Italo Mesones

THE GROWTH-DEFENSE TRADE-OFF AND HABITAT SPECIALIZATION BY PLANTS IN AMAZONIAN FORESTS

Tropical forests include a diversity of habitats, which has led to specialization in plants. Near Iquitos, in the Peruvian Amazon, nutrient-rich clay forests surround nutrient-poor white-sand forests, each harboring a unique composition of habitat specialist trees. We tested the hypothesis that the combination of impoverished soils and herbivory creates strong natural selection for plant defenses in white-sand forest, while rapid growth is favored in clay forests. Recently, we reported evidence from a reciprocal-transplant experiment that manipulated the presence of herbivores and involved 20 species from six genera, including phylogenetically independent pairs of closely related white-sand and clay specialists. When protected from herbivores, clay specialists exhibited faster growth rates than white-sand specialists in both habitats. But, when unprotected, white-sand specialists outperformed clay specialists in white-sand habitat, and clay specialists outperformed white-sand specialists in clay habitat. Here we test further the hypothesis that the growth defense trade-off contributes to habitat specialization by comparing patterns of growth, herbivory, and defensive traits in these same six genera of white-sand and clay specialists. While the probability of herbivore attack did not differ between the two habitats, an artificial defoliation experiment showed that the impact of herbivory on plant mortality was significantly greater in white-sand forests. We quantified the amount of terpenes, phenolics, leaf toughness, and available foliar protein for the plants in the experiment. Different genera invested in different defensive strategies, and we found strong evidence for phylogenetic constraint in defense type. Overall, however, we found significantly higher total defense investment for white-sand specialists, relative to their clay specialist congeners. Furthermore, herbivore resistance consistently exhibited a significant trade-off against growth rate in each of the six phylogenetically independent species-pairs. These results confirm theoretical predictions that a trade-off exists between growth rate and defense investment, causing white-sand and clay specialists to evolve divergent strategies. We propose that the growth-defense trade-off is universal and provides an important mechanism by which herbivores govern plant distribution patterns across resource gradients.

THE CONTRIBUTION OF EDAPHIC HETEROGENEITY TO THE EVOLUTION AND DIVERSITY OF BURSERACEAE TREES IN THE WESTERN AMAZON

Abstract —Environmental heterogeneity in the tropics is thought to lead to specialization in plants and thereby contribute to the diversity of the tropical flora. We examine this idea with data on the habitat specificity of 35 western Amazonian species from the genera Protium, Crepidospermum, and Tetragastris in the monophyletic tribe Protieae (Burseraceae) mapped on a molecular‐based phylogeny. We surveyed three edaphic habitats that occur throughout terra firme Amazonia: white‐sand, clay, and terrace soils in eight forests across more than 2000 km in the western Amazon. Twenty‐six of the 35 species were found to be associated with only one of three soil types, and no species was associated with all three habitats; this pattern of edaphic specialization was consistent across the entire region. Habitat association mapped onto the phylogenetic tree shows association with terrace soils to be the probable ancestral state in the group, with subsequent speciation events onto clay and white‐sand soils. The repeated gain of clay association within the clade likely coincides with the emergence of large areas of clay soils in the Miocene deposited during the Andean uplift. Character optimizations revealed that soil association was not phylogenetically clustered for white‐sand and clay specialists, suggesting repeated independent evolution of soil specificity is common within the Protieae. This phylogenetic analysis also showed that multiple cases of putative sister taxa with parapatric distributions differ in their edaphic associations, suggesting that edaphic heterogeneity was an important driver of speciation in the Protieae in the Amazon basin.

A floristic study of the white-sand forests of Peru.

Abstract Tropical forests occurring on white-sand soils have a unique structure and are famous for their endemism. Yet, no comprehensive floristic study has ever been undertaken in white-sand forests in the western Amazon. Here, we present the results of floristic inventories from 16 plots in seven sites from the Peruvian Amazon to investigate diversity, species composition, and endemism in white-sand forests. We compare our results to a large data set from terra firme forests from more fertile soils in the same region. We found that white-sand forest plots have extremely low average species diversity (41.5 species per 0.1-ha plot) and that white-sand plots have significantly different species composition from terra firme plots. We classify 114 species as endemic to white sand, with another 21 species that can be considered facultative specialists or cryptic endemics. These endemics and specialists are extremely dominant, accounting for more than 83% of the total number of stems surveyed in white-sand forest plots. We place our results in the context of the role of environmental heterogeneity influencing patterns of species diversity and the conservation of Amazonian forests.

Insect herbivores, chemical innovation, and the evolution of habitat specialization in Amazonian trees

Herbivores are often implicated in the generation of the extraordinarily diverse tropical flora. One hypothesis linking enemies to plant diversification posits that the evolution of novel defenses allows plants to escape their enemies and expand their ranges. When range expansion involves entering a new habitat type, this could accelerate defense evolution if habitats contain different assemblages of herbivores and/or divergent resource availabilities that affect plant defense allocation. We evaluated this hypothesis by investigating two sister habitat specialist ecotypes of Protium subserratum (Burseraceae), a common Amazonian tree that occurs in white-sand and terra firme forests. We collected insect herbivores feeding on the plants, assessed whether growth differences between habitats were genetically based using a reciprocal transplant experiment, and sampled multiple populations of both lineages for defense chemistry. Protium subserratum plants were attacked mainly by chrysomelid beetles and cicadellid hemipterans. Assemblages of insect herbivores were dissimilar between populations of ecotypes from different habitats, as well as from the same habitat 100 km distant. Populations from terra firme habitats grew significantly faster than white-sand populations; they were taller, produced more leaf area, and had more chlorophyll. White-sand populations expressed more dry mass of secondary compounds and accumulated more flavone glycosides and oxidized terpenes, whereas terra firme populations produced a coumaroylquinic acid that was absent from white-sand populations. We interpret these results as strong evidence that herbivores and resource availability select for divergent types and amounts of defense investment in white-sand and terra firme lineages of Protium subserratum, which may contribute to habitat-mediated speciation in these trees.

Comparing composition and diversity of parasitoid wasps and plants in an Amazonian rain-forest mosaic

Local species richness and between-site similarity in species composition of parasitoid wasps (Hymenoptera: Ichneumonidae; Pimplinae and Rhyssinae) were correlated with those of four plant groups (pteridophytes, Melastomataceae, Burseraceae and Arecaceae) in a western Amazonian lowland rain forest mosaic. The mosaic structure of the forest was related to variation in soils within the non-inundated terrain. Significant matrix correlation between patterns in parasitoid wasp species composition and plant species composition was found. Most of the overall correlation was due to idiobiont parasitoids of weakly concealed hosts, which attack host larvae and pupae in exposed situations, with two of the four ecologically defined parasitoid groups showing no correlation at all. A positive correlation between the number of plant species and the number of Pimplinae and Rhyssinae species at a site was found when the latter was corrected for collecting effort. Consequently, the degree of floristic difference between sites may be indicative of the difference in species composition of ichneumonids, and the species richness of plants may serve as a predictor of the species richness of parasitoid wasps. Although these results were obtained in a mosaic including structurally and floristically clearly different types of rain forest, the correlation coefficients were relatively low, and the present results lend only weak support to the idea of using plant distributions as indicators of animal distributions.

Herbivory, growth rates, and habitat specialization in tropical tree lineages: implications for Amazonian beta-diversity

Tropical plant diversity is extraordinarily high at both local and regional scales. Many studies have demonstrated that natural enemies maintain local diversity via negative density dependence, but we know little about how natural enemies influence beta-diversity across habitats and/or regions. One way herbivores could influence plant beta-diversity is by driving allocation trade-offs that promote habitat specialization across resource gradients. We therefore predicted that increasing resource availability should be accompanied by increasing herbivory rates and decreasing plant allocation to defense. Second, relative abundances within plant lineages are predicted to reflect patterns of habitat specialization and allocation trade- offs. A phylogenetic context is vital not only to compare homologous plant traits (including defense strategies) across habitat types, but also to connect evolutionary trade-offs to patterns of species diversification in each phylogenetic lineage. We tested these predictions for trees in white-sand, clay terra firme, and seasonally flooded forests in Peru and French Guiana that represent the range of soil fertility, forest structure, and floristic compositions found throughout the Amazon region. We established 74 0.5-ha plots in these habitats and sampled all trees. Within 12 representative plots we marked newly expanding leaves of 394 saplings representing 68 species, including the most abundant species in each plot in addition to species from five focal lineages:SwartziaandInga(Fabaceae), Protieae (Burseracaeae), Bombacoideae (Malvaceae), andMicropholis(Sapotaceae). We measured total leaf production rates for each sapling and calculated relative herbivory impact as the ratio between herbivory rate and leaf production rate. Herbivory rates averaged 2.1%per month, did not correlate with leaf production rate, and were similar across habitats. Relative herbivore impacts exceeded leaf production rates for most species. Leaf production rate averaged 2.8%, was significantly higher in seasonally flooded forests than the other two habitats, and exhibited significant correlations with specific leaf area. Species with high herbivory rates exhibited significantly lower relative abundances in terra firme forests. Overall, focal species within lineages present contrasting patterns regarding their herbivory rates and leaf production rate within habitats. These results highlight why a lineage-based approach is necessary when attempting to connect hypotheses regarding evolutionary trade-offs to community assembly patterns.

Taxonomic and functional composition of arthropod assemblages across contrasting Amazonian forests.

Arthropods represent most of global biodiversity, with the highest diversity found in tropical rain forests. Nevertheless, we have a very incomplete understanding of how tropical arthropod communities are assembled. We conducted a comprehensive mass sampling of arthropod communities within three major habitat types of lowland Amazonian rain forest, including terra firme clay, white-sand and seasonally flooded forests in Peru and French Guiana. We examined how taxonomic and functional composition (at the family level) differed across these habitat types in the two regions. The overall arthropod community composition exhibited strong turnover among habitats and between regions. In particular, seasonally flooded forest habitats of both regions comprised unique assemblages. Overall, 17·7% (26 of 147) of arthropod families showed significant preferences for a particular habitat type. We present a first reproducible arthropod functional classification among the 147 taxa based on similarity among 21 functional traits describing feeding source, major mouthparts and microhabitats inhabited by each taxon. We identified seven distinct functional groups whose relative abundance contrasted strongly across the three habitats, with sap and leaf feeders showing higher abundances in terra firme clay forest. Our novel arthropod functional classification provides an important complement to link these contrasting patterns of composition to differences in forest functioning across geographical and environmental gradients. This study underlines that both environment and biogeographical processes are responsible for driving arthropod taxonomic composition while environmental filtering is the main driver of the variance in functional composition.

There's no place like home: seedling mortality contributes to the habitat specialisation of tree species across Amazonia

Understanding the mechanisms generating species distributions remains a challenge, especially in hyperdiverse tropical forests. We evaluated the role of rainfall variation, soil gradients and herbivory on seedling mortality, and how variation in seedling performance along these gradients contributes to habitat specialisation. In a 4-year experiment, replicated at the two extremes of the Amazon basin, we reciprocally transplanted 4638 tree seedlings of 41 habitat-specialist species from seven phylogenetic lineages among the three most important forest habitats of lowland Amazonia. Rainfall variation, flooding and soil gradients strongly influenced seedling mortality, whereas herbivory had negligible impact. Seedling mortality varied strongly among habitats, consistent with predictions for habitat specialists in most lineages. This suggests that seedling performance is a primary determinant of the habitat associations of adult trees across Amazonia. It further suggests that tree diversity, currently mostly harboured in terra firme forests, may be strongly impacted by the predicted climate changes in Amazonia.

Peatland forests are the least diverse tree communities documented in Amazonia, but contribute to high regional beta‐diversity

Western Amazonia is known to harbour some of Earths most diverse forests, but previous floristic analyses have excluded peatland forests which are extensive in northern Peru and are among the most environmentally extreme ecosystems in the lowland tropics. Understanding patterns of tree species diversity in these ecosystems is important both for quantifying beta‐diversity in this region, and for understanding determinants of diversity more generally in tropical forests. Here we explore patterns of tree diversity and composition in two peatland forest types – palm swamps and peatland pole forests – using 26 forest plots distributed over a large area of northern Peru. We place our results in a regional context by making comparisons with three other major forest types: terra firme forests (29 plots), white‐sand forests (23 plots) and seasonally‐flooded forests (11 plots). Peatland forests had extremely low (within‐plot) alpha‐diversity compared with the other forest types that were sampled. In particular, peatland pole forests had the lowest levels of tree diversity yet recorded in Amazonia (20 species per 500 stems, Fishers alpha 4.57). However, peatland pole forests and palm swamps were compositionally different from each other as well as from other forest types in the region. Few species appeared to be peatland endemics. Instead, peatland forests were largely characterised by a distinctive combination of generalist species and species previously thought to be specialists of other habitats, especially white‐sand forests. We suggest that the transient nature and extreme environmental conditions of Amazonian peatland ecosystems have shaped their current patterns of tree composition and diversity. Despite their low alpha‐diversity, the unique combination of species found in tree communities in Amazonian peatlands augment regional beta‐diversity. This contribution, alongside their extremely high carbon storage capacity and lack of protection at national level, strengthens their status as a conservation priority.

Origin and maintenance of chemical diversity in a species-rich tropical tree lineage

Plant secondary metabolites play important ecological and evolutionary roles, most notably in the deterrence of natural enemies. The classical theory explaining the evolution of plant chemical diversity is that new defences arise through a pairwise co-evolutionary arms race between plants and their specialized natural enemies. However, plant species are bombarded by dozens of different herbivore taxa from disparate phylogenetic lineages that span a wide range of feeding strategies and have distinctive physiological constraints that interact differently with particular plant metabolites. How do plant defence chemicals evolve under such multiple and potentially contrasting selective pressures imposed by diverse herbivore communities? To tackle this question, we exhaustively characterized the chemical diversity and insect herbivore fauna from 31 sympatric species of Amazonian Protieae (Burseraceae) trees. Using a combination of phylogenetic, metabolomic and statistical learning tools, we show that secondary metabolites that were associated with repelling herbivores (1) were more frequent across the Protieae phylogeny and (2) were found in average higher abundance than other compounds. Our findings suggest that generalist herbivores can play an important role in shaping plant chemical diversity and support the hypothesis that chemical diversity can also arise from the cumulative outcome of multiple diffuse interactions.A high frequency and abundance of secondary metabolites associated with defence against >230 insect herbivore species suggests that generalist herbivores play a crucial role in shaping plant chemical diversity among Amazonian Protieae trees.