Ecological consequences of amphibian larvae and their native and alien predators on the community structure of temporary ponds

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Morphological and life‐history responses of anurans to predation by an invasive crayfish: an integrative approach

Predator‐induced phenotypic plasticity has been widely documented in response to native predators, but studies examining the extent to which prey can respond to exotic invasive predators are scarce. As native prey often do not share a long evolutionary history with invasive predators, they may lack defenses against them. This can lead to population declines and even extinctions, making exotic predators a serious threat to biodiversity. Here, in a community‐wide study, we examined the morphological and life‐history responses of anuran larvae reared with the invasive red swamp crayfish, Procambarus clarkii, feeding on conspecific tadpoles. We reared tadpoles of nine species until metamorphosis and examined responses in terms of larval morphology, growth, and development, as well as their degree of phenotypic integration. These responses were compared with the ones developed in the presence of a native predator, the larval dragonfly Aeshna sp., also feeding on tadpoles. Eight of the nine species altered their morphology or life history when reared with the fed dragonfly, but only four when reared with the fed crayfish, suggesting among‐species variation in the ability to respond to a novel predator. While morphological defenses were generally similar across species (deeper tails) and almost exclusively elicited in the presence of the fed dragonfly, life‐history responses were very variable and commonly elicited in the presence of the invasive crayfish. Phenotypes induced in the presence of dragonfly were more integrated than in crayfish presence. The lack of response to the presence of the fed crayfish in five of the study species suggests higher risk of local extinction and ultimately reduced diversity of the invaded amphibian communities. Understanding how native prey species vary in their responses to invasive predators is important in predicting the impacts caused by newly established predator–prey interactions following biological invasions.     

An invasive species may be better than none: invasive signal and native noble crayfish have similar community effects

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Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians

Aim Early assessment of the impact of invasive alien species is crucial to set up timely management, but often the impact is evident when it is too late for action. We evaluated relationships between the alien crayfish, Procambarus clarkii, the distribution of native amphibians, and the abundance of their larvae. We assessed whether considering measures of reproductive success provide a more prompt measure of impact than considering just species distribution. Location One hundred and twenty‐five wetlands in Northern Italy, in an area recently invaded by P. clarkii. Methods We surveyed wetlands to assess the presence of breeding activity of amphibians and the distribution of P. clarkii. We measured the abundance of amphibian larvae before metamorphosis through pipe sampling. We built models analysing the relationships between amphibian and crayfish distribution, while taking into account spatial autocorrelation and environmental features. Analyses were performed at both the species level (generalized linear models and spatial eigenvector mapping) and community level (constrained redundancy analysis). Results In terms of breeding site distribution, only two amphibians (Lissotriton vulgaris and Hyla intermedia) were negatively associated with P. clarkii, while the relationships between other the species and P. clarkii were positive or not significant. However, larval abundance for all amphibian species was negatively associated with the alien crayfish. Analyses performed at community and single species levels yielded consistent results. Main conclusions Procambarus clarkii impacts amphibians through different processes. Newts probably avoid invaded wetlands for breeding. Other species attempt breeding in wetlands with crayfish, but suffer very low success. Considering distribution data alone would not provide a correct picture of the impact of this alien species; measures of reproductive success may allow a more accurate assessment of the impact.     

Is the exotic red swamp crayfish (Procambarus clarkii) a current threat for the Mediterranean tree frog (Hyla meridionalis) in the Camargue (Southern France)?

The non-indigenous red swamp crayfish (Procambarus clarkii) has been shown to be a threat for amphibian conservation. Many amphibian species breed in temporary ponds to diminish predation risk as such ecosystems are free of large predators. However P. clarkii, occurring as an invasive species in the Camargue delta, can readily disperse on the ground and thus colonize isolated ponds. We studied the current impact of the exotic crayfish on the reproductive success of the Mediterranean tree frog (Hyla meridionalis). In a mesocosm experiment, we tested the effect of two crayfish densities (1 and 3 crayfish/m²) on tadpole abundance. We also tested in a field experiment, within a temporary pond, the crayfish’s predation on the tree frog’s eggs. Finally, we developed site occupancy models using data from 20 ponds to assess the effect of crayfish abundance on tadpole abundance. Neither the experiments, nor the site occupancy models showed a negative impact of the current crayfish abundance on the tree frog populations breeding in ponds. We found that recorded crayfish densities were lower than in other areas where crayfish has impacted amphibian populations, but we hypothesize that current crayfish abundance in the area may increase in the future, thus impacting tree frog populations.     

Embryonic and larval defensive responses of agile frog (Rana dalmatina) to alien crayfish

Red swamp crayfish Procambarus clarkii, a widespread invasive alien crayfish, represents a serious threat for several freshwater species, including amphibians, which are declining at a global scale. As a shared coevolutionary history is the main factor determining the emergence of antipredator responses, Anuran tadpoles may not be able to cope effectively with this introduced predator. We performed two experiments to assess agile frog's (Rana dalmatina) defensive responses to both P. clarkii and native dragonfly larvae (Anax imperator). First, we conditioned embryos (collected from two ponds 30 km away from each other) with predators’ chemical cues to explore possible variation in hatching time caused by predation risk. In the second experiment, to evaluate how predators’ diet affects tadpole behavior, we conditioned tadpoles for a 5‐week period with cues from tadpole‐fed and gammarid‐fed predators and recorded behavioral and morphological responses. Embryos did not alter hatching time in the presence of any predator cue, while tadpoles from both populations strongly reduced activity and visibility when raised in the presence of tadpole‐fed dragonfly larvae. Morphological changes were less straightforward and were induced only in one population, for which broader tails and a slight increase in body size of tadpoles exposed to tadpole‐fed predators were observed. The lack of defensive responses in crayfish‐exposed tadpoles suggests that the spreading of this invasive species in agricultural lowlands of northern Italy may represent a further threat to their conservation.     

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.     

Multi‐faceted impacts of native and invasive alien decapod species on freshwater biodiversity and ecosystem functioning

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Anthropogenic changes to leaf litter input affect the fitness of a larval amphibian

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Niche differentiation among invasive crayfish and their impacts on ecosystem structure and functioning

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Reproductive dynamics of three amphibian species in Mediterranean wetlands: the role of local precipitation and hydrological regimes

1. Although the influence of water availability and precipitation regimes on amphibians has been studied at large scales, whether and how interannual rainfall and hydrological variations affect amphibians dynamics at a local scale have rarely been addressed. In this respect, accounting for variations in species detectability in space and time has also been overlooked. 2. We assessed the effects of rainfall and hydrological variations on the breeding dynamics of three amphibian taxa: Pelodytes punctatus, Hyla meridionalis and Pelophylax spp. in 20 ponds of the Camargue region (southern France) over a 7‐year study period. 3. We used multiple season occupancy models to test the effect of winter–spring rainfall and interannual variations in hydroperiod, mean water depth and drought events on tadpole presence in spring (March–June), a proxy for breeding dynamics. 4. We used an independent survey with spatial replicates (dipnet sweeps) to disentangle the relative contributions of phenology and detectability to the absence of records in a given month. For the three taxa considered, the probability of missing a species when that species was actually present in a pond was most often negligible. Hence, we could consider that multiseason models properly tracked changes in species phenology. 5. Pelodytes punctatus was first detected in March, while the two other taxa appeared later in April. Hyla meridionalis appeared as a mid‐season species with much more synchronous pond occupancy than Pelodytes punctatus. The detection peak of Pelophylax spp. was short and unexpectedly early for this taxon. 6. Seasonal winter–spring rainfall was associated with a decrease in extinction rates and even more strongly with an increase in colonisation rates at individual ponds. 7. Colonisation rate increased following an annual drought and was best modelled as a negative quadratic effect of the variance of pond hydroperiod. Extinction probability was best modelled by a negative quadratic effect of mean water level. Hence, breeding was more stochastic (i) in unpredictable and shallow ponds because of yearly drying up and (ii) in highly predictable and deep ponds, possibly due to the presence of predators such as fish and crayfish. 8. Overall, we show that ponds with intermediate rather than extreme variations in environmental conditions currently correspond to optimal breeding sites. Our study demonstrates that amphibian monitoring coupled with fine‐scale analysis of environmental conditions is necessary to understand species dynamics in the long run and to inform conservation efforts for these species.     

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.     

Crayfish invasion facilitates dispersal of plants and invertebrates by gulls

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Optimising control of invasive crayfish using life‐history information

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Effects of an introduced crayfish, Procambarus clarkii, on the distribution of south-western Iberian amphibians in their breeding habitats

The introduction of exotic species in aquatic habitats is one of the causes for the amphibian declines observed worldwide. In the 1970s, the red swamp crayfish Procambarus clarkii was introduced in the southwest Iberian Peninsula, where no native crayfish occur. In this study we assess the effect of P. clarkii presence in the breeding site distribution of each of the 13 southwest Iberian amphibians, while simultaneously accounting for the effects of potentially confounding habitat variables, as well as for the effects of the other large aquatic predators in the study area – predatory fish. Amphibian species richness was lower in places where P. clarkii was present than in places without P. clarkii , regardless of fish presence. After accounting for habitat variables and fish, crayfish presence was a negative predictor of the breeding probability for all urodeles ( Pleurodeles waltl , Salamandra salamandra , Triturus boscai and T. marmoratus ) and for two anurans ( Pelobates cultripes and Bufo bufo ). The majority of the species affected usually breed in temporary ponds without fish, but that may be colonized by the crayfish. The ongoing expansion of P. clarkii may eventually lead to a growing isolation of amphibian populations and ultimately to local extinctions and a permanent alteration of the amphibian communities in southwest Iberian Peninsula.     

Infection with a trematode parasite differentially alters competitive interactions and antipredator behaviour in native and invasive crayfish

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Stable Isotopes Reveal Trophic Partitioning and Trophic Plasticity of a Larval Amphibian Guild

Temporary ponds are highly variable systems where resource availability and community structure change extensively over time, and consequently the food web is highly dynamic. Amphibians play a critical role both as consumers and prey in aquatic communities and yet there is still little information on the trophic status of most amphibians. More importantly, little is known about the extent to which they can alter their trophic ecology in response to changing conditions. We experimentally investigated the effects of increased amphibian density, presence of intraguild competitors, and presence of native and invasive predators (either free or caged) on the trophic status of a Mediterranean amphibian guild, using stable isotopes. We observed variations in δ ¹³C and δ ¹⁵N isotopic values among amphibian species and treatments and differences in their food sources. Macrophytes were the most important food resource for spadefoot toad tadpoles (Pelobates cultripes) and relatively important for all anurans within the guild. High density and presence of P. cultripes tadpoles markedly reduced macrophyte biomass, forcing tadpoles to increase their feeding on detritus, algae and zooplankton, resulting in lower δ ¹³C values. Native dytiscid predators only changed the isotopic signature of newts whereas invasive red swamp crayfish had an enormous impact on environmental conditions and greatly affected the isotopic values of amphibians. Crayfish forced tadpoles to increase detritus ingestion or other resources depleted in δ ¹³C. We found that the opportunistic amphibian feeding was greatly conditioned by intra- and interspecific competition whereas non-consumptive predator effects were negligible. Determining the trophic plasticity of amphibians can help us understand natural and anthropogenic changes in aquatic ecosystems and assess amphibians’ ability to adjust to different environmental conditions.     

Native predators living in invaded areas: responses of terrestrial amphibian species to an Argentine ant invasion

Predator–prey interactions play a key role in the success and impacts of invasive species. However, the effects of invasive preys on native predators have been poorly studied. Here, we first reviewed hypotheses describing potential relationships between native predators and invasive preys. Second, we examined how an invasive prey, the Argentine ant (Linepithema humile), affected a native terrestrial amphibian community. In the field, we looked at the structure of the amphibian community in invaded versus uninvaded areas and characterized amphibian trophic ecology. The amphibian community sampled seemed to show a species-dependent response in abundance to invasion: adults of the natterjack toad (Bufo calamita), the species demonstrating the highest degree of ant specialization, were less abundant in invaded areas. Although available ant biomass was significantly greater in invaded than in uninvaded areas (only Argentine ants occurred in the former), amphibians consumed relatively fewer ants in invaded areas. In the lab, we quantified amphibian consumption of Argentine ants versus native ants and assessed whether consumption patterns could have been influenced by prior exposure to the invader. The lab experiments corroborated the field results: amphibians preferred native ants over Argentine ants, and prior exposure did not influence consumption. Differences in preference explained why amphibians consumed fewer Argentine ants in spite of their greater relative availability; they might also explain why the most ant-specialized amphibians seemed to avoid invaded areas. Our results suggest the importance to account for predator feeding capacities and dietary ranges to understand the effects of invasive species at higher trophic levels.     

Causes and consequences of crayfish extinction: Stream connectivity,habitat changes,alien species and ecosystem services

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A laboratory study of the effects of shelter availability and invasive crayfish on the growth of native stream fish

1. The alteration of stream habitats by urbanisation reduces the availability of shelter. Reduced shelter availability may increase both predation risks and metabolic costs, negatively affecting the growth performance of stream fish. Although urbanised streams often allow the establishment of invasive species, the additive or interactive effects of shelter availability and invasive species are rarely explored. The invasive red swamp crayfish (Procambarus clarkii) is a strong shelter competitor and predator in streams. 2. We conducted a stream‐channel experiment to investigate how shelter availability and this invasive crayfish species affect the growth performance (measured as the loss in body mass under starved conditions) of two native benthic species, Japanese crucian carp (Carassius auratus complex) and an endangered cobitid fish (Lefua echigonia). 3. We found that both the absence of shelter and the presence of crayfish increased body mass loss in the crucian carp. However, the growth performance of the crucian carp was improved by the presence of shelter except in the presence of crayfish, in which case the shelter available did not ameliorate the negative effect of the crayfish on growth performance (i.e. an interactive effect). This result suggests that crayfish may affect the growth performance of the crucian carp through chemical cues as well as through shelter occupancy. 4. In contrast, shelter availability is the primary factor affecting the body mass loss of the cobitid fish. However, the growth performance of these fish was unaffected by the presence of crayfish. The change in the growth performance of the cobitid fish in response to the absence of shelter was greater than that of the crucian carp. This finding suggests that the cobitid fish may be more vulnerable than the crucian carp to a reduction in shelter availability. 5. Our study demonstrates that reduced shelter availability and/or crayfish invasion can have significant, indirect negative effects on the growth performance of native fish, but whether those effects are interactive might vary depending on the species. Our findings have clear implications for stream restoration and habitat assessment.