Attila Hettyey

Female partner preferences enhance offspring ability to survive an infection

BackgroundIt is often suggested that mate choice enhances offspring immune resistance to infectious diseases. To test this hypothesis, we conducted a study with wild-derived house mice (Mus musculus musculus) in which females were experimentally mated either with their preferred or non-preferred male, and their offspring were infected with a mouse pathogen, Salmonella enterica (serovar Typhimurium).ResultsWe found that offspring sired by preferred males were significantly more likely to survive the experimental infection compared to those sired by non-preferred males. We found no significant differences in the pathogen clearance or infection dynamics between the infected mice, suggesting that offspring from preferred males were better able to cope with infection and had improved tolerance rather than immune resistance.ConclusionOur results provide the first direct experimental evidence within a single study that partner preferences enhance offspring resistance to infectious diseases.

Assessing Risk and Guidance on Monitoring of Batrachochytrium dendrobatidis in Europe through Identification of Taxonomic Selectivity of Infection

Amphibians are globally threatened, but not all species are affected equally by different threatening processes. This is true for the threat posed by the chytridiomycete fungus (Batrachochytrium dendrobatidis). We compiled a European data set for B. dendrobatidis to analyze the trends of infection in European amphibians. The risk of infection was not randomly distributed geographically or taxonomically across Europe. Within countries with different prevalence, infection was nonrandom in certain amphibian taxa. Brown frogs of the genus Rana were unlikely to be infected, whereas frogs in the families Alytidae and Bombinatoridae were significantly more likely to be infected than predicted by chance. Frogs in the 2 families susceptible to B. dendrobatidis should form the core of attempts to develop spatial surveillance studies of chytridiomycosis in Europe. Ideally, surveys for B. dendrobatidis should be augmented by sampling the widespread genus Pelophylax because this taxon exhibits geographically inconsistent overinfection with B. dendrobatidis and surveillance of it may facilitate recognition of factors causing spatial variability of infection intensity. Several European amphibian taxa were not represented in our data set; however, surveillance of unsampled species should also occur when warranted.

Behavioural consistency and life history of Rana dalmatina tadpoles

AbstractThe focus of evolutionary behavioural ecologists has recently turned towards understanding the causes and consequences of behavioural consistency, manifesting either as animal personality (consistency in a single behaviour) or behavioural syndrome (consistency across more behaviours). Behavioural type (mean individual behaviour) has been linked to life-history strategies, leading to the emergence of the integrated pace-of-life syndrome (POLS) theory. Using Rana dalmatina tadpoles as models, we tested if behavioural consistency and POLS could be detected during the early ontogenesis of this amphibian. We targeted two ontogenetic stages and measured activity, exploration and risk-taking in a common garden experiment, assessing both individual behavioural type and intra-individual behavioural variation. We observed that activity was consistent in all tadpoles, exploration only became consistent with advancing age and risk-taking only became consistent in tadpoles that had been tested, and thus disturbed, earlier. Only previously tested tadpoles showed trends indicative of behavioural syndromes. We found an activity—age at metamorphosis POLS in the previously untested tadpoles irrespective of age. Relative growth rate correlated positively with the intra-individual variation of activity of the previously untested older tadpoles. In previously tested older tadpoles, intra-individual variation of exploration correlated negatively and intra-individual variation of risk-taking correlated positively with relative growth rate. We provide evidence for behavioural consistency and POLS in predator- and conspecific-naive tadpoles. Intra-individual behavioural variation was also correlated to life history, suggesting its relevance for the POLS theory. The strong effect of moderate disturbance related to standard behavioural testing on later behaviour draws attention to the pitfalls embedded in repeated testing.

Choice of experimental venue matters in ecotoxicology studies: Comparison of a laboratory-based and an outdoor mesocosm experiment.

The heavy application of pesticides and its potential effects on natural communities has attracted increasing attention to inadvertent impacts of these chemicals. Toxicologists conventionally use laboratory-based tests to assess lethal concentrations of pesticides. However, these tests often do not take into account indirect, interactive and long-term effects, and tend to ignore different rates of disintegration in the laboratory and under natural conditions. Our aim was to investigate the importance of the experimental venue for ecotoxicology tests. We reared tadpoles of the agile frog (Rana dalmatina) in the laboratory and in outdoor mesocosms and exposed them to three initial concentrations of a glyphosate-based herbicide (0, 2 and 6.5 mg a.e./L glyphosate), and to the presence or absence of caged predators (dragonfly larvae). The type of experimental venue had a large effect on the outcome: The herbicide was less lethal to tadpoles reared in outdoor mesocosms than in the laboratory. Further, while the herbicide had a negative effect on development time and on body mass in the laboratory, tadpoles exposed to the herbicide in mesocosms were larger at metamorphosis and developed faster in comparison to those reared in the absence of the herbicide. The effect of the herbicide on morphological traits of tadpoles also differed between the two venues. Finally, in the presence of the herbicide, tadpoles tended to be more active and to stay closer to the bottom of laboratory containers, while tadpole behaviour shifted in the opposite direction in outdoor mesocosms. Our results demonstrate major discrepancies between results of a classic laboratory-based ecotoxicity test and outcomes of an experiment performed in outdoor mesocosms. Consequently, the use of standard laboratory tests may have to be reconsidered and their benefits carefully weighed against the difficulties of performing experiments under more natural conditions. Tests validating experimentally estimated impacts of herbicides under natural conditions and studies identifying key factors determining the applicability of experimental results are urgently needed.

Variation in Chemical Defense Among Natural Populations of Common Toad, Bufo bufo, Tadpoles: the Role of Environmental Factors

Defensive toxins are widespread in nature, yet we know little about how various environmental factors shape the evolution of chemical defense, especially in vertebrates. In this study we investigated the natural variation in the amount and composition of bufadienolide toxins, and the relative importance of ecological factors in predicting that variation, in larvae of the common toad, Bufo bufo, an amphibian that produces toxins de novo. We found that tadpoles’ toxin content varied markedly among populations, and the number of compounds per tadpole also differed between two geographical regions. The most consistent predictor of toxicity was the strength of competition, indicating that tadpoles produced more compounds and larger amounts of toxins when coexisting with more competitors. Additionally, tadpoles tended to contain larger concentrations of bufadienolides in ponds that were less prone to desiccation, suggesting that the costs of toxin production can only be afforded by tadpoles that do not need to drastically speed up their development. Interestingly, this trade-off was not alleviated by higher food abundance, as periphyton biomass had negligible effect on chemical defense. Even more surprisingly, we found no evidence that higher predation risk enhances chemical defenses, suggesting that low predictability of predation risk and high mortality cost of low toxicity might select for constitutive expression of chemical defense irrespective of the actual level of predation risk. Our findings highlight that the variation in chemical defense may be influenced by environmental heterogeneity in both the need for, and constraints on, toxicity as predicted by optimal defense theory.

Inducible chemical defences in animals

Phenotypic plasticity is extremely widespread in the behaviour, morphology and life-history of animals. However, inducible changes in the production of defensive chemicals are described mostly in plants and surprisingly little is known about similar plasticity in chemical defences of animals. Inducible chemical defences may be common in animals because many are known to produce toxins, the synthesis of toxins is likely to be costly, and there are a few known cases of animals adjusting their toxin production to changes in environmental conditions. We outline what is known about the occurrence of inducible chemical defences in animals and argue that there is immense potential for progress in this field. Possible directions include surveying diverse taxa to explore how general its occurrence may be and testing for selection acting on inducible chemical defences. Data on inducible chemical defences would provide insight into life-history tradeoffs by enabling novel tests of how time-costs and resource-costs affect life-history. If the synthesis of toxic compounds by animals proves accessible to manipulation, as it is in plants and fungi, this will open the way to refined estimates of the fitness costs of defence, ultimately providing a clearer picture of how plasticity evolves and is maintained in nature.

No observable effect of a glyphosate-based herbicide on two top predators of temporal water bodies.

It has been implied that the application of pesticides is involved in the world-wide decline of biodiversity, but little is known about the influence of these chemicals on key predators of temporary wetlands. The direct impacts were examined of a frequently applied glyphosate-based herbicide on larval Aeshna cyanea (Müller, 1764; Odonata, Insecta) and adult male Lissotriton vulgaris (Linnaeus, 1758; Caudata, Amphibia), 2 top predators of Central European ephemeral ponds. The effects of herbicide exposure were measured on survival, behavior, body mass change, and predatory activity in an outdoor mesocosm experiment lasting for 17 d. No significant effects of exposure were observed in either predator species. The results suggest that the herbicide has no immediate effect on the predators studied at environmentally relevant concentrations and that these predators can also fulfill their top-down regulatory role in contaminated ecosystems.

Reproductive interference between Rana dalmatina and Rana temporaria affects reproductive success in natural populations

Experimental evidence suggests that reproductive interference between heterospecifics can seriously affect individual fitness; support from field studies for such an effect has, however, remained scarce. We studied reproductive interference in 25 natural breeding ponds in an area where two ranid frogs, Rana dalmatina and Rana temporaria, co-occur. The breeding seasons of the two species usually overlap and males of both species are often found in amplexus with heterospecific females, even though matings between heterospecifics produce no viable offspring. We estimated species abundance ratios based on the number of clutches laid and evaluated fertilization success. In ponds with low spatial complexity and a species abundance ratio biased towards R. temporaria, the average fertilization success of R. dalmatina eggs decreased, while this relationship was not detectable in spatially more complex ponds. Fertilization success of R. temporaria did not decrease with increasing relative numbers of heterospecifics. This asymmetry in fitness effects of reproductive interference may be attributed to R. temporaria males being more competitive in scramble competition for females than R. dalmatina males. Our study is among the first to demonstrate that in natural breeding populations of vertebrates interference among heterospecifics has the potential to substantially lower reproductive success at the population level, which may in turn affect population dynamics.

Effects of a glyphosate-based herbicide and predation threat on the behaviour of agile frog tadpoles

The widespread application of pesticides emphasises the importance of understanding the impacts of these chemicals on natural communities. The most commonly applied broad-spectrum herbicides in the world are glyphosate-based herbicides, which have been suggested to induce significant behavioural changes in non-target organisms even at low environmental concentrations. To scrutinize the behavioural effects of herbicide-exposure we exposed agile frog (Rana dalmatina) tadpoles in an outdoor mesocosm experiment to three concentrations of a glyphosate-based herbicide (0, 2 and 6.5mg acid equivalent (a.e.) / L). To assess whether anti-predator behaviour is affected by the pesticide, we combined all levels of herbicide-exposure with three predator treatments (no predator, caged Aeshna cyanea dragonfly larvae or Lissotriton vulgaris newt adults) in a full factorial design. We observed hiding, activity, proximity to the predator cage and vertical position of tadpoles. We found that at the higher herbicide concentration tadpoles decreased their activity and more tadpoles were hiding, and at least at the lower concentration their vertical position was closer to the water surface than in tadpoles of the control treatment. Tadpoles also decreased their activity in the presence of dragonfly larvae, but did not hide more in response to either predator, nor did tadpoles avoid predators spatially. Further, exposure to the herbicide did not significantly influence behavioural responses to predation threat. Our study documents a definite influence of glyphosate-based herbicides on the behaviour of agile frog tadpoles and indicates that some of these changes are similar to those induced by dangerous predators. This may suggest that the underlying physiological mechanisms or the adaptive value of behavioural changes may similar.

Age- and environment-dependent changes in chemical defences of larval and post-metamorphic toads

BackgroundChemical defences are widespread in animals, but how their production is adjusted to ecological conditions is poorly known. Optimal defence theory predicts that inducible defences are favoured over constitutive defences when toxin production is costly and the need for it varies across environments. However, if some environmental changes occur predictably (e.g. coupled to transitions during ontogeny), whereas others are unpredictable (e.g. predation, food availability), changes in defences may have constitutive as well as plastic elements. To investigate this phenomenon, we raised common toad (Bufo bufo) tadpoles with ad libitum or limited food and in the presence or absence of chemical cues on predation risk, and measured their toxin content on 5 occasions during early ontogeny.ResultsThe number of compounds showed limited variation with age in tadpoles and was unaffected by food limitation and predator cues. The total amount of bufadienolides first increased and later decreased during development, and it was elevated in young and mid-aged tadpoles with limited food availability compared to their ad libitum fed conspecifics, whereas it did not change in response to cues on predation risk. We provide the first evidence for the active synthesis of defensive toxin compounds this early during ontogeny in amphibians. Furthermore, the observation of increased quantities of bufadienolides in food-restricted tadpoles is the first experimental demonstration of resource-dependent induction of elevated de novo toxin production, suggesting a role for bufadienolides in allelopathy.ConclusionsOur study shows that the evolution of phenotypic plasticity in chemical defences may depend on the ecological context (i.e. predation vs. competition). Our results furthermore suggest that the age-dependent changes in the diversity of toxin compounds in developing toads may be fixed (i.e., constitutive), timed for the developmental stages in which they are most reliant on their chemical arsenal, whereas inducible plasticity may prevail in the amount of synthesized compounds.