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The 3 antbird (Thamnophilidae) species that were the focus of Edwin O. Willis' seminal research on army-ants and their avian attendants on Barro Colorado Island, Panama. (A) Ocellated Antbird (Phaenostictus mcleannani), (B) Bicolored Antbird (Gymnopithys bicolor), and (C) Spotted Antbird (Hylophylax naevioides). Photos courtesy of John Whitelaw © 2016.
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Army-ants (particularly swarm-raiding species Eciton burchellii and Labidus praedator) are keystone predators in Neotropical forests. Hundreds of associated species from diverse taxa depend on them for survival, the most conspicuous of which are the ant-following birds. These birds forage on cryptic arthropods and vertebrates as they attempt to esc...
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... was the first to test this hypothesis. He color-banded individuals of 3 antbird species (family Thamnophilidae)-the Ocellated Antbird (Phaenostictus mcleannani), the Bicolored Antbird (Gymnopithys bicolor), and the Spotted Antbird (Hylophylax naevioides; Figure 2) to assess their space use and territorial dynamics. Based on hundreds of hours of observations of individuals at and away from ant swarms, TABLE 1. Five key research areas and the future opportunities that they present for conceptual advances using ant-followers as a model system. ...
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... For example, Aguaruna people use the name kuncháu to refer to both the White-plumed Antbird (Pithys albifrons) and the Bicolored Antbird (Gymnopithys bicolor), members of the Thamnophilidae (whose Greek roots mean "ant-loving") family. The Aguaruna describe these species as walking with ants in the same way that people walk their dogs [32], while the ecological explanation for this behavior is that that antbirds follow army ant swarms to forage on arthropods and small vertebrates attempting to escape becoming prey to the ants [38]. Another contrast in Aguaruna and scientific interpretations of bird ecology applies to lekking (from the Swedish word for "play"), a courtship behavior that may include elaborate displays by males to attract mates in species such as hummingbirds (Trochilidae), cotingas (Cotingidae), and manakins (Pipridae). ...
Western Amazonia hosts the highest bird diversity in the world, yet in many regional indigenous territories, biodiversity remains poorly known to science. Between 2004 and 2020, we conducted research with members of 10 indigenous Aguaruna communities in four regions of the northern Peruvian Amazon, recording a total of 427 bird species, including eight wintering Nearctic migratory species. Past studies suggested that unique Aguaruna names exist for the majority of bird species present, and this hypothesis was a focus of our research. We identified unique Aguaruna names for ~38% (161) of bird species documented and generic (shared) Aguaruna names for an additional ~31% (132) of bird species documented; the remaining ~31% (134) of bird species documented had no known Aguaruna name. Avian family membership was a significant predictor of whether a bird species had a unique Aguaruna name. Avian families in which a majority of species had unique Aguaruna names included parrots (Psittacidae), manakins (Pipridae), and nightjars (Caprimulgidae), comprising many conspicuous species in terms of their appearance, vocalizations, and/or behavior. Avian families in which a majority of species had no Aguaruna name included ovenbirds and woodcreepers (Furnariidae), tyrant flycatchers (Tyrannidae), and hummingbirds (Trochilidae), comprising many small, cryptic, forest interior species. Collaborative research on avian ecology together with studies of indigenous names and knowledge offers a basis on which to increase conservation engagement with indigenous people.
... Indeed, obligate ant followers are parasites on army ant swarms "stealing" about 30% of the daily leaf litter food requirement from migrating ant colonies (Wrege et al., 2005). Thus, although army ants and low-elevation invertivorous neotropical birds might be engaged in exploitation competition (because of yetto-be investigated dietary overlaps), army ants are still indispensable facilitators for dozens of bird species in obtaining food on a daily basis (Martínez et al., 2021). ...
Using data on bird species elevational distributions from the world's mountain ranges, bird diets, and the distribution of the ant genus Oecophylla, we report that global patterns in bird elevational diversity show signals of competition with ants. Oecophylla is an abundant and effective predator of invertebrates, preying on the same species that invertivorous birds feed on. In mountain ranges with Oecophylla present in the foothills, the maximum species richness of invertivorous birds (but not other trophic guilds) occurs, on average, at 960 m, ca. 450 m higher than in mountain ranges without Oecophylla, resulting in a mid‐elevation peak in bird species richness. Where Oecophylla is absent, bird species richness for all guilds generally show monotonic declines with increasing elevation. We argue that Oecophylla reduces prey density for invertivorous birds and that low prey abundance reduces invertivorous bird density, which in turn is correlated with lower bird species richness. These findngs suggest that competition between distantly related taxa can set range limits, leading to emergent diversity patterns over large scales.
... We excluded birds of prey (hawks, eagles, falcons) because they are not at the same trophic level as most flocking species. We excluded obligate ant-following species as their flocks typically rely on spatially concentrated food sources (Mart ınez et al. 2021). Finally, we excluded species for which flocking propensity was based on fewer than 10 individual observations to minimize estimate bias for species that are not recorded frequently. ...
Mixed-species flocking is common in birds and is associated with increased foraging efficiency and reduced predation pressure. The propensity to join mixed-species flocks within a community varies across species, possibly reflecting species-specific needs for increased protection from predators, opportunities to increase foraging efficiency, or both. Earlier studies on predictors of mixed-species flocking propensity across species typically focused on local communities, with or without accounting for phylogenetic relatedness. Here, we examined predictors of mixed-species flocking propensity across the published literature using a phylogenetic linear mixed model framework. We obtained 724 mixed-species flocking propensity estimates from 31 different study sites located primarily in South America and East Asia. Flocking propensity was associated with diet, foraging strata, and foraging behaviour and was inversely related to body mass. Controlling for phylogeny and body mass, flocking propensity was significantly lower for nectarivores than for species with other diets, lower for species foraging on the ground than in higher strata, and lower for sallying species than for bark and near-perch foragers. These results suggest that variation across species in the tendency to join mixed-species flocks can be predicted from knowledge about various species-specific ecological traits in birds.
... Ant-following birds are highly diverse in the Neotropics, encompassing several orders and about 41 families (Willis and Oniki 1978;Martínez et al. 2021) across a wide range of elevation (i.e., from sea level to ~3000 m asl). More than 30 species of ant-following birds can swarm around a large ant colony (Willis and Oniki 1978;O'Donnell 2017). ...
... Facultative ant-following birds feed opportunistically when army ants move through their territory; this category of specialization of ant-following behavior also includes ant-followers that regularly chase army ants beyond their territory, but also feed independently of the ants (Willis and Oniki 1978;O'Donnell 2017). The study of the biogeography of bird species that vary in the specialization of ant-following behavior was recently highlighted as a research opportunity to advance our understanding of ant-followers (Martínez et al. 2021), and the authors suggest that ant-following behavior is geographically constrained by the presence of swarming army-ant species. ...
... To test our hypothesis that the intensity of the interaction is reflected in the overlap of geographic ranges between army ants and ant-following birds, we analyzed the geographic ranges of two species of army ants and ten species of ant-following birds. We selected the two species of army ants that represent most of the army ant swarms in the region, Eciton burchellii and Labidus praedator (Coates-Estrada and Estrada 1989; Martínez et al. 2021). We also selected five obligate and five facultative ant-following bird species (Table 1) ...
Biogeography has as a central theme, which is the study of geographic ranges of species that are determined by evolutionary history, abiotic factors, and biotic interactions. Understanding the influence of biotic interactions on geographic ranges is a topic that has been little explored, especially in a way that compares species that vary in intensity of interaction. Here, we assessed interaction intensity as a determinant of geographic range overlap between ant-following birds and army ants in Mexico and Central America. We hypothesized that the intensity of the interaction between army ants and ant-following birds, obligate or facultative, predicts the overlap of geographic ranges of interacting species, as well as the extension of geographic ranges. We generated species distribution models with MAXENT and estimated the percentage of overlap between two species of army ants and 10 species of ant-following birds. Contrary to our predictions, Bayesian regression models found no support for an estimated higher range overlap for obligate ant-following birds and army ants, or wider geographic ranges for facultative ant-following bird species. However, our results suggested trends for higher percentages of range overlap between obligate ant-following birds and army ants, and for geographic ranges of facultative ant-following birds extending to areas without the presence of army ants. Our research encourages further exploration of the biogeography of biotic interactions as part of a quantitative gradient of intensities and not as qualitative categories, integrating spatial and temporal variation in the intensity of interaction.
... Species interactions are the foundation of ecosystems, linking individual behaviour to community structure and ecosystem functioning. These interactions range in degree of specialization from opportunistic to obligate (Blüthgen et al., 2006;Devictor et al., 2010) and in category, from predator-prey and host-parasite interactions (Pollock et al., 2021;Schmitz, 2017), to commensal and mutualistic relationships, such as pollination and seed dispersal (Leigh Jr, 2010;Li et al., 2016). Species interactions connect individual organisms and populations across trophic levels, and strengthen and stabilize communities and ecosystems (Ives et al., 2000;Ives & Carpenter, 2007). ...
... Schemske et al., 2009). Disturbance foraging interactions may revolve around highly specialized species that provide frequent or high-intensity disturbances like swarm-raiding ants (Craig, 2022;Martínez et al., 2021). The behaviour may occur across diverse taxa, or alternatively be phylogenetically conserved within specific clades. ...
... swarm-raiding ants of the Afrotropical genus Dorylus in Africa and the Neotropical species Eciton burchellii and Labidus praedator were associated with nearly 500 different attendant bird species in our study. Our findings are consistent with previous reviews of ant-following behaviour in both Afrotropical(Craig, 2022) andNeotropical(Martínez et al., 2021) birds and reinforce the ecological importance of ants(Schultheiss et al., 2022), and swarm-raiding ants in particular, as highly important species in tropical terrestrial systems (Pérez-Espona, 2021). Our results are especially concerning due to the high sensitivity of swarm-raiding ants to global change such as forest fragmentation(Kumar & O'Donnell, 2007;Peters et al., 2008) and climate change(Baudier et al., 2015). ...
Species interactions link animal behaviour to community structure and macroecological patterns of biodiversity. One common type of trophic species interaction is disturbance foraging—the act of obtaining food at a disturbance created by another organism. Disturbance foraging is widespread across the animal kingdom, especially among birds, yet previous research has been largely anecdotal and we still lack a synthetic understanding of how this behaviour varies geographically, phylogenetically and ecologically. To address these gaps, we conducted a comprehensive literature review to test focal hypotheses about disturbance foraging behaviour in birds. We found that avian disturbance foraging was geographically ubiquitous, occurring in both aquatic and terrestrial habitats across six continents and four oceans. Consistent with predictions based on established species diversity gradients in different habitat types, the majority of terrestrial observations occurred at tropical latitudes, whereas aquatic observations took place most frequently in temperate marine waters. Although disturbance foraging was widespread across the avian phylogeny, contrary to our prediction, the behaviour was also conserved phylogenetically (Pagel's λ = 0.7) and clustered within suboscine landbirds in terrestrial environments and seabirds in aquatic environments. Similarly, although disturbers were taxonomically diverse as we predicted, interactions were unexpectedly dominated by swarm‐raiding ants in terrestrial environments and cetaceans in aquatic environments. Diet and body mass were also important predictors of disturbance foraging associations: Responders followed disturbers with similar diets and larger body sizes. Overall, our hypothesis‐testing framework provides insight into the importance of geography, phylogeny and ecology as predictors of disturbance foraging behaviour. We anticipate that this comprehensive assessment of disturbance foraging will serve to generate additional hypotheses and spark future research and management considerations about this fascinating but poorly studied suite of species interactions, especially as biotic interactions face unprecedented risks in our rapidly changing world.
... Indeed, obligate ant followers are parasites on army ant swarms, "stealing" about 30% of the daily leaf litter food requirement from migrating ant colonies (46). Thus, while army ants and lowelevation invertivorous neotropical birds might be engaged in exploitation competition (because of yet-to-be investigated dietary overlaps), army ants are still indispensable facilitators for dozens of bird species in obtaining food on a daily basis (47). ...
Across the world's mountains, elevation-species richness relationships are highly variable. Here, using data on bird species elevational distributions from all 46 of the world's major mountain ranges, bird species dietary traits, and the distribution of the low-elevation ant genus Oecophylla, we show that global patterns in bird elevational diversity are likely to be affected by competition with ants. Oecophylla is an exceptionally abundant and aggressive predator of invertebrates, which preys on the same species that sympatric invertivorous bird species feed on. In mountain ranges with Oecophylla present in the foothills, maximum species richness of invertivorous birds occurs, on average, at 960m, ~450m higher than in mountain ranges without Oecophylla. Further, in mountain ranges with Oecophylla, species richness of invertivorous birds increases initially with with elevation to produce a mid-elevation peak in invertivore bird species richness. Where Oecophylla is absent, invertivore bird species richness generally shows monotonic declines with increasing elevation. We attribute the pattern to the following mechanism: first, Oecophylla reduces prey density for invertivorous birds; second, low invertebrate prey abundance reduces invertivorous bird density and third, lower bird density is correlated with lower bird species richness. Because invertivores dominate montane bird communities, global elevational bird diversity patterns are also driven by Oecophylla. The findings emphasize how competitive interactions between distantly related taxa set geographical range limits.
... Schomburgk (1848, p. 287) in Guiana and Bates (1863, p.473) in Brazil both noted the regular association of Neotropical antbirds (Family Formicariidae) and other bird species with swarms of army ants (Family Formicidae, Sub-family Dorylinae, genus Eciton, Borowiec 2016) and this bird-ant interaction has been studied extensively (see reviews by Willis and Oniki 1978;Willson 2004;Martínez et al. 2021). In Africa, there were also early reports of birds which foraged at columns of driver ants (Sub-family Dorylinae, genus Dorylus, Borowiec 2016) from Du Chaillu (1862) in Gabon, and by Reichenow (1875) and Sjöstedt (1895) in Cameroon. ...
... From these tables it is clear that specialist ant-followers in Africa are restricted to quite a small number of bird families and genera. By comparison, in the much richer Neotropical avifauna, more than 460 bird species have been recorded as ant-followers, with some categorised as "obligate" ant-followers, that are primarily dependent on ant swarms for foraging throughout the year and seek out army ants on a daily basis (Willson 2004;Martínez et al. 2021). While it is likely that some additional African species will prove to be "regulars" on closer examination, African birds may be less dependent on ants than the obligate Neotropical species, since all of the driver ants spend significant periods underground, and often show nocturnal activity. ...
Ant-following birds have been studied extensively in the Neotropics, but much less information is currently available for the Afrotropics. There are published records of 168 African bird species from 37 families foraging in association with driver ants (Dorylus, sub-family Dorylinae). However, of 52 bird species assessed as regular ant-followers, 38 belong to three families, which are disproportionately represented compared to other large Afrotropical bird families: Muscicapidae (18 spp.), Pycnonotidae (13 spp.) and Turdidae (7 spp.). The extent to which these birds are dependent on ants through their annual cycle is not known. African driver ants forage primarily under shaded, humid conditions by day, and may spend a month or longer underground. Conservation assessments of African forest habitats suggest that both driver ants and ant-following birds may be especially sensitive to the loss of forest cover.
... For the understory and midstory mixed-flockers, the largest 3 species differed significantly by mass, whereas the smallest 3 overlapped broadly in mass, but were uniquely separated by bill length. The 5 ant-following species had nearly discrete distributions along the mass niche axis, which likely corresponds to their interspecific dominance hierarchies at the front of raiding army ant swarms (Pierpont 1986, Willis and Oniki 1978, Martínez et al. 2021. MacArthur (1958) was able to mostly separate 5 warbler species into unique foraging locations on coniferous trees; however, those species still overlapped considerably in their use of the top and outermost portions of the trees. ...
... Antfollowing woodcreepers are large-bodied with heavier, more powerful bills than woodcreepers that join mixedspecies flocks. For ant-following birds in general, larger size allows a species to dominate smaller birds at ant swarms (Pierpont 1986, Martínez et al. 2021, and we found that ant-following woodcreepers separated neatly by mass (Figure 4), mirroring dominance hierarchies (Martin and Ghalambor 2014). On the other hand, we found substantial overlap in body size for woodcreepers that follow mixed-species flocks (Figure 4). ...
... Although our myrmecophily estimates for the four facultative woodcreepers overlapped ( Figure 5B), this measure does not reflect realized cooccurrences at swarms. When birds do co-occur at swarms, they adhere to mass-based dominance hierarchies (Willis and Oniki 1978, Pierpont 1986, Martínez et al. 2021. Space at swarms is divided into distinct foraging zones, with the lowest area closest to the swarm front (average width about 9-10 m; Willson 2004) considered to be the most profitable region for prey (Willis and Oniki 1978). ...
Woodcreepers (Dendrocolaptinae) represent a remarkably uniform group of brownish birds that move by hitching up tree trunks as they forage for arthropod prey. Despite these superficial similarities, we were able to uniquely differentiate the niches of all 13 species north of Manaus by integrating morphological traits (e.g., mass and bill size) with behavioral traits (e.g., sociality, stratum use, and foraging maneuvers). The 5 ant-following (myrmecophilous) species, with their larger bodies and heavier bills, were morphologically distinct from the 7 species that join mixed-species flocks. A combination of vertical stratum, mass, and bill length further distinguished among mixed-flocking species. Two canopy species—the solitary Dendrexetastes rufigula and the mixed-flocking Lepidocolaptes albolineatus—consistently foraged at higher strata than other species. For the remaining mixed-flocking species, the largest 3 species differed significantly by mass, whereas the smallest 3 species, which overlapped broadly in mass, were uniquely distinguished by bill length. The 5 ant-following species differed in their degree of specialization on ant swarms, from facultative (Hylexetastes perrotii) to obligate (Dendrocincla merula). The ant-followers also showed nearly discrete mass distributions that essentially differed by Hutchinsonian 1:1.3 ratios, which likely allows them to maintain interspecific dominance hierarchies at the front of raiding army ant swarms. The behaviors we quantified (sociality, vertical strata, and myrmecophily), together with morphology (mass and bill size), separated all 13 species. We speculate that niche partitioning and competitive exclusion allow each woodcreeper to uniquely access invertebrate prey, permitting coexistence and contributing to high alpha diversity at our study site.
... However, the ecological relevance of army ants goes beyond their impact as predators. Their large colonies sustain a diverse fauna of associated species, many of which depend on the presence of their army ant hosts (Gotwald Jr, 1995;Kronauer, 2020;Martínez et al., 2021;Rettenmeyer, 1961). Besides attracting conspicuous swarm followers such as specialized birds that feed on arthropods escaping from the ants (Gotwald Jr, 1995;Martínez et al., 2021), army ants also host a microcosm of invertebrates that take advantage of the abundant colony resources (Gotwald Jr, 1995;Kronauer, 2020;Rettenmeyer, 1961). ...
... Their large colonies sustain a diverse fauna of associated species, many of which depend on the presence of their army ant hosts (Gotwald Jr, 1995;Kronauer, 2020;Martínez et al., 2021;Rettenmeyer, 1961). Besides attracting conspicuous swarm followers such as specialized birds that feed on arthropods escaping from the ants (Gotwald Jr, 1995;Martínez et al., 2021), army ants also host a microcosm of invertebrates that take advantage of the abundant colony resources (Gotwald Jr, 1995;Kronauer, 2020;Rettenmeyer, 1961). These guests, or myrmecophiles, can be purely phoretic using the ants solely as dispersal agents, or they feed on the ants' refuse or prey as commensals. ...
Tropical rainforests are among the most diverse biomes on Earth. While species inventories are far from complete for any tropical rainforest, even less is known about the intricate species interactions that form the basis of these ecological communities. One fascinating but poorly studied example are the symbiotic associations between army ants and their rich assemblages of parasitic arthropod guests. Hundreds of these guests, or myrmecophiles, have been taxonomically described. However, because previous work has mainly been based on haphazard collections from disjunct populations, it remains challenging to define species boundaries. We therefore know little about the species richness, abundance and host specificity of most guests in any given population, which is crucial to understand co-evolutionary and ecological dynamics. Here, we report a quantitative community survey of myrmecophiles parasitizing the six sympatric Eciton army ant species in a Costa Rican rainforest. Combining DNA barcoding with morphological identification of over 2,000 specimens, we discovered 62 species, including 49 beetles, 11 flies, one millipede and one silverfish. At least 14 of these species were new to science. Ecological network analysis revealed a clear signal of host partitioning, and each Eciton species was host to both specialists and generalists. These varying degrees in host specificities translated into a moderate level of network specificity, highlighting the system's level of biotic pluralism in terms of biodiversity and interaction diversity. By providing vouchered DNA barcodes for army ant guest species, this study provides a baseline for future work on co-evolutionary and ecological dynamics in these species-rich host–symbiont networks across the Neotropical realm.
... Insectivorous tropical birds help dissect the present and potential future causes of species extirpations and extinctions, and the stakes of this impoverishment. These birds' extraordinary sensitivity to human impacts is particularly well-documented in the Neotropics (e.g., Robinson, 1999;Sekercioglu et al., 2002Sekercioglu et al., , 2004Sekercioglu et al., , 2019Sodhi et al., 2004;Stratford and Robinson, 2005;Sigel et al., 2006Sigel et al., , 2010Stouffer et al., 2006;Kumar and O'Donnell, 2007;Laurance et al., 2011;Newbold et al., 2013;Martínez et al., 2021), which comprise the focus of this review. Nonetheless, such sensitivity likely applies to the tropics more generally (e.g., Adeney et al., 2006;Peters et al., 2008;Peters and Okalo, 2009;Bregman et al., 2014), warranting inclusion of literature from the Paleotropics. ...
... Sensitivity of tropical insectivorous birds to forest loss and fragmentation is widespread in the Neotropics (Maldonado-Coelho and Marini, 2004;Barlow et al., 2006;Robinson and Sherry, 2012;Tobias et al., 2013;Sekercioglu et al., 2019) and Paleotropics (Lens et al., 2002;Bregman et al., 2014;Powell et al., 2015;Martínez et al., 2021). This literature repeatedly emphasizes the relatively great vulnerability of tropical insectivorous birds, and adds perspective to the BDFFP results. ...
... Antfollowing bird declines imply food declines as pivotal, because the ants make prey conspicuously available to the birds, but other factors include poor dispersal by these birds (patch isolation), large home-ranges, and edge effects on habitat quality . Additionally, both the army ants and ant-following birds are sensitive to changing rainfall and temperatures, making these birds vulnerable to climate change threats (Martínez et al., 2021). ...
Epigraph: “The house is burning. We do not need a thermometer. We need a fire hose.” (P. 102, Janzen and Hallwachs, 2019). Insectivorous birds are declining widely, and for diverse reasons. Tropical insectivorous birds, more than 60% of all tropical birds, are particularly sensitive to human disturbances including habitat loss and fragmentation, intensive agriculture and pesticide use, and climate change; and the mechanisms are incompletely understood. This review addresses multiple, complementary and sometimes synergistic explanations for tropical insectivore declines, by categorizing explanations into ultimate vs. proximate, and direct versus indirect. Ultimate explanations are diverse human Anthropocene activities and the evolutionary history of these birds. This evolutionary history, synthesized by the Biotic Challenge Hypothesis (BCH), explains tropical insectivorous birds' vulnerabilities to many proximate threats as a function of both these birds' evolutionary feeding specialization and poor dispersal capacity. These traits were favored evolutionarily by both the diversity of insectivorous clades competing intensely for prey and co-evolution with arthropods over long evolutionary time periods. More proximate, ecological threats include bottom-up forces like declining insect populations, top-down forces like meso-predator increases, plus the Anthropocene activities underlying these factors, especially habitat loss and fragmentation, agricultural intensification, and climate change. All these conditions peak in the lowland, mainland Neotropics, where insectivorous bird declines have been repeatedly documented, but also occur in other tropical locales and continents. This multiplicity of interacting evolutionary and ecological factors informs conservation implications and recommendations for tropical insectivorous birds: (1) Why they are so sensitive to global change phenomena is no longer enigmatic, (2) distinguishing ultimate versus proximate stressors matters, (3) evolutionary life-histories predispose these birds to be particularly sensitive to the Anthropocene, (4) tropical regions and continents vary with respect to these birds' ecological sensitivity, (5) biodiversity concepts need stronger incorporation of species' evolutionary histories, (6) protecting these birds will require more, larger reserves for multiple reasons, and (7) these birds have greater value than generally recognized.
