The Influence of Host Plant Extrafloral Nectaries on Multitrophic Interactions: An Experimental Investigation

RESEARCH ARTICLE The Influence of Host Plant Extrafloral Nectaries on Multitrophic Interactions: An Experimental Investigation Suzanne Koptur1*, Ian M. Jones1, Jorge E. Peña2 1 Department of Biological Sciences, Florida International University, Miami, Florida, United States of America, 2 Tropical Research and Education Center, University of Florida, Homestead, Florida, United States of America * a11111 OPEN ACCESS Citation: Koptur S, Jones IM, Peña JE (2015) The Influence of Host Plant Extrafloral Nectaries on Multitrophic Interactions: An Experimental Investigation. PLoS ONE 10(9): e0138157. doi:10.1371/journal.pone.0138157 Editor: Anna R. Armitage, Texas A&M University at Galveston, UNITED STATES Received: May 14, 2015 Accepted: August 25, 2015 Published: September 22, 2015 Copyright: © 2015 Koptur et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All arthropod census data and caterpillar rearing files are available from the Dryad database: doi:10.5061/dryad.47ct0. Abstract A field experiment was conducted with outplantings of the native perennial shrub Senna mexicana var. chapmanii in a semi-natural area adjacent to native pine rockland habitat in southern Florida. The presence of ants and the availability of extrafloral nectar were manipulated in a stratified random design. Insect communities were monitored and recorded over a period of six months with a view to addressing three main questions. Do ants provide biotic defense against key herbivores on S. chapmanii? Is the presence of ants on S. chapmanii mediated by EFN? Finally, are there ecological costs associated with the presence of ants on S. chapmanii, such as a reduction in alternative predator or parasitoid numbers? Herbivores on S. chapmanii included immature stages of three pierid butterflies, and adult weevils. Eight species of ants were associated with the plants, and other predators included spiders, ladybugs, wasps, and hemipterans. Parasitic, haemolymph-sucking midges (Ceratopogonidae) and parasitoid flies were also associated with the caterpillar herbivores, and possibly the extrafloral nectaries of the plants. The presence of ants did not appear to influence oviposition by butterflies, as numbers of lepidopterans of all developmental stages did not differ among treatments. Significantly more late instar caterpillars, however, were observed on plants with ants excluded, indicating that ants remove small caterpillars from plants. Substantially more alternative predators (spiders, ladybugs, and wasps) were observed on plants with ants excluded. Rates of parasitization did not differ among the treatments, but there were substantially fewer caterpillars succumbing to virus among those collected from control plants. We provide a rare look at facultative ant-plant mutualisms in the context of the many other interactions with which they overlap. We conclude that ants provide some biotic defense against herbivores on S. chapmanii, and plants benefit overall from the presence of ants, despite negative impacts on non-ant predators. Funding: Support was provided by sabbatical leave support and a subsequent research grant to SK from the College of Arts and Sciences at FIU. Competing Interests: The authors have declared that no competing interests exist. PLOS ONE | DOI:10.1371/journal.pone.0138157 September 22, 2015 1 / 18 Extrafloral Nectaries, Ants, and the Associated Arthropod Community Introduction Extrafloral nectaries (EFNs) have been reported in 93 plant families and 332 genera [1], and may be found on almost any vegetative or reproductive plant structure [1, 2, 3, 4]. While extrafloral nectar (EFN) may be consumed by a broad range of arthropods, its discovery by ants is thought to be of greatest importance to plant defense [1, 5, 6]. While defending their resource, many ant species show territorial aggressiveness towards, or even prey on other insects that they encounter [1]. Since Thomas Belt first hypothesized the mutualism between plants and defensive ants [7], many studies have supported ants as biotic defenders of plants [6, 8, 9, 10]. Ant-plants may be placed into two categories based on their defensive strategy. Myrmecophytic plants provide nesting sites and are permanently occupied by specialized ant species, while myrmecophylic plants provide unspecialized food rewards, most commonly extrafloral nectar (EFN) or honeydew (through associations with honeydew producing hemipterans), and foster only facultative interactions with ants. While the defensive role of ants on myrmecophytic plants is well supported [8, 9, 10], the defensive benefits of EFN attracted ants have been empirically demonstrated only relatively rarely [11, 12, 13, 14]. Indeed, several studies of EFN mediated ant-plant interactions have observed neutral or even negative effects on plant fitness [15, 16, 17]. In some cases the chemical composition of EFN appears to be tailored to attract defensive ants, and discourage exploiters [18]. Many facultative mutualisms between ants and EFN producing plants, however, offer low levels of species specificity and nectar is, therefore, available to be exploited by a host of arthropods which may confer no benefits to the plant (nectar thieves), and may even deter ants [19]. For example, 14 families of Diptera and 5 families of wasps have been observed at the EFNs of Lima beans alone [20]. The importance of EFN on the biology of nonant consumers, however, has rarely been studied [21]. Ants, themselves, vary in their defensive qualities [9, 22, 23], and even the most effective ant bodyguards may not be exclusively beneficial for plants [24]. Mutualisms between plants and ants do not occur in isolation, but within a complex web of biotic interactions. In the cactus Ferocactus wislizeni, for example, plants defended by the most aggressive ants, Solenopsis xyloni, suffer reduced herbivory and produce more flowers. Those flowers, however, receive fewer and shorter visits from pollinators, deterred by the same ferocious ants [24]. Other studies have also observed that pollinators recognize the danger posed by ants [25, 26]. Assunção et al. [26] placed plastic ants on the petals of Heteropterys pteropetala. Flowers with plastic ants produced significantly less fruit than control flowers. Aggressive ants have also been observed to reduce the numbers of other beneficial insects, such as predators and parasitoids, on EFN bearing plants [6, 22]. In the EFN bearing tree, Qualea multiflora, both ants and spiders reduce herbivory rates, and an interaction effect has been observed whereby the best protected plants are those that harbor both ants and spiders. In many cases, however, ants outcompete spiders, with detrimental effects on plant defense [27]. Conflict between mutualisti (...truncated)