Yves Basset

Low host specificity of herbivorous insects in a tropical forest

Two decades of research have not established whether tropical insect herbivores are dominated by specialists or generalists. This impedes our understanding of species coexistence in diverse rainforest communities. Host specificity and species richness of tropical insects are also key parameters in mapping global patterns of biodiversity. Here we analyse data for over 900 herbivorous species feeding on 51 plant species in New Guinea and show that most herbivorous species feed on several closely related plant species. Because species-rich genera are dominant in tropical floras, monophagous herbivores are probably rare in tropical forests. Furthermore, even between phylogenetically distant hosts, herbivore communities typically shared a third of their species. These results do not support the classical view that the coexistence of herbivorous species in the tropics is a consequence of finely divided plant resources; non-equilibrium models of tropical diversity should instead be considered. Low host specificity of tropical herbivores reduces global estimates of arthropod diversity from 31 million (ref. 1) to 4–6 million species. This finding agrees with estimates based on taxonomic collections, reconciling an order of magnitude discrepancy between extrapolations of global diversity based on ecological samples of tropical communities with those based on sampling regional faunas.

Why Are There So Many Species of Herbivorous Insects in Tropical Rainforests

Despite recent progress in understanding mechanisms of tree species coexistence in tropical forests, a simple explanation for the even more extensive diversity of insects feeding on these plants has been missing. We compared folivorous insects from temperate and tropical trees to test the hypothesis that herbivore species coexistence in more diverse communities could reflect narrow host specificity relative to less diverse communities. Temperate and tropical tree species of comparable phylogenetic distribution supported similar numbers of folivorous insect species, 29.0 ± 2.2 and 23.5 ± 1.8 per 100 square meters of foliage, respectively. Host specificity did not differ significantly between community samples, indicating that food resources are not more finely partitioned among folivorous insects in tropical than in temperate forests. These findings suggest that the latitudinal gradient in insect species richness could be a direct function of plant diversity, which increased sevenfold from our temperate to tropical study sites.

Arthropod diversity in a tropical forest

Assessing Creepy Crawlies Arthropods are the most diverse group of terrestrial animal species, yet estimates of the total number of arthropod species have varied widely, especially for tropical forests. Basset et al. (p. 1481, see the cover) now provide more reliable estimates of total arthropod species richness in a tropical rainforest in Panama. Intensive sampling of a half hectare of forest yielded just over 6000 arthropod species. Scaling up this result to the whole forest suggests that the total species diversity lies between 17,000 and 40,000 species. Total arthropod species richness in a tropical rainforest can be best predicted by plant diversity. Most eukaryotic organisms are arthropods. Yet, their diversity in rich terrestrial ecosystems is still unknown. Here we produce tangible estimates of the total species richness of arthropods in a tropical rainforest. Using a comprehensive range of structured protocols, we sampled the phylogenetic breadth of arthropod taxa from the soil to the forest canopy in the San Lorenzo forest, Panama. We collected 6144 arthropod species from 0.48 hectare and extrapolated total species richness to larger areas on the basis of competing models. The whole 6000-hectare forest reserve most likely sustains 25,000 arthropod species. Notably, just 1 hectare of rainforest yields >60% of the arthropod biodiversity held in the wider landscape. Models based on plant diversity fitted the accumulated species richness of both herbivore and nonherbivore taxa exceptionally well. This lends credence to global estimates of arthropod biodiversity developed from plant models.

Low beta diversity of herbivorous insects in tropical forests.

Recent advances in understanding insect communities in tropical forests have contributed little to our knowledge of large-scale patterns of insect diversity, because incomplete taxonomic knowledge of many tropical species hinders the mapping of their distribution records. This impedes an understanding of global biodiversity patterns and explains why tropical insects are under-represented in conservation biology. Our study of approximately 500 species from three herbivorous guilds feeding on foliage (caterpillars, Lepidoptera), wood (ambrosia beetles, Coleoptera) and fruit (fruitflies, Diptera) found a low rate of change in species composition (beta diversity) across 75,000 square kilometres of contiguous lowland rainforest in Papua New Guinea, as most species were widely distributed. For caterpillars feeding on large plant genera, most species fed on multiple host species, so that even locally restricted plant species did not support endemic herbivores. Large plant genera represented a continuously distributed resource easily colonized by moths and butterflies over hundreds of kilometres. Low beta diversity was also documented in groups with differing host specificity (fruitflies and ambrosia beetles), suggesting that dispersal limitation does not have a substantial role in shaping the distribution of insect species in New Guinea lowland rainforests. Similar patterns of low beta diversity can be expected in other tropical lowland rainforests, as they are typically situated in the extensive low basins of major tropical rivers similar to the Sepik–Ramu region of New Guinea studied here.

Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest

1. The extent to which plant-herbivore feeding interactions are specialized is key to understand the processes maintaining the diversity of both tropical forest plants and their insect herbivores. However, studies documenting the full complexity of tropical plant-herbivore food webs are lacking. 2. We describe a complex, species-rich plant-herbivore food web for lowland rain forest in Papua New Guinea, resolving 6818 feeding links between 224 plant species and 1490 herbivore species drawn from 11 distinct feeding guilds. By standardizing sampling intensity and the phylogenetic diversity of focal plants, we are able to make the first rigorous and unbiased comparisons of specificity patterns across feeding guilds. 3. Specificity was highly variable among guilds, spanning almost the full range of theoretically possible values from extreme trophic generalization to monophagy. 4. We identify guilds of herbivores that are most likely to influence the composition of tropical forest vegetation through density-dependent herbivory or apparent competition. 5. We calculate that 251 herbivore species (48 of them unique) are associated with each rain forest tree species in our study site so that the ∼200 tree species coexisting in the lowland rain forest community are involved in ∼50,000 trophic interactions with ∼9600 herbivore species of insects. This is the first estimate of total herbivore and interaction number in a rain forest plant-herbivore food web. 6. A comprehensive classification of insect herbivores into 24 guilds is proposed, providing a framework for comparative analyses across ecosystems and geographical regions.

phylogenetic dispersion of host use in a tropical insect herbivore community

Theory has long predicted that insect community structure should be related to host plant phylogeny. We examined the distribution of insect herbivore associations with respect to host plant phylogeny for caterpillars (Lepidoptera), beetles (Coleoptera), and grasshoppers and relatives (orthopteroids) in a New Guinea rain forest. We collected herbivores from three lineages of closely related woody plants and from more distantly related plant lineages in the same locality to examine the phylogenetic scale at which host specificity can be detected in a community sample. By grafting molecular phylogenies inferred from three different genes into a supertree, we developed a phylogenetic hypothesis for the host community. Feeding experiments were performed on more than 100 000 live insects collected from the 62 host species. We examined patterns of host use with respect to the host plant phylogeny. As predicted, we found a negative relationship between faunal similarity, defined as the proportion of all herbivores feeding on two hosts that are shared between the hosts, and the phylogenetic distance between hosts based on DNA sequence divergence. Host phylogenetic distance explained a significant fraction of the variance (25%) in herbivore community similarity, in spite of the many ecological factors that probably influence feeding patterns. Herbivore community similarity among congeneric hosts was high (50% on average) compared to overlap among host families (20-30% on average). We confirmed this pattern using the nearest taxon index (NTI) and net relatedness index (NRI) to quantify the extent of phylogenetic clustering in particular herbivore associations and to test whether patterns are significantly different from chance expectations. We found that 40% of caterpillar species showed significant phylogenetic clustering with respect to host plant associations, somewhat more so than for beetles or orthopteroids. We interpret this as evidence that a substantial fraction of tropical forest insect herbivores are clade specialists.

The global distribution of diet breadth in insect herbivores

Significance Dietary specialization determines an organism’s resource base as well as impacts on host or prey species. There are important basic and applied reasons to ask why some animals have narrow diets and others are more generalized, and if different regions of the Earth support more specialized interactions. We investigated site-specific host records for more than 7,500 species of insect herbivores. Although host specialists predominate, the proportion of specialists is affected by the diversity of hosts and shifts globally, supporting predictions of more exclusive tropical interactions. These results not only affect our understanding of the ecology of food webs, but also have implications for how they respond to environmental change, as well as for ecosystem management and restoration. Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.

Quantifying Uncertainty in Estimation of Tropical Arthropod Species Richness

There is a bewildering range of estimates for the number of arthropods on Earth. Several measures are based on extrapolation from species specialized to tropical rain forest, each using specific assumptions and justifications. These approaches have not provided any sound measure of uncertainty associated with richness estimates. We present two models that account for parameter uncertainty by replacing point estimates with probability distributions. The models predict medians of 3.7 million and 2.5 million tropical arthropod species globally, with 90% confidence intervals of [2.0, 7.4] million and [1.1, 5.4] million, respectively. Estimates of 30 million or greater are predicted to have <0.00001 probability. Sensitivity analyses identified uncertainty in the proportion of canopy arthropod species that are beetles as the most influential parameter, although uncertainties associated with three other parameters were also important. Using the median estimates suggests that in spite of 250 years of taxonomy and around 855,000 species of arthropods already described, approximately 70% await description.

Local Communities of Arboreal Herbivores in Papua New Guinea: Predictors of Insect Variables

As a contribution to enlarging and widening the array of studies available for examination of insect—plant relations, this study contrasts local and regional predictors of species richness and host specificity of leaf—chewing insects feeding on New Guinea trees. I tested the degree to which the variance in local insect variables (species richness, ratio of specialist to generalist chewers, abundance, and biomass) for leaf chewers associated with different species of tropical trees was accounted for by local and regional host—related variables, and by local abundance of potential enemies. Leaf—chewing insects feeding externally on ten species of forest trees were collected over a 1—yr field study in a submontane area in Papua New Guinea. The tree species were taxonomically distant, and the list included species of different successional status, different patterns of leaf production, and different heights. The affinity of chewing insects with particular tree species was ascertained by feeding trials in the laboratory. Local insect species richness varied greatly among tree species, by more than four—fold between the poorest (18 species) and the richest (94 species) tree species. The proportion of specialist insect species associated with particular tree species was significantly different among tree species and ranged from 16 to 72%. Trees supporting a rich fauna usually also supported a high proportion of specialists. The abundance and biomass of leaf—chewing insects per host species was difficult to predict. However, path analyses showed that most of the causal variance in insect species richness and in the ratio of specialist to generalist chewers was accounted for by five properties of the tree species: numbers of young leaves available throughout the year, ant (i.e., enemy) abundance, leaf palatability, leaf water content, and altitudinal range. Most of the variation in local species richness could be predicted from local processes (i.e., food resources and abundance of enemies), not from regional processes. This study and others suggest that in complex environments, such as tropical rain forests, local processes may be comparatively more important in maintaining the local species richness of insect herbivores than in less complex ones, such as temperate woodlands. The implications of these findings are evident: the effects of moderate habitat fragmentation and ecological stress may be more pronounced in tropical systems than in temperate systems and may result in a greater proportional loss of local biodiversity in the former.

Quantifying Biodiversity: Experience with Parataxonomists and Digital Photography in Papua New Guinea and Guyana

menting biodiversity (e.g., Stork 1993, May 1994, Blackmore 1996, Janzen 1997, Cresswell and Bridgewater 2000). A large part of this biodiversity is represented by insect herbivores feeding on tropical vegetation (Wilson 1988). Many authors have commented on the theoretical and ethical aspects of this quest (e.g., May 1994, 1999) and on whether it can be achieved within a reasonable time frame given the taxonomic facilities available worldwide (e.g., Raven and Wilson 1992, Janzen 1993, Krishtalka and Humphrey 2000). However, few workers have proposed practical measures to inventory insect species in tropical rain forests (but see Hammond 1994, Oliver et al. 2000). In this article, we describe a first step toward documenting this rich insect fauna: training local people in the basics of insect collecting, mounting, and sorting; in digital photography; and in simple, yet powerful, computer databases. The work of these trainees can yield high-quality insect material and data, which are also available for subsequent taxonomic studies, within a relatively short period of time. This speed is important because species depletion resulting from the reduction of tropical habitats is rapid (e.g., Reid 1992). We discuss training and use of parataxonomists with particular reference to insect herbivores, with examples from two research projects in Papua New Guinea (PNG) and Guyana. Identifying, describing, and storing insect specimens are separate issues, which we do not address (see Miller 1991, Raven and Wilson 1992, New 1998). The research projects and their specific problems The first research project began in 1994 in Madang, PNG, and focuses on the local species richness and host specificity of insect herbivores feeding on 60 species of rain forest trees in the Moraceae, Euphorbiaceae, Rubiaceae, and other plant families. The second project started in 1996 at Mabura Hill, Guyana, and investigates the influence of selective logging on insect herbivores feeding on seedlings in a forest plot of 1 km2. Both studies face similar challenges that are typical for eco-entomological surveys of