• Abstract and Figures
• Public Full-text

Proc. Nati. Acad. Sci. USA Vol. 78, No. 3, pp. 1976-1979, March 1981 Population Biology Enemy deterrence in the recruitment strategy of a termite: Soldier-organized foraging in Nasutitermes costalis (communication/ant predation/chemical ecology/defensive behavior/caste evolution) JAMES F. A. TRANIELLO* Department of Biology, Museum of Comparative Zoology Laboratories, Harvard University, Cambridge, Massachusetts 02138 Communicated by Edward 0. Wilson, December 15, 1980 ABSTRACT The nasute soldiers of the neotropical termite eight 45 x 60 cm glass foraging plates supported on oil traps. Nasutitermes costalis function as scouts by exploring new terrain Decayed birch was used as food, and large test tubes fitted with for food in advance of the worker caste and regulate foraging ac- tight cotton plugs provided moisture. The colony of N. costalis tivity by laying trails composed of sternal gland pheromone. Ad- ditional soldiers are at first recruited in large numbers, and sub- on which most observations and experiments were performed sequently workers appear as the pheromone concentration has thrived in the laboratory for 7 yr, continually expanding its increases. The role of the nasutes in the organization of foraging nest. is extremely unusual for the soldier caste in social insects and ap- In the laboratory, groups of soldiers of N. costalis periodically pears tobe a component of a foraging/defense system that controls emerge in "pseudopod" fashion from the nest or the termini of the recruitment of foragers and effectively deters attacks by ants, existing foraging trails and slowly extend and expand. When the most fierce and important predators of termites. offered a foraging arena with food, "pseudopods" of 100-200 soldiers slowly advance and explore the new area. After the food In both the higher and lower termites, the soldier caste is often is located, the investigative web of soldier trails coalesces into equipped with elaborate and bizarre armament for defensive one or two main routes and is immediately followed by the re- purposes. In some species the mandibles are enlarged and cruitment of additional soldiers and subsequently workers. highly sclerotized, whereas in others they are vestigial and the Typically 700-1000 soldiers arrive at the food and patrol the head capsule has become an ampule-shaped structure for dis- surrounding area during the next 30-45 min. The recruitment pensing defensive secretions (1-3). The extreme degree of de- of workers parallels the soldier pattern, but is delayed by ap- fensive specialization is reflected not only in morphological proximately 30 min and reaches a maximum 1.5 hr later (Fig. modifications but also in the impoverished behavioral reper- 1). This pattern was invariably observed in more than 50 ob- toire of the termite soldier and suggests a limited, exclusively servation periods. protective role in the organization of termite societies. How- The recruitment of soldiers and the initial stages of worker ever, in addition to their defensive functions, soldiers of Na- recruitment appear to be regulated entirely by the soldier caste. sutitermes costalis are responsible for discovering new food The following observations and experiments support this sources and communicating their location to workers. In this hypothesis. species the soldier caste is responsible for two social processes (i) Soldiers consistently explore new areas for food without that appear to be closely associated: the organization of foraging any worker accompaniment. When clean glass plates are con- and colony defense. nected to occupied areas by a wire-gauze bridge, soldiers in- The genus Nasutitermes is one of the most widespread and vestigate the new area and recruit additional soldiers in large ecologically significant genera of the higher termites (4). Non- numbers. After 50-60 soldiers explore the surface, a few work- reproductive castes are divided into (i) small and large workers rise dra- which tend brood, construct the nest, and forage (5, 6) and (ii) ers appear. While the number of soldiers continues to soldiers, or nasutes, which respond to defensive contingencies. matically, less than 5% of the total number of termites are work- When a soldier contacts an enemy, the mandibular muscles ers. In the absence of food, workers soon return to the occupied contract and project from the snout a sticky, irritating secretion area while soldiers continue exploratory behavior. Therefore, produced in the frontal gland (3, 7). Colonies of N. costalis are scouting parties are composed almost entirely of soldiers that arboreal, and foraging trails guide termites from the carton nest mass recruit to new areas. to decaying wood on the ground. Soon after foraging is in prog- (ii) After soldiers locate wood, workers are recruitedfollowing ress, workers cover the food source in a sheath of fecal material a 20- to 30-min delay. However, the delay in worker recruit- and debris; the foraging trail is protected by an arcade (semi- ment is not an intrinsic temporal characteristic of the recruit- circular in cross section) of similar composition (8). Although ment system. If soldiers are prevented from returning to the this prominent aspect of the biology of Nasutitermes has long nest after contacting wood, workers do not appear, although been reported in the literature (9-12), details of the mecha- other soldiers are continually recruited. Worker recruitment nisms involved in the organization of foraging have been can be delayed indefinitely in this way and can be induced at undescribed. any time by allowing soldiers that have contacted the food METHODS AND RESULTS source to return to the nest. Colonies of N. costalis and Nasutitermes corniger were reared (iii) Both stages of foraging behavior-soldier and worker in the laboratory in large plastic containers and given access to recruitment-can be experimentally induced with extracts of the sternal gland, the source of trail pheromone in termites (13). The publication costs ofthis article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertise- * Present address: Boston University, Department of Biology, 2 Cum- ment" in accordance with 18 U. S. C. §1734 solely to indicate this fact. mington Street, Boston, MA 02215. 1976 Downloaded by guest on September 27, 2021 Population Biology: Traniello Proc. Natl. Acad. Sci. USA 78 (1981) 1977 1000. protected and subject to predation, as during the early stages of foraging, when thousands of termites file in the open be- tween the nest and food source. It is possible that the early re- cruitment of a large soldier force provides an initial line of de- fense that deters ant predation by eliminating scouts that potentially could organize swift, massive raids. Predatory strat- egies of ants can be divided into three principal types: (i) fa- cultative predation by solitary foraging ants such as the ponerine species Pachycondyla and Odontomachus, (ii) organized attacks by species such as Solenopsis that are able to assemble a large worker force in a brief time period through mass recruitment, and (iii) predation by obligate termitophagous species [Pachy- condyla (= Termitopone) laevigata]. The effectiveness of nasute defensive tactics in coping with these types of predation was tested in the following manner. 100 In the first series of experiments, groups of 25 soldiers were placed in the foraging arenas ofvarious species ofponerine ants, and the results of 1:1 encounters between the ants and soldiers E were recorded. The results are presented in Table 1. Among the solitary foraging species, even the most efficient species Rhytidoponera metallica and Odontomachus bauri were successful in disabling and retrieving soldiers in only 18% 00 and 26% of encounters, respectively. The ability of 0. bauri workers to prey upon the nasutes might be attributed to their "strike and recoil" predatory behavior (21), which permits them to avoid the discharge of a soldier following contact. The spe- cialized termite predator P. laevigata never organized a raid after encountering nasutes, and most interactions resulted in avoidance or grooming. A particularly pugnacious ant, Solenopsis invicta, was used to simulate predation by a mass-recruiting species. In this series 1 2 3 4 5 6 7 of experiments, termite colonies were given access to a new Time, hr foraging plate (24 x 60 cm divided into 2 x 2 cm quadrats) on which was located a piece of birch. As soon as the nasutes ex- FIG. 1. Recruitment responses of soldiers and workers during for- plored the new area and began recruitment, a colony of S. in- aging organization. At time = 0, a fresh foraging plate with wood was connected to an occupied plate. Curves were fitted to the data by eye. victa was connected to the same plate with a 125-cm-long dowel O. Workers; *, soldiers. bridge. The plate was photographed at various time intervals to record the defensive behavior of the termites. The results are presented in Table 2. Solutions made from a single soldier sternal gland have a re- cruitment effect only on other soldiers. However, worker re- Table 1. Results of encounters between workers of various cruitment can be initiated by increasing the concentration of trails prepared from the sternal glands of soldiers. The results species of ponerine ants and termite soldiers of this procedure suggest that workers are recruited because Results of encounters, no.* of the cumulative effect of soldier-generated trails. The ex- Total perimental manipulation of pheromone concentration permits encounters, C the artificial induction of the typical pattern of foraging no. A B I II D organization. Species The soldiers, which are dependent on the workers for nu- Ectatomma trition, make the "decision" to begin foraging. As worker traffic tuberculatum 80 38 7 20 15 0 increases, the trail takes on its characteristic form and soldiers E. ruidum 114 46 26 16 26 0 flank the sides of the trail and the of the others Odontomachus bauri 81 23 25 6 6 21 periphery wood; O.

Load more

  4

Copy Link