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Superior predatory ability and abundance predicts potential ecological impact towards early-stage anurans by invasive 'Killer Shrimp' (Dikerogammarus villosus).

ABSTRACT: Invasive alien species negatively impact upon biodiversity and generate significant economic costs worldwide. Globally, amphibians have suffered considerable losses, with a key driver being predation by large invasive invertebrate and vertebrate predators. However, there is no research regarding the potential ecological impact of small invertebrate invaders. The invasive freshwater amphipod Dikerogammarus villosus can act as a top predator capable of displacing native amphipods and preying heavily upon a range of native species. Listed as one of Europe's top 100 worst invaders, D. villosus has significantly restructured freshwater communities across western Europe and is expected to invade North America in the near future. Here we explore the ecological impact of invasive D. villosus upon UK native and invasive amphibians (Rana temporaria and Xenopus laevis respectively) using the "Relative Impact Potential" (RIP) metric. By combining estimations of per capita effects (i.e. functional response; FR) and relative field abundances, we apply the RIP metric to quantify the potential ecological impact of invasive D. villosus upon embryonic and larval amphibian prey, compared to the native amphipod Gammarus pulex. Both native and invasive amphipods consumed early-stage amphibians and exhibited potentially destabilising Type II FRs. However, larger body size in invasive D. villosus translated into a superior FR through significantly lower handling times and subsequently higher maximum feeding rates-up to seven times greater than native G. pulex. Higher invader abundance also drove elevated RIP scores for invasive D. villosus, with potential impact scores predicted up to 15.4 times greater than native G. pulex. Overall, D. villosus is predicted to have a greater predatory impact upon amphibian populations than G. pulex, due primarily to its larger body size and superior field abundance, potentially reducing amphibian recruitment within invaded regions.

SUBMITTER: Warren DA

PROVIDER: S-EPMC7907340 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Superior predatory ability and abundance predicts potential ecological impact towards early-stage anurans by invasive 'Killer Shrimp' (Dikerogammarus villosus).

Warren Daniel A DA Bradbeer Stephanie J SJ Dunn Alison M AM

Scientific reports 20210225 1

Invasive alien species negatively impact upon biodiversity and generate significant economic costs worldwide. Globally, amphibians have suffered considerable losses, with a key driver being predation by large invasive invertebrate and vertebrate predators. However, there is no research regarding the potential ecological impact of small invertebrate invaders. The invasive freshwater amphipod Dikerogammarus villosus can act as a top predator capable of displacing native amphipods and preying heavi ...[more]

PMID: 33633148

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Project description:The amphipod Dikerogammarus villosus has colonized most of the European main inland water bodies in less than 20 years, having deteriorating effect on the local benthic communities. Our aim was to reveal the species phylogeography in the native Black Sea area, to define the source populations for the colonization routes in continental Europe and for the newly established UK populations. We tested for the loss of genetic diversity between source and invasive populations as well as along invasion route. We tested also for isolation by distance. Thirty three native and invasive populations were genotyped for mtDNA (COI, 16S) and seven polymorphic nuclear microsatellites to assess cryptic diversity (presence of deeply divergent lineages), historical demography, level of diversity within lineage (e.g., number of alleles), and population structure. A wide range of methods was used, including minimum spanning network, molecular clock, Bayesian clustering and Mantel test. Our results identified that sea level and salinity changes during Pleistocene impacted the species phylogeography in the Black Sea native region with four differentiated populations inhabiting, respectively, the Dnieper, Dniester, Danube deltas and Durungol liman. The invasion of continental Europe is associated with two sources, i.e., the Danube and Dnieper deltas, which gave origin to two independent invasion routes (Western and Eastern) for which no loss of diversity and no isolation by distance were observed. The UK population has originated in the Western Route and, despite very recent colonization, no drastic loss of diversity was observed. The results show that the invasion of the killer shrimp is not associated with the costs of loosing genetic diversity, which may contribute to the success of this invader in the newly colonized areas. Additionally, while it has not yet occurred, it might be expected that future interbreeding between the genetically diversified populations from two independent invasion routes will potentially even enhance this success.

Project description:Temperature is a crucial factor determining biology and ecology of poikilothermic animals. It often constitutes an important barrier for invasive species originating from different climate zones but, on the other hand, may facilitate the invasion process of animals with wide thermal preferences and high resistance to extreme temperatures. In our experimental study, we investigated the thermal behaviour of two Ponto-Caspian amphipod crustaceans-Dikerogammarus villosus and Dikerogammarus haemobaphes. Both species are known to live under a wide range of thermal conditions which may promote their invasion. Moreover, both these amphipods are hosts for microsporidian parasites which co-evolved with them within the Ponto-Caspian region and spread in European waters. As the presence of a parasite may influence the thermal preferences of its host, we expected to observe behavioural changes in infected individuals of the studied amphipods leading to (1) behavioural fever (selecting a warmer habitat) or (2) anapyrexia (selecting a colder habitat). The experiment (N = 20) was carried out for 30 min in a 100 cm. 20 cm from boths sides were not avaliable for amphipods long thermal gradient (0-40 °C), using 30 randomly selected adult amphipod individuals of one species. At the end of each trial, we checked the position of amphipods along the gradient and determined their sex and infection status (uninfected or infected by one of microsporidium species). D. villosus was infected with Cucumispora dikerogammari whereas D. haemobaphes was a host for C. dikerogammari, Dictyocoela muelleri or D. berillonum. Thermal preferences of amphipods depended on their species and sex. Females of D. villosus preferred warmer microhabitats (often much above 30 °C) than conspecific males and females of D. haemobaphes, whereas no significant differences were found among males of both species and both sexes of D. haemobaphes. Moreover, infected males of D. villosus stayed in warmer water more often than uninfected males of this species, selecting temperatures higher than 30 °C, which may be explained either as a behavioural fever constituting a defence mechanism of a host against the infection, or as a parasite manipulation of the host behaviour increasing the parasite fitness. On the other hand, none of the parasite species affected the thermal preferences of D. haemobaphes, including also C. dikerogammari, changing the behaviour of D. villosus. Our research presents the complexity of the thermal behaviour of studied amphipods and the evidence that microsporidia may trigger a change in temperature preferendum of their host species and those observations may be the result of different host-parasite coevolution time which may vary for the two host species (Poulin, 2010).

Project description:A large number of descriptive surveys have shown that microbial communities experience successional changes over time and that ecological dominance is common in the microbial world. However, direct evidence for the ecological processes mediating succession or causing ecological dominance remains rare. Different dispersal abilities among species may be a key mechanism. We surveyed fungal diversity within a metacommunity of pitchers of the model carnivorous plant Sarracenia purpurea and discovered that the yeast Candida pseudoglaebosa was ecologically dominant. Its frequency in the metacommunity increased during the growing season, and it was not replaced by other taxa. We next measured its competitive ability in a manipulative laboratory experiment and tracked its dispersal over time in nature. Despite its dominance, C. pseudoglaebosa is not a superior competitor. Instead, it is a superior disperser: it arrives in pitchers earlier, and disperses into more pitchers, than other fungi. Differential dispersal across the spatially structured metacommunity of individual pitchers emerges as a key driver of the continuous dominance of C. pseudoglaebosa during succession.IMPORTANCE Microbial communities are ubiquitous and occupy nearly every imaginable habitat and resource, including human-influenced habitats (e.g., fermenting food and hospital surfaces) and habitats with little human influence (e.g., aquatic communities living in carnivorous plant pitchers). We studied yeast communities living in pitchers of the carnivorous purple pitcher plant to understand how and why microbial communities change over time. We found that dispersal ability is not only important for fungal communities early in their existence, it can also determine which species is dominant (here, the yeast Candida pseudoglaebosa) long after the species and its competitors have arrived. These results contrast with observations from many human-influenced habitats, in which a good competitor eventually outcompetes good dispersers, since humans often design these habitats to favor a specific competitor. This study will help microbiologists understand the qualities of microbial species that enable takeover of new habitats in both natural and human-influenced environments.

Project description:Predators shape prey populations by elimination of individuals (consumptive effects) and by inducing modifications in prey behaviour, physiology or morphology (NCE-non-consumptive effects). Due to the resource allocation to defence, decreased feeding and higher stress, the costs of predator NCEs can be considerable. Therefore, the resistance to NCEs may be crucial for population growth and interspecific competition. We tested the resistance of Ponto-Caspian gammarids Dikerogammarus villosus and Pontogammarus robustoides to NCEs imposed by their predator, the racer goby Babka gymnotrachelus. As D. villosus is often avoided by predators in the presence of alternative food, we hypothesised that it would bear lower behavioural and physiological costs of anti-predator responses. We tested gammarid feeding in short-time experiments (2-4 h) with food (chironomid larvae) located at various distances from the stony shelter (to enforce food searching, Experiment I) or in the direct gammarid proximity (no searching needed, Experiment II). Moreover, we checked the predator effect on gammarid growth in a 2-week Experiment III. Both gammarids exposed to predators reduced feeding efficiency outside the shelter (Experiment I). Contrary to our expectations, the response of D. villosus was stronger. When food was provided in their direct proximity (Experiment II), the feeding of both species was unaffected by predators, indicating that a shelter supplied with food can reduce predator NCEs. The growth of P. robustoides was reduced in the presence of predators (Experiment III), whereas that of D. villosus was unaffected. Although D. villosus has a more effective defence strategy than P. robustoides, it bears similar or even higher behavioural costs of NCEs. However, it exhibits the higher resistance to the long-term predator presence, sustaining its growth rate under such conditions. This may be one of the factors contributing to the great invasion success of D. villosus, currently taking place in European fresh waters.

Dataset Information

Superior predatory ability and abundance predicts potential ecological impact towards early-stage anurans by invasive 'Killer Shrimp' (Dikerogammarus villosus).

Publications

Superior predatory ability and abundance predicts potential ecological impact towards early-stage anurans by invasive 'Killer Shrimp' (Dikerogammarus villosus).

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