predatory behavior in dominant arboreal ant species: the case of crematogaster sp.(hymenoptera:...

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Journal of Insect Behavior [joib] PP102-298890 March 1, 2001 20:56 Style file version Feb 08, 2000

Journal of Insect Behavior, Vol. 14, No. 2, 2001

Predatory Behavior in Dominant Arboreal AntSpecies: The Case of Crematogaster sp.(Hymenoptera: Formicidae)

Freddie-Jeanne Richard,1,2 Andre Fabre,1 and Alain Dejean1,3

Accepted August 14, 2000, Revised November 17, 2000

Crematogaster sp. is a dominant arboreal ant species that captures and re-trieves very large prey. Hunting workers forage collectively thanks to short-range recruitment. They detect prey by contact, then rapidly attack, seizingsmall prey by the body and large prey by a leg. In this study, almost all theactive prey were spread-eagled by several workers, even when small enoughto permit a single worker to easily master them. While certain workers spread-eagled the prey, others deposited venom on the prey body using their spatulatedsting (topical action of the venom). The well-developed arolia on the pretar-sus of workers’ legs have crucial importance for the success of prey capture(spread-eagling) and transport in an arboreal habitat. These results are com-pared with those known for other arboreal-dwelling generalist predator antspecies.

KEY WORDS: arboreal ants; Crematogaster; predatory behavior; Cameroon.

INTRODUCTION

Ants have evolved a large variety of foraging strategies depending on theirbehavioral repertoire and on parameters related to food sources (Traniello,

1LET (UMR-CNRS 5552), Universite Paul Sabatier, 118 route de Narbonne, 31062 ToulouseCedex 4, France.

2LECA (ERS 2041), Universite Paul Sabatier, 118 route de Narbonne, 31062 Toulouse Cedex4, France.

3To whom correspondence should be addressed. Fax: (33) 05 61 55 61 96. e-mail: [email protected].

271

0892-7553/01/0300-000271$19.50/0 C© 2001 Plenum Publishing Corporation



272 Richard, Fabre, and Dejean

1989; Holldobler and Wilson, 1990). The behavioral flexibility of the workerscan permit the provisioning colonies to adjust to environmental changes. Thisis the case when foraging workers adapt their behavior according to preycharacteristics (Dejean, 1987; Schatz et al., 1997).

Dominant arboreal ant species that belong to the subfamiliesFormicinae, Dolichoderinae, and Myrmicinae have very large, polydomouscolonies. They are characterized by a strong aggressiveness toward otherdominants at both intra- and interspecific levels. As a consequence, competi-tion for the control of space results in a three-dimensional mosaic distributionof their territories. They feed principally on the honeydew of Hemiptera ofthe ancient suborder Homoptera (i.e., sternorrhyncha, Cicadomorpha, andFulgomorpha) that they intensively tend, on extrafloral nectar when avail-able, and on prey belonging to different arthropod taxa (Holldobler andWilson, 1978; Holldobler and Lumdsen, 1980; Majer, 1993; Adams, 1994;Orivel and Dejean, 1999; Dejean et al., 2000).

Until now the predatory behavior of dominant arboreal ants has beenstudied only in the case of Oecophylla longinoda (Dejean, 1990; Holldoblerand Wilson, 1990; Wojtusiak et al., 1995). During hunting, numerous work-ers ambush prey on the leaves and branches of the supporting tree. Whena worker seizes a prey, the emission of an alarm pheromone attracts nest-mates situated in the vicinity. Each worker seizes the prey by an appendageor by the body and pulls backward. As a result, the prey is spread-eagled,then cooperatively retrieved, so that venom is not used (Dejean, 1990). Thisstrategy requires that workers have very powerful adhesive pads, or arolia,an indispensable feature of arboreal life (Orivel and Dejean, 1999).

We investigate here whether the characteristics of the predatory behav-ior of O. longinoda can be extrapolated to another dominant ant species,Crematogaster sp. We hypothesize that workers of this species are able tocapture and/or cooperatively retrieve large prey in spite of their very smallrelative size.

MATERIALS AND METHODS

Study Species

This study concerns a Crematogaster species that, although very fre-quent in southern Cameroon, has not been identified, so that we assigned thecode “tsapi” when we deposited voucher specimens in the Natural HistoryMuseum, London. The nests of Crematogaster sp. are built with carton inthe hollowed branches or trunks of relatively small trees (less than 15 m in



Predatory Behavior in Crematogaster sp. 273

height) situated along forest edges and even in villages and cities. After arain, the workers (3.25 to 5.05 mm in length) deposit on their supportingtree bark and leaves dark spots similar to those described as landmarks inOecophylla by Holldobler and Wilson (1978). Apparently the colonies donot surpass several dozens of thousands of individuals, but this is enough tooccupy the canopy of one or several small trees.

Predatory Behavioral Studies

We conducted a field study on four colonies, but mostly on one of theminstalled on a Cassia javanica (Cesalpiniaceae) in Yaounde (Cameroon). Ineach case, we first installed a plywood plate (80 × 40 cm) against the treetrunk at 80 cm in height. During 1 week, workers marked these plates thatwe then used as experimental territories.

We compared the behavior of the workers when confronted with ter-mites (Macrotermitidae) and grasshoppers of different sizes. The tested ter-mites included workers (4–4.7 mm long; n= 52) and soldiers (4.7–5 mmlong; n = 42) of Microcerotermes fuscotibialis and workers (5–7.2 mm long;n = 54), small soldiers (7.5 mm long; n = 55), and large soldiers (13 mmlong; n= 63) of Macrotermes bellicosus. The tested grasshoppers were small(3–5 mm long; n = 18), medium-sized (6–11 mm long; n = 30), and large-sized (12–19 mm long; n = 38) tettigoniids (Homorocoryphus sp.). We cutoff the tibia of their posterior legs to prevent them from jumping. These preywere between one and five times larger than the Crematogaster sp. workers(3.25- to 5.05-mm total length). The behavioral sequences were recorded bydirect observation from the introduction of the prey into the center of thehunting areas (on the plate of plywood) until they were captured and re-trieved to the nest. A full repertoire of behavioral sequences was first estab-lished during preliminary experiments. Referring to this full list, we recordedeach behavioral act performed (detection, opening of the mandibles, attack,seizure, nestmate recruitment, spread-eagling the prey, and cutting up andtransporting the prey) and the part of the prey body seized by the ants (seealso Orivel et al., 2000). This allowed us to build a flow diagram with tran-sition frequencies between each behavioral act. We also calculated the per-centages of cases for the prey body part seized between the different preytested.

Statistical tests were made from raw data using Fisher’s exact tests(StatXact 3.1 software). Appropriate probabilities were adjusted for thenumber of simultaneous tests, using the sequential Bonferroni procedure(Rice, 1989).




RESULTS

Predatory Sequences

Detection–Palpation. The prey were always detected by contact, suggest-ing that in this case vision plays only a minor role (Figs. 1 and 2). Termiteswere never antennated, while grasshoppers were during 1 to 3 s.

Attack–Seizure. Seizure was accomplished by a very rapid lunge, andonly small Microcerotermes workers were seized mostly by the body, whileall other prey were generally seized by a leg (Fig. 3). We therefore noted

Fig. 1. Sequences of behavioral events observed in Crematogaster sp. during attempts at cap-turing various termites. PE, prey escape.




Fig. 2. Sequences of behavioral events observed in Crematogaster sp. during attempts at cap-turing grasshoppers of different sizes. D-P, detection by contact and palpation.




Fig. 3. Parts of the prey body seized by Crematogaster sp. workers. Comparisons: seizure by a legversus another part of the prey body (calculated P value using Fisher exact tests and sequentialBonferroni procedure).

B C D E F

A 0.0025∗ 1.1 × 10−8∗∗∗ 6.5 × 10−9∗∗∗ 2.0 × 10−11∗∗∗ 6.8 × 10−13∗∗∗B 0.009 (NS) 0.0011∗∗ 5.9 × 10−5∗∗∗ 3.5 × 10−6∗∗∗C 0.50 (NS) 0.22 (NS) 0.034 (NS)D 1.00 (NS) 0.30 (NS)E 0.37 (NS)

a significant difference when comparing Microcerotermes workers with allother tested prey and nonsignificant differences between the grasshoppersand the different castes of Macrotermes as well as between these castes(Fig. 3). After antennal contact or later after attack, the prey sometimesescaped or were abandoned.




Recruitment. The capture of a prey by one worker was noted only forsmall grasshoppers (16.7% of the cases), while in the other cases nestmateswere recruited at short range. The worker that discovered a prey waggedits flexed gaster above its thorax and head, probably releasing an alarmpheromone. Nestmates in the surrounding area immediately became excitedand ran in several directions, but mostly toward the worker that discoveredthe prey. After the first attempt at seizure, the workers that discovered preywere able to immobilize them thanks to the strenght of their adhesive padsand claws, despite the difference in size, until nestmates situated in the vicinityarrived. The first ant often continued to immobilize the prey even after thearrival of further workers.

Recruited workers first came into contact with the lifted gaster of therecruiting worker, then seized the prey in turn and pulled backward. If theprey struggled, they also lifted and wagged their gasters. As a result, new nest-mates were attracted, so that the number of workers recruited was regulatedby the prey’s reaction.

Spread-Eagling and Cutting Up the Prey on the Spot. Each recruitedworker seized a part of the prey, then pulled backward, resulting in thespread-eagling of the prey. Only 1.8% of Mi. fuscotibialis workers and 50.1%of the small grasshopper (3.5–5 mm) were cooperatively retrieved withoutbeing spread-eagled. The number of workers involved in spread-eagling theprey increased with prey size. It varied from two workers for the captureof small termites to eight workers for the 12- to 19-mm-long grasshoppers(Fig. 4). This behavior is possible thanks to a very well-developed aroliumat the extremity of the pretarsus of each leg and curved claws, permittingthe workers to adhere well to different substrates (Fig. 5). The last recruitedworkers did not participate in spread-eagling the prey, but climbed on theprey to spread their venom on its body with their spatulated stings (Fig. 5)and began to cut up the prey on the spot. The workers retrieved whole onlysmall prey (3.7% of the termite workers, 2.3% of the Mi. fuscotibialis soldiers,and 33.3% of the small grasshoppers).

The duration of the spread-eagling and cutting up of the prey was from2 to 4 min in most cases, but in one case lasted up to 157 min. This dependedon the prey size, cuticle toughness, and number of recruited workers. As arule, the legs and the antennae of the prey were severed first and immediatelyretrieved by the workers. In some cases, additional nestmates were recruitedat short range and the remaining parts of the corpse were dissected intosmaller pieces. Small cut-up pieces of prey were retrieved by single workers,while large pieces or entire prey were retrieved cooperatively by 2 to 15 work-ers. We never noted long-range recruitment for the capture of the testedprey.




Fig. 4. Number of workers participating in spread-eagling the prey according toits size.

Fig. 5. Electron micrograph of the pretarsa of a Crematogaster sp. worker showing the well-developed arolium (black arrow) and spread, horn-shaped claws (A) and the spatula-shapedsting (B). Scale bar = 50 µm.




Efficiency of the Predatory Strategy Adopted

For termites, the percentages of successful prey capture decreased ac-cording to size and subcaste (Figs. 1 and 2), ranging from a total of 66.7and 74.4% of the cases for the workers and soldiers of Mi. fuscotibialis,respectively (nonsignificant difference; Table I), to 34.9% for the largeMa. bellicosus soldiers (nonsignificant difference from both small soldiersand workers, but a significant difference between the latter two; Table I).Grasshoppers were captured at a rate of 88.9% for small individualsand 52.6% for large individuals, the difference being significant. LargeMa. bellicosus soldiers, very aggressive and agile, were frequently abandonedby the ants (63.9%). This occurred mostly during the solitary phase, prior toany recruitment. As a result, we noted significant differences when comparingthem to Microcerotermes and small grasshoppers, while other comparisonsresulted in nonsignificant differences (Table I).

When a prey succeeded in escaping, the ants usually became extremelyexcited. The workers made very tight circles around the point of prey en-counter, with an obvious increase in their speed and the sinuosity of theirpath.

The number of prey escapes decreased from one step of the predatorysequence to the next. After recruitment, prey escape was exceptional, sug-gesting that the likelihood of the prey escaping decreased strongly as thenumber of recruited workers increased. Note that most of the prey that es-caped were then attacked and successfully captured by other workers thatwere joining the first zone of attack.

DISCUSSION

The well-developed arolia in the form of adhesive pads and spread,horn-shaped claws on the pretarsa of Crematogaster sp. workers allow goodadherence to the substrate, permitting them to immobilize, spread-eagle,and retrieve large insects, as has been noted for Oecophylla (Freeland et al.,1982; Wojtusiak et al., 1995). Other arboreal-dwelling Crematogaster speciesas well as Oecophylla have been noted to adhere very well to a smooth surface(Federle et al., 2000).

In this study, Crematogaster sp. always detected the tested prey by con-tact, resulting in a high proportion of prey escape at this stage of the predatorysequence. Detection of the prey by contact has been also noted in two otherarboreal ants (but nondominant species): Polyrhachis laboriosa, a diurnalFormicinae, and Pachycondyla goeldii, a nocturnal Ponerinae (Dejean et al.,1994; Orivel et al., 2000). On the other hand, Oecophylla workers detect prey




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by sight at long range, even when small. The approach with the mandiblesopen is rapid and direct (Dejean, 1990).

The reaction of Crematogaster sp. workers to an escaping prey by in-creasing both their speed and the sinuosity of their path seems general inpredatory ants and is known as “reserve behavior” (Dejean and Corbara,1998; Orivel et al., 2000, and papers cited therein). The circular paths aroundthe point of prey encounter, combined with the greater speed and increasein the aggressiveness of the workers, raise the chance of again finding thenkilling the escaped prey, particularly when the workers are able to use theirvenom during the first attack.

Crematogaster sp. uses a group hunting strategy for a large range of preythat are first seized by a leg in the majority of the cases. Only very small preywere captured by individual workers and were seized mostly by the body. Asa result, although prey were detected by contact, the workers that discoveredthem were able to adapt their seizure to the prey size.

Each foraging worker is surrounded by several nestmates situated withinthe range of short-range recruitment. Indeed, the density of hunting workerswithin the territories of dominant arboreal ants is usually very high, mak-ing short-range recruitment efficient (Holldobler and Wilson, 1978; Dejean,1990). We noted here that capture was successful exclusively if the first antwas able to keep hold of the prey until the arrival of its nestmates. Grouphunting with recruitment is considered to be more evolved than solitary hunt-ing because it implies cooperation between workers and enables a greaterrange of prey sizes that a species can exploit (Traniello, 1989; Schatz et al.,1997). This species captures very large prey items, as do Oecophylla andMyrmicaria opaciventris (Wojtusiak et al., 1995; Kenne et al., 2000). In con-trast, in Polyrhachis laboriosa, a nondominant arboreal formicine ant, work-ers forage mainly individually. When they kill large prey that they cannottransport solitarily, they recruit nestmates at long-range to retrieve them(Dejean et al., 1994).

In conclusion, as has been noted for O. longinoda (Dejean, 1990;Wojtusiak et al., 1995), the group hunting strategy of Crematogaster sp. work-ers permits them to capture prey of a wide range of sizes thanks to short-rangerecruitment and the spread-eagling of the prey. The capture of a prey by asingle worker is exceptional and concerns only very small insects. Neverthe-less, O. longinoda killed the prey only by stretching, while Crematogaster sp.workers used their venom and cut up the prey on the spot.

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Adams, E. S. (1994). Territory defense by the ant Azteca trigona: Maintenance of an arborealant mosaic. Oecologia 97: 202–208.




Dejean, A. (1987). Effect of prey size on predatory behavior of Serrastruma serrula(Hymenoptera: Formicidae, Myrmicinae). Sociobiology 13: 295–306.

Dejean, A. (1990). Prey capture strategy of the african weaver ant. In Vander Meer, R. K., Jaffe,K., and Cedeno, A. (eds.), Applied Myrmecology, a World Pespective, Vol. 43, WestviewPress, Boulder, pp. 472–481.

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Holldobler, B., and Lumdsen, C. J. (1980). Territorial strategies in ants. Science 210: 732–739.Holldobler, B., and Wilson, E. O. (1978). The multiple recruitment systems of the African weaver

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Holldobler, B., and Wilson, E. O. (1990). The Ants, Harvard University Press, Cambridge, MA.Kenne, M., Schatz, B., Durand, J.-L., and Dejean, A. (2000). Hunting strategy of a generalist

ant species proposed as a biological agent against termites. Entomol. Exp. Appl. 94: 31–40.Majer, J. D. (1993). Comparison of the arboreal ant mosaic in Ghana, Brasil, Papua New Guinea

and Australia: Its structure and influence of ant diversity. In LaSalle, J., and Gauld, I. D.(eds.), Hymenoptera and Biodiversity, CAB International, Wallingford, pp. 115–141.

Orivel, J., and Dejean, A. (1999). L’adaptation a la vie arboricole chez les fourmis. Ann. Biol.38: 1–18.

Orivel, J., Souchal, A., Cerdan, P., and Dejean, A. (2000). Prey capture behavior of the arborealponerine ant Pachycondyla goeldii (Hymenoptera: Formicidae). Sociobiology 35: 131–140.

Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43: 223–225.Schatz, B., Lachaud, J. P., and Beugnon, G. (1997). Graded recruitment and hunting strate-

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Traniello, J. F. A. (1989). Foraging strategies of ants. Annu. Rev. Entomol. 34: 191–210.Wojtusiak, J., Godzinska, E. J., and Dejean, A. (1995). Capture and retrieval of very large prey

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predatory behavior in dominant arboreal ant species: the case of crematogaster sp.(hymenoptera:...

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