ArticlePDF Available

Patterns of Survival, Growth and Maturation in Turtles

Wiley
Oikos
Authors:

Abstract

A review of published data suggests that turtles (Order Testudines) resemble other previously studied vertebrate and invertebrate groups in terms of the relationships among growth trajectories, adult survival rates, and ages at maturation. For example, most turtles mature at around 70% of maximum size, as do other reptiles. Adult lifespans are proportional to age at maturity, and the relationship between these two variables is similar in turtles to that documented in other reptiles. Although the ratio of the von Bertalanffy growth constant (k) to the adult instantaneous mortality rate (M) appears to be higher than ratios reported for other animals (including squamate reptiles), the general relationship between these two variables corresponds with that seen in other reptiles. These analyses show that turtles exhibit patterns of growth, survivorship and maturation that are of the same form as those that are present in other types of organisms in which growth continues after maturity.
A preview of the PDF is not available
... After hatching, juveniles were transferred to artificial water tanks, where their mortality rate over the one-month rearing period was 0.05, calculated by dividing the number of juvenile deaths by the total number of hatchlings at the start of the rearing period. We highlight that this juvenile mortality rate is lower than that in the wild (Andrade, 2008;Iverson, 1991;Mogollones et al., 2010;Shine and Iverson, 1995), as turtles in the tanks are protected from predators, receive adequate feeding, and are shielded from diseases. Following this, the juveniles were released into their natural habitat. ...
Article
Full-text available
The yellow-spotted river turtle (Podocnemis unifilis) is widely distributed across the Amazon, Orinoco, and Essequibo River basins. Studies from the Amazon and Orinoco regions highlight the species’ importance to local communities for food, income, and cultural heritage, as well as the significant threats it faces. To expand knowledge in the Essequibo River basin and assist with population management, the goal of this study was to assess turtle and egg consumption, as well as nest and turtle numbers, in the South Rupununi River in Guyana, and finally to propose sustainable management strategies that balance conservation goals with community needs, by comparing egg consumption rates with potential flood-related losses. Based on interviews conducted with 125 out of 185 Wapichan households from Sand Creek community, our findings showed that 12.0% of households (n = 15) collect annually an average of 41.87 eggs per household, while 22.4% of households (n = 28) harvest an average of 3.32 turtles per household per year. Households with more children tend to consume higher amounts of turtle eggs and meat, and those engaging in turtle harvesting report higher levels of turtle meat consumption. The primary motivation for turtle capture is consumption, particularly during culturally significant occasions, though turtles are also used for local trade, as pets, and for their shells. At the community level, the estimated annual consumption of 929 eggs is lower than the estimated 1,210 eggs lost annually to flooding on monitored beaches. However, the estimated 138 turtles harvested village-wide exceeds the number of adult turtles observed per survey day in 2021 (n = 13) and 2022 (n = 19). Our analysis suggests that during years with early floods, local egg demand could be met by rescuing at-risk nests located near the river, without increasing natural egg mortality. To offset wild turtle harvests, we recommend hatching at least 182 rescued eggs ex-situ and managing them through extensive farming systems. This approach could reduce adult turtle harvests, particularly of females. To achieve sustainable management, we propose monitoring all beaches where eggs are harvested, implementing a nest rescue program during floods, and establishing extensive turtle farming systems. These measures could shift egg harvesting from wild populations to controlled ex-situ programs, helping to conserve the yellow-spotted river turtle while supporting community needs.
... For example, the ratio between the body length at the age of sexual maturity and maximum body length of an adult individual is 0.95 for the Asian elephant (Elephas maximus), 0.9 for the fur seal (Arctocephalus forsteri) and 0.97 for the polar bear (Ursus maritimus) [71][72][73]. In snakes, tortoises, and lizards, this ratio is on average 0.68, 0.70, and 0.74, respectively [74,75]. ...
Article
Various environmental morphological and behavioral factors may be decisive in the longevity of representatives of various taxa. Long-lived species develop systems aimed at increasing the body’s stability and defense, and ultimately increasing life expectancy. In addition, long-living species are characterized by different levels of manifestation of factors favorable to longevity (gerontological success): body size, slow metabolism, level of activity of the body’s repair systems and antioxidant defense systems, resistance to toxic substances and tumor formation, and the presence of neotenic characteristics. Continuing the work on mammals, in this work we studied the characteristics that distinguish long-lived ectotherms (crocodiles and turtles) and compared them with those of other representatives of ectotherms (squamates and amphibians) and endotherms (birds and mammals). The article also discusses mathematical indicators used to assess the predisposition to longevity in different species. These indicators include both standard ones (mortality rate, maximum lifespan, coefficient of variation of lifespan) and derivatives from them. evolutionary patterns of aging are further explained by protective phenotypes and life history strategies. The work assessed the relationship between lifespan and various studied factors, including body size and temperature, encephalization, protection of occupied econiches, the presence of protective structures (for example, shell and osteoderms), environmental temperature, etc.), and their influence on the distribution of lifespan as a statistical quantities. The hypothesis about the level of metabolism and temperature as the most determining factors of longevity was not confirmed. It turned out that animals protected by shells (turtles with their exceptional longevity) live longer than species that have poison or lack protective devices. The improvement of methods of defense against external threats in long-lived ectotherms is consistent with the characteristics of long-lived endotherms (for example, naked mole rats that live in tunnels underground, or bats and birds, whose ability to fly is also one of the best methods of defense).
... Significance levels (p) are provided for phylogenetic generalized least squares and phylogenetic ANOVA analyses of DRs for BSI and biome, respectively. long generation times (McGaugh, 2012) requiring a long time for the offspring to reach sexual maturity (between 5 and 50 years depending on the species), as well as a significant longevity of adult individuals (Shine and Iverson, 1995). But exhibit very variable reproductive rates across species, with some Testudinidae females producing less than 10 eggs (Epperson and Heise, 2003), and sea species with more than 40 offspring, typically around 90, and sometimes up to 200 each year (Hirth, 1980). ...
Article
Full-text available
The resource-use hypothesis proposed by Elisabeth S. Vrba suggests that lineages display varying tendencies toward generalism or specialization in biome occupancy, with a tendency towards the accumulation of specialists due to their higher rate of speciation through vicariance. It also posits differences in biome occupancy patterns driven by the environmental characteristics of biomes, with a higher presence of biome specialist species in biomes that are placed in the extremes of the global climatic gradients. Here, we tested this hypothesis in turtles, a very ancient and morphologically stable lineage, representing a remarkable diversity with 357 species, many of which are threatened with extinction. We analyzed the resource-use hypothesis in a phylogenetic context within the Testudines lineage. For this purpose, a presence/absence matrix was compiled for all species across all 10 terrestrial biomes. Their distribution across biomes was contrasted with 10,000 Monte Carlo simulations. The relationship between diversification rates and both the biomic specialization index and the biomes occupied by specialists species was evaluated. The results demonstrate strong consistency with Vrba`s hypothesis, revealing a higher number of biome specialist species than expected by chance, with a significant accumulation of species in tropical ecosystems. These trends also were observed for ecological groups (terrestrial and freshwater species). In addition, higher diversification rates were observed for biome specialist species, although the particular biome occupied did not significantly influence their diversification rates.
... However, data are usually not based on individuals, but are estimated from the smallest recorded size at reproduction and maximum asymptotic size in a large number of individuals. This assumes that individuals vary little in age at first reproduction and maximum size can be estimated from growth models (Shine & Iverson, 1995). However, frequently used sigmoidal models of growth are often imprecise (Campos et al., 2014), and data are not usually presented to indicate whether individuals follow the mean trajectory or remain parallel to it for most of their life (Magnusson, 2012). ...
Article
We recaptured 26 female and 24 male Pantanal caimans Caiman yacare of known-age up to 36 years after marking. The relationship between clutch size and age for known-age females was highly variable although one female captured multiple times between 18 and 26 years of age showed little variation in clutch size. Captured known-age females attending nests varied from 73 cm to 89 cm snout-vent length and from 9 to 36 years old. These females continued to grow long after their first capture, so cessation of growth does not appear to be related to reproduction. Most known-age animals were recaptured within 10 km of where they hatched, but usually on a different ranch, so ranches cannot be used as autonomous management units. Our data indicate that the ratio of snout-vent length (SVL) at first reproduction (73 cm) to mean asymptotic SVL reported for this species (85.7 cm SVL) is much higher in female Pantanal caimans (0.85) than has been reported for most other reptiles (0.7).
... Reptiles have a significant positive relationship between somatic growth and adult mortality rates (Shine and Iverson 1995). A somatic growth rate assessment for P. grozugi in the Black River revealed exceptionally low Brody growth coefficients (i.e. ...
Article
Full-text available
Estimating the key demographic parameters of animal populations can enhance our understanding of system dynamics and assist in developing and improving conservation decision–support models. The Rio Grande cooter Pseudemys gorzugi is a conservation reliant freshwater turtle native to lower Rio Grande River Basin (USA and Mexico), with limited knowledge regarding its natural history and population dynamics. In this study, we used seven years of capture–mark–recapture data from the northern edge of the species' range to estimate survival probabilities, changes in abundance, and the probability of transitioning between different size classes while explicitly accounting for the sampling process. We found relatively high survival probabilities across different strata, with large juveniles exhibiting the highest survival (0.98) and small juveniles the lowest (0.71). However, transition probabilities between strata were low, indicating slow somatic growth rates. Our pattern‐oriented modelling revealed a low overall mean estimate of egg survival (0.024), warranting further empirical confirmation. Our study provides the first comprehensive demographic analysis of P. gorzugi encompassing an array of size and sex classes. Overall, we consider the population of P. gorzugi in the Black River robust, highlighting the importance of this river system to the species' persistence in the northern extent of its range, where the population is isolated from its broader distribution. The demographic estimates and ecological insights provided by our study offer critical data for parameterizing decision‐support models to ensure that P. gorzugi conservation strategies are grounded in the best available science.
... For example, the ratio between the body length at the age of sexual maturity and maximum body length of an adult individual is 0.95 for the Asian elephant (Elephas maximus), 0.9 for the fur seal (Arctocephalus forsteri) and 0.97 for the polar bear (Ursus maritimus) [71][72][73]. In snakes, tortoises, and lizards, this ratio is on average 0.68, 0.70, and 0.74, respectively [74,75]. ...
Article
Various environmental morphological and behavioral factors can determine the longevity of representatives of various taxa. Long-lived species develop systems aimed at increasing organism stability, defense, and, ultimately, lifespan. Long-lived species to a different extent manifest the factors favoring longevity (gerontological success), such as body size, slow metabolism, activity of body's repair and antioxidant defense systems, resistance to toxic substances and tumorigenesis, and presence of neotenic features. In continuation of our studies of mammals, we investigated the characteristics that distinguish long-lived ectotherms (crocodiles and turtles) and compared them with those of other ectotherms (squamates and amphibians) and endotherms (birds and mammals). We also discussed mathematical indicators used to assess the predisposition to longevity in different species, including standard indicators (mortality rate, maximum lifespan, coefficient of variation of lifespan) and their derivatives. Evolutionary patterns of aging are further explained by the protective phenotypes and life history strategies. We assessed the relationship between the lifespan and various studied factors, such as body size and temperature, encephalization, protection of occupied ecological niches, presence of protective structures (for example, shells and osteoderms), and environmental temperature, and the influence of these factors on the variation of the lifespan as a statistical parameter. Our studies did not confirm the hypothesis on the metabolism level and temperature as the most decisive factors of longevity. It was found that animals protected by shells (e.g., turtles with their exceptional longevity) live longer than species that have poison or lack such protective adaptations. The improvement of defense against external threats in long-lived ectotherms is consistent with the characteristics of long-lived endotherms (for example, naked mole-rats that live in underground tunnels, or bats and birds, whose ability to fly is one of the best defense mechanisms).
... Freshwater turtles play critical roles in their respective environments (Congdon et al. 1986;Mitchell 1988;Shine and Iverson 1995;Ernst and Lovich 2009;Mitchell and Buhlmann 2009;Lovich et al. 2018) and studying them in situ can be inherently difficult given their natural history. Most field study methods consist of snorkeling, sounding pole surveys, visual encounter with or without binoculars from a shore or boat, or trapping with baited and un-baited hoop nets or basking traps (MacCulloch and Gordon 1978;Vogt 1980;Sterrett et al. 2010). ...
Article
Full-text available
Aquatic remotely operated vehicles (ROV) show merit in providing in situ observations of sea turtles and freshwater turtles. However, turtles must be spotted above the water surface first then an ROV deployed for underwater observation. None have been used as a tool to survey for turtles solely under the water surface without direct observation first. Here we report on observations of two types of aquatic ROVs used during a mock turtle survey to determine the potential of freshwater turtles being found under the water surface without being directly observed first and if accurate species identification could be done.
... We used SVL to fit a von Bertalanffy growth model (Fabens 1965), which has been shown to reflect the growth patterns of snakes recaptured during field studies appropriately (Shine and Charnov 1992;Shine and Iverson 1995;Blouin-Demers et al. 2002). We fit the von Bertalanffy model as follows: ...
Article
Full-text available
Reintroduction of species at sites where populations have been extirpated has become a common technique in wildlife conservation. To track progress towards reintroduction success, effective postrelease monitoring is needed to document vital rates of individuals and the corresponding impact on population trajectories. We assessed growth and body size in Eastern Indigo Snakes (Drymarchon couperi) using a data set from multiple projects across the species' distribution, including free-ranging wild snakes, snakes reared in captive-breeding programs, and snakes released at two reintroduction sites. We used these data to fit a von Bertalanffy growth model in a Bayesian framework to quantify differences in growth among three broad categories of snakes (wild, captive, and reintroduced), while accounting for measurement error across various projects. We also compared changes in body mass of captive-born individuals from four captive rearing facilities. Asymptotic snout–vent length across all groups was 185 cm (95% credible interval = 177–194 cm) for males and 157 cm (95% credible interval = 153–161 cm) for females. Reintroduced snakes had a higher growth coefficient than either captive or wild snakes (e.g., captive females = 1.20 [1.06–1.35] d–1; wild females = 1.22 [0.95–1.49] d–1; reintroduced females = 1.62 [1.21–2.05] d–1), indicating that current captive-breeding and rearing efforts for indigo snakes produce similar or faster growth trends compared to wild populations. Furthermore, daily changes in juvenile body weight relative to body size were similar in three of the four captive rearing facilities (mean for females at Orianne Center for Indigo Conservation = 0.57 [0.48–0.65]; Zoo Atlanta = 0.55 [0.37–0.72]; Welaka National Fish Hatchery = 0.55, [0.36–0.73]; Auburn University = 0.39 [0.21–0.58]). Long-term project success for indigo snake reintroductions will depend on continuing to implement best practices in an adaptive management framework.
Article
Full-text available
Background Body size is a critical trait that influences an animal’s physiology, behavior, and ecology. However, the molecular mechanisms underlying its evolution remain poorly understood, particularly in snakes. Snakes exhibit an extremely wide range of body sizes and strong ecological adaptability. Among snake species, the maximum body mass exceeds the minimum by over 200,000-fold, while the maximum body length surpasses the minimum by more than 110-fold. Results Through phylogenomic and comparative genomic analyses of 26 snake genomes, we identified 77 body size-associated genes (BSAGs) related to body length or body mass, highlighting key genetic drivers of body size evolution. Functional enrichment analyses revealed that metabolic pathways, particularly fatty acid metabolism and oxidoreductase activity, underwent significant expansion and positive selection, suggesting metabolic adaptations crucial for meeting the energetic demands of increased body size. Immune system-related genes, including those involved in antigen processing and presentation, similarly showed signatures of expansion and adaptive evolution, highlighting strengthened immune defenses in large-bodied snakes. Additionally, key candidate genes, such as YAP1, PLAG1, MGAT1 and SPRY1, exhibited both strong selection signals and correlation signals, and are functionally involved in developmental pathways critical for growth regulation. Conclusions Our findings reveal a complex interplay of sensory, immune, metabolic, and growth-related genetic adaptations driving large body size evolution in snakes. This study provides novel insights into the molecular underpinnings of snake body size diversification and advances our understanding of their evolutionary history.
Thesis
Full-text available
Life history and ecology of Sonoran Mud Turtles (Kinosternon sonoriense) were studied in 10 populations in Arizona. Ovulation occurred for the first time at close to 6 years of age in females from all populations, but slow-growing individuals in one population failed to mature until a minimum size was reached. Populations varied in egg size and relationship between egg width and pelvic opening. Within populations, egg size appeared to be optimized, but variation among populations indicated coevolution of egg size and pelvic opening, and apparent concomitant evolution of shell shape. Hatchlings were larger in populations with large eggs. These populations also had high adult survivorship but low pre-adult survivorship. Other reproductive traits co-varied among populations. Populations characterized by large eggs had small clutches (by weight and number of eggs), low growth rates and high reproductive outputs in early adulthood, and weak size-fecundity relationships. Small egg populations consistently had the reverse of these characteristics. Additionally, data on clutch frequency indicate females in large egg populations produce more clutches/yr than those in small egg populations, holding annual reproductive output (weight of eggs as a proportion of body size) relatively constant. Size-fecundity relationships, but not adult survivorship, appear to have a strong effect on reproductive pattern. Reproductive pattern in large egg populations could not be explained by demographic models requiring maximized lifetime output of eggs. It appeared that females were maximizing the number of lifetime clutches in response to low and/or variable nest, hatchling, and early juvenile survivorship.
Article
Capture-recapture measurements of 11 wild green turtles, Chelonia mydas, and of 28 wild loggerhead turtles, Caretta caretta, in Florida indicate that growth in straight-line carapace length fits von Bertalanffy growth models better than logistic models. The von Bertalanffy model for green turtle growth yields estimates for age at maturity of between 18 and 27 years, based on the carapace length of the smallest nesting female (88 cm) and the mean length of all nesting females (99 cm). The model for loggerheads yields estimates of between 12 and 30 years, also based on carapace measurements of the smallest nesting female (74 cm) and the mean carapace length of all nesting females (92 cm). It is suggested that the upper estimates provide more realistic indications of mean age at first maturity.
Article
The mud turtle does not vary geographically in body size, but the number of eggs per clutch is significantly higher at cooler latitudes. Scrutiny of a single population in South Carolina revealed a decrease in average clutch size during the egg-laying season. Although female body size, climate and season may be independently or interactively important in influencing clutch size, a high, unexplained variance indicates the influence of other factors. Multiple clutches within a season by individuals are frequent among South Carolina mud turtles and 2 clutches per year may be laid in cooler regions. Although clutch size did not vary annually in South Carolina, clutch frequency and the proportion of females laying eggs did. -from Author
Article
Chelodina longicollis in the vicinity of Armidale, NSW show typical temperate-zone chelonian gametogenic patterns. Mating is in September and ovulation occurs during late October and November. A single clutch is laid in November or December. The nesting season lasts c1 months although commencement date varies each year. There are significant positive correlations between female size/clutch size and female size/egg diameter. Natural incubation period is 110-120 days (nest temperature 21.5oC; range 12.5-32.0oC). Minimum estimate of nest predation at one study site was 49%. Nest predation in the general study area was probably greater. Hatchlings emerge from the nest in late March and go directly to water. Data indicated a Slobodkin Type IV survivorship curve with mortality primarily affecting eggs, hatchlings and juveniles. Estimated non-juvenile mortality was <2% per annum. -from Author
Article
We used data from a natural population of slider turtles, Trachemys scripta, (n = 70) to compare a von Bertalanffy growth equation constructed from known-age data with one constructed using Fabens' method (under the assumption that ages were not known). The 95% confidence intervals revealed no significant differences in estimates of variables a, b, or k for the two equations, both of the form: Lt=a(1-be-kt). We also examined the effects of truncated samples on Fabens' method by omitting large and small individuals. Fabens' method underestimated the asymptotic value, a, and overestimated the intrinsic growth factor, k, when larger individuals were omitted. The omission of small individuals resulted in little change in estimated values. Our findings confirm the utility of Fabens' method in estimating growth curves for animals of unknown age if data are available across all size classes. Although data on large individuals may be more important in arriving at accurate estimates of variable values, data on small individuals may be necessary to determine if another model (i.e., logistic) might provide a better descriptor of growth trajectories.