Myrmecological News 13 57-71 Vienna, April 2010
A masterpiece of evolution – Oecophylla weaver ants (Hymenoptera: Formicidae)
Ross H. CROZIER†, Philip S. NEWEY, Ellen A. SCHLÜNS & Simon K.A. ROBSON
Abstract Oecophylla species are among the most iconic tropical ants, but a broad review of their biology has been lacking. The two living species of Oecophylla are widespread in the Old World tropics and are similar in presenting the most sophisticated nest-building activities of all weaver ants. Workers draw leaves together, often forming long chains, and glue them together with larval silk. Chain formation promises to provide a major subject for the development of models of the self-organization of complex behavior. The colonies are very large and highly polydomous. Queens are pre- dominantly though not exclusively once-mated and colonies are usually single-queened, but most Northern Territory (Australia) colonies are polygynous. The workers are highly polymorphic (seen also in a fossilized colony), show complex polyethism, and present a much-studied rich pheromonal repertoire for the colony's tasks. Colony odor is partly learned, showing a "nasty neighbor" effect in reactions to other colonies of this highly territorial ant, and partly intrinsic to each individual. The odor varies over time and differs between the nests of a colony. Not surprisingly, Oecophylla ants are hosts to a variety of inquilines, such as spiders, which mimic the colony odor to escape detection. In addition, a con- stellation of Homoptera benefit from ant protection, yet the activities of the ants in controlling pest species make these ants beneficial insects (they are also human food in some areas). We speculate that the existence of Oecophylla blocks other weaver ants from evolving highly complex social organization, an idea which could be tested with further knowl- edge on the timing of ant adaptive radiations. Key words: Weaver ants, Oecophylla, self-organization, insect sociobiology, biogeography, colonymate recognition, nest- building, colony genetic structure, polygyny, polyandry, economic significance, review. Myrmecol. News 13: 57-71 (online 21 December 2009) ISSN 1994-4136 (print), ISSN 1997-3500 (online) Received 26 August 2009; revision received 7 October 2009; accepted 9 October 2009 Prof. Dr. Ross H. Crozier†, Dipl. Biol. Ellen A. Schlüns (contact author) & Dr. Simon K.A. Robson, School of Marine & Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia. E-mail: [email protected] Dr. Philip S. Newey, School of Marine & Tropical Biology, James Cook University, Cairns, Queensland 4870, Australia.
Introduction
Ant researchers working in the Old World tropics will be where R is average annual rainfall in mm and Tmin is the familiar with weaver ants of the genus Oecophylla, justly mean minimum temperature in °C. Global warming is like- described as one of the four pinnacles of ant social evolu- ly to lead to an expansion of the Oecophylla ranges. tion (HÖLLDOBLER & WILSON 2009). By reviewing the Their prominent leaf nests (Fig. 2), glued ("woven") current state of research concerning these ants, we hope to together with silk from the larvae, can readily be seen on highlight their importance for understanding the evolution many trees in open and closed forests, and their large col- of ants and of sociality in general. By identifying the gaps ony sizes (often over 500,000 workers, LOKKERS 1990), in our current knowledge, we seek to provide some direc- polydomy, territoriality (HÖLLDOBLER & LUMSDEN 1980) tion for future research on this important genus. The two and aggressive defenses make them hard to ignore. As we currently recognised species (BOLTON & al. 2007) have very detail further below, aspects such as the high degree of co- extensive ranges (Fig. 1) – O. longinoda occurs in a wide operation required to build the leaf nests, the three-dimen- band across equatorial Africa, and O. smaragdina occurs sional colony territories, huge colony sizes, and their ex- in Sri Lanka and much of India through Indo-China and tensive chemical repertoires make the species major sub- southern China to the Indomalayan region, northern Aus- jects for evolutionary and ecological studies. tralia and Melanesia (COLE & JONES 1948). Oecophylla We sound a note of caution as to how many species of smaragdina has been the more intensively studied species, Oecophylla there are. Two are currently recognized, but with but as will become clear during our review O. longinoda eight subspecies for O. longinoda and six for O. smarag- is better known for some aspects. LOKKERS (1986, 1990) dina, see BOLTON & al. (2007). In addition to the morpho- noted that in Australia their distribution is bounded joint- logical variation implied by the recognition of subspecies, ly by temperature and humidity, and provided a formula there is considerable variation between reports from the said to hold for other regions as well, namely that the same species in such matters as the propensity to thelytoky boundary to suitable territory is given by: (parthenogenesis in which females produce exclusively fe- 4 .26 * log(R) + 23.5 * log(Tmin) – 42.4 = 0 male offspring without fertilization, WHITE 1973), together
Fig. 1: Distributions of the two currently-recognized species of Oecophylla, and fossil sites (numbered, some numbers cover two nearby sites), from DLUSSKY & al. (2008), after LOKKERS (1986), by permission. Sympatric pairs of fossil species have been found twice – O. brischkei and O. crassinoda in the Eocene (Baltic amber, site 1) and O. atavina and O. megarche in the Oligocene (Isle of Wight, site 2), whereas the extant species are allopatric. Site 7 is where the fossil nest of O. leakeyi was found.
Fig. 2: A leaf-nest of Oecophylla smaragdina, Cape Tribulation, North Queensland, Australia. Photo court- esy Alex Wild/myrmecos.net. with, in O. smaragdina, marked phylogeographic structure If Oecophylla species have an impressive present and (AZUMA & al. 2006) and big differences in microsatellite their study a glorious future, they also have a rich past. allele frequencies between Australia and Java (E.A. Schlüns, Notable is the only intact fossil ant colony, of O. leakeyi, unpubl.). These differences in reports may reflect differ- preserved in a lower Miocene deposit from Kenya (WIL- ences in biology between cryptic species (CROZIER 1970). SON & TAYLOR 1964). Oecophylla leakeyi individuals were
58 larger than those of any other species, but present a similar allometry and bimodal size distribution to living species (WILSON & TAYLOR 1964). Eleven unequivocal fossil spe- cies are known, predominantly from mid-Eocene to Oligo- cene in Europe (DLUSSKY & al. 2008), speaking for signi- ficant climate change since then! On the basis of mitochon- drial sequence divergence, AZUMA & al. (2006) estimate that the two living species diverged 11.3 - 13.3 million years ago, in the Miocene, and the groups they found for O. smaragdina diverged between 3.6 and 7.8 million years ago, a recency which may explain the similarity in their morphology and biology. Social structure Life cycle: The life cycle of an O. smaragdina colony starts with a mated queen finding a sheltered site for a first nest between leaves of a tree or shrub and laying a batch of about 35 eggs within 5 - 10 days after dealation / shedding her wings (LOKKERS 1990). Further brood development strongly depends on temperature. At 30°C LOKKERS (1990) found larvae emerging from about day eight. Pupae fol- Fig. 3: Oecophylla species show a triphasic allometry, with low after day 17 and the first adult worker appeared after this plot for O. smaragdina showing that the majors and 28 days. These first workers are intermediate in size (LOK- minors have different slopes and are connected by inter- KERS 1990) to the distinct minor and major castes appear- mediates. From WILSON (1953), by permission. ing later (COLE & JONES 1948). As soon as last-instar lar- vae arise (around day 15), they are used by the queen to seal from a continuous to a dimorphic distribution of worker the nest chamber with silk. Below 20°C and above 35°C castes. The two worker castes show a clear division of la- brood development stalls mostly due to temperature sen- bor with the minors staying inside the nest (caring for brood, sitivity of the pupae, which inhibits colony growth in sea- etc.) and the majors performing outdoor tasks (e.g., forag- sonal climates during the cooler months. One to three days ing, defence) (HÖLLDOBLER & WILSON 1977c). HÖLLDOB- after the first worker emerges the nest is opened through LER (1983) also found age polyethism. Older workers are a hole and outside activity starts. Interestingly, LOKKERS stationed in barrack nests along the colony periphery and (1990) did not find prey retrieved until five weeks after the act as guards and defenders. HÖLLDOBLER (1983) also de- nest was opened. As in many other ants, the survival rates scribed the territorial behavior of O. smaragdina as very of new colonies is very low (GREENSLADE 1971) because similar to its sister species in tropical Africa using different of high intra- and interspecific competition and disease. cues for recruitment to new food or terrain, for marking Those colonies surviving the founding stage will develop their own territory, for long-range recruitment to intruders into colonies consisting of at least half a million individu- and for short-range recruitment to intruders or prey. As ex- als occupying several good-sized trees (HÖLLDOBLER & pected from demographic theory, CHAPUISAT & KELLER WILSON 1990). When the queen dies the workers activate (2002) found that the minor workers live longer than the their ovaries and produce a last set of male brood before majors. the colony shrinks as worker numbers reduce over the fol- Depending on the climate, activity outside the nest oc- lowing months (LOKKERS 1990). Worker reproduction may curs constantly in the wet tropics or in a diurnal pattern be delayed because even the queen's corpse may yield queen in the drier part of seasonal climates (LOKKERS 1990). In pheromones for up to half a year (HÖLLDOBLER & WILSON North Queensland, activity is seven times higher in the wet 1983a). GREENSLADE (1971) proposed an average colony season than during the dry season and ceases completely life span of about eight years and synchrony of founding below 12°C (LOKKERS 1990). While prey is brought in new colonies as the old ones die. New sexuals are pro- mainly during daylight hours (which perhaps reflects their duced during the wet season and released synchronously excellent eye sight enabling a visual hunting technique), after heavy rainfall to take part in aerial swarm mating (in brood is transported after dark (LOKKERS 1990). North Queensland, LOKKERS 1990; this locality is near the In North Queensland, the growth of a colony is highest southern edge of the range and the situation is likely to dif- during the wet season, when temperature, humidity and fer elsewhere). There is a pronounced size dimorphism be- food availability (after flowering and leaf flushing of the tween the two sexes. The queens are a lot larger and heav- trees and subsequently increased abundance of prey) are ier than the males. But we could not find any counts or bio- most suitable. Brood production then peaks and, following mass estimates so that sex allocation theory cannot yet be a lag of about a month, worker numbers increase to reach tested in this species. the maximum in March. During the wet season colonies The workers of O. smaragdina are highly polymorphic. tend to spread out through their territory and then contract WILSON (1953) showed that the change of head size and to fewer and bigger nests during the dry months (LOKKERS shape follows an unusual triphasic allometry with few in- 1990). While larvae are present at all times of the year, termediate sized individuals and the majors far out num- pupae are absent for three months in the cooler and drier bering the minors (Fig. 3). This species could therefore be season. The continuous presence of larvae may be favoured a valuable model system to understand allometric changes by selection to be able to weave at all times. Eggs and
59 very young larvae are kept in the same nest as the queen. Later older larvae are distributed throughout the colony. Ants of this species can dominate up to 50 to 75% of the trees in a given location depending on season (LOK- KERS 1990). The expansion of a colony is generally limited only by the availability of trees and competition with other colonies of their own or a few other dominant ant species resulting in a mosaic of colonies across the landscape (HÖLL- DOBLER 1983). The genetic structure of colonies and populations: Studies of genetic colony structure and its causes and con- sequences have been fundamental to understanding not only the evolution of eusociality but also conflicts arising within colonies and their resolution (e.g., worker reproduction and sex allocation). In particular, the knowledge accumulating Fig. 4: Variation between localities in the effective number on deviations from the norm in genetic structure has helped of queens in Oecophylla smaragdina, as determined from in unravelling the factors mediating queen, worker and male analyses of microsatellite analyses of 52 colonies from behavior. Such deviations alter the structure of popula- Australia and Indonesia, from SCHLÜNS & al. (2009), by tions and may ultimately lead to diversification and speci- permission. ation events (AVISE 2004). The genetic structure of the archetypical ant colony is simple (CROZIER & PAMILO 1996). A single once-mated queen produces full-sibling workers and new female and male reproductives. Yet, due to relatedness asymmetries caused by male haploidy, various conflicts may arise among the different colony members. Differences from this arche- typical breeding and mating behavior that alter relationship structure of colonies have thus gathered particular attention in order to gain insight into how kin selection and other forces might have shaped the life history and behavior of an ant species. Oecophylla smaragdina promises to be a very interesting study organism because its genetic colony struc- ture deviates from the archetypical case and also varies among populations (SCHLÜNS & al. 2009). This is a rare case where colony relatedness is reduced by both polygyny and polyandry at levels specific to each population. Of three Fig. 5: Variation between queens of Oecophylla smarag- locations studied, one in Java maintains the highest related- dina of three localities in the effective number of matings, ness among nestmates due to a very low incidence of both as inferred from worker microsatellite analyses of 85 col- polygyny and polyandry. Two Australian populations tend onies, from SCHLÜNS & al. (2009), by permission. to have greatly reduced colony relatedness and thus an in- creased intra-colonial genetic variation. Colonies in the true swarm mating and the entry of males into foreign nests. Northern Territory are often polygynous and sometimes Yet it is uncommon for unrelated queens to continue to polyandrous and have therefore the greatest genetic varia- cooperate after the first worker emergence (KELLER 1995, tion (Fig. 4). Up to five unrelated queens were found to con- BERNASCONI & STRASSMANN 1999), because the selective tribute equally to the worker offspring in a colony (SCHLÜNS advantage of greater competitiveness through faster initial & al. 2009). But this estimate is a minimum due to sample growth and an advantage at raiding other new colonies size and could well be higher. This finding confirms the ob- wears off as competitors are eliminated. The colony lifespan servations of polygyny reported by PEETERS & ANDERSEN reported for the Northern Territory of seven years (PENG (1980) for incipient colonies and PENG & al. (1998) also for & al. 2004) agrees with all nestmate queens stemming from mature colonies (by nest dissections). After flying, queens the colony's founding, with no further queens added during found a colony together (PEETERS & ANDERSEN 1980), and the colony's life. continue living together in the same nest, probably until The queens in a polygynous Northern Territory colony they die of natural causes. HÖLLDOBLER & WILSON (1977b) live in the same nest but in different compartments (PENG recorded swarm mating in Oecophylla ants, but VANDER- & al. 1998). The small number of queens make it an exam- PLANK (1960) wrote that males enter foreign nests and mate ple of oligogyny (HÖLLDOBLER 1962), and the probable ter- with virgin queens within. LOKKERS (1990) found many ritoriality suggests that it is a case of paragyny (PAMILO colony-founding queens, but never saw them leaving their 1991). natal nests, inferring that flights occur after dark. Given that In contrast to those in the Northern Territory, colo- these authors reported results from different localities, there nies in Queensland have an intermediate variability since is room for comparative studies between divergent sites. they are often polyandrous and only sometimes polygynous. The finding (SCHLÜNS & al. 2009) that colony-founding Queensland queens mate up to five times, sometimes with queens are unrelated suggests that intranidal mating of re- skewed contributions by the males (Fig. 5). This finding latives is quite unlikely, but does not distinguish between implies very different mating and colony-founding behavi-
60 ors in these three populations. Such a skew in male contri- differences and geographical and colonial variation in these butions in the production of new queens (as seen in the mandibular gland contents. workers) could create different selection forces on males An alarm response and various types of aggressive among populations with varying mating frequencies. behavior are also elicited by the contents of the Dufours Although polygyny and polyandry each appeared to and venom glands in the ants' abdomens (BRADSHAW & al. vary in incidence between locations, there was no corre- 1979a). The main components, n-undecane and formic acid, lation between the two. This indicates that within-colony appear to act synergistically to stimulate an attack response genetic variation is not the only factor that influences queen from major workers. number and multiple mating by queens in this species The sternal gland, identified for the first time in O. longi- (SCHLÜNS & al. 2009). noda, appears to release a pheromone that is used for short A larger study covering a greater geographical range is range recruitment, inducing workers to gather into small needed to provide a stronger test for this hypothesis and clusters (HÖLLDOBLER & WILSON 1977c). The rectal gland to discover the trends in environmental parameters that drive appears to be the source of trail pheromones (HÖLLDOB- these population differences. LER & WILSON 1977c), but also of colony-specific terri- In the populations where polygyny was rare, in the few torial pheromones (HÖLLDOBLER & WILSON 1977a). cases it did occur reproduction was often skewed in worker These studies are all based on O. longinoda. Similar production, making the colony functionally close to mono- behavioral patterns in O. smaragdina suggest a similar role gynous. In sharp contrast, colonies of the polygynous pop- for these glands in this species, but no comparable studies ulation in the Northern Territory rarely showed any skew. have so far been conducted. This may conceal some impor- The mode of colony foundation was correlated with the tant differences between the species. Rectal discharges like queen number in mature colonies. PEETERS & ANDERSEN those described for O. longinoda occur in O. smaragdina, (1980) observed pleometrosis (multiple queens founding a although whether they serve the same function is unknown colony together) in the Northern Territory, but other auth- (HÖLLDOBLER 1983). OFFENBERG (2007) found a clear cor- ors reported haplometrosis in Queensland (DODD 1902) relation between the density of these anal spots and wor- and India (MAXWELL-LEFROY & HOWLETT 1909). This ker activity, but this does not reveal anything about their apparent contradiction is now resolved with the demon- function. However, OFFENBERG & al. (2004) found that the stration of population differences in queen number and that beetle Rhyparida wallacei, a prey item of O. smaragdina, polygyny, when present, is functional. This makes O. sma- preferred to feed on leaves that were free of these dis- ragdina an excellent study system for the evolution of gen- charges, suggesting that they signalled the presence of the etic variation within colonies. ants. It remains to be seen whether they also serve as a ter- Apart from studying the causes underlying the occur- ritorial signal for conspecifics. rence of polygyny and polyandry in only some popula- Colonymate / kin recognition: Cuticular hydrocarbons tions, testing sex allocation theory and conflict resolution (CHCs) are generally recognized to play a key role in in- over male production will be interesting areas to explore in sect recognition systems (HOWARD & BLOMQUIST 2005), this species. Size differences between queens and males, the including nest- or colonymate recognition in social insects multiple mating of queens, and the occurrence of worker (DANI 2006). Direct behavioral evidence for CHCs as reproduction suggest a strongly male-biased numerical sex nestmate-recognition cues has been found in several ant ratio in Australia, but possibly less in other, genetically less species (AKINO & al. 2004, TORRES & al. 2007, MARTIN & variable populations, as in Indonesia. Split sex ratios seem al. 2008). unlikely as in all reports known to us both males and fe- Two main models have been proposed for understand- males were found. A prediction from this is that worker re- ing colony odor in social insects, the "gestalt" model, and production (through males) is more prominent in the Aus- the "individualistic" model (CROZIER & DIX 1979, CROZIER tralian populations. & PAMILO 1996). According to the gestalt model, individu- Although workers in general do not contribute to the als continually exchange chemical cues with other individu- production of male brood, when the queen dies the worker- als, usually via trophallaxis (BOULAY & al. 2000) or allo- produced males are reared as a last effort to increase their grooming (SOROKER & al. 1998, LENOIR & al. 2001). This fitness before the colony dies (CROZIER 1970, HÖLLDOB- results in a more or less uniform odor across the colony, LER & WILSON 1983b). consisting of a blend of individual odors. According to the individualistic model, each individual retains its own odor, A complex chemical world with little or no exchange between individuals taking place. Oecophylla has one of the most complex chemical re- The colony odor therefore consists of a greater or lesser pertoires among the ants, although most of the studies to variety of odors depending on the level of genetic and / or date are of O. longinoda. Here we consider the role of phe- environmental diversity within the colony. romones in alarm and recruitment behavior, and the role The gestalt model is now widely accepted as the gen- of cuticular hydrocarbons (CHCs) in nestmate recognition. eral rule among eusocial insects (LENOIR & al. 1999). How- Pheromones: Analysis of the glandular contents of ever, there are some indications that a perfect colony ge- Oecophylla has been restricted to O. longinoda. BRAD- stalt is not always realised. Many aggression bioassays re- SHAW & al. (1975, 1979b) described several secretions from veal a range of responses by individuals towards the same the mandibular gland that seem to elicit alarm / attack re- intruder. BOULAY & al. (2000), for example, argued in fa- sponses of various intensities. Hexanal triggers alarm be- vour of the gestalt model for Camponotus fellah, despite re- havior, while 1-hexanol draws the ants towards the source; porting that upon re-introduction to their colony of origin, at closer range, 3-undecanone and 2-butyl-2-octanal elicit a workers that had been isolated from their colony for up to bite response. BRADSHAW & al. (1979c) found both caste 40 days could be attacked by one worker and simultaneously
61 solicited for trophallaxis by another. Some individuals ap- However, additional analysis of spectra (NEWEY & al. 2009a) pear to make recognition errors when confronted with an indicates that the differences between colonies occur mainly intruder, while others do not, suggesting some degree of in the locations and widths of certain peaks, while differ- variation in the templates against which intruders are as- ences between nests within colonies occur mainly in the sessed. Furthermore, some "non-self" (TSUTSUI 2004) indi- amplitudes of peaks. Thus intra-colonial differences do not viduals from another colony are incorrectly recognised as necessarily obscure inter-colonial differences. Intra-colonial "self" while others are not. This suggests some degree of variation may result from limited exchange of workers be- variation in the signals borne by colony members, as well tween nests. HÖLLDOBLER (1983) found that workers in the as in the templates against which they are assessed. In large "barrack" nests at the edges of colonies demonstrated a colonies, perhaps with multiple queens and / or multiple high degree of site fidelity. This may also be true of wor- queen-mating, or with heterogeneous microhabitat condi- kers in other nests: perhaps there is some degree of fide- tions across the range of the colony, complete mixing of lity to the nest in which the worker first eclosed. This re- the colony odor might be difficult to maintain. In the poly- mains to be tested. domous Australian meat ant, Iridomyrmex purpureus, for Overall, NIRS assigned 76.5% of workers to the cor- example, there appear to be both colony specific and nest rect colony (of four) (NEWEY & al. 2008b). This finding (within colony) specific chemical signals (VAN WILGEN- indicates that there is likely to be some overlap in odor be- BURG & al. 2006). tween colonies, a result supported by CHC analysis (ELGAR Early evidence for colonymate recognition in O. sma- & ALLAN 2006). This might also be expected to result in ragdina is based on direct observation of the response of recognition errors, with some intruders mistakenly identi- colony members to intruders from other colonies (HÖLL- fied as colonymates. NEWEY & al. (2008a) demonstrated DOBLER 1983), which is typically aggressive. HÖLLDOBLER that the level of aggression shown towards intruders from (1983) found that the strength of aggressive response de- different colonies varied significantly, with some colonies pended on where the intruder was found, with a stronger showing very little aggression towards intruders from some response elicited when the intruder was inside the territo- alien colonies. In fact, the level of aggression increased rial boundaries of the colony. linearly as the spectral distance between colonies, as meas- Most of what is known about the CHCs of O. sma- ured using NIRS, increased (NEWEY & al. 2008a). Similar ragdina derives from a series of studies of the myrmeco- results have been obtained for other social insects when philous salticid spider Cosmophasis bitaeniata that feeds on measuring the chemical distance between colonies using the larvae of O. smaragdina. ALLAN & al. (2002) found that CHCs (SUAREZ & al. 2002, KAIB & al. 2004, D'ETTORRE O. smaragdina workers were more aggressive, and re- & al. 2006, FOITZIK & al. 2007). Furthermore, in O. sma- sponded aggressively more frequently, towards filter pa- ragdina the level of aggression expressed towards different pers soaked in CHC extracts of ants from alien colonies intruders from the same alien colony also showed a great than to those soaked in extracts of ants from their own col- deal of variability, suggesting that there may be consid- ony. ELGAR & ALLAN (2004) found that the CHC profile erable variation in either the odor or recognition template of C. bitaeniata resembled that of the larvae in the colony, even between individuals in the same nest. Recent research rather than that of the workers. As larvae are easily ex- suggests both that some ants are consistently more aggres- changed between colonies (P.S. Newey, unpubl.), this sug- sive than others (CROSLAND 1990) and, more significantly, gests that the CHC profile of larvae (and, therefore, the that individuals may assess intruders using templates based spider) do not contain the signal used by workers to dif- on their individual odor, rather than the colony odor (P.S. ferentiate between colonymates and non-colonymates, de- Newey & al., unpubl.). This diversity of templates may spite the fact that the CHC profiles of larvae differed be- serve to provide the colony with defence against intruders tween colonies (ELGAR & ALLAN 2004), as did those of spi- from a range of conspecific colonies, in that workers may ders (ELGAR & ALLAN 2006). vary in which intruders they most readily detect. Recent work on colonymate recognition has focussed It has been demonstrated in several ant species that on laboratory-based behavioral studies and the use of near- colony odor is not fixed, but changes over time, as in So- infrared reflectance spectroscopy (NIRS) to determine col- lenopsis invicta (see VANDER MEER & al. 1989), Temno- ony odor. The latter involves generating absorption spectra thorax lichtensteini (see PROVOST & al. 1993), Cataglyphis in the near-infrared, from about 4000 per cm to 12500 per iberica (see DAHBI & LENOIR 1998), Formica truncorum cm (wavenumber). Functional groups in molecules have (see NIELSEN & al. 1999), Aphaenogaster senilis (see LE- characteristic vibration frequencies within certain sections NOIR & al. 2001), and Linepithema humile (see SUAREZ & of this range (SCARFF & al. 2006) and this provides a broad al. 2002). Using NIRS, NEWEY & al. (2009b) showed that picture of the chemical "signature" of any scanned sample. colony odor in O. smaragdina also exhibited temporal The method lacks the chemical specificity of Gas Chroma- variation. However, they also demonstrated that the spectra tography / Mass Spectroscopy, which is generally used to of nests from the same colony, when separated for up to determine the CHC profile of a colony, but is attractive be- three months, changed in parallel with each other (NEWEY cause it is rapid and inexpensive: a sample can be scanned & al. 2009b). The level of aggression between separated in less than a minute. nests did not increase significantly over that time period, NEWEY & al. (2008b) found that NIRS could be used to although the frequency of trophallaxis did increase. Imper- differentiate between colonies of O. smaragdina and also fect exchange of CHCs between nests within a polydomous between nests within colonies. This indicates that, while colony could lead to incompatibility between nests if the there are differences in odor between colonies, there are also odors diverged sufficiently. In polygynous colonies, this significant differences within colonies, suggesting that there could result in colony budding, but in monogynous colo- is, at best, only an imperfect colony gestalt in this species. nies this is not possible, and would result in loss of colo-
62 nial integrity. The parallel changes in separated colony frag- ments of O. smaragdina suggest that there is an underly- ing mechanism, probably genetic, preventing radical diver- gence between nests. This may be a necessary adaptation for a species with very large polydomous colonies, but with only a single queen. It would be interesting to see whether this is also the case in other populations of O. smaragdina in which polygyny has been reported (PENG & al. 1998, SCHLÜNS & al. 2009). Colonymate recognition in O. smaragdina probably also has a learning component. Colonies are more aggressive towards intruders from neighboring colonies, with which they have presumably had prior contact, than they are to- wards intruders from more distant colonies (P.S. Newey & al., unpubl.). This is the opposite of the "dear enemy" ef- fect (FISHER 1954), and might be termed the "nasty neigh- bor" effect (MULLER & MANSER 2007). This could reflect either a difference in the capacity to recognise intruders, or a differential response to intruders depending on their col- ony of origin. Our research indicates that colonies are both more aggressive towards individuals, and aggressive towards a higher proportion of individuals, from neighboring colo- nies than from distant colonies (P.S. Newey, unpubl.). This suggests that there is both a behavioral and a perceptual component to this effect. The behavioral component is clear from the fact that, among individuals towards which an ag- gressive response occurred, this response was greater to- wards intruders from neighboring colonies. The perceptual component is indicated by the fact that a smaller proportion Fig. 6: Workers of Oecophylla smaragdina form chains to of workers from distant colonies than from neighboring pull leaves together in nest-building, from HÖLLDOBLER colonies elicited any level of aggressive response. While we & WILSON (1990), by permission. cannot completely rule out the possibility that recipients made a behavioral decision to treat some workers from a occasional stray representing no real threat, colony defences colony aggressively and some non-aggressively, it seems seem to be directed towards the more immediate threat more likely that the difference was the result of misidenti- posed by neighboring colonies, with whom they are likely fication. We found no evidence that intruders from distant to compete for resources, and against whom they need to colonies were avoided rather than engaged in conflict, as defend an extensive territory. might have been expected if they were recognised as alien masterful conspecifics. Furthermore, workers from recipient colonies Behavioral complexity, cooperation and building were more likely to engage in grooming or trophallaxis with workers from unfamiliar than from familiar colonies. We Perhaps one of the most distinctive behavioral attributes of therefore conclude that intruders from distant colonies are O. smaragdina involves the manner in which nestmates of more likely to be misidentified as colonymates than workers multiple castes (including larvae) cooperate to construct from neighboring colonies; in addition, when intruders are arboreal silk nests. Workers form living chains to cross gaps correctly identified as alien conspecifics, they are greeted and bring leaves together at the work site (Fig. 6). Addi- with a more aggressive response when they originate from tional workers then hold final instar larvae in their mandi- a neighboring colony than when they originate from a more ble at the work sites (Fig. 7), and use the silk produced by distant colony. It seems clear from this that experience the larvae to fasten together leaves to form the nest walls plays an important role in the ability of weaver ants to dif- (HÖLLDOBLER & WILSON 1977b). Together, workers and ferentiate between self and other, and in determining the larvae act as a living moveable sewing machine, a skill con- level of aggression directed towards those identified as sidered to play a significant role in the ability of Oeco- other. HÖLLDOBLER (1983) also suggested that workers phylla to achieve such large colonies and ecological domi- might become sensitised to heterospecific enemies. nance (HÖLLDOBLER & WILSON 1990). Oecophylla smaragdina colonies appear to possess an Green tree ants as arboreal builders: The nests of incomplete colony gestalt odor, with limited exchange of Oecophylla have attracted attention for many years. The workers between nests resulting in significant intra-colo- habitation of arboreal nests constructed of leaves glued nial variation. However, this variation seems to be limited together with "white material" appears to have been first by an underlying mechanism that prevents the odor be- noted by BANKS (unknown date of online publication) dur- tween nests from drifting too far apart. This is certainly ing James Cook's voyage to Australia in the late 18th cen- aided by some exchange of chemicals between nests. Col- tury. Later studies of O. smaragdina determined that the onies also show considerable variation in their capacity to white material used was larval silk, and described how wor- identify intruders from different colonies. However, as con- kers can form chains to bring together leaf material to con- tact between widely separated colonies is unlikely, with an struct their arboreal nests (RIDLEY 1894, and DOFLEIN 1905
63
thought in O. smaragdina, as shown by SCHLÜNS & al. (2009), and a comparison with non-social Hymenoptera might prove instructive because in such cases there can be no differential selection on gland size due to sociality. Comparison with other weaving ants: The incorpora- tion of silk into nests is known from a number of ant spe- cies, but the source of this silk is often uncertain. Silk has been described in the earthen nests of some Temnothorax (Myrmicinae, BARONI URBANI 1978) but the source of this silk is unknown. Struck by the resemblance of Technomyr- mex bicolor nests to "miniature" ones of Polyrhachis, JA- COBSON & FOREL (1909) suggested that this dolichoderine ant is also a weaver, but this seems unlikely. The terrestrial nests of Melissotarsus emeryi contain silk strands produced from specialized glands in the hypostoma of the workers, but M. emeryi is the only known ant in which workers can produce silk (Myrmicinae, FISHER & ROBERTSON 1999). Arboreal silk nests are produced by Dolichoderus sulcati- ceps (Dolichoderinae, MASCHWITZ & al. 1991), but the silk is from spiders (ROHE & MASCHWITZ 2003). The use of larval silk in arboreal nests appears to be lim- Fig. 7: An Oecophylla smaragdina worker stimulates a larva ited to three genera within the Camponotini: Camponotus, to produce a silk thread which is passed back and forth Polyrhachis and Oecophylla. Weaving has likely evolved over the gap to fasten the leaves together, from HÖLLDOB- independently four times, twice in Camponotus (subgen- LER & WILSON (1983b), by permission. era Dendromyrmex and Karavaievia) and once each in the other genera (JOHNSON & al. 2003), but further studies are needed. Recent research on the nesting habits of the genus cited by HEMMINGSEN 1973). These studies were followed Polyrhachis suggests that nesting habits can be much more with more general ones of the ecology of both extant Oeco- variable than previously thought (ROBSON & KOHOUT 2007). phylla species, O. smaragdina (see COLE & JONES 1948) Nest location (arboreal or terrestrial) and the inclusion of and O. longinoda (see WAY 1954). silk in nests can be variable within individual species, and Nest building involves both the preparation of the sub- the presence or absence of cocoons varies between species strate and the gluing of the substrate together with larval within the genus. The use of spider rather than larval silk is silk. Workers combine to form living chains. Leaves in close known in some Polyrhachis species (ROBSON 2004) and proximity can be drawn together through the actions of suspected in others (ROBSON & KOHOUT 2008), and the multiple individuals aligning themselves along leaf peri- use of non-larval silk may provide an explanation for ob- meters and pulling the edges together, or via the forma- servations mentioned above of silk nests in Temnothorax. tion of living chains, that bridge gaps and are shortened HÖLLDOBLER & WILSON (1983b) place Oecophylla at to draw leaves together (HÖLLDOBLER & WILSON 1977b). the top of three levels of sophistication in the weaver-ant Nest weaving involves workers holding larvae and initi- life style. The first grade is occupied by species of Campo- ating silk production through a series of complex behavi- notus (Dendromyrmex). Dendromyrmex larvae contribute oral interactions at the work site (HÖLLDOBLER & WIL- to nest architecture by emitting silk in the nest, but they are SON 1990). A division of labor involving nest weaving is neither held nor manipulated by workers (WILSON 1981). likely, though the actual details are uncertain. Some studies The second grade comprises various Camponotus (Karava- of O. longinoda have reported that only major workers ievia) and Polyrhachis species in which workers hold lar- hold spinning larvae (HÖLLDOBLER & WILSON 1990), vae which emit silk to fill the spaces between leaves and while others report that both minor and majors are involved, other structural elements, but do not otherwise adjust the though the sites of weaving can be different (minors in- substrate (MASCHWITZ & al. 1985). The third grade is re- side nests, majors outside, HEMMINGSEN 1973). Only final- presented solely by Oecophylla, in which the silk-producing instar larvae appear to be involved in silk production: Lar- larvae are always held by workers, the larvae do not pupae vae allocate all of their silk to the colony nest (they pupate in cocoons and alone among all weaving ants, the workers without cocoons), and they possess relatively larger silk extensively adjust the substrate by pulling leaves together glands and a more modified external silk apparatus than the (HÖLLDOBLER & WILSON 1983b). larvae of other ant species (figure 2 in HÖLLDOBLER & HÖLLDOBLER & WILSON (1983b) note that the two WILSON 1983b). lower levels of weaver ant organization show how the Cooperation between larvae and adults in weaving: high level of sophistication achieved by Oecophylla could Male larvae have silk glands that are relatively smaller than have evolved, while filling in little about the actual details. those of female larvae (WILSON & HÖLLDOBLER 1980). HÖLLDOBLER & WILSON (1983b) also discuss two hypo- WILSON & HÖLLDOBLER (1980) suggest that this sex dif- theses on why not all weaver ants have achieved the level ference may reflect the lower levels of relatedness of males shown by Oecophylla. The first hypothesis is that all weaver- than females to other nestmates: males may have less incen- ant lineages are indeed evolving to the Oecophylla level, tive to cooperate in nest building than females. However, but that a combination of extinctions and new originations we now know that this difference is smaller than was then of weaving mean that there are always species further back
64 on the path. The second hypothesis is that species at the Associations – friends and enemies three grades are more or less in a stable state – that the level each has reached is appropriate for it given its eco- Oecophylla smaragdina has some interesting relationships logical niche. We incline to the second hypothesis. Thus, with other fauna. The parasitic and mutualistic associations honey bees such as Apis mellifera have a much more ela- that other species have with weaver ants is probably worth borate social organization than bumble bees, but the life a review of its own. Here we will only consider some of cycle of the latter bees enables them to survive in higher the more important and interesting of these. latitudes than can honey bees (GOULSON & SPARROW 2009). Enemies: One of the most closely studied relationships However, given that there are no fossil Dendromyrmex (see is with the predatory spider, Cosmophasis bitaeniata, which BOLTON 2003) and that the sole Polyrhachis fossil is quite is both a visual and a chemical mimic of the ant. This salti- recent (Upper Mioncene; WAPPLER & al. 2009), we can- cid spider feeds on the ant larvae and appears to be quite not be sure of the dates of origin of the weaver ants in these comfortable inside ant nests, although it tends to avoid di- groups. rect contact with major workers (ALLAN & ELGAR 2001). Chain formation as an experimental system: Social The CHC profile of the spider most closely resembles that insects play a key role in advancing our understanding of of the larvae in the host colony (ELGAR & ALLAN 2006), how complex systems solve problems, via the relative ease and is almost certainly obtained either through eating or with which they can be experimentally manipulated and the handling its prey (ELGAR & ALLAN 2004). Although the diversity of problems they solve on a daily basis. Com- CHC profile of larvae varies between colonies, colonies prised of relatively simple individuals, as a group they dis- readily accept larvae from alien conspecific colonies. This play a "collective intelligence that seems far beyond the means that spiders are likely to be able to move between capabilities of single individuals" (BONABEAU & al. 1997). colonies, although they appear to have more success acquir- A new science has emerged that develops problem-solving ing larvae from minor workers in their host colony than algorithms inspired by the behaviors of social insects and from minor workers from other colonies (ELGAR & ALLAN recognizes biologists as "providers" of innovative ideas 2006). The difference appears to be the result of changes (BONABEAU & al. 2000, DORIGO & STÜTZLE 2004). Exem- in the behavior of the spider rather than of the ants, as no plary studies of real-life problem solving such as the man- change in activity was recorded by workers in the presence ner in which colonies of honey bees and ants select new of spiders from colonies other than their own (ELGAR & nest sites (PRATT & al. 2002, SEELEY & VISSCHER 2004) ALLAN 2006). Oecophylla smaragdina are also host to Myr- and the foraging of ants (DENEUBOURG & al. 1983, BEEK- marachne spiders, which show a large measure of inde- MAN & al. 2001, BURD & al. 2002) have naturally lead to pendence in their speciation pattern from the wide range advances in our understanding of more general principles of host ants they mimic (CECCARELLI & CROZIER 2007). such as social insect nest-site selection (FRANKS & al. 2002), The larvae of two lycaenid butterflies, Liphyra brasso- teamwork (ANDERSON & FRANKS 2003, SUMPTER 2006), lis and L. grandis, feed exclusively on larvae of the wea- self-assembly (ANDERSON & al. 2002), foraging behavior ver ant (BRABY 2000). The larvae of L. brassolis are flat and (SUMPTER & PRATT 2003), colony organization (BONA- broadly oval (PIERCE & al. 2002), and their tough exterior BEAU & al. 1997), group decision making (DETRAIN & DE- probably protects them from the ants (BRABY 2000). Wheth- NEUBOURG 2008, PASSINO & al. 2008) and cognition (SEE- er any chemical mimicry is also involved is not known. LEY & al. 2006). These, in turn, have lead to significant ad- However, nests sometimes contain several of these large vances in our ability to find optimal solutions to problems and conspicuous predators and the workers exhibit no ob- facing humans, such as traffic flow (DUSSUTOUR & al. vious reaction to their presence (P.S. Newey, unpubl.), sug- 2004), communication networks (BONABEAU & al. 2000, gesting that some chemical disguise may also be in effect. DORIGO & STÜTZLE 2004) and clustering algorithms for Most ant / lycaenid associations appear to be mutualistic to internet searches (SCHOCKAERT & al. 2007). An example some degree, and these predatory associations are among of the impressive extent to which insects can be used to only 37 confirmed cases worldwide of ant-parasitic lycae- solve practical problems involves allowing live insects to nids (DANIELS 2004). cohabit with robots to optimize the problem solving capa- Friends: The larvae of many lycaenid butterflies secrete bilities of the combined group (HALLOY & al. 2007). ant-appeasement substances or attractants, as well as su- Studies of the building behavior of Oecophylla promise gary food solutions, from epidermal glands. These enable to contribute significantly to our understanding of problem them to live within the protection of ant nests. Within Aus- solving in complex systems and the production of collec- tralia, the larvae of eight species of lycaenid butterflies tive systems through self-assembly. Building on earlier are attended by weaver ants. Arhopala centaurus, A. ma- studies of the organization of group behavior (SUDD 1963), dytus, A. micale, Hypolycaena phorbas, and Anthene sel- recent studies have demonstrated how population size and tuttus are obligate myrmecophiles, tended exclusively by individual probabilities of entering or leaving chains explain weaver ants (BRABY 2000). Anthene lycaenoides and Naca- much of the observed dynamics of chain formation in Oeco- duba berenice are facultative myrmecophiles attended by a phylla (LIONI & al. 2001, LIONI & DENEUBOURG 2004). range of ant species including weaver ants (BRABY 2000), Despite the amazing ability of Oecophylla workers to form while Theclinesthes miskini has been recorded as associ- "bridges, ladders, pulling chains and droplets" we know lit- ated with weaver ants only once (BRABY 2000). Anthene tle of the proximate mechanisms underlying these behav- emolus, an obligate myrmecophile associated exclusively iors (ANDERSON & al. 2002). The behavior in which Oeco- with weaver ants in south-east Asia, also appears to give phylla workers form groups that hang then drop from the off alarm pheromones when disturbed, to which the ants end of branches, for example, resembles water dripping from respond (FIEDLER & MASCHWITZ 1989). Whether or not a leaky tap (BONABEAU & al. 1998). this is true of other lycaenids is not known. These associa-
65
Fig. 8: Oecophylla smaragdina workers congregating on a dead Forest Kingfisher (Todiramphus macleayii), courtesy David Browning.
tions are mutualistic because the larvae acquire some pro- these associations are obligate or exclusive between spe- tection from predators, and are also carried to food sources cies is largely unknown, although some weaver ant asso- at some stages in their development (FIEDLER & MASCH- ciations with Homoptera may be exclusive, or nearly so WITZ 1989), while ants receive food that is rich in carbo- (WAY 1963). In general there is a paucity of detailed stud- hydrates. ies of weaver ant / trophobiont associations other than those Weaver ants also derive food from a range of other involving lycaenids. insect species that excrete solutions rich in sugars, amino Economic significance acids and other nutrients. In the Solomon Islands O. sma- ragdina is reported to attend at least nine species of seden- Oecophylla smaragdina is not only ecologically important, tary Homoptera (GREENSLADE 1972). BLÜTHGEN & FIED- as one of the dominant species in the forest canopies of LER (2002) identified trophobionts from seven families (ex- northern Australia and south-east Asia (BLÜTHGEN & STORK cluding lycaenids) associated with weaver ants at a rain- 2007, DAVIDSON 2007), but is also of considerable eco- forest site in far north Queensland, Australia. Although ant nomic importance as a biological control agent, as food and / trophobiont associations are generally assumed to be mu- medicine, and also as a potential pest itself. tualistic, evidence of benefits to the trophobionts appears Biological control agent: Written records indicate that to be largely anecdotal (HÖLLDOBLER & WILSON 1990). Oecophylla smaragdina was recognised in China as a bi- Early studies yielded conflicting evidence concerning the ological control agent as early as 304 A.D. (VAN MELE extent to which ants provided protection for trophobionts 2008). Recent research has demonstrated its effectiveness (WAY 1963). More recent evidence suggests that protec- in controlling several pests in mango orchards (PENG & tion from parasitism is one likely benefit in some rela- CHRISTIAN 2004, 2005, 2006, BLÜTHGEN & STORK 2007, tionships. For example, trophobiotic associations with two DAVIDSON 2007, PENG & CHRISTIAN 2007), cashew planta- ant species, Camponotus brutus and Myrmicaria opaci- tions (PENG & al. 1999, 2005), citrus orchards (VAN MELE ventris, reduce egg parasitism in Caternaultiella rugosa & CUC 2000, VAN MELE & al. 2002), coconut planta- (Heteroptera: Plataspidae) (GIBERNAU & DEJEAN 2001). tions (KUMARESAN 1996) and cocoa plantations (WAY & There is some evidence that O. longinoda reduces the level KHOO 1989, 1991). For example, weaver ants, combined of parasitism among the homopterans it attends (WAY 1963). with soft chemical applications, reduce the numbers of Both Oecophylla species also transport homopterans to suit- Jarvis's fruit fly, Bactrocera jarvisi, in mango plantations, able feeding locations (WAY 1963). The degree to which compared with treatment by chemical insecticides, signifi-
66 cantly reducing the level of rejected fruit (PENG & CHRIS- reluctance to deploy large-scale biocide application means TIAN 2006). that the use of Oecophylla species in biological control Food and medicine: Throughout south-east Asia, wea- should be re-examined. ver ants are a significant commercial product. In Java the larvae and pupae of weaver ants are harvested and sold as Acknowledgements food for song birds or as fishing bait (CÉSARD 2004). Small RHC's work on ants is supported by the Australian Re- larvae (either of workers or early instar queens) are prefer- search Council (DP0665890). For scholarship support red as bird food. In the markets, 1 kg of larvae sells for be- EAS and PSN thank James Cook University and EAS tween US$3.5 and US$5.00 (CÉSARD 2004). In Thailand, also the CERF program for financial support. We thank H. large queen larvae and pupae are harvested as a food pro- Schlüns and two anonymous reviewers for constructive duct for human consumption (SRIBANDIT & al. 2008). This comments. not only provides food for the family, but also as much as Zusammenfassung 30% of the total family income for collectors (SRIBANDIT & al. 2008). In parts of India the workers themselves are Arten der Gattung Oecophylla gehören zu den bekanntes- consumed, and even used in the making of chutney (OUDHIA ten Ameisen in den Tropen, jedoch fehlt bis heute ein brei- 2002)! ter Überblick über ihre Biologie. Die zwei heute lebenden Extracts from the ants are used by Indian traditional hea- Oecophylla-Arten sind in den Altwelttropen weit verbrei- lers to treat a range of common maladies (OUDHIA 2002). tet und ähneln sich in dem komplexesten Nestbauverhalten Weaver ants are also reportedly used by indigenous Aus- aller Weberameisen. Arbeiterinnen ziehen Blätter zusam- tralian women to produce a remedy for colds and flu (WAT- men, was oft mit dem Bilden langer Ketten verbunden ist, SON 2002). und kleben sie mit der Seide ihrer Larven aneinander. Die Pest: Although generally regarded as beneficial within Kettenbildung verspricht ein wichtiges Themengebiet für the agricultural industry, O. smaragdina can also sometimes die Entwicklung von Modellen zur Selbstorganisation kom- be regarded as a pest, being an opportunistic and aggres- plexen Verhaltens zu bieten. Die Kolonien sind sehr groß sive feeder (Fig. 8). Even when the benefits of weaver ants und hochgradig polydom. Die Königinnen sind meist, je- to the quality of mango fruit are acknowledged, the ants are doch nicht immer, einfach verpaart und die Kolonien nor- still often regarded as a nuisance pest during harvesting malerweise monogyn, außer im Northern Territory (Aus- (SINZOGAN & al. 2008). The use of weaver ants as a bio- tralien), wo sie polygyn sind. Die Arbeiterinnen sind stark logical control agent on coffee plantations in Sri Lanka has polymorph (wie schon bei einer fossilisierten Kolonie do- reportedly been abandoned for just this reason (CÉSARD kumentiert) und zeigen einen komplexen Polyethismus und 2004). ein viel untersuchtes, reichhaltiges Pheromonrepertoire für die verschiedenen Aufgabenbereiche der Kolonie. Der Ko- Outlook loniegeruch, teils erlernt und teils jedem Individuum in- It is our impression that research into the living Oecophylla trinsisch, weist in den Reaktionen gegenüber anderen Ko- species has been uneven. The glandular contents are better lonien dieser hochgradig territorialen Ameise einen "nasty known in O. longinoda, and O. smaragdina has been more neighbor"-Effekt auf. Der Geruch verändert sich mit der studied for behavior, population structure and colony struc- Zeit und unterscheidet sich zwischen Nestern einer Kolo- ture. The two species are generally regarded as very sim- nie. Es ist nicht überraschend, dass Oecophylla-Ameisen ilar, but are estimated to have separated over 10 million Wirte einer Reihe von Inquilinen sind (wie z.B. Spinnen), years ago (AZUMA & al. 2006) and surprises may result die den Koloniegeruch imitieren, um einer Entdeckung zu from work making them equally well-known. Further, the entgehen. Zusätzlich profitieren verschiedene Homopteren importance of these species to insect sociobiology makes vom Schutz der Ameisen, dennoch eignen sich diese Amei- them worthwhile subjects for exhaustive study to test for the sen auf Grund ihres Verhaltens als Nutzinsekten zur Schäd- presence of sibling species (SCHLICK-STEINER & al. 2009); lingskontrolle. In verschiedenen Regionen werden sie auch given the very large ranges involved it is likely (CROZIER vom Menschen gegessen. Wir spekulieren, dass die Exis- 1981) though not certain (WARD 1989) that such sibling tenz von Oecophylla die Evolution hochkomplexer sozi- species do occur. Thus, TAYLOR (2008) considers that O. aler Organisation bei anderen Weberameisen verhindert, longinoda comprises several cryptic species. Discovery that eine Idee, die mit größerem Wissen über die zeitliche Ab- there are more species than currently recognized would place folge von adaptiven Radiationen innerhalb der Ameisen ge- apparent geographic variation in biology in a new light. testet werden könnte. Oecophylla species present a tractable system for study- ing a complex behavior, namely the construction of the leaf References nests. How this cooperative system is controlled, and the AKINO, T., YAMAMURA, K., WAKAMURA, S. & YAMAOKA, R. 2004: degree to which it differs between the species, are fruitful Direct behavioral evidence for hydrocarbons as nestmate re- subjects for future study. Combination of such studies with cognition cues in Formica japonica (Hymenoptera: Formici- further molecular phylogenetic studies may allow identifi- dae). – Applied Entomology and Zoology 39: 381-387. cation of correlates in habitat or sociality mediating these ALLAN, R.A., CAPON, R.J., BROWN, W.V. & ELGAR, M.A. 2002: complex behaviors. Mimicry of host cuticular hydrocarbons by salticid spider Cos- Oecophylla species have unusual economic potential for mophasis bitaeniata that preys on larvae of tree ants Oeco- ants, not only in their interactions with beneficial and pest phylla smaragdina. – Journal of Chemical Ecology 28: 835-848. insects, but also in medicinal terms. Although it is likely ALLAN, R.A. & ELGAR, M.A. 2001: Exploitation of the green that in many places their use as biological control agents tree ant, Oecophylla smaragdina, by the salticid spider Cosmo- has been superseded by the use of insecticides, increasing phasis bitaeniata. – Australian Journal of Zoology 49: 129-137.
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