Biotic resistance or invasional meltdown? Diversity reduces invasibility but not exotic dominance in southern California epibenthic communities

High community diversity may either prevent or promote the establishment of exotic species. The biotic resistance hypothesis holds that species-rich communities are more resistant to invasion than species-poor communities due to greater interspecific competition. Conversely, the invasional meltdown hypothesis proposes that greater exotic diversity increases invasibility via facilitative interactions between exotic species. To evaluate the degree to which biotic resistance or invasional meltdown influences marine community structure during the assembly period, we studied the development of marine epibenthic “fouling” communities at two southern California harbors. We found that fewer exotic species established as total and exotic richness increased during community assembly and that this effect remained after accounting for space availability. We also found that changes in exotic abundance decreased over time. Throughout the assembly period, gains in exotic abundance were greatest when space was abundant and richness was low. Altogether, we found greater support for biotic resistance than invasional meltdown, suggesting that both native and exotic species contribute to biotic resistance during early community development. However, this resistance may not reduce the total dominance of exotic species.

Seed dispersal interactions promoting plant invasions.

Animal dispersers are essential for many non-native plants since they facilitate seed movement and might promote seed germination and seedling establishment, thereby increasing their chances of invasion. This chapter reviews the published literature on seed dispersal of non-native plant species by native and/or non-native animals. The following questions are addressed: (i) Are interactions between non-native plants and their animal dispersers evenly studied worldwide? (ii) Which are the distinctive traits (i.e. geographical origin, life form, dispersal strategy and propagule traits) of non-native plants that are dispersed by animals? (iii) Which are the most studied groups of dispersers of non-native plants around the world? (iv) Does the literature provide evidence for the Invasional Meltdown Hypothesis (non-native plant-non-native disperser facilitation)? (v) What is the role of animal dispersers at different stages of the non-native plant regeneration process? Our dataset of 204 articles indicates that geographical distribution of the studies was highly heterogeneous among continents, with the highest number coming from North America and the lowest from Asia and Central America. Most of the non-native plants involved in dispersal studies were woody species from Asia with fleshy fruits dispersed by endozoochory. More than the half of the animal dispersal agents noted were birds, followed by mammals, ants and reptiles. The dominance of bird-dispersal interactions over other animal groups was consistent across geographical regions. Although most of the studies involved only native dispersers, interactions among non-native species were detected, providing support for the existence of invasional meltdown processes. Of the total number of reviewed articles reporting seed removal, 74% evaluated seed dispersal, but only a few studies included seed germination (35.3%), seedling establishment (5.4%) or seed predation (23.5%). Finally, we discuss some research biases and directions for future studies in the area.

Disruption of cross-feeding interactions by invading taxa can cause invasional meltdown in microbial communities

The strength of biotic interactions within an ecological community affects the susceptibility of the community to invasion by introduced taxa. In microbial communities, cross-feeding is a widespread type of biotic interaction that has the potential to affect community assembly and stability. Yet, there is little understanding of how the presence of cross-feeding within a community affects invasion risk. Here, I develop a metabolite-explicit model where native microbial taxa interact through both cross-feeding and competition for metabolites. I use this model to study how the strength of biotic interactions, especially cross-feeding, influence whether an introduced taxon can join the community. I found that stronger cross-feeding and competition led to much lower invasion risk, as both types of biotic interactions lead to greater metabolite scarcity for the invader. I also evaluated the impact of a successful invader on community composition and structure. The effect of invaders on the native community was greatest at intermediate levels of cross-feeding; at this ‘critical’ level of cross-feeding, successful invaders generally cause decreased diversity, decreased productivity, greater metabolite availability, and decreased quantities of metabolites exchanged among taxa. Furthermore, these changes resulting from a successful primary invader made communities further susceptible to future invaders. The increase in invasion risk was greatest when the network of metabolite exchange between taxa was minimally redundant. Thus, this model demonstrates a case of invasional meltdown that is mediated by initial invaders disrupting the metabolite exchange networks of the native community.

Soil-microbes-mediated invasional meltdown in plants

While most alien species fail to establish, some invade native communities and become widespread. Many of these communities have been invaded by multiple aliens, suggesting that aliens may cause invasional meltdowns. Here, we tested whether and how a third plant species affects the competitive outcome between alien and native plants through its soil legacy. We first conditioned soil with one of ten species (six natives and four aliens) or without plants. Then, we grew on these 11 soils, five aliens and five natives without competition, and with intra- or interspecific competition (all pairwise alien-native combinations). We found that aliens were not more competitive than natives when grown on soil conditioned by other natives or on non-conditioned soil. However, aliens were more competitive than natives on soil conditioned by other aliens. Although soil conditioning rarely affected the strength of competition between later plants, soil conditioned by aliens changed the competitive outcomes by affecting growth of aliens less negatively than that of natives. Microbiome analysis confirmed this finding by showing that the soil-legacy effects of one species on later species were less negative when their fungal endophyte communities were less similar; and that fungal endophyte communities were less similar between two aliens than between aliens and natives. Our study suggests that coexistence between aliens and natives is less likely with more alien species. Such invasional meltdown is likely mediated by spill-over of fungal endophytes, some of which are pathogenic.

Disruption of cross-feeding interactions by invading taxa can cause invasional meltdown in microbial communities

The strength of biotic interactions within an ecological community affects the susceptibility of the community to invasion by introduced taxa. In microbial communities, cross-feeding is a widespread type of biotic interaction that has the potential to affect community assembly and stability. Yet, there is little understanding of how the presence of cross-feeding within a community affects invasion risk. Here, I develop a metabolite-explicit model where native microbial taxa interact through both cross-feeding and competition for metabolites. I use this model to study how the strength of biotic interactions, especially cross-feeding, influence whether an introduced taxon can join the community. I found that stronger cross-feeding and competition led to much lower invasion risk, as both types of biotic interactions lead to greater metabolite scarcity for the invader. I also evaluated the impact of a successful invader on community composition and structure. The effect of invaders on the native community was greatest at intermediate levels of cross-feeding; at this “critical” level of cross-feeding, successful invaders generally causing decreased diversity, decreased productivity, greater metabolite availability, and decreased quantities of metabolites exchanged among taxa. Furthermore, these changes resulting from a successful primary invader made communities further susceptible to future invaders. The increase in invasion risk was greatest when the network of metabolite exchange between taxa was minimally redundant. Thus, this model demonstrates a case of invasional meltdown that is mediated by initial invaders disrupting the metabolite exchange networks of the native community.

How direct and indirect non-native interactions can promote plant invasions, lead to invasional meltdown and inform management decisions.

In 1999, Daniel Simberloff and Betsy Von Holle introduced the term 'invasional meltdown'. The term and the concept have been embraced and critiqued but have taken a firm hold within the invasion biology canon. The original formulation of the concept argued two key points: first, biologists rarely study how non-natives interact with one another. Second, nearly all the conceptual models about the success and impact of invasive species are predicated on the importance of competitive interactions and an implicit assumption that non-natives should interfere with establishment, spread and impact of other non-natives. In response, Simberloff and Von Holle called for more research on invader interactions and proposed an alternative consequence of non-native species interactions - invasional meltdown - where facilitative interactions among non-natives could increase the invasion rate or ecological impacts in invaded systems. This chapter outlines the primary pathways in which direct and indirect interactions among non-natives could lead to invasional meltdown. It provides examples of how different types of interactions among non-natives could lead to net positive effects on the invasion success of non-native plants or the impact of non-native plants on invaded ecosystems. Direct effects are by far the most commonly explored form of non-native- non- native interaction, primarily focusing on plant mutualisms with pollinators, seed dispersers or soil microbial mutualists. There are, however, also examples of non-native plants that benefit from commensal and even herbivorous interactions with other non-natives. Indirect interactions among non-natives are very infrequently studied. Although examples are scarce, non-natives may indirectly benefit other non-native plants through trophic cascades, apparent competition and indirect mutualisms. It remains unclear whether indirect effects are important pathways to invasional meltdown. More work is needed on studying ecosystems that are invaded by multiple non-native species and we need to consider the full range of interactions among non-natives that could either stymie or promote their spread, population growth and impact. Only then can we address how common facilitative interactions are relative to competitive interactions among non-natives or provide robust suggestions on how to manage ecosystems.

Seed dispersal interactions promoting plant invasions.

Animal dispersers are essential for many non-native plants since they facilitate seed movement and might promote seed germination and seedling establishment, thereby increasing their chances of invasion. This chapter reviews the published literature on seed dispersal of non-native plant species by native and/or non-native animals. The following questions are addressed: (i) Are interactions between non-native plants and their animal dispersers evenly studied worldwide? (ii) Which are the distinctive traits (i.e. geographical origin, life form, dispersal strategy and propagule traits) of non-native plants that are dispersed by animals? (iii) Which are the most studied groups of dispersers of non-native plants around the world? (iv) Does the literature provide evidence for the Invasional Meltdown Hypothesis (non-native plant-non-native disperser facilitation)? (v) What is the role of animal dispersers at different stages of the non-native plant regeneration process? Our dataset of 204 articles indicates that geographical distribution of the studies was highly heterogeneous among continents, with the highest number coming from North America and the lowest from Asia and Central America. Most of the non-native plants involved in dispersal studies were woody species from Asia with fleshy fruits dispersed by endozoochory. More than the half of the animal dispersal agents noted were birds, followed by mammals, ants and reptiles. The dominance of bird-dispersal interactions over other animal groups was consistent across geographical regions. Although most of the studies involved only native dispersers, interactions among non-native species were detected, providing support for the existence of invasional meltdown processes. Of the total number of reviewed articles reporting seed removal, 74% evaluated seed dispersal, but only a few studies included seed germination (35.3%), seedling establishment (5.4%) or seed predation (23.5%). Finally, we discuss some research biases and directions for future studies in the area.