Plant Invasions

The Role of Biotic Interactions

Anna Traveset, David M. Richardson, Anna Traveset, David M Richardson

• Verlag: CAB International
• Jahr: 2020
• ISBN:
  9781789242195
• Thema: Sciences biologiques
• Thema: Botanique

There are many books on aspects of plant invasions, but none that focus on the key role of species interactions in mediating invasions. This book reviews exciting new findings and explores how new methods and tools are shedding new light on crucial processes in plant invasions.In 23 chapters, with contributions from 51 authors, the book addresses: · the main theories and hypotheses in plant invasion ecology that invoke species interactions;· plant invasions that are facilitated by, or benefit from, by mutualistic interactions and release from enemies;· antagonistic interactions that prevent or hinder plant invasions;· impacts of plant invasions on native species interactions and ecosystem functioning;· the interaction-network approach to understanding plant invasions;· the importance of considering species interactions in managing plant invasions

1 Plant Invasions: The Role of Biotic Interactions – An Overview

Anna Traveset^1* and David M. Richardson²

¹Mediterranean Institute of Advanced Studies, CSIC-UIB, E07190 Esporles, Mallorca, Balearic Islands, Spain; ²Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

*Corresponding author: [email protected]

© CAB International 2020. Plant Invasions: The Role of Biotic Interactions (eds Anna Traveset and David M. Richardson) DOI: 10.1079/9781789242171.0001

Abstract

Diverse biotic interactions between non-native plant species and other species from all taxonomic groups are crucial mediators of the dynamics of plant invasions. This chapter reviews the key hypotheses in invasion ecology that invoke biotic interactions to explain aspects of plant invasion dynamics. We examine the historical context of these hypotheses and assess the evidence for accepting or rejecting their predictions.

Most hypotheses invoke antagonistic interactions, mainly competition, predation, herbivory interactions and the role of pathogens. Only in the last two decades have positive (facilitative/mutualistic) interactions been explicitly included in invasion biology theory (as in ecological theory in general). Much information has accumulated in testing hypotheses relating to biotic resistance and Enemy Release Theory, although many of the emerging generalizations are still contentious. There is growing consensus that other drivers of plant invasion success, such as propagule pressure and disturbance, mediate the outcome of biotic interactions, thereby complicating our ability to make predictions, but these have rarely been assessed in both native and adventive ranges of non-native invasive species. It is also widely acknowledged that biogeographic comparisons, more than common garden experiments, are needed to shed light on many of the contradictory results. Contrasting findings have also emerged in exploring the roles of positive interactions. Despite strong evidence that such interactions are crucial in many communities, more work is needed to elucidate the factors that influence the relative importance of positive and negative interactions in different ecosystems. Different types of evidence in support of invasional meltdown have emerged for diverse habitats and across spatial scales. In light of increasing evidence that biotic indirect effects are crucial determinants of the structure, dynamics and evolution of ecological communities, both direct and indirect interactions involving native and non-native species must be considered to determine how they shape plant invasion patterns and the ecological impacts of non-native species on recipient communities.

Research that examines both biotic interactions and the factors that mediate their strength and alter interaction outcomes is needed to improve our ability to predict the effects of novel interactions between native and non-native species, and to envisage how existing invaded communities will respond to changing environmental conditions. Many opportunities exist for manipulating biotic interactions as part of integrated control strategies to reduce the extent, density and impacts of non-native plant invasions. These include the introduction of species from the native range of the non-native plant for biological control, diverse manipulations of plant—herbivore interactions and many types of interaction to enhance biotic resistance and steer vegetation recovery following non-native plant control.

1.1 The Role of Biotic Interactions in Ecology and Biogeography

1.1.1 Types of biotic interactions

Biotic interactions are those relationships that occur between at least two organisms of one or more species. The outcome of such relationships may result in the involved organisms benefiting, being harmed or being unaffected, depending on the environmental context in which the interaction takes place. Most biotic interactions involve the uptake of resources (nutrients, light, water, etc.) needed to survive, while others involve the exchange of goods and services such as protection, shelter or transport. Biotic interactions have long been categorized based on their effects on the interacting species (Fig. 1.1). Thus, competition exists when individuals of the interacting species are impaired due to resource or space limitation.

Predation is another antagonistic interaction that takes place when one individual benefits from another species by consuming it, either totally or partially, potentially leading to death of the prey. Variations of this antagonistic interaction include parasitism and herbivory, in which the consequences for the ‘attacked’ individual depend on the magnitude and duration of the interaction. When only one interacting species is negatively affected, the interaction is termed amensalism. Mutualism, on the other hand, is a win—win interaction involving two individuals of different species both of which benefit from the interaction. The most widespread examples of this category of interaction in plant ecology are pollination, seed dispersal and symbiosis (the latter defined as mutualism in which there is prolonged physical intimacy between partner species, e.g. mycorrhizal and endophytic fungi; Bronstein, 2015). When only one species benefits the interaction is called commensalism. Despite this operational categorization, there is often a continuum of interactions that extends from antagonism to mutualism depending on the context, on the costs and benefits that they represent, or on the stage of the life history of the interacting species (e.g. Pringle, 2016; Fig. 1.1). For instance, one animal species may act as a herbivore (or nectar robber) at the flowering stage, but may be a legitimate seed disperser of the same plant species later in the plant’s life cycle. In the case of sexual deception, plants (mainly orchids) fool pollinators by producing structures that resemble female pollinators without providing them with any reward.

Fig. 1.1. Interaction compass displaying the range of possible interspecific biotic interactions. Signs indicate individual fitness or population growth rate: (+) positive effect, (-) negative effect and (0) neutral or no effect. The magnitude of the net interaction effect increases away from the centre. Despite such an operational categorization of interactions, a continuum of interactions exists – extending from antagonism to mutualism – depending on (a) the context, e.g. nutrient availability and density– dependent population dynamics; (b) the costs and benefits that they represent; or (c) the stage of the life history of the interacting species (adapted from Fig. 2 in Richardson et al., 2000a and Fig. 1 in Pringle, 2016).

1.1.2 The influence of biotic interactions in ecological and evolutionary processes

All of the biotic interactions mentioned above potentially affect different components of individual fitness (survival, growth, reproductive success), thereby influencing demographic, ecological (e.g. population growth rate, species abundance and distribution) and evolutionary processes (e.g. natural selection, gene flow, coevolution). We cannot understand the evolution of species without considering such interactions, and biotic interactions actually promote the evolution of multiple adaptations. They are therefore among the most important drivers (if not the most important one) of the huge biodiversity on Earth. Mutualistic interactions between plants and fungal symbionts were crucial for the colonization of land and have driven the diversification of life (Kiers et al., 2010). To comprehend patterns of biodiversity at local, regional or global scales, it is now widely acknowledged that we must consider not only the species that live in particular areas but also interactions among them (see below). Several studies in the last two decades have highlighted the importance of integrating biotic interactions into models to achieve more accurate predictions of the spatial and temporal variation of species distribution, and to understand community assembly patterns (e.g. Guisan and Thuiller, 2005; Boulangeat et al., 2012; Godsoe et al., 2017; Pearson et al., 2018a). Using a novel integrated approach to interaction distribution modelling, Gravel et al. (2018) developed a quantitative theory to explain turnover of interactions in space and time. They propose that the ecological niche should encompass the effect of the environment on both species distribution (the Grinnellian dimension of the niche) and the ecological interactions among species (the Eltonian dimension), and call for adopting the view that community structure is best represented as a network of ecological interactions.

Besides being fundamental drivers of biodiversity and helping to explain the spatial and temporal distribution of species, biotic interactions also play fundamental roles in ecosystem functioning. They mediate most energy and nutrient assimilation and their flow through trophic chains and the decomposition of organic matter. Many plants depend, for instance, on indirect interactions with bacteria to obtain the nitrogen they need to perform photosynthesis; c. 80% of legumes (with c. 20,000 species, including many important crops) have rhizo-bial symbiosis. Nearly 95% of the world’s plant species belong to families that are characteristically mycorrhizal (Pringle et al., 2009). More than 90% of flowering plants are pollinated by animals (Ollerton et al., 2011), and many plants produce seeds that rely on dispersal by animals to sustain populations and to colonize new habitats (up to 90% of plant species in the tropics require animals for dispersal; Farwig and Berens, 2012). Many plant—plant interactions are also mediated by interactions with other organisms, notably herbivores and pathogens (see below).

Interactions among species have been included in ecological theory since the early 20th century, especially after Lotka (1925) and Volterra (1926) developed their famous equations that described competition and predation between two or more species as a means to understand population growth and species coexistence in a community. Subsequent decades saw vigorous debates over Gause’s (1934) ‘competitive exclusion principle’ which posited that two species cannot coexist on one limiting resource (Hart et al., 2018). Another topic of hot debate was whether populations were regulated by density-dependent or density-independent factors. Hutchinson’s (1957) formalization of the niche concept invoked only antagonistic interactions, leading to widespread acceptance that the ‘realized niche’ (parts of the environment that a species occupies in the presence of interactors, e.g. competitors, predators) is always smaller than the ‘fundamental niche’ (parts of the environment that a species can occupy in the absence of interactions with other species). Ecologists have for decades built theories of community organization that drew, explicitly or implicitly, on Hutchinson’s conceptualization of the niche. MacArthur and Levins (1967) developed the concept of ‘limiting similarity’, the minimal niche difference between two competing species that would allow them to coexist. Community ecology progressed over the ensuing half century thanks to the development of this theoretical framework that, it was thought, provided a foundation for predicting the number and types of species in natural communities based on a functional limit to the similarity of competing species (May and McArthur, 19 72; May, 1977). However, predictions of limiting similarity were found to be model-dependent, and the comparison of models including interspecific interactions gave similar results to models that excluded them (i.e. null models). Such findings challenged the overly simplistic idea that interspecific competition was the only or even the most important factor involved in structuring communities. It was not until early in the 21st century (Bruno et al., 2003) that positive interactions such as mutualism or commensalism began being incorporated explicitly in theoretical models, although previous studies had already dragged facilitation into modern community ecology (e.g. Bertness and Callaway, 1994). Such work showed that the realized niche can in fact be larger than the fundamental niche, and that ‘incorporating facilitative interactions into ecological theory would lead to more accurate and inclusive understanding of natural communities’ (Mittelbach and McGill, 2019). Many subsequent studies have shown that positive interactions are at least as important as negative ones in mediating the structure and functioning of ecosystems (Kiers et al., 2010).

Contrary to classic models that consider mutualisms to be destabilizing (May, 1981; Allesina and Tang, 2012), ecologists now recognize that these positive interactions are fundamental determinants of community-wide stability (Mougi and Kondoh, 2012; McIntire and Fajardo, 2014). The biological mechanisms that underlie the stabilizing effects of mutualisms are, however, still far from clear. Network studies have shed light on such mechanisms (Benadi et al., 2012; Minoarivelo and Hui, 2016; Hale et al., 2020). Benadi et al. (2012) were the first to consider the stability of a pollination network in a broad context, by evaluating the variation in the pollination mutualism and the degree of resource competition among plant species. They found that the effects of pollinators on the stability of the plants they visit depend on the extent to which plant resource use overlaps, and on the degree of pollinator specialization. Minoarivelo and Hui (2016) pointed out that it is necessary to distinguish ecological from evolutionary stability, and claimed that inferring network function from structure is problematic. More recently, Hale et al. (2020) suggested that mechanistic network theory could synthesize different types of ecological interactions, thereby elucidating how mutualism can enhance the diversity, stability and function of complex ecosystems.

The study of biotic interactions involving invasive species has particularly contributed substantially to the advancement of ecology and biogeography. In fact, non-native species provide natural ‘species-addition experiments’ in a wide range of habitat types which allow us to assess whether and how their effects can drive...

Inhaltsverzeichnis

• Cover
• Half-title Page
• Title Page
• Copyright
• Contents
• List of Contributors
• Acknowledgements
• Glossary
• 1. Plant Invasions: The Role of Biotic Interactions – An Overview
• 2. The Role of Biotic Interactions in Invasion Ecology: Theories and Hypotheses
• 3. Soil Biota and Non-native Plant Invasions
• 4. Pollination Interactions Promoting Plant Invasions
• 5. Seed Dispersal Interactions Promoting Plant Invasions
• 6. Ungulates as Dispersal Vectors of Non-native Plants
• 7. The Role of Plant–Plant Facilitation in Non-native Plant Invasions
• 8. How Direct and Indirect Non-native Interactions Can Promote Plant Invasions, Lead to Invasional Meltdown and Inform Management Decisions
• 9. Biotic Resistance to Plant Invasionsm
• 10. EICA 2.0: A General Model of Enemy Release and Defence in Plant and Animal Invasions
• 11. The Role of Pathogens in Plant Invasions
• 12. Direct and Indirect Effects of Herbivores Influencing Plant Invasions
• 13. Impacts of Non-native Plants on Plant–Pollinator Interactions
• 14. The Effect of Non-native Plant Invasions on the Dispersal of Native Seeds
• 15. Allelopathic Disruptions of Biotic Interactions Due to Non-native Plants
• 16. Competition Between Native and Non-native Plants
• 17. Indirect Biotic Interactions of Plant Invasions with Native Plants and Animals
• 18. How a Network Approach Has Advanced the Field of Plant Invasion Ecology
• 19. Molecular Ecology of Plant–Microbial Interactions During Invasions: Progress and Challenges
• 20. How Can Progress in the Understanding of Antagonistic Interactions be Applied to Improve Biological Control of Plant Invasions?
• 21. Restoration of Pollination Interactions in Communities Invaded by Non-native Plants
• 22. Restoration of Seed Dispersal Interactions in Communities Invaded by Non-native Plants
• 23. Multiple Feedbacks Due to Biotic Interactions across Trophic Levels Can Lead to Persistent Novel Conditions That Hinder Restoration
• Taxonomic Index
• General Index
• Backcover