Developmental biology and ecology of the Kemp's ridley sea turtle. Lepidochelys kempii, in the eastern Gulf of Mexico
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Despite its biological importance in shaping both individual fitness and population structure, much remains to be learned about the hatchling emergence ecology of most freshwater turtles. Here, we provide some of the first details on these early life stages for the Ouachita map turtle ( Graptemys ouachitensis ) obtained during 2015–2017 along the lower Wisconsin River, Iowa County, Wisconsin, and integrate our results into related research within the genus Graptemys . Dedicated trail cameras over in situ turtle nests provided otherwise difficult to obtain observational data relevant to natural hatchling emergence without disturbing nests or hatchlings. In contrast to some earlier reports for Graptemys , hatchling emergence was mostly diurnal and synchronous, primarily in the morning soon after soil temperatures began to rise from overnight low values. Data suggest a temperature change model of cueing hatchling emergence, which may represent a local or regional adaptation to reduce nocturnal predation risks, mostly from raccoons ( Procyon lotor ), or may simply reflect default diurnal hatchling activity patterns when not affected by thermal constraints. Aside from predation, hatchlings on this small study site are affected by vegetative shading, leading to relatively long times to first emergence periods (mean, 82.3 d), low mean nest temperatures (25.9°C), and a likely male-biased sex ratio. These findings highlight the value of hatchling emergence studies in revealing important influences on population viability and in guiding appropriate habitat management in conservation efforts.
In the 1994 Recovery Plan for the Mojave population of the desert tortoise, Gopherus agassizii, the US Fish and Wildlife Service established 6 recovery units by using the best available data on habitat use, behavior, morphology, and genetics. To further assess the validity of the recovery units, we analyzed genetic data by using mitochondrial deoxyribonucleic acid (mtDNA) sequences and nuclear DNA microsatellites. In total, 125 desert tortoises were sampled for mtDNA and 628 for microsatellites from 31 study sites, representing all recovery units and desert regions throughout the Mojave Desert in California and Utah, and the Colorado Desert of California. The mtDNA revealed a great divergence between the Mojave populations west of the Colorado River and those occurring east of the river in the Sonoran Desert of Arizona. Some divergence also occurred between northern and southern populations within the Mojave population. The microsatellites indicated a low frequency of private alleles and a significant correlation between genetic and geographic distance among 31 sample sites, which was consistent with an isolation-by-distance population structure. Regional genetic differentiation was complementary to the recovery units in the Recovery Plan. Most allelic frequencies in the recovery units differed. An assignment test correctly placed most individuals to their recovery unit of origin. Of the 6 recovery units, the Northeastern and the Upper Virgin River units showed the greatest differentiation; these units may have been relatively more isolated than other areas and should be managed accordingly. The Western Mojave Recovery Unit, by using the new genetic data, was redefined along regional boundaries into the Western Mojave, Central Mojave, and Southern Mojave recovery units. Large-scale translocations of tortoises and habitat disturbance throughout the 20th century may have contributed to the observed patterns of regional similarity. ?? 2007 Chelonian Research Foundation.
A mark-recapture project on Macrochelys temminckii was conducted between 1997 and 2000 at Sequoyah National Wildlife Refuge, Muskogee and Sequoyah counties, in eastern Oklahoma. Turtles were captured in all streams and exhibited equal sex ratios, marked sexual-size dimorphism, and population densities between 28 and 34 animals per km stretch of stream. There was evidence of past population perturbations, with very few large adults captured, and a cohort of subadults highly underrepresented. ?? 2008 Chelonian Research Foundation.
We studied the population structure and growth of western pond turtles (Actinemys marmorata) at Vandenberg Air Force Base along the coast of central California in April 1995 and June 1996. We captured 179 individuals (115 males, 27 females) from 7 ponds during 26 days of trapping. Many turtles were adult-sized, but based on scute annuli, 74% were < 10 years of age, including many 2- to 3-year-olds. This population structure likely was due to a relatively fast growth rate, especially compared with closely related aquatic turtles in eastern North America. Mean clutch size was 5.2, but 66.7% of females were gravid, and 1 female produced 2 clutches. These reproductive data are similar to those reported for other populations in the southern portion of the species' range. Females reached reproductive maturity as early as 4 years of age. The relatively mild temperatures of California's Mediterranean climate, especially when compared to the seasonal extremes in more continental and northern regions of North America, may explain the different growth rates and population characteristics of freshwater turtles from these 2 regions of North America. ?? 2008 Chelonian Research Foundation.
Culverts are often used to increase the permeability of roaded landscapes for wildlife, including turtles. Although the benefits of culverts as safe passages for turtles are well documented, under some conditions culverts can entrap them and cause mortality. Here we report a culvert-related mortality in the federally threatened desert tortoise ( Gopherus agassizii ) at a wind energy facility in California and offer simple recommendations to mitigate the negative effects of culverts for wildlife in general.
Little is known about the movement behavior of the stripe-necked musk turtle, Sternotherus minor peltifer . Using radiotelemetry, we calculated mean (± SD) home range length, which was 341.4 ± 90.3 m, with home range length not differing between the sexes (males, 335 ± 194 m; females, 346 ± 79.5 m). Sternotherus m. peltifer were active in every month of the year but decreased their movement distance and frequency between December and March; during nonwinter and winter periods, individuals used limestone bluffs most often.
We scored 48 Malaclemys terrapin nests destroyed by raccoons on Fisherman Island, Virginia, for the presence or absence of tree canopy, shrub canopy, no canopy, bare sand, grass cover, and herbaceous cover. Significantly more nests than expected were found in the open with no vegetation cover and observed distances of predator-destroyed nests from the edge of the nearest habitat island of woody vegetation were significantly different from a normal distribution; most were placed near the island margin. Our results underscore the need to understand the influence of predator search behavior on terrapin nest survival in different habitat types.
Unique among turtles as the only exclusively estuarine species, the diamondback terrapin’s (Malaclemys terrapin) life history predisposes it to impacts from humans both on land and in the near-shore environment. Terrapins are found in salt marshes and mangroves along the Atlantic and Gulf coasts from Massachusetts to Texas. Whereas previous dietary studies have elucidated terrapins’ role in temperate salt marsh food webs, food resources for terrapins inhabiting subtropical mangrove habitats have not been studied. We examined dietary resource use for diamondback terrapins in subtropical mangrove creek and island habitats within Everglades National Park, Florida, to determine foraging strategies of terrapins inhabiting south Florida (SF) mangrove systems. Fecal analysis revealed 6 categories of food items, with gastropods, crabs, and bivalves being the dominant food items. Multivariate analysis revealed differences in food sources based on habitat more so than by terrapin size class. Our results revealed that like their counterparts in temperate salt marshes, SF terrapins consume similar prey categories but with different species and abundances comprising each category.
A head-started Kemp’s ridley sea turtle (Lepidochelys kempii) was documented nesting on South Walton Beach, Florida on 25 May 2015. This record supports the possibility that exposure to Florida waters after being held in captivity through 1–3 yrs of age during the head-starting process may have influenced future nest site selection of this and perhaps other Kemp’s ridley turtles. Such findings could have important ramifications for marine water experimentation and release site selection for turtles that have been reared in captivity.
Nest-site selection by most turtles affects the survival of females and their offspring. Although bog turtles ( Glyptemys muhlenbergii ) do not typically leave their wetlands for nesting, nest-site selection can impact hatching success and hatchling survival. Between 1974 and 2012, we monitored the fates of 258 bog turtle eggs incubated in the field and 91 eggs incubated under laboratory conditions from 11 different bogs, fens, or wetland complexes in New Jersey and Pennsylvania. Laboratory-incubated eggs exhibited the greatest hatching success (81%), but we did not detect a significant difference in hatching success between nests protected with predator excluder cages (43%) and unprotected nests (33%). However, we found significantly lower predation rates in protected nests, suggesting that while predator excluder cages successfully reduced predation, other environmental factors persisted to reduce egg survival in the field. Natural hatching success was potentially reduced by poor weather conditions, which may have resulted in embryo developmental problems, dehydration, or embryos drowning in the egg. Our results suggest that egg depredation, coupled with embryo developmental problems and infertility, are limiting factors to hatching success in our study populations. Using predator excluder cages to protect bog turtle eggs in the field, or incubating eggs in the laboratory and releasing hatchlings at original nesting areas, may be an effective conservation tool for recovering populations of this federally threatened species.
Managers making decisions may benefit from a well-informed understanding of a species' population size and trends. Given the cryptic nature and habitat characteristics of the western pond turtle ( Emys marmorata ), however, imperfect detection may be high and population estimates are frequently varied and unreliable. As a case study to investigate this issue, we used temperature dataloggers to examine turtle behavior at 2 long-term monitoring sites with different hydrological characteristics in Sequoia National Park, California, to determine if common stream-survey techniques are consistent with site-specific turtle behavior. Sycamore Creek is an intermittent stream that dries up every summer while the North Fork Kaweah River flows year-round. We found that while turtles spent most of the recorded time in the water (55% in Sycamore Creek and 82% in the North Fork Kaweah River), the timing of traditional surveys only coincided with the turtles' aquatic activity in the North Fork Kaweah River. At Sycamore Creek, turtles were most likely to be in the water at night. In contrast, failure to detect turtles in North Fork Kaweah River is likely owing to the larger size and complexity of the underwater habitat. In both streams, turtles were also more likely to be in the water in the weeks leading up to important changes in hydroperiods. Our findings illustrate the effects that differences in water permanence can have on turtle behavior within the same watershed and how phenotypic plasticity may then affect detection during surveys. Our study highlights the importance of tailoring survey practices to the site-specific behavioral traits of the target species.
Worldwide, scientists have headstarted threatened and endangered reptiles to augment depleted populations. Not all efforts have been successful. For the threatened Agassiz's desert tortoise ( Gopherus agassizii ), one challenge to recovery is poor recruitment of juveniles into adult populations, and this is being addressed through headstart programs. We evaluated 8 cohorts of juvenile desert tortoises from 1 to 8 yrs old in a headstart program at Edwards Air Force Base, California, for health, behavior, and growth. We also examined capacities of the headstart pens. Of 148 juveniles evaluated for health, 99.3% were below a prime condition index; 14.9% were lethargic and unresponsive; 59.5% had protruding spinal columns and associated concave scutes; 29.1% had evidence of ant bites; and 14.2% had moderate to severe injuries to limbs or shell. Lifetime growth rates for juveniles 1–8 yrs of age were approximately two times less than growth rates reported for wild populations. Tortoises in older cohorts had higher growth rates, and models indicated that high density in pens and burrow sharing negatively affected growth rates. Densities of tortoises in pens (205–2042/ha) were 350–3500 times higher than the average density recorded in the wild (< 1/ha) for tortoises of similar sizes. The predominant forage species available to juveniles were alien annual grasses, which are nutritionally inadequate for growth. We conclude that the headstart pens were of inadequate size, likely contained too few shelters, and lacked the necessary biomass of preferred forbs to sustain the existing population. Additional factors to consider for future reptilian headstart pens include vegetative cover, food sources, soil seed banks, and soil composition.
The nesting ecology of Apalone spinifera in large North American rivers is largely unknown despite the wide distribution of the species in these naturally dynamic ecosystems. We describe the nesting locations, timing, behavior, and habitat of A. spinifera in relation to natural and anthropogenic factors in the Missouri River. Nesting followed annual peak river stage, mostly occurred in the afternoon when air temperatures were 25°–30°C, and did not occur when human activity was nearby. Apalone spinifera nested in June in a year with average discharge (2012), but nested 20 d later in a year with a large flood event (2011). During the average discharge year, 90% of nests were found on islands, but similar proportions of nests were found on island and mainland habitats during the flood year because many islands were inundated. Nests were mostly in mixed-gravel substrates where vegetation cover was sparse or absent. Depredation occurred only after the emergence of hatchlings (∼ 60 d after nesting) and more often on nests on the mainland than on islands. Emergence rates were ∼ 1.5 times higher in the average year than the flood year, and emergence rates were higher in mixed-gravel nests than in pure-sand nests in 2011. In artificial nests, incubation temperatures averaged ∼ 4.3°C higher in mixed-gravel than in sand substrates, and freezing temperatures in winter penetrated to depths greater than the mean egg chamber depth (7.5 cm) for up to 3 wks. Therefore, incubation might be accelerated in mixed-gravel substrates. Accelerated incubation would enhance reproductive success because freezing temperatures preclude hatchlings from overwintering in nests in our study area. Mountain snowmelt-driven hydrology, coupled with the onset of freezing temperatures in autumn, might create a temporal “runoff-freeze squeeze” that limits the successful reproduction of A. spinifera in some years. However, high runoff also scoured vegetation from shorelines where A. spinifera nested in subsequent years. Natural variation in annual discharge might therefore be crucial to conservation of A. spinifera in large rivers.
We present a review and analysis of the conservation status and International Union for Conservation of Nature (IUCN) threat categories of all 360 currently recognized species of extant and recently extinct turtles and tortoises (Order Testudines). Our analysis is based on the 2018 IUCN Red List status of 251 listed species, augmented by provisional Red List assessments by the IUCN Tortoise and Freshwater Turtle Specialist Group (TFTSG) of 109 currently unlisted species of tortoises and freshwater turtles, as well as re-assessments of several outdated IUCN Red List assessments. Of all recognized species of turtles and tortoises, this combined analysis indicates that 20.0% are Critically Endangered (CR), 35.3% are Critically Endangered or Endangered (CR+EN), and 51.9% are Threatened (CR+EN+Vulnerable). Adjusting for the potential threat levels of Data Deficient (DD) species indicates that 56.3% of all data-sufficient species are Threatened. We calculated percentages of imperiled species and modified Average Threat Levels (ATL; ranging from Least Concern = 1 to Extinct = 8) for various taxonomic and geographic groupings. Proportionally more species in the subfamily Geoemydinae (Asian members of the family Geoemydidae) are imperiled (74.2% CR+EN, 79.0% Threatened, 3.89 ATL) compared to other taxonomic groupings, but the families Podocnemididae, Testudinidae, and Trionychidae and the superfamily Chelonioidea (marine turtles of the families Cheloniidae and Dermochelyidae) also have high percentages of imperiled species and ATLs (42.9–50.0% CR+EN, 73.8–100.0% Threatened, 3.44–4.06 ATL). The subfamily Rhinoclemmydinae (Neotropical turtles of the family Geoemydidae) and the families Kinosternidae and Pelomedusidae have the lowest percentages of imperiled species and ATLs (0%–7.4% CR+EN, 7.4%–13.3% Threatened, 1.65–1.87 ATL). Turtles from Asia have the highest percentages of imperiled species (75.0% CR+EN, 83.0% Threatened, 3.98 ATL), significantly higher than predicted based on the regional species richness, due to much higher levels of exploitation in that geographic region. The family Testudinidae has the highest ATL (4.06) of all Testudines due to the extinction of several species of giant tortoises from Indian and Pacific Ocean islands since 1500 CE. The family Testudinidae also has an ATL higher than all other larger polytypic families (≥ 5 species) of Reptilia or Amphibia. The order Testudines is, on average, more imperiled than all other larger orders (≥ 20 species) of Reptilia, Amphibia, Mammalia, or Aves, but has percentages of CR+EN and Threatened species and an ATL (2.96) similar to those of Primates and Caudata (salamanders).
Noninvasive fecal genotyping can be a useful tool for population monitoring of elusive species. We tested extraction protocols on scat samples from the threatened Mojave Desert tortoise, Gopherus agassizii, to evaluate whether scat-based mark–recapture and population genetic monitoring studies are feasible.We extracted DNA from G. agassizii scat samples collected in California and Nevada using several extraction protocols and evaluated the reliability of resulting genotypes using quality scores, maximum likelihood reliability estimates, and paired scat and blood genotypes from the same individuals. Finally, we assessed probabilities of identity and sibship, and locus amplification quality, and calculated genotyping error rates for 19 microsatellite loci to determine the best set of loci to use with G. agassizii scat extractions. We found that genotype quality depended more on the sample quality than on the extraction method, and that the Qiagen DNeasy Plant Mini extraction kit is an efficient method for extracting tortoise DNA from tortoise scat. We identified 6 G. agassizii microsatellite loci that can be used to generate a unique molecular tag for individual tortoises. We characterized the reliability of an additional 13 microsatellite loci for use in population genetic analyses where additional power at the expense of some increase in error may be advantageous. As proof of concept, with very low error rates, we matched 3 opportunistically collected scat samples to blood genotypes from animals captured during population surveys within the study area and discovered at least 3 new individuals, even after 2 yrs of extensive survey work. These results suggest that genotyping of field-collected scat can complement existing methods used in long-term demographic and movement studies of G. agassizii and other, closely related, tortoise species.
Despite its importance to individual fitness and population dynamics, the dispersal behaviors of most neonate freshwater turtles after nest emergence are poorly known. We studied the initial dispersal tendencies of neonate Ouachita map turtles ( Graptemys ouachitensis ) exiting natural nests during 2015–2017 along the Wisconsin River, Wisconsin. Overall, dispersal was nonrandom, and hatchlings largely oriented toward the nearest substantial vegetative cover, a woodland north of the nesting area. However, variation sometimes occurred in routes taken among hatchlings within a clutch. Directional changes within an individual's dispersal track, including route reversals, were also observed. As our work appears to be the first to use standalone trail cameras as a primary data-gathering tool for a hatchling dispersal study, it highlights the potential benefits and limitations of this technique for similar research.
Dermatemys mawii is a critically endangered freshwater turtle endemic to Central America. In the wild, these turtles are thought to be wholly herbivorous as adults and feed on a variety of vegetation; however, no studies have quantitatively assessed potential dietary differences based on biotic and abiotic factors. The purpose of our study was to describe and quantify the wild diet of D. mawii and assess differences based on habitat, maturity, and sex. We evaluated the stomach contents of 66 turtles legally harvested by local hunters for personal consumption throughout the country of Belize. Percent volume (by displacement) and percent frequency of each stomach item were used to calculate an index of relative importance (IRI). One algal and 6 plant families contributed to an overall diet composition consisting of leaves, flowers, stems, seedpods, seeds, and fruit. Rocks and invertebrates were also consumed, although we believe these to be incidental consumption. The leaves of the riparian tree Inga edulis were present in 73.1% of turtle stomachs and accounted for almost half of the total volume of all stomach contents combined. We used Spearman rank correlation coefficients to test the null hypothesis that there was no correlation in the rankings of stomach items (i.e., there were differences) when comparing turtles by habitat, age, and sex. There were significant differences in the ranking of food items between river and lagoon habitats, with lagoon turtles relying heavily on the algae Nitella sp.; however, the stomach contents from both habitats were equally diverse (H rivers = 1.68, H lagoons = 1.64). There were no differences in IRIs between adults and juveniles or between males and females. Our results emphasize the importance of habitat in D. mawii diet selection and the importance of leaves from riparian plants species that are shed into their aquatic habitats.