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