 2015; Young et al. 2007; Young et al.

2010). Diet was specifically suggested to be one of the selective forces that influenced the morphology of the dentary in some of those analyses (Badyaev and Foresman 2004,

Young et al. 2007, Cornette et al. 2015). The greater connection between diet and morphology in the dentary may be a consequence of the delayed ossification of the dentary during ontogeny. Indeed, prior studies have showed that the development of late- maturing mandible characteristics is partially dictated by the functional demands experienced by shrews (Young and Badyaev 2006, 2010). Interestingly, the elements of the dentary that show the greatest amount of variation among different diet hardness categories in my study (i.e. coronoid process, double mandibular articulation, and angular process) are all late-maturing characteristics (Young and Badyaev 2006, 2010).

The morphospace occupation of species within each bite force category across my broad sample of soricid species provides some support at the family level for the functional equivalence hypothesis observed within Sorex (Young et al. 2007). Thus, for example, it appears that Blarina hylophaga can acquire and process hard foods through a

40 different morphology than Scutisorex and Myosorex (Figure 5). The coronoid process of

B. hylophaga, unlike those of Scutisorex and Myosorex, has a concave anterior edge, a feature observed mostly among soft diet species, but it is much more robust than the coronoid processes of Scutisorex and Myosorex. Additionally, the double mandibular articulation of B. hylophaga resembles that of soft diet species, but the location of the ventral end of the articulation overlaps the connection between the articulation and angular process instead of projecting out forming a double articulation like in all the other species. This feature in B. hylophaga could affect the location of TMJ and potentially reduce the distance from TMJ to bite point, which could allow species to produce greater bite force. (Cornette et al. 2015; Dötsch 1986; Young et al. 2007, 2009). I do not detect such pattern of functional equivalence through different morphologies in the skull (lateral or ventral view). The dentary of shrews appears to follow a different evolutionary pattern than the upper jaw, an issue that is yet to be explored across a broad range of soricid species.

Changes in craniodental morphology are not the only adaptions to processing hard food items in shrews. There is also evidence that the size of shrews plays a role. Indeed, my analysis of centroid size demonstrates that the skull and dentary of hard food consumers are significantly larger than soft food consumers (Figure 2). Larger skulls are known to be able to generate a stronger bite force than smaller skulls of similar shape

(Ellis et al. 2009; Maestri et al. 2016; Nogueira et al. 2009; Tsang and Flynn 2015;

Verwaijen et al. 2002), including in shrews (Young et al. 2007). Increased skull size leads to increased surface area for muscle attachment and therefore increased muscle mass and

41 increased bite force (Becerra et al. 2014; Greaves 2000; Herrel et al. 2008; Law et al.

2018; Nogueira et al. 2009).

In addition to finding strong evidence that both the size and the shape of the craniodental apparatus of shrews enable dietary specializations, I also provide quantitative data to support a role of evolutionary history in shaping the morphology of the skull and dentary of soricids. The lambda value I calculated indicates that there is a weak phylogenetic signal in the dataset (Hall, et al. 2012; Smith et al. 2018; Verde

Arregoitia et al. 2017). Nonetheless, after taking phylogenetic relationships into account, the classification accuracy greatly increases from 66.7% in the CVA to 83.3% in the pFDA; the accuracy was improved for each of the food hardness category as well (Table

7). A role of evolutionary history in shaping the cranial morphology of shrews was also recovered by a prior study that found a significant phylogenetic signal in mandible shape and a moderate, non-significant signal in skull shape (Rey et al. 2019). The evolutionary history of shrews may have canalized their craniodental morphology, leading to the diverse adaptations in shrew taxa that acquire and process hard prey apparent in my analyses.

Shrews are one of the few mammalian groups that includes venomous species

(Cuenca-Bescós and Rofes 2007; Kowalski et al. 2017; Martin 1981; Tomasi 1978). The others are the families Solenodontidae (solenodon) and Ornithorhynchidae (platypus) as well as the subfamily Desmodontinae (vampire bats) (Ligabue-Braun et al. 2012). The venom of shrews has been hypothesized to enable them to hunt larger prey, reduce the time required to handle prey, and increase the amount of prey hoarding (Kowalski et al.

2017; Kowalski and Rychlik 2018). Among the four currently known venomous shrews, three are included in my analyses (Blarina brevicauda, Neomys anomalus, Neomys fodiens) (Ligabue-Braun et al. 2012). Among those, only Neomys fodiens is a hard food consumer; the others are all soft food eaters. N. fodiens is particularly interesting because it differs from all other hard-food consumers in the morphology of the dentary and that of the ventral view of the skull. It is located closer to soft-food consumers in the lateral dentary morphospace (Figure 5). It differs from other hard food consumers in having a coronoid process with concave (rather than straight) anterior and posterior edges. The resulting smaller surface area of the coronoid process for the insertion of the m. temporalis would lead to a smaller bite force in N. fodiens (Becerra et al. 2014; Greaves

2000; Herrel et al. 2008; Law et al. 2018; Nogueira et al. 2009). It is most similar in ventral skull morphology to the soft food consumer Nemomys anomalus and intermediate food consumer Sorex bendirii (Figure 4). The posterior end of the palatine of N. fodiens is not as mediolaterally expanded as that of other hard diet species; its basicranium and pterygoid are also mediolaterally compressed compared to other hard food consumers.

The more restricted palatine of N. fodiens would transmit stress less efficiently when manipulating hard objects compared to other hard diet species (Dumont et al. 2005;

Thomason and Russell 1986). In fact, my CVA suggests that N. fodiens should be classified as an intermediate hardness species. The presence of venom in N. fodiens may enable the species to prey on harder invertebrates by overcoming the obstacle of needing to generate greater bite force when catching prey.

The results of my analyses demonstrate an association between craniodental morphology and dietary specialization across a broad sample of shrew species.

Specifically, I show that species with a hard food diet display a number of morphological adaptations compared to taxa with soft and intermediate hardness diet. The morphospace approach adopted in my analyses could benefit studies of shrew ecology, particularly with regards to niche differentiation and overlap. Indeed, many shrew species are known to live in sympatry (e.g., Churchfield et al. 1999; Churchfield and Rychlik 2006; Rychlik

2000; Rey et al. 2019). Some of these communities have been studied through the lens of a morphospace. Rey et al. (2019), for example, investigated the relationship between climatic niche and cranial morphology for nine sympatric shrew species. An analysis of sympatric shrew species across habitats exploring differentiation in craniodental morphology and diet would enable a systematic assessment of niche partitioning within the family. In addition, the results of my analyses could be used to investigate the diet of extinct soricids, in particular in entirely extinct shrew clades (Gunnell et al. 2008).

Together, the fossil record and ecological analyses will help shed light on the processes of adaptive radiation in Soricidae.

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Appendix A. List of all shrew species included in the analyses, their diet category, and supporting diet data

Subfamily Tribe Genus Species Diet References Soricinae Blarinini Blarina hylophaga Hard Anderson and Fleharty (1967); Bee et al. (1981); Davis and Schmidly (1994); Ritzi et al. (2005) Crocidurinae - Crocidura lasiura Hard Churchfield et al. (1999); Crocidurinae - Crocidura montis Hard Clausnitzer et al. (2003) Myosoricinae - Myosorex cafer Hard Churchfield (1985) Myosoricinae - Myosorex varius Hard Rowe-Rowe (1986) Soricinae Nectogalini Neomys fodiens Hard Castien and Gosalbez (1999); Churchfield (1985); Chuchfield and Rychlik (2006); Niethammer (1978); Wołk (1976) Crocidurinae - Scutisorex somereni Hard Churchfield et al. (2007) Crocidurinae - Crocidura buettikoferi Intermediate Churchfield et al. (2004) Appendix A continue

Appendix A continue Crocidurinae - Crocidura douceti Intermediate Churchfield et al. (2004) Crocidurinae - Crocidura nimbae Intermediate Churchfield et al. (2004) Crocidurinae - Crocidura russula Intermediate Bever (1983); Brahmi et al. (2012); Crocidurinae - Crocidura suaveolens Intermediate Bauerová (1988); Jakub et al. (2017); Kuviková (1987) Soricinae Notiosoricini Notiosorex crawfordi Intermediate Hoffmeister and Goodpaster (1962); Punzo 2003 Soricinae Soricini Sorex alpinus Intermediate Klenovsek et al. (2013) Soricinae Soricini Sorex araneus Intermediate Churchfield et al. (2012); Klenovsek et al. (2013) Soricinae Soricini Sorex arcticus Intermediate Buckner (1964); Jones et al. (1983) Soricinae Soricini Sorex bendirii Intermediate Whitaker and Maser (1976) Appendix A continue

Appendix A continue Soricinae Soricini Sorex dispar Intermediate Conaway and Pfitzer (1952); Conner (1960); Richmand and Grimm (1950) Soricinae Soricini Sorex gracillimus Intermediate Churchfield et al. (1999) Soricinae Soricini Sorex merriami Intermediate Johnson and Clanton (1954) Soricinae Soricini Sorex pacificus Intermediate Whitaker and Maser (1976) Soricinae Soricini Sorex tundrensis Intermediate Churchfield and Sheftel (1993); Dokuchaev et al. (2015) Crocidurinae - Suncus murinus Intermediate Advani and Rana (1981); Khanum et al. (2017) Soricinae Blarinini Blarina brevicauda Soft Hamilton (1941); Whitaker and Mumford (1972); Appendix A continue

Appendix A continue Soricinae Blarinini Blarina brevicauda Soft Whitaker and French (1984) Soricinae Blarinini Blarina carolinensis Soft McCay (1998); Whitaker (1994); Sylvester et al. (2012); Whitaker and Ruckdeschel (1996); Crocidurinae - Crocidura cyanea Soft Dickman (1995) Crocidurinae - Crocidura fuscomurina Soft Dickman (1995) Crocidurinae - Crocidura hirta Soft Dickman (1995) Crocidurinae - Crocidura olivieri Soft Churchfield et al. (2004) Soricinae Blarinini Cryptotis parva Soft Whitaker and Mumford (1972) Soricinae Nectogalini Neomys anomalus Soft Santamarina (1993) Soricinae Soricini Sorex cinereus Soft Bellocq et al. (1994); McCay and Storm (1997); Whitaker and French (1984); Appendix A continue

Appendix A continue Soricinae Soricini Sorex cinereus Soft Whitaker and Mumford (1972) Soricinae Soricini Sorex coronatus Soft Castién and Gosálbez (1995); Castién and Gosálbez (1999) Soricinae Soricini Sorex fumeus Soft Hamilton (1941); Linzey (2016); Whitaker and French (1984); Whitaker et al. (1975) Soricinae Soricini Sorex hoyi Soft Whitaker and Cudmore (1987); Whitaker and French (1984) Soricinae Soricini Sorex isodon Soft Churchfield and Sheftel (1993); Churchfield et al. (1999) Soricinae Soricini Sorex longirostris Soft French (1980); Whitaker and Mumford (1972)

Appendix A continue

Appendix A continue Soricinae Soricini Sorex minutus Soft Castien and Gosalbez (1999); Chuchfield and Rychlik (2006); Klenovsek et al. (2013) Soricinae Soricini Sorex monticolus Soft Carraway and Verts (1994); Gunther et al. (1983); McCracken (1990) Soricinae Soricini Sorex palustris Soft Linzey and Linzey (1973); Whitaker and French (1984) Soricinae Soricini Sorex trowbridgii Soft Jameson (1955); Whitaker and Maser (1976) Soricinae Soricini Sorex vagrans Soft McCracken (1990); Whitaker and Maser (1976)

Appendix B. References for diet data in Appendix A.

Advani, R. and B.D. Rana. 1981. Food of the house shrw, Suncus murinus sidensis in the Indian desert. Acta theriologica. 26(7): 133-134.

Anderson, K.W. and E.D. Fleharty. 1967. Mammalian distribution within biotic communities of northeastern Jewell County, Kanasa. Fort Hays Studies-New Series, Science Series. 6: 1-46.

Bannaikova, A.A., D. Chernetskaya, A. Raspopova, D. Alexandrov, Y. Fang, N. Dokuchaev, B. Sheftel and V. Lebedev. 2018. Evolutionary history of the genus Sorex (Soricidae, Eulipotyphala) as inferred from multigene data. Zoological Scripta. 47: 518-538.

Bauerová, Z. 1988. The food of Crocidura suaveolens. Folia Zoologica. 37: 301-308.

Becerra, F., A.I. Echeverría, A. Casinos, and A.I. Vassallo. 2014. Another one bites in the dust: bite force and ecology in three caviomorph rodents (Rodentia, Hystricognathi). Journal of Experimental Zoology. 321A: 220-232.

Bee, J.W., G. Glass, R.S. Hoffmann and R.R. Patterson. 1981. Mammals in Kansas. University of Kansas Printing Service, Lawrence.

Bellocq, M.I., J.F. Bendell, and D.G.L. Innes. 1994. Diet of Sorex cinereus, the Masked Shrew, in relation to the abundance of lepidoptera larvae in Northern Ontario. The American Midland Naturalist. 132(1): 68-73.

Bever, K.V. 1983. Zur Nahrung der Hausspitzmaus, Crocidura russula (Hermann, 1780). Säugetierkundliche Mitteilungen. 31: 13-26.

Brahmi, K., S. Aulagnier, S. Slimani, C.S. Mann, S. Doumandji, and B. Baziz. 2003. Diet of the Greater White-toothed Shrew Crocidura russula (Mammalia: Soricidae) in Grande Kabylie (Algeria). Italian Journal of Zoology. 79(2): 239-245.

Brant, S.V. and G. Orti. 2002. Molecular phylogeny of Short-tailed Shrews, Blarina (Insectivora: Soricidae). Molecular Phylogenetics and Evolution. 22(2): 163-173.

Buckner, C.H. 1964. Metabolism, food capacity and feeding behaviour in four species of shrews. Canadian Journal of Zoology. 42: 259-279.

Carraway, L.N. and B.J. Verts. 1994. Relationship of mandibular morphology to relative bite force in some Sorex from western North America. In J.F. Merritt, G.L. Kirkland Jr. and R.K. Rose (Eds.), Advances in the Biology of Shrews (pp. 201- 210), Special Publication, Carnegie Museum of Natural History, Pittsburgh.

Carraway, L.N., B.J. Verts, M.L. Jones and J.O. Whitaker Jr. 1996. A search for age- related changes in bite force and diet in shrews. The American Midland Naturalist. 135(2): 231-240.

Castién, E. and J. Gosálbez. 1995. Diet of Sorex coronatus in the western Pyrenees. Acta theriologica. 40(2): 118-121.

Castién, E. and J. Gosálbez. 1999. Habitat and food preferences in a guild of insectivorous mammals in the Western Pyrenees. Acta Theriologica. 44: 1-13.

Churchfield, S. 1985. Diets of two syntopic small mammals in the Inyanga National Park, Zimbabwe. South African Journal of Zoology. 20(2): 65-67.

Churchfield, S. and B.I. Sheftel. 1993. Food niche overlap and ecological separation in a multi-species community of shrews in the Siberian taiga. Journal of Zoology. 234: 105-124.

Churchfield, S. 1994. Foraging strategies of shrews, and the evidence from field studies. In J.F. Merritt, G.L. Kirkland Jr. and R.K. Rose (Eds.), Advances in the Biology of Shrews (pp. 77-87), Special Publication, Carnegie Museum of Natural History, Pittsburgh.

Churchfield, S., P. Barriere, R. Hutterer and M. Colyn. 2004. First results on the feeding ecology of sympatric shrews (Insectivora: Soricidae) in the Tai National Park, Ivory Coast. Acta Theriologica. 49(1): 1-15.

Churchfield, S., D. Dieterlen, R. Hutterer and A. Dudu. 2007. Feeding ecology of the armored shrew, from the north-eastern Democratic Republic of Congo. Journal of Zoology. 273: 40-45.

Churchfield, S., L. Rychlik and J.R.E. Taylor. 2012. Food resources and foraging habits of the common shrew, Sorex araneus: does winter food shortage explain Dehnel’s phenomenon? OIKOS. 121(10): 1593-1602.

Clausnitzer, V., S. Churchfield, and R. Hutterer. 2003. Habitat occurrence and feeding ecology of Crocidura montis and Lophuromys flavopunctatus on Mt. Elgon, Uganda. African Journal of Ecology. 41: 1-8.

Conaway, C.H. and D.W. Pfitzer. 1952. Sorex palustris and Sorex dispar from the Great Smokey Mountains National Park. Journal of Mammalogy. 33(1):106-108.

Conner, P.F. 1960. The small mammals of Otsego and Schoharie Counties, New York. Bulletin (New York State Museum and Science Service). 382: 1-84.

Davis, W.B. and D.J. Schmidly. 1994. The mammals of Texas. Texas Parks and Wildlife Press, Austin.

Dickman, C.R. 1995. Diets and habitat preferences of three species of crocidurine shrews in arid southern Africa. Journal of Mammalogy. 237: 499-514.

Dokuchaev, N.E., L.G. Emelyanova and P.T. Orekhov. 2015. Shrews of the Nadym River Basin (north of western Siberia). Contemporary Problems of Ecology. 8(1): 51-55.

French, T.W. 1980. Sorex longirostris. Mammalian Species (pp. 1-3). The American Society of Mammalogists.

Gunther, P.M., B.S. Horn, and G.D. Babb. 1983. Small mammal populations and food selection in relation to timber harvest practices in western Cascade mountains. Northwest Science. 57: 32-44.

Hoffmeister, D.F. and W.W. Goodpaster. 1962. Life history of the Desert Shrew Notiosorex crawfordi. The Southwestern Association of Naturalists. 7(3/4): 236- 252.

Jakub, K., K. Peter, T. Filip, M. Ševčík, and B. Ivan. 2017. Diet of shrews (Soricidae) in urban environment (Nitra, Slovakia). Rendiconti Lincei. 28: 559-567.

Jameson, E.W., Jr. 1955. Observations on the biology of Sorex trowbridgei in the Sierra Nevada, California. Journal of Mammalogy. 36(3): 339-345.

Johnson, M.L. and C.W. Clanton. 1954. Natural history of Sorex merriami in Washington State. The Murrelet. 35(1): 1-4.

Jones, J.K., D.M. Armstrong, R.S. Hoffmann, and C. Jones. 1983. Mammals of the northern Great Plains (pp. 379). University of Nebraska Press, Lincoln.

Khanam, S., M. Mushtaq, M.S. Nadeem, and A.R. Kayani. 2017. Population characteristics of Suncus murinus in rural commensal habitats of Pothwar, Pakistan. Asian Journal of Agriculture and Biology. 5(4): 270-279.

Klenovsek, T., T. Novak, M. Cas, T. Trilar and F. Janzekovic. 2013. Feeding ecology of three sympatric Sorex shrew species in montane forest of Slovenia. Folia Zoologica. 63(3): 193-199.

Kuviková, A. 1987. Nahrung der zwei Arten der Gattung Crocidura, C. leucodon and C. suaveolens in der Slowakei (Mammalia, Soricidae). Lynx. 23: 51-54.

Linzey, D.W. and A.V. Linzey. 1973. Notes on food of small mammals from Great Smokey Mountain National Park, Tennesse – North Carolina. Journal of the Elisha Mitchell Scientific Society. 89(12): 6-14.

Linzey, D.W. 2016. Mammals of Great Smoky Mountains National Park: 2016 Revision. Southern Naturalist. 15: 1-93.

McCay, T.S. and G.L. Storm. 1997. Masked Shrew (Sorex cinereus) abundance, diet, and prey selection in an irrigated forest. The American Midland Naturalist. 138(2): 268- 275.

McCay, T.S. 2001. Blarina carolinensis. Mammalian Species. 673: 1-7.

McCracken, K.E. 1990. Microhabitat and dietary partitioning in three species of shrews at Yellow Bay, Montana. Graduate Student Thesis, Dissertations, & Professional Papers. 7014.

Niethammer, J. 1978. Weitere Beobachtungen über syntope Wasserspitzmäuse der Arten Neomys fodiens und N. amomalus. Zeitschrift für Säugetierkunde. 43: 313-321.

Punzo, F. 2003. Observations on the diet composition of the Gray Shrew Notiosorex crawfordi (Insectivora), including interactions with large arthropods. Texas Journal of Science. 55(1): 75-86.

Richmand, N.D. and W.C. Grimm. 1950. Ecology and distribution of the shrew Sorex dispar in Pennsylvania. Ecology. 31(2): 279-282.

Ritzi, M., B.C. Bartels, and D.W. Sparks. 2005. Ectoparasites and food habits of Elliot’s Short-tailed Shrew, Blarina hylophaga. Southwestern Association of Naturalists. 50(1): 88-93.

Rowe-Rowe, D.T. 1986. Stomach contents of small mammals from the Drakensberg, South Africa. South African Journal of Wildlife Research. 16(1): 32-35.

Santamarina, J. 1993. Feeding ecology of a vertebrate assemblage inhabiting a stream of NW Spain (Riobo; Ulla basin). Hydrobiologia. 252: 175-191.

Sylvester, T.L., J.D. Hoffman, and E.K. Lyons. 2012. Diet and Ectoparasites of the Southern Short-Tailed Shrew (Blarina carolinensis) in Louisiana. Western North American Naturalist. 72(4): 586-590.

Whitaker, J.O., Jr. G.S. Jones and D.D. Pascal Jr. 1975. Notes on mammals of the Fires Creek Area, Nantahala Mountain, North Carolina, including their ectoparasites. Journal of the Elisha Mitchell Scientific Society. 91: 13-17.

Whitaker, J.O., Jr. and C. Maser. 1976. Food habits of five Western Oregon shrews. Northwest Science. 50(2): 102-107.

Whitaker, J.O., Jr. and T.W. French. 1984. Foods of six species of sympatric shrews from New Brunswick. Canadian Journal of Zoology. 62(2): 622-626.

Whitaker, J.O., Jr. and W.W. Cudmore. 1987. Food and ectoparasites of shrews of south central Indiana with emphasis on Sorex fumeus and Sorex hoyi. Proceedings of the Indiana Academy of Science. 96: 543-552.

Whitaker, J.O., Jr., G.D. Hartman and R. Hein. 1994. Food and ectoparasites of the Southern Short-tailed Shrew, Blarina carolinensis (Mammalia: Soricidae), from South Carolina. Brimleyana. 21: 97-105.

Wołk, K. 1976. The winter food of the European Water-shrew. Acta Theriologica. 21: 117- 129.

Appendix C. Figures showing cranial musculature of dissected Sorex trowbridgii.

Figure 7. Lateral view of skull of dissected Sorex trowbridgii. Colors: blue circle, temporalis; red circle, masseter.

Figure 8. Dorsal view of skull of dissected Sorex trowbridgii.

Figure 9. Ventral view of skull of dissected Sorex trowbridgii.