Intraspecific differentiation of social behavior and shelter selection in Mesobuthus gibbosus (Brullé, 1832) (Scorpiones: Buthidae)

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1 J Ethol (2009) 27: DOI /s ARTICLE Intraspecific differentiation of social behavior and shelter selection in Mesobuthus gibbosus (Brullé, 1832) (Scorpiones: Buthidae) Dimitris Kaltsas Æ Iasmi Stathi Æ Moysis Mylonas Received: 21 July 2008 / Accepted: 15 December 2008 / Published online: 3 February 2009 Ó Japan Ethological Society and Springer 2009 Abstract We compared seasonal shelter selection and social behavior of Mesobuthus gibbosus from autumn to mid-summer in two similar phryganic ecosystems, in continental Greece (near Volos city) and in insular Greece (eastern Crete), and in the laboratory under simulated abiotic conditions. Our results showed that shelter selection is a critical indicator of the seasonal social behavior of the species. The abrupt climatic changes in spring caused a differentiation in shelter selection between the cold (November February) and the warm (March June) at both sites. Sociality was exhibited only during winter in the field and was more extensive under cold conditions in the laboratory. Co-occurrence of scorpions proved to be age-specific, facilitated by population density and by harsh abiotic conditions during winter, and negatively influenced by intraspecific competition, which was higher in continental Greece. The response of scorpions to changes of abiotic factors reveals synchronization of seasonal shelter selection with climatic changes. Keywords Scorpion Cohabitation Sociality Intraspecific competition Parasocial route Greece D. Kaltsas I. Stathi M. Mylonas Department of Biology, University of Crete, Vassilika Vouton, P.O. Box 2208, Irakleio, Crete, Greece D. Kaltsas (&) I. Stathi M. Mylonas Natural History Museum of Crete, University of Crete, Knossos Av., P.O. Box 2208, Irakleio, Crete, Greece dimitris@nhmc.uoc.gr Introduction The general seasonal phenology of most scorpion species is described by a simple pattern (Maury 1973). Populations are active during warmer months and inactive during colder months (e.g. Zinner and Amitai 1969; Polis and McCormick 1986). Only in deserts does activity decrease during s of extreme summer heat (Polis and McCormick 1986). The spatial distribution of scorpions is influenced by many factors including temperature, precipitation, soil or rock characteristics, and environmental physiognomy (Polis 1990). Substantial selective forces favor the evolution of homing behavior (Polis et al. 1986) and scorpions, which are burrowing species, live the great majority of their existence under stones, inside burrows (Polis 1990). Scorpion species have been reported expanding or contracting their habitats as a function of season (Zinner and Amitai 1969) or age (Polis et al. 1986). In some species, especially buthids (Polis 1990), individuals have been observed aggregating under stones during winter (Stahnke 1966; Zinner and Amitai 1969; Eastwood 1978). Sociality among scorpions was first reviewed by Wilson (1975) and later by Polis and Lourenço (1986) and by Polis (1990). Two evolutionary routes are distinguished: the familial route (aggregation of relatives), which includes the subsocial stage (newborn scorpions staying with their mothers just until their first molt) and the communal/ parasocial route (aggregation of nonrelatives). Although sociality of scorpions has been studied on the species level (McAlister 1966; Stahnke 1966; Mahsberg 1990; Warburg 2000), the mechanisms which determine seasonal shelter selection and favor coexistence of scorpions have not been thoroughly studied. The objective of our study was to explore qualitatively and quantitatively these patterns comparatively in a continental and an insular

2 468 J Ethol (2009) 27: population of Mesobuthus gibbosus, a species widely distributed in both continental and insular Greece (Kaltsas et al. 2006). Materials and methods The species M. gibbosus (Brullé, 1832) is the only buthid in the Balkan Peninsula and is distributed throughout its southern part (Albania, Bulgaria, former Yugoslav Republic of Macedonia, Greece, Montenegro), and in Turkey. It is xerophilic and thermophilic (Crucitti and Marini 1987) mainly opportunistic, errant, non-cannibalistic, and a dominant species in the Aegean region (Kaltsas et al. 2008). Field studies The study was conducted in two similar arid phryganic (Mediterranean shrubs) ecosystems, one in insular south Greece (Toplou, eastern Crete) and the other in continental central Greece (Alykes, near Volos city) (Table 1). At both sites no other scorpion species is present. The average density of the population in Volos during the study was 1.24 ± 0.33 times higher than that in Crete (Kaltsas et al. 2006). Observations were conducted monthly from October 2001 to June 2002 in Crete and from October 2003 to June 2004 in Volos, by searching for scorpions under stones, the main habitat of M. gibbosus (Kaltsas et al. 2006), during daytime. Specifically, we applied quadrat sampling (20 m 9 20 m), in order to cover the whole area of both sites. The interval July September (main of reproduction of M. gibbosus) was excluded, to rule out co-occurrence records of mating scorpions. The surface of stones in the two sites was measured by multiplying their maximum length by their width (assuming the stones to be Table 1 The main characteristics of the two study sites rectangular). When a scorpion was captured, the body length was measured (mesosoma? metasoma). Sex and age-class identification were as suggested by Kaltsas et al. (2008). During all sampling we measured air temperature and air relative humidity at the ground surface, using a Kestrel 3,000 portable weather meter. Laboratory studies For our experimental studies we collected 24 healthy and unharmed scorpions from each site (eight males, eight nongravid females, eight juveniles) and marked them with enamel paint on a specific segment of the mesosoma or/and the metasoma, in order to distinguish all individuals by their unique mark. The 24 scorpions of each population were kept in a transparent plastic container ( m) with soil as substrate (depth 15 cm) and eight stones collected from the respective site. The stones in each container were placed from one side of the container to the other, in accordance with their size (stones I IV; Fig. 1). The surfaces of the stones in the two containers were equal. The photo, air temperature, and relative humidity in the laboratory were set to their respective means during the cold and warm s of the year in the field (Table 2). Each phase of the experiment lasted 30 consecutive days and observations were made daily, at the same time every day, when the lights were on, as done in the field studies (during daytime). Observations were made once each day, to avoid false recordings because of stress, because in several cases when a stone was turned some scorpions ran off when exposed to light. Data analyses On several occasions we compared two samples in order to test whether they were statistically different. This was carried out by using either a Mann Whitney test for analyzing non-parametric data or a t test for parametric data. Conformity of data to the normality criterion was evaluated with the Shapiro Wilk test and the Kolmogorov Smirnoff Study site characteristics Toplou (Crete) Alykes (Volos) Coordinates N, E N, E Area 27,000 m 2 25,500 m 2 Elevation 200 m 130 m (approx.) Substrate Limestone Limestone Dominant plant species Annual precipitation Thymus capitatus, Phlomis lanata 350 mm (55.3% during winter) Thymus capitatus, Phlomis fruticosa 500 mm (36.4% during winter) The rainfall data were taken from the website Fig. 1 Ground plan of the two plastic containers in the laboratory with stones of different size (I IV)

3 J Ethol (2009) 27: Table 2 The abiotic conditions under which the scorpions of the two populations were studied in the laboratory test. We applied general linear models (GLM) to examine if shelter selection of scorpions (surface area of stones) at the two sites (in the field) differed per age-class or/and of sampling. We set stone surface as the dependent variable, age-class of scorpions and sampling as categorical predictors, and body length of scorpions as the continuous predictor. We also used GLM to analyze the results of our experimental studies. The differentiation was that all measurements (60 in total) for each individual were averaged prior to the analysis, and thus the sampling was not included. The multiple measurements for every individual were averaged in order to avoid pseudoreplication (Cooper and Ginnett 1998; Kuhar 2006) and, ultimately, to avoid type I errors (Hulbert 1984). To examine whether cohabitation of scorpions in the laboratory differed in relation to stone surface per/within of sampling and per/within population, we used repeated measures MANOVA. Repeated measures statistics is a design which serves as a tool against pseudoreplication (Machlis et al. 1985; Kuhar 2006). We set the 30 daily measurements of cohabitant scorpions under each stone during each phase of the experiments (cold/warm ) as the dependent variables. The categorical predictors were stone size (types I IV) and either population (Crete/Volos) or (cold/warm). Results In the field Volos Cold Warm Crete Cold Warm Air temperature ( C) Air relative humidity (%) Photo 10 h 13 h 30 min 10 h 13 h 30 min We compared the number of stones measured in 60 quadrats within each site and found that the availability of stones at the two sites did not differ statistically (Mann Whitney test: n = 120, P = 0.237). Hence, we were able to compare shelter selection between the populations of the two study sites. The number of scorpions captured per month is shown in Table 3. The main difference between the two sampling sites was that the number of monthly captures in Crete was approximately stable (except for a slight decrease in December) whereas in Volos there was an abrupt decrease Table 3 The number of observations at both sites Total Male Female Immature Crete Volos Crete Volos Crete Volos Crete Volos October November December January February March April May June Total Fig. 2 A rare case of cohabitation of a male (above) and a female (below) inside a burrow in Alykes (continental Greece) of captures during winter, a during which no males were observed. When searching for scorpions under a stone, they would be found at the edge of their burrows, outside burrows, or clinging to the underside of the stone. Generally, the burrows had a narrow entrance and were not deep (approximately 5 cm). During the cold, mature scorpions seemed to exhibit low levels of metabolism; they were inactive, with their legs and pedipalps huddled towards their body, and most of them were hidden inside burrows (Crete: 81.7%; Volos: 85.2%). In contrast with this, juveniles were always alert (more kinetic than mature scorpions with their metasoma lifted), most often observed outside burrows (Crete: 50.9%; Volos: 56.1%). Males began to be increasingly active from March to summer. Cohabitation of scorpions was observed more often in Crete than in Volos (Fig. 2; Table 4). No more than two scorpions were co-occurrent

4 470 J Ethol (2009) 27: Table 4 Cohabitant scorpions observed during the field studies No. of co-occurrent scorpions Frequency of co-occurrence (%) Crete Volos Crete Volos October November December January February March April May June Total Table 5 t Test results from comparison of shelter selection of mature and immature scorpions during the cold and warm s of the year at each study site and between the two sites during each Crete (cold/warm ) Volos (cold/warm ) Cold (Crete/Volos) Warm (Crete/Volos) Mature Immature n t P n t P \ \ \ \ in Volos whereas in Crete cohabitation of three, four, or five scorpions was observed three times, once, and twice respectively, throughout the winter. Generally, co-occurrent scorpions were either all mature or all immature. There was only one observation of mature immature coexistence (during January, in Volos). Air temperature (t test: n = 27, t =-0.841, P = 0.413) and air relative humidity (t test: n = 27, t = 0.8, P = 0.436) at the two sites were not statistically different. Both measured abiotic factors changed abruptly after the cold of the year (November February) at both study sites. Compared with the cold, air relative humidity was significantly lower (Crete: n = 27, t = , P = 0.001; Volos: n = 27, t = 8.466, P = 0.003) and air temperature was significantly higher (Crete: n = 2, t = , P = 0.006; Volos: n = 27, t =-3.239, P = 0.047) during the warm (March June). The surface of stones under which scorpions hid decreased significantly from cold to warm at both sites (Table 5). In Volos, scorpions in general were found under larger stones than in Crete and there was significant statistical difference in Table 6 The average number of scorpions observed under stones (types I IV; Fig. 1), the number of co-occurrent individuals under stones (in parentheses), and the average number of individuals observed in the corners of the two plastic containers Av. no. of scorpions under stones shelter selection per age-class between the two populations, except for immature scorpions during the cold (Table 5). General linear models showed that shelter selection of scorpions differed significantly among age-classes (Crete: n = 290, F = , P \ ; Volos: n = 269, F = 43.02, P \ ) and of sampling (Crete: F = 19.09, P = ; Volos: F = , P \ ), and was primarily influenced by the body length of scorpions at both sites (Crete: F = , P \ ; Volos: F = , P \ ). Generally, small stones were occupied by small scorpions (mainly juveniles) during the cold of the year (November February) and by juveniles and small mature individuals during the warm (March June). Experimental studies Av. no. of scorpions in corners Crete Volos Crete Volos Cold I (2) II 0.95 (2 3) 1.2 (2) III 2.5 (2 4) 2.6 (2 4) IV 7.8 (4 13) 7 (4 11) Warm I 1.4 (2) 1.3 (2) II 2.25 (2 4) 2.25 (2 3) III 2.45 (2 4) 2.75 (2 4) IV 3.3 (2 5) 3.5 (2 4) Under cold conditions scorpions from both populations tended to aggregate under the largest stones (IV: Fig. 1; Table 6). Under warmer conditions, shelter selection was less strict and more scorpions were observed staying in the corners of the containers. The highest numbers of cohabitant scorpions were observed under type IV stones in both containers. Generally, when there were [5 cohabitant scorpions (only mature), they formed a circle with their prosoma facing the center. No more than four scorpions (from both sites) were observed together under stones of smaller surface area (types I III). Juveniles were most often observed under small stones (I, II) and were more alert than mature scorpions. Most of the co-occurrent scorpions were exclusively mature or immature. The observations of mature immature coexistence

5 J Ethol (2009) 27: Table 7 Repeated measures MANOVA results (n = 16 in all analyses) Wilks value F Effect df Error df P Cold Intercept Population Stone surface Population 9 S. surface Warm Intercept , \ Population Stone surface Population 9 S. surface Crete Intercept Period Stone surface Period 9 S. surface Volos Intercept Period Stone surface Period 9 S. surface comprised only 12.12% (Crete) and 9.79% (Volos) of the total. General linear models showed that shelter selection of scorpions from both sites differed significantly among ageclasses (Crete: n = 24, F = 29.87, P \ ; Volos: n = 24, F = 4.78, P = 0.04) and body length of scorpions (Crete: F = 51.68, P \ ; Volos: F = 13.89, P = 0.001). Social behavior (cohabitance of scorpions) during the simulated cold and warm s differed statistically in terms of stone size (types I IV) and did not differ between the two populations (Table 7). The social behavior of both populations (co-occurrence under stones) differed in relation to (cold/warm) and stone surface (Table 7). Discussion The social behavior of scorpions has been studied at the level of foraging activity and brood care (Polis and McCormick 1987; Mahsberg 1990), whereas few studies focus on cohabitation in the same shelter (Warburg 2000). Unlike other scorpion species, such as Scorpio maurus (Shachak and Brand 1983), Compsobuthus werneri (Warburg 2000), Centruroides exilicauda (Stahnke 1966), and Pandinus imperator (Mahsberg 2001), M. gibbosus proved to be a species which exhibits relatively low levels of sociality, even compared with its congener M. martensii (Polis 1990). The characteristics of a narrow entrance and shallow burrows are the opposite of those (complex structure, wider, deeper) of burrows built by scorpion species with high levels of sociality (Mahsberg 2001). This differentiation is also common in other arthropods, for example spiders, isopods, and insects, and some mammals (Linsenmair 1984; Hölldobler and Wilson 1990; Sherman et al. 1991; Avilés 1997), species of which exhibit different levels of sociality. Co-occurrence of scorpions was observed only during winter in the field (Table 4) and was much more common during the simulated cold in the laboratory (Table 6), a fact which indicates that sociality was a response to the inhospitable environmental conditions. To maintain comfortable conditions under stones, individuals oriented with the head toward a central point, possibly a unique behavior of the genus Mesobuthus. The seasonal activity of scorpions and their active metabolic rate, as ectotherms, is largely a function of environmental temperature and relative humidity (Brownell 2001). When the warm began at both sites in March, the densities of both populations approximately doubled (Kaltsas et al. 2006), and scorpions occupied smaller stones. Hence, the major influence of (cold/warm) on shelter selection reflects the effect of harsher abiotic factors during winter on the seasonal social behavior of the species. Mature and immature scorpions were rarely cohabitant. Co-occurrence of unrelated individuals corresponds to the communal stage of sociality along the parasocial evolutionary route (Wilson 1975). The age-specific limitation of

6 472 J Ethol (2009) 27: sociality was probably a result of intraspecific competition and different specialization of prey selection based on size (Polis and McCormick 1987; Warburg 2000), which is a fact in M. gibbosus populations (Kaltsas et al. 2008): generally, small predators (scorpions) attack small prey, because of limited food requirements and avoidance of foraging failure (correlation of predator prey body lengths, Pearson s r = 0.8). The possibility of cannibalism avoidance should be ruled out, because M. gibbosus is generally a non-cannibalistic species (Kaltsas et al. 2008). During all experiments, small scorpions (juveniles) were generally found under small stones and were more alert than mature individuals during the cool, as is the case in other scorpion species (Polis 1980), although they were less abundant than males and females at both sites (Table 3). The selection of smaller shelters by juveniles, most of which were observed outside burrows, was probably because of the abiotic conditions underneath them, especially during the cold. Specifically, it has been shown that juveniles of M. gibbosus prefer lower temperatures compared with adults (Kaltsas et al. 2008). Such generalized age-specific behavioral differences are of the same extent as those between different scorpion species and probably evolved in response to similar selective forces (Polis 1984). Shelter selection proved to be a key-factor in revealing the social behavior of M. gibbosus. Scorpions in Volos were found under larger stones compared with the population in Crete (Table 5) and were comparatively less co-occurrent during the field studies (Tables 4 and 6). The low levels of sociality exhibited by the scorpions in Volos were probably a result of the comparatively higher interspecific and intraspecific competition there (Kaltsas et al. 2006). Therefore, considering the higher population density in Crete, it is likely that density compensation (MacArthur et al. 1972) in the island population (Kaltsas et al. 2006) favoured sociality. On the other hand, in the laboratory, where densities and competition were equal, there was no difference in social behavior and shelter selection between the two populations (Table 7). These results imply the significance of density in facilitating cohabitance, as reported for other scorpion species also (Warburg 2000), and the negative influence of intraspecific competition in the social behavior of scorpions. Our results indicate that seasonal shelter selection and social behavior of M. gibbosus are regulated by climatic factors and differ in relation to intraspecific competition. Climatic cues operate as signals of fluctuation in prey abundance for many scorpion species (Zinner and Amitai 1969; Polis 1980; Warburg and Polis 1990). 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