Elsevier

Biological Conservation

Volume 214, October 2017, Pages 136-146
Biological Conservation

A guide for ecologists: Detecting the role of disease in faunal declines and managing population recovery

https://doi.org/10.1016/j.biocon.2017.08.014Get rights and content

Highlights

  • Diseases have caused declines and extinctions of fauna worldwide.

  • Emerging infectious diseases increase concerns of further detrimental effects on fauna.

  • Ecological studies into causes of declines often ignore disease as a factor.

  • We propose a disease investigation framework to assist in detecting disease in wildlife.

Abstract

Biodiversity is declining at an alarming rate, especially among vertebrates. Disease is commonly ignored or dismissed in investigations of wildlife declines, partly because there is often little or no obvious clinical evidence of illness. We argue that disease has the potential to cause many species declines and extinctions and that there is mounting evidence that this is a more important cause of declines than has been appreciated. We summarise case studies of diseases that have affected wildlife to the point of extinction and bring together the experiences of wildlife managers, veterinarians, epidemiologists, infectious disease specialists, zoologists and ecologists to provide an investigation framework to help ecologists and wildlife managers address disease as a factor in wildlife declines. Catastrophic declines of wildlife may be the result of single or multiple synergistic causes, and disease should always be one factor under consideration, unless proven otherwise. In a rapidly changing world where emerging infectious diseases have become increasingly common, the need to consider diseases has never been more important.

Introduction

The world's biological diversity continues to decline at an unprecedented rate (Butchart et al., 2010, Tittensor et al., 2014). The major causes of species declines are attributed to anthropogenic activities, including habitat destruction, over-exploitation, climate change and invasive species, or a combination of these factors (Ducatez and Shine, 2017, Schipper et al., 2008). Infectious disease, although ubiquitous in all species, is rarely investigated, despite compelling and accumulating evidence of disease causing population declines and even species extinctions.

The role of disease as a major factor in species declines has generally been identified when it has appeared as a major emergence event, resulting in the mass morbidity and mortality of large, gregarious or regularly monitored animals. The African rinderpest pandemic in the late 19th century is a seminal example (Daszak et al., 2000), extirpating > 90% of Kenya's buffalo (Syncerus caffer) and causing a trophic cascade. Much of Hawaii's endemic avifauna became extinct following the introduction of the mosquito vectors of birdpox and avian malaria (Warner, 1968). Ebola virus eliminated 90–95% of critically endangered western gorillas (Gorilla gorilla) in the Congo and Gabon in the early 21st century (Bermejo et al., 2006). Populations of the African wild dog (Lycaon pictus) became extinct in the Serengeti in 1991 due to canine distemper and rabies (Daszak et al., 2000). The fungus Pseudogymnoascus destructans, white-nosed syndrome (WNS), which was first documented in bats in 2006, has killed millions of bats across north America and poses an extinction threat to some species, such as the Indiana bat (Myotis sodalist) (Thogmartin et al., 2013). In 2015, 62% of the global population of critically endangered saiga antelope (Saiga tatarica) died suddenly due to an opportunistic pathogen, the Pasteurella bacterium (Milner-Gulland, 2015).

Yet diseases that cause mass mortalities are likely to represent a fraction of the true number of cases in which infectious disease plays a role in population declines (Grogan et al., 2014). We suggest that disease is likely to be an unrecognised contributor to declines as well as an obvious sole cause (De Castro and Bolker, 2005, Pedersen et al., 2007, Reiss et al., 2015, Schloegel et al., 2006, Smith et al., 2006, Tompkins et al., 2015). In this capacity, disease may contribute to population declines through influencing demographic parameters, whereby: (i) an increase in mortality occurs in addition to other top-down effects (additive versus compensatory mortality; Kistner and Belovsky, 2014), (ii) the population cannot compensate for the increased mortality by increasing recruitment (Muths et al., 2011, Scheele et al., 2015); or (iii) a decrease in recruitment is observed (Fig. 1).

Disease can cause population declines through decreased reproductive success, affecting fertility, fecundity, and neonatal survival. Such diseases may be particularly difficult to detect due to subtle or inapparent clinical signs (Scott, 1988). Recent examples include malaria in wild birds (Knowles et al., 2010), porcine reproductive and respiratory syndrome virus in wild boars (Sus scrofa) (Reiner et al., 2009), and bacterial infections in wild ungulates (Pioz et al., 2008). Infectious diseases may also increase mortality while decreasing recruitment, exacerbating population-level impacts, for example, chlamydial disease in koalas (Phascolarctos cinereus) (Polkinghorne et al., 2013).

Another, and perhaps more insidious, mechanism by which disease may contribute to population declines is through fundamentally altering population structure, and dispersal and migratory patterns (Fig. 1). Pathogens and their vectors often demonstrate tropism, or a specificity for population subgroups, organs, or tissue, potentially leading to changes in population sex ratio, age structure, behaviour, timing of breeding, and dispersal tendencies (Kolby et al., 2010, McDonald et al., 2014), even in populations with high abundance (Lacy, 2000) and therefore triggering detrimental Allee effects (Berec et al., 2007). Furthermore, infections may contribute to altered secondary sex ratios. For example, toxoplasmosis, caused by the parasite Toxoplasma gondii, has been reported to increase the proportion of male offspring in rodent species (Kankova et al., 2007).

Multi-disciplinary approaches to identifying and controlling emerging infectious diseases have been developed recently (Daszak et al., 2013, Plowright et al., 2008, Skerratt et al., 2007, Skerratt et al., 2009), but wildlife ecologists do not commonly consider these approaches. Our aims are (1) to develop a framework, directed at wildlife ecologists, for investigation of disease as a potential factor in wildlife population declines, and (2) to demonstrate how wildlife ecologists can apply these approaches to investigating vertebrate declines.

A common challenge in transdisciplinary research is terminology. Here, we define terms that have a common usage but sometimes different meaning across disciplines (Box 1). The term ‘disease’ is used commonly in the literature, often without much specificity. In a general sense, it can include all pathogenic infectious agents (e.g. bacteria, viruses, and parasites), as well as the resulting individual or population level effects of such infections (e.g. disease outbreaks). The term, ‘disease’, also encompasses ‘non-infectious diseases’ (those not caused by infectious agents) such as poisoning, hyperthermia and starvation (Haydon et al., 2002, Porta et al., 2014).

Section snippets

Detection difficulties

There is a general consensus across the ecology, epidemiology and veterinary disciplines that we lack important background knowledge for most of the diseases that affect wildlife species (Pedersen et al., 2007). One of the explanations for this is that it can be challenging to detect influential (or indeed any) diseases in wildlife. For example, diseases that cause spatiotemporally diffuse morbidity are dramatically under-reported compared with those causing mass mortality events (Stallknecht,

Disease investigation framework

We propose a disease investigation framework, modelled on the outbreak investigation approach used in epidemiology (sensu Reingold, 1998), to assist investigators from diverse backgrounds who are attempting to include assessment of disease as one of the many potential factors in faunal declines.

Given that declines are often identified by scientists who work outside of an epidemiological discipline, and often have little to no experience in identifying symptoms of disease, we argue that this

Disease and mammal declines in Australia

Inattention to disease as a factor in species declines is nowhere better exemplified than in Australia, where 25 mammal species became extinct in the second half of the 19th century and early 20th century, most in remote arid and semi-arid regions (Fisher et al., 2014, Woinarski et al., 2011). This wave of extinctions comprises one third of global mammal extinctions in a country that represents only 6% of the world's mammals (Fisher et al., 2014). These lessons and the suggested approaches to

Conclusions

Determining the causes of faunal population declines is complex, and resources are limited. By fusing lessons from informative case studies with approaches from epidemiologists and ecologists we have developed a framework for practitioners at the frontline to assist in the investigation and detection of disease as a driver in declining native mammals. Knowing what to look for and when, and taking appropriate observations and samples for analysis in suitable laboratories can assist in maximising

Acknowledgements

Funding for the symposium and workshop that led to this paper was provided by James Cook University's Centre for Tropical Environmental and Sustainability Science through their flagship program, led by Drs Sandra Abell and Noel Preece ‘Australia's northern development and imperilled biodiversity’. The flagship funded a visit to Brisbane by Noel Preece. Distinguished Professor Bill Laurance supported and encouraged us throughout the project. One Health Alliance provided support for a workshop in

References (124)

  • A. Polkinghorne et al.

    Recent advances in understanding the biology, epidemiology and control of chlamydial infections in koalas

    Vet. Microbiol.

    (2013)
  • G. Reiner et al.

    Porcine reproductive and respiratory syndrome virus (PRRSV) infection in wild boars

    Vet. Microbiol.

    (2009)
  • J. Rong et al.

    A high prevalence of Theileria penicillata in woylies (Bettongia penicillata)

    Exp. Parasitol.

    (2012)
  • B.C. Scheele et al.

    Low impact of chytridiomycosis on frog recruitment enables persistence in refuges despite high adult mortality

    Biol. Conserv.

    (2015)
  • B.C. Scheele et al.

    After the epidemic: ongoing declines, stabilizations and recoveries in amphibians afflicted by chytridiomycosis

    Biol. Conserv.

    (2017)
  • I. Abbott

    Mammalian faunal collapse in Western Australia, 1875–1925: the hypothesised role of epizootic disease and a conceptual model of its origin, introduction, transmission and spread

  • R.A. Alford et al.

    Global amphibian declines: a problem in applied ecology

    Annu. Rev. Ecol. Syst.

    (1999)
  • C.T. Atkinson et al.

    Changing climate and the altitudinal range of avian malaria in the Hawaiian islands - an ongoing conservation crisis on the island of Kaua'i

    Glob. Chang. Biol.

    (2014)
  • N. Beeton et al.

    Models predict that culling is not a feasible strategy to prevent extinction of Tasmanian devils from facial tumour disease

    J. Appl. Ecol.

    (2011)
  • M.D. Bennett et al.

    The first complete papillomavirus genome characterized from a marsupial host: a novel isolate from Bettongia penicillata

    J. Virol.

    (2010)
  • L. Berger et al.

    Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America

    Proc. Natl. Acad. Sci. U. S. A.

    (1998)
  • M. Bermejo et al.

    Ebola outbreak killed 5000 gorillas

    Science

    (2006)
  • J. Bielby et al.

    Modelling extinction risk in multispecies data sets: phylogenetically independent contrasts versus decision trees

    Biodivers. Conserv.

    (2010)
  • C.J.A. Bradshaw et al.

    Disease and the devil: density-dependent epidemiological processes explain historical population fluctuations in the Tasmanian devil

    Ecography

    (2005)
  • C.J.A. Bradshaw et al.

    Novel coupling of individual-based epidemiological and demographic models predicts realistic dynamics of tuberculosis in alien buffalo

    J. Appl. Ecol.

    (2012)
  • R.W. Braithwaite et al.

    Demographic variation and range contraction in the northern quoll, Dasyurus hallucatus (Marsupialia: Dasyuridae)

    Wildl. Res.

    (1994)
  • S.H.M. Butchart et al.

    Global biodiversity: indicators of recent declines

    Science

    (2010)
  • G. Caughley

    Directions in conservation biology

    J. Anim. Ecol.

    (1994)
  • G.C. Caughley et al.

    Conservation Biology in Theory and Practice

    (1996)
  • W.E. Cook et al.

    Disappearance of bovine fetuses in northwestern Wyoming

    Wildl. Soc. Bull.

    (2004)
  • P. Daszak et al.

    Emerging infectious diseases of wildlife—threats to biodiversity and human health

    Science

    (2000)
  • P. Daszak et al.

    Interdisciplinary approaches to understanding disease emergence: the past, present, and future drivers of Nipah virus emergence

    Proc. Natl. Acad. Sci. U. S. A.

    (2013)
  • F. De Castro et al.

    Mechanisms of disease-induced extinction

    Ecol. Lett.

    (2005)
  • S. Ducatez et al.

    Drivers of Extinction Risk in Terrestrial Vertebrates

    Conserv. Lett.

    (2017)
  • B. Epstein et al.

    Rapid evolutionary response to a transmissible cancer in Tasmanian devils

    Nat. Commun.

    (2016)
  • S.A. Field et al.

    Making monitoring meaningful

    Austral Ecol.

    (2007)
  • M.C. Fisher et al.

    Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host

    Annu. Rev. Microbiol.

    (2009)
  • D.O. Fisher et al.

    The current decline of tropical marsupials in Australia: is history repeating?

    Glob. Ecol. Biogeogr.

    (2014)
  • S. Godfrey et al.

    Bettongs and blood parasites: what's driving declines in the woylie (Bettongia penicillata)?

  • L.F. Grogan et al.

    Surveillance for emerging biodiversity diseases of wildlife

    PLoS Pathog.

    (2014)
  • R.K. Hamede et al.

    Biting injuries and transmission of Tasmanian devil facial tumour disease

    J. Anim. Ecol.

    (2013)
  • D. Haydon et al.

    Identifying reservoirs of infection: a conceptual and practical challenge

    Emerging Infectious Disease Journal

    (2002)
  • E.P. Hoberg et al.

    Evolution in action: climate change, biodiversity dynamics and emerging infectious disease

    Philos. Trans. R. Soc. B

    (2015)
  • B. Jackson et al.

    Research on small mammal decline and disease: Rattus rattus as a potential disease vector

  • K.E. Jones et al.

    Global trends in emerging infectious diseases

    Nature

    (2008)
  • S. Kankova et al.

    Influence of latent toxoplasmosis on the secondary sex ratio in mice

    Parasitology

    (2007)
  • A. Kilpatrick et al.

    Predicting the global spread of H5N1 avian influenza

    Proc. Natl. Acad. Sci. U. S. A.

    (2006)
  • E.J. Kistner et al.

    Host dynamics determine responses to disease: additive vs. compensatory mortality in a grasshopper–pathogen system

    Ecology

    (2014)
  • S.C.L. Knowles et al.

    Context-dependent effects of parental effort on malaria infection in a wild bird population, and their role in reproductive trade-offs

    Oecologia

    (2010)
  • J.E. Kolby et al.

    Amphibian chytrid fungus Batrachochytrium dendrobatidis in Cusuco National Park, Honduras

    Dis. Aquat. Org.

    (2010)
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