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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,
article info
Article history:
Received 17 January 2020
Received in revised form 27 February 2020
Accepted 27 February 2020
Flight initiation distance
Recognition ability
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 (
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: (C. Feng), (W. Liang).
Contents lists available at ScienceDirect
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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
2. Methods
2.1. Study area
This study was conducted in a coastal tidal at (21
N, 108
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
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.
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).
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.
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
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... marmota) select regions with large stones to allow better vigilance (Borgo, 2003). Furthermore, species like alpine marmot and some waterbirds can behaviorally reduce flight initiation distance (FID) to optimize their fitness by the accustomed to nonfatal human activities (Feng & Liang, 2020;Louis & Le Berre, 2000;Thibault et al., 2020). ...
... The differentiation may arise because the optimal strategy to survival for LDP individuals is to flee early like NP individuals when threatened however the distance to a potential refuge (Li et al., 2011). Shorter flee distance and longer FID guarantees the safety of unaccustomed LDP individuals under the disturbances of human activities (Feng & Liang, 2020;Zaman et al., 2019). ...
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... Recently, some guidelines and rules in these locations have already been put in place to reduce disturbance to the SSME. Providing a sound basis for these guidelines requires quantification of the effects of human disturbances and documenting how the changes in the nature of these disturbances may impact the target species (Feng and Liang, 2020;Shen et al., 2020). However, the human-induced disturbances to the local breeding population have yet to be Normally, responses that are directly related to energy trade-offs such as fleeing and vigilance, are used as measures of an animal's fearfulness and are considered to indicate varying levels of habituation (Frid and Dill, 2002;Blumstein et al., 2003). ...
... However, the human-induced disturbances to the local breeding population have yet to be Normally, responses that are directly related to energy trade-offs such as fleeing and vigilance, are used as measures of an animal's fearfulness and are considered to indicate varying levels of habituation (Frid and Dill, 2002;Blumstein et al., 2003). These responses have often been evaluated by monitoring behavioral budgets (particularly the alert time (AT); French et al., 2019;Santiago et al., 2020) or by measuring the flight initiation distance (FID), i.e., the distance between predator and prey when prey start to flee (Feng et al., 2020;Zhou and Liang, 2020). These responses are presumed to be costly, and non-benign consequences of human disturbance have been observed in many species (Lazarus, 2003;Inger et al., 2006). ...
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Human proximity often has negative consequences for wildlife. In response to human disturbance, animals may display a variety of potentially costly behavioural responses, such as vigilance or flight, which were often used as measures of fearfulness and to indicate varying habituation levels. With rapid human development, the globally endangered Scaly-sided Merganser (Mergus squamatus) may be vulnerable to anthropogenic interference. However, human-induced disturbances to a local breeding population have not been quantified. In this study, we tested how flight initiation distance (FID) and behavioural budget (alert time (AT) in particular) changes in relation to human presence in this species in Changbai Mountain, China. The results showed that individuals who experienced greater levels of human disturbance had shorter FIDs, which indicate that the local population may be habituated to human approach. However, this species spent more time being vigilant in its behavioral budget, which suggested that some other human-induced stimuli may impose negative effects on the species. This study will allow managers to better understand the response of this endangered species to different human-induced disturbances and provided scientific basis for local wildlife managers to establish buffer distance for SSME in Changbai Mountain.
... 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). ...
War influences wildlife in a variety of ways but may influence their escape responses to approaching threats, including humans, because of its effect on human populations and behavior and landscape change. We collected 1,400 flight initiation distances (FIDs) from 157 bird species in the dry zone of Sri Lanka, where civil war raged for 26 years, ending in 2009. Accounting for factors known to influence FIDs (phylogeny, starting distance of approaches, body mass, prevailing human density, group size, and location), we found that birds have longer FIDs in the part of the dry zone that experienced civil war. Larger birds-often preferred by human hunters-showed greater increases in FID in the war zone, consistent with the idea that war was associated with greater hunting pressure and that larger birds experienced longer-lasting trauma or had more plastic escape behavior than smaller species. While the mechanisms linking the war and avian escape responses remain ambiguous, wars evidently leave legacies that extend to behavioral responses in birds.
... 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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Human disturbance is caused by the anthropogenic activities in the environment. While human threat to wildlife is considered to be complex (nonlethal recreations and lethal hunting activities). To date, there has been few studies that focus on nest defense behavior of animals to human disturbance. In this study, we tested whether the behavioral response of Oriental reed warblers Acrocephalus orientalis against a human intruder are similar to other nest intruders. We used dummies of common cuckoo Cuculus canorus (the parasite), Eurasian sparrowhawk Accipiter nisus (the predator), Oriental turtle dove Streptopelia orientalis (the neutral control), also a human intruder to induce the nest defense behaviors and alarm calls of Oriental reed warblers. Our results showed that Oriental reed warblers performed less intense nest defense behavior and uttered the least number of calls and shortest duration of calls to a human intruder than those to other nest intruders, suggesting that human pose a low threat level to warblers. Warblers produced different number and duration of alarm calls against the cuckoos, sparrowhawks and doves, even though they performed similar behavioral responses to the three types of avian intruder, indicating that they could distinguish the three types of avian intruders. The present study provided experimental evidence for the different behavioral responses between human disturbance and other types of intruders and suggested that the less intense behavioral response to human disturbance may be the result of habituation.
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I outline how understanding the mechanism of behavioural plasticity is important for predicting how organisms will respond to rapidly changing and novel environments. I define two major forms of behavioural plasticity: developmental and activational. Developmental plasticity refers to the capacity of a genotype to adopt different developmental trajectories in different environments. Activational plasticity refers to differential activation of an underlying network in different environments such that an individual expresses various phenotypes throughout their lifetime. I suggest that the costs and benefits of these two forms of behavioural plasticity may differ: developmental plasticity is slow, but results in a wider range of more integrated responses. Furthermore, the neural costs associated with activational plasticity may be greater because large neural networks must be maintained past an initial sampling and learning phase. While the benefits of plasticity are realized in variable environments, I argue that fine-grained and coarse-grained variation may differentially select for activational and developmental plasticity, respectively. Because environmental variation experienced by an organism is largely determined by behaviour, developmental plasticity may still evolve in fine-grained environments if niche choice results in coarse-grained 'realized' variation. Behavioural plasticity should impact evolution in novel environments because it increases the chances of survival in these environments. Developmental behavioural plasticity may be particularly important for diversification in novel environments because it can impact not only survival, but also the development of signals and preferences important in mate choice. Future areas of research on behavioural plasticity and rapid environmental change include stress as a mechanism underlying rapid integrated responses and life history perspectives on predicting developmental versus evolutionary responses.
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Numerous species have adapted to humans, especially invasive species associated with humans in towns and cities. Short flight distances of populations adapted to urban environments reflect changes in behavior and physiology, reflecting phenotypic plasticity or evolution. Here, I tested the hypothesis that the decrease in flight distance to a potential predator (an approaching human) reflected adaptation to urbanization, using a data set of flight distances of 44 common species of European birds in different stages of adaptation to urban environments. Urban populations had consistently shorter flight distances than rural populations of the same species. Variation in relative flight distance of urban populations was predicted by the number of generations since urbanization, as expected by a gradual process of adaptation. Furthermore, species with relatively large populations in urban environments would be an indication of local adaptation to urban environments. Relative flight distance of urban population was shorter for species with large populations in urban compared to rural habitats. Species that had adapted to urban environments as shown by short flight distances were less susceptible to predation by the European sparrowhawk Accipiter nisus than species with relatively long flight distances in urban populations. These findings provide evidence consistent with the hypothesis that recent changes in the tameness of urban birds, as reflected by their relatively short flight distances, is an adaptation to the novel urban environment.
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In group-living animals, it is adaptive to recognize conspecifics on the basis of familiarity or group membership as it allows association with preferred social partners and avoidance of competitors. However, animals do not only associate with conspecifics but also with heterospecifics, for example in mixed-species flocks. Consequently, between-species recognition, based either on familiarity or even individual recognition, is likely to be beneficial. The extent to which animals can distinguish between familiar and unfamiliar heterospecifics is currently unclear. In the present study, we investigated the ability of eight carrion crows to differentiate between the voices and calls of familiar and unfamiliar humans and jackdaws. The crows responded significantly more often to unfamiliar than familiar human playbacks and, conversely, responded more to familiar than unfamiliar jackdaw calls. Our results provide the first evidence that birds can discriminate between familiar and unfamiliar heterospecific individuals using auditory stimuli.
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While many domestic and laboratory animals recognize familiar humans, such ability in wild animals is only anecdotally known. Here we demonstrate experimentally that a cognitively advanced, social bird, the American crow, Corvus brachyrhynchos, quickly and accurately learns to recognize the face of a dangerous person and continues to do so for at least 2.7 years. We exposed wild crows to a novel ‘dangerous face’ by wearing a unique face mask as we trapped, banded and released 7–15 birds at five sites near Seattle, WA, U.S.A. After trapping, crows consistently used harsh vocalizations to scold and mob people of different sizes, ages, genders and walking gaits who wore the dangerous mask, even when they were in crowds. In contrast, prior to trapping, few crows scolded people who wore the dangerous mask. Furthermore, after trapping, few crows scolded trappers who wore no mask or who wore a mask that had not been worn during trapping. In a fully crossed, balanced experiment in which each site had a unique trapping (dangerous) mask and five neutral masks, crows scolded and mobbed a mask more when it was the dangerous mask at that site than when it was a neutral mask at another site. When simultaneously presented with a person in the dangerous mask and a person in the neutral mask, crows typically ignored the neutral mask and followed and scolded the person wearing the dangerous mask. Risky, aggressive scolding by crows was sensitive to variable costs across study sites; aggression was less where people persecuted crows most. We suggest that conditioned and observational learning of specific threats may allow local bird behaviours to include aversions to individual people.
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Male and female zebra finches are affected by the colour of plastic leg bands worn by opposite-sex conspecifics. They find certain colours more attractive, and others less attractive, than the natural unbanded condition. Females prefer red-banded males over unbanded ones, and avoid light-blue and light-green banded males. Males prefer black and pink banded females and avoid those wearing light-blue or light-green bands. These findings may have utility for the study of mate choice in monogramous species; they also raise important questions about a widely used experimental technique.
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Individuals face evolutionary trade-offs between the acquisition of costly but accurate information gained firsthand and the use of inexpensive but possibly less reliable social information. American crows (Corvus brachyrhynchos) use both sources of information to learn the facial features of a dangerous person. We exposed wild crows to a novel 'dangerous face' by wearing a unique mask as we trapped, banded and released 7-15 birds at five study sites near Seattle, WA, USA. An immediate scolding response to the dangerous mask after trapping by previously captured crows demonstrates individual learning, while an immediate response by crows that were not captured probably represents conditioning to the trapping scene by the mob of birds that assembled during the capture. Later recognition of dangerous masks by lone crows that were never captured is consistent with horizontal social learning. Independent scolding by young crows, whose parents had conditioned them to scold the dangerous mask, demonstrates vertical social learning. Crows that directly experienced trapping later discriminated among dangerous and neutral masks more precisely than did crows that learned through social means. Learning enabled scolding to double in frequency and spread at least 1.2 km from the place of origin over a 5 year period at one site.
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Recognition of a particular individual occurs when we reactivate links between current perceptual inputs and the previously formed representation of that person. This recognition can be achieved by identifying, separately or simultaneously, distinct elements such as the face, silhouette, or voice as belonging to one individual. In humans, those different cues are linked into one complex conceptual representation of individual identity. Here we tested whether rhesus macaques (Macaca mulatta) also have a cognitive representation of identity by evaluating whether they exhibit cross-modal individual recognition. Further, we assessed individual recognition of familiar conspecifics and familiar humans. In a free preferential looking time paradigm, we found that, for both species, monkeys spontaneously matched the faces of known individuals to their voices. This finding demonstrates that rhesus macaques possess a cross-modal cognitive representation of individuals that extends from conspecifics to humans, revealing the adaptive potential of identity recognition for individuals of socioecological relevance.
Human intrusion can be a serious problem for birds because it can cause displacement, prevent access to resources, and reduce reproduction and survival. The factors that influence avian tolerance to intrusion are poorly understood. We studied passerine responses to intrusion in Wyoming montane forests during the breeding season by using two indices of intrusion tolerance: detectability period, the amount of time that a bird remains near its initial flush point; and approach distance, how close one can get to a bird before it flushes. A solitary observer experimentally approached focal individuals and recorded detectability period, approach distance, the seasonal and daily timing of intrusion, number of nearby conspecifics, number of nearby heterospecific individuals, and surrounding vegetation conditions. Using data from the literature, we also assessed influences of migratory status, body mass, conspicuousness, and height above the ground at which species are active during the breeding season. Detectability period was significantly shorter, indicating intrusion tolerance was lower, when fewer conspecifics were nearby. Approach distance was significantly longer, indicating tolerance was lower, for more-conspicuous species and for species that are active closer to the ground. Effects of other variables studied were not significant. These results demonstrate that social and biological factors can influence tolerance to intrusion. Intrusion-induced behaviors such as nest abandonment and decreased nest attentiveness have led to reduced reproduction and survival in species that are intolerant of intrusion. With knowledge of factors that influence tolerance, the risk of disturbing birds that are sensitive to intrusion could be reduced.
In this report we describe a method of examining the tolerance of birds to humans, namely by measuring the distance to which birds will allow a person to approach them before flying off (flush distance). We studied the tolerance of Indian birds to approaching people by recording the flush distance for 925 individuals of 138 species of residents (birds breeding in India) and migrants (birds that are not known to breed in India). Over 20% of the variance in flush distance was accounted for by the number of people situated within 50 m, the distance to the closest person, the bird's migratory status, the number of people approaching, the time of day, and the bird's total body-length (including tail). For migratory species, 43% of the variability in flush distance was accounted for by distance to the closest other person, time of day, number of people originally within 50 m, number of people approaching, flock size, and species size. For resident species, only 18% of the variance was accounted for by distance to the closest other person, number of people within 50 m, and number of people approaching. Migrants were thus more responsive to the effect of humans, and their response was also influenced by their own size (body length) and flock size. Migratory species were less tolerant of people, flushing sooner than residents, and being more sensitive to the number of approaching people. We suggest that resident birds in North India have become habituated to the non-violent protective behaviour of the Hindu people towards birds, whereas migrants from farther north are more wary. Alternatively migrants, being less familiar than residents with the local predators and hiding places, may be more wary than residents on their home territory. Enhanced wariness results in more time spent alert or fleeing, with resultant greater energy-demand and decreased time for feeding.
When approached by humans, virtually all species flee, but we lack an understanding of the factors that influence flight response among species. Understanding this variation may allow us to understand how ‘fear’ structures communities, as well as to predict which species are likely to coexist with humans. I used flight initiation distance (FID) as a comparative metric of wariness and examined the relative importance of life history and natural history traits in explaining variation in FID in 150 species of birds. In a series of comparative analyses, I used independent contrasts to control for phylogenetic similarity and regressed continuous life history traits against flight initiation distance. Body size had a large and significant effect in explaining variation in flightiness: larger species initiated flight at greater distances than smaller species. After controlling for variation explained by body size, there was a nonsignificant positive relation between the age of first reproduction and FID. There were no relations between FID and clutch size, number of days spent feeding young, longevity, or habitat density. I used concentrated changes tests to look for evidence of coevolution between flightiness and dichotomous traits. Flightiness evolved multiple times and some clades were flightier than others. Flightiness was more likely to evolve in omnivorous/carnivorous species and in cooperatively breeding species. These results suggest that body size and age of first reproduction are important in explaining variation in disturbance tolerance in birds, and that species that capture live prey and those that are highly social are relatively wary. The results suggest a novel mechanism of how anthropogenic disturbance may contribute to extinction.