Human–wildlife interactions involving anthropogenic foods (e.g. crops, fish captured with hooks or traps, food waste, provisioned foods) often result in death or injury (to humans or to wildlife), the culling of ‘problem’ wildlife, property damage, and economic loss (e.g. Bryant, 1994; Conover et al., 1995; Herrero, 2001; McGrath, 2001; McNay, 2002; Osborn, 2002; Gilman et al., 2006). Management of these interactions requires information on how animals learn to use anthropogenic foods, both to develop effective mitigation measures and to predict which animals are likely to acquire these undesirable behaviours (Whittaker & Knight, 1998; Taylor & Knight, 2003; Breck et al., 2008; Mazur & Seher, 2008). Many taxa that use anthropogenic foods, including elephants, cetaceans, canids, ursids and primates, have the capacity to acquire novel foraging behaviours in part through social learning (Box & Gibson, 1999; Galef & Giraldeau, 2001; Galef & Laland, 2005; Breck et al., 2008; Mazur & Seher, 2008). Despite this, few studies have examined whether social learning can influence how wild animals learn to use anthropogenic foods (Rendell & Whitehead, 2001a,b; Whitehead et al., 2004; Breck et al., 2008; Hoppitt & Laland, 2008; Mazur & Seher, 2008). Here, we examine whether social learning influenced bottlenose dolphins (Tursiops aduncus) that learned to accept food from recreational fishers in Western Australia, and whether predictor variables could be developed to indicate whether animals would learn to acquire anthropogenic foods, based on individual-specific data (Finn, 2005; Finn, Donaldson & Calver, 2008).
How can social learning influence how animals learn about anthropogenic foods?
Animals that learn to eat anthropogenic foods are often described as ‘food-conditioned’ (Breck et al., 2008; Mazur & Seher, 2008), ‘conditioned’ (Finn et al., 2008) or ‘conditioned to human interaction by food reinforcement’ (Samuels & Bejder, 2004), on the basis that they have acquired food-based behaviours through operant conditioning. In this context, operant conditioning is a learning process in which animals learn about anthropogenic food sources through: (1) their exposure to certain food-related human stimuli (e.g. campsites, human provisioners, fishing gear); (2) the utilization of particular behaviours in response to those stimuli (e.g. opening a lid, solicitous behaviours); (3) a food reward that positively reinforces these behaviours (e.g. food scraps) (Reynolds, 1975; McFarland, 1981; Whittaker & Knight, 1998; Samuels & Bejder, 2004; Young & Cipreste, 2004; Breck et al., 2008). Operant conditioning with food reinforcement implies a determinant role for human-related factors in acquiring novel behaviours. In natural environments, the deliberate or inadvertent presentation of a food source exposes animals to food-related stimuli and, for the period that it is available, sustains reinforcement for behaviours developed in response to these stimuli. Where feeding is deliberate, human provisioners can selectively reinforce certain conditioned behaviours, such as solicitous gestures (Mann, 2001; Durden, 2005; Finn et al., 2008).
The determinant role of human-related factors in the conditioning process suggests that animals may typically acquire behaviours for feeding on anthropogenic foods largely or solely through individual asocial learning (i.e. through their own independent experience of an environment containing anthropogenic food sources). Asocial learning is likely to be sufficient for the conditioning of species that receive limited maternal care and are solitary as juveniles and adults, and thus have few opportunities for observations of conspecifics interacting with anthropogenic foods. However, social learning could influence conditioning in more social species, particularly if social learning also influences the acquisition of the information and skills underlying natural behaviours (Whiten & Ham, 1992; Giraldeau, Caraco & Valone, 1994; Heyes & Galef Jr, 1996; Laland, Richerson & Boyd, 1996; Boran & Heimlich, 1999; Byrne, 1999; Galef & Giraldeau, 2001; Osborn, 2002; Whitehead et al., 2004; Breck et al., 2008; Hoppitt & Laland, 2008; Laland, Atton & Webster, 2011; Slagsvold & Wiebe, 2011; Thornton & Clutton-Brock, 2011). Social learning may be particularly important in species with extended periods of juvenile dependence and social structures involving long-term relationships between individuals (e.g. bottlenose dolphins: Wells, Scott & Irvine, 1987; Connor, Smolker & Richards, 1992; Connor et al., 2000; Rendell & Whitehead, 2001a; Lusseau, 2003; Krützen et al., 2005; Sargeant et al., 2005, 2007; Sargeant & Mann, 2009).
Further, as operant conditioning is a learning process, animals may integrate information and skills that are individually and socially acquired, making the ultimate acquisition of a learned behaviour the result of both individual experience and social influences (Galef & Giraldeau, 2001; Sargeant & Mann, 2009). For learned behaviours involving anthropogenic foods, social learning could occur through mechanisms ranging from stimulus or local enhancement to imitative learning (Whiten & Ham, 1992; Zentall, 2006; Hoppitt & Laland, 2008). These considerations suggest how social learning could play a facilitative or supplementary role in the acquisition of learned behaviours involving the use of anthropogenic foods, and thus potentially influence which individuals within a population become conditioned to human interaction (Rendell & Whitehead, 2001a,b). This view avoids the either/or dichotomy between asocial and social learning that sometimes characterizes debate over concepts such as culture and tradition (e.g. Heyes & Galef Jr, 1996; Rendell & Whitehead, 2001a,b; Whitehead et al., 2004; Krützen et al., 2005; Laland & Janik, 2006; Sargeant et al., 2007).
Human–dolphin interactions and anthropogenic food sources
Both bottlenose dolphin species (common bottlenose dolphin Tursiops trunactus and Indo-Pacific bottlenose dolphin T. aduncus) may engage in interactions with humans that are illegal, harmful or undesirable, based on their learning to accept food from recreational fishers or to obtain fish from fishing gear (depredation) (e.g. Bryant, 1994; Samuels & Bejder, 2004; Durden, 2005; Finn et al., 2008; Donaldson, Finn & Calver, 2010). Such interactions are particularly prevalent when dolphins exhibit long-term fidelity to (or seasonal occupancy of) coastal or estuarine areas that have high levels of human use, and thus may interact frequently with recreational users, tourism operators and commercial fishermen (Wells et al., 1987; Connor et al., 2000; Samuels, Bejder & Heinrich, 2000; Bejder & Samuels, 2003; Samuels et al., 2003).
Finn et al. (2008) documented a long-term (1993–2003) human–wildlife interaction based on recreational fishers illegally feeding members of a resident bottlenose dolphin (T. aduncus) community in Cockburn Sound, Western Australia. They found that the number of dolphins exhibiting behaviours indicative of conditioning to human interaction by food reinforcement increased over time, from 1 in 1993 to 14 by mid-2003. The availability of long-term ecological and behavioural information for known individuals provided a unique opportunity to examine whether social learning influenced the apparent conditioning of dolphins to human interaction in Cockburn Sound.
Here we developed predictor variables for whether dolphins in Cockburn Sound became conditioned, based on environmental (distribution of recreational boats), biological (age-class and sex) and behavioural (ranging and association patterns) data, and examined the contribution of these variables using a generalized linear model. Our focus was whether the conditioning of individual dolphins was associated with four variables: (1) sex; (2) age-class; (3) use of areas with high densities of recreational boats prior to becoming conditioned; (4) patterns of associations prior to becoming conditioned. We used the findings from the model to examine the following hypotheses:
- Exposure to human provisioners H0: Whether a dolphin became conditioned showed no association with the frequency with which individuals utilized areas with high densities of human provisioners;
- Behavioural propensities H0: Whether a dolphin became conditioned showed no association with age-class or sex; and
- Social learning H0: Whether a dolphin became conditioned showed no relationship with individual patterns of association.
We consider the findings to illustrate how long-term and individual-specific data can be used to identify key factors associated with harmful human–wildlife interactions and, for social species, to examine the potential influence of social learning.