Download Ecology and conservation of avian insectivores

Biological Conservation xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Special Issue Article: Tropical Insectivores
Ecology and conservation of avian insectivores of the rainforest
understory: A pantropical perspective
Luke L. Powell a,b,⇑, Norbert J. Cordeiro c,d, Jeffrey A. Stratford a,e
a
Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas da Amazônia, CP 478, Manaus, AM 69011-0970, Brazil
School of Renewable Natural Resources, RNR 227, Louisiana State University and Louisiana State University Agriculture Center, Baton Rouge, LA 70803-6202, USA
c
Department of Biological, Chemical, and Physical Sciences, Roosevelt University, 430 S. Michigan Avenue, Chicago, IL 60605, USA
d
Life Sciences, Science and Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA
e
Department of Biology and Health Sciences, Wilkes University, PA 18766, USA
b
a r t i c l e
i n f o
Article history:
Received 17 February 2015
Received in revised form 20 March 2015
Accepted 21 March 2015
Available online xxxx
Keywords:
Understory insectivores
Rainforests
Pantropical
Fragmentation
Deforestation
Mixed species flocks
a b s t r a c t
Avian insectivores of the tropical rainforest understory (‘‘understory insectivores’’) are common, diverse,
and often sensitive to disturbance of tropical forest, making them useful as sentinels of rainforest ecosystem change. At the 2013 joint American Ornithologists’ Union and Cooper Ornithological Society meeting
in Chicago, USA, researchers convened a symposium to address the ecology and conservation of understory insectivores. This Special Issue of Biological Conservation is the result of that symposium: a collection of articles that unites our efforts to further understand and conserve understory insectivores. In this
introductory paper, we review the diversity and ecology of understory insectivores, identify threats to the
guild, discuss hypotheses on drivers of population declines, and make suggestions for future research.
Deforestation and forest degradation are the immediate threats to this guild, with agricultural expansion
(particularly oil palm plantations), urbanization, road expansion and logging leading the list. Although
vulnerabilities of this guild are most evident in the Neotropics, there are few studies from Asia and fewer
still from Africa—we recommend increased geographic coverage. If we are to understand the vulnerabilities of understory insectivores from a pantropical perspective, researchers should prioritize understanding the most serious threats (e.g., edge effects, deforestation, fragmentation, etc.) and standardize efforts
to gauge understory insectivores’ response to these threats (e.g., via species richness, abundance, demographic metrics). A coordinated approach by researchers working in tropical rainforests across the globe
can help us understand the ecology of understory insectivores and meaningfully apply conservation and
management actions.
Published by Elsevier Ltd.
1. Avian insectivores of the tropical rainforest understory: An
introduction
1.1. Degradation and loss of tropical rainforests
Tropical rainforests, which harbor at least half of the earth’s terrestrial biodiversity, are the most diverse terrestrial biome (Dirzo
and Raven, 2003). This diversity is in jeopardy, however, as more
than half of the area covered by closed-canopy tropical forests
has already been cleared (Wright, 2005), and forest loss continues
at a rapid pace—over 7 million ha/year (Achard et al., 2014).
Furthermore, tropical forests are more threatened than temperate
⇑ Corresponding author at: Migratory Bird Center, Smithsonian Conservation
Biology Institute, National Zoological Park, Washington, DC 20013-7012, USA.
E-mail address: [email protected] (L.L. Powell).
forests; tropical forests represent just 36% of the world’s landmass
but have suffered 54% of forest loss since 2001 (135 billion ha,
Global Forest Watch, 2015). Deforestation is the main threat to
tropical forests, with agricultural expansion the dominant cause
(Geist and Lambin, 2002). Accompanying an expanding agricultural landscape is the increasing network of roads that is fragmenting remaining tracts of forests, creating vast areas of edge-affected
forest, and allowing people, alien species and disease to colonize
previously inaccessible areas (Laurance et al., 2014a).
Insectivorous birds of the tropical rainforest understory (hereafter understory insectivores) are a taxonomically and ecologically
diverse group that are vulnerable to forest loss, fragmentation, and
other forms of forest degradation, making them ideal sentinels for
threatened tropical rainforests. In this introductory paper to this
special issue, we review the diversity and ecology of understory
insectivores, identify threats to the guild, discuss hypothetical
http://dx.doi.org/10.1016/j.biocon.2015.03.025
0006-3207/Published by Elsevier Ltd.
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
2
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
drivers of population declines, and offer suggestions for conservation-applied research.
1.2. This Special Issue of Biological Conservation
For the joint American Ornithologists’ Union/Cooper
Ornithological Society conference in August 2013, Powell organized a symposium on the sensitivity of understory insectivores
to the loss, fragmentation, and degradation of tropical forests.
Bringing together 13 presenters plus dozens of other researchers
from around the globe, the symposium and the discussions that
followed confirmed the need to call attention to the global risks
to this diverse avian guild.
To evaluate the effects of different types of disturbance on the
ecology and conservation of understory insectivores, a comprehensive pantropical overview is necessary. The study sites covered by
papers in this special issue occur in tropical and subtropical moist
broadleaf forest (Olson et al., 2001). The biogeographic regions covered by tropical rainforests transcend strict latitudinal limits, as
other factors such as rainfall and ocean currents affect climate
and thus the distribution of rainforest taxa. We therefore include
Pavlacky et al. (2015) as the South East Queensland Biogeo
graphic Region of Australia shares ancient origins with a previously
widespread tropical rainforest ecosystem that has contracted as
Australia has dried (Webb et al., 1984; Fig. 1). This special issue
provides representation from throughout the world’s tropical rainforests to capture much of the extraordinary diversity of understory insectivores. Nonetheless, it is important to note that this
special issue does not include contributions from important rainforest regions in Central Africa, Madagascar, New Guinea, northern
Australia and much of Asia (Fig. 1).
1.3. Overview of the taxonomy and ecology of the understory
insectivores
In the Neotropics, understory insectivores are dominated by suboscine songbirds of the antbird (Thamnophilidae), ovenbird
(Furnariidae, including woodcreepers: subfamily Dendr ocolaptinae),
antthrush
(Formicariidae),
and
tyrant-flycatcher
(Tyrannidae) families. Many Neotropical understory insectivores
participate in mixed foraging flocks. In Amazonia, for instance,
Thamnomanes antshrikes lead dozens of mostly suboscine passerines in highly stable flocks, which congregate in the same location
over months or even years (Munn and Terborgh, 1979; Powell,
1985). These multispecies Neotropical flocks defend their territories
communally, with pairs of individuals of the same species aggressively defending territorial boundaries (Jullien and Thiollay, 1998).
Interspecific territoriality is characteristic of Neotropical flocks,
which stabilizes flock cohesion in time and space, sometimes over
decades (Martinez and Gomez, 2013).
Neotropical understory insectivores are often associated with
the army ant Eciton burchellii (Willis and Oniki, 1978). Swarms of
thousands to millions of raiding ants carpet the rainforest floor,
attracting ant-following birds that capture the fleeing arthropods.
Although there have been recent research advances on ant-following birds, the system is understood in much greater detail in the
Neotropics than in the Paleotropics, primarily due to the pioneering work of E.O. Willis and colleagues (Willis and Oniki, 1978)
and more recent work by Susan Willson and Johel ChavesCampos (Willson, 2004; Chaves-Campos and DeWoody, 2008;
Chaves-Campos et al., 2009). As with mixed-flock species, ant-following birds can be either obligate (found foraging only in mixed
species or army ant swarms) or facultative (joining periodically;
Powell, 1989; Brumfield et al., 2007).
African understory insectivores have very little taxonomic overlap with their New World counterparts. African rainforest understories are dominated by several families of the Old World
superfamily Sylvioidea, including greenbuls (Pycnonotidae), Old
World warblers (Sylviidae), and several families of the superfamily
Musicapoidea, including Old World flycatchers (Muscicapidae) and
thrushes (Turdidae). In the Afrotropics mixed species foraging
flocks are less rigidly organized, occurring more as waves through
the forest (McClure, 1967). The social dynamics of mixed-species
flocks are poorly understood in Africa; however, in this issue,
Cordeiro et al. (2015) showed that in Tanzania, the Square-tailed
Drongo (Dicrurus ludwigii) was a key nuclear species in mixed-species flocks and that mixed flocks were larger in the presence of this
species. Social dynamics and the importance of ant swarms are less
known in the Afrotropics. However, it is clear that some Old World
thrushes and bulbuls follow driver ants in the genus Dorylus
(Chapin, 1932; Brosset, 1969).
Asian rainforests are also well represented by the Muscicapidae
and Sylvioidea, but particularly diverse are the babblers
(Sylvioidea: Timaliidae; Sangster et al., 2010; Corlett and Primack,
2011; Fregin et al., 2012). As is true in the Afrotropics, mixed species
foraging flocks in Asia are also not rigidly organized. These flocks
tend to be dominated by timaliid babblers and white-eyes
(Zosterops; e.g., Kotagama and Goodale, 2004; Goodale et al.,
2009). Australian rainforests harbor a diverse assemblage of understory insectivores, including pittas (Pittidae), scrub-birds and lyrebirds (superfamily Menuroidea), gerygones, thornbills and
scrubwrens (Acanthizidae), logrunners (Orthonychidae), shrikethrushes
(Colluricinclidae),
fantails
(Rhipiduridae)
and
Australasian robins (Petroicidae; Pavlacky et al., 2015). In Australia
and New Guinea, endemic families dominate, such as Australian
babblers (Pomatostomidae), Australasian warblers (Acanthizidae),
pitohuis (Pachycephalidae), fairy-wrens (Maluridae), monarch
Fig. 1. Distribution of the study sites used in this special issue. Basemaps from GlobalForestWatch.org represent the distribution of remaining forest (green) and forest change
(blue = gain, pink = loss, purple = both loss and gain) from 2001 to 2013. Two letter abbreviations refer to Brazilian and Australian states/provinces. (For interpretation of the
references to color in this figure legend, the reader is referred to the web version of this article.)
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
flycatchers (Monarchidae), and birds of paradise (Paradisaediae;
Corlett and Primack, 2011), which can be frugivorous or insectivorous. Ant-swarm attendance, however, is not reported from
Australasian rainforests.
Most understory insectivores can also be placed into several
broad groups based on foraging tactic (e.g., sallying species, arboreal gleaners, or terrestrial species). These groups make for convenient ecological classification and many birds within these groups
respond to environmental changes similarly. However, group
assignments are not always mutually exclusive; a species can be
an arboreal gleaner and be associated with army ants, such as
the White-chinned Woodcreeper (Dendrocincla merula; Johnson
et al., 2013). Many different groups are often well represented
within a single family, where species show remarkable versatility
in their foraging niches. The Neotropical family Furnariidae, for
example, includes bark-gleaners (e.g., woodcreepers; Powell
et al., 2015), professional ant-followers, obligate mixed-species
flock participants (Colorado and Rodewald, 2015), and terrestrial
insectivores (Powell et al., 2013). Although not covered in this special issue, the vangas of Madagascar (Vangidae) are perhaps even
more ecologically versatile than the Furnariidae. In the absence
of many other rainforest avian taxa in Madagascar, vangas have
evolved to fill a diverse range of niches. Included in the Vangidae
are the toucan-like Helmet Vanga (Euryceros prevostii), the barkcreeping Nuthatch Vanga (Hypositta corallirostris), the insect-probing Sickle-billed Vanga (Falculea palliata), the aerial Flycatcher
Vanga (Pseudobias wardi) and the terrestrial Crossley’s Babbler
Vanga (Mystacornis crossleyi; Corlett and Primack, 2011). This variety of niches, even within the broader foraging groups, highlights
the ability of understory insectivores to specialize and is certainly
relevant to understanding the impacts of human-caused
disturbance.
Sallying insectivores capture understory insects using aerial
foraging maneuvers in which they catch arthropods while on the
wing and return to a perch. They are often small and nimble, with
unrelated species commonly called flycatchers (e.g., Old World
Muscicapidae, New World Tyrannidae) or warblers (e.g., Old
World
Sylviidae,
New
World
Parulidae,
Australasian
Acanthizidae). In the Amazon, sallying insectivores are abundant
and species-rich in the understory and include active foragers
(e.g., many tyranid flycatchers) and species with sit-and-wait tactics (e.g., puffbirds: Galbulidae; Johnson et al., 2013). Arboreal
gleaners catch prey on plant substrates such as trunks, branches
and leaves. In the Neotropics, arboreal gleaners are exemplified
by the woodcreepers (Dendrocolaptinae). Although this group
has similar body forms, they have a remarkable array of bill adaptations from the stubby-billed Glyphorynchus spirurus (Wedgebilled Woodcreeper) to Campylorhampus scythebills, which have
absurdly long, curved bills exceeding half the length of their bodies. A number of species of pyconotid greenbuls in Africa function
as arboreal gleaners, but the diversity of foraging adaptations is not
nearly as striking.
Finally, terrestrial insectivores are usually strong-legged, drabcolored, stocky birds that make their livings by walking or hopping
along the forest floor searching for prey. Terrestrial insectivores
may simply scan the surface of the leaf litter or may be more active
by flipping leaves in search of small arthropods. The logrunners
(genus Orthonyx) of Australia and New Guinea possess highly specialized morphological adaptations for foraging in leaf litter, allowing a 90° lateral sweep of the femur (Boles, 1993). Some species
pounce on terrestrial arthropods from an elevated perch (e.g.,
Australasian robins, Petroicidae). The exceptional Ringed Antpipit
(Corythopis torquatus, Tyrannidae) is considered a terrestrial insectivore but sallies upwards for insects on the undersides of living
leaves (Ridgely and Tudor, 1994).
3
2. Why the concern about understory insectivores?
2.1. Understory insectivores are sensitive to forest degradation and
loss
Current estimates of globally threatened and near-threatened
bird species include 23% of the approximately 10,000 described
species (BirdLife International, 2015). The bulk of these species
occur in tropical forests, and because vulnerability is strongly predicted by ecological specialization (S
ß ekercioğlu, 2011), it is not surprising that one of the most at-risk groups is understory
insectivores (Tobias et al., 2013).
Studies on the effects of forest fragmentation on tropical understory birds followed soon after MacArthur and Wilson’s landmark
study on island biogeography (1967). Charles Leck, working in
Ecuador (1979), E.O. Willis and James Karr’s work on Barro
Colorado Island (Willis, 1974; Karr, 1982) and Willis’ work in isolated woodlots in the Atlantic rainforest (Willis, 1979) were among
the pioneering studies of tropical forest fragmentation. These studies identified large-bodied birds, understory insectivores, and
predatory birds as being particularly vulnerable to fragmentation.
These early studies were followed by long-term studies, notably
from the Biological Dynamics of Forest Fragments Project
(BDFFP) near Manaus, Brazil (e.g. Stouffer and Bierregaard, 1995),
and Robinson’s (1999) research in Panama. Their studies
demonstrated the relative long-term nature of species loss and
reduced abundances from fragmented and isolated habitats.
Investigations in Afrotropical forests (Newmark, 1991; Lens et al.,
2002; Beier et al., 2002; Korfanta et al., 2012), Brazil’s Atlantic rainforest (Ribon et al., 2003), and Asian rainforests (Lambert and
Collar, 2002; S
ß ekercioğlu et al., 2002; Sodhi et al., 2005; Waltert
et al., 2004) followed suit, providing further empirical evidence
on the acute sensitivity of understory insectivores to habitat fragmentation. A recent review by Bregman et al. (2014) largely confirmed that relative to other guilds, insectivores in the tropics are
most at risk from habitat fragmentation across habitats and geographic regions.
Understory insectivores are differentially affected by deforestation, fragmentation and disturbance. Of the different foraging tactics, terrestrial insectivores may be among the most sensitive, as
several studies across tropical regions have shown that this group
is among the first to disappear when the forest is disturbed
(Stratford and Stouffer, 1999; Canaday and Rivadeneyra, 2001;
Peh et al., 2005; Pavlacky et al., 2015) and among the last to return
after pasture abandonment and subsequent forest regrowth
(Powell et al., 2013, 2015). Of nine species of terrestrial insectivores studied by Stratford and Stouffer (1999) that occurred in eleven forest fragments, only a single species was able to colonize
forest fragments < 100 ha after their isolation – the Thrushlike
Antpitta (Myrmothera campanisona), a species associated with treefalls and other disturbance (Stratford and Stouffer, 2013). Most of
the species that were present before the fragments were isolated
(74 occurrences) were absent after isolation (19 occurrences;
Stratford and Stouffer, 1999).
Whereas agriculture is the primary agent to forest loss and fragmentation globally (Geist and Lambin, 2002), there is considerable
variability in the types of threats that understory insectivores face;
these include timber harvesting, agriculture and infrastructure/
urbanization (sensu Sodhi et al., 2008). The Asian peninsula has been
proportionally hardest hit by deforestation due to urbanization
(Castelletta et al., 2000; Sodhi et al., 2008). The remaining larger
wild tracts of Malaysia and Indonesia, and now parts of Papua
New Guinea, have succumbed and continue to be affected by the
oil palm industry, with logging being an additional agent of disturbance (Boucher et al., 2011). In Africa, particularly upper Guinea
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
4
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
forests (Arcilla et al., 2015), logging and associated fragmentation
and habitat loss continue to be chief threats. In Australia, approximately 20% of tropical rainforest and 60% of subtropical rainforest
has been cleared within the last 200 years (Catterall et al., 2004).
Although the majority of Australian rainforest has been protected
since 2000, the restoration and conservation of remnant rainforests
are ongoing challenges (Bradshaw, 2012; Catterall et al., 2004). In
the Neotropics, agricultural expansion for soybean and cattle
ranching dominate as agents of forest loss, and urbanization has
continued to play a major role in deforestation, especially cities
that function as major transportation hubs in the large expanses
of forests. On the bright side, over the last ten years, Brazil has used
remote sensing and enforcement to considerably slow deforestation rates in the Amazon (Macedo et al., 2012).
Urbanization and major road development are particularly worrisome globally. As human populations grow and become increasingly urbanized, urban areas expand, but this is a land conversion
that becomes a permanent feature of the landscape (Pickett et al.,
2001). Urbanization is expected to accelerate in developing
countries where human population growth is concentrated
(McDonald et al., 2008), and its negative impact on forest birds is
already well known (Borges and Guiherme, 2000; Lim and Sodhi,
2004).
2.2. Understory insectivores are important members of tropical forests
Lagging behind our ability to document patterns is our quest to
understand the ecological consequences of bird species loss. In a
seminal meta-analysis of 113 experiments evaluating the trophic
cascades among insectivorous vertebrates (birds, bats and lizards),
invertebrates and plants, Mooney et al. (2010) found that predation by vertebrates reduced predatory and herbivorous invertebrates by 38% and 39%, respectively. This led to an indirect
benefit for plants with damage reduced by 40% and biomass
increasing by 14%. Given the conservation implications of these
findings for vertebrates as a whole, comparable experimental
research to quantify the direct and indirect effects of understory
insectivores on ecosystems (i.e., ecosystem services) is particularly
needed. However, several new studies have been instructive. For
example, Michel et al. (2014) found that Costa Rican plants suffered greater plant damage when understory birds were excluded
from rainforest interior plants. Additionally, species loss may have
consequences for organisms that interact with insectivores, such as
the skippers (Lepidoptera) that are associated with the feces of
army-ant following birds (Devries et al., 2008). We know so little
about most tropical birds that we have not identified their diets
beyond insect orders, nor do we know the impact of their foraging
on prey abundance. We do know that invertebrate and vertebrate
predators, such as frogs and lizards are consumed by some understory insectivores (Chesser, 1995; Poulin et al., 2001). Thus, losing
understory insectivores in forested ecosystems may have cascading effects that go beyond their direct effects on prey, but affect
multiple trophic levels (Stratford and S
ß ekercioğlu, in press). This
is clearly an area needing more research.
3.1. Vegetation changes
Tropical birds, particularly insectivores, are closely tied to vegetation structure (Stratford and Sßekercioğlu, in press). Thus removing forest and converting it to some other land use (e.g., oil palm
plantations, cropland, or urban) will make these sites unusable
for most understory insectivores. Not all forest disturbances are
so dramatic; selective logging and shade grown coffee plantations
are examples of forest disturbances where some of the forest structure remains intact. Selective logging in Amazonian (e.g. Thiollay,
1997) and Bornean forests (Lambert, 1992) was associated with
the loss of understory insectivores, whereas in this issue, Arcilla
et al. (2015) found that generalists were more vulnerable to logging than specialists in the rainforests of Upper Guinea, an
African biodiversity hotspot. In Australian rainforests, understory
insectivores declined with reduced stand basal area and subsequent invasion of a thicket-forming weed (Pavlacky et al., 2015).
If they are properly managed with an adequate overstory,
Neotropical and African shade coffee plantations can have greater
diversity of understory insectivores than sun coffee plantations
(Greenberg et al., 1997). African shade coffee plantations in
Ethiopia have more understory insectivore species than rainforest,
but understory forest specialists are most abundant in rainforest
(Buechley et al., 2015). Neotropical shade-grown plantations have
reduced species richness compared to forested sites, but maintain
large numbers of wintering migratory birds (Greenberg et al.,
1997). Forest fragments, even if not directly affected by humans,
will have altered vegetation. Edge effects include reduced canopy
cover and more dense undergrowth (Laurance et al., 2002). In this
issue, Stratford and Stouffer (2015) found that fragmentation-sensitive Neotropical species were associated with some elements of
vegetation structure that were not found in 10- and 1-ha forest
fragments. However, in a montane Kenyan forest, the Whitestarred Robin (Pogonocichla stellata), was able to use fragments
despite the vegetation differences between fragments and larger
forest tracts (Githiru et al., 2007). These differences between
Neotropical and Afrotopical understory insectivores are perplexing, and research would benefit from a broader unified approach.
It remains unknown how the relationship between vegetation
structure and understory insectivores scales up to larger landscapes. In this issue, Anjos et al. (2015) predicted that more specialists would be found in the botanically rich evergreen forests
of the Atlantic Rainforest of Brazil compared to the nearby evergreen-deciduous mixed forest and semideciduous forest types.
However the mixed forests had the same number of specialists
as the evergreen forest. In Gondwana Rainforests of Australia,
stand condition at the local scale was a somewhat better predictor
of avian species richness than forest composition at the landscape
scale, with less support for the effects of patch size and isolation
(Pavlacky et al., 2015). A standardized protocol for quantifying vegetation would allow researchers to test hypotheses related to the
relationship between birds and their sensitivities to vegetation
structure. Terrestrial laser scanning (Richardson et al., 2014) is
one emerging technology that would assist in standardizing vegetation measurements, as well as in reducing error and effort.
3.2. Reduced prey abundance
3. Why are understory insectivores lost from degraded and
fragmented forests?
A number of hypotheses been have proposed (Robinson and
Sherry, 2012; Stratford and Robinson, 2005) that are based on
the focal species responses to forest disturbance (e.g., sensitivity
to microclimate in fragments) or based on species interactions in
disturbed areas (e.g., increased nest predation in fragments).
The effect of forest disturbance on prey abundance and the
potential effect on understory insectivores are logistically difficult
to test. Trophic interactions between understory birds and insects
are complicated by species rich invertebrate communities (Lawton
et al., 1998), highly specialized avian diets (Sherry, 1984) and
undocumented dietary composition. The few tests of the prey-limitation hypotheses lend little support. For example, Sßekercioğlu
et al. (2002) found no differences in insect abundance between
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
fragments and forest. Although prey abundance may not be important, how prey is captured (foraging tactic) consistently emerges as
a predictor of sensitivity to disturbance, which may result more
from microhabitats searched than prey types per se. For example,
in this issue, Arcilla et al. (2015) found that sallying insectivores
were more sensitive to logging in African forests than other species. Answering whether loss of microhabitat structure or a
decrease in prey type could induce such an effect is vital, and in
this issue, Hamer et al. (2015) offer a direction toward this answer
based on stable isotopes, a technique that has seldom been applied
in the tropics. The authors determined that Bornean birds at higher
trophic levels are more vulnerable to disturbance (Hamer et al.,
2015), thereby suggesting a link between diet and vulnerability.
We suggest researchers further try to establish the link between
diet and vulnerability, by taking advantage not only of stable isotope analysis, but also DNA barcoding to identify prey items at ever
finer taxonomic scales, allowing for targeted assessment of prey
abundance and type. Many soft-bodied insects are quickly
digested, creating a negative bias for those taxa (Rosenberg and
Cooper, 1990). Further, techniques that sample vegetation for
arthropods are often biased (Cooper et al., 2012), and do not
necessarily sample the same arthropods that birds eat. Genetic
sequencing approaches using feces (i.e., molecular scatology) have
been mostly limited to mammals and other taxa with separate
solid and liquid waste extraction. However, high throughput
(AKA next generation) sequencing can use feces to quantify songbird diets non-invasively (Jedlicka et al., 2013; Vo and Jedlicka,
2015) with basic (i.e. often order- or family-level) but rapidly
improving taxonomic specificity. Using these new genetic techniques, we can look at the mechanisms for disappearances of
understory birds through differences in diet; in other words, does
what birds are eating change with disturbance – are they eating
fewer calorie-rich arthopods in disturbed areas? This technique
can also help us understand how vegetation structure (Stratford
and Stouffer, 2015) or light/heat (Pollock et al., 2015) interact with
arthropod communities, and ultimately understory bird communities. Although this technique is currently costly (lab costs of
$10,000 per instrument run of several hundred feces samples),
sequencing runs are increasingly affordable with newer and more
efficient sequencing machines. Furthermore, in tropical institutions where resources are scarce, opportunities can be cultivated
through collaboration with researchers in wealthier economies,
thus helping to bridge the economic divide and, at the same time,
increase local capacities.
3.3. Altered microclimate
The vegetation hypothesis does not rule out the possibility
that the same changes in vegetation induced by edge effects
are also associated with microclimate changes such as increased
light intensity and increased temperatures. These changes may
themselves make fragments physiologically unsuitable for understory birds (Stratford and Robinson, 2005). Patten and SmithPatten (2012) found that light was one of the key factors in edge
avoidance by disturbance-sensitive species. In this issue, Pollock
et al. (2015) also found that many understory insectivores
avoided brighter sites. Light can affect birds directly by
interfering with searching for prey or indirectly by behavioral
avoidance. Histological comparisons of retinas and behavioral
experiments that compare microclimate sensitive species with
generalists may also permit us to untangle the confounding interactions between vegetation structure, prey availability, and
microclimate.
5
3.4. Dispersal limitation
In small populations, such as those in forest fragments, extinction is inevitable and maintenance of metapopulations relies on
organisms being able to disperse throughout the landscape
(Hanski, 1994, 1998). Whereas dispersal limitation may not provide a mechanism of species loss per se, it can limit re-colonization of truly isolated fragments—even if they contain suitable
habitat. Stouffer and Bierregaard (1995) proposed that fragmentation-sensitive understory insectivores, particularly terrestrial insectivores, had limited dispersal ability in Manaus, Brazil.
Similarly, Lens et al. (2002) showed that the inability to move
between and among fragments coupled with tolerance to habitat
disturbance reduced the ability of species to persist in an East
African fragmented forest landscape. Many understory insectivores are sedentary residents with short wings (i.e., low wing
aspect ratio), relatively poor flying ability (Moore et al., 2008),
and from the little we know, relatively short dispersal distances
(<400 m for five Amazonian species, Bates, 2002; median for
Thamnophilus atrinucha: 300 m, Tarwater, 2012; median for
Myrmeciza exsul: 800 m, Woltmann et al., 2012b) which may
make them poor dispersers and thus vulnerable to local extinction in fragmented landscapes (Lens et al., 2002; Claramunt
et al., 2012; Woltmann et al., 2012a; Powell, 2013).
The nature of the matrix between habitable patches will influence dispersal decisions. Stouffer and Bierregaard (1995), found
colonization rates of forest fragments by understory insectivores
were strongly influenced by the major vegetation types surrounding fragments. Asymmetric dispersal from intact to fragmented
rainforests resulted in source-sink dynamics for a sedentary, terrestrial insectivore, Australian Logrunner (Orthonyx temminckii),
but the immigration rates declined when the between-population
landscapes were fragmented (Pavlacky et al., 2012). In this issue,
Powell et al. (2015) show that two Amazonian woodcreeper species recover to primary forest-like movement rates in secondary
forest only about 15 years old. However, a terrestrial species of
the forest interior, the Rufous-capped Antthrush (Formicarius
colma), showed reduced movement into secondary forest even
three decades after pasture abandonment.
3.5. Area sensitivity
Understory insectivores will be absent from small forest fragments if they are area-sensitive and unable to use the surrounding
matrix to supplement their dietary and breeding requirements. As
deforestation and fragmentation continue to push understory
insectivores into increasingly smaller fragments of primary forest,
it becomes critical to understand the minimum area requirements
of understory bird species (Sodhi et al., 2008). In Manaus, Brazil the
Minimum Critical Size of Ecosystems Project (later renamed the
BDFFP) was designed to address the question of the minimum size
of rainforest required to maintain the animal community
(Bierregaard et al., 1992). Though originally slated for several
1000 ha fragments, the project eventually isolated just two
100 ha fragments, four 10 ha fragments and five 1 ha fragments.
Nevertheless, results clearly showed that even 100 ha fragments
are not nearly large enough to sustain the entire understory bird
community (Stouffer et al., 2011), and the critical minimum fragment size required to do so remains unclear in the Neotropics
and elsewhere. Importantly, after isolation (and subsequent re-isolations) forest fragments at the BDFFP occurred as small ‘‘islands’’
within a vast ‘‘sea’’ of continuous forest, whereas many other fragmented landscapes are heavily deforested, but are separated by a
matrix of cultivation (e.g. Newmark, 1991) or mixed second
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
6
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
growth and cultivation (e.g. Lens et al., 2002; Peters and Okalo,
2009).
Given the enormous increases edge habitat and secondary forest in the tropics, it is critical that we embrace the shift from binary
approaches (i.e., habitat/no habitat) with origins in Island
Biogeography Theory (MacArthur and Wilson, 1967) toward landscape ecology approaches that incorporate crucial edge and matrix
effects (Laurance, 2008). Secondary forest matrices are now pervasive throughout the tropics; for example, by 2002, the area of secondary forest in the Brazilian Amazon had increased to
161,000 km2, about the size of Uruguay (Neeff et al., 2006). Once
sufficiently mature, secondary forest can buffer some of the effects
of area and isolation (Stouffer and Bierregaard, 2007; Powell et al.,
2013, 2015), allowing previously isolated forest fragments to be
connected by a more amenable matrix. Granted, there is no substitute for primary forest to sustain biological diversity (Gibson et al.,
2011), but anthropogenic habitats such as shade coffee and secondary forests may help conserve understory insectivores in the
form of buffers, corridors for dispersal and other landscape connections. However, the extent to which these altered habitats provide
viable breeding opportunities for rainforest interior species is not
fully understood.
3.6. Nest predation
The mesopredator release hypothesis posits that fragmented
landscapes have reduced top predators, which allows for the population increase of mesopredators that can reduce avian populations through increased nest predation (Crooks and Soule,
1999; Schmidt, 2003). In fragmented tropical forests, evidence
for the mesopredator release hypothesis is equivocal (Robinson
and Sherry, 2012). Nest success is highly variable, making inferences about fragmentation effects difficult (Robinson et al.,
2000). In this issue, Visco and Sherry (2015) examined nest predation and predators on Chestnut-backed Antbirds (M. exsul) in Costa
Rica, finding that predation rates were lower in forest fragments
than in a large forest tract, providing evidence against the
mesopredator release hypothesis—at least for one avian species.
One clear result is that snakes are the primary nest predators in
Panama (Robinson et al., 2005) and Costa Rica (Visco and Sherry,
2015). There are fewer studies of nest predation on understory
insectivores from tropical sites outside of the Neotropics. In
Africa, Githiru et al. (2005) used plasticine eggs to find that mammals were the primary nest predators and fragments of comparable sizes experienced similar predation rates. In Malaysia, Cooper
and Francis (1998) used artificial nests and found predation rates
were highest along edges of logged forests and lowest in intact forests. Great caution should be used in interpreting the differences
between sites since different methods of inferring nest predation
(i.e., using unmanipulated natural nests, artificial nests with quail
eggs, or artificial nests with plasticine eggs) will reveal different
sets of nest predators (Moore and Robinson, 2005). Furthermore,
a remarkable result from the Taita Hills, Kenya, showed that in
one understory insectivore species persisting in fragments and
with a 69% overall rate of nest predation over three years of study,
nest predation was lower at the edge than interior (Spanhove et al.,
2014). With additional studies from the understudied Paleotropics,
the potential to develop a conceptual framework around nest predation is more likely. We therefore urge more studies of nest predation at tropical sites, particularly in Paleotropical forests, using
videography to monitor nests.
3.7. Emerging threats: Infectious diseases and climate change
Increased international trade and transportation is predicted to
intensify the incidence of wildlife diseases (Pongsiri et al., 2009).
Already, several diseases, such as Newcastle disease, West Nile
and avian malaria (Plasmodium spp. and Haemoproteus spp.) are
quickly spreading globally and generally have strong negative
effects on naïve bird populations (Kilpatrick et al., 2007;
Svensson-Coelho et al., 2013; Asghar et al., 2015). An important
example is that of the introduced avian malaria Plasmodium relictum in Hawaii, where the endemic honeycreeper, ‘Apapane
Himatione sanguinea, was estimated to have lost >50% of first-year
juveniles and >25% of adults due to this parasite over a 7-year period (Atkinson and Samuel, 2010). This mortality was closely tied to
season, where optimum weather conditions (rainfall and temperature) in the fall promoted mosquito abundance, thus increasing
infection rates. In Hawaii, the distribution of native forest birds is
presently impacted by a range of environmental factors, particularly avian malaria (van Riper III et al., 1986). Recent phylogenetic
and ancestral reconstruction analyses of avian malarial parasites in
three African ecosystems, two of them rainforests, showed almost
a four times greater evolutionary transition rate for generalist
parasites to become specialists than the reverse (Loiseau et al.,
2012). A concern here is that as malaria-competent generalist
avian hosts invade increasingly disturbed rainforest tracts, the
chance of introducing novel parasites to susceptible specialist
understory insectivores increases, thus posing a potentially severe
conservation threat. These studies exemplify that this body of
research is urgently required, especially baseline data before
emerging infectious diseases become pandemic.
Although an obvious effect of human activity is how we alter
landscapes though land-use change, humans are also altering the
climate in ways that less directly impact tropical birds. In particular, precipitation regimes in the tropics will change in the future
and will affect birds by altering plant communities (Rompre
et al., 2007; Harris et al., 2011; Wormworth and S
ß ekercioğlu,
2011; Sßekercioğlu et al., 2012). Changing precipitation in the tropics will also impact invertebrate prey populations that could affect
understory insectivores in ways that are not necessarily predictable (Sßekercioğlu et al., 2012). For example, changing precipitation affects tropical tree phenology (Walther et al., 2002),
which will affect the amount of leaf litter and, in turn, affect leaf
litter arthropods. Additionally, altered precipitation regimes will
affect fire dynamics (Román-Cuesta et al., 2014), including the
penetration of fire into forest fragments (Laurance et al., 2014b).
Effects of climate change will likely occur in all tropical sites, and
a coordinated effort to get baseline data on abundances and distributions should be pursued as quickly as possible. Because the
effort required to get these baseline data exceeds the number of
professional tropical ornithologists, wherever feasible we urge
the development of citizen-science projects. In this issue, Boyle
and Sigel (2015) show that a standardized citizen science approach
can quantify avian populations over large scales.
4. Where to go from here? A research prospectus for the ecology
and conservation of understory insectivores
4.1. Increase geographic coverage
Of paramount importance is to identify the ecological and taxonomic groups that are most sensitive to forest loss and degradation
and how these patterns vary geographically. Patterns of species’
sensitivities are known for many lowland Neotropical forests
(e.g., Robinson, 1999; Stouffer and Bierregaard, 1995; Sigel et al.,
2010), but are poorly known in most other tropical forests.
Researchers should focus efforts on filling these geographic gaps
in our knowledge. Examples of such recent initiatives include the
Equatorial Guinea Bird Initiative (https://www.kickstarter.com/
projects/1663751187/equatorial-guinea-bird-initiative) from the
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
Lower Guinea Forests of Central Africa, and species recovery in
newly afforested sub-tropical forests of China (Zhang et al.,
2011). An additional example is that of the Stability of Altered
Forest Ecosystems (SAFE) Project that offers new opportunities to
experimentally research the effects of forest fragmentation on
understory insectivores (among other taxa) in Borneo, where primary rainforests are under immediate threat from oil palm expansion (Ewers et al., 2011). Tropical regions that require more
research to note patterns of impacted species include Africa,
Southeast Asia, western India, and Madagascar. We understand
very little of the ecological roles of understory insectivores
pantropically, as well as the consequences on ecosystems when
these communities are altered.
4.2. Standardizing efforts to understand the guild: a pantropical effort
To understand the vulnerabilities faced by understory insectivores, we need to understand if they respond similarly to equivalent threats from different biogeographic realms and if the
mechanisms of sensitivity are similar. Currently, there is no consensus on either of these aspects, and the causes are likely to vary
geographically (Stratford and Robinson, 2005). Not since David
Pearson (1977) worked in Ecuador, Bolivia, Peru, Gabon, Borneo
and New Guinea has an ornithologist attempted a standardized
cross-continental comparison of tropical rainforest bird communities, and a pantropical comparison has never been undertaken
from a conservation standpoint. To date, pantropical comparisons
have been difficult, including in this special issue, because research
questions and subsequent study designs are not standardized
among studies. For example, just within this special issue,
responses of understory insectivores to disturbance are quantified
with movement rates (Powell et al., 2015), nest success (Visco and
Sherry, 2015), audiovisual sampling (Boyle and Sigel, 2015;
Cordeiro et al., 2015; Pavlacky et al., 2015), experimental playbacks
(Cordeiro et al., 2015), and mist-net derived species richness estimates (Arcilla et al., 2015; Buechley et al., 2015). Granted, no one
‘‘correct’’ metric exists to quantify understory birds’ vulnerability
to disturbance, but coordinated efforts and study designs will
greatly facilitate cross-tropical comparisons. For example, standardized mist-netting specifically designed to estimate survival
(sensu Ruiz-Gutiérrez et al., 2012) in primary forest vs. disturbed
forest (e.g. edge, fragments, secondary forest) can provide both a
direct estimate of fitness (i.e. survival) as well as comparisons of
community composition across habitats and rainforest regions.
Wolfe et al. (2014) used mist-netting efforts in an analysis of variation in understory insectivore survival across primary forests in
Amazonia; similar efforts could be undertaken that incorporate
degraded forests and across rainforest regions. Such standardized
designs will help identify characteristics of understory insectivores
(e.g. wing aspect ratio, dispersal ability, small body size, trophic
level, foraging technique) that make them vulnerable to disturbances, not only locally, but also globally across the tropics. Even
a rudimentary understanding of the characteristics that make
understory insectivores vulnerable to disturbances across rainforest regions will help focus conservation actions on the most vulnerable taxa. Continued collaborative efforts through symposia,
workshops, grant proposals, review papers and meta-analyses will
help foster a more coordinated, global effort.
4.3. Standardizing how we study threats to understory insectivores
To design an effective standardized protocol, researchers must
first agree on the most pressing question(s) as determined by factors threatening tropical understory birds. Researchers could focus
on myriad factors including (i) agriculture (Buechley et al., 2015),
(ii) forest edges, (iii) fragmentation per se (Pavlacky et al., 2015;
7
Cordeiro et al., 2015), (iv) habitat loss (Pavlacky et al., 2015), (v)
degradation and logging (Hamer et al., 2015; Arcilla et al., 2015),
(vi) natural enemies, (vii) climate change, or (viii) emerging infectious diseases. Given that climate change and habitat loss are the
greatest threats to biodiversity today (Sala et al., 2000), and vulnerability to climate change is very difficult to estimate empirically
(Wormworth and Sßekercioğlu, 2011), we suggest that a more practical approach would be to examine the effects of habitat loss,
which in the tropics is driven primarily by expansion of agricultural fields, such as oil palm plantations in Australasia (Boucher
et al., 2011). Thus one critical question that needs to be addressed
pantropically is how to manage human-modified landscapes that
support sustainable populations of the understory bird community. Furthermore, identifying the characteristics of species lost
from smaller, more isolated areas are of great interest at the local
and landscape scales. Likewise, it is essential to know (in a
pantropical framework) maximum distance from the edge of an
oil palm (or other) plantation at which the primary forest understory bird community is affected, and to understand the characteristics of the species that drop out of the community when
approaching the edge. Evaluating the consequences of forest modification with remnant patches embedded in a broader landscape
context may provide additional insights for the conservation of
understory insectivores (Laurance, 2008). If we can understand
the characteristics that make birds vulnerable to disturbances in
a standardized pantropical framework, then we can apply general
conservation and management guidelines worldwide without an
in-depth knowledge of the avifauna in a given location. This is critical as some biomes (Atlantic rainforest, (Anjos et al., 2015), Upper
Guinea forests (Arcilla et al., 2015)) may be disappearing too fast to
fully understand the vulnerabilities of the bird community.
Coordinating our efforts to standardize studies of relevant disturbances pantropically and to standardize how we quantify life-history characteristics that may indicate vulnerability to disturbances
will be critical as tropical forests continue to be lost and degraded.
4.4. Mixed-species flocks and ant-following birds: what we know and
what we are missing
Understanding the dynamics of mixed-species flocks and antfollowing birds will be essential as disturbance continues to accelerate in tropical forests because these groups consist of species
that depend on the presence of other species, so conservation
efforts cannot simply be species-specific. For example, in this issue
Cordeiro et al. (2015) showed that the Square-tailed Drongo (D.
ludwigii) is a key nuclear species in East African mixed-species
flocks, and that flocks are larger in the presence of this species.
Similarly, in ant-following flocks in Kenyan fragments, species
richness of flocks declined in smaller fragments and degraded forest, and this decline was largely attributed to reduced abundance
of specialized ant-followers (Peters et al., 2008). The relevance of
these findings is underscored by evidence showing that, in
mixed-species flocks, nuclear species or flock leaders maintain
beneficial associations with other flocking species (Hino, 1998;
Srinivasan et al., 2010), especially among insectivores (Kotagama
and Goodale, 2004). Such associations have their rewards: species
that frequent flocks increase their survival (Jullien and Clobert,
2000; Cruz-Angón et al., 2008) and therefore losing flock leaders
that help aggregate such flocks can ultimately diminish avian communities in multiple ways (Dolby and Grubb, 2000; MaldonadoCoelho and Marini, 2004; Stouffer and Bierregaard, 1995). Will
conservation efforts directed at flock leaders have a disproportionately positive effect? Will the loss of mixed-species flocks from
fragmented landscapes have major impact on prey populations?
How do urban and suburban habitats affect flock composition?
These are issues begging more research, especially because a
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
8
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
number of understory insectivores are among those specialized
species that either join mixed-species flocks or follow ant swarms.
Our knowledge about mixed-species flocks and ant-following
species continues to grow, especially in Asia and Africa, as compared to the relatively better-known Neotropics. However, there
is much opportunity for discovery in all regions. In this issue,
Colorado and Rodewald (2015) show that in the Andes, anthropogenic habitats with overstory trees can help promote mixedspecies flock presence, but that only flocks in rainforest retain
forest specialists such as bark and foliage insectivores. Furthermore,
Mokross et al. (2014) found that in the central Amazon, associations among flocking species break down with increased disturbance. Ant-following birds tend to disappear quickly as army-ants
are excluded after forest fragmentation in the Neotropics
(Stouffer and Bierregaard, 1995) and Africa (Peters and Okalo,
2009), but at least in Amazonia, these groups seem to recover in
<30 years if secondary forest is allowed to regenerate (Powell
et al., 2013). Generally speaking, understanding the dynamics of
these fascinating examples of convergent evolution of multi-species social systems can be generalized to promote a pantropical
understanding of tropical understory bird ecology.
5. Conclusions
The papers in this special issue fill many gaps in our understanding of tropical understory insectivores, but several crucial
questions remain unanswered. Many of the results from these
papers were unexpected. For instance, Anjos et al. (2015) found
that the forests with the highest plant diversity did not have the
most habitat specialists, Boyle and Sigel (2015) found smaller-bodied birds were more sensitive to habitat loss than larger-bodied
birds, and Buechley et al. (2015) found greater species richness
of understory insectivores in Ethiopian shade coffee farms than
in nearby forest. Arcilla et al. (2015), working in Ghanaian forests,
found that the relative abundance of understory generalists was
lower in logged than unlogged forest, a result contrasting numerous tropical studies suggesting that forest specialists are more
negatively impacted (Bregman et al., 2014). Understory insectivores in Gondwana rainforests of Australia are often considered
resilient to landscape change, yet many of the life history traits
involved with vulnerability are inherent to this group (Pavlacky
et al., 2015). In fact, there were few consistencies between tropical
sites in findings or in techniques.
More generally, we need to expand our basic understanding of
the effects of forest disturbance on understory insectivores, especially in understudied locations. Research should be standardized
to maximize the probability that important generalities will
emerge, with which meaningful conservation actions can be
applied pantropically. These studies should be followed by tests
of hypotheses to determine the mechanisms of species loss.
Some of these hypotheses require natural history data related to
diet, social interactions, and habitat requirements. Additionally,
landscape modeling incorporating dispersal abilities can improve
conservation strategies. We recognize the complexities involved
in the causes and conservation of understory insectivores and we
hope this special issue encourages collaboration among conservation biologists, particularly between institutions from
advanced economies and developing nations in the tropics. It is
through such collaborative networks that infrastructure develops
and scientific capacity grows, ultimately supporting more strategic
conservation measures for tropical understory insectivores.
Acknowledgments
The authors would like the thank Richard Primack, Mauro
Galetti, Senthil Annamalai R., and Sandra Broese for help with this
special issue. We thank Nicole Arcilla, Jeffrey Brawn, Evan
Buechley, Keith Hamer, Luc Lens, David Pavlacky Jr., Henry
Pollock, James Remsen, Çağan S
ß ekercioğlu, Phil Stouffer and Tom
Sherry for providing friendly reviews of this manuscript, and
David Pavlacky with help on Australian bird ecology. A constructive review from an anonymous reviewer improved this manuscript. We acknowledge and thank both the governmental and
non-governmental organizations that allowed for field studies on
their lands as well as the local people that share the forest with
us and the diversity around them.
References
Achard, F., Beuchle, R., Mayaux, P., Stibig, H.J., Bodart, C., Brink, A., Carboni, S.,
Desclée, B., Donnay, F., Eva, H.D., Lupi, A., Raši, R., Seliger, R., Simonetti, D., 2014.
Determination of tropical deforestation rates and related carbon losses from
1990 to 2010. Glob. Change Biol. 20, 2540–2554.
Anjos, L., Collins, C., Holt, R., Volpato, G., Lopes, E., Bochio, G., 2015. Can habitat
specialization patterns of Neotropical birds highlight vulnerable areas for
conservation in the Atlantic rainforest, southern Brazil? Biol. Conser., this issue.
Arcilla, N., Holbech, L.H., O’Donnell, S., 2015. Severe declines of understory birds
follow illegal logging in Upper Guinea forests of Ghana, West Africa. Biol.
Conser., this issue.
Asghar, M., Hasselquist, D., Hansson, B., Zehtindjiev, P., Westerdahl, H., Bensch, S.,
2015. Hidden costs of infection: chronic malaria accelerates telomere
degradation and senescence in wild birds. Science 347, 436–438.
Atkinson, C.T., Samuel, M.D., 2010. Avian malaria Plasmodium relictum in native
Hawaiian forest birds: epizootiology and demographic impacts on8 apapane
Himatione sanguinea. J. Avian Biol. 41, 357–366.
Bates, J.M., 2002. The genetic effects of forest fragmentation on five species of
Amazonian Birds. J. Avian Biol. 33, 276–294.
Beier, P., Van Drielen, M., Kankam, B.O., 2002. Avifaunal collapse in West African
forest fragments. Conserv. Biol. 16, 1097–1111.
Borges, S.H., Guiherme, E., 2000. Comunidade de aves em um fragmento florestal
urbano em Manaus, Amazonas, Brasil. Ararajuba 8, 17–23.
Buechley, E.R., S
ß ekercioğlu, Ç.H., Atickem, A., Gebremichael, G., N’dungu, J.K.,
Mahamued, B.A., Beyene, T., Mekonnen, T., Lens, L., 2015. Importance of
Ethiopian shade coffee farms for forest bird conservation. Biol. Conser., this
issue.
Bierregaard, R.O., Lovejoy, T.E., Kapos, V., dos Santos, A.A., Hutchings, R.W., 1992.
The biological dynamics of tropical rainforest fragments. Bioscience 42, 859–
866.
Birdlife International, 2015. Birdlife Data Zone [WWW Document]. <http://www.
birdlife.org/datazone/home> (accessed 02.02.15).
Boyle, A., Sigel, B.J., 2015. Ongoing changes in the avifauna of La Selva Biological
Station, Costa Rica: twenty-three years of Christmas Bird Counts. Biol. Conser.,
this issue.
Bregman, T.P., S
ß ekercioğlu, Ç.H., Tobias, J.A., 2014. Global patterns and predictors of
bird species responses to forest fragmentation: implications for ecosystem
function and conservation. Biol. Conserv. 169, 372–383.
Brumfield, R.T., Tello, J.G., Cheviron, Z.A., Carling, M.D., Crochet, N., Rosenberg, K.V.,
2007. Phylogenetic conservatism and antiquity of a tropical specialization:
army-ant-following in the typical antbirds (Thamnophilidae). Mol. Phylogenet.
Evol. 45, 1–13.
Brosset, A., 1969. La vie sociale des oiseaux dans une foret equatoriale du Gabon.
Biol. Gabonica 5, 29–69.
Boles, W.E., 1993. A logrunner Orthonyx (Passeriformes: Orthonychidae) from the
Miocene of Riversleigh, north-western Queensland. Emu 93, 44–49.
Boucher, D.H., Boucher, D., Elias, P., Lininger, K., May-Tobin, C., Roquemore, S.,
Saxon, E., 2011. The root of the problem: what’s driving tropical deforestation
today? Union of Concerned Scientists, 113 pp. <http://www.ucsusa.org/sites/
default/files/legacy/assets/documents/global_warming/UCS_RootoftheProblem_
DriversofDeforestation_FullReport.pdf>.
Bradshaw, C.J.A., 2012. Little left to lose: deforestation and forest degradation in
Australia since European colonization. J. Plant Ecol. 5, 109–120.
Canaday, C., Rivadeneyra, J., 2001. Initial effects of a petroleum operation on
Amazonian birds: terrestrial insectivores retreat. Biodivers. Conserv. 10, 567–
595.
Castelletta, M., Sodhi, N.S., Subaraj, R., 2000. Heavy extinctions of forest avifauna in
Singapore: lessons for biodiversity conservation in Southeast Asia. Conserv.
Biol. 14, 1870–1880.
Catterall, C.P., Kanowski, J., Wardell-Johnson, G.W., Proctor, H., Reis, T., Harrison, D.,
Tucker, N.I.J., 2004. Quantifying the biodiversity values of reforestation:
perspectives, design issues and outcomes in Australian rainforest landscapes.
In: Lunney, D. (Ed.), Conservation of Australia’s Forest Fauna. Royal Zoological
Society of New South Wales, Mosman, New South Wales, Australia, pp. 359–
393.
Chapin, J.P., 1932. The birds of the Belgian Congo, Part I. Bull. Am. Mus. Nat. Hist. 65,
1–756.
Chaves-Campos, J., DeWoody, J.A., 2008. The spatial distribution of avian relatives:
do obligate army-ant-following birds roost and feed near family members? Mol.
Ecol. 17, 2963–2974.
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
Chaves-Campos, J., Araya-Ajoy, Y.M., Lizana-Moreno, C.A., Rabenold, K.N., 2009. The
effect of local dominance and reciprocal tolerance on feeding aggregations of
ocellated antbirds. Proc. Roy. Soc. B: Biol. Sci. 276, 3995–4001.
Chesser, R.T., 1995. Comparative diets of obligate ant-following birds at a site in
northern Bolivia. Biotropica 27, 382–390.
Claramunt, S., Derryberry, E.P., Remsen, J.V., Brumfield, R.T., 2012. High dispersal
ability inhibits speciation in a continental radiation of passerine birds. Proc.
Roy. Soc. B: Biol. Sci. 279, 1567–1574.
Colorado, G.J., Rodewald, A.D., 2015. Response of mixed-species flocks to habitat
alteration and deforestation in the Andes. Biol. Conser., this issue.
Cooper, D.S., Francis, C.M., 1998. Nest predation in a Malaysian lowland rain forest.
Biol. Conserv. 85, 199–202.
Cooper, N.W., Thomas, M.A., Garfinkel, M.B., Schneider, K.L., Marra, P.P., 2012.
Comparing the precision, accuracy and efficiency of branch clipping and sweep
netting for sampling arthropods in two Jamaican forest types. J. Field Ornithol.
83, 381–390.
Cordeiro, N.J., Borghesio, L., Joho, M.P., Monoski, T.J., Mkongewa, V.J., Dampf, C.J.,
2015. Forest fragmentation in an African biodiversity hotspot impacts mixedspecies bird flocks. Biol. Conser., this issue.
Corlett, R.T, Primack, R.B., 2011. Tropical Rainforests: An Ecological and
Biogeographical Comparison, second ed. Wiley-Blackwell.
Crooks, K.R., Soule, M.E., 1999. Mesopredator release and avifaunal extinctions in a
fragmented system. Nature 400, 563–566.
Cruz-Angón, A., Sillett, T.S., Greenberg, R., 2008. An experimental study of habitat
selection by birds in a coffee plantation. Ecology 89, 921–927.
Devries, P.J., Austin, G.T., Martin, N.H., 2008. Diel activity and reproductive isolation
in a diverse assemblage of Neotropical skippers (Lepidoptera: Hesperiidae).
Biol. J. Linn. Soc. 94, 723–736.
Dirzo, R., Raven, P.H., 2003. Global state of biodiversity and loss. Annu. Rev. Environ.
Resour. 28, 137–167.
Dolby, A.S., Grubb Jr., T.C., 2000. Social context affects risk taking by a satellite
species in a mixed-species foraging group. Behav. Ecol. 11, 110–114.
Ewers, R.M., Didham, R.K., Fahrig, L., Ferraz, G.F., Hector, A., Holt, R.D., Kapos, V.,
Reynolds, G., Sinun, W., Snaddon, J.L., Turner, E.C., 2011. A large-scale forest
fragmentation experiment: the Stability of Altered Forest Ecosystems Project.
Philos. Trans. Roy. Soc. B 366, 3292–3302.
Fregin, S., Haase, M., Olsson, U., Alström, P., 2012. New insights into family
relationships within the avian superfamily Sylvioidea (Passeriformes) based on
seven molecular markers. BMC Evol. Biol. 12, 157.
Gibson, L., Lee, T.M., Koh, L.P., Brook, B.W., Gardner, T.A., Barlow, J., Peres, C.A.,
Bradshaw, C.J.A., Laurance, W.F., Lovejoy, T.E., Sodhi, N.S., 2011. Primary forests
are irreplaceable for sustaining tropical biodiversity. Nature 478, 378–381.
Githiru, M., Lens, L., Bennun, L., 2007. Ranging behaviour and habitat use by an
Afrotropical songbird in a fragmented landscape. Afr. J. Ecol. 45, 581–589.
Githiru, M., Lens, L., Cresswell, W., 2005. Nest predation in a fragmented
Afrotropical forest: evidence from natural and artificial nests. Biol. Conserv.
123, 189–196.
Geist, H.J., Lambin, E.F., 2002. Proximate causes and underlying driving forces of
tropical deforestation. Bioscience 52, 143–150.
Goodale, E., Nizam, B.Z., Robin, V.V., Sridhar, H., Trivedi, P., Kotagama, S.W.,
Padmalal, U.K.G.K., Perera, R., Pramod, P., Vijayan, L., 2009. Regional variation in
the composition and structure of mixed-species bird flocks in the Western
Ghats and Sri Lanka. Curr. Sci. 97, 648–663.
Global Forest Watch. <www.GlobalForestWatch.org> (accessed 17 January 2015).
Greenberg, R., Bichier, P., Angon, A.C., Reitsma, R., 1997. Bird populations in shade
and sun coffee plantations in central Guatemala. Conserv. Biol. 11, 448–459.
Hamer, K.C., Newton, R.J., Edwards, F.A., Benedick, S., Bottrell, S.J., Edwards, D.P.,
2015. Impacts of selective logging on insectivorous birds in Borneo: the
importance of trophic position, body size and foraging height. Biol. Conserv.,
this issue.
Hanski, I., 1994. Patch-occupancy dynamics in fragmented landscapes. Trends Ecol.
Evol. 9, 131–135.
Hanski, I., 1998. Metapopulation dynamics. Nature 396, 41–49.
Harris, J.B., S
ß ekercioğlu, Ç.H., Sodhi, N.S., Fordham, D.A., Paton, D.C., Brook, B.W.,
2011. The tropical frontier in avian climate impact research. Ibis 153, 877–882.
Hino, T., 1998. Mutualistic and commensal organization of avian mixed-species
foraging flocks in a forest of western Madagascar. J. Avian Biol. 29, 17–24.
Jedlicka, J.A., Sharma, A.M., Almeida, R.P.P., 2013. Molecular tools reveal diets of
insectivorous birds from predator fecal matter. Conserv. Genet. Resour. 5, 879–
885.
Johnson, E.I., Stouffer, P.C., Vargas, C.F., 2013. Diversity, biomass, and trophic
structure of a central Amazonian rainforest bird community. Rev. Bras.
Ornitologia 19, 1–16.
Jullien, M., Thiollay, J., 1998. Territoriality and dynamic of Neotropical forest
understorey bird flocks. J. Anim. Ecol. 67, 227–252.
Jullien, M., Clobert, J., 2000. The survival value of flocking in Neotropical birds:
reality or fiction? Ecology 81, 3416–3430.
Karr, J.R., 1982. Avian extinction on Barro Colorado island, Panama: a reassessment.
Am. Nat. 119, 220–239.
Kilpatrick, A.M., LaDeau, S.L., Marra, P.P., 2007. Ecology of West Nile virus
transmission and its impact on birds in the western hemisphere. Auk 124,
1121–1136.
Korfanta, N.M., Newmark, W.D., Kauffman, M.J., 2012. Long-term demographic
consequences of habitat fragmentation to a tropical understory bird
community. Ecology 93, 2548–2559.
9
Kotagama, S.W., Goodale, E., 2004. The composition and spatial organization of
mixed-species flocks in a Sri Lankan rainforest. Forktail 20, 63–70.
Lambert, F.R., 1992. The consequences of selective logging for Bornean lowland
forest birds. Philos. Trans. Roy. Soc. Lond. Ser. B: Biol. Sci. 335, 443–457.
Lambert, F.R., Collar, N.J., 2002. The future for Sundaic lowland forest birds: longterm effects of commercial logging and fragmentation. Forktail 18, 127–146.
Laurance, W.F., 2008. Theory meets reality: how habitat fragmentation research has
transcended island biogeographic theory. Biol. Conserv. 141, 1731–1744.
Laurance, W.F., Lovejoy, T.E., Vasconcelos, H.L., Bruna, E.M., Didham, R.K., Stouffer,
P.C., Gascon, C., Bierregaard, R.O., Laurance, S.G., Sampaio, E., 2002. Ecosystem
decay of Amazonian forest fragments: a 22-year investigation. Conserv. Biol. 16,
605–618.
Laurance, W.F., Sayer, J., Cassman, K.G., 2014a. Agricultural expansion and its
impacts on tropical nature. Trends Ecol. Evol. 29, 107–116.
Laurance, W.F., Andrade, A.S., Magrach, A., Camargo, J.L.C., Campbell, M., Fearnside,
P.M., Edwards, W., Valsko, J.J., Lovejoy, T.E., Laurance, S.G., 2014b. Apparent
environmental synergism drives the dynamics of Amazonian forest fragments.
Ecology 95, 3018–3026.
Lawton, J.H., Bignell, D.E., Bolton, B., Bloemers, G.F., Eggleton, P., Hammond, P.M.,
Hodda, M., Holt, R.D., Larsen, T.B., Mawdsley, N.A., Stork, N.E., Srivastava, D.S.,
Watt, A.D., 1998. Biodiversity inventories, indicator taxa and effects of habitat
modification in tropical forest. Nature 391, 72–76.
Leck, C.F., 1979. Avian extinctions in an isolated tropical wet-forest preserve,
Ecuador. Auk 96, 343–352.
Lens, L., VanDongen, S., Norris, K., Githiru, M., Matthysen, E., 2002. Avian persistence
in fragmented rainforest. Science 298, 1236–1238.
Lim, H.C., Sodhi, N.S., 2004. Responses of avian guilds to urbanisation in a tropical
city. Landscape Urban Plann 66, 199–215.
Loiseau, C., Harrigan, R.J., Robert, A., Bowie, R.C., Thomassen, H.A., Smith, T.B.,
Sehgal, R.N., 2012. Host and habitat specialization of avian malaria in Africa.
Mol. Ecol. 21, 431–441.
MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton
University Press.
Macedo, M.N., DeFries, R.S., Morton, D.C., Stickler, C.M., Galford, G.L., Shimabukuro,
Y.E., 2012. Decoupling of deforestation and soy production in the southern
Amazon during the late. Proc. Natl. Acad. Sci. 109, 1341–1346.
Maldonado-Coelho, M., Marini, M.Â., 2004. Mixed-species bird flocks from Brazilian
Atlantic forest: the effects of forest fragmentation and seasonality on their size,
richness and stability. Biol. Conserv. 116, 19–26.
Martinez, A.E., Gomez, J.P., 2013. Are mixed-species bird flocks stable through two
decades? Am. Nat. 181, E53–E59.
McClure, H.E., 1967. Composition of mixed species flocks in lowland and submontane forests of Malaya. Wilson Bull. 79, 131–154.
McDonald, R.I., Kareiva, P., Forman, R.T.T., 2008. The implications of current and
future urbanization for global protected areas and biodiversity conservation.
Biol. Conserv. 141, 1695–1703.
Michel, N.L., Sherry, T.W., Carson, W.P., 2014. The omnivorous collared peccary
negates an insectivore-generated trophic cascade in Costa Rican wet tropical
forest understorey. J. Trop. Ecol. 30, 1–11.
Mokross, K., Ryder, T.B., Côrtes, M.C., Wolfe, J.D., Stouffer, P.C., 2014. Decay of
interspecific avian flock networks along a disturbance gradient in Amazonia.
Proc. Roy. Soc. B 281, 20132599.
Mooney, K.A., Gruner, D.S., Barber, N.A., Van Bael, S.A., Philpott, S.M., Greenberg, R.,
2010. Interactions among predators and the cascading effects of vertebrate
insectivores on arthropod communities and plants. Proc. Natl. Acad. Sci. 107,
7335–7340.
Moore, R.P., Robinson, W.D., 2005. Artificial bird nests, external validity, and bias in
ecological field studies. Ecology 85, 1562–1567.
Moore, R.P., Robinson, W.D., Lovette, I.J., Robinson, T.R., 2008. Experimental
evidence for extreme dispersal limitation in tropical forest birds. Ecol. Lett.
11, 960–968.
Munn, C.A., Terborgh, J.W., 1979. Multi-species territoriality in Neotropical foraging
flocks. Condor 81, 338–347.
Neeff, T., Lucas, R.M., Santos, J.R., Brondizio, E.S., Freitas, C.C., 2006. Area and age of
secondary forests in Brazilian Amazonia 1978–2002: an empirical estimate.
Ecosystems 9, 609–623.
Newmark, W.D., 1991. Tropical forest fragmentation and the local extinction of
understory birds in the Eastern Usambara Mountains, Tanzania. Conserv. Biol. 5,
67–78.
Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N.,
Underwood, E.C., D’amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J.,
Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P.,
Kassem, K.R., 2001. Terrestrial ecoregions of the world: a new map of life on
earth. Bioscience 51, 933–938.
Patten, M.A., Smith-Patten, B.D., 2012. Testing the micro climate hypothesis: light
environment and population trends of Neotropical birds. Biol. Conserv. 155, 85–
93.
Pavlacky Jr., D.C., Possingham, H.P., Goldizen, A.W., 2015. Integrating life history
traits and forest structure to evaluate the vulnerability of rainforest birds along
gradients of deforestation and fragmentation in eastern Australia. Biol.
Conserv., this issue.
Pavlacky Jr., D.C., Possingham, H.P., Lowe, A.J., Prentis, P.J., Green, D.J., Goldizen,
A.W., 2012. Anthropogenic landscape change promotes asymmetric dispersal
and limits regional patch occupancy in a spatially structured bird population. J.
Anim. Ecol. 81, 940–952.
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025
10
L.L. Powell et al. / Biological Conservation xxx (2015) xxx–xxx
Pearson, D.L., 1977. A pantropical comparison of bird community structure on six
lowland forest sites. Condor 79, 232–244.
Peh, K.S.H., Jong, J.d., Sodhi, N.S., Lim, S.L.H., C.A.M., Yap, 2005. Lowland rainforest
avifauna and human disturbance: persistence of primary forest birds in
selectively logged forests and mixed-rural habitats of southern Peninsular
Malaysia. Biol. Conserv. 123, 489–505.
Peters, M.K., Likare, S., Kraemer, M., 2008. Effects of habitat fragmentation and
degradation on flocks of African ant-following birds. Ecol. Appl. 18, 847–858.
Peters, M.K., Okalo, B., 2009. Severe declines of ant-following birds in African
rainforest fragments are facilitated by a subtle change in army ant
communities. Biol. Conserv. 142, 2050–2058.
Pickett, S.T., Cadenasso, M., Grove, J., Nilon, C., Pouyat, R., Zipperer, W., Costanza, R.,
2001. Urban ecological systems: linking terrestrial ecological, physical, and
socioeconomic components of metropolitan areas. Annu. Rev. Ecol. Syst., 127–
157
Pollock, H.S., Cheviron, Z.A., Agin, T.J., Brawn, J.D., 2015. Absence of microclimate
selectivity in insectivorous birds of the Neotropical forest understory. Biol.
Conserv., this issue.
Pongsiri, M.J., Roman, J., Ezenwa, V.O., Goldberg, T.L., Koren, H.S., Newbold, S.C.,
Ostfeld, R.S., Pattanayak, S.K., Salkeld, D.J., 2009. Biodiversity loss affects global
disease ecology. Bioscience 59, 945–954.
Powell, G.V.N., 1985. Sociobiology and adaptive significance of interspecific foraging
flocks in the Neotropics. Ornithological Monogr. 36, 713–732.
Powell, G.V.N., 1989. On the possible contribution of mixed species flocks to species
richness in neotropical avifaunas. Behav. Ecol. Sociobiol. 24, 387–393.
Powell, L.L., Stouffer, P.C., Johnson, E.I., 2013. Recovery of understory bird
movement across the interface of primary and secondary Amazon rainforest.
Auk 140, 459–468.
Powell, L.L., 2013. Recovery of Understory Bird Movement in Post-pasture
Amazonia (Ph.D. dissertation), Louisiana State University, Baton Rouge,
LA.
Powell, L.L., Wolfe, J.D. Johnson, E.I., Hines, J.E., Nichols, J.D., Stouffer, P.C., 2015.
Heterogeneous movement of insectivorous Amazonian birds through primary
and secondary forest: a case study using multistate models with radiotelemetry
data. Biol. Conserv., this issue.
Poulin, B., Lefebre, G., Ibañez, R., Jaramillo, C., Hernández, C., Rand, A.S., 2001. Avian
predation upon lizards and frogs in a neotropical forest understory. J. Trop. Ecol.
17, 21–40.
Ribon, R., Simon, J.E., Theodoro De Mattos, G., 2003. Bird extinctions in Atlantic
forest fragments of the Viçosa region, southeastern Brazil. Conserv. Biol. 17,
1827–1839.
Ridgely, R.S., Tudor, G., 1994. The Birds of South America. Volume II. The Suboscine
Passerines. University of Texas Press.
Ruiz-Gutiérrez, V., Doherty Jr., P.F., Santana, E.C., Martínez, S.C., Schondube, J.,
Munguía, H.V., Iñigo-Elias, E., 2012. Survival of resident Neotropical birds:
Considerations for sampling and analysis based on 20 years of bird-banding
efforts in Mexico. Auk 129, 500–509.
Richardson, J.J., Moskal, L.M., Bakker, J.D., 2014. Terrestrial laser scanning for
vegetation sampling. Sensors 14, 20304–20319.
Robinson, W.D., 1999. Long-term changes in the avifauna of Barro Colorado Island,
Panama, a tropical forest isolate. Conserv. Biol. 13, 85–97.
Robinson, W.D., Robinson, T.R., Robinson, S.K., Brawn, J.D., 2000. Nesting success of
understory forest birds in central Panama. J. Avian Biol. 31, 151–164.
Robinson, W.D., Rompre, G., Robinson, T.R., 2005. Videography of Panama bird nests
shows snakes are principal predators. Ornitologia Neotrop. 16, 187–195.
Robinson, W.D., Sherry, T.W., 2012. Mechanisms of avian population decline and
species loss in tropical forest fragments. J. Ornithol. 153, S141–S152.
Román-Cuesta, R., Carmona-Moreno, C., Lizcano, G., New, M., Silman, M., Knoke, T.,
Malhi, Y., Oliveras, I., Asbjornsen, H., Vuille, M., 2014. Synchronous fire activity
in the tropical high Andes: an indication of regional climate forcing. Glob.
Change Biol. 20, 1929–1942.
Rompre, G., Robinson, W.D., Desrochers, A., Angehr, G., 2007. Environmental
correlates of avian diversity in lowland Panama rain forests. J. Biogeogr. 34,
802–815.
Rosenberg, K.V., Cooper, R.J., 1990. Approaches to avian diet analysis. Stud. Avian
Biol. 13, 80–90.
Sala, O., Chapin III, F., Armesto, J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald,
E., Huenneke, L., Jackson, R., Kinzig, A., 2000. Global biodiversity scenarios for
the year 2100. Science 287, 1770–1774.
Sangster, G., Alström, P., Forsmark, E., Olsson, U., 2010. Multi-locus phylogenetic
analysis of Old World chats and flycatchers reveals extensive paraphyly at
family, subfamily and genus level (Aves: Muscicapidae). Mol. Phylogenet. Evol.
57, 380–392.
Schmidt, K.A., 2003. Nest predation and population declines in Illinois songbirds: a
case for mesopredator effects. Conserv. Biol. 17, 1141–1150.
Sßekercioğlu, Ç.H., 2011. Functional extinctions of bird pollinators cause plant
declines. Science 331, 1019–1020.
Sßekercioğlu, Ç.H., Ehrlich, P.R., Daily, G.C., Aygen, D., Goehring, D., Sandí, R., 2002.
Disappearance of insectivorous birds from tropical forest fragments. Proc. Natl.
Acad. Sci. 99, 263–267.
Sßekercioğlu, Ç.H., Primack, Richard B., Wormworth, J., 2012. The effects of climate
change on tropical birds. Biol. Conserv. 148, 1–18.
Sherry, T.W., 1984. Comparative dietary ecology of sympatric, insectivorous
neotropical flycatchers (Tyrannidae). Ecol. Monogr. 54, 313–338.
Sigel, B., Robinson, W.D., Sherry, T.W., 2010. Comparing bird community responses
to forest fragmentation in two lowland Central American reserves. Biol.
Conserv. 143, 340–350.
Sodhi, N.S., Koh, L.P., Prawiradilaga, D.M., Tinulele, I., Putra, D.D., Tan, T.H.T., 2005.
Land use and conservation value for forest birds in Central Sulawesi (Indonesia).
Biol. Conserv. 122, 547–558.
Sodhi, N.S., Posa, M.R.C., Lee, T.M., Warkentin, I.G., 2008. Effects of disturbance or
loss of tropical rainforest on birds. Auk 125, 511–519.
Spanhove, T., Callens, T., Hallmann, C.A., Pellikka, P., Lens, L., 2014. Nest predation in
Afrotropical forest fragments shaped by inverse edge effects, timing of nest
initiation and vegetation structure. J. Ornithol. 155, 411–420.
Srinivasan, U., Raza, R.H., Quader, S., 2010. The nuclear question: rethinking species
importance in multi-species animal groups. J. Anim. Ecol. 79, 948–954.
Stouffer, P.C., Bierregaard, R.O., 1995. Use of Amazonian forest fragments by
understory insectivorous birds. Ecology 76, 2429–2445.
Stouffer, P.C., Bierregaard, R.O., 2007. Recovery potential of understory bird
communities in Amazonian Forest Fragments. Rev. Bras. Ornitologia 15, 219–
229.
Stouffer, P.C., Johnson, E.I., Bierregaard, R.O., Lovejoy, E., 2011. Understory bird
communities in Amazonian rainforest fragments: species turnover through 25
years post-isolation in recovering landscapes. PlosONE 6, e20543.
Stratford, J.A., Robinson, W.D., 2005. Gulliver travels to the fragmented tropics:
geographic variation in mechanisms of avian extinction. Front. Ecol. Environ. 3,
85–92.
Stratford, J.A., Sß ekercioğlu, Ç.H., in press. Birds in forest ecosystems. In: Peh, K.,
Corlett, R., Bergeron, Y., (Eds.), Handbook of Forest Ecology, Routledge.
Stratford, J.A., Stouffer, P.C., 1999. Local extinctions of terrestrial insectivorous birds
in a fragmented landscape near Manaus, Brazil. Conserv. Biol. 13, 1416–1423.
Stratford, J.A., Stouffer, P.C., 2013. Microhabitat associations of terrestrial
insectivorous birds in Amazonian rainforest and second-growth forests. J.
Field Ornithol. 84, 1–12.
Stratford, J.A., Stouffer, P.C., 2015. Forest fragmentation alters microhabitat
availability for Neotropical terrestrial insectivorous birds. Biol. Conserv., this
issue.
Svensson-Coelho, M., Blake, J.G., Loiselle, B.A., Penrose, A.S., Parker, P.G., Ricklefs, R.E.,
2013. Diversity, prevalence, and host specificity of avian Plasmodium and
Haemoproteus in a western Amazon assemblage. Ornithological Monogr. 76, 1–
47.
Tarwater, C.T., 2012. Influence of phenotypic and social traits on dispersal in a
family living, tropical bird. Behav. Ecol. 23, 1242–1249.
Thiollay, J.M., 1997. Disturbance, selective logging and bird diversity: a Neotropical
forest study. Biodivers. Conserv. 6, 1155–1173.
Tobias, J.A., S
ß ekercioğlu, Ç.H., Vargas, F.H., 2013. Bird conservation in tropical
ecosystems: challenges and opportunities. In: MacDonald, D. (Ed.), Key Topics
in Conservation Biology, vol. 2. Wiley-Blackwell, Oxford, pp. 258–276.
van Riper III, C., van Riper, S.G., Goff, M.L., Laird, M., 1986. The epizootiology and
ecological significance of malaria in Hawaiian land birds. Ecol. Monogr. 56, 327–
344.
Waltert, M., Mardiastuti, A.N.I., Mühlenberg, M., 2004. Effects of land use on bird
species richness in Sulawesi, Indonesia. Conserv. Biol. 18, 1339–1346.
Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C.,
Fromentin, J.-M., Hoegh-Guldberg, O., Bairlein, F., 2002. Ecological responses
to recent climate change. Nature 416, 389–395.
Webb, L.J., Tracey, J.G., Williams, W.T., 1984. A floristic framework of Australian
rainforests. Aust. J. Ecol. 9, 169–198.
Willis, E.O., 1974. Populations and local extinctions of birds on Barro Colorado
Island, Panama. Ecol. Monogr. 44, 153–169.
Willis, E.O., 1979. The composition of avian communities in remanescent woodlots
in southern Brazil. Papeis Avulsos de Zoologia 33, 1–25.
Willis, E.O., Oniki, Y., 1978. Birds and army ants. Annu. Rev. Ecol. Syst. 9, 243–263.
Willson, S.K., 2004. Obligate army-ant-following birds: a study of ecology, spatial
movement patterns, and behavior in Amazonian Peru. Ornithological Monogr.,
1–67
Wolfe, J.D., Stouffer, P.C., Seeholzer, G.F., 2014. Variation in tropical bird survival
across latitude and guilds: a case study from the Amazon. Oikos 123, 964–970.
Woltmann, S., Kreiser, B.R., Sherry, T.W., 2012a. Fine-scale genetic population
structure of an understory rainforest bird in Costa Rica. Conserv. Genet. 13,
925–935.
Woltmann, S., Sherry, T.W., Kreiser, B.R., 2012b. A genetic approach to estimating
natal dispersal distances and self-recruitment in rainforest resident birds. J.
Avian Biol. 43, 33–42.
Wormworth, J., S
ß ekercioğlu, Ç.H., 2011. Winged Sentinels: Birds and Climate
Change. Cambridge University Press, Cambridge, UK.
Wright, S.J., 2005. Tropical forests in a changing environment. Trends Ecol. Evol. 20,
553–560.
Visco, D.M., Sherry, T.W., 2015. Increased abundance, but reduced nest predation on
an understory bird in tropical rainforest fragments: surprising impacts of a
single, pervasive snake species. Biol. Conserv., this issue.
Vo, A.T.E., Jedlicka, J.A., 2015. Protocols for metagenomic DNA extraction and
Illumina amplicon library preparation for fecal and swab samples. Mol. Ecol.
Resour. 6, 1183–1197.
Zhang, Q., Han, R., Zou, F., 2011. Effects of artificial afforestation and successional
stage on a lowland forest bird community in southern China. For. Ecol. Manage.
261, 1738–1749.
Please cite this article in press as: Powell, L.L., et al. Ecology and conservation of avian insectivores of the rainforest understory: A pantropical perspective.
Biol. Conserv. (2015), http://dx.doi.org/10.1016/j.biocon.2015.03.025