Biological Conservation 188 (2015) 1–10
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Biological Conservation
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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 b 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 article info abstract
Article history: Avian insectivores of the tropical rainforest understory (‘‘understory insectivores’’) are common, diverse, Received 17 February 2015 and often sensitive to disturbance of tropical forest, making them useful as sentinels of rainforest ecosys- Received in revised form 20 March 2015 tem change. At the 2013 joint American Ornithologists’ Union and Cooper Ornithological Society meeting Accepted 21 March 2015 in Chicago, USA, researchers convened a symposium to address the ecology and conservation of under- Available online 9 April 2015 story insectivores. This Special Issue of Biological Conservation is the result of that symposium: a collec- tion of articles that unites our efforts to further understand and conserve understory insectivores. In this Keywords: introductory paper, we review the diversity and ecology of understory insectivores, identify threats to the Understory insectivores guild, discuss hypotheses on drivers of population declines, and make suggestions for future research. Rainforests Pantropical Deforestation and forest degradation are the immediate threats to this guild, with agricultural expansion Fragmentation (particularly oil palm plantations), urbanization, road expansion and logging leading the list. Although Deforestation vulnerabilities of this guild are most evident in the Neotropics, there are few studies from Asia and fewer Mixed species flocks still from Africa—we recommend increased geographic coverage. If we are to understand the vulnerabili- ties of understory insectivores from a pantropical perspective, researchers should prioritize understand- ing 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, demo- graphic 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 forests; tropical forests represent just 36% of the world’s landmass introduction but have suffered 54% of forest loss since 2001 (135 billion ha, Global Forest Watch, 2015). Deforestation is the main threat to 1.1. Degradation and loss of tropical rainforests tropical forests, with agricultural expansion the dominant cause (Geist and Lambin, 2002). Accompanying an expanding agricul- Tropical rainforests, which harbor at least half of the earth’s ter- tural landscape is the increasing network of roads that is fragment- restrial biodiversity, are the most diverse terrestrial biome (Dirzo ing remaining tracts of forests, creating vast areas of edge-affected and Raven, 2003). This diversity is in jeopardy, however, as more forest, and allowing people, alien species and disease to colonize than half of the area covered by closed-canopy tropical forests previously inaccessible areas (Laurance et al., 2014a). has already been cleared (Wright, 2005), and forest loss continues Insectivorous birds of the tropical rainforest understory (here- at a rapid pace—over 7 million ha/year (Achard et al., 2014). after understory insectivores) are a taxonomically and ecologically Furthermore, tropical forests are more threatened than temperate 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 ⇑ Corresponding author at: Migratory Bird Center, Smithsonian Conservation special issue, we review the diversity and ecology of understory Biology Institute, National Zoological Park, Washington, DC 20013-7012, USA. insectivores, identify threats to the guild, discuss hypothetical E-mail address: [email protected] (L.L. Powell). http://dx.doi.org/10.1016/j.biocon.2015.03.025 0006-3207/Published by Elsevier Ltd. 2 L.L. Powell et al. / Biological Conservation 188 (2015) 1–10 drivers of population declines, and offer suggestions for con- which stabilizes flock cohesion in time and space, sometimes over servation-applied research. decades (Martinez and Gomez, 2013). Neotropical understory insectivores are often associated with the army ant Eciton burchellii (Willis and Oniki, 1978). Swarms of 1.2. This Special Issue of Biological Conservation thousands to millions of raiding ants carpet the rainforest floor, attracting ant-following birds that capture the fleeing arthropods. For the joint American Ornithologists’ Union/Cooper Although there have been recent research advances on ant-follow- Ornithological Society conference in August 2013, Powell orga- ing birds, the system is understood in much greater detail in the nized a symposium on the sensitivity of understory insectivores Neotropics than in the Paleotropics, primarily due to the pioneer- to the loss, fragmentation, and degradation of tropical forests. ing work of E.O. Willis and colleagues (Willis and Oniki, 1978) Bringing together 13 presenters plus dozens of other researchers and more recent work by Susan Willson and Johel Chaves- from around the globe, the symposium and the discussions that Campos (Willson, 2004; Chaves-Campos and DeWoody, 2008; followed confirmed the need to call attention to the global risks Chaves-Campos et al., 2009). As with mixed-flock species, ant-fol- to this diverse avian guild. lowing birds can be either obligate (found foraging only in mixed To evaluate the effects of different types of disturbance on the species or army ant swarms) or facultative (joining periodically; ecology and conservation of understory insectivores, a comprehen- Powell, 1989; Brumfield et al., 2007). sive pantropical overview is necessary. The study sites covered by African understory insectivores have very little taxonomic over- papers in this special issue occur in tropical and subtropical moist lap with their New World counterparts. African rainforest under- broadleaf forest (Olson et al., 2001). The biogeographic regions cov- stories are dominated by several families of the Old World ered by tropical rainforests transcend strict latitudinal limits, as superfamily Sylvioidea, including greenbuls (Pycnonotidae), Old other factors such as rainfall and ocean currents affect climate World warblers (Sylviidae), and several families of the superfamily and thus the distribution of rainforest taxa. We therefore include Musicapoidea, including Old World flycatchers (Muscicapidae) and Pavlacky et al. (2015) as the South East Queensland Biogeo thrushes (Turdidae). In the Afrotropics mixed species foraging graphic Region of Australia shares ancient origins with a previously flocks are less rigidly organized, occurring more as waves through widespread tropical rainforest ecosystem that has contracted as the forest (McClure, 1967). The social dynamics of mixed-species Australia has dried (Webb et al., 1984; Fig. 1). This special issue flocks are poorly understood in Africa; however, in this issue, provides representation from throughout the world’s tropical rain- Cordeiro et al. (2015) showed that in Tanzania, the Square-tailed forests to capture much of the extraordinary diversity of under- Drongo (Dicrurus ludwigii) was a key nuclear species in mixed-spe- story insectivores. Nonetheless, it is important to note that this cies flocks and that mixed flocks were larger in the presence of this special issue does not include contributions from important rain- species. Social dynamics and the importance of ant swarms are less forest regions in Central Africa, Madagascar, New Guinea, northern known in the Afrotropics. However, it is clear that some Old World Australia and much of Asia (Fig. 1). thrushes and bulbuls follow driver ants in the genus Dorylus (Chapin, 1932; Brosset, 1969). 1.3. Overview of the taxonomy and ecology of the understory Asian rainforests are also well represented by the Muscicapidae insectivores and Sylvioidea, but particularly diverse are the babblers (Sylvioidea: Timaliidae; Sangster et al., 2010; Corlett and Primack, In the Neotropics, understory insectivores are dominated by sub- 2011; Fregin et al., 2012). As is true in the Afrotropics, mixed species oscine songbirds of the antbird (Thamnophilidae), ovenbird foraging flocks in Asia are also not rigidly organized. These flocks (Furnariidae, including woodcreepers: subfamily Dendr ocolapti- tend to be dominated by timaliid babblers and white-eyes nae), antthrush (Formicariidae), and tyrant-flycatcher (Zosterops; e.g., Kotagama and Goodale, 2004; Goodale et al., (Tyrannidae) families. Many Neotropical understory insectivores 2009). Australian rainforests harbor a diverse assemblage of under- participate in mixed foraging flocks. In Amazonia, for instance, story insectivores, including pittas (Pittidae), scrub-birds and lyre- Thamnomanes antshrikes lead dozens of mostly suboscine passeri- birds (superfamily Menuroidea), gerygones, thornbills and nes in highly stable flocks, which congregate in the same location scrubwrens (Acanthizidae), logrunners (Orthonychidae), shrike- over months or even years (Munn and Terborgh, 1979; Powell, thrushes (Colluricinclidae), fantails (Rhipiduridae) and 1985). These multispecies Neotropical flocks defend their territories Australasian robins (Petroicidae; Pavlacky et al., 2015). In Australia communally, with pairs of individuals of the same species aggres- and New Guinea, endemic families dominate, such as Australian sively defending territorial boundaries (Jullien and Thiollay, 1998). babblers (Pomatostomidae), Australasian warblers (Acanthizidae), Interspecific territoriality is characteristic of Neotropical flocks, 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.) L.L. Powell et al. / Biological Conservation 188 (2015) 1–10 3
flycatchers (Monarchidae), and birds of paradise (Paradisaediae; 2. Why the concern about understory insectivores? Corlett and Primack, 2011), which can be frugivorous or insectivo- rous. Ant-swarm attendance, however, is not reported from 2.1. Understory insectivores are sensitive to forest degradation and Australasian rainforests. loss Most understory insectivores can also be placed into several broad groups based on foraging tactic (e.g., sallying species, arbor- Current estimates of globally threatened and near-threatened eal gleaners, or terrestrial species). These groups make for conveni- bird species include 23% of the approximately 10,000 described ent ecological classification and many birds within these groups species (BirdLife International, 2015). The bulk of these species respond to environmental changes similarly. However, group occur in tropical forests, and because vulnerability is strongly pre- assignments are not always mutually exclusive; a species can be dicted by ecological specialization (Sßekerciog˘lu, 2011), it is not sur- an arboreal gleaner and be associated with army ants, such as prising that one of the most at-risk groups is understory the White-chinned Woodcreeper (Dendrocincla merula; Johnson insectivores (Tobias et al., 2013). et al., 2013). Many different groups are often well represented Studies on the effects of forest fragmentation on tropical under- within a single family, where species show remarkable versatility story birds followed soon after MacArthur and Wilson’s landmark in their foraging niches. The Neotropical family Furnariidae, for study on island biogeography (1967). Charles Leck, working in example, includes bark-gleaners (e.g., woodcreepers; Powell Ecuador (1979), E.O. Willis and James Karr’s work on Barro et al., 2015), professional ant-followers, obligate mixed-species Colorado Island (Willis, 1974; Karr, 1982) and Willis’ work in iso- flock participants (Colorado and Rodewald, 2015), and terrestrial lated woodlots in the Atlantic rainforest (Willis, 1979) were among insectivores (Powell et al., 2013). Although not covered in this spe- the pioneering studies of tropical forest fragmentation. These stud- cial issue, the vangas of Madagascar (Vangidae) are perhaps even ies identified large-bodied birds, understory insectivores, and more ecologically versatile than the Furnariidae. In the absence predatory birds as being particularly vulnerable to fragmentation. of many other rainforest avian taxa in Madagascar, vangas have These early studies were followed by long-term studies, notably evolved to fill a diverse range of niches. Included in the Vangidae from the Biological Dynamics of Forest Fragments Project are the toucan-like Helmet Vanga (Euryceros prevostii), the bark- (BDFFP) near Manaus, Brazil (e.g. Stouffer and Bierregaard, 1995), creeping Nuthatch Vanga (Hypositta corallirostris), the insect-prob- and Robinson’s (1999) research in Panama. Their studies ing Sickle-billed Vanga (Falculea palliata), the aerial Flycatcher demonstrated the relative long-term nature of species loss and Vanga (Pseudobias wardi) and the terrestrial Crossley’s Babbler reduced abundances from fragmented and isolated habitats. Vanga (Mystacornis crossleyi; Corlett and Primack, 2011). This vari- Investigations in Afrotropical forests (Newmark, 1991; Lens et al., ety of niches, even within the broader foraging groups, highlights 2002; Beier et al., 2002; Korfanta et al., 2012), Brazil’s Atlantic rain- the ability of understory insectivores to specialize and is certainly forest (Ribon et al., 2003), and Asian rainforests (Lambert and relevant to understanding the impacts of human-caused Collar, 2002; Sßekerciog˘lu et al., 2002; Sodhi et al., 2005; Waltert disturbance. et al., 2004) followed suit, providing further empirical evidence Sallying insectivores capture understory insects using aerial on the acute sensitivity of understory insectivores to habitat frag- foraging maneuvers in which they catch arthropods while on the mentation. A recent review by Bregman et al. (2014) largely con- wing and return to a perch. They are often small and nimble, with firmed that relative to other guilds, insectivores in the tropics are unrelated species commonly called flycatchers (e.g., Old World most at risk from habitat fragmentation across habitats and geo- Muscicapidae, New World Tyrannidae) or warblers (e.g., Old graphic regions. World Sylviidae, New World Parulidae, Australasian Understory insectivores are differentially affected by deforesta- Acanthizidae). In the Amazon, sallying insectivores are abundant tion, fragmentation and disturbance. Of the different foraging tac- and species-rich in the understory and include active foragers tics, terrestrial insectivores may be among the most sensitive, as (e.g., many tyranid flycatchers) and species with sit-and-wait tac- several studies across tropical regions have shown that this group tics (e.g., puffbirds: Galbulidae; Johnson et al., 2013). Arboreal is among the first to disappear when the forest is disturbed gleaners catch prey on plant substrates such as trunks, branches (Stratford and Stouffer, 1999; Canaday and Rivadeneyra, 2001; and leaves. In the Neotropics, arboreal gleaners are exemplified Peh et al., 2005; Pavlacky et al., 2015) and among the last to return by the woodcreepers (Dendrocolaptinae). Although this group after pasture abandonment and subsequent forest regrowth has similar body forms, they have a remarkable array of bill adap- (Powell et al., 2013, 2015). Of nine species of terrestrial insecti- tations from the stubby-billed Glyphorynchus spirurus (Wedge- vores studied by Stratford and Stouffer (1999) that occurred in ele- billed Woodcreeper) to Campylorhampus scythebills, which have ven forest fragments, only a single species was able to colonize absurdly long, curved bills exceeding half the length of their bod- forest fragments < 100 ha after their isolation – the Thrushlike ies. A number of species of pyconotid greenbuls in Africa function Antpitta (Myrmothera campanisona), a species associated with tree- as arboreal gleaners, but the diversity of foraging adaptations is not falls and other disturbance (Stratford and Stouffer, 2013). Most of nearly as striking. the species that were present before the fragments were isolated Finally, terrestrial insectivores are usually strong-legged, drab- (74 occurrences) were absent after isolation (19 occurrences; colored, stocky birds that make their livings by walking or hopping Stratford and Stouffer, 1999). along the forest floor searching for prey. Terrestrial insectivores Whereas agriculture is the primary agent to forest loss and frag- may simply scan the surface of the leaf litter or may be more active mentation globally (Geist and Lambin, 2002), there is considerable by flipping leaves in search of small arthropods. The logrunners variability in the types of threats that understory insectivores face; (genus Orthonyx) of Australia and New Guinea possess highly spe- these include timber harvesting, agriculture and infrastructure/ cialized morphological adaptations for foraging in leaf litter, allow- urbanization (sensu Sodhi et al., 2008). The Asian peninsula has been ing a 90° lateral sweep of the femur (Boles, 1993). Some species proportionally hardest hit by deforestation due to urbanization pounce on terrestrial arthropods from an elevated perch (e.g., (Castelletta et al., 2000; Sodhi et al., 2008). The remaining larger Australasian robins, Petroicidae). The exceptional Ringed Antpipit wild tracts of Malaysia and Indonesia, and now parts of Papua (Corythopis torquatus, Tyrannidae) is considered a terrestrial insec- New Guinea, have succumbed and continue to be affected by the tivore but sallies upwards for insects on the undersides of living oil palm industry, with logging being an additional agent of distur- leaves (Ridgely and Tudor, 1994). bance (Boucher et al., 2011). In Africa, particularly upper Guinea 4 L.L. Powell et al. / Biological Conservation 188 (2015) 1–10 forests (Arcilla et al., 2015), logging and associated fragmentation 3.1. Vegetation changes and habitat loss continue to be chief threats. In Australia, approxi- mately 20% of tropical rainforest and 60% of subtropical rainforest Tropical birds, particularly insectivores, are closely tied to veg- has been cleared within the last 200 years (Catterall et al., 2004). etation structure (Stratford and Sßekerciog˘lu, in press). Thus remov- Although the majority of Australian rainforest has been protected ing forest and converting it to some other land use (e.g., oil palm since 2000, the restoration and conservation of remnant rainforests plantations, cropland, or urban) will make these sites unusable are ongoing challenges (Bradshaw, 2012; Catterall et al., 2004). In for most understory insectivores. Not all forest disturbances are the Neotropics, agricultural expansion for soybean and cattle so dramatic; selective logging and shade grown coffee plantations ranching dominate as agents of forest loss, and urbanization has are examples of forest disturbances where some of the forest struc- continued to play a major role in deforestation, especially cities ture remains intact. Selective logging in Amazonian (e.g. Thiollay, that function as major transportation hubs in the large expanses 1997) and Bornean forests (Lambert, 1992) was associated with of forests. On the bright side, over the last ten years, Brazil has used the loss of understory insectivores, whereas in this issue, Arcilla remote sensing and enforcement to considerably slow deforesta- et al. (2015) found that generalists were more vulnerable to log- tion rates in the Amazon (Macedo et al., 2012). ging than specialists in the rainforests of Upper Guinea, an Urbanization and major road development are particularly wor- African biodiversity hotspot. In Australian rainforests, understory risome globally. As human populations grow and become increas- insectivores declined with reduced stand basal area and subse- ingly urbanized, urban areas expand, but this is a land conversion quent invasion of a thicket-forming weed (Pavlacky et al., 2015). that becomes a permanent feature of the landscape (Pickett et al., If they are properly managed with an adequate overstory, 2001). Urbanization is expected to accelerate in developing Neotropical and African shade coffee plantations can have greater countries where human population growth is concentrated diversity of understory insectivores than sun coffee plantations (McDonald et al., 2008), and its negative impact on forest birds is (Greenberg et al., 1997). African shade coffee plantations in already well known (Borges and Guiherme, 2000; Lim and Sodhi, Ethiopia have more understory insectivore species than rainforest, 2004). 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., 2.2. Understory insectivores are important members of tropical forests 1997). Forest fragments, even if not directly affected by humans, will have altered vegetation. Edge effects include reduced canopy Lagging behind our ability to document patterns is our quest to cover and more dense undergrowth (Laurance et al., 2002). In this understand the ecological consequences of bird species loss. In a issue, Stratford and Stouffer (2015) found that fragmentation-sen- seminal meta-analysis of 113 experiments evaluating the trophic sitive Neotropical species were associated with some elements of cascades among insectivorous vertebrates (birds, bats and lizards), vegetation structure that were not found in 10- and 1-ha forest invertebrates and plants, Mooney et al. (2010) found that preda- fragments. However, in a montane Kenyan forest, the White- tion by vertebrates reduced predatory and herbivorous inverte- starred Robin (Pogonocichla stellata), was able to use fragments brates by 38% and 39%, respectively. This led to an indirect despite the vegetation differences between fragments and larger benefit for plants with damage reduced by 40% and biomass forest tracts (Githiru et al., 2007). These differences between increasing by 14%. Given the conservation implications of these Neotropical and Afrotopical understory insectivores are perplex- findings for vertebrates as a whole, comparable experimental ing, and research would benefit from a broader unified approach. research to quantify the direct and indirect effects of understory It remains unknown how the relationship between vegetation insectivores on ecosystems (i.e., ecosystem services) is particularly structure and understory insectivores scales up to larger land- needed. However, several new studies have been instructive. For scapes. In this issue, Anjos et al. (2015) predicted that more spe- example, Michel et al. (2014) found that Costa Rican plants suf- cialists would be found in the botanically rich evergreen forests fered greater plant damage when understory birds were excluded of the Atlantic Rainforest of Brazil compared to the nearby ever- from rainforest interior plants. Additionally, species loss may have green-deciduous mixed forest and semideciduous forest types. consequences for organisms that interact with insectivores, such as However the mixed forests had the same number of specialists the skippers (Lepidoptera) that are associated with the feces of as the evergreen forest. In Gondwana Rainforests of Australia, army-ant following birds (Devries et al., 2008). We know so little stand condition at the local scale was a somewhat better predictor about most tropical birds that we have not identified their diets of avian species richness than forest composition at the landscape beyond insect orders, nor do we know the impact of their foraging scale, with less support for the effects of patch size and isolation on prey abundance. We do know that invertebrate and vertebrate (Pavlacky et al., 2015). A standardized protocol for quantifying veg- predators, such as frogs and lizards are consumed by some under- etation would allow researchers to test hypotheses related to the story insectivores (Chesser, 1995; Poulin et al., 2001). Thus, losing relationship between birds and their sensitivities to vegetation understory insectivores in forested ecosystems may have cascad- structure. Terrestrial laser scanning (Richardson et al., 2014)is ing effects that go beyond their direct effects on prey, but affect one emerging technology that would assist in standardizing veg- multiple trophic levels (Stratford and Sßekerciog˘lu, in press). This etation measurements, as well as in reducing error and effort. is clearly an area needing more research.
3.2. Reduced prey abundance
3. Why are understory insectivores lost from degraded and The effect of forest disturbance on prey abundance and the fragmented forests? potential effect on understory insectivores are logistically difficult to test. Trophic interactions between understory birds and insects A number of hypotheses been have proposed (Robinson and are complicated by species rich invertebrate communities (Lawton Sherry, 2012; Stratford and Robinson, 2005) that are based on et al., 1998), highly specialized avian diets (Sherry, 1984) and the focal species responses to forest disturbance (e.g., sensitivity undocumented dietary composition. The few tests of the prey-lim- to microclimate in fragments) or based on species interactions in itation hypotheses lend little support. For example, Sßekerciog˘lu disturbed areas (e.g., increased nest predation in fragments). et al. (2002) found no differences in insect abundance between L.L. Powell et al. / Biological Conservation 188 (2015) 1–10 5 fragments and forest. Although prey abundance may not be impor- 3.4. Dispersal limitation tant, how prey is captured (foraging tactic) consistently emerges as a predictor of sensitivity to disturbance, which may result more In small populations, such as those in forest fragments, extinc- from microhabitats searched than prey types per se. For example, tion is inevitable and maintenance of metapopulations relies on in this issue, Arcilla et al. (2015) found that sallying insectivores organisms being able to disperse throughout the landscape were more sensitive to logging in African forests than other spe- (Hanski, 1994, 1998). Whereas dispersal limitation may not pro- cies. Answering whether loss of microhabitat structure or a vide a mechanism of species loss per se, it can limit re-coloniza- decrease in prey type could induce such an effect is vital, and in tion of truly isolated fragments—even if they contain suitable this issue, Hamer et al. (2015) offer a direction toward this answer habitat. Stouffer and Bierregaard (1995) proposed that frag- based on stable isotopes, a technique that has seldom been applied mentation-sensitive understory insectivores, particularly terres- in the tropics. The authors determined that Bornean birds at higher trial insectivores, had limited dispersal ability in Manaus, Brazil. trophic levels are more vulnerable to disturbance (Hamer et al., Similarly, Lens et al. (2002) showed that the inability to move 2015), thereby suggesting a link between diet and vulnerability. between and among fragments coupled with tolerance to habitat We suggest researchers further try to establish the link between disturbance reduced the ability of species to persist in an East diet and vulnerability, by taking advantage not only of stable iso- African fragmented forest landscape. Many understory insecti- tope analysis, but also DNA barcoding to identify prey items at ever vores are sedentary residents with short wings (i.e., low wing finer taxonomic scales, allowing for targeted assessment of prey aspect ratio), relatively poor flying ability (Moore et al., 2008), abundance and type. Many soft-bodied insects are quickly and from the little we know, relatively short dispersal distances digested, creating a negative bias for those taxa (Rosenberg and (<400 m for five Amazonian species, Bates, 2002; median for Cooper, 1990). Further, techniques that sample vegetation for Thamnophilus atrinucha: 300 m, Tarwater, 2012; median for arthropods are often biased (Cooper et al., 2012), and do not Myrmeciza exsul: 800 m, Woltmann et al., 2012b) which may necessarily sample the same arthropods that birds eat. Genetic make them poor dispersers and thus vulnerable to local extinc- sequencing approaches using feces (i.e., molecular scatology) have tion in fragmented landscapes (Lens et al., 2002; Claramunt been mostly limited to mammals and other taxa with separate et al., 2012; Woltmann et al., 2012a; Powell, 2013). solid and liquid waste extraction. However, high throughput The nature of the matrix between habitable patches will influ- (AKA next generation) sequencing can use feces to quantify song- ence dispersal decisions. Stouffer and Bierregaard (1995), found bird diets non-invasively (Jedlicka et al., 2013; Vo and Jedlicka, colonization rates of forest fragments by understory insectivores 2015) with basic (i.e. often order- or family-level) but rapidly were strongly influenced by the major vegetation types surround- improving taxonomic specificity. Using these new genetic tech- ing fragments. Asymmetric dispersal from intact to fragmented niques, we can look at the mechanisms for disappearances of rainforests resulted in source-sink dynamics for a sedentary, ter- understory birds through differences in diet; in other words, does restrial insectivore, Australian Logrunner (Orthonyx temminckii), what birds are eating change with disturbance – are they eating but the immigration rates declined when the between-population fewer calorie-rich arthopods in disturbed areas? This technique landscapes were fragmented (Pavlacky et al., 2012). In this issue, can also help us understand how vegetation structure (Stratford Powell et al. (2015) show that two Amazonian woodcreeper spe- and Stouffer, 2015) or light/heat (Pollock et al., 2015) interact with cies recover to primary forest-like movement rates in secondary arthropod communities, and ultimately understory bird com- forest only about 15 years old. However, a terrestrial species of munities. Although this technique is currently costly (lab costs of the forest interior, the Rufous-capped Antthrush (Formicarius $10,000 per instrument run of several hundred feces samples), colma), showed reduced movement into secondary forest even sequencing runs are increasingly affordable with newer and more three decades after pasture abandonment. efficient sequencing machines. Furthermore, in tropical institu- tions where resources are scarce, opportunities can be cultivated through collaboration with researchers in wealthier economies, 3.5. Area sensitivity thus helping to bridge the economic divide and, at the same time, increase local capacities. Understory insectivores will be absent from small forest frag- ments 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 3.3. Altered microclimate insectivores into increasingly smaller fragments of primary forest, it becomes critical to understand the minimum area requirements The vegetation hypothesis does not rule out the possibility of understory bird species (Sodhi et al., 2008). In Manaus, Brazil the that the same changes in vegetation induced by edge effects Minimum Critical Size of Ecosystems Project (later renamed the are also associated with microclimate changes such as increased BDFFP) was designed to address the question of the minimum size light intensity and increased temperatures. These changes may of rainforest required to maintain the animal community themselves make fragments physiologically unsuitable for under- (Bierregaard et al., 1992). Though originally slated for several story birds (Stratford and Robinson, 2005). Patten and Smith- 1000 ha fragments, the project eventually isolated just two Patten (2012) found that light was one of the key factors in edge 100 ha fragments, four 10 ha fragments and five 1 ha fragments. avoidance by disturbance-sensitive species. In this issue, Pollock Nevertheless, results clearly showed that even 100 ha fragments et al. (2015) also found that many understory insectivores are not nearly large enough to sustain the entire understory bird avoided brighter sites. Light can affect birds directly by community (Stouffer et al., 2011), and the critical minimum frag- interfering with searching for prey or indirectly by behavioral ment size required to do so remains unclear in the Neotropics avoidance. Histological comparisons of retinas and behavioral and elsewhere. Importantly, after isolation (and subsequent re-iso- experiments that compare microclimate sensitive species with lations) forest fragments at the BDFFP occurred as small ‘‘islands’’ generalists may also permit us to untangle the confounding inter- within a vast ‘‘sea’’ of continuous forest, whereas many other frag- actions between vegetation structure, prey availability, and mented landscapes are heavily deforested, but are separated by a microclimate. matrix of cultivation (e.g. Newmark, 1991) or mixed second 6 L.L. Powell et al. / Biological Conservation 188 (2015) 1–10 growth and cultivation (e.g. Lens et al., 2002; Peters and Okalo, Already, several diseases, such as Newcastle disease, West Nile 2009). and avian malaria (Plasmodium spp. and Haemoproteus spp.) are Given the enormous increases edge habitat and secondary for- quickly spreading globally and generally have strong negative est in the tropics, it is critical that we embrace the shift from binary effects on naïve bird populations (Kilpatrick et al., 2007; approaches (i.e., habitat/no habitat) with origins in Island Svensson-Coelho et al., 2013; Asghar et al., 2015). An important Biogeography Theory (MacArthur and Wilson, 1967) toward land- example is that of the introduced avian malaria Plasmodium relic- scape ecology approaches that incorporate crucial edge and matrix tum in Hawaii, where the endemic honeycreeper, ‘Apapane effects (Laurance, 2008). Secondary forest matrices are now perva- Himatione sanguinea, was estimated to have lost >50% of first-year sive throughout the tropics; for example, by 2002, the area of sec- juveniles and >25% of adults due to this parasite over a 7-year per- ondary forest in the Brazilian Amazon had increased to iod (Atkinson and Samuel, 2010). This mortality was closely tied to 161,000 km2, about the size of Uruguay (Neeff et al., 2006). Once season, where optimum weather conditions (rainfall and tempera- sufficiently mature, secondary forest can buffer some of the effects ture) in the fall promoted mosquito abundance, thus increasing of area and isolation (Stouffer and Bierregaard, 2007; Powell et al., infection rates. In Hawaii, the distribution of native forest birds is 2013, 2015), allowing previously isolated forest fragments to be presently impacted by a range of environmental factors, particu- connected by a more amenable matrix. Granted, there is no substi- larly avian malaria (van Riper III et al., 1986). Recent phylogenetic tute for primary forest to sustain biological diversity (Gibson et al., and ancestral reconstruction analyses of avian malarial parasites in 2011), but anthropogenic habitats such as shade coffee and sec- three African ecosystems, two of them rainforests, showed almost ondary forests may help conserve understory insectivores in the a four times greater evolutionary transition rate for generalist form of buffers, corridors for dispersal and other landscape connec- parasites to become specialists than the reverse (Loiseau et al., tions. However, the extent to which these altered habitats provide 2012). A concern here is that as malaria-competent generalist viable breeding opportunities for rainforest interior species is not avian hosts invade increasingly disturbed rainforest tracts, the fully understood. chance of introducing novel parasites to susceptible specialist understory insectivores increases, thus posing a potentially severe 3.6. Nest predation conservation threat. These studies exemplify that this body of research is urgently required, especially baseline data before The mesopredator release hypothesis posits that fragmented emerging infectious diseases become pandemic. landscapes have reduced top predators, which allows for the pop- Although an obvious effect of human activity is how we alter ulation increase of mesopredators that can reduce avian pop- landscapes though land-use change, humans are also altering the ulations through increased nest predation (Crooks and Soule, climate in ways that less directly impact tropical birds. In particu- 1999; Schmidt, 2003). In fragmented tropical forests, evidence lar, precipitation regimes in the tropics will change in the future for the mesopredator release hypothesis is equivocal (Robinson and will affect birds by altering plant communities (Rompre and Sherry, 2012). Nest success is highly variable, making infer- et al., 2007; Harris et al., 2011; Wormworth and Sßekerciog˘lu, ences about fragmentation effects difficult (Robinson et al., 2011; Sßekerciog˘lu et al., 2012). Changing precipitation in the trop- 2000). In this issue, Visco and Sherry (2015) examined nest preda- ics will also impact invertebrate prey populations that could affect tion and predators on Chestnut-backed Antbirds (M. exsul) in Costa understory insectivores in ways that are not necessarily pre- Rica, finding that predation rates were lower in forest fragments dictable (Sßekerciog˘lu et al., 2012). For example, changing precip- than in a large forest tract, providing evidence against the itation affects tropical tree phenology (Walther et al., 2002), mesopredator release hypothesis—at least for one avian species. which will affect the amount of leaf litter and, in turn, affect leaf One clear result is that snakes are the primary nest predators in litter arthropods. Additionally, altered precipitation regimes will Panama (Robinson et al., 2005) and Costa Rica (Visco and Sherry, affect fire dynamics (Román-Cuesta et al., 2014), including the 2015). There are fewer studies of nest predation on understory penetration of fire into forest fragments (Laurance et al., 2014b). insectivores from tropical sites outside of the Neotropics. In Effects of climate change will likely occur in all tropical sites, and Africa, Githiru et al. (2005) used plasticine eggs to find that mam- a coordinated effort to get baseline data on abundances and dis- mals were the primary nest predators and fragments of compara- tributions should be pursued as quickly as possible. Because the ble sizes experienced similar predation rates. In Malaysia, Cooper effort required to get these baseline data exceeds the number of and Francis (1998) used artificial nests and found predation rates professional tropical ornithologists, wherever feasible we urge were highest along edges of logged forests and lowest in intact for- the development of citizen-science projects. In this issue, Boyle ests. Great caution should be used in interpreting the differences and Sigel (2015) show that a standardized citizen science approach between sites since different methods of inferring nest predation can quantify avian populations over large scales. (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, 4. Where to go from here? A research prospectus for the ecology a remarkable result from the Taita Hills, Kenya, showed that in and conservation of understory insectivores one understory insectivore species persisting in fragments and with a 69% overall rate of nest predation over three years of study, 4.1. Increase geographic coverage nest predation was lower at the edge than interior (Spanhove et al., 2014). With additional studies from the understudied Paleotropics, Of paramount importance is to identify the ecological and taxo- the potential to develop a conceptual framework around nest pre- nomic groups that are most sensitive to forest loss and degradation dation is more likely. We therefore urge more studies of nest pre- and how these patterns vary geographically. Patterns of species’ dation at tropical sites, particularly in Paleotropical forests, using sensitivities are known for many lowland Neotropical forests videography to monitor nests. (e.g., Robinson, 1999; Stouffer and Bierregaard, 1995; Sigel et al., 2010), but are poorly known in most other tropical forests. 3.7. Emerging threats: Infectious diseases and climate change Researchers should focus efforts on filling these geographic gaps in our knowledge. Examples of such recent initiatives include the Increased international trade and transportation is predicted to Equatorial Guinea Bird Initiative (https://www.kickstarter.com/ intensify the incidence of wildlife diseases (Pongsiri et al., 2009). projects/1663751187/equatorial-guinea-bird-initiative) from the L.L. Powell et al. / Biological Conservation 188 (2015) 1–10 7
Lower Guinea Forests of Central Africa, and species recovery in Cordeiro et al., 2015), (iv) habitat loss (Pavlacky et al., 2015), (v) newly afforested sub-tropical forests of China (Zhang et al., degradation and logging (Hamer et al., 2015; Arcilla et al., 2015), 2011). An additional example is that of the Stability of Altered (vi) natural enemies, (vii) climate change, or (viii) emerging infec- Forest Ecosystems (SAFE) Project that offers new opportunities to tious diseases. Given that climate change and habitat loss are the experimentally research the effects of forest fragmentation on greatest threats to biodiversity today (Sala et al., 2000), and vul- understory insectivores (among other taxa) in Borneo, where pri- nerability to climate change is very difficult to estimate empirically mary rainforests are under immediate threat from oil palm expan- (Wormworth and Sßekerciog˘lu, 2011), we suggest that a more prac- sion (Ewers et al., 2011). Tropical regions that require more tical approach would be to examine the effects of habitat loss, research to note patterns of impacted species include Africa, which in the tropics is driven primarily by expansion of agricul- Southeast Asia, western India, and Madagascar. We understand tural fields, such as oil palm plantations in Australasia (Boucher very little of the ecological roles of understory insectivores et al., 2011). Thus one critical question that needs to be addressed pantropically, as well as the consequences on ecosystems when pantropically is how to manage human-modified landscapes that these communities are altered. support sustainable populations of the understory bird com- munity. Furthermore, identifying the characteristics of species lost 4.2. Standardizing efforts to understand the guild: a pantropical effort from smaller, more isolated areas are of great interest at the local and landscape scales. Likewise, it is essential to know (in a To understand the vulnerabilities faced by understory insecti- pantropical framework) maximum distance from the edge of an vores, we need to understand if they respond similarly to equiva- oil palm (or other) plantation at which the primary forest under- lent threats from different biogeographic realms and if the story bird community is affected, and to understand the character- mechanisms of sensitivity are similar. Currently, there is no con- istics of the species that drop out of the community when sensus on either of these aspects, and the causes are likely to vary approaching the edge. Evaluating the consequences of forest modi- geographically (Stratford and Robinson, 2005). Not since David fication with remnant patches embedded in a broader landscape Pearson (1977) worked in Ecuador, Bolivia, Peru, Gabon, Borneo context may provide additional insights for the conservation of and New Guinea has an ornithologist attempted a standardized understory insectivores (Laurance, 2008). If we can understand cross-continental comparison of tropical rainforest bird com- the characteristics that make birds vulnerable to disturbances in munities, and a pantropical comparison has never been undertaken a standardized pantropical framework, then we can apply general from a conservation standpoint. To date, pantropical comparisons conservation and management guidelines worldwide without an have been difficult, including in this special issue, because research in-depth knowledge of the avifauna in a given location. This is criti- questions and subsequent study designs are not standardized cal as some biomes (Atlantic rainforest, (Anjos et al., 2015), Upper among studies. For example, just within this special issue, Guinea forests (Arcilla et al., 2015)) may be disappearing too fast to responses of understory insectivores to disturbance are quantified fully understand the vulnerabilities of the bird community. with movement rates (Powell et al., 2015), nest success (Visco and Coordinating our efforts to standardize studies of relevant distur- Sherry, 2015), audiovisual sampling (Boyle and Sigel, 2015; bances pantropically and to standardize how we quantify life-his- Cordeiro et al., 2015; Pavlacky et al., 2015), experimental playbacks tory characteristics that may indicate vulnerability to disturbances (Cordeiro et al., 2015), and mist-net derived species richness esti- will be critical as tropical forests continue to be lost and degraded. mates (Arcilla et al., 2015; Buechley et al., 2015). Granted, no one ‘‘correct’’ metric exists to quantify understory birds’ vulnerability 4.4. Mixed-species flocks and ant-following birds: what we know and to disturbance, but coordinated efforts and study designs will what we are missing greatly facilitate cross-tropical comparisons. For example, stan- dardized mist-netting specifically designed to estimate survival Understanding the dynamics of mixed-species flocks and ant- (sensu Ruiz-Gutiérrez et al., 2012) in primary forest vs. disturbed following birds will be essential as disturbance continues to accel- forest (e.g. edge, fragments, secondary forest) can provide both a erate in tropical forests because these groups consist of species direct estimate of fitness (i.e. survival) as well as comparisons of that depend on the presence of other species, so conservation community composition across habitats and rainforest regions. efforts cannot simply be species-specific. For example, in this issue Wolfe et al. (2014) used mist-netting efforts in an analysis of varia- Cordeiro et al. (2015) showed that the Square-tailed Drongo (D. tion in understory insectivore survival across primary forests in ludwigii) is a key nuclear species in East African mixed-species Amazonia; similar efforts could be undertaken that incorporate flocks, and that flocks are larger in the presence of this species. degraded forests and across rainforest regions. Such standardized Similarly, in ant-following flocks in Kenyan fragments, species designs will help identify characteristics of understory insectivores richness of flocks declined in smaller fragments and degraded for- (e.g. wing aspect ratio, dispersal ability, small body size, trophic est, and this decline was largely attributed to reduced abundance level, foraging technique) that make them vulnerable to distur- of specialized ant-followers (Peters et al., 2008). The relevance of bances, not only locally, but also globally across the tropics. Even these findings is underscored by evidence showing that, in a rudimentary understanding of the characteristics that make mixed-species flocks, nuclear species or flock leaders maintain understory insectivores vulnerable to disturbances across rain- beneficial associations with other flocking species (Hino, 1998; forest regions will help focus conservation actions on the most vul- Srinivasan et al., 2010), especially among insectivores (Kotagama nerable taxa. Continued collaborative efforts through symposia, and Goodale, 2004). Such associations have their rewards: species workshops, grant proposals, review papers and meta-analyses will that frequent flocks increase their survival (Jullien and Clobert, help foster a more coordinated, global effort. 2000; Cruz-Angón et al., 2008) and therefore losing flock leaders that help aggregate such flocks can ultimately diminish avian com- 4.3. Standardizing how we study threats to understory insectivores munities in multiple ways (Dolby and Grubb, 2000; Maldonado- Coelho and Marini, 2004; Stouffer and Bierregaard, 1995). Will To design an effective standardized protocol, researchers must conservation efforts directed at flock leaders have a disproportion- first agree on the most pressing question(s) as determined by fac- ately positive effect? Will the loss of mixed-species flocks from tors threatening tropical understory birds. Researchers could focus fragmented landscapes have major impact on prey populations? on myriad factors including (i) agriculture (Buechley et al., 2015), How do urban and suburban habitats affect flock composition? (ii) forest edges, (iii) fragmentation per se (Pavlacky et al., 2015; These are issues begging more research, especially because a 8 L.L. Powell et al. / Biological Conservation 188 (2015) 1–10 number of understory insectivores are among those specialized special issue. We thank Nicole Arcilla, Jeffrey Brawn, Evan species that either join mixed-species flocks or follow ant swarms. Buechley, Keith Hamer, Luc Lens, David Pavlacky Jr., Henry Our knowledge about mixed-species flocks and ant-following Pollock, James Remsen, Çag˘an Sßekerciog˘lu, Phil Stouffer and Tom species continues to grow, especially in Asia and Africa, as com- Sherry for providing friendly reviews of this manuscript, and pared to the relatively better-known Neotropics. However, there David Pavlacky with help on Australian bird ecology. A construc- is much opportunity for discovery in all regions. In this issue, tive review from an anonymous reviewer improved this manu- Colorado and Rodewald (2015) show that in the Andes, anthro- script. We acknowledge and thank both the governmental and pogenic habitats with overstory trees can help promote mixed- non-governmental organizations that allowed for field studies on species flock presence, but that only flocks in rainforest retain their lands as well as the local people that share the forest with forest specialists such as bark and foliage insectivores. Furthermore, us and the diversity around them. Mokross et al. (2014) found that in the central Amazon, associa- tions among flocking species break down with increased distur- bance. Ant-following birds tend to disappear quickly as army-ants are excluded after forest fragmentation in the Neotropics References (Stouffer and Bierregaard, 1995) and Africa (Peters and Okalo, 2009), but at least in Amazonia, these groups seem to recover in 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. <30 years if secondary forest is allowed to regenerate (Powell Determination of tropical deforestation rates and related carbon losses from et al., 2013). Generally speaking, understanding the dynamics of 1990 to 2010. Glob. Change Biol. 20, 2540–2554. these fascinating examples of convergent evolution of multi-spe- Anjos, L., Collins, C., Holt, R., Volpato, G., Lopes, E., Bochio, G., 2015. Can habitat specialization patterns of Neotropical birds highlight vulnerable areas for cies social systems can be generalized to promote a pantropical conservation in the Atlantic rainforest, southern Brazil? Biol. Conserv. 188, 32– understanding of tropical understory bird ecology. 40. Arcilla, N., Holbech, L.H., O’Donnell, S., 2015. Severe declines of understory birds 5. Conclusions follow illegal logging in Upper Guinea forests of Ghana, West Africa. Biol. Conserv. 188, 41–49. Asghar, M., Hasselquist, D., Hansson, B., Zehtindjiev, P., Westerdahl, H., Bensch, S., The papers in this special issue fill many gaps in our under- 2015. Hidden costs of infection: chronic malaria accelerates telomere standing of tropical understory insectivores, but several crucial degradation and senescence in wild birds. Science 347, 436–438. Atkinson, C.T., Samuel, M.D., 2010. Avian malaria Plasmodium relictum in native questions remain unanswered. Many of the results from these Hawaiian forest birds: epizootiology and demographic impacts on8 apapane papers were unexpected. For instance, Anjos et al. (2015) found Himatione sanguinea. J. Avian Biol. 41, 357–366. that the forests with the highest plant diversity did not have the Bates, J.M., 2002. The genetic effects of forest fragmentation on five species of most habitat specialists, Boyle and Sigel (2015) found smaller-bod- Amazonian Birds. J. Avian Biol. 33, 276–294. Beier, P., Van Drielen, M., Kankam, B.O., 2002. Avifaunal collapse in West African ied birds were more sensitive to habitat loss than larger-bodied forest fragments. Conserv. Biol. 16, 1097–1111. birds, and Buechley et al. (2015) found greater species richness Borges, S.H., Guiherme, E., 2000. Comunidade de aves em um fragmento florestal of understory insectivores in Ethiopian shade coffee farms than urbano em Manaus, Amazonas, Brasil. Ararajuba 8, 17–23. Buechley, E.R., Sßekerciog˘lu, Ç.H., Atickem, A., Gebremichael, G., N’dungu, J.K., in nearby forest. Arcilla et al. (2015), working in Ghanaian forests, Mahamued, B.A., Beyene, T., Mekonnen, T., Lens, L., 2015. Importance of found that the relative abundance of understory generalists was Ethiopian shade coffee farms for forest bird conservation. Biol. Conserv. 188, lower in logged than unlogged forest, a result contrasting numer- 50–60. Bierregaard, R.O., Lovejoy, T.E., Kapos, V., dos Santos, A.A., Hutchings, R.W., 1992. ous tropical studies suggesting that forest specialists are more The biological dynamics of tropical rainforest fragments. Bioscience 42, 859– negatively impacted (Bregman et al., 2014). Understory insecti- 866. vores in Gondwana rainforests of Australia are often considered Birdlife International, 2015. Birdlife Data Zone [WWW Document].
Chaves-Campos, J., DeWoody, J.A., 2008. The spatial distribution of avian relatives: Korfanta, N.M., Newmark, W.D., Kauffman, M.J., 2012. Long-term demographic do obligate army-ant-following birds roost and feed near family members? Mol. consequences of habitat fragmentation to a tropical understory bird Ecol. 17, 2963–2974. community. Ecology 93, 2548–2559. Chaves-Campos, J., Araya-Ajoy, Y.M., Lizana-Moreno, C.A., Rabenold, K.N., 2009. The Kotagama, S.W., Goodale, E., 2004. The composition and spatial organization of effect of local dominance and reciprocal tolerance on feeding aggregations of mixed-species flocks in a Sri Lankan rainforest. Forktail 20, 63–70. ocellated antbirds. Proc. Roy. Soc. B: Biol. Sci. 276, 3995–4001. Lambert, F.R., 1992. The consequences of selective logging for Bornean lowland Chesser, R.T., 1995. Comparative diets of obligate ant-following birds at a site in forest birds. Philos. Trans. Roy. Soc. Lond. Ser. B: Biol. Sci. 335, 443–457. northern Bolivia. Biotropica 27, 382–390. Lambert, F.R., Collar, N.J., 2002. The future for Sundaic lowland forest birds: long- Claramunt, S., Derryberry, E.P., Remsen, J.V., Brumfield, R.T., 2012. High dispersal term effects of commercial logging and fragmentation. Forktail 18, 127–146. ability inhibits speciation in a continental radiation of passerine birds. Proc. Laurance, W.F., 2008. Theory meets reality: how habitat fragmentation research has Roy. Soc. B: Biol. Sci. 279, 1567–1574. transcended island biogeographic theory. Biol. Conserv. 141, 1731–1744. Colorado, G.J., Rodewald, A.D., 2015. Response of mixed-species flocks to habitat Laurance, W.F., Lovejoy, T.E., Vasconcelos, H.L., Bruna, E.M., Didham, R.K., Stouffer, alteration and deforestation in the Andes. Biol. Conserv. 188, 72–81. P.C., Gascon, C., Bierregaard, R.O., Laurance, S.G., Sampaio, E., 2002. Ecosystem Cooper, D.S., Francis, C.M., 1998. Nest predation in a Malaysian lowland rain forest. decay of Amazonian forest fragments: a 22-year investigation. Conserv. Biol. 16, Biol. Conserv. 85, 199–202. 605–618. Cooper, N.W., Thomas, M.A., Garfinkel, M.B., Schneider, K.L., Marra, P.P., 2012. Laurance, W.F., Sayer, J., Cassman, K.G., 2014a. Agricultural expansion and its Comparing the precision, accuracy and efficiency of branch clipping and sweep impacts on tropical nature. Trends Ecol. Evol. 29, 107–116. netting for sampling arthropods in two Jamaican forest types. J. Field Ornithol. Laurance, W.F., Andrade, A.S., Magrach, A., Camargo, J.L.C., Campbell, M., Fearnside, 83, 381–390. P.M., Edwards, W., Valsko, J.J., Lovejoy, T.E., Laurance, S.G., 2014b. Apparent Cordeiro, N.J., Borghesio, L., Joho, M.P., Monoski, T.J., Mkongewa, V.J., Dampf, C.J., environmental synergism drives the dynamics of Amazonian forest fragments. 2015. Forest fragmentation in an African biodiversity hotspot impacts mixed- Ecology 95, 3018–3026. species bird flocks. Biol. Conserv. 188, 61–71. Lawton, J.H., Bignell, D.E., Bolton, B., Bloemers, G.F., Eggleton, P., Hammond, P.M., Corlett, R.T, Primack, R.B., 2011. Tropical Rainforests: An Ecological and Hodda, M., Holt, R.D., Larsen, T.B., Mawdsley, N.A., Stork, N.E., Srivastava, D.S., Biogeographical Comparison, second ed. Wiley-Blackwell. Watt, A.D., 1998. Biodiversity inventories, indicator taxa and effects of habitat Crooks, K.R., Soule, M.E., 1999. Mesopredator release and avifaunal extinctions in a modification in tropical forest. Nature 391, 72–76. fragmented system. Nature 400, 563–566. Leck, C.F., 1979. Avian extinctions in an isolated tropical wet-forest preserve, Cruz-Angón, A., Sillett, T.S., Greenberg, R., 2008. An experimental study of habitat Ecuador. Auk 96, 343–352. selection by birds in a coffee plantation. Ecology 89, 921–927. Lens, L., VanDongen, S., Norris, K., Githiru, M., Matthysen, E., 2002. Avian persistence Devries, P.J., Austin, G.T., Martin, N.H., 2008. Diel activity and reproductive isolation in fragmented rainforest. Science 298, 1236–1238. in a diverse assemblage of Neotropical skippers (Lepidoptera: Hesperiidae). Lim, H.C., Sodhi, N.S., 2004. Responses of avian guilds to urbanisation in a tropical Biol. J. Linn. Soc. 94, 723–736. city. Landscape Urban Plann 66, 199–215. Dirzo, R., Raven, P.H., 2003. Global state of biodiversity and loss. Annu. Rev. Environ. Loiseau, C., Harrigan, R.J., Robert, A., Bowie, R.C., Thomassen, H.A., Smith, T.B., Resour. 28, 137–167. Sehgal, R.N., 2012. Host and habitat specialization of avian malaria in Africa. Dolby, A.S., Grubb Jr., T.C., 2000. Social context affects risk taking by a satellite Mol. Ecol. 21, 431–441. species in a mixed-species foraging group. Behav. Ecol. 11, 110–114. MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton Ewers, R.M., Didham, R.K., Fahrig, L., Ferraz, G.F., Hector, A., Holt, R.D., Kapos, V., University Press. Reynolds, G., Sinun, W., Snaddon, J.L., Turner, E.C., 2011. A large-scale forest Macedo, M.N., DeFries, R.S., Morton, D.C., Stickler, C.M., Galford, G.L., Shimabukuro, fragmentation experiment: the Stability of Altered Forest Ecosystems Project. Y.E., 2012. Decoupling of deforestation and soy production in the southern Philos. Trans. Roy. Soc. B 366, 3292–3302. Amazon during the late. Proc. Natl. Acad. Sci. 109, 1341–1346. Fregin, S., Haase, M., Olsson, U., Alström, P., 2012. New insights into family Maldonado-Coelho, M., Marini, M.Â., 2004. Mixed-species bird flocks from Brazilian relationships within the avian superfamily Sylvioidea (Passeriformes) based on Atlantic forest: the effects of forest fragmentation and seasonality on their size, seven molecular markers. BMC Evol. Biol. 12, 157. richness and stability. Biol. Conserv. 116, 19–26. Gibson, L., Lee, T.M., Koh, L.P., Brook, B.W., Gardner, T.A., Barlow, J., Peres, C.A., Martinez, A.E., Gomez, J.P., 2013. Are mixed-species bird flocks stable through two Bradshaw, C.J.A., Laurance, W.F., Lovejoy, T.E., Sodhi, N.S., 2011. Primary decades? Am. Nat. 181, E53–E59. forests are irreplaceable for sustaining tropical biodiversity. Nature 478, 378– McClure, H.E., 1967. Composition of mixed species flocks in lowland and sub- 381. montane forests of Malaya. Wilson Bull. 79, 131–154. Githiru, M., Lens, L., Bennun, L., 2007. Ranging behaviour and habitat use by an McDonald, R.I., Kareiva, P., Forman, R.T.T., 2008. The implications of current and Afrotropical songbird in a fragmented landscape. Afr. J. Ecol. 45, 581–589. future urbanization for global protected areas and biodiversity conservation. Githiru, M., Lens, L., Cresswell, W., 2005. Nest predation in a fragmented Biol. Conserv. 141, 1695–1703. Afrotropical forest: evidence from natural and artificial nests. Biol. Conserv. Michel, N.L., Sherry, T.W., Carson, W.P., 2014. The omnivorous collared peccary 123, 189–196. negates an insectivore-generated trophic cascade in Costa Rican wet tropical Geist, H.J., Lambin, E.F., 2002. Proximate causes and underlying driving forces of forest understorey. J. Trop. Ecol. 30, 1–11. tropical deforestation. Bioscience 52, 143–150. Mokross, K., Ryder, T.B., Côrtes, M.C., Wolfe, J.D., Stouffer, P.C., 2014. Decay of Goodale, E., Nizam, B.Z., Robin, V.V., Sridhar, H., Trivedi, P., Kotagama, S.W., interspecific avian flock networks along a disturbance gradient in Amazonia. Padmalal, U.K.G.K., Perera, R., Pramod, P., Vijayan, L., 2009. Regional variation in Proc. Roy. Soc. B 281, 20132599. the composition and structure of mixed-species bird flocks in the Western Mooney, K.A., Gruner, D.S., Barber, N.A., Van Bael, S.A., Philpott, S.M., Greenberg, R., Ghats and Sri Lanka. Curr. Sci. 97, 648–663. 2010. Interactions among predators and the cascading effects of vertebrate Global Forest Watch.
and limits regional patch occupancy in a spatially structured bird population. J. Sigel, B., Robinson, W.D., Sherry, T.W., 2010. Comparing bird community responses Anim. Ecol. 81, 940–952. to forest fragmentation in two lowland Central American reserves. Biol. Pearson, D.L., 1977. A pantropical comparison of bird community structure on six Conserv. 143, 340–350. lowland forest sites. Condor 79, 232–244. Sodhi, N.S., Koh, L.P., Prawiradilaga, D.M., Tinulele, I., Putra, D.D., Tan, T.H.T., 2005. Peh, K.S.H., Jong, J.d., Sodhi, N.S., Lim, S.L.H., C.A.M., Yap, 2005. Lowland rainforest Land use and conservation value for forest birds in Central Sulawesi (Indonesia). avifauna and human disturbance: persistence of primary forest birds in Biol. Conserv. 122, 547–558. selectively logged forests and mixed-rural habitats of southern Peninsular Sodhi, N.S., Posa, M.R.C., Lee, T.M., Warkentin, I.G., 2008. Effects of disturbance or Malaysia. Biol. Conserv. 123, 489–505. loss of tropical rainforest on birds. Auk 125, 511–519. Peters, M.K., Likare, S., Kraemer, M., 2008. Effects of habitat fragmentation and Spanhove, T., Callens, T., Hallmann, C.A., Pellikka, P., Lens, L., 2014. Nest predation in degradation on flocks of African ant-following birds. Ecol. Appl. 18, 847–858. Afrotropical forest fragments shaped by inverse edge effects, timing of nest Peters, M.K., Okalo, B., 2009. Severe declines of ant-following birds in African initiation and vegetation structure. J. Ornithol. 155, 411–420. rainforest fragments are facilitated by a subtle change in army ant Srinivasan, U., Raza, R.H., Quader, S., 2010. The nuclear question: rethinking species communities. Biol. Conserv. 142, 2050–2058. importance in multi-species animal groups. J. Anim. Ecol. 79, 948–954. Pickett, S.T., Cadenasso, M., Grove, J., Nilon, C., Pouyat, R., Zipperer, W., Costanza, R., Stouffer, P.C., Bierregaard, R.O., 1995. Use of Amazonian forest fragments by 2001. Urban ecological systems: linking terrestrial ecological, physical, and understory insectivorous birds. Ecology 76, 2429–2445. socioeconomic components of metropolitan areas. Annu. Rev. Ecol. Syst., 127– Stouffer, P.C., Bierregaard, R.O., 2007. Recovery potential of understory bird 157 communities in Amazonian Forest Fragments. Rev. Bras. Ornitologia 15, 219– Pollock, H.S., Cheviron, Z.A., Agin, T.J., Brawn, J.D., 2015. Absence of microclimate 229. selectivity in insectivorous birds of the Neotropical forest understory. Biol. Stouffer, P.C., Johnson, E.I., Bierregaard, R.O., Lovejoy, E., 2011. Understory bird Conserv. 188, 116–125. communities in Amazonian rainforest fragments: species turnover through 25 Pongsiri, M.J., Roman, J., Ezenwa, V.O., Goldberg, T.L., Koren, H.S., Newbold, S.C., years post-isolation in recovering landscapes. PlosONE 6, e20543. Ostfeld, R.S., Pattanayak, S.K., Salkeld, D.J., 2009. Biodiversity loss affects global Stratford, J.A., Robinson, W.D., 2005. Gulliver travels to the fragmented tropics: disease ecology. Bioscience 59, 945–954. geographic variation in mechanisms of avian extinction. Front. Ecol. Environ. 3, Powell, G.V.N., 1985. Sociobiology and adaptive significance of interspecific foraging 85–92. flocks in the Neotropics. Ornithological Monogr. 36, 713–732. Stratford, J.A., Sßekerciog˘lu, Ç.H., in press. Birds in forest ecosystems. In: Peh, K., Powell, G.V.N., 1989. On the possible contribution of mixed species flocks to species Corlett, R., Bergeron, Y., (Eds.), Handbook of Forest Ecology, Routledge. richness in neotropical avifaunas. Behav. Ecol. Sociobiol. 24, 387–393. Stratford, J.A., Stouffer, P.C., 1999. Local extinctions of terrestrial insectivorous birds Powell, L.L., Stouffer, P.C., Johnson, E.I., 2013. Recovery of understory bird in a fragmented landscape near Manaus, Brazil. Conserv. Biol. 13, 1416–1423. movement across the interface of primary and secondary Amazon rainforest. Stratford, J.A., Stouffer, P.C., 2013. Microhabitat associations of terrestrial Auk 140, 459–468. insectivorous birds in Amazonian rainforest and second-growth forests. J. Powell, L.L., 2013. Recovery of Understory Bird Movement in Post-pasture Field Ornithol. 84, 1–12. Amazonia (Ph.D. dissertation), Louisiana State University, Baton Rouge, LA. Stratford, J.A., Stouffer, P.C., 2015. Forest fragmentation alters microhabitat Powell, L.L., Wolfe, J.D. Johnson, E.I., Hines, J.E., Nichols, J.D., Stouffer, P.C., 2015. availability for Neotropical terrestrial insectivorous birds. Biol. Conserv. 188, Heterogeneous movement of insectivorous Amazonian birds through primary 109–115. and secondary forest: a case study using multistate models with radiotelemetry Svensson-Coelho, M., Blake, J.G., Loiselle, B.A., Penrose, A.S., Parker, P.G., Ricklefs, data. Biol. Conserv. 188, 100–108. R.E., 2013. Diversity, prevalence, and host specificity of avian Plasmodium and Poulin, B., Lefebre, G., Ibañez, R., Jaramillo, C., Hernández, C., Rand, A.S., 2001. Avian Haemoproteus in a western Amazon assemblage. Ornithological Monogr. 76, 1– predation upon lizards and frogs in a neotropical forest understory. J. Trop. Ecol. 47. 17, 21–40. Tarwater, C.T., 2012. Influence of phenotypic and social traits on dispersal in a Ribon, R., Simon, J.E., Theodoro De Mattos, G., 2003. Bird extinctions in Atlantic family living, tropical bird. Behav. Ecol. 23, 1242–1249. forest fragments of the Viçosa region, southeastern Brazil. Conserv. Biol. 17, Thiollay, J.M., 1997. Disturbance, selective logging and bird diversity: a Neotropical 1827–1839. forest study. Biodivers. Conserv. 6, 1155–1173. Ridgely, R.S., Tudor, G., 1994. The Birds of South America. Volume II. The Suboscine Tobias, J.A., Sßekerciog˘lu, Ç.H., Vargas, F.H., 2013. Bird conservation in tropical Passerines. University of Texas Press. ecosystems: challenges and opportunities. In: MacDonald, D. (Ed.), Key Topics Ruiz-Gutiérrez, V., Doherty Jr., P.F., Santana, E.C., Martínez, S.C., Schondube, J., in Conservation Biology, vol. 2. Wiley-Blackwell, Oxford, pp. 258–276. Munguía, H.V., Iñigo-Elias, E., 2012. Survival of resident Neotropical birds: van Riper III, C., van Riper, S.G., Goff, M.L., Laird, M., 1986. The epizootiology and Considerations for sampling and analysis based on 20 years of bird-banding ecological significance of malaria in Hawaiian land birds. Ecol. Monogr. 56, 327– efforts in Mexico. Auk 129, 500–509. 344. Richardson, J.J., Moskal, L.M., Bakker, J.D., 2014. Terrestrial laser scanning for Waltert, M., Mardiastuti, A.N.I., Mühlenberg, M., 2004. Effects of land use on bird vegetation sampling. Sensors 14, 20304–20319. species richness in Sulawesi, Indonesia. Conserv. Biol. 18, 1339–1346. Robinson, W.D., 1999. Long-term changes in the avifauna of Barro Colorado Island, Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Panama, a tropical forest isolate. Conserv. Biol. 13, 85–97. Fromentin, J.-M., Hoegh-Guldberg, O., Bairlein, F., 2002. Ecological responses Robinson, W.D., Robinson, T.R., Robinson, S.K., Brawn, J.D., 2000. Nesting success of to recent climate change. Nature 416, 389–395. understory forest birds in central Panama. J. Avian Biol. 31, 151–164. Webb, L.J., Tracey, J.G., Williams, W.T., 1984. A floristic framework of Australian Robinson, W.D., Rompre, G., Robinson, T.R., 2005. Videography of Panama bird nests rainforests. Aust. J. Ecol. 9, 169–198. shows snakes are principal predators. Ornitologia Neotrop. 16, 187–195. Willis, E.O., 1974. Populations and local extinctions of birds on Barro Colorado Robinson, W.D., Sherry, T.W., 2012. Mechanisms of avian population decline and Island, Panama. Ecol. Monogr. 44, 153–169. species loss in tropical forest fragments. J. Ornithol. 153, S141–S152. Willis, E.O., 1979. The composition of avian communities in remanescent woodlots Román-Cuesta, R., Carmona-Moreno, C., Lizcano, G., New, M., Silman, M., Knoke, T., in southern Brazil. Papeis Avulsos de Zoologia 33, 1–25. Malhi, Y., Oliveras, I., Asbjornsen, H., Vuille, M., 2014. Synchronous fire activity Willis, E.O., Oniki, Y., 1978. Birds and army ants. Annu. Rev. Ecol. Syst. 9, 243–263. in the tropical high Andes: an indication of regional climate forcing. Glob. Willson, S.K., 2004. Obligate army-ant-following birds: a study of ecology, spatial Change Biol. 20, 1929–1942. movement patterns, and behavior in Amazonian Peru. Ornithological Monogr., Rompre, G., Robinson, W.D., Desrochers, A., Angehr, G., 2007. Environmental 1–67 correlates of avian diversity in lowland Panama rain forests. J. Biogeogr. 34, Wolfe, J.D., Stouffer, P.C., Seeholzer, G.F., 2014. Variation in tropical bird survival 802–815. across latitude and guilds: a case study from the Amazon. Oikos 123, 964–970. Rosenberg, K.V., Cooper, R.J., 1990. Approaches to avian diet analysis. Stud. Avian Woltmann, S., Kreiser, B.R., Sherry, T.W., 2012a. Fine-scale genetic population Biol. 13, 80–90. structure of an understory rainforest bird in Costa Rica. Conserv. Genet. 13, Sala, O., Chapin III, F., Armesto, J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, 925–935. E., Huenneke, L., Jackson, R., Kinzig, A., 2000. Global biodiversity scenarios for Woltmann, S., Sherry, T.W., Kreiser, B.R., 2012b. A genetic approach to estimating the year 2100. Science 287, 1770–1774. natal dispersal distances and self-recruitment in rainforest resident birds. J. Sangster, G., Alström, P., Forsmark, E., Olsson, U., 2010. Multi-locus phylogenetic Avian Biol. 43, 33–42. analysis of Old World chats and flycatchers reveals extensive paraphyly at Wormworth, J., Sßekerciog˘lu, Ç.H., 2011. Winged Sentinels: Birds and Climate family, subfamily and genus level (Aves: Muscicapidae). Mol. Phylogenet. Evol. Change. Cambridge University Press, Cambridge, UK. 57, 380–392. Wright, S.J., 2005. Tropical forests in a changing environment. Trends Ecol. Evol. 20, Schmidt, K.A., 2003. Nest predation and population declines in Illinois songbirds: a 553–560. case for mesopredator effects. Conserv. Biol. 17, 1141–1150. Visco, D.M., Sherry, T.W., 2015. Increased abundance, but reduced nest predation in Sßekerciog˘lu, Ç.H., 2011. Functional extinctions of bird pollinators cause plant the chestnut-backed antbird in costa rican rainforest fragments: surprising declines. Science 331, 1019–1020. impacts of a pervasive snake species. Biol. Conserv. 188, 22–31. Sßekerciog˘lu, Ç.H., Ehrlich, P.R., Daily, G.C., Aygen, D., Goehring, D., Sandí, R., 2002. Vo, A.T.E., Jedlicka, J.A., 2015. Protocols for metagenomic DNA extraction and Disappearance of insectivorous birds from tropical forest fragments. Proc. Natl. Illumina amplicon library preparation for fecal and swab samples. Mol. Ecol. Acad. Sci. 99, 263–267. Resour. 6, 1183–1197. Sßekerciog˘lu, Ç.H., Primack, Richard B., Wormworth, J., 2012. The effects of climate Zhang, Q., Han, R., Zou, F., 2011. Effects of artificial afforestation and successional change on tropical birds. Biol. Conserv. 148, 1–18. stage on a lowland forest bird community in southern China. For. Ecol. Manage. Sherry, T.W., 1984. Comparative dietary ecology of sympatric, insectivorous 261, 1738–1749. neotropical flycatchers (Tyrannidae). Ecol. Monogr. 54, 313–338.