Behavioral Profiles Related to Dominance Hierarchy in Associated ...

Journal of Insect Behavior, Vol. 11, No. 6, 1998

Behavioral Profiles Related to Dominance Hierarchy in Associated Foundresses of Belonogaster juncea juncea (F.) (Hymenoptera: Vespidae) Maurice Tindo1 and Alain Dejean2,3 Accepted January 26, 1998; revised May 20, 1998

This study was conducted to examine the phenomenon of task partitioning among associations of foundresses of the primitively eusocial wasp Belonogaster juncea juncea (F.). The time-activity budget for five main behavioral categories (foraging, building, feeding, inactivity, and reproduction) for each foundress belonging to trigynic associations was recorded using the instantaneous scanning technique. After ranking the individuals on the basis of agonistic encounters, data were submitted to a canonical discriminant analysis. The results show behavioral differences between individuals of each rank. The proportion of time allocated to foraging behavior is a good rank index. The females of the first rank spent less time on foraging behavior and significantly more time (13.6% of their time) on reproductive behavior than females of other ranks. The females of the second rank also spent less time on foraging behavior and showed a tendency toward building behavior. The females of the third rank spent significantly more time (77.28% of their time) on foraging behavior. The behavioral profile of each foundress was therefore determined by its rank on the dominance scale. KEY WORDS: polistine wasps; Belonogaster; foundation of colonies.

INTRODUCTION Among polistine wasps, Jeanne (1980) distinguished independent-founding from swarm-founding species. In the former case, queens initiate new colonies singly 1Laboratoire

de Zoologie, Universite de Yaounde I, B.P. 812 Yaounde, Cameroun. (UMR CNRS 5552) Universite Toulouse III, 118 Route de Narbonne, 31062 Toulouse, France. 3To whom correspondence should be addressed. 2 LET

845 0892-7553/98/1100-0845$15.00/0 © 1998 Plenum Publishing Corporation

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or in small groups (without the aid of workers) and exert a physical dominance over their nestmates (no use of a pheromonal means of control). Independentfounding polistine wasp species were recorded among five genera (Belonogaster, Mischocyttarus, Parapolybia, Polistes, and Ropalida), but most of the studies on social organization concerned the two latter genera (Gadagkar, 1991; Reeve, 1991). In many Polistes species a linear dominance hierarchy is established among associated females (Pardi, 1948; Strassmman et al., 1984). This hierarchy determines the type of work accomplished by each individual in the colony. For instance, the dominant females tend to specialize in tasks which do not require them to leave the nest, such as egg-laying (minimize their risk of encountering predators in the field), whereas the others become sterile and act as workers (auxiliaries). The genus Belonogaster, which is African, belongs to the primitively eusocial Polistinae and comprises species which build nests consisting of a single comb. The social behavior of two species of Belonogaster, one tropical and the other from a temperate climate, is already well known (Marino Piccioli and Pardi, 1970; Keeping, 1990, 1992). In both species the colony is organized on the basis of a linear hierarchy, with the egg layer occupying the top-ranking position. Concerning B. juncea the only behavioral description made to date was by Roubaud (1916). The subspecies B. j. juncea is widely distributed throughout the campus of the University of Yaounde I (Cameroon), where it practices both haplometrotic and pleometrotic colony foundation (Tindo et al., 1997a; Tindo and Dejean, 1998). A linear dominance hierarchy also exists among associated foundresses, and five main behavioral forms have been distinguished among associated foundresses of B. j. juncea, namely, foraging, building, feeding, inactivity, and reproductive behavior (Tindo and Dejean, 1995, 1997). In this paper, after ranking all individuals according to the postures adopted during two-wasp encounters, the distribution of different behavioral forms among individuals belonging to each rank is established. MATERIALS AND METHODS Field studies were conducted from October 1992 to May 1994 on 15 associations of three females. The colonies studied contained eggs or eggs and larvae but no pupae. The selected nests were found on buildings of the campus of the University of Yaounde I. All females of each colony were individually labeled with two spots of quick-dry paint on the mesoscutum or on the wings. Three sampling methods were used (see Altmann, 1974). (1) Ad libitum sampling was employed to construct the behavioral repertoire of B. j. juncea (28 h of observations in total). (2) Instantaneous scanning was used to record the most frequent items such as a time-activity budget (i.e., proportion of time spent in each behavioral state). The sampling session was 2 h/individual. One

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session was subdivided into 24 subsessions of 5 min each. Every minute the type of activity in which each wasp was engaged was noted. The beginning of each subsession was chosen randomly between 0600 and 1100 h and 1500 and 1800 h, both of which are periods of high activity. (3) During the scanning, it was possible to record all occurrences of rare behaviors (principally dominancesubordinate behaviors). In the end, the compilation of all sequences provided the frequency of each behavioral event. Ranking the Wasps The compilation of the occurrence of all acts of dominance behavior results in the dominance frequency of each individual. In the associations of two females, the hierarchical rank is easily determined. In trigynic associations, the individual that dominates both of the others has the first rank, while the individual that is dominated by both of the others occupies the third rank. The remaining female, which is dominated by only the highest-ranking female, therefore occupies the second rank. Behavioral Repertoire According to the ad libitum sampling technique, the behavioral repertoire of B. j. juncea comprises 39 items (Tindo and Dejean, 1997). During the present sampling period, corresponding only to the foundation and the colonies, 27 items belonging to six categories of behavior were recorded and used for analysis. Beside the dominance subordinate behaviors, the 19 other items were reorganized using the hierarchical cluster analysis method (Tindo and Dejean, 1997). Thus the following five main behavioral roles were defined. Foraging: (1) absence from nest; (2) land with liquid material, which is followed by trophallaxis with one or several nestmates; (3) land with prey; (4) give prey. Building: (5) land with pulp; (6) malaxate pulp; (7) cell enlargement; (8) pedicel reinforcement; (9) Giravolta—pedicel rubbing with the abdominal sternites (Marino Piccioli and Pardi, 1970). Feeding: (10) receive prey; (11) malaxate prey; (12) feed larvae; (13) solicitation of larval secretion. Inactivity: (14) guarding; (15) resting; (16) self-cleaning. Reproduction: (17) inspection (antennate the nest pedicel or cells containing eggs, larvae, or pupae); (18) cell initiation; (19) egg laying. Note that the latter two behaviors were associated during cluster analysis (both are initiated by the alpha female), although they are quite different. Data Analysis After ranking the three associated individuals, in order to establish the relationship between the rank and the different behavioral forms displayed in a

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colony, the data were submitted to a canonical discriminant analysis, which yielded a new set of variables called canonical variates that maximize the between-rank variations, thus resulting in the best separation between ranks.

RESULTS Behavioral Profiles Related to the Dominance Hierarchy In the numerical results of the canonical discriminant analysis (Table I), two canonical variates were determined. The first variate accounts for 62.12% of the total variance and has foraging behavior (weighting = 0.844) as its dominant term. This axis opposes mainly individuals that performed on-nest activities (negative side) to those that performed off-nest activities (positive side) (Fig. 1). The second canonical variate accounts for 37.67% of the total variance. It opposes inactivity (positive side), its dominant term (weighting = 0.710), to activities of feeding, foraging, and reproduction (negative side), with the weighting of the latter being the highest of the three (-0.698). Nevertheless, five reproductive females of 15 are situated on low positive values (Fig. 1), as reproductive females are frequently inactive (see Fig. 2). As a consequence, the most significant differences between hierarchical rank can be described using foraging behavior, which has "absence from nest" as the main component. Therefore, each individual can be assigned to one hierarchical rank according to the proportion of time spent outside the nest. Figure 1 shows the projection of individuals in the plane formed by the two

Table I. Results of Canonical Discriminant Analysis: Coordinates of Different Behavioral Forms on the Two Canonical Variates and Percentage and Cumulative Variance Explained by These Variates Canonical variate Behavioral item Foraging Reproduction Inactivity Building Feeding % variance explained cumulative variance (%)

1

2

0.844 -0.636 -0.597 -0.263 -0.208

-0.435 -0.698 0.710 0.063 - 0.285

62.12 62.12

100

37.67

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Fig. 1. Results of canonical discriminant analysis; projection of individuals belonging to three dominance ranks in the plane formed by the two canonical variates. The three ranks are well separated, with 88.88% of individuals correctly assigned to their respective ranks.

Fig. 2. Mean behavioral profiles of each hierarchical rank. The proportion of time spent on foraging behavior is a good rank index. Statistical comparisons between the mean time-activity budgets (percentage) of the three hierarchical ranks (Friedman test followed by an a posteriori test). NS, nonsignificant difference; *P < 0.05; **P < 0.01; ***P < 0.001.

Activity Foraging Building Feeding Inactivity Reproduction

First rank

9.16 3.61 3.44 67.17 12.61

± ± ± ± ±

9.51 3.49 4.20 14.04 4.71

1st vs. 2nd NS NS NS * *

Second rank 28.39 ± 2.39 ± 1.17 ± 63.06 ± 4.63 ±

20.68 2.74 1.72 16.61 2.92

2nd vs. 3rd ** * NS * *

Third rank 78.08 0.17 0.50 20.94 1.33

± ± ± ± ±

16.75 0.65 0.99 15.44 1.75

1 st vs. 3rd *** * NS *** ***

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canonical variates, with 88.89% of the females being correctly assigned to their original rank. Two individuals of the first rank were assigned to the second, and vice versa. Only one female of the third rank was assigned to the second. Thus the behavioral profile of the second may be the most similar to that of the first. Main Features of Each Dominance Rank The mean proportion of time spent on each behavioral form by individuals belonging to a given dominance rank and the results of statistical comparisons calculated by means of a Friedman test followed by an a posteriori test are presented in Fig. 2. Note that feeding behavior did not vary significantly between ranks, while other behavioral forms generally did. The first rank comprises individuals that spent significantly more time (12.61% of their total time) on reproductive behavior than other ranks and less time (9.16%) on foraging behavior. Individuals belonging to the second rank had a behavioral profile intermediate between the first and the third. Like females of the first rank, they spent more time being inactive on the nest and less time (4.63%) on reproductive behavior and showed a tendency toward building activity. The females of the third rank spent time mainly on foraging behavior (77.08%). DISCUSSION Among associated foundresses of polistine wasps, a linear dominance hierarchy determines the role filled by each individual (Pardi, 1948; Strassmann et al., 1984; Pratte, 1989). The aggressive behavior of the alpha females toward the beta and the gamma females inhibits the ovarian development and the endocrine activity of the corpora allata of the latter two (Roseler et al., 1984, 1986). In P. dominulus, alpha females spent significantly more time on behaviors related to reproduction and attendance of the nest, while beta females spent a greater amount of time on cell elongation than other classes (Pratte, 1989). In this study, focused on trigynic associations, the analysis of the timeactivity budget for five behavioral forms displayed in the colony shows that there are behavioral differences between associated foundresses in relation to their dominance ranking. The main difference between these females belonging to three hierarchical ranks corresponds to the proportion of time allocated to foraging behavior. This behavior is highly correlated with the first canonical variate, which accounts for 62.12% of the total variance between individuals. The highest-ranking individuals, which spent little time (9.26% of their total time-activity budget) on foraging behavior, load negatively on the first variate, while the third-ranked individuals, which spent most of their time (77.28%) on this behavior, load positively on this variate. The second-ranked individuals


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have an intermediate loading. According to these results, an individual's rank can be easily determined using the proportion of time spent on the nest as shown in Polistes metricus (Gamboa and Dropkin, 1979) and in P. dominulus (Pratte, 1989). Note that the dominant female is relatively easy to identify, as she performs abdominal wagging, a behavior rarely observed in subordinates from preemergence colonies and never in those from postemergence colonies (Tindo et al., 1997b). However, 5 of 45 females were not correctly assigned to their respective ranks. This may be due to the fact that the colonies studied were not exactly at the same stage of development. Colonies at the larval stage needed more food than those at the egg stage. Thus the absence of larvae in the nest created a tendency for females to stay on the nest and therefore have a profile similar to that of females of higher ranking. The results shown here were conducted on relatively early preworker, multiple-foundress associations (absence of pupae). They throw some light on the organization of associated foundresses of Belonogaster, made up of a dominant female (egg-layer; performs abdominal wagging) and, among the subordinate females, true foragers, which spent most of their time on foraging, and females with an intermediate status, which spent less time on foraging and most of their time on the nest, inactive. We cannot exclude that the behavioral profiles may change when pupae appear as recorded in several Polistes species (Reeve, 1991). ACKNOWLEDGMENTS We are grateful to Dr. E. Francescato (University of Florence, Florence, Italy) for her help in the field and her numerous suggestions and to Dr. J. L. Durand for statistical advice. This study was supported by a project (CAMPUS 108/CD/90) of the French Ministry of Co-operation. REFERENCES Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour 49: 227-265. Gadagkar, R. (1991). Belonogaster, Mischocyttarus, Parapolybia, and independent-founding Ropalidia. In Ross, K. C., and Matthews, R. W. (eds.), The Social Biology of Wasps, Comstock, Ithaca, NY, and London, pp. 149–190. Gamboa, G. J., and Dropkin, J. A. (1979). Comparisons of behaviors in early vs late foundress associations of the paper wasp, Polistes metricus (Hymenoptera: Vespidae). Can. Entomol. 111: 919-926. Jeanne, R. L. (1980). Evolution of social behavior in the Vespidae. Annu. Rev. Entomol. 25: 371-396. Keeping, M. G. (1990). Colony foundation and nestmate recognition in the social wasp Belonogaster petiolata. Ethology 85: 1-12. Keeping, M. G. (1992). Social organization and division of labour in colonies of the polistine wasp, Belonogaster petiolata. Behav. Ecol. Sociobiol. 31: 211-224. Marino Piccioli, M. T. (1970). The extraction of the larval peritrophic sac by the adults in Belonogaster (Hymenoptera Vespidae). Monit. Zool, Ital. 2 (Suppl.): 203-206.

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Marino Piccioli, M. T., and Pardi, L. (1970). Studi sulla biologia de Belonogaster (Hymenoptera, Vespidae). I. Sull'ethogramma di Belonogaster griseus (Fab.) [sic.]. Monit. Zool. Ital. 3: 197-225. Pardi. L. (1948). Dominance order in Polistes wasps. Physiol. Zool. 21: 1- 13. Pratte, M. (1989). Foundresses association in the paper wasp Polistes dominilus (Christ) (Hymenoptera: Vespidae). Effects of dominance hierarchy on the division of labour. Behaviour 111: 208–219. Reeve, H. K. (1991). Polistes. In Ross, K. C., and Matthews, R. W. (eds.), The Social Biology of Wasps, Comstock, Ithaca, NY, and London, pp. 99-148. Roseler, P. F., Roseler, I., Strambi, A., and Augier, A. (1984). Influence on insect hormones on the establishment of dominance hierarchies among foundresses of the paper wasp, Polistes gallicus. Behav. Ecol. Sociobiol. 15: 133-142. Roseler, P. F., Roseler, I., and Strambi, A. (1986). Studies of the dominance hierarchy in the paper wasp, Polistes gallicus (L.) (Hymenoptera, Vespidae). Monit. Zool. Hal. 20: 283-290. Roubaud, E. (1916). Recherches biologiques sur les guepes solitaires et sociales d'Afrique. La genese de la vie sociale et l'evolution de l'instinct maternel chez les vespides. Ann. Sci. Nat. Zool. (Ser. 10) 1: 1-160. Strassmann, J. E., Meyer, D. C., and Matlock, R. L. (1984). Behavioural castes in the social wasp Polistes exclamans (Hymenoptera: Vespidae). Sociobiology 8: 211-224. Tindo, M., and Dejean, A. (1995). Structure de la hierarchie de dominance chez Belonogaster juncea juncea (Vespidae: Polistinae). Actes Coll. Insectes Soc. 10: 21-29. Tindo, M., and Dejean, A. (1997). Behavioural roles and task partitioning in the primitively eusocial wasp: Belonogaster juncea juncea (Hymenoptera: Vespidae). Behav. Proc. 41: 201-210. Tindo, M., and Dejean, A. (1998). Rhythm of activity and feeding behavior of the wasp Belonogaster juncea juncea (Hymenoptera: Vespidae). Sociobiology 32 (in press). Tindo, M., D'Agostino, P., Francescato, E., Dejean, A., and Turillazzi, S. (1997a). Associative colony foundation in the tropical wasp Belonogaster juncea juncea (Hymenoptera: Vespidae). Insectes Soc. 44: 365-377. Tindo, M., Francescato E., and Dejean, A. (1997b). Abdominal vibrations in a primitively eusocila wasp Belonogaster juncea juncea (Hymenoptera: Vespidae). Sociobiology 29: 255-261. Tindo, M., Turillazzi, S., and Dejean, A. (1997c). Behavioural role differenciation in the primitively eusocial wasp Belonogaster juncea juncea (Hymenoptera: Vespidae). J. Insect Behav. 10: 571-580.