The cave bear’s hibernation: reconstructing the physiology and behaviour of an extinct animal

Abstract

When studying an extinct species such as the cave bear (Ursus spelaeus ROSENMÜLLER 1794), it is possible to apply a variety of molecular biology techniques such as the study of stable isotopes or mitochondrial DNA (mDNA) to infer patterns of behaviour or physiology that would otherwise remain concealed. Throughout Europe and along time, differences in the isotopic values (δ¹³C and δ¹⁵N) of cave bears arise from environmental differences and the Pleistocene climatic evolution. The climate determines the hibernation length, during which the cave bears undergo a particular physiology that can be related to an increase in δ¹⁵N during climate cooling. In order to verify whether hibernation affected the isotopic values, we compared cave bears in different ontogenetic stages. The results show that perinatal values reflect the values for mothers during hibernation, while juveniles show differences in maternal investment. A previous study in the literature based on complete mitochondrial DNA sequences of several individuals collected from closely situated caves showed that each cave housed, almost exclusively, a single lineage of haplotypes. This pattern suggests extreme fidelity to the birth site, or homing behaviour, and that cave bears formed stable maternal social groups, at least for the purpose of hibernation. Studies of this type offer unexpected data on the palaeobiology of this extinct animal.     

Was the European cave bear an occasional scavenger?

Rabal‐Garcés, R., Cuenca‐Bescós, G., Canudo, J.I. & de Torres, T. 2011: Was the European cave bear an occasional scavenger? Lethaia, Vol. 45, pp. 96–108. The cave bear Ursus spelaeus fossils remains are quite abundant in the Late Pleistocene site of Coro Tracito (Huesca, Spain). The site constitutes the highest mountain record of cave bears in the Iberian Peninsula. Being a monospecific locality, it permits the study of the biology and dietary habits of this species. The study of the limb bones established first, the mortality pattern of this population of Ursus spelaeus and, second, the alteration pattern due to carnivore tooth‐marks. Some authors have performed similar analyses in the same kind of skeletal elements in other cave bear localities all over Europe and, therefore it has been possible to compare our results with those from other sites. The tooth‐marks found in the bones of cave bears, especially in monospecific sites, have been attributed to a scavenging behaviour. In agreement with the authors, our analysis presented here supports the hypothesis of scavenging behaviour for cave bears. □Behaviour, Late Pleistocene, Spain, taphonomy, tooth‐marks, Ursus spelaeus.     

From a molecules’ perspective – contributions of ancient DNA research to understanding cave bear biology

Abstract

Few members of the Pleistocene megafauna have been as extensively studied as cave bears. Multidisciplinary research into cave bears has provided insights into their morphology, ecology, and evolution. Genetic studies have profited from the availability of large numbers of well-preserved remains. As a result, ‘ancient DNA (aDNA)’ from cave bears has provided significant insights into cave bear ecology, phylogeography and even potential causes of their extinction. Here I review the contributions that genetic research has made to our understanding of cave bear biology and evaluate the potential that new, genomic tools provide to shed further light onto how these iconic representatives of the Pleistocene megafauna lived and died.     

Longevity and life history of cave bears – a review and novel data from tooth cementum and relative emergence of permanent dentition

Abstract

Longevity and other life history variables are key to understanding evolutionary processes and the biology of extinct animals. For the past 20 years, the lifespan of cave bears received an increased interest. Studies focusing on incremental lines of tooth cementum resulted in detailed mortality patterns from different localities. In this review, we summarise literature on age estimation as well as mortality of different European cave bear localities and present novel data on longevity from 94 teeth originating from 20 European localities. Additionally, the relative tooth emergence pattern of the permanent dentition is investigated under the Schultz’s rule framework of possible life history implications. For this, the known sequences of extant bear species are compared with the one of cave bears. Our results suggest that the typical duration of the life of cave bears was 19 years but data from literature show that in rare cases ages of up to 30–32 years were achieved. Additionally, we present the oldest known age for the Middle Pleistocene cave bear Ursus deningeri, 29 years. The tooth eruption pattern of cave bears exhibits a heterochronic shift that implies, under the assumption of Schulz’ rule, a slightly faster life history than closely related species.     

Taphonomy and palaeoecology of the late Pleistocene to middle Holocene small mammal succession of El Harhoura 2 cave (Rabat-Témara, Morocco)

The relationship between local and global climatic variations and the origin and dispersal of Homo sapiens in Africa is complex, and North Africa may have played a major role in these events. In Morocco, very few studies are specifically dedicated to small fossil vertebrates, and neither taphonomic nor palaeoecological studies have been undertaken on these taxa, particularly in archaeological contexts. The late Pleistocene to middle Holocene succession of El Harhoura 2 cave, situated in the region of Témara, yields an exceptionally rich small vertebrate assemblage. We present the results of a first systematic, taphonomic, and palaeoecological study of the small mammals from Levels 1 to 8 of El Harhoura 2. The absence of bone sorting and polishing, as well as the presence of significant traces of digestion indicate that the small mammal bones were accumulated in the cave by predators and that no water transport occurred. Other traces observed on the surface of bones consist mainly of root marks and black traces (micro-organisms or more probably manganese) which affected the majority of the material. The percentage of fragmentation is very high in all stratigraphic levels, and the post-depositional breakage (geologic and anthropogenic phenomena) obscure the original breakage patterns of bones by predators. According to the ecology of the different species present in the levels of El Harhoura 2, and by taking into account possible biases highlighted by the taphonomic analysis, we reconstruct the palaeoenvironmental evolution in the region. For quantitative reconstructions we used two indices: the Taxonomic Habitat Index (THI) and the Gerbillinae/Murinae ratio. Late Pleistocene accumulations were characterised by a succession of humid (Levels 3, 4a, 6, and 8) and arid (Levels 2?, 5, and 7) periods, with more or less open landscapes, ending in an ultimate humid and wooded period during the middle Holocene (Level 1). We discuss particular limits of our results and interpretations, due to an important lack of taxonomic, ecological, and taphonomic knowledge in North Africa.     

Can wing morphology inform conservation priorities for Southeast Asian cave bats?

Adaptations for foraging in the complex airspaces of forest interiors may make bat species in the Asian tropics particularly susceptible to forest loss. However, ecomorphological analysis of Vietnamese bat assemblages challenges the hypothesis that, due to their greater vagility, cave‐roosting bats are less vulnerable to habitat fragmentation than foliage‐roosting species. Of the 13 most highly adapted forest‐interior species in our study, eight were cave‐roosting members of the Rhinolophidae and Hipposideridae and had wing morphologies closely resembling five foliage‐roosting members of the Murininae and Kerivoulinae—species typically thought to have low vagility. Overall, both cave‐roosting and foliage‐roosting bats exhibited a wide range of flight indices and species' wing designs corresponded with preferred foraging habitats, suggesting that foraging strategy may outweigh roost preference as a determinant of bat wing morphology and flight performance. Consequently, where such variation occurs, cave‐roosting bat ensembles are likely to include species with low vagility and similar sensitivity to habitat fragmentation. This could have important conservation implications as Asian karst formations support high cave densities and important bat diversity yet increasingly represent forest refugia in anthropogenic landscapes. We, therefore, advocate greater consideration of species vagility in determining conservation priorities for the region's bat fauna.     

Migratory behaviour of the Schreiber's bat: when, where and why do cave bats migrate in a Mediterranean region?

Regional migrations are important elements of the biology of bats, but remain poorly understood. We obtained a large dataset of recoveries of ringed Miniopterus schreibersii to study the patterns and drivers of migration of a Mediterranean cave-dwelling bat. In spite of the mildness of Mediterranean winters, in average years bats hibernated, and few movements were recorded during this period. After hibernation, females migrated to spring roosts, and again to maternity roosts just before parturition. This late arrival at nurseries could be a strategy to avoid a harmful build-up of parasites. Soon after the juveniles were weaned, the mothers migrated to the roosts where they spent autumn and sometimes also winter. Juveniles remained in the warm nurseries longer, presumably because high roost temperatures speed up growth. The pattern of migration of males was similar to that of females, but they left hibernacula later and remained more mobile during the maternity season. They also arrived at the hibernacula later, possibly because they needed time to build up fat stores after the energetically costly mating season. Maternity colonies spent the yearly cycle in well-defined home ranges (mean=19 030 km²), which overlapped greatly. Bats were furthest from the maternity sites during hibernation, but even then 80% remained within 90 km of them. Each hibernaculum attracted bats from multiple nurseries, from within a mean range of 10 770 km². We tested two potential drivers for migration – temperature in the roosts and at the foraging areas – but our results supported only the first one. Bats migrated to reach the roosts most thermally suited for each phase of their life cycle, indicating that roost temperature and associated metabolic advantages are key drivers for regional migrations of cave-dwelling bats.     

The state of the art of biospeleology in Russia and other countries of the former Soviet Union: a review of the cave (endogean) invertebrate fauna. 1. Introduction—crustacea

At least 308 species or subspecies of stygo- or troglobionts and at least 735 species or subspecies of mostly presumed stygo- or troglophiles representing 17 phyla, 38 classes, 90 orders, and 278 families of invertebrates are currently known to populate the caves and subterranean waters of Russia and other countries of the former Soviet Union. The main evolutionary burst in the endogean habitats including the MSS (milieu souterrain superficiel, or mesovoid shallow stratum) is observed in arthropods, primarily crustaceans, collembolans, and beetles. The major centers of taxonomic diversity among stygo- and troglobionts within the study region are the Caucasus (181 species, or almost 59%) and Crimea (44 species, or over 14%), which are montane karstified “glacial” refugia of the nemoral biota. The contribution of the other major regions including karstified areas is considerably smaller and gradually decreases from Central Asia (35 species; over 11%), the Far East (33; nearly 11%), the Ukrainian Carpathians with Podolia (12; almost 4%), the Russian Plain (7; over 2%), the Urals and Ural region (7; over 2%) to Siberia (5 species; 1.6%). Inventorying remains a topical problem in assessing the stygo- and troglofaunas of the territories in question. The most complete bibliography possible is included.     

Deciphering archaeological palimpsests with bone micro-fragments from the Lower Magdalenian of El Mirón cave (Cantabria,Spain)

Abstract

Modern excavation techniques aim accurately to recover extant archaeological data. Usually bone micro-fragments are gathered as a result, however, during archaeological analysis these remains are often set apart as indeterminate bones and generally do not contribute to the interpretation of the deposits. How to decipher archaeological palimpsests using these small bone fragments is the aim of this paper. El Mirón Cave, located in northern Iberia, contains a very rich Cantabrian Lower Magdalenian deposit (17–15 uncal ka BP) with high densities of faunal remains and artefacts. Here, we present zooarchaeological, taphonomic and spatial distribution analyses of macromammal finds, including those small bone fragments, accumulated during a series of intensive and repeated human occupations found in the outer vestibule excavation area. Our results show that a broad spectrum of activities was performed there, including meat, marrow and grease processing and waste abandonment. We propose that bone micro-fragments must be considered when addressing human subsistence reconstructions from animal remains, as they represent the leftovers of the chaîne opératoire of animal carcass exploitation. The archaeological implications of their inclusion are extremely valuable, especially when deciphering palimpsests. A multidisciplinary approach to study these small animal remains provides information that otherwise would be missed.     

A show cave management: Anthropogenic CO2 in atmosphere of Výpustek Cave (Moravian Karst,Czech Republic)

Anthropogenic impact on CO₂ levels was studied in the Bear Chamber of the Výpustek Cave, a show cave in the Moravian Karst (Czech Republic), during a period of active ventilation and enhanced attendance. The study showed that the natural CO₂ levels were controlled by (i) the natural CO₂ influxes from soils/epikarst (up to ∼5.64 × 10⁻² mol s⁻¹); and, (ii) the advective CO₂ fluxes out of cave atmosphere (up to 4.66 × 10⁻² mol s⁻¹). During visitor presence, the anthropogenic CO₂ flux into the chamber reached up to ∼0.13 mol s⁻¹ and exceeded all other CO₂ fluxes. The reachable anthropogenic steady states at sufficient duration of stay (up to 2.65 × 10⁻¹ mol m⁻³) could exceed the natural CO₂ levels by factor of more than nine based on the number of visitors. Recession analysis of anthropogenic pulses showed that intervals between individual visitor groups would have to be up to ∼6 h long if the cave environment has to return to natural conditions. As such pauses between individual tours are hardly realizable, a risk analysis was conducted to find the consequences of breaking natural conditions. It showed that the condition under which dripwater becomes aggressive to calcite (i.e., the point when P_CO2 in cave atmosphere exceeds the hypothetical CO₂ concentrations in epikarst that has participated on the water formation, P_CO2(H) = 10^−1.56) is potentially reachable under extreme conditions only (enormous visitor stay period and visitor number). In case of condensed water, however, any increase in CO₂ concentration will cause an increase of water aggressiveness to calcite. Therefore, in the periods and sites of enhanced condensation, it is important to strive for preservation of natural conditions.     

Postglacial vegetation history in Luxembourg: new charcoal data from the cave of la Karelslé (Waldbillig, eastern Gutland)

The archaeological site of La Karelslé (Waldbillig, Luxembourg) provides the first important charcoal sequence in Luxembourg for the development of Holocene plant cover. During the Pre-boreal, the results show open woodland vegetation dominated by Pinus sylvestris type in association with Betula sp. and Rosaceae. After an important gap covering the Boreal and the early Atlantic, the data reveal the dominance of a deciduous Quercus woodland with Tilia sp., Fraxinus excelsior and Corylus avellana. Finally during the sub-Boreal, the assemblages indicate a cooler and wetter climate and Quercus woods with Fagus sylvatica and Taxus baccata. There is no clear evidence for human impact. Received June 5, 2001 / Accepted December 3, 2001     

What happens to dead birds left in a cave and its vicinity for a quarter of a century? A taphonomic experiment

Abstract

This paper describes a bird carcass-monitoring experiment carried out in a limestone cave and its immediate vicinity in southern Poland for almost a quarter of a century. Some specimens deposited outside the cave were preserved almost intact, others were only a little weathered. Soft tissues and remnants of feathers were preserved in some of the samples inside the cave. Stages of bone modifications that can occur in a cave have been distinguished and illustrated for the first time. Also, bird bones from owl pellets have been used in a carcass-monitoring experiment for the first time. Bone modifications in the form of wrinkling, bending and/or collapsing of the bone surface were recorded only on the bones of birds that decomposed inside the cave, and not on bones that had been isolated from owl pellets prior to their deposition in the cave. Therefore, it is postulated that avian – and possibly also small mammal – bones that have been defleshed, either by people or animals, have a greater chance to survive and fossilize than bones deposited as complete carcasses in a cave. This agrees with the generally accepted notion that larger assemblages of small vertebrates in caves are usually the result of predator accumulation.     

Taxonomic,phylogenetic and ecological diversity of Niphargus (Amphipoda: Crustacea) in the Hölloch cave system (Switzerland)

Groundwater belongs to the spatially most extensive, but least explored freshwater systems. On a global scale, the species richness of several subterranean invertebrate taxa parallels species richness found in surface waters, while on a local scale species richness hardly exceeds 20 species. This results in a high contribution of groundwater ecosystems to regional β- and γ-diversity, and to a smaller degree to α-diversity, and deserves focused attention. In general, more species are to be found in large cave systems. The second largest cave system in Europe is Hölloch in Switzerland. In this paper we revised the taxonomic, phylogenetic and ecological diversity of the amphipod community in the Hölloch cave system. While previous records listed five geographically widespread species of the genus Niphargus for this cave system, we could not confirm the presence of any of those species, but rather found three highly distinct species new to science. In this paper we describe Niphargus styx sp. nov., Niphargus murimali sp. nov., and Niphargus muotae sp. nov., and suggest that previous records from that cave were probably misidentifications. Although amphipod species richness in this cave system seems to be lower than previously thought in terms of absolute numbers, the cave retained its regional and international importance in terms of nature conservation for multiple reasons. First, all newly described species are probably endemic to this cave system. Second, they are phylogenetically distantly related and exhibit moderate to high phylogenetic diversity. Third, the species, as inferred from their functional morphology, are also ecologically highly divergent. Based on geographic distribution of their nearest relatives, we hypothesize that the cave system was most likely independently colonized from North, West and South and that the pre-adapted ancestors occupied different ecological niches within the system.

http://zoobank.org/urn:lsid:zoobank.org:pub:A19309E5-C06B-4844-A4D8-7571F05F25C9     

Spatial segregation among age classes in cave salamanders: habitat selection or social interactions?

Within species, individuals with different sexes, morphs and age classes often show spatial segregation. Both habitat selection and social processes have been proposed to explain intraspecific spatial segregation, but their relative importance is difficult to assess. We investigated spatial segregation between age classes in the cave salamander Hydromantes (Speleomantes) strinatii, and used a hypothetico-deductive approach to evaluate whether social or ecological processes explain segregation pattern. We recorded the location and age class of salamanders along multiple caves; we measured multiple microhabitat features of different sectors of caves that may determine salamander distribution. We assessed age-class segregation, and used generalized mixed models and an information-theoretic framework, to test if segregation is explained by social processes or by differences in habitat selection. We found significant age-class segregation, juveniles living in more external cave sectors than adults. Multiple environmental features varied along caves. Juveniles and adults showed contrasting habitat selection patterns: juveniles were associated with sectors having high invertebrate abundance, while adults were associated with scarce invertebrates and low temperature. When the effect of environmental features was taken into account, the relationship between juveniles and adults was non negative. This suggests that different habitat preferences, related to distinct risk-taking strategies of age classes, can explain the spatial segregation. Juveniles require more food and select more external sectors, even if they may be risky. Conversely, adults may trade off food availability in favour of safe areas with stable micro-climate.     

When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders

Convergence, i.e., similarity between organisms that is not the direct result of shared phylogenetic history (and that may instead result from independent adaptations to similar environments), is a fundamental issue that lies at the interface of systematics and evolutionary biology. Although convergence is often cited as an important problem in morphological phylogenetics, there have been few well-documented examples of strongly supported and misleading phylogenetic estimates that result from adaptive convergence in morphology. In this article, we propose criteria that can be used to infer whether or not a phylogenetic analysis has been misled by convergence. We then apply these criteria in a study of central Texas cave salamanders (genus Eurycea). Morphological characters (apparently related to cave-dwelling habitat use) support a clade uniting the species E. rathbuni and E. tridentifera, whereas mitochondrial DNA sequences and allozyme data show that these two species are not closely related. We suggest that a likely explanation for the paucity of examples of strongly misleading morphological convergence is that the conditions under which adaptive convergence is most likely to produce strongly misleading results are limited. Specifically, convergence is most likely to be problematic in groups (such as the central Texas Eurycea) in which most species are morphologically very similar and some of the species have invaded and adapted to a novel selective environment.     

A new species of mite (Acari: Histiostomatidae) phoretic on Gymnomus caesius (Diptera: Heleomyzidae) from Vlčie Diery cave

A new species of histiostomatid mite — Myianoetus sovat sp. n., based on the deutonymph, is described from the fly Gymnomus caesius. It differs from other species of Myianoetus by more characters of idiosomal morphometry, body and leg chaetotaxy, solenidiotaxy and shape of the adhering disc and its structures.     

The spread of agriculture in northern Iberia: new archaeobotanical data from El Mirón cave (Cantabria) and the open-air site of Los Cascajos (Navarra)

This paper presents archaeobotanical results from the Neolithic levels (5,300–4,000 b.c.) of two recently excavated sites in northern Iberia: El Mirón cave (Cantabria) and the open-air site of Los Cascajos (Navarra). A cereal grain from El Mirón is currently the earliest domesticated plant remain from this region. Despite the large number of samples examined, plant remains are few. They include basically cereals (Triticum monococcum, T. dicoccum, T. aestivum/durum/turgidum and Hordeum vulgare) and some nuts and fruits (Corylus avellana, Quercus sp., Vitis sp., etc.). The presence of free-threshing wheats at El Mirón opens up an interesting subject for debate, as until now naked wheats have been absent from the early Neolithic archaeobotanical record of the coastal Cantabrian region. Hulled wheat chaff is the main plant component from Los Cascajos, south of the Cantabrian Cordillera in Navarra, indicating waste from processing activities. The association of barley almost exclusively with both a burial and a ritual vase in Los Cascajos could be related specific rituals or ceremonies.     

Developing indices of relative abundance for monitoring cave and ground wētā (Orthoptera) in southern beech forest,New Zealand

We sampled populations of forest-floor dwelling cave and ground wētā using footprint tracking tunnels and spotlight transect counts in southern beech forest, New Zealand. Samples were compared to estimates of wētā density based on mark–recapture estimates from 25?m² enclosures. Both activity indices captured variability in cave wētā in time and space, were strongly correlated with each other, and have the potential for monitoring cave wētā activity levels. Comparisons between indices and cave wētā density estimates were equivocal, as recapture rates were too low to calculate high-resolution density estimates. We also found that cave wētā counts had a curved relationship increasing with temperature, and a negative relationship with increasing shrub and woody debris cover. Based on these preliminary results, tracking tunnels could be a viable method of monitoring cave wētā as they appear more efficient than transect counts and are relatively inexpensive. However, further calibration trials are needed to determine if indices mirror robust population density estimates.