Farmers and Ranchers: Food Cultivation Strategies and. Associated Behaviors of Ants

Transcription

1 Farmers and Ranchers: Food Cultivation Strategies and Associated Behaviors of Ants Victoria Wheeler BSPM 507 Insect Behavior Abstract Ants have various feeding strategies and many behaviors associated with these. Some of the most interesting involve the cultivation of fungi and the tending of honeydewproducing insects. In this review, fungus cultivating ant "farmers" as well as aphidtending ant "ranchers" are covered, and studies of their behaviors used to care for their food sources are summarized. Introduction Ants have long fascinated people. We marvel at their complex societies comprised of tiny workers toiling for the benefit of a queen, at burly soldiers patrolling the land, at their burrows that sprawl underground. These traits are impressive to us because they are things we associate with ourselves, yet here they are, performed by the tiny ant. Ants have an amazing array of behaviors that serve them well, including an array of food collection and production strategies. Though many ants are predators and scavengers, a variety of species have developed food production strategies that are especially interesting. While other ants are committed to a life of hunting for prey or gathering other food sources, some species have gone a different route, taking to the life of a

2 farmer. These ants form mutualistic relationships with fungal and animal species that they cultivate and protect in order to gain food benefits. Discussion Cultivation of Fungus The ants of the tribe Attini are a large monophyletic group of New World ants. These ants are obligate agriculturalists - they cannot subsist without their cultivated crop, a fungus that serves as the only food source of the larvae as well as a main part of the adult diet (Mueller et al., 2005). The basidomycete fungi cultivated by the numerous attine are polyphyletic (Chapela, 1994). The ants provide the fungus with a place to go, protection, and dispersal opportunities. When a new queen leaves the nest, she takes with her a small pellet of fungal material with her in a structure known as an infrabuccal pocket, which she uses to "seed" a fungus garden in her new nest (Mueller, 2001). The substrates used by Attine species varies, with a few genera using highly specific substrates (Atta, Acromyrmex, Cyphomyrmex) and other genera using a wide variety of substrates, including leaf cuttings as well as decayed material, insect frass, and flowers (De Fine Licht, 2010). The fungal cultivars of fungus cultivating ants are susceptible to infection with pathogens, including parasitic fungi in the genus Escovopis, and members of this genus are second only to the symbiotic fungus in prevalence in ant gardens (Currie, 1999a). As is true with human crops, these ant-grown monocultures can be susceptible to disease and parasites. As such, the ants have developed behavioral strategies and other mechanisms to cope with this potential for infection. Currie and Stuart (2001) studied the

3 behavior of Atta columbica ants in relation to pathogenic fungus species including the specialized Escovopis and the generalist Trichoderma. The researchers introduced the spores of these fungi to the gardens of the ants and monitored their behavior. The researchers were looking at fungus grooming behavior, in which ants clean their fungal crop with their mouthparts, as well as weeding, which involves the removal of infected material from the nest. In both treatments, the fungus-grooming response was directed and much faster than the response in gardens treated with water, the control. The grooming behavior was altogether rare in the control. Furthermore, the response was stronger and lasted longer in cases of infection with Escovopis than Trichoderma. Weeding behavior, defined as removal of garden material, especially infected material, was only observed in about 5% of the control gardens, while it occurred in 50%-70% of the experimental gardens, indicating that weeding is also a directed behavior in response to infection. More similar to the strategy humans use to combat crop diseases and parasites is the actinomycete bacteria apparently used by ants to control parasites. These filamentous actinomycetes produce antibacterial compounds (Currie, 1999b). The ants use several different bacteria and antifungals in their defense, and while certain species may have coevolved with the ants, others may be acquired from the environment (Barke, 2010). The infrabuccal pocket, mentioned before as important in dispersal to new colonies, may also be important with regard to control of pathogens by the ants. In addition to fungus grooming and weeding behaviors, Tachymyrmex zeteki ants were found to use their infrabuccal pouches in fungal disease control. In a study by Little et al. (2006), the ants

4 were found to collect parasitic Escovopsis spores. Actinomycete bacteria within the pouches release an antibiotic presumed to kill the fungal parasites. The researchers data also showed the ants distinguished between viable and non-viable Escovopsis spores. When the pockets are full, the ants expel the material as pellets, which they deposit in piles. These pellets were found to contain few or no viable Escovopsis spores. It is unclear why the ants collect these pellets into piles near their gardens. In our own society, the workforce is specialized and production is optimized as a result. Abramowski et al. (2010) investigated the ants' behavioral defenses as they relate to caste specialization. Many ant species produce specialized castes that perform different tasks. This study looked at Acromyrmex octospinosus major and minor workers. The effect of infection with Escovopsis fungus was tested. Both castes were present and participated in removal of infected spores. In the experimental groups, minor workers were observed to show the most fungus grooming behavior. Few weeding events were observed, but the overwhelming majority of those observed were performed by major workers. These differences are likely to be related to the sizes of each caste being optimized for certain tasks. In general, minor workers tended to be in contact with the garden more often than majors. The researchers also tested the effect of worker mixtures, finding that in early infection stages, gardens with minors only performed the best, followed by a mixed group and finally majors only, indicating that at this stage, fungus grooming is most important to controlling infection. If Escovopsis was given time to establish itself before workers were introduced, major workers performed as well as minors, indicating they may have a larger role in disease control at this later stage in which grooming is less

5 effective. It is apparent that different castes are optimized for different tasks, and their is indeed a division of labor in fungus tending behaviors. In human agriculture and life, it is important to keep crops and areas free of debris, especially debris that is potentially infective. Bot et al. (2001) found that waste management behaviors were also important to long term health in Attine ant colonies. They studied various species of leafcutter ants, which tend to be large societies that produce a lot of waste which is subsequently deposited in dumps above or below ground. Some, such as Atta cephalotes, have specific dump workers which begin life in garden areas. As they grow older, they move away to riskier foraging or waste management behaviors. In this way, only older, less valuable workers are exposed to outside danger. The study found the specialized parasite Escovopsis to be abundant in waste material of Atta columbia, present in 70% of colonies. The researchers concluded that an important function of dumps is to prevent reinfection of the fungal crop, as much of the waste is infected with its parasites. Interactions With Honeydew-Producing Insects Ants also form mutualistic relationships with various honeydew-producing Hemipterans such as aphids, treehoppers and leafhoppers. These animals secrete honeydew, often upon antennal palpation by their ant "shepherds", which is then easily collected and transported by the ant. The ants also expel competing herbivores and protect their Hemipteran symbionts from predators in addition to keeping the colony clean. Honeydew is the currency in this relationship, and as long as the cost is low and the benefit is high, the mutualism is retained (as

6 summarized by Detrain et al., 2010). Unlike ant-fungus mutualisms, these mutualisms are generally considered to be facultative as opposed to obligate (Nielsen et al., 2010). The ants promote survival of the symbiotic Hemipterans while behaving antagonistically toward non-symbiotic ones. They also provide benefits to the host plants, preventing them from excessive herbivory by excluding more damaging species (Minarro et al. 2010). Perhaps one of the most interesting of these mutualisms is between the nomadic herdsman Dolichoderous cuspidatus and its mealybug, Malaicoccus formicarii. These ants act much like human herdsman, tending their herds and even moving them to different "pastures". D. cuspidatus interacts very specifically with M. formicarii. They are not observed to hunt, but accept dead prey they find. The mealybugs feed on sap from young shoots and are attended by many ant workers, and the ants and mealybugs aggregate closely during feeding. The workers form trails from the nest and to feeding sites, and new feeding sites are scouted as necessary. At feeding sites, mealybugs continuously secrete their honeydew which is immediately consumed by the ants. When disturbed, ants carry mealybugs, which remain still during transport. They are also transported to new nests and when new colonies are formed. To protect the mealybugs, the ants form a tentlike structure over them during rain and defend them aggressively against any arthropod intruders. The researchers also tested whether the two species could live independently. Without the mealybugs, the ants gradually died off, seemingly from a lack of food. The mealybugs appeared unwilling to forage, and those that did were soon overcome by their own waste (Maschwitz and Hanel, 1984).

7 Investigated by Moya-Raygoza and Nault (2000), the Hemipteran Dalbulus quinquenotatus is a leafhopper species attended by Brachymyrmex, Camponotus, and Pheidole ant species. In these interactions, significantly more leafhoppers were present where they were attended versus when they were unattended, indicating the protective behavior of attendant ants is important to the survival of the treehoppers. Tending ants protect the leafhoppers from arthropod predators, including spiders. Without the ants, they die out quickly. The ant shepherds are also important to the host plant. The ants remove competitive herbivores (D. gelbus) that would otherwise damage the plant, and in lean times, also remove excess D. quinquenotatus to avoid stressing the plant host. However, if the ants did not have sufficient insect prey to receive the proper amounts of protein, they resorted to consuming the Hemipterans themselves. Additionally, though the leafhoppers were obligate myrmecophiles, the ants appeared to be more flexible. If offered sufficient insect prey and supplemental honey, few ants bothered to tend the leafhoppers, unlike some other Hemipteran-ant mutualisms. Not only do ants defend their aphids against predators, but Nielsen et al. (2010) found that Formica podzolica, which tends Aphis asclepiadis, has specific behaviors to prevent and control the spread of disease in the aphid. The ants respond to dead aphids, removing carcasses experimentally infected by a fungal pathogen quickly and more frequently than uninfected dead aphids and uninfected live aphids. Additionally, more of the fungal cadavers were placed further from the feeding site than non-fungal ones. Infected living aphids elicited a similar response, with infected aphids being removed much faster. Ants also more frequently performed self grooming after handling infected aphids than after

8 handling non-infected aphids. Aphid grooming was also increased. Though the ants are facultative aphid mutualists, the benefits of tending the ants is presumed to be high enough that these behaviors have evolved, and the fungus might actually reinforce this mutualistic relationship. Certain ant species also limit the dispersal of their Hemipteran symbionts. Oliver et al. (2007) studied the effect Lasius niger ant semiochemicals might have on Aphis fabae and Acyrthosiphon pisum aphid dispersal. Semiochemicals are used by ants to signal other ants, and there is evidence that other species respond to them as well. Aphids moved at a slower pace and dispersed shorter distances when in the presence of ant semiochemicals. Presence of actual ants had no effect. In this way ants can limit the local dispersal of the aphids. Long distance dispersal can be controlled by removing or inhibiting wing growth in the aphid species. By limiting their dispersal, ants benefit by securing access to this high quality food source. Detrain et al. (2010) investigated the effect honeydew itself can have an effect on ant behavior. Lasius niger, an aphid-tending ant, was tested for preferences to sugars, individual and social responses to sugars. The sugars sucrose and fructose were the most common of 9 sugars detected in the Aphis fabae honeydew. While foraging, the scouts appear to find sugar sources by chance. Ants laid more trails upon return to the colony when they had ingested melezitose, sucrose or raffinose, but not toward fructose or glucose. All five of these sugars, however, caused ant scouts to spend much longer drinking from these sources. Though the abundant sugars did not elicit much of a social

9 response, the more honeydew specific sugars elicited a strong response, indicating that they may serve as a signal of an aphid colony's presence. Aphids produce a high quality, steady supply of sugar readily usable by the ants. This is a resource viewed as valuable and worth defending, and the ants increase recruitment of workers in response. It is not clear, however, whether the ant's preferences shaped or were shaped by honeydew composition. Matsuura and Yashiro (2006) studied Stomaphis hirukawai is an aphid species that feeds on the woody parts of hinoki cypress. It possesses extremely large mouthparts that it has a difficult time withdrawing quickly enough to escape predation. It is therefore dependent upon its attendant ant, Lasius productus, for defense. The ant, in turn, has little else to eat in the cypress habitat and is therefore dependent upon the aphid for food. Curiously, this aphid has females, males and eggs which are found in the nest of the ants. L. productus workers collected the eggs, placed them in the nest, and groomed them. Survival rates were much greater for these eggs than untended ones. Starving the ants did not cause them to consume the eggs. It is not clear whether the ants care for the aphids and their eggs for their own benefit, or whether the aphids are somehow controlling the behavior of the ants. The humble ant has developed a striking variety of life strategies, and mutualistic relationships with other species are among the most interesting. These complex relationships range from facultative to obligate and benefit both the ants and the others they have aligned themselves with. This is an area of special interest for behavioral

10 research as a huge variety of behavior is observable in the various ant species as well as their symbiotic partners. It is also an interesting area of study for subjects such as pest management, and perhaps there is even something to be learned from the ant about agriculture. References Abramowski, D., Currie, C.R., Poulsen, M. (2010) Caste specialization in behavioral defenses against fungus garden parasites in Acromyrmex octospinosus leaf-cutting ants. Insect. Soc. Vol. 58, pp Barke, J., Seipke, R.F., Grüschow, S., Heaven, D., Drou, N., Bibb, M.J., Goss, R.M.J., Yu, D.W., Hutchings, M.I. (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biology. Vol. 8, pp Bot, A.M.N., Currie, C.R., Hart, A.G., Boomsma, J.J. (2001) Waste management in leaf-cutting ants. Ethology Ecology & Evolution. Vol. 13, pp Chapela, I.H., Rehner, S.A., Schultz, T.R., Mueller, U.G. (1994) Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science. Vol. 266, pp Currie, C.R., Mueller, U.G., Malloch, D. (1999a) The agricultural pathology of ant fungus gardens. Proc. Natl. Acad. Sci. USA. Vol. 96, pp Currie, C.R., Scott, J.A., Summerbell, R.C., Malloch, D. (1999b) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature. Vol. 398, pp Currie, C.R., Stuart, A.E. (2001) Weeding and grooming of pathogens in agriculture by ants. Proc. R. Soc. Lond. B. Vol. 268, pp

11 De Fine Licht, H.H., Boomsma, J.J. (2010) Forage collection, substrate preparation, and diet composition in fungus-growing ants. Ecological Entomology. Vol. 35, pp Little, A.E.F., Takahiro, M., Mueller, U.G., Currie, C.R. (2006) Defending against parasites: fungus growing ants combine specialized behaviors and microbial symbionts to protect their fungus gardens. Biology Letters. Vol. 2, pp Maschwitz, U., Hanel, H. (1984) The migrating herdsman Dolichoderus (Diabolus) cuspidatus: an ant with a novel mode of life. Behavioral Ecology and Sociobiology. Vol. 17, pp Matsuura, K., Yashiro, T. (2006) Aphid egg protection by ants: a novel aspect of the mutualism between the tree-feeding aphid Stomaphis hirukawai and its attendant ant Lasius productus. Naturwissenschaften. Vol. 93, pp Minarro, M., Fernandez-Mata, G., Medina, P. (2010) Role of ants in structuring the aphid community. Ecological Entomology. Vol. 35, pp Moya-Raygoza, G., Nault, L.R. (2000) Obligatory mutualism between Dalbulus quinquenotatus (Homoptera: Cicadellidae) and Attendant ants. Annals of the Entomological Society of America. Vol. 93, Mueller, U.G., Gerardo, N.M., Aanen, D.K., Six, D.L., Schultz, T.R. (2005) The Evolution of Agriculture in Insects. Annu. Rev. Ecol. Evol. Syst. Vol. 36, pp Mueller, U.G., Schultz, T.R., Currie, C.R., Adams, R.M.M., Malloch, D. (2001) The Origin of the Attine Ant-Fungus Mutualism. The Quarterly Review of Biology. Vol. 76, pp Nielsen, C., Agrawal, A.A., Hajek, A.E. (2010) Ants defend aphids against lethal disease. Biology Letters. Vol. 6, pp Oliver, T.H., Mashanova, A., Leather, S.R., Cook, J.M., Jansen, V.A.A. (2007) Ant semiochemicals limit apterous aphid dispersal. Proceedings of the Royal Society. Vol.

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