Wildlife responses to human disturbance may be detected at several levels, such as changes in sensory detection, physiology, behaviour, fitness, space use, and population growth rate (Tablado and Jenni 2017). Both comparative and experimental approaches have been used to assess individual behavioral, distributional, demographic, and population responses to human disturbance (Gill 2007, Kerbiriou et al. 2009). If animals respond behaviorally or physiologically to human disturbance, their fitness (reproductive output and survival as proxies) and habitat use may be compromised, even by single events (Bowles 1995, Knight and Gutzwiller 1995, Wingfield et al. 1997, Frid and Dill 2002, Buckley 2011 in Tablado and Jenni 2017). The decline of many species has been directly or indirectly linked to human disturbance (Reijnen et al. 1996, Brawn et al. 2001, Beebee and Griffiths 2005, Reed and Merenlender 2011). Indeed, human activities in an area can appear to be neutral or even benign in their effect on wildlife, but may ultimately cause populations to decline over time (Lowe et al. 2014).
Animals may perceive visitors as potential predators and respond to disturbance accordingly, whether from a noisy, low-flying helicopter or from a quiet wildlife photographer (Frid and Dill 2002). Many authors have investigated the responses of breeding birds to human disturbance, such as the energy costs of earlier flight initiation and vigilance (e.g., González et al. 2006, Poudel et al. 2015), changes in habitat use (e.g., Lafferty 2001, Fernández-Juricic et al. 2002, Markovchick-Nicholls et al. 2008, Lowe et al. 2014), reduced parental care (e.g., Burger 1994, Verhulst et al. 2001, Bautista et al. 2004, Yasué and Dearden 2006), and decreased reproductive success (Safina and Burger 1983, Bailly et al. 2016). Behavioral responses to human disturbance vary among species (Blumstein et al. 2005), with, e.g., group-living species more likely to suffer from injuries during panic behavior (Carney and Sydeman 1999).
Wildlife observers and photographers actively seek and approach wildlife, unlike other recreationists who mostly encounter wildlife accidentally (Speight 1973). This nonconsumptive recreation activity may effect birds because of their more frequent and longer duration (Boyle and Samson 1985). However, few studies have addressed the influence birdwatchers and photographers may exert on a species when it is the target of their concerted interest.
The Blue-crowned Laughingthrush Garrulax courtoisi, a group-living species, is listed as Critically Endangered (CR) by IUCN, with a total known population size of around 240 mature individuals (BirdLife International 2016). It is confined to an extremely small breeding range in Jiangxi Province, China, where its breeding sites are distributed in stands of broad-leaved trees beside a number of villages near the tributaries of the LeAn River. Disturbance from villagers’ daily activities cannot be avoided, but the birds appear to be accustomed to them. Each year, they arrive at the breeding sites in mid-late April, breed colonially and cooperatively without territory. Three or four eggs are laid in each clutch. Although resident in Wuyuan, however, they leave the breeding ground a few days after the young have fledged and wander throughout the nonbreeding season.
The species was treated as a subspecies of Yellow-throated Laughingthrush Garrulax galbanus for many years (see Collar 2006), but its sudden appearance in trade around 1990, with birds being acquired by several western institutions, led conservationists to note its distinctiveness (Long et al. 1994). However, the provenance of these traded birds was unclear, and indeed the whereabouts of any wild population was unknown until searches through the 1990s were finally rewarded with the ‘rediscovery’ of the species in 2000 in a small cluster of villages in the region of Wuyuan in Jiangxi Province (Hong et al. 2003). Since then, this rare and beautiful bird has attracted the attention of many birdwatchers and photographers from all over the world.
Of the Laughingthrush breeding sites, Shimen village is the best known to bird photographers because the large size (more than 50 breeding individuals each year) and stability (it can be found in the same area from April to July every year) of this subpopulation make the species easy to find and be photographed. During our studies, we observed many visitors pursuing birds from dawn to dusk to take photographs, frequently involving flashing lights and mechanical camera sounds. Birds in Shimen have been disturbed by visitors ever since the rediscovery of the species, and from our observations, the subpopulation over the site has suffered far longer and stronger disturbance from birdwatchers and photographers than those at the other sites. Consequently, aware that disturbance can induce changes in nest position (Morán-López et al. 2006, Chen et al. 2011) and that such changes might be disadvantageous to the species, we investigated the effects of visitors on nest-site selection of the Laughingthrush.
Wuyuan is known as “China’s most beautiful landscape,” with rich bird diversity (He et al. 2014), therefore the area attracts a large number of tourists, birdwatchers, and photographers every year. It is a part of the Huangshan Mountains, with 83% mountainous area and a 100–150 m average altitude. The villages were built along the main river, the LeAn River, which is a branch of the Raohe River, and its tributaries. Fengshui forests, mainly composed of broad-leaved trees, are the main breeding area of the Blue-crowned Laughingthrush in the villages. These forests are small in area and isolated from each other and other forests.
From 2012 to 2016 we conducted field investigations in nine breeding sites of the Blue-crowned Laughingthrush in Wuyuan, named Shimen (here after SM), Jinpan (JP), Hexi (HX), Taibai (TB), Haikou (HA), Hokou (HO), Caomen (CM), Zhongyun (ZY), and Linhe (LH). All of them are villages bordering rivers with adjacent broad-leaved woodland or stands of broad-leaved old trees, but the sizes of the breeding subpopulations they host vary considerably. SM and JP are only a few hundred meters apart, on opposite sides of the same river, and they host the same flock of Laughingthrushes that gather there when the birds arrive from their (as yet unknown) wintering area; however, when breeding begins, the flock separates into two breeding subpopulations; we therefore treated them as separate breeding sites.
Almost all photographs of the Blue-crowned Laughingthrush published online or in print were taken in SM. We counted the online posts of photographs of this species in Birdnet (http://www.birdnet.cn/portal.php), the main web site for bird photo sharing in China, as a measure of the degree of disturbance from photographers in SM. The SM site was the best known breeding site for the Laughingthrush, and it was also the only site with convenient room and board accommodations for bird visitors before 2015. However, photographers did not indicate where their photos were taken when they uploaded these pictures so we cannot be sure that all the pictures were taken in SM. Even if some of them were taken in the other sites, the ratio was too small to largely influence the overall trend of the amount of Laughingthrush’s pictures taken in SM.
We searched villages with suitable habitats and recorded the number of nests in each breeding site since 2012 (Table 1). We also measured the nest height above ground (NHAG), tree height (TH), and diameter at breast height (DBH) of the trees used for breeding, and compared clutch size and brood size in each nest in SM with the other sites for comparison. We chose an area without Laughingthrush nests in the same forest as a control area without breeding nest of the Laughingthrush in SM, recorded the species, and measured the TH value of all trees in this area for comparison with the nest area. Because the NHAG value may increase with tree height, which varies with tree species and age, we excluded the data from bamboo (n = 4), plum trees (n = 1), pear trees (n = 2), and osmanthus (n = 13) when comparing the NHAG value because these species cannot reach as high as the other trees.
Because all Laughingthrush breeding sites were in or near villages, they all fell within an area encompassing the villagers’ daily activities. We therefore tried to assess this basic level of villager disturbance by one parameter, DB, i.e., nest distance to human buildings (house, road, and bridge).
Because nest inspections by researchers may affect incubation and food-provisioning schedules, we climbed trees to check the eggs only once, and in as brief a time as possible (a few minutes) when the parents were both absent. Though we found many nests, we were only able to examine the clutch size of nine nests directly because they were built at the end of thin branches, quite high to observe and climb. However, because the nest structure stretched somewhat after the eggs hatched and the nest bottom was thin and transparent, and the nestlings would stick their heads out the nest when they beg for food, we were able to count nestlings by monocular telescope. Although most of the nest bottom became thin enough to see the nestlings, it still required a long observation, thus counting was easier when the adults fed the young.
Nine breeding sites, five of them previously undisclosed, have been recorded since 2012 (see Birdlife international 2016). Because SM was almost the only site known and disturbed by bird photographers before 2015, we used data from the other eight sites for comparison, to assess the impact of disturbance on the Laughingthrush.
We checked clutch and brood sizes of the Laughingthrush in SM and other sites. However, nests checked for eggs were not always the same as those checked for nestlings. So we assumed that no individual differences occurred in hatching ability, and the breeding success ratio was calculated as the ratio of the number of nestlings and clutch size in SM.
All statistical tests were performed using SPSS 17.0. The statistical significance level was set at p < 0.05. ANOVA analysis was done to check the differences of DB, DBH, NHAG, clutch size, and brood size values between SM and other sites. T-test statistic, degrees of freedom (df) and P-values from these models are presented. Additionally, means are presented as back-transformed parameter estimates, with the upper and lower 95% confidence limits. GLM methods and correlation tests were undertaken to determine the relationship between these parameters.
From 2012 to 2016, 169 nests were found in the nine breeding sites but only 144 were used because of accessibility. SM was the largest subpopulation with most breeding pairs. The other subpopulations held fewer breeding individuals and were less stable than SM, and in some years some sites were entirely unoccupied (Table 1).
In the years following its rediscovery, the Blue-crowned Laughingthrush became increasingly well known. Photographs of it appeared on Birdnet from 2007 onward, and rose dramatically after 2010 (Fig. 1), reflecting a major increase in the number of photographers and the levels of disturbance they created.
Nests in SM averaged 119.2 ± 7.1 m from buildings, a much father distance than at the other sites where they averaged only 13.4 ± 2.9 m from buildings (F1,93 = 104.2, p < 0.001).
All nests were built in broad-leaved (but not fruit) trees in SM, while bamboo, fruit trees, and conifers were also used for nesting at other sites (including JP, across the river from SM). Hackberry Celtis sinensis, Chinese ash Pterocarya stenoptera, and Chinese sweet gum Liquidambar formosana were selected most in SM (Fig. 2). Camphor trees were used the most for nesting at all other sites (Fig. 2). Nest trees in SM were similar in height but higher in crown density compared with nest trees in all other sites.
Tree height was similar in all sites (Fig. 3; F2,129 = 0.0, p = 0.934). However, DBH was smaller in SM (43.7 ± 2.2 cm) than at the other sites (98.7 ± 7.3 cm; F1,129 = 80.9, p < 0.001).
In SM, the height of nesting trees was higher (19.1 ± 0.5 m, n = 144) than the height of non-nesting trees (F1,224 = 12.4, p = 0.001). Also, in SM the tree species chosen for nesting tended to be the highest species there (Fig. 3).
Nest height above ground (NHAG) was higher at SM (15.9 ± 0.5 m; n = 59) than at other sites (10.8 ± 0.8; n = 30; excluding data from bamboo and fruit trees: n = 7; F = 27.8, p < 0.001; Fig. 4). However, at SM, NHAG differed between years, being lower in 2004 (10.9 ± 2.5 m) than in other years (Fig. 4).
NHAG increased with TH in both SM and other sites, but decreased after it reached the highest value in the other sites, not in SM. Besides this, the rise range in SM was larger than the other sites, with no obvious fall after the peak. Birds in SM seemed still to nest higher compared with other sites, even allowing for tree height (Fig. 5).
TH of nesting trees in SM from 2012 to 2016 showed no significant differences (see Fig. 5; F4,77 = 0.5, p = 0.720); nor did NHAG (F4,77 = 0.7, p = 0.568). However, ratio of NHAG and TH seemed to differ between years (F4,77 = 3.2, p = 0.018; Table 2; Fig. 4). This means birds at SM seemed to adjusted their nest position for some reason in different years.
Wildlife tends to select more concealing habitat to counteract the influence of disturbance (Chen et al. 2011). The greater DB values in SM suggest that it is visitors rather than villagers that are the source of disturbance. The tree species selected for nesting at SM possess more crown density than at other sites, indicating a greater requirement for seclusion in birds at SM. It is generally known that DBH increases with tree age; the higher DBH value at other sites reflects the fact that the nest trees are older and therefore taller. In fact, nest trees at other sites were always isolated or more distant from each other compared with SM. Although the number of photographs posted online reveal that disturbance increased dramatically from 2012 to 2015, nest height showed no significant differences in these four years (F3,56 = 1.0, p = 0.420), and we infer that the Laughingthrushes had already increased the height of their nest positions as a response to visitors disturbance before our study began. Nevertheless, the ratio of TH and NHAG rose generally from 2012 to 2016, possibly responding to the enhanced disturbance pressure by photographers. However, the difference might be due to other factors such as competition for nest sites, which would weaken the effect of disturbance on nesting tree choice and then nest height.
Laughingthrushes in SM now nest higher (and previously at SM itself) and select tree species offering more cover than at other sites, and this behavior appears to be correlated with targeted disturbance by birdwatchers and photographers. Nest outcomes and reproductive success have been related to nest height above ground and concealment in many studies (Mitrus and Soćko 2008, Coppedge 2010, Endo 2012). Hatching rate of the endangered Spanish Imperial Eagle Aquila adalberti was affected negatively by the frequency of human activities around nest sites. Hatching success of the Blue-crowned Laughingthrush in 2004 (although n = 6) was as high as 94.7% (Liao et al. 2007), much higher than SM now. Social species are more flighty than noncooperative breeders when humans approach (Blumstein 2006). Blue-crowned Laughingthrushes are cooperative breeders and they monitor both conspecifics and predators, which make them more responsive to human disturbance.
Predation is the most important factor influencing breeding success in natural conditions (Nilsson 1984, Martin 1995, Wesolowski and Tomialojc 2005). Colonially nesting birds are more vulnerable to disturbance because breeding individuals concentrate in a small area (Buckley and Buckley 1976, Manuwal 1978). Eggs or nestlings are defenseless when adults are absent; this greater exposure to predators may increase mortality. Chinese Goshawk Accipiter soloensis, Besra A. virgatus, Japanese Sparrowhawk Accipiter gularis, and Black Baza Aviceda leuphotes (but in recent years no corvids) occur in the breeding areas and could more easily prey upon the eggs, nestlings, and even adult Laughingthrushes when high nests are more exposed. As the largest breeding group, SM should contribute most to overall population growth. Disturbance might therefore be constraining breeding success, leaving the total population size unchanged at about 200–240 individuals since the rediscovery of this species in 2000.
Whether animals under pressure shift their habitats depends on the relative costs and benefits of moving elsewhere (Frid and Dill 2002). Breeding pairs moved to JP to nest in 2013 and 2015 (see Table 1), and this might reflect high disturbance levels for the breeding subpopulation in SM.
Only a few bird photographers knew of the other breeding sites in the past. However, they still preferred SM because of the large number of birds and convenient accommodation in the village. However, some people began to take pictures in JP in 2015, and some photographers shifted to CM in 2016 because they were rejected and forbidden by the administrative department in Wuyuan to take photos in SM. Excessive pursuit and disturbance of these birds during the breeding season may exacerbate their endangered status. If the breeding site at SM and other potential breeding areas are developed as new tourist venues, further disturbance will result. Unfortunately, the Blue-crowned Laughingthrush is still not classified as a protected animal in China, so there is no legal basis for regulating the behavior of photographers and birdwatchers in Wuyuan. Because the species ranges over a wide area in the villages it is very difficult to provide practical measures that could protect it from disturbance, and at present the only solution is to improve the photographers’ awareness of the problem and appeal to their self-restraint.
We are grateful to Mr F.Q. He and Y.H. Hong who supplied information we needed, and to Mr N. Collar and P.R. Henry who gave us a lot of help on the written modifications. Thanks to N. Collar for insightful suggestions. This research was funded by the National Natural Science Foundation of China (No. 31360521), National Science and technology support project (No. 2012BAC11B02), Science and technology project of Jiangxi Province (20132BAB214013, 2013BBG7004), and Project of Jiangxi Provincial Education Department (GJJ13277).
Bailly, J., R. Scheifler, S. Berthe , V.-A. Clément-Demange, M. Leblond, B. Pasteur, and B. Faivre. 2016. From eggs to fledging: negative impact of urban habitat on reproduction in two tit species. Journal of Ornithology 157:377–392. http://dx.doi.org/10.1007/s10336-015-1293-3
Bautista, L. M., J. T. García, R. G. Calmaestra, C. Palacín, C. A. Martín, M. B. Morales, R. Bonal, and J. Viñuela. 2004. Effect of weekend road traffic on the use of space by raptors. Conservation Biology 18(3):726-732. http://dx.doi.org/10.1111/j.1523-1739.2004.00499.x
Beebee, T. J. C., and R. A. Griffith. 2005. The amphibian decline crisis: a watershed for conservation biology? Biological Conservation 125:271-285. http://dx.doi.org/10.1016/j.biocon.2005.04.009
BirdLife International. 2016. Garrulax courtoisi. IUCN Red List of Threatened Species, Cambridge, UK. [online] URL: http://www.iucnredlist.org/details/22732350/0
Blumstein, D. T. 2006. The multipredator hypothesis and the evolutionary presistence of antipredator behavior. Ethology 112(3):209-217. https://doi.org/10.1111/j.1439-0310.2006.01209.x
Blumstein, D. T., E. Fernández-Juricic, P. A. Zollner, and S. C. Garity. 2005. Inter-specific variation in avian responses to human disturbance. Journal of Applied Ecology 42:943-953. http://dx.doi.org/10.1111/j.1365-2664.2005.01071.x
Bowles, A. E. 1995. Responses of wildlife to noise. Pages 109-156 in R. L. Knight and K. Gutzwiller, editors. Wildlife and recreationists: coexistence through management and research. Island, Washington, D.C., USA.
Boyle, S. A., and F. B. Samson. 1985. Effects of noconsumptive recreation on wildlife: a review. Wildlife Society Bulletin 13(2):110-116.
Brawn, J. D., S. K. Robinson, and F. R. Thompson III. 2001. The role of disturbance in the ecology and conservation of birds. Annual Review of Ecology, Evolution, & Systematics 32:251-276. http://dx.doi.org/10.1146/annurev.ecolsys.32.081501.114031
Buckley, P. A., and F. G. Buckley. 1976. Guidelines for protection and management of colonially nesting waterbirds. North Atlantic Regional Office, National Park Service, Boston, Massachusetts, USA.
Buckley, R. 2011. Tourism and environment. Annual Review of Environment and Resources 36:397-416. http://dx.doi.org/10.1146/annurev-environ-041210-132637
Burger, J. 1994. The effect of human disturbance on foraging behavior and habitat use in piping plover (Charadrius melodus). Estuaries 17(3):695-701. http://dx.doi.org/10.2307/1352418
Carney, K. M., and W. J. Sydeman. 1999. A review of human disturbance effects on nesting colonial waterbirds. Waterbirds 22:68-79. http://dx.doi.org/10.2307/1521995
Chen, J.-N., N.-F. Liu, C. Yan, and B. An. 2011. Plasticity in nest selection of Black Redstart (Phoenicurus ochruros): a response to human disturbance. Journal of Ornithology 152(3):603-608. http://dx.doi.org/10.1007/s10336-010-0622-9
Collar, N. J. 2006. A partial revision of the Asian babblers (Timaliidae). Forktail 22:85-112.
Coppedge, B. R. 2010. Red-winged blackbird nest success in Oklahoma Tallgrass Prairie. Proceedings of the Oklahoma Academy of Science 90:61-68.
Endo, S. 2012. Nest-site characteristics affect probability of nest predation of Bull-headed Shrikes. Wilson Journal of Ornithology 124(3):513-517. http://dx.doi.org/10.1676/11-164.1
Fernández-Juricic, E., M. D. Jimenez, and E. Lucas. 2002. Factors affecting intra- and inter-specific variations in the difference between alert distances and flight distances for birds in forested habitats. Canadian Journal of Zoology 80:1212-1220. http://dx.doi.org/10.1139/z02-104
Frid, A., and L. M. Dill. 2002. Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology 6(1):11. http://dx.doi.org/10.5751/es-00404-060111
Gill, J. A. 2007. Approaches to measuring the effects of human disturbance on birds. Ibis 149(S1):9-14. http://dx.doi.org/10.1111/j.1474-919x.2007.00642.x
González, L. M., B. E. Arroyo, A. Margalida, R. Śanchez, and J. Oria. 2006. Effect of human activities on the behaviour of breeding Spanish imperial eagles (Aquila adalberti): management implications for the conservation of a threatened species. Animal Conservation 9(1):85-93. http://dx.doi.org/10.1111/j.1469-1795.2005.00016.x
He, F. Q., J. S. Lin, Y. Y. Wang, G. F. Wang, Y. H. Hong, P. J. Zheng, C. Wen, Z. Lin, and Q. H. Shi. 2014. Bird records from Wuyuan, NE Jiangxi of SE China. Chinese Journal of Zoology 49(2):170-184. [Translated from the Chinese.]
Hong, Y. H., F. Q. He, R. Wirth, D. Melville, P. J. Zheng, X. Z. Wang, G. F. Wang, and Z. H. Liu. 2003. Little-known Oriental bird: Courtois’s Laughingthrush Garrulax galbanus courtoisi. Oriental Bird Club Bull 38:35-40.
Kerbiriou, C., I. Le Viol, A. Robert, E. Porcher, F. Gourmelon, and R. Julliard. 2009. Tourism in protected areas can threaten wild populations: from individual response to population viability of the chough Pyrrhocorax pyrrhocorax. Journal of Applied Ecology 46(3):657-665. http://dx.doi.org/10.1111/j.1365-2664.2009.01646.x
Knight, R. L., and D. N. Cole. 1995. Wildlife responses to recreationists. Pages 51-69 in R. L. Knight and K. Gutzwiller, editors. Wildlife and recreationists: coexistence through management and research. Island, Washington, D.C., USA.
Knight, R. L., and K. J. Gutzwiller, editors. 1995. Wildlife and recreationists: coexistence through management and research. Island, Washington, D.C., USA.
Lafferty, K. D. 2001. Birds at a southern California beach: seasonality, habitat use and disturbance by human activity. Biodiversity & Conservation 10(11):1949-1962. http://dx.doi.org/10.1023/A:1013195504810
Liao, W. M., Y. H. Hong, S. B. Yu, X. Z. Ouyang, and G. X. He. 2007. A study on the propagation habitat of Garrulax galbanus courtoisi and the relationship of the birds with village forests in Wuyuan, Jiangxi Province. Acta Agriculture Universitatis Jiangxiensis 29(5):837-841. [Translated from the Chinese.]
Long, A., M. Crosby, and T. Inskipp. 1994. A review of the taxonomic status of the Yellow-throated Laughingthrush Garrulax galbanus. Oriental Bird Club Bull 19:41-48.
Lowe, A., A. C. Rogers, and L. Durrant. 2014. Effect of human disturbance on long-term habitat use and breeding success of the European Nightjar, Caprimulgus europaeus. Avian Conservation & Ecology 9(2):6. http://dx.doi.org/10.5751/ACE-00690-090206
Manuwal, D. 1978. Effect of man on marine birds: a review. Pages 140–160 in C. M. Kirkpatrick, editor. Wildlife and people: Proceedings of the John S. Wright Forestry Conference. Department of Forestry and Natural Resources and Cooperative Extension Services, Purdue University, Lafayette, Indiana, USA.
Markovchick-Nicholls, L., H. M. Regan, D. H. Deutschman, A. Widyanata, B. Martin, L. Noreke, and T. A. Hunt. 2008. Relationships between human disturbance and wildlife land use in urban habitat fragments. Conservation Biology 22(1):99-109. http://dx.doi.org/10.1111/j.1523-1739.2007.00846.x
Martin, T. E. 1995. Avian life history evolution in relation to nest sites, nest predation, and food. Ecological Monographs 65:101-127 http://dx.doi.org/10.2307/2937160
Mitrus, C., and B. Soćko. 2008. Breeding success and nest-site characteristics of Red-breasted Flycatchers Ficedula parva in a primeval forest. Bird Study 55(3):203-208. http://dx.doi.org/10.1080/00063650809461523
Morán-López, R., J. M. Sánchez Guzmán, E. Costillo Borrego, and A. Villegas Sánchez. 2006. Nest-site selection of endangered Cinereous Vulture (Aegypius monachus) populations affected by anthropogenic disturbance: present and future conservation implications. Animal Conservation 9(1):29-37. http://dx.doi.org/10.1111/j.1469-1795.2005.00003.x
Nilsson, S. G. 1984. The evolution of nest-site selection among hole nesting birds: the importance of nest predation and competition. Ornis Scandinavica 15:167-175. http://dx.doi.org/10.2307/3675958
Poudel, B. S., P. G. Spooner, and A. Matthews. 2015. Pastoralist disturbance effects on Himalayan marmot foraging and vigilance activity. Ecology Research 31:1-12.
Reed, S. E., and A. M. Merenlender. 2011. Effects of management of domestic dogs and recreation on carnivores in protected areas in northern California. Conservation Biology 25:504-513. http://dx.doi.org/10.1111/j.1523-1739.2010.01641.x
Reijnen, R., R. Foppen, and H. Meeuwsen. 1996. The effects of traffic on the density of breeding birds in Dutch agricultural grasslands. Biology Conservation 75:255-260. http://dx.doi.org/10.1016/0006-3207(95)00074-7
Safina, C., and J. Burger. 1983. Effects of human disturbance on reproductive success in the Black Skimmer. Condor 85(2):164-171. http://dx.doi.org/10.2307/1367250
Speight, M. C. D. 1973. Outdoor recreation and its ecological effects: a bibliography and review (Discussion Papers in Conservation 4). University College London, London, UK.
Tablado, Z., and L. Jenni. 2017. Determinants of uncertainty in wildlife responses to human disturbance. Biological Reviews 92(1):216-233. http://dx.doi.org/10.1111/brv.12224
Verhulst, S., K. Oosterbeek, and B. J. Ens. 2001. Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers. Biology Conservation 101(3): 375-380. http://dx.doi.org/10.1016/s0006-3207(01)00084-2
Wesolowski, T., and L. Tomialojc. 2005. Nest sites, nest depredation, and productivity of avian broods in a primeval temperate forest: do the generalisations hold? Journal of Avian Biology 36(5):361-367. http://dx.doi.org/10.1111/j.0908-8857.2005.03570.x
Wingfield, J. C., K. Hunt, C. Breuner, K. Dunlap, G. S. Fowler, L. Freed, and J. Lepson. 1997. Environmental stress, field endocrinology, and conservation biology. Pages 95-131 in J. R. Clemmons and R. Buchholz, editors. Behavioral approaches to conservation in the wild. Cambridge University Press, Cambridge, UK.
Yasué, M., and P. Dearden. 2006. The effects of heat stress, predation risk and parental investment on Malaysian Plover nest return times following a human disturbance. Biology Conservation 132:472-480. http://dx.doi.org/10.1016/j.biocon.2006.04.038