Open circles represent control plants (receiving lanolin-filled vials); filled squares represent plants receiving a persistent application of vials containing 10nghr cis -3-hexenyl acetate ( z 3HAC) dissolved in lanolin.

Frost Department of Biology, University of Louisville, Louisville, KY, USA 40292 Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Christopher J.

Frost.

Yet, ecological costs associated with volatile exposure alone are unclear.

In a common garden experiment, we tested the hypothesis that exposure to a single HIPV would decrease herbivore damage at the cost of reduced plant growth and reproduction.

Lima bean ( Phaseolus lunatus ) and pepper ( Capsicum annuum ) plants were exposed to a persistent, low-dose (10nghour) of the green leaf volatile cis -3-hexenyl acetate ( z3 HAC), a ubiquitous HIPV.

Natural herbivory was reduced in z3 HAC-exposed lima bean plants, but not in pepper.

Cyanogenic potential, a putative defense mechanism in lima bean, was lower in z3 HAC-exposed leaves, suggesting a growth-defense tradeoffs from z3 HAC exposure alone.

Plant species-specific responses to an identical priming cue have important implications for ecological costs and benefits of volatile-mediated inter-plant communication under field conditions.

Introduction Production and utilization of airborne chemical cues is prevalent within the plant kingdom.

Plants depend on airborne chemical signaling for pollination ( Muhlemann et al., 2014 ), indirect defense ( Mumm and Dicke, 2010 ), protection from pathogens ( Farag et al., 2013 ), and herbivore resistance ( Frost et al., 2008c ).

Volatile communication is also pivotal for plant-plant signaling, and selection for such signaling depends on honest cues that reliably confer ecologically relevant information.

For example, herbivory is a fundamental ecological interaction that impacts plant fitness, and many plants increase the production and emission of volatile compounds in response to herbivore damage ( Turlings et al., 1995 ).

Such herbivore-induced plant volatiles (HIPVs) are potentially reliable cues around which plant-plant eavesdropping could be evolutionarily adaptive( Rodriguez-Saona and Frost, 2010 ).

Undamaged plants (or parts of the same plant ( Frost et al., 2007; Heil and Silva Bueno, 2007 )) eavesdropping on HIPVs from a plant experiencing herbivory may directly trigger stress responses ( Arimura et al., 2002; Heil and Karban, 2010; Pearse et al., 2013 ), or alternatively prime responses for future potential herbivory ( Frost and Hunter, 2008 ).

GLV exposure alters gene expression profiles related to specialized metabolite production and accumulated secondary metabolite precursors in preparation for inducing resistance ( Pastor et al., 2014 ).

For example, the GLV cis -3-hexenyl acetate ( z 3HAC) induces transcriptional changes in poplar ( Frost et al., 2008c ) and maize ( Engelberth et al., 2004 ) that prime oxylipin signaling and induced resistance.

Ecological theory posits that induced resistance by plants against herbivores is a cost-savings strategy to restrict the deployment of costly specialized defensive metabolites until necessary ( Accamando and Cronin, 2012; Cipollini et al., 2003 ).

However, inducible resistance generates a period of vulnerability between the time of attack and the upregulation of resistance ( Cipollini and Heil, 2010 ).

Perception of early reliable cues may overcome such a vulnerability by allowing a plant to anticipate a probable attack.

In other words, perception of a priming stimulus, such as an HIPV, may induce physiological changes that incur costs that are less expensive than induced resistance itself.

Non-volatile priming agents -amino butyric acid (BABA) ( van Hulten et al., 2006 ) and snail mucus ( Orrock, 2018 ) both support this prediction.

Similarly, costs associated with volatile perception alone that initiate priming should be less severe than costs of induced resistance to actual herbivory( Martinez-Medina et al., 2016 ).

For example, whereas bacterial-derived volatiles 3-pentanol and 2-butanone decrease reproductive output in field-grown Cucumis sativa ( Song and Ryu, 2013 ), wild tobacco ( Nicotiana attenuata ) exposed to airspace of experimentally clipped sagebrush produce more seeds (i.e., higher presumptive fitness) relative to control plants ( Karban and Maron, 2002 ).

These results suggest that ecological costs of exposure to volatile cues may be context dependent, but comparative costbenefit tradeoffs for perception of HIPVs alone among sympatric field-grown plants is currently lacking.

Here, we report a common garden field experiment with lima bean ( Phaseolus lunatus ) and chili pepper ( Capsicum annuum ) testing the hypothesis that field plants subject to a persistent dose of an ostensibly reliable volatile cue incur consistent costs reflected in reduced growth and reproduction.

We treated individuals of both species to repeated low-dose applications of z3 HAC and measured their growth, reproduction, and herbivore damage throughout the growing season.

Methods and Materials Study Site and Plants A common garden experiment was established on a 54m 2 plot within Blackacre Conservancys community garden in Louisville, Kentucky (381133.8N 853128.3W; Supplemental Fig.

Height measurements and leaf counts for Phaseolus lunatus (lima bean) and Capsicum annuum (pepper) grown in a common garden field experiment Height for (A) lima bean was measured from the base of the longest runner to the uppermost branching point;(C) pepper height was measured from the base of the main stalk to the uppermost branching point.

Leaf counts for (B) lima bean and (D) pepper included all mature leaves on each plant.

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