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The Evolution of Antipredator Defenses in Tenrecs

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The Evolution of Antipredator Defenses in Tenrecs SMALL BUT SPINY: THE EVOLUTION OF ANTIPREDATOR DEFENSES IN TENRECS A THESIS Presented to the University Honors Program California State University, Long Beach In Partial Fulfillment of the Requirements for the University Honors Program Certificate Colin Stensrud Spring 2017 1 2 Abstract Various mammalian taxa have evolved different forms morphological adaptations to aid in preventing death by predators, including spines, quills, dermal plates, and noxious chemical sprays. The development of these traits has previously been linked to intermediate body size and an openness of habitat, as well as a low metabolic rate and insectivorous diet. One family, Tenrecidae, contains several species that have evolved spines despite a small body size. I investigated the ecological factors that favored the evolution of spines within this group, focusing on conspicuousness to predators through body size and openness of habitat. I compiled hair and spine measurements along with natural history data and ran comparative phylogenetic analyses to study the morphological and ecological factors that favored the evolution of these antipredator defenses. I show that as tenrecs evolve a larger body size and move into a more open habitat, they are more likely to evolve spines. I discuss how this defense may have evolved due to the tenrec diet, metabolic rate, and smaller size of Malagasy predators. Introduction When animals are required to venture into the open to search for food or find mates, selection favors adaptations that minimize the risk of detection and predation in the form of an assortment of antipredator behaviors (Lima and Dill 1990). Some species, however, may spend more time in open areas away from refuge than others, in which case specialized morphological defenses may aid in surviving confrontations with predators. (Caro 2005; Emlen 2008). Sticklebacks in marine environments containing predators have spines and armored plates, but these are reduced in freshwater environments with fewer predators. (Reimchen 1992; Barrett et al. 2008). Other studies have demonstrated that prey in exposed aquatic environments (e.g. pelagic zones) with variation in the abundance of predators relying on vision to detect prey show 1 plasticity in protective morphology development (O’Brien et al. 1979; Stenson 1987; Smith & Jennings 2000). In fact, mammalian species of intermediate size and living in open habitats are more conspicuous to predators, and may not have the chance to escape fast predators (Stankowich & Campbell 2016, Stankowich & Caro 2009). This necessitates more permanent defenses that increase the chance of survival when they cannot reach safety. Many mammal taxa have evolved forms of antipredator defense, including spines, quills, keratinized dermal plates, and noxious chemical sprays (Stankowich 2012). Lovegrove (2000, 2001) showed that mammals of intermediate size face higher predation risk, being too big to run away from predators but too small to successfully defend themselves. This requires them to either attain morphological adaptations that allow for higher running speeds (requiring a high basal metabolic rate (BMR)) or develop body armor (requiring lower BMRs). Myrmecophagous mammals (those that consume ants and termites) have been shown to have lower BMRs than mammals with other feeding styles, as well as the tendency to favor body armor over high locomotor ability and escape speed (McNab 1984). Stankowich and Campbell (2016) found that as small mammal lineages evolve a more intermediate size in an open habitat, they are more likely to evolve some form of body armor (spines, quills, noxious sprays, and dermal plates); this is especially true in insectivores, whose diet may favor body armor evolution due to reduced reliance on vision and olfaction while rooting around for prey on the ground. Their study. however, was very broad and coarsely scored defenses through pictures rather than actual study skins; a more thorough analysis of individual mammalian taxa is advisable. Here, I focused on the sources of selection that influenced the evolution of antipredator defenses within a unique family of mammals, the tenrecs (Tenrecidae). 2 Tenrecidae is a family of insectivorous mammals in the order Afrosoricida, comprised of four subfamilies: Potamogalinae (endemic to mainland Africa), Tenrecinae, Geogalinae, and Oryzorictinae (all endemic to Madagascar). Comprising 31 species in eight genera, the tenrecs of Madagascar have demonstrated substantial adaptive radiation within a basic body plan (Figure 1). Tenrecs rely on auditory and chemical communication over visual and retain the primitive mammal characteristics of internal testes, cloaca, and large litters of altricial young; additionally, many species of tenrec undergo daily torpor (Garbutt 2007; Eisenberg & Gould 1970). From a single ancestral colonization event, they have diversified to fill several mammalian niches occupied elsewhere by multiple families. Potamogalinae (Figure 1a), the otter-shrews, are native to West and Central Africa. They resemble otters (Lutrinae) in body morphology (save for a much smaller size) and behavior, living a highly aquatic lifestyle near streams and rivers where they emerge from burrows at night to feed on crustaceans, insects, and aquatic vertebrates such as fish and amphibians, searching for prey with their long whiskers (Ciszek & Myers 2000). Geogalinae (Figure 1h), the large-eared tenrecs, consists of only one genus and species, Geogale aurita. This small species is believed to be one of the first tenrec species to evolve, possibly resembling the earliest Eutherian mammals; it has a myrmecophagous diet, and extends its large ears to detect prey when foraging (Garbutt 2007). Oryzorictinae (Figure 1f; 1g), the furred tenrecs, is the most speciose subfamily. Limnogale (aquatic tenrec) is semi-aquatic like some rodents (e.g. muskrat: Ondatra zibethicus; European water vole: Arvicola amphibious) while Oryzorictes (mole tenrecs) are highly specialized fossorial tenrecs that resemble moles (Talpidae), having spade-like feet, long claws, and reduced eyes and ears. Microgale (the shrew tenrecs) consists of twenty-two species that exhibit a wide range of morphological variation, with 3 some having long prehensile tails for a partially arboreal lifestyle (M. longicaudata, M. principula), and others resembling true shrews (Soricidae: Garbutt 2007). Antipredator defenses likely evolved only once in the evolution of Tenrecidae; all species within the subfamily Tenrecinae have spine-like hairs along their dorsum, often resembling hedgehogs (Erinaceinae) in appearance. All live a terrestrial lifestyle save for Echinops (lesser hedgehog tenrec; Figure 1b), which is semi-arboreal. Tenrec ecaudatus (common tenrec; Figure 1e) has the largest mass of all the tenrecs, reaching up to 2kg. The genus Hemicentetes (streaked tenrecs; Figure 1d) has long, wide spines, and their characteristic black & yellow/white coloration resembles a neotenic form of the common tenrec. H. semispinosus form multi- generational family groups that are the most complex of any insectivore. Additionally, this species is the only known mammal to perform stridulation, creating low-frequency ultrasonic sounds for communication during foraging using a cluster of quills on their dorsum (Garbutt 2007; Eisenberg & Gould 1970). The evolution of antipredator defenses within such a diverse mammalian taxon begs the question of what sorts of selective pressures favored the evolution of spines in this group. In this study I compiled measurements of spine length from museum specimens across fourteen species of tenrecs, representing eight genera with at least one species from each subfamily (with Tenrecinae represented in full) with data on body mass, habitat use, and habitat openness in a series of comparative phylogenetic analyses. Following Stankowich and Campbell (2016), I hypothesized that an increase in body size and exposure within their habitat favored the evolution of spines within Tenrecinae. 4 Materials & Methods Spine Measurement Data for this study came from 14 species in the Tenrecidae family; I measured five specimens from each of five species. The specimens used were from the National Museum of Natural History in Washington, D.C. and the Natural History Museum of London. Two body regions on each specimen (nape of the neck (between the ears) and dorsal lumbar region) were sampled with 5 hairs/spines measured per region. I selected the most robust hairs or spines in each species and measured their width using digital calipers to the nearest .01mm and length using a modified plastic ruler as a depth gauge to measure length from the skin to the tip of the hair or spine. I averaged all these measurements together across all specimens for a species and named these measures Front Length, Front Width, Back Length, and Back Width. The average volume of the hair or spines from each region was calculated using the equation for the volume of a cylinder (V=πr2h) where r = Width/2 and h = Length to form Front Volume and Back Volume measures. After initial collection, due to the unusual shape of their spines being flat rather than cylindrical, I realized that Hemicentetes spp. required an additional Thickness measurement, which I subsequently took from the smallest dimensions of specimens at the Field Museum in Chicago. The Front Volume and Back Volume measures for Hemicentetes spp. were calculated using Volume = Length x Width x Thickness. Natural History Data Species Body Mass (g) were taken from the Pantheria
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