bs_bs_banner Austral Entomology (2014) 53, 337–346 Seasonal shifts in macronutrient preferences in supercolonies of the invasive Yellow Crazy Ant Anoplolepis gracilipes (Smith, 1857) (Hymenoptera: Formicidae) on Christmas Island, Indian Ocean Kirsti L Abbott,1*† Peter T Green2 and Dennis J O’Dowd1 1School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia. 2Department of Botany, La Trobe University, Bundoora, Vic. 3086, Australia. Abstract The timing and duration of sexual brood production in ants can affect their rate of spread and colony growth. Because protein is key to larval growth, queen survival and fecundity, macronutrient collection by foraging workers is expected to favour protein prior to and throughout gyne production. However, food preference driven by the production of gynes may be overridden by a preference associated with worker production, especially if investment in workers vastly outweighs that of sexual brood and workers are produced on different schedules. Food preferences alone may not indicate the availability of that food type in the environ- ment. On Christmas Island, Indian Ocean, sexual brood of the invasive Yellow Crazy Ant, Anoplolepis gracilipes (Smith, 1857), was produced annually during a single period associated with the onset of the wet season. However, workers were produced continuously throughout the year and colony investment to worker production measured by the standing biomass of eggs, larvae and pupae, typically exceeded 98%. High, aseasonal investment in worker production, together with aseasonal worker activity, would suggest that there should be no seasonal preference shown by workers at food stations containing both protein and carbohydrate. However, workers showed a preference for one food type over another on 46 of 61 occasions at one site and on 31 of 41 occasions at another. When a preference was shown, it was predominantly for protein-rich food during the dry season and almost always for carbohydrate at the onset and during the wet season. We suggest that these preferences reflect seasonal shortages in key resources when invertebrates (protein-rich) are scarce during the dry season and honeydew from scale insects (carbohydrate) is depleted by rain during the wet season. On Christmas Island, timing and duration of the dry season preference for protein has been exploited by the control program for A. gracilipes supercolonies, which deploys a toxin in a proteinaceous bait matrix during dry periods. Key words control program, invasive ant, life history, mutualism, seasonality. INTRODUCTION colony growth and reproduction at this time (Tobin 1995; Davidson 1997; Nation 2001) and that it is larvae present in the Life histories and mating patterns of ants can provide insight colony that increases the proportion of protein in their diet into their phenomenal ecological success (Hölldobler & (Dussutour & Simpson 2009). However, there is increasing Wilson 1990; Peeters & Molet 2010). The timing and duration evidence that carbohydrate-rich honeydew from hemipteran of sexual brood production can have significant implications mutualists can have greater benefits in terms of colony growth for colony growth, dispersal of queens, colony-founding strat- than proteinaceous insect prey (Shik & Silverman 2013). egies and rate of colony spread (Hölldobler & Wilson 1990). The food choices made by worker ants are driven by their Founding queen ants typically require large metabolic reserves individual nutritional needs, and information given to them by to sustain ovary development, egg production and larval colony members about the requirements of conspecifics in the growth at their new nest site (Brian 1973; Hölldobler & Wilson nest (Cook et al. 2010) and reproductive status of the colony 1990; Nation 2001) and are dependent upon workers to (Stein et al. 1990). Workers choose carbohydrates to fuel their retrieve these food items. It is generally nitrogen in the form of own activity and collect proteinaceous foods to either pass amino acids and proteins that is the limiting resource for onto developing larvae, the queen, other workers or to hoard for extraction when necessary (Cook et al. 2010). Recruitment to food sources depends not only on the rate of information *[email protected] transfer between workers and on recruitment strategy (Cassill †Present address: School of Environmental and Rural Science, Univer- 2003) but also on the quality, stability and perceived quantity sity of New England, Armidale, NSW 2350, Australia. of the resource (Sundstrom 1993; Kay 2002). Interpreting © 2014 Australian Entomological Society doi:10.1111/aen.12081 338 K L Abbott et al. patterns of recruitment to different food choices is complicated can provide the ants with a pulse of protein-rich food at the by other factors such as division of labour, overlapping gen- onset of the wet season if the crabs migrate through erations and foraging costs (Cook et al. 2010). The relative supercolonies that lie in their path (O’Dowd et al. 2003; Green availability of complementary resources in the environment & O’Dowd 2009; Green et al. 2011). can also affect the feeding preferences of workers (Kay 2003), An understanding of the reproductive phenology and food perhaps more so than nutritional needs of the colony. There preference of A. gracilipes may help predict population esca- can also be temporal variation in the resource requirements of lation and supercolony spread. Moreover, in areas where ant colonies; both temperate and tropical ant species have A. gracilipes has become a serious invader (Lewis et al. 1976; cyclical patterns of brood production (Stein et al. 1990; Lester & Tavite 2004; Abbott et al. 2007; Green & O’Dowd Noordijk et al. 2008; Hart & Tschinkel 2012), and the onset of 2009; Hoffmann & Saul 2010; Savage et al. 2011), life history a wet or dry season can provide strong environmental cues for knowledge can benefit conservation management by highlight- patterns of food collection and recruitment. However, little is ing when ant colonies prefer, or at least recruit, to and collect known about how the interaction between seasonality and a specific food type. The timing of a particular food preference brood production affects food choices by ants. by foraging A. gracilipes can help managers time the applica- Traditionally, the study of ant reproductive phenology has tion of a corresponding bait matrix for maximum uptake by emphasised periods during which sexuals are produced and the workers and prevent the production of sexual brood. resource demands that places on the colony as a whole and the Here, we first describe the reproductive phenology of foraging preferences of individual workers. There are older A. gracilipes in high-density supercolonies on Christmas studies that have linked periods during which brood (including Island, with particular emphasis on the timing and duration of sexuals) are produced to a notable preference for protein sexual vs. worker brood production. Second, we quantify over among foraging workers (e.g. Sorensen et al. 1983; Stein et al. time the relative investment of colony resources in the produc- 1990). However, these studies have not focused on the timing tion of workers compared with reproductive brood to determine of the production of gynes alone and linked any shift in sea- which is more likely to drive temporal variation in feeding sonal food preference with temperature rather than with any preferences by the workers of this species. Third, we document biotic variables. Food preference of S. invicta has also been forager recruitment to carbohydrate and protein-rich foods, and labelled ‘idiosyncratic’ (Glunn et al. 1981). In ant species that evaluate these patterns as a potential indicator of colony macro- form high-density supercolonies where the ratio of gynes to nutrient requirements vs. environmental availability. workers is generally low, colony food preference may be driven more by the nutritional requirements of the workers and their production schedules than by queens. In these species, METHODS AND MATERIALS the workers’ need for energy may drive recruitment to, and collection of, food types high in sugars. Carbohydrates in the Study sites form of excretory honeydew from scale insects are an impor- tant dietary component for species of invasive ants that typi- Christmas Island is an elevated oceanic limestone island that cally have high ratios of workers to gynes (Heller 2004; lies 360 km south of Java in the north-eastern Indian Ocean Abbott 2005; Helms 2013). Indeed, the five species of invasive (105°40′E, 10°30′S). This elevated (to 364 m) small island ants whose impacts are considered the most damaging have (135 km2) experiences a monsoonal climate in which most of disproportionately high numbers of workers; these species are the 2000 mm mean annual rainfall occurs between December also associated with honeydew-producing insects in their and May (Falkland 1986). Approximately 74% of the island is introduced range (Helms 2013). still covered with floristically simple rainforest; tall evergreen The invasive yellow crazy ant, Anoplolepis gracilipes, has rainforest occurs on deep soils in the higher regions of the become a widespread pest in tropical and subtropical locations island, while shorter, more deciduous forest occurs on shal- worldwide (Wetterer 2005). On Christmas Island (Indian lower soil on fringing terraces. Common tree species include Ocean), this species forms a mosaic of high- and low-density Barringtonia racemosa, Celtis timorensis,