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August 2015 PALEOEPIDEMIOLOGY OF INTESTINAL PARASITES AND LICE IN PRE-COLUMBIAN SOUTH AMERICA * Adauto Araujo Fundação Oswaldo Cruz, [email protected]

Karl J. Reinhard University of Nebraska at Lincoln, [email protected]

Daniela Leles Fundação Oswaldo Cruz

Luciana Sianto Fundação Oswaldo Cruz

Alena Iniguez Fundação Oswaldo Cruz

See next page for additional authors Follow this and additional works at: http://digitalcommons.unl.edu/natresreinhard Part of the Archaeological Anthropology Commons, Ecology and Evolutionary Biology Commons, Environmental Public Health Commons, Other Public Health Commons, and the Parasitology Commons

Araujo, Adauto; Reinhard, Karl J.; Leles, Daniela; Sianto, Luciana; Iniguez, Alena; Fugassa, Martin; Arriaza, Berrnardo; Orellana, Nancy; and Ferreira, Luiz Fernando, "PALEOEPIDEMIOLOGY OF INTESTINAL PARASITES AND LICE IN PRE- COLUMBIAN SOUTH AMERICA *" (2015). Karl Reinhard Papers/Publications. 39. http://digitalcommons.unl.edu/natresreinhard/39

This Article is brought to you for free and open access by the Natural Resources, School of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Karl Reinhard Papers/Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Adauto Araujo, Karl J. Reinhard, Daniela Leles, Luciana Sianto, Alena Iniguez, Martin Fugassa, Berrnardo Arriaza, Nancy Orellana, and Luiz Fernando Ferreira

This article is available at DigitalCommons@University of Nebraska - Lincoln: http://digitalcommons.unl.edu/natresreinhard/39 Vo lumen 43, N° 2, 20II. Paginas 303-313

Chungara, Revista de Antropologfa Chilena

PALEOEPIDEMIOLOGY OF INTESTINAL PARASITES

AND LICE IN PRE-COLUMBIAN SOUTH AMERICA *

PALEOEPIDEMIOLOGiA DE PARAsITOS INTESTINALES Y PIOJOS EN SUDAMERICA PRECOLOMBINA

Adauto Araujo', Karl ReinharJ2, Daniela Leles', Luciana Sianto', Alena Iniguez3, Martin Fugassa4, BernardoArriaza5,6,7, Nancy Orellana6,8,9, and Luiz Fernando Ferreira'

Some human parasites originated in prehominid ancestors in Africa. species, such as Enterobius vermicularis (pinworm), hookworms and Trichuris trichiura are shared by humans and other close phylogenetic primates (Pan and Gorilla), showing that they infected a common ancestor to this group. When humans migrated from Africa to other continents they carried these parasites wherever climate conditions allowed parasite transmission from to host. Other parasites, however, were acquired throughout human biological and social evolutive history when new territories were occupied. Paleoparasitology data is a valuable source to recover emergence and disappearance of parasite infections through analysis of archaeological remains. Parasites can be used as biological markers of prehistoric human migrations. They are also indicators of diet, as parasite life cycles are related to specific kinds of food consumed by human groups in the differenthabitats they occupied. We review paleoparasitological findings in South America, comparing human-host and intestinal parasites with life conditions and environmental relationships through time. Key words: Paleoparasitology, , , infectious diseases, ancient diseases, parasite-human evolution.

Algunos pardsitos humanos se originaron en ancestrales prehomfnidos de Africa. Especies de nemdtodos tales como Enterobius vermicularis y Trichuris trichiura son compartidos por los humanos y otras primates Jilogeneticamente emparentados (Pan and Gorilla), lo cual indica que tales pardsitos antiguamente infectaron a un ancestro comlin de estos grupos. Cuando los humanos migraron desde Africa a otras continentes, llevaran consigo pardsitos a lugares donde las condiciones climdticas permitieran su transmision de huesped a huesped. Sin embargo, otras pardsitos fueron adquiridos a traves de la historia evolutiva humana biologica y social. durante la ocupacion de nuevos territorios. Las evidendas paleoparasitologicas. encontradas a traves del andlisis de material arqueol6gico. son una fuente valiosa para recuperar informaci6n de infecciones parasitarias emergentes y desaparecidas. Las pardsitos pueden ser usados como marcadores biologicos de migraciones humanas prehistoricas. Ademds de esto. son indicadores de dieta. debido a que los dclos de vida parasitarios estdn relacionados con dertos alimentos que fueron consumidos por grupos humanos en los diferentes hdbitats oc upados. El objetivo de esta revision bibliogrdJica es reunir los ha­ llazgos paleoparasitol6gicos en Sudamerica y comparar la relacion huesped humano y pardsitos intestinales con condiciones de vida y relaciones ambientales a traves del tiempo. Palabras claves: paleoparasitologfa. copralitos. momias. enfermedades infecciosas. enfermedades antiguas. evolucion pardsito-humano.

Parasites have been found in ancient remains eggs. Protozoan cysts, however, are not as easy to throughout the world (Bouchet et al. 2003; identify. Nevertheless, serologic techniques have been Gonc;alves et al. 2003). Coprolites and latrine successfully applied to identify Giardia duodenalis, contents are the main source of intestinal parasite Giardia intestinalis and Entamoeba histolytica

* Este articulo fue presentado en el Ta ller de Bioarqueologfa "Avances y Desaffos del Paleoambiente y la Paleoparasitologfa", Arica, noviembre 2008. De 15 ponencias expuestas 7 fueron seleccionadas para ser evaluadas por investigadores externos. Luego fueron editadas por Bernardo Arriaza y Nancy Orellana, en su calidad de editores invitados en este mlmero. Escola Nacional de SaMe Publica, Funda�ao Os waldo Cruz, Rua Leopoldo Bulhoes 1480, CEP 2104 1-210, Rio de Janeiro, Brasil. [email protected]; [email protected]; [email protected] University of Nebraska, Lincoln, Nebraska, Estados Unidos. kreinhard [email protected] Instituto Oswaldo Cruz, Funda�ao Oswaldo Cruz, Av. Brasil 4365, CEP 21045-900, Rio de Janeiro, Brasil. [email protected] CONICET-Universidad Nacional de Mar del Plata, Argentina. [email protected] Instituto de Alta Investigaci6n, Universidad de Tarapaca, Arica, Chile. [email protected] Convenio de Desempeiio-UTAIMineduc, Universidad de Tarapaca, Arica, Chile. Departamento de Antropolog[a, Universidad de Tarapaca, Arica, Chile. Universidad de la Cordillera, La Paz, Bolivia. [email protected] Museo Nacional de Etnograffa y Folklore, La Paz, Bolivia.

Recibido: enero de 2010. Aceptado: noviembre 2010. 304 A. Araujo, K. Reinhard, D. LeJes, L. Sianto, A. Iniguez, M. Fugassa, B. Arriaza, N. Orellana, and L. F. Ferreira

antigens in human coprolites (Gonc;:alveset al. 2002, (1971 ) hypotheses about the impact of agriculture 2004; Le Bailly et al. 2008). Other parasites, such on . Reinhard showed that zoonotic as the protozoan Trypanosomacruzi was recovered infections, long standing in ancient populations, from mummified tissues and bone fragments by nearly disappeared in horticulturalists as human­ molecular biology techniques (Aufderheide et al. specific parasites emerged. Martinsonet al. (2003), 2004; Fernandes et al. 2008; Ferreira et al. 2000; Reinhard and Buikstra (2003) and Santoro et al. Guhl et al. 1999,2000; Lima et al. 2008). (2003) continued to explore the impact of parasitic Parasitology is relevant to anthropology and the disease ecology in the Andes. They clearly defined impact of parasites on human culture can be seen the role of trade, dress, and water contamination in language, art, religion, biology and archaeol­ on parasitic disease among the Chiribaya of Peru ogy (Araujo et al. 2003). Parasites and parasitic (Martinson et al. 2003;Reinhard and Buikstra 2003). disease have cultural expressions as represented in Santoro et al. (2003) demonstrated that empire de­ Moche ceramic art (Heck 2004). The use of regular velopment dramatically modifiedparasite ecology parasitological techniques,modified and adapted to of the L1uta Valley, Chile, during Inka expansion paleoparasitological research increased and expanded to this lowland territory. parasite findings to other kinds of archaeological Reinhard (1992) noted that the most sensational remains (Fugassa et al. 2006; Fugassa, Sardella contribution of paleoparasitology was towards a et al. 2008; Harter et al. 2003; Harter-Lailheugue better understanding of the first human migrations and Bouchet 2006). to the New World. In addition,Araujo et al. (1981), Araujo, Reinhard et al. (2008), and Montenegro History of Paleoparasites Found on et al. (2006) stated that human coastal and trans­ Archaeological Remains oceanic migrations also need consideration because helminth could not survive the colder Beringia cli­ Since the firststudies in South American human mate. Further work by Reinhard and Bryant (2008) coprolites (Pizzi and Schenone 1954), paleopara­ introduced the concept of pathoecology, which sitology has developed as a new research line and links parasitism to diet,environmental stress, and this new science appeared based on solid data other culturally-definedbehaviors in the definition founded on parasite findings from well-dated and of ancient disease. well-identified context, as predicted by Cockburn Molecular biology techniques were also applied (1967). Common wisdom about human health in diagnosing intestinal parasites. Loreille et al. conditions and parasite infections in the New World (2001) and Loreille and Bouchet (2003) discussed was challenged by paleoparasitological finds. the origin and evolution of Ascaris lumbricoides Hookworm (ancylostomids),whipworm (Trichuris and Ascaris suum parasitism based on DNA stud­ trichiura),pinworm (Enterobius vermicularis),and ies performed on parasite eggs recovered from roundworm (Ascaris lumbricoides) were found mediaeval latrines in Europe. Recently,Leles et al. infecting prehistoric populations both in North and (2008) applied molecular biology techniques and South America. were able to recover ancient Ascaris lumbricoides Paleoparasitology focuses on the recovery of DNA sequences from South American samples, parasites from archaeological sites to further elu­ negative by microscopy. These findings illustrate cidate the ancient impacts of parasites on culture. the importance of molecular biology techniques in Tracing the origins of parasites is one research thread diagnosing parasites in ancient remains. Molecular of importance to paleopathology (Reinhard 1990). biology techniques allow the study of genetic evolu­ Parasitism has a central role in bioarchaeology tion of parasites and the timing of their introduction (Reinhard 2008; Reinhard and Bryant 2008) and has into human populations (Dittmar et al. 2006; long been recognized as a tool for the archaeologist Dittmar 2009). By recovering aDNA (ancient DNA) (Reinhard 1992). sequences and genotyping parasites from human As reviewed by Reinhard and Bryant (2008),the remains increases the possibility to reconstruct the relation between cultural development and the nature early dispersion patterns of parasites (Raoult and of parasitism has long been investigated. Reinhard Drancourt 2008). (1988) first formalized this area of research in the This paper summarizes the extent of the knowl­ Southwestern United States by testing Cockburn's edge of intestinal parasite remains from South Paicocpidcllliolot!y of illlcSlillal IXlra,itcs alld licc ill prc-( 'oluillhiall South Aillerica 305

America. As such. it familiarizcs the reader with thc beforc thc coming of Europeans and Africans to current findings of parasites from this ecologically the Americas (Ferreira et al. 19XX). These results divcrse and culturally complex arca. Wc rcview werc used to trace prehistoric migration routes for intestinal parasite infections in pre-Columbian the peopling of the continent (Araujo et al. 19XI: South America. Paleoparasitological data is used Araujo. Reinhard et al. 200X: Araujo. Reinhard by archaeologists and anthropologists to reconstruct and Ferreira 200X: Reinhard et al. 20(1). Wild ancient events based on parasite life cycles and bio­ animal coprolites were also examined from many logical re4uirements to maintain transmission from archaeological sites. especially focused on parasites host to host. Climate changes are also associated of animals that may infect humans (Chame 20m; with the presence of parasite infections in ancient Sianto et al. 20(5). Due to the collaboration with people. For this purpose. paleoparasitological data the University of Nebraska. Lincoln. ancient food gathered by the laboratories of Funda<;ao Oswaldo remains turnedto be also a research line at Funda<;ao Cruz. U niversidad Nacional de Mar del Plata. and Oswaldo Cruz (FIOCRUZ). Molecular paleoparasi­ Universidad de Tarapaca-Arica. as well as data tology has a special laboratory to develop techni4ues from other sources published in the literature were and diagnoses in conditions avoiding modern DNA reviewed. The goal of this paper is to discuss pa­ contamination. The Laboratory of Paleoparasitology leoparasitology results in South America aiming to at FIOCRUZ. also has an image bank that will soon improve techni4ues and integrate data obtained by bc available on the Internet. the laboratories involved in this matter. A considerable amount of American paleopara­ sitological data appeared recently in the literature. Techniques Used to Analyse Even SouthernPatagonian coprolites were collected Bioarchaeological Material and examined (Fugassa 2007. 200X: Fugassa. Bayer and Sardella 200X). However as climatic conditions in Organic remains were examined by parasito­ Patagonia are not conducive to preservation. organic logical regular techni4ues after rehydration using matcrials arc continuously exposed to extreme dryness a trisodium phosphate a4ueous solution (Na1PO�­ and cold and sometimes to water percolation. Due to O.S'/r). According to the nature of the sample. the scarcity of coprolites and other organic material different techni4ues are recommended. For most a microscopic method was developed to search for analyses. spontaneous sedimentation in parasites at the Laboratory of Paleoparasitology of glass jars is recommended (Araujo et al. 199X: the University Nacional de Mar del Plata. Argentina Lutz 1919). To prevent bacterial and fungal growth or (Fugassa et al. 20(6). The method used sediments taphonomic processes that may cause DNA degrada­ recovered from the pelvic girdle and proved to be tion. thus interfering in molecular biology techni4ue effective: it allowed for recovery of parasite eggs that may be applied. all the rcmaining sedimcnt in from human sacral foramina stored in museum and the jars should be prescrved refrigerated (Pruvost scicntilic institutions (Jones 1982: Fugassa. Denegri et al. 2(07). et al. 2006: Reinhard 1992). The main reason for In some archaeological contexts. coprolites pursuing paleoparasitological research in Argentina are the main source for paleoparasitology analysis. is to understand the impact of disease during the For example. in northeasthern Brazil coprolites paicoepidemiological transition caused by the contact are found dispersed in archaeological layers under of Europeans with Patagonian Aborigins. rock-shelters or inside caves (Bouchet et al. 2(03). At the Universidad Nacional Mayor de San Mummitied bodies are rarely found in Brazilian Marcos in Lima. Peru. Ines Garate and her team archaeological sites. According to Mendon<;a de applied regular parasitological techniques to examine Souza (pel's. comm. 200X) preservation of the dead human coprolites excavated in the archaeological site was never a common practice among Brazilian of CamI to search for parasites (Garate et al. 2(05). indigenous cultures because they believe the soul Caral is the oldest city of the western hemisphere. should be released soon after death. Just after death datcd of 5000 years before present (BP) (Solis the individual was cremated. buried. or sometimes et al. 200 I ). Paleoparasitological research started the ashes were eaten by others (Chagnon 19X3). recently exploring this archaeological site material. Paleoparasitological research in Brazil started with an and lirst results are expected to be published soon. interest in knowing what parasite infections existed Paicoparasitology in Peruvian archaeological remains 306 A. Araujo. K. Reinhard, D. Leles. L. Sianto, A. Iniguez. M. Fugassa. B. Arriaza. N. Orellana. and L. F. Ferreira

has a tradition in coprolite (Patrucco et al. 1983) Whipworm, and roundworm infection were the same, and analysis (Fornaciari et al. 1992; prevalence rates among pre-Columbian populations Salo et al. 1994), but also on ectoparasites (Rick and transmission dynamics should behave in a dif­ et al. 2002; Dittmar 2000; Dittmar et al. 2003; Raoult ferent way according to the different cultures where et al. 2008). Another group interested in paleopara­ they were infecting. Parasite transmission dynamics sitological research was recently created by Luis was not the same in the city of Caral, in Peru, or in Huaman and Hugo Flores, and their students at the the Atacama Desert where the Chinchorros lived, and Universidad Cayetano Heredia. The main interest in the semi-arid region of Brazilian northeast where of these specialists is plant and food remains and hunter-gathering strategy was used by pre-historic parasite associated with food resources and diet. groups. Thus, generalization on parasites and ecology Regarding the study of parasites in mummified may lead to erroneous interpretations (Figure I and bodies, the Chinchorro mummies of NorthernChile Table I). Brazilian groups were numerous and lived present an interesting challenge. The most ancient in crowded villages before the European continent mummies were prepared by defleshing the body conquest (Heckenberger et al. 2008). Contrary to to the bones and taking out abdominal viscera so what is the common knowledge, Amerindian groups intestinal contents are not expected to be found. living in the Brazilian coast where numerous and Desert climate is especially suitable to preserve just before European conquest some groups were coprolites and paleoparasites. Fouant et al. (1982) displaced to the interior after tribal wars, and in tum reported a low incidence of parasites in Chilean exterminated small groups of hunter-gatherers living and Peruvian mummies. Considering the tradition in caves and rock-shelters (Medeiros 2002). of paleoparasitological research in Chile, the inter­ Studies about the impact of European contact ests varied from tuberculosis and Chagas disease with indigenous population opened a new line of (Rothhammer et al. 1985), intestinal parasites, and research, especially regarding paleoepidemiological diet as well as implications of ENSO phenomenon transition unleashed by European arrival (Guich6n (Arriaza et al. 2010; Williams et al. 2008). et al. 2006). Fugassa, Cicchino et al. (2008) showed In all the laboratories involved in paleoparasi­ that hunter-gatherer groups of Patagonia would have tologial research, ectoparasites have been studied. had a parasitological profile, zoonosis caused by Mummies of humans and other animals have been close wild animals contact or ingestion of inter­ searched for lice, fleas, and other arthropods. It is mediate hosts meat and vegetables contaminated important to look for parasites in the wrapping tis­ with parasite eggs or cysts, as well as arthropods, sues of the mummies and collect sediment samples such as oribatids, which are intermediate hosts for near the body. anoplocephalids. After European contact parasite infections and relative abundance of the common Intestinal Parasites human intestinal worms Ascaris lumbricoides and Trichuris trichiura changed significantly (Fugassa Paleoparasitological research proved that et al. 2006). Crowding indigenous populations common intestinal parasites infected pre-Columbian in religious missions, reducing mobility of the people long before European and African migra­ nomadic groups, and the fast and abundant ar­ tions (Gonc;alves et al. 2003). Data also showed rival of domestic animals, mainly sheeps, caused that Amerindians acquired infections by eating a rapid change of the helminth and protozoan intermediate hosts or being in close contact with fauna, due to human/animal parasite cross infec­ vectors and hosts of parasites that infect humans tions. European also caused a reduction of local (Patrucco et al. 1983; Sianto et al. 2005). fauna. Europeans also introduced food storage, Some intestinal parasites that originated in attracting rodents and their parasites to dwellings hominid African ancestors were introduced into (Guich6n et al. 2006). South America with their human hosts long before Trichuris trichiura (whipworm) infection European conquest (Araujo, Reinhard, Ferreira was common in South America on both sides of et al. 2008). Prehistoric people who lived on the the Andean cordillera (Gonc;alves et al. 2003). American continent were infected with common Whipworm eggs were the first to be found in a bacteria, , and helminths as in other parts South American mummy, together with Entamoeba of the world. Although hookworms, pinworm, coli cysts (Pizzi and Schenone 1954). Enterobius Paleoepidemiology of intestinal parasites and lice in pre-Columbian South America 307

16

12-�. 15 --. 23 13 --..... 24 14-----.. 18 32 ----.... 1 9 .�.,...... -

...-- 11

Figure I. Map of South America showing the location of paleoparasitological findings listed in Table I. Mapa de Sudamerica. muestra la localizaci6n de los paleopardsitos hal/ados. citados en la Tabla I. 308 A. Araujo, K. Reinhard, D. Leles, L. Sianto, A. Iniguez, M. Fugassa, B. Arriaza, N. Orellana, and L. F. Ferreira

Table I. Summary of South American paleoparasitological findings. Resumen de los hallazgos paleoparasitol6gicos en Sudamerica.

South America Country Archaeological Site No Date Parasites Reference

Pie de Palo not available Ent erobius vermicularis Fugassa et al. 2006

Enterobius vermicularis Perito Moreno, Santa Cruz 2 6,540±II 0 BP Rabditoid larvae Fugassa 2008 Tric huris sp.

Nombre de Jesus, Cabo Virgenes 3 not available Ascaris lumbricoides Fugassa et al. 2006

Orejas de Burro, Santa Cruz 4 3,720-3,978 BP Ascaridid Fugassa 2006

Valle Encantado, Neuquen 5 1,000-500 BP Anc ylostomid Gon�alves et al. 2003 Argentina Las Mandibulas, Tierra del Fuego 6 Historic Capillarids Fugassa et al. 2008

Caleta Falsa, Tierra del Fuego 7 850 years BP Capillarids Fugassa et al. 2008

Cerro Norte XI, Pali Aike, Santa Cruz 8 not available Capillarids new fi ndings

Salitroso, Santa Cruz 9 not available Trichuris trichiura new findings

Parador Nativo, Rio Negro 10 1,513±48 BP Tric huris trichiura Fugassa et al. 2006

Centro Minero, Rio Negro II 689±44 BP Tric huris trichiura Fugassa et al. 2006

Huamey Valley 12 1,000 AD Trichuris trichiura Patrucco et al. 1983

Coast (southern) 13 10,000-4,000 BP D. pac ijic um Patrucco et al. 1983 Peru Osmore, Peru 14 1,020-1,476 BP D. pac ijic um Patrucco et al. 1983

Huaca Prieta 15 3,000 BP Diphyllobotrium sp. Callen and Cameron 1960

Toea do Meio, Piauf 16 8,800±60 BP Asc aris lumbricoides Leles et al. 2008

Lapa Pequena, Minas Gerais 17 8,000-7,000 BP Ascaris lumbricoides Gon�al yes et al. 2003

Ascaris lumbricoides Santa Elina, Mato Grosso 18 4,000-2,000 BP Gon�alves et al. 2003 Hymenolepis nana

Gruta do Gentio II, Minas Gerais 19 3,490±I20-4,30±70 BP Ascaris lumbricoides Leles et al. 2008 Ascaris lumbricoides Gentio Cave, Minas Gerais 20 3,490±1 20-430±70 BP Gon�alves et al. 2003 Brazil Acantocephala Pedra Furada, Piauf I 21 not available Trichuris trichiura Gon�al yes et al. 2003

Tric huris trichiura Boqueirao Soberbo, Minas Gerais 22 4,905±85-1 ,325±60 BP Ferreira et al. 1984 Acantocephala

Estrago Cave, Pernambuco 23 2,000 BP Trichuris trichiura Gon�alves et al. 2003

Itacambira, Minas Gerais 24 not available Trichuris trichiura Confalonieri 1988

Sftio do Meio, Piauf 25 not available Aneylostomid Gon�al yes et al. 2003

D. pacijic um Ferreira et al. 1984 Tiliviche, Iquique 26 4,110-1,950 BC Enterobius vermieularis Gon�alves et al. 2003 Aneylostomid

Tul

1,200-1,500 AD Tric huris trichiura Lluta Valley, Arica 28 Santoro et al. 2003 Chile (Inka period) Hymenolepis nana

Toconao, San Pedro de Atacama 29 2,500-2,100 BP Anc ylostomid Gon�alves et al. 2003

EI Plomo, Santiago 30 Pre-Columbian Trichuris trichiura Ferreira et al. 1984

Catarpe, San Pedro de Atacama 31 1,450-1,525 AD Tric honstrongylus sp. Gon�al yes et al. 2003

San Miguel de Azapa 32 4,000-5,000AP Dyp hyllobotrium sp. Reinhard and Urban 2003 Paleoepidemiology of intestinal parasites and lice in pre-Columbian South America 309

vermicularis (pinworm) eggs, curiously, were only paleoparasitological analysis. Diphyllobothrium found among ancient populations who lived on the pacificum was a common intestinal infection in Pacific side. Molecular biology studies, however, the past as it is today in the Pacific coast. The con­ showed interesting results, with two different pin­ sumption of raw fish is a common habit in many worm lineages in the Pacificcoast populations. One countries and different cultures all over the world. had the same sequences of North American lineages, Baer et al. (1967) reported the presence of D. pa­ but the other showed divergent nucleotides in some cificum in modern Peruvian coast population, later sequences (Iniguez et al. 2003). According to the D. pacificum infection was confirmed in Peruvian authors, this may be interpreted as the consequence and Chilean pre-Columbian coprolites (Araujo of different origins. While one was introduced by et al. 1983; Ferreira et al. 1984; Patrucco et al. 1983; human pre-historic migrations that crossed the Bering Reinhard and Urban 2003). Diphyllobothrium paci­ Land Bridge more than 20,000 years ago, the other ficum human transmission is due to the consumption lineage suggests an introduction by another route, in of raw fish containing parasites. this case supporting transpacific contacts of Asian Echinostoma sp. eggs were found in a Brazilian people in pre-Columbian times (Araujo, Reinhard mummy (Sianto et al. 2005). As this parasite was and Ferreira 2008; Iniguez et al. 2006). not recorded in modern South American popula­ Regarding intestinal protozoan infection, South tion, the finding was carefully investigated before American paleoparasitology data is not as represen­ publishing this information. It is interesting to note tative, although the two most prevalent protozoan that this case of Echinostoma human infection in parasites found in coprolites and sediments were pre-historic South America was associated with Entamoeba histolytica and Giardia intestinalis a case of Chagas disease, with intestinal lesions (Gon�alves, Araujo et al. 2002; Gon�alves, da Silva characterized by megacolon (Fernandeset al. 2008). et aI. 2004).Antigens of Giardia sp., Cryptosporidium In this case two important points should be em­ sp., Cyclospora sp., and Helicobacter pilori, were phasized: firstly, the description of Chagas disease identified in Andean mummies dated up to 3,000 lesions in a mummy outside the Andean region, years by fluorescent microscopy (Allison et al. 1999; confirmed by molecular paleoparasitology studies Ortega and Bonavia 2003). (Fernandes et al. 2008); secondly, an infection by As evidenced by paleoparasitology finds, Echinostoma in South American human population common human intestinal parasites were infect­ not yet described (Sianto et al. 2005). These find­ ing South American pre-Columbian populations. ings point to the need of further detailed studies at Although data are still missing for many South this archaeological site. American countries, an interesting paleoparasito­ logical picture has been traced from Argentinean, Animal Parasites in Humans Bolivian, Brazilian, Chilean, and Peruvian archaeo­ logical material (Ferreira et al. 2008). When these The presence of animal parasites in human findings are compared with North American pa­ coprolites shows the use of different foodresources. leoparasitology, a similar picture appears and human However, these habits may still be maintained today strategies to confront differentenvironments can be by traditional groups. For example, Coimbra Jr. seen between the continents (Reinhard 1992). and Mello (198 1) found Capillaria eggs in modern Many of these parasites originated in Old World Amazonian Indian group, and Fugassa, Bayer and human populations (Araujo and Ferreira 1995). They Sardella (2008) identified Capillaria eggs in animal came out of Africa with the peopling of Europe. coprolites in Patagonia, which may point to a po­ From there, they spread through the world where tential source of infection for humans in this region. climate conditions allowed transmission (Araujo, Capillaria species rarely infect humans, but eggs Reinhard and Ferreira 2008). However, humans can pass with feces when humans eat an infected acquired other parasites from animals whenever host. Thus, the eggs can be found in human feces, humans invaded new habitats, adopted new habits, but disappear after a few days. or created new technologies amplifying their range Fugassa et al. (2006) presented an overview of of influence on the environment. human and animal intestinal helminths and proto­ Humans adopted food habits according to the zoa found in archaeological material excavated in occupied region. This is evidenced by coprolite Patagonia. These findings illustrate the diversity 310 A. Araujo, K. Reinhard, D. Leles, L. Sianto, A. Iniguez, M. Fugassa, B. Arriaza, N. Orellana, and L. F Ferreira

of parasites that can be found in archaeological South American mummies recording new finds of remains, in close contact with humans beginning Anthropophthirus capitis (a new genus proposed 10,000 years ago. Therefore, paleoparasitology is by Retana-Salazar and Ramirez-Morales 2006 to a powerful tool to investigate the variety of food substitute Pediculus humanus capitis) in mummies sources used by humans at different times by of the Chinchorro tradition dated to 4,000 years. studying organic remains preserved in archaeo­ This new species proposal is very controversial, logical sites. but it was proposed due to genetic similitudes found between Pediculus human us (human body Ectoparasites lice) and the Parapediculus (ectoparasite of South American monkeys). South American mummies provided positive To conclude, South American paleoparasitolo­ results for ectoparasites. In the fur of mummified gists, together with North American colleagues, are guinea pigs (Cavia aperea f. porcellus), numerous building an evolving picture of parasite infections well-preserved ectoparasites (lice, fleas, ) could dated from the peopling of the Americas (Araujo, be recovered (Dittmar 2002; Dittmar et al. 2003). Reinhard and Ferreira 2008; Araujo, Reinhard Moreover, paleoparasitological examination of et al. 2008). Paleoparasitological data, through the Amerindian clothes provided parasite finds, such use of microscopic, immunology and molecular as ectoparasites (Fugassa et al. 2007). Molecular techniques, is an efficient way to provide informa­ biology studies were also performed (Dittmar tion about human behavior in the past, contributing et al. 2003; Raoult et al. 2008), as well as pa­ to understanding the origin and evolution of in­ leoepidemiological and quantitative attempts fectious diseases and their impact on prehistoric to evaluate head lice infection (Reinhard and populations. Buikstra 2003). Head lice were found still at­ Acknowledgements: Supported by the Brazilain tached to hair fragments of a skeleton dated to agencies CNPq, CAPES, and FAPERJ. We also 10,000 years in northeastern Brazilian (Araujo want to thanks the Convenio Desempefio UTA­ et al. 2000). Crablouse was also found infecting MINEDUC for their support and the manuscript Peruvian mummies (Rick et al. 2002). Rivera et editors, and outside reviewers for their comments al. (2008) reviewed the findings of head lice in and suggestions.

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