STRUCTURE OF A POPULATION OF THE AMPHISBAENIAN TROGONOPHIS WIEGMANNI IN NORTH AFRICA

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2 Herpetologica, 67(3), 2011, E 2011 by The Herpetologists League, Inc. STRUCTURE OF A POPULATION OF THE AMPHISBAENIAN TROGONOPHIS WIEGMANNI IN NORTH AFRICA JOSÉ MARTÍN 1,3,NURIA POLO-CAVIA 2,ADEGA GONZALO 1,PILAR LÓPEZ 1, AND EMILIO CIVANTOS 1 1 Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, Madrid, Spain 2 Departamento de Biología, Universidad Autónoma de Madrid, Ciudad Universitaria de Cantoblanco, E Madrid, Spain ABSTRACT: Amphisbaenians are a group of reptiles specialized for a fossorial life, which makes the study of their peculiar biological and ecological adaptations difficult. The population biology of amphisbaenians is almost unknown. We described the seasonal variation in the size, age, and sex structure of a population of the amphisbaenian Trogonophis wiegmanni from the Chafarinas Islands, in North Africa. We specifically described body size (length and weight), frequency distribution of newborn and older juvenile individuals and adults, sex ratio of adults (which did not differ from a 1:1 ratio), and proportion of juveniles and newborn individuals in the population. The results indicated that T. wiegmanni is a viviparous species that delays reproduction until at least 2.5 yr, that almost half of adult females do not reproduce every year, and that females have a very small brood size (i.e., reproductive females give birth to a single juvenile at the beginning of autumn). We also used our data to infer growth and survival of juveniles, suggesting that mortality of newborn individuals is low. There are many aspects of the population biology of amphisbaenians that remain unknown and further studies are clearly needed. Key words: Amphisbaenians; Growth; North Africa; Population structure; Sex ratio; Trogonophis AMPHISBAENIANS are a group of reptiles morphologically specialized for a fossorial life (i.e., reduced vision, elongated body, loss of limbs and compact skull; Gans, 1974, 1978, 2005). These adaptations constrain amphisbaenians to solve their ecological demands with a suite of original responses different from those of epigeal reptiles (e.g., Colli and Zamboni, 1999; Gomes et al., 2009; López et al., 1998; Martín et al., 1990, 1991). However, there is very little information on the biology and ecology of most species of amphisbaenians. This is because of their fossorial secretive habits that make observations difficult. Most amphisbaenians are only found accidentally, for example, when digging or lifting stones. Thus, the few available data on amphisbaenian ecology are fragmentary, often based on the examination of small samples, and heavily dependent on anecdotal observations. To understand the ecology of a species, an important step is to determine the age size structure of their populations. This is relevant because males, females, and immature individuals may be subject to different selective pressures (e.g., Pilorge et al., 1987), and growth, fecundity and survivorship may vary 3 CORRESPONDENCE: , jose.martin@mncn.csic.es between sexes and age classes. Also, although the sex ratio of animal populations is usually one-to-one (Fisher, 1930), significant deviations from this ratio have been reported in several groups, including many reptiles, which may be explained by factors such as higher mortality, higher rates of emigration among one sex, or temperature-dependent sex determination (M Closkey et al., 1998; Stamps, 1983). However, because of their secretive habits, the population biology of most species of amphisbaenians is practically unknown, although data on population structure and growth are available for three amphisbaenian species of the genus Bipes (Papenfuss, 1982). The amphisbaenian Trogonophis wiegmanni Kaup, 1830, is a representative of the family Trogonophidae in North Africa (Gans, 2005). It is a Mograbian endemic with a range in the Mediterranean biome that extends from southwest Morocco to northeast Tunisia (Bons and Geniez, 1996). It lives buried in the soil in areas with sandy soils and abundance of leaf litter (Civantos et al., 2003), and it is usually found under rocks or dead wood, especially in the wetter seasons; in summer it is usually found buried deep in the ground (Bons and Geniez, 1996). Little research has been carried out on this species or other members of its family, but there is some information on its thermal 250

3 September 2011] HERPETOLOGICA 251 biology (Gatten and McClung, 1981; López et al., 2002), activity metabolism (Kamel and Gatten, 1983), and microhabitat selection (Civantos et al., 2003). The reproductive biology of amphisbaenians is also poorly known (Colli and Zamboni, 1999; Papenfuss, 1982; Vega, 2001; Webb et al., 2000; reviewed in Andrade et al., 2006), but in T. wiegmanni there are data on the seasonal development of reproductive organs (Bons and Saint Girons, 1963). Individual T. wiegmanni have delayed sexual maturity, which occurs at an age of 2.5 yr. In males, spermatogenesis occurs at a higher rate in spring and during prenuptial periods. In females, ovulation occurs by the end of June, but it seems that females do not necessarily ovulate and reproduce each year and probably often have a biannual reproductive cycle. Copulation takes place in June. In contrast to most amphisbaenian species, which are oviparous (Andrade et al., 2006), T. wiegmanni is viviparous, with the young (only one in most cases) being born in September (Bons and Saint Girons, 1963). However, all these data were inferred from a small sample of amphisbaenians captured in a variety of locations, and there is no information relating this reproductive biology to population structure. In this article we describe the seasonal variation in structure of a population of T. wiegmanni from the Chafarinas Islands in North Africa. In these islands, amphisbaenians are abundant and easy to find under rocks (Martín et al., in press a), and we were able to obtain a large amount of data from the same population. We specifically describe size, age, and sex structure of this population in spring and in autumn, and also examine whether there were differences between populations inhabiting different islands. We discuss how these data could be used to understand the population and reproductive biology of this amphisbaenian. MATERIALS AND METHODS Study Area We conducted field work at the Chafarinas Islands (Spain), a small island archipelago located in the southwestern area of the Mediterranean Sea (35u119N, 2u259W; datum 5 ETRS89), 2.5 nautical miles to the north of the Moroccan coast (Ras el Ma, Morocco) and 27 miles to the east of the Spanish city of Melilla. It consists of three islands: Congreso, Isabel II (the only one inhabited), and Rey Francisco. Congreso is the westernmost, largest (25.6 ha), and highest (137 m above seal level [asl]) of the islands. Isabel II (15.1 ha; 35 m asl) is located between Congreso (at 1 km) and Rey Francisco (at 175 m), which is the most eastern, smallest (13.9 ha), and lowest (31 m asl) of the islands. The islands present a dry, warm, Mediterranean climate that is strongly influenced by dominant winds from the east and west. Vegetation reflects the aridity of the climate (an average annual precipitation of 300 mm), high soil salinity, and guano accumulation from numerous seabird colonies. Hence, current vegetation is dominated by plants adapted to the salinity and drought, such as species of Atriplex, Suaeda, and Salsola. In general, the soils of the islands are poorly developed. Soils are characterized by a thin layer of rich organic matter, where the vegetation settles, that is underlain almost directly by the original volcanic rock (andesite or basalt). Sampling Procedures The study area was visited during 2 wk in September 2009 (autumn) and March 2010 (spring). We did not sample the area in summer because in this season amphisbaenians are buried deep in the ground and are very hard to find. We searched for amphisbaenians by lifting all stones found during the day between 0700 and 1800 (GMT) as we followed different random routes that covered all the habitats available in the three islands. We captured amphisbaenians by hand, gathered morphological measurements in situ, and released them at their exact point of capture in less than 1 min. For each individual we measured body mass with a Pesola spring scale (to the nearest 0.01 g) and snout-to-vent length (SVL; from the tip of the snout to the extreme posterior point of the cloacal flap) with a metallic ruler (to the nearest 1 mm). We ensured that the same individuals were not measured twice by avoiding sampling the same areas twice within the same season. All biometrical variables were log 10 transformed prior to analysis to meet assumptions

4 252 HERPETOLOGICA [Vol. 67, No. 3 FIG. 1. Size (snout-to-vent length) frequency distribution of all Trogonophis wiegmanni measured in spring (middle March) and autumn (middle September). Size classes are based on 5-mm increments in body length. of normality and homoscedasticity. To evaluate differences in body size (SVL or body weight), we performed two-way or three-way analyses of variance (ANOVA), with sex (for adults only), season, and island as factors. Pairwise comparisons were based on Tukey s honestly significant difference (HSD) tests (Sokal and Rohlf, 1995). We determined the sexes of adult amphisbaenians by examining the cloacas and carefully everting the hemipenis of males slightly. Juveniles could not be reliably sexed. We considered adults to be those amphisbaenians with a SVL. 120 mm based on published data on the maturity of reproductive organs, which correspond to individuals that are at least 2.5 yr old (Bons and Saint Girons, 1963). We tested for differences between observed sex ratios and a theoretical one of 1:1 using x 2 tests. In autumn, it was possible to distinguish easily between newborn individuals (born in that September) and older juveniles born in the two previous reproductive seasons. In spring, there is still a clear size difference between newborn (born in the previous September) and older juveniles. Newborn individuals were characterized because they were clearly smaller and also because they presented brighter yellow body background colorations than older individuals, and very dark purple or black heads, which become lighter in older individuals. Nevertheless, it was possible for a fast-growing newborn to be erroneously categorized as an older juvenile, or for a slow-growing older juvenile to be categorized as a newborn. However, we assumed that these two possibilities are equally likely and would cancel each other (Papenfuss, 1982). Changes in the ratio of juveniles or newborn individuals to adults between seasons and islands were tested with x 2 tests. To test whether or not all females reproduce each year (Bons and Saint Girons, 1963), we inferred the proportion of reproductive females in the population from the number of newborn individuals in relation to the number of adult females, assuming that each reproductive female gave birth to a single juvenile (Bons and Saint Girons, 1963). We estimated growth and survivorship of newborn individuals from the size age structure of the population by comparing the mean SVL and the relative numbers of newborn individuals captured in autumn with those of newborn individuals found in spring, and the sizes and numbers of these newborn individuals with the sizes and numbers of 1 yr old juveniles found in autumn (see Papenfuss, 1982, for a similar procedure). RESULTS Size Distribution We collected data on 381 amphisbaenians, of which 249 were adults (124 in spring and 125 in autumn). The mean (61 SE) SVL of adult amphisbaenians was mm (range mm; Fig. 1). There was no significant variation in SVL of adults between sexes (three-way ANOVA; F 1, , P ), or between seasons (F 1, , P ) or islands (F 2, , P ), and all the interactions were nonsignificant (F, 1.54, P in all cases).

5 September 2011] HERPETOLOGICA 253 Mean (61 SE) body weight of adult amphisbaenians was g (range g). Males were significantly heavier than females ( g vs g, respectively; three-way ANOVA; F 1, , P ), but there was no significant variation between seasons (F 1, , P ) or islands (F 2, , P ), and all the interactions were nonsignificant (F, 1.31, P in all cases). We captured a total of 132 juvenile amphisbaenians (71 in spring and 61 in autumn). The mean (61 SE) SVL of all juveniles was mm (range mm; Fig. 1). However, juveniles could be clearly assigned to different age size classes. In the autumn sample, we found small newborn individuals (born at the end of summer and beginning of autumn, i.e., in September) and large juveniles with an age of 1 or 2 yr from previous cohorts born in the previous years. In the spring sample, we found 6-mo-old small juveniles (born in the previous September) and older large juveniles with an age of 1.5 yr, whereas individuals older than 2.5 yr had already become adults. When considering these age classes, there were significant differences in SVL of newborn individuals between seasons (two-way ANOVA; F 1, , P, ) and between islands (F 2, , P, ), but the interaction was nonsignificant (season 3 island: F 2, , P ; Fig. 1). Newborn individuals were significantly larger in spring ( mm, range mm) than in autumn ( mm, range mm), indicating that births occurred in autumn. Also, newborn individuals were significantly smaller (Tukey s tests, P, 0.02 in both cases) on Rey Island ( mm) than on Congreso ( mm) or Isabel Islands ( mm), but did not differ between Congreso or Isabel Islands (P ). Similarly, there were significant differences in body weight of newborn individuals between seasons (two-way ANOVA; F 1, , P ) and between islands (F 2, , P, 0.001), although the interaction was nonsignificant (season 3 island: F 2, , P ). Newborn individuals were significantly heavier in spring ( g, range g) than in autumn ( g, range g), and significantly lighter (Tukey s tests, P, 0.01 in both cases) on Rey Island ( g)thanonCongreso( g) or Isabel Islands ( g), but did not differ between Congreso or Isabel Islands (P ). In older juveniles that were born in the previous reproductive seasons, SVL ( mm, range mm) was not significantly different between seasons (two-way ANOVA; season: F 1, , P ) or islands (island: F 2, , P ), and the interaction was nonsignificant (season 3 island: F 2, , P ; Fig. 1). Similarly, the body weights of older juveniles ( g, range g) were not significantly different between seasons (two-way ANOVA; season: F 1, , P ) or islands (island: F 2, , P ), and the interaction was nonsignificant (season 3 island: F 2, , P ). Sex Ratios of Adults The numbers of adult amphisbaenians of each sex captured throughout the study period (males, n 5 120, 48.2%; females, n 5 129, 51.8%) indicated that the observed sex ratio of adults was 1:1.07 (males:females), which did not differ significantly from a theoretical sex ratio of 1:1 (x , df 5 1, P ). The adult sex ratios were similar on the three islands (Congreso: 1:1, x , df 5 1, P ; Isabel: 1:1.16, x , df 5 1, P ; Rey: 1:1.05, x , df 5 1, P ) and did not differ significantly among islands (x , df 5 2, P ). Also, there were no significant differences in the adult sex ratio between seasons (spring: 1:1.25, autumn: 1:0.92; x , df 5 1, P ). Proportions of Juveniles and Newborn Individuals in the Population The proportion of juveniles in the population (34.65%; juveniles:adults 5 1:1.89) did not differ significantly between islands (x , df 5 2, P ) or between seasons (x , df 5 1, P ; Fig. 2). If we considered only the proportion of newborn individuals with respect to the adults (69 vs. 249, 27.71%; newborns:adults 5 1:3.61), there were no significant differences between seasons (spring: 32.26%, 1:3.10; autumn: 23.20%, 1:4.31; x , df 5 1, P ) or islands

6 254 HERPETOLOGICA [Vol. 67, No. 3 of births, these data suggested that mortality of newborn individuals was low in their first 1.5 yr of life. FIG. 2. Relative frequency distribution of Trogonophis wiegmanni age classes (adult males, adult females, juveniles, and newborn individuals) in spring (middle March) and autumn (middle September), in each of the three islands (C: Congreso; I: Isabel; R: Rey). (x , df 5 2, P ; Fig. 2). The ratio of newborn individuals to the number of adult females was low (1:1.87), suggesting that almost half of females did not reproduce in that year. This proportion did not differ significantly between seasons (spring: 1:1.72; autumn: 1:2.07; x , df 5 1, P ) or islands (x , df 5 2, P ). Growth and Survival of Juveniles Considering the seasonal changes in average size in the population of newborn and older juveniles, we could estimate that newborn individuals grew through their first autumn and winter (since their birth in September to the next spring, when they reached an age of 6 mo) an average of 7 mm in SVL (i.e., 1.2 mm/month). Also, in one more year (since their first spring to the next spring, when they reached an age of one and a half year), they grew about 21 mm in SVL (i.e., 1.75 mm/month). Finally, in a second year, these juveniles would reach the adult condition, when they were 2.5 yr old, by growing at least 17 mm more (i.e., 1.4 mm/month). Relative numbers of newborn individuals in spring did not differ significantly from the relative number of newborn individuals found in the previous autumn (x , df 5 1, P ; Fig. 1). Similarly, in spring, the relative numbers of newborn individuals did not differ significantly from the relative numbers of 1.5-yr-old juveniles (x , df 5 1, P ; Fig. 1), Assuming that there were no large interannual variations in the number DISCUSSION Our study, based on a large amount of data collected from three island populations and in two different seasons, provides a comprehensive picture of the structure of the population of T. wiegmanni in the Chafarinas Islands. We have specifically described the size frequency distribution, and proportions of newborn and older juvenile individuals and adults. The results also indicated that T. wiegmanni are viviparous, that females delay reproduction until an age of 2.5 yr, that almost half of adult females do not reproduce every year, and that females have a very small brood size (i.e., a single juvenile at the beginning of autumn). These data confirm some previous suggestions based on the examination of seasonal changes in reproductive organs of this amphisbaenian (Bons and Saint Girons, 1963). This intensive field study avoided several problems that can result from using fragmentary data or from biases in collection of specimens found occasionally over large areas and long time periods. We could readily analyze the age structure of juvenile T. wiegmanni because it was easy to differentiate the successive cohorts of individuals by size differences. In contrast, it was not possible to characterize the age structure of adults because age and size are probably not directly correlated in adults, and individuals of different age may have a wide overlap in body size. However, if we extrapolate from the growth rate (about 1.4 mm/month) estimated for juveniles, then the largest adults in our sample would take at least 6 yr to reach that size, and the majority of adults in this population (those with an average SVL size of about 150 mm) would be at least 4 yr old. Nevertheless, most adult T. wiegmanni in the population were probably older because, as occurs in many reptiles, growth rate should decrease with age and should vary widely among individuals (see review in Andrews, 1982), which would explain the accumulation of individuals with similar sizes but probably belonging to different cohorts.

7 September 2011] HERPETOLOGICA 255 The sex ratio of adult T. wiegmanni in this population did not differ from 1:1, which is similar to that found in some amphisbaenian species (Bernardo-Silva et al., 2006; Gomes et al., 2009; Vega, 2001), but not in others, in which sex ratios are female biased (Colli and Zamboni, 1999; Filogonio et al., 2009; Papenfuss, 1982). This variation might reflect phylogenetic or ecological differences. However, it could also be explained by sampling bias, because most of the published data come from small samples collected in different places and at different times, whereas few studies have analyzed large samples collected in short periods that did not introduce bias in sex ratio estimations. Nevertheless, strongly female-biased sex ratios have also been found in many lizards (Galán, 2004; Heulin, 1985; Schoener and Schoener, 1980), which has been suggested as a characteristic of polygynous, territorial species (Schoener and Schoener, 1980; Stamps, 1983). Biased sex ratios are attributable to between-sex differences in mortality rates, or to mobility and migratory behavior (M Closkey et al., 1998). Therefore, it is likely that a 1:1 sex ratio in T. wiegmanni indicates that this amphisbaenian is not polygynous and that births and mortality are not sex biased. Our results showed the presence of the smallest newborn individuals in the autumn sample only, which indicated that births occurred exclusively at the end of summer and beginning of autumn, as was suggested previously (Bons and Saint Girons, 1963). Juveniles were born with an average weight of 0.8 g, which represented about 16% of the weight of a female. Also, data on proportion of newborn individuals with respect to the number of adult females indicated that almost half of females did not reproduce in a year. Trogonophis wiegmanni is unusual among amphisbaenians in being viviparous (Bons and Saint Girons, 1963). Viviparity is relatively uncommon in reptiles and is expected to be particularly rare in burrowing squamates because distension of the body during gestation may impose high locomotory costs to females (Shine, 1985). Nevertheless, viviparity is a derived trait that has evolved independently at least three times in amphisbaenians (Andrade et al., 2006). It is likely that in T. wiegmanni, viviparity evolved as an adaptation to severe summer drought (coinciding with the gestation period), which might subject eggs laid in the soil to high mortality. It is also possible that negative effects of viviparity on burrowing performance explain why litter size is small and reproduction by females is not annual. The stability of the underground environment might explain why we did not find many differences between the populations of T. wiegmanni inhabiting the three islands that form the Chafarinas Archipelago. Basic population structure was very similar among islands, although there are clear differences in population densities among islands (Martín et al., in press a). The only difference found was that newborn individuals were slightly smaller on Rey Island than on the other two islands. This small difference might suggest a sampling bias or that there was a small asynchrony between islands in the dates when most births occurred. Alternatively, females on Rey Island might give birth to smaller juveniles. The population density of amphisbaenians is apparently higher on Ray Island (Martín et al., in press a), which may increase competition for resources and limit size of newborn individuals. Further studies should examine these possibilities and the reasons that caused interisland differences. Also, future studies should examine the effects of potential interannual variation in climatic conditions on reproductive success in amphisbaenians. The reproductive characteristics of T. wiegmanni (i.e., late and infrequent reproduction and very small brood size) suggest that it is a k-strategist (Pianka, 1970). Other amphisbaenians that have been examined also show a similar k-strategy and a low reproductive potential compared to most lizards (e.g., Andrade et al., 2006; Papenfuss, 1982; Vega, 2001). These similarities may be explained by energetic constraints of the subterranean environment. Moreover, amphisbaenians are a tropical group and T. wiegmanni lives in its northern distribution range, which has been suggested to explain its low reproductive capabilities (Bons and Saint Girons, 1963). However, in other animals, small brood size and low reproductive output can be compensated with a greater parental care to increase survival of juveniles. Newborn T. wiegmanni

8 256 HERPETOLOGICA [Vol. 67, No. 3 are often found in close company of an adult (Martín et al., in press b), which suggests that juveniles are allowed to remain within their parents territories until they are older, which could enhance offspring fitness by providing access to parentally defended high-quality habitats, as occurs in some viviparous skinks (Bull and Baghurst, 1998; Langkilde et al., 2007). These factors might explain the observed high survival of newborn individuals, inferred from the similar numbers of newborn and older juveniles in the population. Many aspects of the population biology of this and other amphisbaenians remain unknown, such as the spatial and interannual variation in life-history traits and the causes that explain variation among species. Given the special characteristics of amphisbaenians among reptiles, we encourage further studies that should help to understand the evolution of many biological and ecological traits. Finally, all this information might then be incorporated into studies of population viability and conservation status. Acknowledgments. We thank three anonymous reviewers for helpful comments. The personal and facilities of the field station of the Refugio Nacional de Caza de las Islas Chafarinas provided logistical support. Transport to and from Chafarinas Islands was provided by the Ministerio de Medio Ambiente s boat Zafarín. We thank Rosa Arribas, Javier Díaz, and Gonzalo Martínez for friendship and help in the Islands. Legal authorization and financial support for the study was provided by the Organismo Autónomo de Parques Nacionales (Spain), with additional financial support from a Ministerio de Ciencia e Innovación project (MCI-CGL / BOS). LITERATURE CITED ANDRADE, D. V., L. B. NASCIMENTO, AND A. S. ABE Habits hidden underground: A review on the reproduction of the Amphisbaenia with notes on four neotropical species. Amphibia-Reptilia 27: ANDREWS, R. 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