Brian C. Bock

Population genetics of the endangered South American freshwater turtle, Podocnemis unifilis, inferred from microsatellite DNA data

We studied the population genetics of Podocnemis unifilis turtles within and among basins in the Orinoco and Amazon drainages using microsatellites. We detected high levels of genetic diversity in all sampled localities. However, ‘M-ratio’ tests revealed a substantial recent population decline in ten localities, in accord with current widespread exploitation. Our results reveal a consistent pattern across multiple analyses, showing a clear subdivision between the populations inhabiting the Amazon and Orinoco drainages despite a direct connection via the Casiquiare corridor, and suggesting the existence of two biogeographically independent and widely divergent lineages. Genetic differentiation followed an isolation-by-distance model concordant with hypotheses about migration. It appears that migration occurs via the flooded forest in some drainages, and via river channels in those where geographic barriers preclude dispersal between basins or even among nearby tributaries of the same basin. These observations caution against making generalizations based on geographically restricted data, and indicate that geographically proximate populations may be demographically separate units requiring independent management.

A Comparison of Maternal and Temperature Effects on Sex, Size, and Growth of Hatchlings of the Magdalena River Turtle (Podocnemis lewyana) Incubated under Field and Controlled Laboratory Conditions

Abstract During two nesting seasons we monitored 19 naturally incubated nests of Podocnemis lewyana obtained from two sites in the Mompos Depression of northern Colombia. We incubated another nine nests in the laboratory under similar humidity conditions, but at six different temperatures. We sexed the hatchlings obtained from all nests to confirm for the first time the occurrence of temperature-dependent sex determination in this species and quantify sex ratios and the pivotal temperature for this population. In both nesting seasons, the majority of the nests in the field produced hatchlings of both sexes, but sex ratios differed between study beaches/years. The pivotal temperature documented (33.4°C) appears to be among the highest reported for a turtle species. Incubation conditions in the naturally incubated nests also influenced hatching success rates and incubation periods, but not hatchling size or weight. Hatchlings obtained from the nests incubated in the laboratory were reared for one month in order to study the influence of pre-hatching factors on growth rates. In these nests we documented maternal effects on egg size, initial hatchling size, and weight and growth rates. Incubation temperature also influenced hatching success rates, sex ratios, growth rates, and hatchling size, but not hatchling weight.

Distribution and Status of Podocnemis lewyana in the Magdalena River Drainage of Colombia

ABSTRACT We obtained evidence of the continued presence of Podocnemis lewyana in 18 different sites within the Magdalena River drainage of northern Colombia. However, abundances at most sites were low, even in areas where the species had previously been reported as common. Although hunting of adults is no longer commercially viable, local people consume individuals that are captured incidentally while fishing. Hunting of eggs during the incubation period each year continues to be intensive. Turtle abundances were negatively related to human densities throughout this area. In the Chicagua River, where turtle abundances were highest, we conducted standardized shoreline censuses of basking adults and documented abundances of approximately 6 individuals/km2. Turtles often basked on mud banks, beaches, or emergent logs in aggregations made up of all size classes. Pilot trapping efforts also succeeded in capturing all size classes of turtles, which suggests that more intensive monitoring programs would be feasible. Given the evidence of declines in most areas of the range of this species, the current lack of regulation of its exploitation, and the projections for continued human population growth in this area, we recommend its International Union for Conservation of Nature (IUCN) status be changed from Endangered to Critically Endangered (CR A2acd).

Application of the micronucleus test and comet assay in Trachemys callirostris erythrocytes as a model for in situ genotoxic monitoring

Trachemys callirostris is a turtle species endemic to northern South America. In northern Colombia it occurs in the middle and lower Magdalena River drainage and its principal tributaries (lower Cauca and San Jorge rivers) and in other minor drainages such as the lower Sinú River. In recent years, industrial, agricultural, and mining activities have altered natural habitats in Colombia where this species occurs, and many of the pollutants released there are known to induce genetic alterations in wildlife species. The micronucleus test and comet assay are two of the most widely used methods to characterize DNA damage induced by physical and chemical agents in wildlife species, but have not been employed previously for genotoxic evaluations in T. callirostris. The goal of this study was to optimize these genotoxic biomarkers for T. callirostris erythrocytes in order to establish levels of DNA damage in this species and thereby evaluate its potential as a sentinel species for monitoring genotoxic effects in freshwater environments in northern Colombia. Both genotoxic techniques were applied on peripheral blood erythrocytes from 20 captive-reared T. callirostris individuals as a negative control, as well as from samples obtained from 49 individuals collected in Magangué (Magdalena River drainage) and 24 individuals collected in Lorica (Sinú River drainage) in northern Colombia. Negative control individuals exhibited a baseline frequency of micronuclei of 0.78±0.58 and baseline values for comet tail length and tail moment of 3.34±0.24µm and 10.70±5.5, respectively. In contrast, samples from both field sites exhibited significantly greater evidence of genotoxic effects for both tests. The mean MN frequencies in the samples from Magangué and Lorica were 8.04±7.08 and 12.19±12.94, respectively. The mean tail length for samples from Magangué and Lorica were 5.78±3.18 and 15.46±7.39, respectively. Finally, the mean tail moment for samples from Magangué and Lorica were 23.59±18.22 and 297.94±242.18, respectively. The frequency of micronuclei in the samples was positively related to comet tail length and tail moment. Thus, this study showed that both genotoxicity biomarkers may be applied to T. callirostris erythrocytes as a sentinel organism for assessing the effects of environmental pollutants in freshwater ecosystems in northern South America.

Preovulatory Maternal Effects on Intra- and Interpopulation Variation in Sex Ratios and Phenotypic Characteristics of Magdalena River Turtles (Podocnemis lewyana)

Abstract:  In oviparous species, preovulatory maternal effects such as investment in yolk quantity and composition or levels of yolk steroid hormones might potentially affect hatchling body sizes, growth rates, performance, and sex in species with temperature-dependent sex determination. We investigated the effects of egg mass and levels of testosterone and 17&bgr;-estradiol in the yolk on the phenotypes of hatchling Magdalena River Turtles (Podocnemis lewyana) in three populations in the Magdalena River drainage of northern Colombia. We hypothesized that, under homogeneous incubation conditions, the differences documented among clutches would be attributable to familial effects, caused by either heritable genetic factors or preovulatory maternal effects. Eggs were incubated artificially at the pivotal temperature for the species (33.4°C) and hatchlings were reared in the laboratory for 2 mo. Two eggs from each clutch were tested for testosterone and 17&bgr;-estradiol levels. Sex ratios, hatchling size, mass, and righting times varied both between clutches within a site and between populations. Egg mass was positively related to hatchling body size and mass, both at hatching and at 2 mo of age. Levels of 17&bgr;-estradiol concentrations influenced hatching success rates and incubation periods. Sex ratios were marginally related to 17&bgr;-estradiol levels, with clutches and sites with higher levels tending to produce fewer males. Our results provide evidence that preovulatory maternal effects play a role in influencing phenotypic attributes related to hatchling survivorship such as size, growth rate, and performance, and also seem to interact with incubation temperature to determine the sex of each individual and the sex ratio of the clutch, which has implications for both parental and offspring fitness.

A Plea to Redirect and Evaluate Conservation Programs for South America’s Podocnemidid River Turtles

Abstract We review the current practices of podocnemidid turtle conservation programs in South America and summarize the direct and indirect negative consequences that some of these practices may have on the populations we are attempting to manage. We argue that programs that only focus on nest transfer and head-starting as their conservation strategies would be better served by redirecting their efforts toward the protection of subadults and adults and in conducting monitoring programs designed to evaluate the impact of their management practices. Also, we make suggestions for other ways that the management of podocnemidid populations may be improved without resorting to manipulative ex situ practices that may well do more harm than good.

Life History and Demographic Characteristics of the Magdalena River Turtle (Podocnemis lewyana): Implications for Management

We conducted a four-year study of the life history parameters of the endangered freshwater turtle Podocnemis lewyana (Testudines: Podocnemididae) in four channels connecting wetlands to the Magdalena River in northern Colombia. Using capture–mark–recapture techniques, we documented body size growth rates, sex ratios, and size class distributions, and estimated survival rates for juveniles and adults. We also used body size/clutch size and body size/track width correlations to estimate the body sizes of females that nested in beaches in the Magdalena River near the study sites. The body size at first nesting (30 cm straight-line carapace length) was comparable to the estimate obtained by inspecting the reproductive tracts of 70 females using a sonograph. Growth rate analyses showed adult males to be smaller than adult females with an estimated size at sexual maturity of 20 cm straight-line carapace length. Females begin nesting at 5–6 years of age and may lay up to four clutches annually with a mean clutch size of 22 eggs. The overall sex ratio was 1♀:0.72♂, but this parameter varied among study sites, as did size class distributions, with juveniles more abundant in the two shallower channels and adults more abundant in the two deeper channels. Survival estimates increased with increasing body sizes. We constructed a projection matrix using these estimates of the key life history parameters for this population and used an uncertainty analysis to create a distribution of possible asymptotic population growth rates (&lgr;), to estimate the vectors of stable age distribution and reproductive values, and conduct an elasticity analysis. Results indicated that the population is declining 8.8% annually, probably as a result of illegal over-exploitation of adults that are harvested as by-catch by local fishermen, and especially of reproductive females that are captured while nesting. Elasticity analyses indicated that the most effective way to help this population recover is to increase adult survival rates, since this transition alone accounted for 62% of the contribution of all vital rates to the population growth rate. Traditional management methods that rely entirely on nest transfer and head-starting will likely be of limited impact.

Population Genetics of the Slider Turtle (Trachemys scripta callirostris) in the Mompos Depression, Colombia

Abstract Allozyme analyses were conducted on samples obtained from Trachemys scripta callirostris adults harvested in the Mompos Depression of Colombia. Genetic variability was low and there was no apparent genetic structure at either the micro- or macrogeographic scale, which contrasts markedly with the results of previous studies of a Trachemys population in the southeastern United States. These results have management implications for this subspecies and also suggest the need for further studies of the population genetics and systematics of other tropical Trachemys populations.

NIVELES DE MERCURIO EN HUEVOS, EMBRIONES Y NEONATOS DE Trachemys callirostris (TESTUDINES, EMYDIDAE)

We quantified total mercury concentrations in eggshells, egg yolks, and embryos from 16 nests of the Colombian Slider (Trachemys callirostris). Nests were collected in different stages of development, but estimated time of incubation in natural substrates was not correlated with mercury levels in the eggs, suggesting that mercury was not absorbed from the substrate, but more likely passed on to the embryos during folliculogenesis by the reproductive females who had bioaccumulated the mercury from environmental sources. Mean mercury concentrations were higher in embryos than in eggshells or egg yolks, indicating that embryos also bioaccumulate mercury present in other egg tissues. Intra-clutch variation in egg yolk mercury concentrations was relatively high. Egg yolk mercury concentrations were not associated with any of the fitness proxies we quantified for the nests (hatching success rates, initial neonate sizes and first-month juvenile growth rates). After five months of captive rearing in a mercury-free laboratory environment, 86 % of the juveniles had eliminated the mercury from their tissues.

Survivorship rates of adult Anolis mariarum (Squamata: Polychrotidae) in two populations with differing mean and asymptotic body sizes

Comparamos las sobrevivencias de los adultos en dos poblaciones de la lagartija Anolis mariarum con distintos promedio y asintotas de sus tamanos corporales, para examinar una prediccion de la teoria de mortalidad especifica de edad; que las poblaciones que experimentan mayor mortalidad de los adultos deben exhibir maduracion sexual mas temprana y menores tamanos corporales en los adultos. Utilizamos la tecnica de maxima verosimilitud para evaluar diferentes modelos de sobrevivencia y una tecnica de modelopromediado para estimar sobrevivencia y probabilidades de recaptura para cada sexo y sitio. La longitud relativa de la cola no afecto las tasas de sobrevivencia de los adultos en estas poblaciones, pero el tamano corporal estuvo relacionado con la sobrevivencia, siendo los individuos mas grandes en el momento de la primera captura los que presentaron las tasas de sobrevivencia mas bajas; por lo tanto, el tamano corporal fue incluido como una covariable en algunos de los modelos examinados. Los analisis revelaron que los machos de ambos sitios presentan mayores sobrevivencias que las hembras, pero no encontramos diferencias entre los sitios entre las tasas de sobrevivencia o las probabilidades de captura para cada sexo. Aun asi, las diferencias documentadas en los tamanos corporales entre estos sitios pueden representar adaptaciones en las historias de vida ante diferentes tasas de mortalidad en las clases de edad tempranas como huevos o juveniles en cada sitio, o por otra parte puede representar un caso de plasticidad fenotipica ante diferentes condiciones ambientales, las cuales no parecen estar relacionadas con diferencias en las sobrevivencias de los adultos. Los estimativos de sobrevivencia anual (11.7% a 21.2%) fueron altos para este Anolis continental de pequeno tamano. Este es el primer reporte para el genero en que la sobrevivencia de los machos excede a la de las hembras.