Parasites and Biological Invasions

By Alison M Dunn, Karolina Bacela-Spychalska, Louise Barwell and 23 more

Biological invasions - the introduction, establishment and spread of invasive alien species - are complex global phenomena that can cause significant environmental, ecological, and economic harm. Along with the direct effects of an invasive host organism, there is the additional threat of co-introduced pathogenic and parasitic species. Co-introduced parasites can affect the success of the invasive organism but can also go on to infect hosts in the new range, resulting in novel ecological interactions and complex impacts. These 'Invasive Parasites' can have profound impacts on the success of a biological invasion, and can pose a significant risk to wildlife, in addition to organisms cultured for agriculture and aquaculture.

Compiling information on parasite invasions for the first time, this unique book:

- provides an in-depth resource on parasite invasions, revealing the subtleties underlying biological invasions and co-introduced disease;
- examines the phenomenon and consequences of parasite release in invaded host communities;
- explores parasite invasion impacts, interactions and diagnostic techniques;
- includes case studies across a broad range of hosts (plants, vertebrates and invertebrates) and parasites (viruses to large Metazoa), from a plethora of aquatic and terrestrial environments.

Authored by leading researchers in the discipline, this new book is a useful tool for helping invasion researchers incorporate disease data into their invasion models, as well a vital resource for researchers, policy makers, and environmental managers that are more generally interested in the myriad consequences of species invasions

• Language: English
• Publisher: CAB International
• Release date: Oct 31, 2023
• ISBN: 9781789248135

Book preview

1 Parasites in Biological Invasions: an Introduction

Alison M. Dunn¹*, April M.H. Blakeslee² and Jamie Bojko³,⁴

¹University of Leeds, Leeds, UK; ²East Carolina University, Greenville, North Carolina, USA; ³Teesside University, Middlesbrough, UK; ⁴National Horizons Centre, Teesside University, Darlington, UK

*Corresponding author: [e-mail]

© CAB International 2023. Parasites and Biological Invasions (eds J. Bojko et al.)

DOI: 10.1079/9781789248135.0001

Abstract

Biological invasions can result in the co-introduction of parasitic hitchhikers. These ‘invasive parasites’ include viruses, bacteria, fungi, protists and metazoan symbionts, and they can have diverse effects on the ecological and evolutionary dynamics of their invasive hosts and recipient communities. Some invasive parasites are agents of disease, and the spread of these parasites could ultimately harm biodiversity, global economies and human health. In this introduction, we highlight the significance of researching and understanding parasite invasions, and we include key examples that demonstrate why investigations of parasite invasions should be a critical scientific objective across institutions and management agencies around the globe. The introduction to this book provides an overview of each chapter and their broad aims. The layout of chapters follow the ‘introduction, arrival, establishment and impact’ process of a biological invasion, but the examples in this book specifically draw upon bioinvasions that are understood to have accompanying parasitological implications.

1.1 Background

Invasive species are one of the key drivers of global biodiversity loss (IPBES, 2023), with their impact on agriculture, aquaculture and ecosystem function and services estimated to cause economic losses totalling between US$47 and US$163 billion per annum (Diagne et al., 2021). Parasitic diseases similarly threaten biodiversity and ecosystem services (Roy et al., 2017; Paseka et al., 2020). For example, the ongoing European-wide decline in populations of ash trees (Fraxinus excelsior) is driven by the invasive fungus Hymenoscyphus fraxineus, which has both economic and ecological impacts. Extinctions are predicted for a swathe of communities that are directly or indirectly dependent on ash trees for food and/or habitat (Hultberg et al., 2020). Furthermore, the H. fraxineus invasion is considered to have a £15 billion economic impact in Britain alone (Hill et al., 2019). Another interesting and informative example comes from a castrating, body-snatching parasite, Loxothylacus panopaei (Rhizocephala), which infects several species of mud crab. L. panopaei has invaded western Atlantic estuaries along the US coast following intentional translocations of eastern oysters (Crassostrea virginica) from the Gulf of Mexico to the Chesapeake Bay (Fig. 1.1). Oysters provide habitat for numerous species, and it is likely that infected mud crabs were part of those translocations (Hines et al., 1997). As mud crabs in the Atlantic are naive to the parasite, they are highly susceptible, and prevalence of infection can reach upwards of 90% (vs 10% in the Gulf of Mexico) (Tepolt et al., 2020). Recent work suggests the parasite can strongly impact host populations in the invasive range (Blakeslee et al., 2021); these population-level effects could then scale up to the community level, given that mud crabs are a vital part of estuarine food webs in these regions (Eash-Loucks et al., 2014).

The rhizocephalan parasite Loxothylacus panopaei with a pair of claws and multiple legs.

Fig. 1.1. A rhizocephalan parasite, Loxothylacus panopaei, which invaded Atlantic estuaries of the US east coast with translocations of eastern oysters from the Gulf of Mexico. The parasite now infects native mud crab hosts from Maryland to Florida, sometimes at very high infection prevalence. Photo courtesy of Carter Stancil and April Blakeslee.

Invasive species and parasitic disease are often closely linked. Parasites may be co-introduced with their invasive host, with the potential to spread to new hosts in the invasive range. For example, outbreaks of Aphanomyces astaci vectored by invasive crayfish are driving declines and extinction of native crayfish in Europe (Filipová et al., 2013). Conversely, invaders may lose their parasites during the invasion process, potentially enhancing invasion success and impact (Torchin et al., 2003; Blakeslee et al., 2013). For example, loss of lungworm has increased the survival and growth of invasive cane toads in Australia (Finnerty et al., 2018). Some invasive species are themselves parasites, such as Batrachochytrium dendrobatidis which causes chytrid disease and is driving large-scale amphibian declines (Scheele et al., 2019). Parasites are also often key to the ecological and societal impact of an invasive species. If you consider the International Union for Conservation of Nature (IUCN) list ‘100 of the World’s Worst Invasive Alien Species’, the environmental impacts of a quarter of the species listed are linked to diseases of wildlife (Hatcher et al., 2012), and 16% of those listed are linked to the spread and impact of human diseases (Vilà et al., 2021). It is therefore vital to investigate, document and expand our understanding of the role of species invasions on host–parasite interactions, community- and ecosystem-level changes, and impacts on human health and commercial industries.

In this book, we take a broad view of parasites, to include microparasites (viruses, bacteria, protists) and macroparasites across terrestrial and aquatic systems around the world. In some instances, parasitic co-invaders can exhibit different symbiotic relationships with invasive and native species. For example, A. astaci is parasitic on white-clawed crayfish (Austropotamobius pallipes) and can cause high levels of mortality, but it is asymptomatic on invasive crayfish hosts (Pacifastacus leniusculus) which can vector the parasite between water bodies. Symbionts in this case could be considered either commensal or parasitic; however, here, we use parasites as primary examples over commensal associations. The term invasive alien species (IAS; European Commission, 2014; the UK term invasive non-native species (INNS) is synonymous) refers to animals and plants that are introduced accidentally or deliberately into a natural environment where they are not normally found, with serious negative consequences for their new environment. We use ‘invasive’ as an umbrella term for species (including parasites) that have been introduced outside their native ranges, have become established, and have then spread beyond their point of introduction (Blackburn et al., 2011). The term ‘invasive parasite’ is used throughout, whether impact or harm on recipient communities has been documented; however, the majority of examples in this book involve invasive parasites that have been documented to have ecological, economic or human health impacts.

This book falls into two broad but overlapping sections. The earlier chapters (Chapters 2–5, this volume) explore the introduction, establishment and spread of invasive parasites, the detection of parasites, and factors affecting parasite and host success. The later chapters (Chapters 6–9, this volume) explore the impact of invasive parasites on novel hosts and invaded communities, and methods of measuring and predicting impact. They also explore invasive parasites in the context of other global stressors, as well as their effect on human health and food security. Throughout the chapters, the authors draw examples from terrestrial, marine and freshwater ecosystems as well as exploring invasive parasites in wild and managed populations. The chapters involve collaborations among invasion biologists, disease ecologists and parasitologists, and provide expertise across a variety of disciplines within these fields. The authors come from a range of scientific sectors, including academics at universities and research institutes, government researchers at local and national laboratories, and managers from governmental agencies. This broad coverage of discipline and expertise ensures a mix of both basic and applied research, as well as links to policy. To check which host taxa and parasite/symbiont taxa are mentioned in each chapter refer to Figs 1.2 and 1.3, respectively.

1.2 Introduction, Establishment and Spread of Invasive Parasites

The nature of biological invasion events is unpredictable (Roy et al., 2014). In turn, parasite invasions and their disease outcomes are also difficult to predict and detect (Roy et al., 2017), since they lead to novel host–parasite interactions with no previous co-evolutionary history (Dunn and Hatcher, 2015). Detecting parasites is a key challenge to our understanding and managing invasive pathogens. In Chapter 2, this volume, Jamie Bojko, Amber Collings, Amy Burgess and Jack Goode review several diagnostic methods used for the detection and diagnosis of invasive symbionts, particularly for invasive parasites. Gross pathology, histology, electron microscopy, CT scanning, molecular diagnostics, biosensors and metagenomic/metatranscriptomic tools are included. The chapter concludes with a need to better explore symbiont diversity in invasive species, filling in taxonomic gaps with an aim to better understand symbiont-invasion dynamics.

When species invade novel communities, it can seem paradoxical that they may outperform native species in those same communities, given the potential for significant losses in genetic diversity during the invasion process. A possible mechanism that could explain this outcome is the loss of natural enemies (i.e. enemy release), specifically parasites. In Chapter 3, this volume, Osamu Miura and Mark Torchin describe multiple examples of parasite release around the world, and also demonstrate a strong, positive correlation between hosts that have demonstrated losses in parasite diversity with those demonstrating reductions in genetic diversity.

Parasites can inform a number of conservation-related questions, including host invasion histories. April Blakeslee and Chris Moore, in Chapter 4, this volume, describe the use of parasites as ecological and evolutionary tools for resolving questionable invasion histories, such as those species that have been given cryptogenic (= origin uncertain) classification. To resolve questionable invasion histories, two common signatures of invasion – parasite escape and genetic founder effects – can be examined together to determine whether a cryptogenic host conforms to expectations consistent with invasion (i.e. lower parasite burdens and genetic bottlenecks in non-native vs native populations, as demonstrated in Chapter 3).

An illustration of a circle with multiple interconnected lines between host taxa and the chapters in the book.

Fig. 1.2. This figure can be used to check which host taxa are mentioned in each chapter. Chapters 2–9 of this book include a range of native or invasive host examples that are associated with invasive parasites. The broad host taxa included in each chapter are noted by coloured triangles in each ‘chapter box’. The numbers adjacent to the triangles indicate the number of mentions/examples from that host taxonomic group in each chapter. The colour of the triangles is based on the ‘host group’ key at the foot of the figure. Coloured lines represent common examples of host groups that link chapters, and the thickness of the line is dependent on the number of examples from the host taxonomic group, where a thicker line represents more available mentions/examples.

Click to see the long description.

Biological invasions result in the introduction of symbionts – these can be commensal, mutualistic or pathogenic in nature. Louise Barwell, Bethan Purse and Helen Hesketh (Chapter 5, this volume) identify a range of ‘bio-characteristics’ that can appear to make a symbiont more ‘invasive’, including more likely to survive an invasion. Much of our understanding of such characteristics is derived from parasitology, epidemiology, biogeography and biological control literature, including literature on One Health issues. Greater collaboration and increased knowledge flows between invasion ecology and other disciplines are needed to generate/test hypotheses linking parasite bio-characteristics to fitness and performance metrics (trait complexes). In this chapter, first steps are presented to build a conceptual trait-based framework for understanding parasite invasiveness.

1.3 Impact, Novel Hosts and Invasive Parasites in Recipient Communities

The success of a biological invasion is often affected by parasitism, or indeed the absence of parasites. In Chapter 6, this volume, Daniel Warren, Karolina Bacela-Spychalska, Michal Grabowski and Jamie Bojko explore a range of systems for which parasitism affects native/invader trophic interactions, illustrating how parasitic infection may magnify or reduce the impact of a biological invader and how the effect of parasites may be incorporated into existing metric calculations. They use the Relative Impact Potential metric which compares consumption of prey/resources, as well as relative abundances, to predict the total potential impact of invasive alien species, but importantly by incorporating invasive parasites.

An illustration of a circle with multiple interconnected lines between parasite taxa and the chapters in the book.

Fig. 1.3. This figure can be used to check which parasite/symbiont taxa are mentioned in each chapter. Chapters 2–9 of this book include a range of parasite examples. The broad parasite taxa included in each chapter are noted by coloured triangles in each ‘chapter box’. The numbers adjacent to the triangles indicate the approximate number of mentions/examples from that parasite taxonomic group in each chapter. The colour of the triangles is based on the ‘parasite group’ key at the foot of the figure. Coloured lines represent common examples of parasite groups that link chapters, and the thickness of the line is dependent on the number of examples from the parasite taxonomic group, where a thicker line represents more available mentions/examples.

Click to see the long description.

When parasites invade new regions, host–parasite interactions within recipient communities can change significantly. In Chapter 7, this volume, David Thieltges and Anouk Goedknegt examine the ecological consequences of parasite invasions from a conceptual and illustrative perspective, focusing on both direct and indirect effects of parasite invasion on recipient communities. The chapter explores the consequences of parasite invasion (e.g. parasite spillover, parasite spillback, density-mediated indirect effects, trait-mediated indirect effects), across a variety of parasite taxonomic groups.

Invasive species are one of a suite of anthropogenic stressors that affect ecosystems worldwide. In Chapter 8, this volume, Jamie Bojko, Helen Roy, Amy Burgess, Lucy Butler, Freya Pellie and Alison Dunn explore the interactions of invasive parasites with other key global stressors, such as climate change and pollution. This chapter examines how these abiotic stressors may act at each stage of the invasion process, from the likelihood of introduction and establishment to ecosystem impact. They explore wild and managed population examples and illustrate the importance of multiple anthropogenic stressors on the emergence of zoonotic diseases.

Finally, global food security is vital for the continued survival of humans – with a need to protect livestock, crops and natural resources from parasites. In Chapter 9, this volume, Louisa Wood, Morag Clinton, David Bass, Jamie Bojko, Rachel Foster, James Guilder, Adam Kennerley, Ed Peeler, Ava Waine and Hannah Tidbury introduce a range of culture systems (agriculture, aquaculture, fisheries, etc.) and explore the potential or direct impact from invasive parasites, including any associated policy in place to control/mitigate them and their impact. The chapter concludes by stating that parasites introduced by biological invasions constitute a more unpredictable form of risk, and that diagnostic methods are vital, but most importantly, study groups from a range of backgrounds (policy, pathology, social science, economics, ecology) are needed to advance global food security through communication and understanding the present risks.

1.4 Conclusions

Parasites are an ecologically and economically vital group of organisms that are frequently overlooked in studies of invasion biology. This book takes a broad view of invasive parasites, improving our understanding of the introduction, establishment and spread of invasive parasites, their detection, and the factors that impact parasite and host success. In our concluding chapter (Chapter 10, this volume), the editors Jamie Bojko, Alison Dunn and April Blakeslee provide an overview of the main outcomes of the book, and identify several key interdisciplinary approaches and questions that will help to further develop our understanding of invasive parasites and our ability to predict and manage them.

References

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2 Diagnosing Invasive Parasites

Jamie Bojko¹,²*, Amber J. Collings³, Amy L. Burgess¹,² and Jack A. Goode⁴

¹National Horizons Centre, Teesside University, Darlington, UK; ²Teesside University, Middlesbrough, UK; ³Keele University, Newcastle-under-Lyme, UK; ⁴NHS England, Quarry House, Leeds, UK

*Corresponding author: [e-mail]

© CAB International 2023. Parasites and Biological Invasions (eds J. Bojko et al.)

DOI: 10.1079/9781789248135.0002

Abstract

Microorganisms are everywhere and biological invasions are no exception. In this chapter, we present an arsenal of diagnostic and research tools that can help the invasion biologist to identify, characterize, quantify and understand the symbiotic assemblage that co-invades alongside their invasive or non-native host. We provide details on pathological, molecular and data processing (bioinformatic) approaches that are necessary to define the co-invading ‘pathobiome’, composed of commensal, mutualistic and parasitic species from large metazoan parasites through to bacteria and viruses.

2.1 Introduction

There are microorganisms on the book you are holding right now, or on the keyboard and computer screen that you used to look at this book chapter. As you breathe, you are launching microorganisms from your mouth and into your surroundings, and as you turn the page or touch the keyboard you are leaving a microbial fingerprint behind. Microorganisms are almost impossible to avoid and are a crucial element of any biological entities’ lifestyle; we need them to survive (our microbiome), but they can also contribute to the cause of our death or change the way we feel and behave (our pathobiome) (Bass et al., 2019). Most often their presence or impact is neglected, especially when exploring the effects of biological invasions.

Invasion biology aims to predict which species can arrive, establish, survive and may become harmful to native species, environments and ecosystems (an invader; ‘invasive’) and which may translocate, but cause little to no impact (‘non-native’) at the new area (Chapter 6, this volume). This aim is relevant to the study of invasive non-native microorganisms, symbiotic species capable of co-invading via an invasive or non-native host (vector) and entering a new ecosystem without being lost along the way (Chapter 3, this volume). Such microbial invaders are often symbiotic, sharing either a mutualistic, commensal or parasitic relationship with their host. Cataloguing microbes from an invasive non-native population (diversity and burden), determining the effect on that population due to the presence of the symbiont (impact), and finally determining whether the symbiont poses any threat to native species (risk assessment), are all stepping stones in the field of invasive parasite biology. This final step of conducting a risk assessment makes strong ties between the study area and policy/legislation relevant to invasive parasites (Chapter 9, this volume).

Parasites can be difficult to detect, and often require specific, and sometimes costly, diagnostic methods to define their species and their quantity/burden in the host. In this chapter, we explore a range of diagnostic methods that can be used to detect and identify known parasitic organisms, or search for unknown symbionts residing in invasive host populations. We explain the importance of incorporating diagnostic methods into bioinvasion science and hope to equip readers with the tools needed to incorporate symbiont diagnostics into their own research, experimental development and understanding.

2.2 Diagnostic Potential for Invasive Symbionts

For new invaders, there are often few taxonomic keys, available diagnostics or detailed literature, unless dedicated studies have been conducted on a host species in its native or invasive habitats (Bojko et al., 2021). Often this means that research into a new invader must start from square one – searching for parasites and other symbionts.

In terms of impact, parasites are often the most important symbionts. They can either infect the host and contribute to the mortality and behavioural alteration of naive native species (Bruemmer et al., 2010; Hatcher et al., 2019), or they can help to control invaders by altering their behaviour and lowering their population size (Bojko et al., 2019). Developing an insight into the diverse array of symbionts that can colonize an invader is an important step towards the ‘pathobiome approach’ (Bojko et al., 2021) – moving away from single parasite effects and exploring the overall risk posed by the introduction of an ‘invasive pathobiome’ and the consequences it may have to a native ecosystem and the native species therein. In this section, we explore the detection of single parasites through to cataloguing the host’s microbiome and pathobiome, using a range of pathological and molecular tools.

2.2.1 Pathological screening tools

Several pathological tools are available to screen for parasites in invasive and non-native hosts. Broadly, these include ‘wet-preparation’ or dissection methods, histology and electron microscopy. Wet-preparation and histological methods rely on visual observation of parasites via the naked eye or light microscopy (often restricted to 100 × magnification). Electron microscopy, including both scanning and transmission methods, can provide more detailed views of pathologies and parasite ultrastructure and development (Fig. 2.1). The use of these tools helps to define whether a microorganism is truly parasitic, by determining the pathology it induces, as well as providing morphological evidence of its presence.

Wet-preparation methods are often most useful when searching for metazoan macroparasites that are identifiable using morphological keys. For example, observation and taxonomic identification of Gyrodactylus salaris, an invasive fish monogenean, is possible using morphological keys (Shinn et al., 2004). Histological techniques provide a capacity to visually search for viruses, bacteria and other microparasites that may be observed by the pathology they cause, other than observing the parasite itself. Scanning electron microscopy (SEM) can reveal the detailed surface ultrastructure of host tissues and associated microbes. Finally, transmission electron microscopy (TEM) can be used to attain internal ultrastructural data on a given parasite, as well as visualize the cytological response of the infected cell(s)/tissues.

A photo and three micrographs, a through c, of the infection of a shrimp by a parasite.

Fig. 2.1. Pathology associated with a Cucumispora ornata infection of Dikerogammarus haemobaphes (demon shrimp). Visualization of the parasite has been made using histology (a), transmission electron microscopy (b), and scanning electron microscopy (c). In all instances, the green arrow indicates one or more microsporidian spore from the muscle tissue of the amphipod host. From Bojko et al., 2015.

Click to see the long description.

We suggest the following methodology when conducting a disease screening study:

1. Obtain valid licensing and ethical approval for your study organism. This will include collection method(s), euthanization techniques, and the dissection plan for the invasive or non-native species you are working with. In addition, you will need to prepare chemicals (using appropriate labelling and Control of Substances Hazardous to Health Regulations (COSHH) awareness) for the various pathological methods you choose to use, such as a histological fixative, electron microscopy preservative, and an ethanol or RNAlater solution for sampling tissues for molecular diagnostics (DNA/RNA/protein), biosensor or genomic techniques (see sections 2.2.2 , 2.2.3 and 2.2.4 ). If working with live organisms or cell culture, you may have the capacity to run multi-omics tools on swabs and attain pathological information via