Behavioral Ecology
doi:10.1093/beheco/ars163
Advance Access publication 17 October 2012
Original Article
Tropical birds take small risks
Anders Pape Møllera and Wei Liangb
aLaboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment
362, F-91405 Orsay Cedex, France and bMinistry of Education Key Laboratory for Tropical Plant and
Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou 571158, People’s Republic
of China
The life history of tropical birds differs from that of their temperate counterparts by late start of reproduction, small clutch
sizes, and high rates of adult survival. Thus, tropical species should have greater residual reproductive value than temperate
species. Therefore, tropical birds can be predicted to take smaller risks than closely related temperate birds in order not to jeopardize their prospects of survival, which is the single most important component of fitness, and which is greater in tropical than
in temperate species. We estimated flight distances as a measure of risk-taking behavior of common species of birds for populations living in tropical areas in China (mainly Hainan) and in temperate Europe (mainly Denmark and France), predicting that
flight distances should be longer in tropical than in temperate populations, and that the difference in flight distance between
these 2 environments should be positively correlated with the difference in clutch size. Mean flight distance was more than twice
as large in tropical compared with temperate populations for 25 pairs of taxa. The difference in flight distance between tropical
and temperate taxa decreased with the difference in clutch size between the 2 environments. These findings are consistent with
the hypothesis that tropical birds take smaller risks than closely related temperate taxa to minimize the risk of early death due to
predation. Key words: birds, clutch size, flight distance, life history, risk-taking, tropics. [Behav Ecol]
Introduction
T
he life histories of tropical animals differ from those of
other climate zones by older age of first reproduction,
lower annual reproductive rates, and higher annual rates of
adult survival (Skutch 1976; Johnston et al. 1997; Ghalambor
and Martin 2001; Peach et al. 2001). Although there is considerable heterogeneity in life history among tropical species,
there are some striking contrasts with species from the temperate zone. Among tropical species, close relatives may differ
considerably in adult survival rate with some tropical passerines having annual survival rates in excess of 90%, when their
temperate relatives only survive with a probability of 50% or
less (e.g., Peach et al. 2001).
There is a long history of the relative importance of predation being greater in tropical than in temperate climate
zones, whereas the reverse applies to abiotic factors, dating
back to Darwin (1871) and Wallace (1889). Schemske et al.
(2009) recently reviewed the literature on latitudinal gradients in interspecific interactions, reporting a lack of studies
of latitudinal gradients in antipredator behavior. The underlying ecological factors accounting for differences in life history between the tropics and the temperate zone range from
weather-induced mortality in the temperate zone (Ashmole
1963; Newton 1998), and food and food availability (Skutch
1949; Lack 1954), predation and risk of predation (Slagsvold
1982; Skutch 1985; Ghalambor and Martin 2001), and parasites and disease (Moreau 1944; Guégan et al. 2003; Guernier
et al. 2004). Predation and risk of predation are known to
strongly affect life history either through direct or indirect
Address correspondence to A.P. Møller. E-mail: anders.moller@
u-psud.fr.
Received 16 May 2012; revised 30 August 2012; accepted 1
September 2012.
© The Author 2012. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
effects. These effects include smaller clutches, smaller eggs,
shorter time to relaying, and higher frequency of relaying in
the presence of predation (e.g., Slagsvold 1982; Zanette et al.
2011). Ghalambor and Martin (2001) have shown that parent
birds in South America reduce their nest visits less often than
closely related species in North America, when a nest predator is presented near the nest. The opposite applies when
a predator of adults is presented near the nest, with adults
reducing feeding rates the most in South America, suggesting that South American species reduced their mortality risk
to themselves more than phylogenetically and ecologically
similar North American species, even when this imposed a
cost on their offspring. In contrast, North American species
reduced the risk to their offspring even when imposing a risk
to themselves (Ghalambor and Martin 2001). Independent
of the causes of these differences in life history, many tropical species have very high adult survival rates suggesting that
individuals of such species adopt risk-aversive strategies to
ensure survival. Thus, these findings can be extended to the
nonbreeding season and to nonbreeding contexts during
the breeding season because species with slow life histories
should on average take small risks not to jeopardize their own
probability of survival.
The response of animals to the approach of a potential
predator is vigilance and/or flight (Ydenberg and Dill 1986).
Flight distance is defined as the distance at which an individual
moves away from an approaching predator, typically a human
(Burger and Gochfeld 1991a, 1991b; Fernández-Juricic et al.
2001, 2002; Blumstein 2003), because animals are supposed
to perceive humans as potential predators (Frid and Dill
2002). Animals have to balance the costs and benefits from
staying put against the costs and benefits of fleeing. Staying
put may further increase the risk of death and hence reduce
future reproductive success, whereas fleeing prematurely
will increase the metabolic cost, but also reduce food intake.
As an example, short flights by small birds can increase the
268
metabolic cost more than 20-fold (Tatner and Bryant 1986),
implying that individuals that fly away when an approaching
predator is still far away will pay the cost of false negatives.
Thus, any individual will continuously have to weigh these
costs and benefits in order to optimize its fitness, resulting in
a difference in this trade-off between taxa living in temperate
and tropical climatic zones.
The concept of risk-taking also implies that flight initiation
distance (the distance at which an individual takes flight when
approached by a potential predator; FID) is correlated with
risk of predation, that is, that an individual indeed incurs a
fitness cost by taking greater risks. Møller et al. (2008) tested
this underlying assumption using FID of common passerine
birds and risk of being killed by a sparrowhawk Accipiter nisus.
Across the range of FID from means of 5–50 m, the risk of
predation relative to the expectation based on the abundance
of different prey species increased from predation being 100
times less frequent than expected by chance to almost 100
times more common than expected by chance. Likewise,
Møller et al. (2010) showed that susceptibility to cat predation was negatively related to flight distance of male birds
when singing. Finally, Møller et al. (2011) showed that birds
with shorter flight distance for their body size were more
likely to be hit by a car than expected from their abundance.
Therefore, there is evidence suggesting that FID and flight
reactions are under current selection due to predation.
FID is an estimate of the risk that an individual is willing to
take given its state. Residual reproductive value is defined as
the remaining contribution of survival and reproductive success for an individual of a given age (Roff 2002). Given that
the future fitness contribution of an individual is a function
of its likelihood of survival and future reproductive success,
and given that FID should be optimized to maximize survival and reproduction, we should expect FID to reflect the
residual reproductive value of an individual. Therefore, we
can predict from life-history theory the observable differences
in risk-taking for different categories of individuals, be it sex,
age, or experience. In addition, we should expect FID to be
correlated with life history. Indeed, comparative analyses of
birds have shown that mean and variance of FID is correlated with components of life history. Møller and Garamszegi
(2012) have shown for European birds that species with relatively longer FID started their reproduction at older age and
had lower annual fecundity and higher adult survival rate
than species with shorter FID. In addition, bird species with
more variable FID start to reproduce earlier, have higher
annual fecundity, senesce faster, and have a longer breeding
season. These effects were all independent of body mass and
similarity among taxa due to common phylogenetic descent.
Thus, FID as a measure of risk-taking provides reliable information about a whole suite of life-history traits. Finally, individual birds are highly consistent in their flight distance
independent of the context as shown by studies of repeatability of flight distance (Carrete and Tella 2010; Møller 2010;
Møller and Garamszegi 2012) suggesting that flight distance
represents an inherent component of personality (Møller
and Garamszegi 2012). Thus, there is no evidence of habituation to human proximity in terms of flight distances being
reduced when the frequency of human encounters increases.
The objectives of this study were to test whether tropical
populations of birds take smaller risks when confronted with an
approaching potential predator than populations of the same
species or closely related species in the temperate zone. This
study extends the work by Ghalambor and Martin (2001) by
testing whether adult birds, even when not reproducing, take
smaller risks in the tropics than in the temperate zone. We did
so by estimating flight distances of common birds in China
(Hainan) and Europe (Denmark and France). We exploited
Behavioral Ecology
the fact that many species that are widely distributed in the
Palearctic zoogeographical region reach the tropics in southern
China (MacKinnon and Phillipps 1999), thereby allowing comparison between populations of the same species living in very
different climatic zones. In addition, we obtained information
on clutch size in Europe and China, predicting that the difference in clutch size should predict the difference in risk-taking
between climate zones. Finally, we tested if flight distance of the
same species in a national park with little or no human disturbance was shorter than the flight distance in areas inhabited
by humans, assuming that birds in inhabited areas would have
been selected to have long flight distances due to hunting and
other forms of prosecution.
Materials and methods
Study areas
We recorded FID of common birds in tropical areas in China
and in temperate areas in Europe. More than 70% of all data
from China were collected in the Diaoluoshan National Forest
Park (18°43′N, 109°52′E) during February 2011, which is during the breeding season with many residents already building
nests, laying eggs, or feeding young. This national park, consisting of pristine tropical forest with the exception of secondary
forest at the edges, has an area of 380 km2, although the data
were collected in the surroundings of the main buildings of the
national park located far away from the edge where intruders
are most likely. Annual rainfall is 1870–2760 mm and average
annual temperature 24.4 ºC. Although national parks may suffer from human exploitation, we did not encounter any locals
except for a handful of tourists during our visit. Furthermore,
none of the species that we studied is known to be consumed
in the area. In addition, we collected flight distances for birds
in nearby Sanya (18°15′N, 109°30′E) and adjoining villages.
Again, we found little evidence of exploitation of local birds,
with barn swallows Hirundo rustica and tree sparrows Passer montanus breeding in many houses. W.L. and his students collected
the remainder of the data in Haikou City (20°02′N, 110°20′E),
Hainan Island, Tongguling National Nature Reserve (19°36′N,
110°57′E), Hainan Island, and Dongguan City (23°02′N,
113°43′E), Guangdong Province, China.
Likewise, we collected information on FID in Northern
Denmark (mainly around the town Brønderslev [57°12′N,
10°00′E] and nearby rural areas) and Ile-de-France, France
(mainly around the city Orsay [48°04′N, 2°11′E] and nearby
rural areas) during February–September 2006–2012 (see
Møller and Garamszegi 2012 for further details). We avoided
inclusion of the same individual more than once by restricting
observations in a given location to a single individual of
each of the 2 sexes. More than 95% of all data from China
and 100% of all data from Europe were collected by A.P.M.
We reached very similar conclusions when we excluded the
data for the 3 species collected by W.L. and his students,
demonstrating that there was no bias in the data due to data
being collected by different observers.
Flight distances
All flight distance data were collected from birds during the
breeding season, although all birds observed near nests or
dependent fledglings were excluded to avoid that flight distance behavior reflects reproductive effort. We estimated FID
using a technique modified from that developed by Blumstein
(2006). In brief, when an individual bird had been located
with a pair of binoculars, the observer, while looking at the
bird, moved at a normal walking speed toward the individual,
while recording the number of steps (which approximately
269
Møller and Liang • Risk-taking in tropical birds
equals the number of meters, Møller et al. 2008). The distance at which the individual took flight was defined as FID,
whereas the starting distance was the distance from where
the observer started walking up to the position of the bird.
If the individual was positioned in the vegetation, the height
above ground was recorded to the nearest meter. FID was estimated as the Euclidian distance that equals the square root of
the sum of the squared horizontal distance and the squared
height above ground level (Blumstein 2006):
FID = √(Horizontal distance2) + (Height2).
A full description of different cross-validations of the data
between observers, seasons, years, and areas is reported by
Møller (2008a, 2008b, 2008c). The cross-validations showed
that estimates of FID are consistent when comparing data
published by Blumstein (2006) and unpublished data for
the same species by A.P.M., with the cross-validation explaining 78% of the variance. Likewise, when comparing estimates
based on 2 observers in the same site (E. Flensted-Jensen
and A.P.M.), the cross-validation explained 79% of the variance. Furthermore, when comparing estimates from different
countries (A.P.M.), the cross-validation explained 81% of the
variance, and when comparing estimates from different years
(A.P.M.), it explained 90% of the variance (Møller 2008a,
2008b, 2008c).
Previous studies have shown that starting distance (the distance at which an individual is first approached) is strongly
positively correlated with FID (e.g. Blumstein 2003, 2006),
thereby causing a problem of collinearity. We eliminated this
problem by searching habitats for birds with a pair of binoculars when choosing an individual for estimating FID, only
choosing individuals that were located a minimum of 30 m
from the observer. In this way, we assured that most individuals were approached from a distance of at least 30 m, thereby
keeping starting distances constant across species. FID was
weakly negatively related to starting distance in a model that
included species, age, habitat, country, and body mass as factors (partial F1,4188 = 37.97, P < 0.0001), explaining only 1%
of the variance. None of the results presented here changed
statistically when including starting distance as an additional
variable, and we thus excluded this variable from all subsequent analyses for simplicity.
Variation in FID among years was negligible, accounting for
0.7% of the variance in a model that also included species,
habitat (urban or rural), and country as additional predictor
variables (partial effect of year: F2,3971 = 30.44, P < 0.001). In
contrast, species accounted for 57.5% of the variance (partial
effect of species: F132,3971 = 45.51, P < 0.001), justifying the use
of mean FID for species as the measure of behavior.
Analyses
We log10-transformed mean and variance in FID before
analyses.
We used a pairwise comparative approach to test the predictions relying on values for sister taxa (Møller and Birkhead
1992). The logic behind sister taxa comparisons is that most
phenotypic traits are the same for each pair of taxa because
they share most of their evolutionary past from phylogenetic descent, with only the recent past since the 2 taxa split
accounting for independent evolution. In addition, pairwise
comparisons are particularly powerful because such comparisons will account not only for known confounding variables
(because the 2 taxa of a pair are generally similar with respect
to a given confounding variable) but, most importantly, also,
because each pair of taxa are similar for variables that have
not yet been identified as confounding a comparison. We
used the phylogeny reported by Davis (2008) for identification of pairs of closely related species.
Comparative analyses can be strongly affected by sampling
effort, and Garamszegi and Møller (2010) showed recently
that the effect of sample size in comparative analyses was as
great as the effect of similarity due to common phylogenetic
descent. Exclusion of species with small sample sizes will
result in exclusion of rare species, when inclusion of such
species may increase the scope of generalization beyond common and abundant species (Garamszegi and Møller 2012).
Hence, it is important to address problems of heterogeneity in sampling effort although this is rarely done in behavioral ecology or evolutionary biology studies. Heterogeneity
in sampling effort cannot be addressed by including sample
size as an additional predictor variable, but requires that
each observation contributes to test statistics relative to its
importance through weighting procedures. Most statistical
approaches assume that all data points provide equally precise information about the deterministic part of total process
variation, that is, the standard deviation (SD) of the error
term is constant over all values of the predictor variables
(Sokal and Rohlf 1995). We weighted each observation (difference in mean FID or SD in FID) by sample size in order
to use all data in an unbiased fashion, thereby giving each
datum a weight that reflects its degree of precision due to
sampling effort (Draper and Smith 1981; Neter et al. 1996).
If the analyses were made by relating log-transformed mean
FID (or log-transformed SD in FID) as the response variable
and species pair and region (China or Europe) weighted by
sample size for each population as predictors, the conclusions
remained unchanged.
Results
Clutch size
Summary statistics
We used our data on clutch size reported by Cramp and
Perrins (1977–1994) and Glutz von Blotzheim and Bauer
(1985–1997) for Europe and Wu (1986), Zhao (2001), and
W.L. for China. For species from China we relied on the most
common clutch size reported in handbooks as an estimate of
mean clutch size. Therefore, the precision of clutch size estimates is likely to differ between China and Europe. However,
there is no reason to believe that this will cause any systematic bias in the statistical tests because the null hypothesis still
predicts that the difference in clutch size between China and
Europe is zero independent of the estimation methods.
The data set is reported in the Electronic Supplementary
Material Table S1, and the data on FID from within and
outside a national park are reported in the Electronic
Supplementary Material Table S2.
Summary statistics for means and SD in flight distances are
reported in Table 1. Mean FID for China was twice as long as
mean FID for Europe, which amounted to a highly significant
difference (Figure 1 and Table 1). A similar conclusion was
reached if we restricted the analyses to different populations
of the same species (t = −8.27, degrees of freedom [df] = 10,
P < 0.0001). There was a significant difference in SD in
FID, with the mean SD being 70% larger in China than in
Europe (Table 1). There was also a significant difference if
we only compared different populations of the same species
(t = −3.02, df = 10, P = 0.013).
Mean clutch size was significantly larger in Europe than in
China, with the mean difference exceeding 20% (Table 1).
This difference was also significant when only comparing populations of the same species (t = −4.18, df = 10, P = 0.0019).
270
Behavioral Ecology
Table 1 Mean and standard errors of mean and SD of FID (m) for pairs of
populations of birds in the temperate and the tropical zone
Variable
Temperate
zone
Tropical zone
t
P
Mean FID
Range in means
SD FID
Range in SD
N
Clutch size
N
7.7 (0.5)
5.0–24.4
4.3 (0.4)
0.5–12.7
25
4.93 (0.15)
21
15.6 (2.1)
7.2–82.5
7.3 (1.7)
2.8–39.2
25
4.05 (0.11)
21
−13.39
<0.0001
−4.64
<0.0001
6.48
<0.0001
N is the number of populations and t and P are test statistics for paired
t-tests based on log10-transformed values.
only comparing different populations of the same species
(F = 5.70, df = 1,9, r2 = 0.39, P = 0.0083, slope [standard error,
SE] = −1.432 [0.600]).
Flight distance in areas with and without human inhabitants
We were able to obtain FID estimates for 9 species from the
Tongguling National Park and from nearby inhabited areas
in Sanya, Hainan. Neither mean FID nor SD in FID differed
significantly between these 2 types of habitats in a paired test
(mean [SE] for park: 19.77 m [4.11], outside park: 11.27
[1.78]; SD [SE] for park: 15.86 [6.44], outside park: 5.65
[0.68], paired t-test based on log10-transformed data: mean:
t = −1.89, df = 8, P = 0.10; SD: t = −1.28, df = 8, P = 0.24). These
conclusions were unaltered in tests that were not weighted by
sample size (mean: t = −1.21, df = 8, P = 0.26; SD: t = −0.26,
df = 8, P = 0.80) and in nonparametric Wilcoxon matchedpairs tests (mean: S = −8.50, P = 0.36; SD: S = −2.50, P = 0.82).
Flight distance and clutch size
Difference in mean FID between China and Europe was negatively correlated with difference in mean clutch size between
China and Europe (Figure 2). This relationship accounted
for 31% of the variance and hence represented a large effect
(F = 8.67, df = 1,19, r2 = 0.31, P = 0.0083, slope [SE] = −0.199
[0.068]). There was also a significant relationship when
Figure 1 Mean (SE) flight initiation distance (m) for populations of birds
from the temperate and tropical zones. The line is Y = X.
Figure 2 Difference in flight distance between populations of birds from
the tropical and the temperate zones in relation to difference in
clutch size between populations of birds from the tropical and the
temperate zones.
Discussion
The main findings of this study of risk-taking as reflected by
FID of populations of common bird species from China and
Europe were that (1) FID were on average twice as long in
China as in Europe for populations of the same species or
populations of closely related species; (2) difference in logtransformed FID between China and Europe decreased with
difference in log-transformed clutch size between the 2 study
areas for populations of the same species or pairs of closely
related species; and (3) log-transformed FID for the same
species did not differ consistently in paired tests between populations in a national park and populations from inhabited
areas in tropical China.
We predicted that tropical populations of birds on average
would take much smaller risks than temperate conspecifics
or closely related heterospecifics, when confronted with a
potential predator. Indeed, this prediction was confirmed
by the finding that mean flight distance in Europe was only
half as long as that in China. We found a similar pattern in
comparisons based on populations of the same species and
in comparisons based on populations of the same or closely
related species, showing consistency in research findings.
These findings corroborate the ideas initially proposed
by Wallace (1889) suggesting that predation plays a much
greater role in tropical than in temperate climates, while the
opposite applies to abiotic causes of death. Birds in China
may have been prosecuted as pests or captured for use as pets
or food more often than birds in Europe. For example, Mao
Zedong initiated in 1958 an attempt to exterminate sparrows
throughout China (http://en.wikipedia.org/wiki/Four_
Pests_Campaign). Such human activities would undoubtedly
select for longer flight distances, hence providing an
alternative explanation for the main result that we reported.
We explicitly tested if flight distance was affected by human
presence by comparing mean flight distance estimates
obtained from national parks and from nearby inhabited
areas with continuous presence of humans. This comparison
did not reveal any consistent difference in mean or SD in
flight distance. We also note that none of the species that we
studied were a preferred source of meat making it unlikely
that flight distances would reflect persecution. Finally, flight
distance is independent of whether a species is hunted or
not once differences in body size have been accounted for
(Møller 2008c, p. 1309). Alternatively, we could expect that
flight distances actually would decrease in inhabited areas
because frequent encounters between birds and humans
would select for shorter flight distances to save energy caused
271
Møller and Liang • Risk-taking in tropical birds
by flight when a bird is approached by a human. Furthermore,
humans may provide a refuge for birds from predators, which
generally have much longer flight distances than their prey
(Møller 2012a), and differences in predator community
between urban and rural habitats is a likely explanation for
differences in antipredator behavior (Møller et al. 2008;
Møller and Ibáñez-Álamo 2012). Indeed, urban birds have
much shorter flight distances than rural conspecifics (Cooke
1980; Møller 2008a, 2012b), and the difference in flight
distance increases with time since urbanization (Møller
2008a). These differences are not due to habituation because
individuals are highly consistent in their flight distance
among contexts (Carrete and Tella 2010; Møller 2010; Møller
and Garamszegi 2012). If this hypothesis were correct, we
would expect longer flight distances in the national park
than in the nearby agricultural and urban habitats. That was
not the case either. Hence, there was no empirical evidence
suggesting that the comparison in flight distance between the
temperate and the tropical zones could be accounted for by
differences in human presence.
If flight distances vary consistently between environments,
and if flight distances constitute behavioral means of reducing the risk of predation, as already shown (Møller et al.
2008, 2010, 2011), then we should expect physiological and
morphological adaptations to improve the efficiency of such
behavior. Indeed, Møller (2009a) has reported that basal
metabolic rate is greater in species with long flight distances,
allowing such species to take flight earlier than others, and
Møller et al. (unpublished data) have shown that bird species
with long flight distances for their body size had large wing
areas and large aspect ratios. An alternative proximate explanation for the findings reported here is that the effectiveness of flight at reducing the risk of predation varies between
temperate and tropical zones, with this effectiveness being
greater in temperate zones. If that was the case, we should
expect selection for greater flight ability and maneuverability in the tropics, where predation pressure is expected to be
the greatest (Darwin 1871; Wallace 1889). We are only aware
of a single study addressing this question. Data on wing loading and aspect ratio in different populations of barn swallows
H. rustica show the opposite pattern, with larger wing areas
and hence smaller wing loadings and large aspect ratios at
high latitudes (Møller et al. 1995). Hence, this alternative is
not supported by available data.
If life history was the underlying basis for changes in flight
distance, we should be able to demonstrate differences in
flight distance between tropical and temperate zones being
correlated with differences in life history. Indeed we have
shown here that this was the case for clutch size. This finding is consistent with the hypothesis that flight distance is
adjusted to life history, and that flight distance can be considered an integral behavioral measure of this life history.
These findings extend the study by Ghalambor and Martin
(2001) by showing that, not only in the reproductive tradeoff between risk avoidance for self and parental care but also
between risk avoidance for offspring and parental care, birds
living in environments that favor late start of reproduction,
low rates of reproduction, and high rates of survival will be
selected to take small risks independent of whether they are
reproducing or not. We should expect similar relationships
between difference in adult survival rate between China and
Europe and difference in flight distance. Unfortunately, we
do not have sufficient survival data from China to make such
a test.
This study has a number of implications for future studies. First, we predict for intraspecific studies that residual
reproductive value will be greater in China than in Europe,
and individuals with higher residual reproductive value will
take smaller risks in both China and Europe. Second, the
much greater diversity of the predator community in China
compared with Europe (Cramp and Perrins 1977–1994;
MacKinnon and Phillipps 1999) raises questions about the
degree of specialization in terms of antipredator behavior
in the 2 environments. We already know that many different
components of antipredator behavior covary and change in
response to changes in the predator community, as shown in
comparisons of antipredator behavior in nearby urban and
rural habitats (Møller and Ibáñez-Álamo 2012). It would be
interesting to test if such changes in antipredator behavior
between China and Europe are correlated with changes in
flight distance.
In conclusion, we have shown consistent differences in
flight distance between sister taxa of birds in the tropics and
the temperate zones with the former taking much smaller
risks than the latter. These differences in flight distance could
be accounted for by differences in life history implying that it
is differences in life history that are driving behavioral differences in risk-taking behavior. These findings could be further
tested by comparing survival rates as reflected by age ratios of
birds from the 2 areas, with the prediction that differences in
flight distance should be correlated with differences in age
ratios. They may also have conservation implications with
tropical birds being more prone to disturbance than temperate zone birds.
Supplementary material
Supplementary material can be found at http://www.beheco.
oxfordjournals.org/.
Funding
No funding was acquired for this study.
We thank C. Yang, Y. Cai, L. Wang, and T. Su for assistance with data
collection in the field. Funding was provided by the National Natural
Science Foundation of China (No. 31071938 to WL) and Program
for New Century Excellent Talents in University (NCET-10-0111 to
WL) D. Blumstein and an anonymous reviewer provided constructive
criticism.
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