Carbon Dioxide, a Releaser for Digging Behavior in Solenopsis Geminata (Hymenoptera: Formicidae)

Psyche: A Journal of Entomology, Sep 2018

The behavior of ants digging through sand or clay in the direction of trapped nestmates has been described by Belt (1874) and Lafleur (I940). Wilson (1958) showed that in Pogonomyrmex badius (Latreille) this behavior pattern is released by a volatile substance originating from the mandibular glands. Later, McGurk et al. (1966) identified the responsible compound as 4-methyl-3-heptanone. At the same time, Blum and Warter (1966) isolated 2-heptanone from Conomyrma pyramica (Roger) and described its function as the releaser of alarm and digging behavior. Spangler (1968) reported that not only whole workers, but also amputated parts as well as larvae and pupae of Pogonomyrmex occidentalis (Cresson) attract workers of this species and release digging behavior. Forrest (1963) studied Lasius flavus nearcticus and four species of Acanthomyops and found that workers also dig to free ants of another species but attack them as soon as they are released.

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Carbon Dioxide, a Releaser for Digging Behavior in Solenopsis Geminata (Hymenoptera: Formicidae)

International Journal of Soleno 0 0 Biological Labora.tories, Harvard University CARBON DIOXIDE, A RELEASER FOR DIGGING BEHAVIOR IN SOLENOPSIS GEMINATA (HYMENOPTERA: FORMICIDAE)* The behavior of ants digging through sand or clay in the direction of trapped nestmates has been described by Belt (1874) and Lafleur (94o). Wilson I958) showed that in Pogonomyrmex badius (Latreille) this behavior pattern is. released by a volatile substance originating rom the mandibular glands. Later, McGurk et al. (1966) identified the responsible, compound as 4-methyl-3-heptanone. At the same time, Blum and Warter (1966) isolated 2-heptanone rom Conomyrma pyramica (Roger) and described its function as the releaser of alarm and digging beha.vior. Spangler (I968) reported that not only whole workers, but also, amputated parts as well as larvae and pupae of Pogonomyrmex occidentalis (Cresson) attract workers of this species and release digging behavior. Forrest (I963) studied Lasius ]fayus nearcticus and four species of Acanthomyops and found that workers also dig to free ants of another species but attack them as soon as they are released. During studies on a colony of Solenopsis geminata (Fabricius), I noticed that returning foragers started to remove a plug of cotton moun.ting, even if the position of the entrance was rotated through used to block the .entrance of an articial nest immedia.tely after its 8o During most of these actions, they used their mandibles to chew away small pieces of the obstacle. The purpose of the present paper is to. report on the (inding that this behavior is released by the carbon dioxide produced by the ants trapped inside the nest. - stopper and blocked again by gluing a piece o an index card (Oxford, 7182 B) to it. The bottom o this stopper was perforated with a needle approximately 5o times, which allowed vola.tiles produced inside the vial to penetrate but at the same time prevented contact between the trapped ants and the cardboard. A capillary (i.d. mm) was efficient enough to supply the trapped ants with the necessary oxygen, and a layer o moist cotton guaranteed the essential humidity. The control bottle was prepared in the same way but contained only moist cotton. The test- and the control-tube were presented simultaneously on top of the nest and left there for 20-22 hours. Because the cardboa,rd covering the hole on top of the stopper was the only material the ants could remove in attempting to reach the trapped workers, all their digging activity was directed towards these areas. After each test, the pieces of cardboard were therefore removed and the "damage" done to them by the digging ants examined. The following scoring system was used to quantify the findings: o No visible chewing marks on the surface of the cardboard Superficial chewing marks 2 Heavy chewing marks 3 Only a transparent film of cardboard remains at the site of digging 4 The diameter of the hole dug is < mm 5 The diameter of the hole dug is > mm 6 The diameter’ of the hole dug is > 2 mm 7 The diameter of the hole dug is > 3 mm If the ants worked on more than one place, the different scores were added. Each test was repeated at least five times. RESt:LTS Fifteen to thirty minutes after the bottles were placed on top of the nest, some workers could be observed palpating the surface of the ca.rdboard-seal on the test-tube with their antennae. Others just rested on this place for a few minutes, their antennae slightly raised. Suddenly, a single ant started to work on the cardboard with its mandibles, rather hesitating at first, but gradually with more vigor. When one individual became involved in such activity, it soon was joined by at least another ant, and occasionally I noticed up to ten workers chewing at the same spot. The digging ants sometimes were replaced by other nestmates after various times, or they continued working until a hole was punctured. Very often, however, they abandoned this behavior before an opening was. created, leaving only chewing-marks of different intensities. Table I. Result of the digging behavior released by trapped workers, females, males or brood (larvae and pupae approx. :I). The mean activity is based o.n eight repetitions. Average digging Trapped individuals response Range 200 workers 5.6 5-6 I5 winged females 5.o 2-8 2o winged males 4.6 2-6 2oo larvae & pupae 4.6 2-6 Control o.4 o-3 The first experiment showed that the behavior pattern just described can be released by trapped workers, females, males, and even brood (Table I). The positive result obtained with brood indicates that the "rescue" activity can be initiated by something more than stridulation o the trapped individuals, the mechanism in leaf-cutting ants (Markl, 967). Stridulation can also be ruled out by trapping dead ants which have been killed by chilling just before the experiment. In series A, the dead workers were presented intact, whereas in series B, they were homogenized, transferred to a small piece of cotton and trapped in this way. In both cases the small pieces of cardboard were replaced after :o hours and the experiment stopped after 44 hours. Figure : shows that the homogenized ants release a stronger digging activity than the intact ones and that this activity increases with (dead ants intact) B (dead ants homogenized 44h ;:’Oh 44h :.’.>.’,;.:.’._.: ’) increasing decomposition time o the dead ants. There are at least 2 possible explanations to this phenomena: t. The chemical releaser for digging behavior is produced somewhere inside the ant’s body and, therefore, requires some time to diffuse to the surface of a dead worker to become active. This diffusion time is reduced if the workers are homogenized. 2. The responsible pheromone is a product o decomposition. Decomposition sta.rts slower in intact ants, because an uninjured integument represents a certain barrier or external factors which induce or accelerate the decomposition process. The rst explanation is weakened by the act that I did not succeed in localizing a gland responsible or the production o a pheromone. The second explanation, on the other hand, is slightly supported by the ollowing finding: In Solenopsis saevissima, products o decomposition accumulate in the body o dead workers no sooner than 24 hours (Wilson et al. x958). That is about the period during which I could not observe any digging behavior toward trapped geminata-corpses (see Fig. 2). Looking therefore or volatile products o decomposition that are also emitted by the living ants and brood, it seemed reasonable, to suspect a substance such as carbon dioxide. To obtain initial information about the value o this prediction, a small plastic container holding 0.5 ml of M NaOH was introduced into the spa.ce between top and bottom o the stopper (c. Fig. ). A second stopper was prepared in the same way, but the co.ntainer was filled only with o.5 ml distilled water. Each stopper was used to seal a vial containing 5o workers. A third bottle did not contain ants and its container was empty. Table 2 shows that the presence of NaOH- a powerful absorbent or CO2 actually influences the digging behavior negatively. It reduces the average digging response to almost the same low level as ound in the control. This result supports the CO2-hypothesis, but is not absolutely conelusive, because Sodium hydroxide could absorb other volatiles beside CO2. In an a.ttempt to get a more direct proof, I performed the following experiment: 5 bottles were prepared in the way shown in Figure except that they did not contain any ants. They we’re then connected with U-shaped pieces of glass tubing (i.d. 1.5; ram) as demonstrated on top of Figure 3. After the. whole system has been placed on a Wilson nest, a slow CO2-stream (3.5 cm3/min) was pressed into one end of the tubing. Due to loss of CO2 through the cardboard and perhaps tiny leaks in the stoppers, only traces of this gas, left the opening at the other end. I, thereby, got a more o,r less continuous gradient from a relatively high CO2-concentration (vial to a relatively low concentration (vial 5). Simultaneously I employed a second system of the same design, but compressed air was used instea.d of CO2 (control). In 2o hour-intervals, the. cardboard on each stopper was replaced by a new one. The results of five repetitions can be taken from Figure 3 (bottom). It is evident that a relatively low concentration of CO2 is able to release the same behavior pattern as do trapped workers. However, the efficiency of this releaser decreases with increasing concentration. It might be of interest to notice that ants which punctured the cardboard of vial 3 died .or were at least anesthetized after penetra.tion into. the interior of the stopper, whereas this effect could not 2 3 4 5 be observed in either vial 4 or 5. This means that only concentrations ot: carbon dioxide which are harmless 1:or these animals act as a highly efficient digging stimulus. No positive result could be registered in the control experiment, which indicates that pure air is completely inactive as a releaser o1: digging behavior. If the CO2 produced by trapped workers of 8olenopsis geminata is the only sub.stance responsible for the release of the described behavior, members of this species should also dig toward locked up ants of other species. I therefore trapped 5o workers of Solenopsis geminata, 5o workers of the closely related fire ant Solenopsis saevissima (Myrmicinae) and 3o,workers of Acanthomyops interjectus, belonging to a different subfamily (Formicinae). The control-vial was empty. The 4 tubes were presented to the geminata-colony simultaneously, and the results are shown in Table 3. All three species released digging behavior that is definitely above the control. The relatively small activity toward d canthomyops interjectus is probably due to the fact that A canthomyops species produce volatiles which have a strong repellant effect against members of other ant species (Regnier and Wilson, I968 and pers. commun.). DISCUSSION CO2 is well known to attract the blood-feeding sexes of haematophagou’s arthropods (Reeves, Wiesinger, Carcia, Fallis and Smith, Nelson, Wilson et al., Kato et al., De Foliart and Morris, Thompson, in Anderson and Olkowski, I968). Lacher (I964) found receptor cells on the antennae of workers and males of the honey bee which respond specifically to CO2. Lacher (I964) and Boeck et al. (I965) speculated that this CO.-response may serve the colony in controlling the concentration of carbon dioxide in the interior of the hive. Such a function, however, remains without proof. In the myrmecine ant Solenopsis saevissima, Wilson (I962b) demonstrated that carbon dioxide acts as a weak attractant that finally leads to settling. Because the same behavior could be observed during these studies on 8olenopsis geminata, I consider the digging activity released by CO2 as a by-product of attraction enabling the ants to get closer to the source of the stimulus. This interpretation is supported by the observation that if there is no hindrance between the workers and the source of CO2, the ants are merely attracted to. the. place where the concentration is most convenient; no digging behavior can be observed in such a case. The results presented in this paper offer a possible explanation to all the observations of digging behavior toward trapped ants as cited in the introduction. This of course does not mean that the same mechanism works in all ant species. The finding that single individuals of Pogonomyrmex badius or even parts of a worker release digging behavior (Spangler, 1968) indicates that this species is extremely sensitive to CO2, or it could also be that other chemical stimuli are involved. The whole surface of the ant’s body as well as larvae and pupae could be contaminated by 4-methyl-3-heptanone, the compound identified as releaser for alarm and digging behavior (McGurk et al., I966). Because CO2-concentrations up to 1-2% were demonstrated in the interior of ant nests (Poitier and Duval, 1929; Raffy, I929) , this simple molecule could accomplish the ollowing functions in a 8olenopsis geminata colony" I. It acts as a. pheromone to control settling inside the nest (Wilson, I962b). 2. It diffuses through the nest entrance and serves as an orientation aid, at least in the near vicinity o.f the nest. [Wilson (I962b) concluded that fire ant workers are able to move up CO2 gradients.] 3- It acts as a "rescue"-pheromone in case groups of ants are trapped following a major cave-in. 4. The CO2 produced by large piles of brood attracts the workers necessary to take care of the larvae and pupae. Although there may exist other or stronger stimuli which control these behavior patterns, CO2 at least plays an important supportive role. S U)MMARY Workers of Solenopsis geminata are attracted to low concentrations of CO and try to dig through all obstacles in order to get close enough to the source of this chemical stimulus. 2t.CKNOWLEDGEM ENTS Thanks are due to Dr. E. O. Wilson and Mr. J. M:. Reichson for their reading o. the manuscript. The author is also grateful to Miss N. K. Lind, who oered many useful suggestions. This work was supported by Grant No.. GB7734 of the U. S. National Science Foundation (Dr. E. O. Wilson sponsor) and a grant rom the Swiss National Science Foundation. LITERATURE CITED ANDERSON, J. R. AND W. OLKOWSKI 1968. Carbon dioxide as an attractant for host-seeking Cephenemfia females (Diptera: Oestridae). Nature 220: 190-191. BELT, T. 1874. The naturalist in Nicaragua. Murray, Lo.ndon, 403 pp. BLUM, M. S. AND S. L. WARTER 1955. Chemical releasers of social behavior. VII. The isolation of 2-heptanone rom Conomyrma pyramica (Hymenoptera" Formicidae: Dolichoderinae) and its modus operandi as a releaser of alarm and digging behavior. Ann. Ent. Soc. Amer. 59: 774-779. BOECKH, J., K. E. KAISSLING AND D. SCHNEIDER 1965. Insect olfactory receptors. Cold Spring Harbor Symposia on quantitative Biology 0" 26-280. FORREST, H. F. 193. Three problems in invertebrate behavior. II. The digging out o trapped or buried ants by other workers. Ph.D. Thesis, Rutgers, 91-219. RAFFY, A. 1929. 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Walter Hangartner. Carbon Dioxide, a Releaser for Digging Behavior in Solenopsis Geminata (Hymenoptera: Formicidae), Psyche: A Journal of Entomology, DOI: 10.1155/1969/58428