Stable isotopes and the metabolism of the European cave bear

Isotopic analyses of fossil bones of the extinct European cave bear indicate that this animal was a hibernator with the same unusual metabolic processes as some modern bear species. This finding provides useful biological and archaeological information on an extinct species, and the methods themselves may prove generally useful in studies of the metabolisms of modern bears, other hibernators, and perhaps of starving animals. Received: 6 October 1997 / Accepted: 31 March 1998     

The story continues: recent advances on the life and death of the Pleistocene cave bear

ABSTRACT

In this issue, we cover an exceptional topic in Vertebrate Paleobiology that has been an enjoyable challenge for scientists and the popular media alike: the life and death of the Pleistocene cave bear (Ursus spelaeus). As an icon of the ice-age, the cave bear inhabited the glacial ecosystems of Eurasia, and it was the inspiration of a popular book written in 1976 by Björn Kurtén, entitled The cave bear story: life and death of a vanished animal. Although ‘The life and death’ was a summary of the knowledge acquired on cave bear biology at that time, four decades later, many aspects of its palaeoecology, extinction and evolution are still a matter of debate. With this volume, we aim to bring together the most recent research on cave bear biology in order to provide an update on the palaeoecology, biogeography, systematics, and phylogeny of this recently extinct ursine bear. We thus organised a symposium on the 1st of August 2017 as part of the three-day Annual Meeting of the European Association of Vertebrate Palaeontologists (EAVP) in Munich, Germany, that was an additional opportunity to announce the volume and to discuss this exciting subject face-to-face among specialists.     

Limb bone proportions and body mass of the cave bear (Ursus spelaeus)

The European cave bear evolved during the Middle Pleistocene and adapted to mountain environments. Earlier workers have described the cave bear as a robust bear. In this study the cave bears limb bone morphology is compared to the limb bone morphology of extant bears. Body mass estimates for the cave bear are made both based on different limb bone characters and based on dental and cranial characters. The shafts are wider in the cave bear limb bones than in the extant bear limb bones, and consequently the shaft widths give higher weight estimates to the cave bear than the other dimensions. The widened shafts are suggested to be a special adaptation (of presently unknown significance) rather than an indicator of an increased body mass.     

The largest European lion Panthera leo spelaea (Goldfuss 1810) population from the Zoolithen Cave,Germany: specialised cave bear predators of Europe

Remains of 13 individuals with 3/1 male/female ratio of the extinct Upper Pleistocene lion Panthera leo spelaea (Goldfuss, 1810) from the Zoolithen Cave near Burggeilenreuth (Bavaria, Germany) include the holotype skull and all paratype material. The highest mortality rate for the Zoolithen Cave lions is in their reproductive adult ages. Bite marks on lion bones or skulls are results of hyena activities, or rare cannibalism of lions under stress situations. Lions were possibly also killed in battles with cave bears during predation on hibernating bears in winter times. This cave bear hunt specialisation in caves overlaps with the ecological behaviour of cave bear feeding by Ice Age-spotted hyenas. Both largest Ice Age predators, lions and hyenas, had to specialise on feeding herbivorous cave bears in boreal forest mountainous cave rich regions, where the mammoth steppe megafauna prey was absent. This cave bear hunt by felids, and scavenging by hyenas and other large carnivores such as leopards and wolves explains why cave bears hibernated deep in to the European caves, for protection reasons against predators. Within such lion–cave bear and even lion–hyena conflicts in the caves lions must have been killed sometimes, explaining mainly the skeleton occurrences in different European caves.     

Hunting to extinction: biology and regional economy influence extinction risk and the impact of hunting in artiodactyls

Half of all artiodactyls (even-toed hoofed mammals) are threatened with extinction, around double the mammalian average. Here, using a complete species-level phylogeny, we construct a multivariate model to assess for the first time which intrinsic (biological) and extrinsic (anthropogenic and environmental) factors influence variation in extinction risk in artiodactyls. Globally artiodactyls at greatest risk live in economically less developed areas, have older weaning ages and smaller geographical ranges. Our findings suggest that identifying predictors of threat is complicated by interactions between both biological and anthropogenic factors, resulting in differential responses to threatening processes. Artiodactyl species that experience unregulated hunting live in significantly less economically developed areas than those that are not hunted; however, hunted species are more susceptible to extinction if they have slower reproductive rates (older weaning ages). In contrast, risk in non-hunted artiodactyls is unrelated to reproductive rate and more closely associated with the economic development of the region in which they live.     

Probable predation on Upper Cambrian trilobites and its relevance for the extinction of soft-bodied Burgess Shale-type animals

The lower Rabbitkettle Formation of northwestern Canada is a monofacial Upper Cambrian unit of variably calcareous, argillaceous siltstone and fine-grained sandstone with rare bioclastic grainstone, deposited on a gentle slope below fair-weather wave base with no discernible fluctuation in water depth. The trilobite fauna is a mixture of pandemic agnostoids and Laurentian polymeroids, including protaspides and meraspides, and individuals are disarticulated, non-abraded and mostly oriented convex-upward. Bioclasts are interpreted as in situ elements affected only by weak bottom currents and storm-induced turbulence. A major proportion of the larger (≥5 mm across) polymeroid cranidia and pygidia in the lower part (Marjuman) of the formation are broken; large thoracic segments are often broken at the axial furrow and some broken free cheeks occur, but essentially no broken agnostoids or hypostomes were observed. Trilobites are not broken in upper beds (Steptoean), above the base of the Glyptagnostus retculatus Zone. Physical breakage cannot be dismissed entirely, but most damage is interpreted to be due to size-selective predation, possibly through lethal blows similar to those delivered by some extant stomatopod crustaceans. A possible culprit may be an animal akin to Yohoia , known from the Middle Cambrian Burgess Shale. The distribution of attacked trilobites serves as a proxy for the presence and disappearance of soft-bodied carnivores. In the Rabbitkettle Formation, it suggests that Burgess Shale-type animals may have persisted into the Late Cambrian but suffered extinction at the Marjuman-Steptoean 'biomere' event when most trilobite species vanished.     

Stable isotope evidence for the consumption of millet and other plants in Bronze Age Italy

Stable carbon and nitrogen isotope analysis was carried out on human and animal bones from four inland Early and Middle Bronze Age sites in Northern and Southern Italy. The main aims of the investigation were to explore the contribution of plant foods to the human diet and to examine any dietary differences between and within each of the sites. At two of the sites in Northern Italy, human and animal bones were significantly enriched in ¹³C. This finding was attributed to the consumption of domestic millets (Panicum miliaceum and/or Setaria italica), which are C₄ pathway plants. Conversely, individuals from the two Bronze Age sites in Southern Italy were significantly depleted in ¹³C compared to those from the north. Here, millet was absent from the diet, and protein from C₃ plants made a much greater dietary contribution than animal protein. This finding highlights the importance of cereal cultivation, most likely of wheat and barley, in the south of Italy during the Bronze Age. Overall, our results support the idea that the widespread cultivation of millet first occurred in Northern Italy, following its introduction from across the Alps in Central Europe. Finally, we found no significant differences in the stable isotope values between individuals at each site, when grouped by their sex or presence of grave goods. This leads to the conclusion that any status difference that may have existed is not reflected in the long‐term dietary record, or at least not as measurable by stable isotope analysis. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Testing phylogenetic hypotheses for reconstructing the evolutionary history of Dolichopoda cave crickets in the eastern Mediterranean

Aim To investigate the molecular phylogenetic divergence and historical biogeography of cave crickets belonging to the genus Dolichopoda (Orthoptera, Rhaphidophoridae). Location Caves in continental and insular Greece. Methods We sequenced 1967 bp of mitochondrial DNA, corresponding to three fragments of the small and large subunit of the ribosomal RNA (16S and 12S rRNA, respectively) and to the subunit I of cytochrome oxidase (COI), to reconstruct phylogenetic relationships among all 30 known Greek species of Dolichopoda. Alternative hypotheses about the colonization of the Hellenic Peninsula by Dolichopoda species were tested by comparing the degree of discordance between species trees and gene trees under four plausible biogeographical scenarios. Results The present study revealed a rather well resolved phylogeny at species level, identifying a number of clades that represent long‐separated lineages and diverse evolutionary histories within the genus Dolichopoda. Two main clades were revealed within Hellenic–Aegean species, identifying a north‐western and a south‐eastern species group. Based on Bayesian analysis, we applied a relaxed molecular clock to estimate the divergence times between the lineages. The results revealed that the origins of eastern Mediterranean lineages are much older than those of previously studied western Mediterranean Dolichopoda. Tests of alternative biogeographical hypotheses showed that a double colonization of the Hellenic Peninsula, following separate continental and trans‐Aegean routes during the Messinian stage, best accounts for the present distribution of Greek Dolichopoda species. Main conclusions Reconstruction and biogeographical hypothesis testing indicated that the colonization of Greece by Dolichopoda species comprised two episodes and two different routes. The southern lineage probably arose from a trans‐Aegean colonization during the Messinian salinity crisis (5.96–5.33 Ma). The northern lineage could be the result of dispersal from the north through the Balkan Peninsula. The opening of the Mid‐Aegean Trench could have promoted an initial diversification within the uprising Anatolian Plateau, while the Messinian marine regression offered the conditions for a rapid dispersal through the whole Aegean–Hellenic region. In addition, climatic events during the Plio‐Pleistocene may have been responsible for the speciation within each of the two different phylogeographical units, principally attributable to vicariance events.     

The Vallonnet cave on the northern Mediterranean border: A record of one of the oldest human presences in Europe

Prehistoric sites testifying to human presence older than one million years in Europe are rare, and in the current state of knowledge, the oldest of them have been dated to around 1.4–1.5 Ma. The Vallonnet cave at Roquebrune-Cap-Martin in the Alpes-Maritimes, on the Mediterranean border, is one of the oldest sites in France to have yielded evidence of human activity: a lithic assemblage of about a hundred pieces and traces of butchery on bones of an Epivillafranchian fauna. The archaeological levels of this small cave were recently dated between 1.1 and 1.2 Ma by U-Pb correlated with paleomagnetic data. The site was occupied alternately by large carnivores that used it as a den or a lair, and by hominins that stayed there briefly in bivouac. The lithic remains are mainly percussion tools, shaped pebbles, flakes and cores, whose raw materials are local, or even semi-local, and on the whole not very diversified with mainly limestone, and to a lesser extent sandstone, quartzite, flint and quartz. This assemblage is attributed to a Mode 1 technology (Oldowayen), among which macro-tools (hammerstones, shaped and fractured pebbles) are found alongside rarer elements resulting from debitage operating chains aimed at producing sharp-edged flakes, very rarely retouched. The bipolar-on-anvil flaking technique could be identified from the characteristics of some artifacts. Several refitting flakes on shaped pebbles or percussion tools attest to knapping and percussion activities in the cave. Hominins consumed the remains of large herbivore carcasses, as attested by the presence of cutting and fracturing marks on some bones. The presence of a freshwater source in the immediate vicinity, and the knapping and butchering activities here therefore document the subsistence behavior of Lower Pleistocene human groups, certainly in competition with the carnivores present.     

Spatial variability of stable carbon and nitrogen isotope ratios in a Mediterranean coastal lagoon

Exploring the trophic pathway of organic matter within the Mauguio lagoon (southern France, western Mediterranean), we found spatial differences in the isotopic composition (both δ¹³C and δ¹⁵N values) of organic matter sources (primary producers, particulate and sedimentary organic matter), which were mirrored in the upper trophic levels (invertebrates and fish). On average, δ¹³C was heavier by about 1.5–2‰ in the location under marine influence than in the sites influenced by freshwater discharge. The opposite trend was found for δ¹⁵N, which attained maximum values in the north-central zone influenced by freshwater delivery. For both C and N stable isotope ratios, the highest spatial variability was found in organic matter sources (2–3‰), while invertebrates and fish exhibited less variability (\~1–2‰). The differences observed may be related to both anthropogenic (wastewater input) and natural (marine vs. terrestrial inputs) factors. Discharge of wastewater, which affects the innermost location, generally determines an increase in the relative abundance of ¹⁵N. In addition, terrestrially derived nutrients and organic matter, which also affect the innermost location, are known to determine a shift towards ¹³C-depleted values. Our results substantiate the finding that the analysis of carbon and nitrogen stable isotopes can help in elucidating origin and fate of organic matter in coastal lagoons, which are characterised by a great spatial variability and complexity.     

Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis

The diet of the dusky grouper Epinephelus marginatus , from the Balearic Islands, western Mediterranean, consisted primarily of crustaceans, molluscs and fishes, but diet composition varied with body size. The smaller dusky groupers (<300 mm L _T) fed primarily on crustaceans, and particularly on brachyurans, which accounted for 46% of the prey identified. As dusky groupers grew, cephalopods became increasingly important and constituted 10 to 40% of the prey identified in subadult and adult specimens. The largest dusky groupers fed primarily on fishes that represented 40·9% of prey identified. These shifts in diet were accompanied by a positive selection of increasingly large prey and by an expansion of trophic niche. δ ¹⁵N values of dusky grouper white muscle ranged from 8·8 to 13·1% and 71% of the variation in δ ¹⁵N was explained by differences in dusky grouper size. δ ¹³C values ranged from – 17·9 to – 15·9%, and no significant body size effect on δ ¹³C was detected. Stomach content and ¹³C values indicated that from 1 year old, the diet of E. marginatus was based on the benthic food web. The enrichment in δ ¹⁵N registered from juvenile to large males was c . 3·8%. Overall, there was good agreement between gut content and stable isotope data indicating that the latter may be useful as a tool in trophic studies in marine protected areas where sampling for fishes is not allowed.     

Nature and timing of biotic recovery in Antarctic benthic marine ecosystems following the Cretaceous–Palaeogene mass extinction

Taxonomic and ecological recovery from the Cretaceous–Palaeogene (K–Pg) mass extinction 66 million years ago shaped the composition and structure of modern ecosystems. The timing and nature of recovery has been linked to many factors including palaeolatitude, geographical range, the ecology of survivors, incumbency and palaeoenvironmental setting. Using a temporally constrained fossil dataset from one of the most expanded K–Pg successions in the world, integrated with palaeoenvironmental information, we provide the most detailed examination of the patterns and timing of recovery from the K–Pg mass extinction event in the high southern latitudes of Antarctica. The timing of biotic recovery was influenced by global stabilization of the wider Earth system following severe environmental perturbations, apparently regardless of latitude or local environment. Extinction intensity and ecological change were decoupled, with community scale ecological change less distinct compared to other locations, even if the taxonomic severity of the extinction was the same as at lower latitudes. This is consistent with a degree of geographical heterogeneity in the recovery from the K–Pg mass extinction. Recovery in Antarctica was influenced by local factors (such as water depth changes, local volcanism, and possibly incumbency and pre‐adaptation to seasonality of the local benthic molluscan population), and also showed global signals, for example the radiation of the Neogastropoda within the first million years of the Danian, and a shift in dominance between bivalves and gastropods.     

Isotopic evidence for divergent diets and mobility patterns in the Atacama Desert,northern Chile,during the Late Intermediate Period (AD 900–1450)

The decline of the Tiwanaku state saw the emergence of two new cultures—Pica‐Tarapacá and Atacama—during the Late Intermediate Period in northern Chile. Archeological evidence suggests that both groups practised maize agriculture and pastoralism, but that their interaction zones differed significantly. Marine resources are common at Pica‐Tarapacá sites, even those far from coast, while Atacama sites in the desert oases and precordilleran area seem to have directed their networks towards the highlands. Here we apply stable carbon, nitrogen, and oxygen isotope analysis on human bone and enamel to test dietary patterns and residential mobility at two sites, Pica 8 and Quitor 6, representing the Pica‐Tarapacá and Atacama cultures, respectively. Our results show that diet at the two sites indeed differed: significant but variable consumption of marine resources and maize is indicated at Pica 8, despite being an inland site, while diet at Quitor 6 was based mainly on terrestrial resources. The use of seabird guano and llama dung as fertilizers and extreme aridity may have contributed to the high nitrogen isotope values observed in Pica 8 humans. The δ¹⁸O values in Pica 8 individuals are generally lower than for Quitor in spite of its greater distance from the Andes. All three isotopes suggest the presence of at least five nonlocals in the 30 measured at Pica 8. This evidence for human mobility is consistent with the high levels of trade and interaction observed in the archeological record, and begins to quantify the degree of movement of specific individuals. Am J Phys Anthropol 156:374–387, 2015. © 2014 Wiley Periodicals, Inc.     

Habitats, abundance patterns and isotopic signals of morphotypes of the planktonic foraminifer Globigerinoides ruber (d'Orbigny) in the eastern Mediterranean Sea since the Marine Isotopic Stage 12

The chemical composition of shells of the planktonic foraminifer Globigerinoides ruber (white) is frequently used to determine past sea surface conditions. Recently, it has been shown that arbitrarily defined morphotypes within this species exhibit different chemical and isotopic signatures. Here, we investigate the occurrence through time and in space of morphological types of G. ruber (white) in late Quaternary and Holocene sediments of the central and the eastern Mediterranean Sea. In 115 samples representing two distinct time intervals (MIS 1–2 and MIS 9–12) at ODP Site 964 and the piston core GeoTü-SL96, we have defined three morphological types within this species and determined their relative abundances and stable isotopic composition. A quantitative analysis of morphological variation within G. ruber (white) in four samples revealed that the subjectively defined morphotypes occupy separate segments of a continuous and homogenous morphospace. We further show that the abundance of the morphotypes changes significantly between glacials and interglacials and that the three morphotypes of G. ruber show significant offsets in their stable isotopic composition. These offsets are consistent within glacial and interglacial stages but their sign is systematically reversed between the two Sites. Since the isotopic shifts among the three G. ruber morphotypes are systematic and often exceed 1‰, their understanding is essential for the interpretation of all G. ruber-based proxy records for the paleoceanographic development of the Mediterranean during the late Quaternary.     

Fire affects wood formation dynamics and ecophysiology of Pinus pinaster Aiton growing in a dry Mediterranean area

The increase in frequency and intensity of wildfires is seriously affecting forest ecosystems, especially in drought-prone areas. Trees’ recovery after fire is related to direct tree damage and is influenced by climate conditions, such as warm temperature and water shortage. In this study, we evaluate the post-fire effects on a Pinus pinaster Aiton forest growing in a hot and dry area of the Mediterranean region by comparing burned trees with severe crown reduction against unburned and not-defoliated trees. Inter-annual analyses of dendrochronology and stable isotopes in tree rings were combined with xylogenesis monitoring to investigate the effects of fire on tree growth, ecophysiological processes and wood formation. Tree-ring and isotope data showed a growth reduction and a decrease in photosynthetic activity in the burned trees, compared to control individuals, in the three years after fire. Further, the monitoring of cambial activity demonstrated a negative influence of warm and dry periods on wood formation, low xylem production, a delay in phenology and a reduction in xylem plasticity in burned trees. Our findings suggest that substantial photosynthetic limitations caused by crown defoliation and recurrent drought events could lead to severe growth decrease and reduction of trees ability to regain the pre-disturbance productivity rates.     

Stable isotopes analysis to assess the trophic role of ants in a Mediterranean agroecosystem

1 Stable isotopes signatures (δ¹³C and δ¹⁵N) of the most important tree‐dwelling ants in an olive orchard were examined, together with the signatures of the most common herbivores, predators and sap‐sucking insects. The olive orchard consists of separate subunits (trees) surrounded by a matrix of grasses or bare ground, and the role of ants in such a system is not fully understood. 2 None of the selected ant species was exclusive to the olive trees because they were also observed foraging on vegetation (mainly thistle) under the tree crowns. Hence, the relative contributions of these two sources of energy (olive trees versus herbs/grasses) were assessed by comparing the δ¹³C of ants with the signatures of plants and those of other arthropods collected on the trees and on nearby thistles. Next, the trophic level occupied by the ants and their ecological role within the olive food web were determined by examining the δ¹⁵N values and their relationship with indices of ecological performance measuring the potential pressure exerted by each species on the ecosystem. 3 The analysis of ¹³C signatures revealed a different contribution of the two energy sources, olive trees versus herbs and grasses, with the former being more important for ants. The analysis of ¹⁵N signatures suggested separate roles for different ant species: some (Crematogaster scutellaris, Lasius lasioides) occupied a higher trophic level, mostly involved in predation, whereas others (Camponotus piceus, Camponotus lateralis) occupied a lower level, probably involved more in homopteran tending. A fifth species (Camponotus aethiops) was in an intermediate position. Finally, the δ¹⁵N levels of the species were significantly correlated with indices of ecological performance.     

Environmental and human factors influencing rare plant local occurrence, extinction and persistence: a 115-year study in the Mediterranean region

Aim Assessing whether environmental and human factors influenced the spatial distribution and the dynamics of regionally rare plant species since the late nineteenth century, and whether these spatial and temporal patterns of rare species occurrences differ according to their chorology (level of endemism and biogeographic affinity). Location An area extending over 6250 km² in the French Mediterranean Region. Methods We used two botanical surveys achieved in 1886 and in 2001, and considered species rare if occurring in only one or two sites in the study area. Each rare species was assigned to a group of endemism level (restricted endemic, non‐endemic), and of biogeographic affinity (Mediterranean, South/Central European, Mountain, Eurosiberian). A 1 × 1 km grid was applied to the study zone. Generalized linear models were developed to study the spatial distribution and the fate of rare species occurrences (local extinction vs. local persistence between 1886 and 2001), as a function of environmental and human variables. Multivariate analyses were used to test whether the spatial distribution and the fate of rare species occurrences differed according to their chorology. Results In 2001, rare species as a whole tended to occur at higher altitude, in zones dominated by semi‐natural open habitats, and where cultivated area had decreased in the last 30 years. Between 1886 and 2001, rare species were the most prone to local extinction in zones where human population density, cultivated area and livestock density had increased the most. Between 1886 and 2001, rare species had a higher probability of local persistence in zones of high altitude and steep slope, on basic bedrocks and with low cultivated area. Rare species with Mountain and Eurosiberian affinities occurred in marginal habitats in the study region, i.e. on gneiss‐micaschist bedrocks and at high altitudes, whereas Mediterranean and South/Central European rare species occupied more varied environmental conditions. Between 1886 and 2001, Eurosiberian rare species showed high rates of local extinction whereas Mediterranean rare species had a significantly higher probability of local persistence. Restricted endemic species mostly occurred in zones of high slope, low human population density, and where cultivated area had decreased in the last 30 years. Occurrences of restricted endemics remained significantly stable between 1886 and 2001. Main conclusions Environmental and land‐use changes that occurred over the twentieth century in the Mediterranean Basin had significant impacts on the spatial distribution and on the long‐term dynamics of rare species occurrences. Urbanization and recent agriculture intensification, occurring mainly in coastal plains and littoral zones, caused most local extinctions of rare species from 1886 to 2001. Local populations of Eurosiberian species, which reach their range limits in marginal zones of the Mediterranean, also appear to be highly vulnerable. Conversely, most restricted endemic species occur in habitats with harsh topography and low human disturbance and have a higher potential of local persistence.