Reinforcing effects of non-pathogenic bacteria and predation risk: from physiology to life history

The important ecological role of predation risk in shaping populations, communities and ecosystems is becoming increasingly clear. In this context, synergistic effects between predation risk and other natural stressors on prey organisms are gaining attention. Although non-pathogenic bacteria can be widespread in aquatic ecosystems, their role in mediating effects of predation risk has been ignored. We here address the hypothesis that non-pathogenic bacteria may reinforce the negative effects of predation risk in larvae of the damselfly Coenagrion puella. We found synergistic effects for all three life history variables studied: mortality increased, growth reductions were magnified and bacterial load was higher when both non-lethal stressors were combined. The combined exposure to the bacterium and predation risk considerably impaired the two key antipredator mechanisms of the damselfly larvae: they no longer reduced their food intake under predation risk and showed a synergistic reduction in escape swimming speed. The reinforcing negative effects on the fitness-related traits could be explained by the observed synergistic effects on food intake, swimming muscle mass, immune function and oxidative damage. These are likely widespread consequences of energetic constraints and increased metabolic rates associated with the fight-or-flight response. We therefore hypothesize that the here documented synergistic interactions with non-pathogenic bacteria may be widespread. Our results highlight the ignored ecological role of non-pathogenic bacteria in reinforcing the negative effects of predation risk on prey organisms.     

Combined Effects of Virus, Pesticide, and Predator Cue on the Larval Tiger Salamander (Ambystoma tigrinum)

Emerging diseases and environmental contamination are two of the leading hypotheses for global amphibian declines. Yet few studies have examined the influence of contaminants on disease susceptibility, and even fewer have incorporated the role of natural stressors such as predation. We performed a factorial study investigating the interaction of the insecticide carbaryl, dragonfly predator cue, and the emerging pathogen Ambystoma tigrinum virus (ATV) on fitness correlates and disease susceptibility in tiger salamander larvae. Four week old larvae were exposed for 22 days in a 2 (0, 500 μg/l carbaryl) × 2 (control, predator cue water) × 2 (0, 1 × 10⁴ pfu ATV) factorial designed laboratory study. Results show significant impacts to survival of larvae for both virus and predator cue treatments, as well as an interactive effect between the two, in which predator cue strongly exacerbated disease-driven mortality. There was a clear pattern of reduced survival with the addition of stressors, with those where all three stressors were present exhibiting the worst effects (a decrease in survival from 93 to 60%). On those that survived, we also detected several sub-lethal impacts in mass, SVL, and development. Predator cue and pesticide treatments significantly reduced both SVL and mass. Virus and predator treatments significantly slowed development. Stressors also exhibited opposing effects on activity. Predator cue caused a significant reduction in activity, whereas virus caused a significant increase in activity over time. These results highlight the importance of examining combined natural and introduced stressors to understand potential impacts on amphibian species. Such stressors may contribute to the emergence of ATV in particular regions, raising concerns about the influence of pesticides on disease emergence in general.     

Consequences of an amphibian malformity for development and fitness in complex environments

1. Environmental stressors have both lethal and sublethal effects, such as altered developmental rates and the induction of malformations. Ecological interactions, including predation and competition, often amplify such effects, for instance by inducing behavioural changes that increase susceptibility to the stress. 2. Using experimental mesocosms, we asked whether the density of conspecific competitors and predation risk from larval water beetles (Dytiscus spp.) affect the development of malformations in tadpoles of the wood frog (Rana sylvatica). We also examined whether such malformities increase the susceptibility of tadpoles to predation. 3. The risk of predation decreased the frequency of malformities in both low‐ and high‐density treatments, although this effect was greater at low density. Behavioural observations suggested that reductions in activity by amphibian larvae induced by predators mediated these responses by decreasing cumulative exposure to ultraviolet‐B radiation, the putative stressor causing the observed malformity. These results suggest that predators can reduce negative impacts of stressors by inducing behavioural changes in prey organisms. 4. Malformed individuals were twice as vulnerable to predators as non‐malformed individuals, suggesting that sublethal effects can ultimately cause increased mortality.     

Effects of species‐specific interactions with predation risk on the relative species sensitivities to a pesticide in water boatmen (Corixidae)

There is increasing concern that synergistic interactions between stressors may result in accelerated biodiversity loss. Yet, the prevalence and magnitude of these interactions remain one of the largest uncertainties in projections of future ecological change. Synergistic interactions between pesticide stress and predation risk are receiving increasing attention because they indicate that standard pesticide tests in the absence of predation risk may underestimate effects that occur under natural conditions. We questioned whether synergisms (or interactions in general), by differently shaping individual species’ sensitivities, can modulate species sensitivity rankings (SSRs) in survival and growth rate. Using laboratory and outdoor mesocosm experiments with five species of water boatmen (Hemiptera: Corixidae) we studied mortality and growth rate over seven days of exposure. We evaluated the presence and nature of interactions between the pesticide endosulfan and predation risk and tested to what extent this affected the SSRs to endosulfan. The combined exposure to the pesticide and predation risk resulted in synergistic effects for survival (Sigara lateralis) and growth rate (Sigara iactans) and in an antagonistic effect for growth rate (Hesperocorixa linnaei and female Sigara striata). These results suggest that standard tests may underestimate the pesticide effect in a natural predator environment for some species. While the effects of these interactions on SSRs were not strong and SSRs remained largely similar in the absence and presence of predation risk, some obvious species rank shifts occurred for growth rate which may potentially affect community structure through changed competitive strength. The study of SSRs and their dependency on biotic stressors may provide a simple conceptual and predictive framework to increase our understanding of how stressors like pesticides may differentially affect community structure in the absence and presence of another stressor.     

Exposure to a heat wave under food limitation makes an agricultural insecticide lethal: a mechanistic laboratory experiment

Extreme temperatures and exposure to agricultural pesticides are becoming more frequent and intense under global change. Their combination may be especially problematic when animals suffer food limitation. We exposed Coenagrion puella damselfly larvae to a simulated heat wave combined with food limitation and subsequently to a widespread agricultural pesticide (chlorpyrifos) in an indoor laboratory experiment designed to obtain mechanistic insights in the direct effects of these stressors in isolation and when combined. The heat wave reduced immune function (activity of phenoloxidase, PO) and metabolic rate (activity of the electron transport system, ETS). Starvation had both immediate and delayed negative sublethal effects on growth rate and physiology (reductions in Hsp70 levels, total fat content, and activity levels of PO and ETS). Exposure to chlorpyrifos negatively affected all response variables. While the immediate effects of the heat wave were subtle, our results indicate the importance of delayed effects in shaping the total fitness impact of a heat wave when followed by pesticide exposure. Firstly, the combination of delayed negative effects of the heat wave and starvation, and the immediate negative effect of chlorpyrifos considerably (71%) reduced larval growth rate. Secondly and more strikingly, chlorpyrifos only caused considerable (ca. 48%) mortality in larvae that were previously exposed to the combination of the heat wave and starvation. This strong delayed synergism for mortality could be explained by the cumulative metabolic depression caused by each of these stressors. Further studies with increased realism are needed to evaluate the consequences of the here‐identified delayed synergisms at the level of populations and communities. This is especially important as this synergism provides a novel explanation for the poorly understood potential of heat waves and of sublethal pesticide concentrations to cause mass mortality.     

Does simultaneous UV-B exposure enhance the lethal and sub-lethal effects of aquatic hypoxia on developing anuran embryos and larvae?

Recent catastrophic global amphibian declines have been partially linked to increases in UV-B radiation as a consequence of stratospheric ozone depletion. Previous studies have shown that in the presence of other environmental stressors including aquatic pH and temperature and the presence of contaminants or pathogens, the lethal effects of UV-B on amphibian larvae are enhanced due to interactions between the stressors. Little is known about the interactions between UV-B and aquatic hypoxia, a common and significant natural stressor of amphibian larvae. We examined the potential effects of UV-B and aquatic hypoxia in combination on embryonic survival, developmental rate, body mass and locomotor performance of embryos and larvae of the striped marsh frog, Limnodynastes peronii. We found that while both UV-B and hypoxia independently had substantial negative effects on the developing embryos of L. peronii, they did not interact in a multiplicative or antagonistic manner. The effects of the stressors in combination were as might be predicted based on the knowledge of their independent actions alone (i.e. an additive effect). In all cases developing embryos exposed to both UV-B and hypoxia were more severely affected than those exposed to either UV-B or hypoxia alone. The results of this study show the importance of examining both the direct actions of individual stressors and how these may be influenced by the presence of other environmental factors.     

Complex impact of an invasive crayfish on freshwater food webs

Invasive alien species can have complex effects on native ecosystems, and interact with multiple components of food webs, making it difficult a comprehensive quantification of their direct and indirect effects. We evaluated the relationships between the invasive crayfish, Procambarus clarkii, amphibian larvae and predatory insects, to quantify crayfish impacts on multiple levels of food webs, and to evaluate whether crayfish predation of aquatic insects has indirect consequences for their preys. We used pipe sampling to assess the abundance of crayfish, amphibian larvae and their major predators (Ditiscidae, Notonectidae and larvae of Anisoptera) in invaded and uninvaded ponds within a human dominated landscape. We disentangled the multivariate effects of P. clarkii on different components of food web through a series of constrained redundancy analyses. The crayfish had a negative, direct impact on both amphibian communities and their predators. Amphibian abundance was negatively related to both predators. However, the negative, direct effects of crayfish on amphibians were much stronger than predation by native insects. Our results suggest that this crayfish impacts multiple levels of food webs, disrupting natural prey-predator relationships.     

Experimental examination of the effects of ultraviolet-B radiation in combination with other stressors on frog larvae

Ultraviolet-B radiation (UVB) is a ubiquitous stressor with negative effects on many aquatic organisms. In amphibians, ambient levels of UVB can result in impaired growth, slowed development, malformations, altered behavior and mortality. UVB can also interact with other environmental stressors to amplify these negative effects on individuals. In outdoor mesocosm and laboratory experiments we studied potential synergistic effects of UVB, a pathogenic fungus, Batrachochytrium dendrobatidis (Bd), and varying temperatures on larval Cascades frogs (Rana cascadae). First, we compared survivorship, growth and development in two mesocosm experiments with UVB- and Bd-exposure treatments. We then investigated the effects of UVB on larvae in the laboratory under two temperature regimes, monitoring survival and behavior. We found reduced survival of R. cascadae larvae with exposure to UVB radiation in all experiments. In the mesocosm experiments, growth and development were not affected in either treatment, and no effect of Bd was found. In the laboratory experiment, larvae exposed to UVB demonstrated decreased activity levels. We also found a trend towards reduced survival when UVB and cold temperatures were combined. Our results show that amphibian larvae can suffer both lethal and sublethal effects when exposed to UVB radiation.     

An examination of multiple factors affecting community structure in an aquatic amphibian community

Summary The potential effects of multiple factors structuring certain larval amphibian communities were studied using a pen experiment in a natural pond. Potential factors (predation and competition from other species) were allowed to act in a stepwise fashion such that their relative importance could be evaluated. Based on a previous study, it was hypothesized that predation by Ambystoma salamander larvae on other larval amphibian species would be the most important factor. Survival of Ambystoma jeffersonianum salamander larvae and Rana sylvatica tadpoles was significantly depressed only by Ambystoma opacum predation. Survival of Ambystoma maculatum salamander larvae was significantly greater in the absence of both A. opacum and A. jeffersonianum predators. The virtual elimination of Hyla chrysoscelis larvae in all treatments also can be largely attributed to Ambystoma predation. Thus, Ambystoma predation was the dominant factor determining larval survival of four amphibian prey species in the experimental communities.     

Influence of ultraviolet-B radiation on growth,prevalence of deformities,and susceptibility to predation in Cascades frog (<Emphasis Type="Italic">Rana cascadae</Emphasis>) larvae

Ambient levels of ultraviolet-B radiation (UVB) have a variety of detrimental effects on aquatic organisms. These include death and effects on growth, development, physiology, and behavior. Amphibians show all of these effects. However, the effects vary with species, life history stage, and ecological context. Little is known about the implications of the detrimental effects of UVB on ecological dynamics. Our study was designed to test how UVB may affect predator–prey interactions, an important ecological dynamic. Specifically, we tested the effect of UVB on the susceptibility of Cascades frog (Rana cascadae) larvae to predation by rough-skinned newts (Taricha granulosa). We also further examined the sublethal effects of UVB on growth and development in Cascades frog larvae. We found no direct effect of UVB exposure on survival. However, UVB-exposed frog larvae displayed decreased growth and increased prevalence of deformities. UVB also caused increased susceptibility to predation, but there was a significant treatment–block interaction. UVB increased susceptibility to predation in two out of five blocks of Cascades frogs. The other three blocks did not show an effect of UVB on susceptibility to predation. Our study suggests that UVB can alter susceptibility to predation in at least one amphibian species. UVB-induced alteration of predator–prey interactions could potentially lead to changes at the population, community, and ecosystem levels. Handling editor: K. Martens     

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.     

No evidence for a cost of selection by carbaryl exposure in terms of vulnerability to fish predation in <Emphasis Type="Italic">Daphnia magna</Emphasis>

Natural populations are exposed to multiple stressors. These stressors may interact, leading to synergistic or antagonistic responses. In addition to these direct interaction effects, there may also be an interaction between stressors through a selection effect: as the population genetically responds to one stressor, it may become more vulnerable to another one, for instance because of an associated reduction in genetic variation. We here capitalized on a selection experiment involving the exposure of Daphnia populations to carbaryl pulses to test the hypothesis that selection imposed by this pesticide may increase vulnerability to fish predation in the resulting population. A direct predation experiment with individuals isolated from carbaryl-exposed and non-exposed populations revealed no effect of prior selection by carbaryl exposure on mortality due to stickleback predation.     

Developmental and Evolutionary History Affect Survival in Stressful Environments

The world is increasingly impacted by a variety of stressors that have the potential to differentially influence life history stages of organisms. Organisms have evolved to cope with some stressors, while with others they have little capacity. It is thus important to understand the effects of both developmental and evolutionary history on survival in stressful environments. We present evidence of the effects of both developmental and evolutionary history on survival of a freshwater vertebrate, the rough-skinned newt (Taricha granulosa) in an osmotically stressful environment. We compared the survival of larvae in either NaCl or MgCl₂ that were exposed to salinity either as larvae only or as embryos as well. Embryonic exposure to salinity led to greater mortality of newt larvae than larval exposure alone, and this reduced survival probability was strongly linked to the carry-over effect of stunted embryonic growth in salts. Larval survival was also dependent on the type of salt (NaCl or MgCl₂) the larvae were exposed to, and was lowest in MgCl₂, a widely-used chemical deicer that, unlike NaCl, amphibian larvae do not have an evolutionary history of regulating at high levels. Both developmental and evolutionary history are critical factors in determining survival in this stressful environment, a pattern that may have widespread implications for the survival of animals increasingly impacted by substances with which they have little evolutionary history.     

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.     

水蛭捕食两栖类卵

许多卵生动物具有对付食卵者的精巧策略以降低死亡率,因为早期发育阶段的捕食压力能显著影响具复杂生活史动物的生存。两栖动物卵被水蛭等很多物种所捕食。我们查阅了水蛭捕食两栖类卵的文献,发现27篇论文。在所报道的水蛭捕食两栖类卵的例子中,无尾类(3.6%,n=591)明显多于有尾类(1.6%,n=255)。此外,我们第一次记录到水蛭捕食四趾螈(Salamandrina perspicillata)卵,这也是西欧有尾类的第一例报道。我们没有发现两个两栖动物类群间存在差异。然而,当我们分别分析来自北美、欧洲和亚洲三个地区的数据时,发现北美的有尾类和无尾类间存在显著差异。水蛭可捕食各生活史阶段的两栖动物,因此,水蛭应归为一些两栖类的天敌。     

Effects of an infectious fungus, Batrachochytrium dendrobatidis, on amphibian predator-prey interactions

The effects of parasites and pathogens on host behaviors may be particularly important in predator-prey contexts, since few animal behaviors are more crucial for ensuring immediate survival than the avoidance of lethal predators in nature. We examined the effects of an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis, on anti-predator behaviors of tadpoles of four frog species. We also investigated whether amphibian predators consumed infected prey, and whether B. dendrobatidis caused differences in predation rates among prey in laboratory feeding trials. We found differences in anti-predator behaviors among larvae of four amphibian species, and show that infected tadpoles of one species (Anaxyrus boreas) were more active and sought refuge more frequently when exposed to predator chemical cues. Salamander predators consumed infected and uninfected tadpoles of three other prey species at similar rates in feeding trials, and predation risk among prey was unaffected by B. dendrobatidis. Collectively, our results show that even sub-lethal exposure to B. dendrobatidis can alter fundamental anti-predator behaviors in some amphibian prey species, and suggest the unexplored possibility that indiscriminate predation between infected and uninfected prey (i.e., non-selective predation) could increase the prevalence of this widely distributed pathogen in amphibian populations. Because one of the most prominent types of predators in many amphibian systems is salamanders, and because salamanders are susceptible to B. dendrobatidis, our work suggests the importance of considering host susceptibility and behavioral changes that could arise from infection in both predators and prey.     

The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism

Natural enemies not only influence prey density but they can also cause the modification of traits in their victims. While such non-lethal effects can be very important for the dynamic and structure of prey populations, little is known about their interaction with the density-mediated effects of natural enemies. We investigated the relationship between predation rate, prey density and trait modification in two aphid-aphid predator interactions. Pea aphids (Acyrthosiphon pisum, Harris) have been shown to produce winged dispersal morphs in response to the presence of ladybirds or parasitoid natural enemies. This trait modification influences the ability of aphids to disperse and to colonise new habitats, and hence has a bearing on the population dynamics of the prey. In two experiments we examined wing induction in pea aphids as a function of the rate of predation when hoverfly larvae (Episyrphus balteatus) and lacewing larvae (Chrysoperla carnea) were allowed to forage in pea aphid colonies. Both hoverfly and lacewing larvae caused a significant increase in the percentage of winged morphs among offspring compared to control treatments, emphasising that wing induction in the presence of natural enemies is a general response in pea aphids. The percentage of winged offspring was, however, dependent on the rate of predation, with a small effect of predation on aphid wing induction at very high and very low predation rates, and a strong response of aphids at medium predation rates. Aphid wing induction was influenced by the interplay between predation rate and the resultant prey density. Our results suggests that density-mediated and trait-mediated effects of natural enemies are closely connected to each other and jointly determine the effect of natural enemies on prey population dynamics.     

Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems

The field of ecotoxicology is experiencing a surge in attention among ecologists as we gain a deeper appreciation for how contaminants can impact natural ecosystems. This interest is particularly strong in aquatic systems where many non-target organisms experience pesticides. In this article, we assess how pesticides affect freshwater systems by applying the conceptual framework of density- and trait-mediated indirect effects from the field of basic ecology. We demonstrate the utility of this framework for understanding the conditions under which pesticides affect species interactions, communities and ecosystems. Through the integration of laboratory toxicity tests and this ecological framework, ecotoxicologists should be better able to identify the mechanisms through which pesticides affect communities and ecosystems. We also identify several areas of research that are in critical need of empirical attention including synergistic effects between pesticides and natural stressors, the importance of pesticides on community assembly via habitat preferences and oviposition effects, the timing and frequency of pesticide applications, pesticide effects on population dynamics, the evolution of pesticide resistance in non-target organisms and ecosystem recovery. With this knowledge, one can improve upon management decisions and help protect non-target species that are of conservation concern.     

Biotic interactions govern genetic adaptation to toxicants

The genetic recovery of resistant populations released from pesticide exposure is accelerated by the presence of environmental stressors. By contrast, the relevance of environmental stressors for the spread of resistance during pesticide exposure has not been studied. Moreover, the consequences of interactions between different stressors have not been considered. Here we show that stress through intraspecific competition accelerates microevolution, because it enhances fitness differences between adapted and non-adapted individuals. By contrast, stress through interspecific competition or predation reduces intraspecific competition and thereby delays microevolution. This was demonstrated in mosquito populations (Culex quinquefasciatus) that were exposed to the pesticide chlorpyrifos. Non-selective predation through harvesting and interspecific competition with Daphnia magna delayed the selection for individuals carrying the ace-1^R resistance allele. Under non-toxic conditions, susceptible individuals without ace-1^R prevailed. Likewise, predation delayed the reverse adaptation of the populations to a non-toxic environment, while the effect of interspecific competition was not significant. Applying a simulation model, we further identified how microevolution is generally determined by the type and degree of competition and predation. We infer that interactions with other species—especially strong in ecosystems with high biodiversity—can delay the development of pesticide resistance.     

The Respiratory Transition from Water to Air Breathing During Amphibian Metamorphosis

SYNOPSIS. Profound developmental changes occur in the morphologyand physiology of the respiratory system of amphibians duringthe transition from strictly aquatic to dual aquatic-aerialbreathing. This developmental transition usually involves modificationsin ventilatory mechanisms and/or respiratory surfaces {e.g.,degeneration of gills, ventilation of functional lungs). Boththe first appearance of obligate air breathing and the subsequentdependence upon it by amphibian larvae are sensitive to a varietyof environmental stressors during critical developmental periods.These stressors include oxygen availability, ambient temperature,the risk of predation and mode of feeding.