Parasitism of prehistoric humans and companion animals from Antelope Cave, Mojave County, northwest Arizona

Previously, we reported a tick recovered from Antelope Cave in extreme northwest Arizona. Further analyses of coprolites from Antelope Cave revealed additional parasitological data from coprolites of both human and canid origin. A second tick was found. This site is the only archaeological locality where ticks have been recovered. We also discovered an acanthocephalan in association with Enterobius vermicularis eggs in the same coprolite. This association shows that the coprolite was deposited by a human. This discovery expands our knowledge of the range of prehistoric acanthocephalan infection. In addition, findings from canid coprolites of Trichuris vulpis are reported. This is the first published discovery of T. vulpis from a North American archaeological context. The close association of dogs with humans at Ancestral Puebloan (Anasazi) sites raises the potential that zoonotic parasites were transferred to the human population. The archaeological occupation is associated with the Ancestral Pueblo culture 1,100 yr ago.     

The finding of Enterobius vermicularis eggs in pre-Columbian human coprolites

Enterobius vermicularis eggs were found in human coprolites collected in the archaeological site of Caserones, Tarapaca Valley, Chile, dating from 400 BC to 800 AD. The human pinworm had already been found in other pre-historic archaeological sites in America, and its introduction in this continent is discussed.     

Molecular paleoparasitological diagnosis of Ascaris sp. from coprolites: new scenery of ascariasis in pre-Colombian South America times

Paleoparasitological studies using microscopy showed that Ascarisand Trichuris trichiura are the human intestinal parasites most found in archaeological sites. However, in pre-Columbian South American archaeological sites, Ascaris is rare. In this work we standardized a molecular methodology for Ascaris diagnosis directly from ancient DNA retrieved from coprolites. Using cythochrome b gene (142 bp) target, ancient DNA sequences were retrieved from South American samples, negative by microscopy. Moreover, the methodology applied was sensitive enough to detect ancient DNA extracted from 30 Ascaris eggs from an European coprolite. These results revealed a new scenery for the paleodistribution of Ascaris in South America.     

Insights from Characterizing Extinct Human Gut Microbiomes

In an effort to better understand the ancestral state of the human distal gut microbiome, we examine feces retrieved from archaeological contexts (coprolites). To accomplish this, we pyrosequenced the 16S rDNA V3 region from duplicate coprolite samples recovered from three archaeological sites, each representing a different depositional environment: Hinds Cave (∼8000 years B.P.) in the southern United States, Caserones (1600 years B.P.) in northern Chile, and Rio Zape in northern Mexico (1400 years B.P.). Clustering algorithms grouped samples from the same site. Phyletic representation was more similar within sites than between them. A Bayesian approach to source-tracking was used to compare the coprolite data to published data from known sources that include, soil, compost, human gut from rural African children, human gut, oral and skin from US cosmopolitan adults and non-human primate gut. The data from the Hinds Cave samples largely represented unknown sources. The Caserones samples, retrieved directly from natural mummies, matched compost in high proportion. A substantial and robust proportion of Rio Zape data was predicted to match the gut microbiome found in traditional rural communities, with more minor matches to other sources. One of the Rio Zape samples had taxonomic representation consistent with a child. To provide an idealized scenario for sample preservation, we also applied source tracking to previously published data for Ötzi the Iceman and a soldier frozen for 93 years on a glacier. Overall these studies reveal that human microbiome data has been preserved in some coprolites, and these preserved human microbiomes match more closely to those from the rural communities than to those from cosmopolitan communities. These results suggest that the modern cosmopolitan lifestyle resulted in a dramatic change to the human gut microbiome.     

Determination of prehistoric use of arrowhead (Sagittaria,Alismataceae) in the Great Basin of North America by scanning electron microscopy

Analyses of human coprolites from Dryden Cave, Nevada, indicated that the prehistoric population that inhabited the rockshelter included locally available herbs in their diet. Plant epidermal tissue remains have been identified as fragments from roots ofSagittaria (Alismataceae), a genus of semi-aquatic monocots. Other remains from the coprolites included fish bones, freshwater diatoms, seeds, and pollen. This assemblage supports the hypothesis that this prehistoric population principally exploited the available lacustrine resources of the area; comparisons with other archaeological sites suggests that this pattern had an extremely long history of development in the Great Basin.     

Dioctophymidae eggs in coprolites from Neolithic site of Arbon-Bleiche 3 (Switzerland)

Dioctophymidae eggs were found in human coprolites dated from 3,384 to 3,370 BC from the site Arbon-Bleiche 3, Switzerland. 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.     

Enterobius vermicularis: ancient DNA from North and South American human coprolites

A molecular paleoparasitological diagnostic approach was developed for Enterobius vermicularis. Ancient DNA was extracted from 27 coprolites from archaeological sites in Chile and USA. Enzymatic amplification of human mtDNA sequences confirmed the human origin. We designed primers specific to the E. vermicularis 5S ribosomal RNA spacer region and they allowed reproducible polymerase chain reaction identification of ancient material. We suggested that the paleoparasitological microscopic identification could accompany molecular diagnosis, which also opens the possibility of sequence analysis to understand parasite-host evolution.     

Cultural ecology of prehistoric parasitism on the Colorado Plateau as evidenced by coprology

The study of coprolites (desiccated feces) is recognized as a viable method for analyzing parasitism of prehistoric peoples. Eight species of helminth parasites, including nematodes, cestodes, and acanthcephalans, have been recovered from archaeological sites on the Colorado Plateau. The comparative analysis of parasitological findings illustrates the effects of changing subsistence strategies and varying life-style on prehistoric human parasitism. This comparative study is based on the analysis of coprolites recovered from one Archaic hunter-gatherer site and two Anasazi agricultural villages. Hunter-gatherers are represented by coprolites from Dust Devil Cave in south-eastern Utah. Coprolites of prehistoric agriculturalists from Antelope House in Canyon de Chelly, Arizona, and from Salmon Ruin in northwestern New Mexico were studied. The results demonstrate that helminth parasitism increased with the advent of agriculture. Between the agricultural sites, differences in patterns of excreta disposal, foraging behavior, and local ecology resulted in pronounced variations in both percentage of coprolites containing parasite remains and the number of parasite species represented.     

A palaeoparasitological analysis of rodent coprolites from the Cueva Huenul 1 archaeological site in Patagonia (Argentina)

The aim of the present study was to examine the parasite fauna present in rodent coprolites collected from Cueva Huenul 1 (CH1), northern Neuquén (Patagonia, Argentina), an archaeological site that provides stratified sequences of archaeological and palaeontological remains dating from the Late Pleistocene/Early Holocene Transition to the Late Holocene period. Twenty rodent coprolites collected from different sedimentary units from the site, with ages ranging from 13.844 ± 75-1.416 ± 37 years BP, were examined for parasites. Each coprolite was processed as a whole: rehydrated, homogenised, spontaneously sedimented and examined using light microscopy. The coprolites and the eggs of any parasites present were described, measured and photographed. In all, 158 parasite eggs were found in 10 coprolites. The faeces were positive for Viscachataenia quadrata Denegri, Dopchiz, Elissondo & Beveridge and Monoecocestus sp. Beddard (Cestoda: Anoplocephalidae) and for Heteroxynema (Cavioxyura) viscaciae Sutton & Hugot (Nematoda: Oxyuridae). The coprolites examined were tentatively attributed to Lagidium viscacia Molina (Mammalia, Rodentia, Caviomorpha, Chinchillidae). The life cycles of these parasites are discussed.     

Analysis of ancient DNA from coprolites: a perspective with random amplified polymorphic DNA-polymerase chain reaction approach

The aim of this work was to determine approaches that would improve the quality of ancient DNA (aDNA) present in coprolites to enhance the possibility of success in retrieving specific sequence targets. We worked with coprolites from South American archaeological sites in Brazil and Chile dating up to 7,000 years ago. Using established protocols for aDNA extraction we obtained samples showing high degradation as usually happens with this kind of material. The reconstructive polymerization pretreatment was essential to overcome the DNA degradation and the serial dilutions helped with to prevent polymerase chain reaction (PCR) inhibitors. Moreover, the random amplified polymorphic DNA-PCR has been shown to be a reliable technique for further experiments to recover specific aDNA sequences.     

The finding of eggs of Diphyllobothrium in human coprolites (4,100-1,950 B.C.) from northern Chile

Twenty six coprolites from an archaeological site in the province of Iquique, northern Chile, were examined for parasites. Coprolites were found in two excavation units, I and II (Tiliviche site), dated respectively at 5,900 B.C. to 4,110 B.C. and 4,110 B.C. to 1,950 B.C., and identified as of human origin. Only at the unit II coprolites containing helminth eggs identified as Diphyllobothrium pacificum were found. The presence of this tapeworm, a parasite of the American Sea Lion, in human coprolites, points to a diet which included marine fishes and provides information on the antiquity of infection by Diphyllobothrium pacificum. It is interesting to note that Baer (1969) suggests the presence of this tapeworm in pre-Columbian populations when diagnosing the first human cases in today's population in Peru.     

Syphacia sp. (Nematoda: Oxyuridae) in coprolites of Kerodon rupestris Wied, 1820 (Rodentia: Caviidae) from 5,300 years BP in northeastern Brazil

We present the results of paleoparasitological analyses in coprolites of Kerodon rupestris, rodent endemic to rocky areas of Brazil's semiarid region. The coprolites were collected from excavations at the archaeological site of Toca dos Coqueiros, in the National Park of Serra da Capivara, southeastern of state of Piauí. Syphacia sp. (Nematoda: Oxyuridae) eggs were identified in coprolites dated at 5,300 ± 50 years before present. This is the first record of the genus Syphacia in rodent coprolites in the Americas.     

家养食草动物粪便中的花粉及菌孢子类型及其对人类活动的指示意义

考古遗址中动物粪化石中的微体植物遗存是重建过去生态环境以及人类活动的重要材料,然而对于能够指示人类活动的粪化石孢粉组合类型及其特征仍然缺乏清楚的认识。本文研究了山羊(Capra aegagrus)、绵羊(Ovis aries)、牛(Bos taurus)、骆驼(Camelus)、牦牛(Bos grunniens)和马(Equus caballus)等几种中国常见的家养食草类动物粪便中的主要孢粉和真菌孢子类型。通过分析这些动物粪便的花粉组合特征,探讨了花粉和菌孢子等微体植物遗存对生态环境及人类活动的指示意义。花粉种类丰度低、一些特征种属花粉(如禾本科、藜科)含量高是家养食草类动物粪便花粉组合的主要特征,可以用于指示人类的饲养行为。家养食草动物粪便中的粪生真菌孢子类型主要有Sporormiella,Sodaria,Pleospora,Coniochaeta,Thecaphora and Dictyosporium。研究表明真菌孢子的分布主要受到动物活动范围的影响,这使得利用粪生菌孢子(如Sporormiella)并结合其他记录来反映人类的饲养或游牧活动成为可能。     

New record of anoplocephalid eggs (Cestoda: Anoplocephalidae) collected from rodent coprolites from archaeological and paleontological sites of Patagonia,Argentina

Results of paleoparasitological examination of rodent coprolites collected from archaeological and paleontological sites from Patagonia, Argentina, are present. Each coprolite was processed, rehydrated, homogenized, spontaneously sedimented and examined using light microscope. Coprolites and eggs were described, measured and photographed, and were compared with current faeces of Lagidium viscacia. Eggs with morphological features, attributed to an anoplocephalid cestode were found in samples collected from Cueva Huenul 1 (36°56′45″S, 69°47′32″W, Neuquén Province, Holocene) and Los Altares Profile (43º53′35″S, 68º23′21″W, Chubut Province, Late Holocene). These are the first findings of this anoplocephalid from faecal material from patagonic rodents.     

Trichuris sp. from 1,040 +/- 50-year-old Cervidae coprolites from the archaeological site Furna do Estrago, Pernambuco, Brazil

We present results of the paleoparasitological analysis of Cervidae coprolites that were recovered from the archaeological site Furna do Estrago, Pernambuco, Brazil. Trichuris sp. eggs were recovered from the coprolite samples dated 1,040 ± 50 years before present. This is the first record of Trichuris sp. in semiarid Cervidae, unexpectedly recorded in archaeological material.     

河南灵井许昌人遗址鬣狗粪化石的初步研究

河南灵井许昌人遗址是我国近年来发掘的最为重要的古人类遗址之一。该遗址中出土了大量的石器、骨器、动物化石、粪便化石等遗存以及人类头盖骨化石等。我们对该遗址出土的鬣狗粪化石进行了类型学及其包含的微体化石等方面研究,从分析统计结果来看,鬣狗粪化石中包含了丰富的古信息,如古寄生虫卵、动物毛发、孢粉、植硅体、真菌等。本文主要针对鬣狗粪化石中古寄生虫卵及动物毛发进行分析,探讨了作为寄主鬣狗罹患的寄生虫病,以及鬣狗的食物来源等情况,为深入理解更新世晚期人类适应环境与气候提供新的证据。     

SL1 RNA gene recovery from Enterobius vermicularis ancient DNA in pre-Columbian human coprolites

Enterobius vermicularis, pinworm, is one of the most common helminths worldwide, infecting nearly a billion people at all socio-economic levels. In prehistoric populations the paleoparasitological findings show a pinworm homogeneous distribution among hunter-gatherers in North America, intensified with the advent of agriculture. This same increase also occurred in the transition from nomad hunter-gatherers to sedentary farmers in South America, although E. vermicularis infection encompasses only the ancient Andean peoples, with no record among the pre-Colombian populations in the South American lowlands. However, the outline of pinworm paleoepidemiology has been supported by microscopic finding of eggs recovered from coprolites. Since molecular techniques are precise and sensitive in detecting pathogen ancient DNA (aDNA), and also could provide insights into the parasite evolutionary history, in this work we have performed a molecular paleoparasitological study of E. vermicularis. aDNA was recovered and pinworm 5S rRNA spacer sequences were determined from pre-Columbian coprolites (4110 BC-AD 900) from four different North and South American archaeological sites. The sequence analysis confirmed E. vermicularis identity and revealed a similarity among ancient and modern sequences. Moreover, polymorphisms were identified at the relative positions 160, 173 and 180, in independent coprolite samples from Tulán, San Pedro de Atacama, Chile (1080-950 BC). We also verified the presence of peculiarities (Splicing leader (SL1) RNA sequence, spliced donor site, the Sm antigen biding site, and RNA secondary structure) which characterise the SL1 RNA gene. The analysis shows that the SL1 RNA gene of contemporary pinworms was present in pre-Columbian E. vermicularis by 6110 years ago. We were successful in detecting E. vermicularis aDNA even in coprolites without direct microscopic evidence of the eggs, improving the diagnosis of helminth infections in the past and further pinworm paleoepidemiological studies.     

The state of the art of paleoparasitological research in the Old World

Paleoparasitology in the Old World has mainly concerned the study of latrine sediments and coprolites collected from mummified bodies or archaeological strata, mostly preserved by natural conditions. Human parasites recovered include cestodes, trematodes, and nematodes. The well preserved conditions of helminth eggs allowed paleoepidemiological approaches taking into account the number of eggs found by archaeological stratum. Tentatively, sanitation conditions were assessed for each archaeological period.     

Plant microfossil analysis of coprolites of the critically endangered kakapo (Strigops habroptilus) parrot from New Zealand

We present here the results of the analysis of pollen, spores, starch and other microscopic plant material in 52 coprolites of the critically endangered kakapo (Strigops habroptilus), a New Zealand endemic parrot. The six sampling sites (caves, rock overhangs) are in widely separate geographic regions in the South Island, across an altitudinal range encompassing lowland, montane and sub-alpine environments. Radiometric testing gives average ages of discrete coprolite groups ranging from modern to 2514 ± 43 ¹⁴C yr BP (Wk-19164). A wide variety of plant taxa is identified in the coprolites, comprising cones, flowers, leaves and fronds of ~ 30 podocarps, dicotyledonous trees, shrubs and lianas, grasses, ferns, lycopods, mosses and liverworts. This supports previous observations that kakapo are versatile feeders, using a broad spectrum of foods that may only be available for short periods and intermittent years. Many of the food taxa we identify are consistent with the studies of modern kakapo diet. We also identify several new foods, potentially of value in developing food supplements to increase breeding frequency of the current kakapo population. The most commonly identified plant parts in coprolites were fern fronds (monoletes, Hymenophyllum, Cyathea smithii), followed by podocarp cones and leaves. Lack of starch in the coprolites suggests that the lycopod and fern rhizomes reported in modern kakapo diet were not commonly eaten. The data provide initial botanical evidence of diet from coprolites of an extant bird.     

Ecological analysis of acari recovered from coprolites from archaeological site of northeast Brazil

Coprolite samples of human and animal origin from the excavations performed at the archaeological site of Furna do Estrago, at Brejo da Madre de Deus in the state of Pernambuco, Brazil and sent to the Paleoparasitology Laboratory at Escola Nacional de Saúde Pública-Fiocruz, Rio de Janeiro, were analyzed for mites. After rehydratation and sedimentation of the coprolites, the alimentary contents and the sediments were examined and the mites collected and prepared in definitive whole mounts, using Hoyer's medium. Mites of the following suborders and orders were recovered: suborder Acaridia; order Gamasida; order Ixodida with the familiy Ixodidae (Ixodes sp. and Amblyomma sp. larvae, scutum, idiosoma, gnathosoma); order Oribatida (Aphelacarus sp., Apolohmannia sp., Eophypochthonius sp., Cosmochthonius sp., Pterobates sp., Poronoticae with pteromorphae not auriculate); order Astigmata with the families Atopomelidae (Chirodiscoides caviae), Anoetidae hypopus, Acaridae (Suidasia pontifica), Glycyphagidae (Blomia tropicalis), Pyroglyphidae (Hirstia passericola); order Actinedida with the family Tarsonemidae (Iponemus radiatae). The present work discusses the possibility of the preservation of the mite groups found up to the present day. We also discuss their relationship with the environment and their importance to present populations.