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Ecological and Histological Aspects of Tail Loss in Spiny Mice (Rodentia: Muridae, Acomys) with a Review of Its Occurrence in Rodents

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Ecological and Histological Aspects of Tail Loss in Spiny Mice (Rodentia: Muridae, Acomys) with a Review of Its Occurrence in Rodents J. Zool., Lond. (1999) 249, 187±193 # 1999 The Zoological Society of London Printed in the United Kingdom Ecological and histological aspects of tail loss in spiny mice (Rodentia: Muridae, Acomys) with a review of its occurrence in rodents Eyal Shargal1, Lea Rath-Wolfson2, Noga Kronfeld1 and Tamar Dayan1* 1 Department of Zoology, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel 2 Rabin Medical Center, Golda Campus, Petah Tiqva, Israel (Accepted 16 December 1998) Abstract Many individual nocturnal common spiny mice Acomys cahirinus and diurnal golden spiny mice A. russatus in the ®eld are found missing all or part of their tails. Possibly, this is a predator avoidance mechanism. A 25-month ®eld study revealed that at Ein Gedi (Israel) percentage tail-loss is 63% in male and 44% in female golden spiny mice, and 12% in male and 25% in female common spiny mice. Tail loss is signi®cantly more common in golden spiny mice than in common spiny mice, possibly re¯ecting differences in predation risk or predator ef®ciency between the different microhabitats used by these species and in their different activity times. However, inter- and intraspeci®c aggressive interactions may also account in part for this pattern. Few signi®cant differences in longevity, body mass, or reproductive condition were found between tailed and tail-less spiny mice, suggesting an advantage to tail-less individuals. Histological sections revealed a plane separating the skin layer from the underlying muscles and vertebrae, facilitating loss of the skin with little bleeding. The remainder (muscles and bone) is later chewed off by the mouse. A survey of published cases of tail loss in rodents revealed that this phenomenon occurs in at least 35 species and has evolved separately in eight rodent families, with no clear pattern in systematics, geography, or habitat use. Key words: spiny mice, tail loss, autotomy, histology, predation INTRODUCTION (Rathmayer & Bevengut, 1986; Formanowicz, 1990), arms (Oji & Okamoto, 1994) and tails (Feder & Arnold, Autotomy, the loss of a body part, sometimes accom- 1982; Ducey, Brodie & Barness, 1993). panied by subsequent regeneration, is a common feature Among vertebrates, caudal autotomy, the ability to of many invertebrates and vertebrates. It is often con- shed the tail (as de®ned by Arnold, 1988; see also Roth sidered an anti-predatory defence mechanism (e.g., & Roth, 1984 for alternative de®nitions) in reptiles and Robinson, Abele & Robinson, 1970; Arnold, 1984; amphibians is a common and well recognized anti- Cooper & Vitt, 1985; Formanowicz, Brodie & Bradley, predator defence mechanism and has been studied at 1990), in which body parts that are attacked by a both the anatomical±histological and ecological± predator may be sacri®ced in order to save the indivi- evolutionary levels (e.g. Arnold, 1984; Abdel-Karim, dual animal. This mechanism has apparently evolved 1993; Salvador et al., 1996). In mammals, accounts of independently in disparate taxa such as spiders (e.g. tail loss among rodents have appeared sporadically in Klawinski & Formanowicz, 1994; Cloudsley- the literature throughout this century and have usually Thompson, 1995), insects (e.g. Carlberg, 1981, 1984; been related to predator avoidance (e.g. Cuenot, 1907; Rietschel, 1987), echinoderms (e.g. Lawrence, 1992), Gogl, 1930; Layne, 1972; see also Heneberg, 1910). crustaceans (e.g. Hirvonen, 1992; Abello et al., 1994; Early research dealing with the tail histology of these Juanes & Smith, 1995), slugs (e.g. Deyrup-Olsen, species revealed interspeci®c differences in the Martin & Paine, 1986; Pakarinen, 1994), reptiles (e.g. mechanism of tail loss (Mohr, 1941). Generally, studies Arnold, 1988), and amphibians (e.g. Labanick, 1984). of tail loss in rodents were not accompanied by ®eld The sacri®ced organs include chelipeds (e.g. Robinson research and reports of the extent of this phenomenon et al., 1970; Juanes & Smith, 1995), walking legs in natural populations remain largely anecdotal. We studied tail loss in two sympatric congeneric *All correspondence to: T. Dayan, Department of Zoology, Tel Aviv species of spiny mice: the common spiny mouse Acomys University, Ramat Aviv, Tel Aviv 69978, Israel cahirinus and the golden spiny mouse A. russatus. The 188 E. Shargal ET AL. two species co-occur in areas of rocky deserts in the probability of survival estimates because of the low south of Israel and are active at different times: population densities, which would render the results A. cahirinus is nocturnal while A. russatus is diurnally inaccurate. The limited trapping period (25 months) active (e.g. Kronfeld et al., 1994), apparently as a result meant that estimated longevity of some individuals was of interspeci®c competition with A. cahirinus (Shkolnik, arti®cially reduced. This bias should affect tailed and 1971). We encountered many individuals of the two tail-less mice to the same degree, but may result in a species that had lost their tail both in the ®eld and in reduced difference between the 2 groups. our captive colony. To study a possible cost in reproduction associated Our ®eld and laboratory study of tail loss in spiny with tail loss, we also compared the reproductive condi- mice set out to: look at the histological mechanism of tion (pregnancy or evident nipples for females and tail loss; determine the extent of this phenomenon in scrotal testes for males) of mice with and without tails, free-living populations; assess possible associated costs using a 2-tailed chi-square test, during the period of in longevity, body mass, and reproduction; gain insight reproduction (February±August; Shargal, 1997). into the possible ecological-evolutionary basis for this Regarding a possible cost in physical condition, we phenomenon. compared the mean body mass of mice with and Here we report the results of our study. We also without tails using a Student's t-test (excluding survey the literature on tail autotomy in rodents in an immature individuals). attempt to ®nd an ecological and/or taxonomic pattern for this phenomenon. RESULTS MATERIALS AND METHODS When one gently holds the tail of an individual spiny mouse, the animal immediately walks away ± the skin of We studied histological sections of tails of both species the tail separates easily from the underlying muscles and of spiny mice, and for comparison of the laboratory vertebral column, with only slight bleeding, and breaks, house mouse (Mus musculus). We examined intact tails, leaving only the sheath (consisting of epidermis and tails that had just lost their skin sheath (mice were upper part of the dermis only) in one's grasp. There is sacri®ced within 2 min of skin sheath loss), and tails no need to exert pressure or to pull. The remainder of that had been partially lost some time ago. Tails were the tail, bone and tissue, is later consumed by the routinely ®xed in buffered formalin 10% and then mouse, which is left with a considerably shorter tail or embedded in paraf®n. We took longitudinal sections no tail at all. stained with H&E (haematoxylin and eosin). Longitudinal histological sections revealed the We trapped common spiny mice and golden spiny presence of a longitudinal plane between the skin and mice for 25 consecutive months in a 5000 m2 grid near the underlying muscles and vertebrae (Fig. 1). This Kibbutz Ein-Gedi, Israel, near the Dead Sea (31828' N, plane, which is formed by a separation in the connective 35823' E, 100±350 m below sea level), using 200 tissue ®bres that bind the skin to the underlying tissues, Sherman collapsible traps during the ®rst year and 100 enables the skin to separate with ease (Fig. 2). This traps subsequently. We trapped each month for 3 phenomenon was found in both species. In the tail of consecutive days and nights, checking the traps at dawn the laboratory mouse there is no such plane, and the and dusk and at 4 equal intervals during the day. We skin is fully connected with connective tissue to the recorded the species, sex, reproductive condition, and underlying layers (Fig. 3). condition of the tail of each individual trapped, and The occurrence of this separating plane appears to marked individuals by toe-clipping.{ facilitate the loss of the skin sheath and of the ensuing We compared the percentage tail loss of the different tail. However, in those tails that were only partially lost, sexes and species using 2-tailed chi-square tests. In order we observed ®brosis in the remaining stump. This part to study a possible cost in longevity associated with tail could then no longer disconnect with ease when tugged. loss, we compared the length of time during which We were unable to discern any speci®c points where the individual mice were repeatedly captured (months skin is most likely to break. However, connective tissue between ®rst and last record) for individuals with tails ®bres do occur sporadically along the plane and may be and those without part or all of their tail, using a t-test the points where the skin tears. This histology may (after ascertaining normality of distributions using the account for the degree of variation in tail loss encoun- Shapiro±Wilk's W-test). Only individuals that were tered in the ®eld (see below). trapped for more than 1 month, and therefore deemed In the 25-month ®eld study we found a high per- to be residents, were included in the analysis, thus centage of individuals with partial or total tail loss: 17 excluding transients. We did not use the Jolly-Seber out of 27 (c. 63%) male A. russatus, seven out of 16 (c. 44%) female A. russatus, three out of 26 (c. 12%) of { Editor's note: The Ethical Committee of the Zoological male A. cahirinus, and four out of 16 (25%) female Society of London considers that toe-clipping is no longer A.
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