Summary. In neotropical swarm-founding wasps, caste dif-ferences can be arranged along a spectrum ranging from taxa in which queens and workers are externally similar, toothers with fairly distinct caste attributes. In this study,queen-worker differences progressively increase duringcolony development in Protopolybia exigua and Chartergusglobiventris. In Apoica flavissima, morphological caste dif-ferences are clearly pre-imaginally determined and have novariation in different phases of the colony cycle. Non-in-seminated layers are abundant in P. exigua during the wholecolony cycle, restricted to some phases in C. globiventris,and completely absent in A. flavissima. Based on these re-ported traits plus data from the literature, social regulation inepiponine castes can be morphologically and reproductivelyfixed, morphologically fixed but reproductively inducibledepending the colony cycle, reproductively inducible through-out colony cycle, or reproductively inducible throughoutcolony cycle only in some periods.

Key words: Vespidae; Epiponini, Polistinae, social wasps,caste differences, colony cycle, queen-worker conflict.

Introduction

Insect societies display a diversity of intra-specific differ-ences in all components of their colony organization. Thereare differences in colony size, in the number of reproductivefemales per colony, and in the pattern of behavioral andmorphological differentiation between reproductive (queens)and non-reproductive (workers) individuals. Good examples are found in the social wasps. In polistines, both indepen-dent- and swarm-founding species exist, and castes can be behaviorally (more basal) and morphologically (morederived) determined. In fact, although caste differences in

Polistinae are less conspicuous than in the Vespinae (Sprad-bery, 1973), the combination of morphological and behav-ioral traits can be quite complex (Jeanne, 1980; Jeanne et al.,1995).

The Epiponini belong to the swarm-founding polistines(Carpenter, 1993, 1997). Neotropical, polygynic, and abun-dant, these wasps represent the greatest species radiation ofsocial Vespidae. Morphological caste differences are absentor not clear in some species, but some of them presentmorphological differences (Richards, 1978; Jeanne, 1980).Richards (1978) recognized three different forms of queen-worker distinction: (a) size and allometric differences, withqueens larger than workers [Agelaia areata (Jeanne andFagen, 1974), A. vicina (Sakagami et al., 1996; Baio et al.,1998), A. pallipes and A. multipicta (Noll et al., 1997b), Protonectarina sylveirae (Shima et al., 1996b), Polybiascutellaris (Noll et al., 1997a), Epipona guerini (Hunt et al., 1996)]; (b) size and allometric differences, with queens smaller than workers [Apoica flavissima (Shima et al., 1994) and A. pallens (Jeanne et al., 1995), Polybiadimidiata (Shima et al., 1996a)]; and (c) morphological differences slight or indistinct [Parachartergus smithii(Mateus et al., 1997), Pseudopolybia vespiceps (Shima et al., 1998), Chartergellus communis (Mateus et al., 1999),Brachygastra lecheguana (Shima et al., 2000)]. In species of the second group, queens are significantly smaller than workers in some measurements and larger in others, but they did not differ in the overall size. According to Jeanneet al. (1995), this “non-size-based” caste differentiation can be explained by an ontogenetic reprogramming in thegrowth parameters (see also Wheeler, 1991). Jeanne (1980)suggested that pre-imaginal caste determination could be acharacteristic of all swarm-founding polistines. Changes ingrowth parameters were detected also in Epipona guerini(Hunt et al., 1996), and Pseudopolybia difficilis (Jeanne,1996).

Insectes soc. 49 (2002) 62–740020-1812/02/010062-13 $ 1.50+0.20/0© Birkhäuser Verlag, Basel, 2002

Insectes Sociaux

Research article

Castes and the influence of the colony cycle in swarm-founding polistinewasps (Hymenoptera, Vespidae, Epiponini)

F.B. Noll 1, 2 and R. Zucchi2

1 Museum of Biological Diversity, Department of Entomology, The Ohio State University, 1315 Kinnear Road, Columbus, OH 43212, USA2 Departamento de Biologia, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto –

SP 14040-901, Brazil, e-mail: fernandobn@ffclrp.usp.br

Received 2 November 2000; revised 16 March and 25 September 2001; accepted 13 November 2001.

Insectes soc. Vol. 49, 2002 Research article 63

individuals were measured and dissected. In large colonies where casteswere hard to identify, one hundred individuals were chosen randomly.After identifying some morphological characters to discriminate queens,such as abdominal size, all individuals having such a pattern were col-lected and used in the analysis. The following characters were measuredunder a binocular microscope with an ocular micrometer (smallest unit = 0.01 mm): head width (HW), minimum interorbital distance(IDm), width of mesoscutum (MSW), alitrunk length (AL), basal widthof tergite II (T2BW), and partial length of the forewing (WL). Ovarycondition was determined by dissection under a stereomicroscope. Thespermatheca from each dissected female was removed and put on a slidein a 1:1 solution of glycerin and alcohol (70%) in order to check forinsemination under a microscope.

Before statistical analysis, data were log transformated in order toavoid problems of variance. Two groups, queens with ovarian develop-ment and insemination and workers regarding the remaining females,were determined for statistical purposes. Means and standard deviationswere calculated from the five morphological measurements. One-way ANOVA was used for mean comparisons. The contribution of eachvariable to caste discrimination was examined using discriminant func-tion analysis using the stepwise method (Rao, 1973). In this method,variables are successively added to the model based on the higher F toenter values, adding no more variables when the F-ratio is no longersignificant. Stepwise addition of variables sometimes results in modelswhere variables may be included although they no longer explain a sig-nificant fraction of the variance. Wilks’ Lambda values were used toinfer the individual contribution of each variable to the model. TheWilks’ lambda statistic for the overall discrimination is computed as theratio of [the determinant of the within-groups variance/covariancematrix] to [the determinant of the total variance/covariance matrix].When this value is close to 1.0, then the residual is high and the variable is not a good discriminator, while a value closer to 0 means thatthe residual is low and the variable is a good discriminator. ANCOVAwas used with alitrunk length (AL) as a covariate based on its effi-ciency in previous publications (Jeanne et al., 1995; Jeanne, 1996; Huntet al., 1996).

In all colonies, number of individuals, number of combs, and brooddistribution were censused. The meconia were counted for each cell inorder to evaluate the number of generations produced. These data wereused to infer the stage in which the colonies were found.

Results

Nests and colony phase

Using brood distribution, number of meconia, and presenceof males (Table 1), three phases in the colony cycle weredefined (see Noll and Zucchi, 2000):

1. Pre-emergence. In the pre-emergence phase, no adult off-spring had been produced (mostly eggs and some younglarvae).

2. Worker production. Different-aged brood and at least oneadult generation (as ascertained by meconial counts) insome cells characterize the (worker) emergence phase.

3. Male production. The male production phase is distin-guished from the previous due to the presence of males.

In Apoica flavissima, three colonies were in the pre-emer-gence phase (colonies I, II, and III) and two in the workerproduction phase (IV and V) (Table 1). Only eggs were foundin cells in colonies I and II. In colony III, larvae and pupaewere found. In these colonies (I–III), workers had plentifulfat bodies, suggesting their young age. In Protopolybia exigua,

The frequent occurrence of non-inseminated laying fe-males in epiponines suggests reproduction may not be entire-ly the charge of queens. They were called “intermediates”(Richards and Richards, 1951) because, in some species,only insemination can determine the individual’s status asreproductive or not (see above). Even though these non-inseminated laying females have mainly been found inspecies with low caste dimorphism [Richards and Richards(1951), Mateus et al. (1997), Carpenter and Ross (1984),Shima et al. (1998), Mateus et al. (1999), Shima et al.(2000)], they have also been found in species with caste dif-ferences (Naumann, 1970; Simões, 1977; Noll et al., 1996).Although polygyny is widespread among epiponines, theircolonies cycle from polygyny (many queens) to oligogyny(few queens), and, eventually monogyny (one queen) in thecourse of the colony’s life (West-Eberhard, 1978, 1981). Sucha cycle may explain monogynic records in other epiponinewasps (Richards, 1978; West-Eberhard, 1973). This cyclicaloligogyny (West-Eberhard, 1978) seems to be important inthe maintenance of high genetic relatedness found in theEpiponini (Queller et al., 1988, 1993; Hughes et al., 1993).Workers are periodically testing queens, and, depending ontheir responses, queens are removed or not from the colony(West-Eberhard, 1978, 1981). On the other hand, aggressiveinteractions among queens are lacking in Metapolybiaaztecoides (West-Eberhard, 1978), Agelaia pallipes (Simões,1977) and Parachartergus colobopterus (Herman et al.,2000), which suggests that only workers would be involvedin queen selection. However, how workers choose among thequeens in a colony is not clear. It has been suggested thatworkers recognize more fecund queens and they discriminateagainst those queens with inhibited ovaries (Herman et al.,2000). Another possibility is that queen size could be im-portant for that process. In some Polybia, queens as a groupare hardly distinguished from workers based on body sizeearly in the colony cycle, and in the later stage of the colonycycle, queens are the largest individuals, probably due to the elimination of smaller queens (Noll and Zucchi, 2000).However, the present paper demonstrates that size differ-ences between female castes increase as the colony cycleproceeds in some epiponine species, and that in other speciesthis difference does not change with colony cycle, or that thesize differences between castes are absent throughout thecolony cycle.

Materials and methods

This work is based on three species of Epiponini: Apoica flavissima vander Vecht (five colonies collected in Brazil: Chapadinha, MaranhãoState, Nova Xavantina, Mato Grosso State, Chapada dos Guimarães,Mato Grosso State, and Bonito, Mato Grosso do Sul State), Protopoly-bia exigua de Saussure (five colonies collected in Pedregulho, SãoPaulo State), and Chartergus globiventris de Saussure (eight coloniescollected in Nova Xavantina, Mato Grosso State). Adult wasps werefixed in Dietrich’s solution. From each of these colonies 100 workersand all queens were subjected to measurements and dissections. Whencastes could be discriminated by size or color, all possible queens wereselected and from the remaining individuals; 100 workers were arbi-trarily selected. In small colonies where castes were not obvious, all

64 F.B. Noll and R. Zucchi Caste differences and colony cycle in swarm-founding wasps

two colonies were in the pre-emergence phase and three inthe worker-production phase (Table 1). In Chartergus globi-ventris, colonies contained different numbers of combs anddifferent sizes were found. One nest was in pre-emergence,five in the worker production phase and two were in the maleproduction phase (Table 1).

Ovary development and insemination

Three main ovarian development types were recognized as:type W, with filamentous ovarioles bearing no visible orslightly developed oocytes; type I, with ovarioles with someoocytes at the beginning of development or some in finalphase of vitellogenesis; and type Q, with well developed andlonger ovarioles each bearing from two to several matureoocytes. Because only Q type females contained sperm in thespermatheca, females with ovaries W, I, and Q can be charac-terized as workers, non-inseminated laying females andqueens, respectively.

In Apoica flavissima, only W and Q ovary types werefound in all colonies. In Protopolybia exigua, W, I and Qovaries were found in all colonies. In Chartergus globi-ventris, the three ovary types were found, but in colonies I, II, and VI–VIII, only W and Q patterns were found. Incolonies I and II, queens had shorter ovaries than those of queens in colonies IV–VIII. In colony III, queens hadboth ovary sizes (4 queens with larger ovaries and 22 withsmaller ovaries).

Morphological differences between castes

Apoica flavissimaQueen-worker dimorphism in Apoica flavissima is deter-mined by queens smaller than workers in some body parts,but larger in others (Shima et al., 1994). Such a pattern isfound in the colonies studied here. In general, all queenswere clearly distinct from workers (Fig. 1). All charactersmeasured were significantly different between queens andworkers, except the width of mesoscutum (MSW) in colonyII, alitrunk length (AL) in colonies IV and V, and wing length (WL) in colony III (Table 2). Covariance analysis(ANCOVA), using AL as a covariate, castes as the indepen-dent variable and other measured characters as dependentvariables (Table 2), were the same as those found using one-way ANOVA (Table 2).

Discriminant function analyses revealed that not all cha-racters were important in queen-worker separation (Table 3).The lower Wilks’ Lambda values (from 0.1 to 0.2) showedthat most characters used in the discriminant function weregood enough to discriminate castes independently (Table 3).This is true for all colonies, except for colony IV that pre-sented values around 0.6 (Table 3).

Protopolybia exiguaQueen-worker differences in Protopolybia exigua have beenpreviously reported for one colony (Simões, 1977; Noll et al.,1996). Compared to workers, queens show only larger bodyparts. Such a pattern was found in the colonies studied here(Fig. 2). Differences of mean values of five measured char-acters were found between workers and queens, except HWin colony III (Table 4). ANCOVA analysis showed significantdifferences in most characters (Table 4). Also, not all charac-

Table 1. Colony and nest composition

Phase Colony Females Males Combs Larvae Meconiaand

Worker Intermediate Queen Pupae

Apoica Pre-emergence I 2230 (99%) 0 22 (1%) 0 1 Absent 0flavissima II 1663 (99.6%) 0 7 (0.4%) 0 1 Absent 0

III 215 (90.7%) 0 22 (9.3%) 0 1 Present 0

Worker IV 1951 (99.9%) 0 2 (0.1%) 0 1 Present 1production V 198 (94%) 0 12 (6%) 0 1 Present 1

Protopolybia Pre-emergence IV 29 (32%) 30 (34%) 30 (34%) 0 1 Absent 0exigua V 34 (32%) 40 (38%) 32 (30%) 0 2 Absent 0

Worker I 22 (24%) 47 (52%) 22 (24%) 0 2 Present 1production II 20 (34.5%) 57 (59%) 14 (6.5%) 0 1 Present 3

III 19 (20%) 71 (76%) 4 (4%) 0 1 Present 1

Chartergus Pre-emergence VI 67 (84%) 0 13 (16%) 0 4 Absent 0globiventris Worker I 45 (83%) 0 9 (17%) 0 3 Present 1

production II 118 (93%) 0 9 (7%) 0 3 Present 1III 81 (69%) 10 (9%) 26 (22%) 0 9 Present 1VII 995 (99.1%) 0 9 (0.9%) 0 5 Present 3VIII 788 (97.2%) 0 22 (2.8%) 0 4 Present 3

Male production IV 238 (77%) 53 (17%) 17 (6%) 299 17 Present > 1V 298 (77%) 80 (21%) 8 (2%) 197 22 Present > 1

Insectes soc. Vol. 49, 2002 Research article 65

Figure 1. Plots (in mm) of head width (HW) versus basal width oftergum II (T2BW) in five colonies (I–V) of Apoica flavissima. Queens= white squares; Workers = black circles. Colonies I–III were in pre-emergence phase of the colony cycle and colonies IV–V, worker

production. Each ellipse encompasses 80% of the variation found ineach group. A- discrimination between all queens and workers of Apoicaflavissima using the log-log plots

66 F.B. Noll and R. Zucchi Caste differences and colony cycle in swarm-founding wasps

Table 2. Queen and worker means, One-way ANOVA and ANCOVA analyses for each morphometrical variable in Apoica flavissima

Phase Characters Means ± SD One-way ANOVA ANCOVA (AL as covariate)

Queens Workers F P > F MS MS F p-levelEffect Error

Colony I Pre- HW 6.74 ± 0.07 7.08 ± 0.13 130.6 < 0.001 0.48 0.01 83.84 < 0.001(22 queens emergence AL 11.78 ± 0.22 12.13 ± 0.28 23.53 < 0.001and MSW 4.98 ± 0.09 4.79 ± 0.12 43.89 < 0.001 0.62 0.01 78.33 < 0.00178 workers) T2BW 3.57 ± 0.06 3.10 ± 0.12 275.5 < 0.001 1.68 0.01 171.47 < 0.001

WL 11.92 ± 0.13 12.60 ± 0.27 119.8 < 0.001 2.06 0.03 65.80 < 0.001

Colony II HW 6.54 ± 0.20 7.12 ± 0.09 216.9 < 0.001 0.41 0.01 54.89 < 0.001(7 queens AL 11.34 ± 0.55 12.27 ± 0.28 110.0 < 0.001and MSW 4.98 ± 0.23 4.96 ± 0.12 6.29 0.5993 workers) T2BW 3.53 ± 0.14 3.15 ± 0.09 108.5 < 0.001 0.55 0.01 67.36 < 0.001

WL 11.51 ± 0.62 12.75 ± 0.18 190.7 < 0.001 1.77 0.04 45.00 < 0.001

Colony III HW 6.07 ± 0.13 6.33 ± 0.13 70.44 < 0.001 1.36 0.01 97.74 < 0.001(22 queens AL 10.46 ± 0.23 10.25 ± 0.34 8.63 0.004and MSW 4.55 ± 0.15 4.26 ± 0.12 87.29 < 0.001 0.96 0.01 74.31 < 0.00178 workers) T2BW 3.20 ± 0.20 2.70 ± 0.16 151.15 < 0.001 3.38 0.03 130.02 < 0.001

WL 10.62 ± 0.22 10.74 ± 1.16 0.23 0.63

Colony IV Worker HW 6.43 ± 0.14 6.80 ± 0.11 23.69 < 0.001 0.27 0.01 23.65 < 0.001(2 queens production AL 10.91 ± 0.29 11.18 ± 1.48 0.06 0.80and MSW 4.64 ± 0.22 4.57 ± 0.11 0.69 0.4198 workers) T2BW 3.21 ± 0.07 3.00 ± 0.11 7.12 0.009 0.09 0.01 6.98 < 0.001

WL 11.02 ± 0.29 12.00 ± 0.34 16.09 < 0.001 1.91 0.12 16.46 < 0.001

Colony V HW 6.36 ± 0.13 6.85 ± 0.17 92.17 < 0.001 2.41 0.03 93.14 < 0.001(12 queens AL 11.03 ± 0.27 11.30 ± 1.13 0.63 0.43and MSW 4.62 ± 0.13 4.38 ± 0.09 66.24 < 0.001 0.64 0.01 70.58 < 0.00188 workers) T2BW 3.39 ± 0.10 2.97 ± 0.11 168.54 < 0.001 1.88 0.01 177.51 < 0.001

WL 11.58 ± 0.35 12.08 ± 0.36 20.52 < 0.001 2.64 0.13 20.38 < 0.001

Table 3. Discriminant morphometric variables between queens and workers in Apoica flavissima, based on discriminant function analyses using thestepwise procedure. Original data are based on mm

Phase Step Variable Wilks’ Lambda F P > F

Pre-emergence Colony I 1 T2BW 0.117 31.2 < 0.0012 HW 0.082 8.60 0.0053 MSW 0.090 13.4 0.0014 WL 0.073 2.97 0.0925 AL 0.070 1.01 0.320

Colony II 1 HW 0.174 52.9 < 0.0012 T2BW 0.165 44.6 < 0.0013 MSW 0.148 30.7 < 0.0014 WL 0.132 17.3 < 0.001

Colony III 1 T2BW 0.340 14.12 < 0.0012 HW 0.385 28.79 < 0.0013 MSW 0.315 5.88 0.017

Worker production Colony IV 1 HW 0.658 9.31 0.0032 T2BW 0.665 10.4 0.0023 WL 0.702 16.25 < 0.0014 MSW 0.654 8.68 0.004

Colony V 1 T2BW 0.282 106.2 < 0.0012 HW 0.240 76.5 < 0.0013 MSW 0.150 12.3 0.0014 WL 0.137 3.10 0.082

Insectes soc. Vol. 49, 2002 Research article 67

Figure 2. Plots (in mm) of width of mesoscutum (MSW) versus basalwidth of tergum II (T2BW) in five colonies (I–V) of Protopolybiaexigua. Queens = white squares; Workers = black circles. Colonies IV–V were in pre-emergence phase of the colony cycle and colonies

I–III, worker production. Each ellipse encompasses 80% of the varia-tion found in each group. A- discrimination between all queens andworkers of Protopolybia exigua using the log-log plots

68 F.B. Noll and R. Zucchi Caste differences and colony cycle in swarm-founding wasps

Table 4. Queen and worker means, One-way ANOVA and ANCOVA analyses for each morphometrical variable in Protopolybia exigua

Phase Characters Means ± SD One-way ANOVA ANCOVA (AL as covariate)

Queens Workers F P > F MS MS F p-levelEffect Error

Colony IV Pre-(30 queens emergence HW 3.54 ± 0.04 3.49 ± 0.05 23.14 < 0.001 0.00 0.00 1.78 0.19and AL 2.57 ± 0.06 2.49 ± 0.07 29.35 < 0.00165 workers) MSW 2.76 ± 0.07 2.65 ± 0.08 41.05 < 0.001 0.02 0.00 6.71 0.01

T2BW 1.65 ± 0.05 1.57 ± 0.08 34.32 < 0.001 0.03 0.00 7.29 0.01WL 4.56 ± 0.07 4.44 ± 0.11 31.74 < 0.001 0.04 0.01 5.26 0.02

Colony V HW 3.52 ± 0.06 3.45 ± 0.05 37.60 < 0.001 0.01 0.00 4.58 0.03(32 queens AL 2.45 ± 0.09 2.32 ± 0.08 55.45 < 0.001and MSW 2.66 ± 0.08 2.51 ± 0.10 56.86 < 0.001 0.04 0.00 8.52 < 0.00174 workers) T2BW 1.67 ± 0.09 1.59 ± 0.06 28.15 < 0.001 0.01 0.00 2.53 0.12

WL 4.59 ± 0.11 4.37 ± 0.14 58.55 < 0.001 0.07 0.01 7.34 0.01

Colony I Worker HW 3.53 ± 0.03 3.48 ± 0.04 11.16 0.002 0.00 0.00 0.75 0.39(22 queens production AL 2.63 ± 0.04 2.51 ± 0.05 39.55 < 0.001and MSW 2.78 ± 0.05 2.62 ± 0.06 67.17 < 0.001 0.03 0.00 11.77 < 0.00169 workers) T2BW 1.72 ± 0.02 1.58 ± 0.06 65.30 < 0.001 0.04 0.00 16.01 < 0.001

WL 4.64 ± 0.05 4.46 ± 0.10 34.83 < 0.001 0.02 0.01 2.75 0.10

Colony II HW 3.50 ± 0.03 3.47 ± 0.08 3.05 0.05 0.00 0.00 1.42 0.24(14 queens AL 2.52 ± 0.05 2.39 ± 0.10 22.78 < 0.001and MSW 2.79 ± 0.07 2.64 ± 0.12 19.46 < 0.001 0.02 0.00 4.88 0.0379 workers) T2BW 1.67 ± 0.06 1.54 ± 0.09 22.19 < 0.001 0.02 0.00 4.69 0.04

WL 4.64 ± 0.12 4.39 ± 0.09 55.94 < 0.001 0.19 0.01 23.78 < 0.001

Colony III HW 3.51 ± 0.02 3.45 ± 0.08 2.20 0.15(4 queens AL 2.71 ± 0.05 2.56 ± 0.08 12.04 0.002and MSW 2.84 ± 0.09 2.70 ± 0.10 7.25 0.01 0.02 0.00 4.88 0.0390 workers) T2BW 1.73 ± 0.05 1.51 ± 0.11 14.84 < 0.001 0.02 0.00 4.69 0.04

WL 4.73 ± 0.02 4.46 ± 0.10 29.10 < 0.001 0.19 0.01 23.78 < 0.001

Table 5. Discriminant morphometric variables between queens and workers in Protopolybia exigua based on discriminant function analyses using thestepwise procedure. Original data are based on mm

Phase Step Variable Wilks’ Lambda F P > F

Pre-emergence Colony IV 1 AL 0.65 5.20 0.0252 T2BW 0.63 1.77 0.1873 WL 0.63 2.04 0.1574 MSW 0.62 1.14 0.288

Colony V 1 WL 0.60 2.39 0.132 MSW 0.60 3.51 0.063 AL 0.60 3.31 0.07

Worker production Colony I 1 AL 0.342 19.952 0.0002 T2BW 0.291 11.002 0.0023 HW 0.257 4.989 0.031

Colony II 4 MSW 0.255 4.665 0.0371 WL 0.41 9.15 0.0052 T2BW 0.35 2.27 0.1413 HW 0.38 5.78 0.022

Colony III 4 MSW 0.36 3.46 0.0711 WL 0.64 19.71 0.0002 MSW 0.40 5.16 0.0353 HW 0.36 3.14 0.092

Insectes soc. Vol. 49, 2002 Research article 69

ters were important in queen-worker discrimination models(Table 5), and even though some of them were included in thediscriminant model, they were not statistically significant(Table 5). Such differences in the significance of discrimi-nating characters were confirmed by the different Wilks’Lambda values shown in the discriminant function. In colonyI and II, Wilks’ Lambda was around 0.3 to 0.4 for all charac-ters, good enough to discriminate the castes independently.

However, in other colonies Wilks’ Lambda values werehigher (around 0.6), which means that only a combination ofthese variables can predict caste differences.

Chartergus globiventrisCaste differences in C. globiventris are less conspicuous thanin the previous species (Fig. 3). Differences between workersand queens in mean values of the five characters measured

Figure 3. Plots (in mm) of width of mesoscutum (MSW) versus basalwidth of tergum II (T2BW) in eight colonies (I–VIII) of Chartergusglobiventris. Queens = white squares; Workers = black circles. ColonyVI was in pre-emergence phase, colonies I–III and VII–VIII, worker

production and colonies IV–V, male production. Each ellipse encom-passes 80% of the variation found in each group. A- discriminationbetween all queens and workers of Chartergus globiventris using thelog-log plots

70 F.B. Noll and R. Zucchi Caste differences and colony cycle in swarm-founding wasps

Table 6. Queen and worker means, One-way ANOVA and ANCOVA analyses for each morphometrical variable in Chartergus globiventris

Colony Chartergus Characters Means ± SD One-way ANOVA ANCOVA (AL as covariate)Phase globiventris

Queens Workers F P > F MS MS F p-levelEffect Error

Pre- Colony VI HW 5.12 ± 0.13 5.03 ± 0.24 1.51 0.23emergence (13 queens AL 6.23 ± 0.28 6.08 ± 0.22 3.63 0.06

and MSW 4.09 ± 0.10 4.03 ± 0.10 3.85 0.06100 workers) T2BW 4.75 ± 0.17 4.73 ± 0.15 0.17 0.69

WL 5.14 ± 0.10 5.12 ± 0.12 0.35 0.56

Worker Colony I HW 5.30 ± 0.08 5.14 ± 0.11 18.27 < 0.001 0.02 0.00 7.92 0.01production (9 queens AL 6.41 ± 0.18 6.11 ± 0.27 9.87 0.003

and MSW 4.16 ± 0.06 3.98 ± 0.13 14.95 < 0.001 0.08 0.01 6.62 0.0145 workers) T2BW 4.96 ± 0.24 4.74 ± 0.19 9.77 0.003 0.08 0.03 2.60 0.11

WL 5.43 ± 0.09 5.26 ± 0.16 9.97 0.003 0.06 0.02 3.30 0.08

Colony II HW 5.13 ± 0.066 5.09 ± 0.099 1.90 0.17(9 queens AL 6.16 ± 0.233 5.96 ± 0.262 4.57 0.04and MSW 4.03 ± 0.066 3.91 ± 0.103 12.12 < 0.001 0.07 0.01 8.23 0.0190 workers) T2BW 4.83 ± 0.100 4.61 ± 0.149 18.48 < 0.001 0.30 0.02 14.46 0.00

WL 5.19 ± 0.143 5.20 ± 0.119 0.04 0.86

Colony III HW 5.12 ± 0.096 5.15 ± 0.097 1.54 0.22(26 queens AL 6.16 ± 0.312 6.19 ± 0.298 0.22 0.64and MSW 4.06 ± 0.122 4.12 ± 0.115 3.88 0.0678 workers) T2BW 4.65 ± 0.182 4.77 ± 0.166 0.64 0.02 0.25 0.02 10.51 0.002

WL 5.21 ± 0.121 5.28 ± 0.134 5.09 0.03 0.08 0.02 5.08 0.026

Colony VII HW 5.25 ± 0.04 5.11 ± 0.11 14.08 < 0.001 0.02 0.01 2.53 0.12(9 queens AL 6.43 ± 0.11 6.13 ± 0.18 23.55 < 0.001and MSW 4.17 ± 0.08 4.05 ± 0.11 9.91 0.003 0.01 0.01 1.07 0.3191 workers) T2BW 4.84 ± 0.08 4.66 ± 0.15 12.95 < 0.001 0.02 0.01 1.11 0.30

WL 5.25 ± 0.17 5.14 ± 0.25 5.28 0.03 0.06 0.06 1.14 0.29

Colony VIII HW 5.17 ± 0.12 5.07 ± 0.19 5.66 0.002 0.04 0.03 1.42 0.24(22 queens AL 6.31 ± 0.25 6.11 ± 0.20 16.20 < 0.001and MSW 4.12 ± 0.10 4.04 ± 0.11 11.20 0.001 0.01 0.01 1.71 0.1979 workers) T2BW 4.79 ± 0.15 4.69 ± 0.16 7.02 0.009 0.00 0.02 0.13 0.72

WL 5.19 ± 0.20 5.13 ± 0.24 3.37 0.07 0.01 0.05 0.22 0.64

Male Colony IV HW 5.09 ± 0.081 5.04 ± 0.09 3.41 0.07production (17 queens AL 6.42 ± 0.166 6.16 ± 0.215 21.92 < 0.001

and MSW 4.08 ± 0.07 4.01 ± 0.092 9.94 0.002 0.01 0.01 1.23 0.2783 workers) T2BW 4.80 ± 0.114 4.71 ± 0.156 4.34 0.04 0.00 0.02 0.01 0.91

WL 5.20 ± 0.121 5.21 ± 0.127 0.12 0.73

Colony V HW 5.16 ± 0.078 5.12 ± 0.098 1.31 0.26(8 queens AL 6.25 ± 0.144 6.13 ± 0.188 3.38 0.07and MSW 4.10 ± 0.052 3.98 ± 0.099 10.57 0.002 0.05 0.01 7.01 0.00992 workers) T2BW 4.78 ± 0.125 4.63 ± 0.152 7.10 0.009 0.06 0.02 3.73 0.056

WL 5.28 ± 0.096 5.24 ± 0.160 0.48 0.49

were found (Table 6) in colonies I and VII and were not foundin colony VI (Table 6). In the other colonies some measuredcharacters were not significant (Table 6). Discriminant func-tion analyses show that only a few characters compose thediscriminant models (Table 7). These small differences in thesignificance of discriminating characters were confirmed bydifferent Wilks’ Lambda values shown in the discriminantfunction. In all colonies, Wilks’ Lambda varied around 0.7 to 0.9 (Table 7).

Discussion

Morphological caste differences

Apoica flavissimaIn all samples, queens and workers showed clear differencesin some of their body parts. In addition, the five charactersused in the analyses were good discriminators; only in a few cases did they show no difference. Also, castes can be

Insectes soc. Vol. 49, 2002 Research article 71

Table 7. Discriminant morphometric variables between queens and workers in Chartergus globiventris based on discriminant function analyses usingthe stepwise procedure. Original data are based on mm

Phase Chartergus globiventris Step Variable Wilks’ Lambda F P > F

Pre-emergence Colony VI 1 MSW 0.904 2.962 0.0922 T2BW 0.911 3.379 0.0733 AL 0.896 2.543 0.118

Worker Production Colony I 1 HW 0.78 5.42 0.022 MSW 0.74 2.75 0.10

Colony II 1 T2BW 0.83 10.68 0.0022 WL 0.82 9.27 0.0033 MSW 0.78 3.75 0.0564 AL 0.76 1.83 0.180

Colony III 1 T2BW 1.000 9.643 0.002

Colony VII 1 MSW 0.78 10.13 0.0032 HW 0.68 2.53 0.118

Colony VIII 1 AL 0.900 6.533 0.0122 MSW 0.856 1.480 0.227

Male Production Colony IV 1 AL 0.89 17.162 < 0.0012 WL 0.81 7.323 < 0.0013 MSW 0.77 2.659 < 0.001

Colony V 1 MSW 0.93 4.51 0.042 T2BW 0.90 1.21 0.27

Table 8. Different types of caste system in the Epiponini based on studies of more than one nest; studies of only one nest not included

Species Pattern Physical caste Ovary development Timing of caste Sourcedifferences in non-inseminated determination

females

Chartergellus communis, Reproductively Absent Always Imaginal Mateus et al. (1999), Parachartergus smithii inducible throughout Mateus et al. (in prep.)

cycle

Synoeca cyanea, Reproductively Absent Cycle dependent Imaginal Noda (2000), West-S. surinamensis, inducible sometimes Eberhard (1978, 1981)Metapolybia aztecoides

Protopolybia exigua, Morphologically fixed, Fixed, size Always Pre-imaginal Present data, P. sedula reproductively Baio (1997)

inducible cycle- dependent sometimes

Chartergus globiventris, Reproductively Size cycle- Cycle dependent Pre-imaginal Present data, Polybia scutellaris, inducible sometimes dependent Noll and Zucchi (2000), P. occidentalis, Shima et al. (in prep.) P. paulista, Protonectarina sylveirae

Apoica flavissima, Morphologically Fixed Never Pre-imaginal Present data, Agelaia vicina and reproductively Noll et al. (in prep.)

fixed

72 F.B. Noll and R. Zucchi Caste differences and colony cycle in swarm-founding wasps

discriminated based on a single morphological character.ANCOVA analyses supported differences between castes,indicating that variance effects are not affecting such differ-ences. Comparing our data with those of Shima et al. (1994),the main difference is related to width of mesoscutum; thismeasure was larger in queens in the present data and smallerin Shima et al. (1994). Even though fewer variables weremeasured in this work, the pattern found (queens have somebody parts larger than that of workers and others smaller) issimilar to that found by Jeanne et al. (1995) for A. pallens.Also, all morphological variables easily discriminate queensfrom workers in all analyzed colonies. The absence of non-inseminated laying females in all colonies suggests thatworkers’ ovaries are suppressed (Sakagami et al., 1996; Nollet al., 1997b; Baio et al., 1998; Herman et al., 2000).

Protopolybia exiguaAccording to Noll et al. (1996), Protopolybia exigua presentsslight caste differentiation between queens and workers, atleast in the early stages of nest development. In the analyzedcolonies, not only slight differences but also more distinctcaste differences were found. Some morphological differ-ences detected in ANOVA analyses were not different aftertesting them using ANCOVA analyses, which suggests thatsome differences are only due to different variances. Basedon discriminant analyses, smaller differences were found inthe colonies in early stages of the colony cycles, and largerdifferences in colonies in the later stages. Wilks’ Lambdavalues support this statement because, in early stages, mor-phological variables were able to discriminate castes onlywhen associated and not when considered independently.This is different from colonies in later stages of the colonycycle, in which Lambda values were high enough to discrim-inate castes based on single morphological characters.

Queen-worker differences are more pronounced in thecolonies with a small number of queens, suggesting that thesame pattern of queen elimination found in some species ofPolybia (Noll and Zucchi, 2000) could be applied here. How-ever, in P. exigua, non-inseminated egg layers were found inall colony stages.

Chartergus globiventrisCaste differences in C. globiventris were less distinct than in P. exigua. Decreasing queen number with increasing castedifference (Noll and Zucchi, 2000) applies also to C. globi-ventris because queens were more distinct than workers insome colonies than in other colonies. This pattern is differentfrom P. exigua, in which non-inseminated laying femaleswere few and found only in some colonies with a highernumber of queens.

Caste systems in the Epiponini

The combination of morphological differences and ovariandevelopment has been important to infer some aspects of thesocial biology of these wasps (Richards, 1978). In someEpiponini, morphological and physiological discontinuity

between castes seems to be subject to variation according tothe colony cycle development, while in other epiponines sucha phenomenon seems not to occur. Colony cycle apparentlyoperates as a modulator of social organization in these wasps.Cyclical oligogyny may be related to the increase of castedifferences in some species because larger queens often have higher survivorship (Noll and Zucchi, 2000). As insome other epiponines (West-Eberhard, 1978; Strassmann et al., 1998), queen number also varied in the present study.In C. globiventris and P. exigua, as queen number decreasesduring the colony cycle, differences between castes in-creased, as previously noticed for some Polybia (Noll andZucchi, 2000). This sort of increase in caste differences is probably due to exclusion of smaller queens (Noll andZucchi, 2000). In C. globiventris and P. exigua, queen bodysize may be important for competitive ability, as in otherwasp societies with multiple queens (Noll and Zucchi, 2000),and workers may be fundamental in the queen eliminationprocess (West-Eberhard, 1978, 1981; Forsyth, 1978; Hermanet al., 2000).

In contrast to other species studied here, caste differencesin Apoica flavissima did not vary during the colony cycle.That pattern suggests that in species with clear pre-imaginaldetermination, size may not be related to queen selection.Similarly, size has no special importance in other speciessuch as Chartergellus communis. However, in C. communis,queen-worker differences were absent (Mateus et al., 1999).

Worker ovarian development is another interesting com-ponent of colony cycle in epiponines. As stated by Richards(1978: 27): “In many species a few or even many inter-mediates occur with the ovarioles slightly enlarged. In othercharacters intermediates are sometimes more like workers,sometimes more like queens, and while their significance isuncertain it seems likely that they may have different origins,perhaps as suppressed queens or as egg-laying workers, orperhaps even, in some cases, as a stage in the development ofqueens.”

In Apoica flavissima, workers are sterile in the wholecolony cycle, suggesting that only queens are reproductives.In Protopolybia exigua and Chartergellus communis (Mateuset al., 1999), non-inseminated laying females were present in the whole colony cycle. In Chartergus globiventris andPolybia paulista (Noll and Zucchi, 2000) non-inseminatedlaying females occurred only in some phases of the colonycycle. Richards (1971) assumed that non-inseminated layingfemales can produce both trophic eggs and males but,Forsyth (1978), West-Eberhard (1978) and Gastreich et al.(1993) considered them only as young non-inseminatedqueens. Richards (1971) and West-Eberhard (1978) conside-red ovarian development in non-inseminated laying femalesrelated to queen number. That is, in the presence of a fewqueens, they have large ovaries and with many queens, smallovaries.

The number of studies on the biology of swarm-foundingneotropical wasps is so low that generalizations are difficultto make. However, different types of caste differences can beclearly delimited. Present data combined with other data inthe literature (Table 8) suggest that five different patterns

Insectes soc. Vol. 49, 2002 Research article 73

the loss of dominance in the colony as observed in somespecies of Bombus (Sakagami, 1976), so that ovariandevelopment in young females would represent a queenproduction phase.

5. Morphological differences between castes are constantand queens are always distinct from workers during thecolony cycle. Non-inseminated laying females are absentthroughout the whole colony cycle, suggesting that work-ers do not develop their ovaries adequately to becomelayers. This pattern is recognized in some Apoica andAgelaia (Table 8) and would fit the definition of castedifferences for higher eusociality: queens differ fromworker in both morphology and physiology.

These examples illustrate how caste systems in neotropicalswarm-founding wasps can be more complex and diversethan usually considered. In fact, it is possible that differentschemes of queen selection in epiponines during cyclicaloligogyny can exist, and they can be size dependent or not. Inthe former, larger queens would preferentially survive versussmaller ones, while in the latter queen size is an independenttrait and selection of larger inter-caste differences would notoccur.

Acknowledgements

The authors acknowledge the financial support by FAPESP (proc. 95/09226-1 and 01/02491-4) and The Ohio State University Post-DoctoralFellowship. Special thanks to Sidnei Mateus for helping in field collec-tions, Kurt M. Pickett, John Wenzel (The Ohio State University), andtwo anonymous reviewers for corrections on the manuscript and impor-tant suggestions.

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