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.
Herbivory is viewed as a major driver of plant evolution and the mostimportant energy pathway from plants to higher trophic levels. Therefore, understandingpatterns of herbivory on plants remains a key focus in evolution and ecology. Theevolutionary impacts of leaf herbivory include altering plant fitness, local adaptation, theevolution of defenses, and the diversification of plants as well as natural enemies. Leafherbivory also impacts ecological processes such as plant productivity, communitycomposition, and ecosystem nutrient cycling. Understanding the impact of herbivory onthese ecological and evolutionary processes requires species-specific, as opposed tocommunity-level, measures of herbivory. In addition, species-specific data enables the use ofmodern comparative methods to account for phylogenetic non-independence. Althoughhundreds of studies have measured natural rates of leaf consumption, we are unaware of anyaccessible compilation of these data. We created such a data set to provide the raw dataneeded to test general hypotheses relating to plant–herbivore interactions and to test theinfluence of biotic and abiotic factors on herbivory rates across large spatial scales. A largerepository will make this endeavor more efficient and robust. In total, we compiled 2641population-level measures for either annual or daily rates of leaf herbivory across 1145 speciesof vascular plants collected from 189 studies. All damage measures represent naturaloccurrences of herbivory that span numerous angiosperm, gymnosperm, and fern species. Toenable researchers to explore the causes of variation in herbivory and how these mightinteract, we added information about the study sites including: geolocation, climateclassification, habitat descriptions (e.g., seashore, grassland, forest, agricultural fields), andplant trait information concerning growth form and duration (e.g., annual vs. perennial). Wealso included extensive details of the methodology used to measure leaf damage, includingseasons and months of sampling, age of leaves, and the method used to estimate percentagearea missing. We anticipate that these data will make it possible to test important hypothesesin the plant–herbivore literature, including the plant apparency hypothesis, the latitudinalherbivorydefense hypothesis, the resource availability hypothesis, and the macroevolutionaryescalation of defense hypothesis
Rapid adoption of conservation measures is key to protecting insect populations
Abstract. 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 tradeoffs. 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: Swartzia and Inga (Fabaceae), Protieae (Burseracaeae), Bombacoideae (Malvaceae), and Micropholis (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.
Tropical forests are predicted to harbor most of the insect diversity on earth, but few studies have been conducted to characterize insect communities in tropical forests. One major limitation is the lack of consensus on methods for insect collection. Deciding which insect trap to use is an important consideration for ecologists and entomologists, yet to date few study has presented a quantitative comparison of the results generated by standardized methods in tropical insect communities. Here, we investigate the relative performance of two flight interception traps, the windowpane trap, and the more widely used malaise trap, across a broad gradient of lowland forest types in French Guiana. The windowpane trap consistently collected significantly more Coleoptera and Blattaria than the malaise trap, which proved most effective for Diptera, Hymenoptera, and Hemiptera. Orthoptera and Lepidoptera were not well represented using either trap, suggesting the need for additional methods such as bait traps and light traps. Our results of contrasting trap performance among insect orders underscore the need for complementary trapping strategies using multiple methods for community surveys in tropical forests.
Research on canopy arthropods has progressed from species inventories to the study of their interactions and networks, enhancing our understanding of how hyper-diverse communities are maintained. Previous studies often focused on sampling individual tree species, individual trees or their parts. We argue that such selective sampling is not ideal when analyzing interaction network structure, and may lead to erroneous conclusions. We developed practical and reproducible sampling guidelines for the plot-based analysis of arthropod interaction networks in forest canopies. Our sampling protocol focused on insect herbivores (leaf-chewing insect larvae, miners and gallers) and non-flying invertebrate predators (spiders and ants). We quantitatively sampled the focal arthropods from felled trees, or from trees accessed by canopy cranes or cherry pickers in 53 0.1 ha forest plots in five biogeographic regions, comprising 6,280 trees in total. All three methods required a similar sampling effort and provided good foliage accessibility. Furthermore, we compared interaction networks derived from plot-based data to interaction networks derived from simulated non-plot-based data focusing either on common tree species or a representative selection of tree families. All types of non-plot-based data showed highly biased network structure towards higher connectance, higher web asymmetry, and higher nestedness temperature when compared with plot-based data. Furthermore, some types of non-plot-based data showed biased diversity of the associated herbivore species and specificity of their interactions. Plot-based sampling thus appears to be the most rigorous approach for reconstructing realistic, quantitative plant-arthropod interaction networks that are comparable across sites and regions. Studies of plant interactions have greatly benefited from a plot-based approach and we argue that studies of arthropod interactions would benefit in the same way. We conclude that plot-based studies on canopy arthropods would yield important insights into the processes of interaction network assembly and dynamics, which could be maximised via a coordinated network of plot-based study sites.
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.
Growth defense tradeoff theory predicts that plants in low-resource habitats invest more energy in defense mechanisms against natural enemies than growth, whereas plants in high-resource habitats can afford higher leaf loss rates. A less-studied defense against herbivores involves the synchrony of leaf production, which can be an effective defense strategy if leaf biomass production exceeds the capacity of consumption by insects. The aim of this study was to determine whether leaf synchrony varied across habitats with different available resources and whether insects were able to track young leaf production among tree habitat specialists in a tropical forest of French Guiana. We predicted that high-resource habitats would exhibit more synchrony in leaf production due to the low cost and investment to replace leaf tissue. We also expected closer patterns of leaf synchrony and herbivory within related species, assuming that they shared herbivores. We simultaneously monitored leaf production and herbivory rates of five pairs of tree species, each composed of a specialist of terra firme or white-sand forests within the same lineage. Our prediction was not supported by the strong interaction of habitat and lineage for leaf synchrony within individuals of the same species; although habitat specialists differed in leaf synchrony within four of five lineages, the direction of the effect was variable. All species showed short time lags for the correlation between leaf production and herbivory, suggesting that insects are tightly tracking leaf production, especially for the most synchronous species. Leaf synchrony may provide an important escape defense against herbivores, and its expression appears to be constrained by both evolutionary history and environmental factors
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