Scott Chamberlain

Quantitative synthesis of context dependency in ant–plant protection mutualisms

Context dependency, variation in the outcome of species interactions with biotic and abiotic conditions, is increasingly considered ubiquitous among mutualisms. Despite several qualitative reviews of many individual empirical studies, there has been little quantitative synthesis examining the generality of context dependency, or conditions that may promote it. We conducted a meta-analysis of ant-plant protection mutualisms to examine the generality of context-dependent effects of ants on herbivory and plant performance (growth, reproduction). Our results show that ant effects on plants are not generally context dependent, but instead are routinely positive and rarely neutral, as overall effect sizes of ants in reducing herbivory and increasing plant performance were positive and significantly greater than 0. The magnitude of these positive effects did vary, however. Variation in plant performance was not explained by the type of biotic or abiotic factor examined, including plant rewards (extrafloral nectar, food bodies, domatia), ant species richness, plant growth form, or latitude. With the exception of plant growth form, these factors did contribute to the effects of ants in reducing herbivory. Reductions in herbivory were greater for plants with than without domatia, and greatest for plants with both domatia and food bodies. Effect sizes of ants in reducing herbivory decreased, but remained positive, with latitude and ant species richness. Effect sizes in reducing herbivory were greater in tropical vs. temperate systems. Although ant-plant interactions have been pivotal in the study of context dependency of mutualisms, our results, along with other recent meta-analyses, indicate that context dependency may not be a general feature of mutualistic interactions. Rather, ant-plant protection mutualisms appear to be routinely positive for plants, and only occasionally neutral.

How context dependent are species interactions

The net effects of interspecific species interactions on individuals and populations vary in both sign (-, 0, +) and magnitude (strong to weak). Interaction outcomes are context-dependent when the sign and/or magnitude change as a function of the biotic or abiotic context. While context dependency appears to be common, its distribution in nature is poorly described. Here, we used meta-analysis to quantify variation in species interaction outcomes (competition, mutualism, or predation) for 247 published articles. Contrary to our expectations, variation in the magnitude of effect sizes did not differ among species interactions, and while mutualism was most likely to change sign across contexts (and predation least likely), mutualism did not strongly differ from competition. Both the magnitude and sign of species interactions varied the most along spatial and abiotic gradients, and least as a function of the presence/absence of a third species. However, the degree of context dependency across these context types was not consistent among mutualism, competition and predation studies. Surprisingly, study location and ecosystem type varied in the degree of context dependency, with laboratory studies showing the highest variation in outcomes. We urge that studying context dependency per se, rather than focusing only on mean outcomes, can provide a general method for describing patterns of variation in nature.

Does phylogeny matter? Assessing the impact of phylogenetic information in ecological meta‐analysis

Meta-analysis is increasingly used in ecology and evolutionary biology. Yet, in these fields this technique has an important limitation: phylogenetic non-independence exists among taxa, violating the statistical assumptions underlying traditional meta-analytic models. Recently, meta-analytical techniques incorporating phylogenetic information have been developed to address this issue. However, no syntheses have evaluated how often including phylogenetic information changes meta-analytic results. To address this gap, we built phylogenies for and re-analysed 30 published meta-analyses, comparing results for traditional vs. phylogenetic approaches and assessing which characteristics of phylogenies best explained changes in meta-analytic results and relative model fit. Accounting for phylogeny significantly changed estimates of the overall pooled effect size in 47% of datasets for fixed-effects analyses and 7% of datasets for random-effects analyses. Accounting for phylogeny also changed whether those effect sizes were significantly different from zero in 23 and 40% of our datasets (for fixed- and random-effects models, respectively). Across datasets, decreases in pooled effect size magnitudes after incorporating phylogenetic information were associated with larger phylogenies and those with stronger phylogenetic signal. We conclude that incorporating phylogenetic information in ecological meta-analyses is important, and we provide practical recommendations for doing so.

taxize: taxonomic search and retrieval in R

All species are hierarchically related to one another, and we use taxonomic names to label the nodes in this hierarchy. Taxonomic data is becoming increasingly available on the web, but scientists need a way to access it in a programmatic fashion that’s easy and reproducible. We have developed taxize, an open-source software package (freely available from http://cran.r-project.org/web/packages/taxize/index.html) for the R language. taxize provides simple, programmatic access to taxonomic data for 13 data sources around the web. We discuss the need for a taxonomic toolbelt in R, and outline a suite of use cases for which taxize is ideally suited (including a full workflow as an appendix). The taxize package facilitates open and reproducible science by allowing taxonomic data collection to be done in the open-source R platform.

Density-mediated, context-dependent consumer-resource interactions between ants and extrafloral nectar plants.

Interspecific interactions are often mediated by the interplay between resource supply and consumer density. The supply of a resource and a consumers density response to it may in turn yield context-dependent use of other resources. Such consumer-resource interactions occur not only for predator-prey and competitive interactions, but for mutualistic ones as well. For example, consumer-resource interactions between ants and extrafloral nectar (EFN) plants are often mutualistic, as EFN resources attract and reward ants which protect plants from herbivory. Yet, ants also commonly exploit floral resources, leading to antagonistic consumer-resource interactions by disrupting pollination and plant reproduction. EFN resources associated with mutualistic ant-plant interactions may also mediate antagonistic ant-flower interactions through the aggregative density response of ants on plants, which could either exacerbate ant-flower interactions or alternatively satiate and distract ants from floral resources. In this study, we examined how EFN resources mediate the density response of ants on senita cacti in the Sonoran Desert and their context-dependent use of floral resources. Removal of EFN resources reduced the aggregative density of ants on plants, both on hourly and daily time scales. Yet, the increased aggregative ant density on plants with EFN resources decreased rather than increased ant use of floral resources, including contacts with and time spent in flowers. Behavioral assays showed no confounding effect of floral deterrents on ant-flower interactions. Thus, ant use of floral resources depends on the supply of EFN resources, which mediates the potential for both mutualistic and antagonistic interactions by increasing the aggregative density of ants protecting plants, while concurrently distracting ants from floral resources. Nevertheless, only certain years and populations of study showed an increase in plant reproduction through herbivore protection or ant distraction from floral resources. Despite pronounced effects of EFN resources mediating the aggregative density of ants on plants and their context-dependent use of floral resources, consumer-resource interactions remained largely commensalistic.

Do extrafloral nectar resources, species abundances, and body sizes contribute to the structure of ant-plant mutualistic networks?

Recent research has shown that many mutualistic communities display non-random structures. While our understanding of the structural properties of mutualistic communities continues to improve, we know little of the biological variables resulting in them. Mutualistic communities include those formed between ants and extrafloral (EF) nectar-bearing plants. In this study, we examined the contributions of plant and ant abundance, plant and ant size, and plant EF nectar resources to the network structures of nestedness and interaction frequency of ant–plant networks across five sites within one geographic locality in the Sonoran Desert. Interactions between ant and plant species were largely symmetric. That is, ant and plant species exerted nearly equivalent quantitative interaction effects on one another, as measured by their frequency of interaction. The mutualistic ant–plant networks also showed nested patterns of structure, in which there was a central core of generalist ant and plant species interacting with one another and few specialist–specialist interactions. Abundance and plant size and ant body size were the best predictors of symmetric interactions between plants and ants, as well as nestedness. Despite interactions in these communities being ultimately mediated by EF nectar resources, the number of EF nectaries had a relatively weak ability to explain variation in symmetric interactions and nestedness. These results suggest that different mechanisms may contribute to structure of bipartite networks. Moreover, our results for ant–plant mutualistic networks support the general importance of species abundances for the structure of species interactions within biological communities.

Traits and phylogenetic history contribute to network structure across Canadian plant–pollinator communities

Interaction webs, or networks, define how the members of two or more trophic levels interact. However, the traits that mediate network structure have not been widely investigated. Generally, the mechanism that determines plant-pollinator partnerships is thought to involve the matching of a suite of species traits (such as abundance, phenology, morphology) between trophic levels. These traits are often unknown or hard to measure, but may reflect phylogenetic history. We asked whether morphological traits or phylogenetic history were more important in mediating network structure in mutualistic plant-pollinator interaction networks from Western Canada. At the plant species level, sexual system, growth form, and flower symmetry were the most important traits. For example species with radially symmetrical flowers had more connections within their modules (a subset of species that interact more among one another than outside of the module) than species with bilaterally symmetrical flowers. At the pollinator species level, social species had more connections within and among modules. In addition, larger pollinators tended to be more specialized. As traits mediate interactions and have a phylogenetic signal, we found that phylogenetically close species tend to interact with a similar set of species. At the network level, patterns were weak, but we found increasing functional trait and phylogenetic diversity of plants associated with increased weighted nestedness. These results provide evidence that both specific traits and phylogenetic history can contribute to the nature of mutualistic interactions within networks, but they explain less variation between networks.

Pollinators visit related plant species across 29 plant-pollinator networks.

Understanding the evolution of specialization in host plant use by pollinators is often complicated by variability in the ecological context of specialization. Flowering communities offer their pollinators varying numbers and proportions of floral resources, and the uniformity observed in these floral resources is, to some degree, due to shared ancestry. Here, we find that pollinators visit related plant species more so than expected by chance throughout 29 plant–pollinator networks of varying sizes, with “clade specialization” increasing with community size. As predicted, less versatile pollinators showed more clade specialization overall. We then asked whether this clade specialization varied with the ratio of pollinator species to plant species such that pollinators were changing their behavior when there was increased competition (and presumably a forced narrowing of the realized niche) by examining pollinators that were present in at least three of the networks. Surprisingly, we found little evidence that variation in clade specialization is caused by pollinator species changing their behavior in different community contexts, suggesting that clade specialization is observed when pollinators are either restricted in their floral choices due to morphological constraints or innate preferences. The resulting pollinator sharing between closely related plant species could result in selection for greater pollinator specialization.

Rphylip: an R interface for PHYLIP

Summary The phylogeny methods software package PHYLIP has long been among the most widely used packages for phylogeny inference and phylogenetic comparative biology. Numerous methods available in PHYLIP, including several new phylogenetic comparative analyses of considerable importance, are not implemented in any other software. Over the past decade, the popularity of the R statistical computing environment for many different types of phylogenetic analyses has soared, particularly in phylogenetic comparative biology. There are now numerous packages and methods developed for the R environment. In this article, we present Rphylip, a new R interface for the PHYLIP package. Functions of Rphylip interface seamlessly with all of the major analysis functions of the PHYLIP package. This new interface will enable the much easier use of PHYLIP programs in an integrated R workflow. In this study, we describe our motivation for developing Rphylip and present an illustration of how functions in the Rphylip package can be used for phylogenetic analysis in R.

How do plants balance multiple mutualists? Correlations among traits for attracting protective bodyguards and pollinators in cotton (Gossypium)

Many species, both plants and animals, are simultaneously engaged in interactions with multiple mutualists. However, the extent to which separate traits that attract different mutualist guilds display negative or positive relationships remains largely unstudied. We asked whether correlations exist among extrafloral nectary traits to attract arthropod bodyguards and floral traits to attract pollinator mutualists. For 37 species in the cotton genus (Gossypium), we evaluated correlations among six extrafloral nectary traits and four floral traits in a common greenhouse environment, with and without correction for phylogenetic non-independence. Across Gossypium species, greater investment in extrafloral nectary traits was positively correlated with greater investment in floral traits. Positive correlations remained after accounting for the evolutionary history of the clade. Our results demonstrate that traits to maintain multiple mutualist guilds can be positively correlated across related species and build a more general understanding of the constraints on trait evolution in plants.