Terrestrial Life Stages Research Articles

Upland Habitat Quality and Historic Landscape Composition Influence Genetic Variation of a Pond-Breeding Salamander

Understanding the temporal and spatial scale at which habitat alteration impacts populations is important for conservation and management. Amphibians have declined more than other vertebrates, and pond-breeding species are particularly susceptible to habitat loss and fragmentation because they have terrestrial and aquatic life stages. One approach to management of pond-breeding species is protection of core upland habitat surrounding the breeding pond. We used genetic variation as an indicator of population status in a common amphibian species, spotted salamanders (Ambystoma maculatum), to determine how amount of suitable upland habitat relates to population status in the greater Charlotte, North Carolina, USA metropolitan area. We developed candidate models to evaluate the relative influence of historical and contemporary forested habitat availability on population genetic variation at two spatial scales of upland area (164 m and 2000 m) at four time intervals over the past seven decades (1938, 1978, 1993, 2005). We found that historical land cover best predicted contemporary allelic richness. Inbreeding coefficient and observed heterozygosity were not effectively predicted by forest cover at either spatial or temporal scales. Allelic richness was best predicted at the smaller spatial scale in the 1993 time interval. Predicting and understanding how future landscape configuration affects genetic variation of common and rare species is imperative for the conservation of amphibian and other wildlife populations.

Glyphosate applications on arable fields considerably coincide with migrating amphibians

Glyphosate usage is increasing worldwide and the application schemes of this herbicide are currently changing. Amphibians migrating through arable fields may be harmed by Glyphosate applied to field crops. We investigated the population-based temporal coincidence of four amphibian species with Glyphosate from 2006 to 2008. Depending on a) age- and species-specific main migration periods, b) crop species, c) Glyphosate application mode for crops, and d) the presumed DT50 value (12 days or 47 days) of Glyphosate, we calculated up to 100% coincidence with Glyphosate. The amphibians regularly co-occur with pre-sowing/pre-emerging Glyphosate applications to maize in spring and with stubble management prior to crop sowing in late summer and autumn. Siccation treatment in summer coincides only with early pond-leaving juveniles. We suggest in-depth investigations of both acute and long-term effects of Glyphosate applications on amphibian populations not only focussed on exposure during aquatic periods but also terrestrial life stages.

Terrestrial pesticide exposure of amphibians: An underestimated cause of global decline?

Amphibians, a class of animals in global decline, are present in agricultural landscapes characterized by agrochemical inputs. Effects of pesticides on terrestrial life stages of amphibians such as juvenile and adult frogs, toads and newts are little understood and a specific risk assessment for pesticide exposure, mandatory for other vertebrate groups, is currently not conducted. We studied the effects of seven pesticide products on juvenile European common frogs (Rana temporaria) in an agricultural overspray scenario. Mortality ranged from 100% after one hour to 40% after seven days at the recommended label rate of currently registered products. The demonstrated toxicity is alarming and a large-scale negative effect of terrestrial pesticide exposure on amphibian populations seems likely. Terrestrial pesticide exposure might be underestimated as a driver of their decline calling for more attention in conservation efforts and the risk assessment procedures in place do not protect this vanishing animal group.

Toxicity of pesticides to aquatic and terrestrial life stages of amphibians and occurrence, habitat use and exposure of amphibian species in agricultural environments

The aim of this study was to provide EFSA with information relating to assessment of the risk to amphibians posed by pesticide exposure. In the first part of the study the European amphibian species associated with agricultural habitats were identified with the aim of collating information for representative species such as body size and life-cycle. Also collated were the results of studies of amphibians in European agricultural habitats to provide information on activity in areas where they may be at risk of exposure to pesticides. Several studies of the use of agricultural habitats were found providing information on migration distances and associations with particular crops although the data is patchy. The second part of the study collated information useful to risk assessment for terrestrial habitats. Information was presented on possible assessment of dietary exposure but methods for estimating dermal exposure have not yet been developed due to lack of necessary information. Other routes of exposure such as soil ingestion and inhalation were considered but no methods specific to amphibians were found. Finally, toxicity data for both the aquatic and terrestrial stages were gathered for comparison with fish and bird/mammal data respectively. A substantial quantity of data was found for aquatic exposure and after quality assessment data for each time period were presented. Far less information was found for terrestrial amphibians and what is available is of variable quality. More information is required to allow the assesment of exposure, particularly dermal exposure and the relative toxicity of pesticides to terrestrial amphibians and other vertebrate groups.

All the better to see you with: a review of odonate color vision with transcriptomic insight into the odonate eye

Although dragonflies and damselflies (Insecta: Odonata) represent some of the most advanced visual systems among insects, odonate visual systems are not as well understood as those of model or more economically important insects. Yet, with their large and complex eyes, aquatic and terrestrial life stages, entirely carnivorous lifestyle, exceptional mating behaviors, diversity in coloration, occupancy of diverse light environments, and adult success that is completely dependent on vision, it would seem studying the visual system of Odonata at the molecular level would yield highly rewarding scientific findings related to predator/prey interactions, the physiological and molecular shifts associated with ecological shifts in light environments, and the role of vision on behavioral ecology. Here, we provide a review of odonate color vision. The first odonate opsin sequences are published using a degenerate PCR approach for both dragonfly and damselfly lineages as well as a transcriptome approach for a single species of damselfly. These genetic data are combined with electrophysiology data from odonates to examine genotype/phenotype relationships in this visual system. Using these data, we present the first insights into the evolution and distribution of the visual pigments (opsins) among odonates. The integration of molecular and behavioral studies of odonate vision will help answer long-standing questions about how sensory systems and coloration may coevolve.

Amphibians at risk? Susceptibility of terrestrial amphibian life stages to pesticides

Current pesticide risk assessment does not specifically consider amphibians. Amphibians in the aquatic environment (aquatic life stages or postmetamorphic aquatic amphibians) and terrestrial living juvenile or adult amphibians are assumed to be covered by the risk assessment for aquatic invertebrates and fish, or mammals and birds, respectively. This procedure has been evaluated as being sufficiently protective regarding the acute risk posed by a number of pesticides to aquatic amphibian life stages (eggs, larvae). However, it is unknown whether the exposure and sensitivity of terrestrial living amphibians are comparable to mammalian and avian exposure and sensitivity. We reviewed the literature on dermal pesticide absorption and toxicity studies for terrestrial life stages of amphibians, focusing on the dermal exposure pathway, that is, through treated soil or direct overspray. In vitro studies demonstrated that cutaneous absorption of chemicals is significant and that chemical percutaneous passage, P (cm/h), is higher in amphibians than in mammals. In vivo, the rapid and substantial uptake of the herbicide atrazine from treated soil by toads (Bufo americanus) has been described. Severe toxic effects on various amphibian species have been reported for field-relevant application rates of different pesticides. In general, exposure and toxicity studies for terrestrial amphibian life stages are scarce, and the reported data indicate the need for further research, especially in light of the global amphibian decline.

Do effects of mercury in larval amphibians persist after metamorphosis?

Despite widespread concern about the role of environmental contaminants in global amphibian declines, and evidence that post-metamorphic life stages contribute disproportionately to amphibian population dynamics, most studies in amphibian ecotoxicology focus on larval life stages. Studies that focus solely on early life stages may miss important effects of contaminant exposure, such as latent effects that manifest some time after previous exposure. Moreover, it is often assumed that effects observed in amphibian larvae will persist to affect survival or reproduction later in life. We used terrestrial enclosures to determine whether exposure to mercury (Hg) through maternal transfer and/or larval diet had any adverse effects in post-metamorphic American toads (Bufo americanus). We found a 5% difference in size at metamorphosis that was attributed to maternal Hg exposure persisted for 1year in the terrestrial environment, resulting in a 7% difference at the conclusion of the study. Although patterns of survival differed among treatments through time, we found no overall difference in survival after 1year. We also found no evidence of emergent latent effects in the terrestrial toads that could be attributed to earlier exposure. Our results indicate that adverse effects of maternal Hg exposure that were observed in larval amphibians may persist to affect later terrestrial life stages but that no novel adverse effects developed when animals were raised in a semi-natural environment. Moreover, we found no evidence of persistent effects of dietary Hg exposure in larvae, highlighting a need for greater focus on maternal effects in amphibian ecotoxicology. Finally, we suggest an increase in the use of longitudinal studies to better understand contaminant impacts to amphibian populations via effects in both aquatic and terrestrial life stages.

Using expert opinion to prioritize impacts of climate change on sea turtles’ nesting grounds

Managers and conservationists often need to prioritize which impacts from climate change to deal with from a long list of threats. However, data which allows comparison of the relative impact from climatic threats for decision-making is often unavailable. This is the case for the management of sea turtles in the face of climate change. The terrestrial life stages of sea turtles can be negatively impacted by various climatic processes, such as sea level rise, altered cyclonic activity, and increased sand temperatures. However, no study has systematically investigated the relative impact of each of these climatic processes, making it challenging for managers to prioritize their decisions and resources. To address this we offer a systematic method for eliciting expert knowledge to estimate the relative impact of climatic processes on sea turtles’ terrestrial reproductive phase. For this we used as an example the world’s largest population of green sea turtles and asked 22 scientists and managers to answer a paper based survey with a series of pair-wise comparison matrices that compared the anticipated impacts from each climatic process. Both scientists and managers agreed that increased sand temperature will likely cause the most threat to the reproductive output of the nGBR green turtle population followed by sea level rise, then altered cyclonic activity. The methodology used proved useful to determine the relative impact of the selected climatic processes on sea turtles’ reproductive output and provided valuable information for decision-making. Thus, the methodological approach can potentially be applied to other species and ecosystems of management concern.

Survival and Breeding Frequency in Marbled Salamanders (Ambystoma opacum): Implications for Spatio-temporal Population Dynamics

Despite known population-level sensitivity to adult vital rates, there is a shortage of robust estimates of adult survival and breeding frequency for pond-breeding amphibians. Evaluating the applicability of metapopulation principles to amphibians has also been constrained by the lack of demographic studies scaled beyond individual breeding populations. We investigate spatial and temporal demographic variability among six proximate breeding populations of Marbled Salamanders (Ambystoma opacum) in western Massachusetts, USA, focusing on the terrestrial adult life stage. Between 1999 and 2004, we captured and photographed approximately 1700 breeding adults, each between one and 12 times, at drift fences encircling breeding sites. After constructing individual capture histories from field data, we applied maximum likelihood approaches to estimate parameters for survival in the pond basins during breeding periods, survival in upland habitat during breeding and non-breeding periods, and both breeding and capture probabilities. Models selected using Akaike's Information Criteria suggested that there was moderate variability in pond survival across years, but that generally, pond and upland survival varied little among populations within years. This suggests that asynchronous variability indicative of metapopulation dynamics is unlikely to be significant in the adult stage, at least among nearby populations in similar upland forests. An integrated measure of annual survival was 0.66 (SE = 0.02) for males and 0.62 (SE = 0.01) for females. Average breeding probabilities were very high (0.96; SE = 0.01) for males and high (0.67; SE = 0.02) for females, resulting in estimates of 2.5 and 2.0 lifetime breeding attempts, respectively. These parameter estimates will be used to develop spatially explicit population models to guide conservation and forest management strategies for A. opacum and other pond-breeding amphibians with similar life histories. Additional empirical work that estimates the effects of alternative management strategies on these vital rates will greatly improve the utility of these models.

Influence of Landscape Elements in Riparian Buffers on the Conservation of Semiaquatic Amphibians

Studies on riparian buffers have usually focused on the amount of land needed as habitat for the terrestrial life stages of semiaquatic species. Nevertheless, the landscape surrounding wetlands is also important for other key processes, such as dispersal and the dynamics of metapopulations. Multiple elements that influence these processes should therefore be considered in the delineation of buffers. We analyzed landscape elements (forest cover, density of roads, and hydrographic network) in concentric buffers to evaluate the scale at which they influence stream amphibians in 77 distinct landscapes. To evaluate whether our results could be generalized to other contexts, we determined whether they were consistent across the study areas. Amphibians required buffers of 100-400 m of suitable terrestrial habitat, but interspecific differences in the amount of habitat were large. The presence of amphibians was related to roads and the hydrographic network at larger spatial scales (300-1500 m), which suggests that wider buffers are needed with these elements. This pattern probably arose because these elements influence dispersal and metapopulation persistence, processes that occur at large spatial scales. Furthermore, in some cases, analyses performed on different sets of landscapes provided different results, which suggests caution should be used when conservation recommendations are applied to disparate areas. Establishment of riparian buffers should not be focused only on riparian habitat, but should take a landscape perspective because semiaquatic species use multiple elements for different functions. This approach can be complex because different landscape elements require different spatial extents. Nevertheless, a shift of attention toward the management of different elements at multiple spatial scales is necessary for the long-term persistence of populations.

Abundance patterns of dragonflies along a wetland buffer

Local abundance of animals with aquatic and terrestrial life stages may be useful to determine criteria for protective buffers around wetlands. Maiden flights and daily commutes of adult Odonata (damselflies, dragonflies) occur between wetland breeding area and adjacent upland habitat used for foraging, maturation, and nocturnal roosting. We measured abundance of dragonflies adjacent to a wetland in Mississippi, USA to determine if abundance varied with distance from water. Sexually mature males and combined females/prereproductive adult males (females-immatures) were recorded 10- 160 m from the littoral edge of a 185 ha shallow reservoir. The number of dragonflies was dominated by Celithemis eponina throughout the study period. Mean abundance did not change with distance from water out to 160 m, both for all species combined and for each of three dominant species. In the assemblage, mature males outnumbered females-immatures in the 10-40 m distance, whereas the reverse occurred in the 130-160 m distance. At the species-level, there was a mixed response in the mature male: female-immature ratio, with little resemblance to the assemblage pattern. Results of this study suggest that wide buffer zones around wetlands may be essential to protect Odonata assemblages, especially females and sexually immature adults. Furthermore, odonate flight behavior may serve as a useful bio- criterion to determine the width of ecologically significant wetland buffers.

Ecological characterization and cladocerans, calanoid copepods and large branchiopods of temporary ponds in a Mediterranean island (Sicily, southern Italy)

Temporary waters have been sporadically investigated in Sicily. These environments reflect the climatic features of the Mediterranean area with a winter ponding phase and a more or less prolonged dry period in summer. Their biota, especially those organisms strictly linked to aquatic environments and without any terrestrial life stage, have to exhibit special adaptations to survive the dry phases that are recurrent in such ecosystems. This study included more than 250 water bodies distributed on the whole Sicilian territory and on the small circum-Sicilian islands. This paper represents a first attempt to characterize Sicilian temporary waters from an ecological point of view and is mainly based on some of their limnological features and on the crustacean components of their communities. In particular, the groups which have been taken into consideration are those of cladocerans, calanoid copepods, and large branchiopods (notostracans, anostracans, and spinicaudatans).

DIETS OF NEWLY METAMORPHOSED AMPHIBIANS IN WEST TEXAS PLAYAS

Abstract Although amphibians are the dominant vertebrate inhabiting playa wetlands during spring and summer in the Southern Great Plains, little is known about their diet and role in playa trophic structure. Because new metamorphs are more numerous than other terrestrial life stages of amphibians, we describe the diets of recently ( 95%); therefore, we also examined this influence on diets of Great Plains toad metamorphs. Diets of all 3 species were dominated by coleopteran taxa, and diversity of prey taxa did not vary among species. Amount of specific prey consumed varied among species, with Great Plains toads preying more on scarab beetles and formicid ants than New Mexico spadefoots and tiger salamanders. New Mexico spadefoot metamorphs consumed more chrysomelid and elaterid beetles than tiger salama...

Fire and amphibians in North America

Information on amphibian responses to fire and fuel reduction practices is critically needed due to potential declines of species and the prevalence of new, more intensive fire management practices in North American forests. The goals of this review are to summarize the known and potential effects of fire and fuels management on amphibians and their aquatic habitats, and to identify information gaps to help direct future scientific research. Amphibians as a group are taxonomically and ecologically diverse; in turn, responses to fire and associated habitat alteration are expected to vary widely among species and among geographic regions. Available data suggest that amphibian responses to fire are spatially and temporally variable and incompletely understood. Much of the limited research has addressed short-term (1–3 years) effects of prescribed fire on terrestrial life stages of amphibians in the southeastern United States. Information on the long-term negative effects of fire on amphibians and the importance of fire for maintaining amphibian communities is sparse for the majority of taxa in North America. Given the size and severity of recent wildland fires and the national effort to reduce fuels on federal lands, future studies are needed to examine the effects of these landscape disturbances on amphibians. We encourage studies to address population-level responses of amphibians to fire by examining how different life stages are affected by changes in aquatic, riparian, and upland habitats. Research designs need to be credible and provide information that is relevant for fire managers and those responsible for assessing the potential effects of various fuel reduction alternatives on rare, sensitive, and endangered amphibian species.

PREDATOR-INDUCED LIFE-HISTORY PLASTICITY UNDER TIME CONSTRAINTS IN POOL FROGS

The mere presence of predators often decreases the growth rate of prey individuals, which devote energy and time to predator avoidance mechanisms. However, if time constraints are present, the prey individuals might be forced to neglect predators in order to grow faster. Amphibian larvae lower their activity when exposed to predators, which increases their survival probability but lowers their growth rate. I investigated how time constraints affect the growth strategies of pool frogs (Rana lessonae) in the presence and absence of caged (i.e., nonlethal) predators, and what the consequences are for their survival during the larval and the subsequent terrestrial life stage. In two outdoor experiments, I limited the available development time by delaying the hatching date, and by simulating pond drying. Tadpoles whose hatching date was experimentally delayed reduced their development and their activity less in the presence of predators than did control tadpoles. The survival consequences of caged predators was similar for early- and late-hatched tadpoles. Tadpoles exposed to falling water level increased their developmental rate compared to constant-water-level controls. In response to predators, however, tadpoles decreased activity and developmental rate, regardless of the water level treatment. Survival in treatments combining fast drying and caged predators was lower than in the other treatments. These results suggest that time constraints critically affect the role of predators in the life history of pool frogs and might change the relative importance of lethal and nonlethal predator effects on their population dynamics.

Mortality of Apatania fimbriata (Insecta: Trichoptera) during embryonic, larval and adult life stages

1. Egg masses, oviposition site preferences, and abiotic and biotic factors causing mortality during embryonic, larval and adult life stages of Apatania fimbriata were studied. Laboratory investigations provided information on the temperature dependence of embryonic development, measured as an increase in egg volume.2. A. fimbriata laid hemispherical egg masses, consisting of a transparent matrix containing a mean of 208 eggs. Egg masses were laid on stones situated just above the water surface in dark cavities in the stream bank.3. Two hundred egg masses were mapped and individually monitored during embryonic development. There was no significant correlation between mortality during embryonic development and any of the abiotic parameters measured. First‐instar larvae of Osmylus fulvicephalus consumed developing eggs, and chironomids preyed on newly hatched larvae.4. A mean of seventy‐two females emerged per metre of stream. Mortality during the 1993/94 life cycle was measured as a percentage of the potential number of eggs laid. Female mortality between emergence and oviposition was ≈ 80%. Eight per cent of individuals were lost during embryonic development. Larval mortality to emergence in 1994 was 11.3%. This indicates that the terrestrial life stage is probably decisive in the regulation of A. fimbriata populations.5. Duration of embryogenesis at constant temperatures (4–20 °C) in the laboratory was described best by a negative exponential function. This species is cold stenothermal and there was no hatching success at 20 °C.6. Egg volumes during embryonic development increased sigmoidally over time.

Behavioral and physiological responses of the terrestrial life stages of the Jefferson salamander, Ambystoma jeffersonianum, to low soil pH

Terrestrial metamorphs of the salamander, Ambystoma jeffersonianum, were exposed to four levels of pH on artificial substrates in the laboratory. Short-term exposure (7 d) to pH levels between 3.5 and 5.0 had no effect on total body mass, Na+, K+, Ca2+, and Mg2+ concentrations. However, at 14 d in both laboratory experiments and in field microcosms, whole body water and Na+ concentrations were significantly lower at the lower pH level. Terrestrial metamorphs and adults of the Jefferson salamander preferred artificial substrates that were higher in pH. Ponds not utilized for breeding all had adjacent soil pH below 3.7. Pond water and soil pH were directly and highly correlated. Soil pH may indirectly affect breeding success of Jefferson salamanders by influencing pond pH or directly by physiologically stressing the terrestrial life stages. Laboratory data implicate direct effects on the physiology of terrestrial young of the year salamanders by induction of loss of body water and Na+. Apparently, soil pH is a critical factor not only in the selection of vernal ponds by Jefferson salamander adults for breeding, but in determining the likelihood of reproductive success as judged by recruitment into the adult population.

Mortality of the terrestrial adult and aquatic nymphal life stages of Baetis vernus and Baetis rhodani in the Breitenbach, Germany (Insecta: Ephemeroptera)

SUMMARY1. The mortality of Baetis vernus Curtis and Baetis rhodani Pictet during the terrestrial‐aerial and aquatic life stages was studied at the Breitenbach near Schlitz, Hesse, Germany. The number of females emerging from the stream was recorded with emergence traps. To estimate mortality of females of both species during terrestrial life, numbers of emerging females were compared with numbers of females returning to the stream for oviposition, as shown by numbers of egg masses found in the stream.2. Mortality of female B. vernus during their terrestrial life stage was 98.8%. It was 91.2 and 96.6%, respectively, during the first and second generations of B. rhodani.3. To estimate the mortality of both sexes of B. rhodani during the aquatic life stage, the number of eggs laid by the first generation was compared with the number of adults emerging during the second generation.4. Mortality during the aquatic phase (both sexes combined) of B. rhodani was 91.1%.5. Mortality during the terrestrial life stages was at least as high, if not higher than during the aquatic stages. Evidently, there is a considerable export of organic material into the terrestrial environment around the stream. Mortality during terrestrial life may be an important regulator of population size.

Body Size and Metabolic Rate in Salamanders

Body Size and Metabolic Rate in Salamanders

Polymorphism in the Damselflies, Enallagma civile (Hagen) and E. praevarum (Hagen)

Polymorphic head color patterns are described in Enallagma civile (Hagen) and E. praevarum (Hagen). Three phenotypic classes exist in the head pattern. A dimorphic prothoracic color pattern is given for E. praevarum. These traits are shown to have similar heritability over wide environmental ranges. The phenotypes of head pattern differ in frequency between the sexes, change in frequency through selection during development to maturity, and exist as similar frequencies in successive adult generations. The latter two observations are only demonstrated for E. civile. These data suggest a balanced polymorphism having the fitness values of males and females differing in both direction and degree. The hypothesis is taken that a single gene pair determines the three head patterns expressing all three genotypes. Further field and laboratory culture comparisons support this concept. The fitness values also appear to change between an individual's aquatic and terrestrial life stages. The dimorphic prothoracic pattern of E. praevarum also differs in expression between sexes, is suggested as a single gene pair determination, and is inherited independently of head pattern.