Differential outcomes of novel plant-herbivore associations between an invading planthopper and native and invasive Spartina cordgrass species Article (Published Version) Harkin, Claire and Stewart, Alan J A (2021) Differential outcomes of novel plant-herbivore associations between an invading planthopper and native and invasive Spartina cordgrass species. Oecologia. ISSN 0029-8549 This version is available from Sussex Research Online: http://sro.sussex.ac.uk/id/eprint/98196/ This document is made available in accordance with publisher policies and may differ from the published version or from the version of record. If you wish to cite this item you are advised to consult the publisher’s version. Please see the URL above for details on accessing the published version. Copyright and reuse: Sussex Research Online is a digital repository of the research output of the University. Copyright and all moral rights to the version of the paper presented here belong to the individual author(s) and/or other copyright owners. To the extent reasonable and practicable, the material made available in SRO has been checked for eligibility before being made available. Copies of full text items generally can be reproduced, displayed or performed and given to third parties in any format or medium for personal research or study, educational, or not-for-profit purposes without prior permission or charge, provided that the authors, title and full bibliographic details are credited, a hyperlink and/or URL is given for the original metadata page and the content is not changed in any way. http://sro.sussex.ac.uk Oecologia https://doi.org/10.1007/s00442-021-04898-8 PLANT-MICROBE-ANIMAL INTERACTIONS – ORIGINAL RESEARCH Diferential outcomes of novel plant‑herbivore associations between an invading planthopper and native and invasive Spartina cordgrass species Claire Harkin1 · Alan J. A. Stewart1 Received: 9 March 2021 / Accepted: 23 March 2021 © The Author(s) 2021 Abstract Non-native plants may beneft, briefy or permanently, from natural enemy release in their invaded range, or may form novel interactions with native enemy species. Likewise, newly arrived herbivores may develop novel associations with native plants or, where their hosts have arrived ahead of them, re-establish interactions that existed previously in their ancestral ranges. Predicting outcomes from this diversity of novel and re-established interactions between plants and their herbivores presents a major challenge for invasion biology. We report on interactions between the recently arrived invasive planthopper Prokelisia marginata, and the multi-ploidy Spartina complex of four native and introduced species in Britain, each repre- senting a diferent level of shared evolutionary history with the herbivore. As predicted, S. alternifora, the ancestral host, was least impacted by planthopper herbivory, with the previously unexposed native S. maritima, a nationally threatened species, sufering the greatest impacts on leaf length gain, new leaf growth and relative water content. Contrary to expecta- tions, glasshouse trials showed P. marginata to preferentially oviposit on the invasive allododecaploid S. anglica, on which it achieved earlier egg hatch, faster nymphal development, larger female body size and greatest fnal population size. We suggest P. marginata is in the process of rapid adaptation to maximise its performance on what is now the most abundant and widespread host in Britain. The diversity of novel and re-established interactions of the herbivore with this multi-ploidy complex makes this a highly valuable system for the study of the evolutionary ecology of plant–insect interactions and their infuence on invasion dynamics. Keywords Prokelisia marginata · Biological invasions · Plant–insect interactions · Polyploidy · Enemy release Introduction known to have become naturalised outside their native range, with almost 5000 of them causing harm to the environment, Biological invasions are recognised as one of the primary the economy or human health (RBG Kew 2016). drivers of biodiversity loss, responsible for signifcant eco- A popular explanation for the success of invasive plants is logical and economic costs worldwide (Mack et al. 2000; that they often arrive in their new range without the full suite IPBES 2019). Most ecological communities now contain of natural enemies (herbivores, fungi and other pathogens) at least one non-native species, with invaders already rep- with which they have co-evolved (Maron and Vila 2001; resenting over a ffth of many countries’ fora (Mooney and Keane and Crawley 2002). Newly arrived plants may beneft Cleland 2001). At least 13,168 species of vascular plant are from such natural enemy release, briefy or permanently, or they may form novel interactions with native enemy spe- Communicated by Ian Kaplan. cies in the new range. Likewise, newly arrived herbivores may develop novel associations with native plants or, where * Claire Harkin their hosts have arrived ahead of them, re-establish interac- [email protected] tions that existed previously in their ancestral ranges. Pre- Alan J. A. Stewart dicting the outcomes from such a diversity of novel and re- [email protected] established interactions between plants and their herbivores 1 School of Life Sciences, University of Sussex, presents a major challenge for invasion biology (Chun et al. Brighton BN1 9QG, UK Vol.:(0123456789)1 3 Oecologia 2010; Pearse et al. 2013; Bezemer et al. 2014; deJonge et al. predicting the outcome of biological invasions mediated by 2019). plant–herbivore interactions (Hull-Sanders et al. 2009). This One frequently encountered circumstance of particular may necessitate system-by-system investigations to inform interest concerns where a non-native introduced plant is reu- management interventions. nited with its herbivore after temporarily beneftting from The introduction of the cordgrass Spartina alternifora natural enemy escape in its new range. This may happen Loiseleur to Britain from North America, its hybridization because the herbivore arrives naturally or anthropogenically, with a threatened native congeneric species, including a the latter being either accidental or as a deliberate attempt at chromosomal doubling event, and subsequent re-connection biocontrol. The strength and character of the re-established in the new range with its ancestral herbivore, the planthopper association between plant and herbivore may difer from that Prokelisia marginata Van Duzee, provides a unique oppor- found in their native range due to the infuence of a suite tunity to test these predictions. Here, we compare the impact of biotic and abiotic factors (Mitchell et al. 2006). As the of exposure to P. marginata on four species of Spartina in plant and herbivore share a long evolutionary history prior Britain with diferent histories of co-occurrence with the to their introduction into the new range, the prediction is that herbivore: the introduced ancestral host S. alternifora, the the plant in its non-native environment will be less severely native and previously unexposed S. maritima, the homoploid afected by the herbivore than native congenerics with no hybrid of these two species, S. x townsendii, and the allo- prior exposure. Indeed, some studies show reassociation dodecaploid S. anglica which arose from a chromosomal with historic enemies can result in levels of plant defence doubling of S. x townsendii. Also, we investigate whether greater than those displayed in their shared native range P. marginata makes a preferential choice between the host (Zangerl and Berenbaum 2005; Lu and Ding 2012), although species, and the impact that these host species have on P. evidence that greater defence results in greater compara- marginata performance and ftness outcomes. We hypoth- tive performance remains equivocal (Chun et al. 2010). Due esise that: (1) P. marginata will preferentially select S. to the greater length of shared evolutionary time in which alternifora, the species with which it has the longest shared reciprocal adaptations have been able to develop, the her- evolutionary history, for feeding and oviposition; (2) host bivore is predicted to perform better on its coevolved host plant species will have a signifcant impact on P. marginata compared to on congeneric natives. Coevolved hosts have life history traits, with the planthopper achieving the greatest been shown to support a greater abundance and diversity performance outcomes when raised on species with which it of insect herbivores, with signifcant host discrimination by has the longest shared evolutionary history; (3) exposure to phloem-feeding insects persisting despite the assumed palat- P. marginata feeding and oviposition will have a deleterious ability of novel alternatives (Burghardt and Tallamy 2013). impact on all species of Spartina, but the severity of impact Such preferences are frequently correlated with greater per- will be related to the extent of shared evolutionary history, formance outcomes (Gripenberg et al. 2010). i.e. least for S. alternifora and greatest for S. maritima; and A further complication may arise if ploidy levels dif- (4) the level of impact will not difer signifcantly between fer amongst sympatric congeneric species. Polyploidy is S. x townsendii and S. anglica, despite their difering ploidy widespread in plants (Ramsey and Schemske 1998), espe- levels, because they share identical evolutionary histories cially grasses (Stebbins 1956), and in particular occurs at with the planthopper