A Natural History of Bat Foraging: Evolution, Physiology, Ecology, Behavior, and Conservation

A Natural History of Bat Foraging: Evolution, Physiology, Ecology, Behavior, and Conservation offers an all-inclusive resource on all aspects encompassing the vital process of foraging for bats. The book explores knowledge in the field, including sensory ecology, the development of cognitive maps, bat microbiomes, and molecular approaches to studying a bat’s diet. It covers the importance of foraging in biology, from evolution and natural selection, to physiology, behavior, ecology, and natural history. In addition, it provides a unique focus on the implications of bat foraging for conservation purposes, including the role that molecular biology can play in preventing species depletion or extinction.

With over 1,400 species, bats are among the most diverse vertebrate groups, having evolved an astonishingly broad range of foraging strategies to adapt to nearly all global regions and environments. The book assesses manmade and environmental issues that bats must overcome to ensure survival and prevent extinction. Written by international leaders in bat research, this is the ideal resource for bat specialists and conservationists, as well as zoologists, animal behaviorists, and academics associated with such disciplines.

• Offers multiple expert perspectives on bat foraging behavior, a key element that influences ecosystem dynamics and modern animal ecology
• Formatted in an easy-to-read structure throughout all chapters
• Addresses the conservation and protection status for bat foraging for current and future practical applications

• Language: English
• Publisher: Academic Press
• Release date: Nov 21, 2023
• ISBN: 9780323972611

Book preview

Chapter 1: Introduction

Danilo Russo ¹ , and Brock Fenton ²       ¹ Animal Ecology and Evolution Laboratory (AnEcoEvo), Dipartimento di Agraria, Università degli Studi di Napoli Federico II, Portici, Italy      ² Department of Biology, University of Western Ontario, London, ON, Canada

Abstract

This book explores the intricate world of bat foraging, examining their diverse strategies and adaptations in various environments. From the evolutionary origins of their diets to their remarkable anti-predatory adaptations, it delves into the sophisticated sensory systems guiding their nocturnal hunts and their critical ecological roles. The book emphasizes the interconnected relationships and dependencies within bat ecosystems, providing valuable insights into population dynamics, interspecific interactions, and ecosystem structure. By shedding light on the captivating world of bat foraging, it aims to inspire further research into these fascinating mammals and their vital role in our planet's biodiversity and sustainability.

Keywords

Bats; Ecological interactions; Ecosystem services; Foraging behavior; Foraging ecology; Microbiomes; Trophic guilds

Foraging is the behavior exhibited by animals searching for and acquiring food in their environment. It encompasses activities and strategies used by animals to locate, obtain, and consume food, involving a range of behaviors such as searching, capturing, handling, and eating a food item. Foraging is a vital activity for animals as it directly influences their survival, reproduction, and overall fitness (Stephens et al., 2007). The specific foraging behaviors employed by animals can vary greatly depending on their species, ecological niche, available resources, and evolutionary adaptations. The study of animal foraging behavior helps us understand how animals adapt to their environment (Dehnhard et al., 2020), make optimal foraging decisions (Trapanese et al., 2019), and allocate their energy and time to optimize food intake and ultimately fitness (Latty and Trueblood, 2020). Analyzing foraging provides invaluable insights into how animals have adapted to their environment: it offers a precious way to link individual behavior to higher organizational levels such as population dynamics, interspecific interactions, energy fluxes, and ultimately, ecosystem structure and processes (Abrams, 1984; Petchey et al., 2008; Brose, 2010; Gil et al., 2018). This book is about foraging in bats, exploring this fascinating issue from different perspectives and scales and evaluating the influence of this crucial aspect of bat behavior not only on the ecology of these outstanding mammals but also on the status and future of our planet and our own lives.

Bats (order Chiroptera) are a diverse group of mammals, numbering over 1460 species (Simmons and Cirranello, 2023) and, in mammals, are second only to rodents in terms of global species richness (Fig. 1.1). This overwhelming diversity is the result of a long evolutionary history that has led to an astonishing range of foraging strategies used by bats in almost every habitat worldwide to acquire food. Nocturnality (Rydell and Speakman, 1995) and active flight (Hedenström and Johansson, 2015) add further spatial and temporal perspectives to the natural history of bat foraging, making bats an especially interesting case within mammals from the ecological but also evolutionary viewpoint. To fully understand this present-day diversity in foraging strategies, it is therefore paramount to delve into the remote past, studying ancient bats to unveil the origins of diverse diets and foraging strategies in present-day species, as Simmons and Jones discuss in Chapter 2.

Figure 1.1  A compilation of close-up images showcasing the remarkable diversity of bat species. Arranged from top to bottom and left to right:Row 1 Nycteris thebaica; Rhinolophus simulator; Hipposideros speoris; Desmodus rotundus; Row 2 Molossus nigricans; Mormoops megalophylla; Diclidurus albus; Leptonycters yerbabuenae; Row 3 Lophostoma evotis (with ears up); Lophostoma evotis (ears down); Thyroptera tricolor; Noctilio leporinus; Row 4 Pteropus poliocephalus; Epomophorus walbergi; Uroderma bilobatum; Centurio senex.

Bat predation also exerts powerful selective pressure that has elicited astonishing antipredatory adaptations in certain prey species. In response to this evolutionary challenge, bats have developed an array of behavioral and physiological countermeasures. In Chapter 3, Barber and Ratcliffe illuminate the enthralling case of tympanate moths, which stands as one of the most captivating examples of the ongoing evolutionary arms race.

In Chapter 4, Diebold and Moss explore how foraging bats use a diverse range of sensory cues to locate food sources in various environments. Bats have evolved sophisticated systems, which are crucial to collect the sensory information needed to find food, and these solve very different tasks depending on the bat's dietary specialization, from insects, fruit, nectar and pollen to small vertebrates, and even blood.

The bats' long evolutionary history has led to today's surprising range of foraging strategies bats use to feed on a broad range of food items: arthropods and plants but also vertebrates such as fishes, frogs, rodents, birds, rodents, and even other bats, not to mention the three bat species that feed on blood in the Neotropics. For many of these species, echolocation plays a pivotal role in the context of their foraging strategies. The use of echolocation and the various foraging strategies used by bats are comprehensively covered in Chapter 5 by Schnitzler and Denzinger.

One captivating aspect of bat foraging ecology is their remarkable ability to acquire food in seemingly inhospitable habitats, such as deserts. These arid regions are home to a variety of fascinating bat species that exhibit astonishing strategies, such as scorpion hunting, which demands the bats to be resilient to the arthropod's venom. In Chapter 6, Conenna and Korine delve into the spatial and temporal movements of bats in the desert while also exploring their dietary preferences and adaptations to survive in these challenging environments.

A further characteristic that cannot be neglected is the highly gregarious nature of bats, often forming numerous colonies made of one or more species, and the diversity of bat social systems, whose dynamics are certainly complex and still poorly understood. The use of social information to increase foraging success and how it interacts with the distribution of trophic resources is, therefore, a fascinating field of study which we have just begun to explore and is presented in Chapter 7 by Kohles and Dechmann.

The spatial challenges encountered by bats become particularly intriguing when they pursue migrant insect prey. Insect migration is a captivating and still inadequately comprehended phenomenon that holds significant relevance to the investigation of bat foraging behavior. The predation of bats on these insects carries substantial ecological implications and bears crucial consequences for ecosystem services, especially considering the role of certain migratory insect species as agricultural pests, as Krauel et al. highlight in Chapter 8.

In Chapter 9, Mikula et al. cover the role of bats as prey in ecosystems, illustrating the diverse range of bat predators, touching upon the behavioral responses of bats to predation and the potential evolutionary consequences of predation on bat nocturnality. The chapter remarks on the need for further research on interactions between bats and their predators, identifying important topics for future studies.

Chapter 10, by McGuire and Boyles, focuses on the energetic aspects of bat foraging, highlighting the significant impact flight has on their daily energy expenditure. The review delves into the energy costs involved in obtaining food and accessing energy from their diet while also considering the consequences of changes in food availability across diverse spatial and temporal conditions. By examining both energy costs and gains, McGuire and Boyles provide valuable insights into the foraging ecology of bats.

In Chapter 11, Voigt et al. explore the captivating realm of migratory bats, which traverse vast distances seasonally, yet encounter significant metabolic challenges along their journey. The chapter endeavors to unravel the pivotal role of foraging in aiding these bats in their arduous task while highlighting the plethora of intriguing questions that continue to captivate the scientific community in relation to this awe-inspiring subject matter.

The study of microbiomes in animal physiology and ecology is of ever-growing importance, as it sheds light on the intricate interactions between animals and their associated microbial communities, influencing various aspects of their health, behavior, and ecological roles. In Chapter 12, Ingala illustrates gut microbiomes in bats and how these play crucial roles in bat physiology, ranging from nutrient acquisition to immunity. Given the diverse foraging strategies and diets exhibited by bats, from insectivory to herbivory, the composition and function of these gut communities show remarkable variation.

Chapter 13 challenges the classical view of bat trophic guilds, revealing that exceptions previously overlooked are increasingly evident with advanced analytical methods. In this chapter, Clare and Oelbaum stress the importance of thorough dietary analysis and caution against under-reporting or overgeneralizing bat diets to safeguard their ecological significance.

In Chapter 14, Becker et al. uncover the complex interactions between bat foraging, contaminants, and infection, shedding light on the impacts on bat health, zoonotic risk, and conservation practices and showing how diverse foraging strategies shape exposure to harmful substances and parasites.

Yu and Muchhala, in Chapter 15, unveil the crucial ecological services rendered by bats as they consume insects, fruits, and nectar, which, in turn, contribute to pest regulation, pollination, and seed dispersion. Delving into the varied eating habits and foraging patterns of bats, the chapter explores their far-reaching ecological and economic implications but also highlights the existing knowledge gaps on the economic benefits derived from bat-dependent ecosystem services.

Bat foraging exhibits a complex web of ecological interactions, encompassing predator–prey dynamics and mutualistic relationships like plant pollination and seed dispersal. Human activities pose threats to bats by modifying or disturbing these interactions. Therefore, safeguarding and restoring bat habitats are essential for preserving bats and promoting a One Health Strategy that addresses wildlife health, ecosystem health, and human health interconnections. In Chapter 16, Frick et al. emphasize these aspects, along with the importance of establishing and maintaining robust foraging habitats that could potentially benefit local communities.

The intricate world of bat foraging offers a captivating and multifaceted lens through which we can explore the diverse strategies and adaptations these remarkable mammals employ to survive in a variety of environments. From the evolutionary origins of their diets to the astounding antipredatory adaptations they have developed, from the sophisticated sensory systems guiding their nocturnal hunts to the critical ecological roles they play, bat foraging behavior unveils a rich tapestry of interconnected relationships and dependencies. As we investigate more comprehensively the complex interplay between bats and their environments, we uncover invaluable insights into population dynamics, interspecific interactions, and the intricate balance of ecosystem structure and processes. We hope that this book successfully sheds light on the fascinating world of bat foraging, sparking curiosity and inspiring further research into the extraordinary ecology, behavior and evolution of these fascinating mammals and their vital role in the broader fabric of our planet's biodiversity and sustainability.

References

1. Abrams P.A. Foraging time optimization and interactions in food webs. Am. Nat. 1984;124(1):80–96.

2. Brose U. Body‐mass constraints on foraging behaviour determine population and food‐web dynamics. Funct. Ecol. 2010;24(1):28–34.

3. Dehnhard N, Achurch H, Clarke J, Michel L.N, Southwell C, Sumner M.D, Eens M, Emmerson L.High inter‐and intraspecific niche overlap among three sympatrically breeding, closely related seabird species: generalist foraging as an adaptation to a highly variable environment?J. Anim. Ecol. 2020;89(1):104–119.

4. Gil M.A, Hein A.M, Spiegel O, Baskett M.L, Sih A. Social information links individual behavior to population and community dynamics. Trends Ecol. Evol. 2018;33(7):535–548.

5. Hedenström A, Johansson L.C. Bat flight: aerodynamics, kinematics and flight morphology. J. Exp. Biol. 2015;218(5):653–663.

6. Latty T, Trueblood J.S. How do insects choose flowers? A review of multi‐attribute flower choice and decoy effects in flower‐visiting insects. J. Anim. Ecol. 2020;89(12):2750–2762.

7. Petchey O.L, Beckerman A.P, Riede J.O, Warren P.H. Size, foraging, and food web structure. Proc. Natl. Acad. Sci. U. S. A. 2008;105(11):4191–4196.

8. Rydell J, Speakman J.R. Evolution of nocturnality in bats: potential competitors and predators during their early history. Biol. J. Linn. Soc. 1995;54(2):183–191.

9. Simmons N.B, Cirranello A.L. Bat Species of the World: A Taxonomic and Geographic Database. 2023. 

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10. Stephens D.W, Brown J.S, Ydenberg R.C, eds. Foraging: Behavior and Ecology. University of Chicago Press; 2007.

11. Trapanese C, Meunier H, Masi S. What, where and when: spatial foraging decisions in primates. Biol. Rev. 2019;94(2):483–502.

Chapter 2: Foraging in the fossil record

Diet and behavior of the earliest bats

Nancy B. Simmons ¹ , and Matthew F. Jones ²       ¹ Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, New York, NY, United States      ² Biodiversity Knowledge Integration Center, School of Life Sciences, Arizona State University, Tempe AZ, United States

Abstract

Understanding the origins of the diverse diets and foraging strategies seen in extant bats requires a comparative perspective including consideration of adaptations seen in ancient bats. While most fossil taxa are known only from craniodental fragments, Eocene lagerstätten preserve multiple species of bats known from entire skeletons, some with fossilized stomach contents. Analyses of available data indicate that Eocene bats were primarily insectivorous animalivores or omnivores. Perch hunting probably represents the primitive foraging strategy for Chiroptera. Laryngeal echolocation evolved early in the bat clade, but many of the more primitive bat taxa were probably gleaners that detected their prey using acoustic cues and vision. However, some ancient bats apparently hunted by aerial hawking using echolocation just as most bats do today. The presence of diverse bat faunas on three continents in the early Eocene suggests that bats were already well established, speciose, and ecologically diverse worldwide by this time.

Keywords

Chiroptera; Diet; Echolocation; Eocene; Foraging; Fossils; Vision

The Eocene brought mammals mean

And bats began to sing;

Their food they found by ultrasound

And chased it on the wing.

Pye (1968: 797)

Introduction

Living bats exhibit a greater range of diets and foraging strategies than any other mammalian order. Extant bat lineages include species that range from strict insectivores to carnivores, piscivores, frugivores, nectarivores, palynivores, granivores, sanguinivores, and many species have mixed diets that overlap two or more of these categories (Gardner, 1977; Freeman, 1998, 2000; Rex et al., 2010; Dumont et al., 2012; Santana et al., 2011a,b; Clare et al., 2014; Nogueira et al., 2005; Dumont, 2003). Methods of detecting and acquiring food similarly vary across chiropteran lineages. Most extant species are thought to obtain food by aerial hawking for flying insect prey, but many other species are gleaners, instead plucking food items from surfaces and branches, while yet others trawl for prey from the surface of water (Audet et al., 1991; Barclay and Brigham, 1991; Kalko et al., 1998; Kalka and Kalko, 2006; Santana et al., 2011a,b). Detection of food objects may depend on echolocation, listening for prey-generated sounds, olfaction, vision, or some combination of these senses, and getting to food once detected may involve behaviors ranging from continuous flight to perch-hunting, hovering, or even quadrupedal walking (Audet et al., 1991; Barclay and Brigham, 1991; Kalka and Kalko, 2006; Norberg and Rayner, 1987; Hessel and Schmidt, 1994; Thies et al., 1998; Riskin et al., 2006; Page and Bernal, 2020). Understanding the evolutionary history of this complex array of diets and foraging habits requires a comparative phylogenetic perspective, one that includes consideration of the diets and adaptations seen in the earliest bats—those known only from fossils.

The fossil record of bats begins in the early Eocene, approximately 55 Ma (Gunnell and Simmons, 2005; Brown et al., 2019). Early Eocene (Ypresian; 56–47.6 Ma) bats are known from multiple continents including North America, South America, Europe, Africa, Australia, Asia, and the Indian subcontinent (Gunnell and Simmons, 2005; Brown et al., 2019; Hand et al., 2016; Jones et al., 2021; Simmons et al., 2016; Smith et al., 2012; Hand and Sigé, 2018; Tejedor et al., 2005). Most of these fossils consist of fragments of skulls, jaws, and teeth (Gunnell and Simmons, 2005; Brown et al., 2019; Smith et al., 2012; Tejedor et al., 2005). However, some early bat fossils are spectacularly well preserved—particularly those from lagerstätten in the Green River Formation (USA: Wyoming; ∼52.5 Ma) and the Messel Pit (Grube Messel; Germany: Hesse; ∼47 Ma) (Jepsen, 1966; Richter and Storch, 1980; Habersetzer et al., 1994; Simmons and Geisler, 1998; Simmons et al., 2008; Habersetzer et al., 1992). Specimens from these localities include nearly complete articulated skeletons, some of which even contain fossilized stomach contents (Richter and Storch, 1980; Habersetzer et al., 1992, 1994). However, even fragmentary fossils may preserve important clues to foraging habits in ancient bats due to observed links between morphological and ecological traits in bats (Simmons et al., 2008, 2010, 2016; Jepsen, 1966; Simmons and Geisler, 1998; Novacek, 1985; Czaplewski and Baker, 2022).

Living bats (crown clade Chiroptera) are currently classified in 21 families each containing from one to over 500 species (Simmons and Cirranello, 2022). Several of these groups have fossil records that extend back into the Eocene and/or Oligocene including Emballonuridae, Nycteridae, Hipposideridae, Rhinolophidae, Vespertilionidae, and Mormoopidae (Smith et al., 2012; Simmons and Geisler, 1998; Simmons, 2005; Ravel et al., 2014, 2016; Morgan et al., 2019). Phylogenetic relationships of extant bats are typically assessed with molecular tools that depend on tissue samples and DNA sequencing (e.g., Eick et al., 2005; Stadelmann et al., 2007; Agnarsson et al., 2011), but placing fossils into evolutionary context and dating divergence points requires analyses of phenotypic data (e.g., Simmons and Geisler, 1998; O'Leary et al., 2013; Ravel et al., 2015, Rietbergen et al., 2023). Based on morphological comparisons, 11 extinct families of bats are currently recognized (Table 2.1).

While relationships of many of these taxa remain enigmatic, phylogenetic analyses of the better-known families (e.g., those known from more than just teeth) have indicated that several groups clearly fall outside the crown clade and thus may provide insights into early bat evolution that cannot be garnered from examination of only extant lineages (Gunnell and Simmons, 2005; Simmons and Geisler, 1998; O'Leary et al., 2013; Ravel et al., 2015; Rietbergen et al., 2023). Two families, Onychonycteridae and Icaronycteridae, are thought to represent the most-basal branch(es) in Chiroptera, with Archaeonycteridae, Palaeochiropterygidae, Hassianycteridae, and perhaps Tanzanycteridae, also representing stem lineages (Gunnell and Simmons, 2005; Simmons and Geisler, 1998; Simmons et al., 2008; O'Leary et al., 2013; Rietbergen et al., 2023). Among the remaining, Mixopterygidae, Philisidae, and Speonycteridae are hypothesized to belong within the crown group (e.g., Ravel et al., 2015; Maitre et al., 2008; Czaplewski and Morgan, 2012), while Necromantidae and Aegyptonycteridae occupy more uncertain positions within Chiroptera (Simmons et al., 2016; Hand et al., 2012).

Table 2.1

Dental morphology and diet

The primary clues for reconstructing diets of extinct bats come from teeth, which are the most commonly fossilized part of the bat skeleton (Brown et al., 2019). Dental morphology is highly correlated with diet in bats as in other mammals (Freeman, 1984, 1988, 1998, 2000; Santana et al., 2011b; López-Aguirre et al., 2022; Villalobos-Chaves and Santana, 2022) (Fig. 2.1), which allows analyses of diet in fossil taxa (e.g., Simmons et al., 2016; Horáček and Špoutil, 2012; Yohe et al., 2015). Most extant bat species are thought to be either entirely or primarily insectivorous and, like other insectivorous mammals, are characterized by a tribosphenic dentition (Santana et al., 2011b; Freeman, 1984; Horáček and Špoutil, 2012; Slaughter, 1970; Fenton and Simmons, 2015). This sometimes makes it difficult to distinguish isolated fossil dental remains of bats from those of other ancient mammals including Paleogene marsupials, leptictids, eulipotyphlans, adapisoricids, nyctitheres, and other dentally primitive therians (Hand et al., 1994, 2012, 2015, 2016; Smith et al., 2012; Hand and Sigé, 2018; Horáček and Špoutil, 2012; Hooker, 1996; Sigé et al., 2012).

Although the majority of extant bats are primarily insectivorous, other prey is regularly taken by a few bat species including both fish and terrestrial vertebrates (Norberg and Fenton, 1988; Gual-Suárez and Medellín, 2021). However, most carnivorous and piscivorous bats also eat insects and other arthropods (Santana et al., 2011a,b; Norberg and Fenton, 1988; Gual-Suárez and Medellín, 2021). For this reason, researchers have long distinguished animal-eating or animalivorous taxa from those that feed partly or entirely on plant products (Freeman, 1984, 1988, 1998, 2000; Rex et al., 2010; Santana et al., 2011a,b; Simmons et al., 2016; López-Aguirre et al., 2022; Norberg and Fenton, 1988; Gual-Suárez and Medellín, 2021). In this context, animalivory is an umbrella term that covers insectivorous, carnivorous, and piscivorous species, as well as those that have mixed diets including arthropods and other prey (Freeman, 1984, 1998, 2000; Santana et al., 2011a,b; Simmons et al., 2016; Norberg and Fenton, 1988; Gual-Suárez and Medellín, 2021). Dental morphology in plant-eating bats including frugivores, nectarivores, and granivores is often highly modified to the point that molar cusps and crests cannot be easily homologized with those of animalivorous taxa (Simmons et al., 2016; Freeman, 1988, 1995; López-Aguirre et al., 2022; Slaughter, 1970) (Fig. 2.1). Vampire bats represent a special case with an extensively modified dentition preserving barely any trace of ancestral tribosphenic traits (López-Aguirre et al., 2022; Slaughter, 1970).

All extant animalivorous bats have a dilambdodont tribosphenic dentition including a W-shaped ectoloph on the anterior upper molars (M1 and M2) and a well-developed talonid on the lower molars (Freeman, 1984, 1998, 2000; Santana et al., 2011b; Simmons et al., 2016; Slaughter, 1970; Norberg and Fenton, 1988) (Fig. 2.1). The primitive dental formula for bats includes 3 molars, and all extant animalivorous bats retain M3 although this tooth may be reduced somewhat in size and have an incomplete N- or V-shaped ectoloph; concomitantly, the lower m3 may have a reduced talonid (Simmons et al., 2016; Freeman, 1988, 1995; Slaughter, 1970; Koopman and MacIntyre, 1980). Multivariate dental topographic analysis and phylogenetic comparative methods indicate that in at least some lineages (e.g., Noctilionoidea), animalivorous taxa tend to have larger lower molars than plant-eating forms (López-Aguirre et al., 2022). In another lineage (Molossidae), smaller bats with higher molar topographic values (sharper, more complex molars) and more gracile heads mainly feed on softer insects, whereas bigger bats with lower molar topographic values (blunter, less complex molars) and more robust heads mostly feed on tougher insects (Villalobos-Chaves and Santana, 2022).

Fig. 2.1  Representative examples of upper premolars and molars from extant bats (not to scale) illustrating differences in tooth morphology that reflect dietary differences. A) Myotis myotis, an insectivore. B) Chrotopterus auritus, an animalivore who eats both vertebrates and insects. C) Phyllostomus hastatus, a specialized omnivore. D) Artibeus obscurus, a frugivore. E) Hylonycteris underwoodi, a nectarivore. P2-4 denotes upper premolars; M1-3 denotes upper molars.

Smaller-bodied animalivorous bat species tend to be mostly or entirely insectivorous, but as body size increases some species often include small vertebrates in their diet (Freeman, 1984, 1998, 2000; Santana et al., 2011a,b; Simmons et al., 2016; Norberg and Fenton, 1988). However, body size alone does not predict carnivorous or piscivorous habits. Some living bats that have medium or large body size (≥17 g) apparently prey only on insects (e.g., Saccolaimus peli, Hipposideros commersoni, Cheiromeles spp. (Norberg and Fenton, 1988)), while at least one tiny bat species (Micronycteris microtis, 5–7 g) occasionally eats lizards (Santana et al., 2011a). The ability to consume vertebrate prey apparently does not require large body size, although a predator must be large enough to overpower its prey and must have a sufficient gape and bite force to grasp, kill, and process it (Santana et al., 2011a,b; Simmons et al., 2016; Norberg and Fenton, 1988). Including vertebrates in the diet may actually have facilitated the evolution of larger body sizes in some lineages of animalivorous bats (e.g., by providing a selective advantage to increased body size by virtue of increasing available prey types), rather than large body size being a requirement for carnivory (Freeman, 2000; Simmons et al., 2016; Hand, 1985).

Carnivorous bats lack specialized carnassial teeth, but those that regularly eat vertebrate prey do show some dental modifications (Freeman, 1984, 1998; Simmons et al., 2016). Evolution of carnivory in bats is typically associated with elongation of the metastylar shelf and relative elongation of the postmetacrista on M1 and M2 (Freeman, 1984, 1998; Simmons et al., 2016; Hand, 1985) (Fig. 2.1). In concert with elongation of the postmetacrista, the paracone and metacone are often located closer together (Freeman, 1984, 1998), thus reducing the relative length of the postparacrista and premetacrista so that the W-shaped ectoloph in these species is highly asymmetrical (Simmons et al., 2016). In contrast, insectivorous bats (and those that are more omnivorous) typically have a more symmetrical W-shaped ectoloph in which the preparacrista and postmetacrista are subequal in length, and the postparacrista and the premetacrista are subequal in length (Freeman, 1984, 1998). The intraloph (distance between the paracone and metacone on the same tooth) and interloph (distance between the metacone on one tooth and the paracone on the tooth behind it) are close to subequal in noncarnivorous bats, but the intraloph is much smaller than the interloph in carnivorous species, especially on M2-M3 (Simmons et al., 2016; Freeman, 1984) (Fig. 2.1).

Although carnassial teeth are absent in Chiroptera, other shearing structures are present in some taxa. Czaplewski and Baker (2022) identified carnassiform notches—named for their resemblance to similar features on the carnassial teeth of carnivorans—on the teeth of many tribosphenic bats. A carnassiform notch consists of a small cleft in the edge of a talonid shearing crest accompanied by an adjacent accessory trough on the basinward side of the notch. These notches are hypothesized to improve the functional efficiency of shearing, specifically sectioning chitin, in bats with insectivorous or insectivorous–omnivorous dietary habits (Czaplewski and Baker, 2022). Most bats have upper molars with a basal distolingual cingulum or shelf (sometimes called a hypocone basin or shelf even if no hypocone is present), and many have a hypocone (Freeman, 1998; Simmons et al., 2016; Slaughter, 1970). The hypocone, which is typically quite small, is usually formed from the crestlike edge of the distolingual cingulum (Simmons et al., 2016; Slaughter, 1970). Slaughter (1970) hypothesized that molar cingulae function to protect the gums by deflecting prey exoskeletal fragments away from the alveoli. Carnivorous bats typically have a very large hypocone shelf or basin, but the hypocone itself is poorly developed or absent (Freeman, 1998; Simmons et al., 2016). This arrangement is congruent with the observation of Hunter and Jernvall (1995) that presence of a hypocone is incompatible with carnassiform upper molars since it disrupts occlusal contact between metacrista and paracristid, which are the primary shearing blades emphasized in carnivorous mammals. Possession of a well-developed hypocone is therefore generally thought to be associated with herbivory (including frugivory and other forms of plant eating) in mammals (Hunter and Jernvall,