Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host

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Parasites and invasions: a biogeographic examination of parasites and hosts in native and introduced ranges

Aim To use a comparative approach to understand parasite demographic patterns in native versus introduced populations, evaluating the potential roles of host invasion history and parasite life history. Location North American east and west coasts with a focus on San Francisco Bay (SFB). Methods Species richness and prevalence of trematode parasites were examined in the native and introduced ranges of two gastropod host species, Ilyanassa obsoleta and Littorina saxatilis. We divided the native range into the putative source area for introduction and areas to the north and south; we also sampled the overlapping introduced range in SFB. We dissected 14,781 snails from 103 populations and recorded the prevalence and identity of trematode parasites. We compared trematode species richness and prevalence across the hosts’ introduced and native ranges, and evaluated the influence of host availability on observed patterns. Results Relative to the native range, both I. obsoleta and L. saxatilis have escaped (lost) parasites in SFB, and L. saxatilis demonstrated a greater reduction of trematode diversity and infection prevalence than I. obsoleta. This was not due to sampling inequalities between the hosts. Instead, rarefaction curves suggested complete capture of trematode species in native source and SFB subregions, except for L. saxatilis in SFB, where infection was extremely rare. For I. obsoleta, infection prevalence of trematodes using fish definitive hosts was significantly lower in SFB compared to the native range, unlike those using bird hosts. Host availability partly explained the presence of introduced trematodes in SFB. Main conclusions Differential losses of parasite richness and prevalence for the two gastropod host species in their introduced range is probably the result of several mechanistic factors: time since introduction, propagule pressure, vector of introduction, and host availability. Moreover, the recent occurrence of L. saxatilis’ invasion and its active introduction vector suggest that its parasite diversity and distribution will probably increase over time. Our study suggests that host invasion history and parasite life history play key roles in the extent and diversity of trematodes transferred to introduced populations. Our results also provide vital information for understanding community‐level influences of parasite introductions, as well as for disease ecology in general.     

A trematode parasite alters growth,feeding behavior,and demographic success of invasive rusty crayfish (Orconectes rusticus)

Nonindigenous species can cause major changes to community interactions and ecosystem processes. The strong impacts of these species are often attributed to their high demographic success. While the importance of enemy release in facilitating invasions has often been emphasized, few studies have addressed the role of parasites in the invasive range in controlling demographic success of potential invaders. Here we examine whether a trematode parasite (Microphallus spp.) can contribute to previously documented alternate states in the abundance of invasive rusty crayfish (Orconectes rusticus) in north temperate lakes in Wisconsin, USA. Microphallus infect O. rusticus after emerging from their first intermediate host, a hydrobiid snail. As previously documented, O. rusticus reduce densities of hydrobiid snails through direct predation and destruction of macrophyte habitat. Therefore, if Microphallus substantially reduce O. rusticus fitness, these parasites may reinforce a state of low crayfish abundance, and, at the other extreme, abundant crayfish may repress these parasites, reinforcing a state of high crayfish abundance. From samples collected from 109 sites in 16 lakes, we discovered (1) a positive relationship between crayfish infection intensity and hydrobiid snail abundance, (2) a negative relationship between parasite prevalence and crayfish abundance, and (3) a negative relationship between parasite prevalence and crayfish population growth. With experiments, we found that infection with Microphallus reduced foraging behavior and growth in O. rusticus, which may be the mechanisms responsible for the population reductions we observed. Overall results are consistent with the hypothesis that Microphallus contributes to alternate states in the abundance and impacts of O. rusticus.     

Invasive parasites are detectable by their abundance-occupancy relationships: the case of helminths from Liza haematocheilus (Teleostei: Mugilidae)

The biogeographic patterns of abundance and prevalence of helminths from Liza haematocheilus were studied across its native (Sea of Japan) and introduced (Sea of Azov) distribution ranges. Abundance-occupancy relationships (AORs) were tested for the core-satellite and enemy release (ERH) species hypotheses in eight and 14 host samples from the native and introduced host ranges, respectively. The AOR model fitted parasite data extremely well, irrespective of whether the host or the parasite species were native or invasive. Except for co-introduced monogeneans, species were less abundant and prevalent in the introduced host population than in the native one, which agrees well with the ERH. Two occupancy patterns were observed. A unimodal, right-skewed distribution of prevalence frequency was common for the acquired groups of helminth parasites in the introduced range, whereas a bimodal distribution was more common in the native range. Core species in the native range were monogeneans, adult and larval digeneans, whereas host-specific, co-introduced monogeneans were the only core species in the introduced range. Acquired grey-mullet specialists and host generalists infected only a small portion of the introduced host population with low mean abundance. These results indicate that strict host specificity, together with a direct life cycle, are the traits that enabled helminth species to entirely occupy the invasive host population. The AORs showed that parasite individuals tend to accumulate in a relatively small fraction of susceptible introduced hosts, probably as an adaptation to enhance mating opportunities, thereby providing a mechanistic explanation of the ERH. All this evidence suggests that co-introduced and acquired species use the introduced host population in very different ways. Therefore, we posit that the examination of AORs can be instrumental in understanding the role of co-introduced parasites in invasion theory.     

Local diversity reduces infection risk across multiple freshwater host‐parasite associations

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Is invasion success explained by the enemy release hypothesis?

A recent trend in invasion ecology relates the success of non‐indigenous species (NIS) to reduced control by enemies such as pathogens, parasites and predators (i.e. the enemy release hypothesis, ERH). Despite the demonstrated importance of enemies to host population dynamics, studies of the ERH are split – biogeographical analyses primarily show a reduction in the diversity of enemies in the introduced range compared with the native range, while community studies imply that NIS are no less affected by enemies than native species in the invaded community. A broad review of the invasion literature implies at least eight non‐exclusive explanations for this enigma. In addition, we argue that the ERH has often been accepted uncritically wherever (i) NIS often appear larger, more fecund, or somehow ‘better’ than either congeners in the introduced region, or conspecifics in the native range; and (ii) known enemies are conspicuously absent from the introduced range. However, all NIS, regardless of their abundance or impact, will lose natural enemies at a biogeographical scale. Given the complexity of processes that underlie biological invasions, we argue against a simple relationship between enemy ‘release’ and the vigour, abundance or impact of NIS.     

Parasite-mediated enemy release and low biotic resistance may facilitate invasion of Atlantic coral reefs by Pacific red lionfish (<Emphasis Type="Italic">Pterois volitans</Emphasis>)

Successful invasions are largely explained by some combination of enemy release, where the invader escapes its natural enemies from its native range, and low biotic resistance, where native species in the introduced range fail to control the invader. We examined the extent to which parasites may mediate both release and resistance in the introduction of Pacific red lionfish (Pterois volitans) to Atlantic coral reefs. We found that fewer lionfish were parasitized at two regions in their introduced Atlantic range (The Bahamas and the Cayman Islands) than at two regions in their native Pacific range (the Northern Marianas Islands and the Philippines). This pattern was largely driven by relatively high infection rates of lionfish by didymozoan fluke worms and parasitic copepods (which may be host-specific to Pterois lionfishes) in the Marianas and the Philippines, respectively. When compared with sympatric, native fishes in the Atlantic, invasive lionfish were at least 18 times less likely to host a parasite in The Bahamas and at least 40 times less likely to host a parasite in the Cayman Islands. We found no indication that lionfish introduced Pacific parasites into the Atlantic. In conjunction with demographic signs of enemy release such as increased density, fish size, and growth of invasive lionfish, it is possible that escape from parasites may have contributed to the success of lionfish. This is especially true if future studies reveal that such a loss of parasites has led to more energy available for lionfish growth, reproduction, and/or immunity.     

Reduction in post-invasion genetic diversity in <Emphasis Type="Italic">Crangonyx pseudogracilis</Emphasis> (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites?

Parasites can strongly influence the success of biological invasions. However, as invading hosts and parasites may be derived from a small subset of genotypes in the native range, it is important to examine the distribution and invasion of parasites in the context of host population genetics. We demonstrate that invasive European populations of the North American Crangonyx pseudogracilis have experienced a reduction in post-invasion genetic diversity. We predict that vertically transmitted parasites may evade the stochastic processes and selective pressures leading to enemy release. As microsporidia may be vertically or horizontally transmitted, we compared the diversity of these microparasites in the native and invasive ranges of the host. In contrast to the reduction in host genetic diversity, we find no evidence for enemy release from microsporidian parasites in the invasive populations. Indeed, a single, vertically transmitted, microsporidian sex ratio distorter dominates the microsporidian parasite assemblage in the invasive range and appears to have invaded with the host. We propose that overproduction of female offspring as a result of parasitic sex ratio distortion may facilitate host invasion success. We also propose that a selective sweep resulting from the increase in infected individuals during the establishment may have contributed to the reduction in genetic diversity in invasive Crangonyx pseudogracilis populations.     

Comparison of invertebrate herbivores on native and non‐native Senecio species: Implications for the enemy release hypothesis

The enemy release hypothesis posits that non‐native plant species may gain a competitive advantage over their native counterparts because they are liberated from co‐evolved natural enemies from their native area. The phylogenetic relationship between a non‐native plant and the native community may be important for understanding the success of some non‐native plants, because host switching by insect herbivores is more likely to occur between closely related species. We tested the enemy release hypothesis by comparing leaf damage and herbivorous insect assemblages on the invasive species Senecio madagascariensis Poir. to that on nine congeneric species, of which five are native to the study area, and four are non‐native but considered non‐invasive. Non‐native species had less leaf damage than natives overall, but we found no significant differences in the abundance, richness and Shannon diversity of herbivores between native and non‐native Senecio L. species. The herbivore assemblage and percentage abundance of herbivore guilds differed among all Senecio species, but patterns were not related to whether the species was native or not. Species‐level differences indicate that S. madagascariensis may have a greater proportion of generalist insect damage (represented by phytophagous leaf chewers) than the other Senecio species. Within a plant genus, escape from natural enemies may not be a sufficient explanation for why some non‐native species become more invasive than others.     

Has the introduction of brown trout altered disease patterns in native New Zealand fish?

1. It is well recognised that non-indigenous species (NIS) can affect native communities via the 'spillover' of introduced parasites. However, two other potentially important processes, the 'spillback' of native parasites from a competent NIS host, where the latter acts as a reservoir leading to amplified infection in native hosts, and the 'dilution' of parasitism by a NIS host acting as a sink for native parasites, have either not been tested or largely overlooked.
2. We surveyed the helminth parasite fauna of native New Zealand fish in Otago streams that varied in the abundance of introduced brown trout Salmo trutta , to look for evidence of spillback and/or dilution. Spillover is not an issue in this system, with trout introduced as parasite-free eggs.
3. Seven native parasite species were present across 12 sites; significant inverse relationships with an index of trout abundance (i.e. dilution) were documented for three species infecting the native upland bully Gobiomorphus breviceps , and one species infecting the native roundhead galaxias Galaxias anomalus .
4. An inverse relationship between bully energy status and infection intensity of one parasite species suggests that parasite dilution could have positive effects on bully populations. Our failure to detect similar relationships for the other parasites does not preclude the possibility that dilution is beneficial to native fish, since parasites may have subtle or unmeasured impacts.
5. The parasite dilution patterns reported are compelling in that they occurred across several native host and parasite species; as such they have important implications for invasion ecology, providing an interesting contrast to the largely negative impacts reported for NIS. Mechanisms potentially responsible for the patterns observed are discussed.     

Complex interactions among a nematode parasite (Daubaylia potomaca), a commensalistic annelid (Chaetogaster limnaei limnaei), and trematode parasites in a snail host (Helisoma anceps)

Many biotic interactions can affect the prevalence and intensity of parasite infections in aquatic snails. Historically, these studies have centered on interactions between trematode parasites or between trematodes and other organisms. The present investigation focuses on the nematode parasite Daubaylia potomaca and its interactions with a commensal, Chaetogaster limnaei limnaei , and a variety of trematode species. It was found that the presence of C. l. limnaei indirectly increased the mean intensity of D. potomaca infections, apparently by acting as a restraint for various trematode parasites, particularly the rediae of Echinostoma sp. In turn, Echinostoma sp. rediae adversely affected the mean intensity of D. potomaca by their consumption of both juvenile and adult nematodes present in tissues of the snail. These organisms not only belong to 3 different phyla but occupy distinct trophic levels as well. The complex interactions among these 3 organisms in the snail host provide an excellent example of biotic interactions influencing the infection dynamics of parasites in aquatic snails.     

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.     

Aggregation patterns of helminth populations in the introduced fish, Liza haematocheilus (Teleostei: Mugilidae): disentangling host–parasite relationships

A number of hypotheses exist to explain aggregated distributions, but they have seldom been used to investigate differences in parasite spatial distribution between native and introduced hosts. We applied two aggregation models, the negative binomial distribution and Taylor’s power law, to study the aggregation patterns of helminth populations from Liza haematocheilus across its native (Sea of Japan) and introduced (Sea of Azov) distribution ranges. In accordance with the enemy release hypothesis, we predicted that parasite populations in the introduced host range would be less aggregated than in the native host area, because aggregation is tightly constrained by abundance. Contrary to our expectation, aggregation of parasite populations was higher in the introduced host range. However, the analyses suggested that the effect of host introduction on parasite aggregation depends on whether parasite species, or higher level taxonomic groups, were acquired in or carried into the new area. The revealed similarity in the aggregation parameters of co-introduced monogeneans can be attributed to the repeatability and identity of the host–parasite systems. In contrast, the degree of aggregation differed markedly between regions for higher level taxa, which are represented by the native parasites in the Sea of Japan versus the acquired species in the Sea of Azov. We propose that the host species plays a crucial role in regulating infra-population sizes of acquired parasites due to the high rate of host-induced mortality. A large part of the introduced host population may remain uninfected due to their resistance to native naïve parasites. The core concept of our study is that the comparative analysis of aggregation patterns of parasites in communities and populations, and macroecological relationships, can provide a useful tool to reveal cryptic relationships in host–parasite systems of invasive hosts and their parasites.     

An efficient strategy to estimate intensity and prevalence: sampling metacercariae in fishes

Accurate estimates of population-level parameters of parasites, such as prevalence and mean intensity, require large sample sizes. The processing of such samples becomes an overwhelming task when parasites are abundant, as with trematode metacercariae in fishes. In the present study, a subsampling method reduced processing time while maintaining an accurate estimation of metacercariae prevalence and intensity across 3 trematode species and 2 fish species. By double sampling, we generated regression models to predict total intensity from a combination of subsamples. The key to this approach lies in choosing the best strategy from a large number of potential subsampling routines. We selected the most efficient routine by weighing the costs and benefits of each. This approach, however, could not provide an estimate of parasite abundance when no parasites occurred in the initial subsample. To estimate prevalence accurately, our subsampling algorithm prescribed an additional sampling sequence using a new, optimal regression model. In addition, we optimized the technique to measure three parasite species infecting a single host simultaneously. This efficient subsampling procedure decreased the overall processing time per host by up to 91% while obtaining accurate (R2 > 0.8) estimates for both prevalence and intensity.     

Ecological determinants of parasite acquisition by exotic fish species

Disease‐mediated threats posed by exotic species to native counterparts are not limited to introduced parasites alone, since exotic hosts frequently acquire native parasites with possible consequences for infection patterns in native hosts. Several biological and geographical factors are thought to explain both the richness of parasites in native hosts, and the invasion success of free‐living exotic species. However, the determinants of native parasite acquisition by exotic hosts remain unknown. Here, we investigated native parasite communities of exotic freshwater fish to determine which traits influence acquisition of native parasites by exotic hosts. Model selection suggested that five factors (total body length, time since introduction, phylogenetic relatedness to the native fish fauna, trophic level and native fish species richness) may be linked to native parasite acquisition by exotic fish, but 95% confidence intervals of coefficient estimates indicated these explained little of the variance in parasite richness. Based on R²‐values, weak positive relationships may exist only between the number of parasites acquired and either host size or time since introduction. Whilst our results suggest that factors influencing parasite richness in native host communities may be less important for exotic species, it seems that analyses of general ecological factors currently fail to adequately incorporate the physiological and immunological complexity of whether a given animal species will become a host for a new parasite.     

Little evidence for release from herbivores as a driver of plant invasiveness from a multi‐species herbivore‐removal experiment

Enemy release is frequently posed as a main driver of invasiveness of alien species. However, an experimental multi‐species test examining performance and herbivory of invasive alien, non‐invasive alien and native plant species in the presence and absence of natural enemies is lacking. In a common garden experiment in Switzerland, we manipulated exposure of seven alien invasive, eight alien non‐invasive and fourteen native species from six taxonomic groups to natural enemies (invertebrate herbivores), by applying a pesticide treatment under two different nutrient levels. We assessed biomass production, herbivore damage and the major herbivore taxa on plants. Across all species, plants gained significantly greater biomass under pesticide treatment. However, invasive, non‐invasive and native species did not differ in their biomass response to pesticide treatment at either nutrient level. The proportion of leaves damaged on invasive species was significantly lower compared to native species, but not when compared to non‐invasive species. However, the difference was lost when plant size was accounted for. There were no differences between invasive, non‐invasive and native species in herbivore abundance. Our study offers little support for invertebrate herbivore release as a driver of plant invasiveness, but suggests that future enemy release studies should account for differences in plant size among species.     

Biogeography of parasitism in freshwater fish: spatial patterns in hot spots of infection

Contrary to species occurrence, little is known about the determinants of spatial patterns of intraspecific variation in abundance, particularly for parasitic organisms. In this study, we provide a multi‐faceted overview of spatial patterns in parasite abundance and examine several potential underlying processes. We first tested for a latitudinal gradient in local abundance of the regionally most common parasite species and whether these species achieve higher abundances at the same localities (shared hot spots of infection). Secondly, we tested whether intraspecific similarity in local abundance between sites follows a spatial distance decay pattern or is better explained by variation in extrinsic biotic and abiotic factors between localities related to local parasite transmission success. We examined the infection landscape of a model fish host system (common and upland bullies, genus Gobiomorphus: Eleotridae) across its entire distributional range. We applied general linear models to test the effect of latitude on each species local abundance independently, including the abundance of each co‐infecting species as another predictor. We computed multiple regressions on distance matrices among localities based on abundance of each of the four most common trematode species, as well as for geographic distance, biotic and abiotic distinctness of the localities. Our results showed that the most widely distributed parasites of bullies also achieve the highest mean local abundances, following the abundance – occupancy relationship. Variation in local abundance of any focal parasite species was independent of latitude, the abundance of co‐occurring species and spatial distance or disparity in biotic attributes between localities. For only one parasite species, similarity of abundance between sites covaried with the extent of abiotic differences between sites. The lack of association between hot spots of infection for co‐occurring species reinforces the geographic mosaic scenario in which hosts and parasites coevolve by suggesting non‐deterministic, species‐specific variation in parasite abundance across space.     

Associations between shorebird abundance and parasites in the sand crab, Emerita analoga, along the California coast

I investigated spatial variation in the prevalence and abundance of 4 species of parasites in the sand crab, Emerita analoga, on 8 sandy beaches along 800 km of the California coast, to assess the importance of bird abundance for the distribution of parasites among sand crab populations. I collected sand crabs and counted shorebirds and gulls at each beach during June and November 1994. Sand crabs served as intermediate hosts for 4 species of parasites, including a trematode, Spelotrema nicolli (Cable and Hunnienen, 1938); an acanthocephalan, Polymorphus kenti (Van Cleave, 1947); a nematode, Proleptus sp., and an unidentified trypanorhynch tapeworm. Among sand crab populations, there was substantial spatial variation in the prevalence and abundance of each parasite species. No latitudinal pattern was apparent for any of the 4 species observed. Temporally, parasite prevalence and abundance was significantly different between dates for all 4 parasites. Specifically, sand crab populations experienced higher trematode, nematode, and trypanorhynch prevalence and abundance in November than in June. In contrast, prevalence and abundance of acanthocephalans were higher in June than in November. There were strong positive associations between bird abundance and prevalence of parasitic infection for trematodes and acanthocephalans for some dates but not for nematodes or trypanorhynchs, which use elasmobranchs as definitive hosts. The spatial variation in prevalence and abundance of trematodes and acanthocephalans observed among sand crab populations may be attributed to the distribution and abundance of shorebirds and gulls that serve as definitive hosts.     

Experimental warming drives a seasonal shift in the timing of host‐parasite dynamics with consequences for disease risk

Multi‐species experiments are critical for identifying the mechanisms through which climate change influences population dynamics and community interactions within ecological systems, including infectious diseases. Using a host–parasite system involving freshwater snails, amphibians and trematode parasites, we conducted a year‐long, outdoor experiment to evaluate how warming affected net parasite production, the timing of infection and the resultant pathology. Warming of 3 °C caused snail intermediate hosts to release parasites 9 months earlier and increased infected snail mortality by fourfold, leading to decreased overlap between amphibians and parasites. As a result, warming halved amphibian infection loads and reduced pathology by 67%, despite comparable total parasite production across temperature treatments. These results demonstrate that climate–disease theory should be expanded to account for predicted changes in host and parasite phenology, which may often be more important than changes in total parasite output for predicting climate‐driven changes in disease risk.