J. Nathaniel Holland

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.

Population Dynamics and Mutualism: Functional Responses of Benefits and Costs

We develop an approach for studying population dynamics resulting from mutualism by employing functional responses based on density‐dependent benefits and costs. These functional responses express how the population growth rate of a mutualist is modified by the density of its partner. We present several possible dependencies of gross benefits and costs, and hence net effects, to a mutualist as functions of the density of its partner. Net effects to mutualists are likely a monotonically saturating or unimodal function of the density of their partner. We show that fundamental differences in the growth, limitation, and dynamics of a population can occur when net effects to that population change linearly, unimodally, or in a saturating fashion. We use the mutualism between senita cactus and its pollinating seed‐eating moth as an example to show the influence of different benefit and cost functional responses on population dynamics and stability of mutualisms. We investigated two mechanisms that may alter this mutualisms functional responses: distribution of eggs among flowers and fruit abortion. Differences in how benefits and costs vary with density can alter the stability of this mutualism. In particular, fruit abortion may allow for a stable equilibrium where none could otherwise exist.

A consumer–resource approach to the density-dependent population dynamics of mutualism

Like predation and competition, mutualism is now recognized as a consumer-resource (C-R) interaction, including, in particular, bi-directional (e.g., coral, plant-mycorrhizae) and uni-directional (e.g., ant-plant defense, plant-pollinator) C-R mutualisms. Here, we develop general theory for the density-dependent population dynamics of mutualism based on the C-R mechanism of interspecific interaction. To test the influence of C-R interactions on the dynamics and stability of bi- and uni-directional C-R mutualisms, we developed simple models that link consumer functional response of one mutualistic species with the resources supplied by another. Phase-plane analyses show that the ecological dynamics of C-R mutualisms are stable in general. Most transient behavior leads to an equilibrium of mutualistic coexistence, at which both species densities are greater than in the absence of interactions. However, due to the basic nature of C-R interactions, certain density-dependent conditions can lead to C-R dynamics characteristic of predator-prey interactions, in which one species overexploits and causes the other to go extinct. Consistent with empirical phenomena, these results suggest that the C-R interaction can provide a broad mechanism for understanding density-dependent population dynamics of mutualism. By unifying predation, competition, and mutualism under the common ecological framework of consumer-resource theory, we may also gain a better understanding of the universal features of interspecific interactions in general.

Evolutionary stability of mutualism: interspecific population regulation as an evolutionarily stable strategy.

Interspecific mutualisms are often vulnerable to instability because low benefit : cost ratios can rapidly lead to extinction or to the conversion of mutualism to parasite–host or predator–prey interactions. We hypothesize that the evolutionary stability of mutualism can depend on how benefits and costs to one mutualist vary with the population density of its partner, and that stability can be maintained if a mutualist can influence demographic rates and regulate the population density of its partner. We test this hypothesis in a model of mutualism with key features of senita cactus (Pachycereus schottii) – senita moth (Upiga virescens) interactions, in which benefits of pollination and costs of larval seed consumption to plant fitness depend on pollinator density. We show that plants can maximize their fitness by allocating resources to the production of excess flowers at the expense of fruit. Fruit abortion resulting from excess flower production reduces pre–adult survival of the pollinating seed–consumer, and maintains its density beneath a threshold that would destabilize the mutualism. Such a strategy of excess flower production and fruit abortion is convergent and evolutionarily stable against invasion by cheater plants that produce few flowers and abort few to no fruit. This novel mechanism of achieving evolutionarily stable mutualism, namely interspecific population regulation, is qualitatively different from other mechanisms invoking partner choice or selective rewards, and may be a general process that helps to preserve mutualistic interactions in nature.

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.

Abiotic factors shape temporal variation in the structure of an ant-plant network

Despite recognition of key biotic processes in shaping the structure of biological communities, few empirical studies have explored the influences of abiotic factors on the structural properties of mutualistic networks. We tested whether temperature and precipitation contribute to temporal variation in the nestedness of mutualistic ant–plant networks. While maintaining their nested structure, nestedness increased with mean monthly precipitation and, particularly, with monthly temperature. Moreover, some species changed their role in network structure, shifting from peripheral to core species within the nested network. We could summarize that abiotic factors affect plant species in the vegetation (e.g., phenology), meaning presence/absence of food sources, consequently an increase/decrease of associations with ants, and finally, these variations to fluctuations in nestedness. While biotic factors are certainly important, greater attention needs to be given to abiotic factors as underlying determinants of the structures of ecological networks.

Comment on “Asymmetric Coevolutionary Networks Facilitate Biodiversity Maintenance”

Bascompte et al. (Reports, 21 April 2006, p. 431) used network asymmetries to explain mathematical conditions necessary for stability in historic models of mutualism. The Lotka-Volterra equations they used artificially created conditions in which some factor, such as asymmetric interaction strengths, is necessary for community coexistence. We show that a more realistic model incorporating nonlinear functional responses requires no such condition and is consistent with their data.

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.

EFFECTS OF POLLEN LOAD AND DONOR DIVERSITY ON SEED AND FRUIT MASS IN THE COLUMNAR CACTUS, PACHYCEREUS SCHOTTII (CACTACEAE)

As seed and fruit size can influence the success of later life history stages, it is important to understand their sources of variation. In this study, we examined the effects of pollen load and donor diversity on variation in seed and fruit mass of outcrossing senita cacti (Pachycereus schottii) in the Sonoran Desert. By massing all individual seeds per fruit from pollen supplementation and donor diversity experiments, we were able to examine their effects on seed and fruit mass, compared with intra‐ and interplant variation. Seed and fruit mass showed up to 13‐ and 15‐fold variations, respectively. Pollen load did statistically increase seed and fruit mass, but it explained <6% of their variation. Pollen donor diversity did not affect seed or fruit mass. Variation in seed and fruit mass was explained by interplant variation (19%), intraplant variation among fruits (30%), and intrafruit variation (50%). These results indicate that intra‐ and interplant sources, excluding pollen load and donor diversity but possibly including environmental, architectural, and maternal effects, contribute to the substantial variation observed in seed and fruit mass of senita cacti. Such variation may prove useful for plant recruitment under the highly variable water‐ and nutrient‐stressed conditions of desert environments.

Life Cycle and Growth of Senita Moths (Lepidoptera: Pyralidae): a Lepidopteran with Less than Four Instars?

Abstract Despite great variation in instar number among Insecta, no Lepidopteran has been observed to have less than four larval instars. I report in this work on the life cycle and growth of the senita moth, Upiga virescens Hulst, which forms an obligate pollinating predispersal seed-eating mutualism with senita cacti (Lophocereus schottii Engelmann) in the Sonoran Desert of North America. From 1996 to 1999, I studied larval growth and life cycle associations of U. virescens with L. schottii in the field by labeling cohorts of eggs laid in flowers and following them through pupation. All life stages of U. virescens were associated with flowers, fruit, or cactus stems of L. schottii. Among the five cohorts studied, larval growth consistently conformed to Dyar’s rule. Only three larval instars were identified among the >500 larvae for which head capsule widths were measured. I discuss and dismiss the feasibility of a fourth undetected instar. I then discuss selection pressures that may have contributed to the evolutionary loss of an instar, including a time and/or size constraint on larval growth, as well as the nutritional quantity and quality of larval food.