In Australia, a multi-million-dollar industry is based on viewing the Australian fur seal (Arctocephalus pusillus doriferus), predominantly through boat visits to breeding colonies. Regulation of boat approaches varies by site and no systematic investigations have been performed to inform management guidelines. To investigate possible effects of disturbance, experimental boat approaches were made to a colony at Kanowna Island in northern Bass Strait and seal responses were monitored using instantaneous scan sampling. Colony attendance (individuals remaining ashore) was found to be influenced by approach distance and time of day, but was not affected by environmental variables or season, whereas onshore resting behavior was influenced by approach distance, time of day, ambient temperature and wind direction. Onshore resting behavior decreased following experimental boat approaches to 75 m, but changes in abundance of individuals ashore were not observed at this distance. In contrast, approaches to 25 m elicited a strong response, with a steep decline in the number of individuals ashore. This response was strongest when approaches occurred in the morning, with a decline of approximately 47% of individuals, compared to a decline of 21% during afternoon approaches. With regard to onshore resting behavior, afternoon approaches to 75 m led to minimal response. The remaining three combinations of approach distance and time of day had a similar pattern of reductions in the proportion of individuals engaging in onshore resting behavior. The strongest response was again seen during approaches to 25 m conducted in the morning. These behavior changes suggest that unrestricted boat-based ecotourism at Australian fur seal colonies has the potential to increase energy expenditure and reduce the number of seals ashore. Increasing minimum approach distances to ≥75 m and/or restricting visits to afternoons may minimize these impacts at Kanowna Island during the post-molt and non-breeding seasons. As several studies have demonstrated considerable intra-species variation in seal responses to boat approaches, research at other colonies is needed before these findings can be generalized to the remainder of the Australian fur seal population.

Arctocephalus pusillus, pinnipeds, disturbance, ecotourism, tourism management

Despite their association with the marine environment, pinnipeds must haul-out on land or ice to rest, evade marine predators, and molt. In addition, they give birth and nurse their young ashore (Gentry and Kooyman 1986; Riedman 1990). While ashore, seals utilize sight, smell and hearing to detect potential above-water threats and to perceive the level of risk these threats present to their survival (Frid and Dill 2002; Nordstrom 2002). When a perceived above-water threat is detected, and individuals deem this threat to be significant, seals will respond by fleeing to the relative safety of the water (Cowling et al. 2015). In gregarious pinnipeds, individuals often detect threats and perceive risk based on the responses of their neighbors, leading to large-scale cascading responses in densely occupied areas that can result in injuries and have significant impacts on colony attendance (Barton et al. 1998; Jay et al. 1998; Stirling 1972).

Pinniped-based ecotourism activities make use of seal haul-out behavior to observe individuals in their natural habitat (Kirkwood et al. 2003). Although the purpose of ecotourism is to give patrons the opportunity to observe animals in the wild engaging in typical behaviors (Orams 1995), ecotourism-based human interactions may instead alter pinniped behavior by initiating responses indicative of predation risk (Frid and Dill 2002). Such responses can interrupt vital activities, increase energy expenditure, reduce breeding success and even cause injury or death (Boren et al. 2002; Marmion 1997; Shaughnessy et al. 2008).

Various environmental factors have the potential to influence a seal’s ability to detect threat stimuli and, thus, may also affect responses to anthropogenic disturbance. Wind strength and direction can greatly affect both olfactory and auditory detection of a potential threat (Riedman 1990). Also, sea conditions may influence the willingness of individuals to return to the water, potentially confounding any response to boat-based disturbance. In addition, distance, speed and direction of anthropogenic approach can be important factors in perceived risk, further influencing a seal’s response (Frid and Dill 2002; Shaughnessy et al. 2008).

The Australian fur seal (Arctocephalus pusillus doriferus) is one of the world’s least abundant fur seals and is endemic to Bass Strait, southeastern Australia (Kirkwood et al. 2010). Ecotourism operators visit Australian fur seals at numerous locations, including haul-out sites (where few pup births occur) and breeding colonies (Kirkwood et al. 2003). Previous research on Australian fur seals at haul-outs has indicated that seals there are particularly sensitive to both land- and boat-based approaches (Burleigh et al. 2008; Shaughnessy et al. 2008). When on land, the seals perceive threats by sight, sound and smell, and generally respond by becoming alert (changing posture and looking toward the threat) and moving to the water (Kirkwood and Dickie 2006; Shaughnessy et al. 2008). Responses may be more pronounced at breeding colonies than at haul-outs, as haul-outs contain mainly adult/sub-adult male and juvenile seals, whereas colonies are densely populated with adult females and pups, groups that are particularly sensitive to disturbance (Barton et al. 1998; Boren et al. 2002; Holcomb et al. 2009). In addition, in colonies where seals have access to higher elevations individuals might perceive their distance to water as greater than seals on flat terrain, and thus sense a greater threat from the boat’s approach. They may also detect the boat from a greater distance. Research on New Zealand fur seals has indicated that early detection of a threat tends to moderate responses (Boren 2001).

Despite a multi-million-dollar ecotourism industry based on visits to Australian fur seal breeding colonies (Kirkwood et al. 2003), descriptive and observational data have suggested a heightened response to above-water threats in this species. However, only limited conclusions can be drawn from such data. At the time of undertaking this study management guidelines at Australian fur seal breeding colonies varied by site and season, with minimum approach regulations ranging widely from 30 m (year-round, Seal Rocks) to between 50 m (non-breeding season, Kanowna Island) and 200 m (breeding season, Kanowna Island). These guidelines are largely based on anecdotal evidence. Needlessly strict guidelines may harm ecotour businesses, while unrestricted access could negatively affect seal populations. A recent study on the effects of boat-based approaches on New Zealand fur seals highlighted the ability of evidence-based studies to inform mitigation guidelines (Cowling et al. 2015). However, before evidence-based mitigation guidelines can be proposed for Australian fur seals, controlled studies, which account for potential confounding factors, must be conducted to assess species-specific responses to boat approaches. Therefore, the aims of the present study were to determine seal attendance and behavior in relation to controlled boat approaches at a breeding colony while accounting for potentially confounding environmental variables.

Australian fur seals at the Kanowna Island colony responded to experimental boat approaches to both 75 and 25 m by becoming more active ashore and responded to 25 m approaches by fleeing to the water. Of the factors examined in the present study, proximity of approach had the greatest influence on the ability of seals to detect a boat and perceive it to be a threat. Time of day also influenced the strength of responses (determined by the steepness of decline during the disturbance period) to boat approaches, while environmental factors (temperature, wind speed/direction) were only observed to affect baseline resting behavior.

Australian fur seals, like other fur seals, are thought to rely on olfaction or auditory stimuli as principle means of detecting threats when they are on land (Riedman 1990; Shaughnessy et al. 1999). This is because they are short-sighted when out of water and cannot focus on objects in the distance (Hanke et al. 2006). The results of the present study, in which individuals were disturbed by boats up to 75 m away, suggest initial detection was by olfaction or audition. However, although individuals ashore displayed increased alert behaviors, when boats remained at 75 m this did not translate into animals leaving the colony. In contrast, when boats approached to 25 m, departures occurred. As such, it appears that while olfaction/auditory stimuli play a role in the initial detection of a potential threat, individuals may not respond further until a threat is perceived to be imminent (Tripovich et al. 2012).

The most severe response Australian fur seals exhibited to boat approaches was to flee toward the water; during approaches to 25 m, this caused dramatic changes in colony attendance. The periods fur seals spend ashore at colonies are particularly important for resting, evading predators, molting, breeding and rearing young (Gentry and Kooyman 1986; Riedman 1990). Fleeing behaviors in themselves expend energy, and time spent in the water as a result of flight responses can also be energetically costly due to active movement, being alert for predators and maintaining body temperature (Donohue et al. 2000). The actual energetic costs related to fleeing behaviors in this species are difficult to determine, but could result in the need for additional rest time ashore and/or greater caloric intake.

Fleeing responses to boat approaches may have even greater implications for adult females and pups, which are of particular concern because they are bound to breeding colonies and may be more energetically constrained than other age classes (Barton et al. 1998; Boren et al. 2002; Riedman 1990). Pups are also at risk of being trampled or falling from cliffs as a result of stampedes (Mattlin 1978). In addition, if they flee into the water they would incur high energetic costs and experience greater risk of predation, as they are small and have limited swimming and diving capabilities (Donohue et al. 2000; Shaughnessy et al. 1999). The separation of mother-pup pairs and resulting interruptions to suckling behavior also have serious implications for pup survival (Boren 2001; Kovacs and Innes 1990).

Although boat approaches to 75 m did not significantly impact seal attendance, the observation that approaches to 75 m resulted in significant behavioral changes still has substantial implications. Many seals remaining ashore changed posture and stayed alert for the entire duration of the boat’s visit, investing more time and potentially more energy into vigilance behavior (Amo et al. 2006; Lidgard 1996) than they did before the boat arrived. Thus, events that appear to cause low-level disturbance without large-scale changes in attendance at Australian fur seal colonies could influence a seal’s energy budget. Further investigation of the physiological impacts of disturbance on this species is warranted.

Time of day was also found to influence seal responses to boat disturbance, with individuals showing stronger responses to disturbance during morning approaches. It is possible that the weaker response observed in the afternoon was biased by afternoon trials being preceded by a morning approach, which may have habituated the seals present for the earlier approach or displaced sensitive seals to another location at the colony (Nordstrom 2002). Two approaches occurred on the same day for 80.0% of trials. Further investigation into decreased sensitivity with repeated disturbance, as well as potential temporal and density-dependent responses, is needed to fully explain these results. In relation to vessel approaches, greater caution or greater approach distances may be required at the first approach compared with latter approaches.

While colony-level responses to boat approaches were not found to differ between seasons, ambient temperature did have an effect on baseline resting behavior, with individuals more likely to be resting at cooler temperatures. However, no effect was identified with regard to the number of individuals remaining ashore during boat approaches, suggesting that temperature did not influence individual responses to threat stimuli. Cowling et al. (2015) identified a seasonal influence on seal response to such stimuli, with the proportion of New Zealand fur seals at rest decreasing during summer months. However, Cowling et al. (2015) did not measure ambient conditions directly but rather used time of year as a proxy for weather so it is not clear whether their results were temperature-related or due to other factors, such as breeding cycle. Further studies on the influence of temperature on fur seal behavior, particularly in terms of resting behavior and disturbance, is needed to clarify these relationships.

For many pinniped species, colonies are not restricted to the immediate shoreline and can often extend considerable distances and/or elevations inland (Stevens and Boness 2003). Seals resting inland may be less likely to detect an approaching boat and, because proximity to the water provides a level of security for some seals (van Polanen Petel 2005), they may perceive a higher threat level and, consequently, respond more severely than seals near the water’s edge. Hence, disturbances that affect animals inland at colonies may result in extra energy expenditure due to the greater distances animals must travel to get to water, and may cause injury and even death if stampeding animals fall over cliffs or into crevasses (Mattlin 1978).

In the present study, the number of seals descending from the hinterland above the study area increased during 21.1% of experimental approaches. Three stampedes also occurred there as a result of boat approaches. During one such stampede (the final of the three) in the non-breeding season, two pups were observed to fall >10 m from a cliff and land on rock shelves below. Two of these stampedes occurred during afternoon approaches to 25 m, while one occurred during a morning approach to 75 m. Similar events were observed at a New Zealand fur seal colony due to land-based research activities, with stampedes causing several pups to be trampled to death and another pup dying as a result of falling 10 m off a cliff (Mattlin 1978). Direct injuries or mortalities to pups resulting from boat approaches have not been observed in Australian fur seals or other pinniped species (Boren et al. 2002; Burleigh et al. 2008; Nordstrom 2002; Shaughnessy et al. 2008). Due to the relative rarity of these events, we were unable to determine which approach distance or environmental factors (e.g. wind direction) influenced hinterland stampedes. Nonetheless, these findings do suggest that guidelines at the time of this study allowing 50-m approach distances at Kanowna Island would be unlikely to entirely preclude such events. It is possible that limiting approaches to ≥75 m and to afternoons could minimise hinterland stampedes but further research would be needed to confirm this. While the infrequency of these events suggests they are unlikely to have population-level effects, such disturbance impacts are in violation of state and federal regulations protecting marine mammals (IUCN 2007; Patkin 2005). Thus, the terrain of colony and haul-out sites, particularly seal use of hinterland/elevated regions, should be taken into consideration when developing management guidelines. Haul-out sites or low-lying colonies with limited access to such areas may not need to be managed as stringently as colonies with greater variation in terrain.

There were several limitations to this study. In addition to inter-specific variation among pinnipeds, several previous studies demonstrated a high degree of intra-species variation due to factors including age/sex class present, site type, density ashore and previous exposure to humans (Barton et al. 1998; Boren et al. 2002; Shaughnessy et al. 2008). Hence, developing appropriate management guidelines is challenging without extensive species-specific investigation. As this study was conducted at a single site, interpretation of data with regard to site structure, terrain, population density and previous exposure to vessel traffic must be made with caution, limiting the generalizability of these findings to other breeding sites. In addition, analysis based on boat size and vessel-related noise could not be conducted due to logistical constraints.

Furthermore, colony attendance and onshore behaviour were treated as independent predictor variables within two separate GAMMs. There exists the possibility that different behavioral phenotypes within the population meant that only a certain class of individuals remained onshore during boat approaches – the bold individuals – as such these data may not be truly independent. Model complexity (nested data structure with non-linear responses) excluded us from examining these data using multivariate methods. Therefore, data should be interpreted with the understanding that onshore behavioural responses represent the subset of the population that remained onshore and that this subset may not be a truly random sample of the population as a whole.

In summary, the findings of the present study reveal distinct gradients of response to the approach of boats at an Australian fur seal colony influenced by both approach distance and time of day. These results suggest that unrestricted boat-based ecotourism at colonies, particularly approaches to <75 m, may have implications for energy expenditure and reproductive success in the Australian fur seal. Current guidelines, implemented following this study, now limit boat approaches to 100 m at Kanowna Island from March through October now making them unlikely to affect behaviour at this colony. However, this study was limited to a single colony and further research will be needed to generalize these results to other sites.

We gratefully acknowledge the assistance of many fieldwork volunteers and particularly appreciated the logistical support of Geoff Boyd at Prom Adventurer tours, Caitlin Vertigan, and the staff at Phillip Island Nature Parks, Wilsons Promontory National Park and Wildlife Coast Cruises. Financial and logistical support for this research was provided by Parks Victoria, Phillip Island Nature Parks and the Australian-American Fulbright Commission. The research was conducted under Deakin University Animal Welfare Committee approval A10-2008 and Department of Sustainability and Environment (Victoria) Wildlife Research Permit 10005362.