Skip to main content
Log in

Plant Volatiles Influence the African Weaver Ant-Cashew Tree Mutualism

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Plant volatiles influence virtually all forms of ant-plant symbioses. However, little is known about their role in the mutualistic relationship between the African weaver ant and the cashew tree. In this study, we tested the hypothesis that cashew tree volatiles from plant parts most vulnerable to herbivory viz. inflorescence, leaves, and fruits, are attractive to weaver ants. Using behavioral assays, we show that these volatiles attract weaver ants but without significant difference in preference for any of the odors. These same plant parts are associated with extra floral nectaries (EFNs’) and therefore we evaluated the possibility that the ants associate the volatiles with food rewards. We found that perception of the odors was followed by a searching response that led the ants to non-volatile sugar rewards. More importantly, we observed that weaver ants spent significantly more time around the odor when it was paired to a reward. Chemical analysis of volatiles showed that the plant parts shared similarities in chemical composition, dominated by monoterpenes and sesquiterpenes. Additionally, we evaluated the attractiveness of a synthetic blend of three ocimene isomers ((E)-β-ocimene, (Z)-β-ocimene and allo-ocimene) identified in cashew leaf odor and shown to constitute a candidate kairomone for the cashew pest Pseudotheraptus wayi. We found that the attractiveness of the blend was dose dependent, and the response of the ants was not significantly different to that established with the crude volatiles from plant tissues. These results present new and interesting possibilities for improving weaver ant performance in cashew pest management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adams2 terpenoid/natural product library, Adams RP (1995) Identification of essential oil components by gas chromotography/mass spectrometry, Allured, Carol Stream

  • Agrawal AA, Dubin-Thaler BJ (1999) Induced responses to herbivory in the neotropical ant-plant association between Azteca ants and Cecropia trees: response of ants to potential inducing cues. Behav Ecol Sociobiol 45:47–54

    Article  Google Scholar 

  • Aldrich JR (1988) Chemical ecology of Heteroptera. Annu Rev Entomol 33:211–238

    Article  Google Scholar 

  • Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta 1734:91–111

    Article  CAS  PubMed  Google Scholar 

  • Ayenor GK, Huis AV, Obeng-Ofori D, Padi B, Röling NG (2007) Facilitating the use of alternative capsid control methods towards sustainable production of organic cocoa in Ghana. Int J Trop Insect Sci 27:85–94

    Article  Google Scholar 

  • Bell WJ (1990) Searching behaviour patterns in insects. Annu Rev Entomol 35:447–467

    Article  Google Scholar 

  • Beugnon G, Déjean A (1992) Adapative properties of chemical trail system of the African weaver ant oecophylla longinoda Latreille (Hymenoptera, Formicidae, Forminicae). Ins Soc 39:341–346

    Article  Google Scholar 

  • Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees Apis mellifera. J Comp Physiol 97:107–119

    CAS  Google Scholar 

  • Boucher D, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13:315–347

    Article  Google Scholar 

  • Brown ES (1955) Pseudotheraptus wayi, a new genus and species of Coreid (Hemiptera) injurious to coconuts in East Africa. Bull Entomol Res 46:221–240

    Article  Google Scholar 

  • Bruna EM, Lapola DM, Vasconcelos HL (2004) Interspecific variation in the defensive responses of obligate plant-ants: experimental tests and consequences for herbivory. Oecologia 138:558–565

    Article  PubMed  Google Scholar 

  • Bruna EM, Darrigo MR, Pacheco AMF, Vasconcelos HL (2008) Interspecific variation in the defensive responses of ant mutualists to plant volatiles. Biol J Linn Soc 94:241–249

    Article  Google Scholar 

  • Cheng A, Lou Y, Mao Y, Lu S, Wang L, Chen X (2007) Plant terpenoids: Biosynthesis and ecological functions. J Integr Plant Biol 49:179–186

    Article  CAS  Google Scholar 

  • Crozier RH, Newey PS, Schlüns EA, Robson SKA (2010) A masterpiece of evolution – Oecophylla weaver ants (Hymenoptera : Formicidae). Myrmecol News 13:57–71

    Google Scholar 

  • Dáttilo WFC, Izzo TJ, Inouye BD, Vasconcelos HL, Bruna EM (2009) Recognition of host plant volatiles by Pheidole minutula Mayr (Myrmicinae), an amazonian ant-plant specialist. Biotropica: 1–5

  • Dicke M, Sabelis MW, Takabayashi J, Bruin J, Maarten A (1990) Plant strategies of manipulating predator–prey interactions through allelochemicals: prospects for application in pest control. J Chem Ecol 16:3091–3118

    Article  CAS  PubMed  Google Scholar 

  • Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles 1. Plant Physiol 135:1893–1902

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dwomoh EA, Afun JVK, Ackonor JB, Agene VN (2008) Investigations on Oecophylla longinoda (Latreille) (Hymenoptera: Formicidae) as a biocontrol agent in the protection of cashew plantations. Pest Manag Sci 65:41–46

    Article  Google Scholar 

  • 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 

  • Egonyu JP, Ekesi S, Kabaru J, Irungu L, Torto B (2013) Cashew volatiles mediate short-range location responses in Pseudotheraptus wayi (Heteroptera : Coreidae). Environ Entomol 42:1400–1407

    Article  PubMed  Google Scholar 

  • Farris SM, Schulmeister S (2011) Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects. Proc R Soc B Biol Sci 278:940–951

    Article  Google Scholar 

  • Gammans N, Bullock JM, Gibbons H, Schönrogge K (2006) Reaction of mutualistic and granivorous ants to ulex elaiosome chemicals. J Chem Ecol 32:1935–1947

    Article  CAS  PubMed  Google Scholar 

  • González-Teuber M, Silva Bueno JC, Heil M, Boland W (2012) Increased host investment in extrafloral nectar (EFN) improves the efficiency of a mutualistic defensive service. PLoS One 7:p.e46598

  • Gronenberg W (2008) Structure and function of ant (Hymenoptera: Formicidae) brains: strength in numbers. Myrmecol News 11:25–36

    Google Scholar 

  • Guerrieri FJ, d’Ettorre P (2010) Associative learning in ants: conditioning of the maxilla-labium extension response in Camponotus aethiops. J Insect Physiol 56:88–92

    Article  CAS  PubMed  Google Scholar 

  • Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT (2008) Shared signals –‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol Lett 11:24–34

    PubMed  Google Scholar 

  • Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56:161–180

    Article  CAS  PubMed  Google Scholar 

  • Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61

    Article  CAS  PubMed  Google Scholar 

  • Heil M (2010) Ant–plant mutualisms. eLS. doi:10.1002/9780470015902.a0022558

    Google Scholar 

  • Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–553

    Article  Google Scholar 

  • Heinze J, Hölldobler B, Peeters C (1994) Conflict and co-operation in ant societies. Natur Wissenschaften 497:489–497

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1977) Colony-specific territorial pheromone in the African weaver ant Oecophylla longinoda (Latreille). Proc Natl Acad Sci U S A 74:2072–2075

    Article  PubMed Central  PubMed  Google Scholar 

  • Jersáková J, Johnson SD, Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biol Rev Camb Philos Soc 81:219–235

    Article  PubMed  Google Scholar 

  • Junker RR, Blüthgen N (2010) Floral scents repel facultative flower visitors, but attract obligate ones. Ann Bot 105:777–782

    Article  PubMed Central  PubMed  Google Scholar 

  • Koptur S, Truong N (1998) Facultative ant-plant interactions : nectar sugar preferences of introduced pest ant species in South Florida. Biotropica 30:179–189

    Article  Google Scholar 

  • Millar JG (2005) Pheromones of true bugs. Topics Curr Chem 240:37–84

    CAS  Google Scholar 

  • Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450

    Article  PubMed  Google Scholar 

  • National Institutes of Standards and Technology (2005) NIST/EPA/NIH mass spectral library, http://www.nist.gov

  • Newey PS (2009) Colony-mate recognition in the weaver ant Oecophylla smargdina. Dissertation, James Cook University

  • Olotu IM, Plessis H, Seguni SZ, Maniania KN (2013) Efficacy of the African Weaver ant Oecophylla longinoda (Hymenoptera: Formicidae) in the control of Helopeltis spp (Hemiptera: Miridae) and Pseudotheraptus wayi (Hemiptera: Coreidae) in cashew crop in Tanzania. Pest Manag Sci 69:911–918

    Article  CAS  PubMed  Google Scholar 

  • Perry CJ, Barron AB (2013) Neural mechanisms of reward in insects. Annu Rev Entomol 58:543–562

    Article  CAS  PubMed  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing,Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/

  • Rickson RF, Rickson MM (1998) The Cashew nut, Anacardium occidentale (Anacardiaceae) and its perennial association with ants: extrafloral nectary location and the potential for ant defense. Am J Bot 85:835–849

    Article  CAS  PubMed  Google Scholar 

  • Santos JC, Yamamoto M, Oliveira FR, Del-Claro K (2005) Behavioral repertory of the Weaver ant Camponotus (Myrmobrachys) senex (Hymenoptera: Formicidae). Sociobiology 45:1–12

    Google Scholar 

  • Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Die Naturwissenschaften 92:255–264

    Article  CAS  PubMed  Google Scholar 

  • Schwander T, Rosset H, Chapuisat M (2005) Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav Ecol Sociobiol 59:215–221

    Article  Google Scholar 

  • Turlings TCJ, Wäckers F (2004) Recruitment of predators and parasitoids by herbivore-injured plants. Adv Insect Chem Ecol 2:21–75

    Article  Google Scholar 

  • Turner KM, Frederickson ME (2013) Signals can trump rewards in attracting seed-dispersing ants. PLoS One 8:e71871

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ueda H, Kikuta Y, Matsuda K (2012) Plant communication mediated by individual or blended VOCs ? Plant Signal Behav 7:222–226

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van Mele P (2008) Biological control with the weaver ant Oecophylla Longinoda in Africa: a review of research and development efforts to link farmers to organic markets. Outlooks Pest Manag 19:180–183

    Article  Google Scholar 

  • Van Mele P, Vayssières JF (2007) Weaver ants help farmers to capture organic markets. Pestic News 75:9–11

    Google Scholar 

  • Van Mele P, Vayssières JF, Tellingen V, Vrolijks J (2007) Effects of an African weaver ant, Oecophylla longinoda, in controlling mango fruit flies (Diptera: Tephritidae) in Benin. J Econ Entomol 100:695–701

    Article  PubMed  Google Scholar 

  • Vanderplank FL (1960) The bionomics and ecology of the red tree ant Oecophylla spp and its relationship to the coconut bug Pseudotheraptus wayi Brown (Coreidae). J Anim Ecol 29:15–33

    Article  Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of Infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172

    Article  Google Scholar 

  • Von Mérey GE, Veyrat N, D’Alessandro M, Turlings TCJ (2013) Herbivore-induced maize leaf volatiles affect attraction and feeding behavior of Spodoptera littoralis caterpillars. Front Plant Sci 4:209

    Google Scholar 

  • Way JM, Khoo CK (1992) Role of ants in pest management. Annu Rev Entomol 37:479–503

    Article  Google Scholar 

  • Wijit W (1991) Floral biology of cashew (Anacardium occidentale L.) in relation to pollination and fruit set. Dissertation, University of Adelaide

  • Youngsteadt E, Nojima S, Häberlein C, Schulz S, Schal C (2008) Seed odor mediates an obligate ant-plant mutualism in Amazonian rainforests. Proc Natl Acad Sci U S A 105:4571–4575

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Youngsteadt E, Baca JA, Osborne J, Schal C (2009) Species-specific seed dispersal in an obligate ant-plant mutualism. PLoS One 4:e4335

    Article  PubMed Central  PubMed  Google Scholar 

  • Youngsteadt E, Bustios PG, Schal C (2010) Divergent chemical cues elicit seed collecting by ants in an obligate multi-species mutualism in lowland Amazonia. PLoS One 5:e15822

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank: The USDA/ARS-Centre for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, USA, for funding the research project and the icipe Dissertation Research Internship Programme (DRIP) for the studentship; Dr. Ayuka Fombong (BCED-icipe), Ms. Juliah W. Jacob (BCED-icipe) and Nickson Onyango (icipe) for technical support in the field and laboratory; Dr Rahab Wambui Muinga (Centre Director), Mr Muniu, and Mr Mwinga all of the Kenya Agricultural Research Institute (KARI) Mtwapa research station for assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Baldwyn Torto.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wanjiku, C., Khamis, F.M., Teal, P.E.A. et al. Plant Volatiles Influence the African Weaver Ant-Cashew Tree Mutualism. J Chem Ecol 40, 1167–1175 (2014). https://doi.org/10.1007/s10886-014-0512-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-014-0512-3

Keywords

Navigation