Seasonal Shifts in Macronutrient Preferences in Supercolonies of The

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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 environment. 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 important 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, Cryptocarya nitens, supercolonies (O’Dowd et al. 2003; Abbott 2005; Thomas Hernandia ovigera, Inocarpus fagifer, Pisonia umbellifera, et al. 2010), where it eliminates endemic red land crabs (a Planchonella nitens and Syzygium nervosum. keystone species: Gecarcoidea natalis) causing rapid changes This study was conducted in 2000–2002, when super- in the composition and structure of rainforest (O’Dowd et al. colonies of A. gracilipes were widespread across the island 2003). The density of worker ants in supercolonies can reach (Abbott 2006; Green & O’Dowd 2009). Thirty-four super- 2254 foraging ants/m2 (Abbott 2005), and comparative colonies varying in spatial extent from less than 1 ha to more (O’Dowd et al. 2003, K Abbott unpubl. data 2002) and experi- than 500 ha occupied a total area of more than 2500 ha in mental studies (S Wittman et al. unpubl. data 2012) indicate September 2002 (Fig. 1). Reproductive phenology was studied that these extraordinary densities are facilitated by mutualistic at six supercolony sites, all characterised by extremely high associations with honeydew-producing scale insects, mostly in densities of A. gracilipes workers foraging on the forest floor the canopy of rainforest trees. Most of the proteinaceous intake (>800 ants/m2, Abbott 2005), the absence of red land crabs, in supercolonies is in the form of small litter invertebrates, but widespread seedling recruitment and a relatively thick layer of the annual breeding migration of red land crabs (Hicks 1985) leaf litter. © 2014 Australian Entomological Society Reproduction and food choice of YCA 339

Fig. 1. Study sites on Christmas Island, Indian Ocean. The asterisks indicate 0.25-ha plots, within which all data were collected. Three letter codes are site names used throughout the text.

Table 1 Weights of various life stages Reproductive phenology Life stage Individual (mg) We monitored brood production of A. gracilipes at these six sites from December 2000 to December 2002 (Fig. 1). Yellow Egg masses 0.01† Queen larvae 11.64† crazy ants readily colonise artificial domiciles that can be Other larvae 0.93† harvested from the field for observation of colony composition Queen pupae 23.90† representative of the more fragmented naturally occurring colo- Worker pupae 1.57 nies in the surrounding environment (Vander Goot 1916; Baker Workers 0.87 1976). In each plot, 60 black polyethylene pipes (‘polypipes’; Males 1.79 Dealate queens 33.34 200 mm long, 40 mm diameter) were placed on the ground at Alate queens 33.34 randomly selected locations on 50 m × 50 m grid with intersec- tions at 5-m intervals. The polypipes were capped at one end, †Indicates values taken from Baker (1976), all other values from this study. and small amounts of leaf litter and soil were placed inside to facilitate colonisation byYCA.After 2 months, we commenced collecting five tubes per month from each plot (total 30 tubes Investment of colony resources: each month) to monitor reproduction. Often, there were fewer workers vs. reproductives than five tubes colonised by A. gracilipes. We collected up to five colonised tubes at each site and replaced them so that Colony foraging dynamics may be dictated by temporal vari- artificial nest density remained constant. Occupied tubes were ation in investment of resources to the most abundant castes. selected at random, collected into plastic bags and then frozen Abundance data were converted to standing biomass using until processing. Nine life stages were counted: egg masses, stage-specific masses derived from both this study and from queen larvae, other larvae, queen pupae, other pupae, workers, Baker (1976) (Table 1). At each sampling date, we used the males, dealate queens and alate queens. The mean number of sum of eggs, worker larvae and worker pupae biomass as a individuals in each life stage was calculated using site averages proxy for colony investment to workers, and the sum of queen (up to n = 5 pipes/site) as replicates. Rainfall was recorded at larvae and queen pupae biomass as a proxy for colony invest- Christmas Island airport at 261 m ASL. ment in gynes. We did not include male biomass as their © 2014 Australian Entomological Society 340 K L Abbott et al. presence did not imply that it was their natal nest and their pooled across four or five platforms on each sampling date. contribution to biomass was miniscule. The few sampling dates on which n < 40 were not included in analyses. Food preference

We used food stations to monitor seasonal changes in recruit- RESULTS ment to carbohydrate or protein-rich sources. A food station consisted of an elevated plastic feeding platform Reproductive phenology (10 cm × 8 cm) supported 8 cm above the ground on a steel peg onto which approximately 5 g of both protein-rich (Black Egg masses, workers, worker larvae and worker pupae of & Gold™ tuna/sardine cat food) and carbohydrate-based (fruit A. gracilipes were present in artificial nests all year round, and conserve) were placed at each end of the platform. A narrow adult workers consistently made up over 50% of nest contents plastic ramp at the middle of one edge connected the platform despite their numbers probably being underestimated in the to the ground, and we ensured that this was only point of tubes because most workers would likely be out foraging access by placing a sticky band of Tanglefoot® on the peg (Fig. 2a–d). A. gracilipes workers were often found in the beneath the platform. This design forced worker ants ascend- tubes with only worker larvae and pupae, especially during the ing the ramp to make a choice between food types. Cat food is dry season. Pupae were also found piled up in hollows of litter commonly used in field experiments or collections of ants as a or on leaves on the ground, where workers moved them around protein-rich source (Agosti et al. 2000). Five food stations per continuously. site were used on each sampling date (occasionally four sta- Sexual brood were produced annually, commencing just tions if one malfunctioned), and the number of ants at each prior to the onset of the wet season (Fig. 2e–h). At all sites and food type was recorded after 30 min. Food preference was in both years, we detected males in polypipes commencing in ± monitored weekly at two sites initially (ECR and WAD), and a October, with a peak of 35 12 males per tube (range 3–70, = ± = third (WBT) when the supercolony at WAD collapsed (see n 6) in 2001 and 15 9 per tube (range 0–42, n 5) at one Abbott 2005). At ECR (Fig. 1), observations were made on 61 site only in 2002. The production of males was followed by occasions between February 2001 and November 2002; at the presence of queen larvae, queen pupae, then dealate WAD, observations were matched with ECR until June 2002. (unwinged) queens. There was a conspicuous absence of a Observations at WBT were from August to November 2002. peak of alate (winged) queen production in tubes after queen Rain reduced the numbers of ants that were present on the larvae and pupae were produced. Although dealate queens platforms, and during heavy rains, either baits were washed off were found in all nests throughout the year, their numbers the stations or ants did not recruit to the baits at all. Data were peaked at the end of the 2002 wet season (Fig. 2h; mean ± = not recorded on these occasions. 17 16 queens per tube; range 0–98, n 6). Males were not Although decisions by ants of what type of food to collect seen in any supercolonies from March through to August and when to collect it are driven by both internal and external (except one male at site 1 in April 2002). Single alate queens factors (Cook et al. 2010 and references therein), for analysis, were found infrequently in tubes throughout the year, but it we considered the presence of a worker ant at one or the other was not determined if these queens had newly emerged or food type an independent sampling event. If workers show no were producing brood, or had been inseminated at all. choice, the null expectation would be an even split of workers visiting the two food types, i.e. a proportion of 0.5 at both. We Investment of colony resources: used the normal approximation to the binomial distribution to workers vs. reproductives test for significant departures from this proportion and In supercolonies, A. gracilipes consistently directed most regarded such departures as evidence of ‘preference’ for one colony resources to the production of workers. The mean food type or the other. Critical values of pE, the expected biomass of worker eggs, larvae and pupae varied aseasonally proportion of all ants on the platforms recorded at the throughout the study, between 42 ± 7 mg/pipe/site ± proteinaceous food source (0.5), were calculated as 0.5 E, (mean ± SE) and 447 ± 90 mg/pipe/site (Fig. 2e). Queen = √ where E Z/(2 n). Here, n is the total number of ants at both larvae and queen pupae were completely absent in pipes for food types, and Z takes a value determined by central tendency half the surveys, and when present, their mean biomass varied = theory to reflect a given confidence level. We used Z 1.9599 between a 0.03 ± 0.03 and 36 ± 25 mg/pipe/site. Using (i.e. almost two standard deviations), providing 95% confi- biomasses summed across multiple monthly sampling at each dence intervals of pE against which to compare the observed site, most resources were invested in the production of workers proportion of ants at the protein food source, pO.IfpO fell (98% at ECR, 99% at JAM, 99% at PUM, 99% at WAD, 93% − + between 0.5 E and 0.5 E, then we concluded the propor- at WBT and 99% at WCR; see Fig. 1 for site numbers). tion of ants at protein was not significantly different to the null expectation and concluded that ants showed no preference. If Food preference pO > 0.5 + E, we concluded the ants showed a preference for protein, and if pO < 0.5 − E, we concluded a preference for On most sampling occasions foraging workers of A. gracilipes carbohydrate. Both n and pO were calculated from ant counts rapidly recruited to food stations in large numbers. At ECR, © 2014 Australian Entomological Society Reproduction and food choice of YCA 341

Fig. 2. Brood production in Anoplolepis gracilipes on Christmas Island between December 2000 and November 2002. Monthly values are the mean number of individuals of that life stage per site (n = 6) and in (e) biomass of worker eggs, larvae and pupae (solid line), and gyne larvae and pupae (dashed line). Monthly rainfall for those months in which the study was carried out was taken from Bureau of Meteorology data, recorded at the airport on Christmas Island (j). Shaded regions indicate rainy months.

Fig. 3. Seasonal preferences for carbohydrate- and protein-rich food types in supercolonies of A. gracilipes between February 2001 and November 2002. There were 64 food preference trials at intervals of 1–4 weeks (mostly one or two). At any one survey, there were four or five food stations per site, but these were pooled for analyses. Trial dates were analysed individually. Each test compared the number of ants visiting carbohydrate against a model where ants make random choices (no preference). Solid bars indicate sampling dates where ants showed a statistically significant preference for one food type over another (i.e. a departure from a 50/50 split of all ants found on the food stations. The y-axis is the ratio of the number of ants found on one food type vs. the other, and effectively shows the mag- nitude of the preference. Arrows indicate trial dates on which no significant preference was detected. Other trial dates without blue bars and without arrows indicate dates on which the total number of ants recorded at food stations was not sufficient for analyses (n < 40). WAD was replaced with WBT in July 2002. the median number of ants per food station was 91 after 30 min surveys from mid-June to late November 2002 foraging ants (range 0–228, n = 281 counts pooled across dates); at WAD, it again showed a significant preference for protein, which was 61 (range 0–201, n = 188); and at WBT, it was 22 (range was particularly strong (≥3:1) in late September to early 0–131, n = 55). November. Foraging workers at ECR showed distinct patterns of food Broadly similar patterns were observed at WAD and WBT preference that were broadly aligned with the wet and dry (Fig. 3b). During the dry season of 2001 (mid April to Decem- seasons (Fig. 3a). The commencement of the 2001 dry season ber), foraging ants showed an even ratio of no preference (8/26 in April marked the start of a period lasting until the start of surveys), preference for carbohydrate (9/26 surveys) or pref- October when ants either foraged without preference (8 of 22 erence for protein (9/26 surveys) but not in any obvious tem- surveys), or more commonly (14 of 22 surveys), showed a poral pattern. However, during the following wet season preference for proteinaceous food. However, the preference (January–April 2002) foragers showed a preference for carbo- for protein was usually modest and rarely exceeded 2:1. For- hydrate in all surveys (8/8 surveys). Just as at ECR, in most agers did not show a preference again until late November surveys where preference was shown, it was relatively modest, 2001, at which time they switched to a preference for carbo- but the extreme preference for carbohydrate in the last four hydrate in all wet season surveys (11/11 surveys) to mid-April surveys at WAD just before the supercolony declined com- 2002. Again, the strength of the preference was usually pletely (8:1 in late March, 31:1 in mid-April, 57:1 in late April modest but occasionally exceeded 2:1. The wet season fin- and 56:1 in early June 2002) is notable. Dry season sampling ished in April 2002, and in almost all (18/20) dry season was continued at WBT from mid-September through the end © 2014 Australian Entomological Society Reproduction and food choice of YCA 343 of November 2002, during which time foragers showed a food artificial nest data. In the following wet season, we recorded preference in 9 of 11 surveys, 8 of which were for protein. alate queens and winged males together in canopy malaise traps at the WBT site over the week leading up to 25 January 2002, almost 2 months after the wet season began on 2 Decem- DISCUSSION ber 2001 (Abbott 2006). These observations suggest the occur- rence of mating flights over the duration of the wet season. Phenology However, mating flights have not been recorded in this species, The reproductive phenology of A. gracilipes on Christmas and the dissections of ovaries from these collections have been Island is very similar to patterns observed at other sites with inconclusive as to the timing of mating (C Vanderwoude pers. highly seasonal rainfall, including Indonesia (Van der Goot comm. 2005). In contrast with the highly seasonal nature of 1916), Solomon Islands (Greenslade 1971a,b), Papua New sexual brood production, egg masses, worker larvae and pupae Guinea (Baker 1976), Seychelles (Haines & Haines 1978) and were present in artificial nests year-round with no obvious India (Rao & Veeresh 1991). At all these locations, the pro- seasonal peaks. This is consistent with the aseasonal produc- duction of sexual brood coincides with the transition from the tion schedule for workers found by Haines and Haines (1978) dry to the wet season (see Fig. 4 for details). On Christmas in the Seychelles but differs to the obviously seasonal produc- Island, males were first detected in artificial nests in October, tion of workers in New Guinea (Baker 1976) and the Solomon just before the first rains of the wet season reached peak Islands (Greenslade 1971b) during the rainy season. abundance in November and December, and were largely The wet season on Christmas Island usually occurs from absent by January. Very few alate queens were found in arti- December through to May, but during this study, the wet ficial nests, but half of these were recorded in November and seasons in both 2000/01 and 2001/02 commenced in January December, coincident with males. Alate males were also and finished by April. Observations in the Seychelles suggest recorded in canopy malaise traps at WCR and WBT on that most natural nests typically contained between 27 and 56 29 January 2001 and at ECR on 8 February 2001 (PT Green queens (based on 95% CI; Haines & Haines 1978). On Christ- & DJ O’Dowd unpubl. data 2004), later than indicated by the mas Island, we observed much lower numbers in the artificial

Fig. 4. A comparison of A. gracilipes male, alate and dealate queen phenology between five studies in various locations. Heavy lines indicate the time when most individuals were recorded, and dotted lines indicate the presence of low number of individuals. The wet season is shown in grey and dry season either side. Sources: Indonesia – Van der Goot 1916; Papua New Guinea – Baker 1976; Solomon Islands – Greenslade 1971; Seychelles – Haines & Haines 1978; India – Rao & Veeresh 1991; Christmas Island – this study. © 2014 Australian Entomological Society 344 K L Abbott et al. polypipe nests (Fig. 1), and implicit in this study is the production. The density of workers in supercolonies is con- assumption that colonies in artificial domiciles are represent- sistently and exceptionally high year-round (Abbott 2005) ative of the more fragmented natural colonies (Van der supported by the continuous production of worker brood (this Goot 1916). The only component not accurately represented study). Given this, there must be a consistently high demand at the time of sampling was the total number of workers for both carbohydrate resources to sustain foragers and associated with each nest (Baker 1976). But in natural nests, enhance colony growth (Wilder et al. 2011), and protein-rich queens were more abundant (K Abbott pers. obs. 2002), and resources to sustain larvae and worker brood production by occasionally, we found more than 1000 queens in single queens. Any increased demand for protein coincident with nests; ‘super-nests’ appeared to be relatively common in sexual brood production during the wet season would be a A. gracilipes supercolonies in and under large dead tree trunks tiny fraction of colony demand and would not be detectable and logs on the ground. against the demands associated with worker brood production. A single sexual brood production event has significant The marked seasonality in feeding preferences for comple- implications for the rate of spread of A. gracilipes.Over- mentary resources shown by A. gracilipes in supercolonies crowding of queens in a nest might cause inseminated queens is therefore remarkable and could be driven by relative avail- to leave the nest in polygynous colonies (Hölldobler & Wilson ability in the environment (Kay 2003) rather than by colony 1990). If this is the case, an increase in the number of queens dynamics per se. produced in one nest could increase the rate of movement of This view is supported by the low abundance of litter inver- queens out of the nest and increase the rate of boundary expan- tebrates during the dry season on Christmas Island (Green sion of supercolonies. On Christmas Island, however, such a et al. 1999), similar to patterns in other seasonal forests in the boundary expansion was not observed. During the period from neotropics (Levings & Windsor 1982) and in Australia (Frith November through March, supercolony boundaries were & Frith 1990). Although stand-level production of honeydew either static or contracted (2001 and 2002, respectively; in YCA supercolonies has not been measured on Christmas Abbott 2006). The most rapid rate of supercolony expansion Island, it is likely to be lowest during the wet season; the was during the dry season when sexual brood was not pro- abundance of adult honeydew-producing scale insects is duced, indicating that overcrowding of nests might not be a lowest at this time (G Neumann unpubl. data 2011). Even if reason for an inseminated queen to leave the nest. Rather, it is stand-level honeydew production is aseasonal, its availability more likely that at times of peak forager activity, they accom- to foraging YCA workers could still be highly seasonal pany inseminated queens to new nest sites in areas of increased because heavy rain during the wet season would wash much of food resources, namely honeydew from canopy-dwelling scale it away. insects (Abbott & Green 2007). Alternatively, in the wet It is likely that these seasonal shortages in protein and car- season when protein is abundant, there is little need for forag- bohydrate explain most of the temporal variation in food pref- ers to travel in order to fulfil their protein requirements, so erences by A. gracilipes workers during the study. In any case, queens simply find a new nest site close by. In the dry season the shift away from proteinaceous food occurred just when foragers must travel greater distance to discover protein queens began producing sexual brood just before the start of sources, thereby expanding boundaries, taking queens with the wet season. When considered in this way, the greater-than- them and forming new colonies outside the original expected recruitment to food types in this study may not be a supercolony. preference as such but a measure of foraging effort necessary to gain the required amount of protein and carbohydrate to maintain optimal colony functioning (Dussutour & Simpson Colony investment and food preference 2008, 2012; Cook et al. 2011). This is a more qualitative At high densities in supercolonies, A. gracilipes invests a behavioural trait that has been used to assess the availability of large proportion of colony resources to worker brood relative resources to ants (Kay 2002). to queens. We used the sum of egg masses, worker larvae and The extreme preference shown by workers of A. gracilipes worker pupae as a proxy for colony investment to worker for carbohydrate-based food resources at WAD, but not at production, and the biomass of queen larvae and pupae as the ECR, during the latter part of the 2001/02, wet season is same proxy for investment in queens. Differences in the devel- noteworthy and might aid in future investigation of nutrient opmental times of workers and queens, and the omission of regulation strategies in booming and busting populations of males from these calculations, make these proxies an imper- ants. At most times when there was a preference for carbohy- fect estimate of colony investment in workers vs. gynes, but drate, the ratio of workers at complementary food resources they are likely to be indicative of where most colony resources was around 2:1 to 4:1, but during March–May 2001, the ratio are invested. By biomass, we estimated that at five of six reached 57:1. This coincided with the collapse of the sites, 98% or more of the biomass of immature stages was in supercolony at WAD, with ant density declining almost to nil future worker ants. Similar calculations using data in table 2 by May (Abbott 2005). In all likelihood, supercolony collapse of Baker (1976) yield 93% at his rainforest site in New was driven by a precipitous decline in the density of Guinea. honeydew-producing scale insects, which created an extreme On Christmas Island, there is no obvious reason to expect a scarcity of carbohydrate resources and led to colony decline seasonal shift in food preferences to cater for sexual brood (Wilder et al. 2011). © 2014 Australian Entomological Society Reproduction and food choice of YCA 345

The seasonal shift in recruitment to food types has not been of reproductive phenology and seasonal food preference is well-studied in other locations where A. gracilipes forms likely to play a pivotal role in designing effective control supercolonies. Similar to this study, Haines and Haines (1978) programs for invasive ants. found that most colony investment in the Seychelles was directed to the production of workers (75% by biomass), and that because adult and brood were produced throughout the ACKNOWLEDGEMENTS year leading, they thought there should be aseasonality in food requirements. In the Solomon Islands, Greenslade (1971b) Kent Retallick and Lin Gaff helped with fieldwork. The work noted that occupancy by A. gracilipes in coconut palms har- was funded by an ARC-LINKAGE Grant to DJO and PTG bouring honeydew producers fell during the wet season, which between Monash University and Environment Australia. he interpreted as a shift to searching for prey in the ground layer as it became more abundant under wet conditions. In New Guinea, Baker (1976) was unable to determine if the wet REFERENCES season peak in sexual brood production was associated with a change in food preference or changes in forager efficiency or Abbott KL. 2005. Supercolonies of the invasive yellow crazy ant, intensity. Anoplolepis gracilipes, on an oceanic island: forager patterns, density The idea that ants can change their foraging tactics accord- and biomass. Insectes Sociaux 52, 266–273. Abbott KL. 2006. Spatial dynamics of supercolonies of the yellow crazy ing to changing resource abundance and distribution in order ant, Anoplolepis gracilipes, on Christmas Island, Indian ocean. 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