Spatially limited pathogen pollution in an invasive tick and host system.

Expansion of global commerce has facilitated pathogen pollution via the transportation and translocation of invasive species and their associated parasites and pathogens. In Florida, imported cane toads (Rhinella horribilis) were accidentally and intentionally released on multiple occasions. Early populations were found to be infested with the invasive tick, Amblyomma rotundatum, yet it is unknown if these ticks dispersed with their hosts as cane toads spread throughout much of the state. The objectives of our investigation were to (1) determine if there are fewer tick infestations on toads at the periphery than at the core of their distribution as predicted by founder effect events, and (2) identify if ticks were infected with exotic pathogens. We captured toads from 10 populations across Florida. We collected ticks, vent tissue, and tick attachment site tissue from each toad, then tested samples for bacteria in the genus, Rickettsia. We found that 3/10 populations had toads that were infested with A. rotundatum, and infested individuals were in the earliest introduced populations at the core of their distribution. Pathogen testing confirmed Rickettisa bellii in ticks, but not in toad tissues. Haplotype networks could not clearly distinguish if R. bellii in Florida was more closely related to North or South American strains, but host-tick associations suggest that the pathogen was exotic to Florida. Our investigation demonstrated that an invasive species facilitated the introduction of parasites and pathogens into Florida, yet the invasive tick species encountered limitations to dispersal on this host species. Supplementary Information: The online version contains supplementary material available at 10.1007/s10530-024-03291-9.

Fungal endophytes can modulate plant invasion.

Symbiotic organisms may contribute to a host plant's success or failure to grow, its ability to maintain viable populations, and potentially, its probability of establishment and spread outside its native range. Intercellular and intracellular microbial symbionts that are asymptomatic in their plant host during some or all of their life cycle - endophytes - can form mutualistic, commensal, or pathogenic relationships, and sometimes novel associations with alien plants. Fungal endophytes are likely the most common endosymbiont infecting plants, with life-history, morphological, physiological, and plant-symbiotic traits that are distinct from other endophytic guilds. Here, we review the community dynamics of fungal endophytes during the process of plant invasion, and how their functional role may shift during the different stages of invasion: transport, introduction (colonisation), establishment, and spread. Each invasion stage presents distinct ecological filters that an alien plant must overcome to advance to the subsequent stage of invasion. Endophytes can alternately aid the host in overcoming stage-specific filters, or contribute to the barriers imposed by filters (e.g. biotic resistance), thereby affecting invasion pathways. A few fungi can be transported as seed endophytes from their native range and be vertically transmitted to future generations in the non-native range, especially in graminoids. In other plant groups, alien plants mostly acquire endophytes via horizontal transmission from the invaded plant community, and the host endophyte community is shaped by host filtering and biogeographic factors (e.g. dispersal limitation, environmental filtering). Endophytes infecting alien plants (both those transported with their host and those accumulated in the non-native range) may influence invasion success by affecting plant growth, reproduction, environmental tolerance, and pathogen and herbivory defences; however, the direction and magnitude of these effects can be contingent upon the host identity, life stage, ecological conditions, and invasion stage. This context dependence may cause endophytic fungi to shift to a non-endophytic (e.g. pathogenic) functional life stage in the same or different hosts, which can modify alien-native plant community dynamics. We conclude by identifying paths in which alien hosts can exploit the context dependency of endophyte function in novel abiotic and biotic conditions and at the different stages of invasion.

Specialist reassociation and residence time modulate the evolution of defense in invasive plants: A meta-analysis.

Invasive plants typically escape specialist herbivores but are often attacked by generalist herbivores in their introduced ranges. The shifting defense hypothesis suggests that this will cause invasive plants to evolve lower resistance against specialists, higher resistance against generalists, and greater tolerance to herbivore damage. However, the duration and direction of selective pressures can shape the evolutionary responses of resistance and tolerance for invasive plants. Two critical factors are (1) residence time (length of time that an invasive species has been in its introduced range) and (2) specialist herbivore reassociation (attack by purposely or accidentally introduced specialists). Yet, these two factors have not been considered simultaneously in previous quantitative syntheses. Here, we performed a meta-analysis with 367 effect sizes from 70 studies of 35 invasive plant species from native and invasive populations. We tested how the residence time of invasive plant species and specialist reassociation in their introduced ranges affected evolutionary responses of defenses against specialists and generalists, including herbivore resistance traits (physical barriers, digestibility reducers and toxins), resistance effects (performance of and damage caused by specialists or generalists) and tolerance to damage (from specialists or generalists). We found that residence time and specialist reassociation each significantly altered digestibility reducers, specialist performance, generalist damage, and tolerance to specialist damage. Furthermore, residence time and specialist reassociation strongly altered toxins and generalist performance, respectively. When we restricted consideration to invasive plant species with both longer residence times and no reassociation with specialists, invasive populations had lower resistance to specialists, similar resistance to generalists, and higher tolerance to damage from both herbivore types, compared with native populations. We conclude that the duration and direction of selective pressure shape the evolutionary responses of invasive plants. Under long-term (long residence time) and stable (no specialist reassociation) selective pressure, invasive plants generally decrease resistance to specialists and increase tolerance to generalist damage that provides mixed support for the shifting defense hypothesis.

A Trip Back Home: Resistance to Herbivores of Native and Non-Native Plant Populations of Datura stramonium.

When colonizing new ranges, plant populations may benefit from the absence of the checks imposed by the enemies, herbivores, and pathogens that regulated their numbers in their original range. Therefore, rates of plant damage or infestation by natural enemies are expected to be lower in the new range. Exposing both non-native and native plant populations in the native range, where native herbivores are present, can be used to test whether resistance mechanisms have diverged between populations. Datura stramonium is native to the Americas but widely distributed in Spain, where populations show lower herbivore damage than populations in the native range. We established experiments in two localities in the native range (Mexico), exposing two native and two non-native D. stramonium populations to natural herbivores. Plant performance differed between the localities, as did the abundance of the main specialist herbivore, Lema daturaphila. In Teotihuacán, where L. daturaphila is common, native plants had significantly more adult beetles and herbivore damage than non-native plants. The degree of infestation by the specialist seed predator Trichobaris soror differed among populations and between sites, but the native Ticumán population always had the lowest level of infestation. The Ticumán population also had the highest concentration of the alkaloid scopolamine. Scopolamine was negatively related to the number of eggs deposited by L. daturaphila in Teotihuacán. There was among-family variation in herbivore damage (resistance), alkaloid content (scopolamine), and infestation by L. daturaphila and T. soror, indicating genetic variation and potential for further evolution. Although native and non-native D. stramonium populations have not yet diverged in plant resistance/constitutive defense, the differences between ranges (and the two experimental sites) in the type and abundance of herbivores suggest that further research is needed on the role of resource availability and adaptive plasticity, specialized metabolites (induced, constitutive), and the relationship between genealogical origin and plant defense in both ranges.

How generalist insect herbivores respond to alien plants? The case of Aphis fabae-Myzus persicae-Rhododendron ponticum.

BACKGROUND: The enemy release hypothesis (ERH) predicts that alien plant species are unsuitable hosts for native phytophagous insects. However, the biotic resistance hypothesis (BRH) predicts that generalist herbivores may prefer an alien plant over their common host plant. In this study, we have tested these two hypotheses by comparing the potential colonization of the invasive Pontic rhododendron (Rhododendron ponticum L.) versus the common rearing host plants by two generalist aphid species (Aphis fabae and Myzus persicae). We assessed (i) the probing behavior using the electrical penetration graph (EPG) technique and (ii) survival and fecundity in Petri dishes. RESULTS: The results showed the inability of A. fabae and Myzus persicae to immediately colonize R. ponticum. Despite their ability to feed on this invasive plant, the two aphid species hardly survived and poorly reproduced. CONCLUSION: Our results are consistent with the ERH, since R. ponticum appeared as an unsuitable host for native phytophagous insects. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

A mechanistic framework of enemy release.

The enemy release hypothesis (ERH) is the best-known hypothesis explaining high performance (e.g. rapid population growth) of exotic species. However, the current framing of the ERH does not explicitly link evidence of enemy release with exotic performance. This leads to uncertainty regarding the role of enemy release in biological invasions. Here, we demonstrate that the effect of enemy release on exotic performance is the product of three factors: enemy impact, enemy diversity, and host adaptation. These factors are modulated by seven contexts: time since introduction, resource availability, phylogenetic relatedness of exotic and native species, host-enemy asynchronicity, number of introduction events, type of enemy, and strength of growth-defence trade-offs. ERH-focused studies frequently test different factors under different contexts. This can lead to inconsistent findings, which typifies current evidence for the ERH. For example, over 80% of meta-analyses fail to consider ecological contexts which can alter study findings; we demonstrate this by re-analysing a recent ERH synthesis. Structuring the ERH around factors and contexts promotes generalisable predictions about when and where exotic species may benefit from enemy release, empowering effective management. Our mechanistic factor-context framework clearly lays out the evidence required to support the ERH, unifies many enemy-related invasion hypotheses, and enhances predictive capacity.

Behavior of higher trophic levels associated with an invasive plant varies among populations.

Invasive plants from their native and introduced ranges differ in their interactions with herbivores but it is not known whether they also vary in their interactions with herbivore natural enemies. Here, we used olfactometer bioassays and cage experiments to investigate how foraging behaviors of 2 parasitoid and 1 hyperparasitoid species depended on plant population origin. Triadica sebifera (Euphorbiaceae) is native to China but invasive in the United States. In China, it is fed on by a specialist noctuid Gadirtha fusca (Lepidoptera: Nolidae), which hosts a parasitoid Apanteles sp. (Hymenoptera: Microgastinae) and hyperparasitoid (Hymenoptera: Eurytomidae) plus a generalist aphid Toxoptera odinae (Homoptera: Aphidiidae) parasitized by Lysiphlebus confusus (Hymenoptera: Aphidiinae). Both parasitoids preferred plants infested by their host over herbivore-free plants in olfactometer bioassays. Apanteles sp. and Eurytomid wasps preferred G. fusca infested plants from China populations over those from US populations in olfactometer bioassays but L. confusus wasps did not discriminate between T. odinae infested plants from China vs. US populations. Similarly, G. fusca caterpillars on China population plants were more likely to be parasitized than ones on US population plants when they were in the same cage but odds of parasitism for T. odinae did not differ for those on China vs. US population plants. These results suggest that populations from the native and introduced ranges may differ in traits that impact higher trophic levels. This may have implications for successful control of invasive plants as biocontrol agents are introduced or herbivores begin to feed on them in their introduced ranges.

The great escape: patterns of enemy release are not explained by time, space or climate.

When a plant is introduced to a new ecosystem it may escape from some of its coevolved herbivores. Reduced herbivore damage, and the ability of introduced plants to allocate resources from defence to growth and reproduction can increase the success of introduced species. This mechanism is known as enemy release and is known to occur in some species and situations, but not in others. Understanding the conditions under which enemy release is most likely to occur is important, as this will help us to identify which species and habitats may be most at risk of invasion. We compared in situ measurements of herbivory on 16 plant species at 12 locations within their native European and introduced Australian ranges to quantify their level of enemy release and understand the relationship between enemy release and time, space and climate. Overall, plants experienced approximately seven times more herbivore damage in their native range than in their introduced range. We found no evidence that enemy release was related to time since introduction, introduced range size, temperature, precipitation, humidity or elevation. From here, we can explore whether traits, such as leaf defences or phylogenetic relatedness to neighbouring plants, are stronger indicators of enemy release across species.

Exotic tree species have consistently lower herbivore load in a cross-Atlantic tree biodiversity experiment.

It is commonly expected that exotic plants experience reduced herbivory, but experimental evidence for such enemy release is still controversial. One reason for conflicting results might be that community context has rarely been accounted for, although the surrounding plant diversity may moderate enemy release. Here, we tested the effects of focal tree origin and surrounding tree diversity on herbivore abundance and leaf damage in a cross-Atlantic tree-diversity experiment in Canada and Germany. We evaluated six European tree species paired with six North American congeners in both their native and exotic range, expecting lower herbivory for the exotic tree species in each pair at each site. Such reciprocal experiments have long been called for, but have not been realized thus far. In addition to a thorough evaluation of overall enemy release effects, we tested whether enemy release effects changed with the surrounding tree diversity. Herbivore abundance was indeed consistently lower on exotics across all six tree genera (12 comparisons). This effect of exotic status was independent of the continent, phylogenetic relatedness, and surrounding tree diversity. In contrast, leaf damage associated with generalist leaf chewers was consistently higher on North American tree species. Interestingly, several species of European weevils were the most abundant leaf chewers on both continents and the dominant herbivores at the Canadian site. Thus, most observed leaf damage is likely to reflect the effect of generalist herbivores that feed heavily on plant species with which they have not evolved. At the German site, sap suckers were the dominant herbivores and showed a pattern consistent with enemy release. Taken together, the consistently lower herbivory on exotics on both continents is not purely a pattern of enemy release in the strictest sense, but to some degree additionally reflects the susceptibility of native plants to invasive herbivores. In conclusion, our cross-Atlantic study is consistent with the idea that nonnative trees have generally reduced herbivory, regardless of tree community diversity and species identity, but for different reasons depending on the dominant herbivore guild.

Gyrodactylus sprostonae Ling, 1962 infects an indigenous cyprinid in southern Africa: An expanded description.

Gyrodactylus sprostonae Ling, 1962 is a highly invasive parasite reported across freshwater environments of the northern hemisphere. The taxon was originally described from Carassius auratus (Linnaeus, 1758) and Cyprinus carpio Linnaeus, 1758 in China. This parasite has never been reported in Africa or the southern hemisphere. Recently, this taxon was collected from an indigenous yellowfish, Labeobarbus aeneus (Burchell, 1822), in the Vaal River, South Africa. The present study includes the conclusive identification of the gyrodactylid parasites collected from L. aeneus, including additional taxonomic data, using microscopy and molecular techniques. Microscopy included light microscopy (LM) of whole worms and scanning electron microscopy (SEM) of isolated haptoral sclerites. Additionally, morphometric data were obtained from SEM and compared to that generated using LM. For molecular analysis, the internal transcribed spacer (ITS) region of rDNA was amplified and phylogenetic topologies constructed. The specimens were morphometrically and genetically highly similar to other data for G. sprostonae. Additional point-to-point measurements and ITS rDNA sequences were generated for the taxon, contributing to the morphometric and molecular data for G. sprostonae. The study also includes the first study of the isolated haptoral sclerites of the taxon using SEM, with similar morphometric results to LM. This is the first record of G. sprostonae in the southern hemisphere and from a new, indigenous African host, L. aeneus, indicating host switching to smallmouth yellowfish. Furthermore, these results expand on the knowledge of the distribution of invasive parasites in South Africa, as well as Gyrodactylus species diversity in Africa.

Patterns of host-parasite coinvasion promote enemy release and specialist parasite spillover.

Species invasion and redistribution, driven by climate change and other anthropogenic influences, alter global biodiversity patterns and disrupt ecosystems. As host species move, they can bring their associated parasites with them, potentially infecting resident species, or leave their parasites behind, enhancing their competitive ability in their new ranges. General rules to predict why invading hosts will retain some parasites but not others are relatively unexplored, and the potential predictors are numerous, ranging from parasite life history to host community composition. In this study, we focus on the parasite retention process during host invasion. We used the Global Mammal Parasite Database to identify terrestrial mammal hosts sampled for parasites in both native and non-native ranges. We then selected predictors likely to play a role in parasite retention, such as parasite type, parasite specialism, species composition of the invaded community, and the invading host's phylogenetic or trait-based similarity to the new community. We modelled parasite retention using boosted regression trees, with a suite of 25 predictors describing parasite and host community traits. We further tested the generality of our predictions by cross-validating models on data for other hosts and invasion locations. Our results show that parasite retention is nonrandom and predictable across hosts and invasions. It is broadly shaped by parasite type and parasite specialism, with more specialist parasites that infect many closely related hosts more likely to be retained. This trend is pronounced across parasite types; helminths, however, show a more uniform likelihood of retention regardless of specificity. Overall, we see that most parasites are not retained (11% retained), meaning many invasive species may benefit from enemy release. However, species redistribution does have the potential to spread parasites, and this also has great relevance to understanding conservation implications of species invasions. We see that specialist parasites are most likely to coinvade with their hosts, which suggests that species closely related to the invasive hosts are most likely to be affected by parasite spillover.

Plant-soil interactions in the native range of two congeneric species with contrasting invasive success.

The aim of this study was to compare plant-soil interactions in the native range of two congeneric European species differing in their invasive success in the world: a globally invasive Cirsium vulgare and non-invasive C. oleraceum. We assessed changes in soil nutrients and soil biota following soil conditioning by each species and compared performance of plants grown in self-conditioned and unconditioned soil, from which all, some or no biota was excluded. The invasive species depleted more nutrients than the non-invasive species and coped better with altered nutrient levels. The invasive species had higher seedling establishment which benefited from the presence of unconditioned biota transferred by soil filtrate. Biomass of both species increased in soil with self-conditioned soil filtrate and decreased in soil with self-conditioned whole-soil inoculum compared to unconditioned filtrate and inoculum. However, the increase was smaller and the decrease greater for the invasive species. The invasive species allocated less biomass to roots when associated with harmful biota, reducing negative effects of the biota on its performance. The results show that in the native range the invasive species is more limited by self-conditioned pathogens and benefits more from unconditioned mutualists and thus may benefit more from loss of effectively specialized soil biota in a secondary range. Our study highlights the utility of detailed plant-soil feedback research in species native range for understanding factors regulating species performance in their native range and pinpointing the types of biota involved in their regulation.

Parasites of Perccottus glenii Dybowski, 1877 (Actinopterygii: Odontobutidae) in the native and the introduced host range: Abundance-occupancy and abundance-variance relationships.

The Chinese sleeper Perccottus glenii Dybowski, 1877 is an invasive fish species rapidly expanding in Siberia and Europe. Its native range encompasses the Far East region of Russia, northeastern China and northern North Korea. We studied species composition, prevalence, mean abundance and variance of mean abundance of macroparasites of the Chinese sleeper in the native and the introduced range. The species composition of the parasite component communities differed considerably in the native and the introduced range. The frequency distributions of prevalence, mean abundance and variance of mean abundance of the parasites did not demonstrate any significant differentiation between the two parts of the host range. However, an analysis of the abundance-occupancy and the abundance-variance relationships revealed that the parasite component communities in the two parts of the host range were quite distinct. In the native range, prevalence increased faster and variance increased more slowly with the increasing abundance of the parasites than in the introduced range. These features are mostly associated with considerably increased prevalence, abundance and aggregation of the host-specific cestode Nippotaenia mogurndae in recipient water bodies as compared with the native habitats.

Advancing the missed mutualist hypothesis, the under-appreciated twin of the enemy release hypothesis.

Introduced species often benefit from escaping their enemies when they are transported to a new range, an idea commonly expressed as the enemy release hypothesis. However, species might shed mutualists as well as enemies when they colonize a new range. Loss of mutualists might reduce the success of introduced populations, or even cause failure to establish. We provide the first quantitative synthesis testing this natural but often overlooked parallel of the enemy release hypothesis, which is known as the missed mutualist hypothesis. Meta-analysis showed that plants interact with 1.9 times more mutualist species, and have 2.3 times more interactions with mutualists per unit time in their native range than in their introduced range. Species may mitigate the negative effects of missed mutualists. For instance, selection arising from missed mutualists could cause introduced species to evolve either to facilitate interactions with a new suite of species or to exist without mutualisms. Just as enemy release can allow introduced populations to redirect energy from defence to growth, potentially evolving increased competitive ability, species that shift to strategies without mutualists may be able to reallocate energy from mutualism toward increased competitive ability or seed production. The missed mutualist hypothesis advances understanding of the selective forces and filters that act on plant species in the early stages of introduction and establishment and thus could inform the management of introduced species.

The distribution of covert microbial natural enemies of a globally invasive crop pest, fall armyworm, in Africa: Enemy release and spillover events.

Invasive species pose a significant threat to biodiversity and agriculture world-wide. Natural enemies play an important part in controlling pest populations, yet we understand very little about the presence and prevalence of natural enemies during the early invasion stages. Microbial natural enemies of fall armyworm Spodoptera frugiperda are known in its native region, however, they have not yet been identified in Africa where fall armyworm has been an invasive crop pest since 2016. Larval samples were screened from Malawi, Rwanda, Kenya, Zambia, Sudan and Ghana for the presence of four different microbial natural enemies; two nucleopolyhedroviruses, Spodoptera frugiperda NPV (SfMNPV) and Spodoptera exempta NPV (SpexNPV); the fungal pathogen Metarhizium rileyi; and the bacterium Wolbachia. This study aimed to identify which microbial pathogens are present in invasive fall armyworm, and determine the geographical, meteorological and temporal variables that influence prevalence. Within 3 years of arrival, fall armyworm was exposed to all four microbial natural enemies. SfMNPV probably arrived with fall armyworm from the Americas, but this is the first putative evidence of host spillover from Spodoptera exempta (African armyworm) to fall armyworm for the endemic pathogen SpexNPV and for Wolbachia. It is also the first confirmed incidence of M. rileyi infecting fall armyworm in Africa. Natural enemies were localised, with variation being observed both nationally and temporally. The prevalence of SfMNPV (the most common natural enemy) was predominantly explained by variables associated with the weather; declining with increasing rainfall and increasing with temperature. However, virus prevalence also increased as the growing season progressed. The infection of an invasive species with a natural enemy from its native range and novel pathogens specific to its new range has important consequences for understanding the population ecology of invasive species and insect-pathogen interactions. Additionally, while it is widely known that temporal and geographic factors affect insect populations, this study reveals that these are important in understanding the distribution of microbial natural enemies associated with invasive pests during the early stages of invasion, and provide baseline data for future studies.

Role of enemy release and hybridization in the invasiveness of Impatiens balfourii and I. glandulifera.

Comparative studies with taxonomically and geographically paired alien species that exhibit different degrees of success in their invasions may help to identify the factors that determine invasiveness. Examples of such species in Europe include the noninvasive Impatiens balfourii and invasive I. glandulifera. We tested whether the low invasiveness of I. balfourii in Europe may be explained by strong pressure from local enemies. Earlier studies of these two species provided support for their hybridization. We tested this phenomenon as the potential occurrence of I. glandulifera × I. balfourii hybrids might promote the evolution of the invasiveness of I. balfourii. Both species were germinated from seeds collected in 2015 on the Swiss-Italian border in Insubria and utilized in three experiments: (1) a common garden enemy release test (leaf damage or pest pressure), (2) a test of the pressure exerted by a generalist enemy and (3) hybridization test. In the first test, the effect of enemies was assessed by the level of leaf damage and the number of pests. In the second test, a food choice experiment with a generalist herbivore (Cepaea snails) was performed. In the hybridization test, the plants were placed in a climatic chamber for self-pollination and hand cross-pollination. Analyses of enemy release and Cepaea snail preference revealed that I. balfourii experienced higher enemy pressure than I. glandulifera; however, this was not reflected in the performance of the plants. Although I. glandulifera was larger, I. balfourii had greater fecundity. Thus, the invasion success of I. glandulifera could not be unambiguously attributed to its greater degree of release from enemies compared with the noninvasive I. balfourii. Additionally, we did not obtain any evidence of hybridization between the two species. Thus, we obtained no support for the hypothesis that the evolution of the invasiveness of I. balfourii could be enhanced through hybridization with I. glandulifera.

An intercontinental comparison of insect seed predation between introduced and native oaks.

Novel interactions between introduced oaks and their natural enemies across different continents provide an opportunity to test the enemy release hypothesis (ERH) at local and global scales. Based on the ERH, we assessed the impacts of native seed-feeding insects on introduced and native oaks within and among continents. We combined a common-garden experiment in China and biogeographic literature surveys to measure seed predation by insects and the proportion of acorn embryos surviving after insect infestation among 4 oak species with different geographical origins: Quercus mongolica origin from China, Q. robur and Q. petraea from Europe, and Q. rubra from North America. Mostly supporting the ERH, oaks in introduced continents escaped seed predation compared to those in native continents and compared to other native oaks in introduced continents. Common-garden comparisons showed that total acorn infestation rate of introduced Q. rubra (section Lobatae) was considerably lower than that of native oaks (section Quercus) in China and Europe, likely because of the differences in seed traits associated with different oak sections. Literature surveys showed that seed predation of introduced oaks was lower in the introduced continent than in the native continent. Embryo survival was higher in introduced Q. rubra than native oaks in China and Poland. However, insect seed predation of recently introduced Q. rubra in China was similar to that in Europe, which is not consistent with the ERH. Our results suggest that reduced acorn attack by native insects and higher embryo survival after acorn damage could increase the establishment success or invasion risk of introduced oaks in non-native continents.