the oldest known record of social insects

J. Paleont., 69(3), 1995, pp. 594-599 Copyright © 1995, The Paleontological Society OO22-3360/95/OO69-O594S03.0O

THE OLDEST KNOWN RECORD OF SOCIAL INSECTS XAVIER MARTINEZ-DELCLOS, AND JORDI MARTINELL Department of Geologia dinamica, Geofisica i Paleontologia, Faculty of Geology, University of Barcelona, 08071 Barcelona, Spain in the Lower Cretaceous Konservat-Lagerstatten of Montsec (Lleida Province, Spain) have yielded a wealth of soft-bodied and disarticulated invertebrate organisms. Among these are reproductive termite castes. Although termites have been recorded previously in this deposit (Lacasa and Martinez-Delclos, 1986; Martinez-Delclos, 1991a), in this note we report an exceptional worker specimen. This new specimen represents the earliest report of a social insect in the fossil record. In Cretaceous deposits other social insects and their traces have been found, including: ant castes (Wilson, 1987); wasp nests (Wenzel, 1990); wasps (Carpenter and Rasnitsyn, 1990); and bees (Michener and Grimaldi, 1988a, 1988b). Excavations carried out during the last 15 years in the Konservat-Lagertatten of the Lower Cretaceous lithographic limestones of the Montsec Ranges (Figure 1), Catalonia, Spain ("La Pedrera" and "La Cabrua" fossil-sites), have produced fossils of a large number of soft-bodied and disarticulated organisms (Martinez-Delclos, 1991b). These consist of, principally, arthropods, including crustaceans (Rabada, 1990), spiders (Selden, 1989, 1990), and insects (Martinez-Delclos, 1991c; MarPALEONTOLOGICAL EXCAVATIONS

tinez-Delclos and Ruiz de Loizaga, 1994) and terrestrial and aquatic plants, molluscs, and vertebrates (Martinez-Delclos, 1991a; Barale et al., 1994). These Lagerstatten are represented by 25-30 m of finely laminated limestones that were formed in deep anoxic lakes (Fregenal-Martinez et al., 1992). This stratigraphic sequence was deposited in tectonic grabens during the Early Cretaceous (Berriasian-Valanginian; 130-135 Myr BP), along the northern margin of the Ebro continent (Mercade, 1991). During the last seven years, many studies have been carried out on the biota of Montsec, with emphasis on the study of the taphonomic conservation processes of soft-bodied and easily disarticulated organisms (Martinez-Delclos and Martinell, 1993). Early in the course of these investigations, an important group of termite fossils was recognized among the Montsec collection at the Institut d'Estudis Ilerdencs in Lleida, Spain. This find was important because it represented the earliest record of the insect order Isoptera (Lacasa and Martinez-Delclos, 1986). These fossil termites were described and placed in a new species, Meiatermes bertrani Lacasa and Martinez-Delclos, within the extant family Hodotermitidae (Figure 2). This species is one of the few

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found in Mesozoic strata that preserves body characters (Lacasa and Martinez-Delclos, 1986; Schliiter, 1989; Krishna, 1990). All other Mesozoic termites are recognized solely on the basis of isolated wings (Martinez-Delclos, 1991a; Nel and Paicheler, 1993). The holotype and paratypes are housed in the Institut d'Estudis Ilerdencs in Lleida, Spain. This species also has been recognized in the fossil-site of Barremian age called "Las Hoyas," in Cuenca (Spain). This fossil represents the oldest record of a caste, rather than a sexually mature adult, and the first record of a termite worker caste for the Mesozoic Era. Soldier and worker individuals of termites have been found in Tertiary amber (Carpenter and Hermann, 1979). Wilson (1987) described worker castes of ants in both Cretaceous amber and compressions. Six species of Isoptera have been recorded from the Mesozoic: Cretatermes carpenteri from Cenomanian deposits of Canada (Emerson, 1967), Lutetiatermes prisca and aff. Mastotermes sarthensis from Cenomanian beds of France (Schliiter, 1989), Meiatermes araripena of Aptian age from Brazil (Krishna, 1990), Valditermes acutipenis from Hauterivian rocks of Mongolia (Ponomarenko, 1988), and Valditermes brenanae of Neocomian (Hauterivian) age from England (Jarzembowski, 1981, 1984). As presently known, all Mesozoic termites are from Cretaceous strata and all have been FIGURE /—Geographical location of lithographic limestones outcrops placed in the families Hodotermitidae (Poinar, 1992; Schliiter, from Montsec, in Spain. 1978, 1981; Schlee, 1972; Schlee and Dietrich, 1970; Zherikhin

FIGURE 2—Adult individual (LC-807-IEI), paratype of Meiatermes bertrani Lacasa and Martinez-Delclos, 1986. Photo by D. Serrette. Scale bar: 1 mm.

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FIGURE 4 — 1, head of Meiatermes bertrani Lacasa and Martinez-Delclos, paratype (imago), LC-1283-IEI. 2, head of termite worker (LP032-GDGP).

FIGURE 3 — Worker caste individual (LC-032-GDGP). Photo by J.M" Moraleja. Scale bar: 1 mm.

and Sukatsheva, 1973) and Mastotermitidae (Schliiter, 1989; Jarzembowski, 1991). Hong (1982) described Hebeitermes weichangensis, from the Lower Cretaceous of Gansu Province, in China, and placed it in the family Kalotermitidae. We consider this species, as Jarzembowski (1991) does, a possible Blattodea, not an Isoptera, because of the presence of Sc with five veins, R(?) with five or six veins, the radial field occupies almost half of the wingspan, and presence of the transverse vein r-m in the basal region. These structures from the radial and subcostal field are absent in Isoptera. Nel and Paicheler (1993) considered these species an Insecta order incertae sedis nov. stat. The oldest described occurrence of Cretaceous trace-fossil of a social termite originates from a termite nest found in the Upper Cretaceous of Texas (Rohr et al., 1986). Currently, an apterous individual, of the worker caste, is now documented herein, thus providing evidence for a termite caste never before found in the Mesozoic. This individual (LP-032-GDGP) (Figure 3) was discovered in the "La Pedrera" fossil site at Montsec and is housed in the Department of Geologia dinamica, Geofisica i Paleontologia of the University of Barcelona. This termite worker is 7.2 mm long and is exposed dorsally in a limestone slab. The head is tapered at the back and its length represents a quarter of the total body length. Neither

ocelli nor eyes are evident, possibly due to their reduced size or absence. There is a Y-shaped epicranial suture, robust asymmetrical mandibles, with the right one being wider than the left, and an almost straight epistomal suture. The left mandible has one conspicuous apical tooth and at least two marginal teeth. The head bears two postgenae, a labial postmentum, and a labrum that partially covers the mandible. The pronotal shield is narrower than the head. This character is derived with respect to the Mastotermitidae (the more primitive family of Isoptera), which possess a broader shield. The proximal parts of the forelegs and midlegs and one of the hindlegs are almost complete. The abdomen consists of half of the body length and it is composed of at least nine segments. The characteristics used for the recent classification of workers, such as general color, diminution or absence of eyes, antennal segment number, labrum form, and distribution of setae on the body, have not been preserved adequately enough to allow classification to a family. Among recent termites, the morphological similarity of the head and mandibles between the sexual winged adults and the workers, even within one family, varies considerably (Ahmad, 1950). The mandible of LP-032GDGP is of the chewing type and is very similar to those of Meiatermes winged individuals found at Montsec (Fig. 4.1). A major similarity is an apical tooth curved inwards, which is not a specialized mandibular character that a soldier caste would have. LP-032-GDGP has a very large head in proportion to the rest of the body, which suggests a soldier caste. However, the head measurements are quite similar to those adult individuals found in the same Konservat-Lagerstatten (Figure 5.1, 5.2). It has been assigned to the worker caste because of an absence of eyes, and minimal mandible development which resembles a sexual winged adult (Figure 4.2). The remainder of the body lacks information for classification at a family level. Unfortunately, the presence in the Montsec outcrops of the worker and adult termite {Meiatermes bertrani, Hodotermitidae) does not resolve any of the phylogenetic hypotheses recently proposed for the Isoptera (DeSalle et al., 1992; Nalepa, 1991; Thorne and Carpenter, 1992). Occurrence of Mesozoic termites are very sparse and they do not resolve hypotheses of termite phylogeny.

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FIGURE 5—7, adult individual (LC-807-IEI). 2, termite worker (LP-032-GDGP). Compare both the large head of a termite worker and of the imago, in relation to the rest of the body. Scale bar: 1 mm.

Recent termite phylogeny is mainly based on the type of gut endosymbionts, which are flagellates in the case of Hodotermitidae (Wilson, 1971), and DNA sequences (DeSalle et al., 1992; Nalepa, 1991). Meiatermes bertrani indicates the existence of Hodotermitidae during the Berriasian, where it appears with pronounced derived characters with respect to the individuals of family Mastotermitidae (DeSalle et al., 1992; Thorne and Carpenter, 1992). The derived state of characters are the following: an angular basal suture of the wing, small wing scales, absence of a simple R2 vein, absence of ocelli, an unexpanded pronotum and perhaps hind wings without an anal lobe. The corresponding states of characters are symplesiomorphic in the Mastotermitidae and Valditermes brenanae, which is considered as a Hodotermitidae by Jarzembowski (1991) or a Mastotermitidae by Krishna (1990). The Hodotermitidae has no clear autapomorphies; all specializations of Hodotermitidae can be observed in the other families of termites. On the contrary, Mastotermitidae has two clear autapomorphies with respect to the other families of the Isoptera: 1) the spermatozoa of Recent Mastotermitidae is unique in the animal kingdom in that it has 98-100 flagella and 2) the ootecae structure (Grasse, 1986). Until recently there have not been cladistic studies of the various families of termites. Neither recent nor fossil genera have been examined, but some phylogenies have been determined between Isoptera and other insect orders, particularly the Blattodea and Mantodea. If it is acknowledged that Isoptera is

not the sister-group of Blattodea, as some currently propose, then these insects may have evolved separately from a common, more recent ancestry (DeSalle et al., 1992; Thorne and Carpenter, 1992). Consequently, it is unnecessary to look for the origin of the termites during the Carboniferous, when cockroaches are first recorded. Nalepa's (1991) phylogenetic analysis posits the origin of termites during the Late Carboniferous, since, for this author, Isoptera is the sister-group of Blattodea. Although this hypothesis is not proved because fossil termites are absent from deposits earlier than the Lower Cretaceous, the phylogeny of the dictyopteran complex (monophyletic grouping, including Blattodea, Isoptera, and Mantodea) proposed by Thorne and Carpenter (1992), on the basis of a high number of characters, seems the most accurate. A worthwhile approach to the first hypothesis is that of gap analysis (Marshall, 1991). This analysis establishes, using probability statistics, confidence intervals around the likely time of origin of a taxon, given its density and distribution of occurrence in the fossil record. If termites did originate during the Late Carboniferous, what would the likelihood be that one would encounter at least some fossil occurrences before the Cretaceous? Given the sudden occurrence of at least 15 termite-bearing amber and compression deposits during the Cretaceous and none before, then the origin of the termites is more likely to be during the Jurassic rather than earlier. This evidence supports neither Nalepa's nor Thorne and Carpenter's (1992) phylogenies.

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It may be that the origin of the order Isoptera occurred during the Triassic (Carpenter and Burnham, 1985), and subsequently they became widely distributed, quickly occupying a unique, wood-associated niche with no competitors. The fact that Recent Porotermes, confamilial with Meiatermes, has been found forming colonies in Australia, South Africa, and South America indicates that termite sociality evolved prior to the breakup of Pangaea. Because fossil termites are almost exclusively from waterdeposited sediments or amber, the record is highly selective. It is also possible that the Isoptera appeared before the Jurassic as soil inhabitants of environments where its preservation is extremely unlikely such as forest or savanna. Accordingly, it may have been during the Early Cretaceous when they conquered environments where their preservation allowed for entry into the fossil record. The humid margins of lakes, for example, would be such an environment. Recent evidence from molecular biology indicates that most molecular clocks, as determined by DNA sequence data, tend to have variances in rate (Skelton, 1993). This variability in rate presents difficulties in assessing the time of origin of major clades. The fossil record does not support any particular date for the origin of termites or any particular proposed phylogenetic hypothesis. Presently, the time of appearance of termites is unknown, necessitating further exploration of Triassic and Jurassic strata. ACKNOWLEDGMENTS

Review and helpful criticisms of the manuscript were given by C. C. Labandeira (National Museum Natural History, Washington, D.C.) and A. Nel (Muséum National d'Histoire Naturelle, Paris), as well as P. A. Selden (University of Manchester) and J. L. Sanz (Universidad Autónoma de Madrid). We would like to thank J. M" Moraleja (Museu Geologic del Seminan, Barcelona) and D. Serrette (Muséum National d'Histoire Naturelle, Paris), who took the photographs. This study has been partially funded by the CEE Project CHRX-CT93-0164 and the Public Fundation Institut d'Estudis Ilerdencs. REFERENCES

AHMAD, M. 1950. The phylogeny of termite genera based on imagoworker mandibles. Bulletin of the American Museum of Natural History, 95:41-86. BARALE, G., J. MARTINELL, X. MARTÎNEZ-DELCLOS, F. POYATO-ARIZA,

AND S. WENZ. 1994. Les gisements de calcaires lithographiques du Crétacé inférieur du Montsec (province de Lérida, Espagne): apports récents à la paléobiologie. Geobios Mémoire spéciale, 16:177-184. CARPENTER, F. M., AND L. BURNHAM. 1985. The geological record of

insects. Annual Review Earth Planetary Science, 13:297-314. , AND H. R. HERMANN. 1979. Antiquity of sociality in insects, p. 81-89. In H. R. Hermann (éd.), Social Insects. Academic Press, New York. , AND A. P. RASNITSYN. 1990. Mesozoic Vespidae. Psyche, 97:1— 10. DESALLE, R., JF. GATESY, W. WHEELER, AND D. GRIMALDI.

1992.

DNA

sequences from a fossil termite in Oligo-Miocene amber and their phylogenetic implications. Science, 257:1933-1936. EMERSON, A. E. 1967. Cretaceous insects from Labrador 3. A new genus and species of termite (Isoptera: Hodotermitidae). Psyche, 74: 276-289. FREGENAL-MARTÎNEZ, M., N. MELÉNDEZ, X. MARTÎNEZ-DELCLOS, AND

M. J. RUIZ DE LoizAGA. 1992. Lower Cretaceous lake deposits from la Serra del Montsec. La Cabrua fossil site, Pyrenees. Mid-Congress Excursions. XXV Society International Limnology Congress, Barcelona, 12:1-10. GRASSE, P. P. 1986. Termitologia, volume 3. Anatomie-PhysiologieBiologie-Systématiques des Termites, Masson Ed., Paris, 715 p. HONG, Y. C. 1982. Mesozoic Fossil Insects of Jiuquan Basin in Gansu

Province. Bejing, Geological Publishing House, 223 p. [in Chinese with English summary]. JARZEMBOWSI, E. A. 1981. An early Cretaceous termite from southern England (Isoptera: Hodotermitidae). Systematic Entomology, 6:9196. . 1984. Early Cretaceous insects from southern England. Modern Geology, 9:71-93. . 1991. New insects from the Weald Clay of the Weald. Proceedings of the Geological Association, 102:93-108. KRISHNA, K. 1990. Isoptera, p. 76-81. InD. A. Grimaldi (éd.), Insects from the Santana Formation, Lower Cretaceous, of Brazil. Bulletin of the American Museum of Natural History, 195. LACASA, A., AND X. MARTÎNEZ-DELCLOS. 1986. Meiatermes, nuevo

género fósil de insecto isóptero (Hodotermitidae) de las calizas neocomienses del Montsec (Lérida, España). Institut d'Estudis Ilerdencs, Lleida, Spain, 65 p. MARSHALL, C. R. 1991. Estimation of taxonomie ranges from the fossil record, p. 19-37. In N. L. Gilinsky and P. W. Signor (eds.), Analytical Paleobiology. Short Courses in Paleontology, Number 4, The Paleontological Society. MARTINEZ-DELCLÔS, X. 1991a. Insectes hemimetàbols del Cretaci inferior d'Espanya. Tafonomia i Paleoautoecologia. Unpubl. Ph.D. thesis, University of Barcelona, 789 p. (coord.). 1991b. The Lower Cretaceous Lithographic Limestones of Montsec. Ten Years of Paleontological Expeditions. Institut d'Estudis Ilerdencs, Lleida, Spain, 106 p. . 1991c. Lower Cretaceous insects from Spain. Contributions from the Paleontological Museum, University of Oslo, 364:47-^*8. , AND J. MARTINELL. 1993. Insect taphonomy experiments. Their application to the Cretaceous outcrops of lithographic limestones from Spain. Kaupia, Darmstádter Beitrage zur Naturgeschichte, 2:133-144. , AND M. J. Ruiz DE LOIZAGA. 1994. Les insectes des calcaires lithographiques du Crétacé inférieur d'Espagne. Faune et Taphonomie. Geobios Mémoire spéciale, 16:195-201. MERCADÉ, L. 1991. Sedimentology of the Lower Cretaceous lithographic limestones from the serra del Montsec (Spain), p. 25-31. In X. Martînez-Delclos (coord.), The Lower Cretaceous Lithographic Limestones of Montsec. Ten years of paleontological expeditions. Institut d'Estudis Ilerdencs, Lleida. MICHENER, C. D., AND D. A. GRIMALDI. 1988a. A Trígona from Late Cretaceous amber of New Jersey (Hymenoptera: Apidae: Melponinae). American Museum Novitates, 2917:1-10. , AND . 1988b. The oldest fossil bee: apoid coevolutionary stasis, and the antiquity of social behavior. Proceedings of the National Academy of Sciences USA, 85:6424-6426. NALEPA, C. A. 1991. Ancestral transfer of symbionts between cockroaches and termites: an unlikely scenario. Proceedings of the Royal Society of London, (B), 246:185-189. NEL, A., AND J. C. PAICHELER. 1993. Les Isoptera Fossiles. État actuel des connaissances, implications paléoécologiques et paléoclimatologiques. (Insecta Dictyoptera). Cahiers de Paléontologie, 103-179. POINAR, G. O. 1992. Life in Amber. Stanford University Press, Stanford, California, 350 p. PONOMARENKO, A. G. 1988. Isoptera, p. 71-72. In L. P. Tatarinov (éd.), New species of fossil invertebrates of Mongolia. The Joint Soviet-Mongol Expedition Transactions, 33 [in Russian]. RABADÀ, D. 1990. Crustáceos decápodos de las Hoyas (Cuenca) y del Montsec de Rúbies (Lleida). Calizas litográficas del Cretácico inferior de España. Acta Geológica Hispánica, 25:299-311. ROHR, D. M., A. J. BOUCOT, J. MILLER, AND M. ABBOTT. 1986. Oldest

termite nest from the Upper Cretaceous of West Texas. Geology, 14: 87-88. SCHLEE, D. 1972. Bernstein aus dem Libanon. Kosmos, 68:460-463. , AND H. G. DIETRICH. 1970. Insektenführender Bersteinaus der Unterkreide des Libanon. Neues Jahrbuch für Geologie und Paláontologie Monatshefte:40-50. SCHLÜTER, T. 1978. Zur Systematik und Palökologie harzkonservierter Arthropoda einer Taphozönose aus dem Cenomanium von NWFrankreich. Berliner Geowissenschaft Abhandlungen, 150 p. . 1981. Fossile Insekten aus dem Jura/Kreide-Grenzbereich Sodwest-Agyptens. Berliner Geowissenschaft Abhandlungen, 32:33-61. . 1989. Neue Daten über harzkonservierte Arthropoden aus dem Cenomanium NW-Frankreichs. Documenta naturae, 58:59-70.

PALEONTOLOGICAL NOTES SELDEN, P. 1989. Orb-web weaving spiders in the early Cretaceous. Nature, 340:711-713. . 1990. Lower Cretaceous spiders from the Sierra del Montsech, north-east Spain. Palaeontology, 33:257-285. SKELTON, P. (éd.). 1993. Evolution. A biological and Palaeontological Approach. Addison-Wesley Publications Co., in association with Open University, Avon. THORNE, B. L., AND J. M. CARPENTER.

1992.

Phylogeny of the Dic-

tyoptera. Systematic Entomology, 17:253-268. WENZEL, J. W. 1990. A social wasp's nest from the Cretaceous Period, Utah, USA, and its biogeographical importance. Psyche, 97:21-29.

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WILSON, E. W. 1971. The Insect Societies. Harvard University Press, Cambridge, Massachusetts, 548 p. . 1987. The earliest known ants: an analysis of the Cretaceous species and an inference concerning their social organization. Paleobiology, 13:44-53. ZHERIKHIN, V. V., AND I. D. SUKATSHEVA. 1973. On Cretaceous insect-

bearing "amber" (retinite) from northern Siberia, 24th Annual Report on Lectures in Memory of N. A. Kolodovsky (April, 1971), 24:3-48, Leningrad: Nauka [in Russian].

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