2.More.1'­ JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 68(1), 1995, pp. 43-50

The Roles of Body Size and Dominance in Division of Labor Among Workers of the Eusocial occidentalis (Olivier) (: )

S. O'DoNNELL1,2 AND R. L. JEANNE Department of Entomology, 1630 Linden Drive, University of Wisconsin, Madison, Wisconsin 53706, USA

ABSTRACT: Dominance interactions among workers may influence division of labor within the worker caste ofeusocial colonies. We examined the relationships between body size, dominance interactions, and age-based division oflabor in the advanced eusocial (swarm-founding) wasp Polybia occidentalis (Olivier). Workers progressed through a series oftask sets as they aged (age polyethism), butwithin task sets there was individual variability in the age of first task performance. Smaller-bodied workers passed through the age po­ lyethism sequence more slowly: worker body size, as indicated by the length of the me­ sothoracic wing costa vein, bore a negative relationship with the age of first performance of tasks outside the . Larger-bodied workers therefore performed tasks that removed them from opportunities for direct in the nest interior at an earlier age. Smaller workers were also more likely to be dominant in observed social interactions, suggesting that patterns of social dominance are involved in structuring division of labor among P, occidentalis workers, with larger workers playing a subordinate role.

Workers of a minority of species and of most termites are divided into morphologically distinct castes (Oster and Wilson, 1978; Holldobler and Wilson, 1990). In these species, the allocation of duties in the worker force is based in large part on differences in body size. In contrast, workers of most and of all eusocial with flying workers (bees and ) are monomorphic; body size variation exists, but is distributed unimodally, and growth is isometric. Little is known about the role ofbody size in division oflabor in species with monomorphic worker castes. Waddington (1981) found that body size variation was low in bee species that use cOIlJll1Jlnication for recruitment to food sources relative to species that do not recruit to food, suggesting that selection can act on body size variation to promote effective division of labor in species with monomorphic workers. Furthermore, .,a pattern ofyounger age offirst foraging and/or ofincreased probability offoraging il11arger-bodied workers has been noted in honey bees (Kerr and Hebling, 1964; Waddington, 1988), bumble bees (Free, 1955), and yellowjacket wasps (Spradbery, 1972). Breed et al. (1978) noted the opposite pattern in sweat bees. The relationships of body size to division of labor that have been recorded in monomorphic species are difficult to interpret because it is not known how body size differences translate into behavioral variation. One possibility is that dom­ inance interactions among workers, which may be based on body size differences, playa role in shaping division oflabor. Ifsocial dominance is interpreted broadly as occurring outside the context ofdirect reproductive competition (Jeanne, 1991),

J Corresponding author. 2 Current address: Department of Entomology, University of California, Davis, California 95616, USA. Accepted for publication 31 March 1994. 44 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY then studies on vespine and polistine wasps suggest that social grooming and food solicitation represent dominance interactions among workers (Montagner, 1966; West Eberhard, 1969; Akre et aI., 1976). These interactions among workers may influence task performance. The aim of this study was to determine ifthere is a relationship between body size, the outcome of dominance interactions, and age-based division of labor in the advanced eusocial (swarm-founding) wasp Polybia occidentalis (Olivier). Po­ lybia occidentalis workers exhibit age polyethism, but individuals vary in the rate of passage through the age sequence of tasks (Jeanne et aI., 1988; O'Donnell and Jeanne, 1992). We addressed two questions on division oflabor among P. occidentalisworkers: I. Is worker body size correlated with rate of progression through the age-based task sequence? 2. Are outcomes of social dominance interactions dependent on worker body size such that dominance may playa role in structuring division of labor? Materials and Methods WASP INTRODUCTIONS, BEHAVIORAL OBSERVATIONS, AND COLLECTIONS: Field work was conducted from 28 August to 18 October 1991 at Centro Ecologico la Pacifica in Guanacaste Province, Republic of Costa Rica. Two P. occidentalis colonies of moderate size (Colony A: 4 layers of nest comb, 953 unmarked adults; Colony B: 4 layers of nest comb, 381 unmarked adults at the end of the study) were chosen as subjects for behavioral observations in the field. Polybia occidentalis combs from three other colonies were maintained in the laboratory at ambient temperature. Every 24 hr, all newly-emerged adults were removed from these combs. A cohort of 15 of the young adults was anesthetized with diethyl ether, marked with paint pens for individual recognition, and intro­ duced into one of the observation colonies. These adults are accepted when in­ troduced into non-natal observation colonies (O'Donnell and Jeanne, 1992). Each observation colony received a cohort of introduced wasps every other day. On days alternating with worker introductions, behavioral data were collected by an observer at an observation colony during continuous sessions of 1.5 hr in the morning and I hr in the afternoon. Behavioral acts of all visible wasps were recorded in scan samples of the nest entrance and the entire nest surface every 10 min (see O'Donnell and Jeanne, 1993 for ethogram), and all occurrences of foraging behavior were recorded. Behavioral acts were categorized as occurring inside the nest, on the nest surface, and away from the nest (foraging). Social interactions-solicitation ofcrop contents and grooming-were analyzed as dom­ inance interactions among workers (Jeanne, 1991). Wasps soliciting crop contents antennate and mandibulate the mouthparts and antennae ofnestmates and extend their mouthparts toward the solicited wasp; grooming involves mandibulation of other parts of a nestmate's body and varies in intensity from mild mouthing to violent . A worker was categorized as dominant when she was the active partner in a grooming or solicitation interaction, and as submissive when she was the recipient of grooming or solicitation. Only the relative status (dominant or submissive) ofmarked workers observed in social interactions was recorded during scan samples; intensity of interactions and identity of interacting partners were not noted. VOLUME 68, NUMBER 1 45

After three weeks of observations the colonies were collected by enclosing the nest in a plastic bag with ether. Collections were made at night to ensure that all workers would be present. Marked wasps were sorted from unmarked wasps and stored frozen at 10°C. Upon collection we obtained 109 workers from each colony of differing ages (4 to 23 days) with known behavioral histories. COSTA VEIN LENGTH MEASUREMENTS: Following oven drying, weighing, and lipid extraction (methods and results to be presented elsewhere), costa vein length on the mesothoracic wing was measured to the nearest 0.025 mm using an ocular micrometer at 25 x magnification. The costa was measured in lateral aspect, from the keel across the base of the costa and subcosta veins (beneath the tegula; Fig. 102 in Richards, 1978) to the distal end of the pterostigma. This measurement ofthe wing was chosen over total wing length because the costa is rigid, and was less often bent or damaged than the wing tips. The right mesothoracic wing costa was measured unless itwas damaged, in which case the left wing was used. Survival analysis (SAS, 1985) was used to measure the effect of body size on age of first performance of behavioral acts outside the nest.

Results Costa lengths were obtained from 108 individuals in colony A and from 109 individuals in colony B. Distributions of costa length and of body weight were unimodal (Fig. 1). In both colonies costa vein length was significantly positively correlated with dry body weight (Fig. 1; Colony A: r 0.46, d.f. = 106, P < 0.001; Colony B: r = 0.72, d.£ = 107, P < 0.001). Costa length is therefore a good indicator of body size, although the relationship was weaker in Colony A than in Colony B. Some ofthe variance in dry body weight relative to costa length was due to differences in lipid content among workers (S.O'D., unpubl. data). Distributions of first observed age of task performance differed among behav­ ioral acts in the nest, on the nest, and away from the nest (Survival analysis, Colony A: Wilcoxon X2 = 13.12, d.f. = 2, P < 0.005; Colony B: Wilcoxon X2 50.31, d.£ = 2, P < 0.001). Within colonies there was variation in the age at which workers were first observed outside the nest, but distributions of ages of workers leaving the nest interior did not differ between colonies (Fig. 2; Wilcoxon test for equality ofage distributions, Xl 1.26, d.f. 1, P > 0.25). Smaller wasps spent more days working in the nest interior than larger wasps: costa length was negatively associated with age at first performing outside nest tasks (Survival analysis, Wilcoxon rank test statistic = -3.68, X2 = 8.01, d.f. = I, P < 0.005). Twenty workers from Colony A and 19 from Colony B were observed to engage in grooming and solicitation interactions during the study (Table 1). The distri­ butions of workers with small «colony mean costa length) and large (>colony mean costa length) wings into dominance categories (those dominant in all ob­ served interactions versus those submissive in some or all interactions) were similar in the two colonies (Table 1). When individuals from both colonies were pooled, workers with small wings were significantly more likely to be dominant in all observed social interactions than were workers with large wings (Likelihood ratio X2 = 7.49, d.f. = 1, P < 0.01). This difference was not due to the subordinate workers having been observed more often; the number of records ofsocial inter­ actions did not differ among workers in the two dominance categories (Wilcoxon Z = 1.74, d.f. = 1, P > 0.05). 46 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

COLONY A 0 10.0

-C) 0 00 0 E 9.0 0 0 0 8 0 9 -.c 0 90 -C) 0 0 'a; 8.0 00 o§ 0 80 0 ~ 00 o 0 0 9 § >­ § g o 9 8 0 0880 0 0 -g 7.0 00 00 9 .Q 0 0 a 000 I!­ 000 00 9 0 0 0 e 6.0 o 00 B 0 0 0 5.0 3.9 4.1 4.3 4.5 4.7 Costa vein length (mm)

cOLONYB 10.0 o o 0 o -~9.0 - .c 8.0 -C) '0; ~ 7.0 >­ "0 o .Q 6.0 l!­ e 5.0 o o 0

4.0 -+-___.r----r-.....o--..--....---r-_-..----.--..-----. 3.6 3.8 4.0 4.2 4.4 4.6 Costa vein length (mm)

Fig. I. Dry body weight in mg plotted against costa vein lengths in mm for P. occidentalis workers from two observation colonies. Mean (±SD; sample size) costa lengths were 4.3S(±0.14; n lOS) for Colony A and 4.30(±0.IS; n = 109) for Colony B. VOLUME 68, NUMBER 1 47

1.0

0.8 -CD "..> enCD .c 0.6 Q ..en ---0- Colony A CD --e-- Colony B ..:.::.. 0.4 Q ==.. -£l. 0.2

0.0 ...-----1f-----r----or-----"""T""------. o 5 10 15 20 Age (days) Fig. 2. Distributions of the age of first performance of behavioral acts on the outside surface of the nest by P. occidentalis workers from two colonies. The cumulative proportion of workers added to each colony observed engaging in outside nest tasks is plotted on the Y-axis.

Discussion Polybia occidentalis worker body size was negatively related to age of first performance of out-of-nest tasks. Faster passage through age polyethism or per­ formance ofrisky tasks by larger bodied workers appears to be a common pattern, documented in diverse eusocial insect lineages. Kerr and Hebling (1964) presented data suggesting that among Africanized honey bee (Apis mellifera adansonii) work­ ers, earlier performance of age-based tasks was associated with greater body size. Nowogrodzki (1984) reported not finding this pattern in honey bees, but presented no data. Cidecyan (1984; cited in Waddington, 1988) found that larger bodied honey bees foraged more frequently and differed from smaller bees in rates of performance ofin-hive tasks (the nature ofthese differences was not determined). Studies on bumble bees (Bombus agrorum, B. sy/varum, and B. Jucorum) showed that larger bodied workers were both more likely to forage and began foraging at a younger age than smaller workers (Brian, 1952; Free, 1955). Spradbery (1972) found that foragers of the yelIowjacket VespuJa germanica were larger than nest wasps during the growth phase ofcolony development. Why large body size might be associated with more rapid age polyethism is unknown, both with respect to adaptive value to the colony (if any; Waddington, 1988) and to the mechanisms that underlie the association. One possible mechanism linking body size with division of labor is dominance interactions among workers, which appear to influence division oflabor in diverse insect societies (Jeanne, 1991). Experimentally assembled honey bee colonies with 48 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Table 1. Numbers oflarge winged (individuals with > colony mean costa length) and small winged (individuals with < colony mean costa length) workers observed engaging in grooming and solicitation interactions. Only dominant: worker was the active participant in every grooming or solicitation interaction observed. Some submissive: worker was passive in at least some of the interactions in which she engaged.

Only dominant Some submissive Total Colony A Large winged 4 3 7 Small winged 12 I 13 Totals 16 4 20 Colony B Large winged 5 5 10 Small winged 8 I 9 Totals 13 6 19 varying proportions of workers selected for dominant and subordinate behavior exhibited decreased brood production, comb building, and food hoarding with increasing representation of dominant bees (Hillesheim et aI., 1989). Studies on Polistes paper wasps (reviewed in Reeve, 1991) and bumble bees (Honk et aI., 1981; Doom and Heringa, 1986) suggest a link between low social dominance rank and increased probability of foraging; in some Polistes spp. older workers, which are often smaller, tend to be dominant (Strassmann and Meyer, 1983; Hughes and Strassmann, 1988; S. O'D., pers. obs.). Yellowjacket workers (Vespula spp.) engage in aggressive mauling and more subtle food solicitation interactions, which may incite subordinate individuals to perform tasks outside the nest (Mon­ tagner, 1966; Akre et aI., 1976). The studies on Vespula did not examine the relationship ofbody size with dominance, but Montagner (1966) noted that dom­ inance status did not correlate well with age or ovarian development. We found that smaller P. occidentalis workers were more likely to be dominant in social interactions. Our observations are consistent with the pattern expected ifdominance interactions based on body size influence the rate ofage polyethism, such that subordinate workers move out of the nest at an earlier age. Larger­ bodied wasps apparently move away from opportunities for direct reproduction into more "worker-like" behavioral roles (West Eberhard, 1981) at an earlier age. These results should be considered as preliminary, since the intensity of inter­ actions, and the identity and size of both interacting partners, were not recorded. The pattern of dominant smaller-bodied workers has also been noted in several Po/isles species, but in most of these cases body size was confounded with order of emergence and worker age (reviewed in Reeve, 1991). More data on social interactions among workers and their relation to body size are needed to assess the importance of these factors in regulating division of labor in monomorphic eusocial insects. Our data suggest that dominance interactions among workers playa wider role in polyethism than previously recognized. Acknowledgments Thanks to Keith Waddington and two anonymous reviewers for helpful com­ ments on an earlier version of the manuscript. Research was supported by a VOLUME 68, NUMBER I 49

tropical fellowship (to S.O'D.) from the Organization for Tropical Studies/Pew Charitable Trust, USDA Hatch Grant 3544 (to R.L.J.), and a postdoctoral fel­ lowship from the NSF funded University ofCalifornia at Davis Behavior Research Training Grant (to S.O'D.).

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