Ant-plant Interactions Research Articles

Response of a Predatory ant to Volatiles Emitted by Aphid- and Caterpillar-Infested Cucumber and Potato Plants.

In response to herbivory by insects, various plants produce volatiles that attract enemies of the herbivores. Although ants are important components of natural and agro-ecosystems, the importance of herbivore-induced plant volatiles (HIPVs) as cues for ants for finding food sources have received little attention. We investigated responses of the ant Formica pratensis to volatiles emitted by uninfested and insect-infested cucumber (Cucumis sativus) and potato (Solanum tuberosum) plants. Cucumber plants were infested by the phloem-feeding aphid Aphis gossypii, the leaf chewer Mamestra brassicae or simultaneously by both insects. Potato plants were infested by either Aphis gossypii, by the leaf chewer Chrysodeixis chalcites or both. In olfactometer experiments, ants preferred volatile blends emitted by cucumber plants infested with M. brassicae caterpillars alone or combined with A. gossypii to volatiles of undamaged plants or plants damaged by A. gossypii only. No preference was recorded in choice tests between volatiles released by aphid-infested plants over undamaged plants. Volatiles emitted by potato plants infested by either C. chalcites or A. gossypii were preferred by ants over volatiles released by undamaged plants. Ants did not discriminate between potato plants infested with aphids and caterpillars over plants infested with aphids only. Plant headspace composition showed qualitative and/or quantitative differences between herbivore treatments. Multivariate analysis revealed clear separation between uninfested and infested plants and among herbivore treatments. The importance of HIPVs in indirect plant defence by ants is discussed in the context of the ecology of ant-plant interactions and possible roles of ants in pest management.

Foliar uptake of nitrogen from ant faecal droplets: An overlooked service to ant‐plants

Abstract Nutrient supplies to plants from ants are well known from specialised myrmecophytic symbioses and from plants growing in soil close to ant nests. However, above‐ground nutrient pathways may play a largely unrecognised role also in less specialised ant–plant interactions—the numerous facultative relationships, where ants forage on plants. In a laboratory experiment, weaver ants (Oecophylla smaragdina) were confined to the canopies of coffee (Coffea arabica) seedlings, excluding any ant‐to‐plant transfer of nutrients via the soil strata. When ants were fed 15N‐labelled glycine and subsequently deposited faecal droplets on the seedlings, coffee leaves showed increased levels of 15N and total nitrogen compared to control plants without ants. This was evident for both exposed leaves and leaves covered in plastic bags (i.e. not directly exposed to ants). Thus, nitrogen from ant excretions was absorbed through the coffee leaves, and subsequently, translocated within the plants and possibly leading to the observed higher shoot/root (wet weight) ratios observed on ant‐plants compared to controls. Synthesis. These results reveal an undescribed foliar uptake of ant‐provided nutrients. If this is a general mechanism, a vast amount of ant–plant interactions involves fertilisation. Foliar fertilisation by ants may be an important steady benefit to plants, which has driven the evolution of ant–plant mutualisms in parallel with the well‐recognised but probably more fluctuating benefit from herbivore protection. Given the world‐wide abundance of plant canopies foraged by ants, this nutrient pathway may be of high ecological significance.

Ants at Plant Wounds: A Little-Known Trophic Interaction with Evolutionary Implications for Ant-Plant Interactions.

Extrafloral nectaries (EFNs) allow plants to engage in mutualisms with ants, preventing herbivory in exchange for food. EFNs occur scattered throughout the plant phylogeny and likely evolved independent from herbivore-created wounds subsequently visited by ants collecting leaked sap. Records of wound-feeding ants are, however, anecdotal. By surveying 38,000 trees from 40 species, we conducted the first quantitative ecological study of this overlooked behavior. Ant-wound interactions were widespread (0.5% of tree individuals) and occurred on 23 tree species. Interaction networks were opportunistic, closely resembling ant-EFN networks. Fagaceae, a family lacking EFNs, was strongly overrepresented. For Fagaceae, ant occurrence at wounds correlated with species-level leaf damage, potentially indicating that wounds may attract mutualistic ants, which supports the hypothesis of ant-tended wounds as precursors of ant-EFN mutualisms. Given that herbivore wounds are common, wound sap as a steadily available food source might further help to explain the overwhelming abundance of ants in (sub)tropical forest canopies.

Differences among ant species in plant protection are related to production of extrafloral nectar and degree of leaf herbivory

Many studies assume that all ant species collecting extrafloral nectar defend plants against herbivores, although ant–plant interactions are facultative, generalized and have variable outcomes. With over 280 h of observations in an area of Rupestrian Grasslands (Ouro Preto, Brazil), we described the network of interactions between 2313 ants of 23 species and 200 plants of 10 species. Ants from all species were further submitted to an identical task of finding and removing a standardized herbivore surrogate (termites) to quantify the relative protection effectiveness of different ant species. We then correlated ant protection to the volume and concentration of sugar in the nectar as conditional factors and the herbivory damage as interaction outcome. We found that 11 of the 23 species of ants attacked and removed 933 of 2000 termites. All plant species interacted with effective ant protectors, although the identity of the best protector varied among plants. The degree of ant protection was positively associated with sugar concentration of nectar, which further explained the variation in leaf damage among plant species. Our study provides evidence that ant protection varies among ant species and is enhanced by the plant investment in nectar reward, resulting in less herbivory for the partner plant. We also showed that the most protecting ant species are those that are most connected and thus spread the benefit throughout the network.

Exploring fungus-plant N transfer in a tripartite ant-plant-fungus mutualism.

The plant Hirtella physophora, the ant Allomerus decemarticulatus and a fungus, Trimmatostroma sp., form a tripartite association. The ants manipulate both the plant trichomes and the fungus to build galleries under the stems of their host plant used to capture prey. In addition to its structural role, the fungus also improves nutrient uptake by the host plant. But it still remains unclear whether the fungus plays an indirect or a direct role in transferring nutrients to the plant. This study aimed to trace the transfer of N from the fungus to the plant's stem tissue. Optical microscopy and transmission electron microscopy (TEM) were used to investigate the presence of fungal hyphae in the stem tissues. Then, a 15N-labelling experiment was combined with a nanoscale secondary-ion mass spectrometry (NanoSIMS 50) isotopic imaging approach to trace the movement of added 15N from the fungus to plant tissues. The TEM images clearly showed hyphae inside the stem tissue in the cellular compartment. Also, fungal hyphae were seen perforating the wall of the parenchyma cell. The 15N provisioning of the fungus in the galleries resulted in significant enrichment of the 15N signature of the plant's leaves 1 d after the 15N-labelling solution was deposited on the fungus-bearing trap. Finally, NanoSIMS imaging proved that nitrogen was transferred biotrophically from the fungus to the stem tissue. This study provides evidence that the fungi are connected endophytically to an ant-plant system and actively transfer nitrogen from 15N-labelling solution to the plant's stem tissues. Overall, this study underlines how complex the trophic structure of ant-plant interactions is due to the presence of the fungus and provides insight into the possibly important nutritional aspects and tradeoffs involved in myrmecophyte-ant mutualisms.

Altitudinal variation in ant–aphid mutualism in nitrogen transfer of oak (Quercus liaotungensis)

Ant–plant relationship is a model for the study of the ecology and evolution of interspecific interactions. In direct ant–plant mutualism (i.e., plants providing food or nesting places for ants, and ants protecting the plants in return) ants provide nutrients to plants. However, whether a similar mechanism exists in indirect ant–plant mutualism (i.e., an ant–aphid–plant system) remains unknown. In this work, we used the 15N stable isotope method to study altitudinal variations in the roles of ants in the nutrient transfer of oak (Quercus liaotungensis). Our work shows that ants deliver nitrogen in indirect ant–plant interactions, and that the effect of nutrient transfer differed significantly with altitude. Ants’ trophic level at high altitudes was significantly lower than that at low altitudes, indicating that the degree of ant–aphid mutualism was greater at high altitudes, which may be beneficial in nitrogen transfer. Our work suggests that ant–aphid mutualism might be context dependent, such that it affects nutrient transfer in the food web, and that this context dependency is an important factor that influences altitudinal variation in nutrient transfer.

Assessing the impacts of tramp and invasive species on the structure and dynamic of ant-plant interaction networks

Ants are among the most widespread and damaging of introduced organisms. In the last decade, many studies have documented the negative impact of tramp and invasive ant species (TIS) on native ant species mainly through competitive displacement and behavior. However, despite the great advances in the knowledge of TIS, still little is known about the impacts of these ants on the trophic cascade. In this study we used an approach based on network theory to explore the impact of TIS on the structure and ecological dynamic of a well-sampled and well-known community of ant–plant interactions in a tropical environment in coastal Veracruz, Mexico. We observed that of all the ant-plant interactions recorded, only 15% involved TIS and the ant Paratrechina longicornis (Formicinae) was the unique tramp species to be part of the central core of highly interacting species. We also found that TIS had little impact on the structure and dynamic ant-plant interactions in our study area, although possible indirect effects for specific TIS are also discussed. This study represents a valuable tool to conservation planners, mainly because we show the vulnerability and robustness of a tropical system rich in species and interactions to biological invasions.

Variation in Extrafloral Nectary Productivity Influences the Ant Foraging.

Extrafloral nectar is the main food source offered by plants to predatory ants in most land environments. Although many studies have demonstrated the importance of extrafloral nectaries (EFNs) to plant defense against herbivores, the influence of EFNs secretory activity pattern on predatory ants remains yet not fully understood. Here, we verified the relation between the extrafloral nectar production of a plant community in Cerrado in different times of the day, and its attractiveness to ants. The extrafloral nectaries (EFNs) of seven plant species showed higher productivity overnight. Ant abundance was higher in times of large extrafloral nectar production, however, there was no positive relation between ant richness on plants and EFNs productivity. There was temporal resource partitioning among ant species, and it indicates strong resource competition. The nectar productivity varied among plant species and time of the day, and it influenced the visitation patterns of ants. Therefore, EFNs are a key ant-plant interaction driver in the studied system.

Relación de la jerarquía de dominancia y abundancia en la estructura de la red de interacción planta-hormiga

Relación de la jerarquía de dominancia y abundancia en la estructura de la red de interacción planta-hormiga

Studies on Ant-plant Interaction in a Tropical Mangroves: In Particular Rhizophora Mucronata and Avicennia Marina from Pondicherry Region, South India

A short term field study was undertaken to understand ant-plant interaction in Rhizophora mucronata and Avicennia marina of Pondicherry mangroves. Our study revealed that both tree species Rhizophora mucronata and Avicennia marina of Pondicherry mangroves harbor rich and abundant ant fauna. A total of 10 species were recorded belonging to subfamilies Formicinae, Myrmicinae, Dolichoderinae and Pseudomyrmecinae during one season i.e. post monsoon. The abundance of ants was high in Avicennia marina with 9 species of ants and in compared with Rhizophora mucronata with only 7 species. Ants which were only found in Avicennia marina are Oecophylla smaragdina, Polyrchachis simplex, Camponotus sp. The foods for these ants are available as insects’ eggs, scale insects and carcasses of herbivorous insects. The nesting behavior of these ants is also documented. The mutualistic ant-mangrove plants interaction is quite obvious from the field observations and is recorded with relevant photographs from the study area.

Few Ant Species Play a Central Role Linking Different Plant Resources in a Network in Rupestrian Grasslands.

Ant-plant associations are an outstanding model to study the entangled ecological interactions that structure communities. However, most studies of plant-animal networks focus on only one type of resource that mediates these interactions (e.g, nectar or fruits), leading to a biased understanding of community structure. New approaches, however, have made possible to study several interaction types simultaneously through multilayer networks models. Here, we use this approach to ask whether the structural patterns described to date for ant-plant networks hold when multiple interactions with plant-derived food rewards are considered. We tested whether networks characterized by different resource types differ in specialization and resource partitioning among ants, and whether the identity of the core ant species is similar among resource types. We monitored ant interactions with extrafloral nectaries, flowers, and fruits, as well as trophobiont hemipterans feeding on plants, for one year, in seven rupestrian grassland (campo rupestre) sites in southeastern Brazil. We found a highly tangled ant-plant network in which plants offering different resource types are connected by a few central ant species. The multilayer network had low modularity and specialization, but ant specialization and niche overlap differed according to the type of resource used. Beyond detecting structural differences across networks, our study demonstrates empirically that the core of most central ant species is similar across them. We suggest that foraging strategies of ant species, such as massive recruitment, may determine specialization and resource partitioning in ant-plant interactions. As this core of ant species is involved in multiple ecosystem functions, it may drive the diversity and evolution of the entire campo rupestre community.

Extrafloral‐nectaries and interspecific aggressiveness regulate day/night turnover of ant species foraging for nectar onBionia coriacea

AbstractPlants bearing extrafloral nectaries (EFNs) vary the secretion of nectar between day and night, which creates turnover in the composition of interacting ant species. Daily variation in the composition of ant species foraging on vegetation is commonly observed, but its mechanisms are poorly understood. We evaluated the daily variation in nectar availability and interspecific aggressiveness between ants as possible regulatory mechanisms of the turnover in ant–plant interactions. We hypothesized that (i) plants would interact with more ant species during periods of higher secretion of nectar and that (ii) aggressive ant species would compete for nectar, creating a daily turnover of species collecting nectar. We tested this hypothesis by measuring the production of nectar during the day and night and by experimentally removingEFNs ofBionia coriacea(=Camptosema coriaceum) (Nees & Mart.) Benth. (Fabaceae: Faboideae) plants in a Brazilian savanna (Cerrado). We then compared the abundance and composition of ant species between those treatments and during the day. Our results indicate that more ant workers forage on plants during the day, when nectar was sugary, while more ant species forage at night, when aggressiveness between ant species was lower. We also detected a day/night turnover in ant species composition. Ant species foraging for nectar during the day were not the same at night, and this turnover did not occur on plants withoutEFNs. Both dominant ant species, diurnalCamponotus crassus(Hymenoptera: Formicidae) and nocturnalCamponotus rufipes(Hymenoptera: Formicidae), were the most aggressive species, attacking other ants in their specific periods of forage while also being very aggressive toward each other. However, this aggressiveness did not occur in the absence of nectar, which allowed non‐aggressive nocturnal ant species to forage only during the daytime, disrupting the turnover. We conclude that extrafloral‐nectar presence and interspecific aggressiveness between ants, along with other environmental factors, are important mechanisms creating turnovers in ants foraging on plants.

Changing light conditions in pine rockland habitats affect the intensity and outcome of ant–plant interactions

AbstractExtrafloral nectar (EFN) mediates food‐for‐protection mutualisms between plants and ants. Such mutualisms exist within a complex web of biotic interactions, and in a framework provided by the abiotic environment. Both biotic and abiotic factors, therefore, affect the outcome of ant–plant interactions. We conducted an experiment to determine the effects of ant activity, and light intensity, on herbivory rates, growth, and reproductive fitness in Senna mexicana var. chapmanii, a perennial legume native to pine rockland habitats of south Florida. Forty plants were divided among four treatments in a factorial experimental design with two independent variables: ant activity and light intensity. Plants were divided equally between sunny and shady habitats, and ants were excluded from half of the plants in each habitat type. The presence of ants significantly reduced herbivory rates in S. chapmanii. In shaded habitats, the presence of ants had no effect on plant reproductive fitness, however, in sunny habitats plants with ants produced significantly more seeds over the duration of the 1‐yr study. Ants represent an important biotic defense against herbivores in S. chapmanii; however, their effects on plant fitness are dependent on light conditions. Pine rockland habitats in south Florida have been widely destroyed or mismanaged. In fragments that remain, suppression of fire has led to increased canopy closure and shading of the understory. These changes will likely negatively impact plants that rely on ants for defense. We highlight the importance of conservation efforts to preserve the pine rocklands and the fire regimes on which they rely.

'Hide and seek' is no game in a specialized ant-plant interaction.

This article is a commentary on Chomicki et al., 211: 1358–1370.

Temporal Variation in the Abundance and Richness of Foliage-Dwelling Ants Mediated by Extrafloral Nectar.

Plants bearing extrafloral nectaries (EFNs) are common in the Brazilian cerrado savanna, where climatic conditions having marked seasonality influence arboreal ant fauna organization. These ant-plant interactions have rarely been studied at community level. Here, we tested whether: 1) EFN-bearing plants are more visited by ants than EFN-lacking plants; 2) ant visitation is higher in the rainy season than in dry season; 3) plants producing young leaves are more visited than those lacking young leaves in the rainy season; 4) during the dry season, plants with old leaves and flowers are more visited than plants with young leaves and bare of leaves or flowers; 5) the composition of visiting ant fauna differs between plants with and without EFNs. Field work was done in a cerrado reserve near Uberlândia, MG State, Brazil, along ten transects (total area 3,000 m2), in the rainy (October-January) and dry seasons (April-July) of 2010–2011. Plants (72 species; 762 individuals) were checked three times per season for ant presence. Results showed that 21 species (29%) and 266 individuals (35%) possessed EFNs. These plants attracted 38 ant species (36 in rainy, 26 in dry season). In the rainy season, plants with EFNs had higher ant abundance/richness than plants without EFNs, but in the dry season, EFN presence did not influence ant visitation. Plant phenology affected ant richness and abundance in different ways: plants with young leaves possessed higher ant richness in the rainy season, but in the dry season ant abundance was higher on plants possessing old leaves or flowers. The species composition of plant-associated ant communities, however, did not differ between plants with and without EFNs in either season. These findings suggest that the effect of EFN presence on a community of plant-visiting ants is context dependent, being conditioned to seasonal variation.

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.

Food source availability and interspecific dominance as structural mechanisms of ant-plant-hemipteran multitrophic networks

Extrafloral nectar of plants and honeydew of hemipterans is a food source extensively explored by ants. Although basically a sugary liquid food, nectar and honeydew are composed of different nutrients and offered in distinct ways; thus, ants must interact differently with plants and hemipterans. In this study we assessed the availability and dominance of nectar of extrafloral nectaries and honeydew of sap-sucking hemipterans (i.e., sugar-based resources) as mechanisms regulating interaction frequency and structuring ant-plant-hemipteran networks. We studied 12 plant species (240 shrubs, 20 per species) and 12 hemipteran species (240 aggregations, 20 per species) that interacted with 26 ant species in an area of Rupestrian Fields (Rocky Montane Savannah), Brazil. We observed that the 7 ant species that collected honeydew were a subset of the 25 ant species feeding on nectar, but the highly interacted species Camponotus crassus was the same for both subnetworks. The ant-plant subnetwork exhibited a nested pattern of interaction with a low degree of specialization, while the ant-hemipteran subnetwork exhibited lower nestedness but higher specialization. We found a positive relationship between the offer of EFNs and the number of interactions with ants, probably resulting from reduced competition in plants with high availability of EFNs. However, hemipteran species that were most abundant did not interact with more species of ants, probably because of the numerical dominance of the species tending all hemipteran aggregations, regardless of size. However, segregation between ant species was higher than expected by chance for both plants and hemipterans, confirming a deterministic factor (i.e., competition between ant species) regulating the frequency of interactions. In summary, the availability of ENFs seems to be an important mechanism regulating ant-plant interactions, while numerical dominance seems to be an important mechanism structuring ant-hemipteran interactions.

Foliage-dwelling ants in a neotropical savanna: effects of plant and insect exudates on ant communities

Ant dominance in tropical ecosystems can be explained by a capacity to exploit liquid foods such as extrafloral nectaries (EFNs) and secretions from honeydew-producing hemipterans (HPHs). Such nutritious exudates may determine ant distribution in space and shape specialization in ant–plant interactions. We provide a first assessment of how EFNs and HPHs mediate the structure of ant assemblages, ant visitation intensity, and characteristics of ant–plant interaction networks across space in Brazilian “cerrado” savanna. We used arboreal pitfall traps to sample visiting ants in four cerrado localities and recorded the presence of lepidopteran larvae to determine their possible response to ant visitation. Ant species composition and richness did not differ regardless of the presence of liquid rewards on plants, and most network patterns did not show consistent differences. However, in two of the four sites, ant densities were higher on plants with HPHs or EFNs due to increased activity by Camponotus and Pseudomyrmex ants. At these two sites, plants with liquid food sources had a more specific ant assemblage (higher specialization d′) than did plants without resources, and caterpillars were more frequently found on plants with fewer workers of Camponotus and Pseudomyrmex. Plants with HPHs had increased ant visitation and accumulated more ant species than did plants with EFNs or without liquid foods. Ant response to such food sources may thus depend on local conditions and identity of ant species, and may determine how ant assemblages are structured. Results highlight how different patterns of ant visitation to liquid resources can produce distinctive effects on herbivore infestation.

Loss and gains in ant–plant interactions mediated by extrafloral nectar: fidelity, cheats, and lies

All mutualistic plant–animal interactions are mediated by costs and benefits in relationships where resources (from plants) are exchanged by services (from animals). The most common trading coin that plants offer to pay for animal services is nectar; the main servers are hymenopterans. Extrafloral nectar (EFN) is produced in almost all aboveground plant parts not directly related with pollination, and their true function has long been an issue of discussion among naturalists and will be our main subject. The protective function of extrafloral nectaries (EFNs) is reviewed and considered with an alternative hypothesis, presenting not only ants, but also spiders and wasps as potential and effective agents in these protective interactions. Despite their likely relevance, the phenological variation (mainly sequential flowering and resprouting) of host plants mediating these interactions have been generally ignored. We discuss how the outcomes of each ant–EFN bearing plant interaction vary depending on physical and biotic changes in interacting organisms (internal factors such as phenology and species identity) as well as in their environments (external factors such as climatic variation), all of which may modify the character of each interaction. We propose that ant–EFN bearing plant interactions serve an excellent and unique model to test the “Geographic Mosaic Theory” of coevolution providing us a more clear view of how evolution has structured these plant–animal ecological networks.

Sampling effort differences can lead to biased conclusions on the architecture of ant–plant interaction networks

The study of plant–animal interactions using ecological networks as a tool has been intensified in recent years. However, one of the biggest criticisms of these studies is how sampling effort can affect the observed interaction patterns within these plant–animal networks. In this study we empirically evaluated how variation in sampling effort (comparing cumulative vs monthly sampled networks) influences the values of network descriptors more frequently used in the literature (i.e. number of links per species, network size, diversity of interactions, network specialization, robustness, nestedness, and modularity). For this, we studied interaction networks between ants and plants bearing extrafloral nectar sampled over 12 months in a tropical environment on the coast of Mexico. In general, all network descriptors used in this study were influenced by sampling effort via its effects on the record of new ant–plant interactions throughout the year. Interestingly, network specialization and the modularity tended to decrease with the increase of sampling effort, while all the other network descriptors tended to increase along with the sampling effort. Our study highlights the importance of standardizing data sampling in comparative studies to make sure that the results found in studies dealing with ecological networks are reliable, since the intensity of the sampling effort can directly affect the structure of plant–animal interaction networks.