2012 COURSE DATES: AUGUST 4 – 17, 2012 - Sirenian International

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and respond to human encounters by fleeing and retreating to cover”. A gradual reduction of such avoidance commonly is labelled habituation. However humanewildlife encounters represent a complexity of interaction stimuli that render the unitary term habituation problematic (Bejder et al., 2009). With this point in mind, it is surprising that wildlife habituation continues to be treated uncritically within the context of nature-based tourism and sustainable tourism management. Successful commercial wildlife viewing requires that visitors are concentrated in well-defined locations where interactions with wild animals are predictable and constant (Whittaker, 1997). Usually, viewing wildlife takes place where sightings are most consistent, focal animals can be viewed in abundance or, where spectacular behaviours may be predictably observed and experienced (e.g. courtship and socialising behaviours). The critical nature of these sites, in terms of site ecology and wildlife behaviours, raises two important points; (1) That the behavioural state of wild animals varies significantly over time (e.g. across times of day, through different stages of the breeding cycle and across life course) and (2) that animal responses to external stimuli (e.g. the presence of tourists) is likely to vary over time, as influenced by these temporal determinants. These points raise the challenge of understanding and responding to the potential adverse impacts of humanewildlife interactions, not only for the sake of the focal animals, but also from an experiential standpoint with the aim of (1) reducing avoidance, flight or retreat responses and (2) mitigating adverse impacts on animals that may otherwise discontinue critical, site-specific behaviours e.g. by instigating site abandonment. Furthermore, increasingly tourists seek to be assured that their mere presence at wildlife viewing sites (and their associated behaviours) are not to the detriment of the animals that they seek to experience first hand, either in terms of the welfare of individual animals or wider population fitness (Higham & Lusseau, 2004; Muloin, 1998). Such concerns on the part of tourists (and site managers) are well founded. Knight (2009) critiques the dichotomy between wildlife viewing and wildlife hunting as non-consumptive and consumptive respectively, highlighting that viewing and hunting wildlife have some fundamental similarities. First, both engage in locating and identifying target wild animals, which are generally “wary of human presence and reluctant to expose themselves to human eyes” (Knight, 2009: p. 169). Such wariness may be expressed through anti-predatory adaptations, both physical (e.g. camouflage colouration) and behavioural (e.g. concealment) to avoid detection. The directed, intensive and sustained tourist gaze offers a second parallel with hunting (and predation more generally), which also is likely to trigger alarm and anti-predatory responses in individual animals or groups of animals. Tourist satisfaction is commonly associated with close-up, unconstrained and prolonged interactions with wild animals, the experience of critical behaviours (e.g. hunting, feeding, socialising and courtship) and, in some cases, immediate proximity extending to touch (e.g. Muloin, 1998). Although there are some exceptions to this rule (Orams, 2000), the importance of managing ‘humane wildlife viewing interactions’ (as opposed to ‘non-consumptive viewing’ e given the consumptive nature of pursuit, intensive gaze and proximal interaction) is evident. Knight (2009: p. <strong>17</strong>3) proposes that “there appear to be three main ways in which wild animals can be made available for human viewing: capture and confinement; habituation and attraction.” The first, capture and confinement, brings with it behavioural diminution associated with wild animals being physically removed from their natural ecosystem. Also, in many cases, the capture and confinement of ‘charismatic’ wild animals is illegal. The last, attraction, through interventions such as provisioning (i.e. feeding) is J.E.S. Higham, E.J. Shelton / Tourism Management 32 (2011) 1290e1298 1291 equally unpalatable due to its association with manipulated wildlife distributions, compromised feeding (e.g. predatoreprey) relationships, increased probability of aggressive behaviour (both towards animals and people) and consequential diminished behaviours (Orams, 1995). Attraction of animals through supplemental feeding, while affording close and enduring viewing opportunities, also compromises the notion of wild, creating indistinct dividing lines between animals that are wild and those that are confined, tamed or domesticated (Knight, 2009). Of the three approaches to making wild animals viewable, this leaves habituation. Habituation has been defined as “a decrease in the strength of a response after repeated presentations of a stimulus that elicits that response” (Mazur, 2006). As such, habituation typically is viewed as a negative consequence of human interactions with wildlife due to the likely consequential reduction of population fitness arising from reduced danger flight response. However, habituation has been actively applied by zoological scientists in their field studies (i.e. in the wild), having been pioneered by primatologists such as Jane Goodall (Tanzania) working with chimpanzees (Pan troglodytes) and Dian Fossey (Rwanda) with gorillas (Gorilla gorilla) (Knight, 2009). Interestingly, Fossey’s habituation of Gorillas made possible the development of Gorilla tourism as an alternative to Gorilla poaching (Shackley, 1995). Yet habituation has never been treated critically in the specific context of sustainable commercial wildlife viewing (Nisbet, 2000). The relationship between tourists and wild animals is extremely complex (Bejder et al., 2009). Duffus and Dearden (1990) contend that this complexity arises from the interplay of three key components of the wildlife experience; site users, focal wildlife species (both individual animals and local animal populations) and the wider ecology of the viewing site. Given these components, considerations of habituation in ecotourism can be contemplated only in terms of site users (e.g. visitor management, guiding practice), the focal wildlife population (i.e. species-level variables and characteristics of individual animals) and the wider ecology of the focal species (e.g. spatio-temporal ecology) (Higham et al., 2008). Duffus and Dearden (1990) highlight also the temporal dimension in so far as tourist interactions with wildlife animals vary within diurnal, seasonal and life course timeframes, a point that has been inadequately addressed in academic discussions of habituation (Bejder et al., 2009). Following Duffus and Dearden (1990) then, some species of wild animals, and some individual animals, demonstrate a well-established response of inquisitiveness to humans or signs of human activity. Others are intensely private, remain concealed from onlookers, and flee readily from human interaction. In terms of inquisitiveness and active interaction, gulls are a ubiquitous example but rarely are gulls the focal species of interest to ecotourism operators and their visitors (Shelton & Higham, 2007). Useful approaches to the task of analysing the behaviour of species that are of tourist interest should, however, prove to be of considerable value. Applied behaviour analysis, based on the notion of stimulus control and situated within learning theory, is well suited to provide a formulative framework for those humanewildlife interactions that are of interest to commercial tourism operators. In this respect, the term habituation has been described as any situation where wildlife come to tolerate the presence of humans without any obvious signs of physiological or behavioural response (Shackley, 1996). Under this definition, habituation may be considered a mitigation or cessation of impact. The use of the term habituation in tourism and recreation has been applied also when animals approach people, or scavenge for food (Newsome et al., 2005). Park managers in North America attempt to educate the public not to engage in behaviours that will merge habituation and approach-for-food, particularly in the case of deer (The National Park Service, 2006a, 2006b) and bears (Davis, Wellwood, & Ciarniello, 2002).
1292 To be as useful as possible, habituation must be distinguished from foraging or increased approach behaviour, even though the three phenomena regularly occur together (Davis et al., 2002). The starting point for such an undertaking is a critical behavioural analysis of wildlife habituation. In response to this need, a critical discussion of animal responses to human presence in presented, in order to achieve a more fine-grained understanding of habituation in all of its complexity. This critique provides a platform from which then to consider habituation within the context of sustainable wildlife tourism management. 3. A behavioural formulation of wildlife habituation A behavioural formulation of wildlife habituation should begin by acknowledging the poor fit between observable animal behaviour and internal state (Ellenberg et al., 2006). In other words, the apparent tolerance of some wildlife species to approach and observation may not necessarily mean that these wild animals are not being impacted. Bejder et al. (2009) explain that wildlife tolerance of human stimuli may arise from various factors including: (1) Displacement: e.g. less tolerant individual animals may be displaced, resulting in a bias towards more tolerant animals that remain at a given site. (2) Physiology: e.g. reduced responsiveness to human stimuli due to physiological impairment. (3) Ecology: e.g. lack of suitable adjacent habitat to which animals may otherwise relocate. This poor fit has been demonstrated in the case of penguins (Ellenberg et al., 2006) where artificial eggs placed under incubating birds record elevated heart rate in birds that outwardly appeared to be unaffected when approached (Nimon, Schroter, & Stonehouse, 1995). An understanding of habituation must acknowledge both the presence and absence of specific behaviours, and that impacts of significance at both the individual and species level may arise from both behavioural classes. The presence or absence of behaviours may vary at different scales of analysis, from individual animals to Table 1 A critical behavioural formulation of the unitary term habituation. J.E.S. Higham, E.J. Shelton / Tourism Management 32 (2011) 1290e1298 entire populations (Bejder et al., 2006; Lusseau, 2003; Shelton & Higham, 2007), and is dynamic over time. Following Bejder et al. (2009), a behavioural formulation of habituation in the specific context of wildlife-based tourism may be presented in four parts; 1. Avoidance/approach behaviours, 2. Tolerance, 3. Habituation and 4. Sensitisation (Table 1). 3.1. Avoidance/approach behaviour An important starting point for any critical discussion of habituation is an understanding of the complexity of avoidance and approach behaviours. The avoidance behaviours of cetaceans when engaged in interactions with tourist vessels have been particularly well researched (Baker, Perry, & Vequist, 1988; Corkeron, 1995; Lusseau, 2003; Salden, 1988; ). Although responses to boat traffic vary between species, some show signs of active avoidance, ranging from altered movement patterns (Bejder, Dawson, & Harraway,1999; Campagna, Rivarola, Greene, & Tagliorette, 1995; Edds & MacFarlane, 1987; Nowacek, Wells, & Solow, 2001; Salvado, Kleiber, & Dizon, 1992), increases in dive intervals (Baker & Herman, 1989; Baker et al., 1988; Blane, 1990; Janik & Thompson, 1996; MacGibbon, 1991) and increases in swimming speed (Blane & Jaakson, 1995; Williams, Trites, & Bain, 2002). Avoidance behaviours in Bottlenose dolphins (Tursiops truncatus) have been shown to vary at an individual level (Lusseau, 2003), where male animals show a greater propensity to avoid boat traffic than females with calves (see Higham & Lusseau, 2004). These studies present clear evidence of animal avoidance behaviours, not only as a result of the presence of boats, but also arising from the manoeuvring of boats, including sudden changes in vessel speed and rapid approaches (Constantine, 2001; Gordon, Leaper, Hartley, & Chappell, 1992; MacGibbon, 1991). In 2006, the <strong>International</strong> Whaling Commission reached agreement that “there is compelling evidence that the fitness of individual odontocetes repeatedly exposed to whale-watching vessel traffic can be compromised and that this can lead to population-level effects” (IWC, 2006). This consensus has been reached in light of recent studies that suggest avoidance responses from cetaceans when Concept Variables Cases 1. Avoidance/approach Avoidance response (e.g. pre-emptive avoidance) Male Bottlenose dolphins (Tursiops truncatus) behaviour Response behaviours (e.g. generalised vigilance, concealment, discontinuation of critical behaviours) Male Bottlenose dolphins (Tursiops truncatus) Stimulus control (i.e. group and individual behaviours) Adele penguins (Pygoscelie adeliae); Little penguins (Eudyptula minor); Bottlenose dolphins (Tursiops truncatus) Exploratory approach behaviour Elephant seal (Mirounga leonine) Opportunistic approach behaviour Buller’s mollymawk (Diomedea bulleri); Giant petrel (Macronectes giganteus) Discriminative stimulus Fantail/piwakawaka (Rhipidura fuliginosa); Southern Royal albatross (Diomedea epomophora) 2. Tolerance Intrinsic tolerance Little penguins (Eudyptula minor); Spotted shags (Stictocarbo punctatus); Stewart Island shags (Leucocarbo chalconotus); Little shags (Phalacrocorax melanoleucos) Selective tolerance New Zealand sea lion (Phocarctos hookeri) Seasonal tolerance New Zealand wood pigeon/kereru (Hemiphaga novaseelandiae) 3. Habituation Approach habituation New Zealand dabchick (Poliocephalus rufopectus) Spatio-temporally bound habituation Colonial breeding female New Zealand fur seal (Arctocephalus forsteri). Socially acquired absence of avoidance behaviour New Zealand fur seal (Arctocephalus forsteri) neonates Socially acquired habituation Female New Zealand fur seal (Arctocephalus forsteri) (e.g. new colony recruits) Reduced physiological arousal Northern Royal albatross (Diomedea epomophora sanfordi) Reduced avoidance behaviour Yellow-eyed penguin (Megadyptes antipodes) 4. Sensitisation Sensitisation Stoats(Mustela erminea) (i.e. in the laboratory) Paradoxical sensitisation Galapagos marine iguana (Mblyrhynchus cristatus)
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ECOLOGY, BEHAVIOR & CONSERVATION OF
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ABOUT BELIZE Research Site: The pro
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OUR INVESTIGATION Figure 2. G. crut
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direction, and (e) when ‘travelli
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172 NOTES Caribbean Journal of Scie
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$1.2 million (Moore et al. 2009a).
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animals may adopt microhabitat choi
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2012 COURSE DATES: AUGUST 4 – 17, 2012 - Sirenian International

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