The Scent of Life: Phoretic Nematodes Use Wasp Volatiles and Carbon Dioxide to Choose Functional Vehicles for Dispersal

Abstract

Hitchhikers (phoretic organisms) need vehicles to disperse out of unsuitable habitats. Therefore, finding vehicles with the right functional attributes is essential for phoretic organisms. To locate these vehicles, phoretic organisms employ cues within modalities, ranging from visual to chemical senses. However, how hitchhikers discriminate between individual vehicles has rarely been investigated. Using a phoretic nematode community associated with an obligate fig–fig wasp pollination mutualism, we had earlier established that hitchhiking nematodes make decisions based on vehicle species identity and number of conspecific hitchhikers already present on the vehicle. Here we investigate if hitchhikers can differentiate between physiological states of vehicles. We asked whether phoretic nematodes choose between live or dead vehicles present in a chemically crowded environment and we investigated the basis for any discrimination. We conducted two-choice and single-choice behavioral assays using single nematodes and found that plant- and animal-parasitic nematodes preferred live over dead vehicles and used volatiles as a sensory cue to make this decision. However, in single-choice assays, animal-parasitic nematodes were also attracted towards naturally dead or freeze-killed wasps. The volatile profile of the wasps was dominated by terpenes and spiroketals. We examined the volatile blend emitted by the different wasp physiological states and determined a set of volatiles that the phoretic nematodes might use to discriminate between these states which is likely coupled with respired CO2. We determined that CO2 levels emitted by single wasps are sufficient to attract nematodes, demonstrating the high sensitivity of nematodes to this metabolic product.

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Data Availability

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Acknowledgements

We thank G. Yathiraj for field assistance, and Sunitha Murray for logistic support.

Funding

The Indian Institute of Science (IISc); Department of Science & Technology (DST), DST-FIST, Government of India (GOI); Department of Biotechnology–IISc Partnership Programme, GOI; and Ministry of Environment, Forests and Climate Change, GOI, provided financial support.

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Study conception was by Satyajeet Gupta. Experimental design was finalized by Satyajeet Gupta and Renee M. Borges. Data collection was carried out by Satyajeet Gupta, Kaveri Dey and Anusha L. K. Kumble. All statistical analysis was performed by Satyajeet Gupta. VOCs were identified by Jean-Marie Bessière. The paper was jointly written by Satyajeet Gupta and Renee M. Borges. All authors read and approved the final manuscript.

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Correspondence to Renee M. Borges.

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The authors declare that there is no conflict of interests.

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Gupta, S., Kumble, A.L.K., Dey, K. et al. The Scent of Life: Phoretic Nematodes Use Wasp Volatiles and Carbon Dioxide to Choose Functional Vehicles for Dispersal. J Chem Ecol 47, 139–152 (2021). https://doi.org/10.1007/s10886-021-01242-5

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Keywords

  • Carbon dioxide
  • Conophthorin
  • Fig wasps
  • Nematodes
  • Phoresy
  • Wasp VOCs