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Acromyrmex fowleri: a new inquiline social parasite species of leaf-cutting ants from South America, with a discussion of social parasite biogeography in the Neotropical region

  • C. RabelingEmail author
  • S. Messer
  • S. Lacau
  • I. C. do Nascimento
  • M. BacciJr.
  • J. H. C. Delabie
Research Article

Abstract

Ant inquiline social parasites obligately depend on their hosts for survival and reproduction. Because of their shift from a eusocial to a socially parasitic life history, inquiline social parasites are interesting study systems for exploring the dynamics between conflict and cooperation in eusocial insect colonies. In addition, inquiline social parasites are of interest to evolutionary biology, because some species evolved directly from their hosts via sympatric speciation. With five described species, inquiline social parasites are relatively diverse in the fungus-growing ants. So far, four species have been reported from the leaf-cutting ant genus Acromyrmex and its closely affiliated social parasite genus Pseudoatta. In contrast, only a single parasite species was described from the lower attine genus Mycocepurus. Here, we describe a new species of inquiline social parasite, Acromyrmex fowleri sp. nov., which was discovered 27 years ago in the tropical region of Brazil (State of Bahia), living inside the colonies of its host Acromyrmex rugosus. We also report observations on the behavioral ecology and natural history of A. fowleri and its host. Our study suggests that A. fowleri is an obligate, queen-tolerant, workerless inquiline social parasite of A. rugosus and that A. fowleri represents some but not all morphological and life history characters of the inquiline syndrome, supporting the hypothesis that the complex traits of the inquiline syndrome evolve in a mosaic fashion. Considering that A. fowleri is a new social parasite species from tropical Brazil, we discuss the paradoxical biogeographic distribution of ant social parasites, which we refer to as the “Kutter–Wilson Paradox”, and conclude that the Kutter–Wilson Paradox is a genuine biogeographical pattern, instead of being a mere sampling artifact.

Keywords

Attini Biogeography Formicidae Fungus-growing ants Inquilinism Kutter–Wilson Paradox Latitudinal diversity gradient Myrmecosymbiosis Social parasitism 

Notes

Acknowledgements

We are especially grateful to Marcelo Schlindwein, Clayton and Simon R. Delabie, Gideval J. Carvalho (“Zom”), Peters Langlands, Meredith Cobb, and Katie Watkins for their help with collecting large quantities of alate ants along the beaches of Ilhéus on several occasions, generating the information about the nuptial flight activity of the social parasite and its host. We gratefully acknowledge the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), and the ICMBio for permission to conduct fieldwork in Brazil. We gratefully acknowledge financial support from the US National Science Foundation (NSF DEB-1456964 & DEB-1654829 to CR), FAPESP (2011/50226-0 and 2014/25507-3 to MB), and CNPq (309611/2015-6 and 409721/2016-6 to MB; 307128/2014-8 to JHCD).

References

  1. Adams RMM, Mueller UG, Holloway AK, Green AM, Narozniak J (2000) Garden sharing and garden stealing in fungus-growing ants. Naturwissenschaften 87:491–493CrossRefGoogle Scholar
  2. Autuori M (1942) Contribuicão para o conhecimento da saúva (Atta spp.—Hymenoptera Formicidae). III. Excavação de um saúveiro (Atta sexdens rubropilosa Forel 1908). Arquivos do Instituto Biológico 13:137–148Google Scholar
  3. Beibl J, Stuart RJ, Heinze J, Foitzik S (2005) Six origins of slavery in formicoxenine ants. Insectes Soc 52:291–297CrossRefGoogle Scholar
  4. Beibl J, Buschinger A, Foitzik S, Heinze J (2007) Phylogeny and phylogeography of the Mediterranean species of the parasitic ant genus Chalepoxenus and its Temnothorax hosts. Insectes Soc 54:189–199CrossRefGoogle Scholar
  5. Bekkevold D, Boomsma JJ (2000) Evolutionary transition to a semelparous life history in the socially parasitic ant Acromyrmex insinuator. J Evol Biol 13:615–623CrossRefGoogle Scholar
  6. Belt T (1874) The naturalist in Nicaragua. John Murray, LondonGoogle Scholar
  7. Borgmeier T (1959) Revision der Gattung Atta Fabricius (Hymenoptera, Formicidae). Stud Entomol 2:321–390Google Scholar
  8. Boudinot BE, Sumnicht TP, Adams RMM (2013) Central American ants of the genus Megalomyrmex Forel (Hymenoptera: Formicidae): six new species and keys to workers and males. Zootaxa 3732:1–82CrossRefGoogle Scholar
  9. Brandão CRF (1990) Systematic revision of the Neotropical ant genus Megalomyrmex Forel (Hymenoptera: Formicidae: Myrmicinae), with the description of thirteen new species. Arquivos de Zoologia 31:411–481CrossRefGoogle Scholar
  10. Brandão CRF (1991) Adendos ao catálogo abreviado das formigas da região Neotropical (Hymenoptera: Formicidae). Revista Brasileira de Entomologia 35:319–412Google Scholar
  11. Brandão CRF (2003) Further revisionary studies on the ant genus Megalomyrmex Forel (Hymenoptera: Formicidae: Myrmicinae: Solenopsidini). Papéis Avulsos de Zoologia 43:145–159CrossRefGoogle Scholar
  12. Bruch C (1928) Estudios mirmecológicos. Anales del Museo Nacionalde Historia Natural Buenos Aires 34:341–360Google Scholar
  13. Buschinger A (1986) Evolution of social parasitism in ants. Trends Ecol Evol 1:155–160CrossRefGoogle Scholar
  14. Buschinger A (1990) Sympatric speciation and radiative evolution of socially parasitic ants—heretic hypotheses and their factual background. Zeitschrift Zool Syst Evol 28:241–260CrossRefGoogle Scholar
  15. Buschinger A (2009) Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol News 12:219–235Google Scholar
  16. Cherrett JM (1986) History of leaf-cutting ant problems. In: Lofgren CS, Vander Meer RK (eds) Fire ants and leaf-cutting ants: biology and management. West View Press, Boulder, pp 10–17Google Scholar
  17. Craven SE, Dix MW, Michaels GE (1970) Attine fungus gardens contain yeasts. Science 169:184–186CrossRefGoogle Scholar
  18. Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704CrossRefGoogle Scholar
  19. De Fine Licht HH, Boomsma JJ, Tunlid A (2014) Symbiotic adaptations in the fungal cultivar of leaf-cutting ants. Nat Commun 5:5675CrossRefGoogle Scholar
  20. De Souza DJ, Soares IMF, Della Lucia TMC (2007) Acromyrmex ameliae sp. n. (Hymenoptera: Formicidae): a new social parasite of leaf-cutting ants in Brazil. Insect Sci 14:251–257CrossRefGoogle Scholar
  21. De Souza DJ, Ribeiro MMR, Mello A, Lino-Neto J, Dângelo RC, Della Lucia TMC (2011) A laboratory observation of nuptial flight and mating behaviour of the parasite ant Acromyrmex ameliae (Hymenoptera: Formicidae). Ital J Zool 78:405–408CrossRefGoogle Scholar
  22. Delabie JHC, Fowler HG, Schlindwein MN (1993) Ocorrência do parasita social Pseudoatta sp. nova em ninhos de Acromyrmex rugosus em Ilhéus, Bahia: primeiro registro para os trópicos. In: IV International Symposium on Pest Ants, XI Encontro de Mirmecologia, 21–24 November 1993, Belo Horizonte, BrazilGoogle Scholar
  23. Delabie JHC, do Nascimento IC, Mariano CSF (2002) Estratégias de reprodução e dispersão em formigas attines, com exemplos do sul da Bahia. In: XIX Congresso Brasileiro de Entomologia, 16–21 June 2002, Manaus, BrazilGoogle Scholar
  24. Delabie JHC, Alves HSR, Reuss-Strenzel GM, do Carmo AFR, Nascimento IC (2011) Distribuição das formigas-cortadeiras Acromyrmex e Atta no Novo Mundo. In: Della Lucia TMC (ed) Formigas-Cortadeiras: da bioecologia ao manejo. Editora da UFV, Viçosa, pp 80–101Google Scholar
  25. Della Lucia TMC (2011) Formigas-Cortadeiras: da bioecologia ao manejo. Editora da UFV, ViçosaGoogle Scholar
  26. Dijkstra MB, Boomsma JJ (2003) Gnamptogenys hartmani Wheeler (Ponerinae: Ectatommini): an agro-predator of Trachymyrmex and Sericomyrmex fungus-growing ants. Naturwissenschaften 90:568–571CrossRefGoogle Scholar
  27. Economo EP, Narula N, Friedman NR, Weiser MD, Guénard B (2018) Macroecology and macroevolution of the latitudinal diversity gradient in ants. Nat Commun 9:1778CrossRefGoogle Scholar
  28. Emery C (1909) Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen. Biol Centralblatt 29:352–362Google Scholar
  29. Farji Brener AG, Ruggiero A (1994) Leaf-cutting ants (Atta and Acromyrmex) inhabiting Argentina: patterns in species richness and geographical range sizes. J Biogeogr 21:391–399CrossRefGoogle Scholar
  30. Feitosa RM, Hora RR, Delabie JHC, Valenzuela J, Fresneau D (2008) A new social parasite in the ant genus Ectatomma F. Smith (Hymenoptera, Formicidae, Ectatomminae). Zootaxa 1713:47–52Google Scholar
  31. Fernández F, Sendoya S (2004) Synonymic list of Neotropical ants (Hymenoptera: Formicidae). Biota Colomb 5:3–105Google Scholar
  32. Fernández F, Castro-Huertas V, Serna F (2015) Hormigas cortadoras de hojas de Colombia: Acromyrmex y Atta (Hymenoptera: Formicidae). Fauna de Colomb 5:1–350Google Scholar
  33. Forti LC, de Andrade ML, Andrade APP, Lopes JFS, Ramos VM (2006) Bionomics and identification of Acromyrmex (Hymenoptera: Formicidae) through an illustrated key. Sociobiology 48:135–153Google Scholar
  34. Forti LC, Moreira AA, Andrade APP, Castellani MA, Caldato N (2011) Nidificação e arquitetura de ninhos de formigas-cortadereiras. In: Della Lucia TMC (ed) Formigas-Cortadeiras: da bioecologia ao manejo. Editora da UFV, Viçosa, pp 102–125Google Scholar
  35. Fowler HG (1983) Latitudinal gradients and diversity of the leaf-cutting ants (Atta and Acromyrmex) (Hymenoptera: Formicidae). Rev Biol Trop 31:213–216Google Scholar
  36. Fowler HG (1985) Leaf-cutting ants of the genera Atta and Acromyrmex of Paraguay (Hymenoptera, Formicidae). Deutsche Entomol Zeitschrift 32:19–34CrossRefGoogle Scholar
  37. Fowler HG (1988) Taxa of the Neotropical grass-cutting ants, Acromyrmex (Moellerius) (Hymenoptera: Formicidae: Attini). Científica 16:281–295Google Scholar
  38. Fowler HG, Forti LC, Pereira da Silva V, Saes NB (1986) Economics of grass-cutting ants. In: Lofgren CS, Vander Meer RK (eds) Fire ants and leaf-cutting ants: biology and management. West View Press, Boulder, pp 18–35Google Scholar
  39. Fowler HG, Pagani M, Silva O, Forti L, Pereira-da-Silva V, Vasconcelos H (1989) A pest is a pest is a pest? The dilemma of Neotropical leaf-cutting ants: keystone taxa of natural ecosystems. Environ Manag 13:671–765CrossRefGoogle Scholar
  40. Gallardo A (1916) Notes systématiques et éthologiques sur les fourmis Attines de la République Argentine. Anales del Museo Nacional de Historia Natural de Buenos Aires 28:317–344Google Scholar
  41. Gallardo A (1929) Note sur les mœurs de la fourmi Pseudoatta argentina. Rev Soc Entomol Argentina 2:197–202Google Scholar
  42. Gonçalves CR (1961) O género Acromyrmex no Brasil (Hym. Formicidae). Stud Entomol 4:113–180Google Scholar
  43. Gray KW, Cover SP, Johnson RA, Rabeling C (2018) The dacetine ant Strumigenys arizonica, an apparent obligate commensal of the fungus-growing ant Trachymyrmex arizonensis in southwestern North America. Insectes Soc 65:401–410CrossRefGoogle Scholar
  44. Guerrero RJ, Delabie JHC, Dejean A (2010) Taxonomic contribution to the aurita group of the ant genus Azteca (Formicidae: Dolichoderinae). J Hymenopt Res 19:51–65Google Scholar
  45. Hasegawa E, Tinaut A, Ruano F (2002) Molecular phylogeny of two slave-making ants: Rossomyrmex and Polyergus (Hymenoptera: Formicidae). Ann Zool Fenn 39:267–271Google Scholar
  46. Heinze J, Buschinger A, Poettinger T, Suefuji M (2015) Multiple convergent origins of workerlessness and inbreeding in the socially parasitic ant genus Myrmoxenus. PLoS One 10(7):e0131023.  https://doi.org/10.1371/journal.pone.0131023 CrossRefGoogle Scholar
  47. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, CambridgeCrossRefGoogle Scholar
  48. Hölldobler B, Wilson EO (2011) The leafcutter ants: civilization by instinct. W.W. Norton & Company, New YorkGoogle Scholar
  49. Janda M, Folková D, Zrzavý J (2004) Phylogeny of Lasius ants based on mitochondrial DNA and morphology, and the evolution of social parasitism in the Lasiini (Hymenoptera: Formicidae). Mol Phylogenet Evol 33:595–614CrossRefGoogle Scholar
  50. Jansen G, Savolainen R, Vepsäläinen K (2010) Phylogeny, divergence-time estimation, biogeography and social parasite-host relationships of the Holarctic ant genus Myrmica (Hymenoptera: Formicidae). Mol Phylogenet Evol 56:294–304CrossRefGoogle Scholar
  51. Jonkman JCM (1980) The external and internal structure and growth of nests of the leaf-cutting ant Atta vollenweideri Forel, 1983 (Hym: Formicidae). J Appl Entomol 89:217–246Google Scholar
  52. Kempf WW (1972) Catálogo abreviado das formigas da região Neotropical. Stud Entomol 15:3–344Google Scholar
  53. Kronauer DJC, Gadau J, Hölldobler B (2003) Genetic evidence for intra- and inter-specific slavery in honey ants (genus Myrmecocystus). Proc R Soc Lond B 270:805–810CrossRefGoogle Scholar
  54. Kutter H (1968) Die sozialparasitischen Ameisen der Schweiz. Neujahrsblatt der Naturforschenden Gesellschaft in Zürich 171:1–62Google Scholar
  55. Le Masne G (1956) Recherches sur les fourmis parasites. Plagiolepis grassei et l’évolution des Plagiolepis parasites. Comptes Rendus del’Académie des Sciences 243:673–675Google Scholar
  56. Leppänen J, Seppä P, Vepsäläinen K, Savolainen R (2015) Genetic divergence between the sympatric queen morphs of the ant Myrmica rubra. Mol Ecol 24:2463–2476CrossRefGoogle Scholar
  57. Li H, Sosa-Calvo J, Horn HA, Pupo MT, Clardy J, Rabeling C, Schultz TR, Currie CR (2018) Convergent evolution of complex structures for ant-bacterial defensive symbiosis in fungus-farming ants. Proc Natl Acad Sci USA 115:10720–10725CrossRefGoogle Scholar
  58. Little AEF, Currie CR (2007) Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis. Biol Let 3:501–504CrossRefGoogle Scholar
  59. Lofgren CS, Vander Meer RK (1986) Fire ants and leaf-cutting ants: biology and management. West View Press, Boulder COGoogle Scholar
  60. Longino JT (2003) The Crematogaster (Hymenoptera, Formicidae, Myrmicinae) of Costa Rica. Zootaxa 151:1–150CrossRefGoogle Scholar
  61. Longino JT (2006) A taxonomic review of the genus Myrmelachista (Hymenoptera: Formicidae) in Costa Rica. Zootaxa 1141:1–54Google Scholar
  62. Longino JT (2007) A taxonomic review of the genus Azteca (Hymenoptera: Formicidae) in Costa Rica and a global revision of the aurita group. Zootaxa 1491:1–63Google Scholar
  63. Longino JT (2010) A taxonomic review of the ant genus Megalomyrmex Forel (Hymenoptera: Formicidae) in Central America. Zootaxa 2720:35–58CrossRefGoogle Scholar
  64. Maruyama M, Steiner FM, Stauffer C, Akino T, Crozier RH, Schlick-Steiner BC (2008) A DNA and morphology based phylogenetic framework of the ant genus Lasius with hypotheses for the evolution of social parasitism and fungiculture. BMC Evol Biol 8:237CrossRefGoogle Scholar
  65. Mehdiabadi NJ, Schultz TR (2010) Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini). Myrmecol News 13:37–55Google Scholar
  66. Menzel F, Blüthgen N (2010) Parabiotic associations between tropical ants: equal partnership or parasitic exploitation? J Anim Ecol 79:71–81CrossRefGoogle Scholar
  67. Moreira AA, Forti LC, Andrade APP, Boaretto MAC, Lopes JFS (2004) Nest architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud Neotropical Fauna Environ 39:109–116CrossRefGoogle Scholar
  68. Moser J (1963) Contents and structure of Atta texana nest in summer. Ann Entomol Soc Am 56:286–291CrossRefGoogle Scholar
  69. Mueller UG (2002) Ant versus fungus versus mutualism: ant-cultivar conflict and the deconstruction of the Attini ant-fungus symbiosis. Am Nat 160:67–98Google Scholar
  70. Mueller UG, Rabeling C (2008) A breakthrough innovation in animal evolution. Proc Natl Acad Sci USA 105:5287–5288CrossRefGoogle Scholar
  71. Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol Syst 36:563–595CrossRefGoogle Scholar
  72. Mueller UG, Ishak HD, Bruschi SM, Smith CC, Herman JJ, Solomon SE, Mikheyev AS, Rabeling C, Scott JJ, Cooper M, Rodrigues A, Ortiz A, Brandão CRF, Lattke JE, Pagnocca FC, Rehner SA, Schultz TR, Vasconcelos HL, Adams RMM, Bollazzi M, Clark RM, Himler AG, LaPolla JS, Leal IR, Johnson RA, Roces F, Sosa-Calvo J, Wirth W, Bacci M Jr (2017) Biogeography of mutualistic fungi cultivated by Leafcutter ants. Mol Ecol 26:6921–6937CrossRefGoogle Scholar
  73. Müller F (1874) The habits of various insects. Nature 10:102–103CrossRefGoogle Scholar
  74. Nygaard S, Hu H, Li C, Schiøtt M, Chen Z, Yang Z, Xie Q, Ma C, Deng Y, Dikow RB, Rabeling C, Nash DR, Wcislo WT, Brady SG, Schultz TR, Zhang G, Boomsma JJ (2016) Reciprocal genomic evolution in the ant-fungus agricultural symbiosis. Nat Commun 7:12233CrossRefGoogle Scholar
  75. Powell S, Clark E (2004) Combat between large derived societies: a subterranean army ant established as a predator of mature leaf-cutting ant colonies. Insectes Soc 51:342–351CrossRefGoogle Scholar
  76. Prebus M (2017) Insights into the evolution, biogeography and natural history of the acorn ants, genus Temnothorax Mayr (Hymenoptera: Formicidae). BMC Evol Biol 17:250CrossRefGoogle Scholar
  77. Prebus M, Lubertazzi D (2016) A new species of the ant genus Bothriomyrmex Emery, 1869 (Hymenoptera: Formicidae) from the Caribbean region. Eur J Taxon 211:1–12Google Scholar
  78. Rabeling C, Bacci M (2010) A new workerless inquiline in the Lower Attini (Hymenoptera: Formicidae), with a discussion of social parasitism in fungus-growing ants. Syst Entomol 35:379–392CrossRefGoogle Scholar
  79. Rabeling C, Cover SP, Johnson RA, Mueller UG (2007) A review of the North American species of the fungus-gardening ant genus Trachymyrmex (Hymenoptera: Formicidae). Zootaxa 1664:1–53Google Scholar
  80. Rabeling C, Schultz TR, Pierce NE, Bacci M Jr (2014) A social parasite evolved reproductive isolation from its fungus-growing ant host in sympatry. Curr Biol 24:2047–2052CrossRefGoogle Scholar
  81. Rabeling C, Schultz TR, Bacci M, Bollazzi M (2015) Acromyrmex charruanus: a new inquiline social parasite species of leaf-cutting ants. Insectes Soc 62:335–349CrossRefGoogle Scholar
  82. Savolainen R, Vepsäläinen K (2003) Sympatric speciation through intraspecific social parasitism. Proc Natl Acad Sci USA 100:7169–7174CrossRefGoogle Scholar
  83. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, PrincetonGoogle Scholar
  84. Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci USA 105:5435–5440CrossRefGoogle Scholar
  85. Schultz TR, Bekkevold D, Boomsma JJ (1998) Acromyrmex insinuator new species: an incipient social parasite of fungus-growing ants. Insectes Soc 45:457–471CrossRefGoogle Scholar
  86. Schultz TR, Mueller UG, Currie CR, Rehner SA (2005) Reciprocal illumination: a comparison of agriculture in humans and ants. In: Vega F, Blackwell M (eds) Ecological and evolutionary advances in insect-fungal associations. Oxford University Press, New York, pp 149–190Google Scholar
  87. Soares IMF, Della Lucia TMC, dos Santos AA, do Nascimento IC, Delabie JHC (2006) Caracterização de ninhos e tamanho de colônia de Acromyrmex rugosus (F. Smith) (Hymenoptera, Formicidae, Attini) em restingas de Ilhéus, BA, Brasil. Rev Bras Entomol 50:128–130CrossRefGoogle Scholar
  88. Soares IMF, Della Lucia TMC, Alice S, Pereira JES, Ribiero MMR, De Souza DJ (2010) Comparative reproductive biology of the social parasite Acromyrmex ameliae de Souza, Soares & Della Lucia and of its host Acromyrmex subterraneus subterraneus Forel (Hymenoptera: Formicidae). Neotropical Entomol 39:714–719CrossRefGoogle Scholar
  89. Soares IMF, Della Lucia TMC, De Souza D (2011) Parasitismo social em formigas-cortadeiras. In: Della Lucia TMC (ed) Formigas-Cortadeiras: da bioecologia ao manejo. Editora da UFV, Viçosa, pp 344–358Google Scholar
  90. Solomon SE, Rabeling C, Sosa-Calvo J, Lopes CT, Rodrigues A, Vasconcelos HL, Bacci Jr. M, Mueller UG, Schultz TR (2019) The molecular phylogenetics of Trachymyrmex ants and their fungal cultivars provide insights into the origin and co-evolutionary history of “higher-attine” ant agriculture. Syst Entomol.  https://doi.org/10.1111/syen.12370 Google Scholar
  91. Sosa-Calvo J, Schultz TR, Ješovnik A, Dahan RA, Rabeling C (2018) Evolution, systematics, and natural history of a new genus of cryptobiotic fungus-growing ants. Syst Entomol 43:549–567CrossRefGoogle Scholar
  92. Sumner S, Aanen DK, Delabie J, Boomsma JJ (2004) The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery’s rule. Insectes Soc 51:37–42CrossRefGoogle Scholar
  93. Verza SS, Forti LC, Lopes JFS, Hughes WHO (2007) Nest architecture of the leaf-cutting ant Acromyrmex rugosus rugosus. Insectes Soc 54:303–309CrossRefGoogle Scholar
  94. Verza SS, Mussury RM, Camargo RS, Andrade APP, Forti LC (2017) Oviposition, life cycle, and longevity of the leaf-cutting ant Acromyrmex rugosus rugosus. Insects 8:80CrossRefGoogle Scholar
  95. Ward PS, Brady SG, Fisher BL, Schultz TR (2015) The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae). Syst Entomol 40:61–81CrossRefGoogle Scholar
  96. Wasmann E (1891) Die zusammengesetzten Nester und gemischten Kolonien der Ameisen. Ein Beitrag zur Biologie, Psychologie und Entwicklungsgeschichte der Ameisengesellschaften. Aschendorffsche Buchdruckerei, Münster i. W., GermanyGoogle Scholar
  97. Wasmann E (1915) Das Gesellschaftsleben der Ameisen. Das Zusammenleben von Ameisen verschiedener Arten und von Ameisen und Termiten. Aschendorffsche Buchdruckerei, Münster i. W., GermanyGoogle Scholar
  98. Wcislo WT (1981) The roles of seasonality, host synchrony, and behavior in the evolutions and distributions of nest parasites in Hymenoptera (Insecta), with special reference to bees (Apoidea). Biol Rev 62:515–542CrossRefGoogle Scholar
  99. Wheeler WM (1910) Ants: their structure, development and behavior. Columbia University Press, New YorkGoogle Scholar
  100. Wheeler WM (1919) The parasitic Aculeata, a study in evolution. Proc Am Philos Soc 58:1–40Google Scholar
  101. Wheeler WM (1925) A new guest-ant and other new Formicidae from Barro Colorado Island, Panama. Biol Bull 49:150–181CrossRefGoogle Scholar
  102. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  103. Wilson EO (1984) Tropical social parasites in the ant genus Pheidole, with an analysis of the anatomical parasitic syndrome (Hymenoptera: Formicidae). Insectes Soc 31:316–334CrossRefGoogle Scholar
  104. Wirth R, Beyschlag W, Herz H, Ryel RJ, Hölldobler B (2003) Herbivory of leaf-cutter ants: a case study of Atta colombica in the tropical rainforest of Panama. Ecological Studies, vol 164. Springer, BerlinCrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2019

Authors and Affiliations

  1. 1.School of Life SciencesArizona State UniversityTempeUSA
  2. 2.Laboratório de Biosistemática AnimalUniversidade Estadual do Sudoeste da BahiaItapetingaBrazil
  3. 3.Departamento de Ciências BiológicasUniversidade Estadual do Sudoeste da Bahia, Campus de JequiéJequiéBrazil
  4. 4.Instituto de Biociências de Rio ClaroUniversidade Estadual Paulista (UNESP)Rio ClaroBrazil
  5. 5.Departamento de Ciências Agrárias e AmbientaisUniversidade Estadual de Santa Cruz, UESCIlhéusBrazil
  6. 6.Laboratório de MirmecologiaCEPLAC/CEPEC/SEFITItabunaBrazil

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