REVIEW: Ecological feedbacks can reduce population-level efficacy of wildlife fertility control

Anthropogenic stress on natural systems, particularly the fragmentation of landscapes and the extirpation of predators from food webs, has intensified the need to regulate abundance of wildlife populations with management. Controlling population growth using fertility control has been considered for almost four decades, but nearly all research has focused on understanding effects of fertility control agents on individual animals. Questions about the efficacy of fertility control as a way to control populations remain largely unanswered. Collateral consequences of contraception can produce unexpected changes in birth rates, survival, immigration and emigration that may reduce the effectiveness of regulating animal abundance. The magnitude and frequency of such effects vary with species-specific social and reproductive systems, as well as connectivity of populations. Developing models that incorporate static demographic parameters from populations not controlled by contraception may bias predictions of fertility control efficacy. Many population-level studies demonstrate that changes in survival and immigration induced by fertility control can compensate for the reduction in births caused by contraception. The most successful cases of regulating populations using fertility control come from applications of contraceptives to small, closed populations of gregarious and easily accessed species. Fertility control can result in artificial selection pressures on the population and may lead to long-term unintentional genetic consequences. The magnitude of such selection is dependent on individual heritability and behavioural traits, as well as environmental variation. Synthesis and applications. Understanding species' life-history strategies, biology, behavioural ecology and ecological context is critical to developing realistic expectations of regulating populations using fertility control. Before time, effort and funding are invested in wildlife contraception, managers may need to consider the possibility that many species and populations can compensate for reduction in fecundity, and this could minimize any reduction in population growth rate. Keywords: behaviour, demography, ecological process, fertility control, fitness, immunocontraception, population dynamics, population ecology, wildlife contraception, wildlife management Controlling reproductive capacity of wildlife Humans have been attempting to control the abundance of animals for over 13,000 years (Diamond 2002). Although regulating the herd size of domestic animals has been a feature of human economies for millennia, people have also sought to regulate populations of wild animals using hunting and culling techniques. Recent societal trends have motivated wildlife managers to seek nonlethal strategies of regulating births using fertility control (Hobbs, Bowden & Baker 2000; Porton 2005). This trend may be attributed to an increasingly mutualistic societal view arising from abundance of wildlife in suburban and urban areas (Teel & Manfredo 2009). In such circumstances, perception of wildlife species may focus less on their role as a natural resource and more on how they are part of our social environment (Leong 2010). This may lead humans to be more aware of, and concerned about, the welfare of these species. The balance of human perception and wildlife abundance is precarious because as highly adaptive species increase in density, wildlife–human conflicts increase, and society can then be confounded with the dichotomy of desire for wildlife protection and relief from wildlife conflict (Knuth et al. 2001; Lauber & Knuth 2004; Lauber et al. 2007; Hadidian 2009). The practice of using fertility control to manage reproduction in wildlife emerged over 40 years ago (Asa & Porton 2005). Wildlife managers have been attracted to fertility control as a means to regulate overabundant wildlife when animals threaten people's lives, livelihoods or property; when they cause declines in more desirable species; and when their densities are high enough to increase disease transmission or disrupt ecosystem function (Caughley 1981; Hone 2007). The vast majority of empirical knowledge about wildlife fertility control comes from individual-level studies of drug safety and efficacy (Garrott 1995; Kirkpatrick, Lyda & Frank 2011). As a consequence, we know relatively little about how fertility control influences population ecology. It remains uncertain whether findings of research on the efficacy of fertility control at the individual level can allow inferences to populations. There may be compensation in vital rates that allow individuals to maintain fitness, thus offsetting the effects of fertility control agents. If such compensation occurs, then it may be infeasible to control some wildlife populations using fertility control. Types of fertility control applied to wildlife include products that disturb normal reproductive hormone cascades or interfere with conception, such as immunocontraceptive vaccines, pharmaceuticals, hormone derivatives, agonists, antagonists, mechanical devices and surgical techniques (Asa 2005). All of these methods may prevent births, but they also may induce unintended changes to behaviour and physiology (Nettles 1997; Gray & Cameron 2010). It is not surprising that hormonal derivatives such as melengestrol and levonorgestrel affect behaviour (Gray & Cameron 2010), but it is surprisingly uncertain how variable such behavioural changes can be, even within similar taxa. Stump-tailed macaque Macaca arctoides females, for example, can become markedly more aggressive towards conspecifics when treated with a synthetic progestin (Linn & Steklis 1990), but hamadryas baboon Papio hamadryas females can become more passive when treated with a similar progestin (Portugal & Asa 1995). Any fertility control application that changes the reproductive capacity of an individual has the potential to induce individual behavioural changes that can alter family group structure, influence interspecific and intraspecific interactions and ultimately shape population dynamics in unforeseen ways. Fertility control in free-roaming wildlife populations has been associated with changes in immigration (Ramsey 2005; Merrill, Cooch & Curtis 2006), decreased group fidelity (Nunez et al. 2009; Madosky et al. 2010), increased survival (Caughley, Pech & Grice 1992; Kirkpatrick & Turner 2007; Williams et al. 2007), altered reproductive behaviour (Nunez, Adelman & Rubenstein 2010; Ransom, Cade & Hobbs 2010) and shifted phenology (Ransom, Hobbs & Bruemmer 2013). Understanding and predicting these sometimes subtle and incremental shifts is difficult, and the challenge of separating the influences of multiple population growth controls can be daunting (Sibly & Hone 2002). To exacerbate these problems, the longitudinal studies needed to detect and quantify long-term population-level effects of fertility control treatments are expensive and time-consuming. Insights into population-level effects of fertility control have largely been accomplished through efforts that simulate population dynamics (Caughley, Pech & Grice 1992; Hone 1992; Hobbs, Bowden & Baker 2000; Davis & Pech 2002; Merrill, Cooch & Curtis 2006). Simulation models can be useful tools for screening management alternatives; however, widespread behavioural and demographic changes induced by fertility control may subvert the underlying assumptions of demographic parameters in models that fail to consider these changes. The assumptions of many fertility control population models could be wrong if the vital rates informing them are based on the wealth of a priori ecological knowledge about species and systems before fertility control was applied. Here, we synthesize findings from studies on population-level effects of wildlife fertility control and compare some of those outcomes with those from individual-level studies. We specifically investigate the demographic and behavioural components from wildlife fertility control studies, seeking to understand feedbacks that might be influencing population-level outcomes of fertility control strategies. We attempt to identify some of the underlying processes to help inform modelling efforts and future design for empirical population-level fertility control studies, and ultimately try to determine whether, in fact, nature can overcome control efforts at a scale that makes fertility control ineffective as a wildlife management tool.