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Increasing global human population and constant exploitation and utilization of natural resources have strongly impacted bird populations worldwide. Thus, it is very important for birds to recognize which activities are threatening and which are not. This ability could accelerate the adaptation of certain species to the changing environment. However, few studies have explored the ability of wild birds to recognize human individuals. This study aimed to investigate the ability of waterbirds to identify local fishermen from outsiders. Specifically, two experiments were conducted in the workplace of fishermen, a tidal flat, where a person was dressed up in a casual outfit and a fisherman outfit, respectively, to measure the flight initiation distances (FIDs, the distance at which a prey starts to flee at the approach of a predator) of waterbirds. The FIDs of eight species of waterbirds were significantly different after seeing the fisherman outfit versus the casual outfit. Compared to the casual outfit, the FIDs of birds to the fishermen outfit were noticeably shorter. Thus, waterbirds are able to distinguish between unknown (threatening) and known (non-threatening) human individuals based on the differences in appearance. Our results are of importance for bird conservation and ecotourism.
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Original Research Article
Living together: Waterbirds distinguish between local
shermen and casual outts
Changzhang Feng, Wei Liang
*
Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, 571158,
China
article info
Article history:
Received 17 January 2020
Received in revised form 27 February 2020
Accepted 27 February 2020
Keywords:
Fisherman
Flight initiation distance
Recognition ability
Waterbirds
abstract
Increasing global human population and constant exploitation and utilization of natural
resources have strongly impacted bird populations worldwide. Thus, it is very important
for birds to recognize which activities are threatening and which are not. This ability could
accelerate the adaptation of certain species to the changing environment. However, few
studies have explored the ability of wild birds to recognize human individuals. This study
aimed to investigate the ability of waterbirds to identify local shermen from outsiders.
Specically, two experiments were conducted in the workplace of shermen, a tidal at,
where a person was dressed up in a casual outt and a sherman outt, respectively, to
measure the ight initiation distances (FIDs, the distance at which a prey starts to ee at
the approach of a predator) of waterbirds. The FIDs of eight species of waterbirds were
signicantly different after seeing the sherman outt versus the casual outt. Compared
to the casual outt, the FIDs of birds to the shermen outt were noticeably shorter. Thus,
waterbirds are able to distinguish between unknown (threatening) and known (non-
threatening) human individuals based on the differences in appearance. Our results are of
importance for bird conservation and ecotourism.
©2020 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
Animals are being impacted by human activities day and night, everywhere. Over time, animals might learn to differ-
entiate an unsafe area from the safe one, and to change their behaviors correspondingly (Snell-Rood, 2013;Sih, 2013). For
example, urban animals that are able to learn and memorize different sounds are more likely to gain access to better food and
avoid predation (Cornell et al., 2012). One of the main mechanisms for animals to develop their recognition ability is learning,
i.e., acquiring new information that inuences behavior (Dukas, 2004). To learn is not to adopt the same behavior on specic
stimuli, but to allow animals to improve their own behavioral responses based on their experiences (Dukas, 1998). The most
obvious reason for animals to respond to humans is that they perceive humans as potential predators and respond corre-
spondingly (Frid and Dill, 2002). Although humans, usually, do not present a real risk of predation, the responses of animals to
humans and to true predators are similar (Beale and Monaghan, 2004).
There is increasing evidence supporting the ability of animals to recognize human individuals, with animals continu-
ously adjusting their behaviors in urban areas; however, the potential recognition cues and mechanism remain unclear
*Corresponding author.
E-mail addresses: fengcz@hainnu.edu.cn (C. Feng), liangwei@hainnu.edu.cn (W. Liang).
Contents lists available at ScienceDirect
Global Ecology and Conservation
journal homepage: http://www.elsevier.com/locate/gecco
https://doi.org/10.1016/j.gecco.2020.e00994
2351-9894/©2020 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/).
Global Ecology and Conservation 22 (2020) e00994
(Price et al., 2003;Sol et al., 2013). Previous studies have shown that human facial features represent a reliable standard for
recognition. Dittrich et al. (2010) suggested that the cue of the human face is essential for recognition by birds, whereas
others suggested that clothes and voices aid recognition (Belguermi et al., 2011;Sliwa et al., 2011;Wascher et al., 2012).
The species condence hypothesis (Burley et al., 1982) states that birds focus more on colors in their own familiar envi-
ronments, i.e., the colors found on their own bodies. Thus, birds might react with various ight initiation distances (FIDs, the
distance at which a prey starts to ee at the approach of a predator) to the various colors of human clothes (Gutzwiller and
Marcum, 1997). Ravens (Corvus brachyrhynchos) and mockingbirds (Mimus polyglottos)(Levey et al., 2009) are also able to
identify various human facial features, as the higher cognitive abilitieshypothesis was proposed (Marzluff et al., 2010). In
other words, these two species can rapidly learn to distinguish human individuals because of their higher than average
cognitiveabilities (Marzluff et al., 2010). Lee et al. (2011) even found that wild magpies (Pica pica) can distinguish human
individuals that pose a threat to their nests from those that do not based on their behavior. As a result, the authors proposed
the pre-exposure to stimulihypothesis, which indicates that frequent exposure to humans in urban habitats enhances the
ability of birds to discriminate among human individuals (Lee et al., 2011).
If this mechanism is combined with a higher cognitive ability, some species might be able to learn to distinguish human
individuals more easily. However, few studies have focused on the learning and recognition ability of wild birds. Most of these
studies focus on a single species (Dukas, 2004) rather than a wide variety of sympatric wild birds occupying the same natural
habitat impacted by human activities. Moreover, most birds that have been studied are urban birds. There are few studies on
the adaptation of birds in the natural environments where human disturbance is expanding (Chace and Walsh, 2006).
Habituation to human disturbance is considered a key factor in the successful coexistence of animals with mankind (Díaz
et al., 2013). FID was used as a measure to examine the tolerance and adaptation of a species to human (Burger and Gochfeld,
1991 ;Møller, 2008a). FID is also used to examine the ability of birds to recognize various cues (Gutzwiller and Marcum, 1997).
Based on our observations on waterbirds at the seaside, shermen were close to foraging birds when walking around and
working, the distance between shermen and bird was only a few meters (Fig. 1A and B; ESM Video S1). However, whenever
we moved towards the birds to observe them, they became alert tens of meters away and started to y. Thus, we hypothesized
that, in coastal tidal ats supporting intensive activities of shermen, waterbirds are able to distinguish between local
shermen (who they see continuously) and other people (who are seldom present). To determine whether waterbirds can
Fig. 1. The local shermen were close to foraging birds when walking around and working at the seaside. A and B show different local shermen.
C. Feng, W. Liang / Global Ecology and Conservation 22 (2020) e009942
discriminate between casual outts and shermen outts, we conducted the following experiments. First, the observer wore
a casual outt and approached the birds, and the FIDs were measured. Second, the observer wore a sherman outt and
approached the birds, and the FIDs were measured again. We predicted that the FIDs would be longer in response to the
casual outt compared to the sherman outt. Our results are expected to demonstrate the ability of various sympatric
species of birds to memorize and recognize different cues, and how these variables affect related behaviors such as learning.
Supplementary data related to this article can be found at https://doi.org/10.1016/j.gecco.2020.e00994.
2. Methods
2.1. Study area
This study was conducted in a coastal tidal at (21
32
0
N, 108
07
0
E) in Jiangping Town, Dongxing County, Guangxi Zhuang
Autonomous Region, Southwestern China, during the wintering period (FebruaryeMarch) in 2017 and 2018. In this study
area, waterbirds are relatively abundant, with frequent human disturbance. Every day, many shermen visit frequently this
tidal at to dig for sandworms and snails or to catch shes (ESM Video S1).
2.2. Recording FID
We conducted two groups of experiments in a random order. In the rst group, the observer wore a casual outt (the
casual outt implies some special outt worn on holiday). In the second group, the observer wore a local sherman outt,
with some sherman accessories and tools (Fig. 2). The daily observation time was decided based on the tide table. The
observation time corresponded to the foraging time of waterbirds after the tide ebbed on days that were sunny with low fog
Fig. 2. Outts used to represent a casual person (lef t) and a local sherman (right). The two photos show the same people, Changzhang Feng, who is the rst
author of this paper. Photo by Changzhang Feng.
C. Feng, W. Liang / Global Ecology and Conservation 22 (2020) e00994 3
cover and no wind. FID was determined based on the method proposed by Gutzwiller et al. (1998). Specically, FID was
dened as the distance between the point where the researcher stopped moving because of the escape of the bird. To record
FID, once we found a bird, we used Zeiss binoculars (Zeiss Victory 10 45 T*RF, Carl Zeiss AG, Germany) to identify the bird
individual, and we walked at the normal speed (1 m/s) of a sherman until the bird dodged or ew away. At that point, we
stopped moving, and used the distance measuring function of the binoculars to record the distance between the person and
the take-off point of the bird. To avoid pseudo replication, after every experiment, the experimenter moved 100 m away from
the sample area, and prepared for the next experiment, to avoid repeatedly measuring the same bird individual.
2.3. Data analysis and statistics
Statistical analyses were performed by IBM SPSS 20.0 for Windows (IBM Inc., USA) and values were presented as
mean ±standard deviation (SD). Tests were two-tailed and the signicant level was p<0.05. The one sample Kolmogorov-
Smirnov (KeS) test was used to analyze the normalityof each data group. Since our data did not meet the normal distribution,
the Mann-Whitney Utest, a nonparametric test, was used to determine whether there was a difference between the test
result of sherman outts and that of casual outts.
3. Results
A total of 15 species of waterbirds were observed in the study area. However, only data of eight species belonging to four
families and two orders were included in the nal analysis. These data included 389 FIDs of waterbirds being exposed to
casual outts, and 514 FIDs of waterbirds being exposed to sherman outts (Table 1). Seven bird species were not included in
the nal analysis due to limited sample size (ESM Table S1).
The FIDs of the casual outt group ranged from 19.6 ±4.0 m to 42.2 ±11.2 m, while those of the sherman outt group
ranged from 10.3 ±2.9 m to 20.3 ±5.1 m. In the casual outt group, common redshank (Tringa totanus) had the smallest FID
(19.6 ±4.0), while little egret (Egretta garzetta) had the greatest FID (42.2 ±11.2 m). In the sherman outt group, dunlin
(Calidris alpina) had the smallest FID (10.3 ±2.9 m), while kentish plover (Charadrius alexandrinus) had the greatest FID
(20.3 ±5.1 m) (Fig. 3). The waterbird species with the smallest and greatest FIDs differed in the two groups.
The difference test indicated that there were great differences in the data of all the eight waterbird species between the
casual and sherman outt groups (Mann-Whitney UTest, p<0.0001) (Table 1). The FIDs of the eight waterbird species in the
casual outt group were signicantly greater than those in the sherman group. In other words, when wearing the sherman
outts, the FIDs notably declined. For the eight species of birds, black-headed gull (Chroicocephalus ridibundus) exhibited the
greatest changes in FIDs, declining from 42.0 ±9.3 m to 14.8 ±7.8 m, with a decrease of 27.2 ±5.1 m. In comparison, common
redshank had the smallest changes in FIDs, reducing from 19.6 ±4.1 m to 11.1 ±2.0 m, with a decline of 8.5 ±3.6 m.
4. Discussion
Our results demonstrated that FIDs were greater when the observer was in a casual outt compared to the sherman outt
for all eight species of waterbirds. This conrmed that local waterbirds were able to distinguish casual outts from those of
local shermen.
The FID to human disturbance is an important indicator of the ability of birds to adapt and tolerate humans (Burger and
Gochfeld, 1991). By learning to discriminate between potential enemies and friends, animals may increase the likelihood of
obtaining food and avoid predation (Cornell et al., 2012;Snell-Rood, 2013). The fact that the FIDs of the sherman outt group
were shorter than those of the casual outt group indicate that waterbirds are familiar with and adapted to the local sh-
ermen. All eight species of waterbirds adjusted the FID based on the external features of humans. Black-headed gull exhibited
the greatest difference in its response, moving the furthest distance from the observer in the casual outt. In comparison, this
species moved the shortest distance from the observer in the shermen outt. The tolerance to humans was signicantly
different among the eight species, with this difference being reected by variation in FIDs (Møller, 2010). The FIDs of six of the
species were noticeably different, while those of the related species common redshank and spotted redshank (Tringa
erythropus) were similar.
Table 1
Results of the analysis on the difference between the ight initiation distances (FID) in the casual and sherman groups.
Species Casual FID (m) N¼Fisherman FID (m) N¼ZP
Marsh sandpiper Tringa stagnatilis 21.2 ±5.2 33 12.3 ±3.4 51 1.739 <0.0001
Common greenshank T. nebularia 31.1 ±11.7 60 14.8 ±5.6 160 9.908 <0.0001
Kentish plover Charadrius alexandrinus 32.2 ±6.0 75 20.3 ±5.1 63 0.679 <0.0001
Dunlin Calidris alpina 26.2 ±5.4 38 10.3 ±2.9 64 31.234 <0.0001
Little egret Egretta garzetta 42.2 ±11.8 46 17.8 ±10.1 37 0.048 <0.0001
Spotted redshank Tringa erythropus 20.9 ±4.2 34 11.4 ±3.5 36 2.472 <0.0001
Common redshank T. totanus 19.6 ±4.1 40 11.1 ±2.0 32 13.464 <0.0001
Black-headed gull Chroicocephalus ridibundus 42.0 ±9.3 34 14.8 ±7.8 46 1.252 <0.0001
C. Feng, W. Liang / Global Ecology and Conservation 22 (2020) e009944
Most species react negatively to human disturbance (Carney and Sydeman, 1999). However, it remains unclear why some
species coexist well with humans, while others do not (Cooper and Frederick, 2007). The higher cognitive abilitieshy-
pothesis states that the high perception and fast learning abilities of birds allows them to adapt well to urban habitats,
recognizing human and predators in human residential area (Marzluff et al., 2010). All the eight waterbird species in the study
area were clearly able to recognize and distinguish local shermen outts from casual outts. However, the level of the
recognition ability of each species could not be determined. Stephan et al. (2012) also suggested that species of birds that are
not considered to have higher cognitive abilities have the ability to recognize individuals of different species. The pre-
exposure to stimulihypothesis states that for birds living in urban areas exposed to frequent contact with human individuals
could benet from the ability to recognize various features of humans and adjust their behavior accordingly (Lee et al., 2011).
The waterbirds were exposed to local shermen when foraging over many years, this long-term exposure undoubtedly
enhanced the abilities of the birds to recognize the features of shermen. These abilities could be applied towards learning to
distinguish between threatening and neutral types of humans. Therefore, the present study conrms that wild birds have
similar cognitive learning abilities as urban birds after constant exposure to humans.
Some animals reduce the frequency of monitoring surrounding risks during foraging (Dukas and Kamil, 20 00). However, in
the presence of humans in casual outts, waterbirds maintained quite long FIDs. Thus, the birds remained alert to external
factors, including humans with different features, but were less alert to shermen, with whom they had frequent exposure
and recognized as unthreatening. Through recognizing that shermen do not present a threat, birds are able to conserve
energy by not frequently ying back and forth from foraging spots. By using this tactic, birds could allocate more time and
energy to behaviors producing greater rewards, such as foraging.
Birds are extremely sensitive to visual cues, often using minute features as a basis for recognition (Belguermi et al., 2011).
Previous studies found that birds can recognize people based on their facial features or the colors of clothes (Dittrich et al.,
2010;Sliwa et al., 2011;Wascher et al., 2012). The facial features of humans also inuence the ability of birds to recognize
humans (Dittrich et al., 2010). Fishermen working at our study site wear a variety of clothes, but all wear straw hats with
masks covering their faces and oversleeves to prevent sunburn. Therefore, colors and facial features are not the cues used by
these birds to distinguish casual outts. The birds might recognize people based on the uniform and consistent outt
characteristics.
Although our study conrmed that the wild birds in the study area are able to distinguish humans, it was not possible to
test the ability of all species. Thus, further experiments on the recognition of local residents and outsiders by birds are needed.
In addition, future studies should explore the adaptability of sympatric individuals fromdifferent species in a mixed group to
human disturbance. Moreover, species in our study area differed in FID, and previous studies have shown that FIDs among
species of birds varied signicantly with many potentially confounding factors including life history and body size (Blumstein,
2006;Møller, 2008b), next, more speciesdata should be collected to analyze the related factors of inter-specic differences.
Fig. 3. Flight initiation distances of eight species of waterbirds in the casual and sherman groups. Error bars refer to standard deviation (SD) and all summary
statistics are presented as mean ±SD.
C. Feng, W. Liang / Global Ecology and Conservation 22 (2020) e00994 5
In conclusion, our study showed that waterbirds that were frequently exposed to shermen in a tidal at were able to
distinguish between local shermen and visitors by memorizing the outts of shermen. The birds were also able to estimate
the level of threats of different types of human individuals, adopting different foraging and escape behaviors. In other words,
the birds were habituated to the presence of shermen, and increased their tolerance, but remained alert to other external
threatening factors. Our results are of importance for bird conservation and ecotourism.
Authorscontributions
W.L. developed the research, C.F. conducted eld experiments, performed data analysis, and wrote the draft manuscript.
W.L. revised and improved the manuscript. Both authors approved the nal version.
Compliance with ethical standards
The experiments comply with the current laws of China. 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 supported by the National Natural Science Foundation of China (No. 31772453 and 31970427 to WL).
Declaration of competing interest
The authors declare that they have no known competing nancial interests or personal relationships that could have
appeared to inuence the work reported in this paper.
Acknowledgments
We are grateful to local shermen for assistance with eldwork. We would like to thank two anonymous reviewers for
their helpful comments on an early version of this manuscript.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.org/10.1016/j.gecco.2020.e00994.
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... October-December; see Mikula et al. 2018), breeding (we sampled only nonbreeding birds; Weston et al. 2018), latitude (the latitudinal span was a modest 3.57, 6.27-9.77N; see Poddubnaya et al. 2019), altitude (all locations were in lowland parts of the dry zone below 400 m), and clothing (observers wore dull pants and shirts and wore hats; see Feng and Liang 2020). In a separate study, we showed a series of factors that do not evidently influence FID in Sri Lankan birds: breeding system, habitat, conservation status, migratory status, development (altricial/precocial), nativeness, and diet (Ekanayake et al., forthcoming). ...
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... S.) conducted this experiment was a newly human intruder for Oriental reed warblers. Recent studies found that birds not only can recognize different avian species by some features (Ber ankov a et al., 2014), but also recognize different humans (Feng and Liang, 2020b). Thus, we suggested that the observation data in our experiments were statistically independence.We followed the method in Yu et al. (2017) to score the response of a warbler (response scores hereafter) on a 4-point scale with: (i) warblers produced songs or alarm calls with stationary observing; (ii) warblers produced alarm calls with skipping and flicking of wings; (iii) warblers approached the intruder (<1 m), and performing harassing behavior or attack behavior with no physical encounter; (iv) warblers performed attack behavior with physical impact. ...
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