RESEARCH NOTES 1073 corners (Pig. 1A, B), (4) reduced adhesion pads only in the oral area (Fig. 1B), (5) a pair of lamelliform fourth legs (Fig. 1B), and (6) a 2segmented abdomen (Fig. 1B). We found 14 females and 4 males ofD. ferox. The average body length (in mm) for the female is 33.7 (25.940.3) and for the male, 22.5 (21.2-24.0). Six females and 2 males (NMMBCPC 00001) of D. ferox in our collection have been deposited in the collecüon of the National Museum of Marine Biology and Aquarium located in Checheng, Pingtung, Taiwan. This finding is significant for 2 reasons. First, it extends the distribution of D. ferox from the high-laütude waters of the North Atlantic to the subtropical waters of the western North Pacific, and second, it documents a new host record. This documentation also substantiates that D. ferox is host specific to benthopelagic sharks. We have examined so far 27 Pacific sleeper sharks caught off the east coast of Taiwan from 19 March to 18 May 2002. The copepod parasites found were 0. elongata on the eyes and D. ferox on the head or fins (or both). The prevalence of copepod was high, 29.63% of sharks carrying 0. elongata and another 14.81% carrying D. ferox. The inten- sity of infection for the former was 1.63 (1-2) and for the latter, 4.50 (1-9). It is interesting to note that the 2 species of copepod parasites were not found on the same host (individual) captured off Taiwan. This makes one wonder whether this apparent mutual exclusion is the reason why Benz et ai. (1998) did not find D. ferox on the Pacific sleeper sharks captured m Prince William Sound, Alaska, because 8 sharks that fhey examined were all infected with 0. elongata. Furthermore, G. W. Benz (pers. comm.) did not see D. ferox on Greenland sharks examined in the eastern Canadian Arctic that were infected with 0. elongata on the eyes. We thank the processors of the sleeper sharks in Hualien, Taiwan, Mr. and Mrs. R.-S. Chen and their employees, for allowing us to collect the copepod parasites from their specimens and G. W. Benz for providing us unpubüshed information and valuable comments on the manuscript. Completion of this study was partly funded by a grant from the Paramitas Foundation to J.S.H. LITERATURE CITED BENZ, G. W., Z. LUCAS, AND L. F. LOWRY. 1998. New host and ocean records for the copepod Ommatokoita elongata (Siphonostomato- ida: Lernaeopodidae), a parasite of the eyes of sleeper sharks. Journal of Parasitology 84: 1271-1274. BURMEISTER, H. 1833. Beschreibung einiger neuen oder weniger be- kannten Schmarotzerkrebse, nebst allgemeinen Betrachtungen über die Gruppe, welcher sie angehören. Acta Verhandlungen der Leopoldinisch-Carolinischen Akademie der Naturforscher 17: 269336. CRESSEY, R. F. 1967. Revision of the family Pandaridae (Copepoda: Caligoida). Proceedings of the United States National Museum 121: 1-133. HANSEN, H. J. 1923. Cmstacea Copepoda II. Copepoda parasita and hemiparasita. Danish Ingolf-Expedition 3: 1-92. HEWITT, G. C. 1967. Some New Zealand parasitic Copepoda of the family Pandaridae. New Zealand Journal of Marine and Freshwater Research l: 180-264. KR0YER, H. 1838. Om snyltekrebsene, isaer med Hensyn til den Danske fauna. Naturhistorisk Tidsskrift 2: 8-52. LATREILLE, P. A. 1829. Crustaces, Arachnides et partie des Insectes. In Le regne animal, 2nd ed., Vol. IV, G. Cuvier (ed.). Deterville et Crochard, Paris, France, p. 1-584. MIERS, E. J. 1881. On a small collecüon of Cmstacea made by Edward Whymper, Esq., chiefly in the N. Greenland Seas. Journal of the Linnean Society 15: 59-73. STEPHENSON, K. H. 1940. Parasitic and semiparasitic Copepoda. Zool- ogy of Iceland 3: 1-24. THOMSON, G. M. 1889. Parasitic Copepoda of New Zealand. Transac- tions of the New Zealand Institute 22: 353-376. WANG, J. Y., AND S. C. YANG. 2003. First records of Pacific sleeper sharks {Somniosus pacificus Bigelow and Schroeder, 1944) in the sub-tropical waters of eastern Taiwan. Bulletin of Marine Science. [In PressJ . 'WILSON, C. B. 1907. North America parasitic copepods belonging to the family Caligidae, 3 and 4: Revision of the Pandarinae and the Cecropinae. Proceedings of the United States National Museum 33: 323-490. -. 1920. Report on the parasitic Copepoda collected during the Canadian Arctic Expedition, 1913-18. Report of the Canadian Arctic Expedition, 1913-1918 7(L): 3-16. YAMAGUTI, S. 1963. Pamsitic Copepoda and Branchiura of fishes. Interscience Publisher, New York, 1,104 p. J. Parasitol., 89(5), 2003, pp. 1073-1076 © American Society of Parasitologists 2003 Dioctophymidae Eggs in Coprolites From Neolithic Site of Arbon-Bleiche 3 (Switzerland) M. Le Bailly, U. Leuzinger*, and F. Bauchet, Laboratoire de Paleoparasitologie, EA 3308, associö CNRS ESA 8045, Universitö de Reims, UFR de Pharmacie, 51, rue Cognacq-Jay, 51 096 Reims Cedex, France. *Amt für Archäologie des Kantons Thurgau, Schlossmühlestrasse 15 A, CH 8510 Frauenfeld, Suisse. e-mail: matthieu.lebailly@univ-reims.fr ABSTRACT: Dioctophymidae eggs were found in human coprolites dated from 3,384 to 3,370 BC from the site Arbon-Bleiche 3, Switzeriand. This is the first record of dioctophymiasis in archaeological material. The important percentage of this disease in the studied coprolites raises the question of a higher prevalence during the Neolithic than at present. sponds to the period of transition between the Pfyn and Horgen cultures (Leuzinger, 2000). The level of occupation, 5-40 cm thick, is covered with a layer of sandy sediment. This detrital layer, deposited after a significant mcrease in the level of the lake around 3,350 BC allowed the conservation of the archaeological deposits by creating an anaerobic environment. The data on parasitic disease during the Neolithic are not numerous and are limited to some studies äs the mummy of the ice Ötzie (Aspöck et ai., 1995, 1996) or the site of Chalain in France (Bouchet et ai., 1995; Bauchet, 1997; Dommelier et ai., 1998). This work aims at completing the Information already collected for this period and reports a new parasite from the Neolithic. The prehistoric site Arbon-Bleiche 3 is located in Switzerland (Fig. l), on the bank of the Constance Lake (Bodensee), in a bay between the current municipalities of Arbon (Canton of Thurgovie) and of Steinach (Canton of Saint Gall). It is an ancient lakeside settlement, the occupation of which, äs determined by dendrochronology, spreads during a very short period of 15 yr, from 3,384 to 3,370 BC, and corre- Eighteen coprolites (Pig. 2) taken from the level of occupation were studied. The anthropoid origin of the material is confirmed by the archaeological data and the microscopical analysis of the samples. The identity of the parasites found there, such äs Tcenia sp. (34 |jLm), Diphyllobothrium sp. (53 X 40 (JLITI), Fasciola sp. (132 X 76 (Jim), and the absence of splinters ofbone in the coprolites support this hypothesis, although no pinworm egg {Enterobius vermicularis) was discovered (Hörne, 2002) to confirm it. Each sample was placed for rehydration into a 0.5% trisodic phosphate solution added to 5% glycerinated water for 10 days. The samples were then crushed in a mortar and treated with ultrasound for 3 min at 50 C. The samples were finally filtered in a column of 4 calibrated This content downloaded from 131.152.38.90 on Mon, 26 Apr 2021 15:06:40 UTC^ All use subject to https://about.jstor.org/terms 1074 THE JOURNAL OF PARASITOLOGY, VOL. 89, NO, 5, OCTOBER 2003 ^_ T SWITZERLAND Konstanz Friedrichshafen ^ <^^ Lindau /06> Arbon Bleiche 3 0 10 20 30 km Bregenz Rorschach of this parasite (Georgi, 1980; Measures and Anderson, 1985; Smyth, 1994). Even if Dioctophyma was identified for the first time in a dog, his localization in the peritoneal cavity would suggest that it is not a natural definitive host of the parasite (Mehlhorn, 2001). The life cycle of the Dioctophyme begins when the nonembryonated eggs are expelled from the host with urine. They must gain access to water for further development to take place. The eggs are then ingested by an intermediary host, freshwater oligochaetes {Lumbriculus variegatus) (Karmanova, 1960). The cycle can then continue by a second host, a fish of the Cyprinidae or the Siluridae families, a frag of Rana genus, or directly by the definitive host. However, these various possibilities of transmission lead to the contagion of a mammal, definitive host of this Helminth (Dyer, 1998), by ichtyophagy or by baü-acophagy. The larvae, once released into the intestines, cross the intestinal wall actively and migrate either directly toward kidneys, or through the li ver or other organs (Euzeby, 1963; Kaufmann, 1996). These varied locations could explain the presence of these eggs in the coprolites studied. But the finding of these eggs in coprolites is not surprising because urination and evacuation of intestines take place physiologically at the same time. FIGURE l. Location of Arbon-Bleiche 3, Thurgovie, Switzerland (Leuzinger, 2000). sieves, with mesh sizes of 315, 160, 50, and 25 [jum (Bauchet et ai., 2001). The sediments from the 50- and 25-ijum sieves was used for the analysis by light microscopy. The samples are studied at the rate of 20 slides by taking. In 6 samples, ovoid eggs, in thick pod presenting many polygonal depressions, with 2 polar corks, and a rough size of 73 X 43 [jLm were detected (Woodhead, 1950; Rangueloff Simeonoff, 1961; Neva and Brown, 1994) (Fig. 3). These eggs belong to the Dioctophymidae and, more particularly, to the genera Dioctophyma or Eustrongylus Goeze, 1782 (Brumpt, 1949). The female of this worm can measure up to l m in length, lodges in the kidneys of its definitive host, sclerifies it totally, making them nonfunctional (Narvaez et ai., 1994). The disease produces a number of Symptoms including hematury (Femando, 1983). Canidae, Felidae, numerous Mustelidae, and humans are the potential hosts The lakeside environment of the Arbon habitat and the composition of the paleofauna inventoried on the site, tend to confirm the presence of this parasitic disease. The consumption of many fishes (Cyprinidae, Siluridae, Salmonidae) has been shown by archaeozoologists (De Capitani et ai., 2002). It represents approximately 22% of inhabitants' overall nutrition (Hüster-Plogmann and Leuzinger, 1995). In the same way, the presence and the consumption of frogs (about 20%), especially Rana temporaria, is attested by the zoological analysis (H. Hüster-Plogmann, pers. comm.). Finally, the occurrence and the use of the Mustelidae (Meles meles, Maries martes, Mustela putorius), for für or eating, have also been proved by the archaeozoological studies made on the site (De Capitani et ai., 2002). It is ver y likely that the proximity of these animals and men favored the development of this anthropozoonosis within the Arbon community. If the man-parasite contact and the incidence of the parasitic disease were highly prevalent in the Neolithic when man settled down, data collected here, äs in Chalain (Bouchet, 1997), tend to suggest that parasitoses considered rare nowadays may have been widespread at same '«51? 'y%^ t£^ ?.^ FIGURE 2. Coprolites from Arbon-Bleiche 3. 0 23 mm. This content downloaded from 131.152.38.90 onMon, 26 Apr 2021 15:06:40 UTC All use subject to https://about.jstor.org/terms RESEARCH NOTES 1075 <f {\M .*^ iSK^/' €^ •^MiKS ^SSiF (H1 '^si ^Utai y^t-':^ ^B^ 0 5 |im FIGURE 3. Egg of Dioctophymidae 73 X 43 |jLm (X 1,000) from the neolithic site of Arbon-Bleiche 3 (Switzerland). periods in prehistory. The presence of this parasite in 30% of the coprolites studied at this Neolithic site leads us to conclude that this disease BRUMFT, E. 1949. Precis de Parasitologie, tome I, Editions Masson 6th edition, Paris, France, 1,042 p. was not äs anecdotal äs it is in our time. DE CAPITANI, A., S. DESCHLER-ERB, U. LEUZINGER, E. MARTI-GRÄDEL, Except in Africa and Australia, where it is totally absent, dioctophymiasis is present worldwide (Nozais et ai., 1996). At present, it is rare in Europe. Indeed, only a dozen cases have been documented since the 1970s (Acha and Szyfres, 1989). It is especially abundant in North America. This study provides some information on the historical geography of the parasite. The authors thank their colleague S. Harter and an anonymous reviewer for the sound advice for this article. This work was supported by the Department of Archaeology of Frauenfeld, Switzeriand, and the French Ministry of Research. LITERATURE CITED ACHA, P. N., AND B. SZYFRES. 1989. Zoonoses et maladies transmissibles communes ä l'homme et aux animaux. Office Internationale des Epizooties, Paris, France, 1,065 p. ANONYMOUS. 2002. The giant kidney worm. Seminars in Dialysis 15: 120. ASPÖCK, H., H. AUER, AND 0. PICHER. 1995. The mummy from the Hauslabjoch: A medical parasitology perspective. Alpe Adria Microbiology Journal 2: 105-114. -, AND —. 1996. Trichuris trichiura eggs in the neolithic glacier-mummy from the Alps. Parasitology Today 12: 255-256. BOUCHET, F. 1997. Intestinal capillariasis in neolithic inhabitants ofChalain (Jura, France). The Lancet 349: 256. -, P. PETREQUIN, J. C. PAICHELER, AND S. DOMMELIER. 1995. Pre- miere approche paleoparasitologique du site neolithique de Chalain (Jura, France). Bulletin de la Societe de Pathologie Exotique 88: 265-268. BOUCHET, F., D. WEST, D. CORBETT, AND C. LEFEVRE. 2001. Palaeopar- asitological analysis of a child burial from Adak Island, Central Aleutian Islands. Compte Rendu de l'Academie des Sciences (ser III) 324: 123-127. AND J. SCHIBLER. 2002. Die jungsteinzeitliche Seeufersiedlung Arbon-Bleiche 3. Funde. Archäologie im Thurgau 11, Frauenfeld, 383 p. DOMMELIER, S., S. BENTRAD, F. BOUCHET, J. C. PAICHELER, AND P. PE- TREQUIN. 1998. Parasitoses liees ä l' alimentation chez les populations neolithiques du lac de Chalain (Jura, France). Anthropozoologica 27: 41-49. DYER, N. W. 1998. Dioctophyma renale in ranch mink. Journal of Vet- erinary Diagnostic Investigation 10: 111-113. EUZEBY, J. 1963. Les maladies vermineuses des animaux domestiques et leurs incidences sur la pathologie humaine, Tome premier, Maladies dues aux Nemathelminthes, Fascicule deuxieme. Edition Vigot Freres, 843 p. FERNANDO, S. S. 1983. The giant kidney worm {Dioctophyma renale) infection in man in Australia. American Journal of Surgical Pathology 7: 281-284. GEORGI, J. R. 1980. Parasitology for veterinarians, 3rd ed. W.B. Saun- ders Company, Philadelphia, Pennsylvania, 460 p. HÖRNE, P. D. 2002. First evidence of enterobiasis in ancient Egypt. The Journal of Parasitology 88: 1019-1021. HÜSTER-PLOGMANN, H., AND U. LEUZINGER. 1995. Fischerei und Fis- chreste in der jungsteinzeitlichen Seeufersiedlung in Arbon (TG). Archäologie der Schweiz 18: 109-117. KARMANOVA, E. M. 1960. The life-cycle of the nematode, Dioctophyme renale (Goeze, 1782) parasitic in the kidney of carnivorous animals and man. Doklady Akademii Nauk SSSR 132: 1219-1221. [In Russian.] KAUFMANN, J. 1996. Parasitic infections of domestic animals: A diagnostic manu ai. Birkhäuser, 423 p. LEUZINGER, U. 2000. Die jungsteinzeitliche Seeufersiedlung Arbon-Bleiehe 3. Befunde. Archäologie im Thurgau 9, Frauenfeld, 187 p. MEASURES, L. N., AND R. C. ANDERSON. 1985. Centrarchid fish äs par- atenic host of the giant kidney worm, Dioctophyma renale (Goeze, 1782), in Ontario, Canada. Journal ofWildlife Diseases 21: 11-19. This content downloaded from 131.152.38.90 on Mon, 26 Apr 2021 15:06:40 UTC AU use subject to https://about.jstor.org/terms