Evaluating the impacts of multiple generalist fungal pathogens on temperate tree seedling survival

Abstract

Host-specific mortality driven by natural enemies is a widely discussed mechanism for explaining plant diversity. In principle, populations of plant species can be regulated by distinct host-specific natural enemies that have weak or nonexistent effects on heterospecific competitors, preventing any single species from becoming dominant and thus promoting diversity. Two of the first steps in exploring the role of natural enemies in diversity regulation are to (1) identify potential enemies and (2) evaluate their levels of host specificity by determining if interactions between any one host and its enemy have equivalent survival impacts on co-occurring host species. We developed a bioinformatics framework to evaluate impacts of potential pathogens on seedling survival, for both single and multiple infections. Importantly, we consider scenarios not only if there are specialist pathogens for each plant, but also when generalist pathogens have differential effects on multiple host species, and when co-infection has species-specific effects. We then applied this analytical framework to a field experiment using molecular techniques to detect potential fungal pathogens on co-occurring tree seedling hosts. Combinatorial complexity created by 160 plant-fungus interactions was reduced to eight combinations that affect seedling survival. Potential fungal pathogens had broad host ranges, but seedling species were each regulated by different combinations of fungi or by generalist fungi that had differential effects on multiple plant species. Soil moisture can have the potential to shift the nature of the interactions in some plant-fungal combinations from neutral to detrimental. Reassessing the assumption of single-enemy-single-host interactions broadens the mechanisms through which natural enemies can influence plant diversity.

Linking ecology and plant pathology to unravel the importance of soil-borne fungal pathogens in species-rich grasslands

“…Paraphoma chrysanthemicola on Leucanthemum), or generalist pathogens that have differential effects on multiple host species (e.g. many dicots: Verticillium dahliae, Rhizoctonia solani) (Hersh et al 2012).…”

“…Once these baselines have been set, we need to move to other experimental approaches that reveal the more complex interactions between multiple plant species and different fungal pathogens (e.g. Hersh et al 2012). Also the role of other players in the root microbiome can be incorporated (Mendes et al 2011;Berendsen et al 2018).…”

Phylogenetic congruence between subtropical trees and their associated fungi

“…Multihost fungi vary in host specificity and ecological function depending on both host and environmental condition (Hersh et al., 2012), which makes it difficult to evaluate the impacts of many possible combinations of fungi. Hence, host performance measures, including survival, growth, and reproduction, are commonly used as integrated measures of functional host specificity for the whole fungal community and to represent outcomes of complex plant–fungal interactions (Bever, 1994; Klironomos, 2002; Liu et al., 2012; Mangan et al., 2010).…”

Soil-borne pathogens restrict the recruitment of a subtropical tree: a distance-dependent effect

“…Soil-borne fungal pathogens have been shown to cause density-and/or distance-dependent seedling mortality in tropical forests of central America (Augspurger 1983b(Augspurger , 1984Augspurger and Kelly 1984;Bagchi et al 2010Bagchi et al , 2014Bell et al 2006;Gilbert 2002;Hood et al 2004;Mangan et al 2010), in temperate forests (Hersh et al 2012;Packer and Clay 2000;Reinhart and Clay 2009;Reinhart et al 2003Reinhart et al , 2012, as well as in a subtropical forest (Liu et al 2012a, b). Moreover, it has been suggested that negative plant-soil feedback, likely driven by soilborne pathogens, can regulate variation in the relative abundances of plant species (Klironomos 2002;Mangan et al 2010;McCarthy-Neumann and Ibanez 2013;Bagchi et al 2014).…”