Great Tits Learn Odors and Colors Equally Well, and Show No Predisposition for Herbivore-Induced Plant Volatiles

Ability to efficiently localize productive foraging habitat is crucial for nesting success of insectivorous birds. Some bird species can use olfaction to identify caterpillar-infested trees by detection of herbivore induced plant volatiles (HIPVs), but these cues probably need to be learned. So far, we know very little about the process of olfactory learning in birds, whether insectivorous species have a predisposition for detecting and learning HIPVs, due to the high ecological significance of these odors, and how olfaction is integrated with vision in making foraging decisions. In a standardized setup, we tested whether 35 wild-caught great tits (Parus major) show any preference for widely abundant HIPVs compared to neutral (non-induced) plant odors, how fast they learn to associate olfactory, visual and multimodal foraging cues with food, and whether the olfactory preferences and learning speed were influenced by bird sex or habitat (urban or rural). We also tested how fast birds switch to a new cue of the same modality. Great tits showed no initial preference for HIPVs compared to neutral odors, and they learned all olfactory cues at a similar pace, except for methyl salicylate (MeSA), which they learned more slowly. We also found no differences in learning speeds between visual, olfactory and multimodal foraging cues, but birds learned the second cue they were offered faster than the first one. Bird sex or habitat had no effect on learning speed or olfactory preference, but urban birds tended to learn visual cues more slowly. We conclude that insectivorous birds utilize olfactory and visual cues with similar efficiency in foraging, and that they probably don‘t have any special predisposition toward the tested HIPVs. These results confirm that great tits are flexible foragers with good learning abilities.

Evaluating the impacts of metabarcoding primer selection on DNA characterization of diet in an aerial insectivore, the Purple Martin

DNA metabarcoding is a molecular technique frequently used to characterize diet composition of insectivorous birds. However, results are sensitive to methodological decisions made during sample processing, with primer selection being one of the most critical. The most frequently used DNA metabarcoding primer set for avian insectivores is ZBJ. However, recent studies have found that ZBJ produces significant biases in prey classification that likely influence our understanding of foraging ecology. A new primer set, ANML, has shown promise for characterizing insectivorous bat diets with fewer taxonomic biases than ZBJ, but ANML has not yet been used to study insectivorous birds. Here, we evaluate the ANML primer set for use in metabarcoding of avian insectivore diets through comparison with the more commonly used ZBJ primer set. Fecal samples were collected from both adult and nestling Purple Martins (Progne subis subis) at 2 sites in the USA and 1 site in Canada to maximize variation in diet composition and to determine if primer selection impacts our understanding of diet variation among sites. In total, we detected 71 arthropod prey species, 39 families, and 10 orders. Of these, 40 species were uniquely detected by ANML, whereas only 11 were uniquely detected by ZBJ. We were able to classify 54.8% of exact sequence variants from ANML libraries to species compared to 33.3% from ZBJ libraries. We found that ANML outperformed ZBJ for PCR efficacy, taxonomic coverage, and specificity of classification, but that using both primer sets together produced the most comprehensive characterizations of diet composition. Significant variation in both alpha- and beta-diversity between sites was found using each primer set separately and in combination. To our knowledge, this is the first published metabarcoding study using ANML primers to describe avian diet, and also the first to directly compare results returned by ANML and ZBJ primer sets.

Differences in insectivore bird diets in coffee agroecosystems driven by obligate or generalist guild, shade management, season, and year

Neotropical shade-grown coffee systems are renowned for their potential to conserve avian biodiversity. Yet, little is known about food resources consumed by insectivorous birds in these systems, the extent of resource competition between resident and migratory birds, or how management of shade trees might influence diet selection. We identified arthropods in stomach contents from obligate and generalist insectivorous birds captured in mist-nets at five coffee farms in Chiapas, Mexico between 2001–2003. Overall stomach contents from 938 individuals revealed dietary differences resulting from changes in seasons, years, and foraging guilds. Of four species sampled across all management systems, Yellow-green Vireo (Vireo flavoviridis) prey differed depending on coffee shade management, consuming more ants in shaded monoculture than polyculture systems. Diets of obligate and generalist resident insectivores were 72% dissimilar with obligate insectivores consuming more Coleoptera and Araneae, and generalist insectivores consuming more Formicidae and other Hymenoptera. This suggests that obligate insectivores target more specialized prey whereas generalist insectivores rely on less favorable, chemically-defended prey found in clumped distributions. Our dataset provides important natural history data for many Nearctic-Neotropical migrants such as Tennessee Warbler (Leiothlypis peregrina; N = 163), Nashville Warbler (Leiothlypis ruficapilla; N = 69), and Swainson’s Thrush (Catharus ustulatus; N = 68) and tropical residents including Red-legged Honeycreepers (Cyanerpes cyaneus; N = 70) and Rufous-capped Warblers (Basileuterus rufifrons; N = 56). With declining arthropod populations worldwide, understanding the ecological interactions between obligate and generalist avian insectivores gives researchers the tools to evaluate community stability and inform conservation efforts.

Attraction to Smelly Food in Birds: Insectivorous Birds Discriminate between the Pheromones of Their Prey and Those of Non-Prey Insects

Natural selection has favored the evolution of different capabilities that allow animals to obtain food—e.g., the development of senses for improving prey/food detection. Among these senses, chemical sense is possibly the most ancient mechanism used by organisms for environmental assessment. Comparative studies suggest the prime role of foraging ecology in the evolution of the olfactory apparatus of vertebrates, including birds. Here, we review empirical studies that have shown birds’ abilities to detect prey/food via olfaction and report the results of a study aiming to analyze the specificity of eavesdropping on prey pheromones in insectivorous birds. In a field study, we placed artificial larvae and a dispenser with one of three treatments—prey (Operopthera brumata) pheromones, non-prey (Rhynchophorus ferrugineus) pheromones, or a control unscented dispenser—on the branches of Pyrenean oak trees (Quercus pyrenaica). We then measured the predation rate of birds on artificial larvae. Our results show that more trees had larvae with signs of avian predation when they contained a prey pheromone dispenser than when they contained a non-prey pheromone dispenser or an unscented dispenser. Our results indicate that insectivorous birds can discriminate between the pheromones emitted by their prey and those emitted by non-prey insects and that they only exhibit attraction to prey pheromones. These results highlight the potential use of insectivorous birds in the biological control of insect pests.

High-throughput sequencing reveals dietary segregation in Malaysian babblers

The coexistence of numerous species within a community results from how those species use available resources. Babblers are one of the major groups of Malaysian insectivorous birds, which frequently forage in dense vegetation cover and have a high level of sympatry. Therefore, examining the diet, prey selection and niche segregation of babblers can be challenging. In this study, we used high-throughput sequencing to investigate potential dietary overlap or segregation among 10 babbler species of the four genera of the family Pellorneidae and Timaliidae: Pellorneum, Malacopteron, Stachyris and Cyanoderma in central peninsular Malaysia. We tested the hypothesis that trophically similar species may differ in resource use to avoid competitive exclusion. We identified 81 distinct arthropod taxa from fecal samples, belonging to 71 families representing 13 orders, which were predominantly from 16 dipteran, 13 lepidopteran and 10 coleopteran families. Of all the prey taxa consumed, 45% were found to be distinct across the 10 babbler species, and less than 35% were shared simultaneously by three or more babbler species, indicating minimal dietary overlap. The black-throated babbler Stachyris nigricollis and moustached babbler Malacopteron magnirostre had the most generalist tendencies because they consumed a greater variety of prey taxa. Small dietary overlap values (Ojk) and a relatively wide range of food resources suggest that dietary segregation occurred among the studied babblers. The great diversity of prey consumed revealed the presence of dietary flexibility among the sympatric insectivorous birds, thus reducing any active dietary competition and facilitating the coexistence through niche partitioning.

A larval aggregation pheromone as foraging cue for insectivorous birds

Although birds have traditionally been considered anosmic, increasing evidence indicates that olfaction plays an important role in the foraging behaviours of insectivorous birds. Recent studies have shown that birds can exploit herbivore-induced plant volatiles and sexual pheromones of adult insects to locate their prey. Many insectivorous birds prey on immature insects, providing relevant ecosystem services as pest regulators in natural and agricultural ecosystems. We asked whether birds could rely on chemical cues emitted by the immature stages of insects to prey on them. To address this question, we performed field experiments to evaluate if insectivorous birds can detect the aggregation pheromone produced by the larvae of the carpenter worm, Chilecomadia valdiviana . Groups of five artificial larvae were placed in branches of 72 adult trees in a remnant fragment of a sclerophyllous forest in central Chile. Each grouping of larvae contained a rubber septum loaded with either larval pheromone as treatment or solvent alone as control. We found that the number of larvae damaged by bird pecks was significantly higher in groups with dispensers containing the larval extract than in control groups. Our results show that birds can rely on immature insect-derived chemical cues used for larvae aggregation to prey on them.

Pest-removal services provided by birds on subsistence farms in south-eastern Nigeria

To what extent birds provide the ecosystem service of pest control in subsistence farms, and how this service might depend on retained natural habitats near farmlands is unexplored in West Africa. To fill this knowledge gap, we placed plasticine mimics of insect pests on experimentally grown crops on the Mambilla Plateau, South Eastern Nigeria. We recorded bird attacks on the mimics and the proportion of mimics removed by birds. We also determined the influence of distance of crops from forest fragments on both attack and removal rates. We placed 90 potted plants of groundnut (Arachis hypogea) and bambara nut (Vigna subterranea) along 15 transects running 4.5 km from forest edge into open grassland. Each plant had six of the 540 mimics in total placed on their leaves. We inspected the potted plants weekly for 12 weeks to record (i) the presence of bird beak marks on mimics, and (ii) the number of missing mimics. Once a week we collected all the mimics from the plants and counted the number of assumed beak marks. After counting we replaced the mimics on the plants, mark free. We found a strong positive correlation between the abundance of insectivorous birds and the mean number of missing mimics and/or bird attack marks on mimics. However, this positive effect of insectivorous bird abundance on prey mimic attack/removal became less strong the farther they were from a forest fragment. We found increased predation rates and abundance of insectivorous birds closer to forest fragments. Our data suggest that pest predation may be a key ecosystem service provided by insectivorous birds on Nigerian farmlands. Farmlands that are closer to forest fragments may experience a higher rate of pest control by insectivorous birds than those further away, suggesting that retaining forest fragments in the landscape may enhance pest control services in sub-Saharan subsistence farms.

Sensitivity of Tropical Insectivorous Birds to the Anthropocene: A Review of Multiple Mechanisms and Conservation Implications

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.