It takes two to tango but three is a tangle: mutualists and cheaters on the carnivorous plant <Emphasis Type="Italic">Roridula</Emphasis>

Roridula dentata is associated with hemipterans, which facilitate nitrogen assimmilation from insects. R. dentata is also associated with spiders and their role in digestion is unknown. We quantify approximately how much nitrogen Roridula assimilates from insects through "indirect digestion." Using '¹⁵N we then determine whether nitrogen absorption from hemipteran insects differs with varying spider densities. In this way, we are able to determine their nutritional role. At low spider densities, indirect digestion of prey accounts for approximately 70% of plant nitrogen. These values are comparable to methods of direct prey digestion found in other carnivorous plants. However spiders decrease the numbers of hemipteran individuals inhabiting Roridula plants and also decrease efficiency of indirect prey digestion by up to 30%. We deduce that spiders are cheaters as they exploit plant rewards without offering any rewards in return. However, indirect carnivory is still efficient enough when hemipteran densities are at their lowest, ensuring that the mutualism does not break down.     

Mutualisms and population regulation: mechanism matters

For both applied and theoretical ecological science, the mutualism between ants and their hemipteran partners is iconic. In this well-studied interaction, ants are assumed to provide hemipterans protection from natural enemies in exchange for nutritive honeydew. Despite decades of research and the potential importance in pest control, the precise mechanism producing this mutualism remains contested. By analyzing maximum likelihood parameter estimates of a hemipteran population model, we show that the mechanism of the mutualism is direct, via improved hemipteran growth rates, as opposed to the frequently assumed indirect mechanism, via harassment of the specialist parasites and predators of the hemipterans. Broadly, this study demonstrates that the management of mutualism-based ecosystem services requires a mechanistic understanding of mutualistic interactions. A consequence of this finding is the counter intuitive demonstration that preserving ant participation in the ant-hemipteran mutualism may be the best way of insuring pest control.     

Inferring evolutionary patterns from the biogeographical distributions of mutualists and exploiters

Exploitation may lead to the breakdown of obligate species-specific mutualisms. However, the mutualism between Roridula (plants) and Pameridea (hemipterans) is often exploited by spiders. The aim of the present study was to determine when the exploiters became associated with the Roridula-Pameridea mutualism. The phylogenetic and geographical associations between Roridula and Pameridea are documented and the distribution patterns of Roridula and exploiters are overlaid to see how closely they correlate. A geographical discontinuity in Roridulas ' range divides both the host plants and associated hemipterans into two sister species so that each hemipteran species is associated with a different plant species. This suggests that Roridula was associated with Pameridea before fragmentation/vicariance events split the genus, allowing allopatric speciation. By contrast, Roridula is only associated with exploiters in parts of its current range. This suggests that exploiters are unable to traverse the disjunctions in Roridulas' distribution and that they only developed associations with the mutualism after vicariance events. It is hypothesized that Pameridea and Roridula were closely associated for a long period before the invasion of nonmutualists. The absence of associated nonmutualist species may have helped facilitate the evolution of an obligate interaction between Roridula and Pameridea .  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 541–549.     

Ecological effects of multi‐species,ant–hemipteran mutualisms in citrus

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Ant–scale mutualism increases scale infestation,decreases folivory,and disrupts biological control in restored tropical forests

Ant–hemipteran mutualisms can have positive and negative effects on host plants depending on the level of hemipteran infestation and plant protection conferred by ants against folivory. Differential effects of such mutualisms on plant survival are well documented in undisturbed and ant-invaded systems, but few have explored how anthropogenic disturbance affects interactions between hemipterans and native ant species and what the consequences may be for recovering ecosystems. Within a fragmented landscape in Costa Rica, restored tropical forests harbor a mutualism between the native ant Wasmannia auropunctata and the scale insect Alecanochiton marquesi on the abundant, early-successional tree Conostegia xalapensis. I added A. marquesi scales to C. xalapensis seedlings and either allowed or excluded W. auropunctata to investigate if this mutualism leads to increased scale infestation, decreased scale mortality, and decreased folivory. I also examined whether these effects are mediated by the percentage of remnant forest cover in the landscape. I found that seedlings with ants excluded had fewer scale insects and higher herbivory than plants with ants present. I also found evidence that scale mortality due to fungal attack and parasitism was higher on ant-excluded versus ant-allowed seedlings but only at sites with high surrounding landscape forest cover. Together, these results suggest that mutualisms between scale insects and native ants can promote scale infestation, reduce folivory on native plant species, and potentially disrupt biological control of scale insects in recovering tropical forests. Further, my experiment underscores the importance of remnant tropical forests as sources of biological control in anthropogenically disturbed landscapes. Abstract in Spanish is available with online material.     

Elevated temperatures alter an ant‐aphid mutualism

Ant‐hemipteran mutualisms are keystone interactions that can be variously affected by warming: these mutualisms can be strengthened or weakened, or the species can transition to new mutualist partners. We examined the effects of elevated temperatures on an ant‐aphid mutualism in the subalpine zone of the Rocky Mountains in Colorado, USA. In this system, inflorescences of the host plant, Ligusticum porteri Coult. & Rose (Apiaceae), are colonized by the ant‐tended aphid Aphis asclepiadis Fitch or less frequently by the non‐ant tended aphid Cavariella aegopodii (Scopoli) (both Hemiptera: Aphididae). Using an 8‐year observational study, we tested for two key mechanisms by which ant‐hemipteran mutualisms may be altered by climate change: shifts in species identity and phenological mismatch. Whereas the aphid species colonizing the host plant is not changing in response to year‐to‐year variation in temperature, we found evidence that a phenological mismatch between ants and aphids could occur. In warmer years, colonization of host plant inflorescences by ants is decreased, whereas for A. asclepiadis aphids, host plant colonization is mostly responsive to date of snowmelt. We also experimentally established A. asclepiadis colonies on replicate host plants at ambient and elevated temperatures. Ant abundance did not differ between aphid colonies at ambient vs. elevated temperatures, but ants were less likely to engage in tending behaviors on aphid colonies at elevated temperatures. Sugar composition of aphid honeydew was also altered by experimental warming. Despite reduced tending by ants, aphid colonies at elevated temperatures had fewer intraguild predators. Altogether, our results suggest that higher temperatures may disrupt this ant‐aphid mutualism through both phenological mismatch and by altering benefits exchanged in the interaction.     

Parasites may help stabilize cooperative relationships

Background  

The persistence of cooperative relationships is an evolutionary paradox; selection should favor those individuals that exploit their partners (cheating), resulting in the breakdown of cooperation over evolutionary time. Our current understanding of the evolutionary stability of mutualisms (cooperation between species) is strongly shaped by the view that they are often maintained by partners having mechanisms to avoid or retaliate against exploitation by cheaters. In contrast, we empirically and theoretically examine how additional symbionts, specifically specialized parasites, potentially influence the stability of bipartite mutualistic associations. In our empirical work we focus on the obligate mutualism between fungus-growing ants and the fungi they cultivate for food. This mutualism is exploited by specialized microfungal parasites (genus Escovopsis) that infect the ant's fungal gardens. Using sub-colonies of fungus-growing ants, we investigate the interactions between the fungus garden parasite and cooperative and experimentally-enforced uncooperative ("cheating") pairs of ants and fungi. To further examine if parasites have the potential to help stabilize some mutualisms we conduct Iterative Prisoner's Dilemma (IPD) simulations, a common framework for predicting the outcomes of cooperative/non-cooperative interactions, which incorporate parasitism as an additional factor.     

Impact of a mutualism between an invasive ant and honeydew-producing insects on a functionally important tree on a tropical island

Mutualisms between invasive ants and honeydew-producing Hemiptera have the potential to result in unusually high population levels of both partners, with subsequent major changes to ecosystem composition and dynamics. We assessed the relationship between the invasive ant, Pheidole megacephala, and its hemipteran mutualists, Dysmicoccus sp. and Pulvinaria urbicola, on Cousine Island, Seychelles. We also assessed the impacts of the mutualism on the condition of the hemipteran host plant, Pisonia grandis, a native and functionally important tree species. There was a strong positive relationship between Ph. megacephala activity and hemipteran abundance, and the exclusion of ants from Pi. grandis resulted in a significant decline in Pu. urbicola abundance. High abundance of the mutualists was strongly associated with damage to the Pi. grandis forest. This indicates that the mutualism is contributing to the massive increase in the population levels of the mutualist species, and is intensifying their impacts on the island. The widespread trophobiosis and its associated high densities of mutualists pose serious threats to the ecosystem, highlighting the need to control the ant and associated hemipteran populations.     

The role of plant–mycorrhizal mutualisms in deterring plant invasions: Insights from an individual‐based model

Understanding the factors that determine invasion success for non‐native plants is crucial for maintaining global biodiversity and ecosystem functioning. One hypothesized mechanism by which many exotic plants can become invasive is through the disruption of key plant–mycorrhizal mutualisms, yet few studies have investigated how these disruptions can lead to invader success. We present an individual‐based model to examine how mutualism strengths between a native plant (Impatiens capensis) and mycorrhizal fungus can influence invasion success for a widespread plant invader, Alliaria petiolata (garlic mustard). Two questions were investigated as follows: (a) How does the strength of the mutualism between the native I. capensis and a mycorrhizal fungus affect resistance (i.e., native plant maintaining >60% of final equilibrium plant density) to garlic mustard invasion? (b) Is there a non‐linear relationship between initial garlic mustard density and invasiveness (i.e., garlic mustard representing >60% of final equilibrium plant density)? Our findings indicate that either low (i.e., facultative) or high (i.e., obligate) mutualism strengths between the native plant and mycorrhizal fungus were more likely to lead to garlic mustard invasiveness than intermediate levels, which resulted in higher resistance to garlic mustard invasion. Intermediate mutualism strengths allowed I. capensis to take advantage of increased fitness when the fungus was present but remained competitive enough to sustain high numbers without the fungus. Though strong mutualisms had the highest fitness without the invader, they proved most susceptible to invasion because the loss of the mycorrhizal fungus resulted in a reproductive output too low to compete with garlic mustard. Weak mutualisms were more competitive than strong mutualisms but still led to garlic mustard invasion. Furthermore, we found that under intermediate mutualism strengths, the initial density of garlic mustard (as a proxy for different levels of plant invasion) did not influence its invasion success, as high initial densities of garlic mustard did not lead to it becoming dominant. Our results indicate that plants that form weak or strong mutualisms with mycorrhizal fungi are most vulnerable to invasion, whereas intermediate mutualisms provide the highest resistance to an allelopathic invader.     

Does the host plant affect the benefits from mutualisms? The invasive mealybug and ghost ant association

1. The benefits to trophobionte hemipterans are affected by the ant tending level, which is a widely accepted statement. The ant tending level is closely related to multiple factors. It is clear that the ant tending level can be affected by the temporal factor, age‐specific, the density of the hemipterans, and quantity and quality of honeydew produced by hemipterans. 2. Few studies of ant–hemipteran mutualisms have reported the patterns of host plants‐dependent effects, and whether host plants influence the ant tending level that is also unclear. As such, laboratory experiments were conducted to test whether the colony growth rate of an invasive mealybug Phenacoccus solenopsis Tinsley, parasitism of Aenasius bambawalei Hayat, an dominant parasitoid of P. solenopsis, are affected by tending by ghost ants (Tapinoma melanocephalum(Fabricius)], host plants (tomato and cotton), and interactions between the two factors. The difference in the ant tending level between the host plants was also determined. 3. The results showed that mealybug colony growth and parasitism were significantly affected by ant tending and host plant separately. There were significant interactions between the independent factors on the mealybug colony growth rate and percentage parasitism. These results suggest that benefits to mealybugs are host plant‐dependent.     

Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts

Wolbachia are the most abundant bacterial endosymbionts among arthropods. Although maternally inherited, they do not conform to the widespread view that vertical transmission inevitably selects for beneficial symbionts. Instead, Wolbachia are notorious for their reproductive parasitism which, although lowering host fitness, ensures their spread. However, even for reproductive parasites it can pay to enhance host fitness. Indeed, there is a recent upsurge of reports on Wolbachia‐associated fitness benefits. Therefore, the question arises how such instances of mutualism are related to the phenotypes of reproductive parasitism. Here, we review the evidence of Wolbachia mutualisms in arthropods, including both facultative and obligate relationships, and critically assess their biological relevance. Although many studies report anti‐pathogenic effects of Wolbachia, few actually prove these effects to be relevant to field conditions. We further show that Wolbachia frequently have beneficial and detrimental effects at the same time, and that reproductive manipulations and obligate mutualisms may share common mechanisms. These findings undermine the idea of a clear‐cut distinction between Wolbachia mutualism and parasitism. In general, both facultative and obligate mutualisms can have a strong, and sometimes unforeseen, impact on the ecology and evolution of Wolbachia and their arthropod hosts. Acknowledging this mutualistic potential might be the key to a better understanding of some unresolved issues in the study of Wolbachia–host interactions.     

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.     

A non‐pollinating moth inflicts higher seed predation than two co‐pollinators in an obligate pollination mutualism

1. Mutualisms are relationships of mutual exploitation, in which interacting species receive a net benefit from their association. In obligate pollination mutualisms (OPMs), female pollinators move pollen between the flowers of a single plant species and oviposit eggs within the female flowers that they visit. 2. Competition between co‐occurring pollinator species is predicted to increase pollinator virulence, i.e. laying more eggs or consuming more seeds per fruit. Plants involved in OPMs frequently host various non‐pollinating seed parasites and parasitoids that may influence the outcome of the mutualism. Quantifying the prevalence of parasites and parasitoids and competition between pollinators is important for understanding the factors that influence OPM evolutionary stability. 3. This study investigated the pollination mutualism occurring between the leaf flower plant, Breynia oblongifolia, and its co‐pollinating Epicephala moths. A third moth, Herpystis, also occurs in B. oblongifolia fruits as a non‐pollinating seed parasite. 4. Breynia oblongifolia fruits were collected to quantify seed predation and compare seed predation costs between the three moth species. Results showed that the larvae of the two pollinator species consume similar numbers of seeds, and that adults deposit similar numbers of eggs per flower. As such, no evidence of increases in virulent behaviours was detected as a result of competition between co‐pollinators. 5. By contrast, the seed parasite Herpystis consumed more seeds than either pollinator species, and fruit crops with a high proportion of Herpystis had significantly lower net seed production. 6. This work adds to the growing understanding of the ecology and dynamics of plant–pollinator mutualisms.     

Pameridea (Hemiptera: Miridae): Predaceous bugs specific to the highly viscid plant genus Roridula

Abstract. The South African genus Pameridea and its two species are redescribed. The tribe Pamerideini, founded for this genus only, is removed from synonymy with Mirini (subfamily Mirinae) and transferred to Dicyphini (subfamily Bryocorinae), falling as a synonym of the subtribe Dicyphina. The bugs live only on intensely viscid small shrubs of the genus Roridula. This plant genus is the only member of its family but the bug genus is closely related to two widespread tropical dicyphine genera.     

Growth‐independent cross‐feeding modifies boundaries for coexistence in a bacterial mutualism

Nutrient cross‐feeding can stabilize microbial mutualisms, including those important for carbon cycling in nutrient‐limited anaerobic environments. It remains poorly understood how nutrient limitation within natural environments impacts mutualist growth, cross‐feeding levels and ultimately mutualism dynamics. We examined the effects of nutrient limitation within a mutualism using theoretical and experimental approaches with a synthetic anaerobic coculture pairing fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli and R. palustris resemble an anaerobic food web by cross‐feeding essential carbon (organic acids) and nitrogen (ammonium) respectively. Organic acid cross‐feeding stemming from E. coli fermentation can continue in a growth‐independent manner during nitrogen limitation, while ammonium cross‐feeding by R. palustris is growth‐dependent. When ammonium cross‐feeding was limited, coculture trends changed yet coexistence persisted under both homogenous and heterogenous conditions. Theoretical modelling indicated that growth‐independent fermentation was crucial to sustain cooperative growth under conditions of low nutrient exchange. In contrast to stabilization at most cell densities, growth‐independent fermentation inhibited mutualistic growth when the E. coli cell density was adequately high relative to that of R. palustris. Thus, growth‐independent fermentation can conditionally stabilize or destabilize a mutualism, indicating the potential importance of growth‐independent metabolism for nutrient‐limited mutualistic communities.     

Genetic architecture of multiple mutualisms and mating system in Turnera ulmifolia

Plants often associate with multiple arthropod mutualists. These partners provide important services to their hosts, but multiple interactions can constrain a plant's ability to respond to complex, multivariate selection. Here, we quantified patterns of genetic variance and covariance among rewards for pollination, biotic defence and seed dispersal mutualisms in multiple populations of Turnera ulmifolia to better understand how the genetic architecture of multiple mutualisms might influence their evolution. We phenotyped plants cultivated from 17 Jamaican populations for several mutualism and mating system-related traits. We then fit genetic variance–covariance (G) matrices for the island metapopulation and the five largest individual populations. At the metapopulation level, we observed significant positive genetic correlations among stigma–anther separation, floral nectar production and extrafloral nectar production. These correlations have the potential to significantly constrain or facilitate the evolution of multiple mutualisms in T. ulmifolia and suggest that pollination, seed dispersal and defence mutualisms do not evolve independently. In particular, we found that positive genetic correlations between floral and extrafloral nectar production may help explain their stable coexistence in the face of physiological trade-offs and negative interactions between pollinators and ant bodyguards. Locally, we found only small differences in G among our T. ulmifolia populations, suggesting that geographic variation in G may not shape the evolution of multiple mutualisms.     

Resource exchange and partner recognition mediate mutualistic interactions between prey and their would-be predators

Animals may develop mutualistic associations with other species, whereby prey offer resources or services in exchange for protection from predators. Alternatively, prey may offer resources or services directly to their would-be predators in exchange for their lives. The latter may be the case of hemipterans that engage in mutualistic interactions with ants by offering a honeydew reward. We test the extent to which a honeydew offering versus partner recognition may play a role as proximate mechanisms deterring ants from predating upon their hemipteran partners. We showed that, when presented with a choice between a hemipteran partner and an alternative prey type, mutualist ants were less likely to attack and more likely to remain probing their hemipteran partners. This occurred even in the absence of an immediate sugary reward, suggesting either an evolved or learned partner recognition response. To a similar extent, however, ants were also less likely to attack the alternative prey type when laced with honey as a proxy for a honeydew reward. This was the case even after the honey had been depleted, suggesting an ability of ants to recognize new potential sources of sugars. Either possibility suggests a degree of innate or learned partner recognition.     

Ant-hemipteran trophobioses in a Bornean rainforest – diversity, specificity and monopolisation

Trophobiotic interactions between ants, hemipterans and plants play an important role for all three partners. This study compared a broad spectrum of trophobiotic associations in a tropical rainforest in Sabah, Borneo. We studied partner specificity, ant recruitment, temporal continuity and monopolisation in 218 trophobioses, comprising 58 ant species, 62 hemipteran and over 31 plant species. The most common associations involved Dinochloa trichogona (Poaceae) with coreids and delphacids in the forest understorey, and the invasive weed Chromolaena odorata (Asteraceae) with Aphis gossypii and A. spiraeola in the open vegetation; both associations were attended by a broad spectrum of ant species. In general, associations between hemipterans and plants were highly and significantly specialised, while ants were more opportunistic in their choices of partners, although partitioning was also significant between ant versus hemipteran species and consequently between ant versus plant species. The number of ant workers increased significantly, but at a declining rate, with the number of hemipterans at a trophobiosis. Most trophobioses (96%) were only tended by a single ant species at a time and thus effectively monopolised. Occasionally these guards were replaced by another ant species after a few weeks (11%) or during the night (34%). In order to test whether other sugar-seeking ants as potential competitors occurred in the vicinity of trophobioses, sugar baits were placed next to the trophobioses, on a different branch of the same plant, and on a neighbouring plant. While the hemipteran-tending ant colony mostly monopolised the nearest sugar bait, the number of ant species on more distant baits was significantly higher. Our results show that ant associations with honeydew-producing hemipterans may be relatively opportunistic at the community level, but highly predictable on a smaller spatio-temporal scale in respect to recruitment to, and long term securing of this important resource. Received 23 August 2005; revised 22 November 2005; accepted 19 December 2005.     

Sticky plant captures prey for symbiotic bug: is this digestive mutualism?

Many plants capture and kill insects but, until relatively recently, only carnivorous plants with digestive enzymes were known to gain directly from the nutrients of those insects. Recent studies show that some carnivorous plants lack digestive enzymes and have evolved digestive mutualisms with symbiotic insects that digest their prey for them. Rhododendron macrosepalum, a plant with sticky leaves that captures insects, has an association with symbiotic Mirid bugs that consume the insects captured. Here, we determine what the nature of the relationship is between Mirid and plant. We find that R. macrosepalum has no digestive enzymes of its own but that it does not seem to have the ability to absorb hemipteran faeces through its leaf cuticle. Naturally occurring levels of ¹⁵N and ¹⁴N were used to determine that R. macrosepalum gains no nitrogen through its association with the Mirid bugs and that it obtains all of its nitrogen from the soil. The Mirids, on the other hand, seem to obtain nitrogen from insects captured by the plant, as well as from plant tissues. The relationship between plant and Mirid is not a digestive mutualism but more likely an antagonistic relationship. This study adds to our understanding of how digestive mutualisms evolve and shows that insect capture alone, or in combination with a symbiotic insect relationship does not necessarily make a plant ‘carnivorous’.     

Mutualism in a community context: the positive feedback between an ant–aphid mutualism and a gall-making midge

Although mutualisms are widespread and often described in natural history accounts, their ecological influences on other community members remain largely unexplored. Many of these influences are likely a result of indirect effects. In this field study, we investigated the indirect effects of an ant–aphid mutualism on the abundance, survival rates and parasitism rates of a co-occurring herbivore. Rabdophaga salicisbrassicoides (Diptera: Cecidomyiidae) induces rosette galls on the developing shoots of Salix exigua trees, and populations can reach outbreak densities (up to 1,000 galls/stem) in central Washington State (USA). Ant-tended aphids feed on these same stems and often feed on gall tissue. In this study we used a combination of manipulative experiments and observational surveys to test the hypothesis that the abundances of aphids, ants, and galls have positive and reciprocal effects on one another, in a manner that would create a positive feedback loop in population growth. In addition, we examined whether the combined presence of ants and aphids reduces parasitism rates for the gallers. In support of the positive feedback loop hypothesis, aphids enjoyed higher population growth rates in the presence of ants and galls, the presence of ants and aphids resulted in increased abundance of galls, and the abundances of ants, aphids and galls were all positively correlated with one another. However, the mechanism underlying the positive effect of ants and aphids on galler density remains unknown, as the mutualism did not affect parasitism rates. More broadly, this study demonstrates that mutualisms can have significant and complex indirect effects on community and population ecology.