Leafcutter Bee Nests and Pupae from the Rancho La Brea Tar Pits of Southern California: Implications for Understanding the Paleoenvironment of the Late Pleistocene

The Rancho La Brea Tar Pits is the world’s richest and most important Late Pleistocene fossil locality and best renowned for numerous fossil mammals and birds excavated over the past century. Less researched are insects, even though these specimens frequently serve as the most valuable paleoenvironemental indicators due to their narrow climate restrictions and life cycles. Our goal was to examine fossil material that included insect-plant associations, and thus an even higher potential for significant paleoenviromental data. Micro-CT scans of two exceptionally preserved leafcutter bee nest cells from the Rancho La Brea Tar Pits in Los Angeles, California reveal intact pupae dated between ∼23,000–40,000 radiocarbon years BP. Here identified as best matched to Megachile (Litomegachile) gentilis Cresson (Hymenoptera: Megachilidae) based on environmental niche models as well as morphometrics, the nest cells (LACMRLP 388E) document rare preservation and life-stage. The result of complex plant-insect interactions, they offer new insights into the environment of the Late Pleistocene in southern California. The remarkable preservation of the nest cells suggests they were assembled and nested in the ground where they were excavated. The four different types of dicotyledonous leaves used to construct the cells were likely collected in close proximity to the nest and infer a wooded or riparian habitat with sufficient pollen sources for larval provisions. LACMRLP 388E is the first record of fossil Megachile Latreille cells with pupae. Consequently, it provides a pre-modern age location for a Nearctic group, whose phylogenetic relationships and biogeographic history remain poorly understood. Megachile gentilis appears to respond to climate change as it has expanded its distribution across elevation gradients over time as estimated by habitat suitability comparisons between low and high elevations; it currently inhabits mesic habitats which occurred at a lower elevation during the Last Glacial Maximum ∼21,000 years ago. Nevertheless, the broad ecological niche of M. gentilis appears to have remained stable.     

Cougars’ key to survival through the Late Pleistocene extinction: insights from dental microwear texture analysis

Cougars (Puma concolor) are one of only two large cats in North America to have survived the Late Pleistocene extinction (LPE), yet the specific key(s) to their relative success remains unknown. Here, we compare the dental microwear textures of Pleistocene cougars with sympatric felids from the La Brea Tar Pits in southern California that went extinct at the LPE (Panthera atrox and Smilodon fatalis), to clarify potential dietary factors that led to the cougar''s persistence through the LPE. We further assess whether the physical properties of food consumed have changed over time when compared with modern cougars in southern California. Using dental microwear texture analysis (DMTA), which quantifies surface features in three dimensions, we find that modern and Pleistocene cougars are not significantly different from modern African lions in any DMTA attributes, suggesting moderate durophagy (i.e. bone processing). Pleistocene cougars from La Brea have significantly greater complexity and textural fill volume than Panthera atrox (inferred to have primarily consumed flesh from fresh kills) and significantly greater variance in complexity values than S. fatalis. Ultimately, these results suggest that cougars already used or adopted a more generalized dietary strategy during the Pleistocene that may have been key to their subsequent success.     

Issue Information

Front Cover: Skeleton of a Columbian mammoth (Mammuthus columbi) assembled from bones recovered at the La Brea Tar Pits in Los Angeles, California. Original photograph taken by Jonathan Drury. Reproduced by permission of David A. Gold, Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA.     

Stable isotopes reveal seasonal competition for resources between late Pleistocene bison (Bison) and horse (Equus) from Rancho La Brea,southern California

Determining how organisms partition or compete for resources within ecosystems can reveal how communities are assembled. The Late Pleistocene deposits at Rancho La Brea are exceptionally diverse in large mammalian carnivores and herbivores, and afford a unique opportunity to study resource use and partitioning among these megafauna. Resource use was examined in bison and horses by serially sampling the stable carbon and oxygen isotope values found within tooth enamel of individual teeth of seven bison and five horses. Oxygen isotope results for both species reveal a pattern of seasonal enamel growth, while carbon isotope values reveal a more subtle seasonal pattern of dietary preferences. Both species ate a diet dominated by C₃ plants, but bison regularly incorporated C₄ plants into their diets, while horses ate C₄ plants only occasionally. Bison had greater total variation in carbon isotope values than did horses implying migration away from Rancho La Brea. Bison appear to incorporate more C₄ plants into their diets during winter, which corresponds to previous studies suggesting that Rancho La Brea, primarily surrounded by C₃ plants, was used by bison only during late spring. The examination of intra-tooth isotopic variation which reveals intra-seasonal resource use among bison and horse at Rancho La Brea highlights the utility of isotopic techniques for understanding the intricacies of ecology within and between ancient mammals.     

Isolation of biosurfactant-producing bacteria from the Rancho La Brea Tar Pits

This research was conducted to identify culturable surfactant-producing bacterial species that inhabit the 40,000-year-old natural asphalt seep at the Rancho La Brea Tar Pits in Los Angeles, CA. Using phenanthrene, monocyclic aromatic hydrocarbons, and tryptic soy broth as growth substrates, culturable bacteria from the tar pits yielded ten isolates, of which three species of gamma-proteobacteria produced biosurfactants that accumulated in spent culture medium. Partially purified biosurfactants produced by these strains lowered the surface tension of water from 70 to 35?C55 mN/m and two of the biosurfactants produced ??dark halos?? with the atomized oil assay, a phenomenon previously observed only with synthetic surfactants. Key findings include the isolation of culturable biosurfactant-producing bacteria that comprise a relatively small fraction of the petroleum-degrading community in the asphalt.     

Mandibular shape correlates of tooth fracture in extant Carnivora: implications to inferring feeding behaviour of Pleistocene predators

Percentages of tooth fracture and mandible shape are robust predictors of feeding habits in Carnivora. If these parameters co‐vary above the species level, more robust palaeobiological inferences could be made on fossil species. A test of association is presented between mandible shape and tooth fracture in a subset of extant carnivorans together with large Pleistocene fossil predators from Rancho La Brea (Canis dirus, Panthera atrox, and Smilodon fatalis). Partial least square (PLS) and comparative methods are employed to validate co‐variation of these two parameters in extant carnivorans. Association between mandible shape and percentage of tooth fracture is strongly supported, even if both blocks of data exhibit a phylogenetic signal to a different degree. Dietary adaptations drive shape/fracture co‐variation in extant species, although no significant differences occur in the PLS scores between carnivores and bone/hard food consumers. The fossil species project into PLS morphospace as outliers. Their position suggests a unique feeding behaviour. The increase in the size of prey, together with consumption of skin and hair from carcasses in a cold environment, might have generated unusual tooth breakage patterns in large predators from Rancho La Brea. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 70–80.     

Parallels between playbacks and Pleistocene tar seeps suggest sociality in an extinct sabretooth cat, Smilodon

Inferences concerning the lives of extinct animals are difficult to obtain from the fossil record. Here we present a novel approach to the study of extinct carnivores, using a comparison between fossil records (n=3324) found in Late Pleistocene tar seeps at Rancho La Brea in North America and counts (n=4491) from playback experiments used to estimate carnivore abundance in Africa. Playbacks and tar seep deposits represent competitive, potentially dangerous encounters where multiple predators are lured by dying herbivores. Consequently, in both records predatory mammals and birds far outnumber herbivores. In playbacks, two large social species, lions, Panthera leo, and spotted hyenas, Crocuta crocuta, actively moved towards the sounds of distressed prey and made up 84 per cent of individuals attending. Small social species (jackals) were next most common and solitary species of all sizes were rare. In the La Brea record, two species dominated, the presumably social dire wolf Canis dirus (51%), and the sabretooth cat Smilodon fatalis (33%). As in the playbacks, a smaller social canid, the coyote Canis latrans, was third most common (8%), and known solitary species were rare (<4%). The predominance of Smilodon and other striking similarities between playbacks and the fossil record support the conclusion that Smilodon was social.     

Complete genome sequence of Methanocorpusculum labreanum type strain Z

Methanocorpusculum labreanum is a methanogen belonging to the order Methanomicrobiales within the archaeal kingdom Euryarchaeota. The type strain Z was isolated from surface sediments of Tar Pit Lake in the La Brea Tar Pits in Los Angeles, California. M. labreanum is of phylogenetic interest because at the time the sequencing project began only one genome had previously been sequenced from the order Methanomicrobiales. We report here the complete genome sequence of M. labreanum type strain Z and its annotation. This is part of a 2006 Joint Genome Institute Community Sequencing Program project to sequence genomes of diverse Archaea.     

Attempted DNA extraction from a Rancho La Brea Columbian mammoth (Mammuthus columbi): prospects for ancient DNA from asphalt deposits

Fossil‐bearing asphalt deposits are an understudied and potentially significant source of ancient DNA. Previous attempts to extract DNA from skeletons preserved at the Rancho La Brea tar pits in Los Angeles, California, have proven unsuccessful, but it is unclear whether this is due to a lack of endogenous DNA, or if the problem is caused by asphalt‐mediated inhibition. In an attempt to test these hypotheses, a recently recovered Columbian mammoth (Mammuthus columbi) skeleton with an unusual pattern of asphalt impregnation was studied. Ultimately, none of the bone samples tested successfully amplified M. columbi DNA. Our work suggests that reagents typically used to remove asphalt from ancient samples also inhibit DNA extraction. Ultimately, we conclude that the probability of recovering ancient DNA from fossils in asphalt deposits is strongly (perhaps fatally) hindered by the organic compounds that permeate the bones and that at the Rancho La Brea tar pits, environmental conditions might not have been ideal for the general preservation of genetic material.     

Implications of Diet for the Extinction of Saber-Toothed Cats and American Lions

The saber-toothed cat, Smilodon fatalis, and American lion, Panthera atrox, were among the largest terrestrial carnivores that lived during the Pleistocene, going extinct along with other megafauna ∼12,000 years ago. Previous work suggests that times were difficult at La Brea (California) during the late Pleistocene, as nearly all carnivores have greater incidences of tooth breakage (used to infer greater carcass utilization) compared to today. As Dental Microwear Texture Analysis (DMTA) can differentiate between levels of bone consumption in extant carnivores, we use DMTA to clarify the dietary niches of extinct carnivorans from La Brea. Specifically, we test the hypothesis that times were tough at La Brea with carnivorous taxa utilizing more of the carcasses. Our results show no evidence of bone crushing by P. atrox, with DMTA attributes most similar to the extant cheetah, Acinonyx jubatus, which actively avoids bone. In contrast, S. fatalis has DMTA attributes most similar to the African lion Panthera leo, implying that S. fatalis did not avoid bone to the extent previously suggested by SEM microwear data. DMTA characters most indicative of bone consumption (i.e., complexity and textural fill volume) suggest that carcass utilization by the extinct carnivorans was not necessarily more complete during the Pleistocene at La Brea; thus, times may not have been “tougher” than the present. Additionally, minor to no significant differences in DMTA attributes from older (∼30–35 Ka) to younger (∼11.5 Ka) deposits offer little evidence that declining prey resources were a primary cause of extinction for these large cats.     

Was the Giant Short-Faced Bear a Hyper-Scavenger? A New Approach to the Dietary Study of Ursids Using Dental Microwear Textures

Dramatic environmental changes associated with global cooling since the late Miocene, and the onset of glacial-interglacial cycles in the Pleistocene served as a backdrop to the evolutionary radiation of modern bears (family Ursidae). These environmental changes likely prompted changes in food availability, and triggered dietary adaptations that served as motive forces in ursid evolution. Here, we assess correspondence of dental microwear textures of first and second lower molars with diet in extant ursids. We use the resulting baseline data to evaluate the hypothesis that the Pleistocene giant short-faced bear, Arctodus simus, was a bone consumer and hyper-scavenger at Rancho La Brea, California, USA. Significant variation along the tooth row is consistent with functional differentiation, with the second molar serving as a better dietary recorder than the first. Results evince significant variation among species: carnivorous and omnivorous ursids (Ursus maritimus, U. americanus) have significantly higher and more variable complexity (Asfc) than more herbivorous ones (Ailuropoda melanoleuca, Tremarctos ornatus, U. malayanus), and A. melanoleuca is differentiated from U. maritimus and U. americanus by significantly higher and more variable anisotropy (epLsar) values. Arctodus simus from Rancho La Brea exhibits wear attributes most comparable to its closest living relative (T. ornatus), which is inconsistent with hard-object (e.g., bone) consumption, and the hypothesis that short-faced bears were bone consuming hyper-scavengers across their range.     

Microbial diversity in natural asphalts of the Rancho La Brea Tar Pits

Bacteria commonly inhabit subsurface oil reservoirs, but almost nothing is known yet about microorganisms that live in naturally occurring terrestrial oil seeps and natural asphalts that are comprised of highly recalcitrant petroleum hydrocarbons. Here we report the first survey of microbial diversity in ca. 28,000-year-old samples of natural asphalts from the Rancho La Brea Tar Pits in Los Angeles, CA. Microbiological studies included analyses of 16S rRNA gene sequences and DNA encoding aromatic ring-hydroxylating dioxygenases from two tar pits differing in chemical composition. Our results revealed a wide range of phylogenetic groups within the Archaea and Bacteria domains, in which individual taxonomic clusters were comprised of sets of closely related species within novel genera and families. Fluorescent staining of asphalt-soil particles using phylogenetic probes for Archaea, Bacteria, and Pseudomonas showed coexistence of mixed microbial communities at high cell densities. Genes encoding dioxygenases included three novel clusters of enzymes. The discovery of life in the tar pits provides an avenue for further studies of the evolution of enzymes and catabolic pathways for bacteria that have been exposed to complex hydrocarbons for millennia. These bacteria also should have application for industrial microbiology and bioremediation.     

Microbial Diversity in Natural Asphalts of the Rancho La Brea Tar Pits

Bacteria commonly inhabit subsurface oil reservoirs, but almost nothing is known yet about microorganisms that live in naturally occurring terrestrial oil seeps and natural asphalts that are comprised of highly recalcitrant petroleum hydrocarbons. Here we report the first survey of microbial diversity in ca. 28,000-year-old samples of natural asphalts from the Rancho La Brea Tar Pits in Los Angeles, CA. Microbiological studies included analyses of 16S rRNA gene sequences and DNA encoding aromatic ring-hydroxylating dioxygenases from two tar pits differing in chemical composition. Our results revealed a wide range of phylogenetic groups within the Archaea and Bacteria domains, in which individual taxonomic clusters were comprised of sets of closely related species within novel genera and families. Fluorescent staining of asphalt-soil particles using phylogenetic probes for Archaea, Bacteria, and Pseudomonas showed coexistence of mixed microbial communities at high cell densities. Genes encoding dioxygenases included three novel clusters of enzymes. The discovery of life in the tar pits provides an avenue for further studies of the evolution of enzymes and catabolic pathways for bacteria that have been exposed to complex hydrocarbons for millennia. These bacteria also should have application for industrial microbiology and bioremediation.     

Cretaceous small scavengers: feeding traces in tetrapod bones from Patagonia, Argentina

Ecological relationships among fossil vertebrate groups are interpreted based on evidence of modification features and paleopathologies on fossil bones. Here we describe an ichnological assemblage composed of trace fossils on reptile bones, mainly sphenodontids, crocodyliforms and maniraptoran theropods. They all come from La Buitrera, an early Late Cretaceous locality in the Candeleros Formation of northwestern Patagonia, Argentina. This locality is significant because of the abundance of small to medium-sized vertebrates. The abundant ichnological record includes traces on bones, most of them attributable to tetrapods. These latter traces include tooth marks that provde evidence of feeding activities made during the sub-aerial exposure of tetrapod carcasses. Other traces are attributable to arthropods or roots. The totality of evidence provides an uncommon insight into paleoecological aspects of a Late Cretaceous southern ecosystem.     

An Enlarged Parietal Foramen in the Late Archaic Xujiayao 11 Neurocranium from Northern China,and Rare Anomalies among Pleistocene Homo

We report here a neurocranial abnormality previously undescribed in Pleistocene human fossils, an enlarged parietal foramen (EPF) in the early Late Pleistocene Xujiayao 11 parietal bones from the Xujiayao (Houjiayao) site, northern China. Xujiayao 11 is a pair of partial posteromedial parietal bones from an adult. It exhibits thick cranial vault bones, arachnoid granulations, a deviated posterior sagittal suture, and a unilateral (right) parietal lacuna with a posteriorly-directed and enlarged endocranial vascular sulcus. Differential diagnosis indicates that the perforation is a congenital defect, an enlarged parietal foramen, commonly associated with cerebral venous and cranial vault anomalies. It was not lethal given the individual’s age-at-death, but it may have been associated with secondary neurological deficiencies. The fossil constitutes the oldest evidence in human evolution of this very rare condition (a single enlarged parietal foramen). In combination with developmental and degenerative abnormalities in other Pleistocene human remains, it suggests demographic and survival patterns among Pleistocene Homo that led to an elevated frequency of conditions unknown or rare among recent humans.     

A Suite of Dermestid Beetle Traces on Dinosaur Bone from the Upper Jurassic Morrison Formation,Wyoming, USA

Most studies of insect traces on fossil bone deal with one or two trace morphs found on isolated bone fragments, making it difficult to identify the trace-maker and its behavior. We report the discovery of a suite of insect traces on an articulated Camptosaurus dinosaur skeleton that permits the identification of the trace-maker and interpretations of its behavior. The traces include mandible marks, pits, and shallow bores on cortical bone, and deep, meandering furrows and tunnels (borings) on articular surfaces. The interiors of bones are intensely mined, and the cavities and borings are filled with fine bone fragments (insect frass). The distinctive mandible marks consist of opposing sets of parallel grooves, indicating the maker had two apical teeth set on symmetrical mandibles and that all of the traces were made by a single taxon. Comparison of the fossils with the mandible morphology and bone traces of extant insects indicates dermestid beetles made the traces. Based on extant dermestid behavior, soft tissues were likely absent and the bones were lipid-laden when the traces were made. Examination of more than 5,000 bones from the Morrison and Cedar Mountain formations shows insect traces on bone are common but overlooked and that many bones are substantially damaged by insect mining. The key to the recognition of these important yet subtle traces is a search model and an intense, oblique light source.     

Evolution in the sabre‐tooth cat,Smilodon fatalis,in response to Pleistocene climate change

The late Pleistocene was a time of environmental change, culminating in an extinction event. Few fossil localities record a temporal series of carnivore fossil populations from this interesting interval as well as Rancho La Brea (RLB). We analysed mandibles of Smilodon fatalis from RLB using 2‐D geometric morphometrics to examine whether, and how, mandibular shape changes through time. Smilodon fatalis shows mandibular evolution with oscillations between a small, ancestral‐type morph in pits 77 (≈37 Kybp) and 2051 (≈26 Kybp), a larger, more derived morph in pits 91 (≈28 Kybp) and 61‐67 (≈13.6 Kybp), and an intermediate morph from pit 13 (≈17.7 Kybp). These oscillations end in pit 61‐67, with greatest body size, and are estimated to have its widest gape and lowest bite force. Additionally, variation is lowest in pit 61‐67, which was deposited concurrent with the Bølling–Allerød warming event, which may have important implications for the timing or conditions during the extinction event. Contra to a temporal Bergmann's rule, such rapid warming events appear to be correlated with larger, derived, morphologies whereas static, cooler, climates correlate with gracile, ancestral morphologies.     

Bone-eating Osedax worms lived on Mesozoic marine reptile deadfalls

We report fossil traces of Osedax, a genus of siboglinid annelids that consume the skeletons of sunken vertebrates on the ocean floor, from early-Late Cretaceous (approx. 100 Myr) plesiosaur and sea turtle bones. Although plesiosaurs went extinct at the end-Cretaceous mass extinction (66 Myr), chelonioids survived the event and diversified, and thus provided sustenance for Osedax in the 20 Myr gap preceding the radiation of cetaceans, their main modern food source. This finding shows that marine reptile carcasses, before whales, played a key role in the evolution and dispersal of Osedax and confirms that its generalist ability of colonizing different vertebrate substrates, like fishes and marine birds, besides whale bones, is an ancestral trait. A Cretaceous age for unequivocal Osedax trace fossils also dates back to the Mesozoic the origin of the entire siboglinid family, which includes chemosynthetic tubeworms living at hydrothermal vents and seeps, contrary to phylogenetic estimations of a Late Mesozoic–Cenozoic origin (approx. 50–100 Myr).     

Ecological Changes in Coyotes (Canis latrans) in Response to the Ice Age Megafaunal Extinctions

Coyotes (Canis latrans) are an important species in human-inhabited areas. They control pests and are the apex predators in many ecosystems. Because of their importance it is imperative to understand how environmental change will affect this species. The end of the Pleistocene Ice Age brought with it many ecological changes for coyotes and here we statistically determine the changes that occurred in coyotes, when these changes occurred, and what the ecological consequences were of these changes. We examined the mandibles of three coyote populations: Pleistocene Rancho La Brean (13–29 Ka), earliest Holocene Rancho La Brean (8–10 Ka), and Recent from North America, using 2D geometric morphometrics to determine the morphological differences among them. Our results show that these three populations were morphologically distinct. The Pleistocene coyotes had an overall robust mandible with an increased shearing arcade and a decreased grinding arcade, adapted for carnivory and killing larger prey; whereas the modern populations show a gracile morphology with a tendency toward omnivory or grinding. The earliest Holocene populations are intermediate in morphology and smallest in size. These findings indicate that a niche shift occurred in coyotes at the Pleistocene/Holocene boundary – from a hunter of large prey to a small prey/more omnivorous animal. Species interactions between Canis were the most likely cause of this transition. This study shows that the Pleistocene extinction event affected species that did not go extinct as well as those that did.