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Evolutionary history of host trees amplifies the dilution effect of biodiversity on forest pests [1]

['Andrew V. Gougherty', 'Usda Forest Service', 'Northern Research Station', 'Delaware', 'Ohio', 'United States Of America', 'Department Of Botany', 'University Of British Columbia', 'Vancouver', 'T. Jonathan Davies']

Date: 2024-03

Roles of phylogeny, host range, and pest nativity

The diluting effect of biodiversity on the prevalence of forest pests that we detect supports a growing body of literature on the relationship between host diversity and disease risk (but see Liu and colleagues [10], who found no significant negative effect of species richness on disease in forest ecosystems). However, our analysis is among the first to capture the variability in how individual pests differ in their response along biodiversity gradients and to demonstrate the modifying effect of the phylogenetic composition of host communities. While, in some systems, host abundance can facilitate the dilution effect independent from taxonomic richness or diversity per se [12,42], our results indicate both host diversity and abundance play a role in limiting pest prevalence. High forest tree diversity and low host abundance likely act in concert to reduce pest prevalence by decreasing encounter rates between pests and hosts, providing more suitable habitat for pest natural enemies, and presenting smaller “targets” for dispersing pests, decreasing the likelihood of pest establishment. These mechanisms, however, are magnified when forest trees are distantly related to pest hosts—consistent with the possibility that a single forest could simultaneously dilute one pest and amplify another.

Our work provides little evidence for an effect of nativity on pest responses to biodiversity, even after adjusting for host breadth and forest community composition. The intrinsic and extrinsic factors affecting pest responses to biodiversity thus appear similar for native and non-native species. We did, however, find that non-native pests had higher prevalence overall compared to native pests. This is perhaps not surprising as hosts of non-native pests often have little coevolved resistance, and non-native pests may have fewer top-down controls (e.g., natural enemies), both of which could allow non-native pests to achieve higher prevalence. The severity of pest impacts on host trees could also affect their relative prevalence. Maladaptive hyper-virulence, for example, whereby pests quickly kill hosts, could theoretically increase pest prevalence in the short term but reduce pest prevalence in the long term, as available living hosts become rarer. While non-native pests may be most likely to be out of adaptive equilibrium with their hosts, there is as yet only limited evidence that they have systematically higher impacts on hosts than native pests [43,44].

Somewhat surprisingly, our expectation that specialist pests would more often tend to be diluted and generalist pests more often amplified by diversity was also not supported. There are various possible explanations for why we did not observe a strong effect of host breadth on dilution. For example, if the dominant tree species in a region are few and closely related, and the pest is a specialist on one or more of these dominant trees, then the addition of a host from the regional species pool is less likely to have a strong diluting effect. In our dataset, the southern pine beetle (SPB, D. frontalis), which specializes mostly on Pinus, provides one such example. Forests in the southern US, where SPB occurs, are dominated by numerous pine species (e.g., Pinus palustris, P. taeda, P. echinata, P. elliottii), all of which are hosts to SPB. A diverse tree community in the southern US, hence, is likely to contain numerous pine species which are all competent hosts for the SPB. Conversely, generalist pests may be diluted by diversity if hosts vary widely in their competence. Phytophthora ramorum, a generalist pathogen and causal agent of Sudden Oak Death, for example, has been shown to be diluted by diversity [45]. Importantly, however, while a dilution effect may be observed at the community level, the probability of particular host species being infected by P. ramorum may be independent of diversity or even show the opposite relationship—being amplified by diversity rather than diluted [46]. This may be the case when a single, highly competent host tree dominates pest dynamics in the community.

In addition to information on host competence, other community-level data could help improve our understanding of pest prevalence. Functional traits have been linked to total pest loads and, when aggregated to the community, could affect the likelihood of pests establishing in a forest. For example, the proportion of fast-growing weedy species, which trade defense for growth, may be more likely to amplify pests compared to forests made up of slow-growing species that invest in various defense strategies—as individual species growth rates may be positively associated with herbivory [47]. Total forest productivity, leaf area, or functional type (angiosperm versus gymnosperm), among other forest characteristics, could each affect forest susceptibility to pest attack. Many such traits are phylogenetically conserved [48], and so could be partially captured by our evolutionary distance metric, but future work identifying landscape-level effects could be particularly informative for understanding pest prevalence and how they may shift with future landscape change.

The importance of the evolutionary distance between hosts and forest composition in mediating the dilution effect supports the notion that not all tree species contribute equally to dilution and helps explain the variability in the strength of dilution observed across pest species. This phylogenetic effect likely reflects phylogenetic conservatism in pest–host associations [49–51] and suggests that the addition of tree species to a community that are close relatives to a pest’s preferred hosts may be more likely to amplify than dilute a pest. These dynamics, however, can be complicated by pests’ lifecycle. Pests that rely on a particular sequence of hosts for successful infection (e.g., heteroecious rusts), or are not transmitted uniformly between hosts (for example, when insect vectors have feeding preferences and vary in their abilities to transmit pathogens [52]), may respond differently to diversity than those pests without strict host requirements. In these cases, pests response to diversity may be more impacted by host co-occurrence and, potentially, their interactions. Such a dynamic would complicate pest management as it implies that increasing diversity within forest stands could reduce the prevalence of some pests, while simultaneously increasing the prevalence of others. Pine-oak rust (C. quercuum) provides one such example as it is often managed by removing oaks around pine plantations in the southern US [53]. This native fungus, which alternates between pines and oaks, cannot complete its life cycle on pines alone, so removing oaks (and leaving only pines) can be an effective management strategy to reduce disease risk on economically important pines. This strategy, however, could increase the risk of pests that specialize on pine and reach their highest prevalence in pine monocultures.

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3002473

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