Combined Effects of Atrazine and Chlorpyrifos on Susceptibility of the Tiger Salamander to Ambystoma tigrinum Virus

Several hypotheses have been examined as potential causes of global amphibian declines, including emerging infectious diseases and environmental contaminants. Although these factors are typically studied separately, animals are generally exposed to both stressors simultaneously. We examined the effects of the herbicide atrazine and the insecticide chlorpyrifos on the susceptibility of tiger salamander larvae, Ambystoma tigrinum, to a viral pathogen, Ambystoma tigrinum virus (ATV). Environmentally relevant concentrations of atrazine (0, 20, 200 μg/L) and chlorpyrifos (0, 2, 20, 200 μg/L) were used along with ATV in a fully factorial experimental design whereby individually housed, 4-week-old larvae were exposed for 2 weeks. Atrazine alone was not lethal to larvae, and chlorpyrifos alone was lethal only at the highest concentration. When combined with ATV, chlorpyrifos increased susceptibility to viral infection and resulted in increased larval mortality. A significant interactive effect between atrazine and ATV was detected. Atrazine treatments slightly decreased survival in virus-exposed treatments, yet slightly increased survival in the virus-free treatments. These findings corroborate earlier research on the impacts of atrazine, in particular, on disease susceptibility, but exhibit greater effects (i.e., reduced survival) when younger larvae were examined. This study is the first of its kind to demonstrate decreases in amphibian survival with the combination of pesticide and a viral disease. Further examination of these multiple stressors can provide key insights into potential significance of environmental cofactors, such as pesticides, in disease dynamics.     

The effects of multiple stressors on wetland communities: pesticides,pathogens and competing amphibians

1. Anthropogenic effects have propelled us into what many have described as the sixth mass extinction, and amphibians are among the most affected groups. The causes of global amphibian population declines and extinctions are varied, complex and context‐dependent and may involve multiple stressors. However, experimental studies examining multiple factors contributing to amphibian population declines are rare. 2. Using outdoor mesocosms containing zooplankton, phytoplankton, periphyton and tadpoles, we conducted a 2 × 2 × 3 factorial experiment that examined the separate and combined effects of an insecticide and the fungal pathogen Batrachochytrium dendrobatidis (Bd) on three different assemblages of larval pacific treefrogs (Pseudacris regilla) and Cascades frogs (Rana cascadae). 3. Larval amphibian growth and development were affected by carbaryl and the amphibian assemblage treatment, but only minimally by Bd. Carbaryl delayed metamorphosis in both amphibian species and increased the growth rate of P. regilla. Carbaryl also reduced cladoceran abundance, which, in turn, had positive effects on phytoplankton abundance but no effect on periphyton biomass. Substituting 20 intraspecific competitors with 20 interspecific competitors decreased the larval period but not the growth rate of P. regilla. In contrast, substituting 20 intraspecific competitors with 20 interspecific competitors had no effect on R. cascadae. Results of real‐time quantitative polymerase chain reaction (qPCR) analysis confirmed infection of Bd‐exposed animals, but exposure to Bd had no effects on either species in univariate analyses, although it had significant or nearly significant effects in several multivariate analyses. In short, we found no interactive effects among the treatments on amphibian growth and development. 4. We encourage future research on the interactive effects of pesticides and pathogens on amphibian communities.     

Effects of Turbidity and Visual vs. Chemical Cues on Anti‐Predator Response in the Endangered Fountain Darter (Etheostoma fonticola)

Altered turbidity resulting from anthropogenic stressors is a global problem. Threatened by climate change, pollution, and increased recreational usage, the streams and rivers of central Texas are no exception. The impacts of turbidity include behavioral effects as turbidity degrades visual information, which can impair an animal's ability to accurately detect and respond to a predator. Here, we tested the impact of simulated turbidity on anti‐predator response in the endangered fountain darter, Etheostoma fonticola. We examined the response of E. fonticola to four predator cue treatments (chemical, visual, chemical and visual, and no cues) using a native predator, the green sunfish (Lepomis cyanellus). All cue treatments were tested across two vision levels: clear and impaired, to simulate the visual effects of low turbidity (~30 NTU). Our results indicate that E. fonticola requires a combination of visual and chemical stimuli to respond to a native fish predator. In the absence of one or the other sensory modality, E. fonticola did not show an anti‐predator response. Also, anti‐predator response to a combination of visual and chemical stimuli was only present at the clear vision level. When vision was impaired owing to simulated turbidity, a combination of visual and chemical stimuli did not produce a significant anti‐predator response. These results indicate that blocked or compromised vision hampers anti‐predator response in E. fonticola, which may be of concern regarding the future management of this endangered species.     

Effects of cover and predator size on survival and development of Ranautricularia tadpoles

Size-limited predation is an important process during the development of many aquatic species, and mortality rates of early larval stages and small individuals can be particularly high. Structurally complex habitats can mediate predator-prey interactions and provide a potentially important mechanism for decreasing predation pressure on larvae. To determine whether structurally complex habitats mediate predation on tadpoles of the southern leopard frog (Ranautricularia), we designed a factorial experiment, crossing two levels of cover with three predator treatments (none, small, or large Trameacarolina naiads). Predator size had a larger effect on tadpole performance (survival, mass and age at metamorphosis) than did cover level, largely because small predators were ineffective. Within the large-predator treatment, however, tadpole survival was higher (78%) under high than under low cover (46%), suggesting that increased cover decreased predator foraging efficiency allowing more larvae to reach a size refuge. This study demonstrates that habitat structural complexity can play an important role in mediating predator-prey interactions, even when tadpoles start out at a size disadvantage relative to predators. Consideration of habitat structural complexity in future research should provide a more complete understanding of the role of size relationships in predator-prey systems. Received: 3 January 1997 / Accepted: 10 October 1997     

Synergistic effects of the invasive Chinese tallow (Triadica sebifera) and climate change on aquatic amphibian survival

Changes in climate and the introduction of invasive species are two major stressors to amphibians, although little is known about the interaction between these two factors with regard to impacts on amphibians. We focused our study on an invasive tree species, the Chinese tallow (Triadica sebifera), that annually sheds its leaves and produces leaf litter that is known to negatively impact aquatic amphibian survival. The purpose of our research was to determine whether the timing of leaf fall from Chinese tallow and the timing of amphibian breeding (determined by weather) influence survival of amphibian larvae. We simulated a range of winter weather scenarios, ranging from cold to warm, by altering the relative timing of when leaf litter and amphibian larvae were introduced into aquatic mesocosms. Our results indicate that amphibian larvae survival was greatly affected by the length of time Chinese tallow leaf litter decomposes in water prior to the introduction of the larvae. Larvae in treatments simulating warm winters (early amphibian breeding) were introduced to the mesocosms early in the aquatic decomposition process of the leaf litter and had significantly lower survival compared with cold winters (late amphibian breeding), likely due to significantly lower dissolved oxygen levels. Shifts to earlier breeding phenology, linked to warming climate, have already been observed in many amphibian taxa, and with most climate models predicting a significant warming trend over the next century, the trend toward earlier breeding should continue if not increase. Our results strongly suggest that a warming climate can interact with the effects of invasive plant species, in ways we have not previously considered, to reduce the survival of an already declining group of organisms.     

The non-lethal effects of predators and the influence of food availability on life history of adult Chironomus tentans (Diptera: Chironomidae)

1. We used a laboratory experiment to determine effects of a predator (other than straightforward prey consumption) and food availability, during the larval stage, on adult size, age at emergence and fecundity of Chironomus tentans. 2. Predator presence and decreased food availability resulted in reduced adult emergence. 3. Predator presence and food availability resulted in smaller size and greater age at emergence of male and female chironomids. There were no significant interactions between effects of predator presence and food availability. 4. Predator presence had no significant effect on fecundity. 5. Smaller size and greater age at emergence can have important implications for adult survival, size and age at first reproduction and, thus, intrinsic rate of population growth.     

Predators and trematode parasites jointly affect larval anuran functional traits and corticosterone levels

Non‐consumptive predator effects may have dramatic consequences for host–parasite interactions by influencing the ability of prey items to avoid, resist, or tolerate infection. Both predators and parasites can affect host traits, such as growth rates and behavior, and these effects may in part be mediated through shared physiological pathways (e.g. the glucocorticoid stress hormone, corticosterone [CORT]). Here, we examined the effects of trematode parasites (Digena: Echinostomatidae) and predator (larval odonate) exposure on larvae of two amphibian species (Rana sylvatica and R. clamitans) in laboratory experiments. First, we measured behavior and CORT responses of tadpoles exposed to predator chemical cue in combination with parasite cue or under direct exposure to parasites. We then measured the combined effects of predator cue and parasite infection on survival and traits. Evidence for effects of parasite cue in our study was equivocal, but we found novel interactive effects of parasites and predators on larval frogs. Parasites and predators had antagonistic effects on CORT, behavior, and morphology, and negative synergistic effects on development. In addition, parasite infection and predator cues additively reduced activity levels of both species and growth in wood frogs. Negative effects of parasite infection on survival and traits were dose‐dependent for both species, although wood frogs generally experienced stronger effects of infection than green frogs. Our results emphasize the importance of considering effects of parasites as well as predators, since both can have strong effects on survival and the combination can have both additive and non‐additive effects on key traits. These effects likely have important implications for amphibian population dynamics, community structure, and conservation.     

Habitat selection and consumption across a landscape of multiple predators

Predator community composition can alter habitat quality for prey by changing the strength and direction of consumptive effects. Whether predator community composition also alters prey density via nonconsumptive effects during habitat selection is not well known, but is important for understanding how changes to predator communities will alter prey populations. We tested the hypothesis that predator community composition (presence of caged trout, caged dragonflies, or caged trout + dragonflies) alters colonization of aquatic mesocosms by ovipositing aquatic insects. In a previous experiment in this system, we found a spatial contagion effect, in which insects avoided pools with predators, but only when predator‐free pools were isolated (~5 m away from predator pools). Here, we removed the isolated predator‐free pools, allowing us to test whether insects would make fine‐scale (~1 m) oviposition decisions in the absence of preferred isolated pools. We also estimated consumptive effects by allowing predators to feed on colonists for 5 days following colonization. All insects collected after 21 days were dipterans, dominated by Chironomidae. Total colonization, measured as the number of developing larvae after 21 days, was not affected by either predator presence or composition. Consumption was significant in the trout only treatment, reducing larval insect density by 46 ± 37% (mean ± SE). No other predator treatment significantly reduced prey density, although the proportion of chironomid larvae in protective cases increased in response to direct predation from dragonflies, indicating an antipredatory behavioral response. Taken together, these results reveal that predator community composition altered larval survival and behavior, but colonizing females either did not or could not assess these risks across small scales during oviposition.     

Foraging traits of native predators determine their vulnerability to a toxic alien prey

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Effects of macroalgal exudates and oxygen deficiency on survival and behaviour of fish larvae

Filamentous algae may create anoxic, i.e. oxygen free, conditions during night and fish larvae that commonly spend their first months in the littoral may therefore be subject to anoxia. We conducted two different experiments; firstly, we measured behaviour of pike larvae (Esox lucius L.), such as frequency of prey attacks and time in vegetation, in the presence of a chemical predator cue and oxygen deficiency. In the second experimental set-up, pike larval survival was monitored in water with added macro-algal exudates (excreted from Pilayella littoralis) and a low oxygen level (3 mg l^− 1). Our results showed that oxygen concentration and the chemical predator signal, caused by three-spined sticklebacks, had strong significant effects on the larval prey attacks. The prey attacks were strongly reduced at 3 mg oxygen l^− 1. However, survival of the larvae was not affected by low oxygen and macro-algal exudates. Pike larvae are very tolerant to hypoxia and exudates excreted by the littoral vegetation, whereas prey attacks are strongly decreased in hypoxia when a predator is around. This may have negative consequences for pike larval growth and recruitment in eutrophicated environments.     

Altered predator/prey behavior in polluted environments: implications for fish conservation

Predator/prey behavior has important consequences for individual survival and recruitment into fish populations, both of which can be affected by stressors such as environmental contaminants. The degree to which prey capture or predator avoidance abilities of a predator or prey species are affected will determine the direction in which the balance will be shifted. In a contaminated estuary we have studied, prey capure and predator avoidance of resident mummichogs, Fundulus heteroclitus, are impaired, which may account for individuals in that estuary having reduced growth and longevity compared with those from uncontaminated sites. Exposure to sediments, water, and grass shrimp from the contaminated site can impair the predatory abilities of mummichogs from a clean site. An important prey species, the grass shrimp, Palaemonetes pugio, has a greater population density and a greater proportion of large individuals at the polluted site, apparently because of reduced predation pressure. Mummichog larvae at the polluted site are initially more active and better at prey capture and predator avoidance than larvae from clean sites, but later they become poorer at both. Differences in predator vulnerability among larvae appear to be due to population differences in behavior, which may be due in part to both genetic and environmentally-caused factors. Conservation of fish populations should consider fish behavior and its interaction with contaminants.     

Testing a key assumption of host‐pathogen theory: density and disease transmission

Conventional disease theory suggests that extinction with density‐dependent transmission is unlikely as the threshold host density (KT) is greater than zero. Extinction may result if transmission is frequency dependent or the pathogen has an environmental reservoir. Given the importance of understanding how pathogens affect species richness and diversity there are few empirical tests of these conclusions. We used an Ambystoma tigrinum–Ambystoma tigrinum virus (ATV) model system in the laboratory to examine disease transmission dynamics. Susceptible A. tigrinum larvae were exposed to three different densities and proportions of infected larvae for 24 h. We then housed susceptible hosts individually for 28 days and monitored them for infection. The density of infected hosts to which susceptible hosts were exposed was the best predictor of infection (p=0.037). There was no effect of host clutch on the probability of becoming infected (p=0.67). Larvae in the highest density treatments died sooner than larvae in lower density treatments (p<0.001). Asymptomatic but infected hosts shed sufficient virus into the water in a 24‐h period to infect susceptible hosts without any direct contact between individuals. ATV transmission was best described by a power function, leading to the prediction that extinction of A. tigrinum as a result of this pathogen is unlikely. Indeed, field observations show that larval salamander populations that experience ATV‐driven epidemics may decrease, but not to extinction, and then recover. Disease is proposed as a possible explanation for the global decline of amphibians. Ranaviruses infect many amphibian populations, but based on our results may not be a general cause of declines to extinction. In contrast, frequency dependent transmission, environmental reservoirs and alternative hosts may be the most likely explanation for the enigmatic decline, at times to extinction, of some amphibian populations as a result of emerging infectious diseases, like the chytrid fungus Batrachochytrium dendrobatidis.     

Effects of predator treatments,individual traits,and environment on moose survival in Alaska

We studied moose (Alces alces) survival, physical condition, and abundance in a 3-predator system in western Interior Alaska, USA, during 2001–2007. Our objective was to quantify the effects of predator treatments on moose population dynamics by investigating changes in survival while evaluating the contribution of potentially confounding covariates. In May 2003 and 2004, we reduced black bear (Ursus americanus) and brown bear (U. arctos) numbers by translocating bears ≥240 km from the study area. Aircraft-assisted take reduced wolf (Canis lupus) numbers markedly in the study area during 2004–2007. We estimated black bears were reduced by approximately 96% by June 2004 and recovered to within 27% of untreated numbers by May 2007. Brown bears were reduced approximately 50% by June 2004. Late-winter wolf numbers were reduced by 75% by 2005 and likely remained at these levels through 2007. In addition to predator treatments, moose hunting closures during 2004–2007 reduced harvests of male moose by 60% in the study area. Predator treatments resulted in increased calf survival rates during summer (primarily from reduced black bear predation) and autumn (primarily from reduced wolf predation). Predator treatments had little influence on survival of moose calves during winter; instead, calf survival was influenced by snow depth and possibly temperature. Increased survival of moose calves during summer and autumn combined with relatively constant winter survival in most years led to a corresponding increase in annual survival of calves following predator treatments. Nonpredation mortalities of calves increased following predator treatments; however, this increase provided little compensation to the decrease in predation mortalities resulting from treatments. Thus, predator-induced calf mortality was primarily additive. Summer survival of moose calves was positively related to calf mass (β > 0.07, SE = 0.073) during treated years and lower (β = −0.82, SE = 0.247) for twins than singletons during all years. Following predator treatments, survival of yearling moose increased 8.7% for females and 21.4% for males during summer and 2.2% for females and 15.6% for males during autumn. Annual survival of adult (≥2 yr old) female moose also increased in treated years and was negatively (β = −0.21, SE = 0.078) related to age. Moose density increased 45%, from 0.38 moose/km² in 2001 to 0.55 moose/km² in 2007, which resulted from annual increases in overall survival of moose, not increases in reproductive rates. Indices of nutritional status remained constant throughout our study despite increased moose density. This information can be used by wildlife managers and policymakers to better understand the outcomes of predator treatments in Alaska and similar environments. © 2011 The Wildlife Society.     

Nutrient enrichment in the High Arctic associated with Thule Inuit whalers: a paleolimnological investigation from Ellesmere Island (Nunavut,Canada)

The combined influence of a pesticide (carbaryl) and a cyanotoxin (microcystin LR) on the life history of Daphnia pulicaria was investigated. At the beginning of the experiments animals were pulse exposed to carbaryl for 24 h and microcystins were delivered bound in Microcystis’ cells at different, sub-lethal concentrations (chronic exposure). In order to determine the actual carbaryl concentrations in the water LC–MS/MS was used. For analyses of the cyanotoxin concentration in Daphnia’s body enzyme-linked immunosorbent assay (ELISA) was used. Individual daphnids were cultured in a flow-through system under constant light (16 h of light: 8 h of dark), temperature (20°C), and food conditions (Scenedesmus obliquus, 1 mg of C l⁻¹). The results showed that in the treatments with carbaryl egg numbers per female did not differ significantly from controls, but the mortality of newborns increased significantly. Increasing microcystin concentrations significantly delayed maturation, reduced size at first reproduction, number of eggs, and newborns. The interaction between carbaryl and Microcystis was highly significant. Animals matured later and at a smaller size than in controls. The number of eggs per female was reduced as well. Moreover, combined stressors caused frequent premature delivery of offspring with body deformations such as dented carapax or an undeveloped heart. This effect is concluded to be synergistic and could not be predicted from the effects of the single stressors.     

Two stressors are far deadlier than one

Natural organisms often face a barrage of stressors, both natural and human induced. Two known stressors that impact amphibian populations are pesticides and predators. Recent work by Relyea and by Mills and Relyea reveals strikingly strong, synergistic negative effects of these two factors on amphibian larvae. Adding predation risk on top of supposedly sublethal concentrations of a common pesticide caused a massive increase in larval mortality. Interestingly, the increased mortality did not require exposure to actual predation. That is, simply the 'smell of danger' (predator chemical cues) caused 80-90% of larvae that were held in otherwise 'safe' levels of the pesticide to die. Notably, this effect occurred in some species, but not in others. These new studies highlight the need for further interdisciplinary work on the conditions under which combinations of stressors have particularly strong negative effects on natural organisms.     

When can embryos learn? A test of the timing of learning in embryonic amphibians

Learning is crucial to the survival of organisms across their life span, including during embryonic development. We set out to determine when learning becomes possible in amphibian development by exposing spotted salamander (Ambystoma maculatum) embryos to chemical stimuli from a predator (Ambystoma opacum), nonpredator (Lithobates clamitans), or control at developmental stages 16–21 or 36–38 (Harrison 1969 ). Once exposures were completed and embryos hatched, we recorded the number of movements and time spent moving of individuals in both groups and all treatments. There was no significant difference in number of movements or time spent moving among any of the treatments. The groups that were exposed to predator stimuli and a blank control at stages 36–38 were also tested to determine whether there was a difference in refuge preference or difference in survivorship when exposed to a predator (marbled salamander). There was no difference in survival or refuge preference between individuals; however, all individuals preferred vegetated over open areas regardless of treatment type. We discuss hypotheses for the absence of embryonic learning in this species and suggest it may be the result of the intensity of the predator–prey interaction between the predator, large marbled salamander larvae, and the prey, spotted salamander larvae.     

Tadpole–odonate larvae interactions: influence of body size and diel rhythm

Several studies have shown that prey and predator body size may affect the outcome of predator–prey interactions. However, few studies have taken in account the changes on predator–prey interactions over 24 h. In a tropical freshwater system I evaluated how predator and prey size, and their diel rhythm in activity influenced the interaction between Physalaemus pustulosus tadpoles and dragonfly larvae. Tadpoles of different size classes were exposed to two size classes of the dragonfly larvae Rhionaeschna spec. Feeding trials were conducted during day and night. Tadpole activity showed a diel rhythm and affected size-selective predation of the smallest dragonfly larvae, but not of the larger ones. Predator and prey size had a significant effect on the prey survivorship and prey size had a significant effect on the preference of the predator. The interaction between both factors was significant, indicating that they did not operate independently. I conclude that the predator–prey interactions between odonate larvae and anuran tadpoles were mainly affected by the size of the prey and the predator, and less by the diel activity pattern of the prey.     

Impact of Recombinant Baculovirus Applications on Target Heliothines and Nontarget Predators in Cotton

Recombinant baculoviruses have been genetically engineered to reduce the time to kill infected pests, thus reducing crop damage. In this study, wild-type viruses and recombinant viruses expressing a scorpion toxin were applied to cotton in response to larval infestations of Helicoverpa zea and Heliothis virescens in 1997 and 1998. A chemical standard and an untreated control acted as comparison treatments. The goals of this field study were to (1) assess the efficacy of recombinant baculoviruses in protecting cotton from larval feeding damage; (2) assess the impact of recombinant virus introductions on predator densities and diversity; and (3) determine if cotton predators acquire baculovirus by consuming infected heliothines. When applications were timed at larval emergence, certain recombinant virus treatments protected cotton from damage better than wild-type virus treatments and as well as the chemical standard. Differences in efficacy between recombinant and wild-type baculoviruses were not apparent if treatments were applied 3 to 4 days after peak larval emergence. Predator densities and diversity were similar among recombinant and wild-type baculovirus treatments, whereas plots treated with the chemical standard had consistently smaller predator populations. From polymerase chain reaction analyses of predators in 1997 and 1998, 1.7 and 0.2%, respectively, of predators had consumed a virus-infected heliothine. Nine of the 26 predators carrying viral DNA were positive for recombinant virus. Additionally, 13 of the 26 predators were found to disperse 13.5 to 105 m 2 to 5 days after initial virus applications. Five of these dispersing predators (0.2% of all predators evaluated) carried recombinant viral DNA. These results suggest that the potential for the inadvertent spread of recombinant viral DNA via dispersing predators is low.     

Sublethal pesticide exposure disrupts courtship in the striped lynx spider,Oxyopes salticus (Araneae: Oxyopidae)

The striped lynx spider, Oxyopes salticus, is a dominant predator of pests in agricultural crops where pesticides are readily applied. While past research shows pesticides directly affect the mortality of agricultural pest predators, recent research has found that pesticide exposure may cause sublethal effects in these organisms. This study examined how residues of three common pesticides (active ingredients: bifenthrin, carbaryl, malathion) impact courtship behaviour of O. salticus. Males provided with cues left by females readily performed courting behaviours. However, when females left cues on a substrate containing bifenthrin and carbaryl, males were less likely to perform courtship behaviours and did so for less time. While males on the malathion treatment showed a trend for reduced courting, this was not significantly different from the treatment without pesticides. The cue produced by females is unknown in this species. However, our study found males reduced their courting over time, suggesting that the cue is ephemeral and not long lived. This study adds important insight into the growing evidence that pesticides greatly impact the ecology of agricultural pest predators and other non‐target organisms by altering their behaviour.