Justin D. Congdon

Ecotoxicological Implications of Aquatic Disposal of Coal Combustion Residues In the United States: A Review

We provide an overview of research related to environmental effects of disposal of coal combustion residues (CCR) in sites in the United States. Our focus is on aspects of CCR that have the potential to negatively influence aquatic organisms and thehealth of aquatic ecosystems. We identify major issues of concern, as well as areas in need of further investigation.Intentional or accidental release of CCR into aquatic systemshas generally been associated with deleterious environmental effects. A large number of metals and trace elements are presentin CCR, some of which are rapidly accumulated to high concentrations by aquatic organisms. Moreover, a variety of biological responses have been observed in organisms following exposure to and accumulation of CCR-related contaminants. In some vertebrates and invertebrates, CCR exposure has led to numerous histopathological, behavioral, and physiological (reproductive, energetic, and endocrinological) effects. Fish kills and extirpation of some fish species have been associatedwith CCR release, as have indirect effects on survival and growth of aquatic animals mediated by changes in resource abundance or quality. Recovery of CCR-impacted sites can be extremely slow due to continued cycling of contaminants withinthe system, even in sites that only received CCR effluents forshort periods of time. The literature synthesis reveals important considerations for future investigations of CCR-impacted sites. Many studies have examined biological responses to CCR with respect to Se concentrations and accumulation because of teratogenic andreproductively toxic effects known to be associated with thiselement. However, the complex mixture of metals and traceelements characteristic of CCR suggests that biologicalassessments of many CCR-contaminated habitats should examine avariety of inorganic compounds in sediments, water, and tissuesbefore causation can be linked to individual CCR components. Most evaluations of effects of CCR in aquatic environments havefocused on lentic systems and the populations of animalsoccupying them. Much less is known about CCR effects in loticsystems, in which the contaminants may be transported downstream,diluted or concentrated in downstream areas, and accumulated bymore transient species. Although some research has examinedaccumulation and effects of contaminants on terrestrial and avianspecies that visit CCR-impacted aquatic sites, more extensiveresearch is also needed in this area. Effects in terrestrial orsemiaquatic species range from accumulation and maternal transferof elements to complete recruitment failure, suggesting that CCReffects need to be examined both within and outside of theaquatic habitats into which CCR is released. Requiring specialattention are waterfowl and amphibians that use CCR-contaminatedsites during specific seasons or life stages and are highlydependent on aquatic habitat quality during those periods.Whether accidentally discharged into natural aquatic systems or present in impoundments that attract wildlife, CCR appears topresent significant risks to aquatic and semiaquatic organisms. Effects may be as subtle as changes in physiology or as drasticas extirpation of entire populations. When examined as a whole,research on responses of aquatic organisms to CCR suggests thatreducing the use of disposal methods that include an aquaticslurry phase may alleviate some environmental risks associatedwith the waste products.

Metabolic costs incurred by crayfish (Procambarus acutus) in a trace element-polluted habitat: further evidence of similar responses among diverse taxonomic groups.

Recent studies of several vertebrates and an invertebrate have shown elevated standard metabolic rate (SMR) following chronic exposure to a mixture of trace elements in a contaminated habitat. In this study, we examined whether another invertebrate, a crayfish (Procambarus acutus), also experienced elevated SMR in response to the same contaminants. We compared SMR of individuals inhabiting the contaminated site with SMR of individuals from uncontaminated reference sites. We also examined SMR of individuals collected from the reference areas and exposed in the laboratory for 50 days to sediment and food derived from the contaminated site. Individuals collected from the contaminated site had elevated SMR compared to individuals collected from the unpolluted areas (25.1 vs. 19.2 J g(-1) day(-1)). Individuals exposed to contaminated sediment and food in the laboratory experienced elevations in SMR compared to controls after 27 days of exposure (35.2 vs. 29.4 J g(-1) day(-1)), but after 50 days of exposure, metabolic rate no longer differed between treatments. Growth of contaminant-exposed individuals was lower than growth of reference animals throughout the laboratory study. Elevated SMR associated with contaminant exposure may reflect energy-demanding mechanisms required to combat deleterious effects of contaminants. Our results support the prediction that increases in energy expenditure in the contaminated habitat would negatively influence production processes, such as growth. Results from this study in conjunction with observations from other species suggest that increased SMR is a common response among several taxa to the mixture of contaminants in the study site.

Nondestructive indices of trace element exposure in squamate reptiles

Compared with birds, mammals, fish, and even amphibians, very little is known about the effects of contaminants on reptiles. Recent evidence that many reptile populations may be declining has stimulated demand for toxicological studies of reptiles as well as development of nondestructive sampling techniques useful for assessing and monitoring contaminant exposure. The current study experimentally evaluated the utility of shed skins, tail clips, and blood samples as nondestructive indices of trace element exposure in banded water snakes, Nerodia fasciata. For 13.5 months, snakes were either fed fish from a coal ash-contaminated site or uncontaminated food from a reference site. Snakes fed contaminated prey accumulated As, Cd, Se, Sr, and V in various organs (i.e. liver, kidney, and/or gonads). Moreover, non-parametric discriminant function analysis revealed that snakes could be placed in two groups that reliably reflected their experimental diet based upon Se, Sr, and As concentrations in tail clips, blood, and/or shed skins. We suggest that nondestructive sampling techniques, particularly analyses of blood and tail clips, may be easily applied in evaluations of contaminant exposure in the field and laboratory and may prevent excessive destructive sampling of potentially threatened reptile species.

Field-testing the protandry-based mating system for the lizard, Anolis carolinesis: does the model organism have the right model?

Abstract. Using the lizard Anolis carolinensis as its subject, an early and enduring model of psychobiology was presented in which neuroendocrines and social behavior interact to coordinate reproduction between the sexes. The adaptive context for the model was protandry, here defined as a male-first emergence pattern from winter dormancy to the onset of breeding. In the protandry scenario, males emerge, become reproductive, and contest for territories. Then, pre-reproductive females emerge to settle on male territories, whereby ovarian recrudescence is facilitated by the behavior of courting males. A collateral inference of the protandry sequence is that females are choosing their future mates from among local males and their territories (i.e., intersexual selection). The model and its assumptions, though never validated by field data, have served as the paradigm for many laboratory experiments on A. carolinensis. Recently, however, field studies described an intrasexually selected mating system for A. carolinensis, without evidence of direct female choice. Differences between the selective inferences from the two perspectives led us to test in the field a number of protandry-based characteristics previously ascribed to A. carolinensis. We monitored free-ranging adults across the winter-to-breeding period using data on sex ratios, social behavior, gut contents, sex steroids, and gonadal condition. We found no evidence of protandry, and little support for any of the associated assumptions. Instead, the sexes broadly overlapped in their temporal transition from winter retreats to an active status in the habitat, with average male reproductive development about 1–2xa0weeks in advance of females. We replace the traditional protandry-based A. carolinensis paradigm with a realistic onset sequence into the breeding season and a new model for the species mating system. Our study underscores the need for field validation when laboratory-generated data are fitted to adaptive paradigms.

Assessment in contests of male lizards (Anolis carolinensis) : how should smaller males respond when size matters?

Within a female-defence polygynous mating system, males of the lizard A. carolinensis use an array of stereotyped signals and aggressive tactics to acquire and defend long-term territories containing multiple, sedentary females. In competition, body size appears to be important because size of free-ranging males correlates positively with volume of male territories and number of patrolled females. Therefore, an ability to assess body size during territorial contests should be an adaptive attribute that would influence the tactics of intermale aggression. To examine this premise, we staged contests between 10 pairs of males matched for size (i.e. symmetric contests) and 10 pairs mismatched for size (i.e. asymmetric contests), while all 20 pairs of males were matched for habitat resources, a mate, and resident status. Overall, we found (1) contest profiles best fit the features of a ‘fixed-phase, sequential assessment’ model of game theory, (2) body size and mass were highly correlated with contest outcome, (3) none of 12 signal variables predicted contest outcome, and (4) paired males generally matched aggressive tactics and signalling behaviours. We also examined the asymmetric contest profiles for deviations from the profiles of symmetric contests. We tested the proposition that smaller males of size-mismatched contests would assess their disadvantage and choose a bluff strategy to mitigate risky behaviour and avoid fighting. We found, however, that the risk-mitigation hypotheses were unsupported. Smaller males were not playing a bluff strategy, but rather a hawk strategy. They initiated risky tactics by (1) invading the habitats of their larger opponents, an act that invited retaliation, (2) showing no tendency to stay away from larger opponents, (3) maintaining high levels of aggressive signalling as encounters intensified, and (4) engaging larger opponents in physical fighting, despite losing 90% of their encounters. These empirical results support a recent game theoretical construct (‘Napoleon complex’) that models size-asymmetric contests in which smaller males initiate fights that they usually lose. Our data suggest that, if smaller males of A. carolinensis have breeding territories, then they will engage in costly contests, despite a low probability of defeating larger and equally motivated opponents.

CHAPTER 6 – Structure and Dynamics of a Turtle Community over Two Decades

Population and community levels of organization or association both depend on the success of the individuals that comprise coexisting populations that must persist if community stability is to be maintained. However, some conditions might act selectively and more severely on certain component populations than on entire communities. Documenting the short-term stability and dynamics of community components is a difficult task that requires a period of study that is by definition truly long-term and beyond the scope of a single investigators lifetime. The description of a study as long-term is usually obtained from the investigators perspective of the length of investigation, often with reference to the duration of similar studies. However, findings from the current study and from virtually all other long term studies on turtles suggest that environmental factors or intra-specific interactions are more likely to influence turtle community characteristics than the inter-specific interactions. In any case, documentation of community features among late-maturing and long-lived species is likely to become increasingly difficult because of limited opportunities for the study of natural communities unaffected by human modification.

Effects of food ration on survival and sublethal responses of lake chubsuckers (Erimyzon sucetta) exposed to coal combustion wastes

Study organisms in chronic toxicological bioassays are often provided with excessive resources to remove food limitations as a confounding experimental variable. Under more ecologically realistic situations, resources are often less abundant and such restrictions may alter the responses of organisms to environmental contaminants. Here, we investigated the interaction between resource level and sediment toxicity in the lake chubsucker, Erimyzon sucetta. For 78 days we fed fish one of three ration levels (1X, 2X, 4X; uncontaminated food) that was grazed directly from either clean sand or coal ash-contaminated sediments. Despite provision of uncontaminated food, fish exposed to the contaminated sediments accumulated significant whole body concentrations of As, Se, Sr, and V. Food ration affected the pattern of Se accumulation, with lowest concentrations accumulated by fish supplied with the lowest rations (1X). Paradoxically, fish in the 1X-ash treatment were most adversely effected by ash-exposure, despite having Se burdens much lower than fish in the 2X- and 4X-ash treatments. Fish in the 1X-ash treatment exhibited higher mortality, lower proportional growth, and increased incidence of fin erosion compared to fish provided with higher rations. Such results may, in part, be explained by the apparent inability of fish with reduced rations to maintain positive energy balance, as evidenced by their higher standard metabolic rates compared to control fish fed similar rations. Our results underscore the importance of considering resource quantity and nutritional factors in chronic bioassays in order to draw more ecologically realistic conclusions about contaminant effects.

ANNUAL DIFFERENCES IN FEMALE REPRODUCTIVE SUCCESS AFFECT SPATIAL AND COHORT-SPECIFIC GENOTYPIC HETEROGENEITY IN PAINTED TURTLES

Long‐term ecological data were used to evaluate the relative importance of movements, breeding structure, and reproductive ecological factors to the degree of spatial and age‐specific variation in genetic characteristics of painted turtles (Chrysemys picta) on the E. S. George Reserve in southeastern Michigan. Estimates of the degree of spatial genetic structuring were based on the proportion of total genotypic variance partitioned within and between subpopulations (inferred from hierarchical F‐statistics based on variation at 18 protein loci), and in terms of gene correlations (co‐ancestry among individuals derived from reproductive data on full‐sib families of females nesting at specific nesting areas). Little variation in allele frequency was observed among turtles from different marshes (Fmt = 0.003), though significant variation was observed among turtles from different nesting areas associated with each marsh (Fnm = 0.046). Gene correlations among individuals within nesting areas varied greatly over years (0.032‐0.171; mean = 0.069) and were negatively correlated to the proportion of females that successfully nested during each year. General concordance between independent estimates of genotypic correlations (i.e., Fnm derived from protein electrophoretic variation vs. mean co‐ancestry) suggests that allozyme data, when collected over spatial scales consistent with species behavioral characteristics and reproductive ecology, may accurately reflect the apportionment of gene diversity within and among subpopulations. The magnitude and patterning of allelic variation among nesting areas and individuals appears to be primarily a function of gametic correlations among members of full‐sib families, irrespective of the degree of gene flow or female nesting‐site fidelity. Comparisons of genetic characteristics among 11 cohorts (1974‐1984) revealed that heterozygosity (H) and inbreeding coefficients (F) varied greatly. Cohort estimates of H and F were correlated to female nesting success and to estimates of co‐ancestry for the same years. Results clearly reflect the concomitant importance of ecological factors (principally the proportion of the female population that successfully produce offspring during each year) in determining the magnitude and patterning of gene correlations within and among groups, and to the genotypic composition of offspring born during each year.

Egg Components and Hatchling Lipid Reserves: Parental Investment in Kinosternid Turtles from the Southeastern United States

We measured egg components and pre-ovulatory parental investment in kinosternid turtles (Kinosternon baurii, Kinosternon subrubrum, Sternotherus minor, and Sternotherus odoratus) from the southeastern USA. Allocation patterns were determined by comparing lipid content of eggs and hatchlings, to determine whether females of species with hatchlings that exhibit a delayed nest-emergence strategy: (1) allocate higher proportions of energy storage lipids to eggs, (2) produce hatchlings with higher levels of storage lipids, and (3) have higher levels of pre-ovulatory parental investment in comparison to species whose hatchlings exhibit immediate emergence. Whereas total non-polar lipid (NPL) proportions by dry mass of eggs varied significantly among species, NPL proportions of hatchlings were not significantly different. Pre-ovulatory parental investment in care (proportion of hatchling NPL to egg NPL) was 40, 50, and 55% for K. subrubrum, S. minor, and S. odoratus, respectively. Lipid class composition of eggs and hatchlings was studied to distinguish lipids allocated for energy storage from those allocated to other functions. For both eggs and hatchlings, individual lipid classes (triacylglycerol, triacylglycerol fatty acid, cholesterol, cholesterol ester, and phospholipid) as proportions of total lipid, were similar among species. The major lipid class component of eggs and hatchlings of all species was triacylglycerol (> 83%), an energy storage lipid. Substantial changes in lipid classes during embryogenesis were similar among species and included: (1) depletion of triacylglycerol, (2) increase in cholesterol esters, and (3) changes in phospholipid composition. Incubation time varied significantly among species, and appeared to be responsible for differential energy utilization during embryogenesis. Our results are inconsistent with the previously observed pattern that hatchlings exhibiting a delayed nest-emergence strategy are allocated higher proportions of energy storage lipids than those that exhibit immediate emergence. However, because the species that overwinters in the nest (K. subrubrum) hatches approximately 40 days later than the species that typically does not (S. odoratus), hatchling K. subrubrum may contain higher non-polar lipid proportions than hatchling S. odoratus during similar winter time periods. Kinosternid hatchlings contain enough stored lipids to support basal maintenance costs for substantial time periods. We suggest that such reserves may be critical to hatchling survival during a period of negative energy balance, regardless of nest emergence strategy.

Indeterminate growth in long-lived freshwater turtles as a component of individual fitness

Although evidence that reptiles exhibit indeterminate growth remains equivocal and based on inadequate data, the assumption that they do is still widely accepted as a general trait of reptiles. We examined patterns of variation in adult growth using long-term mark-recapture data on 13 populations of 9 species representing 3 families of freshwater turtles located in South Carolina, Michigan, and Arizona in the USA and in Ontario, Canada. Across 13 study populations, growth rates of all adults and only those that grew averaged 1.5 and 1.9xa0mm/yr respectively. Sources of variation in growth rates included species, population, sex, age, and latitude. Most adults of both sexes with recapture intervals greater than 10xa0years grew, but across all populations an average of 19xa0% of individuals did not grow (some with recapture intervals up to 30xa0years). For known-age adults of three species, the highest growth rates occurred during the 10xa0years following sexual maturity, and the proportions of non-growing individuals increased with age. Growth rates of adults were on average 92xa0% lower than those of juveniles. Based on linear relationships of clutch size and body size of females at average juvenile and adult growth rates it would take 0.7 (0.2–1.2) years and 8.6 (min–maxxa0=xa02.3–18.5) years, respectively, to grow enough to increase clutch size by one egg. The majority of within population variation in adult body size in 3 species appeared to be a combination of differences in ages at maturity and juvenile and early adult growth, rather than indeterminate growth. The results from our study populations indicate that increases in body size (and associated reproductive output) that results from indeterminate growth are not substantial enough to represent a major factor in the evolution of life histories in general or the evolution of longevity and aging specifically.