Structure and vertical stratification of plant galler–parasitoid food webs in two tropical forests

Abstract 1. Networks of feeding interactions among insect herbivores and natural enemies such as parasitoids, describe the structure of these assemblages and may be critically linked to their dynamics and stability. The present paper describes the first quantitative study of parasitoids associated with gall‐inducing insect assemblages in the tropics, and the first investigation of vertical stratification in quantitative food web structure. 2. Galls and associated parasitoids were sampled in the understorey and canopy of Parque Natural Metropolitano in the Pacific forest, and in the understorey of San Lorenzo Protected Area in the Caribbean forest of Panama. Quantitative host–parasitoid food webs were constructed for each assemblage, including 34 gall maker species, 28 host plants, and 57 parasitoid species. 3. Species richness was higher in the understorey for parasitoids, but higher in the canopy for gall makers. There was an almost complete turnover in gall maker and parasitoid assemblage composition between strata, and the few parasitoid species shared between strata were associated with the same host species. 4. Most parasitoid species were host specific, and the few polyphagous parasitoid species were restricted to the understorey. 5. These results suggest that, in contrast to better‐studied leaf miner–parasitoid assemblages, the influence of apparent competition mediated by shared parasitoids as a structuring factor is likely to be minimal in the understorey and practically absent in the canopy, increasing the potential for coexistence of parasitoid species. 6. High parasitoid beta diversity and high host specificity, particularly in the poorly studied canopy, indicate that tropical forests may be even more species rich in hymenopteran parasitoids than previously suspected.     

Between-forest variation in vertical stratification of drosophilid populations

Abstract 1. The spatial distribution pattern of forest‐dwelling drosophilid flies was compared among species and among four forests with markedly different vertical foliage structures, including secondary and primary forests, with special reference to vertical stratification. 2. All 20 drosophilid species analysed showed vertically stratified distribution patterns, which were detected statistically in at least one forest site during the 2‐year study period. As a whole, the vertical distribution patterns were stable, with or without stratification, over the 2 years. 3. The ratio of species with stratified distribution to the total number of species changed in a similar trend with the vertical foliage complexity of forests, both showing a large gap between secondary and primary forests, even for species common to all four forests. 4. Many species, most of which were tree‐sap feeders, showed highly predictable patterns of vertical stratification across forests and years. This was associated strongly with regular preference for microhabitat, mostly for the canopy, suggesting that the unvarying nature of canopy environments in any forest is very important in producing, maintaining, and promoting the vertical stratification in organism abundance, and contributes to the ubiquity of the pattern. 5. Some species with a wider range of food resources than other species, most of which showed no clear preference for the canopy, were characterised by large between‐forest differences in vertical distribution patterns and tended to show non‐stratified patterns in secondary forests, contributing to the lower ratio of species with stratified distribution in the two secondary forests than in the primary forests. 6. The role of forest structure in organising the environment is discussed; it is suggested that vertical complexity of foliage structure affects the prevalence of vertical stratification in animal communities indirectly through the vertical heterogeneity of environmental conditions.     

Food web structure changes with elevation but not rainforest stratum

Changes in species richness along elevational gradients are well documented. However, little is known about how trophic interactions between species and, in particular, the food webs that these interactions comprise, change with elevation. Here we present results for the first comparison of quantitative food webs in forest understorey and canopy along an elevational gradient. Replicate quantitative food webs were constructed for assemblages involving 23 species of cavity‐nesting Hymenoptera and 12 species of their parasitoids and kleptoparasites in subtropical rainforest in Australia. A total of 1589 insects were collected using trap nests across 20 plots distributed at sites ranging from 300 to 1100 m a.s.l. Insect abundance, insect diversity and parasitism rate generally decreased with increasing elevation. Food web structure significantly changed with elevation. In particular, weighted quantitative measures of linkage density, interaction evenness, nestedness (weighted NODF) and potential for enemy mediated interactions (PAC) decreased with increasing elevation, and network specialisation (H₂′) increased with increasing elevation, even after controlling for matrix size; but there was no change in weighted connectance. Changes in forest type and temperature along the elevational gradient are likely to be, at least partly, responsible for the patterns observed. We found no significant differences in insect abundance, insect diversity or parasitism rate between canopy and understorey. Furthermore, there were no differences in food web structure between strata. These results contribute further evidence to studies revealing changes in food web structure along natural environmental gradients and provide information that can potentially be used for predicting how communities may respond to climate change.     

Forest fragmentation leads to food web contraction

Fragmentation and loss of habitat are critical components of the global change currently threatening biodiversity and ecosystem functioning. We studied the effects of habitat loss through fragmentation on food web structure, by constructing and analyzing plant‐herbivore and host‐parasitoid food webs including more than 400 species and over 120 000 feeding records, in 19 Chaco Serrano remnants of differing areas. Food web structure was altered by habitat fragmentation, with different metrics being affected depending on interaction type, and with all changes being driven by the reduced size of networks in smaller fragments. Only connectance varied in both quantitative and qualitative analyses, being negatively related to area. In addition, the interactions were represented by proper successive subsets, modulated mainly by resource availability (plant–herbivore) or consumer specialization (host–parasitoid), as forest size decreased. The results suggest that habitat loss has led to food web contraction around a central core of highly‐connected species, for plant–herbivore as well as for host–parasitoid systems. The study provides new insights into the effects of human perturbations on complex biological systems.     

Vertical stratification of an avian community in New Guinean tropical rainforest

Vertical stratification of avian communities has been studied in both temperate and tropical forests; however, the majority of studies used ground-based methods. In this study we used ground-to-canopy mist nets to collect detailed data on vertical bird distribution in primary rain forest in Wanang Conservation Area in Papua New Guinea (Madang Province). In total 850 birds from 86 species were caught. Bird abundance was highest in the canopy followed by the understory and lowest in the midstory. Overall bird diversity increased towards the canopy zone. Insectivorous birds represented the most abundant and species-rich trophic guild and their abundances decreased from the ground to canopy. The highest diversity of frugivorous and omnivorous birds was confined to higher vertical strata. Insectivorous birds did not show any pattern of diversity along the vertical gradient. Further, insectivores preferred strata with thick vegetation, while abundance and diversity of frugivores increased with decreasing foliage density. Our ground-to-canopy (0–27 m) mist netting, when compared to standard ground mist netting (0–3 m), greatly improved bird diversity assessment and revealed interesting patterns of avian community stratification along vertical forest strata.     

Effects of habitat configuration on host–parasitoid food web structure

The dispersal of organisms among patches affects community structure in spatially heterogeneous habitats. The enhancement of dispersal frequency among patches can be expected to increase potential interaction between organisms in food webs. However, it has been difficult to fairly evaluate the effects of dispersal on the food web structure because the quantification of actual dispersal is difficult. In this study, in order to manipulate the dispersal frequency, two oak plantations (each with 100 oak trees) were established as high-patch connectivity (1-m interval) and low-patch connectivity (3-m interval) plots. Quantitative food webs of herbivores and their parasitoids were constructed for the high- and low-connectivity plots, and quantitative measures of food web metrics as indices of structure were calculated for both webs to examine dispersal effects on food web complexity. In the entire web, 86 herbivore species (Lepidoptera and Coleoptera) were attacked by 50 parasitoid species (Hymenoptera and Diptera). As a result, although we found no significant difference in herbivore abundance between high- and low-connectivity plots, a higher parasitism rate and greater complexity in web structure were observed in many food web metrics for the high-connectivity plot. Furthermore, the parasitoid overlap diagram showed a higher potential for indirect interactions among herbivore species in the high-connectivity plot. These results imply that the increase in dispersal frequency among habitat patches facilitates food web complexity, and the role of dispersal as a determinant of food web structure should be considered in food web ecology.     

Agricultural intensification and cereal aphid–parasitoid–hyperparasitoid food webs: network complexity, temporal variability and parasitism rates

Agricultural intensification (AI) is currently a major driver of biodiversity loss and related ecosystem functioning decline. However, spatio-temporal changes in community structure induced by AI, and their relation to ecosystem functioning, remain largely unexplored. Here, we analysed 16 quantitative cereal aphid–parasitoid and parasitoid–hyperparasitoid food webs, replicated four times during the season, under contrasting AI regimes (organic farming in complex landscapes vs. conventional farming in simple landscapes). High AI increased food web complexity but also temporal variability in aphid–parasitoid food webs and in the dominant parasitoid species identity. Enhanced complexity and variability appeared to be controlled bottom-up by changes in aphid dominance structure and evenness. Contrary to the common expectations of positive biodiversity–ecosystem functioning relationships, community complexity (food-web complexity, species richness and evenness) was negatively related to primary parasitism rates. However, this relationship was positive for secondary parasitoids. Despite differences in community structures among different trophic levels, ecosystem services (parasitism rates) and disservices (aphid abundances and hyperparasitism rates) were always higher in fields with low AI. Hence, community structure and ecosystem functioning appear to be differently influenced by AI, and change differently over time and among trophic levels. In conclusion, intensified agriculture can support diverse albeit highly variable parasitoid–host communities, but ecosystem functioning might not be easy to predict from observed changes in community structure and composition.     

Effects of global environmental changes on parasitoid–host food webs and biological control

Global environmental changes threaten biodiversity and the interactions between species, and food-web approaches are being used increasingly to measure their community-wide impacts. Here we review how parasitoid–host food webs affect biological control, and how their structure responds to environmental change. We find that land-use intensification tends to produce webs with low complexity and uneven interaction strengths. Dispersal, spatial arrangement of habitats, the species pool and community differences across habitats have all been found to determine how webs respond to landscape structure, though clear effects of landscape complexity on web structure remain elusive. The invasibility of web structures and response of food webs to invasion have been the subject of theoretical and empirical work respectively, and nutrient enrichment has been widely studied in the food-web literature, potentially driving dynamic instability and altering biomass ratios of different trophic levels. Combined with food-web changes observed under climate change, these responses of food webs could signal changes to biological control, though there have been surprisingly few studies linking food-web structure to pest control, and these have produced mixed results. However, there is strong potential for food-web approaches to add value to biological control research, as parasitoid–host webs have been used to predict indirect effects among hosts that share enemies, to study non-target effects of biological control agents and to quantify the use of alternative prey resources by enemies. Future work is needed to link food-web interactions with evolutionary responses to the environment and predator–prey interactions, while incorporating recent advances in predator biodiversity research. This holistic understanding of agroecosystem responses and functioning, made possible by food-web approaches, may hold the key to better management of biological control in changing environments.     

Establishment and dominance of an introduced herbivore has limited impact on native host-parasitoid food webs

The gypsy moth is considered one of the most harmful invasive forest insects in North America. It has been suggested that gypsy moth may indirectly impact native caterpillar communities via shared parasitoids. However, the impact of gypsy moth on forest insect food webs in general remains unstudied. Here we assess such potential impacts by surveying forest insect food webs in Ontario, Canada. We systematically collected caterpillars using burlap bands at sites with and without histories of gypsy moth outbreak, and then reared these caterpillars until potential parasitoid emergence. This procedure allowed us to generate quantitative food webs describing caterpillar-parasitoid interactions. We estimated the degree of parasitoid sharing between gypsy moth and native caterpillars. We also statistically modeled the effect of gypsy moth outbreak history and current gypsy moth abundance on standard indices of quantitative food web structure and the diversity of parasitoid communities. Rates of gypsy moth parasitism were very low and gypsy moth shared very few parasitoids with native caterpillars, suggesting limited potential for indirect interactions. We did not detect any significant effects of gypsy moth on either food web structure or parasitoid diversity, and the small amount of parasitoid sharing strongly implies that this lack of significance is not merely due to low statistical power. Our study suggests that gypsy moth has limited impact on native host-parasitoid food webs, at least for species that use burlap bands. Our results emphasize that extrapolations of theoretical and experimental conclusions on the impacts of invasive species should be tested in natural settings.     

Spider diversity responds strongly to edge effects but weakly to vegetation structure in riparian forests of Southern Brazil

Riparian forests bordering open terrestrial environments may have three microhabitats differing in structure and conditions: a grassland/pasture-forest edge (GE), a forest interior (FI) and a river–forest edge. The influence of such edge effects and vegetation characteristics on spider diversity of riparian forests was evaluated in Southern Brazil. Four different rivers were sampled on the tree–shrub strata with a beating tray, twice per season for 2 years. There were six transects per river, two per microhabitat. We compared spider abundance, species richness and composition. Vegetation variables sampled were vertical structure and (horizontal) density, canopy height and cover. Overall 42,057 spiders were sampled, 28 spider families and 440 species. The FI had higher spider abundance than the edges. Average species richness differed among rivers. Microhabitats did not differ in average richness, although overall richness (from sample-based rarefaction) was higher for GE than FI. High abundances in FI may result from lowered stress due to abiotic conditions, while higher GE richness may result from a faunal superposition between forest species and those from the grassland/pasture. Only canopy cover returns a positive relationship with spider diversity (richness and adult abundance). This might result from more spider species preferring to build webs or hunt under low-light environments. Rivers had spider faunas differing in composition but among microhabitats species composition was the same. Vegetation structure has been hypothesized to affect spiders, but this impact might be best seen in specific subgroups or guilds within spiders, not in the whole assemblage.     

Diurnal foraging ant–tree co-occurrence networks are similar between canopy and understorey in a Neotropical rain forest

Discussion of the vertical stratification of organisms in tropical forests has traditionally focused on species distribution. Most studies have shown that, due to differences in abiotic conditions and resource distribution, species can be distributed along the vertical gradient according to their ecophysiological needs. However, the network structure between distinct vertical strata remains little-explored. To fill this gap in knowledge, we used baits to sample ants in the canopy and understorey trees of a Mexican tropical rain forest to record the ant–tree co-occurrences. We examined the ant–tree co-occurrences in the canopy and understorey using complementary network metrics (i.e., specialization, interaction diversity, modularity, and nestedness). In addition, we evaluated co-occurrence patterns between ant species on trees, using C-score analysis. In general, we found no differences in the network structure, although the interaction diversity was greater in the understorey than in the canopy networks. We also observed that co-occurrence networks of each vertical stratum featured four ant species in the central core of highly co-occurring species, with three species unique to each stratum. Moreover, we found a similar trend toward ant species segregation in the both strata. These findings reveal a similar pattern of ant–ant co-occurrences in both vertical strata, probably due to the presence of arboreal-nesting ants in the understorey. Overall, we showed that despite the marked differences in species composition and environmental conditions between understorey and canopy strata, ant–tree co-occurrences in these habitats could be governed by similar mechanisms, related to dominance and resource monopolization by ants.     

Spatio-temporal variation in Lepidopteran larval assemblages associated with oak, Quercus crispula: the importance of leaf quality

Abstract.  1. Lepidoptera larval abundance and diversity in the canopies of oak ( Quercus crispula ) trees and saplings were surveyed in a cool-temperate, deciduous broadleaf forest in northern Japan.
2. In general, newly developed leaves were soft, rich in water and nitrogen, and low in tannin, whereas they became tough, poor in water and nitrogen, and high in tannin as the season proceeded. Leaf quality also varied among forest strata, such variations resulting in seasonal and among-strata differences in the structure of the Lepidoptera larval assemblage.
3. The greater Lepidoptera larval abundance and species richness may related to the higher leaf quality on spring foliage compared with summer foliage. On the other hand, diversity (Shannon's H' ) and evenness (Pielou's J' ) were greater on summer foliage than on spring foliage. Strengthened defences of the host plants against herbivory may cause these differences by filtering the larvae of Lepidoptera species and by constraining the super-dominance of a few species on summer foliage.
4. Canonical Correspondence Analysis (CCA) ordination also revealed a stratified structure of the Lepidoptera larval assemblage in the forest. In both spring and summer, the assemblage composition was more similar between sunlit and shaded canopies than between canopies and saplings. Such assemblage stratification was highly correlated with toughness and tannin content (in spring and summer) or water content (in summer).
5. This study emphasised the importance of spatio-temporal variations in leaf quality, even within the same host plant species, for promoting herbivore diversity in forests.     

Past Human Disturbance Effects upon Biodiversity are Greatest in the Canopy; A Case Study on Rainforest Butterflies

A key part of tropical forest spatial complexity is the vertical stratification of biodiversity, with widely differing communities found in higher rainforest strata compared to terrestrial levels. Despite this, our understanding of how human disturbance may differentially affect biodiversity across vertical strata of tropical forests has been slow to develop. For the first time, how the patterns of current biodiversity vary between three vertical strata within a single forest, subject to three different types of historic anthropogenic disturbance, was directly assessed. In total, 229 species of butterfly were detected, with a total of 5219 individual records. Butterfly species richness, species diversity, abundance and community evenness differed markedly between vertical strata. We show for the first time, for any group of rainforest biodiversity, that different vertical strata within the same rainforest, responded differently in areas with different historic human disturbance. Differences were most notable within the canopy. Regenerating forest following complete clearance had 47% lower canopy species richness than regenerating forest that was once selectively logged, while the reduction in the mid-storey was 33% and at ground level, 30%. These results also show for the first time that even long term regeneration (over the course of 30 years) may be insufficient to erase differences in biodiversity linked to different types of human disturbance. We argue, along with other studies, that ignoring the potential for more pronounced effects of disturbance on canopy fauna, could lead to the underestimation of the effects of habitat disturbance on biodiversity, and thus the overestimation of the conservation value of regenerating forests more generally.     

Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest

Quantitative food webs were constructed to explore the community structure of leaf-mining moths in the family Gracillariidae and their parasitoid wasps in a deciduous forest in Hokkaido, Japan. A whole food web was constructed from data collected from June to October 2001. In the web, 16 leafminer species on seven tree species were attacked by 58 species of hymenopteran parasitoid; 376 links between leafminers and parasitoids were observed. Leafminers were specialist herbivores, but most parasitoids were generalists. Five webs were constructed for the seasonal prevalence of leafminers over the one-year period to reveal the temporal dynamics in community structure. Among the seasonal webs, the first web in June was distinctive because two tree species, Japanese umbrella tree Magnolia obovata and Japanese magnolia M. kobus, supported the community. Second to fourth webs from July to September were dominated by the leafminer species on Japanese oak Quercus crispula, and the fifth web was marked by that on Carpinus cordata. The extent of potential apparent competition among leafminers was evaluated using quantitative parasitoid overlap diagrams. These diagrams suggested that abundant host species are likely to have large indirect effects on less abundant species. Moreover, the potential for apparent competition between leafminer species inhabiting different host tree species can occur, although leafminers sharing the same tree species are prone to interact via shared parasitoids. In this system, particular leafminer species, acting as potential sources of apparent competition, can affect other species as sinks, and control whole-community dynamics. Directed apparent competition may potentially occur around oak trees.     

Heat tolerance variation reveals vulnerability of tropical herbivore–parasitoid interactions to climate change

Assessing the heat tolerance (CTmax) of organisms is central to understand the impact of climate change on biodiversity. While both environment and evolutionary history affect CTmax, it remains unclear how these factors and their interplay influence ecological interactions, communities and ecosystems under climate change. We collected and reared caterpillars and parasitoids from canopy and ground layers in different seasons in a tropical rainforest. We tested the CTmax and Thermal Safety Margins (TSM) of these food webs with implications for how species interactions could shift under climate change. We identified strong influence of phylogeny in herbivore–parasitoid community heat tolerance. The TSM of all insects were narrower in the canopy and parasitoids had lower heat tolerance compared to their hosts. Our CTmax-based simulation showed higher herbivore–parasitoid food web instability under climate change than previously assumed, highlighting the vulnerability of parasitoids and related herbivore control in tropical rainforests, particularly in the forest canopy.     

Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest

The processes maintaining the enormous diversity of herbivore—parasitoid food webs depend on parasitism rate and parasitoid host specificity. The two parameters have to be evaluated in concert to make conclusions about the importance of parasitoids as natural enemies and guide biological control. We document parasitism rate and host specificity in a highly diverse caterpillar-parasitoid food web encompassing 266 species of lepidopteran hosts and 172 species of hymenopteran or dipteran parasitoids from a lowland tropical forest in Papua New Guinea. We found that semi-concealed hosts (leaf rollers and leaf tiers) represented 84 % of all caterpillars, suffered a higher parasitism rate than exposed caterpillars (12 vs. 5 %) and their parasitoids were also more host specific. Semi-concealed hosts may therefore be generally more amenable to biological control by parasitoids than exposed ones. Parasitoid host specificity was highest in Braconidae, lower in Diptera: Tachinidae, and, unexpectedly, the lowest in Ichneumonidae. This result challenges the long-standing view of low host specificity in caterpillar-attacking Tachinidae and suggests higher suitability of Braconidae and lower suitability of Ichneumonidae for biological control of caterpillars. Semi-concealed hosts and their parasitoids are the largest, yet understudied component of caterpillar—parasitoid food webs. However, they still remain much closer in parasitism patterns to exposed hosts than to what literature reports on fully concealed leaf miners. Specifically, semi-concealed hosts keep an equally low share of idiobionts (2 %) as exposed caterpillars.     

Insect Herbivores and Leaf Damage along Successional and Vertical Gradients in a Tropical Dry Forest

The availability and quality of resources for herbivores in tropical dry forests (TDFs) vary in time and space, affecting herbivore guilds differently across spatial scales (both horizontally and vertically), with consequences to the distribution of leaf damage in these forests. We attempted to elucidate the distribution patterns of herbivorous insect guilds and leaf damage throughout the secondary succession and vertical stratification along the rainy season in a Brazilian TDF. With the advance of the succession, a greater richness and abundance of herbivorous insects were found, resulting in higher leaf damage in intermediate and late stages. This pattern, however, was not observed for the frequency of leaf miners. At a smaller spatial scale, the host tree height positively affected the richness and abundance of insects. The higher leaf damage was found in canopy, which also harbored a greater richness and abundance of chewing herbivores compared to the understory at both the beginning and the end of the rainy season. Although for sap‐sucking insects, this was only true at the beginning of the season. We detected a decrease in insect richness and abundance at the end of the rainy season, probably due to a synchronization of insect activity with the availability of young, highly nutritious plant tissues. These results are consistent with other studies that found a general trend of increasing richness and abundance of herbivorous insects and leaf damage throughout the secondary succession (early to late stages) and between vertical strata (understory to canopy), suggesting that forest complexity positively affects herbivores.     

Foliage-canopy structure and height distribution of woody species in climax forests

The correlation between foliage-canopy structure and vertical woody species distribution was examined in seven climax forests ranging from alpine tree limit to tropical rain forest. Foliage density was measured by two-dimensional canopy tomography using photographs. Both foliage density and the vertical species density (the number of woody species having a maximum height within a vertical 1 m) were high in the upper canopy of warm-temperate and subtropical forests, but they were high at lower stratums in the tropical rain forest. Two variables correlated significantly despite the differences in foliage-canopy structures. In contrast to evergreen broad-leaved forests, a clear correlation could not be detected in northern cool-temperate and sub-alpine forests. A possible reason for species convergence in the foliage dense stratum is that species with maximum height in that stratum may be able to survive in the stratum due to symmetrical crown-to-crown interaction. If the maximum height of dwarf species is less than the foliage dense stratum, it may be difficult to survive in the community. The lack of correlation in northern forests may be due to poor canopy tree flora and a mixture of different life forms (non-sprouting trees and sprouting shrubs).     

Importance of the understory stratum to entomofaunal diversity in a temperate deciduous forest

The vertical stratification of lepidopteran and coleopteran communities in a cool-temperate deciduous forest in Japan was examined to evaluate the hypothesis of an expected uniform distribution of mobile flying insects between the canopy and understory of temperate forests. Lepidopteran and coleopteran insects were trapped using light traps at three sites in each of the canopy and understory for three consecutive nights each month from April to October 2001. For Lepidoptera, species richness, abundance, and family richness were significantly higher in the understory than in the canopy. For Coleoptera, only abundance was larger in the canopy relative to the understory; species and family richness did not differ between the strata. The beta diversity of the lepidopteran community was larger between the strata than among sites, but the coleopteran community showed an inverse pattern. These results imply the presence of vertical stratification within the lepidopteran community, but not within the coleopteran community, in the temperate forest. The understory contributes more than the canopy to lepidopteran diversity in the temperate forest, although this stratification may be relatively weak because, in contrast to the situation in tropical forests, the canopy and understory assemblages share many species.