Pathogens and insect herbivores drive rainforest plant diversity and composition

Abstract

Tropical forests are important reservoirs of biodiversity, but the processes that maintain this diversity remain poorly understood. The Janzen-Connell hypothesis suggests that specialized natural enemies such as insect herbivores and fungal pathogens maintain high diversity by elevating mortality when plant species occur at high density (negative density dependence; NDD). NDD has been detected widely in tropical forests, but the prediction that NDD caused by insects and pathogens has a community-wide role in maintaining tropical plant diversity remains untested. We show experimentally that changes in plant diversity and species composition are caused by fungal pathogens and insect herbivores. Effective plant species richness increased across the seed-to-seedling transition, corresponding to large changes in species composition. Treating seeds and young seedlings with fungicides significantly reduced the diversity of the seedling assemblage, consistent with the Janzen-Connell hypothesis. Although suppressing insect herbivores using insecticides did not alter species diversity, it greatly increased seedling recruitment and caused a marked shift in seedling species composition. Overall, seedling recruitment was significantly reduced at high conspecific seed densities and this NDD was greatest for the species that were most abundant as seeds. Suppressing fungi reduced the negative effects of density on recruitment, confirming that the diversity-enhancing effect of fungi is mediated by NDD. Our study provides an overall test of the Janzen-Connell hypothesis and demonstrates the crucial role that insects and pathogens have both in structuring tropical plant communities and in maintaining their remarkable diversity.

Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

“…Along with fungi and insects, the Oomycota have long been thought to be one of the drivers of the JanzenConnell model. However, the degree of host-specificity is unknown for most Oomycota species 46 , and a fungicide study in Belize documented a non-significant effect by these protists 6 . If the Oomycota broadly drive the Janzen-Connell model, then we can expect their diversity to be very high, mirroring tree diversity.…”

“…For example, one hectare can contain more than 400 tree species 2 and one tree can harbour more than 40 ant species 3 . This hyperdiversity of trees has been partially explained by the Janzen-Connell model 4,5 , which hypothesizes that host-specific predators and parasites reduce plant population growth in a density-dependent manner 6,7 . Sampling up in the tree canopies and below on the ground has further led to the view that arthropods are the most diverse eukaryotes in tropical rainforests 8,9 .…”

Phylogenetic structure and host abundance drive disease pressure in communities

“…Pathogens play an important part in shaping the structure and dynamics of natural communities, because species are not affected by them equally 1,2 . A shared goal of ecology and epidemiology is to predict when a species is most vulnerable to disease.…”

“…Plant pathogens can be important drivers of community diversity, structure and dynamics 1,2,10,11 . A basic premise of epidemiology is that pathogen transmission often increases with host density 12,13 .…”

“…Densitydependent disease provides a mechanism for the maintenance of plant diversity in natural communities, in which locally uncommon species enjoy a rare-species advantage-based on lower enemy pressure-that mitigates the competitive impacts of dominant species [3][4][5] . Reports of density-dependent disease dynamics generally infer the potential effects on communities from studies of one or a few species 2 , while community-level studies 1 are scarce but essential to evaluate whether such a rarespecies advantage predicts patterns of disease across a community.…”