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Ant-Pollinator Conflict Results in Pollinator Deterrence but No Nectar Trade-Offs', Frontiers in Plant Science, Vol Edinburgh Research Explorer Ant-Pollinator Conflict Results in Pollinator Deterrence but no Nectar Trade-Offs Citation for published version: Villamil Buenrostro, N, Boege, K & Stone, GN 2018, 'Ant-Pollinator Conflict Results in Pollinator Deterrence but no Nectar Trade-Offs', Frontiers in plant science, vol. 9. https://doi.org/10.3389/fpls.2018.01093 Digital Object Identifier (DOI): 10.3389/fpls.2018.01093 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: Frontiers in plant science Publisher Rights Statement: Copyright © 2018 Villamil, Boege and Stone. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 30. Sep. 2021 ORIGINAL RESEARCH published: 14 August 2018 doi: 10.3389/fpls.2018.01093 Ant-Pollinator Conflict Results in Pollinator Deterrence but no Nectar Trade-Offs Nora Villamil 1*, Karina Boege 2 and Graham N. Stone 1 1 Ashworth Laboratories, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom, 2 Instituto de Ecología, Departamento de Ecología Evolutiva, Universidad Nacional Autónoma de México, Mexico City, Mexico Direct and indirect negative interactions between ant guards and pollinators on ant-plants are expected for two reasons. First, aggressive ants may deter pollinators directly. Second, pollinators benefit from plant investment in reproduction whilst ants benefit from plant investment in indirect defense, and resource allocation trade-offs between these functions could lead to indirect conflict. We explored the potential for ant-pollinator conflict in a Mexican myrmecophile, Turnera velutina, which rewards ants with extrafloral nectar and pollinators with floral nectar. We characterized the daily timing of ant and pollinator activity on the plant and used experiments to test for direct and indirect conflict between these two groups of mutualists. We tested for direct conflict by quantifying pollinator responses to flowers containing dead specimens of aggressive ant species, relative to unoccupied control flowers. We assessed indirect conflict by testing for the existence of a trade-off in sugar allocation between ant and pollinator rewards, evidenced Edited by: Massimo Nepi, by an increase in floral nectar secretion when extrafloral nectar secretion was prevented. University of Siena, Italy Secretion of floral and extrafloral nectar, activity of ants and pollinators, and pollen Reviewed by: deposition all overlapped in daily time and peaked within the first 2 h after flowers opened. Kleber Del-Claro, Federal University of Uberlandia, Brazil We found evidence of direct conflict, in that presence of ants inside the flowers altered Rubén Torices, pollinator behavior and reduced visit duration, although visit frequency was unchanged. Estacion Experimental de Zonas We found no evidence for indirect conflict, with no significant difference in the volume Aridas (EEZA), Spain or sugar content of floral nectar between control plants and those in which extrafloral *Correspondence: Nora Villamil nectar secretion was prevented. The presence of ants in flowers alters pollinator behavior [email protected] in ways that are likely to affect pollination dynamics, though there is no apparent trade- off between plant investment in nectar rewards for pollinators and ant guards. Further Specialty section: This article was submitted to studies are required to quantify the effect of the natural abundance of ants in flowers on Functional Plant Ecology, pollinator behavior, and any associated impacts on plant reproductive success. a section of the journal Frontiers in Plant Science Keywords: Turnera velutina, ant-plant, floral nectar, extrafloral nectar, resource allocation, indirect interactions, Myrmecophily Received: 20 April 2018 Accepted: 05 July 2018 Published: 14 August 2018 INTRODUCTION Citation: Villamil N, Boege K and Stone GN (2018) Ant-Pollinator Conflict Results Extrafloral nectaries, domatia, and food bodies are all means by which ant-plants (comprising in Pollinator Deterrence but no Nectar myrmecophiles and myrmecophytes) (Rosumek et al., 2009; Del-Claro et al., 2016) attract and Trade-Offs. Front. Plant Sci. 9:1093. support ants by providing nesting sites or nutrients (Rico-Gray and Oliveira, 2007; Rosumek et al., doi: 10.3389/fpls.2018.01093 2009). In return, ants attack herbivores, prune climbing vines and prevent fungal and microbial Frontiers in Plant Science | www.frontiersin.org 1 August 2018 | Volume 9 | Article 1093 Villamil et al. Ant-Pollinator Conflict: Deterrence but no Nectar Trade-Offs infestation on plant tissues (Bentley, 1977; Rosumek et al., 2009). Malé et al., 2012). Such castrating behavior inevitably reduces This mutualistic interaction is termed myrmecophily. availability of flowers and hence floral rewards for pollinators. Interactions involving two or more types of mutualists of a It has been suggested that the ultimate cause of castration by single host are common in nature, but multispecies interactions patrolling ants is promoting reallocation of plant resources from are much less studied than pairwise and intraguild mutualisms reproduction to growth (Yu and Pierce, 1998; Frederickson, (Strauss, 1997; Tscharntke and Hawkins, 2002; Strauss and 2009; Malé et al., 2012), and hence increases the availability of Irwin, 2004; Adler, 2008; Melián et al., 2009; Koptur et al., resources on which ant colonies depend. In ant species that are 2015). To date, most research on plant-animal interactions has obligate inhabitants of ant-plants, colony size is limited by the focused on pairwise relationships (e.g., plant-herbivore, plant- number of domatia (Fonseca, 1993, 1999; Orivel et al., 2011), pollinator, plant-fungus) in isolation from the community in which is positively correlated with plant investment in growth. which they are embedded (Strauss, 1997; Herrera, 2000; Dáttilo Consequently, resource allocation strategies toward these two et al., 2016; Del-Claro et al., 2018). This pairwise approach mutualists should be approached in a linked way because plant necessarily oversimplifies reality (Herrera, 2000) since plants investment toward growth may come at the cost of investment to interact sequentially or simultaneously with each of pollinators, reproduction, and vice versa. And so, plant investment in rewards herbivores, herbivore predators and pathogens (Armbruster, for each mutualist reward may be affected, either positively 1997). Furthermore, plant interactions with one partner or via linkage, or negatively via trade-offs. Furthermore, because guild can also affect relationships with other groups or guilds plants interact with both mutualists simultaneously the presence (Armbruster, 1997) and alter outcomes from mutualistic to of one mutualist may increase or decrease presence of the antagonistic (Strauss, 1997; Strauss et al., 1999; Herrera, 2000; other. Strauss and Irwin, 2004; Del-Claro et al., 2016). As a result, a Even in those species that do not castrate their host, growing number of studies are focusing on multispecies and ants’ aggressive behaviors might threaten and deter pollinators, multitrophic interactions (Melián et al., 2009; Fontaine et al., compromising plant reproduction (Ness, 2006; Assunção et al., 2011; Nahas et al., 2012; Pineda et al., 2013; Dáttilo et al., 2014; LeVan et al., 2014). Avoidance of such direct conflict has 2016). It might be expected, for example, that the presence of been suggested to explain plant architecture or behaviors that predatory ants can influence pollinators, with top-down effects reduce spatial (Raine et al., 2002; Malé et al., 2015; Martínez- on plant fitness. This makes ant-plants, which rely on ants for Bauer et al., 2015) or temporal overlap of ant guards and defense against herbivores and on pollinators for seed set, a pollinators (Gaume and Mckey, 1999; Gaume et al., 2005; Nicklen model tritrophic system in which to explore the dynamics of and Wagner, 2006; Ohm and Miller, 2014; Malé et al., 2015), multispecies and multitrophic interactions. and the presence of ant-repelling compounds which exclude ants Here, we focus on disentangling ant-pollinator interactions from flowers when pollen is released (Junker et al., 2007; Willmer that occur when both mutualists share a host plant. Previous et al., 2009; Ballantyne and Willmer, 2012). work has revealed evidence of ant-pollinator conflict in such Extrafloral nectar is a key resource mediating multispecies systems (Yu and Pierce, 1998; Stanton et al.,
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