Protective Ants Research Articles

Sequential Defense Strategies: From Ant Recruitment to Leaf Toughness.

Plants express many types of defenses in response to herbivory damage. These defenses can be displayed as a sequence or they can overlap, increasing efficiency in protection. However, leaf defense shifts during leaf development, including extrafloral nectaries (EFNs), are neglected in natural tropical systems. To address this gap, our study evaluates the shifts in defense strategies of Eriotheca gracilipes, focusing on extrafloral nectaries and leaf toughness across leaf development stages. We also simulate herbivory by cutting the leaves to address the role of visiting ants against herbivores. We observed that E. gracilipes exhibits a defense turnover, shifting from indirect defenses (e.g., EFNs) in young leaves to physical defenses in adult leaves. Simulated herbivory led to heightened ant visitation, which correlated with decreased herbivory rates, indicating that ant recruitment acts as an effective deterrent. We observed a peak of EFN activity in young leaves, increased foliar toughness in adult leaves, and reduced herbivory on ant-patrolled young leaves. Additionally, E. gracilipes demonstrated tolerance to up to 10% foliar loss with no significant impact on leaf asymmetry, although 50% foliar loss increased asymmetry in newly flushed leaves. These results highlight E. gracilipes' adaptive flexibility by attracting protective ants when vulnerable and enhancing structural defenses as leaves develops, E. gracilipes minimizes herbivory impact. This study provides valuable insight into the adaptive roles of EFNs and tolerance in E. gracilipes, contributing to a broader understanding of plant defense strategies.

Ant sharing by plant species bearing extrafloral nectaries has a low impact on plant herbivory in a tropical system

Abstract Plant species bearing extrafloral nectaries (EFNs) may indirectly influence other plant species by sharing protective ants, potentially altering herbivory levels. However, the propagation of indirect effects in this type of mutualism has seldom been investigated. We investigated indirect effects via ant sharing among 21 EFN‐bearing plant species of the tribe Bignonieae distributed on 28 plots in the central Brazilian Amazon. We used an ecological network index to quantify potential indirect effects among plant species through shared dominant and subordinate ant species. Plant species that were more attractive to ants (promoter species) had the highest potential to indirectly influence ant visitation to less attractive plant species (receptor species) in the community, primarily through changes in the attraction of dominant ant species. However, these potential indirect effects did not result in significant differences in herbivory patterns among the studied plants. Ant attendance and herbivory levels were similar among promoter species, neighbouring plants, and non‐neighbouring plants. Unlike other mutualisms involving plants (e.g., pollination), the indirect effects among plant species that share protective ants had limited consequences. The low levels of herbivory and the small foraging areas of shared ant defenders could be responsible for the observed limited impact of indirect interactions among plant species in this system. Synthesis: This study demonstrates that plant species with EFNs can indirectly influence other plant species through ant sharing. The attractiveness of certain plants to ants enables them to affect the ant visitation patterns of less attractive plants in the community. However, these indirect effects did not significantly alter herbivory levels among plants. Overall, this study advances ecological understanding by showing that the sharing of protective ants among plant species can in some cases confer limited costs and benefits, leading indirect interactions to have minimal impact on herbivory patterns.

Excessive nutrient input induces an ecological cost for aphids by modifying their attractiveness towards mutualist ants

Abstract Enhanced soil nutrient availability often favours herbivore performance by bringing the carbon:nutrient ratio of plants closer to herbivore requirements. However, a surplus of nutrients can promote a too low carbon:nutrient ratio in plants, making them of poor quality for herbivores. In addition, increased soil nutrients can trigger cascading effects altering higher trophic levels, resulting in indirect costs for herbivores. Through experiments under three increasing fertilization levels (unfertilized, NPK‐rich, and 2NPK‐rich soils), we studied how the enhancement of soil nutrient availability, by modifying the C:N ratio of thistles, affects the performance and homeostatic response of the aphids, and the consequent ant attraction. Fertilized soils increased the biomass and reduced the C:N ratio of thistles, also increasing aphid abundance. The stoichiometric homeostasis of aphids was modulated through changes in honeydew production and composition; fertilization treatments reduced by more than half the quantity of honeydew secreted and lead to 2.5–6.4 times higher honeydew N concentration compared with the unfertilized treatment. In addition, in the highest fertilization treatment, the aphids increased the content of uric acid (a waste toxic compound involved in amino acid deamination) excreted in their honeydew. Aphid‐infested thistles had the highest number of aphid‐tending ants when they grew on intermediate rich‐substrates. Ants selected honeydew with a lower C:N ratio (compared to unfertilized plants), but fewer workers patrolled plants with the highest fertilization treatment likely due to increased uric acid in the honeydew. We showed that enhanced soil nutrients brought plant C:N ratio closer to aphid requirements, enhancing their performance and promoting ant attendance. But a disproportionate increase in fertilization did not further improve aphid performance while it decreases the attraction of protective ants, which would make aphid populations more vulnerable to attack by natural enemies, inducing an ecological cost. This study highlights the complex role of bottom‐up cascading effects triggered by increases in soil nutrient availability and the importance of evaluating not only the physiological and population cost and benefits of it but also the ecological ones; especially when it alters mutualistic interactions. Read the free Plain Language Summary for this article on the Journal blog.

Safe sex: ant defense does not interfere with pollination in passion flowers

Ant defense against floral enemies incurs a two-fold ant-pollinator conflict, both via pollinator deterrence and nectar or pollen collection by non-pollinating protective ants. Some ant-plants have physical barriers whereas others produce ant-repellent chemicals to avoid ant visitation to flowers and subsequent pollination interference. Passiflora coccinea is a hummingbird-pollinated myrmecophilous plant in which floral enemy repellence occurs without limiting ant access to open flowers. To test the hypothesis that ant activity is restricted within flowers to prevent contact with anthers, we compared ant defense response between reproductive (anthers and stigmas) and non-reproductive (bracts, corona and perianth) floral structures by combining an observational survey with an experimental approach. A few insect species were found to visit flowers without providing pollination service, mostly pollen-collecting bees and nectar-thieving butterflies landing on petals. Ants always attacked floral visitors that landed on non-reproductive structures, but they never attacked insects visiting reproductive structures as ants never accessed anthers. Our results suggest that the differential ant defense response is an adaptative process to prevent ant-pollinator conflict. The eventual mechanism that regulates this process could be closely linked to the corona of filaments that protects nectar chambers, simultaneously restricting ant access to nectar and pollen.

Indirect effects drive coevolution in mutualistic networks

Ecological interactions have been acknowledged to play a key role in shaping biodiversity. Yet a major challenge for evolutionary biology is to understand the role of ecological interactions in shaping trait evolution when progressing from pairs of interacting species to multispecies interaction networks. Here we introduce an approach that integrates coevolutionary dynamics and network structure. Our results show that non-interacting species can be as important as directly interacting species in shaping coevolution within mutualistic assemblages. The contribution of indirect effects differs among types of mutualism. Indirect effects are more likely to predominate in nested, species-rich networks formed by multiple-partner mutualisms, such as pollination or seed dispersal by animals, than in small and modular networks formed by intimate mutualisms, such as those between host plants and their protective ants. Coevolutionary pathways of indirect effects favour ongoing trait evolution by promoting slow but continuous reorganization of the adaptive landscape of mutualistic partners under changing environments. Our results show that coevolution can be a major process shaping species traits throughout ecological networks. These findings expand our understanding of how evolution driven by interactions occurs through the interplay of selection pressures moving along multiple direct and indirect pathways.

Mutualism exploitation: predatory drosophilid larvae sugar-trap ants and jeopardize facultative ant-plant mutualism.

An open question in the evolutionary ecology of ant-plant facultative mutualism is how other members of the associated community can affect the interaction to a point where reciprocal benefits are disrupted. While visiting Qualea grandiflora shrubs to collect sugary rewards at extrafloral nectaries, tropical savanna ants deter herbivores and reduce leaf damage. Here we show that larvae of the fly Rhinoleucophenga myrmecophaga, which develop on extrafloral nectaries, lure potentially mutualistic, nectar-feeding ants and prey on them. Foraging ants spend less time on fly-infested foliage. Field experiments showed that predation (or the threat of predation) on ants by fly larvae produces cascading effects through three trophic levels, resulting in fewer protective ants on leaves, increased numbers of chewing herbivores, and greater leaf damage. These results reveal an undocumented mode of mutualism exploitation by an opportunistic predator at a plant-provided food source, jeopardizing ant-derived protection services to the plant. Our study documents a rather unusual case of predation of adult ants by a dipteran species and demonstrates a top-down trophic cascade within a generalized ant-plant mutualism.

Multitasking in a plant-ant interaction: how does Acacia myrtifolia manage both ants and pollinators?

Plant associations with protective ants are widespread among angiosperms, but carry the risk that ants will deter pollinators as well as herbivores. Such conflict, and adaptations to ameliorate or prevent the conflict, have been documented in African and neotropical acacias. Ant-acacia associations occur in Australia, but little is known of their ecology. Moreover, recent phylogenetic evidence indicates that Australian acacias are only distantly related to African and American acacias, providing an intercontinental natural experiment in the management of ant-pollinator conflict. We examined four populations of Acacia myrtifolia over a 400-km environmental gradient in southeastern Australia using ant and pollinator exclusion as well as direct observation of ants and pollinators to assess the potential for ant-pollinator conflict to affect seed set. Native bees were the only group of floral visitors whose visitation rates were a significant predictor of fruiting success, although beetles and wasps may play an important role as "insurance" pollinators. We found no increase in pollinator visitation or fruiting success following ant exclusion, even with large sample sizes and effective exclusion. Because ants are facultative visitors to A. myrtifolia plants, their presence may be insufficient to interfere greatly with floral visitors. It is also likely that the morphological location of extrafloral nectaries tends to draw ants away from reproductive parts, although we commonly observed ants on inflorescences, so the spatial separation is not strict. A. myrtifolia appears to maintain a generalized mutualism over a wide geographic range without the need for elaborate adaptations to resolve ant-pollinator conflict.

Secretory activity of extrafloral nectaries shaping multitrophic ant-plant-herbivore interactions in an arid environment

In this study, we evaluated the effects of the secretory activity of nectaries on multitrophic interactions involving ants and herbivores foraging on individuals of Prosopis laevigata (Fabaceae) located in the arid Tehuacan-Cuicatlán valley, Mexico. We observed that the secretory activity of nectaries of P. laevigata appeared to follow the predictions of the ‘Optimal Defense Theory’. Specifically, our results suggest that due to high temperature and low humidity during the day, nectaries were more active at night, precisely when herbivores and ants were more abundant. Moreover, protective ants were always more abundant in the apical zones of the branches where youngest leaves are most susceptible to attack by herbivores. We hypothesized that P. laevigata could be optimizing nectar secretion in order to allocate defenses to maximize their individual fitness. Our study contributes to our understanding of how Optimal Defense Theory could shape multitrophic interactions between ants, plants, and herbivores mediated by secretory activity of nectaries in arid environments.

Individual-based ant-plant networks: diurnal-nocturnal structure and species-area relationship.

Despite the importance and increasing knowledge of ecological networks, sampling effort and intrapopulation variation has been widely overlooked. Using continuous daily sampling of ants visiting three plant species in the Brazilian Neotropical savanna, we evaluated for the first time the topological structure over 24 h and species-area relationships (based on the number of extrafloral nectaries available) in individual-based ant-plant networks. We observed that diurnal and nocturnal ant-plant networks exhibited the same pattern of interactions: a nested and non-modular pattern and an average level of network specialization. Despite the high similarity in the ants’ composition between the two collection periods, ant species found in the central core of highly interacting species totally changed between diurnal and nocturnal sampling for all plant species. In other words, this “night-turnover” suggests that the ecological dynamics of these ant-plant interactions can be temporally partitioned (day and night) at a small spatial scale. Thus, it is possible that in some cases processes shaping mutualistic networks formed by protective ants and plants may be underestimated by diurnal sampling alone. Moreover, we did not observe any effect of the number of extrafloral nectaries on ant richness and their foraging on such plants in any of the studied ant-plant networks. We hypothesize that competitively superior ants could monopolize individual plants and allow the coexistence of only a few other ant species, however, other alternative hypotheses are also discussed. Thus, sampling period and species-area relationship produces basic information that increases our confidence in how individual-based ant-plant networks are structured, and the need to consider nocturnal records in ant-plant network sampling design so as to decrease inappropriate inferences.

Context dependency of rewards and services in an Indian ant–plant interaction: southern sites favour the mutualism between plants and ants

Abstract:Protection-based ant–plant mutualisms may vary in strength due to differences in ant rewards, abundance of protective ants and herbivory pressure. We investigated geographical and temporal variation in host plant traits and herbivory pressure at five sites spanning the distribution range of the myrmecophyteHumboldtia brunonis(Fabaceae) in the Indian Western Ghats. Southern sites had, on average, 2.4 times greater abundance of domatia-bearing individuals, 1.6 times greater extrafloral nectary numbers per leaf, 1.2 times larger extrafloral nectary sizes, 2.2 times greater extrafloral nectar (EFN) volumes and a two-fold increase in total amino acid and total sugar concentrations in EFN compared with northern sites. A strong protection-based mutualism with ants occurred at only one southern site where herbivory was highest, suggesting that investments in attracting ants correlate with anti-herbivore benefits gained from the presence of protective ants. Our results confirm a temporally stable north–south gradient in myrmecophytic traits in this ant-plant as several of these traits were re-sampled after a 5-y interval. However, the chemical composition of EFN varied at both spatial and short-term temporal scales suggesting that only repeated measurements of rewards such as EFN can reveal the real spectrum of trait variation in an ant–plant mutualistic system.

Nutritional benefits from domatia inhabitants in an ant–plant interaction: interlopers do pay the rent

Summary How a symbiosis originates and is maintained are important evolutionary questions. Symbioses in myrmecophytes (plants providing nesting for ants) are believed to be maintained by protection and nutrients provided by specialist plant‐ants in exchange for nesting spaces (called domatia) and nourishment offered by ant‐plants. However, besides the benefits accrued from housing protective ants, the mechanisms contributing to the fitness advantages of bearing domatia have rarely been examined, especially because the domatia trait is usually constitutively expressed, and many myrmecophytes have obligate mutualisms with single ant species resulting in invariant conditions. In the unspecialized ant‐plant Humboldtia brunonis (Fabaceae) that offers extrafloral nectar to ants, only some plants produce domatia in the form of hollow internodes. These domatia have a self‐opening slit making them more prone to interlopers and are occupied mostly by non‐protective ants and other invertebrates, especially arboreal earthworms. The protection mutualism with ants is restricted in geographical extent, occurring only at a few sites in the southernmost part of this plant's range in the Western Ghats of India. We examined nutrient flux from domatia residents to the plant using stable isotopes. We found that between 9% (earthworms) and 17% (protective or non‐protective ants) of nitrogen of plant tissues nearest the domatium came from domatia inhabitants. Therefore, interlopers such as earthworms and non‐protective ants contributed positively to the nitrogen budget of localized plant modules of this understorey tree. 15N‐enriched feeding experiments with protective ants demonstrated that nutrients flowed from domatia inhabitants to nearby plant modules. Fruit set did not differ between paired hand‐pollinated inflorescences on domatia and non‐domatia bearing branches. This was possibly due to the nutrient flux from domatia to adjacent branches without domatia within localized modules. This study has demonstrated the nutritive role of non‐protective ants and non‐ant invertebrates, hitherto referred to as interlopers, in an unspecialized myrmecophyte. Our study suggests that even before the establishment of a specialized ant–plant protection mutualism, nutritional benefits conferred by domatia inhabitants can explain the fitness benefits of bearing domatia, and thus the maintenance of a trait that facilitates the establishment of a specialized ant–plant symbiosis.

Habitat edge effects alter ant-guard protection against herbivory

Edge effects are among the most important drivers of species interactions in fragmented habitats, but the impacts of edge effects on multitrophic interactions are largely unknown. In this study we assess edge effects on species interactions within an ant–plant mutualistic system—where ants protect plants against herbivory—to determine whether habitat edges alter the amount of protection ants provide. We focus on a single species of myrmecophytic plant, Solanum americanum, and experimentally manipulate ant access to study plants in large-scale fragmented habitat patches at the Savannah River Site National Environmental Research Park, USA. In this system, S. americanum commonly hosts honeydew-producing aphids that are tended by ants, and grasshoppers are the primary herbivores. We measured edge effects on the per-plant abundance of aphids and protective ants as well as the abundance of grasshoppers in each habitat patch, and we evaluated levels of ant protection against herbivory near and far from habitat edges. We found that ants provided significant protection to plants far from edges, where herbivory pressure was highest, despite the fact that aphids and ants were least abundant on these plants. Conversely, ants did not provide significant protection near edges, where herbivory pressure was lowest and aphids and ants were most abundant. We conclude that a strong edge effect on grasshopper abundance was a key factor determining the amount of protection ants provided against herbivory. Future studies of the impacts of habitat fragmentation on ant–plant mutualisms will benefit from studies of ant behavior in response to herbivory threats, and studies of edge effects on other species interactions may also need to consider how species’ behavioral patterns influence the interactions in question.

Understanding ontogenetic trajectories of indirect defence: ecological and anatomical constraints in the production of extrafloral nectaries.

Early ontogenetic stages of myrmecophytic plants are infrequently associated with ants, probably due to constraints on the production of rewards. This study reports for the first time the anatomical and histological limitations constraining the production of extrafloral nectar in young plants, and the implications that the absence of protective ants imposes for plants early during their ontogeny are discussed. Juvenile, pre-reproductive and reproductive plants of Turnera velutina were selected in a natural population and their extrafloral nectaries (EFNs) per leaf were quantified. The anatomical and morphological changes in EFNs during plant ontogeny were studied using scanning electron and light microscopy. Extrafloral nectar volume and sugar concentration were determined as well as the number of patrolling ants. Juvenile plants were unable to secrete or contain nectar. Pre-reproductive plants secreted and contained nectar drops, but the highest production was achieved at the reproductive stage when the gland is fully cup-shaped and the secretory epidermis duplicates. No ants were observed in juvenile plants, and reproductive individuals received greater ant patrolling than pre-reproductive individuals. The issue of the mechanism of extrafloral nectar release in T. velutina was solved given that we found an anatomical, transcuticular pore that forms a channel-like structure and allows nectar to flow outward from the gland. Juvenile stages had no ant protection against herbivores probably due to resource limitation but also due to anatomical constraints. The results are consistent with the growth-differentiation balance hypothesis. As plants age, they increase in size and have larger nutrient-acquiring, photosynthetic and storage capacity, so they are able to invest in defence via specialized organs, such as EFNs. Hence, the more vulnerable juvenile stage should rely on other defensive strategies to reduce the negative impacts of herbivory.

The evolution of mutualism

Like altruism, mutualism, cooperation between species, evolves only by enhancing all participants' inclusive fitness. Mutualism evolves most readily between members of different kingdoms, which pool complementary abilities for mutual benefit: some of these mutualisms represent major evolutionary innovations. Mutualism cannot persist if cheating annihilates its benefits. In long-term mutualisms, symbioses, at least one party associates with the other nearly all its life. Usually, a larger host harbours smaller symbionts. Cheating is restrained by vertical transmission, as in Buchnera; partner fidelity, as among bull-thorn acacias and protective ants; test-based choice of symbionts, as bobtail squid choose bioluminescent bacteria; or sanctioning nonperforming symbionts, as legumes punish nonperforming nitrogen-fixing bacteria. Mutualisms involving brief exchanges, as among plants and seed-dispersers, however, persist despite abundant cheating. Both symbioses and brief-exchange mutualisms have transformed whole ecosystems. These mutualisms may be steps towards ecosystems which, like Adam Smith's ideal economy, serve their members' common good.

Geographical variation in an ant-plant interaction correlates with domatia occupancy, local ant diversity, and interlopers

Interactions between potentially mutualistic partners can vary over geographic areas. Myrmecophytes, which are plants harbouring ants, often do not exhibit sufficient intraspecific variability to permit comparative studies of myrmecophytic traits over space or time. Humboldtia brunonis (Fabaceae), a dominant, endemic myrmecophyte of the Indian Western Ghats, is unique in exhibiting considerable variability in myrmecophytic traits, e.g. domatia presence, as well as domatia occupancy and associated ant diversity throughout its geographic range. Although its caulinary domatia are occupied by at least 16 ant species throughout its distribution, young leaves and floral buds producing extrafloral nectar (EFN) are protected by ants from herbivory only in the southernmost region, where Technomyrmex albipes (Dolichoderinae) is the most abundant ant species. The extent of protection by ants was positively related to local species richness of ants and their occupancy of domatia. On the other hand, the highest abundance of interlopers in the domatia, including non-protective ants, the arboreal earthworm Perionyx pullus, and other invertebrates, occurred in sites with the least protection from herbivory by ants. Whereas domatia morphometry did not vary between sites, domatia occupied by protective ants and invertebrate interlopers were longer and broader than empty ones at all sites. The lowest percentage of empty domatia was found at the southernmost site. There was a progressive decline in ant species richness from that found at the sites, to that feeding on H. brunonis EFN, to that occupying domatia, possibly indicating constraints in the interactions with the plants at various levels. Our study of this dominant myrmecophyte emphasizes the impact of local factors such as the availability of suitable ant partners, domatia occupancy, and the presence of interlopers on the emergence of a protection mutualism between ants and plants.

Nutritional Ecology: A First Vegetarian Spider

Mutualisms are ubiquitous in nature and equally commonplace is their exploitation. A well-known mutualism has been found to be exploited from a surprising source: the first described vegetarian spider dines on trophic structures produced by acacia trees to reward their mutualistic protective ants.

Induced indirect defence in a lycaenid-ant association: the regulation of a resource in a mutualism.

Indirect defences involve the protection of a host organism by a mutualistic partner. Threat of predation to the host organism may induce the production of rewards and/or signals that attract the mutualistic partner. In laboratory and field experiments we show that threatened lycaenid butterfly larvae (Plebejus acmon) produce more nectar rewards from their gland and were tended by protective ants twice as much as controls. Ant attendance did not affect the leaf consumption or feeding behaviour of larvae in the absence of predators. Inducible nectar production and indirect defence in this system may be a mechanism by which larvae provide rewards for services when they are needed the most. Such a system may stabilize the mutualistic association between lycaenid larvae and ants by preventing exploitation by either partner.

Lycaenid Butterflies and Ants: Selection for Enemy-Free Space

Many lycaenid butterflies counter attacks from natural enemies by associating with protective ants. The acquisition of this enemy-free space has strongly influenced lycaenid evolution. Four major adaptations are discussed: the thick larval cuticle, appeasement pheromones, the nectar gland with associated tentacles, and location of ants by ovipositing adults. The larval nectary is hypothesized to have a sequestering function when ants and larval food are not immediately coincident, and to release sheltering behavior by ants that reduces larval and pupal apparency. In facultative ant relationships the nectary may also function to appease unknown ants. When ants and larval food are coincident, the nectary is often absent or nonfunctional. Lycaenid larvae eat a diversity of unrelated foods, including flowering plants, fungi, lichens, cycads, ferns, conifers, homopterans, and ant larvae. They also milk homopterans and are fed orally by ants. These dietary shifts are apparently strongly conditioned by the d...