Invasive species drive biodiversity loss and lead to changes in parasite–host associations. Parasites are linked to invasions and can mediate invasion success and outcomes. We review theoretical and empirical research into parasites in biological invasions, focusing on a freshwater invertebrate study system. We focus on the effects of parasitic infection on host traits (behaviour and life history) that can mediate native/invader trophic interactions. We review evidence from the field and laboratory of parasite-driven changes in predation, intraguild predation and cannibalism. Theoretical work shows that the trait-mediated effects of parasites can be as strong as classical density effects and their impact on the host’s trophic interactions merits more consideration. We also report on evidence of broader cascading effects warranting deeper study. Biological invasion can lead to altered parasite–host associations. Focusing on amphipod invasions, we find patterns of parasite introduction and loss that mirror host invasion pathways, but also highlight the risks of introducing invasive parasites. Horizon scanning and impact predictions are vital in identifying future disease risks, potential pathways of introduction and suitable management measures for mitigation.

A survey of the average date of references cited in this book serves to illustrate how our understanding of the importance of parasites in ecology has developed. We have come from a realisation that parasites can influence competitive interactions between other species (starting with Park's laboratory study of flour beetles in 1948), through the development of ideas for how parasites interact with predation (perhaps exemplified by manipulative field studies on red grouse (Hudson et al., 1992a; 1992b), to recognition of their effects in more complex modules such as intraguild predation (MacNeil et al., 2003c; Borer et al., 2007a; Hatcher et al., 2008). As this ‘pure’ science has evolved, so has its application to real-world scenarios. Along with the application of Hudson et al.'s work to gamebird management, we now recognise the importance of parasites in biological invasions (red squirrels: Tompkins et al., 2003; amphipods: Dunn, 2009; enemy release: Torchin et al., 2003), and in influencing ecosystem function (ecosystem engineering: Thomas et al., 1999; food webs: Lafferty et al., 2008a; bioenergetics: Kuris et al., 2008; carbon balance: Holdo et al., 2009). As this process of exporting basic model systems (theoretical and empirical) to inform our understanding of natural systems has developed, so has the urgency with which we need to tackle an increasing problem: that of emerging infectious diseases.

Sporadic reports appear of a mysterious disease afflicting people in a far-off country. Within weeks the disease has spread to towns and cities and is reaching epidemic proportions in that country, and within months it has circulated around the world. The origins of this new disease are initially unclear but, mysteriously, large-scale die-offs of wildlife and domestic animals presage the outbreaks in several countries. Many people and animals die; furthermore, we start to see changes throughout natural communities, involving the resources and consumers of afflicted species. Eventually the disease dies out in humans and domestic stock, and the infection, if it persists, goes largely unnoticed in a handful of wildlife species. What was going on? Could we prevent it happening again, and will there be long-term consequences for natural communities? This is the plot behind many B-movies, but also something that happens in reality all the time. For example, the recent sporadic outbreaks of highly pathogenic avian flu involve transmission though a suite of wildfowl and domestic bird species, with occasional spillover into man. At the turn of this new century, as West Nile virus (WNV) spread throughout the United States, its arrival in a new county was heralded by reports of dead and dying birds, also host to the virus.

Introduction

As long ago as the 1940s, the potential importance of parasites in influencing competition between species had been demonstrated experimentally (Park, 1948). These laboratory experiments, which have now become a classic example in ecology, showed that infection by the shared sporozoan parasite Adelina tribolii reversed the outcome of competition between two species of flour beetle (Tribolium castaneum and T. confusum). When A. tribolii was present, T. castaneum was driven extinct in 66 of the 74 mixed-species cultures. In the absence of the parasite, T. confusum went extinct in 12 out of 18 mixed-species replicates. Park also censused single-species beetle populations with and without the parasite, from which he concluded that the parasite induced higher mortality in T. castaneum, and that this effect was largely responsible for the change in competitive outcomes. This example has become a cornerstone for much of the work on the effects of parasites in communities, illustrating three key concepts that will recur in this book:

1. (1) Parasites can alter competitive relationships between host species.

2. (2) By altering interactions such as competition, parasites can play keystone roles in ecological communities. That is, the addition of a parasite species can alter the outcome of an interaction, mediating coexistence or exclusion of one or other host species with knock-on effects throughout the community.

3. (3) Alternative host species can act as reservoirs for parasite amplification, enabling maintenance of higher parasite population densities, and so providing increased opportunities to infect other species in which the parasite is more virulent.

Introduction

Biological invasions are widespread in natural and managed habitats, where they may drive changes in biodiversity and community structure, and are frequently of great economic importance (Mack et al., 2000; Pimentel et al., 2000; Lockwood et al., 2007; McGeoch et al., 2010). Understanding the mechanisms that underpin invasions is essential in predicting and managing invasion outcomes. There is growing evidence that parasites can modify the success of an invasion and its impact on the community. Furthermore, the study of biological invasions provides examples of ongoing, natural experiments in which to observe the effect of parasites on novel hosts and the impact of parasites on the wider community (Prenter et al., 2004; Dunn, 2009).

A biological invasion can be defined as the spread of a non-indigenous species from the point of introduction to some substantial level of abundance (Elton, 1958). When the invasive species is a parasite, or host to a parasite introduced with it, the novel host–pathogen interactions may sometimes also result in emerging infectious diseases (EIDs) (Chapter 8). These can include the spatial range expansion of a parasite within existing host species (e.g. the spread of malaria linked to climate change – discussed in Chapter 8), or a species range expansion to a new host species (such as spread of squirrel pox virus from grey squirrels to red squirrels – discussed in Section 2.6.1).

Introduction

In this chapter we consider how parasitism of plants affects ecological interactions directly involving plants, and also some of the population dynamic and community consequences for higher trophic levels. We might expect many of the aspects of plant–parasite interactions to mirror those in animal systems; however, in most ecosystems plants occupy the position of basal resource, so plant disease systems are potentially the best place to look for strong knock-on effects at higher trophic levels. Anticipating the results, we might expect to observe parasite-mediated or apparent competition (Chapter 2) between plant species, knock-on effects of plant disease to herbivores (mirroring knock-on effects to predators as discussed in Chapter 3), intraguild predation-like interactions between parasitic plants and their hosts or possibly between different plant natural enemies (mirroring results in Chapter 4), with effects propagating to higher trophic levels (predators of herbivores) and influencing community structure as a whole. Not all interactions involving parasites and plants are considered here: parasites of herbivores (grazers) can also affect plants via (inverted) trophic cascades (Grenfell, 1992; Dobson & Crawley, 1994); these are considered in Section 7.2.

This chapter bridges the gap between the preceding chapters that examine the mechanistic effects of parasitism within community modules (such as competition and predation) and chapters still to come which examine the broader community-level impacts of parasitism.

Introduction

The previous chapters give an indication of the numerous potential effects of parasites on ecological communities, and effects of communities on parasites. We have met some of the salient interactions in previous chapters:

• Parasites can act as keystone species determining coexistence outcomes for competing species, or as agents of apparent competition (Chapter 2).

• Parasites can alter predator–prey interactions, engaging in resource competition with predators (as parasites of prey), altering predator–prey dynamics (as parasites of predators, prey or both) and altering interaction strengths via behavioural manipulation (by trophically transmitted parasites) (Chapter 3).

• Parasites can alter or engage in intraguild predation (IGP), altering population dynamic and coexistence outcomes (Chapter 4).

• Parasites of plants can have cascading effects on consumers via their impact on the host plant; a wealth of indirect interactions between pathogens, parasites, herbivores and their natural enemies may result from plant defensive signalling (Chapter 5).

Up to this point we have looked at interactions at the level of the module, concentrating on strongly interacting subsets of species. But what are the consequences of such effects for the broader community? Do parasite-mediated interactions ramify across communities to influence food webs, community stability and structure? Perhaps these module-level interactions are ‘averaged out’ or ‘diluted’ with the addition of further species and are inconsequential for community-level processes.

Introduction

Emerging infectious diseases (EIDs) such as human immunodeficiency virus (HIV), severe acute respiratory syndrome (SARS), malaria and bovine tuberculosis have significant social and economic costs, threatening human health, wildlife conservation, biodiversity and sustainable agriculture. An EID can be broadly defined as a disease that is increasing in range, incidence or impact. This inevitably means that there is some contingency in deciding what classifies as an EID. Pathogens may be classed as emerging for a number of reasons:

1. (1) increasing incidence of infection in a host population;

2. (2) increasing severity of infection (virulence) in a host population;

3. (3) spread to novel populations;

4. (4) spread to novel species;

5. (5) a recently evolved novel pathogen or strain, including drug-resistant strains.

Some researchers confine their definitions to a subset of these processes – for instance, Woolhouse et al. (2005) are generally concerned only with categories 4 and 5 above, whereas others (Ostfeld et al., 2005; MacDonald & Laurenson, 2006) take a broader view. The term ‘re-emergence’ is sometimes used with reference to long-established infectious diseases, such as malaria and bovine tuberculosis, which are increasing in incidence. Partly resulting from differences in classification, estimates for the number of EIDs vary. Childs et al. (2007b) suggest a rule of thumb of about 30 zoonotic human EIDs in the last 30 years, whereas Jones et al. (2008) identify 335 human EID first records between 1940 and 2004; this latter study includes many novel antibiotic-resistant strains of bacteria and novel opportunistic infections associated with the pandemic spread of HIV and AIDS.

Introduction

In the preceding chapter we examined the effects of parasites on interactions between members of the same trophic level (intra- and interspecific competition and apparent competition). We can regard the indirect effects in these systems as horizontal ramifications of parasitism; however, parasites can also have vertical ramifications, affecting the interactions between species at different trophic levels. In this chapter, we look at examples of vertical ramifications, examining the role of parasites in predator–prey interactions. Parasites can enter into predation modules in a variety of ways, and their consequences for population dynamics and community structure will depend on their position in the module. We can distinguish modules involving parasites of the prey species, or of the predator species, or of both (Fig. 3.1). These modules may be further differentiated depending on the degree of predator specialisation. For instance, a specialist predator with population dynamics tightly coupled to that of its prey might be expected to be more sensitive to the impact of parasitism on the prey (Section 3.1). Nevertheless, as we examine in Section 3.2, generalist predators may be influenced by, and influence, parasitism of the prey.

Overview of predation modules

We can get some qualitative understanding of the likely impact of parasites by comparing the topologies of different predation–parasitism modules. Parasites that infect the prey species (Fig. 3.1a) are in essence competing with predators; thus the addition of parasites turns this into a competition module (with the prey/host species the resource).