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On the Factors That Promote the Diversity of Herbivorous Insects and Plants in Tropical Forests

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On the Factors That Promote the Diversity of Herbivorous Insects and Plants in Tropical Forests On the factors that promote the diversity of herbivorous insects and plants in tropical forests Judith X. Becerra1 Department of Biosphere 2, University of Arizona, Tucson, AZ 85721 Edited by Paul R. Ehrlich, Stanford University, Stanford, CA, and approved February 27, 2015 (received for review November 13, 2014) Some of the most fascinating and challenging questions in ecology relationship and potential feedback loop between divergent plant are why biodiversity is highest in tropical forests and whether the chemical defenses in a community and insect herbivore speciali- factors involved are unique to these habitats. I did a worldwide test zation that could have effects on insect and plant diversities (12, of the hypotheses that plant community divergence in antiherbi- 13). In places with mostly highly specialized herbivore–plant as- vore traits results in higher insect herbivore diversity, and that sociations, plant communities tended to have a strong pattern of predominant attack by specialized herbivores promotes plant chemical disparity. This result suggests that disparate defensive richness. I found strong correlative support for both ideas. Butterfly systems in a plant community might promote insect specialization diversity was greatest in regions where the community average because it is difficult to attack other plants that have very different species-pairwise dissimilarity in antiherbivore traits among plant antiherbivore traits relative to those of the current host (14). At species was highest. There was also a strong positive relationship the same time, the tendency of insects to specialize on plants between specialized (insect) vs. generalized (mammal) herbivores species sharing the same defenses would favor plant communities and plant richness. Regions where herbivory impact by mammals with species that have divergent defenses. Similar patterns of was higher than that of insects tended to have lower plant nonrandom defense overdispersion have been reported for other diversities. In contrast, regions in which insects are the main plant genera as well (15, 16). consumers, particularly in the Central and South American tropics, The existence of a feedback between herbivore specialization had the highest plant richness. Latitude did not explain any and plant defense community structure is important because it residual variance in insect or plant richness. The strong connec- tions found between insect specialization, plant defense diver- could potentially reduce niche overlap for both plants and in- gence, and plant and insect diversities suggest that increasing our sects and promote their diversities: specialized herbivores can understanding of the ecology of biological communities can aid in attack conspecific plants or species with similar morphological/ considerations of how to preserve biodiversity in the future. chemical antiherbivore traits keeping plants rare (4, 5, 14). Consequently, communities will tend to assemble or evolve plant diversity | insect diversity | tropical forests | latitudinal diversity plant species with disparate defensive systems. In turn, defensive gradient | insect specialization disparity would make it difficult for insect species to use addi- tional hosts, thus reinforcing insect specialization (13). This nderstanding the evolutionary and ecological processes that feedback mechanism has not been previously investigated at a Umaintain diversity in tropical forests has been one of the global scale but its predictions can be tested. If plant diversity is central goals in biology for many years. Plants and insect herbi- driven by herbivore specialization, we expect communities to ex- vores comprise the leading percentage of species in these eco- hibit a positive relationship between plant species richness and systems, making it of particular importance to know what is driving predominance of attack by specialized herbivores. Additionally, if their diversity (1, 2). Plant and plant-feeding insects also constitute insect diversity is determined by divergent plant defensive traits in an abundant resource base for a variety of consumers, including a community, we expect to find a positive correlation between the birds, mammals, reptiles, amphibians, fish, other insects, and ar- divergence of antiherbivore traits in a plant community and the thropods, and can thus in turn impact their consumer’s diversity. richness of its insect herbivore species. Here I present tests of Increased niche differentiation for both insects and plants these two predictions. could potentially promote coexistence of large numbers of species, and thus many ideas are directed at identifying the potential fac- Significance tors that can lead to a decrease of niche overlap in these organisms (3). A prominent framework for plant diversity is niche differen- A central mission in ecology has been to explain differences in tiation by natural enemy partitioning. Several variants of this mechanism have been published, like the Janzen-Connell hy- biodiversity across the world and across groups of organisms. pothesis, and the Chesson and Kuang model: they concur in This knowledge is not only fundamental as a scientific objec- predicting that natural enemies, when specialized, can keep spe- tive but also for practical issues of major concern to human- cies rare and promote plant coexistence and diversity (4–6). kind. Plants and phytophagous insects comprise the highest Similarly, higher host specificity in tropical insects, and therefore macroscopic diversity on Earth, making it particularly impor- increased niche differentiation through resource partitioning, has tant to know the mechanisms that allow their species to co- often been associated with insect diversity (7, 8). Although these exist. This study suggests that without insect specialization the mechanisms have considerable evidence to support them, there is maintenance of tropical plant diversity might not be possible. still controversy because, among other things, the Janzen–Connell Also, without high divergence of defenses among plants, insect mechanism for high tropical richness appears to operate not only tropical diversity may not persist either. in tropical forests, but also in temperate habitats where plant di- versity is lower (9). Similarly, many temperate insects may be as Author contributions: J.X.B. designed research, performed research, analyzed data, and specialized as ones living in the tropics (10). Another challenge is wrote the paper. that, although it is evident that partitioning resources might lead The author declares no conflict of interest. to narrower insect niches, it is still unclear what drives insect This article is a PNAS Direct Submission. specialization (11). 1Email: [email protected]. Recently, herbivory studies performed in the dry tropical for- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. ests of Mexico with the plant genus Bursera found a positive 1073/pnas.1418643112/-/DCSupplemental. 6098–6103 | PNAS | May 12, 2015 | vol. 112 | no. 19 www.pnas.org/cgi/doi/10.1073/pnas.1418643112 Downloaded by guest on October 2, 2021 Results defenses (spines and hairs). Additionally, although they produce Relating Butterfly Diversity to Community Divergence of Plant many chemical compounds, these compounds tended to belong Antiherbivore Traits. To determine whether community di- to only a few classes of chemical defense compounds. As a con- vergence in antiherbivore traits is driving insect diversity, I mea- sequence, the values of the indices of defense evenness were the sured the average plant species-pairwise dissimilarity in chemical, lowest in these areas (Table S3). biotic (ant-attracting traits), and mechanical/morphological de- Butterfly diversity was greatest in regions such as Costa Rica, fenses (e.g., hairs, spines). This involved comparing each plant PNG, and Ecuador, where the community average dissimilarity in species to each other plant species, then averaging over all pair- antiherbivore traits among plant species was highest. Here, some wise dissimilarities. I did this for seven areas of the world, then mechanical/morphological plant defenses, such as hairs, glandular related this average pairwise dissimilarity to the richness of insect trichomes, and laticifers, occurred frequently, but plants were also herbivores that feed on those plants in those areas. I selected often armed with ant-attracting traits, such as extrafloral nectaries, butterflies as the herbivores to examine because their diversities food bodies, or domatia. Additionally, the plant taxa produced a and hosts are well documented in these seven regions. These wide array of chemical compounds, as illustrated by their high trait places have similar physical dimensions (mean = 54,009 km2, evenness index. Some classes of compounds that are infrequent in other regions studied (e.g., alkaloids, proteins, peptides, iso- SD = 2,089) and are: (i) the joint areas of Burundi and Rwanda; flavones, and triterpenoids) are well represented in these tropical (ii)CostaRica;(iii) Morobe and Northern provinces in Papua New areas. All this resulted in communities where species pairs have Guinea (PNG); (iv) Israel, Mount Hermon, and a portion in the highly disparate plant chemistries. Arizona had intermediate levels East of the Sinai Peninsula (Middle East); (v) the provinces of vi of community chemical dissimilarity and it also had intermediate Napo, Orellana, and Sucumbíos in Ecuador (Ecuador); ( )the values of butterfly diversity.
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