Insectes soc. 47 (2000) 158–163 0020-1812/00/020158-06 $ 1.50+0.20/0 © Birkhäuser Verlag, Basel, 2000
Insectes Sociaux
Research article
Dominance hierarchy in colonies of Belonogaster juncea juncea (Vespidae, Polistinae) M. Tindo 1 and A. Dejean 2 1
2
Laboratoire de Zoologie (Université de Yaoundé I, B.P. 812 Yaoundé, Cameroun) Current address: International Institute of Tropical Agriculture, Humid Forest Ecoregional Center, B.P. 2008 Yaoundé-Messa, Cameroon, e-mail:
[email protected] or
[email protected] LEEC (Université Paris 13, Villetaneuse, France) Current address: Laboratoire d’Ecologie Terrestre (UMR 5552), Université Toulouse III, 118 route de Narbonne, F-31062 Toulouse cedex, France.
Received 21 September 1998; revised 23 September 1999; accepted 28 October 1999.
Summary. Dominance behaviours and the structure of the dominance hierarchy in colonies of Belonogaster juncea juncea are described. The frequency of these behaviours was recorded for each individual by noting “all occurrences of rare behaviours”. Among the dominance behaviours recorded, the most frequent was “grappling,” which represents 69.8% of the total number of dominance interactions observed. The overall frequency of dominance behaviours was 0.4 ± 0.36 and 2.99 ± 1.97 per hour per individual in pre- and post-emergence colonies, respectively. The data were submitted to the Appleby test, which shows the hierarchy’s highly significant level of linearity. The a female showed the highest frequency of dominance interactions and initiated 81.5% and 48.8% of the total dominance interactions observed in pre- and postemergence colonies, respectively. A weekly record of the frequency of dominance interactions throughout the biological cycle shows that this frequency was highest before or immediately after the disappearance of the dominant female. The most aggressive dominance behaviour (falling fights) was observed only during the weeks after the dominant’s departure. This behaviour is thus involved in the establishment of the hierarchy and not in its maintenance, which is accomplished by means of less aggressive behaviours. Key Words: Dominance hierarchy, linearity, Belonogaster, Polistinae.
gaster) and swarm-founding species. In independent-founding species, reproductive division of labour is established by means of physically aggressive behaviours, while in swarmfounding species it is established by means of pheromones. Since Pardi’s seminal study (1948), dominance hierarchy in colonies of wasps belonging to the genus Polistes has received considerable attention (Reeve, 1991; Théraulaz et al., 1992). The most dominant female is the principal if not the sole egg-layer while the others take care of the brood. This is also the case for many species of the genus Mischocyttarus and Ropalidia, but not for Ropalidia marginata, where the egg-layer is not the most behaviourally dominant individual in the colony (Chandrashekara and Gadagkar, 1991; Gadagkar, 1991). In the African genus Belonogaster, only the studies by Marino Piccioli and Pardi (1970) on B. grisea and by Keeping (1992) on B. petiolata examined the aggressive interactions between individuals in the same colony. The subspecies B. j. juncea is widespread on the buildings on the campus of the University of Yaoundé I, where it has an associative mode of colony foundation (Tindo et al., 1997a). Studies on its social organisation have shown behavioural role differentiation among associated foundresses and among individuals belonging to post-emergence colonies (Tindo and Dejean, 1997; Tindo et al., 1997b). In this paper, we describe dominance behaviours and the dynamics of the dominance hierarchy with a further view toward clarifying the influence of this hierarchy on such behavioural differentiation.
Introduction Eusociality can be observed in three wasp subfamilies: Stenogastrinae, Polistinae and Vespinae (Carpenter, 1991). The subfamily Polistinae has been subdivided by Jeanne (1980) into independent-founding (including the genus Belono-
Materials and methods Observations were conducted under natural conditions on eight associations of two foundresses, 15 associations of three, five associations of more than three and 10 post-emergence colonies, where the number
Insectes soc. Vol. 47, 2000 of individuals varied from nine to 16. The colonies studied were attached to a wall or a ceiling on buildings on the campus of the University of Yaoundé I and were observed in situ. The wasps were marked with a spot of quick-drying paint, either on the thorax or on the wings to aid in the recognition of individuals. The technique of noting “all occurrences of rare behaviours” (Altmann, 1974) was used to record the frequency of the behaviours. Individuals were observed during 5-minute sessions. On a given day, three sessions were held in the morning and three in the afternoon. The starting time of each session was chosen randomly between 6:00 a. m. and 11:00 a. m. and 3:00 p. m. and 6:00 p. m., the periods of highest activity (Tindo and Dejean, 1998). This routine was repeated over four days, for a total of 2 h observation on each individual. Thus four successive days were needed to complete the two-hour sampling session. To facilitate data collection, we chose nesting sites with many colonies. During the study of the colony cycle and behavioural profiles, 30 min observation on each individual was performed per week, during 29 weeks. The 30 min were obtained through the compilation of six 5-minute sessions. Additional information was obtained opportunistically, through four naturally-occurring instances of queen replacement. The ranking of all of the individuals of a colony according to a scale of linear dominance is a common practice used by ethologists to describe hierarchical relationships within groups. To justify this practice, some authors underline the remarkable linearity (transitivity) of the dominance hierarchy among observed groups. According to Appleby (1983), this method distorts original data because it oversimplifies dominance relationships between individuals. It only shows the asymmetry between individuals and completely ignores inverse interactions and the frequency variation of these interactions between pairs of individuals. This makes it necessary to objectively estimate the linearity of the dominance hierarchy each time before drawing any conclusions about possible transitivity. We used the hierarchical linearity test proposed by Appleby (1983) to verify the hierarchical linearity of the colonies. After the test, the method of linearisation of Premnath et al. (1990) was used to attribute a hierarchical rank to each individual. This method allows the dominance index (Id) to be calculated for each member of a colony according to the following formula: n
m
n
∑ Bi + ∑ ∑ bji + 1 i=l j=l i=l Id = 0049 n p n ∑ L i + ∑ ∑ lji + 1 i=l
j=l i=l
∑Bi corresponds to the total of the frequencies when a subject dominated other members of the colony; ∑bji is the total of the frequencies indicating when the individuals dominated by a subject dominated, in their turn, other members of the colony; “1 to m” indicates the total number of individuals dominated by the subject; ∑Li is the total of the frequencies indicating that the subject was dominated by the other members of the colony; ∑lji is the total of the frequencies indicating the individuals who dominated the subject and who, in their turn, were dominated by other members of the colony; and “1 to p” indicates the total number of individuals who dominated the subject. Appleby (1983) denoted the high probability of a linear dominance hierarchy in small groups based solely on chance. A strict linear ranking among three, four, and five individuals has a 75%, 37.5% and 11.7 % chance, respectively, of appearing. As a result, no linearity test would be significant in these groups. According to Appleby, one can only test the statistical significance of linearity (to a 5% threshold) for groups of six or more individuals. Therefore, we only undertook linearity tests for post-emergence colonies. For pre-emergence colonies, we merely ranked foundresses according to a linear dominance scale based on the sequence of observed acts of dominance.
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Results Description of types of behaviour a. Dominance acts: (1) Falling fights: a fight between two adults on the nest triggering a fall to the ground. The wasps separate from one another and take up fighting again until one wins (WestEberhard, 1969). This behaviour, which always begins with grappling, can sometimes (one case observed) lead to the death of one of the adversaries. (2) Grappling: one wasp climbing on top of another, the two wasps wrestle while biting and trying to sting one another (Marino Piccioli and Pardi, 1970). The dominant (or the winning) individual is the one who succeeds in bending its abdomen and putting its gaster on the thorax of the other. (3) Biting a nestmate: using the mouthparts to lick or bite another female on the head, thorax, abdomen or wings (West-Eberhard, 1969). This is sometimes followed by grappling. (4) Chasing: movement towards another female with wings raised; can also be followed by grappling. (5) Antennal palpation: antennation of the head, thorax, abdomen or wings of another female. b. Subordination acts: (1) Submission: submit to grappling. (2) Akinesis: posture with antennae and body lying flat on the nest after having submitted to a dominance act (Marino Piccioli and Pardi, 1970). (3) Avoidance: avoiding another nestmate after having submitted to a dominance behaviour.
Frequency of the appearance of these behaviours These different types of behaviours were adopted at variable frequencies. For the 755 occurrences of dominance acts observed, the falling fight represented 0.9 %, grappling 69.8 %, biting 25.2 %, chasing 1.4 %, and antennal palpation 2.7 %. For 81.6 % of the 527 cases of grappling, one of the two females involved was on the nest and the other arrived carrying liquid substances (females arriving without a load are rarely involved in trophallaxis with other nestmates). For the 18.4 % remaining cases, the two individuals involved were present on the nest, as in all of the cases for the other behaviours. Females carrying other provisions were rarely grappled. For each individual, all occurrences of dominance acts recorded over the two hours of observation were summed and divided by two to obtain the dominance frequency per hour; subordination behaviour was treated in the same way to obtain the subordination frequency.
Structure of the dominance hierarchy in pre-emergence colonies The frequency of acts of dominance ranged from 0 to 2.5 with a mean of 0.4 ± 0.35 per hour per wasp (N = 28). All
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Dominance hierarchy in Belonogaster juncea juncea
Figure 1. The average frequency of dominance and subordinate acts as a function of hierarchical rank in trigynous foundations of B. j. juncea (N = 15). The a female initiated 81.5% of all of the dominance acts observed
Structure of the hierarchy in post-emergence colonies The mean frequency of acts of dominance per hour per wasp was 2.99 ± 1.97 (range: 0 to 32.5; N = 35 individuals). With the exception of seven cases out of 530, the observed interactions were asymmetrical, with the dominant female retaining her position such that there was no ambiguity concerning one female’s status of dominant or subordinate in relation to another. Nonetheless, we tested our results using Appleby’s procedure, which enabled us to show that for all of the tested colonies the circular triads (non-transitive) have a probability of P < 10 –9 of appearing. There is thus a very highly significant hierarchical linearity in colonies of B. j. juncea that enabled ranking of individuals according to a scale of linear dominance. To illustrate the dynamics of dominance in the colonies studied, we calculated the mean frequency of acts of dominance and of subordination for each hierarchical rank. These frequencies varied with hierarchical rank (Fig. 2). Females in the first three ranks initiated 82.6% of all of the sequences of dominance observed, with the a females alone initiating 48.8%. The frequencies of acts of dominance directed at other females by the a ones also varied with the recipient’s hierarchical rank (Fig. 3). b females were always dominated by the a females. Gamma individuals were subject to fewer
Figure 2. The average frequency of dominant and subordinate interactions as a function of hierarchical rank in post-emergence colonies of B. j. juncea (N = 10). The a female initiated 48.7 % of all of the sequences of dominance interactions observed. Those from the three highest ranks initiated 82.6 %
acts of dominance from the a females than were b females. Fourth- and fifth-ranked females were subject to fewer acts of dominance from the highest-ranked females than were second- and third-ranked females. Nevertheless, females from the next lowest rank were subject to numerous acts of dominance from the highest-ranked females (example: R7 and R11; Fig. 3). The stability of the hierarchy The frequencies of acts of dominance adopted by dominant females and workers varied from one week to another (Fig. 4a). In fact, the dominant female began to dominate the workers two days after their emergence (Fig. 4a, first peak). The frequency of acts of dominance initiated by the dominant female was almost always greater than that of acts initiated by workers (Fig. 4a). This frequency increased considerably during the week preceding the disappearance of the dominant female (18 th week). During this week the dominant females initiated 88% (22/25) of dominant acts observed in the
Mean frequency/h
of the sequences of observed interactions showed a clear asymmetry with the same female remaining dominant (38 cases). The illustration of the dynamics of individual interactions in pre-emergence colonies is based on the analysis of frequencies of acts of dominance and subordination only in the trigynous associations. In the associations of more than three females, the hierarchy was difficult to define, because of the passivity of some females. The average frequency of acts of dominance and of subordination varied as a function of hierarchical rank in these associations (Fig. 1). The a females initiated 81.5% of all of the dominance sequences observed. The b females were always subject to acts of dominance from the highest-ranked ones. Gamma females were subject to more acts of dominance from b females (65%) than from a females (35%).
Hierarchical rank
Figure 3. The average frequency of dominance interactions received from the a female as a function of rank of recipient. The b female received more interactions than the gamma female who, in her turn, received more than the fourth-ranked female. Nonetheless, lower-ranked females also received a considerable number. The upper bar represent the standard deviation
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Figure 4. Weekly variation in the frequency of dominance acts during the development of Colony N ° FN00 (4 a). The dominant foundress began to dominate workers two days after their emergence (fifth week). This frequency increased considerably during the weeks preceding and following the dominant’s departure (D) from the colony (18 th and 20 th weeks). The most aggressive dominance behaviour, the falling fight, is observed only in the weeks following the dominant’s departure (4 b). During this period, the dominance intensity increased in the colony (4 c)
a
b
c colony. Every individual received at least one dominance act from the a female. After the disappearance of this a female (Fig 4a; 19 th week), the replacement female (which was not the oldest) initiated about 87.5% of all dominance acts observed, including falling fights. It was nonetheless during this week (Fig 4b; 20 th week) that we observed falling fights. After ranking the dominance acts recorded according to their dominance intensity, we computed the mean dominance intensity per week. The result shows that the intensity of the dominance increased during the week after the disappearance of the a female (Fig. 4c) when the other individuals fought amongst themselves to replace her.
Discussion Types of behaviour Aggressive acts are frequent in independent-founding Polistinae and make up an important part of their social organisation. These behaviour patterns have been well-described in many species, but their intensity and frequency vary widely (Gadagkar, 1991; Reeve, 1991; Röseler, 1991). Dominance interactions have been thought to be much milder in some species of Ropalidia (Itô, 1983; 1985) and Mischocyttarus (Jeanne, 1972; Itô, 1984). In Ropalidia marginata, highly
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aggressive dominance interactions such as falling fights increase in both the frequency and intensity during the early stage of colony foundation and immediately after queen replacement (Premnath et al., 1996). According to Premnath et al. (1996), the belief that Ropalidia is generally less violent than Polistes may reflect the fact that most studies on these genera have focused on different stages of colony founding. In B. j. juncea, the recording of the frequency of dominance behaviours throughout the colonial cycle shows that this frequency increases considerably during the weeks preceding the disappearance of the dominant female or just after, when the other females fight amongst themselves to replace her. This is also the case in the early stage of colony foundation. Falling fights, which have never been recorded in either B. grisea or B. petiolata, were observed in B. j. juncea, but only during the period of queen replacement. The work on B. grisea did not focus on the queen replacement period, but Keeping (1997) studied the behaviour of B. petiolata during this period and falling fights were not observed. This may indicate that the establishment of dominance hierarchy is more severe in B. j. juncea than in other studied species of Belonogaster. The types of behaviours used during the establishment of the hierarchy in B. j. juncea are quite different from those used for its maintenance. Falling fights may play a role in the establishment of the hierarchy, while its maintenance is realised through other less aggressive types of behaviour such as grappling, biting, and chasing. Structure of the dominance hierarchy Contrary to B. petiolata, where grappling plays a role in only 6.2% of the cases in the definition of the hierarchical structure (Keeping, 1992), in B. j. juncea it represents 69.6% of the cases. Nonetheless, we have seen that 81.6% of the 527 cases of grappling correspond to the arrival of a foraging worker carrying sugary substances. Grappling behaviour has been observed in B. grisea (Marino Piccioli and Pardi, 1970), in Mischocyttarus (Itô, 1984), and in many species of Ropalidia (Darchen, 1986; Gadakar, 1980; Gadagkar and Joshi, 1982; Itô, 1983; Turillazzi and Marucelli Turillazzi, 1985). Itô (1983; 1993) underlined the ambiguity of this behaviour, called “kiss” in Ropalidia fasciata because it is sometimes directed by subordinate foundresses towards the dominant foundress. But we observed that during trophallaxis (between non-foragers and returning foragers) in B. j. juncea, individuals can adopt postures ranging from face-to-face exchanges to grappling. Thus, grappling seems to have other meanings beside food exchange. Further investigations, especially concerning grappling and trophallaxis would help to clarify the meaning of this behaviour. Here, we consider grappling as the most aggressive behaviour after falling fights. The Appleby test permitted us to confirm that the dominance hierarchy is significantly linear in B. j. juncea colonies, as has been previously noted in B. grisea and B. petiolata (Marino Piccioli and Pardi, 1970; Keeping, 1992).
Dominance hierarchy in Belonogaster juncea juncea
A correlation between the order of emergence of females and their hierarchical ranking has been shown for several Polistes species (Litte, 1977; Théraulaz et al., 1992). Thus the order of emergence is used by these authors to attribute a hierarchical ranking to individuals. For our observations, having been conducted on already-established colonies (individuals of uncertain age), this parameter was not tested and we used the dominance index to rank individuals (which helps to avoid, among other things, relatively frequent inversions between hierarchy and the order of appearance of individuals). Marino Piccioli and Pardi (1970) showed that in B. grisea the frequency of dominance acts by the a female directed at her subordinates decreased with their hierarchical rank, with the b female being subject to more acts than the others. The a females of B. j. juncea also directed more dominance acts towards second-ranked females than towards third-ranked females, etc., but lower-ranked females were also the target of a great number of dominance acts by the a female (Fig. 3). Stability of the hierarchy The hierarchy in B. grisea is unstable, with the females changing hierarchical position over time (Marino Piccioli and Pardi, 1970). This is not the case in B. petiolata (Keeping, 1992) nor in B. j. juncea, where the hierarchy is stable once it has been established. The long period of observation on the latter species permitted us to note the successive replacement of the dominant female (pers. obs.), corresponding possibly to what Marino Piccioli and Pardi (1970) called the unstable hierarchy of B. grisea. The cause of the disappearance of the dominant is not clear but we observed one case where the old dominant attempted several times to rejoin the nest without success. This indicates that death is not the sole cause of this disappearance, and that the dominant position can be actively taken over by other females. This fact explains the increasing frequency of dominance behaviours during the weeks that precede the disappearance of the dominant female or just after, when the other females fight amongst themselves to replace her.
Acknowledgements This research was supported by a project (CAMPUS-108/CD/90) from the French Ministry of Co-operation and a grant from the “Cellule des Relations internationales de l’Université Paris 13”. We would like to thank Michel Pratte for his constructive suggestions on the first manuscript.
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