Ricky-John Spencer

EXPERIMENTALLY TESTING NEST SITE SELECTION: FITNESS TRADE-OFFS AND PREDATION RISK IN TURTLES

The nesting habitat of most freshwater turtle species has been described, but factors influencing maternal nest site selection have rarely been tested experimentally. Offspring fitness is assumed to be the major factor influencing nest site selection because habitat characteristics and nest microenvironments affect offspring survival. However, two opposing factors drive maternal nest site selection: minimizing female mortality and maximizing offspring fitness. In Australia, introduced red foxes are the major predator of turtle nests, and they also destroy nesting females. Thus, females may trade off maximizing nest survival or offspring fitness to avoid predators. In this paper, I show that the risk of predation affects maternal nest site selection and has negative effects on reproductive success in a freshwater turtle. I also show that the mechanisms behind predator detection vary between native and introduced species. From 1996 to 2000, I observed female freshwater turtles, Emydura macquarii, nesting around four lagoons in southeastern Australia to determine nesting habitat characteristics. During 1997 and 1998, foxes were removed from two sites, and nest predation rates declined by >50%, but remained >85% in nonremoval sites. Foxes destroyed ∼3% of the female population only in high-risk areas. Female turtles nest away from shore to maximize offspring fitness when foxes are removed from an area. The dilemma in high-risk areas is that predation risk limits females from nesting in preferred areas away from shore, where nest predation is reduced. However, females may sacrifice some offspring by nesting in inappropriate substrate, where incubation conditions are not optimal, but nest predation is significantly reduced. Nesting turtles do not detect foxes by chemical recognition, but they have an innate avoidance response to the odor of a native predator. Nesting habitat affects offspring fitness, but factors affecting female survival may ultimately drive maternal nest site selection in turtles.

Climate and predation dominate juvenile and adult recruitment in a turtle with temperature-dependent sex determination.

Conditions experienced early in life can influence phenotypes in ecologically important ways, as exemplified by organisms with environmental sex determination. For organisms with temperature-dependent sex determination (TSD), variation in nest temperatures induces phenotypic variation that could impact population growth rates. In environments that vary over space and time, how does this variation influence key demographic parameters (cohort sex ratio and hatchling recruitment) in early life stages of populations exhibiting TSD? We leverage a 17-year data set on a population of painted turtles, Chrysemys picta, to investigate how spatial variation in nest vegetation cover and temporal variation in climate influence early life-history demography. We found that spatial variation in nest cover strongly influenced nest temperature and sex ratio, but was not correlated with clutch size, nest predation, total nest failure, or hatching success. Temporal variation in climate influenced percentage of total nest failure and cohort sex ratio, but not depredation rate, mean clutch size, or mean hatching success. Total hatchling recruitment in a year was influenced primarily by temporal variation in climate-independent factors, number of nests constructed, and depredation rate. Recruitment of female hatchlings was determined by stochastic variation in nest depredation and annual climate and also by the total nest production. Overall population demography depends more strongly on annual variation in climate and predation than it does on the intricacies of nest-specific biology. Finally, we demonstrate that recruitment of female hatchlings translates into recruitment of breeding females into the population, thus linking climate (and other) effects on early life stages to adult demographics.

The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii

We described the diet of Emydura macquarii, an omnivorous turtle from south-eastern Australia, compared its digestive performance on diets of fish or plants at two temperatures, and related how both diet and temperature affect its food selection in nature. Filamentous algae constituted 61% of the stomach content of E. macquarii. The turtles rarely fed on motile prey, but selected carrion from the lagoon bottom and terrestrial insects (Diptera, Hymenoptera and Coleoptera) trapped on the surface of the water. Digestive efficiency of E. macquarii was affected little by body temperature, in contrast to consumption rates and rates of passage which were strongly influenced by both temperature and diet. In combination, these responses resulted in a slower rate of digestion at 20 degrees C than at 30 degrees C. Digestive efficiency of E. macquarii on a herbivorous diet at 30 degrees C (49%) was about half that of turtles on a carnivorous diet (91%), but they had longer transit times (118 h on the plant diet versus 70 h). Lower consumption rates and longer mean retention times in turtles fed plants compared those fed fish relate to slower digestive processing of the plant. Rapid processing and higher consumption rates of fish by E. macquarii resulted in higher energy gains compared to turtles consuming plants (almost 100 times more energy at 30 degrees C). The laboratory results suggest that fish carrion and aquatic and terrestrial invertebrates are probably essential dietary items of E. macquarii in the wild, because its metabolic requirements cannot be met from aquatic macrophytes alone.

Growth patterns of two widely distributed freshwater turtles and a comparison of common methods used to estimate age

Turtles are long lived and demographic models requiring estimates of age, growth, fecundity and survival are central for management. Most studies that estimate age and growth of freshwater turtles use annuli as an index of age without estimating its error and very few studies that use growth models include many juveniles, where growth is often large and variable. In this paper, I compare the reliability of growth annuli and common models in determining age and growth of two widely distributed turtles in Australia. Most turtles are carnivorous during the juvenile stage but many species shift to a lower-quality omnivorous diet prior to maturing. Patterns of growth are often characterised by this dietary shift and I compared the growth of a common omnivorous turtle (Emydura macquarii) and a vulnerable sympatric species that is an obligate carnivore (Chelodina expansa). Mark-recapture programs were established in three lagoons on the Murray River. In total, 1218 hatchling E. macquarii were released into two of the lagoons and growth annuli were found to be unreliable in estimating their age by Year 2. The von Bertalanffy and logistic growth models can reliably estimate age of both male and female E. macquarii and C. expansa respectively. Growth is extremely rapid during the juvenile stage of E. macquarii, but is highly variable in C. expansa, with rapid growth occurring only beyond three years of age. Hence growth models fail to predict age when juveniles are excluded from the analyses. Female E. macquarii delay maturity until 9-12 years of age because clutch size is positively related to body size and they can produce only one large clutch per year. Female C. expansa mature later (at ∼14 years) than female E. macquarii and both species are sexually dimorphic, as males mature earlier at smaller sizes than females. Common growth models describe the growth of two widely distributed freshwater turtles, but different patterns of growth and age at maturity relate to quality of diet and reproduction.

Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings

Incubation temperature affects developmental rates and defines many phenotypes and fitness characteristics of reptilian embryos. In turtles, eggs are deposited in layers within the nest, such that thermal gradients create independent developmental conditions for each egg. Despite differences in developmental rate, several studies have revealed unexpected synchronicity in hatching, however, the mechanisms through which synchrony are achieved may be different between species. Here, we examine the phenomenon of synchronous hatching in turtles by assessing proximate mechanisms in an Australian freshwater turtle (Emydura macquarii). We tested whether embryos hatch prematurely or developmentally compensate in response to more advanced embryos in a clutch. We established developmental asynchrony within a clutch of turtle eggs and assessed both metabolic and heart rates throughout incubation in constant and fluctuating temperatures. Turtles appeared to hatch at similar developmental stages, with less-developed embryos in experimental groups responding to the presence of more developed eggs in a clutch by increasing both metabolic and heart rates. Early hatching did not appear to reduce neuromuscular ability at hatching. These results support developmental adjustment mechanisms of the ‘catch-up hypothesis’ for synchronous hatching in E. macquarii and implies some level of embryo–embryo communication. The group environment of a nest strongly supports the development of adaptive communication mechanisms between siblings and the evolution of environmentally cued hatching.

COUNTERINTUITIVE DENSITY-DEPENDENT GROWTH IN A LONG-LIVED VERTEBRATE AFTER REMOVAL OF NEST PREDATORS

Examining the phenotypic and genetic underpinnings of life-history variation in long-lived organisms is central to the study of life-history evolution. Juvenile growth and survival are often density dependent in reptiles, and theory predicts the evolution of slow growth in response to low resources (resource-limiting hypothesis), such as under densely populated conditions. However, rapid growth is predicted when exceeding some critical body size reduces the risk of mortality (mortality hypothesis). Here we present results of paired, large-scale, five-year field experiments to identify causes of variation in individual growth and survival rates of an Australian turtle (Emydura macquarii) prior to maturity. To distinguish between these competing hypotheses, we reduced nest predators in two populations and retained a control population to create variation in juvenile density by altering recruitment levels. We also conducted a complementary split-clutch field-transplant experiment to explore the impact of incubation temperature (25 degrees or 30 degrees C), nest predator level (low or high), and clutch size on juvenile growth and survival. Juveniles in high-recruitment (predator removal) populations were not resource limited, growing more rapidly than young turtles in the control populations. Our experiments also revealed a remarkably long-term impact of the thermal conditions experienced during embryonic development on growth of turtles prior to maturity. Moreover, this thermal effect was manifested in turtles approaching maturity, rather than in turtles closer to hatching, and was dependent on population density in the post-hatching rearing environment. This apparent phenotypic plasticity in growth complements our observation of a strong, positive genetic correlation between individual body size in the experimental and control populations over the first five years of life (rG - +0.77). Thus, these Australian pleurodiran turtles have the impressive capacity to acclimate plastically to major demographic perturbations and enjoy the longer-term potential to evolve adaptively to maintain viability.

A comparative study of environmental factors that affect nesting in Australian and North American freshwater turtles

The timing of reproductive events is critical for fitness, and these events are often linked to weather and climate. Weather components are thought to influence the nesting behaviour of freshwater turtles, but to date there have been few quantitative studies and no comparative studies. We compared the environmental cues used by nesting Australian (Emydura macquarii andChelodina expansa) and North American (Chrysemys picta) freshwater turtles, and quantified the differences in weather between days with and without nesting activity within the nesting season. We also characterized the diel time of nesting for each species. The results suggest that nesting behaviour is related to warm air and water temperatures in C. picta and to rainfall in E. macquarii and C. expansa. Chrysemys picta primarily nests in the afternoon and evening, E. macquarii is a crepuscular nester, and C. expansa nests diurnally. While changes in life history resulting from climate change are difficult to predict, we suggest that an increase in the number of El Ni˜ no events may have adverse effects on the two Australian species, whereas increases in environmental temperature may expand the number of nesting opportunities for C. picta.

Hatching Behavior in Turtles

Incubation temperature plays a prominent role in shaping the phenotypes and fitness of embryos, including affecting developmental rates. In many taxa, including turtles, eggs are deposited in layers such that thermal gradients alter developmental rates within a nest. Despite this thermal effect, a nascent body of experimental work on environmentally cued hatching in turtles has revealed unexpected synchronicity in hatching behavior. This review discusses environmental cues for hatching, physiological mechanisms behind synchronous hatching, proximate and ultimate causes for this behavior, and future directions for research. Four freshwater turtle species have been investigated experimentally, with hatching in each species elicited by different environmental cues and responding via various physiological mechanisms. Hatching of groups of eggs in turtles apparently involves some level of embryo-embryo communication and thus is not a purely passive activity. Although turtles are not icons of complex social behavior, life-history theory predicts that the group environment of the nest can drive the evolution of environmentally cued hatching.

Diet analysis of mammals, raptors and reptiles in a complex predator assemblage in the Blue Mountains, eastern Australia

South-east Australia has a complex predator assemblage which has historically been vulnerable to introduced species. This is the first Australian field study to analyse samples from members of the families Canidae, Dasyuridae, Strigidae, and Varanidae to describe the diet and diet overlap between these predators. Samples were collected opportunistically and hair and bone analysis was used to identify the content of samples. Wild dogs (Canis lupus) and lace monitors (Varanus varius) predominantly consumed large mammalian prey, which contributed to the high level of diet overlap (Ojk = 0.79) between these two species. Foxes (Vulpes vulpes) and spotted-tailed quolls (Dasyurus maculatus) also had a high level of diet overlap (Ojk = 0.76), a result of their diets containing a high proportion of medium-sized mammals. The diet of wild dogs and foxes showed moderate overlap (Ojk = 0.59), and foxes were more likely to prey on species within the critical weight range than on macropods, which made up a high proportion of the diet of wild dogs. These data confirm that significant diet overlap can occur between predators from different taxonomic classes and further investigation of potential competition will be important to ongoing management.

Clustering of related individuals in a population of the Australian lizard, Egernia frerei.

Stable social aggregations are rarely recorded in lizards, but have now been reported from several species in the Australian scincid genus Egernia. Most of those examples come from species using rock crevice refuges that are relatively easy to observe. But for many other Egernia species that occupy different habitats and are more secretive, it is hard to gather the observational data needed to deduce their social structure. Therefore, we used genotypes at six polymorphic microsatellite DNA loci of 229 individuals of Egernia frerei, trapped in 22 sampling sites over 3500 ha of eucalypt forest on Fraser Island, Australia. Each sampling site contained 15 trap locations in a 100 × 50 m grid. We estimated relatedness among pairs of individuals and found that relatedness was higher within than between sites. Relatedness of females within sites was higher than relatedness of males, and was higher than relatedness between males and females. Within sites we found that juvenile lizards were highly related to other juveniles and to adults trapped at the same location, or at adjacent locations, but relatedness decreased with increasing trap separation. We interpreted the results as suggesting high natal philopatry among juvenile lizards and adult females. This result is consistent with stable family group structure previously reported in rock dwelling Egernia species, and suggests that social behaviour in this genus is not habitat driven.