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Herbivory and Resource Availability Shift Plant Defense and Herbivore Feeding Choice in a Seagrass System

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Herbivory and Resource Availability Shift Plant Defense and Herbivore Feeding Choice in a Seagrass System Oecologia (2019) 189:719–732 https://doi.org/10.1007/s00442-019-04364-6 PLANT-MICROBE-ANIMAL INTERACTIONS – ORIGINAL RESEARCH Herbivory and resource availability shift plant defense and herbivore feeding choice in a seagrass system Gema Hernán1,2 · Inés Castejón1 · Jorge Terrados1 · Fiona Tomas1,3 Received: 15 July 2018 / Accepted: 18 February 2019 / Published online: 26 February 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Numerous hypotheses have been posited to explain the observed variation in plant defense strategies against herbivory. Under resource-rich environments, plants are predicted to increase their tolerance (limiting resource model; LRM) and, while the resource availability hypothesis (RAH) predicts a decrease in constitutive resistance in plant species growing in resource-rich environments, at the intraspecifc level, plants are predicted to follow an opposite pattern (intraspecifc RAH). Furthermore, the efect of multiple factors in modulating plant defense strategies has been scarcely explored and is more difcult to predict. Our aim was to understand how plant defense traits respond to herbivory, resource availability and their interactions, and to assess the efects on plant palatability. To this end, we performed an in situ factorial experiment at two sites simulating three herbivory levels and two nutrient availability conditions with the seagrass Posidonia oceanica. Additionally, we performed a series of feeding experiments with its two main herbivores. While plants decreased their constitutive resistance under nutri- ent fertilization (contrary to intraspecifc RAH but in accordance to the RAH), and did not increase allocation to tolerance (likely due to resource limitation, LRM), simulated herbivory induced resistance traits. However, we found no interactive efects of nutrient fertilization and herbivory simulation on plant defense. Both herbivores responded similarly to changes in plant palatability, strongly preferring nutrient-enriched plants and non-clipped plants. This work highlights the need to better understand the drivers of plant defense intraspecifc variability in response to resources, particularly in habitat-forming species where changes in plant traits and abundance will cascade onto associated species. Keywords Plant–herbivore interactions · Limited resource model · Resource availability hypothesis · Nutrients · Posidonia oceanica Introduction Herbivory is a key ecological process that regulates the fow of energy to upper trophic levels and the composition, abundance and distribution of plant communities (Huntly Communicated by Daniel C. Reed. 1991; Wood et al. 2016). Herbivory has strong efects on Electronic supplementary material The online version of this plant ftness and can be an important pathway of biomass article (https ://doi.org/10.1007/s0044 2-019-04364 -6) contains and nutrient loss in plants (Cebrian 1999). Therefore, plants supplementary material, which is available to authorized users. have evolved diverse defense strategies against herbivory; tolerance strategies that reduce the impact of herbivory on * Gema Hernán [email protected] plant ftness (e.g., increased growth to compensate for leaf loss), and resistance strategies that reduce the preference 1 Department of Marine Ecology, IMEDEA (CSIC-UIB), or performance of herbivores (e.g., production of phenolic Mediterranean Institute for Advanced Studies, compounds; Fritz and Simms 1992). Plant allocation to these Balearic Islands, Spain diferent strategies is determined by a trade-of between ben- 2 Department of Biological Science, Florida State University, efts (i.e., better defense against herbivores) and costs (i.e., Tallahassee, FL, USA less resources available for growth and/or reproduction; 3 Department of Fisheries and Wildlife, Oregon State Bazzaz et al. 1987). Although initially thought otherwise University, Corvallis, OR, USA Vol.:(0123456789)1 3 720 Oecologia (2019) 189:719–732 (Van Der Meijden et al. 1988), recent studies suggests that result in higher limitation not only of carbon fxation but also plants present mixed tolerance-resistance defense mecha- of nutrient acquisition. nisms (Agrawal 2011; Carmona and Fornoni 2013), but that In addition to resource availability, plant defense strate- a trade-of exists between both strategies whereby selection gies against herbivores can respond to diferent consump- for increased resistance can lead to decreased tolerance tion levels. Indeed, herbivore intensity and duration modify (Fineblum and Rausher 2002). In addition, these defenses plant defense responses, with some traits only being induced can be either constitutive (i.e., expressed regardless of the under high herbivory (e.g., secondary metabolites, mineral herbivory pressure sufered by the plant) or induced (i.e., crystals; Vergés et al. 2008; Dostálek et al. 2016; Hartley produced in response to herbivory damage; Agrawal and et al. 2016), while others tend to be induced under mod- Karban 1999; Vergés et al. 2008). Recent studies suggest a erate herbivory (e.g., compensatory growth; Ruiz-R et al. trade-of between both strategies in which plants with higher 2008; Vergés et al. 2008; Sanmartí et al. 2014). Therefore, induced resistance invest less in constitutive resistance (e.g.; increased resource availability (when limiting resources are Kempel et al. 2011; Rasmann et al. 2015). considered) could minimize the costs of defense under dif- Since defense has a cost, availability of resources is an ferent levels of herbivory pressure. Yet, few studies have important determinant of defense strategies in plants. As an assessed the interactive efects of resource availability and explanation of how resources infuence plant allocation to varying herbivory pressure on plant defense strategies (i.e., defense, the Resource Availability Hypothesis (RAH) postu- tolerance and resistance). lates that species adapted to resource-rich environments have Furthermore, the consequences of resource availability higher growth rates and have less constitutive defenses but and herbivory pressure on plants may extend beyond the higher inducible defenses. On the contrary, species adapted individual species of herbivore, as we often fnd several her- to environments with low resource availability will have bivore species feeding on the same plant species. Indeed, lower growth rates and invest more in constitutive defense herbivory damage exerted by one guild or group of herbi- strategies (reviewed in Endara and Coley 2011). Although vores often has strong efects on other herbivores within the the RAH has been refuted by some studies (see Endara and same community due to changes in plant community struc- Coley 2011 and references therein) it is considered as an ture or abundance (Foster et al. 2014) or plant defenses (Del- adequate framework to explain the variation observed in phia et al. 2007; Ramirez and Eubanks 2016). This is even defense strategies under diferent resource availability con- more relevant when herbivory is exerted upon foundation ditions. Recent studies have explored this hypothesis in the species that are the base of ecosystems such as terrestrial context of intraspecifc variations in plant defense (hereafter forests, coral reefs, or kelp beds, since in these ecosystems, intraspecifc RAH) suggesting the opposite pattern. In this grazing-mediated changes cascade through the food web and case, individuals of the same species have higher consti- can have profound ecological impacts such as loss of feeding tutive resistance in high resource environments mediated resources or refuge (Steneck et al. 2002; Ellison et al. 2005; by the higher herbivory pressure found in these environ- Pagès et al. 2012). ments. Accordingly, in low-resource environments, induc- Seagrasses are important foundation species, forming ibility should be more efective and would trade-of with extensive underwater meadows that perform important constitutive resistance (Hahn and Maron 2016). However, functions and provide crucial ecosystem services. Due to some plant species inhabiting high resource environments, their high primary productivity and structural complexity, such as tropical forests, do not bear high herbivory rates and they provide food and shelter for many marine species (Jack- thus, the predictions of the intraspecifc RAH may not be son et al. 2015) and they protect the shore against coastal applicable (Lamarre et al. 2012). Similarly, high resource erosion, stabilize the substrate, and increase water clarity availability should also allow plants to better tolerate and/or (Nordlund et al. 2016). These marine systems in temper- compensate herbivory. In this regard, the Limiting Resource ate regions are undergoing an increase in herbivore pres- Model (LRM; Wise and Abrahamson 2005) states that a sure due to the expansion of tropical species (Vergés et al. plant will become more tolerant when the availability of 2014; Hyndes et al. 2016) that, together with the predicted resources, including limiting resources, increases. However, increase in herbivore feeding rates resulting from higher when herbivory damage afects the use or acquisition of an seawater temperature (Carr and Bruno 2013), may increase alternate resource, plants under high resource availability the grazing pressure in seagrass meadows. In addition, the will not increase their investment in tolerance (Hay et al. commonly observed increases in nutrient concentrations 2011; Hattas et al. 2017). Regarding marine macrophytes in coastal waters (Smith
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