Antagonistic effects of floral scent in an insect–plant interaction

In southwestern USA, the jimsonweed Datura wrightii and the nocturnal moth Manduca sexta form a pollinator–plant and herbivore–plant association. Because the floral scent is probably important in mediating this interaction, we investigated the floral volatiles that might attract M. sexta for feeding and oviposition. We found that flower volatiles increase oviposition and include small amounts of both enantiomers of linalool, a common component of the scent of hawkmoth-pollinated flowers. Because (+)-linalool is processed in a female-specific glomerulus in the primary olfactory centre of M. sexta, we hypothesized that the enantiomers of linalool differentially modulate feeding and oviposition. Using a synthetic mixture that mimics the D. wrightii floral scent, we found that the presence of linalool was not necessary to evoke feeding and that mixtures containing (+)- and/or (−)-linalool were equally effective in mediating this behaviour. By contrast, females oviposited more on plants emitting (+)-linalool (alone or in mixtures) over control plants, while plants emitting (−)-linalool (alone or in mixtures) were less preferred than control plants. Together with our previous investigations, these results show that linalool has differential effects in feeding and oviposition through two neural pathways: one that is sexually isomorphic and non-enantioselective, and another that is female-specific and enantioselective.     

Conflict resolution in an ant–plant interaction: Acacia constricta traits reduce ant costs to reproduction

Many plant species attract ants onto their foliage with food rewards or nesting space. However, ants can interfere with plant reproduction when they visit flowers. This study tests whether Acacia constricta separates visiting ant species temporally or spatially from newly opened inflorescences and pollinators. The diurnal activity patterns of ants and A. constricta pollinators peaked at different times of day, and the activity of pollinators followed the daily dehiscence of A. constricta inflorescences. In addition to being largely temporally separated, ants rarely visited open inflorescences. A floral ant repellent contributes to the spatial separation of ants and inflorescences. In a field experiment, ants of four species were given equal access to inflorescences in different developmental stages. On average, the frequency with which ants made initial, antennal contact with the floral stages did not differ, but ants significantly avoided secondary contact with newly opened inflorescences relative to buds and old inflorescences, and old inflorescences relative to buds. Ants also avoided contact with pollen alone, indicating that pollen is at least one source of the repellent. The results suggest A. constricta has effectively resolved the potential conflict between visiting ants and plant reproduction.     

Long-term temporal variation in the organization of an ant–plant network

Background and Aims

Functional groups of species interact and coevolve in space and time, forming complex networks of interacting species. A long-term study of temporal variation of an ant–plant network is presented with the aims of: (1) depicting its structural changes over a 20-year period; (2) detailing temporal variation in network topology, as revealed by nestedness and modularity analysis and other parameters (i.e. connectance, niche overlap); and (3) identifying long-term turnover in taxonomic structure (i.e. switches in ant resource use or plant visitor assemblages according to taxa).

Methods

Fieldwork was carried out at La Mancha, Mexico, and ant–plant interactions were observed between 1989 and 1991, between 1998 and 2000, and between May 2010 and 2011. Occurrences of ants on extrafloral nectaries (EFNs) were recorded. The resulting ant–plant networks were constructed from qualitative presence–absence data determined by a species–species matrix defined by the frequency of occurrence of each pairwise ant–plant interaction.

Key Results

Network variation across time was stable and a persistent nested structure may have contributed to the maintenance of resilient and species-rich communities. Modularity was lower than expected, especially in the most recent networks, indicating that the community exhibited high overlap among interacting species (e.g. few species were hubs in the more recent network, being partly responsible for the nested pattern). Structurally, the connections created among modules by super-generalists gave cohesion to subsets of species that otherwise would remain unconnected. This may have allowed an increasing cascade-effect of evolutionary events among modules. Mutualistic ant–plant interactions were structured 20 years ago mainly by the subdominant nectarivorous ant species Camponotus planatus and Crematogaster brevispinosa, which monopolized the best extrafloral nectar resources and out-competed other species with broader feeding habits. Through time, these ants, which are still present, lost their position as network hubs and diminished in their importance in structuring the network; simultaneously, plants gained in importance.

Conclusions

The long-term network analysis reveals a decrease in attended plant species richness, a notable increase in plant species participation from 1990 to 2010 (sustained by less plant taxonomic similarity in the older 1990 network), an increase in the number of ant species and a diminishing dominance of super-generalist ants. The structure of the community has remained highly nested and connected with low modularity, suggesting overall a more participative, homogeneous, cohesive interaction network. Although previous studies have suggested that interactions between ants and EFN-bearing plants are susceptible to seasonality, abiotic factors and perturbation, this cohesive structure appears to be the key for biodiversity and community maintenance.     

Ant–plant interaction in the Neotropical savanna: direct beneficial effects of extrafloral nectar on ant colony fitness

Current evidence suggests that ant–plant relationships may influence species composition, abundance, and interactions at the community scale. The main resource that plants offer to ants is extrafloral nectar (EFN) and the major part of published studies shown benefits from ants to plants possessing EFNs. However, the complementary question of whether and how ants benefit from EFNs is rarely addressed. Here, we present the results of a long-term study to demonstrate whether EFN has a positive effect on ant colony fitness. We quantified colony growth rate, survival and the final weight of individuals as measures of benefit derived from EFN. Our results provide clear evidence that EFN can have a significant positive impact on the survivorship, growth and reproduction of the Myrmicinae Cephalotes pusillus. In fact, a diet rich in EFN (providing at least 30 cal per day) resulted in five times more individuals per colony, greater body weights, and more eggs. These results have shed new light on the relationships between ants and EFN-bearing plants such as in tropical and temperate systems. The ant C. pusillus is the first case in which we have firm evidence that EFN improves colony growth and development, corroborating more than 100 years of experimental evidence of benefits to plants in these widespread relationships.     

The effect of disturbance on an ant–plant mutualism

Protective ant–plant mutualisms—where plants provide food or shelter to ants and ants protect the plants from herbivores—are a common feature in many ecological communities, but few studies have examined the effect of disturbance on these interactions. Disturbance may affect the relationship between plants and their associated ant mutualists by increasing the plants’ susceptibility to herbivores, changing the amount of reward provided for the ants, and altering the abundance of ants and other predators. Pruning was used to simulate the damage to buttonwood mangrove (Conocarpus erectus) caused by hurricanes. Pruned plants grew faster than unpruned plants, produced lower levels of physical anti-herbivore defenses (trichomes, toughness), and higher levels of chemical defenses (tannins) and extrafloral nectaries. Thus, simulated hurricane damage increased plant growth and the amount of reward provided to ant mutualists, but did not have consistent effects on other anti-herbivore defenses. Both herbivores and ants increased in abundance on pruned plants, indicating that the effects of simulated hurricane damage on plant traits were propagated to higher trophic levels. Ant-exclusion led to higher leaf damage on both pruned and upruned plants. The effect of ant-exclusion did not differ between pruned and unpruned plants, despite the fact that pruned plants had higher ant and herbivore densities, produced more extrafloral nectaries, and had fewer physical defenses. Another common predator, clubionid spiders, increased in abundance on pruned plants from which ants had been excluded. I suggest that compensatory predation by these spiders diminished the effect of ant-exclusion on pruned plants.     

Abiotic factors shape temporal variation in the structure of an ant–plant network

Despite recognition of key biotic processes in shaping the structure of biological communities, few empirical studies have explored the influences of abiotic factors on the structural properties of mutualistic networks. We tested whether temperature and precipitation contribute to temporal variation in the nestedness of mutualistic ant–plant networks. While maintaining their nested structure, nestedness increased with mean monthly precipitation and, particularly, with monthly temperature. Moreover, some species changed their role in network structure, shifting from peripheral to core species within the nested network. We could summarize that abiotic factors affect plant species in the vegetation (e.g., phenology), meaning presence/absence of food sources, consequently an increase/decrease of associations with ants, and finally, these variations to fluctuations in nestedness. While biotic factors are certainly important, greater attention needs to be given to abiotic factors as underlying determinants of the structures of ecological networks.     

Ecology of a fig ant–plant

Mutualistic interactions are embedded in networks of interactions that affect the benefits accruing to the mutualistic partners. Figs and their pollinating wasps are engaged in an obligate mutualism in which the fig is dependent on the fig pollinator for pollination services and the pollinator is dependent on fig ovules for brood sites. This mutualism is exploited by non-pollinating fig wasps that utilise the same ovules, but do not provide a pollination service. Most non-pollinating wasps oviposit from outside the inflorescence (syconium), where they are vulnerable to ant predation. Ficus schwarzii is exposed to high densities of non-pollinating wasps, but Philidris sp. ants patrolling the syconia prevent them from ovipositing. Philidris rarely catch wasps, but the fig encourages the patrolling by providing a reward through extra-floral nectaries on the surface of syconia. Moreover, the reward is apparently only produced during the phase when parasitoids are ovipositing. An ant-exclusion experiment demonstrated that, in the absence of ants, syconia were heavily attacked and many aborted as a consequence. Philidris was normally rare on the figs during the receptive phase or at the time of day when wasp offspring are emerging, so predation on pollinators was limited. However, Myrmicaria sp. ants, which only occurred on three trees, preyed substantially on pollinating as well as non-pollinating wasps. F. schwarzii occurs in small clusters of trees and has an exceptionally rapid crop turnover. These factors appear to promote high densities of non-pollinating wasps and, as a consequence, may have led to both a high incidence of ants on trees and increased selective pressure on fig traits that increase the payoffs of the fig–ant interaction for the fig. The fig receives no direct benefit from the reward it provides, but protects pollinating wasps that will disperse its pollen.     

Indirect effects of an unspecialized endophytic fungus on specialized plant – herbivorous insect interactions

The effects of Acremonium alternatum Gams (Ascomycotina, Clavicipitacea) on the development and nutrition of diamondback moth larvae Plutella xylostella L. (Lepidoptera, Plutellidae) were studied in the laboratory. All experiments were conducted before the endophyte reached the green parts of the plants; thus P. xylostella, a folivore, was not in direct contact with the endophyte. Larvae feeding on leaves of previously inoculated plants suffered from increased mortality, especially during the first 10 days of development. Likewise, during early development surviving larvae had a reduced relative growth rate (RGR), which, however, did not result in reduced pupal or adult weight. We found sexual differences in the food utilization efficiency; female P. xylostella progeny reacted more sensitively to endophytic infection of cabbage than male larvae. Female larvae feeding on leaves of endophyte-infested plants responded to reduced efficiency of conversion of ingested food (ECI) by increasing their relative consumption rate (RCR). The underlying mechanisms for these results are discussed in relation to changes in plant phytosterol metabolism which could account for reduced larval growth on inoculated cabbage plants. Our data suggest that unspecialized, soil-borne endophytic fungi, even when their association with the host plant is weak, can influence aboveground herbivore development and should be considered when investigating plant-insect interactions. Received: 3 November 1997 / Accepted 29 December 1997     

Plant-mediated effects on an insect–pathogen interaction vary with intraspecific genetic variation in plant defences

Baculoviruses are food-borne microbial pathogens that are ingested by insects on contaminated foliage. Oxidation of plant-derived phenolics, activated by insect feeding, can directly interfere with infections in the gut. Since phenolic oxidation is an important component of plant resistance against insects, baculoviruses are suggested to be incompatible with plant defences. However, plants among and within species invest differently in a myriad of chemical and physical defences. Therefore, we hypothesized that among eight soybean genotypes, some genotypes would be able to maintain both high resistance against an insect pest and high efficacy of a baculovirus. Soybean constitutive (non-induced) and jasmonic acid (JA)-induced (anti-herbivore response) resistance was measured against the fall armyworm Spodoptera frugiperda (weight gain, leaf consumption and utilization). Indicators of phenolic oxidation were measured as foliar phenolic content and peroxidase activity. Levels of armyworm mortality inflicted by baculovirus (SfMNPV) did not vary among soybean genotypes when the virus was ingested with non-induced foliage. Ingestion of the virus on JA-induced foliage reduced armyworm mortality, relative to non-induced foliage, on some soybean genotypes. Baculovirus efficacy was lower when ingested with foliage that contained higher phenolic content and defensive properties that reduced armyworm weight gain and leaf utilization. However, soybean genotypes that defended the plant by reducing consumption rate and strongly deterred feeding upon JA-induction did not reduce baculovirus efficacy, indicating that these defences may be more compatible with baculoviruses to maximize plant protection. Differential compatibility of defence traits with the third trophic level highlights an important cost/trade-off associated with plant defence strategies.     

Thermal tolerance affects mutualist attendance in an ant–plant protection mutualism

The influence of native fauna on non-native plant population growth, size, and distribution is not well documented. Previous studies have shown that native insects associated with tall thistle (Cirsium altissimum) also feed on the leaves, stems, and flower heads of the Eurasian congener C. vulgare, thus limiting individual plant performance. In this study, we tested the effects of insect herbivores on the population growth rate of C. vulgare. We experimentally initiated invasions by adding seeds at four unoccupied grassland sites in eastern Nebraska, USA, and recorded plant establishment, survival, and reproduction. Cumulative foliage and floral herbivory reduced C. vulgare seedling density, and prevented almost any reproduction by C. vulgare in half the sites. The matrix model we constructed showed that this herbivory resulted in a reduction of the asymptotic population growth rate (λ), from an 88 % annual increase to a 54 % annual decline. These results provide strong support for the hypothesis that indigenous herbivores limit population invasion of this non-native plant species into otherwise suitable grassland habitat.     

Effects of food rewards offered by ant–plant Macaranga on the colony size of ants

Myrmecophytes (ant–plants) have special hollow structures (domatia) in which obligate ant partners nest. As the ants live only on the plants and feed exclusively on plant food bodies, sap-sucking homopterans in the domatia, and/or the homopterans honeydew, they are suitable for the study of colony size regulation by food. We examined factors regulating ant colony size in four myrmecophytic Macaranga species, which have strictly species-specific association with Crematogaster symbiont ants. Intra- and interspecific comparison of the plants showed that the ant biomass per unit food biomass was constant irrespective of plant developmental stage and plant species, suggesting that the ant colony size is limited by food supply. The primary food offered by the plants to the ants was different among Macaranga species. Ants in Macaranga beccariana and Macaranga bancana relied on homopterans rather than food bodies, and appeared to regulate the homopteran biomass and, as a consequence, regulate the ants own biomass. In contrast, ants in Macaranga winkleri and Macaranga trachyphylla relied primarily on food bodies rather than homopterans, and the plants appeared to manipulate the ant colony size. Per capita plant investment in ants (ant dry weight plant dry weight^–1) was different among the four Macaranga species. The homoptera-dependent M. beccariana and M. bancana harbored lower biomass of ants than the food-body dependent M. winkleri, suggesting that energy loss is involved in the homoptera-interposing symbiotic system which has one additional trophic level. The plants investment ratio to the ants generally decreased as plants grew. The evolution of the plant reward-offering system in ant–plant–homopteran symbioses is discussed with an emphasis on the role of homopterans.     

Contrasting effects of invasive plants in plant–pollinator networks

The structural organization of mutualism networks, typified by interspecific positive interactions, is important to maintain community diversity. However, there is little information available about the effect of introduced species on the structure of such networks. We compared uninvaded and invaded ecological communities, to examine how two species of invasive plants with large and showy flowers (Carpobrotus affine acinaciformis and Opuntia stricta) affect the structure of Mediterranean plant–pollinator networks. To attribute differences in pollination to the direct presence of the invasive species, areas were surveyed that contained similar native plant species cover, diversity and floral composition, with or without the invaders. Both invasive plant species received significantly more pollinator visits than any native species and invaders interacted strongly with pollinators. Overall, the pollinator community richness was similar in invaded and uninvaded plots, and only a few generalist pollinators visited invasive species exclusively. Invasive plants acted as pollination super generalists. The two species studied were visited by 43% and 31% of the total insect taxa in the community, respectively, suggesting they play a central role in the plant–pollinator networks. Carpobrotus and Opuntia had contrasting effects on pollinator visitation rates to native plants: Carpobrotus facilitated the visit of pollinators to native species, whereas Opuntia competed for pollinators with native species, increasing the nestedness of the plant–pollinator network. These results indicate that the introduction of a new species to a community can have important consequences for the structure of the plant–pollinator network.     

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.     

Timing of butterfly parasitization of a plant–ant–scale symbiosis

In the Southeast Asian tropics, Arhopala lycaenid butterflies feed on Macaranga ant-plants inhabited by Crematogaster (subgenus Decacrema) ants tending Coccus-scale insects. A recent phylogenetic study showed that (1) the plants and ants have been codiversifying for the past 20–16 million years (Myr), and that (2) the tripartite symbiosis was formed 9–7 Myr ago, when the scale insects became involved in the plant–ant mutualism. To determine when the lycaenids first parasitized the Macaranga tripartite symbiosis, we constructed a molecular phylogeny of the lycaenids that feed on Macaranga by using mitochondrial and nuclear DNA sequence data and estimated their divergence times based on the cytochrome oxidase I molecular clock. The minimum age of the lycaenids was estimated by the time-calibrated phylogeny to be 2.05 Myr, about one-tenth the age of the plant–ant association, suggesting that the lycaenids are latecomers that associated themselves with the pre-existing symbiosis of plant, ant, and scale insects.     

Friend or foe? A behavioral and stable isotopic investigation of an ant–plant symbiosis

In ant–plant symbioses, the behavior of ant inhabitants affects the nature of the interaction, ranging from mutualism to parasitism. Mutualistic species confer a benefit to the plant, while parasites reap the benefits of the interaction without reciprocating, potentially resulting in a negative impact on the host plant. Using the ant–plant symbiosis between Cordia alliodora and its ant inhabitants as a model system, I examine the costs and benefits of habitation by the four most common ant inhabitants at La Selva Biological Station, Costa Rica. Costs are measured by counting coccoids associated with each ant species. Benefits include patrolling behavior, effectiveness at locating resources, and recruitment response. I also compare the diets of the four ant species using stable isotope analysis of nitrogen (N) and carbon (C). Ants varied in their rates of association with coccoids, performance of beneficial behaviors, and diet. These differences in cost, benefit, and diet among the ant species suggest differences in the nature of the symbiotic relationship between C. alliodora and its ants. Two of the ant species behave in a mutualistic manner, while the other two ant species appear to be parasites of the mutualism. I determined that the mutualistic ants feed at a higher trophic level than the parasitic ants. Behavioral and dietary evidence indicate the protective role of the mutualists, and suggest that the parasitic ants do not protect the plant by consuming herbivores.     

Conditional outcomes in ant–plant–herbivore interactions influenced by sequential flowering

Mechanisms that affect a host plant’s ability to face herbivory are subjects of ongoing interest. Plant reproductive phenology plays a key role in the dynamics of communities in many ways. In ant–plant–herbivore interactions, host-plant phenology affects traits of its herbivores which in turn determine what traits ants must have to benefit the host-plant. Diversity of plant phenological traits could influence the ecological diversity of coevolved ant–plant mutualisms.