Effect of human recreation on bird anti-predatory response

Introduction

Human disturbance through recreational activities has been found to negatively affect wildlife (Thiel et al., 2007; Kangas et al., 2010; Coppes et al., 2017; Bötsch, Tablado & Jenni, 2017). To protect wild animals from the negative effects of recreation, zones with restricted access or buffer zones around breeding areas are a widely recommended mitigation measure (Rodgers & Smith, 1995; Fernández-Juricic, Jimenez & Lucas, 2001; Blumstein et al., 2003; Ikuta & Blumstein, 2003; Webb & Blumstein, 2005). In order to define these buffer zones an appropriate set-back distance, matching the focal species needs, has to be chosen. Unfortunately, conservation measures often have to be defined quickly and ad hoc, without time for area-specific in-depth studies. Often the so-called flight initiation distance (FID) has been used to define a minimal set-back distance. FID is the distance at which humans can approach a species before triggering its anti-predatory/escape behavior. FIDs have been used widely for decades and still are considered a good surrogate for set-back distances (Samia et al., 2017).

Many modulating factors have been found to affect these FIDs (Gutzwiller & Marcum, 1997; Eason et al., 2006; Thiel et al., 2007; Randler, 2008; Carrete & Tella, 2010; Legagneux & Ducatez, 2013; Cavalli et al., 2016; Wilson-Aggarwal et al., 2016; Lethlean et al., 2017). There are intrinsic differences between species and individuals (Blumstein et al., 2003; Carrete & Tella, 2010), but also many habitat- and context-specific effects have been reported, such as shorter FIDs in denser habitats (Tablado & Jenni, 2017). Recently, studies have shown differences in bird tolerance to human approach across an urban–rural gradient, with urban populations showing reduced FIDs compared to rural conspecifics (McGiffin et al., 2013; Møller et al., 2013; Cavalli et al., 2016). These reduced FIDs have been attributed to habituation to human presence and/or the selection of human-tolerant individuals (personalities) in urban environments (McGiffin et al., 2013; Cavalli et al., 2016; Vincze et al., 2016; Samia et al., 2017; Sprau & Dingemanse, 2017). However, urban and rural habitats do not only differ in the presence of humans but also in habitat structure which might also affect bird escape reactions (FID; Whittingham et al., 2004; Thiel et al., 2007). It remains then unclear whether to what extent the differences in FIDs between urban and rural environments are due to differences between habitats or to the frequency of humans. Moreover, little is known about the effect of lower levels of human presence, such as that occurring during recreation in natural areas, on bird anti-predatory behavior.

Therefore, the aim of this study was to investigate the effect of human presence per se on anti-predatory responses in natural areas (forests). That is, whether FIDs of birds in forests near large urban settlements, and thus often frequented by recreationists, differ from bird FIDs in rarely visited forests of similar structure.

Material and Methods

Results

For each species we had the following FID sample sizes: 73 for Common Blackbird, 121 for Common Chaffinch, 62 for Eurasian Nuthatch, 94 for European Robin, 132 for Great Tit, 39 for Marsh Tit, 23 for Short-toed Treecreeper, 26 for Song Thrush, and 74 for Winter Wren.

All bird species, except the marsh tit, showed a trend towards larger FIDs in forests further away from a city (Fig. 1; Table 1). Considering the PP (Fig. 1) of the regression line slopes, the effect of recreation, approximated as distance to cities, on FID was especially strong in Common Blackbirds, Common Chaffinch, European Robin, Short-toed Treecreeper, and Eurasian Nuthatch.

Apart from distance to cities, other factors that also seemed to determine FID were height above ground and starting distance. The higher above ground a bird was located, the shorter was its horizontal FID (Table 1), whereas the starting distance was positively correlated with the FID (Table 1).

Discussion

Recreation showed a substantial effect on bird anti-predatory responses. Birds had shorter FIDs in forests close to cities (intensively frequented by humans) than in forests further away from cities (i.e., less visited by humans). Because the habitat was very similar, this indicates that the shorter FID is most likely due to human presence. It also agrees with the studies suggesting that the shorter FIDs found in urban environments, when compared to rural ones, are mainly due to human presence (Cavalli et al., 2016). People may be perceived by naive wildlife as predators (Frid & Dill, 2002; Beale & Monaghan, 2004). This may explain why we find large FIDs in forests where birds did not have that much experience with humans (“non-habituated”). In contrast, in forests with higher human frequentation birds could have “habituated” to non-threatening recreationists and reduce their behavioral anti-predatory response. An alternative explanation for our finding could be a redistribution of personalities, as recently shown by Sprau & Dingemanse (2017). That is, personality types could be non-randomly distributed along a gradient with bolder animals being more frequent in forests with more human presence (closer to cities), whereas shyer individuals would be restricted to less frequently visited forests. We also expect that habituation will occur faster or slower depending on the species and the personality of the individuals. Further studies may investigate whether there is a threshold of pedestrians required for birds to become habituated or rearranged according to their personality, resulting in different escape strategy patterns.

Whether non-random settlement or phenotypic plasticity is the driving factor for reduced FIDs in heavily frequented forests cannot be inferred from our data. We acknowledge that with only three forests along a distance-to-the-city gradient, it is hard to generalize and we cannot rule out completely the influences of other local factors. However, the proximity of the three forests (i.e., similar climatic conditions and socio-economic areas), the fact that the species are the same and the similarity in vegetation structure among the three forests, strongly suggests that the effect is most likely due to differences in exposure to humans.

Conclusion

In conclusion, bird anti-predatory responses (FID) are affected by human recreation intensity. Thus, when FID is to be used for defining set-back distances, local FIDs should be measured to avoid mismatching between bird tolerances to humans in areas where the FID was measured and the ones in the local area where it will be applied. If human disturbance already occurred at a given site, the most vulnerable species or individuals might already have left the site. Therefore, FIDs always have to be carefully interpreted before using it to establish set-back distances. Our finding implies that future studies measuring FIDs should also incorporate site-specific human recreation intensity as a modulating factor for FIDs.

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