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Leafcutter ant

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Atta cephalotes, Wilhelma Zoo, Stuttgart

Leafcutter ants are fungus-growing ants that share the behaviour of cutting leaves which they carry back to their nests to farm fungus. Next to humans, leafcutter ants form some of the largest and most complex animal societies on Earth. In a few years, the central mound of their underground nests can grow to more than 30 m (98 ft) across, with smaller radiating mounds extending out to a radius of 80 m (260 ft), taking up 30 to 600 m2 (320 to 6,460 sq ft) and converted into 3.55 m individuals.

Leafcutting groups

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Leafcutter ants are any of at least 55 species[1][2][3] of leaf-chewing ants belonging to the three genera Atta, Acromyrmex, and Amoimyrmex, within the tribe Attini.[4] These species of tropical, fungus-growing ants are all endemic to South and Central America, Mexico, and parts of the southern United States.[5] Leafcutter ants can carry twenty times their body weight[6] and cut and process fresh vegetation (leaves, flowers, and grasses) to serve as the nutritional substrate for their fungal cultivates.[7]

Acromyrmex and Atta ants have much in common anatomically; however, the two can be identified by their external differences. Atta ants have three pairs of spines and a smooth exoskeleton on the upper surface of the thorax, while Acromyrmex ants have four pairs and a rough exoskeleton.[8] The exoskeleton itself is covered in a thin layer of mineral coating, composed of rhombohedral crystals that are generated by the ants.[9] Amoimyrmex and Acromyrmex differ in that Amoimyrmex lacks tubercles on the first gastral segment, and recent phylogenetic evidence shows that Amoimyrmex diverged before the other two genera of leafcutter ants.[4]

Colony lifecycle

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Reproduction and colony founding

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Atta colombica, queen with larvae and workers on substrate

Winged females and males leave their respective nests en masse and engage in a nuptial flight known as the revoada (Portuguese) or vuelo nupcial (Spanish). Each female mates with multiple males to collect the 300 million sperm she needs to set up a colony.[10]

Once on the ground, the female loses her wings and searches for a suitable underground lair in which to found her colony. The success rate of these young queens is very low, and only 2.5% will go on to establish a long-lived colony. To start her own fungus garden, the queen stores bits of the parental fungus garden mycelium in her infrabuccal pocket, which is located within her oral cavity.[11] Colonies are generally founded by individual queens – haplometrosis.[12]: 125  Because colonies with multiple queens over the lifespan of the colony have been found by a large number of investigators – by Weber 1937, Jonkman 1977, Huber 1907, Moser & Lewis 1981, Mariconi & Zamith 1963, Moser 1963, and Walter et al 1938 – it is believable that some colonies have multiple foundresses – termed pleometrosis.[12]: 125  Pleometrosis is confirmed only for Atta texana by Vinson 1985.[12]: 125 

Colony hierarchy

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In leafcutter colonies, ants are divided into castes, based mostly on size, that perform different functions. Acromyrmex and Atta exhibit a high degree of polymorphism, four castes being present in established colonies—minims, minors, mediae, and majors. Majors are also known as soldiers or dinergates. Atta ants are more polymorphic than Acromyrmex, meaning comparatively less difference occurs in size from the smallest to largest types of Acromyrmex.[citation needed]

Leafcutter ant Atta cephalotes
  • Minims are the smallest workers, and tend to the growing brood or care for the fungus gardens. Head width is less than 1 mm.
  • Minors are slightly larger than minim workers, and are present in large numbers in and around foraging columns. These ants are the first line of defense and continuously patrol the surrounding terrain and vigorously attack any enemies that threaten the foraging lines. Head width is around 1.8–2.2 mm.
  • Mediae are the generalized foragers, which cut leaves and bring the leaf fragments back to the nest.
  • Majors, the largest worker ants, act as soldiers, defending the nest from intruders, although recent evidence indicates majors participate in other activities, such as clearing the main foraging trails of large debris and carrying bulky items back to the nest. The largest soldiers (Atta laevigata) may have total body lengths up to 16 mm and head widths of 7 mm.[citation needed]

Ant–fungus mutualism

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Their societies are based on an ant–fungus mutualism, and different species of ants use different species of fungus, but all of the fungi the ants use are members of the family Lepiotaceae. The ants actively cultivate their fungus, feeding it with freshly cut plant material and keeping it free from pests and molds. This mutualistic relationship is further augmented by another symbiotic partner, a bacterium that grows on the ants and secretes chemicals; essentially, the ants use portable antimicrobials. Leaf cutter ants are sensitive enough to adapt to the fungi's reaction to different plant material, apparently detecting chemical signals from the fungus. If a particular type of leaf is toxic to the fungus, the colony will no longer collect it. The only two other groups of insects to use fungus-based agriculture are ambrosia beetles and termites. The fungus cultivated by the adults is used to feed the ant larvae, and the adult ants feed on leaf sap. The fungus needs the ants to stay alive, and the larvae need the fungus to stay alive, so mutualism is obligatory.

The fungi used by the higher attine ants no longer produce spores. These ants fully domesticated their fungal partner 15 million years ago, a process that took 30 million years to complete.[13] Their fungi produce nutritious and swollen hyphal tips (gongylidia) that grow in bundles called staphylae, to specifically feed the ants.[14] Leucoagaricus gongylophorus is the most commonly documented fungi farmed by higher attine ant species.[15][16]

Behaviour

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Workers of Atta colombica at work
Leafcutter ant in Costa Rica

Leafcutter ants have very specific roles in taking care of the fungal garden and dumping the refuse. Waste management is a key role for each colony's longevity. The necrotrophic parasitic fungus Escovopsis threatens the ants' food source and thus is a constant danger to the ants. The waste transporters and waste-heap workers are the older, more dispensable leafcutter ants, ensuring the healthier and younger ants can work on the fungal garden. The Atta colombica species, unusually for the Attine tribe, have an external waste heap. Waste transporters take the waste, which consists of used substrate and discarded fungus, to the waste heap. Once dropped off at the refuse dump, the heap workers organise the waste and constantly shuffle it around to aid decomposition. A. colombica have been observed placing dead ants around the perimeter of the waste heap.[17][18]

In addition to feeding the fungal garden with foraged food, mainly consisting of leaves, it is protected from Escovopsis by the antibiotic secretions of Actinomycetota (genus Pseudonocardia). This mutualistic micro-organism lives in the metapleural glands of the ant.[19] Actinomycetota are responsible for producing the majority of the world's antibiotics today.

Leafcutter ants use chemical communication and stridulation (substrate-borne vibrations) to communicate with each other.[20]

Leafcutter ants prefer disturbed habitats, likely due to higher concentrations of pioneer plant species. These are more attractive food sources because pioneer plants have lower levels of secondary metabolites and higher nutrient concentrations than the shade-tolerant species that will come later.[21]

Parasites

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When the ants are out collecting leaves, they are at risk of attack by some species of phorid flies, parasitoids that lay eggs into the crevices of the worker ants' heads. Often, a minim will sit on a worker ant and ward off any attack.[22]

Also, the wrong type of fungus can grow during cultivation. Escovopsis, a highly virulent fungus, has the potential to devastate an ant garden, as it is horizontally transmitted. Escovopsis was cultured, during colony foundation, in 6.6% of colonies.[23] However, in one- to two-year-old colonies, almost 60% had Escovopsis growing in the fungal garden.[24]

Nevertheless, leafcutter ants have many adaptive mechanisms to recognize and control infections by Escovopsis and other micro-organisms.[25] The most common known behaviors rely on workers reducing the number of fungal spores by grooming, or removing an infected piece of the fungus garden and throwing it away at the waste dump (described as weeding).[26]

Interactions with humans

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In some parts of their range, leafcutter ants can be a serious agricultural pest, defoliating crops and damaging roads and farmland with their nest-making activities.[10] For example, some Atta species are capable of defoliating an entire citrus tree in less than 24 hours. A promising approach to deterring attacks of the leafcutter ant Acromyrmex lobicornis on crops has been demonstrated. Collecting the refuse from the nest and placing it over seedlings or around crops resulted in a deterrent effect over a period of 30 days.[27]

See also

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References

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  1. ^ Shattuck, Steven O. "Acromyrmex". AntWiki. antwiki.org. Retrieved 15 October 2024.
  2. ^ Shattuck, Steven O. "Atta". AntWiki. antwiki.org. Retrieved 15 October 2024.
  3. ^ Shattuck, Steven O. "Amoimyrmex". AntWiki. antwiki.org. Retrieved 15 October 2024.
  4. ^ a b Cristiano, Maykon Passos; et al. (5 December 2020). "Amoimyrmex Cristiano, Cardoso & Sandoval, gen. nov. (Hymenoptera: Formicidae): a new genus of leaf-cutting ants revealed by multilocus molecular phylogenetic and morphological analyses". Austral Entomology. 59 (4): 643–644. doi:10.1111/aen.12493. Retrieved 15 October 2024.
  5. ^ Piper 2007, pp. 11–13.
  6. ^ "Leafcutter Ant" (PDF). Archived from the original (PDF) on February 23, 2018.
  7. ^ Schultz, T. R.; Brady, S. G. (2008). "Major evolutionary transitions in ant agriculture". Proceedings of the National Academy of Sciences of the United States of America. 105 (14): 5435–5440. Bibcode:2008PNAS..105.5435S. doi:10.1073/pnas.0711024105. PMC 2291119. PMID 18362345.
  8. ^ Hedlund, Kye S. (March 2005). "Diagnoses of the North American: Ant Genera (Hymenoptera: Formicidae)". Archived from the original on August 24, 2007.
  9. ^ Li, Hongjie & Sun, Chang-yu (2020), "Biomineral armor in leaf-cutter ants", Nature Communications, 11 (11): 5792, Bibcode:2020NatCo..11.5792L, doi:10.1038/s41467-020-19566-3, PMC 7686325, PMID 33235196.
  10. ^ a b Piper, Ross (2007), Extraordinary Animals: An Encyclopedia of Curious and Unusual Animals, Greenwood Press, p. 298, ISBN 978-0-313-33922-6.
  11. ^ Weber, Neal A. (1972), Gardening Ants, The Attines, The American Philosophical Society, pp. 14, 34, ISBN 978-0-87169-092-0.
  12. ^ a b c Lofgren, Clifford; Meer, Robert K. Vander, eds. (2018). Fire Ants and Leaf-cutting Ants : Biology and Management. New York, NY: Routledge. pp. xv+435. ISBN 978-0-429-03826-6. OCLC 1090012991.
  13. ^ Institution, Smithsonian. "Crop Domestication Is a Balancing Act". Smithsonian Institution. Retrieved 2024-09-29.
  14. ^ Wade, Nicholas (1999-08-03). "For leaf-cutter ants, farm life isn't so simple". The New York Times.
  15. ^ Pathak, Ayush; Kett, Steve; Marvasi, Massimiliano (2019-09-26). "Resisting Antimicrobial Resistance: Lessons from Fungus Farming Ants". Trends in Ecology & Evolution. 34 (11): 974–976. Bibcode:2019TEcoE..34..974P. doi:10.1016/j.tree.2019.08.007. PMID 31564381.
  16. ^ Benjamin, Richard K.; Blackwell, Meredith; Chapela, Ignacio H.; Humber, Richard A.; Jones, KEVIN G.; Klepzig, Kier D.; Lichtwardt, Robert W.; Malloch, David; Noda, Hiroaki (2004-01-01), Mueller, Gregory M.; Bills, GERALD F.; Foster, Mercedes S. (eds.), "Insect- and Other Arthropod-Associated Fungi", Biodiversity of Fungi, Burlington: Academic Press, pp. 395–433, doi:10.1016/b978-012509551-8/50021-0, ISBN 978-0-12-509551-8, retrieved 2022-07-08
  17. ^ Hart, A. G.; Ratnieks, F. L. W. (2002), "Waste management in the leaf-cutting ant Atta colombica", Behavioral Ecology, 13 (2): 224–231, doi:10.1093/beheco/13.2.224.
  18. ^ Bot, A. N. M.; Currie, C. R.; Hart, A. G.; Boomsma, J. J. (2001), "Waste Management in Leaf-cutting Ants", Ethology Ecology and Evolution, 13 (3): 225–237, Bibcode:2001EtEcE..13..225B, doi:10.1080/08927014.2001.9522772, S2CID 18918574.
  19. ^ Zhang, M. M.; Poulsen, M. & Currie, C. R. (2007), "Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants", The ISME Journal, 1 (4): 313–320, Bibcode:2007ISMEJ...1..313Z, doi:10.1038/ismej.2007.41, PMID 18043642.
  20. ^ Hager, Felix A.; Kirchner, Lea; Kirchner, Wolfgang H. (2017-12-15). "Directional vibration sensing in the leafcutter ant Atta sexdens". Biology Open. 6 (12): 1949–1952. doi:10.1242/bio.029587. ISSN 2046-6390. PMC 5769659. PMID 29247049.
  21. ^ Farji-Brener, Alejandro G. (2001). "Why are leaf-cutting ants more common in early secondary forests than in old-growth tropical forests? An evaluation of the palatable forage hypothesis". Oikos. 92 (1). Nordic Society Oikos (Wiley): 169–177. Bibcode:2001Oikos..92..169F. doi:10.1034/j.1600-0706.2001.920120.x. hdl:10088/1425. ISSN 0030-1299.
  22. ^ "Leafcutter Ants", Lincoln Park Zoo, archived from the original on 2008-05-16
  23. ^ Currie, C. R.; Mueller, U. G. & Malloch, D. (1999), "The agricultural pathology of ant fungus gardens", PNAS, 96 (14): 7998–8002, Bibcode:1999PNAS...96.7998C, doi:10.1073/pnas.96.14.7998, PMC 22176, PMID 10393936.
  24. ^ Reynolds, H. T. & Currie, C. R. (2004), "Pathogenicity of Escovopsis weberi: The parasite of the attine ant-microbe symbiosis directly consumes the ant-cultivated fungus", Mycologia, 96 (5): 955–959, doi:10.2307/3762079, JSTOR 3762079, PMID 21148916.
  25. ^ Goes, A. C.; Barcoto, M. O.; Kooij, P. W.; Bueno, O. C.; & Rodrigues, A. (2020), "How do leaf-cutting ants recognize antagonistic microbes in their fungal crops?", Frontiers in Ecology and Evolution, 8 (95): 1–12, doi:10.3389/fevo.2020.00095.
  26. ^ Currie, C. R.; & Stuart, A. E. (2001), "Weeding and grooming of pathogens in agriculture by ants", Proceedings of the Royal Society of London B, 268 (1471): 1033–1039, doi:10.1098/rspb.2001.1605, PMC 1088705, PMID 11375087.
  27. ^ Ballari, S. A. & Farji-Brener, A. G. (2006), "Refuse dumps of the leaf-cutting ants as a deterrent for ant herbivory: does refuse age matter?", The Netherlands Entomological Society, 121 (3): 215–219, Bibcode:2006EEApp.121..215B, doi:10.1111/j.1570-8703.2006.00475.x, S2CID 85410418.
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