Small-scale indirect effects determine the outcome of a tripartite plant–disperser–granivore interaction

The microhabitat in which plants grow affects the outcome of their interactions with animals, particularly non-specialist consumers. Nevertheless, as most research on this topic has dealt with either mutualists or antagonists, little is known about the indirect effects of plant microhabitats on the outcome of tripartite interactions involving plants and both mutualists (e.g. seed dispersers) and antagonists (e.g. granivores). During three consecutive years, we analysed small-scale variations in the interaction of a perennial myrmecochore, Helleborus foetidus, with its seed dispersers and consumers as a function of the intensity of plant cover. Most seeds were released during the day and were rapidly removed by ants. Nevertheless, the proportion of ant-removed seeds was higher for plants located in open microhabitats than for plants surrounded by dense vegetation and rocky cover. Ant sampling revealed that seed removers were equally abundant, irrespective of the level of cover. By contrast, a few tiny ant species that feed on the reward without transporting the seeds were more abundant in highly covered microhabitats, irrespective of hellebore diaspore availability. These “cheaters” decrease the chance of removal by removers and increase the probability of seeds remaining on the ground until night, when granivore mice Apodemus sylvaticus become active. Mice also preferred foraging in covered microhabitats, where they consumed a larger proportion of seeds. Therefore, the density of cover indirectly increased seed predation risk by attracting more seed predators and cheater ants that contribute to increase seed availability for seed predators. Our results emphasize the importance of considering the indirect effects of plant microhabitat on their dispersal success. They highlight the indirect effect of cheaters that are likely to interfere in mutualisms and may lead to their collapse unless external factors such as spatio-temporal heterogeneity in seed availability constrain their effect. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Ants on plants: a meta-analysis of the role of ants as plant biotic defenses

We reviewed the evidence on the role of ants as plant biotic defenses, by conducting meta-analyses for the effects of experimental removal of ants on plant herbivory and fitness with data pooled from 81 studies. Effects reviewed were plant herbivory, herbivore abundance, hemipteran abundance, predator abundance, plant biomass and reproduction in studies where ants were experimentally removed (n = 273 independent comparisons). Ant removal exhibited strong effects on herbivory rates, as plants without ants suffered almost twice as much damage and exhibited 50% more herbivores than plants with ants. Ants also influenced several parameters of plant fitness, as plants without ants suffered a reduction in biomass (−23.7%), leaf production (−51.8%), and reproduction (−24.3%). Effects were much stronger in tropical regions compared to temperate ones. Tropical plants suffered almost threefold higher herbivore damage than plants from temperate regions and exhibited three times more herbivores. Ant removal in tropical plants resulted in a decrease in plant fitness of about 59%, whereas in temperate plants this reduction was not statistically significant. Ant removal effects were also more important in obligate ant–plants (=myrmecophytes) compared to plants exhibiting facultative relationships with hemiptera or those plants with extrafloral nectaries and food bodies. When only tropical plants were considered and the strength of the association between ants and plants taken into account, plants with obligate association with ants exhibited almost four times higher herbivory compared to plants with facultative associations with ants, but similar reductions in plant reproduction. The removal of a single ant species increased plant herbivory by almost three times compared to the removal of several ant species. Altogether, these results suggest that ants do act as plant biotic defenses, but the effects of their presence are more pronounced in tropical systems, especially in myrmecophytic plants. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. N. P. de U. Barbosa, L. Diniz, Y. Oki and F. Pezzini contributed equally to this work and are listed in alphabetical order.     

Ant behaviour and seed morphology: a missing link of myrmecochory

Seed dispersal by ants (myrmecochory) is mediated by the presence of a lipid-rich appendage (elaiosome) on the seed that induces a variety of ants to collect the diaspores. When seeds mature or fall onto the ground, these ant species transport them to their nest. After eating the elaiosome, the seed is discarded in nest galleries or outside, in the midden or farther away, where seeds can potentially germinate. The final location of seeds with their elaiosomes removed was evaluated to assess the importance of possible handles (structures that ants can grasp to carry) in transporting ants during re-dispersal experiments of seeds from nests of six species of ants. The results indicate that seeds remained within the nest because the ants were not able to transport them out of the nest. As a consequence of the elaiosome being removed, small ant species could not take Euphorbia characias seeds out of their nests. Only large ant species could remove E. characias seeds from their nests. Attaching an artificial handle to E. characias seeds allowed small ant species to redistribute the seeds from their nests. On the other hand, Rhamnus alaternus seeds that have a natural handle after the elaiosome removal were removed from the nests by both groups of ant species. If a seed has an element that acts as a handle, it will eventually get taken out of the nest. The ants’ size and their mandible gap can determine the outcome of the interaction (i.e. the pattern of the final seed shadow) and as a consequence, could influence the events that take place after the dispersal process.     

Colony growth in <Emphasis Type="Italic">Myrmica rubra</Emphasis> with supplementation of myrmecochorous seeds

Myrmecochory is an important ant–plant relationship, which presumably has benefits for the reproductive success of ant colonies through the nutritional value of elaiosomes. In a feeding experiment, we provided elaiosomes of Scilla bifolia and Corydalis cava to colonies of Myrmica rubra. Seeds were transported by ant workers to their nests and the elaiosomes were removed afterwards. After 3 months, elaiosome-supplemented colonies contained significantly more worker pupae than control colonies, whereas the number of new female sexuals was reduced. This result is discussed as a possible long-term benefit for M. rubra colonies through myrmecochory by colony growth.     

Spatial variation in the fatty acid composition of elaiosomes in an ant-dispersed plant: Differences within and between individuals and populations

Euphorbia characias is a common myrmecochorous plant of the western Mediterranean Basin whose seeds are dispersed by ants following fruit explosion. The variation in elaiosomes’ fatty acid composition of this species was studied at three hierarchical levels (sub-individual, individual and population) in four populations from the Iberian Peninsula. We found that differences in fruit location on the inflorescence do not seem to influence the fatty acid composition of elaiosomes, providing to each propagule an equal chance of being dispersed. However, significant differences in elaiosome fatty acid composition between individuals and populations were found for most of the compounds identified. The content of oleic acid, a key mediator in the ant–seed interaction, differed widely between populations, probably reflecting geographic variations in co-adaptation between plants and their dispersers. The finding that the fatty acid composition of E. characias elaiosomes is distinct from that of the seed itself, but very similar to that of elaiosomes from unrelated species, reinforces the idea of convergent evolution in the chemical composition of these structures.     

Size and lipid content of nonmyrmecochorous diaspores: effects on the interaction with litter-foraging ants in the Atlantic rain forest of Brazil

Ants are often attracted to diaspores not adapted for dispersal by ants. These diaspores may occasionally benefit from this interaction. We selected six nonmyrmecochorous plant species (Virola oleifera, Eugenia stictosepala, Cabralea canjerana, Citharexylum myrianthum, Alchornea glandulosa and Hyeronima alchorneoides) whose diaspores differ in size and lipid content, and investigated how these features affect the outcome of ant-diaspore interactions on the floor of a lowland Atlantic forest of Southeast Brazil. A total of 23 ant species were seen interacting with diaspores on the forest floor. Ants were generally rapid at discovering and cleaning the diaspore pulp or aril. Recruitment rate and ant attendance were higher for lipid-rich diaspores than for lipid-poor ones. Removal rate and displacement distance were higher for small diaspores. The large ponerine ant Pachycondyla striata, one of the most frequent attendants to lipid-rich arillate diaspores, transported the latter into their nests and discarded clean intact seeds on refuse piles outside the nest. Germination tests with cleaned and uncleaned diaspores revealed that the removal of pulp or aril may increase germination success in Virola oleifera, Cabralea canjerana, Citharexylum myrianthum and Alchornea glandulosa. Gas chromatography analyses revealed a close similarity in the fatty acid composition of the arils of the lipid-rich diaspores and the elaiosome of a typical myrmecochorous seed (Ricinus communis), corroborating the suggestion that some arils and elaiosomes are chemically similar. Although ant-derived benefits to diaspores – secondary dispersal and/or increased germination – varied among the six plant species studied, the results enhanced the role of ant-diaspore interactions in the post-dispersal fates of nonmyrmecochorous seeds in tropical forests. The size and the lipid-content of the diaspores were shown to be major determinants of the outcome of such interactions.     

Secondary seed dispersal by ants in Neotropical cerrado savanna: species‐specific effects on seeds and seedlings of Siparuna guianensis (Siparunaceae)

1. Most woody plant species in tropical habitats are primarily vertebrate‐dispersed, but interactions between ants and fallen seeds and fruits are frequent. This study assesses the species‐specific services provided by ants to fallen arillate seeds of Siparuna guianensis, a primarily bird‐dispersed tree in cerrado savanna. The questions of which species interact with fallen seeds, their relative contribution (versus vertebrates) to seed removal, and the potential effects on seedling establishment are investigated. 2. Seeds are removed in similar quantities in caged and control treatments, suggesting that ants are the main dispersers on the ground. Five ant species attended seeds. Pheidole megacephala (≈0.4 cm) cooperatively transported seeds, whereas the smaller Pheidole sp. removed the seed aril on spot. Large (> 1.0 cm) Odontomachus chelifer, Pachycondyla striata, and Ectatomma edentatum individually carried seeds up to 4 m. Bits of aril are fed to larvae and intact seeds are discarded near the nest entrance. 3. Overall, greater numbers of seedlings were recorded near ant nests than in control plots without nests. This effect, however, was only detected near P. megacephala and P. striata nests, where soil penetrability was greater compared with controls. Soil nutrients did not differ between paired plots. 4. This study confirms the prevalence of ant–seed interactions in cerrado and shows that ant‐derived benefits are species‐specific. Ant services range from seed cleaning on the spot to seed displacement promoting non‐random spatial seedling recruitment. Although seed dispersal distances by ants are likely to be shorter than those by birds, our study of S. guianensis shows that fine‐scale ant‐induced seed movements may ultimately enhance plant regeneration in cerrado.     

Interaction between ants and seeds of a nonmyrmecochorous neotropical tree, Cabralea canjerana (Meliaceae), in the Atlantic forest of southeast Brazil

On the forest floor of two Atlantic forest sites in southeast Brazil, we recorded 26 ant species (12 genera) interacting with the seeds of Cabralea canjerana (Meliaceae), a typical ornithochorous tree whose seeds are covered by a lipid-rich aril. The ants treat the arillate seeds in three different ways: (1) the large ponerine ants Pachycondyla striata and Odontomachus chelifer individually remove the seeds to their nests, (2) many species (Pheidole spp.) recruit workers to remove the aril on the spot, or (3) Solenopsis spp. recruit nestmates and cover the seeds with soil before removing the aril on the spot. The ants remove the aril exceptionally rapidly, and removal greatly facilitates seed germination. Seed predation by insects below fruiting trees is severe, and field experiments using vertebrate exclosures showed that rodents also prey heavily upon seeds found near parent trees. Ponerine ants actively remove seeds from this predation-prone zone. By removing bird-manipulated and naturally fallen seeds, ants can play a key role in the fate of medium-sized seeds like those of C. canjerana.     

Comments on relationships between native seed preferences of shrub-steppe granivores and seed nutritional characteristics

Summary Kelrick et al. (1986) argued that seed preferences of desert granivores are strongly influenced by soluble carbohydrate contents of native seed species. They assumed that bitterbrush (Purshia tridentata) seeds are eaten in their entirety by rodents, but in fact these granivores eat only embryos of bitterbrush seeds. Embryos have a much lower percentage of soluble carbohydrate than whole bitterbrush seeds, and the correlation between preference and soluble carbohydrate content of seeds for six native species becomes non-significant when embryo values are substituted for whole-seed values.     

Importance of elaiosome size to removal of ant-dispersed seeds

Several studies relate removal of diaspores from different ant-dispersed plant species to the size of their claiosomes. This study is the first one to relate intraspecific variation in claiosome size to removal of diaspores by ants. This approach circumvents the problem posed by interspecific variation in chemistry and morphology of elaiosomes. We used the systemHepatica nobilis Mill. (Ranunculaceae) andMyrmica ruginodis Nyl. The elaiosome was the attractive part of the diaspore and its attractiveness decreased quickly after release from the fruit. In experimental runs where ants collected diaspores, the elaiosome size of accepted diaspores was larger than of those rejected and the largest diaspores were collected first. Since size of diaspore, elaiosome and achene were correlated, the diaspores that were removed first had both the largest elaiosome and achene. However, our experiments suggested that elaiosome size was more important to removal than achene size or the elaiosome:achene size ratio. If ant dispersal improves plant fitness, elaiosome size and hence diaspore size would be expected to increase over time. However, such directional selection mediated by the ants is probably counterbalanced by the plant. Seed predators and a negative trade-off between number and size of seeds would, among other factors, select for smaller diaspore size,i.e. counteract the effect of the ants' preference for larger elaiosomes.     

Interaction between ants and fruits of<Emphasis Type="Italic"> Guapira opposita</Emphasis> (Nyctaginaceae) in a Brazilian sandy plain rainforest: ant effects on seeds and seedlings

This study examines the dispersal system of Guapira opposita in a tropical sandy rainforest in southeast Brazil. Guapira trees produce small fruits with a high protein content (28.4%) and low lipid content (0.3%), and the plant is primarily dispersed by birds. Mature fruits of G. opposita can fall spontaneously with the pulp intact, or be dropped by birds with bits of pulp attached. In either case, ground-dwelling ants rapidly remove the fruits to their nest (93% after 12 h). The ponerine ants Odontomachus chelifer and Pachycondyla striata are the main seed vectors among the ants, and together account for 56% (20 of 36) of the ant-fruit interactions recorded on the forest floor. Individual workers of O. chelifer and P. striata transport single fruits to their nests. Bits of pulp are fed to larvae and worker nestmates, and intact seeds are discarded outside the nest. Germination success in Guapira is higher for cleaned seeds (pulp removed) than for seeds coated by pulp. Guapira seedlings and juveniles are more frequent close to Odontomachus nests than at sites without such nests. Soil samples from Odontomachus nests had greater penetrability, and higher concentrations of P, K, and Ca than random soil samples. Field experiments suggest that the association between G. opposita seedlings and O. chelifer nests can potentially render the plant some protection against herbivores. Results indicate that fruit displacement by ponerine ants play an important role in the biology of G. opposita seeds and seedlings in the sandy forest, and illustrate the complex nature of the dispersal ecology of tropical tree species.     

Interactions between Ants and Non‐myrmecochorous Fruits in Miconia (Melastomataceae) in a Neotropical Savanna

The aim of this study was to evaluate the role of ants as secondary seed dispersers of six primarily bird‐dispersed Miconia species in the cerrados of southeastern Brazil. Vertebrate exclosure and seed germination experiments were performed for M. albicans, M. alborufescens, M. corallina, M. ferruginata, M. ibaguensis, and M. irwinii. Excluding vertebrates did not significantly alter fruit removal rate for any of the Miconia species relative to open controls. Fruits on stalks and fallen fruits were removed and transported to nests mainly by species of Atta, Acromyrmex, and Ectatomma (dispersal distance ranging from 0.1 to 45.2 m), while Camponotus ants tended to be observed removing the fruit pulp (seed cleaning) where the fruits were found. Seed manipulation by Atta decreased germination of M. irwinii, but not M. ferruginata. Germination did not occur in intact fruits, and thus seed cleaning was an important service provided by the ants. Ant nest soils did not inhibit germination of any of the Miconia species, suggesting they are a good substrate for long‐lived Miconia seeds. We conclude that ant activity could have important effects on the fate of Miconia seeds adapted for bird dispersal.     

A test of the escape and colonization hypotheses for zoochorous tree species in a Western Amazonian forest

In order to assess the importance of seed dispersal (escape and colonization hypotheses), I used transplant experiments for seeds and seedlings of 5–11 plant species with fleshy fruits in a lowland tropical forest (Tinigua National Park, Colombia). I controlled seed density, distance to parental tree, and habitat type. I monitored seed removal, seedling survival, and seedling growth during the first year of development for an average of 554 seeds and 169 seedlings for each species. I supplemented the experimental results with measurements of natural recruitment. I found little support for the escape hypothesis during the seed and seedling stages. For six species that showed differences in seed removal associated with distance, five showed highest removal away from, than close to parent trees, suggesting predator satiation. Seedling survival during the first year was not consistently associated with low densities and long distances from parent trees. For the majority of species, seedlings did not survive flooding in low basins, and there was growth advantage for most plant species in canopy gaps. These differences imply advantages for seed dispersal to adequate habitats, as predicted by the colonization hypothesis. In contrast to experiments, strong negative distance-dependent effects were evident when analyzing natural recruitment patterns. The ratio between saplings and seedlings was higher away from parent trees for the species with enough recruitment to be analyzed and this suggests that a negative distance-dependent effect may also occur after seedling establishment. This pattern is suspected for several other species, but an analysis with some of the other most common trees showed a variety of negative, neutral, and positive distance dependent effects. This study emphasizes the importance of long-term studies to asses the role of seed dispersal.     

Preliminary Study of Chemical Composition of the Elaiosome of Sloanea hemsleyana (lto) and Its Ecological Function to Attract Dispersal Agent

The chemical composition of the elaiosome of Sloanea hemsleyana (Elaeocarpaceae) was analyzed by gas chromatography mass spectrometry. The relative content of each compound was determined by area normalization. Eleven compounds were identified, accounting for 97.6% of the total oil composition. The major compounds were Palmitic acid (36.0%) and Oleic acid (35.0%), which were favour food for ant. And it was demonstrated that the seed of S.hemsleyana can be dispersed by ant Pheidole sp. in the habitat of Kunming Botanical Garden. As for the defensive function of elaiosome of S.hemsleyana need to be identified in field.     

Seed characteristics and susceptibility to pathogen attack in tree seeds of the Peruvian Amazon

Many studies now suggest that pathogens can cause high levels of mortality in seeds and seedlings. Recruitment from seed to sapling is an important bottleneck for many tree species, and if specialist or generalist pathogens have differential negative effects among species of juvenile trees, then they may have a significant impact on forest community structure. To explore the effects of differential pathogen attack among tropical tree species, we quantified pathogen attack on the seeds of 16 tree species from the southeastern Peruvian Amazon and asked which seed characteristics, including size, hardness, germination time and mode, shade tolerance, and fruit type, were most closely correlated with susceptibility to pathogens. Shade tolerance and seed weight were positively and significantly correlated with susceptibility to pathogen attack by ecological trait regressions (ETRs), and correspondence analysis indicated that there might be increased attack rates in species with brightly colored, pulpy fruits (often dispersed by primates). Only shade tolerance was significantly correlated with pathogen attack when the analyses accounted for phylogenetic relatedness between species. Thus, contrary to standard predictions of size-defense ratios, our results suggest that larger, shade-tolerant seeds tend to be more susceptible to pathogen attack than smaller, light-dependent seeds. Moreover, differential pathogen attack may shape seed community composition, which may affect the successful recruitment of adults.     

The fitness consequences of bearing domatia and having the right ant partner: experiments with protective and non-protective ants in a semi-myrmecophyte

The fitness advantage provided by caulinary domatia to myrmecophytes has never been directly demonstrated because most myrmecophytic species do not present any individual variation in the presence of domatia and the removal of domatia from entire plants is a destructive process. The semi-myrmecophytic tree, Humboldtia brunonis (Fabaceae: Caesalpinioideae), is an ideal species to investigate the selective advantage conferred by domatia because within the same population, some plants are devoid of domatia while others bear them. Several ant species patrol the plant for extra-floral nectar. Fruit production was found to be enhanced in domatia-bearing trees compared to trees devoid of domatia independent of the ant associate. However, this domatium effect was most conspicuous for trees associated with the populous and nomadic ant, Technomyrmex albipes. This species is a frequent associate of H. brunonis, inhabiting its domatia or building carton nests on it. Ant exclusion experiments revealed that T. albipes was the only ant to provide efficient anti-herbivore protection to the leaves of its host tree. Measures of ant activity as well as experiments using caterpillars revealed that the higher efficiency of T. albipes was due to its greater patrolling density and consequent shorter lag time in attacking the larvae. T. albipes also provided efficient anti-herbivore protection to flowers since fruit initiation was greater on ant-patrolled inflorescences than on those from which ants were excluded. We therefore demonstrated that caulinary domatia provide a selective advantage to their host-plant and that biotic defence is potentially the main fitness benefit mediated by domatia. However, it is not the sole advantage. The general positive effect of domatia on fruit set in this ant–plant could reflect other benefits conferred by domatia-inhabitants, which are not restricted to ants in this myrmecophyte, but comprise a large diversity of other invertebrates. Our results indicate that mutualisms enhance the evolution of myrmecophytism.     

Linking traits of foraging animals to spatial patterns of plants: social and solitary ants generate opposing patterns of surviving seeds

Foraging traits of seed predators are expected to impact the spatial structure of plant populations, community dynamics and diversity. Yet, many of the key mechanisms governing distance- or density-dependent seed predation are poorly understood. We designed an extensive set of field experiments to test how seed predation by two harvester ant species interact with seed dispersal in shaping the spatial patterns of surviving seeds. We show that the Janzen–Connell establishment pattern can be generated by central-place foragers even if their focal point is located away from the seed source. Furthermore, we found that differences in the social behaviour of seed predators influence their sensitivity to seed density gradients and yield opposing spatial patterns of surviving seeds. Our results support the predictions of a recent theoretical framework that unifies apparently opposing plant establishment patterns, and suggest that differences in foraging traits among seed predators can drive divergent pathways of plant community dynamics.     

Negative correlation between altitudes and oxygen isotope ratios of seeds: exploring its applicability to assess vertical seed dispersal

Vertical seed dispersal, which plays a key role in plant escape and/or expansion under climate change, was recently evaluated for the first time using negative correlation between altitudes and oxygen isotope ratio of seeds. Although this method is innovative, its applicability to other plants is unknown. To explore the applicability of the method, we regressed altitudes on δ¹⁸O of seeds of five woody species constituting three families in temperate forests in central Japan. Because climatic factors, including temperature and precipitation that influence δ¹⁸O of plant materials, demonstrate intensive seasonal fluctuation in the temperate zone, we also evaluated the effect of fruiting season of each species on δ¹⁸O of seeds using generalized linear mixed models (GLMM). Negative correlation between altitudes and δ¹⁸O of seeds was found in four of five species tested. The slope of regression lines tended to be lower in late‐fruiting species. The GLMM analysis revealed that altitudes and date of fruiting peak negatively affected δ¹⁸O of seeds. These results indicate that the estimation of vertical seed dispersal using δ¹⁸O of seeds can be applicable for various species, not just confined to specific taxa, by identifying the altitudes of plants that produced seeds. The results also suggest that the regression line between altitudes and δ¹⁸O of seeds is rather species specific and that vertical seed dispersal in late‐fruiting species is estimated at a low resolution due to their small regression slopes. A future study on the identification of environmental factors and plant traits that cause a difference in δ¹⁸O of seeds, combined with an improvement of analysis, will lead to effective evaluation of vertical seed dispersal in various species and thereby promote our understanding about the mechanism and ecological functions of vertical seed dispersal.     

Exclusive frugivory and seed dispersal of Rhamnus alaternus in the bird breeding season

We studied avian frugivory and seed dispersal in a dioecious shrub, Rhamnus alaternus, focusing on the quantitative and qualitative components of effectiveness. The study took place at three locations in the northeast of the Iberian Peninsula, and examined bird behaviour, intensity of feeding, and the consequences for seedling emergence. The coincidence between the bird breeding season and fruit ripening of R. alaternus in the absence of other ripe fruit, generates a monospecific interaction. The extant frugivorous species were mainly legitimate seed dispersers and their abundance was low. Sylvia melanocephala and S. undata were the most important at one site whereas S. atricapilla, Erithacus rubecula and Turdus merula predominated at the other two sites. Fruit handling took place directly on the branches. Bird species used microhabitats differently as first post-feeding perch, which usually was a short distance away. The low density of frugivorous birds in all localities, among others factors, resulted in satiation of the disperser community and many mature fruits unconsumed. Both adults and juveniles feed upon the plants and their foraging patterns are similar. Adults of S. melanocephala were observed to feed fruit to nestlings and consequently a second phase of dispersal potentially arises from the transport of fecal sacs. Pulp removal and passage through the digestive tract increased the probability of seedling emergence. This plant-dispersal interaction has important consequences, both positive and negative for the plant. Positively, the fruiting of R. alaternus at a time when other ripe fruits are not available avoids interspecific competition for seed dispersers. In addition, a low density of seed rain may reduce intraspecific competition. Negatively, the low density and small size of the breeding frugivorous bird community limit fruit handling and removal away from the parent plants, while the territorial behaviour of birds at that time of the year reduces the potential distances of seed dispersal.     

A facultative mutualism between aphids and an invasive ant increases plant reproduction

1. The consequences to plants of ant–aphid mutualisms, particularly those involving invasive ants, are poorly studied. Ant–aphid mutualisms may increase or decrease plant fitness depending on the relative cost of herbivory by ant‐tended aphids versus the relative benefit of increased ant suppression of other (non‐aphid) herbivores. 2. We conducted field and greenhouse experiments in which we manipulated the presence and absence of cotton aphids (Aphis gossypii) on cotton plants to test the hypothesis that a mutualism between cotton aphids and an invasive ant, the red imported fire ant (Solenopsis invicta), benefits cotton plants by increasing fire ant suppression of caterpillars. We also manipulated caterpillar abundance to test whether the benefit of the mutualism varied with caterpillar density. 3. We found that more fire ants foraged on plants with cotton aphids than on plants without cotton aphids, which resulted in a significant reduction in caterpillar survival and caterpillar herbivory of leaves, flower buds, and bolls on plants with aphids. Consequently, cotton aphids indirectly increased cotton reproduction: plants with cotton aphids produced 16% more bolls, 25% more seeds, and 10% greater seedcotton mass than plants without aphids. The indirect benefit of cotton aphids, however, varied with caterpillar density: the number of bolls per plant at harvest was 32% greater on plants with aphids than on plants without aphids at high caterpillar density, versus just 3% greater at low caterpillar density. 4. Our results highlight the potential benefit to plants that host ant–hemipteran mutualisms and provide the first experimental evidence that the consequences to plants of an ant–aphid mutualism vary at different densities of non‐aphid herbivores.