Large carnivore impacts are context-dependent
Introduction
When understanding and managing trophic dynamics, what is deemed a natural or unnatural interaction must first be considered (Rolston, 2001). The aim of restoring ‘natural’ systems in the modern era becomes somewhat problematic. Wildlife conservation is still possible in human dominated landscapes but maintaining top-down ecological processes in such landscapes is challenging (Chapron et al., 2014, Linnell et al., 2015, López-Bao et al., 2015). The impacts of world-wide predator decline and the relative importance of direct and indirect species interactions have been highlighted as fundamental ecological questions (Sutherland et al., 2013). Yet caution has been expressed in seeing apex predators like the grey wolf Carnivora Canidae Canis lupus as ecological saviours because ecosystem services may not universally apply, particularly if inhibited by anthropogenic activity (Mech, 2012). Furthermore, there is only one intact terrestrial predator guild in the world (Africa), so all other guilds may reflect the impacts of the Pleistocene megafauna extinctions and shifting baselines to mesopredator-dominated systems (Fleming et al., 2012, Valkenburgh et al., 2015). The question arises as to what the conservation benchmark or baseline is, was or should be given a particular ecological context (Berger, 2008, Hayward, 2009, Hayward, 2012).
Species at higher trophic levels are often lost more rapidly than those at lower trophic levels (Dobson et al., 2006). Apex predator decline and trophic simplification is something of great concern worldwide (Estes et al., 2011, Johnson, 2010, Ripple et al., 2014). It is imperative to understand the interactions and potential impacts of apex predators because their absence or decline can have undesired effects (Berger et al., 2008, Jackson et al., 2001, Terborgh et al., 2001). The consequences of upper trophic level decline and the loss of ecosystem services provided by large carnivores could lead to environmental degradation through the release of top-down control upon herbivores (Beschta and Ripple, 2012, Hebblewhite et al., 2005, Ripple and Larsen, 2000) and mesopredators (Newsome and Ripple, 2014, Prugh et al., 2009, Ritchie and Johnson, 2009). If healthy populations of top predators can be maintained within ecosystems, they should also contain healthy communities and populations of the many species that perform a diversity of ecosystem services at lower trophic levels (Dobson et al., 2006).
As the most dominant landscape user and primary resource consumer on the planet (Paquet and Darimont, 2010), humans greatly modify the landscapes and communities that apex predators interact with through a myriad of disturbance types (Blanc et al., 2006, Frid and Dill, 2002, Sibbald et al., 2011). The positive (Kilgo et al., 1998, Kloppers et al., 2005, Leighton et al., 2010) or negative (Hebblewhite et al., 2005, Jayakody et al., 2008, Pelletier, 2006) nature of this disturbance however depends entirely on management perspective (Reimoser, 2003). Humans can impact apex predators in much the same way as they impact smaller predators and prey species, through density-mediated (consumptive) and trait/behaviourally-mediated (non-consumptive) pathways (Ordiz et al., 2013). Impacts can be direct (Packer et al., 2009, Virgos and Travaini, 2005) or indirect through effects on other species or habitat (Rogala et al., 2011, Sidorovich et al., 2003).
Context-dependent interactions between species are common but often poorly described (Chamberlain et al., 2014). This review examines the contextual impacts of large carnivores and the potential for human interference through effects on species assemblage, environmental productivity, landscape and predation risk (Fig. 1 and Table 1). If we are to predict the consequences of predator management, it is critical to understand the dynamics of interspecific relationships between organisms (Elmhagen et al., 2010, Prugh et al., 2009, Ripple et al., 2014) and to determine if this context can be manipulated to achieve management and ecosystem service goals (Kareiva et al., 2007).
A search of literature was conducted using Web of Science and Google Scholar with “OR” and “AND” search operators and a mixture of key words (apex predator*, large carnivore*, carnivore*, mesopredator release, mesopredator*, mesocarnivore*, large herbivore*, herbivore suppression, grazing, browsing, predation pressure*, interspecific, interspecific interaction*, interspecific killing, predation, intraguild predation, competition, competitor*, trophic cascade*, predation risk*, ecosystem service*). Reference trails, recommended papers or appropriate material already in the possession of the authors were also used to inform this review.
Predators consume prey but they also provide risk (Brown and Kotler, 2007, Fortin et al., 2005). Harassment and the associated energetic losses of responding to predation risk can carry costs to overall fitness (Creel, 2011). Predation risk is a powerful motivator that can affect behaviour and how an animal uses time and space as well as investment in other antipredator strategies (Brown et al., 1999, Ripple and Beschta, 2004, Willems and Hill, 2009). Predation risk and disturbance create trade-offs between avoiding risk or perceived risk and other fitness enhancing activities (e.g. feeding and breeding), such that risk avoidance carries energetic costs in the form of missed opportunities (Brown, 1992, Brown et al., 1999, Eccard and Liesenjohann, 2014). Human disturbance may incur similar responses to risk in wildlife (Erb et al., 2012, Frid and Dill, 2002, Leighton et al., 2010).
Risk-induced interactions between predators and other organisms can have cascading effects (Miller et al., 2012, Ripple et al., 2014, Ritchie and Johnson, 2009). A forager's response to its landscape of fear (Laundré et al., 2014, Laundré et al., 2010) may alter the species composition, behaviour, adaptive evolution or population dynamics of its prey and perhaps its predators or competitors (Brown and Kotler, 2007). Non-consumptive behavioural interactions can be significant ecological drivers and should not be overlooked (Heithaus et al., 2009, Peckarsky et al., 2008, Ritchie and Johnson, 2009).
Section snippets
Interactions with mesopredators
Larger predators can sometimes limit the impacts, range and densities of smaller predators (Henke and Bryant, 1999, Levi and Wilmers, 2012, Prugh et al., 2009). Soulé et al. (1988) observed that, in the absence of larger more dominant predators, smaller predators and omnivore populations explode: increasing abundance by up to ten times that before release. The mesopredator release hypothesis predicts that a decrease in abundance of top-order predators results in an increase in the abundance of
Interactions with large herbivores
Large carnivores can be important mortality drivers of ungulate populations (Jędrzejewski et al., 2002, Melis et al., 2009), maintaining herd health through the removal of unhealthy individuals (Kusak et al., 2012). Although not universal, density-driven terrestrial cascades are common (Schmitz et al., 2000). On Isle Royale, USA for example, wolves have been found to regulate moose Cetartiodactyla Cervidae Alces alces population dynamics and in doing so dampen the effects of climactic change
Conclusions
Interactions between species are complicated. Suppression of one species by another can be driven by a varying intensity of both density- and behaviourally-mediated mechanisms. Impacts from large carnivores will not be homogenous across contexts. Factors intrinsic to prey, predators and the given system (species composition, environmental productivity, landscape, and predation risk) will culminate to produce the resultant dynamics in a given context. The mixture of variables yielding
Acknowledgements
We would like to thank Bangor University and the University of Zagreb for their support of the authors. Both Haswell and Kusak would also like to thank The UK Wolf Conservation Trust, Nacionalni park Sjeverni Velebit and Nacionalni park Plitvička jezera for their continued assistance and support of research efforts with the study of large carnivores in Croatia. We are grateful to Dr. B. Allen and Dr. S. Creel for their useful comments on the manuscript. The authors declare that they have no
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