Social Structure and Reproductive Systems of Tramp Versus Endemic Ants (Hymenoptera: Formicidae) of the Ryukyu Islands!

Home , Ochetellus, Pheidole fervens, Strumigenys lewisi

KATSUSUKE YAMAucm 2 AND KAzuo OGATA 3

ABSTRACT: Currently, 126 ant species have been recorded from the Ryukyu Islands, Japan. Of these, 54 species, many of which are probably new to sci ence, have not yet been identified. A survey on species-habitat relationships made on the island of Okinawa indicated that open lands were occupied pre dominantly by tramp species, but primary forests contained many endemic species. Colony structure and the reproductive system of the eurychoric species are briefly reviewed and discussed. A secondary polygynous and polydomous system is predominant in these species. This system is characterized by intra nidal mating, which may reduce the risk in nuptial flights and ensure the adoption of new queens. A diversity in morphology and behavior, especially in males, seems to develop, provided the workers care for them. Stenochoric forest species are mostly monogynous.

THE RYUKYU ISLANDS form the southern part tramp species in terms of their social struc of the Nansei Islands, situated between 26° ture and reproductive system. and 24° N latitude, comprising the Okinawa Islands and Sakishima Islands. Because they belong to the subtropical zone, the oriental MATERIALS AND MEmODS element is dominant in ant species composi tion (Terayama 1992). In addition, there are The survey was carried out in the Oki many tramp species that have a pan-sub nawa Islands and the Sakishima Islands from tropical or tropical distribution. Such species, 1991 to 1993. as in many parts of the world (e.g., Way The objective of the first sampling method 1953, Wilson and Brown 1958, Greenslade was to determine species-habitat relation 1971; see also H611dobler and Wilson 1990), ships. In several places, time-unit sampling are thought to severely impact the native ant was carried out. As many ant species as pos fauna in this area. Thus, the preservation of sible were collected during a 30-min visual the native component of the biodiversity of manual search on the surface of the ground, an area may depend on the suppression of under stones or wood bark, and around the introduced ant species. bases of tree trunks, over a ca. 200-m 2 area. In this study, we investigated species di The intensive survey was made in Kunigami versity in various subtropical habitats of the son, the northern part of Okinawa Island, Ryukyu Islands, and we discuss the status of with the help of members of the Myrmeco logical Society of Japan in August 1991. The study sites in Kunigami-son are shown in Figure 1. 1 This study was supported in part by a research fund from the Nippon Life Insurance Foundation and by a The surveyed forests of this area consist Grant-in-Aid (No. 05640709) from the Japan Ministry of predominantly of Castanopsis cuspidata var. Education, Science, and Culture. Manuscript accepted sieboldii (Makino) and Persea thunbergii 27 April 1994. Sieb. & ZUCCo We here tentatively distinguish 2 Department of Biology, Faculty of Education, Gifu University, Gifu 501-11, Japan. a "primary" forest from a "secondary" one 3 Institute ofTropical Agriculture, Kyushu University, based on average diameter of trees at ca. 1 m Fulcuoka 812, Japan. above the ground. The primary forest con- 55 56 PACIFIC SCIENCE, Volume 49, January 1995

1-- 128°\- -::--1 KYUSHU #2 Is o~ ~~ Satsunan Islands # 11 v~ \ #1 ," {?- 28°

FIGURE 1. Map showing study sites (circles) oftime-unit sampling in the Kunigami-son area. I, Sate (coastal grass land and periphery of village); 2, Cape Redo (grass land and deforested land); 3, Benoki (a) (deforested land); 4, Ohkuni Forest Road (secondary forest); 5, Yona Experimental Forest (secondary forest); 6, Mt. Terukubi-yama (a) (secondary forest); 7, Benoki (b) (secondary forest); 8, Mt. Terukubi-yama (b) (primary forest); 9, Mt. Nishirne-dake (primary forest); 10, Mt. Yonaha-dake (primary forest); II, Benoki (c) (primary forest); 12, Benoki (d) (primary for est). Triangles indicate tops ofmountains. sists of older trees with a diameter of 60 cm which were obtained by K.Y. in field studies or larger, often having a floor of dead wood of the Sakishima Islands in 1985 for Pheidole (study sites 8-12). The secondary forest con- megacephala (F.), Tetramorium bicarinatum sists of younger trees with a diameter of 40 (Nylander), Anoplolepis longipes (Jerdon), cm or less (sites 4-7). The surveyed open and Paratrechina longicornis (Latreille) are land is represented by a Zoisia tenuifolia also given. Wild. community (site 2) or a Miscanthus si- All the voucher specimens obtained nensis Anders community (sites 1 and 3). All throughout the study are deposited in the In sites were more or less developed and dis- stitute of Tropical Agriculture, Kyushu Uni- turbed by human activities. versity, Fukuoka, Japan. The objective of the second sampling , method was to determine the colony structure and reproductive system. To accomplish this, the whole colony was excavated and the RESULTS of queens was counted for as many number Status ofStenochoric and Endemic Species species as possible. Among polygynous spe Versus Eurychoric and Tramp Species cies, several nests of Hypoponera bondroiti (Forel), Cardiocondyla wroughtonii (Forel), Including this survey, we have counted Cardiocondyla sp. 1, Cardiocondyla sp. 2, and 126 species from the Ryukyu Islands. This several nest fragments of Technomyrmex al number is about 75% of the total number of bipes (Fr. Smith) were sampled and reared in species from the Nansei Islands and about the laboratory of K.Y. for behavioral and half of the total number of Japanese species. morphological studies. A complete list will be presented elsewhere In addition, findings on social structure, (K.O., unpubl. data). One of the impedi-

eM" """ 'WGf )~emw'¥iF--W;ihiidfi'!!imif6FW ,E2U!iiJ1.&!i!Eidiii&S5S¥,biiC;'M Tramp vs. Endemic Ants in the Ryukyus-YAMAUCHI AND OGATA 57

TABLE 1 TABLE 1 (continued)

ANTS FOUND IN KUNIGAMI-SON, OKINAWA ISLAND *50. Strumigenys sp. 1 [kakugao)a 51. Strumigenys sp. 2 [hakake)a Ponerinae *52. Smithistruma leptothrix (Wheeler) 1. Amblyopone si/vestrii (Wheeler) 53. Smithistruma sp. [maruge)a *2. Proceratium japonicum Santschi 54. Pentastruma sauteri Forel 3. Discothyrea sp. [medaka)a 55. Epitritus hexamerus Brown *4. Ectomomyrmex javanus Mayr *5. Brachyponera chinensis Emery Dolichoderinae *6. Trachymesopus pi/osior (Wheeler) *56. Ochetellus itoi (Fore!) *7. Cryptopone sauteri (Wheeler) *57. Tapinoma melanocephalum (F.) *8. Cryptopone sp. [hanadaka)a 58. Tapinoma sp. [konuka)a *9. Ponera sp. 1 [minami-hirne)a *59. Technomyrmex albipes (Fr. Smith) 10. Ponera sp. 2 [arehada-hirne)a Formicinae 11. Ponera sp. 3 [hoso-hirne)a *60. Anoplolepis longipes (Jerdon) 12. Hypoponera bondroiti (ForeI) *61. Paratrechinajiavipes (Fr. Smith) *13. Hypoponera sauteri (ForeI) *62. Paratrechina longicornis (Latreille) 14. Hypoponera sp. [beppin)a *63. Paratrechina sp. (nr. bourbonica)b *15. Leptogenys confucii Forel *64. Camponotus sp. 1 [kebuka-ameiro)a *16. Odontomachus monticola Emery *65. Campono/us sp. 2 [hoso-umematsu)a Cerapachyinae 66. Campono/us sp. 3 [aka-hirazu)a 17. Cerapachys biroi Forel *67. Campono/us sp. 4b 68. Polyrhachis dives Fr. Smith Dorylinae 18. Aenictus lifuiae Terayama NOTE: Asterisks indicate species collected by time-unit Leptanillinae sampling. 19. Protanilla sp. [juzufushi)a a Japanese name (in brackets) follows Mynnecological Soci ety of Japan (1989, 1991, 1992). Pseudomyrmecinae b Unidentified species not shown in Mynnecological Society 20. Tetraponera sp. [oo-nagfushi)a ofJapan guides. Myrmicinae *21. Aphaenogaster sp. [ryukyu-ashinaga)a *22. Pheidole fervens Fr. Smith ments in studying the fauna of this region is *23. Pheidole indica Mayr the high ratio of undescribed species (see 24. Pheidole megacephala (F.) Ogata 1992): 54 species (42.9%) have not *25. Pheidole pieli Santschi been described. The treatment of such species *26. Leptothorax sp. [kiiro-muneboso)a follows that of the Myrmeco10gical Society *27. Cardiocondyla nuda (Mayr) 28. Cardiocondyla wroughtonii (Forel) of Japan (1989, 1991, 1992). 29. Cardiocondyla sp. 1 [hirne-hadaka)a The results of the Kunigami-son survey 30. Cardiocondyla sp. 2 [usukiiro-hadaka)a are shown in Table 1, in addition to the spe *31. Tetramorium bicarinatum (Nylander) cies already recorded and those collected by *32. Tetramorium lanuginosum Mayr *33. Tetramorium nipponense Wheeler general sampling. In total, 68 species are *34. Tetramorium simillimum (Fr. Smith) known from this area. The land area of Ku 2 *35. Monomorium chinense Santschi nigami-son is 194 km , and this size is about 36. Monomoriumjioricola (Jerdon) median between that of Miyako-jima Island *37. Monomoriumfossulatum Emery 2 (148 km ) of the Sakishima Islands and To *38. Monomorium intrudens Fr. Smith 2 39. Monomorium pharaonis (L.) kuno-shima Island (248 km ) ofthe Satsunan *40. Solenopsis sp. [okinawa-tofushi)a Islands. But the species diversity of Kuni *41. Oligomyrmex sauteri Forel gami-son is far richer than that of both those *42. Oligomyrmex sp. [oni-kotsuno)a islands (43 spp. in Miyako-jima, 45 spp. in *43. Vollenhovia sp. 1 [yanbaru-umematsu)a 44. Vollenhovia sp. 2 [okinawa-umematsu)a Tokuno-shima [Terayama 1992]). 45. Myrmecina sp. [kogata-kadofushi]" The number of species collected by the *46. Pristomyrmex pungens Mayr time-unit sampling method was 41. They are *47. Crematogaster laboriosa Fr. Smith divided into two types based on the range of 48. Crematogaster vagula Wheeler distribution: (1) eurychoric species: those 49. Strumigenys lewisi Cameron having a wide geographic distribution, here 58 PACIFIC SCIENCE, Volume 49, January 1995 including ones occurring throughout the humans called tramp species; (2) stenochoric whole Oriental Region or beyond; in partic species: those having a narrow geographic ular, the species expanding by human com distribution, here including species endemic merce and living in close association with to the Ryukyus and ones occurring ex-

TABLE 2 DISTRIBUTION TYPES, HABITATS, AND COLONY STRUCTURE OF 41 SPECIES COLLECTED BY TiME-UNIT SAMPLING IN KUNIGAMI-SON, OKINAWA

b STUDY SlTE

TYPE DISTRIBUTION" SPECIES OL SF PF COLONY STRUCTURE'

Eurychoric Brachyponera chinensis 3 4,5 8,9,10,12 Polygynous (83.3%) species Pristomyrmex pungens 7 T Technomyrmex albipes 3 4,5,6 12 Pheidole indica 2 T Cardiocondyla nuda 2 T Tetramorium bicarinatum 1,2,3 T Tetramorium lanuginosum 1,2 T Tetramorium simil/imum 1,2 Monomorium chinense 1,2 T M onomorium fossulatum 2 Monomorium intrudens 1 T Tapinoma me/anocepha/um 1,2 T Anoplolepis longipes 2 6 T Paratrechina longicornis 2 T Pheidole fervens 1 4,5,7 8,10,11,12 Paratrechina flavipes 3 5,7 9,10,11 Monogynous (16.7%) Paratrechina sp. 1,3 4 Ochetellus itoi 2 Stenochoric Pheidole pieli 6 8,9,10 Polygynous (17.4%) species Tetramorium nipponense 6 12 E Vollenhovia sp. 1 8,10 E Cryptopone sp. 10,11,12 Solenopsis sp. 11 Unknown (13.0%) Strumigenys sp. 1 12 Odontomachus monticola 4,5 9,10,11,12 Ponera sp. 1 5,6,7 10 Monogynous (69.6%) Leptogenys confucii 12 Leptothorax sp. 7 Camponotus sp. 1 5 Camponotus sp. 4 7 Smithistruma leptothrix 3 12 Oligomyrmex sauteri 6 11 E Oligomyrmex sp. 6 12 Proceratium japonicum 9 Cryptopone sauteri 9 Ectomomyrmex javanus 11 Hypoponera sauteri 4 10 E Aphaenogaster sp. 7 Crematogaster laboriosa 2 Camponotus sp. 2 2 Trachymesopus pi/osior 2

"E, species endemic to the Ryukyus (or believed to be so); T, tramp species. • Study sites identified in Figure I. OL, open land; PF, primary forest; SF, secondary forest. 'Percentages of polygynous, monogynous, and unknown species are given for eurychoric species and stenochoric species, respectively.

""h l Ie 'E'ftIN£SLQi!U!i'MRM apia; • 4 Tramp vs. Endemic Ants in the Ryukyus-YAMAucm AND OGATA 59

No. of spp. .------, 15 - Number of species

% Proportion of eurychoric species 100 • Eurychoric spp. 80 o Stenochoric spp.

20 o 2 3 4 5 6 7 8 9 10 11 12 Study site ~ ~ .Open .Secondary • Primary • land forest forest

FIGURE 2. The number of species and proportion of eurychoric species in each study site. Study sites identified in Figure 1. clusively in the Indo-Chinese Subregion, or have a lower proportion of these species. In eastern part of Asia (i.e., Korea, eastern stead, that habitat contained many sten China, Japan, Taiwan). Table 2 shows the ochoric species including several undescribed types of distribution of the 41 species col ones such as Aphaenogaster sp., Oligo lected by the time-unit sampling from the myrmex sp., and Vollenhovia sp. 1, which Kunigami-son area with their colony struc seem to be endemic to the Ryukyus. ture. The ratio of these types in each habitat is Social Structure and Reproductive Systems in shown in Figure 2. Most open lands were Polygynous Species predominantly occupied by eurychoric spe cies, including distinctive tramp species such In this paper, we show just an outline of as Cardiocondyla nuda (Mayr), Tetramorium our results, because the main purpose of the bicarinatum, Technomyrmex albipes, and An paper is to discuss social and reproductive oplolepis longipes. However, primary forests characteristics of stenochoric and endemic A Tetramorium bicarinatum c Anoplolepis longipes o ',-,q $1 \ 0 0 '0 0 ./o .,•••.." ••••[Q]. 0 OJ /' o NESTS ~""7C@CJi;J'$f '''-0<,!;,., ."'.... ,0i------'"~--,O..m-- --....0'..--..--,....' 0 ANT ROUTES ,.: .: "'[J'l 0 SCHOOL BUILDING . 0," I );D:::--._-.... ~ o I -\lX0------Cb------ev--- o o TREES

6 F~EReEO o NESTS ~5 I -~--_. _ o ~---- hUm--u(i)--'®0 ANT ROUTES 3 . ; ROAD

LAWN 5m

B Pheidole megacephala D Paratrechina longicornis • NESTS ;/

f~ TERRACE IIII PARKING LOT ~'"""'U ~ /. ~ j( ROAD ~ I I I \/\ .... __ I I ':,'DI, A: '\ ~'\U~' '-_../1"""'/\~ GARDEN II GARDEN ". \/'0§J ~ , 2 3 4 l DECAYED WOOD ", ~ BLACK PART: NEST \ . ~,-= \ PARKING LOT 6- ~ r=::::/ 1m 10m ROAD Tramp vs. Endemic Ants in the Ryukyus-YAMAUCHI AND OGATA 61

versus eurychoric and tramp species. More mated with winged and wingless females in detailed results will be given in separate pa side the nest. pers. Cardiocondyla sp. 2 has dimorphic males, The results of the queen number survey winged and wingless. The mandibles of the are given in Table 2. Here, Odontomachus latter are sickle-shaped, as are those of C. monticola Emery was monogynous in three wroughtonii. Wingless males fought one an colonies in our survey, but three queens were other until one of the pair was killed. Both obtained from a single colony (K. Tsuji, pers. winged and wingless males mated with comm.). Its status is still unclear. winged queens inside the nest. From the field observations, it was deter In Technomyrmex albipes, both males and mined that Pheidole megacephala, Tetra females show dimorphism: winged and morium bicarinatum, Anoplolepis longipes, wingless. Wingless males mate with wingless and Paratrechina longicornis form poly females inside the nest, and winged males domous colonies in the Nansei Islands (Fig mate with winged females outside the nest ure 3). In these species, many nests were (Yamauchi et al. 1991a). Morphological connected with distinct ant routes. In a col studies revealed that the copulatory organs of ony, several nests contained multiple queens. wingless sexuals were approximately half the The laboratory observations revealed that size of those of winged sexuals in this species in Hypoponera bondroiti, Cardiocondyla nuda, (Figure 4). Crossmating should be impossible Cardiocondyla sp. I (sp. 3 of Myrmecological between winged and wingless sexuals in this Society of Japan [1992]), and Cardiocondyla species. However, in Hypoponera bondrioti, sp. 2 (sp. 5 of Myrmecological Society of Hypoponera sp. (sp. 4 of Myrmecological Japan [1992]) there was no hostility among Society of Japan [1989]; from Honshu, Ja workers from neighboring nests, suggesting pan), and Cardiocondyla sp. 1, in which di that these species are also polydomous (KY., morphic males mate with the same kind of B. Corbara, K Kinomura, and K Tsuji, un females, size differences in male copulatory publ. data, for H. bondroiti; W. Czechowski organs between dimorphic males were much and KY., unpubl. data, for C. nuda). smaller: the mean copulatory organ size of Mating behavior was studied mainly in winged males (or major wingless males) was the laboratory, with a few field observations: 1.2 times less than that of wingless males (or mating pairs were observed inside the nests of minor wingless males) in each species (KO., Pheidole megacephala and Tapinoma mela K Murai, K. Tsuji, and KY., unpubl. nocephalum (F.). data). In Hypoponera bondroiti, nests of which often contained multiple wingless queens, all males were wingless, but they showed size DISCUSSION dimorphism: major and minor males. Each Status ofStenochoric and Endemic Species type of males fought with others of the same Versus Eurychoric and Tramp Species in type, resulting in either a single male of one the Ryukyus size per nest or a pair (major and minor) per nest. No fighting was observed between ma The tendency of the stenochoric species to jor and minor males. Both types of males be found in forests and the eurychoric species

... FIGURE 3. Distribution of nests, ant routes, and number of queens in each nest. A, Tetramorium bicarinatum nested under ground on grass lawn of Kohama-jima Island (Sakishima Islands) (August 1985). D, Pheidole megace phala nested in and under decayed wood at a herbaceous beach of Kohama-jima Island (August 1985). C, Anoplole pis longipes nested under decayed wood, empty cans, empty bags, and other materials in a secondary forest of Irio mote Island (Sakishima Islands) (August 1985). D, Paratrechina longicornis nested in spaces between slates, stones, and bark and stem of trees at City Hall of Ishigaki-jima Island (Sakishima Islands) (August 1985). Numerals in A, D, and Cshow queen number. Numerals in D show nest code: nests 1-7,9, and 10 had 35, 8, 21, 69, 273,4,1,35, and 4 dealated queens, respectively. 62 PACIFIC SCIENCE, Volume 49, January 1995

FIGURE 4. Copulatory organs of Technomyrmex albipes (dorsal view). A, winged male; B, wingless male. Scale, 100 Jilll.

to be observed in open land can be seen in The same tendency was shown by Wilson many islands of the Ryukyus. For example, (1959) in New Guinean ant fauna. He dis the well-known tramp species Pheidole meg cussed this trait in terms of dispersal history, acephala, Monomorium pharaonis (L.), and and later (Wilson 1961) proposed the taxon Cardiocondyla wroughtonii are also common cycle hypothesis. Although we cannot iden in open land throughout the Ryukyus. Phei tify the evolutionary stage of each species dole megacephala is predominant along the because of poor phylogenetic information, seashore. Polyrhachis dives Fr. Smith is still Wilson's species of "stage I," or "the species expanding its distribution in Okinawa (Ta apparently in the process of expansion," cor kamine 1987). These tramp species have in responds to our eurychoric species. In the vaded some secondary forests, but only following discussion we focus on the social rarely primary forests. In contrast, all four of structure and reproductive system ofthe eury the recently described endemic species (Am choric species. blyopone fulvide Terayama, Probolomyrmex okinawaensis Terayama & Ogata, P. long Secondary Polygyny-An Important inodus Terayama & Ogata, and Pheidole Characteristic ofthe Majority ofTramp ryukyuensis Ogata) were obtained from dense Ant Species forests (Ogata 1982, Terayama 1987, Ter ayama and Ogata 1988). These results sug Polygyny is not a rare phenomenon in ant gest that it is especially important to preserve societies. The ratio of the species that have the primary forests for protection of native polygynous colonies is about 50% in Europe ant species in the Ryukyus. Without primary (Bourke 1988), 52.4% in Okinawa, and forests, there will be a diversity of tramp ant 53.1% in Honshu, Japan (K.Y., Y. Ito, and species, but fewer endemic species. K. Kinomura, unpubl. data). The ratio in

M Tramp vs. Endemic Ants in the Ryukyus-YAMAucm AND OGATA 63 eurychoric species, especially in the tramp remover of deleterious genes through natural species, is conspicuously high, whereas the selection, and females enjoy a lower prob endemic or stenochoric species are mostly ability of the expression of the deleterious monogynous. The proportion of polygynous genes in haplodiploid organisms (Matsuda species (including ones that have multiple re 1987). Haplodiploidy seems to be a genetic productive intercastes or workers) exceeds basis for frequent intranidal mating (prob 80% in the eurychoric species in the study ably most of them are inbreeding, but see area (Table 2). Among these polygynous Kaufmann et al. [1992]), which might be species, it is known that new queens (or re widespread in the mating systems of ants, es productive intercastes or workers) are reg pecially of secondary polygynous ones (e.g., ularly adopted by the mother colony (sec Hypoponera spp. [Le Masne 1956, Hamilton ondary polygyny) in Pristomyrmex pungens 1979; KY., B. Corbara, K Kinomura, and Mayr (Tsuji 1988), Cardiocondyla nuda K Tsuji, unpubl. data], Cardiocondyla spp. (yamauchi and Kinomura 1993), Techno [Stuart et al. 1987, Heinze et al. 1993, Ya myrmex albipes (Yamauchi et al. 1991a), for mauchi and Kinomura 1993], Epimyrma spp. example. Secondary polygyny may also be [Buschinger 1989], Technomyrmex spp. found in the other species. [Terron 1972, Yamauchi et al. 1991a], Lasius The adaptive significance of secondary spp. [Yamauchi et al. 1981, Loon et al. 1990], polygyny may be characterized by the fol etc.). lowing: (1) high risk of colony fragmentation Intranidal mating reduces the risk in because of frequent nest destruction or fre volved in nuptial flight and ensures the quent nest relocation (i.e., most fragmented adoption of new queens for the mother nests. colonies can multiply if there is at least some It has also been suggested that secondary survival among queens or reproductive inter polygyny is correlated with independent castes); (2) no ceiling on egg production (i.e., foundation of queens (Keller 1991). The spe the egg production of a colony increases). cies with this type of mating may multiply in Therefore, the size ofthe colony grows. Thus, new places if a queen or a colony fragment secondary polygynous species, usually asso settle there. Moreover, wingless males are ciated with polydomy, can live successfully in advantageous if they do not perform extra frequently disturbed environments and/or in nidal mating, because the colony can reduce habitats that are long-lasting, patchily dis the investment cost for males. For example, tributed, and large enough to support large the weight of the wingless male is approx populations (Holldobler and Wilson 1977; imately half that of the winged male in Car see also Nonacs 1988). They often occupy an diocondyla sp. 1 (Yamauchi and Kinomura area in high density, which makes for a 1993). Moreover, sex ratios are highly fe higher probability of victory in competition male-biased in Cardiocondyla spp. (Kino with other ant species (Higashi and Ya mura and Yamauchi 1987, Yamauchi and mauchi 1979, Yamauchi et al. 1981, 1982). Kinomura 1993) and Technomyrmex albipes Among eurychoric species of the study (Yamauchi et al. 1991a). Therefore, it is not area, only Paratrechina spp. and Ochetellus surprising that wingless males have evolved itoi (Forel) are monogynous. Paratrechina sp. where intranidal mating was established. In (near bourbonica [Forel]) is an excellent fact, wingless males occur in phylogenetically pioneer species. It first appears in bare culti diverse genera such as Hypoponera (poner vated land and in river terraces after flooding, inae), Anergates, Cardiocondyla, Formico for example. xenus (Myrmicinae), Technomyrmex (00 lichoderinae), and Plagiolepis (Formicinae). Intranidal Mating and Wingless Males Inside the nest, males ate taken care ofby toe workers. Therefore, males are relatively free Widespread in Secondary Polygynous Species from natural selection such as predatory Because deleterious genes are more likely pressure. In such a condition, diverse sexual to be expressed in haploids than in diploids, a behavior might have evolved. For example, population ofhaploid males acts as anefficient wingless males of Hypoponera punctatissima 64 PACIFIC SCIENCE, Volume 49, January 1995

(Roger) (Hamilton 1979), H. bondroiti (KY., Technomyrmex albipes. In these species, in B. Corbara, K Kinomura, and K. Tsuji, un tra- and extranidal routes are taken by wing publ. data), and Cardiocondyla spp. (Stuart less and winged sexuals, respectively. In the et al. 1987, Heinze et al. 1993, Yamauchi and former species, crossmating between winged Kinomura 1993) fight one another to mo and wingless sexuals is still possible in the nopolize the nest in which new queens laboratory, but it seems to be rare because of emerge and mate. In C. wroughtonii, wingless the difference in their emergence period (KY., males kill the rival males by manipulating the pers. obs.). In the latter species, however, be nestmate workers with "bite-inducing pher havior and morphology are so differentiated omone" (Yamauchi and Kawase 199Z). In between winged and wingless sexuals that Hypoponera eduardi (Forel) (Le Masne 1956) crossmating should be impossible, despite the and Hypoponera sp. (sp. 4 of Myrmecolog overlap in their emergence period (Yamauchi ical Society of Japan [1989]; KY., pers. et al. 1991a; K.O., K Murai, K Tsuji, and obs.), wingless males mate with callow females K Yamauchi, unpubl. data). even inside the cocoon. Type IV is seen in Hypoponera bondroiti, in which all males are completely wingless but show size dimorphism. They fight one Differentiation in Colony Structure and another inside the nest, and the winner can Reproductive System among Secondary mate with both winged and wingless queens Polygynous Species there. Winged queens generally disperse and Figure 5 is a schematic illustration of typ wingless queens remain in the mother nest ical reproductive systems in polygynous and (KY., B. Corbara, K Kinomura, and K. polydomous species (excluding parasitic Tsuji, unpubl. data). Hypoponera puncta ones), showing morphological differentiation tissima (tramp species [Taylor 1967]) belongs in sexuals. to this type, although male dimorphism is not Type I is the most basic type among polyg known. ynous and polydomous species: the sexuals Type V is represented by Cardiocondyla are winged, and they have alternative mating wroughtonii and Cardiocondyla spp. (spp. 3 tactics: if both sexuals are produced in the 5 of Myrmecological Society of Japan [1992]; same nest during the same period, they mate Yamauchi and Kinomura 1993). In these inside the nest (or very near the nest en species, nuptial flight is reduced. Winged and trance), whereas they flyaway to mating wingless males engage in intranidal mating, places in the absence of counter sexuals. La although the former leave the nest if there are sius sakagamii Yamauchi & Hayashida few or no winged queens. Some of the mated (Yamauchi et al. 1991b) and Formica lugubris queens remain in the nest, but the majority Zetterstedt (temporary social parasite) undertake dispersal flights only after intra (Cherix et al. 1991) are representative exam nidal mating. ples. Type VI is seen in Cardiocondyla nuda and Type II may be a modification of type I: probably many other Cardiocondyla species nuptial flight is reduced here. Lasius neglectus (Heinze et al. 1993, Yamauchi and Kino Loon, Boomsma & Andrasfalvy probably mura 1993). In this type, all males are com belongs to this type (Loon et al. 1990). Many pletely wingless, and mating is conducted in of the best-known tramp species, including side the nest. Most mated winged queens Monomorium pharaonis, Pheidole mega were observed to flyaway for independent cephala, Linepithema humile (Mayr) (for colony foundation only after intranidal mat merly Iridomyrmex humilis [Mayr]), and ing. Wasmania auropunctata (Roger) (see H811 In addition to this kind of sexual re dobler and Wilson 1977) belong to type I or production, asexual reproduction is known in II. the eurychoric Pristomyrmex pungens and Type III is seen in Hypoponera sp. (sp. 4 of Cerapachys biroi Forel. These two species Myrmecological Society of Japan [1989]) and have no queen caste, and the workers pro-

fa 1M. 1M II -T- Inseminated queen ~ virgin winged queen -T--T- '1''1 c1"c1" T inseminated wingless queen fH Dispersal of -T- -T- Y virgin wingless queen BR 1 worker I 1M ~ RQ ~ c1" winged male C~ IF 0' wingless male -t• PO BR brood Reduced nuptial flight TYPE I

/'.-.----(-8--1--)----...... NEST ITT exua season ~ ¥ F~~-----h" BR c1" c1" Nuptial flight (NF) ---+ Independent Intranidal mating (1M) (Outbreeding) colony (Inbreeding) +-1- J -T- -T- foundation l Retention of -T- -T- (RQ) Adopllon of (IF) ..I Colony budding (CB) ---+ Polydomous colony (PO)

Dimorphism in both sexuals Dimorphism in males III V

TT ~~ -T--T- NF c1"c1" ~IF ¥ ¥ NF 11 ~H c1"c1" 1 BR 0'0' /' BR F?10'0' Dispersal IF IM_RQ 1M RQ flight (OF)

CB PO CB PO

Dropout of nuptial flight Dropout of nuptial flight , IV , VI

TT ~~ ~ ~ ~~ F~~ -IF ~~DF_IF BR }IM 1-+0F F I 1M ~RQ 11M - RQ \.. "CB • PO

FIGURE 5. Various types of colony structures and reproductive systems in secondary polygynous species. 66 PACIFIC SCIENCE, Volume 49, January 1995

duce diploid eggs that develop into workers competition in insects. Academic Press, by thelytokous parthenogenesis (Tsuji 1988, New York. Tsuji and Yamauchi 1990). HEINZE, J., S. KUHNHOLZ, K. SCHILDER, and Thus, the majority of the tramp ant spe B. HOLLDOBLER. 1993. Behavior of erga cies seemed well adapted for rapid territory toid males in the ant, Cardiocondyla nuda. expansion by virtue of their specific colony Insectes Soc. 40: 273-282. structure (secondary polygyny) and re HIGASHI, S., and K. YAMAUCHI. 1979. In productive system (using intranidal mating, fluence of a supercolonial ant Formica colony budding together with nuptial or dis (Formica) yessensis Forel on the distribu persal flight, independent colony founda tion ofother ants in Ishikari Coast. Jpn. J. tion), as mentioned above. In addition, an EcoL 29: 257-264. other factor is also important in migration to HOLLDOBLER, B., and E. O. WILSON. 1977. other places: most tramp species live in open The number of queens: An important trait lands where they may have many more op in ant evolution. Naturwissenschaften portunities to come in contact with human 64:8-15. activities. ---. 1990. The ants. Harvard University Press, Cambridge, Massachusetts. KAUFMANN, B., J. J. BOOMSMA, L. PASSERA, and K. N. PETERSEN. 1992. Relatedness ACKNOWLEDGMENTS and inbreeding in a French population of We thank K. Tsuji, M. Woyciechowski, the unicolonial ant Iridomyrmex humilis and unknown referees for comments on the (Mayr). Insectes Soc. 39: 195-213. manuscript, S. Azuma ofRyukyu University, KELLER, L. 1991. Queen number, mode of and the members of the Myrmecological So colony founding and queen reproductive ciety of Japan who helped us in sampling of success in ants (Hymenoptera: For ants in Okinawa. micidae). EthoL EcoL Evo!. 3: 307-316. K!NOMURA, K., and K. YAMAUCHI. 1987. Fighting and mating behaviors of di morphic males in the ant Cardiocondyla LITERATURE CITED wroughtonii. J. EthoL 5: 75-81. BOURKE, A. F. G. 1988. Worker reproduc LE MASNE, G. 1956. La signification des re tion in the higher eusocial Hymenoptera. producteurs apteres chez fourmis Ponera Q. Rev. BioI. 63:291-311. eduardi ForeL Insectes Soc. 3: 239-259. BUSCHINGER, A. 1989. Evolution, speciation, LOON, A. J. VAN, J. J. BOOMSMA, and A. and inbreeding in the parasitic ant genus ANDRASFALVY. 1990. A new polygynous Epimyrma (Hymenoptera, Formicidae). J. Lasius species (Hymenoptera, Formicidae) EvoL BioI. 2: 265-283. from central Europe. I. Description and CHERIX, D., D. CHAUTEMS, D. C. FLETCHER, general biology. Insectes Soc. 37: 348 W. FORTELIUS, G. GRIS, L. KELLER, L. 362. PASSERA, R. ROSENGREN, E. L. VARGO, MATSUDA, H. 1987. Conditions for the evo and F. WALTER. 1991. Alternative re lution of altruism. Pages 67-80 in Y. Ito, productive strategies in Formica lugubris J. L. Brown, and J. Kikkawa, eds. Animal Zett. (Hymenoptera, Formicidae). EthoL societies: Theories and facts. Japan Scien EcoL Evo!. Special Issue 1: 61-66. tific Societies Press, Tokyo. GREENSLADE, P. J. M. 1971. Interspecific MYRMECOLOGICAL SOCIETY OF JAPAN. 1989. A competition and frequency changes guide for the identification of Japanese among ants in Solomon Islands coconut ants (I); Ponerinae, Cerapaehyinae, Pseu plantations. J. AppL EntomoL 8: 323-349. domyrmicinae, Dorylinae and Lep HAMILTON, W. D. 1979. Wingless and fighting tanillinae (Hymenoptera: Formicidae). males in fig wasps and other insects. Pages The Myrmecological Society of Japan, 167-220 in M. S. Blum and N. A. Blum, Tokyo (in Japanese). eds. Sexual selection and reproductive ---. 1991. A guide for the identification Tramp vs. Endemic Ants in the Ryukyus-YAMAUCHI AND OGATA 67

of Japanese ants (In. Dolichoderinae and reproductive division of labor in the Jap Formicinae (Hymenoptera: Formicidae). anese queenless ant Pristomyrmex pun The Myrmecological Society of Japan, gens. Comparison of intranidal and extra Tokyo (in Japanese). nidal workers. Behav. Ecol. Sociobiol. ---. 1992. A guide for the identification 23: 247-255. of Japanese ants (lID. Myrmicinae and Tsun, K., and K. YAMAUCHI. 1990. Com supplement to Leptanillinae (Hyme parison ofcolony structure and behavioral noptera: Formicidae). The Myrmeco10g ontogeny in three extraordinary ant spe ical Society of Japan, Tokyo (in Jap cies of Japan. Pages 384-385 in G. K. anese). Veeresh, B. Mallick, and C. A. Vir NONACS, P. 1988. Queen number in colonies akatamath, eds. Social insects and the en in social Hymenoptera as a kin-selected vironment. Oxford and IBH Publ. Co., adaptation. Evolution 42: 566-580. New Delhi. OGATA, K. 1982. Taxonomic study on the ant WAY, M. J. 1953. The relationship between genus Pheidole Westwood ofJapan, with a certain ant species with particular refer description of a new species (Hyme ence to biological control of the coreid, noptera, Formicidae). Kontyu 50: 189 Theraptus sp. Bull. Entomol. Res. 44 :669 197. 691. ---. 1992. The ant fauna of the Oriental WILSON, E. O. 1959. Adaptive shift and dis region: An overview. Bull. Inst. Trop. persal in a tropical ant fauna. Evolution Agric. Kyushu Univ. 15: 55-74. 13: 122-144. STUART, R. J., A. FRANCOEUR, and R. LOI ---. 1961. The nature of the taxon cycle SELLE. 1987. Lethal fighting among di in the Melanesian ant fauna. Am. Nat. morphic males of the ant, Cardiocondyla 95: 169-193. wroughtonii. Naturwissenschaften 74: 548 WILSON, E. 0., and W. L. BROWN, JR. 1958. 549. Recent changes in the introduced popula TAKAMINE, H. 1987. Distribution of the ant tion of the fire ant Solenopsis saevissima genus Polyrhachis and the ecology of P. (Fr. Smith). Evolution 12:211-218. dives in the Ryukyu Islands. Rep. Oki YAMAucm, K., and N. KAWASE. 1992. nawa BioI. Educ. Soc. 20: 36-42 (in Jap Pheromonal manipulation of workers by anese). fighting male to kill his rival males in TAYLOR, R. W. 1967. A monographic revi the ant Cardiocondyla Wroughtonii. Nat sion of the ant genus Ponera Latreille urwissenschaften 79: 274-276. (Hymenoptera: Formicidae). Pac. Insects YAMAucm, K., and K. KINOMURA. 1993. Monogr.13. Lethal fighting and reproductive strategies TERAYAMA, M. 1987. A new species of Am of dimorphic males in the ant genus Car blyopone (Hymenoptera, Formicidae) diocondyla. Pages 373-402 in T. Inoue from Japan. Edaphologia 36: 31-33. and S. Yamane, eds. Social evolution of ---. 1992. Structure of ant communities insects. Hakuhin-sha, To1uo (in Japanese). in East Asia. I. Regional differences and YAMAucm, K., T. FURUKAWA, K. KINo species richness. Bull. Biogeogr. Soc. Jpn. MURA, H. TAKAMINE, and K. Tsun. 1991a. 47:1-31. Secondary polygyny by inbred wingless TERAYAMA, M., and K. OGATA. 1988. Two sexuals in the dolichoderine ant Techno new species of the ant genus Probolo myrmex albipes. Behav. Ecol. Sociobiol. myrmex (Hymenoptera, Formicidae) from 29: 313-319. Japan. Kontyu 56: 590-594. YAMAucm, K., K. ITO, N. SUZUKI, and T. TERRON, G. 1972. Observations sur 1es male KAMEL 1991b. Mechanism of the reten ergatoides et des males alles chez une tion of new queens in their mother nest in fourmi du genre Technomyrmex Mayr the polygynous ant Lasius sakagamii. Sci. (Hym., Form., Dolichoderinae). Ann. Fac. Rep. Fac. Educ. Gifu Univ. (Nat. Sci.) Sci. Cameroun 10: 107-120. 15:20-24. Tsun, K. 1988. Obligate parthenogenesis and YAMAucm, K., K. KINOMURA, and S. 68 PACIFIC SCIENCE, Volume 49, January 1995

MIYAKE. 1981. Sociobiological studies of ---. 1982. Sociobiological studies of the the polygynic ant Lasius sakagamii. 1 polygynic ant Lasius sakagamii. II. Pro General features of its polydomous sys duction of colony members. Insectes Soc. tem. Insectes Soc. 28: 279-296. 29: 164-174.

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