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Plant reproductive traits mediate tritrophic feedback effects within an obligate brood-site pollination mutualism

  • Plant-microbe-animal interactions - Original research
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Abstract

Plants, herbivores and parasitoids affect each other directly and indirectly; however, feedback effects mediated by host plant traits have rarely been demonstrated in these tritrophic interactions. Brood-site pollination mutualisms (e.g. those involving figs and fig wasps) represent specialised tritrophic communities where the progeny of mutualistic pollinators and of non-mutualistic gallers (both herbivores) together with that of their parasitoids develop within enclosed inflorescences called syconia (hence termed brood-sites or microcosms). Plant reproductive phenology (which affects temporal brood-site availability) and inflorescence size (representing brood-site size) are plant traits that could affect reproductive resources, and hence relationships between trees, pollinators and non-pollinating wasps. Analysing wasp and seed contents of syconia, we examined direct, indirect, trophic and non-trophic relationships within the interaction web of the fig–fig wasp community of Ficus racemosa in the context of brood site size and availability. We demonstrate that in addition to direct resource competition and predator–prey (host–parasitoid) interactions, these communities display exploitative or apparent competition and trait-mediated indirect interactions. Inflorescence size and plant reproductive phenology impacted plant–herbivore and plant–parasitoid associations. These plant traits also influenced herbivore–herbivore and herbivore–parasitoid relationships via indirect effects. Most importantly, we found a reciprocal effect between within-tree reproductive asynchrony and fig wasp progeny abundances per syconium that drives a positive feedback cycle within the system. The impact of a multitrophic feedback cycle within a community built around a mutualistic core highlights the need for a holistic view of plant–herbivore–parasitoid interactions in the community ecology of mutualisms.

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Acknowledgments

We thank R. Yettiraj, Pratibha Yadav and Yuvaraj Ranganathan for help in bagging and fig collection, as well as Doyle McKey, Lawrence Harder, Carol Horvitz, Vignesh Venkateswaran, Lakshy Katariya, Joyshree Chanam and two anonymous reviewers for valuable suggestions on the manuscript. This research was funded by the Ministry of Environment, Forests & Climate Change, and the Department of Biotechnology, Government of India.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Centre for Ecological Sciences, Indian Institute of Science, Bangalore, 560 012, India

    Anusha Krishnan, Mahua Ghara, Srinivasan Kasinathan, Gautam Kumar Pramanik, Santosh Revadi & Renee M. Borges

  2. Botanical Garden, Department of Molecular Biology and Ecology of Plants, George Wise Faculty of Life Science, Tel Aviv University, 69978, Tel Aviv, Israel

    Mahua Ghara

  3. Institute of Microscopy, Anatomy and Neurobiology, Johannes Gutenberg-University Medicine Mainz, Hanns-Dieter-Hüsch-Weg 19, 55128, Mainz, Germany

    Gautam Kumar Pramanik

  4. Unit of Chemical Ecology, Department of Plant Protection and Biology, Swedish University of Agricultural Sciences, 23053, Alnarp, Sweden

    Santosh Revadi

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  1. Anusha Krishnan
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  3. Srinivasan Kasinathan
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  4. Gautam Kumar Pramanik
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Correspondence to Renee M. Borges.

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Communicated by Caroline Müller.

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Krishnan, A., Ghara, M., Kasinathan, S. et al. Plant reproductive traits mediate tritrophic feedback effects within an obligate brood-site pollination mutualism. Oecologia 179, 797–809 (2015). https://doi.org/10.1007/s00442-015-3372-9

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