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We thank J. Delrow, A. Marty, and A. Dawson at the Fred
Hutchinson Cancer Research Center (FHCRC) Genomics
Facility for assistance with RNA-seq; M. Fitzgibbon and
J. Davidson at the FHCRC Bioinformatics Resource for early
assistance with sequence analyses; and J. Vasquez and the
FHCRC Scientific Imaging Facility for help with confocal
microscopy. We also thank members of the Buck laboratory
for helpful discussions. This work was supported by the
Howard Hughes Medical Institute (L.B.B.), NIH grants R01
DC009324 (L.B.B.) and DP2 HD088158 (C. T.), an Alfred
P. Sloan Fellowship (C. T.), and a Dale F. Frey Award for
Breakthrough Scientists from the Damon Runyon Cancer
Research Foundation (C. T.). L.B.B. is on the Board of Directors
of International Flavors & Fragrances. The supplementary
materials contain additional data. N.K.H., C. T., and L.B.B.
designed the research; N.K.H. and C. T. performed the research;
N.K.H., C. T., K.K., Z.L., D.K., X. Y., X.Q., and L.B.B. analyzed
the data; L.P. provided guidance; and N.K.H, C. T., and L.B.B.
wrote the paper.
Materials and Methods
Figs. S1 to S5
Tables S1 to S7
13 August 2015; accepted 27 October 2015
Published online 5 November 2015
Protected areas and global
conservation of migratory birds
Claire A. Runge,1,2 James E. M. Watson,1,3 Stuart H. M. Butchart,4 Jeffrey O. Hanson,5
Hugh P. Possingham,5,6 Richard A. Fuller5
Migratory species depend on a suite of interconnected sites. Threats to unprotected
links in these chains of sites are driving rapid population declines of migrants around the
world, yet the extent to which different parts of the annual cycle are protected remains
unknown. We show that just 9% of 1451 migratory birds are adequately covered by
protected areas across all stages of their annual cycle, in comparison with 45% of
nonmigratory birds. This discrepancy is driven by protected area placement that does not
cover the full annual cycle of migratory species, indicating that global efforts toward
coordinated conservation planning for migrants are yet to bear fruit. Better-targeted
investment and enhanced coordination among countries are needed to conserve migratory
species throughout their migratory cycle.
From the writings of Aristotle (1) to the musings of Gilbert White in Georgian England (2), migratory birds have fas- cinatedandinspiredpeopleforgenerations. Migrants undertake remarkable journeys,
from endurance flights exceeding 10,000 km by
bar-tailed godwits (Limosa lapponica) (3) to the
annual relay of arctic terns (Sterna paradisaea),
which fly the equivalent of the distance to the
moon and back three times during their lives (4).
Migratory species make major contributions to
resource fluxes, biomass transfer, nutrient transport, predator-prey interactions, and food-web
structure within and among ecosystems (5) and
play an important role in human culture (6). Yet
more than half of migratory birds across all major
flyways have declined over the past 30 years (7).
Threats in any one part of a annual cycle can
affect the entire population of a migratory spe-
cies (8), and so environmental management actions
for migrants need to be coordinated across hab-
itat types, seasons, and jurisdictions (8). Pro-
tected area designation is a widely used approach
for averting species loss (9) because it can reduce
habitat loss, habitat degradation, hunting pres-
sure, and disturbance (10). Yet the extent to which
the distributions of migratory species are covered
by protected areas globally is poorly understood.
Many previous global and regional species con-
servation assessments and prioritization analyses
either omit parts of the annual cycle or treat all
species’ distributions as static (9–12). Here, we
explore how protected area coverage of migra-
tory birds varies across their annual cycle and
among countries and compare their current lev-
els of protected area coverage against standard con-
servation targets. Overlaying maps of protected
areas (13) onto distribution maps of the world’s
birds, we assessed whether the proportion of each
species’ distribution covered by protected areas
met a target threshold (9, 11). For migratory spe-
cies, we set targets for each stage of the annual
cycle separately for the 1451 migratory birds, with
mapped distributions throughout their annual
We discovered that 91% of migratory bird species have inadequate protected area coverage for
at least one part of their annual cycle, despite
individual elements of the annual cycle being
well protected for some species (Table 1). This is
in stark contrast to 55% of nonmigratory species
with inadequate protected area coverage across
their global distribution. A typical migrant relies
on two or three disjoint geographic locations, and
the chance that they are all adequately conserved
is probabilistically lower than for a single location (supplementary materials). We found that
migratory species are less likely to meet protection targets as the number of seasonal areas increases and that the proportion of migratory
species meeting targets is consistent with randomly allocated conservation effort (Fig. 1), indicating that despite widespread recognition of the
need for an internationally coordinated approach
to conservation of migratory species, protection
is not yet systematically coordinated across the
seasonal ranges of species. Twenty-eight migratory bird species have no coverage in at least one
part of their annual cycle, and 18 of these have no
protected area coverage of their breeding range.
Two species lack any protected area coverage
across their entire distribution (Table 1). Disturbingly, less than 3% of threatened migratory
bird species have adequate protected area coverage across all parts of their annual cycle (table S1).
Widespread migrants may benefit more from
broader-scale policy responses (such as targeting
1School of Geography, Planning and Environmental
Management, University of Queensland, Brisbane, QLD,
4072, Australia. 2National Center for Ecological Analysis and
Synthesis (NCEAS), University of California, Santa Barbara,
Santa Barbara, CA 93101, USA. 3Global Conservation
Program, Wildlife Conservation Society, New York, NY, USA.
4BirdLife International, Wellbrook Court, Cambridge CB3
0NA, UK. 5School of Biological Sciences, University of
Queensland, Brisbane, QLD 4072, Australia. 6Department of
Life Sciences, Imperial College London, Silwood Park, Ascot,
Berkshire SL5 7PY, England, UK.
*Corresponding author. E-mail: firstname.lastname@example.org