Protection Mutualisms Research Articles

Emerging Trends in Ant-Pollinator Conflict in Extrafloral Nectary-Bearing Plants.

The net outcomes of mutualisms are mediated by the trade-offs between the costs and benefits provided by both partners. Our review proposes the existence of a trade-off in ant protection mutualisms between the benefits generated by the ants' protection against the attack of herbivores and the losses caused by the disruption of pollination processes, which are commonly not quantified. This trade-off has important implications for understanding the evolution of extrafloral nectaries (EFNs), an adaptation that has repeatedly evolved throughout the flowering plant clade. We propose that the outcome of this trade-off is contingent on the specific traits of the organisms involved. We provide evidence that the protective mutualisms between ants and plants mediated by EFNs have optimal protective ant partners, represented by the optimum point of the balance between positive effects on plant protection and negative effects on pollination process. Our review also provides important details about a potential synergism of EFN functionality; that is, these structures can attract ants to protect against herbivores and/or distract them from flowers so as not to disrupt pollination processes. Finally, we argue that generalizations regarding how ants impact plants should be made with caution since ants' effects on plants vary with the identity of the ant species in their overall net outcome.

The Movement Ecology of Mutualism (CSEE/ESA 2022, OOS17)

The Movement Ecology of Mutualism (<scp>CSEE</scp>/<scp>ESA</scp> 2022, <scp>OOS17</scp>)

Prey–predator dynamics with adaptive protection mutualism

Prey can ease the burden of exploitation by attracting a third party that interferes with their predators. Such is the case for plant-ant or aphid-ant mutualisms, where the victim supplies food to the ants, while the ants attack or drive away the offenders. Since ants are adaptive foragers, defense services can be altered by alternative food sources (e.g., other plants, or human-supplied resource). This article explores the prey-predator-ant system, using a model that combines predator-prey population dynamics with ant optimal foraging, where ants consume prey-supplied resources or alternative resources. Feedbacks between prey-predator dynamics and adaptive ant foraging leads to complex dynamics. For a given ant colony size and supply rate of alternative resources, prey can coexist with predators at alternative stable states, or along alternative limit cycles. Limit cycles extend the scope of defensive mutualism beyond the point where ants would abandon prey in favor of alternative resources under equilibrium conditions. These results highlight the importance of trait-mediated indirect interactions for natural mutualistic–antagonistic systems, and potential outcomes of manipulating ant defense services using baits in the case of agriculture.

Lagged effects of herbivory impact host‐choice but not nymphal survivorship in an ant‐protected treehopper

AbstractTheoretical studies have shown that in protection mutualism, the modification of top‐down control by protectors may be destabilizing. Central to this prediction are the assumptions that (1) protection mutualism increases the abundance of protected partners, (2) this increased abundance generates a lagged effect on partner resources, and (3) spatial dynamics can be ignored. Although a number of studies have confirmed that protection mutualism can increase the abundance of protected herbivores, the evidence for a negative effect of protected herbivores on plant quality is mixed, and we are unaware of any studies that have explored the effect of protected herbivores on plant quality across growing seasons. Here, we use the protection mutualism between ants and the treehopper Publilia concava to evaluate the assumption that treehopper herbivory has a lagged effect on plant quality. We also evaluated whether ant protection exacerbated the negative effect of treehoppers on their host plants. We used a two‐way factorial design that manipulated ant and treehopper presence on goldenrod host plants in 1 year and assessed oviposition and survivorship on those same plants in the subsequent year. Treehopper herbivory was associated with a decrease in the probability of oviposition, and female treehoppers laid significantly fewer egg masses on plants that had been fed on the previous year, regardless of ant tending. In contrast, a prior history of herbivory had no impact on future treehopper performance as measured by nymph survival. Ant tending increased treehopper abundance and exacerbated the risk of plant mortality but otherwise did not significantly modify the negative effect of treehopper herbivory on plant quality or future treehopper performance. Although the increase in treehopper abundance associated with ant tending and the lagged oviposition response of treehoppers is consistent with the core assumptions of a model showing that mutualism can be destabilizing, the avoidance of previously occupied plants for oviposition is not. These results highlight the importance of future modeling studies that explore spatiotemporal dynamics in protection mutualism and long‐term field studies that track the effect of mutualism across years.

Plant species specificity of ant–plant mutualistic interactions: Differential predation of termites by Camponotus crassus on five species of extrafloral nectaries plants

AbstractThere is increasing evidence that the outcomes of mutualistic interactions between ants and plants bearing extrafloral nectaries (EFNs) are context‐dependent. In particular, the total number, density, and size of EFNs, as well as the abundance and identity of ants attending host plants, are considered as key factors determining the nature and strength of ant–EFN‐bearing plant interaction. Although many previous studies have investigated context‐dependency in ant–plant protection mutualisms mediated by EFNs, few have tested whether the protective behavior of ants varies among sympatric plant species. In this study, we performed a field experiment to investigate the predatory behavior of a dominant ant species (Camponotus crassus, Formicinae) among five EFN‐bearing plant species growing in the Brazilian savanna. In particular, we studied the variation in the ant abundance, termite predation, and time spent to find termites of C. crassus among the plant species, and further analyzed whether this variation could be related to the extrafloral nectar volume and sugar concentration of each plant species. We found that abundance and termite predation of C. crassus markedly varied among plant species. Specifically, C. crassus ants were significantly more abundant, active, and protective in Qualea multiflora, the plant species that produced significantly higher volumes and sugar concentrations of nectar. Overall, our results suggest that variation in extrafloral nectar volume and sugar concentration can result in plant species specificity of defensive behavior of a dominant foliage‐dwelling ant in the Brazilian savanna.Abstract in Portuguese is available with online material.

Early snowmelt reduces aphid abundance (Aphis asclepiadis) by creating water-stressed host plants (Ligusticum porteri) and altering interactions with ants

Declining snow cover is reshaping ecological communities. Early loss of snow cover initiates changes in key interactions that mediate herbivore abundance, i.e., top-down and bottom-up effects. In this study, we used a field experiment to test the effects of host plant water stress and phenology on the multitrophic interactions that determine aphid abundance. The aphid, Aphis asclepiadis, in our study system colonizes the flowering stalks of the host plant Ligusticum porteri and relies on a protection mutualism with ants. We added snow and water to replicate host plants and tested for a variety of phenological and physiological responses to these treatments. Relative to host plants in ambient conditions, both water and snow addition reduced key signals of water stress (senescence and abscisic acid levels) and increased seed set. While aphid colonies were generally larger with reduced host plant water stress, the ant–aphid mutualism interacted with plant quality in complex ways. Without ant tending, we did not detect differences in aphid colony growth with host plant treatment. When tended by ants, aphid colony growth was greatest on host plants with snow addition. Host plant quality also altered the benefits exchanged in this mutualism. Ant-tended colonies hosted by plants with snow addition produced honeydew enriched in trehalose, which may have decreased both ant and natural enemy abundance. Our results suggest that early loss of snow reduces aphid abundance by creating low-quality, water-stressed host plants, and this effect may be exacerbated by natural enemies and the costs of ant attendance.

Novel plant–insect interactions in an urban environment: enemies, protectors, and pollinators of invasive knotweeds

AbstractRelationships between invasive plants and other species in their introduced ranges may facilitate or hinder the process of invasion. Fallopia japonica (Japanese knotweed), Fallopia sachalinensis (giant knotweed), and their hybrid Fallopia × bohemica (Bohemian knotweed) are widespread invasive plants in North America and Europe. These species possess extrafloral nectaries (EFNs) that attract mutualist insect protectors in their native ranges. Popillia japonica Newman, 1841 (Japanese beetle) is a primary herbivore of invasive Fallopia spp. in these species’ native range in Japan. These natural enemies are reunited in North America, where Fallopia spp. have been repeatedly introduced as ornamental plantings of residential and commercial properties since the 1800s, and the Japanese beetle has become a widespread insect pest. Spread of Fallopia spp. and their hybrids along linear features of urban landscapes such as roads, railways, and waterways make their performance in urban environments important to these invasive species’ impact. To test the role of insect interactions in the success of Fallopia japonica and F. × bohemica in urban conditions in their invasive range, we examined ant visitation, Japanese beetle abundance and herbivory, ant–Japanese beetle interactions, pollinator visits, and seed production. All active herbivory observed was by Japanese beetles. Leaf area loss to herbivory was much lower than levels reported in Japan, suggesting partial enemy release. New Fallopia leaves were more frequently visited by ants than mature leaves, while Japanese beetle herbivory was observed on mature but not on new leaves. All ant species observed visiting invasive Fallopia EFN were native to North America. Active physical defense by these ants against Japanese beetles was observed but was rare. Native and non‐native insects visited Fallopia flowers, followed by seed production. Our results indicate that both native and non‐native species may facilitate invasion of Fallopia through pollination and protection mutualisms.

Extrafloral nectaries in Leguminosae: phylogenetic distribution, morphological diversity and evolution

Extrafloral nectaries (EFNs) mediating ecologically important ant–plant protection mutualisms are especially common and unusually diverse in the Leguminosae. We present the first comprehensively curated list of legume genera with EFNs, detailing and illustrating their systematic and phylogenetic distributions, locations on the plant, morphology and anatomy, on the basis of a unified classification of EFN categories and a time-calibrated phylogeny, incorporating 710 of the 768 genera. This new synthesis, the first since Mckey (1989)’s seminal paper, increases the number of genera with EFNs to 153 (20% of legumes), distributed across subfamilies Cercidoideae (1), Detarioideae (19), Caesalpinioideae (87) and Papilionoideae (46). EFNs occur at nine locations, and are most prevalent on vegetative plant parts, especially leaves (74%) and inflorescence axes (26%). Four main categories (with eight subcategories) are recognised and include the following: formless, trichomatic (exposed, hollow), parenchymatic (embedded, pit, flat, elevated) and abscission zone EFNs (non-differentiated, swollen scars). Phylogenetic reconstruction of EFNs suggests independent evolutionary trajectories of different EFN types, with elevated EFNs restricted almost exclusively to Caesalpinioideae (where they underwent spectacular morphological disparification), flat EFNs in Detarioideae, swollen scar EFNs in Papilionoideae, and Cercidoideae is the only subfamily bearing intrastipular EFNs. We discuss the complex evolutionary history of EFNs and highlight future research directions.

PROTECTION MUTUALISM: AN OVERVIEW OF ANT-PLANT INTERACTIONS MEDIATED BY EXTRAFLORAL NECTARIES

Ants and plants bearing extrafloral nectaries (EFNs) are among the most abundant interacting organisms in the Neotropics, being considered excellent models for studies of ecological interactions. These mutualisms have been studied for more than 150 years. The first studies on this subject addressed the indirect benefit of the presence of ants on plants, reducing the foliar herbivory in most cases. Recently, the direct and indirect benefits of these interactions for ants and for EFNs-bearing plants survivorship, growth and reproduction, have shown conditionality to spatial and temporal variations. Here, we reviewed how the topic “protection mutualism in ant-plant interactions mediated by EFNs” has been approached more recently. A great number of papers dealing with this theme have been published in the last 30 years and new perspectives have emerged in the last decade. We showed how scientific and academic areas are working to improve the knowledge on protection mutualisms considering ant-plant ecological networks and how they can shape communities. Furthermore, we discuss some aspects related with the EFNs evolutionary hypotheses, the existence of conditionalities in ant-plant protection mutualism mediated by EFNs, and we provide some perspectives to inspire new studies that will help in the understanding of these fascinating ecological interactions.

Progressive sensitivity of trophic levels to warming underlies an elevational gradient in ant–aphid mutualism strength

Although species interactions are often proposed to be stronger at lower latitudes and elevations, few studies have evaluated the mechanisms driving such patterns. In this study, we assessed whether, and by which mechanisms, abiotic changes associated with elevation altered the outcome of an ant–aphid protection mutualism. To do so, we characterized the multi‐trophic interactions among the ant Formica podzolica, the aphid Aphis varians, and aphid natural enemies occurring on the plant Chamerion angustifolium within replicate high and low elevation valleys. Low (versus high) elevation sites had longer summers (snowmelt 13 days earlier) and were on average 1.1°C warmer and 41% drier throughout the year. At low elevations, individual ant colonies consumed approximately double the volume of carbohydrate baits, likely due to a higher foraging tempo, and possibly due to a greater demand for sugar‐ versus protein‐rich resources (as indicated by stable isotope analysis). Wild aphid colonies at low elevations were visited by 1.4‐fold more natural enemies (controlling for variation in aphid abundance), while experimental aphid colonies on potted plants were tended 52% more frequently by ants. As a result, ants increased aphid colony survival by 66% at low elevations but had no detectable effect at high elevations; at low (versus high) elevations aphid colonies without ants had lower survival, demonstrating stronger predator effects, while aphid colonies with ants had higher survival, demonstrating even stronger ant benefits. Analyses for the effects of mean summer temperature yielded qualitatively identical results to those based on elevation. Collectively, these findings support predictions for a greater sensitivity of higher trophic levels to warming and demonstrate how species interactions can vary across environmental gradients due to simultaneous changes in species traits and abundances across multiple trophic levels.

Differences in Aggressive Behaviors between Two Ant Species Determine the Ecological Consequences of a Facultative Food-for-Protection Mutualism

Ant-hemipteran mutualisms are widespread interactions in terrestrial food webs with far-reaching consequences for arthropod communities. Several hypotheses address the behavioral mechanisms driving the impacts of this mutualism, but relatively few studies have considered multiple ant species simultaneously as well as interspecific and intraspecific variation in ant behavior. In a series of field experiments that manipulated ant diet, this work examines the role of induced behaviors of forest ant species actively engaged in mutualism with Hemiptera. Based on other work in ant mutualisms, we predicted a higher frequency of aggressive behaviors towards prey and competitors by ants in the presence of honeydew-producing Hemiptera. We specifically compared Camponotus chromaoides and Formica neogagates (Formicidae), two abundant species in temperate forests of the northeastern U.S.A. After manipulating ant diet and interactions with sap-feeders experimentally, we observed 494 one-on-one interactions between ants and competitors, ladybird beetles and caterpillar prey. We found that C. chromaoides, exhibited behavioral dominance over F. neogagates, and C. chromaoides was more likely to attack ladybird beetles, competing ants, and caterpillar prey. However, contrary to other work in ant-Hemipteran mutualisms, we observed no evidence that food rewards provided by sap-feeders induced changes in ant behavior for either ant species examined. These results reveal the importance of considering interspecific differences in behavior as a mechanism underlying the ecological impacts of ant-Hemipteran protection mutualisms.

La defensa de Passiflora caerulea por hormigas reduce el número de huevos y larvas de Agraulis vanillae, pero no el daño por herbivoría

The system consisting of the plant Passiflora caerulea, the ants that visit its extrafloral nectaries and the larvae of the Gulf fritillary butterfly (Agraulis vanillae) that feed on the plant provides an opportunity to explore the effect of one ecological interaction on another. The objective of this work was to study the effect of the mutualism between the ants and the plant on the antagonism between the butterfly larvae and the plant. The general hypothesis tested was that ants protect the plant from the attack of the larvae exchange for the nectar they receive. An ant exclusion experiment was conducted to explore whether their presence affects the presence of eggs and larvae and the damage they produce. This experiment was carried out at Parque Natural Municipal Ribera Norte (PNMRN), located in the San Isidro party, in the province of Buenos Aires, between September 2011 and March 2012. Five different ant morphotypes were recorded on P. caerulea. According to what was expected, there was a negative effect of the ants on the number of eggs and larvae of A. vanillae. However, the presence of ants did not affect the level of herbivory damage observed. In other words, the protection mutualism had a negative effect on the herbivore attacked (in this case, the butterfly), but did not seem to have the expected positive effect on the defended plant (the Passiflora). This reflects the complexity of tripartite interactions in plant-herbivore-ant systems and the multiple factors that may influence how the species involved are affected. From the point of view of the conservation of biodiversity and its functions in a threatened environment, it is remarkable to have registered the occurrence of these interactions in a small urban nature reserve such as PNMRN.https://doi.org/10.25260/EA.18.28.1.0.635

Influence of neighboring plants on the dynamics of an ant-acacia protection mutualism.

Ant-plant protection symbioses, in which plants provide food and/or shelter for ants in exchange for protection from herbivory, are model systems for understanding the ecology of mutualism. While interactions between ants, host plants, and herbivores have been intensively studied, we know little about how plant-plant interactions influence the dynamics of these mutualisms, despite strong evidence that plants compete for resources, that hosting ants can be costly, and that host-plant provisioning to ants can therefore be constrained by resource availability. We used field experiments in a semiarid Kenyan savanna to examine interactions between the ant-plant Acacia drepanolobium, neighboring grasses, and two species of symbiotic acacia-ants with divergent behaviors: Crematogaster mimosae, an aggressive symbiont that imposes high costs to host trees via consumption of extrafloral nectar, and Tetraponera penzigi, a less-protective symbiont that imposes lower costs because it does not consume nectar. We hypothesized that by competing with acacias for resources, neighboring grasses (1) reduce hosts' ability to support costly C.mimosae, while having little or no effect on the ability of hosts to support low-cost T.penzigi, and (2) reduce sapling growth rates irrespective of ant occupant. We factorially manipulated the presence/absence of grasses and the identity of ant occupants on saplings and evaluated effects on colony survivorship and sapling growth rates over 40weeks. Contrary to prediction, the high-cost/high-reward nectar-dependent mutualist C.mimosae had higher colony-survival rates on saplings with grass neighbors present. Grasses appear to have indirectly facilitated the survival of C.mimosae by reducing water stress on host plants; soils under saplings shaded by grasses had higher moisture content, and these saplings produced more active nectaries than grass-removal saplings. Consistent with prediction, survival of low-cost/low-reward T.penzigi did not differ significantly between grass-removal treatments. Saplings occupied by low-cost/low-reward T.penzigi grew 100% more on average than saplings occupied by high-cost/high-reward C.mimosae, demonstrating that mutualist-partner identity strongly and differentially influences demographic rates of young plants. In contrast, contrary to prediction, grass neighbors had no significant net impact on sapling growth rates. Our results suggest that neighboring plants can exert strong and counterintuitive effects on ant-plant protection symbioses, highlighting the need to integrate plant-plant interactions into our understanding of these mutualisms.

Network reorganization and breakdown of an ant-plant protection mutualism with elevation.

Both the abiotic environment and the composition of animal and plant communities change with elevation. For mutualistic species, these changes are expected to result in altered partner availability, and shifts in context-dependent benefits for partners. To test these predictions, we assessed the network structure of terrestrial ant-plant mutualists and how the benefits to plants of ant inhabitation changed with elevation in tropical forest in Papua New Guinea. At higher elevations, ant-plants were rarer, species richness of both ants and plants decreased, and the average ant or plant species interacted with fewer partners. However, networks became increasingly connected and less specialized, more than could be accounted for by reductions in ant-plant abundance. On the most common ant-plant, ants recruited less and spent less time attacking a surrogate herbivore at higher elevations, and herbivory damage increased. These changes were driven by turnover of ant species rather than by within-species shifts in protective behaviour. We speculate that reduced partner availability at higher elevations results in less specialized networks, while lower temperatures mean that even for ant-inhabited plants, benefits are reduced. Under increased abiotic stress, mutualistic networks can break down, owing to a combination of lower population sizes, and a reduction in context-dependent mutualistic benefits.

Large herbivores promote habitat specialization and beta diversity of African savanna trees.

Edaphic variation in plant community composition is widespread, yet its underlying mechanisms are rarely understood and often assumed to be physiological. In East African savannas, Acacia tree species segregate sharply across soils of differing parent material: the ant-defended whistling thorn, A.drepanolobium (ACDR), is monodominant on cracking clay vertisols that are nutrient rich but physically stressful, whereas poorly defended species such as A.brevispica (ACBR) dominate on nutrient-poor but otherwise less-stressful sandy loams. Using a series of field experiments, we show that large-mammal herbivory interacts with soil properties to maintain this pattern. In the absence of large herbivores, transplanted saplings of both species established on both soil types. Browsers strongly suppressed survival and growth of ACDR saplings on sandy soil, where resource limitation constrained defensive investment. On clay soil, ACBR saplings established regardless of herbivory regime, but elephants prevented recruitment to maturity, apparently because trees could not tolerate the combination of biotic and abiotic stressors. Hence, each tree species was filtered out of one habitat by browsing in conjunction with different edaphic factors and at different ontogenetic stages. Browser abundance was greater on sandy soil, where trees were less defended, consistent with predicted feedbacks between plant community assembly and herbivore distributions. By exploring two inversely related axes of soil "quality" (abiotic stress and nutrient content), our study extends the range of mechanisms by which herbivores are known to promote edaphic specialization, illustrates how the high cost of a protection mutualism can constrain the realized niche of host trees, and shows that large-scale properties of savanna ecosystems are shaped by species interactions in cryptic ways that mimic simple abiotic determinism. These results suggest that ongoing declines in large-herbivore populations may relax spatial heterogeneity in plant assemblages and reduce the beta diversity of communities.

Macronutrient Exchange Between the Asian Weaver Ant Oecophylla smaragdina and Their Host Plant

Ant–plant interactions have mainly been considered as a protection mutualism where ants increase plant performance through protection from herbivory. However, host plants may also benefit from nutrients deposited by ants. Nitrogen limits the plant growth in most terrestrial ecosystems and the nutrient exchange between ants and plants may be an important mechanism operating in ant–plant interactions. In this study, we quantified the exchange of macronutrients (carbon and nitrogen) between ants and plants, using the Asian weaver ant Oecophylla smaragdina as a model species in a mango agroecosystem. A method was developed with which the amount of nitrogen retrieved to their host trees could be predicted by the trail density of O. smaragdina. Ant nutrient consumption was calculated based on data on O. smaragdina abundance and per capita consumption rates obtained in laboratory colonies. On a yearly basis, the influx of nitrogen to the host tree, originating from captured prey, averaged 14.4 (range 8.0–46.4) kg N ha−1 y−1. The loss of carbon from the host tree due to ant consumption of exudates from nectaries and tended homopterans averaged 278.1 (range 149.3–939.9) kg C ha−1 y−1. O. smaragdina may provide their host plant with a significant source of nitrogen albeit a substantial amount of carbon is consumed from the host plant. This study reveals that the flow of nutrients between ants and plants may play a critical and underestimated role in ant–plant mutualisms.

Abiotic mediation of a mutualism drives herbivore abundance.

Species abundance is typically determined by the abiotic environment, but the extent to which such effects occur through the mediation of biotic interactions, including mutualisms, is unknown. We explored how light environment (open meadow vs. shaded understory) mediates the abundance and ant tending of the aphid Aphis helianthi feeding on the herb Ligusticum porteri. Yearly surveys consistently found aphids to be more than 17-fold more abundant on open meadow plants than on shaded understory plants. Manipulations demonstrated that this abundance pattern was not due to the direct effects of light environment on aphid performance, or indirectly through host plant quality or the effects of predators. Instead, open meadows had higher ant abundance and per capita rates of aphid tending and, accordingly, ants increased aphid population growth in meadow but not understory environments. The abiotic environment thus drives the abundance of this herbivore exclusively through the mediation of a protection mutualism.

Inherent demographic stability in mutualist-resource-exploiter interactions.

Core principles of ecological theory predict that, in the absence of other factors, mutualisms should experience destabilizing positive feedback and should be vulnerable to extinction through competitive exclusion by exploiter species. Many effective stabilizing mechanisms address one issue or the other, and many turn upon additional features. Using an explicitly demographic approach, I show that indirect, demography-mediated interactions between mutualists and exploiters can enable mutualist-exploiter coexistence, which in turn can stabilize the abundances of mutualists, exploiters, and their shared resources. This occurs because of the distinct resource demographic responses that are inherent to interaction with mutualistic and exploitative partners and can occur in long-lasting, exclusive interactions, such as protection mutualisms, as well as in apparently very different, short-lived mutualistic interactions, such as pollination. The key necessary factor-demographic response to interspecific interaction-is common in nature. Some demographic structure is also necessary and is generated through interspecific interaction in long-lasting associations; it is also very common in natural populations. Thus, the explicitly demographic and multispecies approach taken here constitutes a potentially promising single explanation for the apparent stability of mutualism in a wide range of natural systems.

Dynamic extrafloral nectar production: the timing of leaf damage affects the defensive response in Senna mexicana var. chapmanii (Fabaceae).

• Extrafloral nectar (EFN) mediates food for protection mutualisms between plants and defensive insects. Understanding sources of variation in EFN production is important because such variations may affect the number and identity of visitors and the effectiveness of plant defense. We investigated the influence of plant developmental stage, time of day, leaf age, and leaf damage on EFN production in Senna mexicana var. chapmanii. The observed patterns of variation in EFN production were compared with those predicted by optimal defense theory.• Greenhouse experiments with potted plants were conducted to determine how plant age, time of day, and leaf damage affected EFN production. A subsequent field study was conducted to determine how leaf damage, and the resulting increase in EFN production, affected ant visitation in S. chapmanii.• More nectar was produced at night and by older plants. Leaf damage resulted in increased EFN production, and the magnitude of the response was greater in plants damaged in the morning than those damaged at night. Damage to young leaves elicited a stronger defensive response than damage to older leaves, in line with optimal defense theory. Damage to the leaves of S. chapmanii also resulted in significantly higher ant visitation in the field.• Extrafloral nectar is an inducible defense in S. chapmanii. Developmental variations in its production support the growth differentiation balance hypothesis, while within-plant variations and damage responses support optimal defense theory.

Thermal tolerance affects mutualist attendance in an ant-plant protection mutualism.

Mutualism is an often complex interaction among multiple species, each of which may respond differently to abiotic conditions. The effects of temperature on the formation, dissolution, and success of these and other species interactions remain poorly understood. We studied the thermal ecology of the mutualism between the cactus Ferocactus wislizeni and its ant defenders (Forelius pruinosus, Crematogaster opuntiae, Solenopsis aurea, and Solenopsis xyloni) in the Sonoran Desert, USA. The ants are attracted to extrafloral nectar produced by the plants and, in exchange, protect the plants from herbivores; there is a hierarchy of mutualist effectiveness based on aggression toward herbivores. We determined the relationship between temperature and ant activity on plants, the thermal tolerance of each ant species, and ant activity in relation to the thermal environment of plants. Temperature played a role in determining which species interact as mutualists. Three of the four ant species abandoned the plants during the hottest part of the day (up to 40 °C), returning when surface temperature began to decrease in the afternoon. The least effective ant mutualist, F. pruinosus, had a significantly higher critical thermal maximum than the other three species, was active across the entire range of plant surface temperatures observed (13.8-57.0 °C), and visited plants that reached the highest temperatures. F. pruinosus occupied some plants full-time and invaded plants occupied by more dominant species when those species were thermally excluded. Combining data on thermal tolerance and mutualist effectiveness provides a potentially powerful tool for predicting the effects of temperature on mutualisms and mutualistic species.