Notes on the Biology of the Oriental Amblyoponine Ant Myopopone Castanea: Queen-Worker Dimorphism, Worker Polymorphism and Larval Hemolymph Feeding by Workers

Entomological Science (2010) 13, 199–204 doi:10.1111/j.1479-8298.2010.00384.x

ORIGINAL ARTICLE

Notes on the biology of the Oriental amblyoponine ant Myopopone castanea: Queen-worker dimorphism, worker polymorphism and larval hemolymph feeding by workers

(Hymenoptera: Formicidae)ens_384 199..204

Fuminori ITO Faculty of Agriculture, Kagawa University, Miki, Kagawa, Japan

Abstract Queen-worker dimorphism, worker polymorphism and worker behavior in the Oriental amblyoponine ant Myopopone castanea were studied. Queen body size was large (head width, 3.0 mm) with 24 to 32 ovarioles while workers showed a remarkable size variation in both body size (head width 1.48 to 2.18 mm) and ovariole number (6 to 22). Both head width and abdomen width showed allometric growth against thorax width. Workers performed larval hemolymph feeding as was described for Amblyopone silvestrii queens. Key words: Amblyoponinae, ant, caste dimorphism, Hymenoptera, Myopopone.

INTRODUCTION its distribution is limited to tropical forests in the Oriental tropics to northernmost Australia, and it is not The ant subfamily Amblyoponinae has been regarded as a common species (Brown 1960). In this paper, I give one of the early branching lineages among family For- information on the biology of Myopopone castanea micidae (e.g. Brown 1960; Wilson 1971). Their broad (Smith) observed in West Sumatra, Indonesia, and attachment between petiole and the third segment of Sabah, Borneo. The biological information mentioned abdomen has been considered as an ancestral character. here is fragmentary; however, it is valuable for under- Even though the character status and the phylogenetic standing the diversity of the subfamily Amblyoponinae. position is still controversial (e.g. Hashimoto 1996; Saux et al. 2004; Brady et al. 2006; Rabeling et al. 2008), this ant group is undoubtedly peculiar among STUDY AREA AND METHODS ants. For example, Schoeters et al. (1999) showed that Colony fragments of M. castanea were collected in the venom gland of four amblyoponine genera is similar Sitiung (1°0′S, 101°37′E), near Padang, West Sumatra, to that of mutillid wasps: there is no convoluted gland Indonesia, in January 1993. In Tawau (4°29′N, which is found in all ant species so far studied for venom 117°47′E), Sabah, an alate queen and one incipient gland structure. colony with one dealate queen and brood were collected Among the subfamily Amblyoponinae, the biology in October 1996. Several workers and two alate queens of some species of Amblyopone, two species of Prion- were dissected under a microscope to check the number opelta, a few species of Mystrium and one Ony- of ovarioles and ovarian development. Spermatheca chomyrmex has been reported (e.g. Masuko 1986; Ito size (length of long axis) of one alate queen and a few 1993a,b,c; Ito & Billen 1998; Miyata et al. 2003; Molet workers collected in Sumatra were measured under a et al. 2007, 2009). To date, the monotypic genus light microscope. The result of spermatheca size was Myopopone has been rarely studied, probably because already reported in Ito and Ohkawara (1994). Body size Correspondence: Fuminori Ito, Faculty of Agriculture, (head width, thorax width, width of IVth abdominal Kagawa University, Miki, Kagawa 761-0795, Japan. segment) of all adults in one colony fragment (an alate Email: [email protected] queen and 38 workers) collected in Sitiung and the alate Received 29 July 2009; accepted 24 December 2009. queen from Sabah was measured under a binocular

microscope. I used SMATR 2.0 (Falster et al. 2006) to to the Sumatran queen (2.9 mm); however, the ovariole examine allometric growth of each body part. number was 24. Body size and ovariole number varied One colony fragment with 25 workers and seve- among workers, ranging from 1.48 to 2.18 mm in ral larvae was kept in an artificial nest measuring head width, and 6 to 22 ovarioles. Size distribution of 20 cm ¥ 10 cm ¥ 5 cm, which contained a small box workers was unimodal (head width, Shapiro–Wilk test, (5 cm ¥ 5cm¥ 2 cm) as a nest chamber. The floor of the W = 0.95, P = 0.15), which means that there were no nest was covered with plaster to keep the humidity high. discrete worker subcastes. All dissected workers had Larvae of mealworms Tenebrio molitor L. were fed as empty spermathecae, the size (0.12 mm) of which was prey. All workers were marked individually with enamel remarkably less than the queen (Ito & Ohkawara 1994). paint. Worker behavior was observed for 14 h over I never found developing oocytes in worker ovaries. 10 days. Both head (H) and abdomen (A) width are slightly but significantly allometric against thorax (T) width 1.19 2 RESULTS (H = 0.77 ¥ T , r = 0.94, difference from isometric growth, F = 18.0, P < 0.0001; A = 1.47 ¥ T1.20, r2 = Nest 0.93, difference from isometric growth, F = 17.5, < All nests were found in a dead log or branch fallen on P 0.0001). The number of ovarioles was positively the ground in tropical forests. Most logs and branches correlated with body size (Spearman’s test, Z = 3.4, inhabited by the ants were still hard. Three such nests P = 0.0007, Fig. 3). in Sitiung were completely broken apart, however, we Foraging and prey collected only virgin workers, an alate queen and larvae, suggesting a polydomous nesting system. In the laboratory, most workers of Myopopone left A founding nest with a dealate queen (Fig. 1) was the nest chamber alone. When they found mealworms, collected in Sabah. The Bogor Zoological Museum they stung them and brought the paralyzed prey items to holds many specimens of alate queens which were col- their nest. Mealworms were given to the larvae without lected by light traps. These observations indicate that fragmentation. When I gave termites to the captive the queens fly away for their nuptial flight and that colony, the ants hunted for this prey, but they did not the colony is founded by haplometrosis. feed on the termites. As mentioned by Brown (1960), they seem to be specialist predators on coleopteran Worker polymorphism, queen size and larvae. If large mealworms were given to the colony ovariole number fragment, workers attacked them singly. Adjacent Queen body size is remarkably greater than that of workers sometimes joined the attacks, and one worker workers (Fig. 2). The head width of the alate queen went back to the nest chamber where the worker was collected in Sumatra was 3.00 mm; she had 32 ovarioles shaking her body with antennation to nestmate workers. and a large spermatheca (long axis, 0.22 mm). The head After that, one or two workers left the nest and went width of the alate queen collected in Sabah was similar to foraging arena. These workers brought the prey

Figure 2 Log–log plot of head and abdomen width vs thorax Figure 1 Founding colony of Myopopone castanea. width of Myopopone castanea.

worker monopolized more than 50% of LHF (21 times) and the others only showed the behavior one to three times. Among workers, we never observed aggressive behavior. The relationship between LHF and ovarian development could not be examined, because colony condition was unfortunately poor at the end of the observation. During the observation period, no egg- laying occurred.

DISCUSSION The present results show several remarkable morphological and behavioral characteristics of Myopopone Figure 3 Relationship between abdomen width and ovariole castanea. First, this species exhibits a striking caste number in Myopopone castanea workers. dimorphism between queens and workers. In general, caste dimorphism is weak in poneroid ants (Peeters & Ito 2001). In most poneroid species (sensu Brady et al. 2006), ovariole number of queens is 6 or 8, and there is no difference between queens and workers (Ito & Ohkawara 1994). In the subfamily Amblyoponinae (Table 1), queens and workers have the same ovariole numbers in two species of Amblyopone, four species of Mystrium (8 ovarioles) (Molet et al. 2009), and Ony- chomyrmex hedleyi Emery (6 ovarioles, Peeters 1991). An example of caste dimorphism in ovariole number has been found in Prionopelta kraepelini Forel: queens have six ovarioles while workers have two (Ito & Billen 1998). Compared to these genera, dimorphism between queens and workers in Myopopone castanea is notable. Comparable ovariole numbers of queens in poneroid ants have been reported in ergatoid queens of Leptog- Figure 4 Larval hemolymph feeding by a worker of Myo- popone castanea. enys myops (Emery) (64 ovarioles, Ito 1997) and Pachy- condyla analis (Latreille) (formerly called Megaponera foetens (Fab.)) (32 ovarioles, Peeters 1991), and alate queens of P. (= Brachyponera) chinensis (Emery) (18 to cooperatively; however, they spent more than one hour 36 ovarioles, Gotoh & Ito 2008). for prey retrieval. Unlike Amblyopone reclinata Mayr Second, workers of M. castanea show large variation where an efficient group recruitment system exists in body size and ovariole numbers. In general, polymor- (Ito 1993a; Billen et al. 2005), nestmate recruitment in phism of worker body size is not developed in poneroid M. castanea seems to be unrefined. ants: no species have a distinctive major subcaste (e.g. Frumhoff & Ward 1992; Peeters 1997; Fjerdingstad & Larval hemolymph feeding Crozier 2006). Large body size variation with allometric Workers kept with larvae in the laboratory frequently growth of body parts, however, is known from showed larval hemolymph feeding (hereafter LHF, two ponerine ants, Pachycondyla analis (Crewe et al. Fig. 4). This behavior is very similar to that of queens of 1984) and Centromyrmex bequaerti (Forel) (Dejean Amblyopone silvestrii Wheeler as reported by Masuko & Feneron 1996) and two amblyoponine species, (1986). Workers pinched the larvae with their mandibles Mystrium camillae Emery (Molet et al. 2009) and and licked hemolymph from the wounds. Workers Amblyopone australis Erichson (Peeters & Molet 2010). most often pinched the dorsal integument of the upper In the case of Myopopone, workers show a remarkable abdomen of larvae. Many large larvae had scars which size variation with slight allometric growth. The signifi- seem to be made by LHF. During 14 h of observations of cance of worker size variation in this species is still an orphan colony with 25 workers, LHF was observed unknown; however, one possible explanation is that 38 times. Twelve of the 25 workers performed LHF. One workers can look for prey, mainly coleopteran larvae

Table 1 Queen-worker dimorphism of ovariole number in amblyoponine ants Species Locality Queen Worker References Amblyopone australis Australia 8 8 Peeters (1987) Amblyopone bellii† India – 8 Ito (1993c) Amblyopone reclinata† (= A. sp. W. Java – 8 Ito (1993b) (reclinata group)) Amblyopone sp.† Hong Kong – 8 F. Ito, unpubl. data (2002) Amblyopone silvestrii Japan 6 6 F. Ito, unpubl. data (1994) Myopopone castanea W. Sumatra 32 6–22 Present study Myopopone castanea Sabah 24 – Present study Mystrium camillae Java 8 8 Molet et al. (2009) Mystrium rogeri Madagascar 8 8 Molet et al. (2009) Mystrium mysticum Madagascar 8 8 Molet et al. (2009) Mystrium oberthueri Madagascar 8 8 Molet et al. (2009) Onychomyrmex hedleyi Australia 6 6 Peeters (1987) Prionopelta kraepelini W. Java 6 2 Ito & Billen (1998) †Queenless species. –, no data.

(Brown 1960), in differently sized tunnels in dead logs. of Gnamptogenys (Ectatomminae), Leptanilla japonica The variation of worker ovariole number has been and L. crypeata (Leptanillinae), and Calyptomyrmex reported in some poneroid species (e.g. Villet 1990): the sp. (Myrmiciinae) (Masuko 1986, 1989; Ito 2001; Ito & largest example of the variation is Platythyrea lamellosa Gobin 2008; F. Ito, unpubl. data, 2001), this aberrant (Roger) where four to eight ovarioles are found in feeding mode is one of the important characteristics of workers (Villet 1990). In amblyoponine ants, variation the subfamily Amblyoponinae. of ovariole number in workers has not been reported to Our current knowledge of the natural history of date (Table 1). In M. castanea, six to 22 ovarioles were M. castanea remains sparse; however, the present found in workers. Higher ovariole number is often study indicates that this species shows remarkable caste associated with the capacity of egg production. For dimorphism and worker size polymorphism as often example in Myrmecia froggatti Forel, ovariole number found in the more derived formicoid clade (sensu Brady in workers is positively correlated with the number of et al. 2006), while behavioral characteristics are similar developing oocytes found in ovaries, even when the eggs to the other members of the subfamily Amblyoponinae. seem to have a trophic function (Ito et al. 1994). In Further investigation on the ecology and behavior of this M. castanea, workers with developing oocytes were not species will give an insight into evolution of complex collected in the field, despite the presence of many social traits in ants. queenless nests. Therefore, the significance of the variation of ovariole number is uncertain. Third, workers show larval hemolymph feeding. This ACKNOWLEDGMENTS novel feeding behavior was first discovered in Ambly- opone silvestrii by Masuko (1986). Subsequently it has I thank K. Nakamura and H. Katakura for providing me been found in several ant species. Among amblyo- with the opportunity to conduct this research in Indo- ponine ants, the occurrence of LHF has been reported in nesia, T. Matsumoto for his kind help on the research in Amblyopone spp., Prionopelta kraepelini, Adetomyrma Malaysia, A. Hashim and the late S. Kawamura for their sp., Mystrium camillae and Onychomyrmex (Ito & encouragement and accommodation during my stay in Billen 1998; Masuko 2003; Saux et al. 2004; F. Ito, Sumatra, Lembaga Ilumu Pengetahuan Indonesia for unpubl. data, 1989, 2002). The present study showed research permission, C. Peeters for giving me motivation the occurrence of LHF in Myopopone castanea. Even to write this manuscript and comments, and J. Billen for though we still do not know whether queens of M. comments and English revision. The research was sup- castanea perform LHF, all genera in this subfamily so far ported by Grants-in-Aid for Overseas Research from observed show LHF. Although LHF has been found in a the Japan Ministry of Education, Science and Culture handful of ant species outside of Amblyoponinae, e.g. a (Nos. 02041033, 05041086, 08041136, 11691130) and few species of Proceratium (Proceratiinae), a few species from JSPS for young scientists.

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