Response of tropical avifauna to visitor recreational disturbances: a case study from the Sinharaja World Heritage Forest, Sri Lanka

Nature-based tourism has wide implications for biodiversity-rich tropical countries. Recreational opportunities such as wildlife observation is an important dimension that is often considered in establishing protected areas (PAs), given that it is expected to generate public interest while ensuring the economic viability of their establishment (Suntikul et al. 2010). At present, Sri Lanka’s PA network, especially national parks and forest reserves, are increasingly becoming prime nature-based tourism destinations for both international and domestic tourists (Perera et al. 2012). Since visitor pressure continues to increase on PAs, their administrators are facing the quandary of positively meeting the diverse expectations of visitors while effectively conserving these biological resources.

It has been reported that increased non-consumptive uses of PAs, such as nature-based tourism, cause negative impacts on wildlife. Although the effect of recreational tourists is expected to be less than of logging or fragmentation (Chazdon et al. 2009; Borgmann 2010; Gibson et al. 2011), nevertheless visitors to wildlife refuges can disturb birds, causing them to leave their habitats temporarily or permanently. Recreational disturbances often cause birds to spend considerable amounts from their energy budget to avoid humans, i.e., the vital energy that otherwise could be conserved for survival, migration and breeding. Nature-based recreation can have significant negative effects at the individual, population and community level (Fernández-Juricic and Tellería 2000; Mallord et al. 2007; Steven et al. 2011; González-Oreja et al. 2012; Wang et al. 2013).

Much of the past work on impacts of recreational disturbances on avifauna has been focused on waterbirds, where the negative effects of human recreational activities on their foraging behavior and habitat use have been well documented (Fernández-Juricic and Tellería 2000; Verhulst et al. 2001; Rodgers and Schwikert 2002; Stolen 2003; Pease et al. 2005; Cardoni et al. 2008). Human recreational disturbances are also known to cause reduction of reproductive success and nesting failures (Bolduc and Guillemette 2003; Finney et al. 2005; McGowan and Simons 2006; Steven et al. 2011; Whitfield and Rae, 2014). As explained by Holm and Laursen (2009), disturbances caused by hikers alone can negatively affect territorial densities of certain birds, causing effective habitat loss for breeding. However, such impacts seem to be species-specific and for some birds, human use of recreational trails has no apparent effect on nest survival (Smith-Castro and Rodewald 2010).

Many studies have correlated higher pedestrian or vehicle traffic in wildlife refuges to reduced species richness and abundance of birds (Fernández-Juricic 2000; Bautista et al. 2004; Burger et al. 2004; Marcum 2005; Steven et al. 2011). However, not all bird species are equally affected by human recreational disturbances. Certain avian species can tolerate greater degrees of disturbances (Marcum 2005; Gill 2007; Cardoni et al. 2008). The response of birds to human recreational disturbances may depend on the nature or type of disturbance, as well as on the distance from the disturbance (Fernández-Juricic et al. 2001a; Pease et al. 2005; Ruddock and Whitfield 2007). For instance, contrary to the general belief that motorized nature based tourism activities cause greater disturbances to birds (Stolen 2003; Schlacher et al. 2013), non-motorized recreation such as hiking and biking that often involve close encounters with birds have been found to cause more severe negative effects on a wide range of bird species (Buckley 2004; Pease et al. 2005). In the case of species that are sensitive to human recreational disturbances, continuous exposure to such disturbances may ultimately lead to permanent avoidance of habitats and changes in regular behavioral patterns (Fernández-Juricic 2000; Steven et al. 2011).

One of the key issues that need to be addressed in bird conservation in PAs, subject to human visitation, is whether these recreational disturbances would decrease the probability of habitat occupancy by birds and, if so, what species are likely to be most affected. As recreational activities in PAs are frequently cited as one of the principal issues of concern in biodiversity conservation, a proper understanding of the relationship between human recreational disturbances and their impacts on birds is essential for effective conservation and recreational planning in PAs, particularly those subject to high visitor pressure. Furthermore, such knowledge would be highly valuable in designing and planning sound visitor management strategies, setting appropriate visitor policies/guidelines, as well as setting buffer zones to minimize potential recreational disturbances on birds (Rodgers and Schwikert 2002; Blumstein et al. 2003; Fernández-Juricic et al. 2004). Despite the importance of understanding possible impacts of human disturbances on avifauna, scientific evidence to assess the extent of this impact is limited in the literature, especially for birds in tropical regions (Steven et al. 2011). In order to bridge this information gap, this study investigated the effects of human recreational disturbances on the distribution and abundance of birds along a highly visited nature trail in a tropical lowland rainforest in Sri Lanka. How recreational disturbances occurring at this nature trail affect birds at different distances away from the trail and different vertical strata of the forest, were specifically examined.

Over the 11-month study period, a total of 5167 individual birds belonging to 45 species were encountered at the 27 sampling stations, of which 43 species were resident birds, including 19 endemic species and 2 migrant species (Appendix 1). The Orange-billed Babbler (Turdoides rufescens), the Ashy-headed Laughing-thrush (Garrulax cinereifrons), the Yellow-browed Bulbul (Pycnonotus luteolus) and the Dark-fronted Babbler (Rhopocichla atriceps) were among the most abundant species recorded. A total of 307 point counts were conducted at the 27 sampling stations and an average of 16.83 (SE ± 1.17) number of birds were recorded during a point count with a range of 0–145 birds. A total of 3267 visitors utilized the studied segment of this nature trail while the bird census was ongoing.

Association between disturbance categories and abundance of birds

In general, birds were more abundant in habitat edges near this nature trail (Fig. 2). To test whether the abundance of birds would statistically vary under different intensities of recreational disturbances at each distance level, one-way ANOVA tests were employed. The abundance of birds varied significantly under different intensities of recreational disturbances at each distance level at p < 0.05. Post-hoc comparisons further suggest that the abundance of birds under less recreational disturbances (NRD and LRD) is significantly higher than bird abundance under greater levels of disturbances (MRD and HRD) at the 0 m distance level (Table 2).

Distance from trail (m)	Mean number of birds				One-way ANOVA		Pearson’s correlation
	NRD	LRD	MRD	HRD	F	p	r	p
0	1.53a	1.17a	0.70b	0.28b	12.255	0.001*	−0.134	0.001*
75	0.54a	0.81	0.80	0.92b	3.066	0.027*	0.064	0.006*
150	0.36a	0.53b	0.67b	0.75b	6.848	0.001*	0.104	0.001*

Items with different superscripts (lowercase letters) indicate significant difference of means according to Games-Howell post hoc tests. Items without superscripts do not significantly differ from ones with superscripts

* Statistical significance at α = 0.05 level

Pearson’s correlation tests revealed different types of significant relationships between abundance of birds and disturbance categories at each distance level. A significant negative correlation was observed between the abundance of birds and disturbance category at 0 m distance, while significant positive correlations between the same variables were evident in point count stations located 75 and 150 m away from the trail (Table 2). Thus, the abundance of birds decreased with human disturbance at 0 m distance, while bird abundance increased at 75 and 150 m distance levels with increasing human disturbances occurring at the trail.

The two-way ANOVA revealed no statistically significant interaction between the effects of disturbance level and vertical strata on bird abundance at 0 m distance (F = 0.905, p = 0.521). Bird abundance differed significantly with disturbance (F = 4.617, p < 0.001), but not with vertical strata of the forest (F = 0.245, p = 0.865). Statistically non-significant results for the effects of disturbance level and vertical strata on bird abundance were further evident at the 75 and 150 m distance levels.

Significant negative Pearson’s correlations were observed between disturbance level and abundance of birds occupying the ground and understory (r = −0.230, p < 0.001) and the sub-canopy (r = −0.212, p < 0.001) vertical strata of the forest at 0 m distance. At 75 and 150 m distances away from the nature trail, the correlation between the two variables was insignificant except in the sub-canopy at the 75 m distance level (Table 3). Hence, the abundance of birds occupying ground and understory, as well as the sub-canopy layers at 0 m distance decreased with human disturbances, while bird abundance increased in the sub-canopy layer at the 75 m distance level with increasing disturbances at the nature trail.

Distance from trail (m)	Strata	Mean number of birds				Pearson’s correlation
		NRD	LRD	MRD	HRD	r	p
0	Ground and understory	2.77	2.20	1.23	0.16	−0.230	0.001*
	Sub-canopy	2.92	2.28	0.97	0.41	−0.212	0.001*
	Canopy	1.58	1.88	1.22	1.13	−0.116	0.141
	Above-canopy	1.41	1.54	0.80	1.10	−0.150	0.233
75	Ground and understory	1.52	1.25	1.00	3.00	0.202	0.218
	Sub-canopy	1.86	1.76	1.83	3.83	0.263	0.019*
	Canopy	4.60	1.50	3.50	1.99	−0.289	0.451
	Above-canopy	2.00	2.67	3.00	2.00	0.186	0.474
150	Ground and understory	3.29	4.33	4.83	3.50	0.087	0.492
	Sub-canopy	3.29	4.22	4.05	1.36	0.004	0.958
	Canopy	2.33	2.94	1.67	1.00	−0.062	0.733
	Above-canopy	1.64	2.22	0.67	1.50	−0.114	0.563

* Statistical significance at α = 0.05 level

The impact of human presence and disturbances on birds has been well documented in the literature. As interpreted by Fernández-Juricic et al. (2001a), birds in general perceive human presence as a predation risk and tend to flee or show avoidance behavior. In the context of nature-based tourism, earlier studies have reported low abundance and species richness of birds under higher pedestrian or vehicle traffic in wildlife refuges (Klein et al. 1995; Fernández-Juricic 2000; Bautista et al. 2004; Burger et al. 2004; Marcum 2005). However, these relationships have been observed for avifauna in temperate regions and mostly for aquatic birds (Steven et al. 2011). Focusing on the avifaunal community in this tropical lowland rainforest in Sri Lanka, findings of this study further support the negative relationships found between the abundance of birds and increasing human recreational disturbances, elaborated by previous research.

Our results further suggest that not all tropical bird species are equally affected by human recreational disturbances. As in the case of temperate birds (Marcum 2005; Gill 2007), certain tropical bird species are capable of tolerating greater degrees of human recreational disturbances. The sensitivity of individual bird species to visitor recreational disturbances seems to vary with the stratum/layer of the rain forest usually occupied by bird species. Ashy-headed Laughing-thrush, Dark-fronted Babbler, Spot-winged Thrush and Tickell’s Blue Flycatcher, found to be particularly sensitive to recreational disturbances, are all forest birds that usually occupy the understory and edges of jungle trails (Kotagama and Goodale 2004; Goodale and Kotagama 2005; Harrison and Worfolk 2011; Warakagoda et al. 2012). As the intensity of human recreational disturbances increased, their presence near the trail declined significantly. This suggests that birds generally occupying the ground and understory are likely to be more affected by visitors. The response of birds to human recreational disturbances can vary by the distance to the disturbances (Fernández-Juricic et al. 2001a, b; Borgmann 2010). In the studied segment of our nature trail, only hiking is allowed and the distance between recreationalists using the nature trail and birds occupying the lower strata of the forest is smaller. Past studies have also shown that forms of recreation, such as hiking, can cause significant negative effects on a wide range of bird species (Buckley 2004; Pease et al. 2005).

Black-naped Monarch, Brown-breasted Flycatcher, Brown-headed Barbet, Greater Flameback, Malabar Trogon, Orange-billed Babbler, Sri Lanka Blue Magpie, Sri Lanka Scimitar Babbler and Yellow-browed Bulbul commonly occupy the sub-canopy layer of the forest. Out of nine sub-canopy occupying bird species, Black-naped Monarch, Brown-headed Barbet and Sri Lanka Blue Magpie showed higher tolerance to visitor recreational disturbances. The Brown-headed Barbet is not exclusively a forest bird and a common resident in a variety of habitats, including landscapes modified anthropologically (Harrison and Worfolk 2011). Their greater adaptability to modified habitats may explain why this species is not substantially avoiding edges of our trail under higher intensities of recreational disturbances. Although a forest bird, the Sri Lanka Blue Magpie did not show noticeable signs of avoidance behavior under human presence. Instead, they seem to be attracted towards small to medium sized visitor groups. This was evident by the high number of Sri Lanka Blue Magpies being recorded under low and moderate levels of recreational disturbances and their numbers showing a positive correlation with disturbance level, although the relationship was not statistically significant. This suggests a possible habituation of the Sri Lanka Blue Magpie population ranging around the Kudawa nature trail to low and moderate levels of recreational disturbances or human presence. In fact, during our field studies, it was often observed that a group of Sri Lanka Blue Magpies perching near the trail in anticipation of food, when visitor groups were present. Similar behavioral observations were made on ground occupying Sri Lanka Junglefowl. Visitors feeding blue magpies and junglefowls were a common observation during field studies. Such visitor behavior along with exposure to recurring recreational disturbances can alter the normal behavior of birds and induce habituation to human presence (Marcum 2005; Peters and Otis 2006; Baudains and Lloyd 2007; Smith-Castro and Rodewald 2010).

In general, recreational disturbances had less effect on birds occupying canopy and emergent layers. Layard’s Parakeet and Sri Lanka Crested Drongo commonly occupy the canopy or the upper parts of the sub-canopy (Kotagama and Goodale 2004; Goodale and Kotagama 2005; Harrison and Worfolk 2011; Warakagoda et al. 2012). As indicated by the results of our ANOVAs in Appendix 2, their abundance was found to be independent from the intensity of recreational disturbances at various distances from the trail. Among the bird species occupying the emergent layer of the forest, the Sri Lanka Myna—the only species with sufficient data for analysis in this study, also showed no statistically significant variation in its abundance under different intensities of recreational disturbances at various distances from the trail. Since these species commonly forage and occupy the canopy above 25 m from the ground, they may be less inclined to perceive human presence as a predation risk (Fernández-Juricic et al. 2001b) and thus less concerned about leaving the edges of this nature trail. However, despite being canopy occupants, the abundance of the Red-faced Malkoha and Scarlet Minivet was negatively correlated with the intensity of recreational disturbances at the trail, indicating their comparatively smaller tolerance to human presence.

The abundance of Ashy-headed Laughing-thrush, Brown-breasted Flycatcher, Greater Flameback, Dark-fronted Babbler, Malabar Trogon, Orange-billed Babbler, Spot-Winged Thrush, Sri Lanka Scimitar Babbler and Yellow-browed Bulbul was higher along the jungle trail when no humans were present. These species generally prefer relatively open spaces inside the forest (Harrison and Worfolk 2011; Warakagoda et al. 2012). Under moderate and high recreational disturbances, the abundance of these species increased at the 75 m distance level from the trail. These fluctuations in abundance provide possible evidence for differing fleeing distances of bird species. The Ashy-headed Laughing-thrush, Dark-fronted Babbler, Orange-billed Babbler and Sri Lanka Scimitar Babbler are characteristically weak flyers (Siriwardhane 2007; Harrison and Worfolk 2011; Warakagoda et al, 2012) and do not flush far from the jungle trail. A statistically significant dependence of abundance on the intensity of recreational disturbances was observed for Malabar Trogons, indicating that they flush beyond 50 m under increasing visitor disturbances. However, other species such as the Brown-breasted Flycatcher, Greater Flameback and Yellow-browed Bulbul with good flight abilities did not seem to flush beyond 50 m from the trail. Hence there is only weak evidence to support the hypothesis that strong flyers flush deeper into the forest.

Territory size and territoriality may be important factors that determine how far birds would move away from a disturbance. Species, defending territories, are more likely to have reduced flight initiation distances and are less likely to move out of their territories under disturbances, although such responses are not always universal (Stankowich and Blumstein 2005). The Spot-winged Thrush is a highly territorial bird that seldom abandons its territory under disturbances (Weerakoon 2007). Instead, such species rely on camouflage in the vegetation. The abundance of Tickell’s Blue Flycatcher also did not increase substantially under disturbances in the inner parts of the forest, indicating its territorial behavior (Rasmussen and Anderton 2012).

Another possible factor that can affect the response of different bird species to recreational disturbance in this forest is the predominance of mixed-species bird flocks. Many bird species recorded in this study, such as Orange-billed Babbler, Ashy-headed Laughing-thrush, Dark-fronted Babbler, Malabar Trogon, Red-faced Malkoha, Scarlet Minivet, and Yellow-browed Bulbul are known to participate quite regularly in mixed-species bird flocks (Kotagama and Goodale 2004; Goodale and Kotagama 2005). It was observed that the abundance of these species including the Orange-billed Babbler, the nuclear species of the flock system, were negatively correlated with increasing intensities of recreational disturbances. As such, mixed-species bird flocks may be negatively affected by visitor groups and under such circumstances, a flock can avoid habitat edges and travel quite quickly to the interior of the forest. The increase in abundance of the Malabar Trogon and Black-naped Monarch at 75 m level with the intensity of recreational disturbances may be explained by this phenomenon. Although a bird with a small territory, the abundance of the Dark-fronted Babbler was positively correlated with intensity of recreational disturbance at the 75 m distance level. They are known to join mixed-species foraging bird flocks usually within their territory (Shermila and Wikramasinghe 2013). Moreover, other research suggest that flush distances of certain bird species can be further associated with habitat structure represented by features such as vegetation cover, shrub and tree height (Fernández-Juricic et al. 2001b).

Some limitations of the study should be acknowledged. First, the structure of the forest near this nature trail is somewhat open and disturbed and differs from the forest interior. As such, the ability to detect birds is comparatively higher near the trail than inside the forest. Although efforts were made during the study design to avoid significantly open areas near the trail, higher abundance of birds near the trail may still be affected by greater visibility. All the same, there were several edge-specialists among the bird species recorded. It is well documented that mixed-species bird flocks of the Sinharaja forest tend to use habitat edges such as cut-over areas near the trails quite heavily (Kotagama and Goodale 2004; Goodale and Kotagama 2005). Secondly, the bird activity is relatively high in the early morning, apparently a time of low visitor activity. In general, larger visitor groups were more frequent after 10:00 a.m. while smaller visitor groups including birdwatchers entered the reserve during the early hours of the day, i.e., between 6:00 and 8:00 a.m. The study design accounted for this factor by avoiding bird census for this period, yet the effect of this compounding variable on bird abundance cannot be completely ignored.

Also, it is worth studying the movements of individually marked birds to determine their actual distance of displacement, minimum approaching distance, habitats where they seek refuge when disturbed and how they habituate due to their regular contact with visitors. Such information will be vital in recreational planning and management to minimize the disturbances to avifauna.

Heavy use of nature trails for recreational purposes has affected the bird species that occur on the well-known Kudawa nature trail in the Sinharaja World Heritage Forest. Under high levels of disturbance, bird communities avoided edge habitats and flushed far into the forest (up to 150 m). Certain avian species seem to tolerate greater degrees of recreational disturbances. The sensitivity of individual bird species to visitor recreational disturbances vary with the stratum/layer of the rain forest usually occupied by these bird species. Effects of recreational disturbances were more profoundly felt by birds occupying understory and sub-canopy layers of the forest near the nature trail. Accordingly, the following species, i.e., Ashy-headed Laughing-thrush, Dark-fronted Babbler, Spot-Winged Thrush, Tickell’s Blue Flycatcher, Brown-breasted Flycatcher, Greater Flameback, Malabar Trogon, Orange-billed Babbler, Sri Lanka Scimitar Babbler and Yellow-browed Bulbul avoid habitat edges along the jungle trail under increased visitor activity. Bird species occupying the canopy and higher layers of the forest were more tolerant to recreational disturbances.