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Oecologia

, Volume 158, Issue 1, pp 165–175 | Cite as

Soil temperature, digging behaviour, and the adaptive value of nest depth in South American species of Acromyrmex leaf-cutting ants

  • Martin Bollazzi
  • Jenja Kronenbitter
  • Flavio Roces
Behavioral Ecology - Original Paper

Abstract

In leaf-cutting ants, workers are expected to excavate the nest at a soil depth that provides suitable temperatures, since the symbiotic fungus cultivated inside nest chambers is highly dependent on temperature for proper growth. We hypothesize that the different nesting habits observed in Acromyrmex leaf-cutting ants in the South American continent, i.e. superficial and subterranean nests, depend on the occurrence, across the soil profile, of the temperature range preferred by workers for digging. To test this hypothesis, we first explored whether the nesting habits in the genus Acromyrmex are correlated with the prevailing soil temperature regimes at the reported nest locations. Second, we experimentally investigated whether Acromyrmex workers engaged in digging use soil temperature as a cue to decide where to excavate the nest. A bibliographic survey of nesting habits of 21 South American Acromyrmex species indicated that nesting habits are correlated with the soil temperature regimes: the warmer the soil at the nesting site, the higher the number of species inhabiting subterranean nests, as compared to superficial nests. For those species showing nesting plasticity, subterranean nests occurred in hot soils, and superficial nests in cold ones. Experimental results indicated that Acromyrmex lundi workers use soil temperature as an orientation cue to decide where to start digging, and respond to rising and falling soil temperatures by moving to alternative digging places, or by stopping digging, respectively. The soil temperature range preferred for digging, between 20°C and maximally 30.6°C, matched the range at which colony growth would be maximized. It is suggested that temperature-sensitive digging guides digging workers towards their preferred range of soil temperature. Workers’ thermopreferences lead to a concentration of digging activity at the soil layers where the preferred range occurs, and therefore, to the construction of superficial nests in cold soils, and subterranean ones in hot soils. The adaptive value of the temperature-related nesting habits, and the temperature-sensitive digging, is further discussed.

Keywords

Acromyrmex Ants Nest Excavation Soil climate 

Notes

Acknowledgements

Thanks to Angel Vidal for developing the computer-controlled thermostatic system, and to Annette Laudahn, Steffanie Henkel and Silvia Cardozo for valuable help during the experiments. Thanks to Oliver Geissler for collecting the A.lundi colony. This research was supported by funds from the German Research Council (DFG, grant SFB 554/TP E1) and the German Academic Exchange Service (DAAD, PhD fellowship granted to M. B.).

References

  1. Alvalá RCS, Gielow R, da Rocha HR, Freitas HC, Lopes JM, Manzi AO, Diaz MAFS, Cabral OMR (2002) Intradiurnal and seasonal variability of soil temperature, heat flux, soil moisture content, and thermal properties under forest and pasture in Rondônia. J Geophys Res 107:8043CrossRefGoogle Scholar
  2. Bass M, Cherrett JM (1995) Fungal hyphae as a source of nutrients for the leaf-cutting ant Atta sexdens. Physiol Entomol 20:1–6CrossRefGoogle Scholar
  3. Bollazzi M, Roces F (2002) Thermal preference for fungus culturing and brood location by workers of the thatching grass-cutting ant Acromyrmex heyeri. Insectes Soc 49:153–157CrossRefGoogle Scholar
  4. Bonetto AA (1959) Las hormigas “cortadoras” de la provincia de Santa Fé (Géneros: Atta y Acromyrmex). Ministerio de Agricultura y Ganaderia, Provincia de Santa Fe, ArgentinaGoogle Scholar
  5. Brandão CRF, Mayhé-Nunes AJ (2007) A phyologenetic hypothesis for the Trachymyrmex species groups, and the transition from fungus-growing to leaf-cutting in the Attini. In: Snelling RR, Fisher BL, Ward PS (eds) Advances in ant systematics (Hymenoptera:Formicidae): homage to E.O. Wilson: 50 years of contributions. Memoirs of the American Entomological Institute, vol 80. American Entomological Institute, GainesvilleGoogle Scholar
  6. Brian MV, Brian AD (1951) Insolation and ant populations in the west of Scotland. Trans R Entomol Soc Lond 102:303–330Google Scholar
  7. Bruch C (1923) Estudios mirmecológicos con la descripción de nuevas especies de dípteros (Phoridae) por los Rr. Pp. H. Schmitz y Th. Borgmeier y de una araña (Gonyleptidae) por el Doctor Mello-Leitão. Rev Mus La Plata 27:172–220Google Scholar
  8. Buhl J, Deneubourg J, Grimall AGT (2005) Self-organized digging activtiy in ant colonies. Behav Ecol Sociobiol 58:9–17CrossRefGoogle Scholar
  9. Callcott AMA, Oi DH, Collins HL, Williams DF, Lockley TC (2000) Seasonal studies of an isolated red imported fire ant (Hymenoptera: Formicidae) population in eastern Tennessee. Environ Entomol 29:788–794Google Scholar
  10. Camargo R, Forti LC, Lopes JF, De Andrade APP (2004) Characterization of Acromyrmex subterraneus bruneus (Hymenoptera:Formicidae) young nests in a fragment of the neotropical forest. Rev Árvore 28:309–312CrossRefGoogle Scholar
  11. Campbell GS (1977) An introduction to environmental biophysics. Springer, New YorkGoogle Scholar
  12. Carbonell CS (1943) Las hormigas cortadoras del Uruguay. Rev Asoc Ing Agron Montev 15:30–39Google Scholar
  13. CPTEC (2006) Plataforma de Coleta de Dados. Centro de Previsao de Tempo e Estudos Climaticos. Ministerio de Ciencia e Tecnologia. Brasil. http://satelite.cptec.inpe.br/PCD/
  14. De Andrade ML (1991) Bionomia e Distribução do Gênero Acromyrmex Mayr, 1865 (Hymenoptera: Formicidae) no estado de São Paulo, Brasil., M.S. thesis Universidade Estadual Paulista, Botucatu, São Paulo, BrasilGoogle Scholar
  15. Deneubourg JL, Franks NR (1995) Collective control without explicit coding: the case of communal nest excavation. J Insect Behav 8:417–432CrossRefGoogle Scholar
  16. Diehl-Fleig E, Droste A (1992) Localizaçâo, morfologia externa e flutuações populacionais ao longo do ano de colônias de Acromyrmex heyeri (Hymenoptera: Formicidae). An Soc Entomol Bras 21:21–27Google Scholar
  17. Espina ER, Timaure A (1977) Características de los nidos de Acromyrmex landolti (Forel), en el oeste de Venezuela. Rev Fac Agron Univ Zulia 4:53–62Google Scholar
  18. Farji-Brener AG (1994) Leaf-cutting ants (Atta and Acromyrmex) inhabiting Argentina: patterns in species richness and geographical range sizes. J Biogeogr 21:391–399CrossRefGoogle Scholar
  19. Farji-Brener AG (2000) Leaf-cutting ant nests in temperate environments: mounds, mound damages and nest mortality in Acromyrmex lobicornis. Stud Neotrop Fauna Environ 35:131–138CrossRefGoogle Scholar
  20. Fernandes Soares IM, Della Lucia TMC, dos Santos AA, Cardoso Nascimento I, Delabie JHC (2006) Caracterizaçâo de ninhos e tamanho da colônia de Acromyrmex rugosus (F.Smith) (Hymenoptera, Formicidae, Attini) em restingas de Ilhéus, BA, Brasil. Rev Bras Entomol 50:128–130Google Scholar
  21. Fowler HG (1982) Evolution of the foraging behaviour of leaf-cutting ants (Atta and Acromyrmex). In: Breed MD, Michener CD, Evans HE (eds)The biology of social insects. Proceedings of the 9th congress of the international union for the study of social insects. West View Press, BoulderGoogle Scholar
  22. Fowler HG (1983) Distribution patterns of Paraguayan leaf-cutting ants (Atta and Acromyrmex) (Formicidae: Attini). Stud Neotrop Fauna Environ 18:121–138CrossRefGoogle Scholar
  23. Fowler HG (1985) Leaf-cuttings ants of the genera Atta and Acromyrmex of Paraguay. Dtsch Entomol Z 32:19–34Google Scholar
  24. Fowler HG, Claver S (1991) Leaf-cutter ant assemblies: effects of latitude, vegetation, and behaviour. In: Huxley CR, Cutler DF (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 51–59Google Scholar
  25. Gonçalves CR (1961) O gênero Acromyrmex no Brasil (Hym. Formicidae). Stud Entomol 4:113–180Google Scholar
  26. Griffin DH (1994) Fungal physiology. Wiley-Liss, New YorkGoogle Scholar
  27. Guerra de Gusmão L (1998) Distribução geográfica de formigas cortadeiras do gênero Acromyrmex (Hymenoptera: Formicidae) na zona sul do estado do Rio Grande do Sul, Brasil., M.S. thesis Federal University of Pelotas. Pelotas, Rio Grande do Sul, BrazilGoogle Scholar
  28. Halley JD, Burd M, Wells P (2005) Excavation and architechture of Argentine ant nests. Insectes Soc 52:350–356CrossRefGoogle Scholar
  29. Hansell M (2005) Animal architecture. Oxford University Press, OxfordGoogle Scholar
  30. Harvey P, Pagel M (1991) The comparative method in evolutionary biology. Oxford Univ Press, LondonGoogle Scholar
  31. Hillel D (1998) Environmental soil physics. Academic Press, LondonGoogle Scholar
  32. Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 145:610–632CrossRefGoogle Scholar
  33. Kleineidam C, Rutchy M, Casero-Montes ZA, Roces F (2007) Thermal radiation as a learned orientation cue in leaf-cutting ants (Atta volenweideri). J Insect Physiol 53:478–487PubMedCrossRefGoogle Scholar
  34. Korzukhin MD, Porter SD, Thompson LC, Wiley S (2001) Modeling temperature-dependent range limits for the fire ant Solenopsis invicta (Hymenoptera: Formicidae) in the United States. Environ Entomol 30:645–655CrossRefGoogle Scholar
  35. Kusnezov N (1956) Claves para la identificación de las hormigas de la fauna argentina. Idia August–September:1–58Google Scholar
  36. Kusnezov N (1978) Hormigas argentinas–Clave para su identificación. Miscelánea 61, Ministerio de Cultura y Educación. Fundación Miguel Lillo, TucumánGoogle Scholar
  37. Lapointe SL, Serrano MS, Jones PG (1998) Microgeographic and vertical distribution of Acromyrmex landolti (Hymenoptera: Formicidae) nests in a neotropical savanna. Environ Entomol 27:636–641Google Scholar
  38. Link D, Link FM, Grigoletto PM, Goulart L (2001a) Aspectos morfológicos externos do ninho de Acromyrmex ambiguus em bosques de Eucalipto. In: Anais do XV Encontro de Miremecologia. Londrina, Parana, BrazilGoogle Scholar
  39. Link FM, Link D, Grigoletto PM, Goulart L (2001b) Aspectos morfológicos externos do ninho de Acromyrmex aspersus em bosques de Eucalipto. In: Anais do XV Encontro de Miremecologia. Londrina, Parana, BrazilGoogle Scholar
  40. Link FM, Link D, Grigoletto PM, Goulart L (2001c) Aspectos morfológicos externos do ninho de Acromyrmex crassispinus em bosques de Eucalipto. In: Anais do XV Encontro de Miremecologia. Londrina, Parana, BrazilGoogle Scholar
  41. Markin GP, O’Neal J, Dillier JH, Collins HL (1974) Regional variation in the seasonal activity of the imported fire ant, Solenopsis saevissima richteri. Environ Entomol 3:446–452Google Scholar
  42. Mayhé-Nunes AJ, Jaffé K (1998) On the biogeography of Attini (Hymenoptera:Formicidae). Ecotropicos 11:45–54Google Scholar
  43. Montenegro RA (1973) La fundación del hormiguero en Acromyrmex striatus (Rog.) (Hymenoptera, Formicidae). Stud Entomol 16:343–352Google Scholar
  44. Mueller UG, Schultz TR, Currie CR, Adams RMM, Malloch D (2001) The origin of the attine ant-fungus mutualism. Q Rev Biol 76:169–197PubMedCrossRefGoogle Scholar
  45. Navarro JG, Jaffé K (1985) On the adaptive value of nest features in the grass-cutting ant Acromyrmex landolti. Biotropica 17:347–348CrossRefGoogle Scholar
  46. Ortiz-Jaureguizar E, Cladera GA (2006) Paleoenvironmental evolution of southern South America during the Cenozoic. J Arid Environ 66:498–532CrossRefGoogle Scholar
  47. Passerat de Silans A, Moreira da Silva F, de Assis dos Reis Barbosa F (2006) Determinação in loco da difusividade térmica num solo da região de Caatinga (PB). R Bras Sci Solo 30:41–48Google Scholar
  48. Porter SD (1988) Impact of temperature on colony growth and developmental rates of the ant, Solenopsis invicta. J Insect Physiol 34:1127–1133CrossRefGoogle Scholar
  49. Porter SD, Tschinkel WR (1993) Fire ant thermal preferences: behavioral control of growth and metabolism. Behav Ecol Sociobiol 32:321–329CrossRefGoogle Scholar
  50. Powell RJ, Stradling DJ (1986) Factors influencing the growth of Attamyces bromatificus, a symbiont of attine ants. Trans Br Mycol Soc 87:205–213Google Scholar
  51. Quinlan RJ, Cherrett JM (1978) Aspects of the symbiosis of the leaf-cutting ant Acromyrmex octospinosus (Reich) and its food fungus. Ecol Entomol 3:221–230CrossRefGoogle Scholar
  52. Quinlan RJ, Cherrett JM (1979) The role of fungus in the diet of the leaf-cutting ant Atta cephalotes (L.). Ecol Entomol 4:151–160CrossRefGoogle Scholar
  53. Rasse P, Deneubourg JL (2001) Dynamics of nest excavation and nest size regulation of Lasius niger (Hymenoptera: Formicidae). J Insect Behav 14:433–449CrossRefGoogle Scholar
  54. Roces F, Kleineidam C (2000) Humidity preference for fungus culturing by workers of the leaf-cutting ant Atta sexdens rubropilosa. Insectes Soc 47:348–350CrossRefGoogle Scholar
  55. Roces F, Núñez JA (1989) Brood translocation and circadian variation of temperature preference in the ant Camponotus mus. Oecologia 81:33–37CrossRefGoogle Scholar
  56. Rosenberg NJ, Blad BL, Verma SB (1983) Microclimate—the biological environment. Wiley, New YorkGoogle Scholar
  57. Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. PNAS 105:5435–5440PubMedCrossRefGoogle Scholar
  58. Seeley TD, Heinrich B (1981) Regulation of temperature in the nest of social insects. In: Heinrich B (ed) Insect thermoregulation. Wiley, New York, pp 160–234Google Scholar
  59. Southerland MT (1988) The effects of temperature and food on the growth of laboratory colonies of Aphaenogaster rudis Emery (Hymenoptera: Formicidae). Insect Soc 35:304–309CrossRefGoogle Scholar
  60. Sudd JH (1982) Ants: foraging, nesting, brood behavior, and polyethism. In: Hermann HR (ed) Social insects, vol IV. Academic Press, New York, pp 107–155Google Scholar
  61. Sudd JH, Franks NR (1987) The behavioural ecology of ants. Blackie, GlasgowGoogle Scholar
  62. USDA (1975) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys. USDA-SCS. US Department of Agriculture handbook no. 436. US Government Printing OfficeGoogle Scholar
  63. USDA (2005) Global soil temperature regimes map. World soil resources soil survey division, NRCS-USDA, Washington, DC. http://soils.usda.gov/use/worldsoils/mapindex/str.html
  64. Van Wambeke A (1981) Calculated soil moisture and temperature regimes of South America. Techical monograph no. 2. USDA-SCS-SMSS, Washington DCGoogle Scholar
  65. Weber NA (1959) Isothermal conditions in tropical soil. Ecology 40:153–154CrossRefGoogle Scholar
  66. Weber NA (1972) Gardening ants—the Attines. The American Philosophical Society, PhiladelphiaGoogle Scholar
  67. Zolessi LC, Abenante YP (1973) Nidificación y mesoetología de Acromyrmex en el Uruguay. III. Acromyrmex (A.) hispidus Santschi, 1925 (Hymenoptera: Formicidae). Rev Biol Urug 1:151–165Google Scholar
  68. Zolessi LC, González LA (1974) Nidificación y mesoetología de Acromyrmex en el Uruguay. II. Acromyrmex (Acromyrmex) lobicornis (Emery 1887). (Hymenoptera: Formicidae). Rev Biol Urug 1:37–57Google Scholar
  69. Zolessi LC, González LA (1978) Observaciones sobre el género Acromyrmex en el Uruguay. IV. A. (Acromyrmex) lundi (Guérin, 1838) (Hymenoptera: Formicidae). Rev Fac Human Cienc (Cienc Biol) Montev 1:9–28Google Scholar
  70. Zolessi LC, Philippi ME (1998) Las hormigas cortadoras del Uruguay del género Acromyrmex (Hymenoptera: Formicidae). In: Berti Fillo E, Mariconi FAM, Fontes LR (eds) Formigas cortadeiras dos países do mercosul. FEALQ, Piracicaba, pp 93–98Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Martin Bollazzi
    • 1
  • Jenja Kronenbitter
    • 1
  • Flavio Roces
    • 1
  1. 1.Department of Behavioural Physiology and Sociobiology (Zoology II), BiocenterUniversity of WürzburgAm HublandGermany

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