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Colony Diet Influences Ant Worker Foraging and Attendance Of ORIGINAL RESEARCH published: 28 September 2016 doi: 10.3389/fevo.2016.00114 Colony Diet Influences Ant Worker Foraging and Attendance of Myrmecophilous Lycaenid Caterpillars Sebastian Pohl 1, 2, Megan E. Frederickson 2 †, Mark A. Elgar 1* and Naomi E. Pierce 2 1 School of BioSciences, Faculty of Science, The University of Melbourne, Parkville, VIC, Australia, 2 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA Foraging animals regulate their intake of macronutrients such as carbohydrates and Edited by: proteins. However, regulating the intake of these two macronutrients can be constrained Peter Schausberger, by the nutrient content of available food sources. Compensatory foraging is a University of Vienna, Austria method to adjust nutrient intake under restricted nutrient availability by preferentially Reviewed by: Spencer T. Behmer, exploiting food sources that contain limiting nutrients. Here we studied the potential for Texas A&M University, USA compensatory foraging in the dolichoderine ant Iridomyrmex mayri, which is commonly Konrad Fiedler, University of Vienna, Austria found in associations with caterpillars of the obligatorily ant-associated lycaenid butterfly Kleber Del Claro, Jalmenus evagoras. The caterpillars receive protection against predators and parasites, Universidade Federal de Uberlândia, and reward the ants with nutritional secretions from specialized exocrine glands. These Brazil secretions contain a mixture of sugars and free amino acids, particularly serine. We tested *Correspondence: Mark A. Elgar the influence of nutrient-deficient diets on foraging patterns in I. mayri by recording the [email protected] intake of test solutions containing single types of macronutrients during food preference † Present Address: tests. We also investigated the level of ant attendance on fifth instar J. evagoras Megan E. Frederickson, Department of Ecology and caterpillars to evaluate how changes in diet influenced ant tending of caterpillars and Evolutionary Biology, University of foraging on their secretions. Foragers on a protein diet compensated for the nutritional Toronto, 25 Willcocks Street, Toronto, deficit by increasing the intake of test solutions that contained sucrose, compared to Ontario M5S 3B2, Canada their counterparts on a non-restricted diet. Ants on a sugar diet, however, did not show a Specialty section: corresponding increased consumption of test solutions containing the amino acid serine. This article was submitted to Additionally, compared with their counterparts on a mixed diet, ants on limited nutrient Behavioral and Evolutionary Ecology, a section of the journal diets showed an increase in the number of caterpillar-tending workers, suggesting that Frontiers in Ecology and Evolution the caterpillars’ secretions are suitable to compensate for the ants’ nutritional deficit. Received: 10 June 2016 Keywords: compensatory foraging, geometric framework, nutritional status, species interaction, mutualism, Accepted: 13 September 2016 symbiosis Published: 28 September 2016 Citation: Pohl S, Frederickson ME, Elgar MA INTRODUCTION and Pierce NE (2016) Colony Diet Influences Ant Worker Foraging and Attendance of Myrmecophilous The “Geometric Framework” (Simpson and Raubenheimer, 2012) provides a compelling Lycaenid Caterpillars. theoretical approach to understanding foraging strategies, by assuming that animals have intake Front. Ecol. Evol. 4:114. targets for all relevant nutrients, and thus predicting the simultaneous regulation of nutrient doi: 10.3389/fevo.2016.00114 intake to meet particular target ratios (e.g., relative proportions of protein and carbohydrates) Frontiers in Ecology and Evolution | www.frontiersin.org 1 September 2016 | Volume 4 | Article 114 Pohl et al. Ant Foraging and Caterpillar Attendance for individual organisms (Simpson and Raubenheimer, 1993; secretions of J. evagoras show that they comprise a mixture of Raubenheimer and Simpson, 1999; Simpson et al., 2004; sugars, mainly sucrose and fructose, and up to 14 different free Raubenheimer et al., 2009). This approach has been successfully amino acids, particularly serine (Pierce, 1985; Pierce and Nash, applied to a range of species, from slime molds, through insects 1999). The secretions have yet to be analyzed for additional to humans (Raubenheimer and Simpson, 1993; Simpson et al., compounds that may also play a role in mediating interactions 2003; Behmer, 2009; Dussutour et al., 2010), and furthered the with ants (cf. Hojo et al., 2015). understanding of nutritional dynamics and trophic interactions The presence of sugars in combination with relatively high (Simpson et al., 2015). concentrations of a single amino acid in the secretions of ant- While solitary animals must satisfy their own nutritional tended lycaenid larvae raises the intriguing possibility of larvae needs, food acquisition in social insects requires a more complex providing compensatory nutrients to their tending ants that allow evaluation of specific target ratios, due to their colonial lifestyle as the colony to meet their nutrient intake targets. Providing both well as accommodating the varying nutritional needs of different proteins and carbohydrates hence may be an important feature colony members. Ant larvae, for example, require a protein- of the mutualism between ant-associated lycaenids and their based diet for successful development, whereas a sugar-based attendant ants (Wada et al., 2001; Hojo et al., 2008) because diet is sufficient for worker survival (Hölldobler and Wilson, it guarantees a more consistent reward value than a single 1990). Social insect foragers must take into account the varying nutrient. Interestingly, caterpillars of Niphanda fusca secrete high nutritional needs of different castes when searching for food, concentrations of glycine, which in combination with sugars is while also responding to potential nutrient restrictions in the extremely attractive to their host ants, Camponotus japonicus. food currently available to the colony (Seeley, 1989; Cassill Neither the sugars nor glycine are as attractive alone as when and Tschinkel, 1999a). One way to compensate for nutritional presented together, suggesting that they may act synergistically to deficits is compensatory foraging, in which workers adjust their attract C. japonicus attendant ants (Wada et al., 2001; Hojo et al., preferences in favor of food sources containing limiting nutrients. 2008). Nutrient compensatory foraging ensures that the colony meets The aim of the present study was two-fold. First we its longer-term targets and thus facilitates colony growth and investigated whether compensatory feeding occurs in the reproductive output. Evidence of nutrient compensatory foraging caterpillar-tending dolichoderine ant I. mayri. We kept ant is provided by both field and laboratory studies of honey colony fragments on either a sugar- or protein-deficient diet and bees (Hendriksma and Shafir, 2016) and several species of measured their intake of test solutions containing sucrose and/or ants, including Solenopsis invicta (Sorensen et al., 1985; Cook serine in food preference tests. We predicted that the ants would et al., 2010; Wilder and Eubanks, 2010), Rhytidoponera metallica compensate for a deficit of specific macronutrients by increasing (Dussutour and Simpson, 2008), Ectatomma ruidum (Cook and the intake of test solutions that contained the component missing Behmer, 2010), and Iridomyrmex suchieri (Christensen et al., in their diet. 2010). We then examined whether this diet conditioning influenced The Australian ant genus Iridomyrmex (Formicidae: the number of foragers of I. mayri tending caterpillars Dolichoderinae) contains numerous taxa that are ecologically of J. evagoras. We asked whether workers change their dominant, “agricultural” species that tend extra-floral nectaries tending efforts according to their colony’s nutritional state, and nectar-secreting insects such as hemipterans and the and whether such potential differences in caterpillar tending caterpillars of lycaenid butterflies. Iridomyrmex ants are depend on the respective nature of the nutritional deficit. We often found in association with caterpillars and pupae of the predicted an increase in caterpillar tending as compensation obligatorily ant-associated lycaenid butterfly Jalmenus evagoras for the ants’ nutrient-deficient diets, whether the deficiency (Braby, 2000). The ant workers provide juveniles of J. evagoras was in carbohydrates on the one hand or proteins on the with protection against parasites and predators (Pierce et al., other. 1987), and in turn are rewarded with nutritional secretions from the dorsal nectary organ, a specialized exocrine gland MATERIALS AND METHODS of the butterfly larvae, as well as from single celled epidermal glands called pore cupolae that are found in the epidermis Study Species of larvae and pupae (Kitching, 1983; Pierce and Nash, 1999). The systematics of the ant genus Iridomyrmex has been Although colonies of Iridomyrmex attendant ant species occur problematic for many years (Heterick and Shattuck, 2011; in the absence of J. evagoras and do not depend exclusively on Andersen et al., 2013), and this is reflected in the identification of lycaenids for nutrition (Pierce et al., 1987; Smiley et al., 1988), ants associated with Jalmenus evagoras. The species of ants used the secretions can account for a considerable proportion of in this study were identified by Bob Taylor at CSIRO initially the overall food intake of an ant colony whose workers tend
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