Abstract
Signalling is necessary for the maintenance of interspecific mutualisms but is vulnerable to exploitation by eavesdropping. While eavesdropping of intraspecific signals has been studied extensively, such exploitation of interspecific signals has not been widely documented. The juvenile stages of the Australian lycaenid butterfly, Jalmenus evagoras, form an obligate association with several species of attendant ants, including Iridomyrmex mayri. Ants protect the caterpillars and pupae, and in return are rewarded with nutritious secretions. Female and male adult butterflies use ants as signals for oviposition and mate searching, respectively. Our experiments reveal that two natural enemies of J. evagoras, araneid spiders and braconid parasitoid wasps, exploit ant signals as cues for increasing their foraging and oviposition success, respectively. Intriguingly, selection through eavesdropping is unlikely to modify the ant signal.
Similar content being viewed by others
References
Agrawal A, Fordyce J (2000) Induced indirect defence in a lycaenid-ant association: the regulation of a resource in a mutualism. Proc R Soc B 267:1857–1861
Allan RA, Elgar MA, Capon RJ (1996) Exploitation of an ant chemical alarm signal by the zodariid spider Habronestes bradleyi Walckenaer. Proc R Soc B 263:69–73
Axén AH, Pierce NE (1998) Aggregation as a cost-reducing strategy for lycaenid larvae. Behav Ecol 9:109–115
Axén A, Leimar O, Hoffman V (1996) Signaling in a mutualistic interaction. Anim Behav 52:321–333
Baigrie BD, Thompson AM, Flower TP (2014) Interspecific signaling between mutualists: food-thieving drongos use a cooperative sentinel call to manipulate foraging partners. Proc R Soc B 281:20141232
Barbero F, Thomas JA, Bonelli S, Balletto E, Schonrogge K (2009) Queen ants make distinctive sounds that are mimicked by a butterfly social parasite. Science 323:782–785
Beckers OM, Wagner WE Jr (2012) Eavesdropping parasitoids do not cause the evolution of less conspicuous signalling behaviour in a field cricket. Anim Behav 84:1475–1462
Belwood JJ, Morris GK (1987) Bat predation and its influence on calling behavior in neotropical katydids. Science 238:64–67
Brandley NC, Speiser DI, Johnsen S (2013) Eavesdropping on visual secrets. Evol Ecol 27:1045–1068
Cade W (1975) Acoustically orienting parasitoids: fly phonotaxis to cricket song. Science 190:1312–1313
Cardenas M, Jiros P, Pekar S (2012) Selective olfactory attention of a specialised predator to intraspecific chemical signals of its prey. Naturwissenschaften 99:597–605
Clark RJ, Jackson RR, Cutler B (2000) Chemical cues from ants influence predatory behavior in Habrocestum pulex, an ant-eating jumping spider (Araneae, Salticidae. J Arachnol 28:309–318
Daniels H, Gottsberger G, Fiedler K (2005) Nutrient composition of larval nectar secretions from three species of myrmecophilous butterflies. J Chem Ecol 31:2805–2821
Devries PJ (1990) Enhancement of symbioses between butterfly caterpillars and ants by vibrational communication. Science 248:1104–1106
Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Nat Acad Sci USA 95:8676–8680
Elgar MA, Pierce NE (1988) Male lifetime mating success and female fecundity of an ant–tended lycaenid butterfly. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp. 59–75
Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91
Fatouros NE, Huigens ME, van Loon JJA, Dicke M, Hilker M (2008) Butterfly anti-aphrodisiac lures parasitic wasps. Nature 433:704
Fiedler K, Hölldobler H, Seufert P (1996) Butterflies and ants: the communicative domain. Experientia 52:14–24
Foelix R (2010) Biology of spiders, 3rd edn. Oxford University Press, Oxford
Foster KR, Wenseleers TJ (2006) A general model for the evolution of mutualisms. J Evol Biol 19:1283–1293
Fraser AM, Tregenza T, Wedell N, Elgar MA, Pierce NE (2002) Oviposition tests of ant preference in a myrmecophilous butterfly. J Evol Biol 15:861–870
Fürst MA, Nash DR (2010) Host ant independent oviposition in the parasitic butterfly Maculinea alcon. Biol Lett 6:174–176
Gaskett AC (2007) Spider sex pheromones: emission, reception, structures, and functions. Biol Rev 82:26–48
Gaskett AC, Herberstein ME, Downes BJ, Elgar MA (2004) Life–time male mating preferences in a sexually cannibalistic orb–web spider (Araneae: Araneidae. Behaviour 141:1197–1210
Goodale E, Beauchamp G, Magrath RD, Nieh JC, Ruxton GD (2010) Interspecific information transfer influences animal community structure. Trends in Ecology and Evolution 25:354–361
Henneken J, Jones TM, Goodger J, Walter A, Elgar MA (2016) Diet influences female signals used in male mate choice. Anim Behav 108:215–221
Hojo MK, Wada-Katsumata A, Ozaki M, Yamaguchi S, Yamaoka R (2008) Gustatory synergism in ants mediates a species-specific symbiosis with lycaenid butterflies. J Comp Physiol A 194:1043–1052
Hsieh H-Y, Liere H, Soto EJ, Perfecto I (2012) Cascading trait-mediated interactions induced by ant pheromones. Ecol Evol 2:2181–2191
Igic B, McLachlan J, Lehtinen I, Magrath RD (2015) Crying wolf to a predator: deceptive vocal mimicry by a bird protecting young. Proc R Soc B 282:20150798
Johnson A, Revis O, Johnson JC (2011) Chemical prey cues influence the urban microhabitat preferences of Western black widow spiders, Latrodectus hesperus. J Arachnol 39:449–453
Kim JW, Brown GE, Dolinsek IJ, Brodeur NN, Leduc AOHC, Grant JWA (2009) Combined effects of chemical and visual information in eliciting antipredator behaviour in juvenile Atlantic salmon Salmo salar. J Fish Biol 74:1280–1290
Kitching RL (1983) Myrmecophilous organs of the larvae and pupa of the lycaenid butterfly Jalmenus evagoras (Donovan). J Nat Hist 17:471–481
Lewkiewicz DA, Zuk M (2004) Latency to resume calling after disturbance in the field cricket, Teleogryllus oceanicus, corresponds to population-level differences in parasitism risk. Behav Ecol Sociobiol 55:569–573
Mestre L, Bucher R, Entling MH (2014) Trait-mediated effects between predators: ant chemical cues induce spider dispersal. J Zool 293:119–125
Nakano R, Skals N, Takanashi T, Surlykke A, Koike T, Yoshida K, Maruyama H, Tatsuki S, Ishikawa Y (2008) Moths produce extremely quiet ultrasonic courtship songs by rubbing specialized scales. Proc Nat Acad Sci USA 105:11812–11817
Nelson XJ, Jackson RR (2014) Timid spider uses odor and visual cues to actively select protected nesting sites near ants. Behav Ecol Sociobiol 68:773–780
Oliver JC, Stein LR (2011) Evolution of influence: signaling in a lycaenid-ant interaction. Evol Ecol 25:1205–1216
Patricelli D, Barbero F, Occhipinti A, Bertea CM, Bonelli S, Casacci LP, Zebelo SA, Crocoll C, Gershenzon J, Maffei ME, Thomas JA, Balletto E (2015) Plant defences against ants provide a pathway to social parasitism in butterflies. Proc R Soc B 282:20151111
Peake TM, Terry AMR, McGregor PK, Dabelsteen T (2001) Male great tits eavesdrop on simulated male-to-male vocal interactions. Proc R Soc B 268:1183–1187
Pierce NE, Elgar MA (1985) The influence of ants on host plant selection by Jalmenus evagoras, a myrmecophilous lycaenid butterfly. Behav Ecol Sociobiol 16:209–222
Pierce NE, Mead PS (1981) Parasitoids as selective agents in the symbiosis between lycaenid butterfly larvae and ants. Science 211:1185–1187
Pierce NE, Nash DR (1999) The biology of Australian butterflies. In: Kitching RL, Sheermeyer E, Jones RE, Pierce NE (eds) The imperial blue: Jalmenus evagoras (Lycaenidae). CSIRO Press, Melbourne, pp. 279–315
Pierce NE, Kitching RL, Buckley RC, Taylor MFJ, Benbow KF (1987) The costs and benefits of cooperation between the Australian lycaenid butterfly, Jalmenus evagoras, and its attendant ants. Behav Ecol Sociobiol 21:237–248
Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu Rev Entomol 47:733–771
Ranganathan Y, Borges RM (2009) Predatory and trophobiont-tending ants respond differently to fig and fig wasp volatiles. Anim Behav 77:1539–1545
Rutledge CE (1996) A survey of identified kairomones and synomones used by insect parasitoids to locate and accept their hosts. Chemoecology 7:121–131
Schatz B, Hossaert-McKey M (2010) Ants use odour cues to exploit fig-fig wasp interactions. Acta Oecol 36:107–113
Schonewolf KW, Bell R, Rypstra AL, Persons MH (2006) Field evidence of an airborne enemy-avoidance kairomone in wolf spiders. J Chem Ecol 32:1565–1576
Schurian KG, Fiedler K, Maschwitz U (1993) Parasitoids exploit secretions of myrmecophilous lycaenid butterfly caterpillars (Lycaenidae). J Lep Soc 47:150–154
Seufert P, Fiedler K (1996) Life-history diversity and local coexistence of three closely related lycaenid butterflies (Lepidoptera, Lycaenidae) in Malaysian rainforests. Zool Anzeiger 234:229–239
Siemers BM, Kriner E, Kaipf I, Simon M, Greif S (2012) Bats eavesdrop on the sound of copulating flies. Current Biol 22:R563–R564
Stevens M (2013) Sensory ecology, behaviour, and evolution. Oxford University Press, Oxford
Thomas JA, Elmes GW (1993) Specialized searching and the hostile use of allomones by a parasitoid whose host, the butterfly Maculinea rebeli, inhabits ant nests. Anim Behav 45:593–602
Travassos MA, Pierce NE (2000) Acoustics, context and function of vibrational signalling in a lycaenid butterfly-ant mutualism. Anim Behav 60:13–26
Tuttle MD, Ryan MJ (1981) Bat predation and the evolution of frog vocalizations in the neotropics. Science 214:677–678
Vergara RC, Torres-Araneda A, Villagra DA, Raguso RA, Arroyo MTK, Villagra CA (2011) Are eavesdroppers multimodal? Sensory exploitation of floral signals by a non-native cockroach Blatta orientalis. Current Zool 57:162–174
Wagner D, Kurina L (1997) The influence of ants and water availability on oviposition behaviour and survivorship of a facultatively ant-tended herbivore. Ecol Entomol 22:352–360
Weeks JA (2003) Parasitism and ant protection alter the survival of the lycaenid Hemiargus isola. Ecol Entomol 28:228–232
Zhang S, Koh TH, Seah WK, Lai YH, Elgar MA, Li D (2012) A novel property of spider silk: chemical defence against ants. Proc Roy Soc B 279:1824–1830
Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Q Rev Biol 73:415–438
Acknowledgments
We thank Bill Piel for identifying the spiders and the Australian Research Council (DP120100162) for financial support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Sven Thatje
Rights and permissions
About this article
Cite this article
Elgar, M.A., Nash, D.R. & Pierce, N.E. Eavesdropping on cooperative communication within an ant-butterfly mutualism. Sci Nat 103, 84 (2016). https://doi.org/10.1007/s00114-016-1409-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-016-1409-5