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Vegetation Cover Predicts Temperature in Nests of the Hawksbill Sea Turtle: Implications for Beach Management and Offspring Sex Ratios

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Vegetation Cover Predicts Temperature in Nests of the Hawksbill Sea Turtle: Implications for Beach Management and Offspring Sex Ratios Vol. 20: 41–48, 2013 ENDANGERED SPECIES RESEARCH Published online February 22 doi: 10.3354/esr00489 Endang Species Res Vegetation cover predicts temperature in nests of the hawksbill sea turtle: implications for beach management and offspring sex ratios Stephanie Jill Kamel* Center for Population Biology, Department of Evolution and Ecology, College of Biological Sciences, University of California, 1 Shields Ave, Davis, California 95616, USA ABSTRACT: Whether a sea turtle embryo develops into a male or a female depends, as with many other reptiles, on the temperature during incubation of the eggs. With sea turtles, warm tempera- tures produce 100% females and, thus, increasing global temperatures have the potential to sig- nificantly alter offspring sex ratios. Nest-site selection provides a potential mechanism by which females might adjust the sex of their offspring, but necessitates a reliable cue which provides information about the thermal properties of a nest. Overstory vegetation cover was found to sig- nificantly predict temperatures in nests of the hawksbill sea turtle Eretmochelys imbricata. Nests placed under high vegetation cover are significantly cooler and remain within the male-producing range of temperatures throughout incubation. Interestingly, metabolic heating of the developing clutch is less pronounced under vegetation, further reinforcing the importance of this nesting habitat with respect to the production of males. This underscores the importance of preserving natural vegetation cover at hawksbill nesting beaches in order to maintain the thermal diversity of nesting sites and, potentially, mitigate the impacts of increasing global temperatures. KEY WORDS: Hawksbill · Sex ratio · Vegetation cover · Metabolic heating · Nest-site choice · Climate change Resale or republication not permitted without written consent of the publisher INTRODUCTION increase by at least 0.1°C per decade: within the Caribbean basin, temperatures are expected to In egg-laying species, the nest environment influ- increase by between 1 and 6°C, depending upon ences a wide range of offspring traits, such as size specific emissions scenarios (IPCC 2001, Brohan et (Brown & Shine 2004), performance (Shine & Harlow al. 2006). Increasing temperatures present a chal- 1996, Shine et al. 1997, Gillespie & Wratten 2011), lenge for these species, and a primary conservation and, in species with temperature-dependent sex issue is to understand whether, in response to higher determination, gender (Mrosovsky & Provancha ambient temperatures, individuals will be able to 1992, Roosenburg 1996). For sea turtles, phenotypic adjust the sex ratio of their offspring (Hawkes et al. sex is determined by the temperature during the 2007). middle third of incubation, with warmer tempera- The potential for females to adjust offspring sex tures leading to the development of female offspring ratios becomes all the more critical in species threat- within a thermal tolerance range of 25 to 35°C ened with extinction. Hawksbill sea turtles Eret - (Yntema & Mrosovsky 1982, Ackerman 1997). Aver- mochelys imbricata are listed as Critically Endan- age global surface temperatures are predicted to gered by the IUCN and, globally, populations have *Email: [email protected] © Inter-Research 2013 · www.int-res.com 42 Endang Species Res 20: 41–48, 2013 declined by >80% from historical levels (Meylan & the thermosensitive period of sexual differentiation Donnelly 1999, Mortimer & Donnelly 2008). Over the (TSP) to be about 1°C (Zbinden et al. 2006). There- past decades, hawksbills have been the focus of con- fore, if sand temperatures are below or near piv- servation efforts, most of which have been aimed at otal, metabolic heating may cause feminization of reducing the take of turtles and their eggs. However, clutches thought to be laid in ‘male-producing areas’ the alteration of primary sex ratios as a result of cli- and thus invalidate vegetation cover as a useful cue. mate change could also have serious consequences This paper investigates whether individual nests for population stability. The data on sex ratios appear vary significantly in their thermal properties and to bear this out: in both Antigua and Brazil, hawksbill documents the link between overstory vegetation hatchling sex ratios are highly female biased (God- cover and temperature to assess its utility as a poten- frey et al. 1999, Glen & Mrosovsky 2004). In fact, tial cue for females and as a means of predicting nest Glen & Mrosovsky (2004) show that fewer males sex ratios. Metabolic heating during incubation was were produced in Pasture Bay, Antigua in 2003 as also measured to determine if it obscures any rela- compared to 1989, possibly in response to increasing tionship between vegetation cover and temperature. ambient temperatures. Finally, the effect of metabolic heating and vegeta- Hawksbills are unique among sea turtles as they tion cover on nest hatching success was examined. tend to nest in or near vegetation (Diamond 1976, Horrocks & Scott 1991, Kamel & Mrosovsky 2005, Ditmer & Stapleton 2012). In fact, many hawksbill MATERIALS AND METHODS populations tend to nest in heterogeneous environ- ments, with nesting beaches comprised of a combi- Study site nation of open, sandy areas and more heavily vege- tated patches (Kamel & Mrosovsky 2005). These Guadeloupe, French West Indies, hosts one of beach microhabitats vary widely in their thermal the largest hawksbill nesting populations in the profiles (Kamel & Mrosovsky 2006a) and provide Caribbean (Kamel & Delcroix 2009). Trois Ilets beach ample opportunity for females to select among differ- is located on the western coast of Marie-Galante, a ent nest temperatures. Previous research has identi- small island 40 km southeast of the main island of fied individual variation in female nesting prefer- Guadeloupe. The beach runs in a north−south direc- ences, with some females preferring forested areas, tion and comprises 2.0 km of usable nesting habitat. while others show a preference for open sand (Kamel Beach width varies between 1 and 9 m and is backed & Mrosovsky 2005, 2006b). Substantial variability by a coastal littoral forest. The beach can thus be has also been found in sand temperatures across divided into 4 different zones: forest (completely sur- beach microhabitats, with sand temperatures in the rounded by trees), forest border (near the forest but forest being significantly cooler than in less shaded not completely surrounded), low-lying vegetation areas (Kamel & Mrosovsky 2006a). These sand tem- (presence of grass or beach creepers) and open sand perature data provide suggestive evidence that veg- (largely free of overstory vegetation, save the occa- etation cover can reliably predict sex ratios, since sional overhanging branch). Each beach zone also sand temperatures in the forest are frequently in the corresponds to a particular amount of overstory veg- male-producing range (i.e. below the pivotal temper- etation cover: open sand (0 to 10%), low-lying vege- ature, the temperature producing equal sex ratios tation (11 to 40%), forest border (41 to 70%) and for- when eggs are incubated under constant conditions; est (71 to 100%). Tidal variations along the beach are Mrosovsky & Pieau 1991). However, it is unknown negligible (<0.3 m), except during storms, which typ- how tightly vegetation cover is linked to individual ically occur between August and October. The main nest temperatures and thus how consistently it can nesting season occurs between May and October, be used by females as a predictive cue. with a peak in July. Quantifying the relationship between vegetation cover and nest temperature is particularly important since sea turtles lay large clutches of 100 to 200 eggs, Nest measurements and the subsequent warming of nests during devel- opment (so-called metabolic heating; Broderick et al. Hobo Water Temp Pro data loggers (Onset Com- 2001, Zbinden et al. 2006) might eliminate any corre- puter) were placed in a total of 24 nests and 24 con- lation between sand and nest temperatures. In fact, trol sites. Twelve pairs of data loggers were placed some studies have shown metabolic heating during between 9 and 30 June during the 2002 nesting sea- Kamel: Vegetation cover predicts nest temperatures 43 son, and 12 more, between 7 and 27 June during the emergence, the TSP was also calculated assuming a 2004 nesting season. To do so, nests were excavated development time 4 d shorter than the incubation no later than 8 h after egg deposition, with the eggs’ duration (see Godfrey & Mrosovsky 1997 for details original orientations maintained to minimize poten- on determining this interval). Given that the 2 esti- tial disturbance of the developing embryos. The mates did not differ significantly, results using the number of eggs in a clutch was counted, and then middle third of incubation are given. Metabolic heat- half the eggs were returned to the nest, a data logger ing was calculated as the difference between nest was placed in the centre of the clutch, its depth in temperature and sand temperature at the control site. relation to the sand surface was measured and the As the effect of metabolic heating on sexual differen- remaining eggs were returned. A second data logger tiation was a main issue under study, comparisons of was placed at the same depth at a control site 1 m metabolic heating were restricted to the TSP. Regres- away and under the same amount of vegetation sion analyses were conducted to assess the influence cover. The amount of vegetation cover directly above of temperature and vegetation cover on hatching the nest was measured with a densiometer, which is success. Day of the year of oviposition and year were commonly used to assess canopy density (see Kamel included as variables in the analyses. Given that a & Mrosovsky 2005). pivotal temperature has not been estimated for Nests were monitored nightly, and, once hatch- hawksbills in Guadeloupe, a pivotal temperature of lings had emerged, the number of hatched eggs (only 29.2°C was assumed, calculated from hawksbill eggshell remained) and the number of unhatched clutches collected in Antigua (Mrosovsky et al.
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