Clemson University TigerPrints Publications Biological Sciences 10-2009 Spatial Dynamics of Nesting Behavior: Lizards Shift icrM ohabitats to Construct Nests with Beneficial Thermal Properties Michael W. Sears Clemson University, [email protected] Michael J. Angilletta Robert M. Pringle Follow this and additional works at: https://tigerprints.clemson.edu/bio_pubs Part of the Biology Commons Recommended Citation Please use publisher's recommended citation. This Article is brought to you for free and open access by the Biological Sciences at TigerPrints. It has been accepted for inclusion in Publications by an authorized administrator of TigerPrints. For more information, please contact [email protected]. Notes Ecology, 90(10), 2009, pp. 2933–2939 Ó 2009 by the Ecological Society of America Spatial dynamics of nesting behavior: Lizards shift microhabitats to construct nests with beneficial thermal properties 1,3 1,4 2 MICHAEL J. ANGILLETTA,JR., MICHAEL W. SEARS, AND ROBERT M. PRINGLE 1Department of Biology, Indiana State University, Terre Haute, Indiana 47809 USA 2Department of Biological Sciences, Stanford University, Stanford, California 94305 USA Abstract. Because temperature affects the growth, development, and survival of embryos, oviparous mothers should discriminate carefully among available nesting sites. We combined a radiotelemetric study of animal movements with a spatial mapping of environmental temperatures to test predictions about the nesting behavior of the eastern fence lizard (Sceloporus undulatus). Females made large excursions from their typical home ranges to construct nests in exposed substrates. These excursions appeared to be related solely to nesting because all females returned to forested habitat immediately afterward. On average, ,1% (range ¼ 0–8%, n ¼ 19) of the area used by a female during nesting was contained within the area used before and after nesting. The selection of nesting sites matched predictions based on laboratory studies of embryonic performance; specifically, females nested in extremely open habitat at a mean of 6 cm depth. Spatial mapping of soil temperatures revealed that temperatures of nesting areas exceeded those of areas typically used by females, indicating that females preferred to construct warm nests that speed embryonic growth and development. However, this behavior could reduce the survivorship of females because of the need to rapidly navigate unfamiliar and exposed terrain. Key words: artificial neural network; eastern fence lizard; microhabitat; nesting; reptiles; Sceloporus undulatus; temperature; thermoregulation. When a mother lays her eggs, she possibly initiates her plexity of their environment and identify microhabitats single greatest influence on the success of her offspring that maximize the performance of offspring. (Bernardo 1996). The choice of a nesting site determines Spatially implicit studies of nesting behavior indicate the abiotic and biotic conditions experienced by that mothers can direct offspring toward desirable developing embryos. These early environmental condi- microhabitats. For instance, insects tend to lay eggs on tions affect virtually all aspects of the phenotype, plants that offer better nutrition or fewer competitors including behavior, physiology, morphology, survivor- (Thompson 1988; but see Nylin et al. 1996, Messina ship, and reproduction (see reviews by Deeming and 1998, Pappers et al. 2002). Similarly, both insects and Ferguson 1991, Packard 1991, Cagle et al. 1993, Kam et amphibians avoid laying eggs in ponds that contain al. 1996, Shine and Harlow 1996). Therefore, natural predators (Resetarits 1996, 2001). Abiotic factors, such selection should favor genotypes that discriminate as temperature and water, also influence the sites of carefully among potential nesting sites. Yet, such oviposition (Roosenburg 1996, Ward et al. 1999). discrimination requires mothers to assess environmental Although these examples suggest that females can heterogeneity on several scales. Given the environmental oviposit adaptively on a fine spatial scale, several aspects effects on embryonic development, we should wonder of previous research limit the strength of this inference. whether mothers successfully analyze the spatial com- First, most researchers have underestimated the spatial complexity of the environment by converting continuous Manuscript received 2 December 2008; accepted 8 December variables (e.g., temperature) into discrete variables (e.g., 2008; final version received 18 January 2009. Corresponding warm vs. cool patches). Second, few researchers have Editor: T. D. Williams. analyzed the selection of nesting sites in the context of 3 E-mail: [email protected] 4 Present address: Department of Biology, Bryn Mawr the relative availability of different microhabitats. College, 101 North Marion Avenue, Bryn Mawr, Pennsyl- Finally, researchers who have analyzed both selected vania 19010 USA. and available microhabitats have not done so in a 2933 2934 NOTES Ecology, Vol. 90, No. 10 spatially explicit framework. This last point seems most Ontario, Canada). Females were released at their site of critical because the costs of nesting depend on the spatial capture within one hour. We used a handheld receiver to distribution of preferred sites relative to the spatial locate each female every two to three hours. Females distributions of other resources (e.g., food, refuge). The were captured once per day between 06:00 and 09:00 to ability to test quantitative predictions about nesting in a verify reproductive status by palpation. Thus, we were spatially explicit framework should improve our under- able to specify a narrow window of time during which standing of the benefits, costs, and constraints that nesting had occurred, even if we did not observe a shape the evolution of this behavior. female during nesting. Twenty-one females were mon- We combined a radiotelemetric study of animal move- itored for a mean of 20 d (range ¼ 4–31 d); nineteen of ments with a spatial mapping of environmental temper- these females were monitored for at least one week atures to test an a priori hypothesis about the nesting before and after nesting. behavior of the eastern fence lizard (Sceloporus undu- Nesting sites were determined by a combination of latus). As with any organism, the phenotype of S. direct and indirect observations. Because we located undulatus depends strongly on the temperatures experi- females at regular intervals, we observed 15 of the 21 enced during embryonic development. Relatively high individuals in the act of either digging a nest or laying temperatures speed development without affecting the eggs. Ovipositing females (n ¼ 10) did not respond to our size of offspring at hatching (Andrews et al. 2000, presence; therefore, we approached these individuals Angilletta et al. 2000, Oufiero and Angilletta 2006), yet slowly and placed a marker next to the nesting cavity. excessive heat leads to poor survival (Sexton and Marion We excavated marked nests and measured the depth at 1974, Angilletta et al. 2000). In contrast, hydric which the eggs were deposited. For females that were conditions of the nest have a much smaller effect on the not observed during oviposition (n ¼ 11), we estimated phenotype; at a constant temperature of 288C, water the location of each nest from the position of the female potentials ranging from À530 to À150 kPa did not affect just after oviposition. Because distances between the the development, thermoregulation, locomotion, growth, locations of females before and after oviposition were or survival of offspring (Warner and Andrews 2002a). very small (range ¼ 0–3 m), estimated sites were likely to Based on laboratory experiments, Angilletta and col- have environmental characteristics similar to those of leagues (2000) concluded that lizards in New Jersey actual sites. (USA) should nest in unshaded microhabitats at least 4 During the incubation period, we measured the cm in depth. Their reasoning was simple. The high shading, temperature, and moisture of each nest. Canopy temperatures of unshaded patches would enable rapid cover was estimated using a spherical densiometer development, while 4 cm depth would prevent embryos (Model A; Forest Densiometers, Bartlesville, Oklahoma, from reaching lethally high temperatures. This prediction USA). Temperature was recorded hourly by a miniature has important implications for the spatial distribution of data logger (Thermochron iButton; Dallas Semiconduc- lizards, because unshaded patches occur rarely in forested tors, Dallas, Texas, USA); data loggers were placed in habitats and their surfaces reach lethal temperatures for nests within two weeks of oviposition and were retrieved nesting females. We show that females shift microhabi- in the middle of August, after hatchlings had emerged. tats abruptly during nesting, which maximizes the Because the data loggers were approximately the size of a probability of choosing an optimal site while minimizing lizard egg (Angilletta 1999, Angilletta and Krochmal the probability of experiencing a lethal temperature. 2003), they did not disrupt the transfer of heat between eggs and the surrounding soil. When nesting sites were METHODS estimated, data loggers were placed at the mean depth of During 2001 and 2002, we used radiotelemetry to eggs in actual nests (’6 cm). Soil moisture, estimated as monitor the movements of nesting females on a 4-ha the percentage of water, was determined from soil cores plot in Wharton State Forest (Burlington