Oecologia (1999) 120:515±523
Ó Springer-Verlag 1999
Jean-Paul Lachaud á Alex Cadena Bertrand Schatz á Gabriela PeÂrez-Lachaud Guillermo Ibarra-NuÂnÄez
Queen dimorphism and reproductive capacity in the ponerine ant, Ectatomma ruidum Roger Received: 4 January 1999 / Accepted: 12 May 1999
Abstract We report here the ®rst case of queen dimorphism in a ponerine ant species. A total of 550 colonies of the Neotropical ponerine ant Ectatomma ruidum, from two natural populations in southeastern Mexico, were investigated for polymorphism and reproductive function within the queen caste. The distribution of dierent morphological traits (head and thorax widths, and scutum and alitrunk lengths) was shown to be bimodal. Thorax width and head width were signi®cantly isometric for both macro- and microgynes and thorax proportions did not change with the category of the queen. Microgynes appear as an isometric reduction of the normal queens. On average, macrogynes were found to be approximately 20% larger in size and twice as heavy as microgynes (and up to three times heavier in terms of dry weight). Their wing surface was 72% greater. There was no dierence between the two morphs in terms of their capacity to be inseminated and all dealate females present in natural colonies could be considered as true potentially reproductive queens whatever the class to which they belonged. Ovary size, number of ovarioles per ovary, and number of mature oocytes produced were signi®cantly higher for macrogynes than for microgynes, but small queens were able to function as active egg-layers. However, the number of
J.-P. Lachaud (&) á B. Schatz Laboratoire d'Ethologie et Psychologie Animale, U.M.R.-C.N.R.S. 5550, Universite Paul-Sabatier, 118 route de Narbonne, F-31062 Toulouse Cedex, France J.-P. Lachaud á A. Cadena á G. PeÂrez-Lachaud G. Ibarra-NuÂnÄez El Colegio de la Frontera Sur, Apdo. Postal 36, 30700 Tapachula, Chiapas, Mexico e-mail:
[email protected], Fax: +52-962-81015 B. Schatz School of Biological Sciences, University of Sussex, Brighton BN1 9QG, UK
egg-laying individuals was signi®cantly lower for this form, although egg-laying activity appeared to be independent of queen weight. Despite its markedly reduced reproductive capacity compared to macrogynes, the distribution of the microgyne form of E. ruidum in both studied populations was very broad, reaching one-third of all alate and dealate females and extending to onethird of all colonies. In 72.2% of the colonies where alate and/or dealate microgynes were present, both forms co-occurred. Fat content analysis results supported the idea that semi-claustral independent colony founding, typical for this species, would essentially be achieved by macrogynes, while microgynes would be adopted by established colonies. We argue that queen dimorphism in E. ruidum could represent an attractive alternative dispersal strategy for female sexuals. The small females may constitute an important reserve of potential reproductives at a very low energetic cost to the colony, the production of a macrogyne being about 7.5 times more costly than a microgyne. The signi®cantly greater `wing surface/body weight' ratio of microgynes also suggests their greater capacity for dispersion. The combination of such a capacity for microgynes, along with their ability to contribute in the production of both female morphs, including the reproductively ecient macrogynes, would contribute to insuring genetic reassortment at the population level and could explain, in part, the ecological success of E. ruidum in Neotropical zones. Key words Ponerine ants á Microgynes á Reproductive strategies á Energetic cost á Dispersal
Introduction Queen polymorphism in ants is frequently associated with the existence of dierentiated dispersal strategies and colony-founding strategies (Yamauchi et al. 1991; Heinze and HoÈlldobler 1993; Heinze and Tsuji 1995; McInnes and Tschinkel 1995; Hamaguchi and Kin-
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omura 1996). Such queen polymorphism is expressed by the co-occurrence of two or more morphologically distinct types of queens within a single species. Most cases correspond to the co-occurrence of winged queens and wingless ergatoid queens or intercastes which exhibit a somewhat atrophied thoracic morphology (Heinze and Buschinger 1987; Peeters 1991a; Heinze et al. 1992). However, in some cases, the dierent types of queen do not show conspicuous dierences in thoracic morphology, but only in size with a clear distinction between normal large queens (named macrogynes) and smaller queens (named microgynes) (HoÈlldobler and Wilson 1990). Such miniature queens are, in all cases, isometric reductions of the normal macrogynes but are, in other respects, real reproductive individuals able to produce workers and to contribute to colony development. The presence of microgynes has been reported in some species of myrmicines (Brian and Brian 1955; Elmes 1973, 1976, 1991; McInnes and Tschinkel 1995; Hamaguchi and Kinomura 1996), pseudomyrmicines (Janzen 1973), and formicines (Seifert 1991; Heinze and HoÈlldobler 1993), but no case is known to occur in ponerines, although some degree of isometric size variation has been reported in Ponera coarctata (Liebig et al. 1995) and the presence of intercastes and wingless ergatoid queens is not infrequent in this subfamily (Wheeler 1905; Peeters 1993, 1997). Between 1992 and 1994 we observed the presence of microgynes in various colonies of the ponerine ant Ectatomma ruidum Roger reared in plaster nests, under laboratory conditions, for more than 15 months following their collection. However, due to the long period of time elapsed since their collection, we were not able to determine whether the presence of miniature queens indicated true dimorphism within the queen caste or was an artifact resulting from arti®cial laboratory conditions. This question was resolved by observing the presence, the frequency, and the morphological characteristics of microgynes in a large sample of natural colonies during a 3-year collection period. An attempt was also made to determine their reproductive status and their importance in the reproductive strategies used by E. ruidum.
et al. 1990) and polygynic colonies may represent up to 40% of the total population (Lachaud et al. 1999). Between October 1994 and January 1998, a total of 550 nests, of which 498 contained one or several dealate gynes, were completely excavated from two sites in the Soconusco region of Chiapas, southeastern Mexico. The climate of this region is warm and humid with a mean temperature of 25°C and an annual rainfall up to 4751 mm, the rainy season extending from mid-April to the beginning of November. Almost half of the 52 queenless colonies (46.2%) were collected at the height of the rainy season (July± October), i.e., the period when E. ruidum suers a severe population reduction in the study region due to the frequent ¯ooding and partial or complete destruction of numerous nests (J.P. Lachaud, unpublished data). The ®rst site, located at Finca San Antonio near the archeological zone of Izapa (15 km southeast of Tapachula) corresponded to a cocoa plantation with a mean density of 4500 nests of E. ruidum per hectare. The second site, 5 km away, was located at the Experimental Station INIFAP at Rosario Izapa, an experimental coee plantation where the density reached 11,200 nests per hectare (Schatz et al. 1998). Morphological and ovarian biometrics A total of 273 dealate females were analyzed from seven samples of collected colonies (September 1995, 26 colonies; May 1996, 22 colonies; January 1997, 26 colonies; February 1997, 21 colonies; March 1997, 19 colonies; June 1997, 23 colonies; August 1997, 29 colonies). The majority of these were weighed individually after freezing (n = 230) and/or dissected (n = 219) to determine if they had been inseminated. The individual weights of all the workers from 20 colonies (10 monogynous and 10 polygynous) were also recorded. Some additional variables, like ovary length, number of ovarioles per ovary, number and length of the basal oocytes, and `presence or absence' of yellow bodies in the ovaries (as an indicator of previous oviposition, see Peeters 1987), were also recorded. In some cases, due to loss or crushing of material during dissection, not all of these variables were available for each queen; therefore, for each variable, the sample size is given along with the mean and standard error. To test for an isometric relationship between the two morphs, for a lot of 104 macrogynes and 61 microgynes, measurements (to the nearest 0.02 mm) of the maximum head width in frontal view (excluding eyes), maximum mesonotum width between tegules (corresponding to scutum width), and maximum alitrunk and scutum length were made at ´20 magni®cation, using an ocular micrometer on a binocular dissecting microscope. Additionally, a sample of the left fore and hind wings of alate queens of both types (15 macrogynes, weight range 15±22.1 mg; 22 microgynes, weight range: 5.9±10.4 mg) were mounted and examined under a microscope for surface area determination. Fat analysis
Materials and methods Biological material and study sites E. ruidum is a diurnal earth-dwelling ponerine ant which occurs in plantations and disturbed habitats as well as in damp forests, from sea level to an altitude of 1500±1600 m (Weber 1946; Brown 1958). Widely distributed from Mexico to northern Brazil (Kugler and Brown 1982), the density of the nests of this species may be very high, from 1800 to up to 11,200 nests per hectare (Levings and Franks 1982; Pratt 1989; Lachaud 1990; Schatz et al. 1998). The colonies are essentially monodomous (Jae and Marquez 1987; Breed et al. 1990; Schatz et al. 1998). The typical non-claustral colony foundation used by this species is haplometrotic (Lachaud and Fresneau 1987; J.P. Lachaud, unpublished data), but mature colonies can contain several reproductive queens (Pratt 1989; Breed
Fat content was determined for two lots of virgin alate macro- and microgynes (15 gynes each) selected at random from colonies maintained under laboratory conditions. Two additional lots of ten dealate macrogynes and ten dealate microgynes, 40 days after experimental mating in the laboratory, were also analyzed for fat content determination (insemination was veri®ed on ®ve additional controls for each morph from the same experiment). Fat content was determined gravimetrically (see Peakin 1972). After drying for 24 h at 70°C and individual weighing, each female was soaked in diethyl ether for 2±3 days, dried again for 24 h and reweighed to deduce the weight of extracted fats. Data analysis Means were compared using one-tailed unpaired Student t-tests. Fat percentages were square-root arcsine transformed (Sokal and
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Alate and dealate females of E. ruidum could easily be separated into two size classes. This separation was con®rmed by the weight distribution of dealate gynes which is clearly bimodal (Fig. 1, Table 1). In contrast, the dierentiation of dealate microgynes from workers, which have a mean weight of 7.30 0.03 mg (n =
1815), was more dicult. The overlap between worker and microgyne weight distribution was appreciable (Fig. 1) with a range of 1.9±11.2 mg for workers versus 5.4±12.1 mg for microgynes, although the dierence in mean weight between these castes was highly signi®cant (t = 9.63, df = 1881, P < 0.0001). Bimodality was also observed for the various morphological variables studied (e.g., thorax width, Fig. 2); in all cases the statistical comparison between macroand microgynes was highly signi®cant (Table 1). Nevertheless, with the notable exception of the size, no major changes in thoracic morphology were noted between microgynes and macrogynes, all of which possessed a complete set of thoracic sclerites. When thorax width was plotted against head width (see Elmes 1976, 1991), the linear models for both queen morphs were similar (Fig. 2). Slopes and coecients of the linear regressions for both data sets were tested for homogeneity
Fig. 1 Weight distributions of workers and dealate females (microgynes and macrogynes) of Ectatomma ruidum
Fig. 2 Determination of the bimodal distribution of thorax width (left) and of the isometric relation between thorax width and head width (right) for a sample of macrogynes (solid bars and squares) and microgynes (hatched bars and squares) of E. ruidum
Rohlf 1969) and a t-test applied for means comparison. A chisquare test was used to compare the proportions of macrogynes and microgynes presenting yellow bodies in their ovaries. Finally, a one-way ANOVA was used with ScheeÂ's S-test to detect the eects of the presence of yellow bodies on the dierent ovarian variables. All statistical analyses were performed using StatView SE+ Graphics-1.03 (Abacus Concepts).
Results Morphological comparison
Table 1 Comparison of the weight and representative morphological variables between macrogynes and microgynes of Ectatomma ruidum Variable
Macrogynes
Microgynes
Sample size
Mean SE
Range
Sample size
Mean SE
Range
Weight (mg)
162
17.69 0.16
12.7±22.8
68
9.01 0.17
5.4±12.1
Head width (mm)
104
1.45 0.01
1.28±1.58
61
1.24 0.01
1.18±1.30
Thorax width (mm)
104
1.49 0.01
1.30±1.74
61
1.19 0.01
1.12±1.28
Scutum length (mm)
104
1.42 0.01
1.14±1.52
61
1.15 0.01
1.06±1.24
Alitrunk length (mm)
104
3.40 0.01
3.20±3.66
61
2.83 0.01
2.64±3.00
Wing surface (mm2)
15
32.89 0.51
29.17±36.39
22
19.12 0.41
14.80±22.35
Wing surface/body weight
15
1.92 0.05
1.56±2.18
22
2.28 0.09
1.73±3.43
Statistical comparisons t = 31.626 P < 0.0001 t = 27.005 P < 0.0001 t = 31.488 P < 0.0001 t = 35.365 P < 0.0001 t = 28.791 P < 0.0001 t = 21.132 P < 0.0001 t = 16.023 P < 0.0001
518
(Sokal and Rohlf 1969) and did not dier signi®cantly from one another (F1,161 = 0.0017, P = 0.9667 and F1,161 = 0.2325, P = 0.6304, respectively). Data sets were therefore combined into one linear model (r2 = 0.933). For both micro- and macrogynes, the two morphological variables appeared highly isometric (F1,163 = 2285.149, P < 0.0001). Moreover, when both morphs were divided into two groups according to alitrunk length, the ratio `scutum length/alitrunk length' (`index A'; see Tinaut and Ruano 1992; Heinze and HoÈlldobler 1993) showed a very limited degree of variation according to the queen size evaluated on the basis of alitrunk length alone (Fig. 3; r2 = 0.061), indicating that thorax proportions did not change with the category of the queen. Both queen classes possessed three ocelli and wings or wing remnants. In all cases, wing morphology was similar, with normal long wings. Wing surface was signi®cantly higher for macrogynes than for microgynes, but, surprisingly, the ratio `wing surface/body weight' was signi®cantly greater in microgynes than in macrogynes (Table 1). Comparison of alate females of both morphs maintained in laboratory conditions (Fig. 4), showed that the dry weight of macrogynes was about three times higher than that of microgynes (t = 13.276, df = 28, P < 0.0001) and that their ratio fat/dry weight was also nearly three times higher (t = 9.904, df = 28, P < 0.0001). Despite slight dierences in the values obtained from virgin alate females and dealate females inseminated 40 days prior to analysis, no signi®cant dierence was found within each of the two morphs. Mating does not seem to have a short-term eect on the fat content level. From the 550 complete colonies collected, we obtained a total of 300 dealate microgynes distributed in 142 colonies (25.8% of the colonies) and accounting for 32.1% of the total of 935 dealate females recovered (Table 2). When alate females were also considered, the global frequency of microgynes in the population did not change appreciably: 30.7% of all the colonies (v2 = 0.938, P = 0.3328) and 35.7% of all the females collected (v2 = 2.887, P = 0.0893). Furthermore,
despite a marked dierence in nest density between the two study sites (Izapa 4500 nests/ha, Rosario Izapa 11,200 nests/ha), no dierence was found among these populations in terms of the microgyne frequency in the colonies (v2 = 0.298, P = 0.5854) or the proportion of microgynes among all the females collected (v2 = 0.699, P = 0.4033) (Izapa: 271 colonies studied, 34.5% of alate and dealate microgynes distributed in 30.3% of the colonies; Rosario Izapa: 279 colonies studied, 36.9% of alate and dealate microgynes distributed in 31.2% of the colonies). In most cases, both classes of queen were observed simultaneously within a colony: in 122 out of the 169 colonies where alate and/or dealate microgynes were present (72.2%, Table 2). Nevertheless, from 40 small colonies (11,000 nests/ha, Schatz et al. 1998) which characterizes E. ruidum in the study zone, make solitary founding costly for this species. As suggested for other polygynous ant species (Nonacs 1988; Pamilo 1991; SundstroÈm 1995), such a factor may favor philopatry among reproductive females, with adoption of newly mated queens by their mother or neighboring nests. Nevertheless, in contrast to most secondary polygynous ants Table 4 Relative energetic cost estimate for the production of microgynes versus macrogynes Macrogynes Microgynes Micro/macrogyne coecient
(SundstroÈm 1995), new colony foundation in E. ruidum is not performed by budding or pleometrotic associations (dependent type) but is known to be independent and non-claustral (Lachaud and Fresneau 1987). Thus, for newly mated queens, there may be a trade-o between attempting a haplometrotic foundation, with its associated dispersal risks, and reducing these risks through secondary polygyny although increasing the inbreeding risks at the colony and local population level (see Stille et al. 1991). To assure some genetic ¯ow into colonies, E. ruidum can apparently use two strategies: (1) outbreeding with ¯ying males from foreign colonies, and (2) by means of queen dimorphism. Whereas mating ¯ights are relatively infrequent and only occur in April±May in the study region (Lachaud et al. 1999), sexuals are present in the nests throughout the year and numerous males, which can ¯y tens of meters from their parent colony, have been found outside the nests almost all year round (J.P. Lachaud, unpublished data). Moreover, as reported in a few secondary polygynous ants (Kinomura and Yamauchi 1987; Yamauchi et al. 1991), mating within the nest, involving males from alien neighboring colonies, is easily observed under laboratory conditions (B. Schatz and J.P. Lachaud, unpublished data) and is likely to occur in the ®eld, so that a mating ¯ight may not be essential. Although such a strategy reduces inbreeding, it does not provide a solution for long-range dispersal, which would depend essentially on the greater dispersal capacity exhibited by microgynes, as suggested by the greater wing surface/body weight ratio found in this morph, indicative of the queens `¯oating' capacity. In contrast to other species showing queen polymorphism, like S. geminata (McInnes and Tschinkel 1995) or Polyrachis cf. doddi (Heinze and HoÈlldobler 1993), for which macrogynes present greater dispersal capacities, E. ruidum microgynes are likely to be the dispersive form. Presumably, microgynes ¯y away from their mother colonies and, after mating, penetrate conspeci®c colonies where they can contribute to the production of both female morphs, including the reproductively ecient macrogynes. Despite their reduced reproductive capacity compared to macrogynes, the proportionally lower cost of producing microgynes renders such a strategy a very attractive alternative colony dispersal mechanism (see Yamauchi et al. 1991). By contrast, after mating, macrogynes may show a mixed strategy: some females succeeding in founding a new colony due to their high fat reserves, while many
Alate female dry weight (A) (mg)
Alate female fat content (B) (%)
Relative energetic cost estimate (individual level) (A ´ B)
34.11 2.32 12.47 0.71 0.3656
10.42 0.49 3.73 0.13 0.3580
1 0.13 ±
522
remain to be reincorporated back into their mother or neighboring nests. If this is really the case, the relatedness between dealate macrogyne and microgyne nestmates would be expected to be lower than for dealate macrogyne nestmates alone, resulting in genetic reassortment at the population level. The possibility of queen integration into conspeci®c but non-related nests is very likely to occur under natural conditions. Such behavior has been observed on various occasions under laboratory conditions, for both microgynes and macrogynes from adult colonies (A. Cadena and J.P. Lachaud, unpublished data). Moreover, low intraspeci®c aggressiveness is characteristic of E. ruidum; the penetration of individuals into more or less distant alien colonies is a natural behavioral component of homospeci®c foodrobbing behavior commonly exhibited in this species (Breed et al. 1990, 1992; De Carli et al. 1998). Detailed ecological studies focused on population structure and dynamics, along with a genetic analysis based on microsatellite DNA polymorphism, are required, however, to test such a hypothesis. Acknowledgements We are grateful to G. Beugnon, C. Peeters, J. Valenzuela, T. Williams, P. Pamilo, and two anonymous referees for useful comments on a previous draft of the manuscript, to T. Williams for improvements to the English text, and to J.A. LoÂpez, C. Salvador, J.A. GarcõÂ a, and O.G. LoÂpez for ®eld assistance in collecting the colonies. This research was supported by grants of the ``French Science de la Cognition'' (MESR) to B.S., and the Mexican research program 0574P-N from CONACyT to J.-P.L. and G.I.-N. This work forms part of the MSc thesis of A.C., partially ®nanced by ECOSUR and CONACyT.
References Alexander B, Rozen JG Jr (1987) Ovaries, ovarioles, and oocytes in parasitic bees (Hymenoptera: Apoidea). Pan-Pac Entomol 63:155±164 Billen J (1985) Ultrastructure of the worker ovarioles in Formica ants (Hymenoptera: Formicidae). Int J Insect Morphol Embryol 14:21±32 Breed MD, Abel P, Bleuze TJ, Denton SE (1990) Thievery, home ranges, and nestmate recognition in Ectatomma ruidum. Oecologia 84:117±121 Breed MD, Snyder LE, Lynn TL, Morhart JA (1992) Acquired chemical camou¯age in a tropical ant. Anim Behav 44:519±523 Brian MV, Brian AD (1955) On the two forms macrogyna and microgyna of the ant Myrmica rubra L. Evolution 9:280±290 Brown WL Jr (1958) Contributions toward a reclassi®cation of the Formicidae. II. Tribe Ectatommini (Hymenoptera). Bull Mus Comp Zool Harv 118:173±362 De Carli P, Lachaud JP, Beugnon G, LoÂpez MeÂndez JA (1998) Etudes en milieu naturel du comportement de cleptobiose chez la fourmi neÂotropicale Ectatomma ruidum (Hymenoptera, Ponerinae). Actes Coll Insectes Soc 11:29±32 DuÈssmann O, Peeters C, HoÈlldobler B (1996) Morphology and reproductive behaviour of intercastes in the ponerine ant Pachycondyla obscuricornis. Insectes Soc 43:421±425 Elmes GW (1973) Miniature queens of the ant Myrmica rubra L. (Hymenoptera, Formicidae). Entomologist 106:133±136 Elmes GW (1976) Some observations on the microgyne form of Myrmica rubra L. (Hymenoptera, Formicidae). Insectes Soc 23:3±22 Elmes GW (1991) Mating strategy and isolation between the two forms, macrogyna and microgyna, of Myrmica ruginodis (Hym., Formicidae). Ecol Entomol 16:411±423
Goss S, Fresneau D, Deneubourg JL, Lachaud JP, ValenzuelaGonzaÂlez J (1989) Individual foraging in the ant Pachycondyla apicalis. Oecologia 80:65±69 Hamaguchi K, Kinomura K (1996) Queen-size dimorphism in the facultatively polygynous ant Leptothorax spinosior (Hymenoptera: Formicidae). Sociobiology 27:241±251 Heinze J, Buschinger A (1987) Queen polymorphism in a nonparasitic Leptothorax species (Hymenoptera: Formicidae). Insectes Soc 34:28±43 Heinze J, HoÈlldobler B (1993) Queen polymorphism in an Australian weaver ant, Polyrhachis cf. doddi. Psyche 100:83±92 Heinze J, Tsuji K (1995) Ant reproductive strategies. Res Popul Ecol 37:135±149 Heinze J, HoÈlldobler B, Cover SP (1992) Queen polymorphism in the North American harvester ant, Ephebomyrmex imberbiculus. Insectes Soc 39:267±273 HoÈlldobler B, Wilson EO (1990) The ants. Belknap, Cambridge, Mass Ibarra-NuÂnÄez G (1990) Los artroÂpodos asociados a cafetos en un cafetal mixto del Soconusco, Chiapas, MeÂxico. I. Variedad y abundancia. Folia Entomol Mex 79:207±231 Iwata K, Sakagami SF (1966) Giantism and dwar®sm in bee eggs in relation to the modes of life, with notes on the number of ovarioles. Jpn J Ecol 16:4±16 Jae K, Marquez M (1987) On agonistic behaviour among workers of the ponerine ant Ectatomma ruidum (Hymenoptera: Formicidae). Insectes Soc 34:87±95 Janzen DH (1973) The evolution of polygynous obligate acaciaants in western Mexico. J Anim Ecol 42:727±750 Keller L, Passera L (1989) Size and fat content of gynes in relation to the mode of colony founding in ants (Hymenoptera; Formicidae). Oecologia 80:236±240 Kinomura K, Yamauchi K (1987) Fighting and mating behaviors of dimorphic males in the ant Cardiocondyla wroughtoni. J Ethol 5:75±81 Kugler C, Brown WL Jr (1982) Revisionary & other studies on the ant genus Ectatomma, including the descriptions of two new species. Search Agric 24:1±7 Lachaud JP (1990) Foraging activity and diet in some neotropical ponerine ants. I. Ectatomma ruidum Roger (Hymenoptera, Formicidae). Folia Entomol Mex 78:241±256 Lachaud JP, Fresneau D (1987) Social regulation in ponerine ants. Experientia [Suppl] 54:197±217 Lachaud JP, LoÂpez-MeÂndez JA, Schatz B, De Carli P, Beugnon G (1996) Comparaison de l'impact de preÂdation de deux poneÂrines du genre Ectatomma dans un agroeÂcosysteÁme neÂotropical. Actes Coll Insectes Soc 10:67±74 Lachaud JP, Cadena A, PeÂrez-Lachaud G, Schatz B (1999) Polygynie et strateÂgies reproductrices chez une poneÂrine neÂotropicale, Ectatomma ruidum. Actes Coll Insectes Soc 12:53±59 Levings SC, Franks NR (1982) Patterns of nest dispersion in a tropical ground ant community. Ecology 63:338±344 Liebig J, Heinze J, HoÈlldobler B (1995) Queen size variation in the ponerine ant Ponera coarctata (Hymenoptera: Formicidae). Psyche 102:1±12 McInnes DA, Tschinkel WR (1995) Queen dimorphism and reproductive strategies in the ®re ant Solenopsis geminata (Hymenoptera: Formicidae). Behav Ecol Sociobiol 36:367±375 Nonacs P (1988) Queen number in colonies of social Hymenoptera as a kin selected adaptation. Evolution 42:566±580 Pamilo P (1991) Evolution of colony characteristics in social insects. II. Number of reproductive individuals. Am Nat 138:412±433 Peakin GJ (1972) Aspects of productivity in Tetramorium caespitum L. Ekol Pol 20:55±63 Peeters C (1987) The reproductive division of labour in the queenless ponerine ant Rhytidoponera sp. 12. Insectes Soc 34:75±86 Peeters C (1991a) Ergatoid queens and intercastes in ants: two distinct adult forms which look morphologically intermediate between workers and winged queens. Insectes Soc 38:1±15 Peeters C (1991b) The occurrence of sexual reproduction among ant workers. Biol J Linn Soc 44:141±152
523 Peeters C (1993) Monogyny and polygyny in ponerine ants with or without queens. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, Oxford, pp 234±261 Peeters C (1997) Morphologically ``primitive'' ants: comparative review of social characters, and the importance of queen-worker dimorphism. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, UK, pp 372±391 Peeters C, Crewe R (1985) Worker reproduction in the ponerine ant Ophthalmopone berthoudi ± an alternative form of eusocial organization. Behav Ecol Sociobiol 18:29±37 Pratt SC (1989) Recruitment and other communication behavior in the ponerine ant Ectatomma ruidum. Ethology 81:313±331 Schatz B, Beugnon G, Lachaud JP (1994) Time-place learning by an invertebrate, the ant Ectatomma ruidum Roger. Anim Behav 48:236±238 Schatz B, Lachaud JP, Beugnon G (1995) Spatial ®delity and individual foraging specializations in the neotropical ponerine ant, Ectatomma ruidum Roger. Sociobiology 26:269±282 Schatz B, Lachaud JP, Beugnon G (1996a) Polyethism within hunters of the ponerine ant, Ectatomma ruidum Roger (Formicidae; Ponerinae). Insectes Soc 43:111±118 Schatz B, Lachaud JP, Peeters C, PeÂrez-Lachaud G, Beugnon G (1996b) Existence de microgynes chez la fourmi poneÂrine Ectatomma ruidum Roger. Actes Coll Insectes Soc 10:169±173 Schatz B, Lachaud JP, Beugnon G (1997) Graded recruitment and hunting strategies linked to prey weight and size in the ponerine ant Ectatomma ruidum. Behav Ecol Sociobiol 40:337±349 Schatz B, Lachaud JP, Fourcassie V, Beugnon G (1998) Densite et distribution des nids chez la fourmi Ectatomma ruidum Roger (Hymenoptera; Formicidae; Ponerinae). Actes Coll Insectes Soc 11:103±107
Seifert B (1991) The phenotype of the Formica rufa complex in East Germany. Abh Ber Naturkundemus Goerz 65:1±27 Sokal RR, Rohlf FJ (1969) Biometry: the principle and practice of statistics in biological research. Freeman, San Francisco Stille M, Stille B, Douwes P (1991) Polygyny, relatedness and nest founding in the polygynous myrmicine ant Leptothorax acervorum (Hymenoptera; Formicidae). Behav Ecol Sociobiol 28:91±96 SundstroÈm L (1995) Dispersal polymorphism and physiological condition of males and females in the ant, Formica truncorum. Behav Ecol 6:132±139 Tinaut A, Ruano F (1992) Braquipterismo y apterismo en formicidos. MorfologõÂ a y biometrõÂ a en las hembras de especies õÂ bericas de vida libre (Hymenoptera: Formicidae). Graellsia 48:121±131 Villet M (1989) A syndrome leading to ergatoid queens in ponerine ants (Hymenoptera: Formicidae). J Nat Hist 23:825±832 Villet M, Crewe RM, Duncan FD (1991) Evolutionary trends in the reproductive biology of ponerine ants (Hymenoptera: Formicidae). J Nat Hist 25:1603±1610 Weber NA (1946) Two common ponerine ants of possible economic signi®cance, Ectatomma tuberculatum (Olivier) and E. ruidum Roger. Proc Entomol Soc Wash 48:1±16 Wheeler WM (1905) The ant queen as a psychological study. Popul Sci Month 68:291±299 Wheeler WM (1917) The phylogenetic development of subapterous and apterous castes in the Formicidae. Proc Natl Acad Sci USA 3:109±117 Yamauchi K, Furukawa T, Kinomura K, Takamine H, Tsuji K (1991) Secondary polygyny by inbred wingless sexuals in the dolichoderine ant Technomyrmex albipes. Behav Ecol Sociobiol 29:313±319
