The interplay between defaunation and phylogenetic diversity affect leaf damage by natural enemies in tropical plants
Authors/Creators
- 1. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro
- 2. Nederlands Instituut voor Ecologie
- 3. Sao Paulo State University
Description
- 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, brocket deer; hereafter, large herbivores) on leaf damage of 3,350 understory 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 investigated 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 similarly and positively correlated with leaf damage 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 large herbivores' indirect effects 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.
Notes
Funding provided by: São Paulo Research Foundation
Crossref Funder Registry ID: https://ror.org/02ddkpn78
Award Number: 2014/01986-0
Funding provided by: São Paulo Research Foundation
Crossref Funder Registry ID: https://ror.org/02ddkpn78
Award Number: 2022/09561-4
Funding provided by: São Paulo Research Foundation
Crossref Funder Registry ID: https://ror.org/02ddkpn78
Award Number: 2015/15172-7
Funding provided by: São Paulo Research Foundation
Crossref Funder Registry ID: https://ror.org/02ddkpn78
Award Number: 2015/11521‐7
Funding provided by: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro
Crossref Funder Registry ID: https://ror.org/03kk0s825
Award Number: E-26/200.610/2022
Methods
Our study was carried out in a multi-site, long-term experiment (DEFAU-BIOTA), distributed at four study sites located in protected areas of the Atlantic Forest in the state of São Paulo, Brazil. The four sites have different compositions of large herbivore communities, but nevertheless, a rich assemblage of species can be found in all of them. Due to different human pressures, sites differ in the presence of the largest ground-dwelling mammal species, the white-lipped peccary (Tayassu pecari) and the tapir (Tapirus terrestris) (Galetti et al., 2017). Although both species are present at site Itamambuca [ITA], only white-lipped peccaries are present at Ilha do Cardoso State Park [CAR]; at Carlos Botelho State Park [CBO] only tapirs are found, and neither of the species are present at Vargem Grande [VGM].
In each site, we installed 15 paired plots (5 m long x 3 m wide) in 2009–2010, but some of the plots collapsed over time; as a result, the data in this work were collected in nine paired plots in ITA, 10 in CBO and 12 in CAR and VGM, summing up 86 plots. Each pair consists of a closed, exclusion plot of medium and large mammals (hence simulating defaunation), and an open plot allowing free access to these animals (control). Each plot was subdivided into eight subplots of 1 m2, in which three subplots were randomly chosen and all plants larger than 0,1 m and smaller than 1 m were marked, identified at the lowest possible taxonomic level, and accessed without disturbance to estimate leaf damage.
We evaluated the leaf damage of all marked plants within each selected subplot in July, August, and November 2019. For each individual plant, we randomly chose three mature leaves (when possible; otherwise, we count on the available number per individual, that is, one or two leaves) to estimate their leaf damage according to the percentage of leaf area lost and/or damaged. Next, we visually assigned the following leaf damage categories for each selected leaf: 0 (intact), 1 ( 1–6% of lost and/or damaged leaf area), 2 (6–12%), 3 (12–25%), 4 (25–50 %), 5 (50–75%) and 6 (75–99%). We proceed with this categorization of damage considering four feeding guilds of insect herbivores (internal and external chewers, galls and leaf miners), the guild of pathogens, and the total leaf damage caused by all groups, given that each leaf may be affected by more than one type of damage.
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