Héctor Barrios

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.

Associational resistance and associational susceptibility: specialist herbivores show contrasting responses to tree stand diversification

Heterospecific neighbors may reduce damage to a focal plant by lowering specialist herbivore loads (associational resistance hypothesis), or enhance damage by increasing generalist herbivore loads (associational susceptibility hypothesis). We tested the associational effects of tree diversity on herbivory patterns of the tropical focal tree Tabebuia rosea in an experimental plantation setup, which contained tree monocultures and mixed stands. We found higher herbivore damage to T. rosea at higher tree diversity, indicating that T. rosea did not benefit from associational resistance but rather experienced associational susceptibility. The specific consideration of the two dominant insect herbivore species of T. rosea, the specialist chrysomelid Walterianella inscripta and the specialist pyralid Eulepte gastralis, facilitated understanding of the detected damage patterns. Tree diversity exerted opposite effects on tree infestation by the two herbivores. These findings point to resource concentration effects for the chrysomelid beetle (favored by tree monoculture) and to resource dilution effects for the pyralid caterpillar (favored by tree mixture) as underlying mechanisms of herbivore distribution. A strong contribution of the pyralid to overall damage patterns in diversified stands suggests that associational susceptibility may not necessarily be related to higher abundances of generalist herbivores but may also result from specialized herbivores affected by resource dilution effects. Thus, the identity and biology of herbivore species has to be taken into account when attempting to predict damage patterns in forest ecosystems.

Arthropod Distribution in a Tropical Rainforest: Tackling a Four Dimensional Puzzle

Quantifying the spatio-temporal distribution of arthropods in tropical rainforests represents a first step towards scrutinizing the global distribution of biodiversity on Earth. To date most studies have focused on narrow taxonomic groups or lack a design that allows partitioning of the components of diversity. Here, we consider an exceptionally large dataset (113,952 individuals representing 5,858 species), obtained from the San Lorenzo forest in Panama, where the phylogenetic breadth of arthropod taxa was surveyed using 14 protocols targeting the soil, litter, understory, lower and upper canopy habitats, replicated across seasons in 2003 and 2004. This dataset is used to explore the relative influence of horizontal, vertical and seasonal drivers of arthropod distribution in this forest. We considered arthropod abundance, observed and estimated species richness, additive decomposition of species richness, multiplicative partitioning of species diversity, variation in species composition, species turnover and guild structure as components of diversity. At the scale of our study (2km of distance, 40m in height and 400 days), the effects related to the vertical and seasonal dimensions were most important. Most adult arthropods were collected from the soil/litter or the upper canopy and species richness was highest in the canopy. We compared the distribution of arthropods and trees within our study system. Effects related to the seasonal dimension were stronger for arthropods than for trees. We conclude that: (1) models of beta diversity developed for tropical trees are unlikely to be applicable to tropical arthropods; (2) it is imperative that estimates of global biodiversity derived from mass collecting of arthropods in tropical rainforests embrace the strong vertical and seasonal partitioning observed here; and (3) given the high species turnover observed between seasons, global climate change may have severe consequences for rainforest arthropods.

Insect leaf-chewing damage tracks herbivore richness in modern and ancient forests.

The fossil record demonstrates that past climate changes and extinctions significantly affected the diversity of insect leaf-feeding damage, implying that the richness of damage types reflects that of the unsampled damage makers, and that the two are correlated through time. However, this relationship has not been quantified for living leaf-chewing insects, whose richness and mouthpart convergence have obscured their value for understanding past and present herbivore diversity. We hypothesized that the correlation of leaf-chewing damage types (DTs) and damage maker richness is directly observable in living forests. Using canopy access cranes at two lowland tropical rainforest sites in Panamá to survey 24 host-plant species, we found significant correlations between the numbers of leaf chewing insect species collected and the numbers of DTs observed to be made by the same species in feeding experiments, strongly supporting our hypothesis. Damage type richness was largely driven by insect species that make multiple DTs. Also, the rank-order abundances of DTs recorded at the Panamá sites and across a set of latest Cretaceous to middle Eocene fossil floras were highly correlated, indicating remarkable consistency of feeding-mode distributions through time. Most fossil and modern host-plant pairs displayed high similarity indices for their leaf-chewing DTs, but informative differences and trends in fossil damage composition became apparent when endophytic damage was included. Our results greatly expand the potential of insect-mediated leaf damage for interpreting insect herbivore richness and compositional heterogeneity from fossil floras and, equally promisingly, in living forests.

DNA-based taxonomy of larval stages reveals huge unknown species diversity in neotropical seed weevils (genus Conotrachelus): relevance to evolutionary ecology

High diversity in tropical phytophagous insects may be linked to narrow host specificity and host shifts, but tests are complicated by incomplete taxonomy and difficulties in food source identification. Specimens of the highly diverse New World genus Conotrachelus (Coleoptera: Curculionoidea) were reared from >17,500 fruits (seeds) at six Central American rain forests. Interception traps were used for comparison with assemblages flying in the forest. Mitochondrial cox1 and the nuclear 28S genes were sequenced for 483 larval and adult specimens. A Yule-Coalescent technique was used to group cox1 sequences into putative species (17 from traps, 48 from rearing). Cox1 sequences of 24 species from museum collections provided matches for three species from traps and no match for the reared species. Inga (Fabaceae) was the predominant host among 15 other genera and 67% of the weevils were monophagous. A three gene tree (cox1, rrnL, 28S) recovered four well-supported clades feeding on Inga confirmed by phylogenetic community analyzes that showed phylogenetic conservation of host plant utilization. This suggests that host shifts are not directly involved in speciation, while the broad taxonomic host range and the evolutionary repeated shifts still contribute to the high species richness in Conotrachelus. The DNA-based approach combining species delimitation and phylogenetic analysis elucidated the evolutionary diversification of this lineage, despite insufficient taxonomic knowledge. Conotrachelus is an example of the diverse tropical groups that require DNA-based taxonomy to study their evolutionary ecology.

The Butterflies of Barro Colorado Island, Panama: Local Extinction since the 1930s

Few data are available about the regional or local extinction of tropical butterfly species. When confirmed, local extinction was often due to the loss of host-plant species. We used published lists and recent monitoring programs to evaluate changes in butterfly composition on Barro Colorado Island (BCI, Panama) between an old (1923–1943) and a recent (1993–2013) period. Although 601 butterfly species have been recorded from BCI during the 1923–2013 period, we estimate that 390 species are currently breeding on the island, including 34 cryptic species, currently only known by their DNA Barcode Index Number. Twenty-three butterfly species that were considered abundant during the old period could not be collected during the recent period, despite a much higher sampling effort in recent times. We consider these species locally extinct from BCI and they conservatively represent 6% of the estimated local pool of resident species. Extinct species represent distant phylogenetic branches and several families. The butterfly traits most likely to influence the probability of extinction were host growth form, wing size and host specificity, independently of the phylogenetic relationships among butterfly species. On BCI, most likely candidates for extinction were small hesperiids feeding on herbs (35% of extinct species). However, contrary to our working hypothesis, extinction of these species on BCI cannot be attributed to loss of host plants. In most cases these host plants remain extant, but they probably subsist at lower or more fragmented densities. Coupled with low dispersal power, this reduced availability of host plants has probably caused the local extinction of some butterfly species. Many more bird than butterfly species have been lost from BCI recently, confirming that small preserves may be far more effective at conserving invertebrates than vertebrates and, therefore, should not necessarily be neglected from a conservation viewpoint.

Diversity and composition of arboreal beetle assemblages in tropical pasture afforestations: effects of planting schemes and tree species identity

Timber tree plantations are considered for rehabilitating forest biodiversity in the tropics, but knowledge on determinants of faunal diversity patterns in such human-modified forest landscapes is scarce. We quantified the composition of beetle assemblages on three native timber species (Anacardium excelsum, Cedrela odorata and Tabebuia rosea) planted on former pasture to assess effects of tree species identity, tree species diversity, and insecticide treatment on a speciose group of animals in tropical plantations. The beetle assemblage parameters ‘abundance’, ‘species richness’, ‘Chao1 estimated species richness’ and ‘Shannon diversity’ were significantly reduced by insecticide treatment for each tree species. Shannon diversity increased with stand diversification for T. rosea but not for A. excelsum and C. odorata. Species similarity was highest (lowest species turnover) between beetle assemblages on T. rosea, and it was lowest (highest species turnover) for assemblages on insecticide-treated trees of all timber species. Considering trophic guilds, herbivorous beetles dominated on all tree species and in all planting schemes. Herbivores were significantly more dominant on T. rosea and C. odorata than on A. excelsum, suggesting that tree species identity affects beetle guild structure on plantation trees. Insecticide-treated stands harbored less herbivores than untreated stands, but exhibited a high abundance of predator beetle species. Our study revealed that even young pasture-afforestations can host diverse beetle assemblages and thus contribute to biodiversity conservation in the tropics. The magnitude of this contribution, however, may strongly depend on management measures and on the selected tree species.

Galls Produced by Hylaeogena thoracica (Coleoptera: Buprestidae) and the Effect of the Inquiline Philides anthonomoides (Coleoptera: Curculionidae)

Abstract The ability of Hylaeogena thoracica Waterhouse, 1889 (Coleoptera: Buprestidae) to induce galls on Amphilophium paniculatum (L.) H.B.K (Bignoniaceae) is reported here. Species of Hylaeogena Obenberger, 1923 are associated with vines of the family Bignoniaceae as leafminers, therefore this report represents the first record of the genus acting as a gall inducer. The effect of the inquiline Philides anthonomoides Champion, 1906 (Coleoptera: Curculionidae, Conoderinae) on gall morphology is also described. Most Neotropical conoderines are associated with tree falls and are assumed to be wood-borers. This represents the first report of the species acting as an inquiline in galls. Four parasitoid species belonging to three families of Hymenoptera that emerged from the galls are also reported.

The Saturniidae of Barro Colorado Island, Panama: A model taxon for studying the long-term effects of climate change?

Abstract We have little knowledge of the response of invertebrate assemblages to climate change in tropical ecosystems, and few studies have compiled long‐term data on invertebrates from tropical rainforests. We provide an updated list of the 72 species of Saturniidae moths collected on Barro Colorado Island (BCI), Panama, during the period 1958‐2016. This list will serve as baseline data for assessing long‐term changes of saturniids on BCI in the future, as 81% of the species can be identified by their unique DNA Barcode Index Number, including four cryptic species not yet formally described. A local species pool of 60 + species breeding on BCI appears plausible, but more cryptic species may be discovered in the future. We use monitoring data obtained by light trapping to analyze recent population trends on BCI for saturniid species that were relatively common during 2009‐2016, a period representing >30 saturniid generations. The abundances of 11 species, of 14 tested, could be fitted to significant time‐series models. While the direction of change in abundance was uncertain for most species, two species showed a significant increase over time, and forecast models also suggested continuing increases for most species during 2017‐2018, as compared to the 2009 base year. Peaks in saturniid abundance were most conspicuous during El Niño and La Niña years. In addition to a species‐specific approach, we propose a reproducible functional classification based on five functional traits to analyze the responses of species sharing similar functional attributes in a fluctuating climate. Our results suggest that the abundances of larger body‐size species with good dispersal abilities may increase concomitantly with rising air temperature in the future, because short‐lived adults may allocate less time to increasing body temperature for flight, leaving more time available for searching for mating partners or suitable oviposition sites.

Gall-Inducing Insects and Their Associated Parasitoid Assemblages in the Forests of Panama

During the past 20 years several studies have documented gall-inducing insect species richness in Panama. Additionally, host plant and parasitoid assemblages associated to galls have been studied. The effects of habitat, altitude, vegetation, and climate on the richness of insect gall assemblages have been addressed in these studies. Similarly, the effects of temporal, spatial, and vertical variation on the local richness of gall-inducing species have also been discussed. The use of a crane in the rainforests of Panama has enabled us to study gall communities in the forest canopy. The taxonomic knowledge on oak gall wasps and their patterns in species richness and distribution in Panama have been the focus of attention in recent years. Here, we review the literature documenting the taxonomic diversity of the Cynipidae and oak gall wasps (tribe Cynipini) in the Neotropics, supplementing it with recent field surveys assessing oak gall wasp diversity in montane forests of Panama. In particular, we studied gall wasp diversity associated with Quercus spp. (Fagaceae), the dominant tree genus in montane forests of Panama, and identified a rich gall wasp insect fauna (~65 spp).