Herbivory and inbreeding affect growth, reproduction, and resistance in the rhizomatous offshoots of Solanum carolinense (Solanaceae)

Chad T Nihranz,Rebecca L Kolstrom,Mark C Mescher,Consuelo M De Moraes,Andrew G Stephenson,Rupesh R Kariyat

doi:10.1007/s10682-019-09997-w

Chad T Nihranz, Rebecca L Kolstrom + Show 4 more

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https://doi.org/10.1007/s10682-019-09997-w

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Abstract

Resource sharing within clonal plant networks can occur via the translocation of water, nutrients, and photoassimilates through rhizomes and stolons. Similar mechanisms may mediate the sharing of information (e.g., about herbivory or other environmental stressors) among ramets via molecular or biochemical signals. The storage of such information in belowground structures could facilitate the transmission of appropriate phenotypic responses across growing seasons in perennial species. However, few previous studies have explored the potential transfer of ecologically relevant information within such networks. This study addresses the effects of foliar herbivory and belowground overwintering on the growth and flowering, physical defenses, and herbivore resistance in the clonally spreading species Solanum carolinense L. (Solanaceae). We used rhizomes from inbred and outbred plants that were repeatedly exposed to feeding damage by Manduca sexta L. (Sphingidae) caterpillars and rhizomes from undamaged control plants. These rhizomes were either planted immediately or exposed to overwintering conditions and allowed to produce new ramets (rhizomatous offshoots). We then assessed offshoot emergence, flowering, physical defense traits, and herbivore performance. Relative to controls, offshoots of herbivore-damaged plants exhibited greater spine and trichome densities, and reduced performance of M. sexta larvae. However, they also emerged and flowered significantly later, and produced fewer flowers than offshoots of undamaged plants. Inbreeding also negatively affected offshoot emergence, flowering, trichome production, and herbivore resistance. These effects of parental herbivory were more pronounced in outbred offshoots, indicating that inbreeding may compromise the trans-seasonal induction of plant defenses. Finally, exposure to overwintering conditions increased trichome production and reduced caterpillar performance on offshoots. Together, these results show that induced defenses can be transmitted through rhizomes and affect offshoot growth, flowering, defensive traits, and herbivore resistance. They also document fitness-related costs associated with defense induction in offshoots and suggest that the transfer of defenses across seasons can be compromised by inbreeding.

Highlights

Herbaceous perennial plant species often spread via runners that grow laterally from the parent plant and can produce new shoots (Cook 1985)
Few previous studies have explored the effects of foliar herbivory on rhizomes of vegetatively spreading plants, and none have demonstrated the ability of clonal plants to transmit herbivoreinduced information from parental plants to unconnected offshoots
The current results demonstrate that information concerning plant herbivory can persist in unconnected offshoots grown from rhizomes of S. carolinense, which have never experienced herbivory, and that this information positively influences offshoot defenses against herbivores and negatively impacts herbivore (M. sexta) performance traits (Table 1)

Summary

Introduction

Herbaceous perennial plant species often spread via runners (e.g., stolons and rhizomes) that grow laterally from the parent plant and can produce new shoots (Cook 1985). In response to the threat of herbivory, plants have evolved a great diversity of physical and chemical defense mechanisms. These defenses can affect herbivores directly, by deterring feeding, impeding movement, and limiting access to the surface of plants (Levin 1973; Hanley et al 2007; Howe and Schaller 2008; War et al 2012; Kariyat et al 2017), or indirectly, by attracting predators of the herbivores (Paré and Tumlinson 1999; Kessler and Baldwin 2001; Heil 2008, 2015). Many studies have shown that chewing insect herbivores induce indirect defenses such as volatile organic compounds that attract natural enemies of the herbivores (Paré and Tumlinson 1997; De Moraes et al 1998), as well as direct defenses, such as chemical feeding deterrents, and mechanical defenses, such as spines and trichomes (Holeski 2007; Kariyat et al 2013; Barton 2015)

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