Parasites that change predator or prey behaviour can have keystone effects on community composition

Parasites play pivotal roles in structuring communities, often via indirect interactions with non-host species. These effects can be density-mediated (through mortality) or trait-mediated (behavioural, physiological and developmental), and may be crucial to population interactions, including biological invasions. For instance, parasitism can alter intraguild predation (IGP) between native and invasive crustaceans, reversing invasion outcomes. Here, we use mathematical models to examine how parasite-induced trait changes influence the population dynamics of hosts that interact via IGP. We show that trait-mediated indirect interactions impart keystone effects, promoting or inhibiting host coexistence. Parasites can thus have strong ecological impacts, even if they have negligible virulence, underscoring the need to consider trait-mediated effects when predicting effects of parasites on community structure in general and biological invasions in particular.     

Parasite-mediated predation between native and invasive amphipods

Parasites can structure biological communities directly through population regulation and indirectly by processes such as apparent competition. However, the role of parasites in the process of biological invasion is less well understood and mechanisms of parasite mediation of predation among hosts are unclear. Mutual predation between native and invading species is an important factor in determining the outcome of invasions in freshwater amphipod communities. Here, we show that parasites mediate mutual intraguild predation among native and invading species and may thereby facilitate the invasion process. We find that the native amphipod Gammarus duebeni celticus is host to a microsporidian parasite, Pleistophora sp. (new species), with a frequency of infection of 0-90%. However, the parasite does not infect three invading species, G. tigrinus, G. pulex and Crangonyx pseudogracilis. In field and laboratory manipulations, we show that the parasite exhibits cryptic virulence: the parasite does not affect host fitness in single-species populations, but virulence becomes apparent when the native and invading species interact. That is, infection has no direct effect on G. d. celticus survivorship, size or fecundity; however, in mixed-species experiments, parasitized natives show a reduced capacity to prey on the smaller invading species and are more likely to be preyed upon by the largest invading species. Thus, by altering dominance relationships and hierarchies of mutual predation, parasitism strongly influences, and has the potential to change, the outcome of biological invasions.     

How parasites affect interactions between competitors and predators

We present a synthesis of empirical and theoretical work investigating how parasites influence competitive and predatory interactions between other species. We examine the direct and indirect effects of parasitism and discuss examples of density and parasite-induced trait-mediated effects. Recent work reveals previously unrecognized complexity in parasite-mediated interactions. In addition to parasite-modified and apparent competition leading to species exclusion or enabling coexistence, parasites and predators interact in different ways to regulate or destablize the population dynamics of their joint prey. An emerging area is the impact of parasites on intraguild predation (IGP). Parasites can increase vulnerability of infected individuals to cannibalism or predation resulting in reversed species dominance in IGP hierarchies. We discuss the potential significance of parasites for community structure and biodiversity, in particular their role in promoting species exclusion or coexistence and the impact of emerging diseases. Ongoing invasions provide examples where parasites mediate native/invader interactions and play a key role in determining the outcome of invasions. We highlight the need for more quantitative data to assess the impact of parasites on communities, and the combination of theoretical and empirical studies to examine how the effects of parasitism scale up to community-level processes.     

Effects of plant invasions on the species richness of abandoned agricultural land

While exotic plant invasions are thought to lead to declines in native species, the long-term impacts of such invasions on community structure are poorly known. Furthermore, it is unknown how exotic plant invasions compare to invasions by native species. We present data from 40 yr of continuous vegetation sampling of 10 fields released from agriculture to examine the effects of invasions on species richness. The effects of both exotic and native species invasions on species richness were largely driven by variations among fields with most species not significantly affecting species richness. However, invasion and dominance by the exotics Agropyron repens, Lonicera japonica. Rosa multiflora. Trifolium pratense and the native Solidago canadensis were associated with declines in richness. Invasions by exotic and native species during old field succession have similar effects on species richness with dominance by species of either group being associated with loss of species richness. Exotic species invasions tended to have stronger effects on richness than native invasions. No evidence was found of residual effects of invasions because the impact of the invasion disappeared with the decline of the invading population. When pooled across species, heavy invasion by exotic species resulted in greater loss o species richness than invasion by native species. Studies of invasion that utilize multiple sites must account for variability among sites. In our study, had we no included field as a factor we would have incorrectly concluded that invasion consistently resulted in changes in species richness.     

Parasitism and epibiosis in native and non-native gammarids in freshwater in Ireland

The introduced amphipod crustaceans Gammarus pulex and G. tigrinus are displacing the native G. ducheni celticus in a number of freshwater sites in Northern Ireland. We investigated parasite and epibiont infection in populations in the Rivet Lagan and Lough Neagh where both native and invading species occur. Prevalence of the four parasites and epibionts observed was higher in the native G. d. celticus than in the invading amphipods at both field sites. In Lough Neagh. G. d. celticus individuals suffered higher burdens of the rotifer Embata parasitica and the protozoan Epistylis in comparison with the invading species. These patterns may reflect host specificity by the parasites or may result from different susceptibilities of the native and invading host species. We consider the influence of parasitism on host invasions and resulting species distributions.     

Regional Variation in Parasite Species Richness and Abundance in the Introduced Range of the Invasive Lionfish,Pterois volitans

Parasites can play an important role in biological invasions. While introduced species often lose parasites from their native range, they can also accumulate novel parasites in their new range. The accumulation of parasites by introduced species likely varies spatially, and more parasites may shift to new hosts where parasite diversity is high. Considering that parasitism and disease are generally more prevalent at lower latitudes, the accumulation of parasites by introduced hosts may be greater in tropical regions. The Indo-Pacific lionfish (Pterois volitans) has become widely distributed across the Western Atlantic. In this study, we compared parasitism across thirteen locations in four regions, spanning seventeen degrees of latitude in the lionfish''s introduced range to examine potential spatial variation in parasitism. In addition, as an initial step to explore how indirect effects of parasitism might influence interactions between lionfish and ecologically similar native hosts, we also compared parasitism in lionfish and two co-occurring native fish species, the graysby grouper, Cephalopholis cruentata, and the lizardfish, Synodus intermedius, in the southernmost region, Panama. Our results show that accumulation of native parasites on lionfish varies across broad spatial scales, and that colonization by ectoparasites was highest in Panama, relative to the other study sites. Endoparasite richness and abundance, on the other hand, were highest in Belize where lionfish were infected by twice as many endoparasite species as lionfish in other regions. The prevalence of all but two parasite species infecting lionfish was below 25%, and we did not detect an association between parasite abundance and host condition, suggesting a limited direct effect of parasites on lionfish, even where parasitism was highest. Further, parasite species richness and abundance were significantly higher in both native fishes compared to lionfish, and parasite abundance was negatively associated with the condition index of the native grouper but not that of the lionfish or lizardfish. While two co-occurring native fishes were more heavily parasitized compared to lionfish in Panama any indirect benefits of differential parasitism requires further investigation. Future parasitological surveys of lionfish across the eastern coast of North America and the Lesser Antilles would further resolve geographic patterns of parasitism in invasive lionfish.     

Invasibility as an emergent property of native metapopulation structure

Biological invasions constitute major threats to global biodiversity. Eco‐evolutionary considerations highlight the importance of contemporary evolution in community responses to bioinvasions. However, effects of metapopulation structure on invasion success have been mostly overlooked even though metapopulation structure determines gene flow and is likely to affect evolutionary processes. Here, we investigate a stepping‐stone model with evolving alien native interaction strengths. We demonstrate analytically that the site of invasion can determine the success of an invading consumer because gene flow and demography of a local resource species interact to obstruct local resource adaptation. Our main results are 1) that invasion success is more likely in genetic sink populations of the native species and 2) that invasion is more likely to occur against the migrational flow of native species. These findings suggest that invasibility is best regarded as an emergent property not only of communities but of entire metapopulations. Since migration networks of aliens and natives are often mismatched due to anthropogenic interference, our results indicate how population structure eases the spread of invasives against the migrational flow of natives.     

Resetting our expectations for parasites and their effects on species interactions: a meta-analysis

Despite the ubiquitous nature of parasitism, how parasitism alters the outcome of host–species interactions such as competition, mutualism and predation remains unknown. Using a phylogenetically informed meta-analysis of 154 studies, we examined how the mean and variance in the outcomes of species interactions differed between parasitized and non-parasitized hosts. Overall, parasitism did not significantly affect the mean or variance of host–species interaction outcomes, nor did the shared evolutionary histories of hosts and parasites have an effect. Instead, there was considerable variation in outcomes, ranging from strongly detrimental to strongly beneficial for infected hosts. Trophically-transmitted parasites increased the negative effects of predation, parasites increased and decreased the negative effects of interspecific competition for parasitized and non-parasitized heterospecifics, respectively, and parasites had particularly strong negative effects on host species interactions in freshwater and marine habitats, yet were beneficial in terrestrial environments. Our results illuminate the diverse ways in which parasites modify critical linkages in ecological networks, implying that whether the cumulative effects of parasitism are considered detrimental depends not only on the interactions between hosts and their parasites but also on the many other interactions that hosts experience.     

入侵植物的生理生态特性对碳积累的影响

随着国际贸易的发展和人们交往的增加以及全球环境的变化,生物种类在全球扩散的机会也大大增加,从而为生物入侵创造了机会。生物入侵不仅给农林牧生产造成损失,而且具有长期的生态学效应。外来种的成功入侵不是其自身某一个特性决定的,而是其特性与新的生境综合作用的结果。外来入侵种生理生态特性的研究对其预测和防治具有重要的意义。目前对入侵种生理生态特性的研究较少。已有的研究表明,与本地种相比入侵种可能通过提高光合能力、资源利用率、表型可塑性、化感作用,以及降低繁殖成本等增加植株碳积累,促进其入侵。但并不是所有的入侵种都同时具有这些特性。生境不同限制性资源不同,入侵机制就不同。成功的入侵种应该能够高效地利用生境中的限制性资源,并且能够较快地调节自身的生理特性以适应波动的资源环境。     

The importance of biological inertia in plant community resistance to invasion

Abstract. Insights into the ecology of historic invasions by introduced species can be gained by studying long‐term patterns of invasions by native species. In this paper, we review literature in palaeo‐ecology, forest‐stand simulation modelling, and historical studies of plant species invasions to illustrate the relevance of biological inertia in plant communities to invasion ecology. Resistance to invasion occurs in part because of environmental, demographic, and biotic factors influencing the arrival and establishment of invading species. We propose that biological inertia within the resident community is a fourth component of resistance to invasion, because of the lag time inherent in eliminating resident species and perhaps their traces after environmental conditions become suitable for invasion by immigrating species. Whether or not an introduced species invades can be conditioned by the presence of the pre‐existing community (and/or its legacy) in addition to the other biotic and abiotic factors.     

In tallgrass prairie restorations,relatedness influences neighborhood-scale plant invasion while resource availability influences site-scale invasion

Attempting to control invasive plant species in tallgrass prairie restorations is time-consuming and costly, making improved approaches for predicting and reducing invasion imperative. Both biotic and abiotic factors mediate plant invasions, and can potentially be used by restoration managers to reduce invasion rates. Biotic factors such as plant species richness and phylogenetic diversity of the native community may impact invasion. Relatedness of invading species to those in recipient communities has also been shown to influence invasion success. However, the direction of this influence is variable, reflecting Darwin’s Naturalization Conundrum. Abiotic factors such as fire regime and soil factors may impact invasion by selecting against invasive species or indicating suitable habitats for them. We surveyed 17 tallgrass prairie restorations in Illinois, USA, to investigate the effects of biotic and abiotic factors on invasion by non-native plant species at two different scales. We predicted we would find support for Darwin’s Naturalization Hypothesis at the plot (neighborhood) scale with invasion by distantly related species, and find support for the Pre-adaptation Hypothesis at the site scale. We hypothesized that biotic factors would exert more influence at the neighborhood scale, while abiotic factors would be more influential at a coarser site scale. Contrary to our expectations, at the neighborhood scale we found that closely related invasive species are more likely to invade, supporting the Pre-adaptation Hypothesis. We found that native species richness and age of restoration were negatively correlated with invasion. At the site scale, soil organic matter [SOM] concentrations and heterogeneity in SOM were positively associated with the number of invasive species while pH heterogeneity was negatively associated. Restoration practitioners may be able to reduce plant invasions by increasing native species richness, and non-native species most closely related to the resident community should potentially be prioritized as those most likely to be highly invasive.     

Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail

A robust food web is one in which few secondary extinctions occur after removing species. We investigated how parasites affected the robustness of the Carpinteria Salt Marsh food web by conducting random species removals and a hypothetical, but plausible, species invasion. Parasites were much more likely than free-living species to suffer secondary extinctions following the removal of a free-living species from the food web. For this reason, the food web was less robust with the inclusion of parasites. Removal of the horn snail, Cerithidea californica, resulted in a disproportionate number of secondary parasite extinctions. The exotic Japanese mud snail, Batillaria attramentaria, is the ecological analogue of the native California horn snail and can completely replace it following invasion. Owing to the similarities between the two snail species, the invasion had no effect on predator–prey interactions. However, because the native snail is host for 17 host-specific parasites, and the invader is host to only one, comparison of a food web that includes parasites showed significant effects of invasion on the native community. The hypothetical invasion also significantly reduced the connectance of the web because the loss of 17 native trematode species eliminated many links.     

Can Invasive Species Facilitate Native Species? Evidence of How, When, and Why These Impacts Occur

Although the predatory and competitive impacts of biological invasions are well documented, facilitation of native species by non-indigenous species is frequently overlooked. A search through recent ecological literature found that facilitative interactions between invasive and native species occur in a wide range of habitats, can have cascading effects across trophic levels, can re-structure communities, and can lead to evolutionary changes. These are critical findings that, until now, have been mostly absent from analyses of ecological impacts of biological invasions. Here I present evidence for several mechanisms that exemplify how exotic species can facilitate native species. These mechanisms include habitat modification, trophic subsidy, pollination, competitive release, and predatory release. Habitat modification is the most frequently documented mechanism, reflecting the drastic changes generated by the invasion of functionally novel habitat engineers. Further, I predict that facilitative impacts on native species will be most likely when invasive species provide a limiting resource, increase habitat complexity, functionally replace a native species, or ameliorate predation or competition. Finally, three types of facilitation (novel, substitutive, and indirect) define why exotic species can lead to facilitation of native species. It is evident that understanding biological invasions at the community and ecosystem levels will be more accurate if we integrate facilitative interactions into future ecological research. Since facilitative impacts of biological invasions can occur with native endangered species, and can have wide-ranging impacts, these results also have important implications for management, eradication, and restoration.Contribution Number 2293, Bodega Marine Laboratory, University of California at Davis.     

Evolutionary responses of native plants to novel community members

Both ecological and evolutionary processes can influence community assembly and stability, and native community members may respond both ecologically and evolutionarily as additional species enter established communities. Biological invasions provide a unique opportunity to examine these responses of native community members to novel species additions. Here, I use reciprocal transplant experiments among naturally invaded and uninvaded environments, along with experimental removals of exotic species, to determine whether exotic plant competitors and exotic insect herbivores evoke evolutionary changes in native plants. Specifically, I address whether the common native plant species Lotus wrangelianus has responded evolutionarily to a series of biological invasions by adapting to the presence of the exotic plant Medicago polymorpha and the exotic insect herbivore Hypera brunneipennis. Despite differences in selection regimes between invaded and uninvaded environments and the presence of genetic variation for traits relevant to the novel competitive and plant-herbivore interactions, these experiments failed to reveal evidence that Lotus has responded evolutionarily to the double invasion of Medicago followed by H. brunneipennis. However, when herbivory from H. brunneipennis was experimentally reduced, Lotus plants from source populations invaded by Medicago outperformed plants from uninvaded source populations when transplanted into heavily invaded destination environments. Therefore, Lotus showed evidence of adaptation to Medicago invasion but not to the newer invasion of an exotic shared herbivore. The presence of this exotic insect herbivore alters the outcome of evolutionary responses in this system and counteracts adaptation by the native Lotus to invasion by the exotic plant Medicago. This result has broad implications for the conservation of native communities. While native species may be able to adapt to the presence of one or a few exotics, a multitude of invasions may limit the ability of natives to respond evolutionarily to the novel and frequently changing selection pressures that arise with subsequent invasions.     

Are invasive plant species better competitors than native plant species? – evidence from pair‐wise experiments

Invasive plants often appear to be more competitive than native species, but there have been few tests of this hypothesis. We reviewed published pair-wise experiments between invading and native plant species. Although the designs that have been used allow only limited inferences, the available data suggest that the effect of invasive species on native species is usually stronger than vice versa. Furthermore, mixtures of invasive and native species are generally less productive than monocultures of the native species, but not less than monocultures of the invasive species. However, the selection of invaders and natives for study has not been random, and the data could be biased towards highly competitive invaders and natives that are weaker than average competitors. We attempt to clarify confusion surrounding the concept of competitive superiority in the context of plant invasions, and we discuss the limitations of the methods that have been used to investigate competition between invasive and native species. To rigorously test the generality of the hypothesis that invaders are better competitors than natives we need to compare the effects of closely related native and invasive species on each other. We suggest that the influence of an invading species on total plant community biomass is an important clue in understanding the role of competition in a plant invasion. The role of competition in the establishment and naturalization stages of the invasion process may be very different from its role in the "outbreak" stage.     

The impact of interactions on invasion and colonization resistance in microbial communities

In human microbiota, the prevention or promotion of invasions can be crucial to human health. Invasion outcomes, in turn, are impacted by the composition of resident communities and interactions of resident members with the invader. Here we study how interactions influence invasion outcomes in microbial communities, when interactions are primarily mediated by chemicals that are released into or consumed from the environment. We use a previously developed dynamic model which explicitly includes species abundances and the concentrations of chemicals that mediate species interaction. Using this model, we assessed how species interactions impact invasion by simulating a new species being introduced into an existing resident community. We classified invasion outcomes as resistance, augmentation, displacement, or disruption depending on whether the richness of the resident community was maintained or decreased and whether the invader was maintained in the community or went extinct. We found that as the number of invaders introduced into the resident community increased, disruption rather than augmentation became more prevalent. With more facilitation of the invader by the resident community, resistance outcomes were replaced by displacement and augmentation. By contrast, with more facilitation among residents, displacement outcomes shifted to resistance. When facilitation of the resident community by the invader was eliminated, the majority of augmentation outcomes turned into displacement, while when inhibition of residents by invaders was eliminated, invasion outcomes were largely unaffected. Our results suggest that a better understanding of interactions within resident communities and between residents and invaders is crucial to predicting the success of invasions into microbial communities.     

Invasions cause biodiversity loss and community simplification in vertebrate food webs

Global change is increasing the occurrence of perturbation events on natural communities, with biological invasions posing a major threat to ecosystem integrity and functioning worldwide. Most studies addressing biological invasions have focused on individual species or taxonomic groups to understand both, the factors determining invasion success and their effects on native species. A more holistic approach that considers multispecies communities and species’ interactions can contribute to a better understanding of invasion effects on complex communities. Here we address biological invasions on species‐rich food webs. We performed in silico experiments on empirical vertebrate food webs by introducing virtual species characterised by different ecological roles and belonging to different trophic groups. We varied a number of invasive species traits, including their diet breadth, the number of predators attacking them, and the bioenergetic thresholds below which invader and native species become extinct. We found that simpler food webs were more vulnerable to invasions, and that relatively less connected mammals were the most successful invaders. Invasions altered food web structure by decreasing species richness and the number of links per species, with most extinctions affecting poorly connected birds. Our food web approach allows identifying the combinations of trophic factors that facilitate or prevent biological invasions, and it provides testable predictions on the effects of invasions on the structure and dynamics of multitrophic communities.     

Higher parasite richness, abundance and impact in native versus introduced cichlid fishes

Empirical studies suggest that most exotic species have fewer parasite species in their introduced range relative to their native range. However, it is less clear how, ecologically, the loss of parasite species translates into a measurable advantage for invaders relative to native species in the new community. We compared parasitism at three levels (species richness, abundance and impact) for a pair of native and introduced cichlid fishes which compete for resources in the Panama Canal watershed. The introduced Nile tilapia, Oreochromis niloticus, was infected by a single parasite species from its native range, but shared eight native parasite species with the native Vieja maculicauda. Despite acquiring new parasites in its introduced range, O. niloticus had both lower parasite species richness and lower parasite abundance compared with its native competitor. There was also a significant negative association between parasite load (abundance per individual fish) and host condition for the native fish, but no such association for the invader. The effects of parasites on the native fish varied across sites and types of parasites, suggesting that release from parasites may benefit the invader, but that the magnitude of release may depend upon interactions between the host, parasites and the environment.     

The complex interaction network among multiple invasive bird species in a cavity-nesting community

Alien invasive species have detrimental effects on invaded communities. Aliens do not invade a vacuum, but rather a community consisting of native and often other alien species. Our current understanding of the pathways and network of interactions among multiple invasive species within whole communities is limited. Eradication efforts often focus on a single target species, potentially leading to unexpected outcomes on interacting non-target species. We aimed to examine the interaction network in a cavity-nesting community consisting of native and invasive birds. We studied the nesting cavities in the largest urban park in Israel over two breeding seasons. We found evidence for a complex interaction network that includes negative, neutral and positive interactions, but no synergistic positive interactions among aliens. Three major factors shaped the interaction network: breeding timing, nesting preferences and the ability to excavate or widen the cavities, which were found to be a limited resource. Cavity enlargement by the early-breeding invasive rose-ringed parakeet may enhance breeding of the invasive common myna in previously unavailable holes. The myna excludes the smaller invasive vinous-breasted starling, a direct competitor of the primary nest excavator, the native Syrian woodpecker. Therefore, management and eradication efforts directed towards the common myna alone may actually release the vinous-breasted starling from competitive exclusion by the common myna, increasing the negative impact of the vinous-breasted starling on the native community. As found here, interactions among multiple alien species can be crucial in shaping invasion success and should be carefully considered when aiming to effectively manage biological invasions.