Ant Interactions Research Articles

Structure of ant-diaspore networks and their functional outcomes in a Brazilian Atlantic Forest

Ants are able to interact with fruits and seeds that are not adapted for ant seed dispersal. In Brazil, several studies show interactions of ants with non-myrmecochorous diaspores; however, few of them have studied the structure of ant-fruit networks. The use of the network approach allows visualising multiple interactions between partners and how they are shaped by the community context. Our study aims to investigate ant-fruit networks as well as quantitative and qualitative dispersal components in a fragment of the Brazilian Atlantic Forest. We investigated the structure of interaction networks, diaspore removal rates, diaspore destination and dispersal distance over two years of observation. We constructed three interaction networks: dry season, rainy season and total, with the latter comprising the two formers. The diaspore removal rate, dispersal distance and diaspore destination experiments were performed for the plant species Miconia calvescens, Miconia prasina, Psychotria leiocarpa and Inga edulis. We recorded a large number of interactions, with diaspore cleaning being more frequent than removal. Ant-diaspore networks were nested, non-modular and little specialized. M. calvescens, M. prasina and I. edulis showed higher diaspore removal rates. Diaspore removal distances were the same among M. calvescens, M. prasina and I. edulis. In M. calvescens and I. edulis, the main diaspore destination was the ant’s nest. Our study shows that diaspore cleaning is the most common behavior in ant-diaspore interactions and there are no differences in the organization of interaction networks over the seasons. These results have implications for the future structure of plant communities, considering that a small part of the diaspores is removed, and that most of them are cleaned, favouring germination at the deposition site.

Multi-scale mosaics in top-down pest control by ants from natural coffee forests to plantations.

While top-down control plays an important role in shaping both natural and agricultural food webs, we lack insights into how top-down control effects vary across spatial scales. We used a multi-scale survey of top-down control of coffee pests and diseases by arboreal ants to examine if colony location creates a small-scale mosaic in top-down control around trees and if the strength of that control varies between sites at the landscape scale. We investigated pest and disease levels on coffee shrubs at different distances from shade trees with and without a Crematogaster spp. ant colony in 59 sites along a coffee management intensity gradient in southwestern Ethiopia. Within sites, ants significantly suppressed herbivory and coffee leaf rust at distances less than 10m from nesting trees. Top-down control varied between sites, with stronger top-down control of free-feeding herbivory near ant colonies at sites with lower management intensity and stronger top-down control of a skeletonizer at sites with higher canopy cover. We conclude that the strength of top-down control by ants is highly heterogeneous across spatial scales, as a consequence of the biology of the predator at the small scale and herbivore density or changes in herbivore-ant interactions at the landscape scale.

Interactions of ants with native and invasive lady beetles and the role of chemical cues in intraguild interference

The predator-predator naïveté hypothesis suggests that non-native predators benefit from being unknown to native predators, resulting in reduced intraguild interference with native predators. This novelty advantage should depend on the ability of native predators to recognize cues of non-native predators. Here, we compared ant aggression and lady beetle reaction in four native and the invasive lady beetle species Harmonia axyridis. In addition, we tested whether lady beetle cuticular hydrocarbons (CHCs) are involved in species recognition, which might explain naïveté if the invasive species has a specific CHC profile. To this end, we conducted behavioral assays confronting two native ant species with both living lady beetles and lady beetle elytra bearing or lacking CHCs of different lady beetle species. Finally, we characterized CHC profiles of the lady beetles using GC–MS. In general, the aggression of Lasius niger was more frequent than that of Myrmica rubra and L. niger aggression was more frequent towards most native lady beetle species compared to H. axyridis. The removal of CHCs from lady beetle elytra reduced aggression of both ant species. If CHCs of respective lady beetle species were added on cue-free elytra, natural strength of L. niger aggression could be restored. CHC analyses revealed a distinct cue composition for each lady beetle species. Our experiments demonstrate that the presence of chemical cues on the surface of lady beetles contribute to the strength of ant aggression against lady beetles. Reduced aggression of L. niger towards H. axyridis and reduced avoidance behavior in H. axyridis compared to the equally voracious C. septempunctata might improve the invasive lady beetle’s access to ant-tended aphids.

Chance or Necessity-The Fungi Co-Occurring with Formica polyctena Ants.

Simple SummaryThere are about 13,800 species of ants living around the world, but only some of them have been extensively studied in the context of their non−antagonistic relationships with fungi. The best−known example is the symbiosis between leaf−cutting ants and fungi serving them as food. Others include the relationship between ants living in carton nests in the trees’ canopy with fungi increasing the durability of the nest. Do ants utilize fungi in the northern hemisphere and cooler climatic zone? This question is still open. Our goal was to study the less−obvious interactions between ants and common fungi in temperate climates. In our study, we characterized the mycobiota of the surroundings of Formica polyctena ants. We identified nearly 600 strains and investigated their taxonomic affinity. The most abundant fungi in F. polyctena nests are strains belonging to Penicillium—a genus well−known as an antibiotic producer. Other common and widespread fungi related to Penicillium, such as the toxin−producing Aspergillus species, were isolated very rarely. Additionally, the high diversity and high frequency of Penicillium colonies isolated from ants in this study suggest that certain representatives of this genus may be adapted to survive in ant nests, or that they are preferentially sustained by the insects.Studies on carton nesting ants and domatia−dwelling ants have shown that ant–fungi interactions may be much more common and widespread than previously thought. Until now, studies focused predominantly on parasitic and mutualistic fungi–ant interactions occurring mostly in the tropics, neglecting less−obvious interactions involving the fungi common in ants’ surroundings in temperate climates. In our study, we characterized the mycobiota of the surroundings of Formica polyctena ants by identifying nearly 600 fungal colonies that were isolated externally from the bodies of F. polyctena workers. The ants were collected from mounds found in northern and central Poland. Isolated fungi were assigned to 20 genera via molecular identification (ITS rDNA barcoding). Among these, Penicillium strains were the most frequent, belonging to eight different taxonomic sections. Other common and widespread members of Eurotiales, such as Aspergillus spp., were isolated very rarely. In our study, we managed to characterize the genera of fungi commonly present on F. polyctena workers. Our results suggest that Penicillium, Trichoderma, Mucor, Schwanniomyces and Entomortierella are commonly present in F. polyctena surroundings. Additionally, the high diversity and high frequency of Penicillium colonies isolated from ants in this study suggest that representatives of this genus may be adapted to survive in ant nests environment better than the other fungal groups, or that they are preferentially sustained by the insects in nests.

Abundance, Activity, Diversity, and Species Interactions of Ground-Dwelling Ants (Hymenoptera: Formicidae) in Open Versus Canopied Habitats in Central Georgia (USA)

AbstractThe red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), and ground-dwelling ant species native to Georgia were observed and studied in tree-canopied and open uncanopied habitats in two state parks in central Georgia. Population density, native species diversity, and interactions of native species with each other and with the invasive S. invicta were determined and compared in the two habitats. Sampling methods included pitfall traps, baits, collection of leaf litter, and visual searches. In comparison to the open uncanopied habitats, red imported fire ant population density was lower in tree-canopied habitats, and native ant species diversity was greater in the canopied habitats. We also observed native species competing with red imported fire ants more intensely in canopied than in open habitats primarily by foraging activity and by predation of S. invicta reproductives. Our results suggest that native ant species can suppress S. invicta population numbers and density and that competition by native ant species should be considered in approaches of managing red imported fire ant.

Structure and function of secretory glochids and nectar composition in two Opuntioideae (Cactaceae) species

Cactaceae exhibit highly modified spines that are considered to be extrafloral nectaries (EFNs). Despite their ecological and taxonomical relevance in this family, little is known on their structure and function. We have described the anatomy, ontogenesis, and ultrastructure of the secretory glochids in two Opuntioideae species. Young cladodes of Brasiliopuntia brasiliensis (Willd.) A. Berger and Nopalea cochenillifera (L.) Salm-Dyck were processed for light and electron microscopy studies. The composition of the secretions was analyzed by high performance liquid chromatography. The secretory glochids were soft, massive, and barbed, as well as translucent. Hyaline droplets on the secretory glochid apex were collected by aggressive ants. The secretory glochids originated from the areolar meristem, beginning as small protuberances formed by protoderm and ground meristem. Mature secretory glochids consisted of a central multiseriate axis of ground cells covered by uniseriate epidermis with a continuous cuticle, and exhibited three regions: (i) dilated vascularized base with parenchyma cells exhibiting features associated to nectar secretion; (ii) elongated median region with juxtaposed fusiform non-lignified parenchyma cells; and (iii) tapered apical portion with immature fibers loosely arranged cells. The exudate was sucrose-dominant with a similar amino acid profile in both species. Our results shed light on the secretory activity of glochids in Cactaceae and their role in cactus–ant interactions.

Are ants always mutualistic? Influence of ants and variation in flower-ets of Clerodendrum chinense

Ants are the major mutualists in the plant -ant interaction system playing a major role in the survival of plants by deterring herbivore and increasing plant health and fitness. To get better insights into the ant-plant interaction system, Clerodendrum chinense occupied by Crematogaster roghenoferi were observed for six months to assess the influence of presence and ab-sence of ants on the flowerets blooming.In a total of (n=34) flowerets bunch, 17 were used as control and 17 experimentation that were treated with ant barrier glue to restrict the ants visitation to the flowerets bunch. By using the Students t-test, our study revealed the facultative behaviour of ants. Citing the equal presence of herbivores in both the control and experimented sets, and decreased floweret blooming in anting-continued (control) whereas in-creased floweret blooming in de-anted (experimented). The present study has shown the facultative interaction of C.roghenoferi with C.chinense and its effects on the reproductive structures (flowerets) of the shrub. This study makes a clear case stating that not always an interaction between ant and plant is the mutualism.

Ants Co-Occurring with Predatory Antlions Show Unsuccessful Rescue Behavior towards Captured Nestmates

The interaction of antlions and ants is postulated to be a predator-prey interaction in which the involved parties coevolve. Here, we investigated two issues of potential significance in terms of antlions and ants imposing selective pressures on one another. First, we determined whether trap-building antlions and sand-dwelling ants closely co-occurred in an area inhabited by both. In the field, we found that ants were the main potential prey items in artificial traps placed inside aggregation zones of antlions and that Formica cinerea workers comprised the majority of these ants. Second, we checked whether rescue behavior, a type of prosocial behavior displayed by F. cinerea workers and performed towards nestmates captured by antlions, reduced the hunting success of the latter. In the laboratory, we found that rescue attempts were very rarely successful. Overall, caution must be used when considering the coevolution of antlions and ants. Clearly, even though these two organisms can closely co-occur, the rescue behavior of ants seems to be unrelated to the predatory threat from antlions.

Effect of neighboring seeds associated with habitats on the seed removal of two coexisting myrmecochorous plants in central China

Although neighboring plants can influence animal-seed dispersal interactions, little is known about the effect of neighboring seeds and the influence of habitat on seed dispersal by ants. Here we investigated the influence of neighboring seeds on seed removal in two coexisting myrmecochorous species (Epimedium pubescens and Helleborus thibetanus) from temperate deciduous forests of Qinling Mountains, central China, by examining (1) the potential role of ants and rodents and (2) whether the neighboring seed effect differed between forest edge and interior. We found that, presence of the higher-ESMR (elaiosome: seed mass ratio) E. pubescens did not significantly affect seed removal of the lower-ESMR H. thibetanus. By contrast, the presence of H. thibetanus decreased the seed removal rates of E. pubescens, with only a significant effect in rodent exclusion (ant alone) rather than in both ant exclusion (rodent alone) and full access (rodent+ant). Moreover, we found that those effects were not significantly different between the forest edge and the interior, which may be attributed to a similar pattern of overall seed-dispersing ant abundance in the two habitats. This suggested that neighboring seeds could influence seed removal of the focal plant depending on the absence of rodents; when rodents were present, the interaction of rodents and ants rendered no influence of neighboring seeds on seed removal. Our results show that the neighborhood effect was regulated by both dispersers and predators, and this effect was not context-dependent at a small spatial scale. This study highlights the importance to understand the effect of shared seed-removing animals and habitat context to assess the neighboring seed effect on plant-animal interactions.

Anthropogenic disturbance and rainfall variation threaten the stability of plant–ant interactions in the Brazilian Caatinga

Climate change is projected to exacerbate the effects of anthropogenic disturbance, with negative impacts on ecosystem stability and functioning. We evaluate the additive and combined effects of chronic anthropogenic disturbance (CAD) and rainfall variation on the temporal stability of mutualistic EFN‐bearing plant–ant networks in a Caatinga dry forest. We evaluated whether changes in the stability of these interactions are driven by changes in the stability of the communities of partners involved and/or in ant behavior. We sampled EFN‐bearing plant–ant networks in sixteen 20 × 20 m plots distributed across CAD and rainfall gradients. The stability of EFN‐bearing plant and attendant–ant communities were measured as the inverse of temporal differences in their community structure and composition. We also computed the stability of EFN‐bearing plant–ant networks by measuring the inverse of temporal differences in network specialization metrics. We found that, in general, the structure and composition of plant and ant interacting communities were similarly stable along both environmental gradients. Only CAD and its interaction with rainfall affected the temporal stability of EFN‐bearing plant diversity, which declined as CAD increased, with a more pronounced relationship in wetter areas. However, variation in levels of CAD and, to a lesser extent, rainfall greatly modulated the stability of EFN‐bearing plant–ant network specialization. CAD reduced the stability of network generality (specialization at the ant level), an effect that was much stronger in wetter areas. Meanwhile, the stability in network vulnerability (specialization at the plant level) decreased with the increase of CAD and the decrease of rainfall levels. Finally, there was a trend of decreasing stability in specialization of the overall network with increasing CAD. Our results suggest that changes in the structure of interaction networks are mainly driven by a switch in ant behavior rather than by changes in the structure and composition of plant and ant communities between years.

Social immunity behaviour among ants infected by specialist and generalist fungi.

Social insects are distinguished by their lifestyle of living in groups with division of labour, cooperative brood care, and reproduction limited to a few colony members. Social insects often build large colonies with remarkable densities of highly related individuals and this can lead to an increased pathogen pressure. Our review focuses on interactions of ants with two important taxonomic groups of fungi infecting ants: Hypocreales (Ascomycota) and Entomophthorales (Entomophthoromycotina), and their different infection strategies, including host manipulation for optimal spore dispersal in the specialised ant pathogens. In social insects such as ants, resistance to pathogens is present at the colony level, with social immunity in addition to the individual resistance. We describe how ants use both organizational and behavioural defence strategies to combat fungal pathogens, with emphasis on highly specialised fungi from the genera Ophiocordyceps and Pandora.

A Dynamic Individual-Based Model for High-Resolution Ant Interactions

Ant feeding interactions (i.e., trophallaxis events) are thought to regulate the flow of nutrients and disease within a colony. Consequently, there is great interest in learning which environmental and behavioral factors drive ant trophallaxis. In this paper, we analyze ant trophallaxis behavior in a colony of 73 carpenter ants, observed at 1-s intervals over a period of 4 h. The data represent repeated observations from a dynamic contact network; however, traditional statistical analyses of network models are ill-suited for data observed at such high temporal resolution. We present a model for high-resolution longitudinal network data, where the network is assumed to be a time inhomogeneous, continuous-time Markov chain, with transition rates modeled as a function of time-varying individual and pairwise biological covariates. In particular, the high temporal resolution of the data leads to a tractable likelihood function, and likelihood-based inference procedures are utilized to explain which biological factors drive contact. Our results reveal how differences in ant social castes and individual behaviors, such as ant speed and activity levels, influence patterns of ant trophallaxis in the colony. Supplementary materials accompanying this paper appear online.

The scent of symbiosis: gut bacteria may affect social interactions in leaf-cutting ants

Animal gut microbiota affect host physiology and behaviour. In social insects, where colony level integrity is preserved via a nestmate discrimination system based on cuticular hydrocarbon mixtures, microorganismal effects may therefore influence social dynamics. Although nestmate recognition has undergone a thorough exploration during the last four decades, few studies have investigated the putative role of gut microbes. Here, we integrated 16S rRNA-based microbial community profiling, chemical and behavioural approaches to test whether gut microbes affect nestmate recognition in Acromyrmex echinatior leaf-cutting ants. Treating workers with a sterile diet or with antibiotics resulted in a substantial alteration of their gut microbial communities. In pairwise social interactions, untreated versus antibiotic-treated nestmates behaved more aggressively than other nestmate and non-nestmate pairs, suggesting that bacterial suppression may alter chemical social cues and trigger aggressive behaviour. Chemical analyses of treated individuals revealed a decrease in the abundance of two metapleural gland antifungal compounds, and confirmed the correspondence between aggression levels and chemical profile differences. Feeding microbiota-remodelled ants with conspecific faecal droplets partially restored the original bacterial communities. Ants fed with faecal droplets from different colonies were unusually aggressive compared to pairs fed with faecal droplets from the same colony. We cannot exclude confounding effects resulting from the potentially harmful action of antibiotics on ant hosts. However, our results suggest a correlation between chemical profiles and the presence of certain microbial species in the gut, which may affect nestmate recognition and division of labour. This opens novel questions about the role of symbiotic microorganisms in the evolution of social insect behaviour.

Tree diversity increases robustness of multi-trophic interactions.

Multi-trophic interactions maintain critical ecosystem functions. Biodiversity is declining globally, while responses of trophic interactions to biodiversity change are largely unclear. Thus, studying responses of multi-trophic interaction robustness to biodiversity change is crucial for understanding ecosystem functioning and persistence. We investigate plant-Hemiptera (antagonism) and Hemiptera-ant (mutualism) interaction networks in response to experimental manipulation of tree diversity. We show increased diversity at both higher trophic levels (Hemiptera and ants) and increased robustness through redundancy of lower level species of multi-trophic interactions when tree diversity increased. Hemiptera and ant diversity increased with tree diversity through non-additive diversity effects. Network analyses identified that tree diversity also increased the number of tree and Hemiptera species used by Hemiptera and ant species, and decreased the specialization on lower trophic level species in both mutualistic and antagonist interactions. Our results demonstrate that bottom-up effects of tree diversity ascend through trophic levels regardless of interaction type. Thus, local tree diversity is a key driver of multi-trophic community diversity and interaction robustness in forests.

Ophiocordyceps-ant interactions as an integrative model to understand the molecular basis of parasitic behavioral manipulation.

Ophiocordyceps-infected ants display a substrate biting behavior that aids parasite transmission. World-wide research into this behavioral manipulation has led to new fungal species descriptions, annotated genomes, and detailed field observations. Experimentally tractable modified ant behaviors and the development of infection techniques have enabled the quest for the molecular basis of this phenomenon. Behavioral studies followed by transcriptomics, metabolomics and three-dimensional electron microscopy have led to novel mechanistic hypotheses. This multidisciplinary work represents a big leap forward. However, definitive answers have yet to be obtained. A comprehensive understanding hinges on continued integrative efforts that reveal the precise natural history, behavioral ecology and evolutionary relationships between Ophiocordyceps-ant systems, and the true functions and involvement of genes and metabolites in behavioral manipulation.

Today and tomorrow: impact of climate change on aphid biology and potential consequences on their mutualism with ants

AbstractRecent studies about mutualism consider the complexity and versatility of the relationship, in addition to highlighting the importance of the cost/benefit balance between the two protagonists. Because species interactions are highly dependent on the environment, the climate changes foreseen for the coming years are expected to have significant impacts on the evolution of mutualistic interactions. Among mutualisms, the aphid–ant interaction is well documented, partly explained by the pest status of aphids. This literature review focuses on the impact of climate change (particularly atmospheric carbon dioxide concentration and temperature) on aphid biology and the potential consequences with respect to their mutualistic interactions with ants. We provide an overview of the published reports concerned with the effects of temperature and carbon dioxide on aphids, for which a positive, a negative or no effect has been highlighted. We then discuss how climatic changes can alter four major components of aphid biology that are shaping their interaction with ants: (i) aphid population growth; (ii) aphid behaviour and mobility; (iii) honeydew production and composition; and (iv) semiochemistry. Finaly, we discuss the limitations of such studies on aphid–ant mutualism, as well as the information that is still needed to predict how climate change might impact this type of relationship.

Fungus-Growing Ant's Microbial Interaction of Streptomyces sp. and Escovopsis sp. through Molecular Networking and MALDI Imaging

Microbes associated with fungus-growing ants represent a poorly explored source of natural products. In this study, we used mass spectrometry-based dereplication techniques for identifying a set of secondary metabolites produced during the microbial interaction between Streptomyces sp. (CB0028) and Escovopsis sp. (CBAcro424). Both microorganisms were isolated from the nest of the fungus-growing ant Acromyrmex echinatior. Through MALDI imaging and MS/MS molecular networking, we annotated the siderophores: desferrioxamine B (1), ferrioxamine B (2), ferrioxamine E (3) and the N-formylated peptide SCO-2138/SLI-2138 (4). MALDI imaging experiments suggest that siderophores occurred during the microbial interactions in the fungus-growing ants – microbes symbioses. This is the first report on the production of compounds 1-4 by bacteria associated with fungus-growing ants.

Viral infections in fire ants lead to reduced foraging activity and dietary changes

Despite the presence of conserved innate immune function, many insects have evolved a variety of mechanical, chemical, and behavioral defensive responses to pathogens. Illness-induced anorexia and dietary changes are two behavioral defensive strategies found in some solitary insects, but little is known regarding the role of such behaviors in social insects, especially in ants. In the present study we examined if such reduced foraging activity exists for a social insect, the invasive fire ant Solenopsis invicta, and its viral pathogen, Solenopsis invicta virus 1 (SINV-1). Virus-free fire ant colonies were split into two colony fragments, one of which subsequently was inoculated with SINV-1. Four food resources with different macronutrient ratios were presented to both colony fragments. SINV-1-inoculated colony fragments consistently displayed reduced foraging performance (e.g., foraging intensity and recruitment efficiency), a decline in lipid intake, and a shift in dietary preference to carbohydrate-rich foods compared with virus-free fragments. These findings provide the first evidence for virus-induced behavioral responses and dietary shifts in shaping the host-pathogen interactions in fire ants. The findings also suggest a possible mechanism for how fire ant colonies respond to viral epidemics. Potential implications of these behavioral differences for current management strategies are discussed.

Success of aphid parasitoids and their hosts varies with ant attendance: A field study

AbstractAphid–ant associations are often described as mutually beneficial interactions in which honeydew is traded for protection from predators and parasitoids. The aim of the present study was to determine parasitization avoidance in ant‐tended aphid colonies. Field experiments were carried out on two host plants: hoary cress Lepidium draba (Brassicaceae) and Canadian teasel Cirsium arvense (Asteraceae). Lepidium was host to Acyrthosiphon gossypii (Aphididae) tended by the ant Lasius turcicus (Formicidae) and attacked by two parasitoids, Trioxys asiaticus (Braconidae) and Lysiphlebus fabarum (Braconidae). Cirsium was host to Brachycaudus cardui tended by Crematogaster sordidula and attacked by L. fabarum and Aphidius colemani (Braconidae). The per capita population growth rate of A. gossypii was significantly higher in the presence of ants, while B. cardui was negatively affected, albeit non‐significantly. The parasitism rate of A. gossypii decreased significantly when tended by Lasius turcicus, but the presence of Crematogaster sordidula in colonies of B. cardui significantly increased parasitism. Our results indicate that the effects of ant attendance vary between different aphid–ant interactions. Moreover, parasitoids can benefit from the presence of ants under some conditions.

Effect of tropical forest disturbance on the competitive interactions within a diverse ant community

Understanding how anthropogenic disturbance influences patterns of community composition and the reinforcing interactive processes that structure communities is important to mitigate threats to biodiversity. Competition is considered a primary reinforcing process, yet little is known concerning disturbance effects on competitive interaction networks. We examined how differences in ant community composition between undisturbed and disturbed Bornean rainforest, is potentially reflected by changes in competitive interactions over a food resource. Comparing 10 primary forest sites to 10 in selectively-logged forest, we found higher genus richness and diversity in the primary forest, with 18.5% and 13.0% of genera endemic to primary and logged respectively. From 180 hours of filming bait cards, we assessed ant-ant interactions, finding that despite considered aggression over food sources, the majority of ant interactions were neutral. Proportion of competitive interactions at bait cards did not differ between forest type, however, the rate and per capita number of competitive interactions was significantly lower in logged forest. Furthermore, the majority of genera showed large changes in aggression-score with often inverse relationships to their occupancy rank. This provides evidence of a shuffled competitive network, and these unexpected changes in aggressive relationships could be considered a type of competitive network re-wiring after disturbance.