Hyena Coprolites Research Articles

Middle Stone Age fauna from the RS sub-member (MSA I) at Cave 1B, Klasies River Main site, South Africa

Klasies River is an important site for the study of the evolution of Homo sapiens, understanding modern behaviour and human interaction with the environment during the Middle Stone Age. The faunal sample from the RS sub-member in Cave 1B (MSA I), dating to ca. 115 000 years ago and older, was recently analysed. The results indicate that humans were hunting a variety of prey. The most common taxa in the sample are indeterminate medium birds, indeterminate small mammals, rock hyraxes, and indeterminate medium mammals. Based on multiple lines of evidence including the presence of: cultural artefacts, shellfish, tortoises, large mammals, butchery marks, and burnt specimens; and, a lack of carnivore taxa compared to ungulates (as reflected in the low carnivore-ungulate ratio), hyena coprolites and beak damage, coupled with infrequent baboons and the absence of leopards (as reflected in the low leopard index), it is apparent that humans were the main agent of accumulation of the fauna. However, other agents of accumulation such as brown hyenas, leopards and raptors likely contributed some faunal remains, especially of smaller taxa.

Does size matter? Morphological and content analysis of the coprolites from a Quaternary deposit in the Iberian Peninsula

Coprolites are very abundant in Quaternary deposits. However, they are often overlooked despite offering insights into both the surrounding environment and the species that produced them, particularly when skeletal remains are absent. We selected a Quaternary cave deposit from the Iberian Peninsula, Juan Labranz Cave, where an abundant and diverse coprolite collection was recovered, in order to develop a non-destructive study method that allows an accurate interpretation of the producer. Morphometric analyses of these specimens reveal two distinctive morphotypes associated with the two main carnivore occupations in the cave, hyaenas and bears. Morphotype I resembles hyaena coprolites in shape, texture, and bone inclusions, suggesting spotted hyaena as the most likely producer based on size. On the other hand, morphotype II deviates significantly, with a wrinkled texture and larger size, resembling bear faeces when eating carrion. Differences in bone fragment size and the presence of hair moulds further support these attributions. In conclusion, this study underlines the importance of considering taphonomy, morphology, size, and content in identifying coprolite producers, also high- lighting the relevance of these ichnofossils as indirect evidence of species and for the understanding of their ecological roles in Quaternary environments, where humans and other predators coexist.

Balkan Neanderthals: The Late Pleistocene palaeoecological sequence of Pešturina Cave (Niš, Serbia)

The Central Balkans are a key biogeographical region in Southern Europe, influenced by a central European-Mediterranean climate, which acted as a refugium for flora and fauna, and favored the dispersion of Neanderthals and migration of modern human populations during Late Glacial Period. This study presents pollen analyses of sediment and hyaena coprolites from Pešturina Cave in Serbia to reconstruct the vegetation landscapes faced by Balkan Neanderthals and early Anatomically Modern Humans between MIS 5e-3. Between MIS 5e-5c (archaeological layers 4c and 4b) and MIS 5b-5a (layer 4a), semi-forested environments prevailed, characterized by Pinus, deciduous Quercus, Tilia and other angiosperm woody taxa, accompanied by heliophytes such as Artemisia and Poaceae. During MIS 4-3 (layers 3-2), the vegetation was dominated by Artemisia-Poaceae steppes with Quercus patches, conifers and legumes. Overall across the sequence, pollen assemblages are highly diverse and include a number of deciduous trees and sclerophylls. In addition, the occurrence of several herbaceous taxa reinforces the view that the Balkans were outstanding for endemicity. Neanderthals and early Upper Palaeolithic hominins lived in a highly diverse refugium, offering multiple opportunities for survival during the warm interstadials and, more critically, the cold stadials of the Pleistocene.

The first European woolly rhinoceros mitogenomes, retrieved from cave hyena coprolites, suggest long-term phylogeographic differentiation.

The woolly rhinoceros (Coelodonta antiquitatis) is an iconic species of the Eurasian Pleistocene megafauna, which was abundant in Eurasia in the Pleistocene until its demise beginning approximately 10 000 years ago. Despite the early recovery of several specimens from well-known European archaeological sites, including its type specimen (Blumenbach 1799), no genomes of European populations were available so far, and all available genomic data originated exclusively from Siberian populations. Using coprolites of cave hyenas (Crocuta crocuta spelea) recovered from Middle Palaeolithic layers of two caves in Germany (Bockstein-Loch and Hohlenstein-Stadel), we isolated and enriched predator and prey DNA to assemble the first European woolly rhinoceros mitogenomes, in addition to cave hyena mitogenomes. Both coprolite samples produced copious sequences assigned to C. crocuta (27% and 59% mitogenome coverage, respectively) and woolly rhinoceros (Coelodonta antiquitatis; 27% and 81% coverage, respectively). The sequences suggested considerable DNA degradation, which may limit the conclusions to be drawn; however, the mitogenomes of European woolly rhinoceros are genetically distinct from the Siberian woolly rhinoceros, and analyses of the more complete mitogenome suggest a split of the populations potentially coinciding with the earliest fossil records of woolly rhinoceros in Europe.

Fungal-induced fossil biomineralization

Exceptional preservation of fossils has often been attributed to the actions of bacteria that aid in the preservation of soft tissues that normally decay rapidly. However, it is well known that fungi play a major role in organic matter decomposition, biogeochemical cycling of elements, and metal-mineral transformations in modern ecosystems. Although the fungal fossil record can be traced back over a billion years, there are only a few recorded examples of fungal roles in fossilization. In this research, we have carried out a detailed geobiological investigation on early Pleistocene hyena coprolites (fossilized dung) in an attempt to ascertain possible fungal involvement in their formation. Using an advanced microscopic and mineralogical approach, we found that numerous hydroxyapatite nanofibers (25-34nm on average), interwoven to form spheroidal structures, constituted the matrix of the coprolites in addition to food remains. These structures were found to be extremely similar in texture and mineral composition to biominerals produced during laboratory culture of a common saprophytic and geoactive fungus, Aspergillus niger, in the presence of a solid source of calcium (Ca) and phosphorus (P). This observation, and our other data obtained, strongly suggests that fungal metabolism can provide a mechanism that can result in fossil biomineralization, and we hypothesize, therefore, that this may have contributed to the formation of well-preserved fossils (Lagerstätten) in the geological record. The characteristic polycrystalline nanofibers may also have served as a potential biosignature for fungal life in early Earth and extraterrestrial environments.

Evidence of Toxocara Eggs in Pachycrocuta brevirostris (Gervais, 1850) Coprolites from the Pleistocene of Taurida Cave (Crimea).

Coprolites of the hyena Pachycrocuta brevirostris from the Lower Pleistocene (Upper Villafranchian) of Taurida Cave (Crimea) were studied. One of the three hyena coprolites contained helminth eggs. These eggs were assigned to Toxocara sp. based on their size and morphology. Toxocariasis was evidently a very common infestation among extinct hyena species. The find of toxocara in P. brevirostris coprolite from the Taurida Cave is the earliest evidence of roundworm infestation in P. brevirostris.

Taphonomy of an excavated striped hyena (Hyaena hyaena) den in Arabia: implications for paleoecology and prehistory

Studies of modern carnivore accumulations of bone (i.e., neo-taphonomy) are crucial for interpreting fossil accumulations in the archaeological and paleontological records. Yet, studies in arid regions have been limited in both number and detailed taphonomic data, prohibiting our understanding of carnivore bone-accumulating and -modifying behavior in dry regions. Here, we present a taphonomic analysis of an impressive carnivore-accumulated bone assemblage from the Umm Jirsan lava tube in the Harrat Khaybar region, Saudi Arabia. The size and composition of the bone accumulation, as well as the presence of hyena skeletal remains and coprolites, suggest that the assemblage was primarily accumulated by striped hyena (Hyaena hyaena). Our findings (1) identify potentially useful criteria for distinguishing between accumulations generated by different species of hyenas; (2) emphasize the need for neo-taphonomic studies for capturing the full variation in carnivore bone-accumulating and modifying behavior; (3) suggest that under the right settings, striped hyena accumulations can serve as good proxies for (paleo)ecology and livestock practices; and (4) highlight the potential for future research at Umm Jirsan, as well as at the numerous nearby lava tube systems. We encourage continued neo-taphonomic efforts in regions important in human prehistory, particularly in arid zones, which have received little research attention.

Dermestid pupal chambers on Late Pleistocene faunal bones from Cava Muracci (Cisterna di Latina, central Italy): Environmental implications for the central Mediterranean basin during MIS 3

Cava Muracci (Cisterna di Latina, central Italy) is a complex of seven karst caves located in the Pontine Plain region. One of them, denominate Area 3, displayed a well-preserved Late Pleistocene deposit dating from 35 ka BP and older containing abundant mammal remains and cave hyena coprolites. This work presents the recent discovery from this deposit of fossil bones exposing dermestid pupal chambers and the opportunity these offered to support and improve, with high-resolution inferences, a previous environmental reconstruction based on faunal assemblage and pollen from coprolites. Moreover, ichnological analyses also shed light on some of the post-depositional agents which affected remains within the cave. This paper encourages the valuable support of palaeoichnology, a little exploited and undervalued discipline, to archaeological and palaeoenvironmental studies.

Late Quaternary palaeoenvironments in the central semi-arid region of South Africa from pollen in cave, pan, spring, stream and dung deposits

We have reassessed the palynological record of Equus Cave in the Savanna Biome of the southern Kalahari, one of the longest Late Quaternary pollen records for the semi-arid central interior of South Africa. We combined published pollen results from the cave, derived from hyena coprolites and the rubified deposits in which they occur, into a single sequence. By re-considering the chronology of this sequence, we critically evaluated the palaeoenvironmental record for the site. We compared the pollen evidence from Equus Cave to that from the longer Wonderwerk Cave records (stalagmite, sediments and dung), also located in the Savanna Biome. Then, we contrasted Equus and Wonderwerk records with other previously published pollen sequences derived from a range of sources from several sites in central South Africa. These sites follow a broad northwest to southeast transect of c. 500 km through the Grassland and Nama Karoo Biomes of the Free State and Eastern Cape. Applying Principal Components Analysis to the pollen data, we derived climatic signals at a regional scale to refine reconstructions of Late Quaternary changes for central South Africa.

Palynology and chronology of hyaena coprolites from the Piñar karstic Caves Las Ventanas and Carihuela, southern Spain

This paper presents pollen analyses and radiocarbon dating on Crocuta coprolites from Las Ventanas (LV) and Carihuela (Car) Caves in southern Spain (Granada), with the aim of reconstructing the environmental conditions of these hominin sites. The LV coprolites are radiocarbon dated from c. 37,890 to 6980 cal yr BP, and the Car coprolites from c. 31,063 to 7861 cal yr BP. Overall, the palaeoecological scenario inferred from both coprolite series display similar patterns, with Pinus, Poaceae, and Artemisia as dominant during the full Pleistocene, and an important contribution of Quercus in the most recently dated coprolite samples. While the palynology is consistent with results of former investigations on the past environments in the region as obtained from other deposits (peat bogs, cave infills), the Late Glacial and Holocene chronology of several coprolites in both sites is in conflict with the generally accepted timing of extinction of Crocuta in western Europe. A discussion on the taphonomical processes and potential sources of carbon contamination of the radiocarbon samples is provided. The correlation between pollen from coprolites and from sedimentary records, and the paucity of the fossil bone record suggests nevertheless, that a late survival of Crocuta in southern Spain should not be categorically discarded.

До методики палеогеографічного вивчення відкладів карстових печер України

New approaches developed within the complex palaeogeographic methodology of cave deposits studies for reconstruction of the past ecological conditions are presented in the paper. The relevance and reliability of results of such studies are shown on the cases from the previous research of cave systems in Ukraine. The methodology based of palynological and lithological (including grain-size analysis) study of terrigenous cave deposits is proposed, and the advantages of their complex application within the multidisciplinary palaeoenvironmental study are proved. The reliability of palaeovegetational reconstructions based on pollen studies of clastic cave deposits is confirmed by the compatibility of their results with those obtained from coeval subaerial deposits. The same patterns were shown by a comparison of pollen from hyaena coprolites in the cave and their enclosing sediments. It has been found that the content of redeposited pollen in the clastic sediments of caves depends on their particle size distribution, sharply increasing in sandy deposits. The grain-size composition of cave deposits also provides information on the genesis of deposits and, thus, indirectly, on paleoenvironmental conditions. Changes in clay, large silt and sand fractions are of main importance for the interpretation of the results. A direct correlation of paleoclimatic signals obtained by the results of pollen and lithological analyses with the indicators of magnetic susceptibility has been established. The use of these paleogeographic methods for studying cave deposits, namely pollen analyses, lithological (in particular, grain-size), palaeontological, petromagnetic, palaeogenetic, radiocarbon and paleomagnetic methods, will be able to control the reliability of the reconstruction by collate them. Multidisciplinary study of the cave deposits has a great potential for reconstructions of the ancient Man environments as deposits of many caves include archaeological horizons of different material cultures from the Early Palaeolithic to the Early Iron Age.

Hyena hegemony: biogeography and taphonomy of Pleistocene vertebrate coprolites with description of a new mammoth coprolite ichnotaxon

In 1822, William Buckland first recognized Pleistocene vertebrate coprolites, and they are now known from more multiple localities with a global distribution. Carnivore coprolites dominate, and there are two distinct biogeographic and taphonomic provinces for vertebrate coprolites in the Pleistocene. The Castrocopros province of North and South America is characterized by a dominance of herbivore coprolites, which are preserved almost exclusively in caves. The Hyaenacoprus province in Africa, Europe and Asia is dominated by hyena coprolites that occur mainly in caves, but also in other depositional environments. Pacific Islands may represent a third province characterized by dominant bird coprolites from caves, but the known localities are all Holocene. Mammuthocopros allenorum ichnogen. and ichnosp. nov. is a coprolite of Mammuthus columbi from Utah, USA.

The Late Pleistocene faunal assemblage from Cava Muracci (Latium, Italy): Palaeoenvironmental implications for coastal central Italy during MIS 3

Palaeoenvironmental information on Marine Isotope Stage 3 (MIS 3) coastal Latium is sparse, mainly based on studies of isolated faunal assemblages or long pollen records from lake sediments, often of insufficient resolution to aid in palaeoenvironmental reconstruction. This study describes in detail the Late Pleistocene faunal assemblage from layers SU11 and SU12 of Cava Muracci (Cisterna di Latina, central Italy), the first of which is a partially-preserved hyena den. The first multi-disciplinary palaeoenvironmental reconstruction of coastal Latium between 34–44 ka BP, a critical time span for the presence of the latest Neanderthals and the arrival of Anatomically Modern Humans (AMH), is provided combining palaeoecological inferences from a previous pollen study of hyena coprolites with the palaeontological study described here. The results indicate a temperate climate and a landscape characterised by the coexistence of at least three habitats within a short distance between the coastline and the inland mountains, suitable for a wide variety of species.

Last Neanderthals in the warmest refugium of Europe: Palynological data from Vanguard Cave

This paper presents pollen analyses on hyaena coprolites from Vanguard Cave, Gibraltar, with the aim of depicting the vegetation landscapes of the southern Iberian Neanderthals during the MIS 3. The Palaeolithic vegetation in the surroundings included pine, oak, juniper, Pistacia, and mixed woodlands, savannahs, riverine forest patches, heliophytic matorrals, rocky scrub with chamaephytes and hemicryptophytes, grasslands with heaths, shrubby grasslands, steppe-like saltmarshes, and littoral vegetation. We compare our results to those of previous palaeobotanical study in the adjacent Gorham's Cave providing data for the MIS 3 and MIS 2. Placing the palaeobotanical records of Vanguard and Gorham's Caves in European context, the southern coasts of Iberia emerge as the most thermic refugium of the Late Quaternary, which has important implications for existing arguments about the long survival of Neanderthals in the Iberian Peninsula.

Hyena as a predator of small mammals? Taphonomic analysis from the site of Bois Roche, France

AbstractFeeding behaviors may differ between past and current predators due to differences in the environments inhabited by these species at different times. We provide an example of this behavioral variability in spotted hyena (Crocuta crocuta), for which our analysis of a late Pleistocene micromammal assemblage indicates that hyenas preyed upon small rodents, a feeding habit that is rarely observed today among hyenas.The Bois Roche cave site is situated at the edge of a low bluff overlooking the floodplain of a small stream in Cherves-Richemont (Charente, France). The deposits are dated by electron spin resonance (ESR) to about 69.7 ± 4.1 Ka. Excavations at the site recovered fossil bones and teeth of large and small mammals, together with hyena coprolites. Water screening of the sediments produced large accumulations of rodent remains with low taxonomic diversity. Small mammal bones were recovered from hyena coprolites as well. Descriptions of small mammal bone modification, both from the sediments and coprolites, are reported here. The analysis yielded a distinct taphonomic pattern representative of large carnivores (over 30 kg), which differs from any other modern or fossil predator-accumulated microfaunal assemblage taphonomically analyzed to date. To our knowledge, previous studies of hyena diet have not recorded high concentrations of a single-rodent prey species. We conclude that the low species diversity of this small mammal assemblage most likely relates to a local abundance of the prey species due to an outbreak in the rodent population, rather than from specialist predator behavior and hunting technique.

Late Pleistocene and Holocene environmental changes recorded in deposits of the Bukovynka Cave (the East-Carpathian foreland, Ukraine)

A study of pollen, fossil mammals and lithology (including grain-size analysis) of the terrigenous deposits in the Bukovynka Cave enables the reconstruction of the environments of several geochronologic subdivisions of the Middle Pleniglacial, Late Glacial and Holocene. A comparison of pollen assemblages in surface samples from the cave deposits and from the soils prove the importance of cave palynology for palaeovegetation reconstruction. The same patterns were shown by a comparison of pollen from hyaena coprolites in the cave and their enclosing sediments. In the Trapeznyi Chamber record, the two interstadials and one stadial identified are correlated with those of the Moershoofd interval, and the following stadial (after 41,000 yrs BP) is compared with the Hosselo stadial of Western Europe. In the Sukhyi Chamber record, Late Glacial times (around 10,700 yrs BP) differed from the Holocene in having a much harsher climate (with the spread of boreal forest). During the Holocene, a relatively wet phase, transitional from Atlantic to Early Subboreal, was separated from the similar phase of the Late Subboreal (2800 yrs BP) by a drier Middle Subboreal (with the disappearance of water-loving trees and the existence of steppe rodents). The Subatlantic was the wettest time, with culmination of a broad-leaved flora in the Roman (2300–1800 yrs BP) and Medieval (1000 yrs BP) Warm Periods. The cultivation of Cerealia started from 2800 yrs BP, and forest clearances increased after the Medieval Warm Period.

Characterizing hyena coprolites from two latrines of the Iberian Peninsula during the Early Pleistocene: Gran Dolina (Sierra de Atapuerca, Burgos) and la Mina (Barranc de la Boella, Tarragona)

Coprolites are commonly identified in the Pleistocene archaeo-palaeontological record. They have often been described as indirect evidence for the presence of carnivores (usually hyenids) during the formation of a depositional sequence. However, coprolites are a much larger source of information that can provide data relating to factors affecting an archaeological assemblage, including its taphonomic history and palaeoecology. In this paper, two fossil coprolite accumulations dating to the late Early Pleistocene are described: Level TD6.1 of Gran Dolina (Sierra de Atapuerca, Burgos) and Unit II of la Mina (Barranc de la Boella, Tarragona). The results highlight the morphological homogeneity of these hyena coprolites, despite a considerable variation in size. The presence of microspherulites is clearly identified in all of the analysed hyena coprolites. Their composition is rich in elements characteristic of bone-origin, such as calcium (Ca) and phosphorus (P). A major difference, however, differentiating the remains from these sites was a higher frequency of bone fragments in the la Mina coprolites, regarding to TD6.1. Pollen, spores, and palynomorphs are scarce in the samples from both sites, which in fact share similar ecological characteristics such as the presence of pine, wild grasses, and coprophilous fungi. Hyena coprolites are relatively easy to differentiate from those of other taxa; however, they show intra-specific similarities in their micro- and macro-morphology and composition, despite their wide size range. The species of hyenids responsible for the coprolites is not possible to identify based exclusively on the size range, and the importance of a multidisciplinary study of the latrines and the coprolites is discussed as a source of palaeoecological and taphonomic information. In this study, coprolites are analysed, compared, and attributed to a hyenid, identified as Crocuta crocuta in the case of TD6.1, but without specific attribution in the case of la Mina.

Pollen from Late Pleistocene hyena (Crocuta crocuta spelaea) coprolites: An interdisciplinary approach from two Italian sites

Palynology of fossil faeces is still extremely rare and its contribution to the interpretation of the environment undervalued. In this paper we present the results of pollen analysis performed on cave hyena coprolites [Crocuta crocuta spelaea (Goldfuss, 1832)] from Marine Isotope Stage 3 (MIS 3) sites of Cava Muracci (Cisterna di Latina, central Italy) and Tana delle Iene (Ceglie Messapica, southern Italy). This study provides new insights into the vegetation of the Late Pleistocene of peninsular Italy, until now known only through long pollen records. It also shows how the content of coprolites, combined with faunal data and geochronological investigations, can represent a potential integrative source of palaeoclimatic proxy data. Our results indicate that the surroundings of both of the hyena dens were characterised by a patchy landscape with open lowlands dominated by steppe and grassland vegetation, while a few mesophilous and thermophilous trees were present in more humid areas, probably along the marine coast and inland. The harsh glacial climate appears to have been milder at Cava Muracci than at Tana delle Iene. This could be due either to the different environmental features of the two sites or to the high climatic variability that occurred during MIS3.

A spotted hyaena den in the Middle Palaeolithic of Grotta Paglicci (Gargano promontory, Apulia, Southern Italy)

The Palaeolithic sequence of Grotta Paglicci (Gargano promontory, Apulia, Southern Italy) is one of the most important in the Mediterranean area: It comprises the whole Upper Palaeolithic cultural sequence known for the region, as well as Early Middle Palaeolithic and Lower Palaeolithic levels. These earlier phases are best represented in a collapsed room located outside the present-day cave (the so called “external rock shelter”). In this area, a new excavation, started in 2004, brought to light Middle Palaeolithic animal remains associated with evidence of spotted hyaena (SU 64 and 53). The spatial distribution analysis of remains from SU 53 revealed the presence of a bone accumulation area and a wider dispersal of hyaena coprolites. Three main ungulate species (aurochs, fallow deer and red deer) as well as carnivores (spotted hyaena, wolf, fox, wild cat and lynx) and lagomorphs have been identified. The majority of aurochs remains are located in the main accumulation; among these specimens, a complete metatarsal connected with three tarsal bones has been found; a talus and a complete tibia, probably belonging to the same limb, have also been identified. The multidisciplinary study carried out in this paper highlights a specific bone accumulation and scattering pattern in a spotted hyaena (Crocuta crocuta) den. In addition, taphonomy of lagomorph remains indicates the presence of other depositional agents.

Taphonomy of the reference Miocene vertebrate mammal site of Cerro de la Garita, Spain

This article reports a detailed taphonomic study of the reference Miocene vertebrate site of Cerro de la Garita, (Concud, Teruel, Spain). The sedimentary record of the site indicates that it was a palaeo-lakeshore, and this conclusion is supported by aquatic environment-related taphonomic modifications of its fossils (both on their surfaces and internally). The site provided a water source that appears to have been regularly visited by herbivores. It was, therefore, also likely to have been a good feeding ground for predators and scavengers. Hyaena coprolites have been found at the site, and tooth marks were identified on some fossil bone surfaces. Bone fragments 2–5 cm in length showed clear evidence of heavy digestion and probable regurgitation. Abundant trampling marks were seen on the surface of many of the fossil bones, traits that are congruent with a damp lakeshore environment. Most of the remains were broken, and only a few anatomical elements belonging to the same individual were found close together, although never articulated (i.e. in a manner reflecting their anatomical connections). The fossils showed no signs of selection (either by shape or size) or abrasion, although a certain re-orientation suggests the influence of wave or strand line activity. Despite being an open-air site, none of the fossils appeared to be weathered, further suggesting that the surrounding environment was a damp lakeshore probably shaded by vegetation. Indeed, abundant signs of root activity were observed. No evidence of reworking, that is, post-burial disturbance or diachronic mixing of fossils, was seen, confirming the international value of Cerro de la Garita as a reference site for continental Miocene mammal assemblages.