Ant-plant Interactions Research Articles

Long-term strict ant-plant mutualism identity characterises growth rate and leaf shearing resistance of an Amazonian myrmecophyte

Over 125 million years of ant-plant interactions have culminated in one of the most intriguing evolutionary outcomes in life history. The myrmecophyte Duroia hirsuta (Rubiaceae) is known for its mutualistic association with the ant Myrmelachista schumanni and several other species, mainly Azteca, in the north-western Amazon. While both ants provide indirect defences to plants, only M. schumanni nests in plant domatia and has the unique behaviour of clearing the surroundings of its host tree from heterospecific plants, potentially increasing resource availability to its host. Using a 12-year survey, we asked how the continuous presence of either only M. schumanni or only Azteca spp. benefits the growth and defence traits of host trees. We found that the continuous presence of M. schumanni improved relative growth rates and leaf shearing resistance of Duroia better than trees with Azteca. However, leaf herbivory, dry matter content, trichome density, and secondary metabolite production were the same in all trees. Survival depended directly on ant association (> 94% of trees died when ants were absent). This study extends our understanding of the long-term effects of strict ant-plant mutualism on host plant traits in the field and reinforces the use of D. hirsuta–M. schumanni as a model system suitable for eco-co-evolutionary research on plant–animal interactions.

Plant-ant interactions mediate herbivore-induced conspecific negative density dependence in a subtropical forest

The early growth stage of plants is vital to community diversity and community regeneration. The Janzen-Connell hypothesis predicts that conspecific density dependence lowers the survival of conspecific seedlings by attracting specialist natural enemies, promoting the recruitment and performance of heterospecific neighbors. Recent work has underscored how this conspecific negative density dependence may be mediated by mutualists – such as how mycorrhizal fungi may mediate the accrual of host-specific pathogens beneath the crown of conspecific adult trees. Aboveground mutualist and enemy interactions exist as well, however, and may provide useful insight into density dependence that are as of yet unexplored. Using a long-term seedling demographic dataset in a subtropical forest plot in central China, we confirmed that conspecific neighborhoods had a significant negative effect on seedling survival in this subtropical forest. Furthermore, although we detected more leaf damage in species that were closely related to ants, we found that the presence of ants had significant positive effects on seedling survival. Beside this, we also found a negative effect of ant appearance on seedling growth which may reflect a trade-off between survival and growth. Overall, our findings suggested that ants and conspecific neighborhoods played important but inverse roles on seedling survival and growth. Our results suggest ants may mediate the influence of conspecific negative density dependence on seedling survival at community level.

Obligate Ant-Associated Macaranga bancana is Better Protected from Herbivory Than Facultative Ant-Associated Macaranga tanarius

Protective mutualism between ant and Macaranga plants are complex between-species interactions found only in the tropical environment. In such interactions, plants provide housing structures (in the form of domatia) and food (in the form of food bodies) to their ant symbionts. In return, the ants protect their Macaranga plant hosts against herbivore attacks. Macaranga ant protective mutualism is manifested in a wide range of interactions, from facultative to obligate. In facultative interactions, Macaranga plants attract predatory ants to the plant via food rewards. In return, foraging ants may opportunistically provide protection from insect herbivores. In obligate interactions, plants provide shelter and food rewards to permanent ant partners. We hypothesize that in obligate Macaranga, the host is better protected because of the permanent presence of its resident ant partners, whereas in facultative Macaranga, the defense against insect herbivores may be less efficient depending on the attractiveness of the food rewards and the aggressiveness of the ant species in the plant’s vicinity. In this study, we compare herbivory damage and phytophagous insect herbivore types between a facultative ant-plant M. tanarius and an obligate anti-plant M. bancana. This study further highlights that co-evolved ant partners are more efficient in defending their host plants against phytophagous insect herbivores than facultative ant-plant interactions.

Ants Sleep, Plants do not: The Variation in Species’ Activity Influences the Topology of Interaction Networks

The emergence of graph theory allowed using the complex network approach to aggregate detailed information about interactions between species. Although the use of the complex network approach has improved the understanding about community structuring, few aspects such as the temporal variation in the species’ activity pattern in the networks’ topology were explored so far. The current study used the ecological network approach to investigate ants interacting in the extrafloral nectary (EFN) of plants in order to test the hypothesis that the temporal variation in the foraging behavior of these animals affects the networks’ topology. In order to assess the temporal effect on the interaction networks, 24-hour collections divided in two 12-hour shifts (day and night) were performed in 20 plots, thus totaling 288 collection hours over 6 months. The ant-plant interaction networks presented similarity among the topological metrics assessed throughout the day. Different ant species presented distinct foraging times. Thus, two modules referring to the day and night shifts emerged from the network and presented specific species at each foraging shift. On the other hand, the plants kept on providing the resource (active EFNs) throughout the day. The results found in the current study have shown that ecological networks keep their structures constant; however, the ecological processes ruling these networks can better respond to the effects caused, for example, by the temporal variation in species’ activity. Therefore, it is worth always taking into consideration the importance of ecological processes at the time to analyze interactions in the nature.

Fungi as mutualistic partners in ant-plant interactions.

Associations between fungi and ants living in mutualistic relationship with plants ("plant-ants") have been known for a long time. However, only in recent years has the mutualistic nature, frequency, and geographical extent of associations between tropical arboreal ants with fungi of the ascomycete order Chaetothyriales and Capnodiales (belonging to the so-called "Black Fungi") become clear. Two groups of arboreal ants displaying different nesting strategies are associated with ascomycete fungi: carton-building ants that construct nest walls and galleries on stems, branches or below leaves which are overgrown by fungal hyphae, and plant-ants that make their nests inside living plants (myrmecophytes) in plant provided cavities (domatia) where ants cultivate fungi in small delimited "patches". In this review we summarize the current knowledge about these unsuspected plant-ant-fungus interactions. The data suggest, that at least some of these ant-associated fungi seem to have coevolved with ants over a long period of time and have developed specific adaptations to this lifestyle.

Temporal and spatial variation in extrafloral nectar and associated ants in Canavalia rosea (Fabaceae) on coastal dunes along the Gulf of Mexico

ABSTRACT Extrafloral nectar production can vary depending on the structure of the plant in which it is found, as well as environmental conditions. This can in turn influence plant-ant interactions. We evaluated the role of extrafloral nectaries of Canavalia rosea as ant attractants in a coastal zone of the Gulf of Mexico. We compared the productivity of the extrafloral nectaries present on leaves and inflorescences, as well as between day and night, and described the associated ant community. Nectar volume and concentration were higher in inflorescences than in leaves, and the rate of ant visitation was higher in inflorescences during the day. These results suggest congruence with the Optimal Defense Hypothesis. Nectar volume was generally greater during the night in both structures, but sugar concentration did not differ between day and night. We found a turnover in the ant species visiting C. rosea, with S. geminata being the most abundant species. The extrafloral nectar of C. rosea attracts several ant species and probably other arthropods, providing a valuable resource in a stressful system.

Fungi in ant-plant interactions: a key to enhancing plant nutrient-acquisition strategies.

This article is a Commentary on Gegenbauer et al. (2023), 238: 2210–2223.

Scattered trees as crucial elements in maintaining urban diversity: A case study with canopy ants in a biodiversity hotspot

Urban environments are characterized by profound differences in abiotic conditions compared to natural environments, which filter one part of the biotic communities that endure living in these environments. A conspicuous element in many cities are scattered trees, often included in urban planning around the world. These trees are key elements for urban ecological processes and services and act as habitat islands, providing resources (i.e., food and shelter) for a considerable arthropod diversity, such as ants. Studies involving ants in urban environments often focus on ground-dwelling ants, and few studies seek to glimpse the ants that occupy scattered trees and, even less, how these ants and trees interact within cities. This study aimed to investigate the ant communities foraging day and night on trees in an urban area inside a biodiversity hotspot, the Brazilian Atlantic Forest. Specifically, we investigated how tree characteristics (tree size, tree isolation, and the tree origin, i.e., native and exotic) modulate ant diversity and ant-plant interactions. We found that the ant species composition is different between day and night, as well as the central core of generalist ant species of day and night interaction networks. The tree size increases beta-diversity among trees only of the nocturnal ant community, while none of the tree characteristics shaped the ant community. This study is the first to address the role of scattered trees in maintaining the diversity of arboreal ants in urban landscapes, focusing on species diversity and their interaction networks. Overall, we provide insights supporting the conservation value of scattered trees in maintaining urban biodiversity.

Plant sex changes the outcome of ant–plant interactions in a facultative myrmecophytic cactus

Abstract In exchange for extrafloral nectar, ants deter herbivores from the plants decreasing the herbivore damage, and increasing plant performance in terms of growth and survival. Plants of different sexes may exhibit differences in the investment of resources for defence, thereby differentially decreasing the amount of energy available to other physiological processes. In this context, little is known about sex‐related differences in the outcome of ant–plant interactions in plants bearing extrafloral nectaries (EFNs). In the present study, we conducted ant‐exclusion experiments in the field to test for sex‐related differences in the outcome of ant–plant interactions in vegetative and reproductive buds of Opuntia robusta in individuals of different sexes in two populations: trioecious and dioecious. We applied tanglefoot to some plant and others were allowed ant access, and measured herbivory, relative growth rates and survival probabilities of buds during the growing season when EFNs are active. We counted the number of ants foraging in EFNs of flowers and cladodes of different sexes. We hypothesized that differences in resource investment to defence between sexes change the outcome of ant–plant interactions in terms of the number of ants foraging on EFNs, herbivory, growth, and survival probabilities. Our results suggest sex‐specific strategies in the investment of resources for defence mediated by EFNs in O. robusta, wherein males, females and hermaphrodites from both populations respond differentially to ant presence and herbivores. These sex‐related differences affected the outcome of the ant–plant interactions, influencing changes in number of ants foraging on EFNs, and the resulting herbivory, growth and survival of flowers and cladodes among the different sexes and among populations. Our results suggest that the maintenance of EFNs in O. robusta is costly, reflecting some trade‐offs between growth/survival and defence. Buds visited by ants tended to grow slowly and survive worse in the trioecious population; in the dioecious population they grew slower but survived better. Overall, a greater number of ants visiting EFNs was related to lower herbivore damage, greater growth and survival of flowers and cladodes. Our study underscores the importance of considering plant sex in the outcome of ant–plant interactions. Read the free Plain Language Summary for this article on the Journal blog.

Effect of ants on herbivory levels ofInga laurina: the interplay between space and time in an urban area

AbstractExtrafloral nectary plants not only occur in natural areas but also in urban parks. These areas are prone to edge effects, and plants face different microenvironmental conditions. We investigated the spatial variation of ant–plant interactions in an urban park, and we examined if plants with ants would show lower herbivory levels and if it depended on habitat type (interior or edges). Seedlings ofInga laurinawere set in 200-m long transects (which covered both the west and east edges, and the interior) in an urban park and then experimentally assigned to be either ant-present or ant-excluded plants. Leaf herbivory was investigated throughout the wet season and was influenced by the interaction effect between ants and habitat type. Ants decreased the herbivory on the west edge, but on the east edge results were the opposite. The east edge had higher temperature and sunlight exposure in comparison to the other sites and was assumed to disrupt the stability of ant–plant interactions. In the interior of the fragment, herbivory depended on ant presence/absence and on the location of plants along the transect. Our study highlights how the outcomes of ant–plant interactions are spatially conditioned and affected by different types of habitats.

To each their own! Nectar plasticity within a flower mediates distinct ecological interactions.

Nuptial and extranuptial nectaries are involved in interactions with different animal functional groups. Nectar traits involved in pollination mutualisms are well known. However, we know little about those traits involved in other mutualisms, such as ant-plant interactions, especially when both types of nectaries are in the same plant organ, the flower. Here we investigated if when two types of nectaries are exploited by distinct functional groups of floral visitors, even being within the same plant organ, the nectar secreted presents distinct features that fit animal requirements. We compared nectar secretion dynamics, floral visitors and nectar chemical composition of both nuptial and extranuptial nectaries in natural populations of the liana Amphilophium mansoanum (Bignoniaceae). For that we characterized nectar sugar, amino acid and specialized metabolite composition by high-performance liquid chromatography. Nuptial nectaries were visited by three medium- and large-sized bee species and extranuptial nectaries were visited mainly by ants, but also by cockroaches, wasps and flies. Nuptial and extranuptial nectar differed regarding volume, concentration, milligrams of sugars per flower and secretion dynamics. Nuptial nectar was sucrose-dominated, with high amounts of γ-aminobutyric acid and β-aminobutyric acid and with theophylline-like alkaloid, which were all exclusive of nuptial nectar. Whereas extranuptial nectar was hexose-rich, had a richer and less variable amino acid chemical profile, with high amounts of serine and alanine amino acids and with higher amounts of the specialized metabolite tyramine. The nectar traits from nuptial and extranuptial nectaries differ in energy amount and nutritional value, as well as in neuroactive specialized metabolites. These differences seem to match floral visitors' requirements, since they exclusively consume one of the two nectar types and may be exerting selective pressures on the composition of the respective resources of interest.

Structural Stability of Ant-plant Mutualistic Networks Mediated by Extrafloral Nectaries: Looking at the Effects of Forest Fragmentation in the Brazilian Amazon

Rainforest fragmentation drastically affects biodiversity and species composition, mainly due to habitat loss. Several studies have already shown the effects of forest fragmentation on plant and ant communities. To date, however, there is limited empirical knowledge of how forest fragmentation affects ant-plant interaction in networks. We investigated the effects of the configuration of rainforest fragments on the structure of ant-plant interaction networks mediated by extrafloral nectaries (EFNs). We carried out this study in ten forest fragments, ranging in size from approximately 5 to 3,000 ha, located in the Brazilian Amazon. In each fragment we established a plot of 6,250 m2, in which all ant-plant interactions were recorded, and calculated the following network descriptors: number of interactions, network size, network specialization, diversity of interactions, and nestedness. We used four explanatory variables to investigate the effects of forest fragmentation on these network descriptors: three metrics of the configuration of fragments (i.e., fragment area, edge irregularity, and connectivity) and the forest structure within each fragment, represented by canopy cover. We did not detect any effect of the explanatory variables on the network descriptors. The structural stability of the networks sampled in forest fragments with different configurations is possibly related to the observed constancy of ant species in the central core of highly interacting species. Our results corroborate other studies highlighting the structural stability of these facultative ant-plant networks mediated by EFNs in different spatial and temporal gradients. Nonetheless, the low constancy of plant species in the generalist core should be understood as a warning, mainly because the functionality of this protective mutualism (i.e., food secretions in exchange for protection against herbivory) remains unknown.

Ant-plant symbioses trade-offs and its role in forest restoration projects

Ant-plant symbioses are complex between-species interactions found only in the tropical environment. Typically, in such symbioses, plants provide housing structures and food to their ant symbionts. In return, the ants protect their plants' host against herbivore attack and additional nutrients to help with plants' growth. These win-win interactions range from facultative to obligate mutualism. This proposal aims to test the three main mechanisms: (1) by-product benefits, (2) partner fidelity feedback and (3) partner choice in stabilising the ant-plant mutualism. Understanding the mechanisms are crucial as they form the foundation of the ant-plant distribution and growth, in other words - the health of the myrmecophyte (ants-loving) trees in the forest ecosystem. Hence, ant-plant symbioses are an ideal model system for investigating the effects of anthropogenic changes, such as deforestation and climate change on the outcome of ant-plant mutualistic interactions. This project attempts to identify the mechanisms regulating the mutualistic interactions and, in particular, identify the context in which such mutualistic interactions evolved and adapt to the changing environment. We hypothesise that there will be a higher diversity of obligate mutualistic ant-plant interactions in the undisturbed environment compared to degraded habitat. Furthermore, we expect there are different complexity of symbioses, involving multiple partners (ants-hemipteran insects-bacteria-fungi-plants) that deepen our understanding of how such symbioses can be stabilised. Finally, the deforestation combined with climate change in Southeast Asia will have a detrimental effect on ant-plant symbioses, causing breakdown of mutualistic partners and invasion of cheater ant species that do not confer a protective advantage to their plants' host.

Scale of effect matters: Forest cover influences on tropical ant-plant ecological networks

In the last decade, the number of studies dealing with how species interaction networks are structured by landscape has increased in the literature. However, many studies quantify landscape metrics at one single spatial extent, without considering the effects at multiple spatial extents. To the best of our knowledge, no study has explicitly addressed and discussed the spatial extent at which landscape structure best predicts the organization of ecological networks, which is key to understanding how ecological interactions are affected by landscape modifications. Therefore, two important research questions arise: can the spatial scale at which landscape structure best predicts an ecological response (i.e., scale of effect) magnify our ability to understand ecological networks or can the suboptimal scale just blind our view about what really happens? Motivated by these concerns, we used ant-plant relationships obtained from 16 landscapes in a human-dominated tropical rainforest of Mexico to assess and discuss the spatial extent at which forest cover (%) best predicts ant-plant interaction network patterns (i.e., network size, interaction diversity, network specialization, and nestedness). In general, we observed that smaller scales best predicted the interaction diversity (50 m) and specialization (250 m) of ecological networks involving ants and plants, which are descriptors associated to abundance and the distribution of interactions between plant and ant species. This is possibly because ant-plant relationships are being modulated by processes that act at the microclimatic level due to the biotic and abiotic conditions that forest provides. However, we found that network size and nestedness (i.e., descriptors associated to species detectability and emergent properties) were not associated with forest cover at any analyzed spatial extent. These findings indicate that the ant-plant ecological network structure can be influenced by processes that occur at different spatial extents. Moreover, the results presented here have a direct impact on our theoretical and empirical understanding of how the landscape structure shapes biotic interactions at different spatial extents in highly diverse tropical rainforests.

How to induce ant–plant interactions: Seed baiting to enhance its dispersal as a tool for restoration

AbstractIn degraded drylands, direct sowing is one of the most widespread revegetation practices, but its efficiency is low and usually seed enhancement techniques are needed to increase its success. We evaluated how to induce seed dispersal by ants (myrmecochory), as this interaction could improve the chances of seed germination and seedling establishment, via seed transport to ants' nests where seeds are protected and the soils enriched. Our objective was to develop seeds with the addition of baits attractive to ants without affecting seed germination. First, we tested the attractiveness of baits of different sizes and ingredients by performing cafeteria experiments in nests of the omnivorous ant Dorymyrmex tener, the most abundant and effective seed disperser ant in the Patagonian steppe. Then, we attached the most preferred baits (small baits containing pate, sugar and clay) to seeds of two native plants species (Acaena splendens and Oenothera odorata) with relevant characteristics for restoration purposes and tested their attractiveness to ants. We used different strategies to attach the bait to the seeds (e.g. encrusted, agglomerate and seeds on the surface) looking for the most attractive and simplest one. We found that only baited seeds were removed and the interaction was induced regardless of the way the bait was attached. Also, germination of seeds with bait was similar to that of seeds without bait in O. odorata, but reduced in A. splendens. We showed that it is possible to encourage ants to transport previously non‐attractive seeds through the design of baits, potentially improving direct sowing efficiency.

Changes in the core species of the ant-plant network of oak forest converted to grassland: replacement of its ant functional groups.

Land-use change in terrestrial environments is one of the main threats to biodiversity. The study of ant-plant networks has increased our knowledge of the diversity of interactions and structure of these communities; however, little is known about how land-use change affects ant-plant networks. Here we determine whether the change in land use, from native oak forest to induced grassland, affected the network properties of ant-plant networks in a temperate forest in Mexico. We hypothesize that the disturbed vegetation will be more nested and generalized due to the addition of generalist species to the network. The oak forest network comprises 47 plant species and 11 ant species, while the induced grassland network has 35 and 13, respectively. Floral nectar was the resource used most intensely by the ants in both vegetation types. The ant-plant network of the induced grassland was significantly more nested and generalist than that of the oak forest; however, none of the networks were nested when considering the frequency of interaction. In both vegetation types, the ants were more specialized than the plants, and niche overlap was low. This could be related to the dominant species present in each type of vegetation: Prenolepis imparis in the oak forest and Camponotus rubrithorax in the grassland. The central core of cold climate ant species in the oak forest was replaced by a central core of subordinate Camponotini and tropical specialists in the induced grassland. These results suggest that the increase in nestedness and generalization in the grassland may be related to the loss of the cold climate specialists from the core of the oak forest network. Our findings provide evidence that land-use change increases the level of generalization in the ant-plant interaction networks of temperate forests.

Experimental manipulation of biotic and abiotic parameters changes the outcome of insect-plant interactions

Plants usually respond to environmental shifts with morpho-physiological adjustments, which trickles down to biotic interactions in the insect-plant system. We evaluate how Copaifera langsdorffii, a widespread tree species adapted to multiple ecosystems, responds to shifts in nutrient and water availability through experimental supplementation and how it affects its insect communities. We also evaluate how the presence of extrafloral nectaries (EFN) exudates modifies galling insect diversity and herbivory rates. Such experimental approach is scarce, as we simultaneously evaluate biotic and abiotic factors and cover the entire reproductive cycle of a species in natural environments, bringing important contributions to better understand how bottom-up factors drive species interactions and possibly community assembly. The experiment was set in an ironstone outcrop vegetation, where we deployed supplementation treatments in 80 plant individuals divided into the following field treatments: (T1 = Fertilizer, T2 = EFN simulation (Eppendorf tubes with a 20% sugar solution), T3 = fertilizer + EFN simulation, T4 = water spray, T5 = EFN control (microtube with water), and T6 = Control. We observed lower sclerophylly and greater leaf area in plant individuals that were supplemented with nutrients and water. Herbivory rates were lower and ant abundance was higher in plants with artificial EFNs available. While we did not observe variations in richness and abundance of galling insects, the patterns of co-occurrence of galls varied with the availability of resources (nesting space) in the plant. This study illustrates how variations in nutrient availability to plants modify interactions with insect communities. Ant-plant interactions can have a negative impact on general herbivory rates, however ants seem to have a more harmonious relationship with the galling insects.

Habitat as a conditionality factor of ant-plant mutualistic interaction in the Cecropia-Azteca system

Habitat as a conditionality factor of ant-plant mutualistic interaction in the Cecropia-Azteca system

Females restrict the position of domatia and suffer more herbivory than hermaphrodites inMyriocarpa longipes,a neotropical facultative myrmecophyte

AbstractDomatia are hollow structures in plants occupied by ant colonies, in turn ants provide protection against herbivores. In plants, competition for resources has driven sex-related changes in the patterns of resource allocation to life-history traits and defence traits. The resource-competition hypothesis (RCH) proposes that female plants due to their higher investment in reproduction will allocate fewer resources to defence production, showing greater herbivore damage than other sexual forms. We hypothesise the existence of sex-related differences in defensive traits of domatia-bearing plants, being female plants less defended due to differences in domatia traits, such as size, number of domatia and their position, exhibiting more herbivore damage than hermaphrodite plants ofMyriocarpa longipes, a facultative neotropical myrmecophyte. We found eight species of ants inhabiting domatia; some species co-inhabited the same plant, even the same branch. Our results are consistent with the predictions of RCH, as female plants had ant-inhabited domatia restricted to the middle position of their branches and exhibited greater herbivore damage in leaves than hermaphrodites. However, we did not find differences in domatia size and leaf area between sexual forms. Our study provides evidence for intersexual differences in domatia position and herbivory in a facultative ant–plant mutualism inM. longipes.We highlight the importance of considering the plant sex in ant–plant interactions. Differences in resource allocation related to sexual reproduction could influence the outcome of ant–plant interactions.

Negative effects of ant-plant interaction on pollination: costs of a mutualism

The mutualism of ants and extrafloral nectary (EFN)-bearing plants is known to reduce rates of herbivory. However, ants may have negative impacts on other mutualisms such as pollination, constituting an indirect cost of a facultative mutualism. For instance, when foraging on or close to reproductive plant parts ants might attack pollinators or inhibit their visits. We tested the hypothesis that ants on EFN-bearing plants may negatively influence pollinator behavior, ultimately reducing plant fitness (fruit set). The study was done in a reserve at Brazilian savannah using the EFN-bearing plant Banisteriopsis malifolia (Malpighiaceae). The experimental manipulation was carried out with four groups: control (free visitation of ants), without ants (ant-free branches), artificial ants (isolated branches with artificial ants on flowers) and plastic circles (isolated branches with plastic circles on flowers). We made observations on flower visitors and their interactions, and measured fruit formation as a proxy for plant fitness. Our results showed that pollinators hesitated to visit flowers with artificial ants, negatively affecting pollination, but did not hesitate to visit flowers with plastic circles, suggesting that they recognize the specific morphology of the ants. Pollinators spent more time per flower on the ant-free branches, and the fruiting rate was lower in the group with artificial ants. Our results confirm an indirect cost in this facultative mutualism, where the balance between these negative and positive effects of ants on EFN-bearing plants are not well known.