The ontogeny of morphological defenses in Kemp's ridley (Lepidochelys kempii) and loggerhead (Caretta caretta) sea turtles

Marine turtles are large reptiles that compensate for high juvenile mortality by producing hundreds of hatchlings during a long reproductive lifespan. Most hatchlings are taken by predators during their migration to, and while resident in, the open ocean. Their survival depends upon crypticity, minimizing movement to avoid detection, and foraging efficiently to grow to a size too difficult for predators to either handle or swallow. While these behavioral antipredator tactics are known, changes in morphology accompanying growth may also improve survival prospects. These have been only superficially described in the literature. Here, we compare the similarities and differences in presumed morphological defenses of growing loggerhead (Caretta caretta) and Kemp's ridley (Lepidochelys kempii) posthatchlings, related species that differ in growth rate, timing of habitat shift (the return from oceanic to neritic locations), and size at maturity. In both species, vertebral spination and carapace widening increase disproportionally as small turtles grow, but later in ontogeny, the spines regress, sooner in ridley than in loggerhead turtles. Carapace widening occurs in both species but loggerheads are always longer than they are wide whereas in Kemp's ridley turtles, the carapace becomes as wide as long. Our analysis indicates that these changes are unrelated to when each species shifts habitat but are related to turtle size. We hypothesize that the spines function in small turtles as an early defense against gape‐limited predators, but changes in body shape function throughout ontogeny—initially to make small turtles too wide to swallow and later by presenting an almost flat and hardened surface that large predators (such as a sharks) are unable to grasp. The extremely wide carapace of the Kemp's ridley may compensate for its smaller adult size (and presumed greater vulnerability) than the loggerhead. J. Morphol. 276:929–940, 2015. © 2015 Wiley Periodicals, Inc.     

Early growth and development of morphological defenses in post-hatchling flatbacks (Natator depressus) and green turtles (Chelonia mydas)

Marine turtles produce hundreds of precocial offspring (“hatchlings”) that are virtually defenseless. Many are consumed by predators. Hatchlings improve their survival prospects by migrating to offshore “nursery” areas with lower predator densities and, as they grow, by developing morphological defenses. The flatback turtle (Natator depressus), however, remains in the predator-rich coastal waters of Australia. To gain insights into how they survive there, we compared patterns of early growth and morphological development in flatbacks to their closest relative, the green turtle (Chelonia mydas), which migrates offshore. We found that morphological structures likely to be used in defense are better developed in juvenile flatbacks than in juvenile green turtles. Those structures probably represent one of a suite of characters that enable young flatbacks to survive in coastal habitats where interactions with predators are likely to be more frequent.     

Ontogenetic scaling of bite force in lizards and turtles

Because selection on juvenile life-history stages is likely strong, disproportionately high levels of performance (e.g., sprint speed, endurance, etc.) might be expected. Whereas this phenomenon has been demonstrated with respect to locomotor performance, data for feeding are scarce. Here, we investigate the relationships among body dimensions, head dimensions, and bite force during growth in lizards and turtles. We also investigate whether ontogenetic changes in bite performance are related to changes in diet. Our analyses show that, for turtles, head dimensions generally increase with negative allometry. For lizards, heads scale as expected for geometrically growing systems. Bite force generally increased isometrically with carapace length in turtles but showed significant positive allometry relative to body dimensions in lizards. However, both lizards and turtles display positive allometric scaling of bite force relative to some measures of head size throughout ontogeny, suggesting (1) strong selection for increased relative bite performance with increasing head size and (2) intrinsic changes in the geometry and/or mass of the jaw adductors during growth. Whereas our data generally do not provide strong evidence of compensation for lower absolute levels of performance, they do show strong links among morphology, bite force, and diet during growth.     

The optimal sampling strategy for unfamiliar prey

Precisely how predators solve the problem of sampling unfamiliar prey types is central to our understanding of the evolution of a variety of antipredator defenses, ranging from Müllerian mimicry to polymorphism. When predators encounter a novel prey item then they must decide whether to take a risk and attack it, thereby gaining a potential meal and valuable information, or avoid such prey altogether. Moreover, if predators initially attack the unfamiliar prey, then at some point(s) they should decide to cease sampling if evidence mounts that the type is on average unprofitable to attack. Here, I cast this problem as a "two-armed bandit," the standard metaphor for exploration-exploitation trade-offs. I assume that as predators encounter and attack unfamiliar prey they use Bayesian inference to update both their beliefs as to the likelihood that individuals of this type are chemically defended, and the probability of seeing the prey type in the future. I concurrently use dynamic programming to identify the critical informational states at which predator should cease sampling. The model explains why predators sample more unprofitable prey before complete rejection when the prey type is common and explains why predators exhibit neophobia when the unfamiliar prey type is perceived to be rare.     

Optimal reproductive strategies in age-structured populations of zooplankton

SUMMARY. We describe a model of zooplankton population dynamics that accounts for differences in mortality and physiology among animals of different ages or sizes. The model follows changes in numbers of individuals and changes in individual and egg biomass through time and it expresses mortality and net assimilation as functions of animal size.
We investigated the effect of egg size, age at first reproduction, and size at first reproduction on the per capita growth rates of populations growing under different conditions. In the absence of predation or when exposed to vertebrate predators that prefer large prey, populations achieve maximum growth rates when animals hatch from small eggs and reach maturity quickly at small sizes. Populations exposed to invertebrate predators that concentrate on small animals may increase r in two different ways. One way is for animals to increase juvenile survivorship by hatching from large eggs and by shortening the juvenile period. An alternative strategy is for animals to hatch from small eggs and to postpone maturity until they grow beyond the range of sizes available to their predators. Certain life history strategies maximize r if animals continue to grow after they reach maturity. By growing larger, non-primiparous females are able to hatch larger clutches and thereby increase the overall rate of population growth.
The model analysis shows how to assess age-dependent mortality rates from field data. The net rate of population increase and the age distribution of eggs together provide specific, quantitative information about mortality.     

LIFE-HISTORY EVOLUTION IN GUPPIES (POECILIA RETICULATA) 6. DIFFERENTIAL MORTALITY AS A MECHANISM FOR NATURAL SELECTION

We have previously reported a correlation between the life-history patterns of guppies and the types of predators with which they coexist. Guppies from localities with an abundance of large predators (high predation localities) mature at an earlier age and devote more resources to reproduction than those found in localities with only a single, small species of predator (low predation localities). We also found that when guppies were introduced from a high to low predation locality, the guppy life history evolved to resemble what was normally found in this low predation locality. The presumed mechanism of natural selection is differences among localities in age/size-specific mortality (the age/size-specific mortality hypothesis); in high predation localities we assumed that guppies experienced high adult mortality rates while in the low predation localities we assumed that guppies experienced high juvenile mortality rates. These assumptions were based on stomach content analyses of wild-caught predators and on laboratory experiments. Here, we evaluate these assumptions by directly estimating the mortality rates of guppies in natural populations. We found that guppies from high predation localities experience significantly higher mortality rates than their counterparts from low predation localities, but that these higher mortality rates are uniformly distributed across all size classes, rather than being concentrated in the larger size classes. This result appears to contradict the predictions of the age/size-specific predation hypothesis. However, we argue, using additional data on growth rates and the probabilities of survival to maturity in each type of locality, that the age-specific mortality hypothesis remains plausible. This is because the probability of survival to first reproduction is very similar in each type of locality, but the guppies from high predation localities have a much lower probability of survival per unit time after maturity. We also argue for the plausibility of two other mechanisms of natural selection. These results thus reveal mortality patterns that provide a potential cause of natural selection, but expand, rather than narrow, the number of possible mechanisms responsible for life-history evolution in guppies.     

Relative growth rates of predator and prey dinosaurs reflect effects of predation

Hadrosaurs grew rapidly, and quantifying their growth is key to understanding life-history interactions between predators and prey during the Late Cretaceous. In this study, we longitudinally sampled a sequence of lines of arrested growth (LAGs) from an essentially full-grown hadrosaur Hypacrosaurus stebingeri (MOR 549). Spatial locations of LAGs in the femoral and tibial transverse sections of MOR 549 were measured and circumferences were calculated. For each bone, a time series of circumference data was fitted to several stochastic, discrete growth models. Our results suggest that the femur and the tibia of this specimen of Hypacrosaurus probably followed a Gompertz curve and that LAGs reportedly missing from early ontogeny were obscured by perimedullary resorption. In this specimen, death occurred at 13 years and took approximately 10-12 years to reach 95 per cent asymptotic size. The age at growth inflection, which is a proxy for reproductive maturity, occurred at approximately 2-3 years. Comparisons with several small and large predatory theropods reveal that MOR 549 grew faster and matured sooner than they did. These results suggest that Hypacrosaurus was able to partly avoid predators by outgrowing them.     

Survival and Causes of Mortality of Head-Started Western Pond Turtles on Pierce National Wildlife Refuge,Washington

ABSTRACT The western pond turtle (Actinemys marmorata) is a species of conservation concern over much of its range and is listed as endangered in Washington State. From 2000 to 2004, we used radiotelemetry to document survival and mortality factors of head-started western pond turtles (n = 68) released into Pierce National Wildlife Refuge in southwestern Washington. Survival estimates for first year and older turtles ranged from 86% to 97% and overlapping confidence intervals indicated no detectible differences among age classes or among years. Subadult turtles released at ≥90-mm carapace length apparently avoided capture by most aquatic predators, indicating that terrestrial predators should be the focus of research and management where predation on larger age-classes is a concern. High annual survival combined with the documented nesting by ≥7-year-old female head-started turtles in Washington suggest that recruitment of adults is being achieved; however, head-starting is only practical as an interim solution and strategies for effective removal of aquatic predators must be developed and implemented where natural recruitment is inadequate to maintain populations.     

Effects of tail autotomy on survival,growth and territory occupation in free‐ranging juvenile geckos (Oedura lesueurii)

Abstract Many animals autotomize their tails to facilitate escape from predators. Although tail autotomy can increase the likelihood of surviving a predatory encounter, it may entail subsequent costs, including reduced growth, loss of energy stores, a reduction in reproductive output, loss of social status and a decreased probability of survival during subsequent encounters with predators. To date, few studies have investigated the potential fitness costs of tail autotomy in natural populations. I investigated whether tail loss influenced survival, growth and territory occupation of juvenile velvet geckos Oedura lesueurii in a population where predatory snakes were common. During the 3‐year mark–recapture study, 32% of juveniles voluntarily autotomized their tails when first captured. Analysis of survival using the program mark showed that voluntary tail autotomy did not influence the subsequent survival of juvenile geckos. Survival was age‐dependent and was higher in 1‐year‐old animals (0.98) than in hatchlings (0.76), whereas recapture probabilities were time‐dependent. Growth rates of tailed and tailless juveniles were very similar, but tailless geckos had slow rates of tail regeneration (0.14 mm day⁻¹). Tail autotomy did not influence rock usage by geckos, and both tailed and tailless juveniles used few rocks as diurnal retreat sites (means of 1.64 and 1.47 rocks, respectively) and spent long time periods (85 and 82 days) under the same rocks. Site fidelity may confer survival advantages to juveniles in populations sympatric with ambush foraging snakes. My results show that two potential fitness costs of tail autotomy – decreased growth rates and a lower probability of survival – did not occur in juveniles from this population. However, compared with juveniles, significantly fewer adult geckos (17%) voluntarily autotomized their tails during capture. Because adults possess large tails that are used for lipid storage, the energetic costs of tail autotomy are likely to be much higher in adult than in juvenile O. lesueurii.     

Do trade‐offs between predation pressures on females versus nests drive nest‐site choice in painted turtles?

Predation strongly influences reproductive behaviours because reproducing individuals must balance mortality risks to themselves and to their offspring. In many freshwater turtles, the nest predation risk decreases with nest distance from water, whereas the predation risk to females increases farther from water. To determine whether predation pressure influences the distance from water at which female turtles nest, we measured predation pressure on nesting females and on nests, as well as the distances of nests to water, in two populations of painted turtles. Using models, we found that female survival in both populations was high and did not vary with distance from water. Nest survival was also uncorrelated with nest distance to water, although it was significantly lower than adult survival in both populations and was only 1.2% in one population. Our results suggest that nest sites are not predictably safe from predators. Instead, turtles may hedge their bets by nesting over a wide range of distances from water because any distance is risky for nests and no distance is particularly risky for the nesting female. We suggest that other factors, such as suitable incubation conditions and/or post‐emergence hatchling survival, probably play a larger role than predation in driving nest‐site choice in painted turtles.     

Feedback between size balance and consumption strongly affects the consequences of hatching phenology in size‐dependent predator–prey interactions

In many size‐dependent predator–prey systems, hatching phenology strongly affects predator–prey interaction outcomes. Early‐hatched predators can easily consume prey when they first interact because they encounter smaller prey. However, this process by itself may be insufficient to explain all predator–prey interaction outcomes over the whole interaction period because the predator–prey size balance changes dynamically throughout their ontogeny. We hypothesized that hatching phenology influences predator–prey interactions via a feedback mechanism between the predator–prey size balance and prey consumption by predators. We experimentally tested this hypothesis in an amphibian predator–prey model system. Frog tadpoles Rana pirica were exposed to a predatory salamander larva Hynobius retardatus that had hatched 5, 12, 19 or 26 days after the frog tadpoles hatched. We investigated how the salamander hatch timing affected the dynamics of prey mortality, size changes of both predator and prey, and their subsequent life history (larval period and size at metamorphosis). The predator–prey size balance favoured earlier hatched salamanders, which just after hatching could successfully consume more frog tadpoles than later hatched salamanders. The early‐hatched salamanders grew rapidly and their accelerated growth enabled them to maintain the predator‐superior size balance; thus, they continued to exert strong predation pressure on the frog tadpoles in the subsequent period. Furthermore, frog tadpoles exposed to the early‐hatched salamanders were larger at metamorphosis and had a longer larval period than other frog tadpoles. These results suggest that feedback between the predator‐superior size balance and prey consumption is a critical mechanism that strongly affects the impacts of early hatching of predators in the short‐term population dynamics and life history of the prey. Because consumption of large nutrient‐rich prey items supports the growth of predators, a similar feedback mechanism may be common and have strong impacts on phenological shifts in size‐dependent trophic relationships.     

Developmental causes of allometry: new models and implications for phenotypic plasticity and evolution

Shapes change during development because tissues, organs, and various anatomical features differ in onset, rate, and duration of growth. Allometry is the study of the consequences of differences in the growth of body parts on morphology, although the field of allometry has been surprisingly little concerned with understanding the causes of differential growth. The power-law equation y?=?ax(b), commonly used to describe allometries, is fundamentally an empirical equation whose biological foundation has been little studied. Huxley showed that the power-law equation can be derived if one assumes that body parts grow with exponential kinetics, for exactly the same amount of time. In life, however, the growth of body parts is almost always sigmoidal, and few, if any, grow for exactly the same amount of time during ontogeny. Here, we explore the shapes of allometries that result from real growth patterns and analyze them with new allometric equations derived from sigmoidal growth kinetics. We use an extensive ontogenetic dataset of the growth of internal organs in the rat from birth to adulthood, and show that they grow with Gompertz sigmoid kinetics. Gompertz growth parameters of body and internal organs accurately predict the shapes of their allometries, and that nonlinear regression on allometric data can accurately estimate the underlying kinetics of growth. We also use these data to discuss the developmental relationship between static and ontogenetic allometries. We show that small changes in growth kinetics can produce large and apparently qualitatively different allometries. Large evolutionary changes in allometry can be produced by small and simple changes in growth kinetics, and we show how understanding the development of traits can greatly simplify the interpretation of how they evolved.     

Colony size selection determines adult survival and dispersal preferences: allee effects in a colonial bird

Avian coloniality traditionally has been investigated by examining how breeding success varies with colony size, but other crucial fitness components rarely have been examined. This may lead to wrong conclusions because unmeasured parameters may change the final fitness balance. We used multistate capture-recapture models to investigate adult survival and dispersal in relation to colony size within a long-term monitored population of lesser kestrels (Falco naumanni). Nest predation probability decreases with colony size, and adult survival is predicted to show the same trend because adults are exposed to the same suite of predators. As expected, survival probability was higher in large colonies (0.72+/-0.015; mean+/-SE) than in medium or small colonies (0.65+/-0.02). Additionally, dispersal probabilities were higher going from small to large colonies (0.20+/-0.01) than from large to small (0.08+/-0.01), as predicted by theory of habitat selection shaped by fitness maximization. These asymmetries are likely to generate size-specific colony population dynamics, so they should be taken into account in studies of colonial birds and other metapopulation-like systems. Allee effects, that is, positive density dependence, appear to be the cause of the evolution of dispersal behavior and may explain the maintenance of coloniality in this species.     

Evaluating the effects of trophic complexity on a keystone predator by disassembling a partial intraguild predation food web

1. Many taxa can be found in food webs that differ in trophic complexity, but it is unclear how trophic complexity affects the performance of particular taxa. In pond food webs, larvae of the salamander Ambystoma opacum occupy the intermediate predator trophic position in a partial intraguild predation (IGP) food web and can function as keystone predators. Larval A. opacum are also found in simpler food webs lacking either top predators or shared prey. 2. We conducted an experiment where a partial IGP food web was simplified, and we measured the growth and survival of larval A. opacum in each set of food webs. Partial IGP food webs that had either a low abundance or high abundance of total prey were also simplified by independently removing top predators and/or shared prey. 3. Removing top predators always increased A. opacum survival, but removal of shared prey had no effect on A. opacum survival, regardless of total prey abundance. 4. Surprisingly, food web simplification had no effect on the growth of A. opacum when present in food webs with a low abundance of prey but had important effects on A. opacum growth in food webs with a high abundance of prey. Simplifying a partial IGP food web with a high abundance of prey reduced A. opacum growth when either top predators or shared prey were removed from the food web and the loss of top predators and shared prey influenced A. opacum growth in a non-additive fashion. 5. The non-additive response in A. opacum growth appears to be the result of supplemental prey availability augmenting the beneficial effects of top predators. Top predators had a beneficial effect on A. opacum populations by reducing the abundance of A. opacum present and thereby reducing the intensity of intraspecific competition. 6. Our study indicates that the effects of food web simplification on the performance of A. opacum are complex and depend on both how a partial IGP food web is simplified and how abundant prey are in the food web. These findings are important because they demonstrate how trophic complexity can create variation in the performance of intermediate predators that play important roles in temporary pond food webs.     

The interpretation of stem diameter–height allometry in trees: biomechanical constraints,neighbour effects,or biased regressions?

Static diameter–height allometry data have been used by many ecologists to demonstrate that diameter should increase at a faster rate than height during tree growth, as predicted by biomechanical models. We review the available evidence and examine the potential problems that arise in the interpretation of this relationship. In particular, we reveal how few studies investigating patterns of diameter–height allometry in trees have adequately controlled for neighbour effects. We also demonstrate how the interpretation of diameter–height allometry has suffered from a lack of uniformity in the selection of regression models, and how the use of least squares regression to estimate allometric scaling exponents can be biased. We conclude that most of the published data on static diameter–height relationships in trees tell us virtually nothing about either age (developmental) effects or neighbour effects; they are completely confounded. Further studies are required to analyse the long-term dynamic growth trajectories of individual trees in relation to local neighbour effects, and greater effort must be made to establish the consistent use of unbiased statistical methods between studies.     

First satellite tracks of neonate sea turtles redefine the ‘lost years’ oceanic niche

Few at-sea behavioural data exist for oceanic-stage neonate sea turtles, a life-stage commonly referred to as the sea turtle ‘lost years’. Historically, the long-term tracking of small, fast-growing organisms in the open ocean was logistically or technologically impossible. Here, we provide the first long-term satellite tracks of neonate sea turtles. Loggerheads (Caretta caretta) were remotely tracked in the Atlantic Ocean using small solar-powered satellite transmitters. We show that oceanic-stage turtles (i) rarely travel in Continental Shelf waters, (ii) frequently depart the currents associated with the North Atlantic Subtropical Gyre, (iii) travel quickly when in Gyre currents, and (iv) select sea surface habitats that are likely to provide a thermal benefit or refuge to young sea turtles, supporting growth, foraging and survival. Our satellite tracks help define Atlantic loggerhead nursery grounds and early loggerhead habitat use, allowing us to re-examine sea turtle ‘lost years’ paradigms.     

Early Life-History Consequences of Growth-Hormone Transgenesis in Rainbow Trout Reared in Stream Ecosystem Mesocosms

There is persistent commercial interest in the use of growth modified fishes for shortening production cycles and increasing overall food production, but there is concern over the potential impact that transgenic fishes might have if ever released into nature. To explore the ecological consequences of transgenic fish, we performed two experiments in which the early growth and survival of growth-hormone transgenic rainbow trout (Oncorhynchus mykiss) were assessed in naturalized stream mesocosms that either contained predators or were predator-free. We paid special attention to the survival bottleneck that occurs during the early life-history of salmonids, and conducted experiments at two age classes (first-feeding fry and 60 days post-first-feeding) that lie on either side of the bottleneck. In the late summer, the first-feeding transgenic trout could not match the growth potential of their wild-type siblings when reared in a hydrodynamically complex and oligotrophic environment, irrespective of predation pressure. Furthermore, overall survival of transgenic fry was lower than in wild-type (transgenic = 30% without predators, 8% with predators; wild-type = 81% without predators, 31% with predators). In the experiment with 60-day old fry, we explored the effects of the transgene in different genetic backgrounds (wild versus domesticated). We found no difference in overwinter survival but significantly higher growth by transgenic trout, irrespective of genetic background. We conclude that the high mortality of GH-transgenic trout during first-feeding reflects an inability to sustain the basic metabolic requirements necessary for life in complex, stream environments. However, when older, GH-transgenic fish display a competitive advantage over wild-type fry, and show greater growth and equal survival as wild-type. These results demonstrate how developmental age and time of year can influence the response of genotypes to environmental conditions. We therefore urge caution when extrapolating the results of GH-transgenesis risk assessment studies across multiple life-history or developmental stages.     

Parental care and the ontogeny of predator-avoidance in two species of centrarchid fish

Stamps (1978) suggested that the type and extent of parental care can influence the behavioural ontogeny of the offspring. Largemouth bass (Micropterus salmoides) males guard the fry for up to a month after they leave the nest while rock bass (Ambloplites rupestris) males guard the fry only until they leave the nest. In laboratory experiments, naive largemouth fry displayed reduced predator-avoidance responses to large and small predators during their first 3 weeks of free-swimming. Rock bass fry, on the other hand, avoided predators throughout the study period. From 6 weeks (largemouth) and 5 weeks (rock bass) of age the fry showed a significantly greater response to the large predator than the small predator. The responses of laboratory-reared largemouth bass fry to the small predator changed from avoidance to association as the fry grew. The size of the fry relative to predator size was found to be important.     

Woodland caribou calf mortality in Newfoundland: insights into the role of climate,predation and population density over three decades of study

The rates and causes of juvenile mortality are central features of the dynamics and conservation of large mammals, like woodland caribou (Rangifer tarandus caribou (Gmelin, 1788)), but intrinsic and extrinsic factors may be modified by variations in animal abundance. We tested the influences of population size, climate, calf weight and sex on survival to 6 months of age of 1241 radio-collared caribou calves over three decades, spanning periods of population growth (1979–1997) and decline (2003–2012) in Newfoundland, Canada. Daily survival rates were higher and rose more quickly with calf age during the population growth period compared to the decline. Population size (negatively) and calf weight (positively) affected survival during the decline but neither had a detectable influence during the growth phase. Sex, climate and plant productivity (the latter two derived from the North Atlantic Oscillation and Normalized Difference Vegetation Index, respectively) exerted minimal influence during either phase. Predation was the dominant source of mortality. The mean percentage of calves killed by predators was 30 % higher during the decline compared to the growth phase. Black bears (Ursus americanus) and lynx (Lynx canadensis) were the major predators during the population increase but this changed during the decrease to black bears and coyotes (Canis latrans). Our findings are consistent with the hypothesis that Newfoundland caribou experienced phase-dependent survival mediated proximally by predation and competition for food.