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How to Break into a Microcosm: Localization of Hidden Hosts by Fig Wasp Parasitoids


Affiliations
1 Centre for Ecological Sciences, Indian Institute of Science, Bengaluru 560 012, India; LIVIN Farms Agrifood GmbH, Vienna 1110, Austria
2 Centre for Ecological Sciences, Indian Institute of Science, Bengaluru 560 012, India
3 École Nationale Supérieure de Chimie, 240 Avenue du Professeur Emile Jeanbrau, 34090 Montpellier, France
 

Host-finding behaviour and decision-making in a tri-trophic interaction are often complex, especially when hosts are hidden within plant or animal tissues. We study how parasitoid fig wasps assess fig hosts for ovi-position. These wasps oviposit into fig inflorescences (syconia) in which conspecifics have previously depo-sited eggs, possibly to avoid sib-mating for offspring that will develop and mate within these enclosed inflo-rescences. The syconia previously visited by conspecif-ics can be identified from species-specific chemical footprints left on the outer syconium surface, and these are chemically characterized. The tarsal mor-phology that may facilitate such identification is also described. Fig wasps have a haplodiploid breeding system in which males are haploid, developing from unfertilized eggs, and are much smaller in size than females. We therefore also experimentally determined that these parasitoids do not deposit fertilized eggs destined to become females on male hosts, a behaviour likely driven by the greater nutritional requirements of female offspring compared to the smaller-sized males. We also quantified carbon dioxide (CO2) pro-duction from galls of different species, as species-specific hosts within the syconia are likely identified by differential CO2 production from galls, whose le-vels are assessed via the sensilla present on the parasi-toid ovipositor.

Keywords

Chemical Footprints, Fig Wasps, Hidden Hosts, Oviposition, Parasitoids, Synconia.
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  • Godfray, H. C. J. and Shimada, M., Parasitoids as model organisms for ecologists. Res. Popul. Ecol., 1999, 41, 3–10.

  • Mills, N. J. and Wajnberg, E., Optimal foraging behaviour and efficient biological control. In Behavioral Ecology of Insect Parasitoids from Theoretical Approaches to Field Applications (eds Wajnberg, E., Bernstein, C. and van Alphen, J. J. M.), Blackwell Science, Oxford, 2008, pp. 3–30.

  • van Oudenhove, L., Mailleret, L. and Fauvergue, X., Infochemical use and dietary specialization in parasitoids: a meta-analysis. Ecol. Evol., 2017, 7, 4804–4811.

  • Dicke, M., Vet, L. E. and Wäckers, F. L., How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids. Neth. J. Zool., 1990, 41, 202–213.

  • Chhan, S. and Morse, D. H., To mate or not to mate, and subsequent host search by a haplodiploid female parasitoid wasp. Ethology, 2019, 125, 457–464.

  • Krimmel, B. A. and Morse, D. H., Host-size decisions of female parasitoid wasps seeking hidden hosts. Ecol. Entomol., 2019, 44, 552–559.

  • Borges, M., Colazza, S., Ramirez-Lucas, P., Chauhan, K. R., Moraes, M. C. B. and Richard Aldrich, J., Kairomonal effect of walking traces from Euschistus heros (Heteroptera: Pentatomidae) on two strains of Telenomus podisi (Hymenoptera: Scelionidae). Physiol. Entomol., 2003, 28, 349–355.

  • Rostás, M. and Wölfling, M., Caterpillar footprints as host location kairomones for Cotesia marginiventris: persistence and chemical nature. J. Chem. Ecol., 2009, 35, 20–27.

  • Prokopy, R. J. and Roitberg, B. D., Joining and avoidance behavior in nonsocial insects. Annu. Rev. Entomol., 2001, 46, 631–665.

  • Dittmann, L. and Schausberger, P., Adaptive aggregation by spider mites under predation risk. Sci. Rep., 2017, 7, 10609.

  • Ranganathan, Y. and Borges, R. M., Predatory and trophobionttending ants respond differently to fig and fig wasp volatiles. Anim. Behav., 2009, 77, 1539–1545.

  • Saleh, N. and Chittka, L., The importance of experience in the interpretation of conspecific chemical signals. Behav. Ecol. Sociobiol., 2006, 61, 215–220.

  • Wheeler, C. A. and Cardé, R. T., Following in their footprints: cuticular hydrocarbons as overwintering aggregation site markers in Hippodamia convergens. J. Chem. Ecol., 2014, 40, 418–428.

  • Yadav, P. and Borges, R. M., Why resource history matters: age and oviposition history affect oviposition behaviour in exploiters of a mutualism. Ecol. Entomol., 2018, 43, 473–482.

  • Yadav, P., Desireddy, S., Kasinathan, S., Bessière, J. M. and Borges, R. M., History matters: Oviposition resource acceptance in an exploiter of a nursery pollination mutualism. J. Chem. Ecol., 2018, 44, 18–28.

  • van Baaren, J., Boivin, G., Bourdais, D. and Roux, O., Antennal sensilla of hymenopteran parasitic wasps: variations linked to host exploitation behaviour. In Modern Research and Educational Topics in Microscopy (eds Méndez-Vilas, A. and Díaz, J.), Formatex, Badajoz, Spain, 2007, pp. 345–352.

  • Ma, L., Li, Z. Q., Bian, L., Cai, X. M., Luo, Z. X., Zhang, Y. J. and Chen, Z. M., Identification and comparative study of chemosensory genes related to host selection by legs transcriptome analysis in the tea geometrid Ectropis obliqua. PLoS ONE, 2016, 11, e0149591.

  • Sollai, G., Biolchini, M., Loy, F., Solari, P. and Crnjar, R., Taste input from tarsal sensilla is related to egg-laying behavior in Papilio hospiton. Entomol. Exp. Appl., 2017, 165, 38–49.

  • Quicke, D. L. J., LeRalec, A. and Vilhelmsen, L., Ovipositor structure and function in the parasitic Hymenoptera with an exploration of new hypotheses. Rendiconti, 1999, 47, 197–239.

  • Cerkvenik, U., van de Straat, B., Gussekloo, S. W. and van Leeuwen, J. L., Mechanisms of ovipositor insertion and steering of a parasitic wasp. Proc. Natl. Acad. Sci. USA, 2017, 114, 7822–7831.

  • Ghara, M., Kundanati, L. and Borges, R. M., Nature’s Swiss army knives: ovipositor structure mirrors ecology in a multitrophic fig wasp community. PLoS ONE, 2011, 6, e23642.

  • Goyret, J., Markwell, P. M. and Raguso, R.A., Context- and scale dependent effects of floral CO2 on nectar foraging by Manduca sexta. Proc. Natl. Acad. Sci. USA, 2008, 105, 4565–4570.

  • Yadav, P. and Borges, R. M., The insect ovipositor as a volatile sensor within a closed microcosm. J. Exp. Biol., 2017, 220, 1554– 1557.

  • Yadav, P. and Borges, R. M., Host–parasitoid development and survival strategies in a non-pollinating fig wasp community. Acta Oecol., 2018, 90, 60–68.

  • Ghara, M., Ranganathan, Y., Krishnan, A., Gowda, V. and Borges, R. M., Divvying up an incubator: how parasitic and mutualistic fig wasps use space within their nursery microcosm. Arthropod Plant Interact, 2014, 8, 191–203.

  • Telang, A., Booton, V., Chapman, R. F. and Wheeler, D. E., How female caterpillars accumulate their nutrient reserves. J. Insect Physiol., 2001, 47, 1055–1064.

  • Ghara, M. and Borges, R. M., Comparative life-history traits in a fig wasp community: implications for community structure. Ecol. Entomol., 2010, 35, 139–148.

  • Ranganathan, Y., Ghara, M. and Borges, R. M., Temporal associations in fig–wasp–ant interactions: diel and phenological patterns. Entomol. Exp. Appl., 2010, 137, 50–61.

  • Venkateswaran, V., Shrivastava, A., Kumble, A. L. and Borges, R. M., Life-history strategy, resource dispersion and phylogenetic associations shape dispersal of a fig wasp community. Mov. Ecol., 2017, 5, 25.

  • Weiblen, G. D., How to be a fig wasp. Annu. Rev. Entomol., 2002, 47, 299–330.

  • Conti, E., Salerno, G., Bin, F. and Vinson, S. B., The role of host semiochemicals in parasitoid specificity: a case study with Trissolcus brochymenae and Trissolcus simoni on pentatomid bugs. Biol. Control, 2004, 29, 435–444.

  • Fatouros, N. E., Dicke, M., Mumm, R., Meiners, T. and Hilker, M., Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol., 2008, 19, 677–689.

  • Martin, S. J., Helanterä, H. and Drijfhout, F. P., Colony-specific hydrocarbons identify nest mates in two species of Formica ant. J. Chem. Ecol., 2008, 34, 1072–1080.

  • Curtis, S., Sztepanacz, J. L., White, B. E., Dyer, K. A., Rundle, H. D. and Mayer, P., Epicuticular compounds of Drosophila subquinaria and D. recens: identification, quantification, and their role in female mate choice. J. Chem. Ecol., 2013, 39, 579–590.

  • Peri, E., Frati, F., Salerno, G., Conti, E. and Colazza, S., Host chemical footprints induce host sex discrimination ability in egg parasitoids. PLoS ONE, 2013, 8, e79054.

  • Ozaki, M. et al., Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science, 2005, 309, 311–314.

  • Chen, Y. and Amrein, H., Enhancing perception of contaminated food through acid-mediated modulation of taste neuron responses. Curr. Biol., 2014, 24, 1969–1977.

  • Maher, N. and Thiery, D., Distribution of chemo- and mechanoreceptors on the tarsi and ovipositor of female European grapevine moth, Lobesia botrana. Entomol. Exp. Appl., 2004, 110, 135–143.

  • Loy, F., Solari, P., Isola, M., Crnjar, R. and Masala, C., Morphological and electrophysiological analysis of tarsal sensilla in the medfly Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae). Ital. J. Zool., 2016, 83, 456468.

  • Walker, E. D. and Archer, W. E., Sequential organization of grooming behaviors of the mosquito, Aedes triseriatus. J. Insect Behav., 1988, 1, 97–109.

  • Rebora, M., Salerno, G., Piersanti, S., Michels, J. and Gorb, S., Structure and biomechanics of the antennal grooming mechanism in the southern green stink bug Nezara viridula. J. Insect Physiol., 2019, 112, 57–67.

  • Böröczky, K., Wada-Katsumata, A., Batchelor, D., Zhukovskaya, M. and Schal, C., Insects groom their antennae to enhance olfactory acuity. Proc. Natl. Acad. Sci. USA, 2013, 110, 3615–3620.

  • Ranganathan, Y., Bessiere, J. M. and Borges, R. M., A coat of many scents: cuticular hydrocarbons in multitrophic interactions of fig wasps with ants. Acta Oecol., 2015, 67, 24–33.

  • Scriber, J. M. and Slansky Jr, F., The nutritional ecology of immature insects. Annu. Rev. Entomol., 1981, 26, 183211.

  • Lease, H. M. and Wolf, B. O., Lipid content of terrestrial arthropods in relation to body size, phylogeny, ontogeny and sex. Physiol. Entomol., 2011, 36, 29–38.

  • Lee, K. P., Sex-specific differences in nutrient regulation in a capital breeding caterpillar, Spodoptera litura (Fabricius). J. Insect Physiol., 2010, 56, 1685–1695.


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  • How to Break into a Microcosm: Localization of Hidden Hosts by Fig Wasp Parasitoids

Abstract Views: 334  |  PDF Views: 114

Authors

Pratibha Yadav
Centre for Ecological Sciences, Indian Institute of Science, Bengaluru 560 012, India; LIVIN Farms Agrifood GmbH, Vienna 1110, Austria
Anusha L. K. Kumble
Centre for Ecological Sciences, Indian Institute of Science, Bengaluru 560 012, India
Mahua Ghara
Centre for Ecological Sciences, Indian Institute of Science, Bengaluru 560 012, India
Jean-Marie Bessière
École Nationale Supérieure de Chimie, 240 Avenue du Professeur Emile Jeanbrau, 34090 Montpellier, France
Renee M. Borges
Centre for Ecological Sciences, Indian Institute of Science, Bengaluru 560 012, India

Abstract


Host-finding behaviour and decision-making in a tri-trophic interaction are often complex, especially when hosts are hidden within plant or animal tissues. We study how parasitoid fig wasps assess fig hosts for ovi-position. These wasps oviposit into fig inflorescences (syconia) in which conspecifics have previously depo-sited eggs, possibly to avoid sib-mating for offspring that will develop and mate within these enclosed inflo-rescences. The syconia previously visited by conspecif-ics can be identified from species-specific chemical footprints left on the outer syconium surface, and these are chemically characterized. The tarsal mor-phology that may facilitate such identification is also described. Fig wasps have a haplodiploid breeding system in which males are haploid, developing from unfertilized eggs, and are much smaller in size than females. We therefore also experimentally determined that these parasitoids do not deposit fertilized eggs destined to become females on male hosts, a behaviour likely driven by the greater nutritional requirements of female offspring compared to the smaller-sized males. We also quantified carbon dioxide (CO2) pro-duction from galls of different species, as species-specific hosts within the syconia are likely identified by differential CO2 production from galls, whose le-vels are assessed via the sensilla present on the parasi-toid ovipositor.

Keywords


Chemical Footprints, Fig Wasps, Hidden Hosts, Oviposition, Parasitoids, Synconia.

References





DOI: https://doi.org/10.18520/cs%2Fv121%2Fi1%2F141-147