Deconstruction of a plant‐arthropod community reveals influential plant traits with nonlinear effects on arthropod assemblages

Abstract

Studies of herbivores and secondary consumer communities rarely incorporate a comprehensive characterization of primary producer trait variation, thus limiting our understanding of how plants mediate community assembly of consumers. We took advantage of recent technological developments for efficient generation of phytochemical, microbial and genomic data to characterize individual alfalfa plants (Medicago sativa; Fabaceae) growing in an old‐field, semi‐naturalized state for 770 traits (including 753 chemical features). Using random forest modelling, we investigated the effect of variation in these traits on arthropod and fungal assemblages while accounting for plant genetic structure. We found that traits indicative of plant vigour, including size, percentage of flowering stems and leaf area, were positively associated with arthropod richness and abundance. Most phytochemicals were, by comparison, poor predictors, although phytochemical diversity and several individual phenolic compounds were important. Plants with a higher proportion of flowering stems were hotspots of intertrophic interactions with higher species richness of secondary consumers. The effects of many traits on plant‐associated assemblages were best modelled as nonlinear functions, often incorporating threshold effects. Foliar fungal richness was not well predicted by our models, suggesting we have much to learn regarding the role of plant traits on phyllosphere fungi at small spatial scales. Our results support the need for characterization of multiple axes of plant phenotypes in studies of plant‐arthropod‐microbe communities and demonstrate the value of modern analytical techniques for understanding the nonlinear ways in which plant traits mediate the structure of associated biotic communities. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13060/suppinfo is available for this article.

Linking plant genes to insect communities: Identifying the genetic bases of plant traits and community composition

“…Here, we identified ten new Populus genes that structured associated insect communities, complementing the previously identified list of QTL from Bernhardsson et al () (12 SNPs, 2013) and Dewoody et al () (14 QTL, 2014). Our findings also reveal that ecologically relevant plant traits structure gene–insect associations, highlighting the importance of these traits as the mechanistic bridge between plant genes and insect communities (Barbour et al, ; Barker et al, ; Harrison et al, ; Robinson et al, ).…”

“…SNPs; McKown et al, 2014, Du et al, 2016, Hallingbäck et al, 2016, Fahrenkrog et al., 2017. Several recent studies of Populus have employed greater coverage, but only examined individual tree traits Our findings also reveal that ecologically relevant plant traits structure gene-insect associations, highlighting the importance of these traits as the mechanistic bridge between plant genes and insect communities (Barbour et al, 2015;Barker et al, 2018;Harrison et al, 2018;Robinson et al, 2012).…”

Caterpillars on a phytochemical landscape: the case of alfalfa and the Melissa blue butterfly

“…Of course, most plants do not have the luxury of optimizing defense against a single herbivore, and it is easy to imagine that improvements in defense against one enemy could lead to increased attraction to another, especially given the diversity of effects even within major classes studied here, including saponins and phenolic glycosides. Compounds in the latter class (phenolics) were found to have strong positive and negative effects on assemblages of arthropods associated with the maternal plants from which seeds were collected to start the common garden used in the present study (Harrison et al , 2018).…”

“…Plants used in this project were grown at the University of Nevada, Reno, Main Station experimental farm. The common garden was planted in 2016 with seeds collected the previous year from 45 plants (previously studied by Harrison et al (Harrison et al , 2018)) growing in a fallow field in north-western Nevada on the western edge of the Great Basin Desert. The focal butterfly, L. melissa , was present in the source field but has not yet colonized the university farm where experimental plants were grown.…”

“…Before grinding, five dried leaflets from each sample were weighed to the nearest 0.1 mg, scanned, and area was measured using ImageJ (v.1.52a); specific leaf area (SLA) was calculated as leaf area divided by dry mass. Finally, leaf toughness was measured on fresh material in the common garden, at the start of the experiment (mid-July, when leaves were also sampled for chemistry and protein) and at the end of the experiment (mid-August), from three leaves per plant at each date, with a penetrometer (Chatillon 516 Series) through the center of the middle leaflet, as in (Harrison et al , 2018); the three leaves were selected haphazardly, avoiding the oldest and youngest leaves. The six leaf toughness measurements per plant were averaged for a single toughness measure used in analyses.…”