Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-28T16:14:09.343Z Has data issue: false hasContentIssue false

Assessing parasite epidemiology in the epidemiological importance of Patagonian Late Holocene rockshelters using carnivore coprolites in the past: new data from Piedra Parada, Argentina

Published online by Cambridge University Press:  04 August 2022

Martín H. Fugassa*
Affiliation:
Laboratorio de Parasitología de Sitios Arqueológicos, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Pablo M. Fernández
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina Instituto Nacional de Antropología y Pensamiento Latinoamericano, Buenos Aires, Argentina Universidad de Buenos Aires, Buenos Aires, Argentina
Cristina Bellelli
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina Instituto Nacional de Antropología y Pensamiento Latinoamericano, Buenos Aires, Argentina
Mariana Carballido Calatayud
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina Instituto Nacional de Antropología y Pensamiento Latinoamericano, Buenos Aires, Argentina Universidad de Buenos Aires, Buenos Aires, Argentina
*
Author for correspondence: Martín H. Fugassa, E-mail: mhfugassa@gmail.com

Abstract

The aim of this research was to analyse the variability of parasite assemblages on a small spatial scale, by examining carnivore coprolites from the archaeological site Campo Moncada 2 (CM2), Piedra Parada area, Chubut province, Argentina, and comparing the results with those previously obtained from the archaeological site Campo Cerda 1 (CCe1), located in the same area. Six carnivore coprolites from CM2 were analysed: 4 obtained in sub-level 2a and 2 obtained in sub-level 2a/b. Two radiocarbon dates associated with the coprolites placed the samples chronologically between 780 ± 80 and 860 ± 80 years before present. The rehydrated sediments were sieved and then allowed to sediment spontaneously. The sediment was used for parasitological examination under light microscopy. Conservative estimation of total parasite richness resulted in 21 parasitic taxa. The taxa with the highest fecal prevalence (>50%) corresponded to parasites prevalent in modern carnivores (Alaria sp., Toxocara cf. canis, Toxascaris sp., Eucoleus cf. aerophila, Trichuris sp. and Ancylostomatidae gen. sp.). Assuming that the fox coprolites are contemporaneous, the total fecal parasite richness estimated for CM2 and previously for CCe1 was similar. The high total parasite richness found suggests a network of host–parasite relationships that could include regional hunter-gatherers. The results obtained in carnivore coprolites allow us to infer a very diverse biological community in Piedra Parada area, so the regional caves and rockshelters could have a proportional epidemiological importance as parasite exchange nodes.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amalfitano, G, Petrigh, RS, Loos, J and Fugassa, MH (2017) Ampliación de los estudios parasitológicos en camélidos del sitio arqueológico CCP7, Santa Cruz, Argentina. Anales del Instituto de la Patagonia 45, 101108.Google Scholar
Amin, O (2013) Classification of the Acanthocephala. Folia Parasitologica 60, 273305.CrossRefGoogle ScholarPubMed
Anderson, RC (2000) Nematode Parasites of Vertebrates: Their Development and Transmission, 2nd Edn. Wallingford: CABI Publishing, 650 p.CrossRefGoogle Scholar
Anderson, RC, Chabaud, AG and Willmott, Sh (2009) Keys to the Nematode Parasites of Vertebrates: Archival Volume. Wallingfod: CAB International Publishing, 463 p.CrossRefGoogle Scholar
Araújo, A, Jansen, AM, Reinhard, K and Ferreira, LF (2009) Paleoparasitology of Chagas disease – A review. Memorias do Instituto Oswaldo Cruz 104(suppl. I), 916.CrossRefGoogle ScholarPubMed
Bellelli, C (1988) Recursos minerales: su estrategia de aprovisionamiento en los niveles tempranos de Campo Moncada 2, Valle de Piedra Parada, Río Chubut. In Yacobaccio, , H (Ed), Arqueología Contemporánea Argentina (Actualidad y Perspectiva). Buenos Aires: Editorial Búsqueda, pp. 147176.Google Scholar
Bellelli, C (1991) Campo Moncada 2 (CM2): Momentos tempranos de ocupación del Valle de Piedra Parada, (Chubut, República Argentina). In Niemeyer, H (ed.), Actas del XI Congreso Nacional de Arqueología Chilena. Santiago de Chile: Sociedad Chilena de Arqueología. pp. 225235.Google Scholar
Bellelli, C and Guraieb, G (2019) Reevaluación cronológica de la secuencia arqueológica del curso medio del río Chubut (área Piedra Parada). In Gómez Otero, J, Svoboda, A and Banegas, A (eds), Arqueología de la Patagonia: el pasado en las arenas. Puerto Madryn: IDEAUS – CONICET, pp. 259270.Google Scholar
Beltrame, MO, Fugassa, MH and Sardella, NH (2010) First paleoparasitological results from Late Holocene in Patagonian coprolites, Argentina. Journal of Parasitology 96, 648651.CrossRefGoogle Scholar
Bouchet, F, Guidon, N, Dittmar, K, Harter, S, Ferreira, LF, Chaves, SM, Reinhard, K and Araujo, A (2003) Parasite remains in archaeological sites. Memorias do Instituto Oswaldo Cruz 98, 4752.CrossRefGoogle ScholarPubMed
Bray, RA, Gibson, DI and Jones, A (2008) Keys to the Trematoda, Volume 3. Wallingford: CAB International Publishing, 848 p.CrossRefGoogle Scholar
Bryan, HM, Darimont, ChT, Hill, JE, Paquet, PC, Andrew Thompson, RC, Wagner, B and Smits, JEG (2012) Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago. Parasitology 139, 781790.CrossRefGoogle Scholar
Bush, A, Lafferty, K, Lotz, J and Shostak, A (1997) Parasitology meets ecology on its own terms: Margolis et al revisited. Journal of Parasitology 83, 575583.Google Scholar
Castillo Sánchez, LL, Álvarez, MC, Nuñez, MB, Kaufmann, CA, Alcaraz, AP, Ochoa, AC and Gatica, A (2021) Potencial depredación intragremio? Puma concolor y Lycalopex gymnocercus en el ecotono Chaco-Monte, San Luis, República Argentina. Notas Sobre Mamíferos Sudamericanos 3, 1–9. https://doi.org/10.31687/saremNMS.21.3.3 (Accessed 14 April 2022).CrossRefGoogle Scholar
Chame, M (2003) Terrestrial mammal feces: a morphometric summary and description. Memorias do Instituto Oswaldo Cruz 98, 7194.CrossRefGoogle ScholarPubMed
Craig, HL and Craig, PS (2005) Helminth parasites of wolves (Canis lupus): a species list and an analysis of published prevalence studies in Nearctic and Palearctic populations. Journal of Helminthology 79, 95103.CrossRefGoogle Scholar
Díaz, NI (2010) New historical records of the jaguar (Panthera onca) in Patagonia. Revista Mexicana de Mastozoología 14, 2345.CrossRefGoogle Scholar
Fahrion, AS, Schnyder, M, Wichert, B and Deplazes, P (2011) Toxocara eggs shed by dogs and cats and their molecular and morphometric species-specific identification: is the finding of T. cati eggs shed by dogs of epidemiological relevance? Veterinary Parasitology 177, 186189.CrossRefGoogle ScholarPubMed
Farfán, CA and Jiménez Milón, P (2001) Dieta del zorro andino Pseudalopex culpaeus (Canidae) en el matorral desértico del sur de Perú. Revista de Ecología Latinoamericana 8, 19.Google Scholar
Fernández, PM (2008) Taphonomy and zooarchaeology in the Neotropics: A view from northwestern Patagonian Forest and Steppe. Quaternary International 180, 6374.CrossRefGoogle Scholar
Fernandez, BJ, Cooper, JD, Cullen, JB, Freeman, RS, Ritchie, AC, Scott, AA and Stuart, PE (1976) Systemic infection with Alaria americana (Trematoda). Canadian Medical Association Journal 115, 11111114.Google Scholar
Foreyt, WJ (2001) Veterinary Parasitology Reference Manual, 5th Edn. Ames, IA, USA: Blackwell Publishing Professional, 245 p.Google Scholar
Fugassa, MH (2020) Updated checklist of helminths found in terrestrial mammals of Argentine Patagonia. Journal of Helminthology 94, e170, 1–56.CrossRefGoogle ScholarPubMed
Fugassa, MH and Petrigh, RS (2017) Apex predators, rockshelters, and zoonoses in the Patagonian Holocene. Journal of Parasitology 103, 791794.CrossRefGoogle ScholarPubMed
Fugassa, MH, Denegri, GM, Sardella, NH, Araújo, A, Guichón, RA, Martínez, PA, Civalero, MT and Aschero, C (2006) Paleoparasitological records in a canid coprolite from Patagonia, Argentina. Journal of Parasitology 92, 11101111.CrossRefGoogle Scholar
Fugassa, MH, Sardella, NH and Denegri, GM (2007) Paleoparasitological analysis of a raptor pellet from Southern Patagonia. Journal of Parasitology 93, 421422.CrossRefGoogle ScholarPubMed
Fugassa, MH, Beltrame, MO, Bayer, MS and Sardella, NH (2009) Zoonotic parasites associated with felines from the Patagonian Holocene. Memorias do Instituto Oswaldo Cruz 104, 11771180.CrossRefGoogle ScholarPubMed
Fugassa, MH, Petrigh, RS, Fernández, PM, Catallud, M and Bellelli, C (2018) Fox parasites in pre-Columbian times: evidence from the past to understand the current helminth assemblages. Acta Tropica 185, 380384.CrossRefGoogle ScholarPubMed
Fugassa, MH, Petrigh, RS, Fernández, PM, Carballido Catalayud, M and Bellelli, C (2021) New parasitological and molecular data of carnivore coprolites from Campo Cerda 1 archaeological site (Chubut, Argentina). Insights into human-animal interactions in Patagonia. Journal of Archaeological Science Reports 37, 103018.CrossRefGoogle Scholar
Gibson, D, Jones, A and Bray, R (2002) Keys to the Trematoda, Volume 1. London: CAB International Publishing, 544 p.CrossRefGoogle Scholar
Jackson, D (2007) Estructura, intensidad y reiteración en las ocupaciones paleoindias en cuevas y aleros de Patagonia Meridional (Chile). Revista de Arqueología, Cazadores Recolectores del Cono Sur 2, 6585.Google Scholar
Jones, A, Bray, RA and Gibson, DI (2005) Keys to the Trematoda, Volume 2. Wallingford: CAB International Publishing, 768 p.CrossRefGoogle Scholar
Khalil, LF, Jones, A and Bray, RA (1994) Keys to the cestode parasites of vertebrates. Wallingford: CAB International.CrossRefGoogle Scholar
Kuchta, R, Scholz, T, Brabec, J and Bray, RA (2008) Suppression of the tapeworm order Pseudophyllidea (Platyhelminthes: Eucestoda) and the proposal of two new orders, Bothriocephalidea and Diphyllobothriidea. International Journal for Parasitology 38, 4955.CrossRefGoogle ScholarPubMed
Lesmeister, D, Millspaugh, J, Wade, S and Gompper, M (2008) A survey of parasites identified in the feces of eastern spotted skunks (Spilogale putorius) in Western Arkansas. Journal of Wildlife Diseases 44, 10411044.CrossRefGoogle ScholarPubMed
Levine, ND and Wens, V (1988) Cross-transmission of Eimeria spp. (Protozoa, Apicomplexa) of rodents – a review. Journal of Prolozoology 35, 434437.CrossRefGoogle ScholarPubMed
Ljubaschenko, CJ and Petrov, AM (1962) Krankheiten der Pelztiere, Moskau.Google Scholar
Marchione, P and Bellelli, C (2013) El trabajo del cuero entre los cazadores-recolectores de la Patagonia centro-septentrional. Campo Moncada 2 (valle medio del río Chubut). Relaciones de la Sociedad Argentina de Antropología 38, 223246.Google Scholar
Miotti, L (2006) La fachada atlántica, como puerta de ingreso alternativa de la colonización humana de América del sur durante la transición Pleistoceno/Holoceno. In Jiménez, JC and González, S (eds), II Simposio Internacional El Hombre Temprano en América. México: Museo del Desierto de Coahuila, UNAM, pp. 155188.Google Scholar
Miyazaki, I (1991) An Illustrated Book of Helminthic Zoonoses. Tokyo: International Medical Foundation of Japan, 494 p.Google Scholar
Moleón, M, Kinsella, J, Moreno, P, Ferreyra, H, Pereira, J, Pía, M and Beldoménico, P (2015) New hosts and localities for helminths of carnivores in Argentina. Zootaxa 4057, 106114.CrossRefGoogle ScholarPubMed
Molnar, B, Ciucci, P, Mastrantonio, G and Betschart, B (2019) Correlates of parasites and pseudoparasites in wolves (Canis lupus) across continents: a comparison among Yellowstone (USA), Abruzzo (IT) and Mercantour (FR) national parks. International Journal for Parasitology: Parasites and Wildlife 10, 196206.Google Scholar
Müller Graf, ChDM (1995) A coprological survey of intestinal parasites of wild lions (Panthera leo) in the Serengeti and the Ngorongoro Crater, Tanzania, East Africa. Journal of Parasitology 81, 812814.CrossRefGoogle ScholarPubMed
Nacuzzi, LR (1987) Una hipótesis etnohistórica aplicada a sitios de Patagonia Central y Septentrional. In Comunicaciones de las Primeras Jornadas de Arqueología de la Patagonia. Rawson: Dirección de Cultura de la Provincia, pp. 179184.Google Scholar
Nadler, SA and Ponce de León, G (2011) Integrating molecular and morphological approaches for characterizing parasitic cryptic species: implications for parasitology. Parasitology 138, 16881709.CrossRefGoogle ScholarPubMed
Pérez de Micou, C (1988) Paleoetnobotánica y determinación de territorios de explotación en asentamientos cazadores-recolectores. Precirculados de las Ponencias Científicas presentadas a los Simposios del IX Congreso Nacional de Arqueología Argentina. Universidad de Buenos Aires: Instituto de Ciencias Antropológicas, pp. 5263. Universidad de Buenos Aires: Instituto de Ciencias Antropológicas.Google Scholar
Popiolek, M, Szczesna-Staskiewicz, J, Bartoszewicz, M, Okarma, H, Smalec, B and Zalewski, A (2011) Helminth parasites of an introduced invasive carnivore species, the raccoon (Procyon lotor L.), from the Warta Mouth National Park (Poland). Journal of Parasitology 97, 357360.CrossRefGoogle ScholarPubMed
Poulin, R (1995) Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecology Monographs 65, 6174.CrossRefGoogle Scholar
Poulin, R and Morand, S (2000) The diversity of parasites. Quarterly Review of Biology 75, 277293.CrossRefGoogle ScholarPubMed
Prevosti, FJ, Ramírez, MA, Schiaffini, M, Martin, F, Udrizar Sauthier, DE, Carrera, M and Pardiñas, UFJ (2015) Extinctions in near time: new radiocarbon dates point to a very recent disappearance of the South American fox Dusicyon avus (Carnivora: Canidae). Biological Journal of the Linnean Society 116, 704720.CrossRefGoogle Scholar
Reinhard, K, Fink, M and Skiles, J (2003) A case of megacolon in Rio Grande Valley as a possible case of Chagas disease. Memorias do Instituto Oswaldo Cruz 98(suppl. I), 165172.CrossRefGoogle Scholar
Royal Veterinary College (2021) Available at https://www.rvc.ac.uk/review/parasitology/Flotation/Flotation_fluids/General.htm (Accessed 11 February 2022).Google Scholar
Sardella, NH and Fugassa, MH (2011) Paleoparasitological finding of eggs of nematodes in rodent coprolites dated at the Early Holocene from the archaeological site Cerro Casa de Piedra 7, Santa Cruz, Argentina. Journal of Parasitology 97, 11841187.CrossRefGoogle ScholarPubMed
Shaw, WD and Dobson, AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111S133.CrossRefGoogle ScholarPubMed
Solorzano García, B, Day, J, Gómez-Contreras, M, Cristóbal, J, Osorio-Sarabia, D and Rodríguez-Luna, E (2017) Coprological survey of parasites of free-ranging jaguar (Panthera onca) and puma (Puma concolor) inhabiting 2 types of tropical forests in Mexico. Revista Mexicana de Biodiversidad 88, 146153.CrossRefGoogle Scholar
Soulsby, EJL (1987) Parasitología y enfermedades parasitarias en los animales domésticos, 7th Edn. México: Interamericana, 823 p.Google Scholar
Szczesna, J, Popiolek, M, Schmidt, K and Kowalczyk, R (2008) Coprological study on helminth fauna in Eurasian Lynx (Lynx lynx) from the Bialowieza primaveral forest in eastern Poland. Journal of Parasitology 94, 981984.CrossRefGoogle Scholar
Taglioretti, V, Fugassa, MH, Rindel, D and Sardella, NH (2017) New parasitological findings for Pre-Hispanic camelids. Parasitology 144, 17631768.CrossRefGoogle ScholarPubMed
Walther, BA, Cotgreave, RD, Price, RD, Gregory, RD and Clayton, DH (1995) Sampling effort and parasite species richness. Parasitology Today 11, 306310.CrossRefGoogle ScholarPubMed
Watve, MG and Sukumar, R (1995) Parasite abundance and diversity in mammals: correlates with host ecology. Proceedings of National Academic of Science USA 92, 89458949.CrossRefGoogle ScholarPubMed
Zajac, AM and Conboy, GA (2012) Veterinary Clinical Parasitology, 8th Edn. Iowa: Wiley-Blackwell, 354 p.Google Scholar