The Evolution of Antipredator Defenses in Tenrecs

Home , Afrosoricida, European water vole, Hemicentetes, Lesser hedgehog tenrec, Microgale, Micropotamogale

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

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).

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.

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 (2009) database and Log10 transformed to fit assumptions of normality. Activity was described as either cathemeral (0) or nocturnal (1) based on species descriptions by Garbutt (2007), and Ciszek & Myers (2000). A

Habitat Use score of 0 – 2 was assigned to each species based on descriptions of habitat utilization by Garbutt (2007) and Ciszek & Myers (2000); 0: entirely terrestrial, 1: partially specialized, and 2: highly specialized (be it arboreal, fossorial, aquatic, etc). To score Habitat

Openness, species-level habitat data was taken from the IUCN Redlist database (IUCN 2016); individual species presence and suitability in each habitat was scored: 3 = suitable/major importance, 2 = suitable/not major importance, 1.5 = unknown, 1 = marginal, 0 = not found.

Additionally, following Stankowich & Campbell (2016) each habitat type was given a score between 0 and 1 of the ability to visually detect an animal in the habitat (0 = completely concealed, 1 = completely visible) after examining images of these habitats. The assigned scores were: Subtropical/Tropical Dry Forest (0.6), Subtropical/Tropical Moist Lowland Forest (0.4),

Subtropical/Tropical Moist Montane Forest (0.2), Dry Savanna (0.8), Moist Savanna (0.5),

Subtropical/Tropical Dry Shrubland (0.4), Subtropical/Tropical Moist Shrubland (0.3),

Subtropical/Tropical High Altitude Shrubland (0.5), Subtropical/Tropical Dry Grassland (0.5),

Subtropical/Tropical High Altitude Grassland (0.5), Inland Wetlands (0.4), Arable Land (0.9),

Pastureland (0.8), Plantations (0.5), Rural Gardens (0.5), Urban Areas (0.7), Subtropical/Tropical

Heavily Degraded Former Forest (0.6), Irrigated Land (0.7), Seasonally Flooded Agricultural

Land (0.5). For example, a species of “suitable/major importance” in Subtropical/Tropical Dry

Forest, “suitable/not major importance” in Subtropical/Tropical Dry Shrubland, and “marginal” in Urban Areas would receive an openness score of [(3×0.6)+(2×0.4)+(1×0.7)]/(3+2+1) = 0.55.

Following Stankowich & Campbell (2016), Exposure was calculated by multiplying Body Mass by Openness scores.

Analyses

To condense my hair/spine measures into a single Spininess variable, I ran a phylogenetically corrected Principle Components Analysis (PCA) using the “phylpca” routine in the “phytools” package (Revell 2012) in R (R Core Team 2016) to combine the measurements of

Front Width, Front Volume, Back Width, and Back Volume. The first principle component PC1 explained 86.95% of the variance (PC2 only explained 11.37%) in the scores, therefore I focused on PC1 as the sole composite measure of Spininess. All four measures strongly negatively loaded onto PC1 (-0.47 - -0.97, Table 1); I multiplied PC1 by -1 to produce a Spininess score with positive values indicating larger spines.

To test for the effects of Body Mass, Openness, Activity, Habitat Use, and Exposure, I conducted phylogenetically controlled generalized least squares tests (PGLS) in the “caper” package (Orme et al. 2013) where lambda () was calculated using Maximum Likelihood methods. To this end, I used the first tree in the tree block from Faurby and Svenning’s (2014) mammal supertree and pruned it to include only the 14 Tenrecidae species from our data set.

Following Stankowich & Campbell (2016) we tested Spininess with two different models:

[Log10(Body Mass) + Openness + Habitat Use + Activity] and [Exposure + Habitat Use +

Activity]. Finally, I conducted an ancestral state reconstruction of both Spininess and Exposure using the “contMap” function in “phytools”.

Results

When testing Body Mass and Openness as separate factors against the Spininess PC1 score, I found that as species evolved greater body masses (Fig. 1a; λ = -0.107, t = -3.548, P =

0.006) and moved into more open habitats (Fig. 1b; λ = -0.107, t = -2.705, P = 0.024), they

7 evolved more robust spines. When Body Mass and Openness were combined into the single

Exposure factor, I found that as species became more exposed to predators they evolved more robust spines (Fig. 2; λ = 0.963, t = -3.122, P = 0.011). Activity and Habitat Use had no effect on spininess in either model (all P > 0.515).

Discussion

I found that as tenrecs evolved greater body masses and moved into more open habitats, they were more likely to evolve robust spines for defense. Overall, as species faced greater predator exposure overall they were more likely to develop more robust spines. This supports the results of Stankowich & Campbell (2016) who assessed the roles of body size, openness, and diet across all of Mammalia, and found that as smaller mammals evolve an intermediate body size they are more likely to develop body armor. Tenrecs evolving a larger body size would, in fact, correspond to a small mammal evolving a more intermediate body mass. Additionally, their finding that a primarily insectivorous diet favors the evolution of body armor is supported, given that all species of tenrecs are insectivorous (Garbutt 2007). However, the ‘danger zone’ described by Stankowich & Campbell (~800 g to 9 kg) is well outside the range of every tenrec species save for the common tenrec; the small but well-defended streaked tenrecs only reach masses up to 220 g. The development of defenses despite the small size of tenrecs may see its origin in the smaller size of Euplerids, the Malagasy mammalian carnivore predators. The fossa

(Cryptoprocta ferox) is the largest carnivore on the island, reaching only up to 10 kg (Garbutt

2007), whereas carnivores in mainland Africa can reach upwards of 65 to 200 kg (Hunt 2011,

Harrington 2004). Like tenrecs, extant Eupleridae arose from a single colonization event on

Madagascar and diversified to fill a number ecological niches and body forms (Goodman 2009), resembling cats (Felidae), civets (Viverridae), and mongooses (Herpestidae). While effective

8 spines may have evolved in these smaller prey in response to smaller predators, they are still much less defended than other mammals such as armadillos and porcupines (Stankowich &

Campbell 2016).

Predation experiments by Eisenberg & Gould (1970) on captive tenrecs by mammalian

Malagasy carnivores found that streaked tenrecs were only killed with great difficulty; they were only able to successfully kill the tenrec after fatiguing them through prolonged harassment or by landing a lucky bite to the head (at least not without the prey managing to stick its predator with spines). When Setifer (greater hedgehog tenrec) was presented to Galidia (ring-tailed mongoose), it curled into a ball that the predator was unable to breach, eventually giving up on its would-be prey. These experiments support the results of the present analyses, that the spines of Tenrecinae prove instrumental in surviving attacks from native Malagasy carnivores. Spines and armor on smaller mammals might be ineffective against larger mainland predators if they prove unable to withstand carnivore bite force. Supporting this, bite forces of Malagasy carnivores (35.5 – 145N) are much smaller than predators in mainland Africa (165.6 – 1314.7N;

Christiansen & Wroe 2007). Natural selection, however, likely favors tenrecs to be only as defended as they need to be to survive attacks from Malagasy carnivores and not necessarily stronger mainland predators.

Over the course of their evolutionary history, the Tenrecines moved into more open habitats and evolved larger body sizes, filling an insectivore niche likely not held by any mammalian species previously. This opportunity to feed on abundant arthropods in an unoccupied habitat may have provided them with the necessary nutrition to grow larger bodies; additionally, this extra energy would have facilitated the growth of spines that we see today as they reached the more intermediate body size seen in extant Tenrecinae.

Overall, I found that increasing body mass and habitat openness favored the evolution of antipredator defenses in the Tenrecinae subfamily. Future studies may wish to examine the origin and selection for the yellow/white & black aposematic coloration in the streaked tenrecs, as well as the banded coloration found in the spines of certain Tenrecinae species. Both the common and streaked tenrecs have a unique spine coloration in which the base of the spine is darker, getting lighter as the spine grows further from the body. It’s unclear how the presence of spines and the brightness of the light in the environment affect the evolution of this coloration. Additionally, examinations of BMRs (Lovegrove 2001) and relative brain sizes (Stankowich & Romero 2017) in spiny versus non-spiny tenrecs to determine how the evolution of body armor influences metabolism and intelligence in Tenrecidae may be warranted.

A H

G B

C C

E D

Figure 1. Examples of different tenrec body forms, representing all four subfamilies; each Tenrecinae genus shown on the right. (A) Nimba otter shrew (Micropotamogale lamottei, P.

Vogel); (B) Large-eared tenrec (Geogale aurita, IUCN Afrotheria); (C) Hova mole tenrec (Oryzorictes hova, Association Mitsinjo); (D) Taiva shrew tenrec (Microgale taiva, Association Mitsinjo); (E) Lesser hedgehog tenrec (Echinops telfairi, biolib.cz); (F) Greater hedgehog tenrec (Setifer setosus, biolib.cz); (G) Common tenrec (Tenrec ecaudatus, P. Oxford); (H) Lowland streaked tenrec (Hemicentetes semispinosus, P. Oxford)

A B

Figure 2. Scatterplot showing relationship between Spininess and (A) Body Mass and (B) Openness.

Figure 3. Ancestral tree showing the relationship between Exposure and Spininess. Increasing “warmth” of tree color indicates increasing trait value.

Table 1. Results of Principle Components Analysis (PCA). Principle Component values range from -1 to 1. PC1 (“Spininess”) PC2 Front Width -0.807 -0.028 Front Volume -0.973 -0.228 Back Width -0.470 0.715 Back Volume -0.888 0.456 % Variance Explained 86.95 11.37

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