Non-additive benefit or cost? Disentangling the indirect effects that occur when plants bearing extrafloral nectaries and honeydew-producing insects share exotic ant mutualists

Background and Aims

In complex communities, organisms often form mutualisms with multiple different partners simultaneously. Non-additive effects may emerge among species linked by these positive interactions. Ants commonly participate in mutualisms with both honeydew-producing insects (HPI) and their extrafloral nectary (EFN)-bearing host plants. Consequently, HPI and EFN-bearing plants may experience non-additive benefits or costs when these groups co-occur. The outcomes of these interactions are likely to be influenced by variation in preferences among ants for honeydew vs. nectar. In this study, a test was made for non-additive effects on HPI and EFN-bearing plants resulting from sharing exotic ant guards. Preferences of the dominant exotic ant species for nectar vs. honeydew resources were also examined.

Methods

Ant access, HPI and nectar availability were manipulated on the EFN-bearing shrub, Morinda citrifolia, and ant and HPI abundances, herbivory and plant growth were assessed. Ant-tending behaviours toward HPI across an experimental gradient of nectar availability were also tracked in order to investigate mechanisms underlying ant responses.

Key Results

The dominant ant species, Anoplolepis gracilipes, differed from less invasive ants in response to multiple mutualists, with reductions in plot-wide abundances when nectar was reduced, but no response to HPI reduction. Conversely, at sites where A. gracilipes was absent or rare, abundances of less invasive ants increased when nectar was reduced, but declined when HPI were reduced. Non-additive benefits were found at sites dominated by A. gracilipes, but only for M. citrifolia plants. Responses of HPI at these sites supported predictions of the non-additive cost model. Interestingly, the opposite non-additive patterns emerged at sites dominated by other ants.

Conclusions

It was demonstrated that strong non-additive benefits and costs can both occur when a plant and herbivore share mutualist partners. These findings suggest that broadening the community context of mutualism studies can reveal important non-additive effects and increase understanding of the dynamics of species interactions.     

The Fire Refuge Value of Patches of a Fire‐Sensitive Tree in Fire‐prone Savannas: Callitris intratropica in Northern Australia

Patches of fire‐sensitive vegetation often occur within fire‐prone tropical savannas, and are indicative of localized areas where fire regimes are less severe. These may act as important fire refugia for fire‐sensitive biota. The fire‐sensitive tree Callitris intratropica occurs in small patches throughout the fire‐prone northern Australian savannas, and is widely seen as an indicator of low‐severity fire regimes and of good ecosystem health. Here, we address the question: to what extent do Callitris patches act as refuges for other fire‐sensitive biota, and therefore play a broader conservation role? We contrast floral and faunal species composition between Callitris patches and surrounding eucalypt savanna, using three case studies. In the first case study, a floristic analysis of 47 Callitris patches across Western Australia's Kimberley region showed that woody species in these patches were overwhelmingly widespread, fire‐tolerant savanna taxa. No species of special conservation concern occurred disproportionately within Callitris patches. Similarly, there was no concentration of fire‐sensitive fauna or flora in five Callitris patches in the East Kimberley. Finally, there was no difference in ant species composition among 12 Callitris patches and surrounding eucalypt savannas in Kakadu National Park, Northern Territory, and there were no fire‐sensitive ant species in Callitris patches. Our three case studies from throughout the northwestern Australia provide no evidence that Callitris patches act as important refuges for fire‐sensitive flora or fauna within fire‐prone eucalypt savannas. This calls into question the notion that Callitris is a strong indicator of general ecosystem health.     

The Guianese population of the fire ant Solenopsis saevissima is unicolonial

In this study, conducted in French Guiana, a part of the native range of the fire ant Solenopsis saevissima, we compared the cuticular hydrocarbon profiles of media workers with previous results based on intraspecific aggressiveness tests. We noted a strong congruence between the two studies permitting us to delimit 2 supercolonies extending over large distances (up to 54 km), a phenomenon known as unicoloniality. Solenopsis geminata workers, taken as an out‐group for cluster analyses, have a very different cuticular hydrocarbon profile. Because S. saevissima has been reported outside its native range, our conclusion is that this species has the potential to become invasive because unicoloniality (i.e., the main attribute for ants to become invasive) was shown at least for the Guianese population.     

Day vs. night predation on artificial caterpillars in primary rainforest habitats – an experimental approach

The influence of natural enemies has led to the evolution of various predator avoidance strategies in herbivorous insects. Many caterpillars are exclusively active at night and rest during the day. It is widely assumed that nocturnal activity in caterpillars reduces their risk of falling prey to their natural enemies. To test this hypothesis, we compared predation pressure between day and night in tree‐fall gaps and closed‐canopy forest sites in an Amazonian primary lowland rainforest. Artificial clay caterpillars, showing camouflaged colouration (green), were exposed as potential prey to a natural predator community. Attacks were significantly more frequent during daytime and were reduced by about a quarter at night in tree‐fall gaps, and by a third in closed‐canopy forest sites. This supports the idea of time‐dependent activity in caterpillars as an antipredatory adaptation. Further, independent of the time of day, predation pressure on caterpillars was significantly higher in tree‐fall gaps compared to closed‐canopy forest habitats. Nearly all predation events were caused by arthropods, whereas birds played a negligible role. Across both habitat types and time scales, ants acted as major predator group, emphasising their important role in population control of herbivorous insects in lowland rainforest ecosystems. This is the first experimental study using artificial caterpillars to examine whether time‐scheduling of exposition might influence predation risk amongst undefended, solitary, free‐living lepidopteran larvae.     

Life Inside an Acorn: How Microclimate and Microbes Influence Nest Organization in Temnothorax Ants

Nests provide a buffer against environmental variation, but conditions may also vary at different locations within a nest. Conditions can vary based on abiotic factors, such as moisture and temperature, as well as biotic factors, such as the presence of microbes and potential pathogens. Therefore, characterizing how animals adjust their position inside their nests to track microclimate preferences while at the same time preventing pathogen exposure is necessary to understand the benefits nests provide. Here we studied how colonies of the acorn‐nesting ant Temnothorax curvispinosus responded to experimental manipulation of moisture, temperature, and microbial growth inside their nests. Colonies showed no response to differences in moisture and moved to the bottom of the acorn regardless of moisture treatment. When nests were heated from the top to simulate warming by the sun, workers preferentially moved brood to the warm, upper half of the acorn, which would stimulate brood development. Finally, the strongest factor that influenced colony position was the presence of microbes inside the nest—colonies avoided the bottom of the nest when it was inoculated with microbes, and colonies in new acorns shifted to the top of the acorn over time as mold and other microbes had time to grow. The relatively strong response of T. curvispinosus to microbial growth inside their nests suggests that pathogen pressures—in addition to microclimate—have a significant impact on how colonies use nest spaces. Social insects are known to invest heavily in antimicrobial compounds that kill or slow the growth of microbes, but avoidance may represent an additional line of defense to prevent pathogen exposure.     

Refuse attracts? Effect of refuse dumps of leaf‐cutting ants on floral traits

The nutrient‐rich organic waste generated by ants may affect plant reproductive success directly by enhancing fruit production but also indirectly, by affecting floral traits related with pollinator attraction. Understanding how these soil‐nutrient hot spots influence floral phenotype is relevant to plant–pollination interactions. We experimentally evaluated whether the addition of organic waste from refuse dumps of the leaf‐cutting ant Acromyrmex lobicornis (Hymenoptera: Formicidae: Attini) alters floral traits associated with pollinator attraction in Eschscholzia californica (Ranunculales: Papaveraceae), an entomophilous herb. We analysed flower shape and size using geometric morphometric techniques in plants with and without the addition of refuse‐dumps soil, under greenhouse conditions. We also measured the duration of flowering season, days with new flowers, flower production and floral display size. Plants growing in refuse‐dumps soil showed higher flower shape diversity than those in control soil. Moreover, plants in refuse‐dumps soil showed bigger flower and floral display size, longer flowering season, higher number of flowering days and flower production. As all these variables may potentially increase pollinator visits, plants in refuse‐dumps soil might increase their fitness through enhanced attraction. Our work describes how organic waste from ant nests may enhance floral traits involved in floral attraction, illustrating a novel way of how ants may indirectly benefit plants.     

No mate preference associated with the supergene controlling social organization in Alpine silver ants

Disassortative mating is a powerful mechanism stabilizing polymorphisms at sex chromosomes and other supergenes. The Alpine silver ant, Formica selysi, has two forms of social organization—single‐queen and multiple‐queen colonies—determined by alternate haplotypes at a large supergene. Here, we explore whether mate preference contributes to the maintenance of the genetic polymorphism at the social supergene. With mate choice experiments, we found that females and males mated randomly with respect to social form. Moreover, queens were able to produce offspring irrespective of whether they had mated with a male from the same or the alternative social form. Yet, females originating from single‐queen colonies were more fertile, suggesting that they may be more successful at independent colony founding. We conclude that the pattern of asymmetric assortative mating documented from mature F. selysi colonies in the field is not caused by mate preferences or major genetic incompatibilities between social forms. More generally, we found no evidence that disassortative mate preference contributes to the maintenance of polymorphism at this supergene controlling ant social organization.     

蚂蚁筑巢对西双版纳热带森林土壤易氧化有机碳时空动态的影响

蚂蚁筑巢定居能够形成与巢穴周围显著不同的微生境和土壤养分环境,从而对土壤易氧化有机碳(EOC)产生重要影响.本研究以中国科学院西双版纳勐仑热带植物园白背桐群落为研究对象,比较蚂蚁巢地与非巢地土壤EOC时空分布特征,并分析蚂蚁筑巢引起土壤理化性质的改变对土壤EOC时空动态的影响.结果表明: 研究区蚁巢和非蚁巢地土壤EOC随月份均呈明显的单峰型变化规律,表现为6月>9月>3月>12月;土壤EOC沿土层呈逐渐降低的变化趋势,在0～5 cm土层,蚁巢土壤EOC显著大于非巢地,在5～10和10～15 cm土层的差异不显著.蚂蚁筑巢显著提高了土壤温度、土壤有机碳、土壤易氧化有机碳、土壤微生物生物量碳、全氮、硝态氮和水解氮含量,显著降低了土壤含水率和容重,但对铵态氮、pH值的影响不显著.土壤有机碳、土壤微生物生物量碳是调控蚁巢和非巢地土壤EOC时空变化的主要因子,土壤温度、含水率、全氮和硝态氮等土壤指标对土壤EOC的影响次之.蚂蚁筑巢主要通过改变微生境(土壤温度和水分)及土壤养分(主要是土壤有机碳和微生物生物量碳)的状况,进而调控热带森林土壤易氧化有机碳的时空动态.     

Extended phenotypes and foraging restrictions: ant nest entrances and resource ingress in leaf‐cutting ants

Several factors may restrict the acquisition of food to below the levels predicted by the optimization theory. However, how the design of structures that animals build for foraging restricts the entry of food is less known. Using scaling relationships, we determined whether the design of the entrances of leaf‐cutting ant nests restricts resource input into the colony. We measured nests and foraging parameters in 25 nests of Atta cephalotes in a tropical rain forest. Ant flux was reduced to up to 60% at nest entrances. The width of all entrances per nest increased at similar rates as nest size, but the width of nest entrances increased with the width of its associated trail at rates below those expected by isometry. The fact that entrance widths grow slower than trail widths suggests that the enlargement of entrance holes does not reach the dimensions needed to avoid delays when foraging rates are high and loads are big. The enlargement of nest entrances appears to be restricted by the digging effort required to enlarge nest tunnels and by increments in the risk of inundation, predator/parasitoid attacks and microclimate imbalances inside the nest. The design of the extended phenotypes can also restrict the ingress of food into the organisms, offering additional evidence to better understand eventual controversies between empirical data and the foraging theory. Abstract in Spanish is available with online material.     

The function of extrafloral nectaries in the pollination and reproduction of Sambucus javanica

Sambucus javanica is a perennial herb with extrafloral nectaries (EFNs) on its inflorescences. To explore the ecological functions of EFNs, a factorial combination experiment of ant (access or exclusion) and EFNs (with or without) at the plant level was created in two populations. The role of EFNs in the attraction of ants and flying pollinators, the defensive role of ants against foliar herbivores, the effects of ants on pollinator visitation and the effects of ant–pollinator interactions on fruit production in one or both populations were assessed. Ants were common on the ant-access plants with EFNs, but absent from the ant-access plants without EFNs. Foliar herbivory was independent of ant and EFN treatments and their interactions. The visitation frequency of flying pollinators (honeybees and syrphid flies) and fruit set were significantly higher for plants with EFNs than plants without EFNs, but were not affected by ant treatments or their interactions with EFN treatments. These results suggest that EFNs in S. javanica attracted both ants and flying pollinators, but ants did not present a defensive role against herbivores, did not deter flying pollinators from visiting inflorescences and had no effects on fruit production. In addition, ants were not significant pollen vectors.