Does mixed-species flocking influence how birds respond to a gradient of land-use intensity?

Conservation biology is increasingly concerned with preserving interactions among species such as mutualisms in landscapes facing anthropogenic change. We investigated how one kind of mutualism, mixed-species bird flocks, influences the way in which birds respond to different habitat types of varying land-use intensity. We use data from a well-replicated, large-scale study in Sri Lanka and the Western Ghats of India, in which flocks were observed inside forest reserves, in ‘buffer zones'' of degraded forest or timber plantations, and in areas of intensive agriculture. We find flocks affected the responses of birds in three ways: (i) species with high propensity to flock were more sensitive to land use; (ii) different flock types, dominated by different flock leaders, varied in their sensitivity to land use and because following species have distinct preferences for leaders, this can have a cascading effect on followers'' habitat selection; and (iii) those forest-interior species that remain outside of forests were found more inside flocks than would be expected by chance, as they may use flocks more in suboptimal habitat. We conclude that designing policies to protect flocks and their leading species may be an effective way to conserve multiple bird species in mixed forest and agricultural landscapes.     

Forest structure predicts species richness and functional diversity in Amazonian mixed-species bird flocks

Secondary forest has the potential to act as an important habitat for biodiversity and restoring ecological benefits. Functional diversity, which includes morphological and behavioral traits that mediate species interactions with the surrounding environment, relates to the resilience of ecosystems. To assess the relationship between habitat structural differences in primary and secondary forest and the resultant differences in functional diversity of avian species, we followed 11 mixed-species flocks at the Biological Dynamics of Forest Fragments Project, near Manaus, Brazil. We used remote sensing LiDAR to assess which three-dimensional forest structural features are most closely associated with variation in species richness and functional diversity in secondary and primary tropical forest flocks. The species richness of flocks in primary forest increased in areas with higher elevation and higher leaf area density in the understory and subcanopy but was not correlated with habitat structure in secondary forest. Functional diversity increased at lower elevations and with a denser subcanopy in both primary forest and secondary forest but only increased with greater understory leaf area density in primary forest. Together, these results indicate that a dense subcanopy and understory can be important for mixed-species flocks and that flock richness and functional diversity can be predicted by vegetation structure.     

Edge effect and structure of mixed-species bird flocks in an Afrotropical lowland forest

Avian mixed-species flocks are a dominant feature of tropical moist forests, yet their cost–benefit balance and habitat dependence in Africa are not fully documented. We recorded the composition of mixed-species bird flocks in a pristine Afrotropical lowland forest site in Salonga NP, DRC. Our data showed that at least four types of flock existed, one of which specialized on edge habitats. We used multivariate analyses to further characterize edge effect on the most documented mixed-species flock type and found a significant effect on flock composition. While neither species guild nor preferential foraging stratum played an important role in flock participation, the nucleus role was played by a different species at the edge and in the interior, and both species abundance and associations were habitat-dependant, suggesting “domino effects” on the structure of mixed-species flocks.     

Linking vegetation structure and bird organization: response of mixed-species bird flocks to forest succession in subtropical China

As forests undergo natural succession following artificial afforestation, their bird assemblages also change. However, interspecific avian social organization associated with forest succession has not been fully understood, particularly for mixed-species bird flocks. To disentangle how mixed-species flocks change as a function of local forest structure, we analyzed flock characteristics (particularly species richness, flocking frequency and propensity) and vegetation physiognomies along a presumed successional series (early, middle, and advanced) simultaneously in subtropical forests in southern China. As hypothesized, monthly point counts demonstrated that complexity of flocks increases with the progression of natural forest succession at a local scale. Advanced forests differed significantly from pioneering plantations with respect to vegetation structure, flock characteristics and constituents (especially for understory specialists). Importantly, forest succession affected flock patterns particularly in relation to the flocking propensity of regular species, and the frequency of nuclear species (Huet’s fulvetta Alcippe hueti), which in turn determined flocking occurrence at different successional stands. Canonical correspondence analysis indicated that understory flocking species (mainly Timaliidae babblers) were significantly associated with intact native canopy cover, complex DBH diversity, as well as high densities of dead trees and large trees, representing a maturity level of successional stands. Our study reveals that the effect of natural forest succession on mixed-species bird flocks is species-specific and guild-dependent. From a conservation perspective, despite a high proliferation of pine plantation in southern China, priority should be placed on protecting the advanced forest with a rich collection of understory flocking specialists.     

Interaction networks of avian mixed-species flocks along elevation in the tropical Andes

Ecological communities are comprised of species that interact with each other and those interactions ultimately generate community structure. Network theory provides a useful framework to study communities, by simultaneously considering species composition and the interactions among species. In this study, I use mixed-species flocks as model systems to gain insights on community and network structure. Specifically, I use co-occurrence network analyses to explore if avian mixed-species flocks change in richness and composition and/or in network structure and pair-wise associations, across elevations in the tropical Andes of Bolivia. Networks of flocking species changed both in composition and in the frequency and realization of pair-wise interactions across elevations, but changes in pair-wise associations explained most of network turnover along elevation. Pair-wise interactions changed rapidly, with shared species changing in position and importance within the network. Network dissimilarity was mostly explained by changes in the nature of associations rather than by differences in composition. Altogether, results show that montane mixed-species flocks are composed of loosely connected species and that most species have the potential of switching associations, often increasing in association strength at high elevations (up to 3150 m). Networks increased in connectivity and cohesion with elevation; flocks in lower elevations had more connections and these were less even. Above 3150 m a.s.l., there was rapid decay suggesting that flocks above this critical point are less connected and cohesive. This study exemplifies how combining community, network and pair-wise analyses can provide a more holistic view on the responses of species and assemblages to environmental gradients.     

Importance of intraspecifically gregarious species in a tropical bird community

In both single- and mixed-species social groups, certain participants are known to play important roles in providing benefits. Identifying these participants is critical for understanding group dynamics, but is often difficult with large roving social groups in the wild. Here, we develop a new approach to characterize roles in social groups and apply it to mixed-species bird flocks (flocks hereafter) in an Indian tropical evergreen forest. Two types of species, namely intraspecifically gregarious and sallying species, are thought to play important roles in flocks because studies have shown they attract other flock participants. However, it is unclear why these types are attractive and whether they are essential for flock formation. We address these questions by focusing on the composition of the subset of flocks containing only two species each. In two-species flocks, it is reasonable to assume that at least one species obtains some kind of benefit. Therefore, only those species combinations that result in benefit to at least one species should occur as two-species flocks. Using data from 540 flocks overall, of which 158 were two-species flocks, we find that intraspecifically gregarious species are disproportionately represented in two-species flocks and always lead flocks when present, and that flocks containing them are joined significantly more by other species. Our results suggest that intraspecifically gregarious species are likely to be the primary benefit providers in flocks and are important for tropical flock formation. Our study also provides a new approach to understanding importance in other mixed-species and single-species social groups.     

Species importance in a heterospecific foraging association network

There is a growing recognition of the need to integrate non‐trophic interactions into ecological networks for a better understanding of whole‐community organization. To achieve this, the first step is to build networks of individual non‐trophic interactions. In this study, we analyzed a network of interdependencies among bird species that participated in heterospecific foraging associations (flocks) in an evergreen forest site in the Western Ghats, India. We found the flock network to contain a small core of highly important species that other species are strongly dependent on, a pattern seen in many other biological networks. Further, we found that structural importance of species in the network was strongly correlated to functional importance of species at the individual flock level. Finally, comparisons with flock networks from other Asian forests showed that the same taxonomic groups were important in general, suggesting that species importance was an intrinsic trait and not dependent on local ecological conditions. Hence, given a list of species in an area, it may be possible to predict which ones are likely to be important. Our study provides a framework for the investigation of other heterospecific foraging associations and associations among species in other non‐trophic contexts.     

Avian distribution in treefall gaps and understorey of terra firme forest in the lowland Amazon

We compared the bird distributions in the understorey of treefall gaps and sites with intact canopy in Amazonian terra firme forest in Brazil. We compiled 2216 mist-net captures (116 species) in 32 gap and 32 forest sites over 22.3 months. Gap habitats differed from forest habitats in having higher capture rates, total captures, species richness and diversity. Seventeen species showed a significantly different distribution of captures between the two habitats (13 higher in gap and four higher in forest). Gap habitats had higher capture rates for nectarivores, frugivores and insectivores. Among insectivores, capture rates for solitary insectivores and army ant followers did not differ between the two habitats. In contrast, capture rates were higher in gaps for members of mixed-species insectivore flocks and mixed-species insectivore–frugivore flocks. Insectivores, especially members of mixed-species flocks, were the predominant species in gap habitats, where frugivores and nectarivores were relatively uncommon. Although few canopy species were captured in gap or forest habitats, visitors from forest mid-storey constituted 42% of the gap specialist species (0% forest) and 46% of rare gap species (38% forest). Insectivore, and total, captures increased over time, but did so more rapidly in gap than in forest habitats, possibly as a response to gap succession. However, an influx of birds displaced by nearby timber harvest also may have caused these increases. Avian gap-use in Amazonian terra firme forests differs from gap-use elsewhere, partly because of differences in forest characteristics such as stature and soil fertility, indicating that the avian response to gaps is context dependent.     

How habitat-modifying organisms structure the food web of two coastal ecosystems

The diversity and structure of ecosystems has been found to depend both on trophic interactions in food webs and on other species interactions such as habitat modification and mutualism that form non-trophic interaction networks. However, quantification of the dependencies between these two main interaction networks has remained elusive. In this study, we assessed how habitat-modifying organisms affect basic food web properties by conducting in-depth empirical investigations of two ecosystems: North American temperate fringing marshes and West African tropical seagrass meadows. Results reveal that habitat-modifying species, through non-trophic facilitation rather than their trophic role, enhance species richness across multiple trophic levels, increase the number of interactions per species (link density), but decrease the realized fraction of all possible links within the food web (connectance). Compared to the trophic role of the most highly connected species, we found this non-trophic effects to be more important for species richness and of more or similar importance for link density and connectance. Our findings demonstrate that food webs can be fundamentally shaped by interactions outside the trophic network, yet intrinsic to the species participating in it. Better integration of non-trophic interactions in food web analyses may therefore strongly contribute to their explanatory and predictive capacity.     

Mixed-species flocking of forest birds on Little Barrier Island

Abstract

Three aspects of mixed-species flocking of forest birds on Little Barrier Island were investigated. Whiteheads, fantails, parakeets, and grey warblers occurred more often in flocks than in “non-flocking” situations. Whiteheads were the main lead species, although parakeets formed groups within flocks and occasionally appeared to lead. Whitehead clumps defined the flock centre; only fantails were found commonly in the centre with whiteheads. Birds other than whiteheads generally orientated below or to the side of their nearest neighbours. We suggest that mixed-species flocking is a significant factor influencing the structure of forest bird communities in New Zealand during winter.     

The influence of flocking on the foraging behaviour of the chough (Pyrrhocorax pyrrhocorax) and the Alpine chough (P. graculus) coexisting in the Alps

We studied the flocking and foraging behaviour of the chough Pyrrhocorax pyrrhocorax and the Alpine chough P. gruculus coexisting in the south-western Italian Alps in order to evaluate the costs and benefits of foraging in single- and mixed-species flocks.
In the single-species context, flock size significantly affected the foraging behaviour of the Alpine chough; in larger flocks, the birds stayed for a shorter time in a patch and fed more quickly than in smaller flocks. Flock size did not significantly affect the foraging behaviour of the chough, probably because of the small number of individuals per flock.
The propensity for mixed-species flocking was rather low. The observed frequencies of single-species flocks of choughs and Alpine choughs were significantly higher than those expected on the basis of random flocking, whereas the observed frequencies of mixed-species flocks of the two species were lower than those expected. The stay times became significantly shorter for the chough in the presence of the Alpine chough. Moreover, feeding rates of the Alpine chough were significantly lower in the presence of the dominant chough.
The present study does not confirm the hypothetical foraging advantages of flocking. In single-species flocks, the benefits for the Alpine chough (higher feeding rates in larger flocks) were roughly compensated by the costs (shorter stay times in larger flocks), whereas the chough apparently neither gained benefits nor endured costs.
In mixed-species flocks, the Alpine chough sustained costs due to a reduction of feeding rates and the chough suffered costs due to a reduction of stay times. Hence, on average, single-species flocking gives no evident foraging advantages to either the chough or the Alpine chough, whereas mixed-species flocking provides some disadvantages for both species.     

Advantages of social foraging of Willow Tits Parus montanus

The mean number of Willow Tits Parus montanus in single-species flocks was significantly larger than in mixed-species flocks of Willow and Coal Tits P. ater. Both flock size and the tendency of Willow Tits to join mixed-species flocks were negatively correlated with ambient temperature, probably because each bird, when the metabolic rate of the birds increased, could allocate more time to foraging due to improved predator detection by many eyes. The vigilance time of Willow Tits decreased with flock size and was determined by the total number of individuals in a flock rather than by the number of Willow Tits in mixed-species flocks of Willow and Coal Tits.     

Associations among Antarctic seabirds in mixed-species feeding flocks

We studied ten mixed-species feeding flocks of seabirds and seals off South Georgia (55̀S, 35̀W) to assess the factors that influenced the species composition of the flocks. The ten flocks were distributed between two oceanographic regions; four flocks were observed off the northwestern end of South Georgia, and six off the island's southeastern end. The flocks differed dramatically in size and species composition. The northwestern flocks were ten to 20 times larger and contained more seals and penguins. We tested whether these differences were a consequence of location, because the two regions were populated by different assemblages of species, and determined that this was not the case. Differences in flock size and species composition reflected differences in the depth distribution of the birds' and seals' prey. The northwestern flocks were associated with deep swarms of Antarctic krill Euphausia superba with a significant quantity of krill also present at the surface. We also tested for differential flock participation by the species found in the surrounding waters and classified species by their proclivity to participate in the flocks. Our results indicate that Black-browed Albatross Diomedea melanophris have a strong tendency to join, and diving-petrels Pelecanoides spp. to avoid, mixed-species feeding flocks. We postulate that Black-browed Albatrosses serve as visual cues to the presence of food for one another and for other species, and that diving-petrels avoid mixed-species flocks in part because of the risk of predation.     

Mixed-species bird flocks in dipterocarp forest of north-central Burma (Myanmar)

We studied the bird community in deciduous, dipterocarp forest of north-central Burma (Myanmar) during December 1994, March 1996, and January 1997 and 1999. Most members of this community participated in mixed-species flocks. Seventy-three flocks were encountered during our study, containing 52 species. Of these, 25 species occurred in more than 10% of flocks, and were included in our analyses. There were 26 significant correlations among species pairs, 25 of which were positive. Cluster analysis indicated that there were three principal types of flocks: one consisting mostly of small passerines and picids, commonly including Common Wood-Shrike, Small Minivet and White-browed Fantail, among others; a second type consisting mainly of sylviids, e.g. Arctic, Dusky and Radde's Warblers; and a third type which generally centred around Greater and Lesser Necklaced Laughingthrushes. Bird-eating hawks were numerous at these sites, and we witnessed several attacks on flocks during the study. Thus we infer that enhanced protection from predation is an important benefit conferred by flock membership. In contrast, there was little overlap in foraging behaviour among species, suggesting that foraging facilitation is a relatively minor benefit enjoyed by flock members, although we did observe White-browed Fantails and Greater Racket-tailed Drongos kleptoparasitizing other species on occasion.     

Observations of mixed-species bird flocks at Kichwa Tembo Camp,Kenya

Mixed-species foraging flocks were studied at Kichwa Tembo Camp on the edge of the Masai Mara National Reserve in Kenya between July and September 2004. Observations were made on 29 mixed-species flocks, in which 24 species participated. African Paradise-Flycatcher Terpsiphone viridis, Black-backed Puffback Dryoscopus cubla, Grey-backed Camaroptera Camaroptera brachyura, Collared Sunbird Hedydipna collars and Cabanis's Greenbul Phyllastrephus cabanisi were the most common participants in mixed-species flocks, as well as among the most frequently encountered bird species overall. The Black-backed Puffback was identified as the nuclear species in flocks due to their abundance and frequency with which they were followed by other species. Mixed-species flocks represent another niche dimension in this diverse bird community, but few of these species could be described as flock specialists; most of the birds observed in mixed-species flocks in this study were opportunistic attendant species, including the African Pygmy-Kingfisher Ispidina picta, not previously described as joining mixed-species flocks.     

Aggression in shorebirds in relation to flock density and composition

The aggressive interactions of Turnstones and Purple Sandpipers feeding in wintering mixed-species wader flocks could be classified into those involving food and those involving space. All observed interspecific encounters were of short duration and were initiated and won by the larger species; the majority did not involve food and were resolved by low-intensity displays. Intraspecific interactions (a greater proportion of which involved food) were also resolved quickly and were usually won by the initiator. Space-related encounters between conspecifics were more likely to be resolved than food-related encounters just by threat displays. Aggression rates increased with flock densities. However, the increase in aggression with density was dependent on the species composition of the flock: both Turnstones and Purple Sandpipers were more likely to be involved in fights (both over food and over space) with conspecifics than with other species, indicating that the aggression costs of flocking were less in mixed-species flocks.     

Relationships between frequency of mixed-species flocks, weather and insect activity in a montane cloud forest in Ecuador

The frequency of mixed-species flocks of birds, weather and insect activity were studied in a high-altitude cloud forest in Ecuador. It is generally accepted that participation in mixed-species flocks improves foraging efficiency. If this is true, more flock activity may be expected when food is less available, which may happen during long-lasting periods of rain and otherwise adverse weather conditions. The total number and mean size of flying insects decreased as rainfall increased. The number of flocks observed increased with decreasing number and biomass of insects. Relatively more flocks were seen during rain than during dry weather. No flocks stopped foraging during rain. The flock activity pattern appeared to be the opposite of that found in humid lowlands, probably because of different weather regimes in the two zones. In the lowlands, heavy rain is typically of short duration. In high-altitude cloud forest, the rainfall is often less intense but persists for prolonged periods. Hence, from an energy point of view, cloud forest birds cannot afford to stop foraging during adverse weather conditions when insect availability is low. The results suggest that some mixed feeding parties have evolved in response to low tropical insect availability, necessitating long feeding excursions outside the territory.     

Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions

One of the most important issues in ecology is understanding the causal mechanisms that shape the structure of ecological communities through trophic interactions. The focus on direct, trophic interactions in much of the research to date means that the potential significance of non-trophic, indirect, and facilitative interactions has been largely ignored in traditional food webs. There is a growing appreciation of the community consequences of such non-trophic effects, and the need to start including them in food web research. This review highlights how non-trophic, indirect, and facilitative interactions play an important role in organizing the structure of plant-centered arthropod communities. I argue that herbivore-induced plant responses, insect ecosystem engineers, and mutualisms involving ant–honeydew-producing insects all generate interaction linkages among insect herbivores, thereby producing complex indirect interaction webs on terrestrial plants. These interactions are all very common and widespread on terrestrial plants, in fact they are almost ubiquitous, but these interactions have rarely been included in traditional food webs. Finally, I will emphasize that because the important community consequences of these non-trophic and indirect interactions have been largely unexplored, it is critical that indirect interaction webs should be the focus of future research.     

What can mixed‐species flock movement tell us about the value of Amazonian secondary forests? Insights from spatial behavior

The value of secondary forest for rain forest species remains an important question for conservation in the 21st century. Here, we describe the spatial behavior of understory mixed‐species flocks in a heterogeneous landscape in central Amazonia. Understory mixed‐species flocks represent a diverse, highly organized component of the rich Amazonian avifauna. We recorded movements within 26 flock home ranges in primary forest, secondary forest, interfaces between forest types, and forest fragments. We describe frequency and movement orientation in relation to forest edges, movement patterns and proportion of use between secondary and primary forest, the relation between home range sizes and vegetation height, and home range configuration. Flocks visited only a small portion of forest edges, and showed a tendency for moving parallel to edges next to less‐developed secondary forest. Movement patterns in secondary forests did not show significant differences compared to primary forests. Time spent in secondary forests increased in proportion to mean canopy height. Flocks were consistently present in secondary forests where vegetation height averaged over 15 m, but home ranges were nearly twice as large compared to primary forest. Home range limits tended to be aligned with disturbed vegetation, essentially rearranging a territorial configuration normally adjusted by topography. The spatial behavior of this important subset of the Amazonian avifauna shows that secondary forests are tolerated above a certain development threshold, but perceived as suboptimal habitat until canopy height closely matches primary forests.     

Interspecific primate associations in Amazonian flooded and unflooded forests

Stable associations between two or more primate species are a prominent feature of neotropical forest vertebrate communities and many studies have addressed their prevalence, and their costs and benefits. However, little is known about the influence of different habitat types on the frequency, seasonality, and composition of mixed-species groups in Amazonian forest primates. Here we examine the features of interspecific primate groups in a large mosaic of flooded (várzea and igapó) and unflooded (terra firme) forest in central Amazonia. In total, 12 primate species occurred in the study area, nine of which were observed in mixed-species associations. Primates were more than twice as likely to form associations in várzea forest than in terra firme forest. Squirrel monkeys were most frequently found in mixed-species groups in all forest types, most commonly in association with brown capuchins. Another frequent member of interspecific associations was the buffy saki, which often formed mixed-species groups with tamarins or brown capuchins. There was no seasonality in the frequency of associations in terra firme forest whereas associations in várzea forest were twice as frequent during the late-dry and early-wet seasons than in the late-wet and early-dry seasons. Interspecific primate associations were common in all forest types, but the degrees to which different species associate varied between these environments. We suggest that the temporal variation of várzea forest associations is connected with seasonal changes in habitat structure and resource abundance. However, more work is needed to pinpoint the underlying causes of mixed-species associations in all forest types and their strong seasonality in várzea forest.