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.     

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.     

Helminth eggs in animal coprolites from a Middle Pleistocene site in Europe

This paper reports on the discovery of dicrocoelid eggs in a coprolite collected in an archeological layer dated earlier than 550,000 yr BP (before present) from the Caune de l'Arago cave (Tautavel, Pyrénées-Orientales, France). It is the first trematode egg finding in an isolated coprolite from the Middle Pleistocene context.     

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.     

Methodological innovations for the study of irreplaceable samples reveal giardiasis in extinct animals (Nothrotherium maquinense and Palaeolama maior)

The use of diagnostic methods that prevent irreplaceable samples (from museum collections, archaeological and paleontological samples) of being consumed or that increase their yield is relevant. For museum collections, archaeological and paleontological samples it is essential to conserve samples, subsamples or portions for future research. We are addressing methods for conservation of irreplaceable samples that could be fully consumed. Innovations in methodologies that are used in studies of Paleoparasitology and Paleomicrobiology will contribute to the preservation of collections. Therefore, to the development of archaeology and paleontology in the future, we evaluated whether the discarded material of the immunochromatography test could be used for molecular diagnosis and vice versa. We used a genotyped experimental coprolite positive for Giardia duodenalis. The diagnosis was positive for giardiasis in both cases. This methodology can be corroborated with the coprolite of a Paleolama maior (extinct llama) previously diagnosed for G. duodenalis with an immunoenzymatic test. The residue of the pre-digestion step of the DNA extraction before adding Proteinase K was confirmed positive with the immunochromatographic test. Also, the DNA extraction residue from a coprolite of Nothrotherium maquinense (ground sloth) was tested positive with immunochromatographic test for G. duodenalis. These are the oldest findings for G. duodenalis confirming that this intestinal parasite occurred among Northeastern Brazilian Megafauna animals from the late Pleistocene period, correlated to human occupation. The relevance of these results will allow the study by different methodological approaches from a small amount of material, reusing discarded materials.     

Paleoparasitological analysis of coprolites from K2, an Iron Age archaeological site in South Africa: the first finding of Dicrocoelium sp. eggs

Until now, Dicrocoelium sp. eggs have only been recorded from European and 1 North American archaeological sites. We present evidence for the first record of Dicrocoelium sp. from an African archaeological site. A paleoparasitological study was conducted on 7 coprolite samples from K2, a Late Iron Age site on the farm Greefswald, in the Northern Province of South Africa. Standard parasitological analysis revealed the presence of Dicrocoelium sp. and Trichuris sp. eggs. Today, the parasite does not occur in this region. Trichurid eggs are a relatively common find in paleoparasitological analysis. The presence of Dicrocoelium sp. provides new clues about the antiquity of this parasite, as well as aspects of ancient environment, climate, and interactions among humans, animals, and parasites.     

Tapeworm Eggs in a 270 Million-Year-Old Shark Coprolite

Remains of parasites in vertebrates are rare from the Mesozoic and Paleozoic. Once most parasites that live in – or pass through – the gastrointestinal tract of vertebrates, fossil feces (coprolites) or even intestinal contents (enterolites) can eventually preserve their remains. Here we announce the discovery of a spiral shark coprolite from the Paleozoic bearing a cluster of 93 small oval-elliptical smooth-shelled structures, interpreted as eggs of a tapeworm.The eggs were found in a thin section of an elasmobranch coprolite. Most of the eggs are filled by pyrite and some have a special polar swelling (operculum), suggesting they are non-erupted eggs. One of the eggs contains a probable developing larva. The eggs are approximately 145–155 µm in length and 88–100 µm in width and vary little in size within the cluster. The depositional and morphological features of the eggs closely resemble those of cestodes. Not only do the individual eggs have features of extant tapeworms, but their deposition all together in an elongate segment is typical to modern tapeworm eggs deposited in mature segments (proglottids). This is the earliest fossil record of tapeworm parasitism of vertebrates and establishes a timeline for the evolution of cestodes. This discovery shows that the fossil record of vertebrate intestinal parasites is much older than was hitherto known and that the interaction between tapeworms and vertebrates occurred at least since the Middle-Late Permian.     

Cryptosporidium,Giardia, and Cyclospora in ancient Peruvians

Twenty-two coprolites of human origin, collected from excavations along the north-central coast of Peru, were examined using fluorescent microscopy for the presence of fecal parasites, with emphasis on Cryptosporidium sp., Giardia sp., and Cyclospora sp. Three samples were positive. One coprolite dated between ca. 2,375 and 1,525 BC contained Giardia sp. cysts. This coprolite corresponded to the Peruvian preceramic period. Another positive coprolite ca. AD 770-830 corresponded to Epoch 3 of the Middle Horizon and contained Cryptosporidium sp. oocysts. The third positive coprolite (corresponding to the Middle Horizon. ca. AD 500-900) contained Giardia sp. cysts. This report demonstrates that Giardia sp. and Cryptosporidium sp. were present in Peruvian coastal populations for at least 4,300 and 1,100 BP.     

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.     

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.     

Gar-Bitten Coprolite From South Carolina,USA

Coprolites can preserve a wide range of biogenic components. Of all the coprolites known from the fossil record, hitherto only two are known to preserve vertebrate tooth impressions (i.e., those of chondrichthyans). Here, a coprolite, from a thick lag deposit that includes a mixture of late Cretaceous, early Paleocene, and Plio-Pleistocene taxa at Clapp Creek in Kingstree, Williamsburg County, South Carolina, USA, preserves bite marks most consistent with having been made by a gar, Lepisosteus sp. (Lepisosteidae, Actinopterygii). This is the first-known coprolite to preserve actinopterygian tooth/bite marks. Aborted coprophagy seems unlikely; an accidental or serendipitous strike more likely describes the origin of the score marks over the surface of the coprolite. This coprolite also preserves small paired striations interpreted as evidence of coprophagy by an unknown organism.     

Applying modern analogs to understand the pollen content of coprolites

Most scientists working with coprolites from archaeological contexts assume that human fecal specimens reflect the mixing of the pollen ingested during the period in which the contribution to the coprolite, 19 to 37.5 h, was ingested, that the amount of pollen in a fecal sample directly reflects the amount of pollen originally ingested during that interval, and that differences between the amounts of pollen in different fecal specimens reflect differences in the quantities of pollen ingested at different times. These assumptions were tested and found wanting in an experiment in which two persons sequentially ate separate quantities of 15 pollen types in meals over a four-day interval. The pollen was retrieved and analyzed from feces produced during those four days and five days of subsequent fecal production. Pollen ingested first appeared in relatively small amounts, usually the day after it was ingested. Its concentration per gram of sample then increased rapidly and remained high over a one to three day interval relative to the amounts in previous and subsequent fecal specimens deposited. When pollen concentrations declined some pollen was retained in the gastrointestinal system and much lower concentrations per gram of sample of each type continued to appear in fecal samples for several days. These relatively low pollen concentrations appeared in fecal samples approximately twice as often as did higher concentrations. Our results indicate that comparatively high pollen concentrations can be used to determine that a given pollen type was ingested, but comparisons between pollen concentrations of the same pollen type in different fecal specimens or between different pollen types in the same fecal specimen, cannot be used to determine whether different amounts of pollen were ingested, or what was the relative amount of each ingested. Because pollen concentrations per gram of sample varied widely with time since ingestion, percentages of given pollen types did not occur in predictable patterns and could actually increase as the concentration of the pollen type decreases. Hence, percentages should not be used in coprolite pollen analysis. The experimental results also suggest that variations in the pollen content of different portions of a coprolite are meaningful only in terms of the overall pattern of a sequential group of coprolites.     

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.     

Insights about echinostomiasis by paleomolecular diagnosis

Echinostomiasis is a zoonosis caused by intestinal trematodes and transmitted by the ingestion of mollusks, crustaceans, fish, amphibians, and reptiles, either raw or poorly cooked. Today human infection is endemic in Southeast Asia and the Far East, but has been reported more recently in other regions of the world. Interestingly eggs identified as Echinostoma sp. were found in coprolites from a mummified body human in Brazil, dated 560 ± 40 BP (before present). However, the specific diagnosis based on morphology of the eggs has not been resolved at the species level. As a follow-up to the previous finding, the current study now aims to standardize the methodology for molecular diagnosis and apply it to the coprolite, using current Echinostoma paraensei-positive feces as the reference, and also the same fecal material dried in a stove as an experimental coprolite model. Isolated eggs of E. paraensei and adult worm were included to verify the sensibility and as positive control, respectively. An adult worm of E. luisreyi was used for comparison. PCR using primers in-house for ITS1 region (126 bp) and cox1 (123 bp) of Echinostoma spp. and subsequent nucleotide sequencing were performed. This is the first molecular paleoparasitological diagnosis for echinostomiasis. The methodology was able to amplify specific DNA fragments for the genus Echinostoma sp. in all samples: adult worm, feces, and a single egg of the parasite, in both the experimental coprolite and archaeological sample. Additionally we observed that ancient DNA can also be retrieved without rehydrating the material. The nucleotide sequences from E. paraensei and E. luisreyi are very similar in the fragment analyzed that difficult the differentiation these species, but DNA sequence analysis recovered in the parasite found in the mummy showed more similarity with the species E. paraensei.     

The steroids of 2000-year-old human coprolites.

Six samples of human coprolites, some more than 2,000 years old, were analyzed for fecal steroid composition. Despite this very lengthy period of storage, the fecal steroids of coprolites were remarkably similar to those of stool samples collected today. The sterol nucleus was clearly rather stable under the dry environmental conditions of the Nevada Caves. The steroid content (microgram/g dried weight) of coprolite was low in comparison to that of modern man. The bile acid/cholesterol and plant sterol/cholesterol ratios of the coprolite, however, were similar to these ratios of the stools of modern man. In the six coprolites, an average 73% of the neutral steroids was digitonin-precipitable. This precipitate was composed of cholesterol and three plant sterols (campesterol, stigmasterol, and beta-sitosterol) and their bacteria-modified products. A portion of the neutral steroids had been converted to products tentatively identified as epimers of these steroids. Individual bile acids were identified in the coprolite. The bile acid composition of the coprolite was similar to that of the stool of modern man.     

A new actinomycete from a Guadalupian vertebrate coprolite from Brazil

Coprolites (fossil feces) are important sources of evidence of ancient food webs and ecosystems. Actinomycetes are a fundamental component in the decay of organic matter, and serve as catalysts for nutrient cycles. Recently, gas vesicles filled with numerous verrucose colonies of substrate mycelium of an actinomycete were discovered inside a fossilized spiral amphipolar fish coprolite recovered from mid–Permian deposits of Brazil. These colonies are composed of masses of substrate hyphae, some of which are undergoing segmentation. Arising from the colonies are chains of spores separated by narrow, elongate connectives. The fossil actinomycete is described below as Palaeostromatus diairetus gen. et sp. nov. and represents the oldest known actinomycete associated with vertebrate deposits. Since the colonies occur only inside the coprolite, either Palaeostromatus diairetus gen. et sp. nov. was part of the gut flora or it was acquired from a food source. The only other remains in the coprolite are eighteen paleoniscoid fish scales, which suggests that the producer was a carnivorous/omnivorous fish. This is the oldest record of a direct interaction between vertebrates and actinomycetes.     

Paleoparasitological Surveys for Detection of Helminth Eggs in Archaeological Sites of Jeolla-do and Jeju-do

A paleoparasitological survey to detect helminth eggs was performed in archaeological sites of Jeolla-do and Jeju-do, the Republic of Korea. Total 593 soil samples were collected in 12 sites of Jeolla-do and 5 sites of Jeju-do from April to November 2011, and examined by the methods of Pike and coworkers. A total of 4 helminth eggs, 2 eggs each for Trichuris trichiura and Ascaris sp., were found in soil samples from 1 site, in Hyangyang-ri, Jangheung-eup, Jangheung-gun, Jeollanam-do. The egg-recovery layer was presumed to represent a 19th century farm, which fact suggested the use of human manures. This is the third archaeological discovery of parasite eggs in Jeolla-do. Additionally, no helminth eggs in archaeological sites of Jeju-do is an interesting problem to be solved in the further investigations.     

Turtle Shell Impression in a Coprolite from South Carolina,USA

Coprolites (fossilized feces) can preserve a wide range of biogenic components. A mold of a hatchling turtle partial shell (carapace) referable to Taphrosphys sulcatus is here identified within a coprolite from Clapp Creek in Kingstree, Williamsburg County, South Carolina, USA. The specimen is the first-known coprolite to preserve a vertebrate body impression. The small size of the turtle shell coupled with the fact that it shows signs of breakage indicates that the turtle was ingested and that the impression was made while the feces were still within the body of the predator. The detailed impression could only have survived the act of defecation if the section of bony carapace was voided concurrently and remained bonded with the feces until the latter lithified. Exceptionally, the surface texture of the scutes is preserved, including its finely pitted embryonic texture and a narrow perimeter of hatchling scute texture. The very small size of the shell represented by the impression makes it a suitable size for swallowing by any one of several large predators known from this locality. The coprolite was collected from a lag deposit containing a temporally mixed vertebrate assemblage (Cretaceous, Paleocene and Plio-Pleistocene). The genus Taphrosphys is known from both sides of the Cretaceous–Paleogene (K–Pg) boundary so, based on the size of the coprolite and the locally-known predators, the juvenile turtle could have been ingested by a mosasaur, a crocodylian, or a theropod dinosaur. Unlike mosasaurs and theropod dinosaurs, crocodylian stomachs have extremely high acid content that almost always dissolves bone. Therefore, the likely predator of this turtle was a mosasaur or a (non-avian or avian) theropod dinosaur.     

Microbiota and food residues including possible evidence of pre‐mammalian hair in Upper Permian coprolites from Russia

Coprolites (fossil faeces) provide direct evidence on the diet of its producer and unique insights on ancient food webs and ecosystems. We describe the contents of seven coprolites, collected from the Late Permian Vyazniki site of the European part of Russia. Two coprolite morphotypes (A, B) contain remains of putative bacteria, cyanobacteria, fungi, protists, invertebrate eggs, arthropod elements, undigested bone and tooth fragments, fish scales and elongated hair‐like structures with hollow interiors. Content, size and shape of the coprolites together with the associated body fossil record suggest that the most probable scat‐producers were carnivorous tetrapods; the bone‐rich morphotype A reveals short food retention time and a fast metabolism and is therefore assigned to therapsid carnivores whereas morphotype B with rarer and degraded bones are assigned to archosauromorphs or other non‐therapsid carnivores. The general coprolite matrix contains abundant micron‐sized spheres and thin‐walled vesicles which are interpreted as oxide and phosphatic pseudomorphs after microbial cells. From analyses of the undigested bones, we infer that they represent remains of actinopterygian fish, a therapsid and unrecognizable parts of amphibians and/or reptiles. Additionally, hair‐like structures found in one coprolite specimen occur as diagenetically altered (oxide‐replaced) structures and moulds (or partly as pseudomorphs) in a microcrystalline carbonate‐fluoride‐bearing calcium phosphate. This suggests that the latest Permian therapsids probably were equipped with hair‐like integument or hairsuit. If true, this is by far the oldest evidence of this mammalian character in the stem group of mammals.     

中国宝鸡关桃园新石器遗址中发现的金丝猴头骨及其意义

关桃园遗址位于陕西宝鸡市陈仓区(原宝鸡县,2004年改制)西部深山区拓石镇关桃园村(34°30′N,106°29′E),该村坐落于渭河东北岸一块发育较良好的黄土台地北部,北依骆驼山,南临渭河及西秦岭群峰,东距宝鸡市83km。2002年为配合宝(鸡)—兰(州)铁路二期工程建设,陕西省考古研究所和宝鸡市考古工作队组成联合考古队,从1月至8月底对该遗址进行较大规模的科学发掘,发现了极其丰富的前仰韶时期文化、部分仰韶及周代遗存等(陕西省考古研究所和宝鸡市考古工作队,2006)。根据遗迹之间的打破关系和陶器形制变化的特征,遗存自上而下分为西周文化(Ⅵ期)…