Insectes Sociaux, Paris Masson, Paris, 1981 1981, Volume 28, n ~ 2, pp. 182-190

COMMUNAL SILK-SPINNING BY LARVAE OF DENDROMYRMEX TREE- ( : FORMICIDAE) Edward O. WILSON Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138, U.S.A. Rein le 24 septembre 1979. Accept6 le 30 novembre 1979.

SUMMARY

Dendromyrmex charti[ex and D. [abricii are weaver ants: the mature larvae of these formicine add silk to the arboreal carton nests. This material strengthens the layers of vegetable fibers, 'which form the bulk of the nests and are contributed by the ~vorkers. The communal siLk spinning is the most primitive yet discovered and may represent the first stage in the evolution of 'weaving. The larvae, rather than the workers that hold them in their mandibles, ma~ke the lateral vceaving movements, and their behavior differs from conventional cocoon spinning only in the orientation of the movements relative to the body. Moreover, larvae often contribute silk in this manner even when unattended by vcorkers. Both male and worker-destined larvae spin commu- nally; whether they contribute equal quantities per capita remains to be determined. Other information on the natural history of Dendromyrmex based on field and laboratory studies is reported: the colonies are polydomous; the workers forage nocturnally and accept a 'wide variety of prey. The workers of D. chartilex have unusual genal eyespots and behave in such a way as to resemble polybiine wasps, and it is suggested that they are in fact Batesian mimics of these stinging .

ZUSAMMENFASS UNG

Kommunales Seide-Spinnen (lurch Larven der Dendromyrmex Baumameisen

Dendromyrmex chartifex und D. fabricii sind Weberameisen : Die erwachsenen Larven dieser Formicinen-Arten fiigen den arborealen Kartonnestern Seide zu. Dieses Seide- material verst~irkt die aus pflanzlichen Teilchen bestehenden ~V~inde der Nestkammern, die yon Arbeitern gebaut werden. Das kommunale Seide-Spinnen yon Dendromyrmex ist die bis jetzt primitivste Form dieses Verhaltens und kfnnte die erste Stufe in der Evolution des Webens bei Ameisen darstellen. Nicht die Arbeiter, welche die Larven mit den Mandibeln halten, sondern die Larven machen die seitlich gerichteten Spinnbewegungen. Dieses Verhalten unterscheidet sich vom konventionellen Kokon-Spinnen nur in der Often- tierung der Bewegungen in Bezug zum K6rper. Oft produzieren sogar die Larven Seide zum SILK-SPINNING BY LARVAE OF DENDROMYRMEX 183

Nestbau, ohne dabei yon den Arbeitern gehalten zu ~erden. M~innchenlarven und Arbeiterlarven zeigen kommunales Spinnverhalten; ob beide die gleiche Menge Seide per Individuum produzieren muss noch festgestellt vgerden. Weitere Beobachtungen im Freiland und Laboratorium zur Biologic yon Dendro- myrmex xverden berichtet: Die Kolonien sind polydom; die Arbeiter furagieren nachts und nehmen eine Vielfalt von Insekten als Futterbeute an. Die Arbeiter yon D. chartilex haben auffallende Augenflecken und verhalten sich als ob sic Polybiinen-'Wcspen nachahmten. Es wird vermutet, dass es sich bier um eine Batessche Mimikry dieser stechenden Insektcn handelt.

INTRODUCTION

In several phyletic lines of the subfamily Formicina~ the larvae have evolved the habit of diverting silk from the production of their own cocoons to the construction of parts of the colony's nest. These "weaver ants " include both species of the Old World genus Ofcophylla (H/SLLDOBLER and WILSOn, 1977, 1978), many members of the ~videspread Old World genus Polyrhachis (KARAWAJEW, 1929 ; OVER, 1970), and Camponotus senex of Central and (FOREL, 1905; and personal observation). According to BARON1 URBAm (1978), silk is incorporated into the earthen nests of some Cuban species of the myrmicine subgenus Leptothorax (Macromischa), but this author is unsure .whether the material is obtained from larvae or from some other source such as spider webs. Since no other myrmicine is known to produce silk, the latter alternative seems more probable. (EcophylIa represents an extreme in communal silk spinning by larvae. The final-instar larvae never manufacture cocoons of their o'wn; all of the silk from their hypertrophied silk glands is donated to the construction of the elaborate silk-and-leaf envelopes that exclusively constitute the nests of these ants. The larvae are used like shuttles by the major 'workers. The ants grip them from above at the middle of their bodies and vceave them from side to side while repeatedly drumming them lightly on the )lead ,with the tips of their antennae. The larvae respond by arching their bodies into a shallow S-shape form and releasing threads of silk from the labial sericteries. Thus 'while the larvae produce the silk, the adult major vcorkers guide the silken threads and in effect control the design of the nest. The larvae of the advanced 'weaver ants therefore cooperate 'with the remainder of the colony by providing a specialized form of labor. They also donate part of the protein synthesized -,vithin their own bodies. They have in effect become a separate caste. It would be of substantial interest to trace the early stages in the evolutiorr of this remarkable speciaIization, and the analysis can perhaps be accomplished by a careful study of the various independently evolved but less advanced ,weaver ants. To this end, I have been able to establish that larvae of two species of the Neotropical 184 E. WILSON

tree-ant genus Dendromyrmex regularly contribute silk to the nest construc- tion, but in a simple, generalized manner that appears to be a very early stage in the evolution of communal silk spinning.

NATURAL HISTORY OF DENDROMYRMEX

Dend, omyrmex is a member of the tribe Camponotini characterized by monomorphism in the 'worker caste and a slight constriction of the occipital region into a neck-like form. According to EMERY (1925), its seven species are concentrated mostly in and northern South America, but at least two (chartifex, fabricii) range into Panama. WEBER (1944) reports that all three species he examined in the field (apicalis, chartifex, fabricii) in South and Central America form small colonies that construct oblong carton nests on the leaves of a variety of tree species in rain forest. All of the nests encountered by WEBER 'were at a height of 2-1/2 meters or less, but his observations ,were too limited to preclude their occurrence at higher levels in the forest canopy. Colonies are started by one or several queens, which build miniature carton nests in similar forest sites. Data gathered on D. chartifex and D. [abricii in Panama during the present study (see Acknowledgments) confirm these generalizations. They also show that the carton nests usually contain 30 adults or less. None of the Panama nests contained dealate queens. When the units 'were maintained in the laboratory, either no additional eggs were laid (chartifex) or else those laid -- by 'workers -- developed into males (fabricii). It is therefore apparent that the colonies encountered 'were polydomous, and the units collected were colony fragments. My laboratory studies of chartifex and fabricii have yielded other new facts. The workers are exclusively nocturnal; those of at least chartifex were also found to be nocturnal in the field in Panama (R. E. SILBERGLIED, personal communication). They readily accept sugar water, honey, and a wide variety of freshly cut insects, including Nauphceta cockroaches, tipulids, chironomid midges, mosquitoes, earwigs, and a variety of small moths, 'without apparent discrimination. Since the colony fragments thrived on this diet for a period of months, it is concluded that they are general insectivores and will collect honeydew if given the opportunity. No evidence was found of recruitment to food, even when the colonies were hungry and individual foragers had been excited by the discovery of food items too heavy to carry alone. The 'workers of D. chartifex are characterized by large paired yellowish spots on the genae (cheeks), 'which stand out conspicuously against the dark- brow pigment of the remainder of the body. When the colony is disturbed, many of the 'workers line up side by side along the edge of the nest entrance and face outward, 'while bobbing up and dawn. The visual effect in the SILK-SPINNING BY LARVAE OF DENDROMYRMEX 185 relatively weak lighting of the laboratory and forest is striking: to me the genal spots resemble eyes, and the ants resemble small polybiine wasps. I have considered the possibility that the ants are 'wasp mimics. SILBERGLIED (in litt., 5 August 1978) agrees, stating that in Panama " the most likely model would be a Protopolybia species, possibly pumila (?), that builds small, paper nests under leaves. These nests are quite flat and might be mistaken for a Dendromyrmex.,. The only trouble 'with the Protopolybia species I am thinking of is that it is extremely docile. Another possibility, Metapolybia, also builds small, flat nests; it too is docile." But these 'wasps may not be docile to the visually orienting predators that most endanger them, Dissection of nests of chartifex reveals that they contain substantial layers of silk, 'which are laid down both below and above the main carton layers of vegetable fibers. Some silk also appears to be mixed as a minor component ,with the'vegetable fibers. Additional sheets of silk, limited in extent, are extended over openings in the main carton; it is possible that they represent substrata on which additional layers of vegetable fibers are destined to be laid. By far the greatest bulk of the nests consists of vege- table fibers. The silk is a supporting element and also serves to give the carton walls greater strength, a fact that can be ascertained by making small tears through the 'wails at various positions. Laboratory observations quickly established that the silk is produced by the larvae, in behavior patterns that are primitive in comparison to the advanced (Ecophylla 'weaver ants. Because of the light that it might shed on the evolution of communal spinning, this behavior 'was selected for closer study.

MATERIALS AND METHODS

Five queenless colony fragments of D. chartifex, as well as one solitary colony- founding queen, and four queenless colony fragments of D. fabricii, together 'with an incipient queenright colony, ~vere collected on Barro Colorado Island and'the vicinity of Gamboa, Panama. Voucher specimens with exact locality data have been placed in the ant collection of the Museum of Comparative Zoology. After being transported to the insectary at Harvard University, the ants 'were housed in plastic containers 30 cm long, 24 cm wide, and 10 cm deep, the sides of which were coated with Fluon (Northeast Chemical Co., Inc., Woonsocket, Rhode Island, U.S.A.), a pawdery film ,which is effective in preventing ants from climbing vertical surfaces. The bottoms of the containers ,were covered ~vith solidified plaster of Paris, ,which 'was :kept moist thereafter in order to provide a high level of air humidity. The colony fragments ~vere allowed to move into test tubes (15 cm long ,with inner diameters of 22 ram) which ~were placed on the bottoms of the containers. These test tubes were half filled with veater ~which was trapped 'with tight cotton plugs. The workers foraged from these tubes and the remnants of their carton nests onto the floor of the containers. Observations were made veith a 10X hand lens and dissection microscope set to magnifications of up to 30X. Transmitted light from a microscope usually proved to be adequate to study details of motion of the larvae both inside and outside the cocoons. 286 E. WILSON

RESULTS

Dendromyrmex chartifex (F. smith) (fig. 1)

All tubes containing fully grown chartifex larvae were found to be lined with numerous silk threads within several days following their occupation and to have patches coated by translucent mats of silk after a period of two weeks or more. Subsequent observations revealed that the larvae contri-

Fig. 1. -- A nest of a colony fragment of the ' Dendromyrmex chartifex on Barro Colorado Island, Panama. The ants have constructed the nest by using silk-impregnated carton to close off a natural cavity formed by a fold in the large leaf. To the left a few strands of silk can be seen at the edge of a torn fragment of the carton. The genal spots can be seen on several of the ~vorkers ; these resemble large eyes when the ants stand in the darker recesses around the nest entrance. Photograph by John PICKERING.

Abb. 1. -- Das Nest eines Teiles einer Kolonie der Weberameise Dendromyrmex chartilex auf der Insel Barro Colorado, Panama. Eine natiirliche HiShle, die yon einem gefalteten Blatt gebildet ~vird, 'wurde yon den Ameisen mit Seide impr~i- gniertem Karton verschlossen. Die Augenflecken sind gut bei einigen der abgebildeten Arbeiterinnen zu sehen; sie gleichen grofien Augen, besonders ~venn die Ameisen im dunkleren Hintergrund nahe des Nesteinganges stehen. Photo: John PICKERING. SILK-SPINNING BY LARVAE OF DENDROMYRMEX 187 buting the silk were fully grown; most or all pupated within a week. A few simply transformed into naked pupae, vchile the remainder first spun cocoons that ranged from very thin -- so that the pupa could be seen inside with ordinary artificial light -- to moderately thick, the latter at least superficially similar to the ordinary cocoons of other formicine species. The larvae laid silk onto the floor of the nest tubes while swinging the head and forward third of the body in a side-to-side motion. Close compari- sons made between larvae communally spinning in this manner and those spinning cocoons revealed no differences in the motion except in the orienta- tion of the head-swinging movement. In many instances the communally spinning larvae were held by 'workers. Unlike comparable behavior in (Ecophylla, however, the relative positions of the larva arid worker varied greatly. Although the individual larva 'was invariably held somewhere within the central half of the body (from about 1/4 to 3/4 of the body length behind the head)'with the venter facing downward, the worker holding it sometimes pointed in the same direction as the larva and sometimes in the opposite direction. Furthermore, in the exact reverse of the pattern observed in (Ecophylla, the worker remained stationary while the larva performed all of the movements. Larvae held by workers appeared to arch their bodies in an S-shape similar to the posture of spinning (EcophyIla larvae, with the "neck " bent more than is the case in the resting position and the head aligned closer to the vertical, but the overall twist yeas xveaker than in (Ecophylla. Moreover, the workers did not antennate the larvae on the head in the stereotyped drum- ming pattern characteristic of (EcophyUa. They occasionally played their funi- cular tips over the bodies of the larvae, but the motions were the same as those observed in workers casually inspecting non-spinning larvae and other objects inside the nest. Of equal importance, larvae 'were frequently observed spinning silk onto the nest floor even when unattended. Their activity was indistinguish- able from that of larvae held by .workers, and they sometimes continued without interruption for ten minutes or longer. Although it cou.ld not be determined 'whether some stimulus from the workers is required to initiate communal spinning, it is clear that the larvae do not have to be continuously reinforced, as is the case in (EcophytIa. An effort was made to determine whether some division of labor occurs among the final-instar larvae, with some being distinctly more prone to donate silk. No evidence was obtained of such a phenomenon. All mature larvae observed for a period of several hours or longer contributed at least a smaU amount of silk to the nest floor, and all of the larvae transformed into healthy-appearing worker pupae regardless of the amount they donated. No differences were detected between larvae that spun cocoons (and hence might have donated less silk to the colony) and those that failed to spin cocoons. However, the possibility of some kind of anatomical or physiolo- 188 E. WILSON gical variation correlated with the amount of communal spinning has not been ruled out, and the hypothesis needs to be tested further. An interesting phenomenon of possible social significance is the slow growth of at least a fraction of the D. chartifex larvae. Many of the eggs and small larvae required six months to reach the prepupal stage, even though the colonies were kept at 28-38 ~ C. Because the brood was greatly mixed in age at the time of collection in Panama -- in most cases ranging from eggs or first-instar larvae to pupae -- each colony fragment usually had one or more larvae in the final instar, capable of communal spinning.

Dendromyrmex 1abricii (Roger) The laboratory observations on communal spinning in D. fabricii matched those of D. chartifex in detail. In addition, however, workers in one of the queenless fragments laid eggs and within eight months was producing mature males exclusively. I 'was thus able to determine whether male larvae also contribute silk to nest construction. To be completely certain I transferred the colony fragment to completely clean tubes after the last of the 'worker pupae had eclosed and the adults being produced were exclusively male. Within two weeks, silk strands appeared on the nest floor, and a month later dense mats of silk were present that 'were superficially indistinguishable from those produced simultaneously by worker-destined larvae in a queen- right colony. Although male larvae have thus been shown to contribute silk, the data were not adequate to test the hypotheses that they lay more or less silk than do worker-destined larvae.

DISCUSSION

In every detail communal silk spinning by larvae of Dendromyrmex char- tifex and D. fabricii fits 'what 'we would expect in a very early stage in the evolution of the behavior pattern : the larvae often spin on their awn ; even when held by workers they and not the 'workers perform all the movements ; their spinning movements are superficially indistinguishable from ordinary cocoon spinning except in orientation; the position of the 'workers holding larvae is highly variable ; the workers do not employ special tactile signals of the kind observed in (Ecophylla; the capacity to spin cocoons has been re- tained; and, finally, the silk is a lesser component of the carton nest than is the case in the species of (EcophyUa, Camponotus senex, and at least some Polyrhachis. It is reasonable to conclude that the evolutionary step taken by Dendro- myrmex has consisted of nothing more than altering the orientation of silk spinning in a facultative manner. Such a shift could be accomplished by a genetic change as elementary as the substitution of a single allele. It repre- SILK-SPINNING BY LARVAE OF DENDROMYRMEX 189 sents the earliest conceivable stage in the evolution of communal silk spin- ning. Yet the step is very significant in the sense that it represents the initia- tion of truly cooperative behavior on the part of the Dendromyrmex larvae ; it transforms the final larval instar into a functional caste (for a definition of caste, see OSTER and WILSON, 1978) and in so doing adds a wholly new material to the nest. The capacity to construct nests on the surfaces of live vegetation has been an important factor in the success of large arboreal or semiarboreal ants, 'which otherwise can find few nest sites sufficiently large and protected (WILSON, 1962; H.OLLDOBLER and WILSON, 1978). Kin selection theory (HAMILTON, 1964; TRIVERS and HARE, 1976) predicts that in the haplodiploid hymenopterous societies males should contribute less labor than females to the colony welfare. Ant larvae offer an exceptionally promising stage for the testing of the theory. Whereas it might be argued that the primitive aculeate males became so specialized for reproduction in Mesozoic times that they could then never be modified into a 'worker caste when social behavior was attained, this is not the case for the relatively undif- ferentiated larval stage. In (EcophytIa the theoretical prediction is upheld: male larvae contribute only about one-tenth as much silk to nest construction per capita as do worker-destined larvae (WILSON and HOLLDOBLER, 1980). It was therefore of considerable interest to learn whether a sexual difference also occurs in Dendromyrmex, whose communal spinning was evolved inde- pendently. The answer obtained in the present study is ambiguous: male larvae of D. fabricii contribute silk in substantial amounts, but the data are not adequate to examine the possibility that they donate more or less silk on a per capita basis. Additional studies are planned that 'will attempt to obtain the needed information.

ACKNOWLEDGMENTS. ~ I am grateful to Annette AIELLO, Robert E. SILBERGLIED, John WENZEL, and Joseph WRICHT for supplying the colonies of Dendrornyrmex used in this study, together with field notes on the natural history which are reported herein. The author's research is supported by Grant No. DEB77-27515 from the National Science Foundation.

References

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