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Messages from the Other Side: Parasites Receive Damage Cues from their Host Plants

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Abstract

As sessile organisms, plants rely on their environment for cues indicating imminent herbivory. These cues can originate from tissues on the same plant or from different individuals. Since parasitic plants form vascular connections with their host, parasites have the potential to receive cues from hosts that allow them to adjust defenses against future herbivory. However, the role of plant communication between hosts and parasites for herbivore defense remains poorly investigated. Here, we examined the effects of damage to lupine hosts (Lupinus texensis) on responses of the attached hemiparasite (Castilleja indivisa), and indirectly, on a specialist herbivore of the parasite, buckeyes (Junonia coenia). Lupines produce alkaloids that act as defenses against herbivores that can be taken up by the parasite. We found that damage to lupine host plants by beet armyworm (Spodoptera exigua) significantly increased jasmonic acid (JA) levels in both the lupine host and parasite, suggesting uptake of phytohormones or priming of parasite defenses by using host cues. However, lupine host damage did not induce changes in alkaloid levels in the hosts or parasites. Interestingly, the parasite had substantially higher concentrations of JA and alkaloids compared to lupine host plants. Buckeye herbivores consumed more parasite tissue when attached to damaged compared to undamaged hosts. We hypothesize that increased JA due to lupine host damage induced higher iridoid glycosides in the parasite, which are feeding stimulants for this specialist herbivore. Our results demonstrate that damage to hosts may affect both parasites and associated herbivores, indicating cascading effects of host damage on multiple trophic levels.

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Acknowledgments

Thanks to Adler lab members, D. Chan, L. Ndanga, and A. Soleil with plant propagation and data collection, A. Agrawal and A. Kessler labs for help with phytohormone analysis, C. Joyner and colleagues at the UMass CNS greenhouses, Dudley Farman (Nat Res Inst) for help with chemical analysis, and S. McArt and two anonymous reviewers for providing valuable feedback on this manuscript. Thanks to Fulbright Fellowship (MCT), Faculty for the Future Fellowship (MCT), Plant Biology Graduate program (MCT), USDA/CSREES (Hatch) MAS000411 (LSA) and USDA NRI 2008-02346 (LSA) for funding.

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Author notes

  1. Muvari Connie Tjiurutue

    Present address: Department of Chemistry & Biochemistry, University of Namibia, 340 Mandume Ndemufayo Avenue, Pionierspark, Windhoek, Namibia

Authors and Affiliations

  1. Biology Department, University of Massachusetts Amherst, 221 Morrill Science Center South, 611 North Pleasant Street, Amherst, MA, 01003, USA

    Muvari Connie Tjiurutue & Lynn S. Adler

  2. Natural Resources Institute, University of Greenwich, Central Avenue, Chatham Maritime, Chatham, Kent, ME4 4TB, UK

    Philip C. Stevenson

  3. Royal Botanic Gardens, Kew, Richmond, TW9 3AB, UK

    Philip C. Stevenson

Authors
  1. Muvari Connie Tjiurutue
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  2. Philip C. Stevenson
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  3. Lynn S. Adler
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Correspondence to Muvari Connie Tjiurutue.

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Funding

The study was funded by Fulbright Fellowship (MCT), Faculty for the Future Fellowship (MCT), Plant Biology Graduate program (MCT), USDA/CSREES (Hatch) MAS000411 (LSA) and USDA NRI 2008–02,346 (LSA).

Conflict of Interest

Author LSA has received recent research grants from USDA-AFRI, NSF-DEB, the North American Pollinator Protection Campaign (co-PI), and the Dartmouth Scholarly Innovation and Advancement Awards (co-PI). All other authors declare that they have no conflict of interest.

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Tjiurutue, M.C., Stevenson, P.C. & Adler, L.S. Messages from the Other Side: Parasites Receive Damage Cues from their Host Plants. J Chem Ecol 42, 821–828 (2016). https://doi.org/10.1007/s10886-016-0746-3

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  • DOI: https://doi.org/10.1007/s10886-016-0746-3

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