Behavioral Ecology
doi:10.1093/beheco/arr168
Advance Access publication 4 November 2011
Original Article
Mechanisms underlying small-scale partial
migration of a subtropical owl
Mei-Ling Bai, Lucia Liu Severinghaus, and Mark Todd Philippart
Biodiversity Research Center, Academia Sinica, 128 Academia Road, Section 2, Nankang, Taipei 115,
Taiwan
Partially migratory populations provide excellent opportunities to study why animals migrate. Three hypotheses have been
proposed to explain the variations in individual migratory decisions: the body-size hypothesis, the arrival-time hypothesis, and
the dominance hypothesis. These hypotheses were developed for long-distance migrants breeding in the temperate region;
whether the same mechanisms affect small-scale partial migration in the subtropical zone remain to be examined. In this study,
we analyzed the condition dependence of the small-scale migratory behavior of Lanyu scops owl (Otus elegans botelensis) and
examined the costs and benefits of alternative strategies. We found that migrants gained more weight than residents during the
nonbreeding season. Resident males were more likely to breed the following year than migrant males, and resident females
were more likely to breed successfully than migrant females. Our results showed that male owls tended to be resident, supporting
the arrival-time hypothesis. The sexual difference in migratory tendency does not support the body-size hypothesis, which
predicts the lighter weighted male to be more migratory than the heavier females. Also, within the same sex, migratory tendency
was not related to body mass. The patterns that younger owls and nonbreeders were more migratory than older ones, and
breeders are consistent with the dominance hypothesis. However, Lanyu scops owl does not demonstrate winter food competition
as assumed by the dominance hypothesis. We propose that the difference in the probability of breeding between dominant and
subordinate owls lead to dominance-dependent partial migration. Key words: alternative strategy, arrival-time hypothesis, bodysize hypothesis, condition-dependent decision, dominance hypothesis, partial migration. [Behav Ecol 23:153–159 (2012)]
INTRODUCTION
igration, the seasonal movement between breeding and
nonbreeding areas (Berthold 2001), occurs over a wide
range of taxa and spatial scales (Dingle 1996). Migratory strategies may affect the fitness of individuals and influence the
dynamics of a population (Adriaensen and Dhondt 1990;
Morrissey et al. 2004), as well as alter the structure of communities and cause ecosystem-wide effects (Fryxell and Sinclair
1988; Winemiller and Jepsen 1998; Brodersen, Ådahl, et al.
2008). Partial migration, in which only a portion of a population is migratory, is considered a crucial step in the evolution
of migration by some authors (Bell 2000; Berthold 2001;
Salewski and Bruderer 2007). The coexistence of migratory
and nonmigratory individuals within a population provides an
opportunity to examine the traits related to migratory behavior as well as to analyze the costs and benefits of alternative
strategies.
The migratory behavior in a partially migratory population
can be either obligatory or facultative at the individual level.
For some species, the alternative migratory behavior is a genetically controlled dimorphism unchangeable through an individual’s lifetime (obligatory partial migration; Berthold and
Querner 1982; Biebach 1983). Although for most of the partially migratory species, the migratory behavior is an individual decision, which is often related to the attributes of the
individual, such as sex, age or dominance, or environmental
M
Address correspondence to L.L. Severinghaus. E-mail: zobbowl@
gate.sinica.edu.tw.
Received 2 November 2010; revised 13 May 2011; accepted 11
August 2011.
The Author 2011. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
conditions (facultative partial migration; Smith and Nilsson
1987; Chan 2005; Olsson et al. 2006; Brodersen, Nilsson,
et al. 2008; Ogonowski and Conway 2009). To explain how
such differential decisions arise, 3 hypotheses have been proposed (reviewed by Myers 1981; Ketterson and Nolan 1983;
Boyle 2008). The body-size hypothesis, or foraging-limitation
hypothesis (Boyle 2008), claims that larger and heavier individuals are more likely to remain in the breeding area due to
their ability to endure long periods of food deprivation. The
arrival-time hypothesis suggests that the sex experiencing
more intense intraspecific competition for territories, which
was usually priority dependent, should benefit by returning
earlier to the breeding ground and tend to be nonmigratory.
The dominance hypothesis predicts that subordinate individuals, usually younger ones, are more likely to migrate as they
are out-competed by dominants and forced to leave when
food is scarce. These 3 hypotheses are not mutually exclusive.
They emphasize different mechanisms to explain partial migration, namely, the ability to endure food deprivation, the
need to obtain breeding sites through early occupancy, and
the ability to compete for winter food.
To explain why different migratory strategies are maintained
in a population, one common approach was to analyze the condition dependence of the migratory behavior according to the
3 hypotheses above (e.g., Ketterson and Nolan 1983; Brodersen
et al. 2008; Boyle 2008). Another approach is to evaluate the
costs and benefits of alternative strategies, but existing literature on partial migration contained few empirical studies that
could evaluate the trade-off of different strategies (e.g., Gillis
et al. 2008). Although most studies deal with the longdistance, regional movement of organisms, migration, under
the broad definition of ‘‘the seasonal movement between
Behavioral Ecology
154
breeding and non-breeding areas’’ (Berthold 2001), do occur
locally at altitudinal dimension or at even smaller spatial
scales. Within tropical or subtropical zone, such small-scale
movements could be common but are often overlooked (Levey
and Stiles 1992; Poulin et al. 1993), and the mechanisms remain
poorly understood (Jahn et al. 2010).
We investigated the postbreeding season movement pattern
of the Lanyu scops owl (Otus elegans botelensis) on a subtropical
island. The owl is an insectivorous cavity-nesting species. It
forages in diverse habitats, and its potential prey (insects .
2 cm) is more abundant in edge habitat than in mature forests
throughout the year (Yang MM, unpublished data). However,
tree cavities used for breeding are largely confined to mature
forests, thus the owls aggregate to mature forests during the
breeding season (May to August). Adult owls exhibit high
breeding site fidelity and make breeding attempts in same forest patches every year. At the end of breeding season, some owls
leave the breeding area, whereas others remain (Severinghaus
2002). Their seasonal need for cavities, the uneven distribution
of cavity, as well as food resource on the island provide the
context for the seasonal movement of the owls in parallel to
partial migration. The relatively small scale of these movements
presents a system suitable for close monitoring.
According to the body-size hypothesis, male owls should be
more likely to migrate than females, as male Lanyu scops owls
are lighter than females. This hypothesis also predicts that,
within the same sex, lighter weighted individuals are more
likely to migrate than heavier ones at the end of the breeding
season. Male owls establish territories thorough intensive vocal contests and some fighting. Female contests were also
seen, but much less frequently than between-male contests.
According to the arrival-time hypothesis, female owls should
be more likely to migrate than males. The breeding opportunity of the population is limited by the availability of suitable
cavities (Severinghaus 2007). In a population with limited
breeding opportunities, breeding status usually reflects the
dominance rank of the individuals involved (Sutherland
1996). The owls are capable of breeding in the second year
of their life, but the probability of these birds breeding is
lower than that of older ones. Based on the dominance hypothesis, younger owls should be more likely to migrate than
older ones. The probability of breeding does not change further with age for birds 3 years and older, and about 30% of
this age group are nonbreeders each year (Severinghaus LL,
unpublished data). The dominance hypothesis also suggests
that nonbreeders should be more likely to migrate than
breeders among the older owls.
In this study, we examine the condition dependence of the
owls’ migratory behavior, by analyzing the relationships of an
owl’s migratory strategy with its age, sex, end-breeding-season
body mass, and its reproductive parameters of the year. We also
assess the costs and benefits of the strategies, including the
relationships of an owl’s migratory strategy with its January
body mass, its probability of survival, and its reproductive
parameters of the following year. With the outcome of the analyses, we evaluate whether the 3 hypotheses are applicable to
the small-scale partial migration of this subtropical bird.
excavating species; therefore, tree cavities are formed only
through natural decay and are concentrated in mature forests.
Our study site is a patch of 10-ha mature forest on the southeastern coast of Lanyu. We mapped all the large trees (diameter at 130 cm above ground . 18 cm) and measured the
characteristics of all the cavities known (totaling 296 trees
and 258 cavities, Severinghaus 2007). Vegetation structure of
the study site comprises a canopy layer (height 8–16 m), a herb
layer, and a very open middle layer. The crowns of the canopy
trees are umbrella shaped with leaves clustered on the treetop. Such structure allows high detection rate of the owls,
which frequent the large branches.
Lanyu scops owl (O. e. botelensis) is a subspecies of elegant
scops owl (O. elegans) endemic to Lanyu. It is an insectivorous
owl nesting in cavities. The availability of suitable cavities limits its reproduction (Severinghaus 2007). Since early spring,
male owls compete for cavities through vocal contests and
territorial fights. Females also compete for cavities, but female
contests were much less frequent than between-male contests.
Breeding females lay a clutch of 2 or 3 eggs mainly in the
second half of May. Females incubate for about 1 month, then
both parents feed the nestlings for another month. About
60% of the breeding attempts have at least one fledged young
(Severinghaus 2007), which are further fed by the parents for
2–3 weeks.
Population monitoring
Since 1985, we mist-netted, weighed, and color-ringed owls
regularly in our study site to maintain 80% of the population
individually identifiable. Nestlings were weighed and colorringed at about 3 weeks old. Sexes look alike in this species
except that adult females are slightly larger than adult males
(female 127 6 11 g, male 119 6 9 g). Sex identification in the
field relied on their sex-specific vocalization. Since 1999,
about 20 ll of blood was collected from the alar vein of each
captured individual for sex typing using molecular markers.
Two persons spent 7 nights per month searching for owls in
the study site and recorded the color-ring combination of
each owl observed. We found that the number of owls observed showed an annual cyclic pattern, being highest in
May and lowest in September (Figure 1; Severinghaus 2002).
To examine whether this pattern reflected owl movement or
was an observational bias due to other behavioral changes
(e.g., less vocal) in owls, we conducted monthly standardized
mist netting and radio tracking. We verified that, whereas
METHODS
Study area and species
Lanyu (22.0N, 121.3E), also known as Orchid Island, lies 60
km off the southeastern coast of Taiwan. It is a rugged volcanic
island 46 km2 in area. As a result of frequent strong wind,
scrubby woodlands dominate the landscape. Fragmented mature forests are scattered only in sheltered sites and comprise
about 10% of the island. There is no woodpecker or other
Figure 1
Monthly variation (mean 6 standard deviation) of the number of
banded Lanyu scops owls in the study site between 1999 and 2007.
Modified from Severinghaus (2002).
Bai et al.
•
Partial migration of a subtropical owl
some owls remained in the study site through winter, some
moved to edge habitats on the island at the end of breeding
season and returned to the study site the following spring
(Severinghaus 2002). Owls’ departure from the study site
was not synchronized, with the majority leaving in late July
and August. The timing of their return could be as early as
January, but mostly between February and April.
Data treatment and analyses
We used only data collected between 1999 and 2007 for this
study because almost all nest cavities in the study site were
known since 1999. We termed each owl as either a resident
or a migrant in a given year based on whether it was observed
in the study site between September and December that year.
We treated each owl each year as a separate record because
the status of an owl could change among years. We excluded
the last-year record of each bird from our analyses, as we could
not determine whether it died or emigrated. We categorized
the age of owls as first, second, and third year or older based
on calendar year. Preliminary analysis using known-aged owls
showed no further differentiation in migratory strategy
among birds third year or older. Owls ringed as adult were
considered age unknown the first year after ringing, then
categorized as third year or older in subsequent years.
To investigate the condition dependence of migratory behavior, we used generalized linear mixed models (GLMMs)
with binomial error distribution and logit link function to examine whether migratory strategy was related to age class, sex,
breeding status (if the individual breed or not), breeding success (defined as successful if at least one young fledged),
number of fledglings of the previous breeding season, and
the body mass measured in July/August, prior to the start of
migration. To examine the costs and benefits of alternative
migratory strategies, we used GLMMs with binomial error distribution and logit link function to test if breeding status and
breeding success the following year were related to migratory
strategy, used GLMM with Poisson error distribution and
logarithmic link function to test if the number of fledglings
the following year was related to migratory strategy, and
used GLMM with normal error distribution and identity link
function to evaluate whether the January body mass (post the
defined migration period) was associated with migratory strategy. Because of the small sample sizes for first and second year
age classes, we used only the data of third year or older birds
in all analyses except those regarding age and sex. In all cases,
bird identity was included as a random factor, as some owls
occurred in the data set for several years. While analyzing the
reproductive parameters (breeding status, breeding success,
and number of fledglings) of the following year, previous
breeding status was included as a fixed effect. For the analysis
of body mass, sex and previous breeding status were included
as fixed effects. Significance of each fixed effect was assessed
with Wald statistics. For survival, we considered only knownaged birds and calculated the number of years each was seen
and the percentage of years it adopted nonmigratory strategy
since the third year of its life. We then examined the relationship of 2 variables, using partial correlation analysis with the
bird’s ringing year as the control variable.
RESULTS
The data set included 651 records of 122 males and 107 females. Each year, from 35% to 47% of the owls were categorized as resident, and the ratio showed no significant interyear
variation (chi-square test, v27 ¼ 3.2, P ¼ 0.86). The migratory
strategy of a specific individual could alter between years.
Among the 61 owls present for at least 5 years, only 3 behaved
155
as resident every year and 9 always as migrant. For the following analyses, we considered only the cases with known age
classes, totaling 572 records from 109 males and 95 females.
Age and sex
In male owls, the tendency to be resident increased with increasing age class (Table 1, Figure 2a). For females, the sample sizes of first- and second-year birds were too small to
analyze. Among owls third year or older, more males behaved
as resident than females. There was no detectable sexual difference in migratory strategy in the 2 younger age classes due
to limited sample size.
Reproduction
Among male owls 3 or more years old, more breeders behaved
as resident than nonbreeders (Table 1, Figure 2b). The relationship between breeding status and migratory strategy after the breeding season was only marginally significant in
females. Among breeders, neither breeding success nor fledgling number was associated with migratory strategy in either
sex (Table 1, Figure 2c,d).
The breeding status of male owls was related to both their
migratory strategy and their breeding status of the previous
year. More previous-year residents bred than previous
migrants (Figure 3a; GLMM, F1,185 ¼ 8.2, P , 0.01), and
more previous-year breeders bred than previous nonbreeders (GLMM, F1,185 ¼ 5.7, P , 0.05). Examining only
the breeding males, their breeding success and fledgling
number were not related to their migratory strategy or their
breeding status of the previous year (Figure 3b,c; GLMM,
breeding success, and migratory strategy: F1,132 ¼ 0.1, P ¼
0.79; breeding success and previous breeding status: F1,132 ¼
3.3, P ¼ 0.07; number of fledglings and migratory strategy:
F1,130 ¼ 0.3, P ¼ 0.62; number of fledglings; and previous
breeding status: F1,130 ¼ 1.5, P ¼ 0.23). These results
indicate that resident males had higher chances of obtaining
breeding opportunities than migrant, but once a male owl
obtained a cavity, its success was not influenced by whether it
was a resident or a migrant. If including nonbreeders to compare the overall reproductive output of the 2 strategies, resident males had significantly higher number of fledglings than
Table 1
Results of GLMMs for the condition dependence of the migratory
strategy of Lanyu scops owl
Variable
Age class
Male
Female
Sex
First-year birds
Second-year birds
Third-year or older birds
Breeding status
Male
Female
Breeding success
Male
Female
Number of fledglings
Male
Female
Body weight in July/August
Degrees of
freedom
F
P
2, 217
2, 169
8.4
0.0
,0.001
1.00
1,19
1,19
1, 353
1.8
0.0
34.3
0.20
0.98
,0.0001
1, 186
1, 165
4.2
3.5
,0.05
0.06
1, 132
1, 112
1.4
0.4
0.24
0.52
1, 130
1, 110
1, 70
0.8
0.1
2.2
0.37
0.71
0.14
156
Behavioral Ecology
Figure 2
Condition dependence of the
migratory strategy of Lanyu
scops owl: percentage of residents in relation to (a) age
classes, (b) breeding status,
(c) breeding success, and (d)
number of fledglings.
migroty ones (Figure 3d; GLMM, migratory strategy: F1,183 ¼
4.3, P , 0.05; previous breeding status: F1,183 ¼ 3.8, P ¼ 0.05).
The breeding status of females was not related to their migratory strategy (Figure 3a; GLMM, F1,164 ¼ 1.9, P ¼ 0.17) but
to their breeding status of the previous year (GLMM, F1,164 ¼
4.3, P , 0.05). More previous-year breeders bred than pre-
Figure 3
Costs and benefits associated
with alternative migratory strategies of Lanyu scops owl: the
relationship
between
(a)
breeding status, (b) breeding
success, (c) mean fledgling
number of breeders, and (d)
mean fledgling number of all
birds with the migratory strategy of the previous winter.
vious nonbreeders. Examining only the breeding females, females that were resident the previous year had higher
breeding success (Figure 3b; GLMM, F1,96 ¼ 6.1, P , 0.05),
but their previous breeding status did not have any effect
(GLMM, F1,96 ¼ 0.8, P ¼ 0.37). Their number of fledglings
was related neither to their migratory strategy (Figure 3c;
Bai et al.
•
Partial migration of a subtropical owl
GLMM, F1,95 ¼ 2.1, P ¼ 0.15) nor to their breeding status
(GLMM, F1,95 ¼ 0.4, P ¼ 0.51) of the previous year. Examining
both breeders and nonbreeders, resident females had more
fledglings than migratory females (Figure 3d; GLMM, migratory strategy: F1,163 ¼ 3.9, P , 0.05; previous breeding status:
F1,163 ¼ 3.1, P ¼ 0.08).
157
to the breeding status of the previous year (GLMM, F1,34 ¼ 1.3,
P ¼ 0.27) or the interaction between previous breeding status
and migratory strategy (GLMM, F1,34 ¼ 1.4, P ¼ 0.25).
DISCUSSION
Trade-off between reproduction and survival
Survival
The number of years an owl was observed was not related to the
frequency it bred for either sex (partial correlation, males: r ¼
0.04, N ¼ 32, P ¼ 0.84; females: r ¼ 0.10, N ¼ 26, P ¼ 0.64). No
relationship existed between the number of years a male was
observed and the percentage of years it was a resident (partial
correlation, r ¼ -0.22, N ¼ 32, P ¼ 0.23), but the more frequently a female was a resident, the fewer years it was observed
(partial correlation, r ¼ -0.39, N ¼ 26, P , 0.05).
Body mass
Migratory strategy of owls was not related to their body mass at
the end of the breeding season (Table 1, Figure 4a). Both
sexes gained weight over winter, and migrants were heavier
the following January than residents (Figure 4b; GLMM,
F1,34 ¼ 4.4, P , 0.05). Migratory males were about 5% heavier
than resident males, and migratory females were about 6%
heavier than resident females. January body mass was not related
Through long-term monitoring of the movement pattern,
breeding performance, survival, and body mass, we explored
the costs and benefits associated with alternative migratory
strategies of Lanyu scops owl. Resident owls gain privileges
in reproduction the following spring, and such benefits unfold differently for males and females. Male residents had
a greater chance breeding than male migrants. As cavity availability is limiting (Severinghaus 2007), resident males may
increase their probability of obtaining cavities through prior
occupancy. Residents could familiarize themselves with potential territories and competitors during winter and therefore
increase their dominance in cavity competition (Stamps 1987;
Sandell and Smith 1991; Snell-Rood and Cristol 2005). In
contrast, female residents did not have higher probability of
breeding than female migrants. Yet previous-year breeding
females were more likely to breed compared with previous
nonbreeding females, regardless of their migratory strategy.
This indicates that whether a female breeds or not may be
related to some other unidentified factor, not determined by
priority-dependent cavity occupation. Nevertheless, among
breeding females, residents were more likely to breed successfully than migrants. Cavity flooding after heavy rain is a main
cause for breeding failure in these owls (Severinghaus 2007).
A cavity may get flooded in one rain event but not in another,
and the flooding is usually short term. Therefore, repeated
assessment is necessary to judge the safety of a cavity. We have
observed owls inspecting cavities in winter, presumably to evaluate their qualities. By staying at the breeding site in winter,
resident females may make better assessment of cavities than
migrants. In long-distance migration and altitudinal migration
systems, residents were also found to occupy better territories
and have higher breeding success than migrants (Schwabl
1983; Adriaensen and Dhondt 1990; Gillis et al. 2008).
Migratory owls gained more weight over winter than residents. These owls winter in edge habitats (Severinghaus
2002) where large insects are more abundant than in the
breeding site (Yang MM, unpublished data). As adult owls on
Lanyu have no natural predators, the disadvantage of weight
gain associated with mass-dependent predation (Houston and
McNamara 1993; Metcalfe and Ure 1995) is not an issue, and
their mortality is likely related to the physical condition of the
individuals. Consequently, gaining more weight by wintering in
food-rich habitats should be advantageous. Our results also
suggested that being migratory is beneficial for survival in
females.
Factors underlying different migratory decisions
Figure 4
The relationship between the migratory strategy of owls with (a) the
body mass in July and August and (b) the body mass in the following
January.
We found that the migratory strategy of Lanyu scops owls was
conditional to sex, age, and breeding status: 1) among birds
third year or older, the tendency to be resident was higher in
males than in females; 2) in males, the tendency to be resident was higher in older birds than in younger ones; and 3)
the tendency to be resident was higher in breeders than in
nonbreeders.
The observation that female owls were more migratory than
males is consistent with the arrival-time hypothesis. The underlying mechanism of the arrival time hypothesis is a prioritydependent intraspecific competition for territories (Ketterson
and Nolan 1983). This was verified in our analysis that the
Behavioral Ecology
158
probability of breeding is priority-dependent in males but not
in females.
The patterns that older owls and breeders tended to be resident compared with younger ones and nonbreeders are consistent with the prediction of the dominance hypothesis. Food
competition is the commonly adopted explanation for this
hypothesis, which suggests that dominant individuals may
out-compete subordinates for scarce food resources in winter
(Lundberg 1985; Smith and Nilsson 1987). This explanation
was derived from the studies of temperate birds that are granivores, frugivores, or omnivores in winter and forage in
flocks. In such flocks, foraging success often mirrors dominance rank (Dingemanse and de Goede 2004). However, Lanyu scops owl is an insectivore and never forages in flocks.
Food competition is less likely to be the mechanism driving
the dominance-dependent partial migration for this species.
We propose that the difference in the probability of breeding
between dominants and subordinates could lead to the same
observed pattern. Lanyu scops owls rarely breed in the second
year of their lives (Severinghaus LL, unpublished data). The
low expectancy for young owls to breed very likely favors their
decision to migrate, opting for increased survival and hence
improved opportunity for future reproduction. Our analyses
also showed that current breeders had higher chance to breed
next year than nonbreeders. It could thus be worthwhile for
current breeders to remain in the breeding area and pay the
cost of inferior winter foraging condition.
Our results do not support the body-size hypothesis, as lighter weighted males were less migratory than heavier females,
and within-sex migratory tendency was not related to the body
mass at the end of the breeding season. The body-size hypothesis developed in the temperate region emphasizes the ability
to endure food deprivation under cold weather. This mechanism probably plays a minor role in our study site, where the
climate is relatively mild. At a small spatial scale as in this
study, the difference between the microclimate of alternative
wintering sites is also relatively small. However, within tropical
areas where rainfall variation is great, partial migration could
be induced by limited foraging opportunities (Boyle 2008) or
limited food availability (Jahn et al. 2010).
In summary, we suggest that the competition for limited
breeding resources is the main underlying factor shaping
the partial migration of Lanyu scops owl. Males, which experience intense intrasexual competition for cavities and may gain
significant privileges through prior residency, tend to be resident. Older birds and breeders, which represent the dominant individuals and would have ‘‘more to lose’’ if leaving the
breeding site, also tend to stay. The pattern that males tend to
be resident was also found in many temperate populations
exhibiting long-distance migrations (Smith and Nilsson
1987; Adriaensen and Dhondt 1990; Mazerolle and Hobson
2007). The arrival-time hypothesis may be applicable in different regions and at different spatial scales, when breeding
territories are limited or vary greatly in quality. The body-size
hypothesis emphasizing the ability to endure food deprivation
is probably less applicable in regions with mild climate and at
small spatial scales. The dominance hypothesis based on food
competition is unsuitable for solitude insectivores (Jahn et al.
2010), and we propose a modified dominance hypothesis
driven by differential probability of breeding. As pointed
out by other works (Boyle 2008; Jahn et al. 2010), the leading
hypotheses concerning partial migration may need modification to cover different migratory systems in the tropics.
We deeply appreciate R. Macedo, C. P. Bell, J. Brodersen, and other
anonymous reviewers for their insightful comments on an earlier
draft. We are grateful to Shih-fan Chan for suggestions concerning
data analyses. We thank Chien-hung Yang, Chin-kuo Lee, Jerome
Chien, I-hua Lin, Chien-wei Kuan, Shih-cheng Huang, and Wen-chun
Li for many years of laborious fieldwork, careful data collection, and
numerous discussions. This study was supported by grants from the
National Science Council of Taiwan and Biodiversity Research Center,
Academia Sinica, Taiwan.
REFERENCES
Adriaensen F, Dhondt AA. 1990. Population dynamics and partial
migration of the European robin (Erithacus rubecula) in different
habitats. J Anim Ecol. 59:1077–1090.
Bell CP. 2000. Process in the evolution of bird migration and pattern
in avian ecogeography. J Avian Biol. 31:258–265.
Berthold P. 2001. Bird migration. A general survey. Oxford: Oxford
University Press.
Berthold P, Querner U. 1982. Partial migration in birds: experimental
proof of polymorphism as a controlling system. Experientia. 38:
805–806.
Biebach H. 1983. Genetic determination of partial migration in the
European robin (Erithacus rubecula). Auk. 100:601–606.
Boyle WA. 2008. Partial migration in birds: tests of three hypotheses in
a tropical lekking frugivore. J Anim Ecol. 77:1122–1128.
Brodersen J, Ådahl E, Brönmark C, Hansson L-A. 2008. Ecosystem
effects of partial fish migrations in lakes. Oikos. 117:40–46.
Brodersen J, Nilsson PA, Hansson L-A, Skov C, Brönmark C. 2008.
Condition-dependent individual decision-making determines cyprinid partial migration. Ecology. 89:1195–1200.
Chan K. 2005. Partial migration in the silvereye (Aves Zosteropidae):
pattern, synthesis, and theories. Ethol Ecol Evol. 17:349–363.
Dingemanse NJ, De Goede P. 2004. The relation between dominance
and exploratory behavior is context-dependent in wild great tits.
Behav Ecol. 15:1023–1030.
Dingle H. 1996. Migration: the biology of life on the move. New York:
Oxford University Press.
Fryxell JM, Sinclair ARE. 1988. Causes and consequences of migration
by large herbivores. Trends Ecol Evol. 3:237–241.
Gillis EA, Green DJ, Middleton HA, Morrissey CA. 2008. Life history
correlates of alternative migratory strategies in American dippers.
Ecology. 89:1687–1695.
Houston AI, McNamara J. 1993. A theoretical investigation of the fat
reserves and mortality levels of small birds in winter. Ornis Scand.
24:205–219.
Jahn AE, Levey DJ, Hostetler JA, Mamani AM. 2010. Determinants of
partial bird migration in the Amazon Basin. Anim Ecol.
79:983–992.
Ketterson ED, Nolan V Jr. 1983. The evolution of differential bird
migration. Curr Ornithol. 1:357–402.
Levey DJ, Stiles FG. 1992. Evolutionary precursors of long distance
migration: resource availability and movement patterns in Neotropical landbirds. Am Nat. 140:447–476.
Lundberg P. 1985. Dominance behaviour, body weight and fat variations, and partial migration in European blackbirds Turdus merula.
Behav Ecol Sociobiol. 17:185–189.
Mazerolle DF, Hobson KA. 2007. Patterns of differential migration in
white-throated sparrows evaluated with isotopic measurements of
feathers. Can J Zool. 85:413–420.
Metcalfe NB, Ure SE. 1995. Diurnal variation in flight performance
and hence potential predation risk in small birds. Proc R Soc Lond
B Biol Sci. 261:395–400.
Morrissey CA, Bendell-Young LI, Elliott JE. 2004. Seasonal trends in
population density, distribution, and movement of American Dippers within a watershed of southwestern British Columbia, Canada.
Condor. 106:815–825.
Myers JP. 1981. A test of three hypotheses for latitudinal segregation of
the sexes in wintering birds. Can J Zool. 59:1527–1534.
Ogonowski MS, Conway CJ. 2009. Migratory decisions in birds: extent
of genetic versus environmental control. Oecologia. 161:199–207.
Olsson IC, Greenberg LA, Bergman E, Wysujack K. 2006. Environmentally induced migration: the importance of food. Ecol Lett.
9:645–651.
Poulin B, Lefebvre G, McNeil R. 1993. Variations in bird abundance in
tropical arid and semi-arid habitats. Ibis. 135:432–441.
Salewski V, Bruderer B. 2007. The evolution of bird migration—a
synthesis. Naturwissenschaften. 94:268–279.
Bai et al.
•
Partial migration of a subtropical owl
Sandell M, Smith HG. 1991. Dominance, prior residence, and winter residency in the great tit (Parus major). Behav Ecol Sociobiol. 29:147–152.
Schwabl H. 1983. Auspraegung und Bedeutung des Teilzugverhaltens
einer suedwestdeutschen Population der Amsel Turdus merula.
J Ornith. 124:101–116.
Severinghaus LL. 2002. Home-range, movement and dispersal of
Lanyu Scops Owls (Otus elegans). In: Newton I, Kavanagh RP, Olsen
J, Taylor IR, editors. Ecology and conservation of owls. Melbourne
(Australia): CSIRO Publishing. p. 58–67.
Severinghaus LL. 2007. Cavity dynamics and breeding success of the
Lanyu Scops Owl (Otus elegans). J Ornith. 148:407–416.
159
Smith HG, Nilsson J-A. 1987. Intraspecific variation in migratory pattern of a partial migrant, the blue tit (Parus caeruleus): an evaluation
of different hypotheses. Auk. 104:109–115.
Snell-Rood EC, Cristol DA. 2005. Prior residence influences contest
outcome in flocks of non-breeding birds. Ethology. 111:441–454.
Stamps JA. 1987. The effect of familiarity with a neighborhood on
territory acquisition. Behav Ecol Sociobiol. 21:273–277.
Sutherland WJ. 1996. From individual behaviour to population ecology. Oxford: Oxford University Press.
Winemiller KO, Jepsen DB. 1998. Effects of seasonality and fish movement on tropical river food webs. J Fish Biol. 53:267–296.