Journal of Chemical Ecology, Vol. 16, No. 10, 1990

CASTE-DEPENDENT REACTIONS TO SOLDIER DEFENSIVE SECRETION AND CHIRAL ALARM/RECRUITMENT PHEROMONE

IN Nasutitermes princeps

Y V E S R O I S I N , 1'4 C . E V E R A E R T S , 3 J . M . P A S T E E L S , l a n d

O . B O N N A R D 3

~Laboratoire de Biologie Animale et Cellulaire, C.P~ 160 Universitd Libre de Bruxelles

50 av. F.D. Roosevelt 1050 Bruxelles, Belgium

3 Laboratoire de Zoologie Universit~ de Bourgogne, UA-CNRS 674

6 bd. Gabriel 21000 Dijon, France

(Received October 24, 1989; accepted April 30, 1990)

Abs t rac t - -The soldier frontal gland secretion of Nasutitermes princeps induces strong short-range caste-specific alarm and attraction in both soldiers and workers. Soldiers are excited and patrol the surroundings of the source. The secretion per se does not induce ejection of additional secretion. Large workers of the second stage or older are massively attracted when tested in homogeneous groups. They focus their activities much more accurately than the soldiers around the source. The workers' reaction is less intense in the presence of soldiers. Large and small workers of stage 1 scarcely react at all to the secretion, whether tested in homogeneous or mixed groups. These results suggest the following complementary roles of soldiers and workers in defense. The first line of defense is provided by soldiers, which immobilize and incapacitate mobile enemies with their sticky secretion. Defense then is completed by older large workers as they eliminate the source of disturbance. The absence of reaction of young workers, small or large, confirms previous reports on age polyethism in Nasutitermes observed in other contexts: young workers tend to stay in the nest. Alarm reactions are elicited by a source of (+)-~-pinene, the major monoterpene in the secretion, while its enantiomer, almost absent from the secretion, induces a much weaker reaction.

Key Words--Nasutitermes princeps, Isoptera, Termitidae, termites, defense, alarm recruitment, pheromone, c~-pinene, chirality, polyethism.

2To whom correspondence should be addressed.

2865

0098-0331/90/1000-2865506.00/0 �9 1990 Plenum Publishing Corporation

2866 ROISIN ET AL.

INTRODUCTION

In many Nasutitermitinae, the soldiers are able to squirt a glue onto their ene- mies through their elongated rostrum. This defensive secretion, produced by the soldiers' frontal gland usually consists of a mixture of mono- and diterpenes (Prestwich, 1979, 1983), although sesquiterpenes are also present in some spe- cies (Prestwich and Collins, 1981; Valterova et al., 1987, 1988; Everaerts et al., in preparation). Monoterpenes are toxic to insects by topical application and vapor exposure (Everaerts et al., 1988a, and references therein). They are also irritant and may lead the termites' enemy to further entangle itself by scratching the sprayed area. Moreover, they reduce the evaporation rate of the monoterpenes, prolonging their action (Eisner et al., 1976).

Besides its purely defensive role, the frontal gland secretion has in some instances been shown to elicit alarm among the members of the colony. For example, if a squashed soldier head is placed in the vicinity of a foraging col- umn of Hospitalitermes monoceros, most termites turn back and run away (Maschwitz and Mfihlenberg, 1972). According to Vrkoc et al. (1978), the introduction of various monoterpene vapors in cultures of Nasutitermes costalis and N. rippertii induces the release of additional frontal gland secretion by the soldiers. Various alarm reactions triggered by soldier defensive secretion also have been reported in other nasute termites (Ernst, 1959; Moore, 1974; Eisner et al., 1976; Stuart, 1981; Mill, 1983), or in termites belonging to other subfamilies (Moore, 1968). However, the frontal gland secretion does not elicit alarm reaction in Nasutitermes ephratae (Maschwitz, 1966).

The frontal gland secretion of N. princeps (Desneux), a common species in northeastern New Guinea, has been extensively studied (Braekman et al., 1980; Dupont et al., 1981; Roisin et al., 1987; Everaerts et al., 1988b, 1990). The frontal secretion of Nasutitermes princeps consists of 89 % diterpenes and 11% monoterpenes. (+)-o~-Pinene accounts for more than 80 % of the mono- terpenic content, according to the samples, and its optical purity reaches 99.5 % (Everaerts et al., 1990), as recently observed by Lindstr6m et al. (personal communication) in N. ephratae and N. nigriceps.

In this paper, we will focus our attention on the behavioral effects of the frontal gland secretion on the various castes of N. princeps, and, in addition, we will examine the "pheromonal role of (+)-~x-pinene compared to its enan- tiomer, absent from the natural secretion.

METHODS AND MATERIALS

Materials. Arboreal nests of N. princeps were collected around Hansa Bay, Bogia District, Papua New Guinea. Termites to be used in bioassays were kept in large nest pieces on a water-trapped table and fed with pieces of wood. They

TERMITE ALARM PHEROMONES 2867

remained active and in good condition for at least one week, after which they were discarded and replaced by new ones.

The standard monoterpenes were commercially available compounds (Fluka AG); their GC purity was above 99%. The optical purity of (+) - and (-)-o~-pinene were, respectively, 92% ([a]~ ~ = 48 ~ and 85% ([o!] 2~ = 45~ based on the value reported by Comyns and Lucas (1957).

Methods. The experimental setup is shown in Figure 1. Groups of 40 indi- viduals selected according to their caste and age (see Results) were put in 9-cm Petri dishes, whose bottom was covered with filter paper. On one side of the dish, a glass tube filled with water and plugged with hydrophilous cotton pro- vided moisture, and a small piece of wood provided food and a substrate on or around which the termites invariably gathered (Figure 1A). A circle (33 mm diameter) was drawn with a soft pencil on the filter paper at the opposite side of the dish. A small hole was drilled in the top of the Petri dish, above the center of the circle, allowing the introduction of the item to be tested, i.e., either a paper impregnated with natural secretion or a droplet of hexane solution of monoterpenes (1% v/v). The termites were left undisturbed for a few hours before being tested.

Natural secretions were obtained by squeezing soldier heads with forceps. The droplet of secretion oozing at the nasus tip was collected on a small square (4 mm 2) of filter paper. Once three soldiers had been squeezed, another square

,6, B

FIG. 1. Attraction of large workers (LW2+) by soldier secretion (after photographs). (A) Situation observed before the introduction of the secretion [a: glass tube filled with water providing moisture, b: piece of wood, c: circle (33 mm diameter), d: small hole drilled in the top of the Petri dish]. (B) Situation 35 sec after the introduction of a piece of filter paper impregnated with the secretion (e).

2868 ROISIN ET AL.

of filter paper was used to cover the secretion and so prevent it from sticking accidentally to a termite leg and being dragged.

A Hamilton microsyringe was used to introduce 0.5/~1 of either bidistilled hexane as a blank, or 1% hexane solution of (+) - or ( - ) -~-pinene. In N. prin- ceps, 0.005 t~l (the test amount) is approximately the average amount of (+) - o~-pinene contained in three soldier heads.

The number of individuals inside the circle was noted every 30 sec or every minute for 3 to 5 min after introduction of the tested paper or droplet of solution.

Most experiments were binary comparisons: 20 experimental Petri dishes were prepared, of which 10 would receive one treatment and 10 another. All dishes were treated in short succession, and the same treatment was never repeated more than four times in a row, to ensure a sufficient alternation. This procedure was adopted in order to apply both treatments under similar condi- tions and so obtain two independent series of results suitable for comparison. Indeed, the reactions of the termites showed quantitative but not qualitative variations when tests were performed with insects from different nests, at dif- ferent times. In one experiment, described in Figure 4 below, three treatments were compared following the same principle. All graphs show the average num- bers, with standard error bars, of individuals inside the experimental circle dur- ing the course of the bioassays. After each experiment, the termites, pieces of wood, and filter papers were discarded and the glass tubes and the Petri dishes were cleaned with alcohol.

Four categories of individuals were tested: soldiers, large (female) workers of the first instar (LW1), large workers of the second instar or older (LW2+) , and small (male) workers of the first instar (SW1). Older small workers are very scarce in N. princeps (see Roisin and Pasteels, 1986, for a detailed description of polymorphism and postembryonic development in this species).

RESULTS

Response of Various Castes of N. princeps to Soldier Secretion. The intro- duction of a virgin paper never elicits any reaction. When tested alone, older large workers quickly rush toward a filter paper impregnated with soldier secre- tion (Figure 1B, see also Figure 4b below). The reaction reaches its maximum after 60-90 sec and then gradually subsides. Comparative tests with mixed groups of workers of different subcastes show that LW2 + react much more markedly than LW1 (Figure 2) and SW1 (Figure 3). Mixed groups of young workers (LW1 and SW1) hardly display any reaction at all.

Figure 4 presents the results of comparative tests between LW2 + and sol- diers in either homogeneous or mixed groups. In homogeneous groups, LW2 + proceed en masse toward the soldier secretion (Figure 4b). Pure groups of sol-

TERMITE ALARM PHEROMONES 2 8 6 9

6J

4

2-

0 0 1 2 :3 4 5 min

FIG. 2. Comparative attractiveness of soldier secretion to large workers of different stages: number of workers around the source over time. Mixed groups of 20 large work- ers of stage 2 or older (LW2+, n) and 20 large workers of stage 1 (LW1, D). Mann- Whitney U test: P < 0.001 (0.5-4 rain), P < 0.01 (5 min).

4

0 1 2 3 4 5min

FIG. 3. Comparative attraction of large and small workers to soldier secretion: number of workers around the source over time. Mixed groups of 20 LW2 + (J) and 20 small workers of stage 1 (SWl, O). Mann-Whitney U test: P < 0.001 (0.5-1.5 rain), P < 0.01 (2 rain), P < 0.05 (3-5 rain).

diers display excitement and attraction, yet their reaction is less precisely focused on the test paper, and relatively few individuals remain within the experimental circle (Figure 4a). The soldiers were never observed to squirt their secretion during the tests. Interestingly, the reaction of LW2 + in mixed groups of work- ers and soldiers (Figure 4c) is much weaker than in pure worker groups (Figure 4b).

Response of N. princeps LW2 + to (+)-and (-)-a-Pinene. The massive reaction of LW2 + was used to quantify the response to solutions of chiral c~-pinene.

Pure n-hexane elicits some reaction in N. princeps workers. However, the addition of 1% (+)-o~-pinene greatly increases their response. The maximum response is reached sooner (30 sec) and the reaction fades out faster that with natural secretion (Figure 5). (+)-ot-Pinene is more active than its enantiomer, (-)-~-pinene (Figure 6). Note that in our assays, the reaction to (-)-o~-pinene might even have been enhanced by impurities of ( +)-~-pinene, since the optical purity of the available ( - ) -a-pinene was only 85 %.

2870 ROISIN ET AL.

4 t o

12 �84

p i i J

0 - 0 1 2 3 4 5 rain

FIG. 4. Comparative attractiveness of soldier secretion to soldiers (A) and large work- ers of stage 2 or older (LW2+, B): number of individuals around the source over time. (a) Homogeneous group of 40 soldiers. (b) Homogeneous group of 40 LW2 +. (c) Mixed group of 20 LW2 + and 20 soldiers. Mann-Whitney U test: Soldiers (a v s c) NS; workers (b vs c) P < 0.01 (0.5 min), P < 0.001 (1-3 rain), P < 0.05 (4-5 rain).

DISCUSSION

An alarm effect has been assigned to the frontal gland secretion of several termite species. However , the so-called " a l a r m " behaviors vary widely accord- ing to the species. These various reactions could depend on the context in which the behaviors were observed and also on interspecific differences. For instance, in N. costalis, defensive recruitment is mediated by the trail pheromone pro-

10

5-

T

0 1 2 3 rain

FIc. 5. Attractiveness of (+)-c~-pinene in 1% hexane solution (U) to LW2 + compared with hexane blank (A). Number of LW2 + around source over time. Mann-Whitney U test: P < 0.05 (0.5 rain), P < 0.01 (1-1.5 rain), NS (2-3 rain).

I t ~ I n i

0 1 2 3 rain

TERMITE ALARM PHEROMONES 2871

FI6.6. Compared attractiveness of 1% hexane solutions of (+)-c~-pinene (11) and ( - ) - c~-pinene ([1) to LW2 +. Number of LW2 + around source over time. Mann-Whitney U test: P < 0.01 (0.5 rain), P < 0.05 (1.5 rain), NS (1 rain, 2-3 min).

duced by the sternal gland of the soldiers, whereas both "frontal and sternal gland pheromones have a pronounced effect on arresting mot ion" (Traniello, 1981). In N. exitiosus, soldiers converge toward an item sprayed with soldier secretion; the workers, however, are much less attracted than soldiers (Eisner et al., 1976). In N. corniger, only soldiers are attracted by the secretion, while workers remain in or retreat to the nest (Stuart, 1981).

In contrast, in N. princeps, both large workers and soldiers are attracted by the soldier secretion, but the two castes react in a different way, which can be correlated to their complementary roles in defense. Excited soldiers patrol

2872 Rorsnq ZT AL.

the vicinity of the source over a broader area than the workers, which are more precisely attracted toward the source of monoterpene. This reaction of the sol- diers would increase the probability of encounters with mobile enemies. Inter- estingly, the release of their secretion is not triggered by an immobile item, even impregnated by their secretion. This contrasts with the observations reported by Ernst (1959) and Vrkoc et al. (1978), but agrees with those of Eisner et al. (1976) and Traniello (1981). The role of the workers would be to eliminate the enemies immobilized by the soldiers. Indeed, the workers often isolate the source of disturbance by covering it with building material, and/or by constructing partitions. This, of course, does not imply that the workers will not participate in defense by biting an enemy with their reach. Several authors have shown that workers can be good fighters, especially efficient in termite- termite contests (Andrews, 1911; Eisner et al., 1976; Thome, 1982; Traniello and Beshers, 1985). The much lower reaction of large workers in mixed groups including soldiers is intriguing. It suggests that workers can perceive, at very close range and by another cue that the secretion, the presence of soldiers and will react mainly after soldiers have been mobilized. A comparable delayed reaction of workers was reported by Traniello (1981) during food recruitment in N. costalis. In this species, the differential responses of soldiers and workers depend on their reaction threshold to the trail pheromone: workers need a higher concentration of trail pheromone than soldiers to leave the nest (Traniello and Busher, 1985).

In this paper, we have investigated the short-range reaction to defensive secretion, but not a possible long-range recruitment to the site of disturbance. Defensive recruitment by trail pheromone in N. princeps remains a possibility, which was not tested by our experimental setting.

The nest structure of arboreal Nasutitermes, characterized by wide open- ings between adjacent chambers, is especially suitable for an airborne short- range communication system, allowing rapid diffusion of the recruitment pher- omone as well as troop movements (Deligne and Pasteels, 1982). An exactly opposite situation occurs in the mandibulate Nasutitermitinae Armitermes cha- gresi, whose soldiers block the narrow passages between nest chambers with their head: their defensive secretion consists of low volatile macrocyclic lac- tones devoid of pheromonal properties (Traniello et al., 1984).

The weak reaction of young, either large or small, workers could be expected. In species where several worker subcastes are present, some division of labor is common. Such a polyethism can involve trail-laying and trail-fol- lowing (Pasteels, 1965; Traniello, 1981), nest repair, foraging (McMahan 1970, 1977; Watson and McMahan, 1978), and food gathering and processing (Bad- ertscher et al., 1983). As a rule, the older, most pigmented workers perform most of the extemal chores, while the youngest ones usually work inside the

TERMITE ALARM PHEROMONES 2873

nest. Accordingly, it is not surprising that the older large workers are by far the most responsive worker subcaste to the soldier secretion in N. princeps.

The attractive action of the secretion of N. princeps soldiers can be repro- duced by a 1% solution of (+)-o~-pinene in hexane. During our tests, the work- ers' response was, however, less massive and subsided sooner than with natural secretion, although the amount of (+)-~-pinene presented in solution was com- parable to the average content of three soldier heads. This can be due either to a disturbing effect of the solvent or to the absence of the other components present in the natural secretion: diterpenes could be important in reducing the evaporation of the monoterpenes, and so maintain a suitable gradient for a longer period of time, whereas minor monoterpenes (limonene, a-thujene, sabinene, myrcene, c~-phellandrene, o~-terpinene, and terpinolene) might enhance the effect of ( + )-a-pinene synergistically.

In the present work, the pheromonal properties of (+)-a-pinene are clearly demonstrated in N. princeps: despite identical physical properties, it is more active than its enantiomer, which is almost absent from the soldier cephalic secretion. This is the first time that a differential reaction to both enantiomers of the same molecule has been demonstrated for an alarm/recruitment phero- mone in termites, although this was recently reported for alarm pheromones in ants (Cammaerts et al., 1985; Cammaerts and Moil, 1987), and for potential trail pheromone of some Nasutitermes: in N. costalis, Hall and Traniello (1985) tested the recruitment effects of racemic and chiral cembrene-A, a substance identified as the trail pheromone of N. exitiosus and which could possibly play the same role in some other termite species. Although the recorded responses were very low, the chiral compound was more active that the racemic one.

Acknowledgments--This study was supported by the Belgian F.N.R.S. (postdoctoral fellow- ship to Yves Roisin) and F.R.F.C. (grant 2.4513.90). King Leopold III Biological Station, Laing Island, Papua New Guinea, contribution no. 180.

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