Abstract
Ant-plant mutualisms are a prominent phenomenon in tropical rainforest ecosystems. In South East Asia the most important ant-tree symbiosis is the Macaranga complex. Until now it has been known to consist of four obligate and specific partner organisms, trees, ants, endophytic trophobiotic scale insects and endophytic fungi. Here we show that two more organisms are integrated in the system. In the stem domatia, masses of bacteria were cultivated in piles consisting of plant food body remains and ant faeces. They were consumed by masses of specific bacteriovorous nematodes. The nematodes could be identified as rhabditids, mainly Diploscapter sp., as well as a few Sclerorhabditis specimens belonging to two new species. These genera are known to be myrmecophilous and suspected of being consumed and digested by the ants. We hypothesize that with this new type of two-step association the ants obtain and recycle scarce nutrients. This is important in a system where the specific ants are highly adapted to the association, and depend exclusively on plant resources as they do not hunt and forage off the plant. The nematodes are even vertically transferred by the swarming queens and therefore present in new claustral colony foundations. Nematode breeding was found in three further, but not in all investigated tree-ant associations. These observations underline the still largely unexplored role of micro-symbionts in insects, and a potential new source of complexity in the trophic interactions in tropical ecosystems.
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References
Bignell DE, Roisin Y, Lo N (eds) (2011) Biology of Termites: a Modern Synthesis. Springer. 2nd ed, Dordrecht.
Blatrix R, Bouamer S, Morand S, Selosse MA (2009) Ant-plant mutualisms should be viewed as symbiotic communities. Plant Signal Behav 4:554–556
Blatrix R, Djieto-Lordon C, Mondolot L, La Fisca P, Voglmayr H, McKey D (2012) Plant-ants use symbiotic fungi as a food source: new insight into the nutritional ecology of ant–plant interactions. Proc R Soc B 279:3940–3937
Buschinger A, Klein RW, Maschwitz U (1994) Colony structure of a bamboo dwelling Tetraponera sp. from Malaysia. Insect Soc 41:29–41
Defossez E, Djieto-Lordon C, McKey D, Selosse MA, Blatrix R (2011) Plant-ants feed their host plant, but above all a fungal symbiont to recycle nitrogen. Proc Biol Sci 278:1419–1426
Dransfield J (1979) A Manual to the Rattans of the Malay Peninsula. Malaysian Forest Records 29, Malaysia Forest Department. Kuala Lumpur
Eilmus S, Heil M (2009) Bacterial associates of arboreal ants and their putative functions in an obligate ant-plant mutualism. App Environ Microbiol 75:4324–4332
Esquivel A, Abolafia A, Hanson P, Pinto A (2012) A new species of nematode, Sclerorhabditis neotropicalis sp. n., (Rhabditida), associated with Azteca ants in Cecropia obtusifolia. Nematropica 42:163–169
Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543
Fiala B, Maschwitz U, Tho YP, Helbig AJ (1989) Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79:463–470
Fiala B, Maschwitz U (1990) Studies on the South East Asian ant-plant association Crematogaster borneensis/Macaranga: Adaptations of the ant partner. Insect Soc 37(3): 212--231
Fiala B, Jakob A, Maschwitz U, Linsenmair KE (1999) Diversity, evolutionary specialisation and geographic distribution of a mutualistic ant-plant complex: Macaranga and Crematogaster in South East Asia. Biol J Linn Soc 66:305–331
Hanshew A, McDonald B, Díaz Díaz C, Djiéto-Lordon C, Blatrix R, Currie C (2015) Characterization of actinobacteria associated with three ant-plant mutualisms. Microbial Ecol 69:192–203
Heckroth HP, Fiala B, Gullan PJ, Maschwitz U, Idris AH (1998) The soft scale (Coccidae) associates of Malaysian ant-plants. J Trop Ecol 14:427–443
Heil M, Fiala B, Kaiser W, Linsenmair KE (1998) Chemical contents of Macaranga food bodies: adaptations to their role in ant attraction and nutrition. Funct Ecol 12:117–122
Heil M, Fiala B, Maschwitz U, Linsenmair KE (2001) On the benefits of indirect defence: short- and long-term studies in antiherbivore protection via mutualistic ants. Oecologia 126: 395--403
Hölldobler B, Wilson EO (1990) The ants. Springer, Berlin
Itioka T, Nomura M, Inui Y, Itino T, Inoue T (2000) Difference in intensity of ant defense among three species of Macaranga myrmecophytes in a Southeast Asian dipterocarp forest. Biotropica 32:318–326
Janet C (1894) Études sur les fourmis: pelodera des glandes pharyngiennes de Formica rufa L. Mém Soc Zool France 7:45–62
Kaufmann E, Maschwitz U (2006) Ant-gardens of tropical Asian rainforests. Naturwissenschaften 93:216–227
Kiontke K, Sudhaus W (2006) Ecology of Caenorhabditis species. WormBook (ed) The C. elegans Research Community, WormBook, doi:10.1895/wormbook.1.37.1. http://www.wormbook.org.
Köhler A (2012) Nematodes in the heads of ants associated with sap flux and rotten wood. Nematology 14:191–198
Markin GP, McCoy CW (1968) The occurrence of a nematode, Diploscapter lycostoma, in the pharyngeal glands of the Argentine ant, Iridomyrmex humilis. Ann Am Entomol Soc 61:505–509
Maschwitz U (1974) Vergleichende untersuchungen zur funktion der ameisenmetathoracaldrüse. Oecologia 16:303–310
Maschwitz U, Moog J (2000) Communal peeing: a new mode of flood control in ants. Naturwissenschaften 87:563–565
Mattes M, Moog J, Werner M, Fiala B, Nais J, Maschwitz U (1998) The rattan palm Korthalsia Robusta Bl. And its ant and aphid partners: studies of a myrmecophytic association in the Kinabalu Park. Sabah Parks Nat J 1:47–60
Moog J, Drude T, Maschwitz U, Agosti D (1997) Flood control by ants: water-bailing behaviour in the Southeast Asian plant-ant genus Cladomyrma wheeler (Formicidae, Formicinae). Naturwissenschaften 84:242–245
Moog J, Fiala B, Werner M, Weissflog A, Saw LG, Maschwitz U (2003) Ant-plant diversity in peninsular Malaysia, with special reference to the pasoh forest reserve. In: Okuda T, Manokaran N, Matsumoto Y, Niiyama K, Thomas SC, Ashton PS (eds) Pasoh: ecology of a lowland rainforest in Southeast Asia. Springer, Tokyo, pp. 459–494
Nickle WR, Ayre GL (1966) Caenorhabditis dolichura (A. Schneider, 1866) Dougherty (Rhabditidae: Nematoda) in the head glands of the ants Camponotus herculeanus (L.) and Acanthomyops claviger (Roger) in Ontario. Proc Entomol Soc Ontario 96:96–98
Poinar, Georg Jr. (2012) Nematode parasites and associates of Ants: Past and present. Psyche. doi:10.1155/2012/192017
Scholze VS, Sudhaus W (2011) A pictorial key to current genus groups of ‘Rhabditidae’. J Nematode Morph Syst 14:105–112
Stevens CE, Hume ID (1998) Contribution of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78:393–427
Voglmayr H, Mayer V, Maschwitz U, Moog J, Djieto-Lordon C, Blatrix R (2011) The diversity of ant-associated black yeasts: insights into a newly discovered world of symbiotic interactions. Fungal Biol 115:1077–1091
Wahab A (1962) Untersuchungen über Nematoden in den Drüsen des Kopfes der Ameisen (formicidae). Z Morph Ökol Tiere 52:33–92
Zhao ZQ, Davies KA, Brenton-Rule EC, Grangier J, Gruber MAM, Giblin-Davis RM, Lester PJ (2013) Diploscapter formicidae sp. n. (Rhabditida: Diploscapteridae), from the ant Prolasius advenus (Hymenoptera: Formicidae) in New Zealand. Nematology 15:109–123
Acknowledgments
We thank M. Ruppel, Frankfurt for the scanning electron microscope photos and their interpretation, W. Dorow for ant determination and M. Merbach for support. We are grateful to two anonymous referees for their constructive comments and language editing.
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Maschwitz, U., Fiala, B., Dumpert, K. et al. Nematode associates and bacteria in ant-tree symbioses. Symbiosis 69, 1–7 (2016). https://doi.org/10.1007/s13199-015-0367-6
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DOI: https://doi.org/10.1007/s13199-015-0367-6