Environmental effects are stronger than human effects on mammalian predator-prey relationships in arid Australian ecosystems
Graphical abstract
Introduction
Food web structure and stability in terrestrial systems are influenced by a myriad of biotic, abiotic, and anthropogenic factors (Kershaw, 1969, Krebs, 2008). Commonly discussed factors include climate change, land use change, deforestation and invasive species (e.g. Petchey et al., 1999, Kinnaird et al., 2003, Tylianakis et al., 2008, Sinclair et al., 2013). While the effects of bottom-up factors (e.g. geology or habitat, climate or rainfall) on subsequent population growth within flora and fauna communities may be readily understandable (Robin et al., 2009, White, 2013), a growing body of research points to the effects that top-predators can have in shaping food web structure and stabilising the influence of other factors (Estes et al., 2013, Ripple et al., 2014). Through their suppressive effects on mesopredators and prey, top-predators might provide indirect benefits to some prey and vegetation at lower trophic levels, thereby maintaining ecosystem health and resilience. The strength of such trophic cascades is dependent on the complexity of the system and the number of trophic levels represented (Finke and Denno, 2004, Holt and Huxel, 2007), with top-predators typically exhibiting stronger effects in simpler systems with fewer trophic levels. These findings have led some to suggest that the maintenance, restoration or encouragement of top-predators is essential for the recovery of threatened fauna populations, communities and ecosystems (Ritchie et al., 2012, Ripple et al., 2014). However, there is also a large and growing body of evidence that these expectations are often not realised in situ given highly context-dependent factors and the complexities of even ‘simple’ systems (Sergio et al., 2008, Allen et al., 2014a, Haswell et al., 2017), especially those modified by humans (Linnell, 2011, Fleming et al., 2012, Wikenros et al., 2015). Understanding the relative influence of top-down and bottom-up factors on ecosystems remains a key priority for managers of predators and threatened fauna.
The complete removal of top-predators can have profound effects on ecosystem health and resilience (Estes et al., 2011), but whether or not their restoration can reverse these effects and restore ecosystems to previous benchmarks is less clear (e.g. Marshall et al., 2013). Moreover, whether or not the temporary suppression of common and widespread top-predators causes the same effects as complete predator removal is even less certain (Fleming et al., 2012, Allen et al., 2014a). Bottom-up factors, such as habitat availability, fire, rainfall or drought, are the primary drivers of fauna populations (White, 2013, Lawes et al., 2015). Top-down and bottom-up processes occur simultaneously, and also interact. For example, climate change may foster increased predation of prey fauna reliant on vegetation for food and refuge by increasing the frequency and severity of rainfall and subsequent vegetation shortages (Whetton et al., 1993, Letnic and Dickman, 2010). Such effects of climate change may be particularly important for irruptive or ‘boom and bust’ prey species, typical of desert biota, by extending the period that prey are exposed to high levels of predation (Newsome et al., 1989, Allen and Fleming, 2012). Extended periods of drought are known to exacerbate predation risks to irruptive fauna that typically persist in isolated and low-density populations (e.g. Dickman et al., 1999, Letnic and Dickman, 2006). However, there remains a dearth of studies demonstrating these expected functional relationships for many threatened fauna persisting in desert ecosystems, and identifying the strongest factors influencing prey populations has proved difficult (Holmes, 1995, Marshall et al., 2014, Peterson et al., 2014). All components of food webs interact to some extent (Allen et al., 2017), but few interactions are strong enough to shape them. Although general ecological patterns may already be apparent, the outcomes of global environmental change are highly unpredictable, and ‘the greatest single challenge will be to determine how context alters the direction and magnitude of effects on biotic interactions’ (Tylianakis et al., 2008).
In this study, we investigate the influence of multiple biotic and abiotic factors affecting predator-prey relationships in the arid Strzelecki Desert region of central Australia. The Strzelecki Desert is characterized by a depauperate mammal assemblage comprised of one top-predator (dingoes, Canis familiaris), two mesopredators (European red foxes, Vulpes vulpes, and feral cats, Felis catus) and two common mammalian prey species, European rabbits (Oryctolagus cuniculus) and dusky hopping-mice (Notomys fuscus; hereafter hopping-mice). Other predator and prey species are present (Van Dyck and Strahan, 2008), but persist in variable or low densities that likely have relatively minimal influence on these mammals (Allen et al., 2014a). Beef-cattle grazing is the primary land use in this region (Allen, 2015a). Dingoes, foxes, cats and rabbits were each introduced to Australia. Dingoes arrived approximately 5000 years ago, whereas foxes, cats and rabbits were introduced soon after European colonisation in the late 1700s (Johnson, 2006); each are widespread and common (West, 2008). All three predators are relatively small (< 16 kg mean adult body weight), generalist carnivores with highly overlapping diets primarily consisting of medium and small-sized mammals (e.g. Pavey et al., 2008, Cupples et al., 2011, Glen et al., 2011, Allen and Leung, 2012). Hopping-mice are native and endemic to Australia. Their range has declined by over 90% since the arrival of Europeans and the subsequent ecological changes associated with the introduction of livestock and invasive species (e.g. foxes, cats and rabbits). The Strzelecki Desert is the last stronghold of hopping-mice (Lee, 1995, Moseby et al., 1999, Van Dyck and Strahan, 2008), which are an endangered, ‘old world’ or conilurine rodent (Muridae) with irruptive population cycles typical of many small mammals in arid areas.
Previous desktop, snap-shot and correlative studies (compiled and reviewed in Allen et al., 2013b) have developed the following hypotheses about the contemporary relationships between dingoes and hopping-mice in this study system:
- 1.
Dingo abundance is positively correlated with hopping-mice abundance (presumably because dingoes provide indirect refuge to hopping-mice from mesopredators).
- 2.
The presence of dingoes positively affects hopping-mice foraging behaviour (presumably because hopping-mice perceive foraging in the presence of dingoes to be less of a risk than foraging in their absence).
- 3.
The lower abundance of hopping-mice in the east of the Strzelecki Desert is due to the relative absence of dingoes there (which are excluded by the dingo barrier fence).
- 4.
Contemporary dingo control practices (i.e. repeated broad-scale poison-baiting, undertaken to protect cattle from dingo predation) reduces the abundance of dingoes, and increases the abundance of mesopredators, which reduces the abundance of hopping-mice.
- 5.
Dingoes do not eat hopping-mice in quantities sufficient to threaten the persistence of hopping-mice populations.
Alternative hypotheses for these observations have seldom been assessed, however, and limited experimental work has been undertaken to identify causal relationships driving the observed correlations between dingoes and hopping-mice (Allen, 2011a, Allen et al., 2013b, Newsome et al., 2015). Previous studies have investigated these hypotheses by undertaking snap-shot or single survey studies, collecting meagre amounts of empirical data, followed by extensive and complex post hoc modelling to try and elucidate causal mechanisms from correlative data (e.g. Moseby et al., 2006, Letnic et al., 2009, Letnic and Koch, 2010, Gordon et al., 2015, Gordon et al., 2017). In contrast to this approach, we focus on obtaining high-quality empirical data capable of addressing the above hypotheses directly. We use a variety of complimentary techniques on a variety of data obtained as part of a large-scale manipulative experiment investigating the effects of lethal dingo control on dingo abundance and ecological function (Eldridge et al., 2016). Our primary aim was to characterise the nature of the relationship between dingoes and hopping-mice by testing the five aforementioned hypotheses through assessment of 13 interrelated study questions within three relationship categories.
Section snippets
Data sources
We conducted a systematic and complimentary series of empirical studies against a background of a large-scale and long-term manipulative experiment on dingo ecology and management in northern South Australia, conducted between April 2008 and February 2012. A series of reports based on this experiment have already been published (Table 1; see also Eldridge et al., 2016). Hence here, we focus the present investigation on the behavioural, numerical, spatial, and predatory aspects of the
Results
Primary results are presented in 3.1 Behavioural relationships between dingoes and hopping-mice, 3.2 Spatial and numerical relationships between dingoes and hopping-mice, 3.3 Predatory relationships between dingoes and hopping-mice and summarised in Table 2, with additional detail available in the supplementary material.
Discussion
Drought, flood, fire, habitat availability, provision of artificial water points, competition from livestock and invasive species, predation, and the lethal control of top-predators have each been proposed as biotic and abiotic drivers of threatened fauna populations, including hopping-mice, in arid Australian ecosystems (e.g. Burbidge and McKenzie, 1989, Burbidge et al., 2008, Doherty et al., 2015, Woinarski et al., 2015). Despite many ultimate and proximate causes, the general mechanism of
Conclusions
Our study supports the general view that reductions in food and cover followed by predation (by dingoes in this case) can lead to declines of small mammals in Australia (Allen, 2011a, Lawes et al., 2015, Woinarski et al., 2015), and highlights the relative influence of multiple environmental (bottom-up) and human (top-down) effects on predator-prey interactions. These results have important implications for land managers and policy-makers responsible for the management of predators and prey.
Acknowledgements
This study would not have been possible without the generous support of S. Kidman and Co. cattle company and Mutoroo Pastoral Company, where Greg Campbell, Paul Jonas and Greg Conners granted access to the site. The work was administered by the South Australian Arid Lands Natural Resources Management Board, the Invasive Animals Cooperative Research Centre, and the New South Wales Department of Primary Industries, with financial support obtained from state and federal government funding programs
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