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The Importance of Moisture in the Activity Patterns of the Arid-Dwelling Land Snail Iberus Gualtieranus

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The Importance of Moisture in the Activity Patterns of the Arid-Dwelling Land Snail Iberus Gualtieranus THE IMPORTANCE OF MOISTURE IN THE ACTIVITY PATTERNS OF THE ARID-DWELLING LAND SNAIL IBERUS GUALTIERANUS Gregorio Moreno-Rueda* Estación Experimental de Zonas Áridas (CSIC), La Cañada de San Urbano, Ctra. Sacramento s/n, 04120, Almería, Spain ABSTRACT Weather is one of the prime determinants of activity patterns in snails. Given that snails are hydrophilic and ectothermic, they may be active only when meteorological conditions provide a relatively warm and moist environment. Consequently, both temperature and moisture are among the main factors governing the activity of snails and slugs. However, the relative importance of temperature and moisture varies geographically. For example, in arid Mediterranean environments, moisture may strongly limit activity, while temperature may not. In this study, I examine the activity patterns of the land snail Iberus gualtieranus in an arid environment in SE Spain. This snail showed nocturnal activity, being rarely found during the day, and was active in autumn and winter, but not during spring and summer. Temperature was correlated with the activity of this snail, but this correlation disappeared on controlling for moisture (correlated with temperature). Thus, the effect of temperature on activity was mediated by its effect on moisture. Moisture, therefore, was the most important determinant of activity, explaining 18.4% of variance in number of active individuals. When season, daytime, temperature, and moisture were considered in a full model, moisture explained the seasonal variation in activity, but not the entire daytime variation. That is, after moisture was controlled for, a portion of variance in circadian activity remained explained only by daytime (night vs. day). These results support that, in an arid environment, moisture is the main factor determining activity, especially seasonal activity. Moreover, the snails were primarily nocturnal, regardless of moisture. These results have implications with respect to recent climate warming, which presumably will decrease wetness in the study area by raising temperatures. This in turn will narrow the seasonal activity period, extending the aestivation period, with negative consequences for snail survival. Therefore, this *E-mail: [email protected] 2 Gregorio Moreno-Rueda endangered land snail may be threatened by climate warming, and measures are necessary to avoid its extinction. INTRODUCTION Terrestrial gastropods have permeable skin and move by laying down moist mucus trails, thus suffering high rates of dehydration (Prior, 1985; Luchtel and Deyrup-Olsen, 2001). Consequently, snails and slugs have developed a number of adaptations in order to avoid or minimize the risk of dehydration. They show morphological adaptations, such as the thick white shell of Sphincterochila candidissima, which allows a fresh and wet environment inside, thereby diminishing dehydration (Moreno-Rueda, 2008). Snails also show behavioral adaptations to minimize the risk of dehydration, such as huddling in slugs, which decrease the water loss (Cook, 1981). The main behavioral adaptation is to remain in a protective microhabitat when weather is adverse (dry), and be active only when weather is favorable (wet; Cook, 2001). Consequently, moisture is one of the primary determinants of snail and slug activity patterns (review in Cook, 2001). In addition to wetness, temperature has a role in determining snail activity, a role which is complex. On the one hand, snails and slugs are ectothermic, and therefore they cannot be active when temperatures are very low. Consequently they frequently show hibernation periods in which they are inactive (e.g. Bailey, 1983). On the other hand, the risk of dehydration increases with temperature, and thus temperature may indirectly affect activity by affecting moisture. An optimal temperature for snail activity should be sufficiently high to allow activity, but not so high as to increase the risk of dehydration. In any case, temperature has also been shown to be one of the primary factors determining snail activity (review in Cook, 2001). Conditions of temperature and moisture greatly vary throughout the world (climatic variation). Consequently, the relative importance of the two parameters on snail activity should vary geographically, according to climate. For example, in relatively moist Mediterranean environments, snails such as Theba pisana and Otala lactea are inactive in their refuges only when temperatures are high, in order to avoid heat shock, but wetness does not affect activity in such zones (Moreno-Rueda et al., 2009b). In contrast, in arid Mediterranean environments, the number of snails of the species Sphincterochila candidissima and Iberus gualtieranus found in their refuges was affected mainly by moisture (Moreno-Rueda et al., 2009b). With respect to Iberus g. gualtieranus, previous studies have shown that this snail is mainly nocturnal (Moreno-Rueda, 2006a). The number of individuals found in their primary refuges (karstic crevices in the rocky substrate) is higher in summer, when moisture is the lowest and temperatures are the highest (Moreno-Rueda, 2007). In fact, wetness determines the number of specimens of this species found in their refuges, with more individuals being found sheltered when moisture is low (Moreno-Rueda et al., 2009b). By contrast, although the number of specimens found in the refuges increases with temperature, temperature has no effect on the use of refuges when controlled for moisture (Moreno-Rueda et al., 2009b). According to this information, I predicted that the activity patterns of the arid-dwelling land snail Iberus g. gualtieranus should be determined mainly by moisture, which should be the The Importance of Moisture in the Activity Patterns… 3 main restrictive factor in its environment. I tested this prediction with data of the activity of this snail in Sierra Elvira (SE Spain). THE STUDY SYSTEM Iberus gualtieranus (Linnaeus, 1758) is an endemic land snail of Spain (García San Nicolás, 1956), the subspecies I. g. gualtieranus being endemic to south-eastern Spain (Elejalde et al., 2005, 2008). This subspecies is an arid-dwelling snail characteristic of arid and karstic environments (Alonso et al., 1985). Iberus gualtieranus survives in arid environments such as Sierra Elvira thanks to the use of refuges that protect against dehydration, karstic crevices, which conserve a fresh and moist microclimate (Moreno- Rueda, 2002, 2007). In fact, this subspecies has evolved a flattened shell to enter karstic crevices for shelter (de Bartolomé, 1982; Moreno-Rueda, 2011). However, this snail must seek food in the open, obligating it to move out of these protective microhabitats in the rocky substrate (Moreno-Rueda, 2006a). During these movements, the snail is exposed to predators (such as rats, Rattus rattus, Moreno-Rueda, 2009), and the risk of dehydration, which may be high. Consequently, to survive, this snail must choose the appropriate times to be active. There are only four populations known for this subspecies, all strongly isolated (Ruiz Ruiz et al., 2006) and, consequently, it is considered endangered (Arrébola and Ruiz Ruiz, 2006; Moreno-Rueda and Pizarro, 2007; Moreno-Rueda, 2011). The study was performed in Sierra Elvira (SE Spain; 37º 14' N, 3º 47' W), a small karstic mountain with an altitudinal range of 600-1100 m a.s.l. The climate is accentuated mesomediterranean (Rivas Martínez, 1987). The annual precipitation is less than 500 mm, with five months of drought (Alonso et al., 1985), making this a harsh environment for hydrophilic animals such as gastropods. The habitat in the study zone is composed of rocky substrates with karstic erosion and low vegetal cover, formed primarily by rosemary (Rosmarinus officinalis), other shrubs (Stipa tenacissima, Genista sp.) and grasses, with scattered patches of pines and Holm oaks, and some cultivation of almond and olive trees. SAMPLING METHOD The study was conducted from October 2000 to August 2001, in a 500-m2 site on the Sierra Elvira with the typical habitat of the species (Moreno-Rueda, 2002, 2006b): rocky terrain with a southern orientation and scrubby plants. The study area was divided in plots of 9 m2. This size was chosen for the plots because the maximal distance covered by a specimen in a day is about 2 m (own data). Sampling was performed around the 15th day of the month, with 1-7 days sampling per month. Sampling spanned all hours of the day and the night, and hours were grouped in six intervals: 0-4, 4-8, 8-12, 12-16, 16-20 and 20-24 h (in solar hours, 12 h = midday). Data were grouped in seasons according to the Julian calendar (autumn, winter, spring and summer). I sampled 3-5 plots per day, and no plot was sampled more than once per month. During prospecting, I searched for individuals in bushes, under stones and inside fissures in the rock. For each plot prospected, I recorded the number of individuals found and whether they were active or inactive. An individual was considered inactive when 4 Gregorio Moreno-Rueda its soft body was withdrawn inside the shell and an epiphragm was formed closing the aperture. If the soft body was outside the shell, the animal was considered active. If the soft body was inside the shell, but the aperture was not closed by an epiphragm, the snail was considered active. Inactive snails usually have an epiphragm, while animals without an epiphragm may have simply retracted themselves inside the shell. When sampling was performed, temperature was measured 5 cm above ground using an electronic thermometer (accuracy 0.2 ºC). Soil moisture was measured after the extraction of a cylindrical soil sample (16 cm3). The wet weight (Sw) of the soil was recorded with a spring balance (accuracy 0.1 g), after which the sample was dried at 120ºC for 48 h and the dry weight (Sd) was recorded. The percentage of weight lost ([Sw – Sd] 100) was calculated and used as an index of soil moisture. Also, I recorded whether the sampling was performed during the day or the night (after sundown). The number of active individuals was used to indicate the activity level of the population.
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