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Journal of Animal Ecology 2010, 79, 933–936
doi: 10.1111/j.1365-2656.2010.01739.x
IN FOCUS
Partial migration in tropical birds: the frontier of
movement ecology
A tropical kingbird Tyrannus melancholicus, a widespread species throughout much of the Neotropics which migrates within the Amazon Basin.
Photo by Frank Shufelt.
A. E. Jahn, D. J. Levey, J. A. Hostetler & A. M. Mamani (2010) Determinants of partial bird
migration in the Amazon Basin. Journal of Animal Ecology, 79, 983–992.
Partial migration, in which only some individuals of a species migrate, might be central to the evolution of migratory behaviour and is likely to represent an evolutionary transition between sedentariness
and complete migration. In one of the few detailed, individual-based migration studies of tropical
birds, Jahn et al. study the partial migration system of a South American bird species for the first
time. Food limitation forces the large adult males and small, young females to migrate, contrary to
the expectations of the body size and dominance hypotheses. This study confirms the importance of
food variability as the primary driver of migratory behaviour. There is urgent need for similar studies
on the movement ecology of understudied tropical bird species, whose diversity of migratory behaviour
can shed light on the evolution of bird migration.
Migration is one of the most spectacular, albeit increasingly threatened, phenomena of the living world (Wilcove
2008). Birds provide impressive examples, with some covering more than 80 000 km annually (Gill et al. 2009;
Egevang et al. 2010). Eighteen per cent of the world’s
10 000 bird species undertake regular long-distance
*Correspondence author. E-mail: [email protected]
2010 The Author. Journal compilation 2010 British Ecological Society
migrations (Fig. 1; Sekercioglu 2007) and every year 40
billion birds are estimated to migrate (Wikelski et al.
2007). However, research has mostly focused on discovering the migratory cues and mapping migrations, and the
ecological reasons for bird migration are still vague (Boyle
& Conway 2007; Boyle 2008a). Understanding the drivers
of animal migration is particularly challenging due to the
difficulty and expense of keeping track of birds covering
long distances. Less spectacular but equally important
934 C. H. Sekercioglu
Fig. 1. Extinction risk as a function of long-distance movement. Bird
species with regular long-distance movements are less extinctionprone (threatened, near threatened or extinct) than sedentary birds
(Sekercioglu 2007). The number of species known to undertake that
type of movement is in parentheses. Reprinted with permission from
Sekercioglu (2007) Current Biology, 17, R283–R286.
types of migratory behaviour, such as short-distance, altitudinal and partial migration are particularly understudied.
This is especially true for birds <100 g that cannot be
tracked by satellite even though they make up 65% of the
world’s bird species (Dunning 2007; Wikelski et al. 2007).
Detailed studies of tropical songbird movement can mean
thousands of hours of radiotracking on foot (Sekercioglu
et al. 2007), often in rugged, wet and challenging terrain,
so even less is known about these birds.
Although most bird species do not migrate (Fig. 1), even
seemingly ‘sedentary’ tropical birds can cover hundreds of
kilometres in search of food (Holbrook, Smith & Hardesty
2002), and hundreds of species are involved in shortdistance, altitudinal and partial migrations (Berthold 1999;
Sekercioglu 2007). However, there are few detailed, longterm, individual-based movement studies of tropical birds.
Given the range of migratory behaviour seen in the tropics
(Boyle & Conway 2007), such studies are essential for
revealing the ecological and evolutionary mechanisms
behind bird migration (Levey & Stiles 1992; Chesser &
Levey 1998; Boyle & Conway 2007). Understanding avian
mobility is also important for guiding the conservation of
tropical bird communities and the restoration of their
habitats (Sekercioglu et al. 2007), especially in the face of
climate change threatening hundreds of tropical bird species
with narrow ranges and limited mobility (Sekercioglu et al.
2008).
Partial migration, in which some individuals migrate and
others remain sedentary (Jahn et al. 2010), might be central
to the evolution of migratory behaviour and likely represents
an evolutionary transition between sedentariness and complete migration (Berthold 1999; Boyle 2008b). Although
‘extremely widespread at higher latitudes’ (Berthold 1999),
much less is known about partial migration in the tropics
where only a few studies have been done (Boyle 2008b; Boyle,
Norris & Guglielmo 2010; Jahn et al. 2010). However, most
bird species live in the tropics where the diversity of migratory behaviour exhibited makes migratory research especially
pertinent. The South American austral migration system,
despite being the third major migration system between temperate and tropical regions and the only one in the Southern
Hemisphere (Chesser 1994), has been particularly neglected.
It is therefore welcome that Jahn et al. (2010) in this issue
break the mould and test two important hypotheses of partial
migration on a tropical bird species in the Southern Hemisphere, where there is ‘a unique opportunity to better understand the evolutionary ecology of bird migration’ (Dingle
2008). Jahn et al. (2010) conducted a detailed individualbased study of tropical kingbirds (Tyrannus melancholicus) to
test the dominance and body size hypotheses. According to
the dominance hypothesis, subordinate individuals who are
unable to compete effectively with dominant individuals for
food are more likely to choose migration over competing
for food during times of food scarcity (Gauthreaux 1978;
Ketterson & Nolan 1979). The body size hypothesis predicts
that larger individuals (usually males) are better able to
withstand cold weather and food shortage, which means
smaller individuals are more likely to migrate (Belthoff &
Gauthreaux 1991). Jahn et al. (2010) were unable to test the
arrival time hypothesis, which states that individuals establishing breeding territories (again, usually males) will migrate
less than non-territorial individuals because a shorter migration distance will enable a faster return to breeding areas and
first access to best territories (Ketterson & Nolan 1976). As
all three hypotheses were developed in the north temperate
latitudes and mostly tested there, it is especially important to
know if they can explain partial migration in other parts of
the world (Boyle 2008b).
Tropical kingbirds are common, widespread and mostly
insectivorous Neotropical songbirds found in a range of
open habitats. They belong to the family Tyrannidae, which
is the main bird family in the austral migration system
(Chesser 1994). Tropical kingbirds are completely migratory
south of 18S, but at the grassland study site in the Amazon
basin of Bolivia (1449¢S), they are partially migratory. Jahn
and colleagues combined mark–recapture, radiotracking,
and maximum-likelihood modelling in a rigorous framework
to tease apart the probabilities of detection, migration, survival and permanent dispersal. Individually colour-banded
kingbirds were surveyed every 2 weeks. By radiotracking
individuals, they showed that birds were not moving locally,
but migrating instead. There was strong support for partial
migration, the probability of which was influenced by age,
body mass and the interaction of these with sex in an unexpected pattern. Large adult males and small young females
had the highest probability of migrating. Because older
kingbirds dominate younger kingbirds, the results did not
support the dominance hypothesis for males, underlining the
importance of sexual differences. Similarly, the body size
hypothesis was not supported.
2010 The Author. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 933–936
Partial migration in tropical birds 935
austral migrants are potentially undertaking partial migration (Jahn et al. 2006).
Although habitat, diet and their interaction can be important in determining which birds migrate and which do not
(Boyle & Conway 2007), the variability of access to food
resources has emerged as the primary driver of migratory
behaviour (Levey & Stiles 1992; Chesser 1998; Boyle &
Conway 2007; Boyle, Norris & Guglielmo 2010). In fact, in
South America, open country insectivores show the highest
migratory tendency (Boyle & Conway 2007), whereas insectivorous species of ‘buffered’ tropical forest interior environments are not known to migrate (Chesser et al. 1998). With
this study, Jahn et al. (2010) provide important empirical
support for the importance of resource variability in austral
bird migration by explicitly linking migratory behaviour in a
Neotropical insectivorous bird to seasonal changes in insect
numbers. Tropical forests, commonly thought to be ‘stable
and constant’, can also experience substantial resource variability that has consequences for avian reproductive seasonality (Wikelski, Hau & Wingfield 2000). Many tropical forest
insectivorous bird species faced with resource fluctuations
and increased habitat fragmentation (Sekercioglu et al. 2002)
might be undertaking partial migrations yet to be discovered.
In the only other Neotropical (Cost Rica) partial migration
system studied to date, Boyle, Norris & Guglielmo (2010) also
showed the importance of the interaction of environmental
variation with intrinsic variables like age and sex in determining migration likelihood. However, unlike Jahn and colleagues’ system, Boyle et al. found that inclement weather
(storms and heavy rains) reducing foraging opportunities,
not food shortage per se, was the main driver of migration in
white-ruffed manakins (Corapipo altera). In this system, adult
males were also more likely to migrate, but this was because
they were smaller and did not have the fasting advantages of
the larger females. In both systems, migration likelihood is
influenced by the effect of weather on food obtained, and different ages and sexes vary in their responses to food shortage
based on their body mass. While the Brazilian dry season
reduces insect food abundance and forces some kingbirds to
migrate, in the wet mountains of Costa Rica storms and
These findings complement those of Boyle & Conway
(2007) who conducted a comparative analysis of 379 species
of tyrannid flycatchers to test the evolutionary precursor
hypothesis of migration (Levey & Stiles 1992). After incorporating phylogenetically independent contrasts, Boyle &
Conway (2007) showed the importance of habitat and diet
interaction and foraging behaviour in shaping migratory
behaviour. Their resource variability hypothesis states that
species relying on more seasonal resources are more likely to
evolve migratory behaviour (Boyle & Conway 2007). Jahn
et al. (2010) explain migratory variation among individuals
with their food limitation hypothesis. This modifies the
resource variability hypothesis by proposing different threshold values for individuals based on their sex and age
(Table 1). The variability of the insect resource forces the
largest males and the smallest females to migrate in the dry
season, when insect prey is reduced and the basal energy
requirements of the former and the territorial defence costs
of the latter likely push them above the available energy
threshold (Table 1).
Food limitation is thought to be the main driver of migration in most birds (Alerstam, Hedenstrom & Akesson 2003;
Boyle 2008a). However, additional environmental conditions
such as reduced nest predation, inclement weather or parasites can play critical roles (Alerstam, Hedenstrom & Akesson 2003; Boyle 2010; Boyle, Norris & Guglielmo 2010). The
complex interaction of these factors with habitat, sex, body
mass and other traits (Boyle & Conway 2007; Jahn et al.
2010) make simple explanations difficult. A variety of
research approaches (e.g. bird banding, nest monitoring,
hormonal measurements, radiotracking, population models,
dietary analysis, parasitology) is necessary, especially outside
the well-studied north temperate region. In the Southern
Hemisphere, the migration strategies employed are more varied (Jahn et al. 2010) and opportunities abound to study the
evolutionary ecology of bird migration (Chesser et al. 1998;
Dingle 2008). Therefore, it is remarkable that Jahn et al.
(2010) are the first to study the partial migration system of
any South American bird species, even though this is ornithologically the richest continent and two-thirds of Neotropical
Table 1. A conceptual, simplified framework for the food limitation hypothesis (Jahn et al. 2010) based on hypothetical units of energy required
for basal metabolic rate (BMR) and territorial defence. This table is not based on real data. For the same body mass, BMR and other energy
needs are assumed to be equal for each sex. Males are, on average, larger than females. Males are assumed to be dominant over females, with the
energy cost of territorial defence higher for females with equal body mass. Cost of territorial defence is negatively correlated with body mass,
increasing nonlinearly for females and linearly for males. The maximum energy available in the dry season is 70 units per day per bird, with birds
requiring more than this threshold value (grey) being forced to migrate
Male
Female
Mass (g)
Basal
Defence
Total
30
35
40
45
50
55
42
48
54
60
66
18
15
12
9
6
60
63
66
69
72
Basal
Defence
Total
36
42
48
54
60
36
28
21
15
10
72
70
69
69
70
2010 The Author. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 933–936
936 C. H. Sekercioglu
heavy rains prevent manakins from foraging, forcing them to
choose between fasting or migrating.
Because increased migratory behaviour in birds reduces
extinction likelihood (Sekercioglu 2007), advances in avian
movement ecology will also advance bird conservation biology, especially in the face of climate change. While climate
change is expected to affect sedentary birds more negatively
than migratory species (Sekercioglu et al. 2008), migratory
birds will face their own challenges, such as longer migrations
and simultaneous impacts on wintering, breeding and stopover sites (Huntley et al. 2006).
Unfortunately, detailed movement studies involving longterm bird banding, radiotracking, and satellite telemetry are
lacking for most bird species, especially in the tropics. With
accurate satellite transmitters dropping in price, there is great
promise of testing various migration theories (Alerstam,
Hedenstrom & Akesson 2003), but the high cost (£1000s ⁄
animal) of satellite transmitters and data collection fees make
it prohibitively expensive for most scientists, especially in
tropical, developing countries. Satellite transmitters have
been getting smaller and are now down to 5 g, but this is estimated to be their minimum size limit (Wikelski et al. 2007).
Because the transmitter should ideally not exceed 5% of the
body mass of the study species (Wikelski et al. 2007), the
migrations of birds <100 g cannot be followed, excluding at
least 65% of bird species (Dunning 2007). Wikelski et al.
(2007) proposed the establishment of a global small-animal
tracking system based on the launch of a dedicated satellite
(www.icarusinitiative.org). The cost of £33–66 million is
more than justified by the revolutionary implications for
research on animal ecology, evolution, conservation, agriculture and public health.
Nevertheless, Jahn and colleagues’ elegant and painstaking
study shows that we need not wait for a dedicated satellite to
conduct ground-breaking research on bird migration, especially in the tropics. Thousands of tropical bird species have
never been studied, basic truths about bird migration are
waiting to be discovered, and movement ecology is a scientific
frontier that is wide open.
Cagan H. Sekercioglu*
Department of Biology, University of Utah, Salt Lake City,
UT 84112-0840, USA
References
Alerstam, T., Hedenstrom, A. & Akesson, S. (2003) Long-distance migration:
evolution and determinants. Oikos, 103, 247–260.
Belthoff, J.R. & Gauthreaux, S.A. (1991) Partial migration and differential
winter distribution of house finches in the eastern United-States. Condor, 93,
374–382.
Berthold, P. (1999) A comprehensive theory for the evolution, control and
adaptability of avian migration. Ostrich, 70, 1–11.
Boyle, W.A. (2008a) Can variation in risk of nest predation explain altitudinal
migration in tropical birds? Oecologia, 155, 397–403.
Boyle, W.A. (2008b) Partial migration in birds: tests of three hypotheses in a
tropical lekking frugivore. Journal of Animal Ecology, 77, 1122–1128.
Boyle, W.A. (2010) Does food abundance explain altitudinal migration in a
tropical frugivorous bird? Canadian Journal of Zoology-Revue Canadienne
De Zoologie, 88, 204–213.
Boyle, W.A. & Conway, C.J. (2007) Why migrate? A test of the evolutionary
precursor hypothesis. American Naturalist, 169, 344–359.
Boyle, W., Norris, D. & Guglielmo, C. (2010) Storms drive altitudinal migration in a tropical bird. Proceedings of the Royal Society B: Biological Sciences, 277, 2511–2519.
Chesser, R.T. (1994) Migration in South America: an overview of the austral
system. Bird Conservation International, 4, 91–107.
Chesser, R.T. (1998) Further perspectives on the breeding distribution of
migratory birds: South American austral migrant flycatchers. Journal of Animal Ecology, 67, 69–77.
Chesser, R.T. & Levey, D.J. (1998) Austral migrants and the evolution of
migration in new world birds: Diet, habitat, and migration revisited. American Naturalist, 152, 311–319.
Dingle, H. (2008) Bird migration in the southern hemisphere: a review comparing continents. Emu, 108, 341–359.
Dunning, J.B. (2007) CRC Handbook of Avian Body Masses, 2nd edn. CRC
Press, Boca Raton, FL, USA.
Egevang, C., Stenhouse, I.J., Phillips, R.A., Petersen, A., Fox, J.W. & Silk,
J.R.D. (2010) Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proceedings of the National Academy of Sciences of the United
States of America, 107, 2078–2081.
Gauthreaux, S.A. (1978) The ecological significance of behavioral dominance.
Perspectives in Ethology (eds P.P.G. Bateson & P.H. Klopfer), pp. 17–45.
Plenum Press, New York.
Gill, R.E., Tibbitts, T.L., Douglas, D.C., Handel, C.M., Mulcahy, D.M.,
Gottschalck, J.C., Warnock, N., McCaffery, B.J., Battley, P.F. & Piersma,
T. (2009) Extreme endurance flights by landbirds crossing the Pacific Ocean:
ecological corridor rather than barrier? Proceedings of the Royal Society
B-Biological Sciences, 276, 447–458.
Holbrook, K.M., Smith, T.B. & Hardesty, B.D. (2002) Implications of longdistance movements of frugivorous rain forest hornbills. Ecography, 25,
745–749.
Huntley, B., Collingham, Y.C., Green, R.E., Hilton, G.M., Rahbek, C. & Willis, S.G. (2006) Potential impacts of climatic change upon geographical distributions of birds. Ibis, 148, 8–28.
Jahn, A.E., Levey, D.J., Johnson, J.E., Mamani, A.M. & Davis, S.E. (2006)
Towards a mechanistic interpretation of bird migration in South America.
El Hornero, 21, 99–108.
Jahn, A.E., Levey, D.J., Hostetler, J.A. & Mamani, A.M. (2010) Determinants
of partial bird migration in the Amazon Basin. Journal of Animal Ecology,
79, 983–992.
Ketterson, E.D. & Nolan, V. (1976) Geographic variation and its climatic
correlates in sex-ratio of eastern-wintering Dark-eyed Juncos (JuncoHyemalis Hyemalis). Ecology, 57, 679–693.
Ketterson, E.D. & Nolan, V. (1979) Seasonal, annual, and geographic variation
in sex-ratio of wintering populations of Dark-Eyed Juncos (Junco hyemalis).
Auk, 96, 532–536.
Levey, D.J. & Stiles, F.G. (1992) Evolutionary precursors of long-distance
migration: resource availability and movement patterns in Neotropical landbirds. American Naturalist, 140, 447–476.
Sekercioglu, C.H. (2007) Conservation ecology: area trumps mobility in fragment bird extinctions. Current Biology, 17, R283–R286.
Sekercioglu, C.H., Ehrlich, P.R., Daily, G.C., Aygen, D., Goehring, D. &
Sandi, R. (2002) Disappearance of insectivorous birds from tropical forest
fragments. Proceedings of the National Academy of Sciences, 99, 263–267.
Sekercioglu, C.H., Loarie, S.R., Oviedo Brenes, F., Ehrlich, P.R. & Daily, G.C.
(2007) Persistence of forest birds in the Costa Rican agricultural countryside.
Conservation Biology, 21, 482–494.
Sekercioglu, C.H., Schneider, S.H., Fay, J.P. & Loarie, S.R. (2008) Climate
change, elevational range shifts, and bird extinctions. Conservation Biology,
22, 140–150.
Wikelski, M., Hau, M. & Wingfield, J.C. (2000) Seasonality of reproduction in
a neotropical rain forest bird. Ecology, 81, 2458–2472.
Wikelski, M., Kays, R.W., Kasdin, N.J., Thorup, K., Smith, J.A. & Swenson,
G.W. (2007) Going wild: what a global small-animal tracking system could
do for experimental biologists. Journal of Experimental Biology, 210, 181–
186.
Wilcove, D.S. (2008) No Way Home: The Decline of the World’s Great Animal
Migrations. University of Chicago Press, Chicago, IL, USA.
Received 21 June 2010; accepted 14 July 2010
Handling Editor: Corey Bradshaw
2010 The Author. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 933–936