of E. ruidum, collected in "Rancho San Antonio" in Rozario Izapa near Tuxtla. Chico in the Mexican state of Chiapas, were reared in plaster nests placed in an.
Ins. Soc. 43: 111-118 (1996)
1015-1621/96/020111-08 $1.50 + 0.20/0 9 1996 Birkh~iuser Verlag, Basel
Research article
Polyethism within hunters of the ponerine ant, Ectatomma ruidum Roger (Formicidae, Ponerinae) B. Schatz 1, J.-R L a c h a u d 1,2 and G. Beugnon 1 1 Laboratoire d'Ethologie et de Psychologie Animale. C.N.R.S. - U.R.A. 1837 Universit~ Paul Sabatier, 118, route de Narbonne, 1:-31062 Toulouse Cedex, France 2 El Colegio de la Frontera Sur, Apdo postal 36, Tapachula 30700, Chiapas, Mexico K e y words: Predation, polyethism, food exchange, behavioral flexibility, E c t a t o m m a ruidum.
Summary During laboratory experiments, two categories of prey-foraging workers were found in Ectatomma ruidum: stingers and transporters. When numerous live drosophila were offered to the ants, one group of hunters specialized in killing the prey and another in transporting simultaneously the dead drosophila to the nest. Sometimes, there was a transfer of prey by a stinger towards a transporter, after an active soliciting of the transporter by antennation or by using the forelegs. We found high positive correlations between the colony size and the number of ants in each subcaste. A negative correlation existed between the colony size and the proportion of hunters. However, the proportion of workers in the two behavioral subcastes of hunters was stable in spite of differences in colony size. The phylogenetic interest of this type of cooperative predation is discussed.
Introduction Division of labor has b e e n one of the most studied p h e n o m e n a in ants (H611dobler and Wilson, 1990) and within-caste specialization such as that found in foraging workers appears as the highest degree of polyethism (Oster and Wilson, 1978; Rissing, 1981). Nurses and foragers are the main behavioral subcastes. However, m a n y other subdivisions are possible within b o t h these large behavioral subcastes. In P a c h y c o n d y I a caffraria, for example, foragers can be subdivided in sugar collectors and hunters, in the latter case this can in turn be subdivided into two categories: "stingers" and "transporters" (Agboga and Howse, 1992). In the neotropical ponerine ant Ectatornma r u i d u m , these subdivision a p p e a r to be even m o r e complex. The foragers of this species are distributed into five b r o a d behavioral categories: hunters, sugar collectors, patrollers, non-foragers and unspecialized intermediates (Schatz et al., 1993; 1995). Within the sugar collectors, various specializations can develop according to the location of the food sources and the t e m p o r a l availability of these sources (Schatz et al., 1994; 1995; Passera et
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al., 1994). In addition, behavioral specializations may also exist within the hunter category. In this paper, the behavior of the foragers of Ectatomma ruidum that are not involved in sugar collecting is examined and evidence for a polyethism within the hunters similar to that found in P caffraria is shown. The consequences of the high level of behavioral flexibility encountered in this species are discussed from a phylogenetic viewpoint.
Method
Ectatomma ruidum is a dominant terricolous species (Lachaud, 1990), common in coffee or cocoa plantations, where it preys on a large variety of arthropods (membracids, crickets, flies and termites) (Weber, 1946; Lachaud, 1990). Seven colonies of E. ruidum, collected in "Rancho San Antonio" in Rozario Izapa near Tuxtla Chico in the Mexican state of Chiapas, were reared in plaster nests placed in an experimental room under controlled conditions (temperature: 25 ~ + 1 ~ humidity: 60 % + 5 %; photoperiod: 12:12 L/D). Hunters were offered fruit flies (Drosophila melanogaster) as prey. The experimental set-up was composed of a foraging area (30 • 30 cm) connected at one end with the nest and at the other end with the hunting area. About 35 cm separated the entry of the nest from the hunting area consisting in a petri dish with a diameter of 9 cm where the prey were provided and which was only 1 cm high in order to prevent prey from escaping and to facilitate the predation by ants. During preliminary observations, all workers performing any kind of predatory act were individually marked with color spots of enamel paint on their thorax and gaster. During the test, we placed live drosophila in the hunting area with an approximate constant proportion of 3 to 5 drosophila per hunting worker (number was estimated during preliminary tests). Every 10 minutes over a 2-hour period, we noted all behavioral acts of each marked ant present in the hunting area. The behavioral specializations in a colony containing 240 workers were tested 3 times (with a 2-day interval between each test). The proportions of each behavioral subcaste were measured in the seven laboratory colonies and their relationship with the size of the colony was determined.
Results
Behavioral specializations Within the hunter subcaste, two behavioral specializations can easily be distinguished, according to the behavior performed with the highest frequency: "stingers" and "transporters" (Table 1): This strategy had a very high efficiency: over the three tests, 219 drosophila were killed (91.3 % of the prey available), of these 94.5 % (207 drosophila) were transported and 86.3 % brought into the nest. The difference between the number of killed prey and the number of prey actually brought into the nest can be accounted for by the existence of a saturation phenomenon related to the limited capacity of each colony to absorb large quantities of prey (Lachaud,
P o l y e t h i s m within h u n t e r s of Ectatomma ruidum
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Table 1. Number of behavioral acts performed by each behavioral subcaste of the foraging workers of a colony of 240 Ectatomma ruidum, during 3 tests. A total of 240 drosophila were offered as prey. The number of stingers and transporters corresponds to the total number of individuals which displayed at least once hunting behavior during the 3 tests B e h a v i o r a l acts
Killers (n = 6)
Transporters (n = 28)
Number of prey killings Number of prey transports
204 2
15 203
1990; Lachaud et al., 1990; Breed et al., 1990). This cooperative predation was exhibited for a distance which closely corresponds to the mean foraging distance in natural conditions (Lachaud et al., 1990). Moreover, the same cooperative behavior was observed during complementary tests for distances of i and 2 meters, and thus did not correspond to an artifact linked to the very short foraging distance. The predation sequence can be described as follows. Several hunters are generally present at the beginning of the test. Rapidly, two specializations emerge: stinging of live prey and transport of dead prey. Each "stinger" performs a typical sequence of attack as already described in this species (Lachaud, 1990) and in E. tuberculatum (D6jean and Lachaud, 1992): detection, localization, approach, antennation, seizure with the mandibles and stinging. Sometimes this sequence is interrupted by self-grooming. Once the prey is motionless, it is dropped on the ground and a new attack can begin again. Nevertheless, some stingers sometimes may keep the dead prey in their mandibles while engaging in a new attack, as in some other ponerine ants like Pachycondyla (= Termitopone) laevigata (Wheeler, 1936) and Paltothyreus tarsatus (Ddjean et al., 1993). Generally, dead prey lying on the ground are picked up by the "transporters". In some instances, a transporter can actively solicit a stinger by antennation, or occasionally by tapping it with its forelegs, in order for the stinger to transfer the prey. The prey are transportred one by one and dropped into the nest or given to another soliciting ant which blocks the passage to the nest entrance. Transporters then generally go back to the hunting area.
Behavioral subcaste proportions The proportion of workers in each behavioral subcaste of hunters was not significantly different among the seven colonies, i.e. on average: 22.8 % of hunters were stingers (X2=2.89; ns) and 77.2% of hunters were transporters (X2= 0.86; ns) (Table 2). There were significant positive correlations between the size of the colony and the number of stingers (r = 0.986; p < 0.001) and transporters (r = 0.970; p < 0.001) (Table 2). By contrast, the correlation was negative between colony size and the proportion of both behavioral subcastes of hunters within the colony (r = 0.931; p < 0.001 for the total proportion of hunters).
(84.2) (80.1) (77.4) (75.7) (77.1) (77.6) (74.7)
5.33 6.66 8.00 9.33 12.33 15.00 16.66
1.00 1.66 2.33 3.00 3.66 4.33 5.66
20 30 50 60 70 80 100
24 60 109 130 160 240 350
(15.8) (19.9) (22.6) (24.3) (22.9) (22.4) (25.3)
Average number of transporters and proportion within hunters in %
Average number of stingers and proportion within hunters in %
Number of prey items (drosophila)
Number of ants in the colony
6.33 8.33 10.33 12.33 16.00 19.33 22.33
(26.4) (13.9) (9.5) (9.4) (10.0) (8.1) (6.4)
Average total number of hunters and proportion within colony population in %
l'ahle 2. Number of workers of Ectatomma ruidum specializing as stingers or transporters within the hunter category, according to colony size. (Average values over three tests, see text)
N
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Discussion
Ectatomma ruidum is usually known as a solitary hunter (Lachaud et al., 1984; Lachaud, 1985), each forager remaining faithful to a particular portion of the colony's foraging area, at least for several days. When a forager encounters a food source, its response generally consists of shuttling repeatedly between the food source and the nest. Nevertheless, in some instances, when the food source is large in quantity or size and when the distance to the nest is short (Lachaud et al., 1990), an archaic form of mass recruitment can be used, sometimes involving trail laying (Pratt, 1989) and sometimes not (Lachaud, 1985) according to the type of food encountered (sugar or prey) and to the distance between the food source and the nest. In this study, our experiments show that a collective hunting strategy, intermediate between solitary hunting and recruitment, can also be used during predation on numerous small prey, involving a division of labor within the workers participating in hunting tasks. A study of individual behavior allowed us to distinguish two behavioral categories within the hunters: stingers and transporters. During our tests, drosophila were abundant and small prey, which stay in a particular location, unable to fly out, and thus can be compared with termites in natural conditions. Thus, it is not surprising to find among the hunters of E. ruidum the two behavioral subcastes (stingers and transporters) already identified in the termite hunting ponerine ant Pachycondyla caffraria (Agbogba and Howse, 1992). The possibility that such a within-caste specialization among the hunters of E. ruidum and R caffraria only rarely occurs in nature and is just a laboratory artifact resulting from the high density of easily caught prey cannot be discarded. However, these experiments at least show how such a system can arise in ponerine species. According to previous field experiments (Lachaud et al., 1990; and unpublished data), the 2-hours duration of each predation test as well as the size of the hunting area (9 cm in diameter) seem large enough to allow the activation of a high number of hunters. We could thus have expected a positive correlation between the colony size and the proportion of hunters involved in our experiments. However whereas we found high positive correlation values between the colony size and the number of transporters, as in R caffraria (Agbogba and Howse, 1992), as well as with the number of stingers, a negative correlation existed with the proportion of hunters. Such data allow us to distinguish between the direct effects of colony size and the indirect ones resulting from a modification of the social organization of the colony (i. e. proportion of the population and time-budget devoted to the essential task in the colony) and reflected by the decrease in proportion of the hunter group as the colony size increase (negative correlation). These results support the data reported for the same species by Lachaud and Fresneau (1987) which show that the larger the size of the colony the larger the size of the intermediate-inactive group within the nest and the smaller the size of the foragers group. Nevertheless, unlike in P. caffraria (Agbogba and Howse, 1992), the relative proportion of stingers and transporters among hunters remains stable (about 23 % and 77 % respectively) in spite of the differences in colony size. This stability suggests the existence of direct or indirect communication between the workers of both behavioral subcastes which enables a social regulation of the size of each subcaste. In a very similar way as that hypothesized for Pachycondyla apicalis in the case of social regtdation of nurses loss
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(Lachaud and Fresneau, 1987), the mechanism involved in our experiments may depend upon the competition for task performing: the larger the number of prey being killed in the hunting area, the fewer opportunities for other hunters to act as stingers. Many ponerine species prey solitarily and are, in many cases, opportunists in their choice of prey (Peeters and Crewe, 1987). However, several species use more complex hunting strategies, in which cooperation occurs during the transport of prey by several hunters or during the formation of raiding columns (Ldvieux, 1966; D6jean et al., 1993; Lachaud et al., 1994). The hunting strategy used by E. ruidum also involves cooperation via the existence of relays between stingers and transporters for carrying the dead prey, and between transporters and workers present at the entrance of the nest for introducing these prey into the nest. These two types of "uncoupled" cooperation, in which each ant acts individually and concurrently towards a common aim, with or without direct communication among individuals, can be considered as precursors of more complex forms of cooperation found in other ponerine ants like Paltothyreus tarsatus (H611dobler, 1984; D6jean et al., 1993) and in myrmicines (Agboga, 1982) or ecitonines (Franks, 1987), where more complex interindividual interactions occur among workers. Moreover, it should be noted that during the transfer of prey from the stinger to the transporter, the latter can use its forelegs during solicitation, a behavior only observed among ponerines in the case of food transfer in Odontornachus troglodytes (Lachaud and Ddjean, 1991). The use of the forelegs during food transfer is reminiscent of the ritualized food solicitation signals found in phylogenetically more advanced species like Myrrnica scabrinodis and Lasius emarginatus (Lenoir, 1973) and supports H611dobler's (1985) hypothesis concerning the evolution of the signals involved in social food exchange. The demonstration, in E. ruidum, of the possible existence (according to the circumstances) of a high degree of polyethism among foragers collecting sugar (Schatz et al., 1993, 1994, 1995; Passera et al., 1994; Beugnon et al., 1995) or hunting (these results), and the ability of this species to use some types of cooperation precursor of more complex forms found in myrmicines and ecitonines, provide new interesting arguments to support the very special interest towards the genus Ectatomrna which is considered ancestral to the Myrmicinae (Brown, 1958; Fresneau et al., 1982; Baroni-Urbani et al., 1992). Moreover, the degree of complexity reached by E. ruidum in the division of labor, along with its variety of foraging strategies, once again emphasizes the remarkable flexibility of behavior already pointed out in previous reports (Lachaud, 1985; Corbara et al., 1989; Breed et al., 1992; De Carli et al., 1994; Schatz et al., 1994).
Acknowledgements We thank Jos6 Antonio Lopez-Mendezand Carmelino Salvador for field assistancein collecting the coloniesof Ectatornma ruidum, and Don Erasmo de la Cruz for his hospitalityand for allowing us to collect at Rancho San Antonio. We are also grateful to V. Fourcassi6for his critical reading of the manuscript and to the two anonymousreferees who provided insightfuland constructive comments. This research was supported by grants of the "Sciencede la Cognition" (MESR) to B. S., the "Cognisciences"(CNRS) and PRESCOT programs to G.B. and J. P.L., and the "Conseil R6gional Midi-Pyr6n6es"to G.B.
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