Global Ecology and Conservation 21 (2020) e00873

Contents lists available at ScienceDirect

Global Ecology and Conservation

journal homepage: http://www.elsevier.com/locate/gecco

Original Research Article

Behavioral responses of black-headed gulls (Chroicocephalus

ridibundus) to artificial provisioning in China
Changzhang Feng, Wei Liang*
Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou 571158,
China

a r t i c l e i n f o a b s t r a c t

Article history: Feeding birds is a widespread and popular activity that affects almost all aspects of bird
Received 3 November 2019 ecology. However, few studies are concerned about the impacts of human provisioning on
Received in revised form 5 December 2019 bird behavior. In this study, we compared the foraging distance (FD) and flight initiation
Accepted 5 December 2019
distance (FID) of the black-headed gull (Chroicocephalus ridibundus), a bird that is widely
distributed in urban and rural areas in Kunming, China, under different artificial provi-
Keywords:
sioning intensities. We also conducted a quantitative analysis of the relationship between
Artificial provisioning
artificial provisioning and behavioral changes in these birds. Our results showed that both
Domestication
Birds
the FD and FID of black-headed gulls in urban regions are significantly shorter than those
Flight initiation distance in rural populations. Moreover, urban black-headed gulls exhibited a series of signs of
Migration domestication, such as actively approaching humans to beg for food and foraging when
called or fed by humans, besides a reduction in FID. This suggests that provisioning by
humans has caused black-headed gulls to be less fearful of humans and has reduced their
defenses against predators. We recommend that bird feeding should be carefully and
properly executed, and that the long-term effects of artificial provisioning on wild birds
require further monitoring.
© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC
BY license (http://creativecommons.org/licenses/by/4.0/).

1. Introduction

As the range of activities performed by humans expands, the effects of human disturbance on animals have become one of
the hot topics in ecology and conservation biology (Sih et al., 2011). Artificial provisioning, which refers to providing wild
animals with food, is one of such disturbances, because the supply of food to animal populations is often perturbed through
human activities (Robb et al., 2008; Plummer et al., 2013). A recent study by Díaz Lopez (2019) showed that human activities
can be a source of reliable food resources for species with a high degree of behavioral plasticity. However, this has also been
shown to simultaneously change migratory patterns and social interactions of the common bottlenose dolphin (Tursiops
truncatus) (Díaz Lopez (2019)).
Artificial provisioning for birds has a long history. As early as 1910, bird feeding was regarded as a national recreational
activity in the United Kingdom (UK) (Jones, 2011) and 43% of American families regularly fed birds (Martinson and Flashpoler,
2003). Bird feeding has become an important opportunity for humans to have a close contact with nature, as the scattering of
food attracts birds, enabling close observation and identification. Every year, millions of families around the world provide

* Corresponding author.
E-mail addresses: fengcz@hainnu.edu.cn (C. Feng), liangwei@hainnu.edu.cn (W. Liang).

https://doi.org/10.1016/j.gecco.2019.e00873
2351-9894/© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.
0/).
2 C. Feng, W. Liang / Global Ecology and Conservation 21 (2020) e00873

large quantities of food for wild birds (Orros and Fellowes, 2015) and this affects various aspects of the birds’ biology (Robb
et al., 2008; Jones, 2018). Feeding may affect the abundance and distribution of birds. For instance, part of the reason why the
red kite (Milvus milvus) could be reintroduced in the UK was because residents in southern UK provided these birds with meat
in supplementary feeding sites (Orros and Fellowes, 2015). During winter, food provided by humans can increase the over-
winter survival rate in birds (Grubb, 1990). Meanwhile, increasing in the species and number of birds attracted by food also
increases the possibility of disease transmission among birds in the feeding area (Brown and Hall, 2018). On the other hand,
artificial provisioning may also have several negative effects on current and future breeding in birds (Gonza lez et al., 2006).
Studies have shown that winter provisioning by humans decreases the breeding performance of Eurasian blue tits (Cyanistes
caeruleus) (Plummer et al., 2013) and that providing food for wild birds may increase predation risk of birds and their nests
around feeding sites (Hanmer et al., 2016). In addition, the behavioral responses caused by artificial provisioning can influence
the distribution of individuals by impacting migratory patterns, social systems, and survival rates in the modified habitat.
This, in turn, may affect gene flow and the degree of inbreeding and, hence, the amount of genetic variability and population
viability (Tuomainen and Candolin, 2011).
Artificial provisioning has become a form of selective pressure and can change the life history characteristics of birds
(Kubota and Nakamura, 2000), and the effects of non-lethal human disturbance on birds may become increasingly important
(Jiang and Møller, 2017). As a result of long-term feeding, wild birds may reduce their vigilance against humans and may
become used to being less wary of humans (O’Connell-Rodwell et al., 2000), which means that provisioning can effectively
accelerate the habituation process of urban birds (Jensen et al., 2011). Food provision has always been closely associated with
the domestication of wild birds. However, this may eventually result in a loss of wild traits in birds, particularly for those in
urban habitats (Robb et al., 2008). Studies have shown that flight initiation distance (FID)dthe distance at which birds flee
when humans approachdof birds in urban habitats is significantly shorter than of those from rural habitats (Møller et al.,
2015).
Animals may adapt to human effects through habituation or microevolution. Birds exhibit a “tamed” behavior when
approaching human feeders (Robb et al., 2008). Domestication and urbanization can decrease the fear threshold of animals
towards humans. A recent study indicated that hyraxes (Procavia capensis) living on kopjes among human settlements
showed decreased sensitivity towards human approach and had significantly shorter FID than hyraxes living on kopjes
without human settlements (Mbise et al., 2019). These behavioral responses can be assessed using the minimum approaching
distance (MAD) between humans and birds, i.e., the minimum distance in which there is bird movement or response caused
by human activities (Ferna ndez-Juricic et al., 2005). Most animals constantly maintain a specific safe distance from humans
and other potential predators (Stankowich and Blumstein, 2005). MAD can be estimated using: 1) FID; and 2) foraging
distance (FD), which is the minimum distance between birds that are feeding and humans. FID is a common marker for
measuring the degree of human disturbance on animals (Gutzwiller et al., 1998). Urbanization can cause increased tolerance
towards human disturbance in animals, which is manifested as a shorter FID (Møller, 2012), i.e., birds in urban habitats have
shorter FIDs than birds of the same species in rural habitats (Cooke, 1980). This difference is inferred to be caused by
habituation, local adaptation, and habitat selection (Samia et al., 2015; Vincze et al., 2016; Møller et al., 2015).
Changing food provision is an important intervention in bird ecology, because food plays an important role in the
domestication of wild animals. However, the understanding of the effects of this ubiquitous leisure activity in birds is still
limited, and the risks of this activity are still poorly known. In particular, under the scenario of increasing bird ecotourism, bird
feeding has become one of the largest ecological disruption experiments in multiple ecosystems in the world. However, the
effects of large-scale and broad artificial provisioning on birds are not well understood. Unlike western countries, artificial
provisioning for birds is not widespread and popular in China, for instance, supplementary feeding of wild birds in gardens
and backyards are common in America and Europe (e.g. Petersen, 1951) but rare in China. To our knowledge, the most well-
known wild bird feeding place in China is in Kunming city, with more than ten thousands of wintering black-headed gulls
(Chroicocephalus ridibundus) daily poured into the city zone for feeding, and a large number of people and tourists coming
here to sightsee and feed.
The aim of this study was to compare the behavioral responses of black-headed gulls from regions with different pro-
visioning intensities on the rural-urban spectrum towards food provisioning by humans. For this, we measured the MAD that
urban and rural black-headed gull populations approached humans for food (i.e., FD) and their FID. We predicted that black-
headed gulls from urban regions would have shorter FD and FID, while birds from rural areas would have longer FD and FID.
FD is a form of active approach, while FID is a passive evasion method; these parameters reflect the level of dependence and
adaptability of birds towards humans. The analysis of FD and FID of birds from urban and rural areas may aid in understanding
the responses of birds towards environmental changes and bird domestication in the present era, besides revealing the
process and direction of evolution of urban bird species.

2. Methods

2.1. Study species and study area

The black-headed gull is a migratory bird that primarily breeds in northern Eurasia and overwinters in southern Eurasia.
This bird is also the most commonly observed gull during winter in southern China (Zheng, 2017). In nature, black-headed
gulls mainly feed on insects, small fishes, prawns, and mollusks (Duncan and Green, 2015). Because of food shortage,
 C. Feng, W. Liang / Global Ecology and Conservation 21 (2020) e00873 3

black-headed gulls started entering the city of Kunming in 1985 searching for food, and urban residents provided them with
buns, bread, etc. Since then, human provisioning has been an important food source for the black-headed gull (Li and Liu,
2012). Several thousand black-headed gulls currently engage in foraging in parks in Kunming city during winter every
year; large amounts of food are provided by tourists and urban residents who come to watch and feed these birds (ESM Video
S1). Many black-headed gulls are almost completely dependent on human provisioning and have gradually been employing
new foraging methods that are different from those in nature. Most black-headed gulls forage for food on streets and plazas
and actively approach human feeders (ESM Video S2).
Supplementary data related to this article can be found at https://doi.org/10.1016/j.gecco.2019.e00873.

From November to December 2017, we observed and carried out experiments on the foraging and flush behaviors of
overwintering black-headed gulls at urban and rural areas in Kunming (25
01ʹ N, 102
41ʹ E) in China (Fig. 1). Five wetland
parks in the city were selected as urban sampling sites. These parks were frequently attended by urban residents and foreign
tourists and had shops specialized in selling food for tourists to feed black-headed gulls, thus resulting in intense provisioning.
Seven wetlands with black-headed gull activity were selected as rural sites. In rural areas, both gull population density and
human disturbance are low, and black-headed gulls mostly forage for food naturally. However, sporadic provisioning by
tourists and local residents still occurs (ESM Video S3). All surveys were carried out under sunny days (absence of rain or
snow, wind speed < 4 m/s). The survey period was from 8:00 a.m. to 16:00 p.m.
Supplementary data related to this article can be found at https://doi.org/10.1016/j.gecco.2019.e00873.

2.2. Field data collection

2.2.1. FD measurement
FD was measured as the shortest distance between foraging birds and humans when provisioning was carried out, i.e., the
horizontal distance from the provisioning site to the position of the observer. We usually measure the individual that foraging
freely on the grassland and square, occasionally, several of birds come together and only record the data once. To determine

Fig. 1. Location of urban (Kunming city) and rural sampling sites in the study area. Yellow dots indicate the seven rural survey sites and red dots indicate the five
urban survey sites. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
4 C. Feng, W. Liang / Global Ecology and Conservation 21 (2020) e00873

FD, the observer first hold a piece of bread in his hand and loudly called out to the black-headed gull at the provisioning site.
When black-headed gulls in both urban and rural sites heard this call and saw the bread, they actively approached humans to
beg for food, they keep a distance from humans and constantly shake their heads and call; the only difference between urban
and rural sites was in the stopping distance. For birds that stopped at close distances, food was directly thrown, and the
distance between the provisioning site and the observer was recorded. For birds that stopped further away, the food was
placed at the provisioning site, and the observer slowly retreated until the black-headed gull entered the provisioning site to
feed; this distance between the provisioning site and the observer was recorded. A laser range finder (UT390B, range:
0e40 m, precision: 0.01 m) was used to measure these distances. In order to avoid pseudoreplicates, i.e., to avoid re-
measuring FD for the same individual, each experiment was carried out 10 m away from the previous sampling site, and
did not return.

2.2.2. FID measurement

Birds were approached when they were at a relaxed state (such as resting, feeding, grooming, or chirping). An approximate
walking speed was used to approach one bird at a time. The observer wore neutral clothes and acted as pedestrians when
approaching the bird. The horizontal distance between the position of the bird and the position of the observer when that bird
started to flush away was recorded (following Blumstein, 2006). Birds were approached from a fixed distance, and a constant
starting distance was maintained to eliminate commonality problems caused by starting distance on FID (Blumstein, 2003).

2.3. Data analysis

Data processing and statistical analysis were performed using IBM SPSS 25.0 for Windows (IBM Inc., USA). A nested
ANOVA was used to test whether the differences in FD and FID between urban and rural bird populations were significant. All
tests were two-tailed, with statistical significance at P < 0.05. All data were expressed as mean ± standard deviation
(mean ± SD).

3. Results

From the five urban sites in Kunming in winter 2017, we obtained 1660 FD data points and 1764 FID data points (Fig. 2).
From the seven rural sites, we obtained a total of 2261 FD data points and 2376 FID data points (Fig. 2).

3.1. Comparison of FDs

The FD experiment results showed that the FD values for black-headed gulls in urban and rural areas were 0.59 ± 0.71 m
and 3.45 ± 2.02 m, respectively. There was a significant difference in FD between urban and rural areas (nested ANOVA,
F ¼ 10518.53, P < 0.001) (Table 1). FD in the five urban sites ranged from 0.14 ± 0.29 m to 1.08 ± 0.99 m, and the inter-site
difference was small (<1 m). FD in the seven rural sites ranged from 1.57 ± 0.81 m to 6.43 ± 1.47 m, and inter-site differ-
ences were larger (>2 m, up to 4.8 m).

3.2. Comparison of FIDs

The FID experiment results showed that the FID values for black-headed gulls in urban and rural areas were 1.03 ± 0.58 m
and 6.35 ± 3.51 m, respectively. There was a significant difference in FID between urban and rural areas (nested ANOVA,
F ¼ 13779.501, P < 0.001) (Table 1). FIDs in the five urban sites ranged from 0.84 ± 0.43 m to 1.23 ± 0.77 m, and inter-site
differences were all low (within 0.5 m). FIDs in the seven rural sites ranged from 3.02 ± 1.29 m to 11.26 ± 3.93 m, and
inter-site differences were larger (>3.5 m, up to 8.2 m).

4. Discussion

Our results were similar to what reported by Petersen (1951) and showed that the behavioral responses of black-headed
gulls in urban and rural areas towards artificial provisioning were primarily manifested as extremely significant differences in
FD and FID, which were shorter in black-headed gulls in urban regions than in those from rural regions. Animals view humans
as potential predators and, therefore, normally respond to human behavior by maintaining a safe distance (Frid and Dill,
2002). Taking this into account, bird behavior is expected to be balanced between food provisioning and predation risk
(Blumstein, 2014). However, in the urban provisioning sites in Kunming, black-headed gulls instead seemed to consider
humans as “owners” who provide food. In these places, during daytime, the birds waited to be fed; while tourists shouted and
offered birds bread or other food, black-headed gulls flew in the direction of tourists and sometimes even directly took food
from tourists’ hands, which resulted in short FDs (Fig. 3; ESM Videos S1eS2). This showed that black-headed gulls from urban
regions are highly adapted to human feeding. By contrast, in rural regions, most black-headed gulls naturally foraged for food,
thus resulting in longer FDs. This showed that black-headed gulls in rural regions are still wary of humans. Moreover, in the
seven rural sites, the variations in FD and FID were both large. This was caused by the varying degrees of human provisioning
 C. Feng, W. Liang / Global Ecology and Conservation 21 (2020) e00873 5

Fig. 2. Comparison of (a) foraging distance and (b) flight initiation distance between birds from five urban sites and seven rural sites. Ordinates represent
distance, it can be displayed from figure (a) and (b) that foraging distance and flight initiation distance were shorter in black-headed gulls in urban areas than in
those from rural areas.

and disturbance in the different rural areas. On the other hand, the variations in FD and FID in the five urban sites were both
very small and showed homogeneous trends.
In Kunming city, urban black-headed gulls often flock to beg for food. Our study further proved that food is a major factor
increasing bird tolerance towards humans. Traditionally, flocking is believed to be an effective anti-predation strategy as it can
decrease the probability of individuals being killed (Cresswell, 1994). Flocking decreases monitoring costs through increasing
collective vigilance. In addition, flocking also increases the possibility of searching for foraging sites, while simultaneously
increasing tolerance towards higher levels of disturbance (Roberts, 1996; Samia et al., 2015). The FID in sites under human
disturbance is an important marker that reflects bird tolerance and adaptability towards humans (Blumstein, 2014; Møller
and Garamszegi, 2012), and birds from different regions have showed differences in tolerance of predation risk (Møller,
2010). Urban bird populations have shorter FID than rural populations of the same species and exhibit greater tolerance
towards predation risk (Cooke, 1980; Møller, 2008). Habituation, habitat selection, and food are important factors that
promote reduced FID in urban animals (Samia et al., 2015; Vincze et al., 2016; Møller et al., 2015), and these factors do not act
alone. The present study showed that adaptability towards human disturbance also increased with provisioning intensity. The
mean FID of black-headed gulls in urban regions was significantly lower than that of rural populations. The smaller the FID,
the stronger the adaptability towards human activities (Gutzwiller et al., 1998). In rural regions, FID also decreased as pro-
visioning intensity increased, showing that provisioning could effectively accelerate habituation (Møller et al., 2015).
In general, black-headed gulls prefer to flock to places with people for foraging; they have become urbanized birds that
approach human populations to obtain food and have learned that food is present when there are human crowds (Wu et al.,
2009). The tendency for black-headed gulls to fly towards crowded places has become a fixed behavior (Duncan and Green,
2015). Undoubtedly, black-headed gulls in urban regions obtain food more easily than those in rural regions, especially
because of their food-begging behavior and of the lower predation risk.
Providing food for wild birds may have negative effects and risks. Birds may link humans to the presence of food and, as a
result, reduce their vigilance behaviors against humans (O’Connell-Rodwell et al., 2000). The provisioning activity may cause
6 C. Feng, W. Liang / Global Ecology and Conservation 21 (2020) e00873

Table 1
Differences in foraging distance (FD) and flight initiation distance (FID) between birds from five urban sites and seven rural sites (nested ANOVA).

Type Site Mean (m) SD (m) df F P

FD urban 0.60 0.71 2 10518.53 <0.001
rural 3.45 2.02
FID urban 1.03 0.85 2 13779.501 <0.001
rural 6.35 3.50

Fig. 3. Black-headed gulls in urban regions (a) feeding from a tourist’s hand and (b) waiting for provisioning on the observer’s head.

individuals habituated towards humans to become bolder; some black-headed gulls in Kunming even boldly rested on
tourist’s heads for provisioning (Fig. 3). Reduced fear and predation responses towards humans in black-headed gulls may
reduce their alertness towards carnivores and other predators, making them easier to gather and activity in large numbers at
provisioning areas, so that they can be easily preyed on by the predators who are waiting around here.
Food is an important tool for the domestication of wild animals by humans. An example is the domestic city pigeons,
which descend from the rock pigeons (Columba livia) that were domesticated by humans (Johnston and Janiga, 1995). The
success of urban pigeon populations is attributed to the low levels of predation and all-year round food supply (Sol et al.,
2013). Black-headed gulls currently exhibit a partial loss of wild traits and a high degree of domestication, which is man-
ifested as them following dense human populations and shifting their foraging sites, as well as their adaptation to and
dependence on artificial feeding. These birds have generally developed behavioral adaptations to co-exist with humans; for
instance, they present the unique ability to understand and respond to human commands (Dukas, 2004), linking human calls
to food and flying to humans to beg for food. The possible long-term effects of this process are alarming, as they may lead to
the domestication of black-headed gulls or cause them to become “resident birds” that are unable to return to their breeding
sites (Plummer et al., 2015). A study showed that winter food provisioning could reduce future breeding performance of birds
(Plummer et al., 2013). The effects of large-areas of provisioning on the breeding success of black-headed gulls are still unclear,
considering that they eat a lot of nutritious bread provided by people. Nevertheless, 19.9% of black-headed gulls in Dianchi
Lake were found to be carriers of Toxoplasma gondii, a conflict between humans and birds is unavoidable (Miao et al., 2014).
Because of human provisioning and burgeoning bird ecotourism, we need to understand the disturbance of human activities
on the biological aspects of birds and to propose a manner for humans to live harmoniously with birds (Jones, 2018). This
requires managers to formulate promotion plans, management policies, and conservation plans based on empirical data. The
example presented in this study of human provisioning for black-headed gulls in Kunming demonstrates that birds can co-
exist harmoniously with humans with mutual benefits. However, further detailed monitoring is clearly needed to understand
the long-term effects of artificial provisioning on birds.
 C. Feng, W. Liang / Global Ecology and Conservation 21 (2020) e00873 7

5. Conclusions

The large-scale artificial provisioning in Kunming is an important example of the impact of human disturbance on wild
animals. Our study showed that artificial provisioning may accelerate the domestication of urban black-headed gulls, causing
them to lose their wild nature, thereby increasing their dependence on humans. In other words, black-headed gulls actively
approach humans who feed them and their FD and FID towards humans are reduced. The long-term effects of artificial
provisioning on wild birds require further monitoring.

Authors’ contributions

W.L. designed the study; C.F. carried out field experiments, performed laboratory and statistical analyses and wrote the
draft manuscript. W.L. revised and improved the manuscript. All authors approved the final submission.

Ethical approval

The experiments reported here comply with the current laws of China. Fieldwork was carried out without specific permit.
Experimental procedures were in agreement with the Animal Research Ethics Committee of Hainan Provincial Education
Centre for Ecology and Environment, Hainan Normal University (permit no. HNECEE-2016-004).

Funding

This work was funded by the National Natural Science Foundation of China (Nos. 31772453 and 31970427 to WL).

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have
appeared to influence the work reported in this paper.

Acknowledgments

We would like to thank Prof. Xiaojun Yang, Dr. Feng Dong and Dr. Fei Wu from Kunming Institute of Zoology, Chinese
Academy of Sciences, for their help and cooperation.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.gecco.2019.e00873.

References

Blumstein, D.T., 2003. Flight-initiation distance in birds is dependent on intruder starting distance. J. Wildl. Manag. 67, 852e857.
Blumstein, D.T., 2006. Developing an evolutionary ecology of fear: how life history and natural history traits affect disturbance tolerance in birds. Anim.
Behav. 71, 389e399.
Blumstein, D.T., 2014. Attention, habituation, and antipredator behaviour: implications for urban birds. In: Gil, D., Brumm, H. (Eds.), Avian Urban Ecology:
Behavioural and Physiological Adaptations. Oxford University Press, New York, pp. 41e53.
Brown, L.M., Hall, R.J., 2018. Consequences of resource supplementation for disease risk in a partially migratory population. Phil. Trans. R. Soc. B 373,
20170095.
Cooke, A.S., 1980. Observations on how close certain passerine species will tolerate an approaching human in rural and suburban areas. Biol. Conserv. 18,
85e88.
Cresswell, W., 1994. Flocking is an effective anti-predation strategy in redshanks, Tringa totanus. Anim. Behav. 47, 433e442.
Díaz Lopez, B., 2019. “Hot deals at sea”: responses of a top predator (Bottlenose dolphin, Tursiops truncatus) to human-induced changes in the coastal
ecosystem. Behav. Ecol. 30, 291e300.
Duncan, P., Green, J.A., 2015. Food preference of the black-headed gull Chroicocephalus ridibundus differs along a rural-urban gradient. Bird Study 62, 56e63.
Dukas, R., 2004. Evolutionary biology of animal cognition. Annu. Rev. Ecol. Evol. Syst. 35, 347e374.
Fernandez-Juricic, E., Venier, M.P., Renison, D., Blumstein, D.T., 2005. Sensitivity of wildlife to spatial patterns of recreationist behavior: a critical assessment
of minimum approaching distances and buffer areas for grassland birds. Biol. Conserv. 125, 225e235.
Frid, A., Dill, L.M., 2002. Human caused disturbance stimuli as a form of predation risk. Conserv. Ecol. 6, 11.
Gonza lez, L.M., Margalida, A., S anchez, R., Oria, J., 2006. Supplementary feeding as an effective tool for improving breeding success in the Spanish imperial
eagle (Aquila adalberti). Biol. Conserv. 129, 477e486.
Grubb, T.C., 1990. Supplementary food improves the nutritional condition of wintering woodland birds: evidence from ptilochronology. Ornis Scand. 21,
277e281.
Gutzwiller, K.J., Marcum, H.A., Harvey, H.B., Roth, J.D., Anderson, S.H., 1998. Bird tolerance to human intrusion in Wyoming Montane forests. Condor 100,
519e527.
Hanmer, H.J., Thomas, R.L., Fellowes, M.D.E., 2016. Provision of supplementary food for wild birds may increase the risk of local nest predation. Ibis 159,
158e167.
Jensen, E.L., Dill, L.M., Cahill, J.F., 2011. Applying behavioral-ecological theory to plant defense: light-dependent movement in Mimosa pudica suggests a
trade-off between predation risk and energetic reward. Am. Nat. 177, 377e381.
Jiang, Y., Møller, A.P., 2017. Antipredator escape distances of common and threatened birds. Behav. Ecol. 28, 1498e1503.
8 C. Feng, W. Liang / Global Ecology and Conservation 21 (2020) e00873

Johnston, R.F., Janiga, M., 1995. Feral Pigeons. Oxford University Press, Oxford.
Jones, D., 2011. An appetite for connection: why we need to understand the effect and value of feeding wild birds. Emu 111, ievi.
Jones, D., 2018. The Birds at My Table: Why We Feed Wild Birds and Why it Matters. Cornell University Press, Ithaca.
Kubota, H., Nakamura, M., 2000. Effects of supplemental food on intra and inter-specific behaviour of the varied tit Parus varius. Ibis 142, 312e319.
Li, S., Liu, Z., 2012. Surveys on population dynamics and feeding of wintering black-headed gulls (Larus ridibundus) in Kunming Cuihu Park. Chin J Wildl 33,
146e148.
Martinson, T.J., Flaspohler, D.J., 2003. Winter bird feeding and localized predation on simulated bark-dwelling arthropods. Wildl. Soc. Bull. 31, 510e516.
Mbise, F.P., Fredriksen, K.-E., Ranke, P.S., Jackson, C., Fyumagwa, R., Holmern, T., Fossøy, F., Røskaft, E., 2019. Human habituation reduces hyrax flight
initiation distance in Serengeti. Ethology. https://doi.org/10.1111/eth.12968.
Miao, Q., Han, J., Xiang, X., Yuan, F., Liu, Y., Duan, G., Zhu, X., Zou, F., 2014. Prevalence of antibody to toxoplasma gondii in black-headed gulls (Chroicocephalus
ridibundus), Dianchi Lake, China. J. Wildl. Dis. 50, 717e719.
Møller, A.P., 2008. Flight distance of urban birds, predation, and selection for urban life. Behav. Ecol. Sociobiol. 63, 63e75.
Møller, A.P., 2010. Interspecific variation in fear responses predicts urbanization in birds. Behav. Ecol. 21, 365e371.
Møller, A.P., 2012. Urban areas as refuges from predators and flight distance of prey. Behav. Ecol. 23, 1030e1035.
Møller, A.P., Garamszegi, L.Z., 2012. Between individual variation in risk-taking behavior and its life history consequences. Behav. Ecol. 23, 843e853.
Møller, A.P., Tryjanowski, P., Díaz, M., Kwiecin  ski, Z., Indykiewicz, P., Mitrus, C., 2015. Urban habitats and feeders both contribute to flight initiation distance
reduction in birds. Behav. Ecol. 26, 861e865.
O’Connell-Rodwell, C.E., Rodwell, T., Rice, M., Hart, L.A., 2000. Living with the modern conservation paradigm: can agricultural communities co-exist with
elephants? A five-year case study in East Caprivi, Namibia. Biol. Conserv. 93, 381e391.
Orros, M.E., Fellowes, M.D.E., 2015. Wild bird feeding in an urban area: intensity, economics and numbers of individuals supported. Acta Ornithol. 50,
43e58.
Petersen, E., 1951. Homing experiments with black-headed gull (Larus r. ridibundus L.) and common gull (Larus c. canus L.) in the winter-quarters. Dansk
Ornithol Foren Tidsskr 47, 153e178.
Plummer, K.E., Bearhop, S., Leech, D.I., Chamberlain, D.E., Blount, J.D., 2013. Winter food provisioning reduces future breeding performance in a wild bird.
Sci. Rep. 3, 2002.
Plummer, K.E., Siriwardena, G.M., Conway, G.J., Risely, K., Toms, M.P., 2015. Is supplementary feeding in gardens a driver of evolutionary change in a
migratory bird species? Glob. Chang. Biol. 21, 4353e4363.
Robb, G.N., McDonald, R.A., Chamberlain, D.E., Bearhop, S., 2008. Food for thought: supplementary feeding as a driver of ecological change in avian
populations. Front. Ecol. Environ. 6, 476e484.
Roberts, G., 1996. Why individual vigilance declines as group size increases. Anim. Behav. 51, 1077e1086.
Samia, D.M., Nakagawa, S., Nomura, F., Rangel, T.F., Blumstein, D.T., 2015. Increased tolerance to humans among disturbed wildlife. Nat. Commun. 6, 8877.
Sih, A., Ferrari, M.C.O., Harris, D.J., 2011. Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4, 367e387.
Sol, D., Lapiedra, O., Gonza lez-Lagos, C., 2013. Behavioural adjustments for a life in the city. Anim. Behav. 85, 1101e1112.
Stankowich, T., Blumstein, D.T., 2005. Fear in animals: a meta-analysis and review of risk assessment. Proc. R. Soc. Lond. B 272, 2627e2634.
Tuomainen, U., Candolin, U., 2011. Behavioural responses to human-induced environmental change. Biol. Rev. 86, 640e657.
Vincze, E., Papp, S., Preiszner, B., Seress, G., Bo kony, V., Liker, A., 2016. Habituation to human disturbance is faster in urban than rural house sparrows. Behav.
Ecol. 27, 1304e1313.
Wu, Z., Zhao, X., Wang, Z., Yang, M., 2009. The wildness loss of wintering black-headed gull caused by human feeding and urban wild bird management in
Kunming. Yunnan Geograp. Environ. Res. 21, 1e5.
Zheng, G., 2017. A Checklist on the Classification and Distribution of the Birds of China, third ed. Science Press, Beijing.