- 55 Downloads
When Is it Mutualism?
Mutualism is an interaction between two different species that benefits both partners. In ant-Hemiptera associations, mutualism occurs when ants increase hemipteran fitness while gaining food rewards. Ants can provide hemipterans with protection against natural enemies or abiotic stress, access to new feeding niches, dispersal, and sanitary benefits by removing excess honeydew that might otherwise promote fungal growth. For example, Dolichoderus ants in Malaysia form bivouacs out of their own bodies to protect their honeydew-producing mealybugs (Pseudococcidae) from rain and to herd the mealybugs to the most nutritious feeding sites . Adaptations of Hemiptera to mutualism with ants include the loss of morphological defenses, such as wax excretions, augmentation of anal setae that form a basket for honeydew droplets, and increases in honeydew production and/or changes in honeydew composition when ants are present .
Ants can also kill or remove honeydew-producing hemipterans from plants instead of benefiting them, but predation per se of ant-tended hemipterans may actually be relatively uncommon. For example, Crematogaster ants that live with honeydew-producing soft scale insects (Coccidae) in the ant-plant Macaranga will not eat their coccids even when starving. In facultative associations between ants and aphids, ants may treat aphids as prey primarily when the aphids are walking or moving irregularly. Remarkably, Melissotarsus ants in Africa make wood gallery nests where they live with armored scale insects (Diaspididae), which do not even excrete honeydew. Instead of preying upon their honeydew-less associates, however, the ants appear to eat the wax and protein excretions that the diaspidids typically use to form their protective “armor” . In association, the diaspidids trade their armor for ant-provided protection.
Protection from natural enemies is in fact perhaps the most common benefit to ant-tended hemipterans. Social aphids may even invest less in their characteristic defensive caste (soldiers) when ants are present . Yet the degree of protection that ants provide is context-dependent. The identity and density of the ants, the density of the hemipterans, and the community context can all affect how much protection the hemipterans receive. Because associating with ants can incur costs to hemipterans in terms of growth rate and reproductive investment [4365体育网站], ants may also protect hemipterans successfully from natural enemies without actually improving hemipteran fitness. Moreover, because most ant-tended hemipterans have both sexual and asexual generations, defining fitness benefits to hemipterans can be challenging. For example, hemipteran population growth in an asexual phase may not readily translate to long-term fitness benefits.
Finally, although ants are the more obvious potential aggressors in ant-Hemiptera associations, hemipterans can also turn the tables. One of two root-dwelling morphs of a gall-inducing aphid (Aphididae) in Europe is a parasite of its Tetramorium ant associates. The aphids mimic the chemical profile of the ants’ larvae and are carried to the brood chamber by the ants, where the aphids receive brood care and feed on the hemolymph of the ant larvae .
Cryptic Herbivory and Ant Evolution
The evolution of ant-Hemiptera associations opened up extensive new feeding niches for ancestrally predatory ants and may have influenced their subsequent evolutionary success and ecological dominance. Key innovations that allowed formicines, dolichoderines, and even some myrmecines to obtain their nutrition from honeydew – possibly facilitating diversification in these speciose subfamilies – were modifications to the gut that enable them to maintain large amounts of liquid passively in the crop, or social stomach, for later transfer to nestmates via trophallaxis. The enormous biomass of ants in tropical forest canopies may in fact be supported primarily by hemipteran honeydew, such that canopy ants have been called cryptic herbivores . How ants that feed primarily on sugar-rich honeydews can obtain sufficient nitrogen for their developing larvae is a persistent question, but it is now clear that at least some ants recycle nitrogenous waste products into essential amino acids by way of intestinal symbionts.
Although plants also produce sugar-rich liquid food directly for ants in the form of extrafloral nectar, honeydew can be a more abundant, constant, and nutritious resource for ants . Indeed the preference of dominant arboreal ant species for honeydew over extrafloral nectar shapes ant mosaics in tropical forests around the world. Moreover, most ants in obligate ant-plant relationships365体育网站 tend hemipterans for honeydew in addition to consuming whatever direct food rewards their host plants provide.
Associations with hemipterans have also been important to the success of introduced and invasive species of ants. Invasive ants are frequently associated with high densities of hemipterans. Some invasive ants, such as Linepithema humile365体育网站, may in fact be more reliant on honeydew in their introduced ranges than in their native ranges. To the extent that carbohydrates support ecological dominance in ant communities, these associations may even promote the destructive success of invasive ants in their introduced ranges.
Consequences for Plants
Ant-Hemiptera associations form the basis of innumerable indirect interactions between ants and plants. Although ants can have positive or negative effects on hemipterans, as discussed above, hemipteran-tending ants are often ecological dominants that can have strong effects on the entire plant-based food web. Importantly, even ants that benefit hemipterans can have positive effects on plants if they defend plants from natural enemies more harmful than the hemipterans themselves. A literature survey conducted in 2007 indicated that hemipteran-tending ants in fact usually benefit plants by decreasing net damage, which increases plant growth and/or reproductive investment [5365体育网站]. This result holds for facultative as well as obligate ant-Hemiptera associations and at both tropical and temperate latitudes. Nevertheless, there are also cases where ants increase hemipteran population densities to such an extent that the association introduces a net cost to the plant. Although such negative effects are often assumed in agricultural systems and/or systems with invasive ant species, further experimental work that factorially separates ants from hemipterans is necessary in these and other systems.
Although extrafloral nectaries were once proposed as an adaptation for plants to avoid hemipterans while still attracting ants, recent evidence suggests that honeydew-producing hemipterans can actually generate more effective ant defense than extrafloral nectar under some circumstances. In obligate ant-plant relationships, where plants provide ants with additional direct rewards, including hollow structures for housing and extrafloral nectar, the density of hemipterans can often still be closely related to the effectiveness of ant defense. In East Africa, for example, higher densities of soft-scale insects (Coccidae) indirectly reduced elephant damage to an acacia tree defended by Crematogaster365体育网站 ants, even though the same ants also feed from the tree’s extrafloral nectar. Similar positive effects of hemipterans on ant defense of plants have also been shown in free-living, facultative ant-plant interactions, where ants are attracted to plants for honeydew alone. An open question for future research is whether and how selection acts on plant traits to enhance ant defense indirectly, via honeydew-producing hemipterans.
Consequences for the Community
Hemipteran-tending ants can also change the structure and dynamics of the broader plant-based community. In particular, these ants tend to reduce the abundance and species richness of both non-hemipteran herbivores and other predators. Yet the magnitude and direction of ant community effects depend on how vulnerable a particular guild is to ant predation . Moreover, although relatively few studies have yet measured the effects of ant-Hemiptera associations on entire arthropod communities, these associations are likely to be keystone interactions in some, if not many, terrestrial ecosystems.
- 1.Blüthgen, N., Verhaagh, M., Goitía, W., Jaffé, K., Morawetz, W., & Barthlott, W. (2000). How plants shape the ant community in the Amazonian rainforest canopy: The key role of extrafloral nectaries and homopteran honeydew. Oecologia, 125, 229–240.
- 2.Davidson, D. W., Cook, S. C., Snelling, R. R., & Chua, T. H. (2003). Explaining the abundance of ants in lowland tropical rainforest canopies. Science, 300, 969–972.
- 3.Delabie, J. H. (2001). Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): An overview. Neotropical Entomology, 30, 501–516.
- 4.Stadler, B., & Dixon, A. F. G. (2005). Ecology and evolution of aphid-ant interactions. Annual Review of Ecology Evolution and Systematics, 36, 345–372.
- 5.Styrsky, J. D., & Eubanks, M. D. (2007). Ecological consequences of interactions between ants and honeydew-producing insects. Proceedings of the Royal Society B-Biological Sciences, 274, 151–164.
- 6.Adrián Salazar, Benjamin Fürstenau, Carmen Quero, Nicolás Pérez-Hidalgo, Pau Carazo, Enrique Font, David Martínez-Torres, (2015) Aggressive mimicry coexists with mutualism in an aphid. Proceedings of the National Academy of Sciences 112 (4):1101–1106