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OPEN
received: 07 September 2016 accepted: 01 February 2017 Published: 09 March 2017
Diet of land birds along an elevational gradient in Papua New Guinea Katerina Sam1,2, Bonny Koane3, Samuel Jeppy3, Jana Sykorova2 & Vojtech Novotny1,2 Food preferences and exploitation are crucial to many aspects of avian ecology and are of increasing importance as we progress in our understanding of community ecology. We studied birds and their feeding specialization in the Central Range of Papua New Guinea, at eight study sites along a complete (200 to 3700 m a.s.l.) rainforest elevational gradient. The relative species richness and abundance increased with increasing elevation for insect and nectar eating birds, and decreased with elevation for fruit feeding birds. Using emetic tartar, we coerced 999 individuals from 99 bird species to regurgitate their stomach contents and studied these food samples. The proportion of arthropods in food samples increased with increasing elevation at the expense of plant material. Body size of arthropods eaten by birds decreased with increasing elevation. This reflected the parallel elevational trend in the body size of arthropods available in the forest understory. Body size of insectivorous birds was significantly positively correlated with the body size of arthropods they ate. Coleoptera were the most exploited arthropods, followed by Araneae, Hymenoptera, and Lepidoptera. Selectivity indexes showed that most of the arthropod taxa were taken opportunistically, reflecting the spatial patterns in arthropod abundances to which the birds were exposed. Our knowledge of species richness patterns along elevational gradients has increased considerably over recent decades, but our understanding of the underlying mechanisms shaping these patterns has not1. The relative importance (in terms of species richness and/or abundance) of individual feeding guilds, and trends in feeding preferences in avian communities along elevational gradients have rarely been studied2. However, feeding preferences and trophic niche partitioning might be important mechanisms shaping patterns of species richness along environmental gradients3,4. Although some aspects of feeding ecology of birds along gradients have been studied, including diet breadth5–7, diet overlap8, and diet spatial fluctuation9,10, rigorous community-wide comparison of dietary specialization of birds along elevational gradient and its importance for niche theory have appeared only recently3,4. In Peru, diverging patterns of species richness along environmental gradients were described for individual feeding guilds. Insectivores were dominant at low elevations, while frugivores at higher elevations in bird communities11. On the other hand, insectivores remained the dominant guild along entire elevational gradients in Costa Rica12, the Himalayas3 and Papua New Guinea13. The insectivores at the highest elevations represented 62–66% of their lowland species richness in Peru and Costa Rica, but only 35% in Papua New Guinea, and they were species richer at high than at low elevations in the Himalayas. It has been hypothesised that reduced syntopy among insectivores at high elevations is a response to simplified vegetation11,14, lower habitat complexity13 or an altered food resource base3,13. The availability and exploitation of food resources are crucial to many aspects of avian ecology, and it is increasingly important that we understand their impact on bird community ecology and organization. Yet, quantitative studies of food availability and food exploitation by birds remain rare (e.g. refs 3 and 15). The diet of tropical bird species is poorly known16–18, and rarely confronted with available food resources (but see ref. 3). Prey size is another important factor in prey choice19–24. Prey size is usually positively correlated with predator size in birds20,25–27, including insectivorous birds20,28,29. Thus the size distribution of prey may influence the distribution and survival of individual bird species and affect the structure of avian guilds9,30. Schoener31 1
Biology Centre CAS, Institute of Entomology, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic. 2University of South Bohemia, Faculty of Science, Branisovska 1760, 370 05 Ceske Budejovice, Czech Republic. 3The New Guinea Binatang Research Center, PO Box 604 Madang, Papua New Guinea. Correspondence and requests for materials should be addressed to K.S. (email: [email protected]) Scientific Reports | 7:44018 | DOI: 10.1038/srep44018
1
www.nature.com/scientificreports/ found that large-billed insectivorous birds, which are predators of relatively large prey, were absent at sites where large-bodied prey was rare. Janes20 found that body size of foliage-gleaning birds was correlated more closely with arthropod size than the elevation. The size-related feeding preferences were never studied directly on large scales, and the predator-prey relationship between birds and insect have rarely been investigated along elevational gradients. To redress these knowledge gaps, we quantified food availability and used emetic tartar to estimate the actual diet of birds along an elevational forest gradient in Papua New Guinea. We tested the following predictions: (1) species richness of insectivorous birds will decrease faster than species richness of other feeding guilds11 (2) relative importance of insectivorous birds within a community decreases with increasing elevation11, (3) specialization of insectivorous birds decreases with increasing elevation, (4) body size of insects and birds are correlated along the gradient, and decrease in parallel with increasing elevation20, and (5) diet of birds reflects trends in arthropod abundance along the elevational gradient.
Results
We coerced 999 birds from 99 species mist-netted at eight sites along the altitudinal gradient to regurgitate their stomach contents. Eighty-five birds (8.5%) regurgitated only liquid, and 170 birds (17%) failed to regurgitate. We thus obtained 744 food samples from 99 bird species, and identified 3,480 food items of which 2,730 items were arthropods (complete or their body parts) and the rest plants (seeds or plant fragments; Table S1). Overall, 78 bird species were represented by >3 food samples (35 species were represented by 4–5 samples, and 43 bird species by >5 samples; Table S1) and used in the subsequent analyses. The whole avian community of Mt. Wilhelm included 236 bird species from which 49 were identified as frugivores (Fr), 46 as frugivore-insectivores (Fr-In), 112 as insectivores (In), 17 as insectivore-nectarivores (In-Ne), 11 as nectarivores (Ne) and one as granivore according to the literature (Table S3, Fig. 1a). We were able to further investigate and describe the intake of 12% of these frugivores, 22% of frugivore-insectivores, 47% of insectivores and 62.5% of insectivore-nectarivores. These numbers show that sampling was not balanced across the feeding guilds, and that we were more likely to mist-net insect-eating than fruit-eating birds. The proportions of individual guilds remained the same along the whole elevational gradient. Observational data showed that while the relative importance (i.e. the proportion of all bird species recorded per elevational study site) of insectivorous, insectivore-nectarivorous and nectarivorous guilds increased with increasing elevation, the relative importance of frugivorous and frugivore-insectivorous guilds decreased with increasing elevation (Fig. 1b,c). This result corresponded to the relative importance of plant and animal food items in combined samples, where we observed significantly decreasing (F1,335 = 4.63, p = 0.032, β = −0.012, Fig. 2) importance of plant material (fruits, seed and non-reproductive plant material) and significantly increasing (F1,335 = 4.634, p = 0.032, β = 0.017, Fig. 2) importance of animal material (mostly arthropods). However, somewhat different elevation trends in the importance of plant and animal material were observed within individual feeding guilds (Fig. S2). Sampling of stomach contents was conducted during the wet and the dry season. This might have had an effect on the relative intake of arthropod versus plant matter, although the sites are tropical and there is very low seasonality breeding. We compared relative intake of food matter between the wet and dry seasons for bird species mist-netted in more than four individuals in each season at the same elevation (N = 21 species) to investigate potential confounding effects of seasonality. There was no effect of season on the proportion of plant and animal items in bird diet (Man-Whitney tests, Z = 0.31–1.77, P = 0.61–0.07). Diet varied considerably among conspecific individuals, and more samples would be necessary to describe food exploitation by individual species. About 10–30 samples would be sufficient to describe arthropod exploitation by some species, while we investigated an average of only 9 (range 4–35) samples. We based these estimates on visual investigation of observed and extrapolated food morphotype accumulation curves and corresponding Chao2 estimates for the more extensively sampled bird species (Fig. S3). The overall diversity of arthropod morphotypes in the food of well-sampled bird species (i.e. those with >10 samples including >6 food items) significantly decreased with increasing elevation (Mean H = 0.33 −0.02*Elevation, F(1,228) = 5.424, P = 0.02, Fig. 3). We obtained body length, extrapolated to body weight32, for 1,538 arthropods taken by 62 bird species from all sites (n = 185–123 arthropods/site). We also measured body size and calculated body weight of 8,204 arthropods occurring in forest understory of the study sites. The body size of arthropods present on foliage in the forest understory decreased with increasing elevation (Mean body weight (mg) = 5.7798–0.3509*Elevation (m), Fig. 4). The body size of arthropods present in the forest understory followed similar elevational trends to the body size of arthropods taken by birds (Mean body weight (mg) = 7.6047–0.7884*Elevation (m), Fig. 4). There was no significant difference in the body size of the arthropods that were eaten by birds and those present in forest understory (F7, 8717 = 0.12, P = 0.99; Fig. 4). The elevational trend was caused mainly by the body weight of Araneae, Coleoptera and Hymenoptera (without Formicidae) that decreased significantly with increasing elevation when we tested individual arthropod orders separately. Other orders (Neuroptera, Hemiptera and Diptera) did not show any trend or occurred only scarcely in the samples (n
OPEN
received: 07 September 2016 accepted: 01 February 2017 Published: 09 March 2017
Diet of land birds along an elevational gradient in Papua New Guinea Katerina Sam1,2, Bonny Koane3, Samuel Jeppy3, Jana Sykorova2 & Vojtech Novotny1,2 Food preferences and exploitation are crucial to many aspects of avian ecology and are of increasing importance as we progress in our understanding of community ecology. We studied birds and their feeding specialization in the Central Range of Papua New Guinea, at eight study sites along a complete (200 to 3700 m a.s.l.) rainforest elevational gradient. The relative species richness and abundance increased with increasing elevation for insect and nectar eating birds, and decreased with elevation for fruit feeding birds. Using emetic tartar, we coerced 999 individuals from 99 bird species to regurgitate their stomach contents and studied these food samples. The proportion of arthropods in food samples increased with increasing elevation at the expense of plant material. Body size of arthropods eaten by birds decreased with increasing elevation. This reflected the parallel elevational trend in the body size of arthropods available in the forest understory. Body size of insectivorous birds was significantly positively correlated with the body size of arthropods they ate. Coleoptera were the most exploited arthropods, followed by Araneae, Hymenoptera, and Lepidoptera. Selectivity indexes showed that most of the arthropod taxa were taken opportunistically, reflecting the spatial patterns in arthropod abundances to which the birds were exposed. Our knowledge of species richness patterns along elevational gradients has increased considerably over recent decades, but our understanding of the underlying mechanisms shaping these patterns has not1. The relative importance (in terms of species richness and/or abundance) of individual feeding guilds, and trends in feeding preferences in avian communities along elevational gradients have rarely been studied2. However, feeding preferences and trophic niche partitioning might be important mechanisms shaping patterns of species richness along environmental gradients3,4. Although some aspects of feeding ecology of birds along gradients have been studied, including diet breadth5–7, diet overlap8, and diet spatial fluctuation9,10, rigorous community-wide comparison of dietary specialization of birds along elevational gradient and its importance for niche theory have appeared only recently3,4. In Peru, diverging patterns of species richness along environmental gradients were described for individual feeding guilds. Insectivores were dominant at low elevations, while frugivores at higher elevations in bird communities11. On the other hand, insectivores remained the dominant guild along entire elevational gradients in Costa Rica12, the Himalayas3 and Papua New Guinea13. The insectivores at the highest elevations represented 62–66% of their lowland species richness in Peru and Costa Rica, but only 35% in Papua New Guinea, and they were species richer at high than at low elevations in the Himalayas. It has been hypothesised that reduced syntopy among insectivores at high elevations is a response to simplified vegetation11,14, lower habitat complexity13 or an altered food resource base3,13. The availability and exploitation of food resources are crucial to many aspects of avian ecology, and it is increasingly important that we understand their impact on bird community ecology and organization. Yet, quantitative studies of food availability and food exploitation by birds remain rare (e.g. refs 3 and 15). The diet of tropical bird species is poorly known16–18, and rarely confronted with available food resources (but see ref. 3). Prey size is another important factor in prey choice19–24. Prey size is usually positively correlated with predator size in birds20,25–27, including insectivorous birds20,28,29. Thus the size distribution of prey may influence the distribution and survival of individual bird species and affect the structure of avian guilds9,30. Schoener31 1
Biology Centre CAS, Institute of Entomology, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic. 2University of South Bohemia, Faculty of Science, Branisovska 1760, 370 05 Ceske Budejovice, Czech Republic. 3The New Guinea Binatang Research Center, PO Box 604 Madang, Papua New Guinea. Correspondence and requests for materials should be addressed to K.S. (email: [email protected]) Scientific Reports | 7:44018 | DOI: 10.1038/srep44018
1
www.nature.com/scientificreports/ found that large-billed insectivorous birds, which are predators of relatively large prey, were absent at sites where large-bodied prey was rare. Janes20 found that body size of foliage-gleaning birds was correlated more closely with arthropod size than the elevation. The size-related feeding preferences were never studied directly on large scales, and the predator-prey relationship between birds and insect have rarely been investigated along elevational gradients. To redress these knowledge gaps, we quantified food availability and used emetic tartar to estimate the actual diet of birds along an elevational forest gradient in Papua New Guinea. We tested the following predictions: (1) species richness of insectivorous birds will decrease faster than species richness of other feeding guilds11 (2) relative importance of insectivorous birds within a community decreases with increasing elevation11, (3) specialization of insectivorous birds decreases with increasing elevation, (4) body size of insects and birds are correlated along the gradient, and decrease in parallel with increasing elevation20, and (5) diet of birds reflects trends in arthropod abundance along the elevational gradient.
Results
We coerced 999 birds from 99 species mist-netted at eight sites along the altitudinal gradient to regurgitate their stomach contents. Eighty-five birds (8.5%) regurgitated only liquid, and 170 birds (17%) failed to regurgitate. We thus obtained 744 food samples from 99 bird species, and identified 3,480 food items of which 2,730 items were arthropods (complete or their body parts) and the rest plants (seeds or plant fragments; Table S1). Overall, 78 bird species were represented by >3 food samples (35 species were represented by 4–5 samples, and 43 bird species by >5 samples; Table S1) and used in the subsequent analyses. The whole avian community of Mt. Wilhelm included 236 bird species from which 49 were identified as frugivores (Fr), 46 as frugivore-insectivores (Fr-In), 112 as insectivores (In), 17 as insectivore-nectarivores (In-Ne), 11 as nectarivores (Ne) and one as granivore according to the literature (Table S3, Fig. 1a). We were able to further investigate and describe the intake of 12% of these frugivores, 22% of frugivore-insectivores, 47% of insectivores and 62.5% of insectivore-nectarivores. These numbers show that sampling was not balanced across the feeding guilds, and that we were more likely to mist-net insect-eating than fruit-eating birds. The proportions of individual guilds remained the same along the whole elevational gradient. Observational data showed that while the relative importance (i.e. the proportion of all bird species recorded per elevational study site) of insectivorous, insectivore-nectarivorous and nectarivorous guilds increased with increasing elevation, the relative importance of frugivorous and frugivore-insectivorous guilds decreased with increasing elevation (Fig. 1b,c). This result corresponded to the relative importance of plant and animal food items in combined samples, where we observed significantly decreasing (F1,335 = 4.63, p = 0.032, β = −0.012, Fig. 2) importance of plant material (fruits, seed and non-reproductive plant material) and significantly increasing (F1,335 = 4.634, p = 0.032, β = 0.017, Fig. 2) importance of animal material (mostly arthropods). However, somewhat different elevation trends in the importance of plant and animal material were observed within individual feeding guilds (Fig. S2). Sampling of stomach contents was conducted during the wet and the dry season. This might have had an effect on the relative intake of arthropod versus plant matter, although the sites are tropical and there is very low seasonality breeding. We compared relative intake of food matter between the wet and dry seasons for bird species mist-netted in more than four individuals in each season at the same elevation (N = 21 species) to investigate potential confounding effects of seasonality. There was no effect of season on the proportion of plant and animal items in bird diet (Man-Whitney tests, Z = 0.31–1.77, P = 0.61–0.07). Diet varied considerably among conspecific individuals, and more samples would be necessary to describe food exploitation by individual species. About 10–30 samples would be sufficient to describe arthropod exploitation by some species, while we investigated an average of only 9 (range 4–35) samples. We based these estimates on visual investigation of observed and extrapolated food morphotype accumulation curves and corresponding Chao2 estimates for the more extensively sampled bird species (Fig. S3). The overall diversity of arthropod morphotypes in the food of well-sampled bird species (i.e. those with >10 samples including >6 food items) significantly decreased with increasing elevation (Mean H = 0.33 −0.02*Elevation, F(1,228) = 5.424, P = 0.02, Fig. 3). We obtained body length, extrapolated to body weight32, for 1,538 arthropods taken by 62 bird species from all sites (n = 185–123 arthropods/site). We also measured body size and calculated body weight of 8,204 arthropods occurring in forest understory of the study sites. The body size of arthropods present on foliage in the forest understory decreased with increasing elevation (Mean body weight (mg) = 5.7798–0.3509*Elevation (m), Fig. 4). The body size of arthropods present in the forest understory followed similar elevational trends to the body size of arthropods taken by birds (Mean body weight (mg) = 7.6047–0.7884*Elevation (m), Fig. 4). There was no significant difference in the body size of the arthropods that were eaten by birds and those present in forest understory (F7, 8717 = 0.12, P = 0.99; Fig. 4). The elevational trend was caused mainly by the body weight of Araneae, Coleoptera and Hymenoptera (without Formicidae) that decreased significantly with increasing elevation when we tested individual arthropod orders separately. Other orders (Neuroptera, Hemiptera and Diptera) did not show any trend or occurred only scarcely in the samples (n
