Colony composition of two Malaysian Ponerine ants, Platythyrea tricuspidata and P. quadridenta: sexual reproduction by workers and production of queens (Hymenoptera: Formicidae).
Psyche 101(3-4):209-218, 1994.
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COLONY COMPOSITION OF TWO MALAYSIAN PONERINE ANTS, PLATYTHYREA TRZCUSPIDATA AND l? QUADRIDENTA: SEXUAL REPRODUCTION BY WORKERS AND
PRODUCTION OF QUEENS (HYMENOPTERA: FORMICIDAE) Biological Laboratory,
Faculty of Education,
Takamatsu 760 Japan
Colonies of ponerine ants Platythyrea quadridenta and P. tricus- pidata were collected in the rainforest of West Malaysia. Two colonies of P. tricuspidata were composed only of workers, and three and eight workers were inseminated per colony, respectively. However, active ovaries were found in one of the three, and two of the eight mated workers. P. quadridenta also exhibited sexual reproduction by workers, and there were many sterile mated work- ers. The two largest colonies of P. quadridenta produced alate queens. The significance of queen production and worker sexual reproduction are discussed.
Morphological differentiation associated with division of repro- ductive efforts between queens and workers is an important charac- teristic in the reproductive structure of ant colonies (Holldobler and Wilson 1990). In the subfamily Ponerinae, however, consider- able variation in reproductive structure has been reported in recent years (Peeters 1993). For instance, several species lack morpholog- ical queens and mated workers lay eggs instead (Peeters 1991). Such queenless reproduction has been reported in 10 genera belonging to the four tribes Amblyoponini, Ectatommini, Platythyreini, and Ponerini (Peeters 1991; Ito 1991). In addition, Sommer and Holldobler (1992) have found unexpected variation of Manuscript received 24 June 1994.
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reproductive division of labour in Pachycondyla tridentata, in which mated queens and mated workers exist together and both lay eggs. Reproduction by both queens and workers is also reported in Platythyrea arnoldi (Villet 1993) and Harpegnathos saltator (Peeters pers comm.). These species are good experimental sub- jects for understanding the evolution of morphological castes and their roles in the social organization and colony life-pattern of ants.
In West Malaysia, I studied colony composition of two Platythyrea species (Ponerinae: Platythyreini) and found sexual reproduction by workers in Platythyrea quadridenta and I? tricusp- idata, as well as production of queens in the former species. In this paper, I present information on colony composition and reproduc- tive condition of queens and workers in these two species. Colonies were collected in Ulu Gombak Forest Reserve (350m elevation, 3O 19' latitude, 101 O 43' longitude) near Kuala Lumpur, West Malaysia, from the end of dry season (July) to the rainy sea- son (October), in 1992. Colony composition was assessed just after collection and all individuals were dissected under a binocular microscope to check reproductive condition. Head width (outeror- bital distance), pronotum width, width of IVth abdominal segment and petiole width of several individuals was measured using an ocular micrometer on a binocular microscope. Both species nested in dead branches or large logs on the ground of rainforests. These ants run very rapidly when their nests are disturbed so that it was very difficult to capture all individuals. Therefore, complete collections were made only of two colonies of Platythyrea tricuspidata (colony code, Pt-1 and 2) and 14 colonies of I? quadridenta (Pq- 1 to 14).
Both P. tricuspidata colonies were small (Table 1) and con- tained neither queens, nor queen pupae. All workers had three ovarioles in each ovary and a spermatheca. Three and eight work-
Table 1. Colony composition of Platythyrea tricuspidata (Pt-1,2) and P. quadri- denta (Pq-1-14) collected in West Malaysia.* Number of mated workers having active ovaries was shown in parentheses. Only one dealated queen was mated and had active ovaries. **Not counted just after sampling. Number of Individuals
Colony Dealate Alate
code queens Workers mated* queens Males Pupae Larvae Eggs Pt- 1
-** - -
3(1) 0 0
16 13 14
0 0 1 0 0
3(0) 0 0
2 0 0
3(1) 0 0
7 3 0
0 0 1 4 13
Pq-5 0 10 3(2) 0 0 2 5 5
2(1) 0 1
8 8 1
0 0 4 7 18
0 0 6 19 17
0 0 10 11 6
Pq- 1 0
0 0 7 13 13
0 0 0 15 14 7
Pq- 12 0 3 3 12(3) 0 1 5 25 27
8 0 19 17 11
8 0 33 37 17
ers were inseminated in colonies Pt-2 and Pt-1, respectively. How- ever, active ovaries were only found in one mated worker in Pt-2 and two mated workers in Pt- 1. The other eight mated workers and all virgin workers lacked oocytes and yellow bodies in their ovaries. The body size of workers was quite uniform (Table 2) and did not differ between mated and unmated workers. Platythyrea quadridenta
Queens occurred in only two colonies (Table 1). Worker number was 18.5 å 15 (Mean å SD). Number of inseminated workers was zero to twelve, representing 0 to 60% of worker population per colony. Similarly to P. tricuspidata colonies, 22 out of 48 mated workers (total) were sterile. Four colonies had multiple mated workers with active ovaries (=gamergates) (colony code Pq-4, 9, 13, 14). In another four colonies having multiple mated workers (colony code Pq-3, 6, 7, lo), only one gamergate was present while the other mated workers lacked developed oocytes and
Table 2. Comparison of body size between mated workers and virgin workers, and between fertile mated workers and sterile mated workers in two Platythyrea species. Mean å±S was shown. P. tricuspidata l? quadridenta
Virgin Mated P * Virgin Mated P* fertile sterile
examined 15 3 11 17 4 13
Head width 1.23 å 0.02 1.23 å 0.02 0.60 1.04 å 0.02 1.04 å 0.02 0.82 1.03 å 0.03 1.04 å 0.02 0.27 Pronotum width 1.03 å 0.02 1.03 å 0.01 0.68 0.91 å 0.02 0.92 å 0.01 0.20 0.93 å 0.02 0.92 å 0.01 0.25 Petiole width 0.69 å 0.03 0.68 å 0.01 0.24 0.50 å 0.02 0.50 å 0.02 0.62 0.50 å 0.03 0.50 å 0.01 0.77 Abdomenwidth 1.17å±0.0 1.17k0.02 0.68 0.88k0.02 0.89å±0.0 0.49 0.89å±0.0 0.89å±0.0 0.95
yellow bodies, indicating that these colonies were functionally monogynous. In Pq-5 and Pq-12, there were sterile mated workers, while two and three mated workers had active ovaries, respectively. In one colony (Pq-2), composed of three mated workers and two virgin workers, there were no egg laying individuals. In Pq-11, consisted entirely of virgin workers lacking visible oocytes. This suggests that colony fission had recently occurred in Pq-2 and Pq- 11. In all 14 colonies, no virgin workers had visible oocytes. Head width of workers was significantly different among five measured colonies (ANOVA, F = 16.6, P = 0.0001 , df = 4, ), how- ever, this was not different between Pq-10 and 12 (ANOVA, F = 3.3 , P = 0.1 , df = 1, ). Thus, effects of body size on reproductive conditions were examined in the two colonies (Table 2). All four measures were not different between mated workers and virgin workers, and also between gamergates and mated sterile workers (Table 2), indicating that worker body size does not affect insemi- nation or oocyte development.
Two large colonies (Pq-13 and 14) produced alate queens, and one of these colonies contained one inseminated and dealate queen who had active ovaries. The body size of queens was significantly larger than workers in all four measures (Fig. 1). However, the size difference between the two castes in P. quadridenta is small rela- tive to other ponerine ants in which queens monopolize reproduc- tion while workers are always virgin (c.f. Ito and Ohkawara 1994). In addition, despite the queens' larger overall body size, their reproductive apparatus is almost identical to the workers: both castes had a pair of three ovarioles, and the spermathecae were about the same size.
In the ponerine species having gamergates, the number of mated workers per colony varies greatly. For instance, in the colonies of Diacamma spp., Pachycondyla sublaevis, P. krugeri and Streblo- gnathus aethiopicus, there is only one gamergate per colony and she monopolizes egg production (Peeters and Higashi 1989; Fuku- mot0 et al. 1989; Ito and Higashi 1991; Wildman and Crewe 1988; Ware et al. 1990). Several gamergates occur in Rhytidoponera spp., Ophthalmopone spp. and Arnblyopone sp. (Ward 1983; Peeters 1987; Peeters and Crewe 1985; Ito 1991, 1993a). Worker reproduction
214 Psyche [vo~. 101
Queens 0 Workers
10 Head width
8 Pronotum width
o . . . . . . . . . . . . . . .
in Platythyrea has been reported in five African species, Platythyrea brevidentata, P. cribrinodis, P. schultzei, P. lamellosa, and P. arnoldi (Villet 1990, 1992a, 1993). Except for P. arnoldi, colony of these species contain one garnergate. In the Oriental tropics, the social organization of Platythyrea species has been lit- tle studied.
In Platythyrea tricuspidata and P. quadridenta, mated workers reproduce sexually in West Malaysia. In this study, most colonies contained multiple mated workers, but only a few laid eggs in each colony. The same situation was found in an Indonesian species of Pachycondyla (=Bothroponera) (Ito 1993b). In this case, there is a dominance hierarchy through frequent aggressive antennation, in which one dominant mated worker laid eggs, while low-ranked mated workers were sterile (Ito 1993b). The mechanism regulating oviposition by mated workers in Platythyrea tricuspidata and P. quadridenta is unknown, however, dominance behaviour is a possi- bility. Unlike some queenless species having multiple gamergates such as Rhytidoponera sp. 12 (Peeters 1987), the presence of ster- ile mated workers in Malaysian Platythyrea spp. and Indonesian Pachycondyla (=Bothroponera) sp. indicates that insemination is not always associated with ovarian development, as pointed out in Amblyopone sp. (Ito 1993a) and Ophthalmopone berthoudi (Villet 1992b).
As already reported for P. arnoldi (Villet 1993), P. quadridenta produced alate queens, and one mated dealate queen was found. Queens were not discovered in the colonies of Platythyrea tricusp- idata, but the type specimen of P. tricuspidata subsp. penangensis Wheeler, described from Penang, north Malaysia, is a dealate queen (cited in Brown 1975). Intensive collection may yet provide evidence of queen production in P. tricuspidata. Queens of P. quadridenta were produced in only two colonies which were largest in my collected colonies. This is consistent with characteristics of sexual production in several ant species, in which small colonies produced workers only while large colonies produced queens and males (Holldobler and Wilson 1990). Colony size may be proximate factor for queen production in P. quadri- denta.
Fig. 1. Frequency distribution of body size in queens and workers of Platythyrea quadridenta. 60 = 1 mm.
216 Psyche [vo~. 101
Among ponerine species in which only queens reproduce sexu- ally, queens have a wider IVth abdominal segment than workers (Ito and Ohkawara 1994). Although the number of ovarioles in queens is usually the same as in workers, the width of the sper- matheca is remarkably larger in queens than in workers (Ito and Ohkawara 1994). In comparison, the dimorphism in these charac- ters between female castes was weak in P. quadridenta, suggesting that reproductive specialization between the two castes is less developed. The important difference between the queens and the workers may be mode of colony proliferation: workers may found their colonies only by colonial budding while queens may be able to start their colonies by independent colony foundation, although this has not been confirmed in the field. The significance of sexual reproduction by both queens and workers is suggested in Rhytidoponera metallica, in which repro- duction is mostly performed by mated workers (Haskins and Wheldman 1965), although a small number of alate queens are sometimes produced. Ward (1986) reported in this ponerine ant that a dealate queen could start a new colony independently, and after the queen's death, several workers showed sexual calling behaviour under the queenless condition in the laboratory. This observation indicates that alate queens function as a dispersal form to exploit new habitat and workers function as a non-dispersing form that continues reproduction of successful colonies established in good habitats. Further investigations of the ecology of colony foundation, particularly of the demographic characteristics of colonies founded by queens independently and of colonies founded by workers cooperatively, and of mechanisms regulating queen production are necessary to further our understanding of sexual reproduction by both workers and queens in ponerine ants. I thank C. Peeters and M. Villet for comments on the manuscript and improving English text, H. S. Yong and members of Ulu Gom- bak field station for help in field study and S. Higashi and H. Fukuda for encouragement. This work was supported in part by a Grant-in-Aid for JSPS Fellows from the Ministry of Education, Science and Culture, Japan.
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