Establishing an ant-plant mutualism: foundress queen mortality and acquiring the third partner

Abstract

In the Neotropics, colonies of the ant Pseudomyrmex dendroicus are found in the hollow stems of Triplaris americana. The ants are obligate inhabitants of the ant-plant and they nest and reproduce exclusively in this myrmecophyte. However, this mutualistic association often involves a third partner, scale insects (Coccoidea, Hemiptera). Established colonies of this ant are always associated with scale insects and ants appear to be dependent on the honeydew excretions of their trophobionts. Acquisition of scale insects is therefore an important step in the successful establishment of a new colony. Domatia of juvenile host-plants were dissected to determine (1) how colonies are founded, (2) if there was evidence of co-dispersal between trophobionts and foundress queens. Colony foundation is claustral. Founding queens of Pseudomyrmex chew their entrance holes at the prostoma and then close the hole with debris. 104 queens were located with few or no workers. Of the 104 foundresses, 69 were found dead and only 32 had at least a single trophobiont. Although the association with trophobionts may prove vital to the establishment of the colony, these results indicate that scale insects do not seem to co-disperse with the foundress queens.

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References

  1. Agrawal AA (1998) Leaf damage and associated cues induced aggressive ant recruitment in a neotropical ant-plant. Ecology 79:2100–2112

    Article  Google Scholar 

  2. Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, Cambridge

    Google Scholar 

  3. Blatrix R, Djiéto-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 Biol Sci 279:3940–3947

    PubMed  PubMed Central  Article  Google Scholar 

  4. Benson WW (1985) Amazon ant-plants. In: Prance GT, Lovejoy TE (eds) Amazonia. Pergamon Press, Oxford, pp 239–266

  5. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton

    Google Scholar 

  6. Brandbyge J (1986) A revision of the genus Triplaris (Polygonaceae). Nord J Bot 6:545–570

    Article  Google Scholar 

  7. Brandbyge J (1990) Woody Polygonaceae from Brazil: new species and a new interpretation. Nord J Bot 10:155–160

    Article  Google Scholar 

  8. Brouat C, Gielly L, McKey D (2001) Phylogenetic relationships in the genus Leonardoxa (Leguminosae: Caesalpinioideae) inferred from chloroplast trnL Intron and trnL trn-F intergenic spacer sequences. Am J Bot 88:143–149

    PubMed  CAS  Article  Google Scholar 

  9. Chomicki G, Renner SS (2015) Phylogenetics and molecular clocks reveal the repeated evolution of ant-plants after the late Miocene in Africa and the early Miocene in Australasia and the Neotropics. New Phytol 207:411–424

    PubMed  Article  Google Scholar 

  10. Dáttilo WFC, Izzo TJ, Inouye BD, Vasconcelos HL, Bruna EM (2009) Recognition of host plant volatiles by Pheidole minutula Mayr (Myrmecinae), an Amazonian ant-plant specialist. Biotropica 41:642–646

    Article  Google Scholar 

  11. Davidson DW, McKey D (1993) The evolutionary ecology of symbiotic ant-plant relationships. J Hymenop Res 2:13–83

    Google Scholar 

  12. Davidson DW, Longino JT, Snelling RR (1988) Pruning of host plant neighbors by ants: an experimental approach. Ecology 69:801–808

    Article  Google Scholar 

  13. Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972

    PubMed  CAS  Article  Google Scholar 

  14. Edwards DP, Hassall M, Sutherland WJ, Yu DW (2006) Assembling a mutualism: ant symbionts locate their host plants by detecting volatile chemicals. Insect Soc 53:172–176

    Article  Google Scholar 

  15. Federle W, Maschwitz U, Fiala B (1998) The two-partner ant-plant system of Camponotus (Colobopsis) sp. 1 and Macaranga puncticulata (Formicidae: Formicinae; Euphorbiaceae): myrmecophytic traits of the partner ant. Insect Soc 45:1–16

    Article  Google Scholar 

  16. Fiala B, Maschwitz U (1990) Studies on the South East Asian ant-plant association Crematogaster borneensis/Macaranga: adaptations of the ant partner. Insect Soc 37:212–231

    Article  Google Scholar 

  17. Fonseca CR (1999) Amazonian ant-plant interactions and the nesting space limitation hypothesis. J Trop Ecol 15:807–825

    Article  Google Scholar 

  18. Frederickson ME (2005) Ant species confer different partner benefits on two neotropical myrmecophytes. Oecologia 143:387–395

    PubMed  Article  Google Scholar 

  19. Frederickson ME (2006) The reproductive phenology of an Amazonian ant species reflects the seasonal availability of its nest sites. Oecologia 149:418–427

    PubMed  Article  Google Scholar 

  20. Gaume L, Matile-Ferrero D, McKey D (2000) Colony foundation and acquisition of coccoid trophobionts by Aphomomyrmex afer (Formicinae): co-dispersal of queens and phoretic mealybugs in an ant-plant-homopteran mutualism? Insect Soc 47:84–91

    Article  Google Scholar 

  21. Grangier J, Dejean A, Malé PJG, Solano PJ, Orivel J (2009) Mechanisms driving the specificity of a myrmecophyte-ant association. Biol J Linn Soc 97:90–97

    Article  Google Scholar 

  22. Gullan PJ, Kosztarab M (1997) Adaptations in scale insects. Ann Rev Entomol 42:23–50

    CAS  Article  Google Scholar 

  23. Handa C, Ueda S, Tanaka H, Itino T, Itioka T (2012) How do scale insects settle into the nests of plant-ants on Macaranga myrmecophytes? Dispersal by wind and selection by plant-ants. Sociobiology 59:435–446

    Google Scholar 

  24. Inui Y, Itioka T, Murase K, Yamaoka R, Itino T (2001) Chemical recognition of partner plant species by foundress ant queens in Macaranga-Crematogaster myrmecophytism. J Chem Ecol 27:2029–2040

    PubMed  CAS  Article  Google Scholar 

  25. Janzen DH (1966) Coevolution of mututalism between ants and acacias in Central America. Evolution 20:249–275

    Article  Google Scholar 

  26. Janzen DH (1972) Protection of Barteria (Passifloraceae) by Pachysma ants (Pseudomyrmecinae) in a Nigerian rain forest. Ecology 53:885–892

    Article  Google Scholar 

  27. Jürgens A, Feldhaar H, Feldmeyer B, Fiala B (2006) Chemical composition of leaf volatiles in Macaranga species (Euphorbiaceae) and their potential role as olfactory cues in host-localization of foundress queens of specific ant partners. Biochem Syst Ecol 34:97–113

    Article  Google Scholar 

  28. Kaspari M, O’Donnell S, Kercher JR (2000) Energy, density, and constraints to species richness: ant assemblages along a productivity gradient. Am Nat 155:280–293

    PubMed  Article  Google Scholar 

  29. Keller L, Passera L (1989) Size and fat content of gynes in relation to the mode of colony founding in ants (Hymenoptera; Formicidae). Oecologia 80:236–240

    Article  Google Scholar 

  30. Klein RW, Kovac D, Schellerich A, Maschwitz U (1992) Mealybug-carrying by swarming queens of a Southeast Asian bamboo inhabiting ant. Naturwissenschaften 79:422–423

    Article  Google Scholar 

  31. Larrea-Alcázar DM, Simonetti JA (2007) Why are there few seedlings beneath the myrmecophyte Triplaris americana? Acta Oecol 32:112–118

    Article  Google Scholar 

  32. Longino JT (1989) Geographic variation and community structure in an ant-plant mutualism: Azteca and Cecropia in Costa Rica. Biotropica 21:126–132

    Article  Google Scholar 

  33. Maschwitz U, Fiala B, Moog J, Shaw LG (1991) Two new myrmecophyte associations from the Malay Peninsula: ants of the genus Cladomyrma (Formicidae, Camponotinae) as partners of Saraca thaipigensis (Caesalpiniaceae) and Crypteronia griffithii (Crypteroniaceae). 1. Colony foundation and acquisition of trophobionts. Insect Soc 38:27–35

    Article  Google Scholar 

  34. Michelangeli FA (2003) Ant protection against herbivory in three species of Tococa (Melastomataceae) occupying different environments. Biotropica 35:181–188

    Article  Google Scholar 

  35. Moog J, Saw LG, Hashim R, Maschwitz U (2005) The triple alliance: how a plant-ant, living in an ant-plant, acquires the third partner, a scale insect. Insect Soc 52:169–176

    Article  Google Scholar 

  36. Nishi AH, Romero GQ (2008) Colonization pattern of Cecropia by Azteca ants: influence of plant ontogeny, environment and host plant choice by queens. Sociobiology 52:367–376

    Google Scholar 

  37. Oliveira PS, Oliveira Filho AT, Cintra R (1987) Ant foraging on ant-inhabited Triplaris (Polygonaceae) in Western Brazil a field experiment using live termite baits. J Trop Ecol 3:193–200

    Article  Google Scholar 

  38. Philpott SM, Foster PF (2005) Nest-site limitation in coffee agroecosystems: artificial nests maintain diversity of arboreal ants. Ecol Appl 15:1478–1485

    Article  Google Scholar 

  39. Pitman NCA, Terborgh J, Silman MR, Nuñez P (1999) Tree species distribution in an upper Amazonian forest. Ecology 80:2651–2661

    Article  Google Scholar 

  40. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. University of Chicago Press, Chicago, pp 1–346

    Google Scholar 

  41. Sanchez A (2015) Fidelity and promiscuity in an ant-plant mutualism: a case study of Triplaris and Pseudomyrmex. PLoS One 10:e0143535

  42. Sanchez A, Bellota E (2015) Protection against herbivory in the mutualism between Pseudomyrmex dendroicus (Formicidae) and Triplaris americana (Polygonaceae). J Hymenopt Res 46:71–83

  43. Schremmer F (1984) Untersuchungen und Beobachtungen zur Ökoethologie der Pflanzenameise Pseudomyrmex triplarinus, welche die Ameisenbäume der Gattung Triplaris bewohnt. Zool Jahrb Abt Anat Ontog Tiere 111:385–410

    Google Scholar 

  44. Valverde JP, Hansen P (2011) Parenchyma: a neglected plant tissue in the Cecropia/ant mutualism. Symbiosis 55:47–51

    Article  Google Scholar 

  45. Vasconcelos HL (1991) Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome, and one of its inhabit-ants: ant protection against insect herbivores. Oecologia 87:295–298

    Article  Google Scholar 

  46. Ward PS (1991) Phylogenetic analysis of Pseudomyrmecine ants associated with domatia-bearing plants. In: Huxley CR, Cutler DF (eds) Ant-plant interactions. Oxford University Press, Oxford, pp 335–352

    Google Scholar 

  47. Ward PS (1999) Systematics, biogeography and host plant associations of the Pseudomyrmex viduus group (Hymenoptera: Formicidae), Triplaris- and Tachigali-inhabiting ants. Zool J Linn Soc 126:451–540

    Article  Google Scholar 

  48. Ward PS, Downie DA (2005) The ant subfamily Pseudomyrmecinae (Hymenoptera: Formicidae): phylogeny and evolution of big-eyed arboreal ants. Syst Entomol 30:310–335

    Article  Google Scholar 

  49. Weir TL, Newbold S, Vivanco JM, van Haren M, Fritchman C, Dossey AT, Bartram S, Boland W, Cosio EG, Kofer W (2012) Plant-inhabiting ant utilizes chemical cues for host discrimination. Biotropica 44:246–253

    Article  Google Scholar 

  50. Wheeler WM (1942) Studies of neotropical ant-plants and their ants. Bull Mus Comp Zool 90:41–65

    Google Scholar 

  51. Williams DJ (1998) Mealybugs of the genera Eumyrmococcus Silvestri and Xenococcus Silvestri associated with the ant genus Acropyga Roger and a review of the subfamily Rhizoecinae (Hemiptera, Coccoidea, Pseudococcidae). Bull Nat Hist Mus London 67:1–64

    Google Scholar 

  52. Yu DW, Davidson DW (1997) Experimental studies of species-specificity in Cecropia-ant relationships. Ecol Monogr 67:273–294

    Google Scholar 

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Acknowledgments

Funding for this study was provided by a grant from the Amazon Conservation Association. I am thankful to all the staff and people at Los Amigos, especially Nigel Pitman. I would also like to thank INRENA-Ministerio de Agricultura in Perú for providing the permits necessary for carrying out the experiments in Madre de Dios. Edwin Bellota provided invaluable assistance in the field.

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Sanchez, A. Establishing an ant-plant mutualism: foundress queen mortality and acquiring the third partner. Insect. Soc. 63, 155–162 (2016). https://doi.org/10.1007/s00040-015-0450-2

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Keywords

  • Ant-plant interaction
  • Hemipterans
  • Mutualism
  • Pseudomyrmex
  • Triplaris