Amphibians and agricultural chemicals: Review of the risks in a complex environment

Agricultural landscapes, although often highly altered in nature, provide habitat for many species of amphibian. However, the persistence and health of amphibian populations are likely to be compromised by the escalating use of pesticides and other agricultural chemicals. This review examines some of the issues relating to exposure of amphibian populations to these chemicals and places emphasis on mechanisms of toxicity. Several mechanisms are highlighted, including those that may disrupt thyroid activity, retinoid pathways, and sexual differentiation. Special emphasis is also placed on the various interactions that may occur between different agro-chemicals and between chemicals and other environmental factors. We also examine the indirect effects on amphibian populations that occur when their surrounding pond communities are altered by chemicals.     

Crown condition dynamics of oak in southern Sweden 1988’999

Crown defoliation of oak (Quercus robur and Q. petraea) was analysed in 808 trees during three forest condition surveys (1988, 1993, and 1999) in the southern Sweden. From 1988 to 1999 crown defoliation increased by more than 20%. Changes in crown defoliation were related to the pH in the upper 20–30 cm of the mineral soils, which was closely connected to other measures of soil fertility (cation exchange capacity, CEC and C/N ratio). Trees growing on soils with a high pH (≥4.00, in BaCl₂ filtrate), high CEC and low C/N ratio had significantly lower crown defoliation than trees growing on more acid soils (pH <4.00), indicating that less favourable soil conditions may further enhance oak decline. Age did not differentiate trees with respect to crown defoliation, indicating that decline in crown condition was not due to an age-related increase in crown transparency. Considering only trees younger than 100 years, a significant interaction was observed between changes in crown defoliation and soil pH. Trees younger than 100 years old growing on more acidic soils had a greater increase in crown transparency than trees on more basic soils between 1988 and 1999. Trees ≥100 years old had significantly higher defoliation on more acidic than on more basic soils, however defoliation dynamics of these trees over 1988–99 was not related to soil acidity. Two biotic agents (insect and fungal leaf infections) evaluated in this study did not prove to be important drivers of defoliation dynamics.     

Adaptation to osmotic stress provides protection against ammonium nitrate in Pelophylax perezi embryos

The negative effects of pollution on amphibians are especially high when animals are additionally stressed by other environmental factors such as water salinity. However, the stress provoked by salinity may vary among populations because of adaptation processes. We tested the combined effect of a common fertilizer, ammonium nitrate (0-90.3 mg N-NO₃NH₄/L), and water salinity (0-2‰) on embryos of two Pelophylax perezi populations from ponds with different salinity concentrations. Embryos exposed to the fertilizer were up to 17% smaller than controls. Survival rates of embryos exposed to a single stressor were always below 10%. The exposure to both stressors concurrently increased mortality rate (>95%) of embryos from freshwater. Since the fertilizer was lethal only when individuals were stressed by the salinity, it did not cause lethal effects on embryos naturally adapted to saline environments. Our results underscore the importance of testing multiple stressors when analyzing amphibian sensitivity to environmental pollution.     

Effects of mercury on behavior and performance of northern two-lined salamanders (Eurycea bislineata)

Mercury (Hg) causes a range of deleterious effects in wildlife, but little is known about its effects on amphibians. Our objective was to determine whether Hg affects performance and behavior in two-lined salamanders (Eurycea bislineata). We collected salamanders from Hg-contaminated and reference sites and assessed speed, responsiveness, and prey capture ability. Mercury concentrations were >17× higher in salamanders from the contaminated sites and were among the highest documented in amphibians. In the first, but not in the second, locomotion trial, we found a significant effect of Hg on speed and responsiveness. In the prey capture experiment, reference salamanders ate approximately twice as many prey items as the contaminated salamanders. Together, our results suggest that sublethal Hg concentrations may negatively affect salamanders by reducing their ability to successfully execute tasks critical to survival. Future work is warranted to determine whether Hg has other sublethal effects on salamanders and whether other amphibians are similarly affected.     

Environmental Effects of Aquifer Overexploitation: A Case Study in the Highlands of Mexico

There are several environmental processes occurring under aquifer overexploitation conditions. These processes include groundwater table decline, subsidence, attenuation and drying of springs, decrease of river flow, and increased pollution vulnerability, among others processes. Some of these effects have been observed on the Upper Basin of the Lerma River. The Lerma River begins in the SE of the Valley of Toluca at 2,600 m asl, in the wetland known as Lagoons of Almoloya del Río. This wetland is made up of a group of lagoons, which are an important aquatic system from an environmental point of view. The water inflow of this wetland is a discharge of springs, which occur between the fractured volcanic material of the mountain range and granular volcanic–continental deposits of the Valley of Toluca aquifer. The intensive exploitation of the Valley of Toluca aquifer to supply urban and industrial water to Mexico City and Toluca began in 1950 and is responsible for a steady decline of piezometric levels of 1–3.5 m/yr. Other effects of this exploitation—the drying of the wetland, the decrease of river flow and the land subsidence—caused serious ecological and social impacts. The authorities declared this aquifer as overexploited in order to reduce the exploitation and preserve the availability of water resources in this important region.     

Effects of Amphibian Chytrid Fungus on Individual Survival Probability in Wild Boreal Toads

Abstract: Chytridiomycosis is linked to the worldwide decline of amphibians, yet little is known about the demographic effects of the disease. We collected capture–recapture data on three populations of boreal toads (Bufo boreas [Bufo = Anaxyrus]) in the Rocky Mountains (U.S.A.). Two of the populations were infected with chytridiomycosis and one was not. We examined the effect of the presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis [Bd]; the agent of chytridiomycosis) on survival probability and population growth rate. Toads that were infected with Bd had lower average annual survival probability than uninfected individuals at sites where Bd was detected, which suggests chytridiomycosis may reduce survival by 31–42% in wild boreal toads. Toads that were negative for Bd at infected sites had survival probabilities comparable to toads at the uninfected site. Evidence that environmental covariates (particularly cold temperatures during the breeding season) influenced toad survival was weak. The number of individuals in diseased populations declined by 5–7%/year over the 6 years of the study, whereas the uninfected population had comparatively stable population growth. Our data suggest that the presence of Bd in these toad populations is not causing rapid population declines. Rather, chytridiomycosis appears to be functioning as a low‐level, chronic disease whereby some infected individuals survive but the overall population effects are still negative. Our results show that some amphibian populations may be coexisting with Bd and highlight the importance of quantitative assessments of survival in diseased animal populations.     

Limb Deformities as an Emerging Parasitic Disease in Amphibians: Evidence from Museum Specimens and Resurvey Data

Abstract:   Widespread reports of malformed amphibians are of growing conservation concern. Although accounts of mass malformations (>5%) in North American amphibian populations date back to the 1940s, they are often poorly documented and are rarely explained. We reviewed available information for nine historical accounts from California, Colorado, Idaho, Mississippi, Montana, Ohio, and Texas reported between 1946 and 1988. We then asked the following questions: (1) Which of these cases were associated with Ribeiroia (Trematoda: Digenea) infection? (2) Are malformations still occurring at these sites? And (3) if so, have the frequency or types of abnormalities changed? Each site was resurveyed between 1999 and 2002, and original voucher specimens were redescribed and examined for trematode infection. Direct identification and classification by discriminant function analysis indicated that historical malformations at six of eight sites were associated with infection by Ribeiroia , dating back as far as 1946. Malformations recorded historically at these sites were consistent with the documented effects of Ribeiroia infection, including extra limbs, cutaneous fusion, and bony triangles. Of the six sites that still supported amphibians upon resurvey, three continued to support severe limb malformations at frequencies of 7–50% in one or more species. Although no pesticides were detected, amphibians from each of these sites were infected with Ribeiroia metacercariae. Taken together, these results suggest that Ribeiroia infection has historically been an important cause of mass malformations in amphibians. We conclude that although parasite-induced malformations are not a new phenomenon, there is qualitative evidence suggesting that their prevalence has increased recently, and we highlight the need for long-term research to evaluate the impacts of malformations on amphibian population viability.     

Monitoring Change in Vertebrate Abundance: the Living Planet Index

Abstract:  The task of measuring the decline of global biodiversity and instituting changes to halt and reverse this downturn has been taken up in response to the Convention on Biological Diversity's 2010 target. It is an undertaking made more difficult by the complex nature of biodiversity and the consequent difficulty in accurately gauging its depletion. In the Living Planet Index, aggregated population trends among vertebrate species indicate the rate of change in the status of biodiversity, and this index can be used to address the question of whether or not the 2010 target has been achieved. We investigated the use of generalized additive models in aggregating large quantities of population trend data, evaluated potential bias that results from collation of existing trends, and explored the feasibility of disaggregating the data (e.g., geographically, taxonomically, regionally, and by thematic area). Our results show strengths in length and completeness of data, little evidence of bias toward threatened species, and the possibility of disaggregation into meaningful subsets. Limitations of the data set are still apparent, in particular the dominance of bird data and gaps in tropical-species population coverage. Population-trend data complement the longer-term, but more coarse-grained, perspectives gained by evaluating species-level extinction rates. To measure progress toward the 2010 target, indicators must be adapted and strategically supplemented with existing data to generate meaningful indicators in time. Beyond 2010, it is critical a strategy be set out for the future development of indicators that will deal with existing data gaps and that is intricately tied to the goals of future biodiversity targets.     

Estimating the Density of Honeybee Colonies across Their Natural Range to Fill the Gap in Pollinator Decline Censuses

Abstract: Although pollinator declines are a global biodiversity threat, the demography of the western honeybee (Apis mellifera) has not been considered by conservationists because it is biased by the activity of beekeepers. To fill this gap in pollinator decline censuses and to provide a broad picture of the current status of honeybees across their natural range, we used microsatellite genetic markers to estimate colony densities and genetic diversity at different locations in Europe, Africa, and central Asia that had different patterns of land use. Genetic diversity and colony densities were highest in South Africa and lowest in Northern Europe and were correlated with mean annual temperature. Confounding factors not related to climate, however, are also likely to influence genetic diversity and colony densities in honeybee populations. Land use showed a significantly negative influence over genetic diversity and the density of honeybee colonies over all sampling locations. In Europe honeybees sampled in nature reserves had genetic diversity and colony densities similar to those sampled in agricultural landscapes, which suggests that the former are not wild but may have come from managed hives. Other results also support this idea: putative wild bees were rare in our European samples, and the mean estimated density of honeybee colonies on the continent closely resembled the reported mean number of managed hives. Current densities of European honeybee populations are in the same range as those found in the adverse climatic conditions of the Kalahari and Saharan deserts, which suggests that beekeeping activities do not compensate for the loss of wild colonies. Our findings highlight the importance of reconsidering the conservation status of honeybees in Europe and of regarding beekeeping not only as a profitable business for producing honey, but also as an essential component of biodiversity conservation.     

Climate Change,Multiple Stressors,and the Decline of Ectotherms

Climate change is believed to be causing declines of ectothermic vertebrates, but there is little evidence that climatic conditions associated with declines have exceeded critical (i.e., acutely lethal) maxima or minima, and most relevant studies are correlative, anecdotal, or short‐term (hours). We conducted an 11‐week factorial experiment to examine the effects of temperature (22 °C or 27 °C), moisture (wet or dry), and atrazine (an herbicide; 0, 4, 40, 400 μg/L exposure as embryos and larvae) on the survival, growth, behavior, and foraging rates of postmetamorphic streamside salamanders (Ambystoma barbouri), a species of conservation concern. The tested climatic conditions were between the critical maxima and minima of streamside salamanders; thus, this experiment quantified the long‐term effects of climate change within the noncritical range of this species. Despite a suite of behavioral adaptations to warm and dry conditions (e.g., burrowing, refuge use, huddling with conspecifics, and a reduction in activity), streamside salamanders exhibited significant loss of mass and significant mortality in all but the cool and moist conditions, which were closest to the climatic conditions in which they are most active in nature. A temperature of 27 °C represented a greater mortality risk than dry conditions; death occurred rapidly at this temperature and more gradually under cool and dry conditions. Foraging decreased under dry conditions, which suggests there were opportunity costs to water conservation. Exposure to the herbicide atrazine additively decreased water‐conserving behaviors, foraging efficiency, mass, and time to death. Hence, the hypothesis that moderate climate change can cause population declines is even more plausible under scenarios with multiple stressors. These results suggest that climate change within the noncritical range of species and pollution may reduce individual performance by altering metabolic demands, hydration, and foraging effort and may facilitate population declines of amphibians and perhaps other ectothermic vertebrates. Cambio Climático, Estresantes Múltiples y la Declinación de Ectotermos