The interplay between defaunation and phylogenetic diversity affects leaf damage by natural enemies in tropical plants

Natural enemies play an important role in controlling plant population growth and vegetation dynamics. Tropical rainforests host the greatest diversity of herbivores, from large mammalian ungulates to microscopic pathogens, generating and maintaining plant diversity. By feeding on the same resources, large mammalian herbivores may interfere with plant consumption and leaf damage by important enemy guilds such as invertebrate herbivores and pathogens, triggering indirect trophic cascades. However, the impact of local extinctions of large herbivores on plant-enemy interactions is relatively unknown. We experimentally tested the effects of defaunation of large mammalian herbivores (e.g. peccaries, tapirs and brocket deer; hereafter, large herbivores) on the leaf damage of 3350 understorey plants in tropical rainforests of Brazil. We examined leaf damage in 10,050 leaves from 333 morphospecies by assigning the area consumed or damaged by five guilds of insect herbivores and leaf pathogens within 86 paired open-closed plots and investigating the joint effects of defaunation and plant phylogenetic diversity. Plants released from large herbivores had 9% less leaf damage; this difference was due to the lower leaf pathogens incidence (29%) rather than insect herbivory. Evolutionary distinctness was positively correlated with leaf damage in a similar way in all treatments, suggesting additive effects of defaunation and phylogenetic diversity. Total and pathogenic leaf damage (but not insect damage) decreased with plant richness across treatments, and large herbivores exclusion resulted in increased plant species richness. This suggests that large herbivores exclusion leads to a dilution of total and pathogens' leaf damage by increasing plant species richness. Our results suggest that indirect effects of large herbivores decrease the dilution potential of plant communities against pathogens and rather reinforce their top-down impact on vegetation, demonstrating a previously overlooked cascading effect of large herbivore extinction on forest ecosystems. Synthesis: The extinction of large mammalian herbivores can lead to a decrease in pathogen-driven leaf damage, a previously unknown indirect effect in forest ecosystems, which might have consequences for plant fitness and ultimately for plant diversity. Large herbivores and plant pathogens might have synergistic effects in regulating the diversity of plant communities in some of the most diverse ecosystems on Earth. Os inimigos naturais desempenham um papel importante no controle do crescimento das populacoes de plantas e na dinamica vegetal. As florestas tropicais abrigam a maior diversidade de herbivoros do planeta, desde grandes mamiferos ungulados ate patogenos microscopicos, gerando e mantendo a diversidade vegetal. Ao se alimentar dos mesmos recursos que insetos e patogenos, os grandes mamiferos herbivoros podem interferir no consumo de plantas e nos danos as folhas causados por guildas inimigas, tais como herbivoros invertebrados e patogenos, desencadeando efeitos indiretos em cascatas troficas. Entretanto, o impacto das extincoes locais dos grandes herbivoros nas interacoes entre plantas e seus distintos inimigos naturais e pouco conhecido. Testamos experimentalmente os efeitos da defaunacao de grandes mamiferos herbivoros (por exemplo, queixadas, antas e veados-catingueiros; daqui em diante chamados 'grandes herbivoros') nos danos foliares de 3.350 plantas de sub-bosque em florestas tropicais do Brasil. Examinamos os danos foliares em 10.050 folhas de 333 morfoespecies, atribuindo a area consumida ou danificada a cinco guildas de insetos herbivoros e patogenos foliares em 86 parcelas pareadas (abertas e fechadas) e investigamos os efeitos conjuntos da defaunacao e da diversidade filogenetica das plantas. As plantas nao expostas aos grandes herbivoros apresentaram 9% a menos de danos foliares, sendo essa diferenca atribuida a menor incidencia de patogenos foliares (29%) e nao a herbivoria por insetos. A Distincao Evolutiva das plantas se correlacionou positivamente com os danos foliares e de maneira semelhante em todos os tratamentos, sugerindo efeitos aditivos da defaunacao e da diversidade filogenetica. Os danos foliares totais e patogenicos (mas nao os danos por insetos) diminuiram com a riqueza de plantas entre os tratamentos e a exclusao de grandes herbivoros resultou no aumento da riqueza de especies de plantas. Esse fato sugere que a exclusao de grandes herbivoros leva a uma diluicao dos danos foliares totais e causados por patogenos atraves de um efeito indireto mediado pela riqueza de especies de plantas. Nossos resultados sugerem que os efeitos indiretos dos grandes herbivoros diminuem o potencial de diluicao das comunidades vegetais contra os patogenos e reforcam o seu papel de controladores 'de topo' na vegetacao, demonstrando um efeito cascata anteriormente negligenciado da extincao de grandes herbivoros nos ecossistemas florestais (tropicais). Sintese: A extincao de grandes mamiferos herbivoros pode levar a uma diminuicao dos danos foliares causados por patogenos, um efeito indireto ate entao desconhecido nos ecossistemas florestais, que pode ter consequencias para a aptidao das plantas e, em ultima instancia, para a diversidade vegetal. Grandes herbivoros e patogenos de plantas podem ter efeitos sinergicos na regulacao da diversidade de comunidades vegetais em alguns dos mais diversos ecossistemas do planeta. The extinction of large mammalian herbivores can lead to a decrease in pathogen-driven leaf damage, a previously unknown indirect effect in forest ecosystems, which might have consequences for plant fitness and ultimately for plant diversity. Large herbivores and plant pathogens might have synergistic effects in regulating the diversity of plant communities in some of the most diverse ecosystems on Earth.image