Herbivores on a Dominant Understory Shrub Increase Local Plant Diversity in Rain Forest Communities

Ecology, 91(12), 2010, pp. 3707–3718 Ó 2010 by the Ecological Society of America Herbivores on a dominant understory shrub increase local plant diversity in rain forest communities 1,4 2 1 3 LEE A. DYER, DEBORAH K. LETOURNEAU, GERARDO VEGA CHAVARRIA, AND DIEGO SALAZAR AMORETTI 1Department of Biology, University of Nevada, Reno, Nevada 89557 USA 2Department of Environmental Studies, University of California, Santa Cruz, California 95064 USA 3Department of Biology, University of Missouri, St. Louis, Missouri 63121 USA Abstract. Indirect effects of trophic interactions on biodiversity can be large and common, even in complex communities. Previous experiments with dominant understory Piper shrubs in a Costa Rican rain forest revealed that increases in herbivore densities on these shrubs caused widespread seedling mortality as a result of herbivores moving from Piper to seedlings of many different plant genera. We tested components of the Janzen-Connell hypothesis by conducting focused studies on the effects of specialist and generalist Piper herbivores on local seedling diversity. Whereas specialist herbivores are predicted to increase mortality to neighboring seedlings that are closely related to the source plant, true generalists moving from source plants may cause density-dependent mortality of many species, and possibly increase richness if new species replace abundant species that have been thinned by herbivores. Therefore, we hypothesized that seedling richness would be greater in understory control plots created in patches of Piper that had normal densities of generalist herbivores compared to plots from which we removed generalist herbivores manually from all Piper shrubs. After 15 months, generalist-herbivore-removal plots had .40% fewer seedlings, .40% fewer species, and 40% greater seedling evenness, on average, than control plots with generalist herbivores intact. Using a complementary approach in unmanipulated plots in four forests, we used path analysis to test for a positive association between seedling diversity and herbivore damage on Piper species. In unmanipulated plots, for both generalist and specialist herbivores, our data were significant fits to the causal model that Piper herbivores decrease evenness and increase plant species richness, corroborating the experimental results. Because herbivores changed how individuals were apportioned among the species and families present (lower evenness), one interpretation of these associations between herbivores on Piper shrubs and local seedling richness is that high seedling mortality in dominant families allowed the colonization or survival of less common species. If interspecific or apparent competition allowed for a relative increase in species richness, then the Janzen-Connell hypothesis may extend its predictions to generalist seedling predators. We speculate that apparent competition may explain some of the deviations from neutral model predictions, especially at small scales. Key words: apparent competition; biodiversity; herbivory; Janzen-Connell hypothesis; seedling mortality; tropical rain forest. INTRODUCTION 2008). The diet breadth of these predators has been referred to as ‘‘acute specificity’’ (Norghauer et al. 2010) The role of specialist natural enemies has been or ‘‘high levels of host specificity’’ (Harms et al. 2000). emphasized in the well-known Janzen-Connell hypoth- However, if we generalize the Janzen-Connell hypothesis esis (Janzen 1970, Connell 1971), which posits that high (e.g., Bever 2003), it simply predicts that seed or seedling species richness is maintained by density dependent enemies dispersing from source plants reduce the density mortality of seeds and seedlings as they are attacked by of their host plants along an impact gradient that host-specific predators, pathogens, or herbivores dis- diminishes with distance from the source. The resultant persing from the parent tree. Theoretical and empirical effects on the community will depend on the diet studies of this hypothesis assume that these enemies breadth of these enemies. There are numerous working exhibit a clear preference for plants that are better definitions and measures of diet breadth (e.g., Odegaard competitors or possibly species that tend to form a dense 2000, Odegaard et al. 2000, Irschick et al. 2005, layer of seedlings or saplings (reviewed by Carson et al. Lewinsohn et al. 2005, Novotny and Basset 2005, Dyer et al. 2007), but here we use a common taxonomic Manuscript received 2 September 2008; revised 19 April measure: the number of plant families consumed by an 2010; accepted 22 April 2010. Corresponding Editor: W. P. Carson. herbivore, with specialists consuming plants within one 4 E-mail: [email protected] family and generalists consuming plants in multiple 3707 3708 LEE A. DYER ET AL. Ecology, Vol. 91, No. 12 families (Bernays and Graham 1988, Dyer 1995, Singer richness in a neotropical rain forest after removing and Stireman 2005, Dyer et al. 2007). generalist herbivores from all Piper species in understory If the seed or seedling predators attracted or plots. Understory Piper vines and shrubs are abundant maintained by a source plant are taxonomic specialists, and diverse understory plants, usually ranked in the top then associated plants in the same species, genus or 10 species for high species richness and numerical family will experience density-dependent mortality from abundance in Neotropical forests (Burger 1971, Gentry shared herbivores. True generalist feeders that eat plants and Emmons 1987, Dyer and Palmer 2004, Marquis in all families are on the other end of the theoretical 2004). The plants in this genus host a diverse array of spectrum of diet breadth, and seed or seedling mortality specialist and generalist herbivores (Marquis 1991, caused by these generalists would be increased by Greig 1993, 2004, Letourneau 2004, Dyer et al. 2007: increases in the relative densities of their various host Appendix A), and thus are good candidates for apparent seeds or seedlings in the community (probability of competition with other understory plants through encounter). The likely effect of both specialist and shared herbivores (Strong et al. 1984). Using a generalist movement from the source plant, then, would complementary correlational approach, we also tested be to reduce dominance at the level of species, genus or the effects of generalist versus specialist herbivory on family, with more generalized herbivores affecting more plant species richness in unmanipulated understory taxa than specialists. Since seeds and seedlings are often patches in four forests. We quantified generalist clumped in distribution, both specialists and generalists (orthopteran and lepidopteran) and specialist (lepidop- from source plants may be important in increasing or teran and coleopteran) herbivory on Piper shrubs as maintaining high plant diversity (evenness and richness) potential source plants, and measured herbivory levels in the community. That is, factors that reduce abun- and diversity of neighboring understory plants. The dance and dominance can enhance conditions for the specialists were all restricted to feeding on Piper and recruitment of new species or the persistence of rarer many were monophagous, while the generalists all fed species. on multiple families, with some generalists feeding on Our consideration of the potential importance of plants in over 50 families (Appendix A; Dyer et al. 2007; generalist herbivores stems from previous studies, in L. A. Dyer, unpublished data). We also included light which we documented predictable changes in plant availability (canopy cover) as a predictor variable, species richness after experimental additions of an apex because small changes in light availability can result in predatory beetle that resides in Piper ant-shrubs biologically significant changes in Piper chemistry, (Letourneau and Dyer 1998, Letourneau et al. 2004). herbivory levels, and biodiversity (Denslow 1987, Dyer Indirect effects occurred through four trophic levels; the and Letourneau 1999, 2007). This study is unique in its predatory beetle (Coleoptera: Cleridae) reduced densi- combination of experimental and path analysis ap- ties of resident Pheidole ants (Hymenoptera: Formici- proaches to test for community-level diversity effects. It dae), which were subsequently less effective at reducing is, to our knowledge, the first attempt to test for Janzen- herbivory on the host plant Piper cenocladum C.DC. Connell effects: (1) with patchy understory shrubs as (Piperaceae) (Letourneau and Dyer 1998). These cas- concentrated source pools for enemies, (2) with gener- Piper cading effects that released herbivores on rippled alist seedling predators, and (3) invoking apparent out to the local understory plant community, through competition as a possible mechanism for determining increased herbivory levels and mortality on nearby Piper plants species richness. and on other plantlets (,20 cm; Dyer and Letourneau 1999, Letourneau et al. 2004, Letourneau and Dyer MATERIALS AND METHODS 2005). On poorer quality ultisols the richness of plantlets Study site did not change. However, the species richness of plantlets in understory communities on rich, alluvial We conducted the manipulative study at La Tirimbina soils was significantly lower than that of control plots Reserve, Costa Rica, between May 2004 and August with no beetles, intact ant colonies, and low herbivory. 2005 and collected field data between September 2005 We hypothesized that the ubiquitous Piper,when and

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