Extant Carnivores Research Articles

Cenozoic climate change and the evolution of North American mammalian predator ecomorphology

Abstract The trend of global cooling across the Cenozoic transformed the North American landscape from closed forest to more open grasslands, resulting in dietary adaptations in herbivores in response to shifting resources. In contrast, the material properties of the predator food source (muscle, skin, and bone) have remained constant over this transition, suggesting a corresponding lack of change in predator dietary adaptations. We investigated the North American mammalian predator fossil record using a tooth-shape metric and body mass, predicting that the former would exhibit stability. Instead, we found that mean molar morphology became more blade-like, with our tooth-shape metric sharply increasing in the late Eocene and remaining high from the Oligocene onward. Subsequent tests in extant carnivorans reveal taxa with more bladelike teeth are prevalent in more open environments. Our results reveal an unexpected functional shift among North American predators in response to large-scale environmental changes across the Cenozoic.

Uncovering the mosaic evolution of the carnivoran skeletal system.

The diversity of vertebrate skeletons is often attributed to adaptations to distinct ecological factors such as diet, locomotion, and sensory environment. Although the adaptive evolution of skull, appendicular skeleton, and vertebral column is well studied in vertebrates, comprehensive investigations of all skeletal components simultaneously are rarely performed. Consequently, we know little of how modes of evolution differ among skeletal components. Here, we tested if ecological and phylogenetic effects led to distinct modes of evolution among the cranial, appendicular and vertebral regions in extant carnivoran skeletons. Using multivariate evolutionary models, we found mosaic evolution in which only the mandible, hindlimb and posterior (i.e. last thoracic and lumbar) vertebrae showed evidence of adaptation towards ecological regimes whereas the remaining skeletal components reflect clade-specific evolutionary shifts. We hypothesize that the decoupled evolution of individual skeletal components may have led to the origination of distinct adaptive zones and morphologies among extant carnivoran families that reflect phylogenetic hierarchies. Overall, our work highlights the importance of examining multiple skeletal components simultaneously in ecomorphological analyses. Ongoing work integrating the fossil and palaeoenvironmental record will further clarify deep-time drivers that govern the carnivoran diversity we see today and reveal the complexity of evolutionary processes in multicomponent systems.

Fossil brains provide evidence of underwater feeding in early seals.

Pinnipeds (seals and related species) use their whiskers to explore their environment and locate their prey. Today they live mostly in marine habitats and are adapted for a highly specialised amphibious lifestyle with their flippers for locomotion and a hydrodynamically streamlined body. The earliest pinnipeds, however, lived on land and in freshwater habitats, much like mustelids today. Here we reconstruct the underwater foraging behaviour of one of these earliest pinnipeds (Potamotherium), focusing in particular on how it used its whiskers (vibrissae). For this purpose, we analyse the coronal gyrus of the brain of 7 fossil and 31 extant carnivorans. This region receives somatosensory input from the head. Our results show that the reliance on whiskers in modern pinnipeds is an ancestral feature that favoured survival of stem pinnipeds in marine habitats. This study provides insights into an impressive ecological transition in carnivoran evolution: from terrestrial to amphibious marine species. Adaptations for underwater foraging were crucial for this transition.

Bayesian Prediction of Multivariate Ecology from Phenotypic Data Yields New Insights into the Diets of Extant and Extinct Taxa.

AbstractMorphology often reflects ecology, enabling the prediction of ecological roles for taxa that lack direct observations, such as fossils. In comparative analyses, ecological traits, like diet, are often treated as categorical, which may aid prediction and simplify analyses but ignores the multivariate nature of ecological niches. Furthermore, methods for quantifying and predicting multivariate ecology remain rare. Here, we ranked the relative importance of 13 food items for a sample of 88 extant carnivoran mammals and then used Bayesian multilevel modeling to assess whether those rankings could be predicted from dental morphology and body size. Traditional diet categories fail to capture the true multivariate nature of carnivoran diets, but Bayesian regression models derived from living taxa have good predictive accuracy for importance ranks. Using our models to predict the importance of individual food items, the multivariate dietary niche, and the nearest extant analogs for a set of data-deficient extant and extinct carnivoran species confirms long-standing ideas for some taxa but yields new insights into the fundamental dietary niches of others. Our approach provides a promising alternative to traditional dietary classifications. Importantly, this approach need not be limited to diet but serves as a general framework for predicting multivariate ecology from phenotypic traits.

Dental topographic proxies for ecological characteristics in carnivoran mammals.

Form-function relationships in mammalian feeding systems are active topics of research in evolutionary biology. This is due principally to their fundamental importance for understanding dietary adaptations in extinct taxa and macro-evolutionary patterns of morphological transformations through changing environments. We hypothesize that three-dimensional dental topographic metrics represent stronger predictors for dietary and other ecological variables than do linear measurements. To test this hypothesis, we measured three dental topographic metrics: Relief Index (RFI), Dirichlet Normal Energy (DNE), and Orientation Patch Count Rotated (OPCR) in 57 extant carnivoran species. Premolar and molar dental topographic indices were regressed against activity, diet breadth, habitat breadth, terrestriality, and trophic level variables within a phylogenetic framework. The results of this study showed significant correlations between RFI and the ecological variables diet breadth and trophic level. Weaker correlations are documented between OPCR and activity and between DNE and trophic level. Our results suggest that cusp height is strongly reflective of dietary ecology in carnivorans as a whole, and represents a proxy mainly for different degrees of hypercarnivory observed within this group of predatory mammals.

The impact of environmental factors on the evolution of brain size in carnivorans

The reasons why some animals have developed larger brains has long been a subject of debate. Yet, it remains unclear which selective pressures may favour the encephalization and how it may act during evolution at different taxonomic scales. Here we studied the patterns and tempo of brain evolution within the order Carnivora and present large-scale comparative analysis of the effect of ecological, environmental, social, and physiological variables on relative brain size in a sample of 174 extant carnivoran species. We found a complex pattern of brain size change between carnivoran families with differences in both the rate and diversity of encephalization. Our findings suggest that during carnivorans’ evolution, a trade-off have occurred between the cognitive advantages of acquiring a relatively large brain allowing to adapt to specific environments, and the metabolic costs of the brain which may constitute a disadvantage when facing the need to colonize new environments.

Concealed weapons: A revised reconstruction of the facial anatomy and life appearance of the sabre-toothed cat Homotherium latidens (Felidae, Machairodontinae)

Homotherium is one of the sabre-toothed felid genera with a more extensive overlap in space and time with species of our own genus Homo, who must have been familiar with the animal, but now we only have its fossil remains to infer its life appearance. A revised reconstruction of the soft tissue and life appearance of Homotherium latidens is proposed here on the basis of new observations on the anatomy of extant carnivorans and a re-evaluation of the fairly preserved skull and mandible from the classical Late Pliocene site of Perrier (France). This fossil specimen provides some of the best information available about the morphology of the skull and mandible. Like other large early specimens of Homotherium, it has enormous upper canines relative to skull size and high-crowned enough to protrude beyond the lips in the living animal. On the other hand, observations of facial expressions in living big cats and dissected specimens show that, contrary to previous conclusions, the soft tissue around the mouth and the lower lip in particular can cover the upper canines of large felids, even when those are considerably high-crowned. Such observations lead us to propose a revised hypothesis about the life appearance of Homotherium and other sabre-toothed carnivorans, where the upper canines may have been covered in life when the mouth was completely closed.

Climbing Adaptations of an Enigmatic Early Arctoid Carnivoran: the Functional Anatomy of the Forelimb of Amphicynodon leptorhynchus From the Lower Oligocene of the Quercy Phosphorites (France)

This paper provides a detailed description and the functional anatomy of the forelimb of an early Oligocene genet-sized arctoid carnivoran, Amphicynodon leptorhynchus, to infer its probable lifestyle. This work represents the first insights into the functional anatomy of the postcranial skeleton and palaeoecology of an emblematic member of the first radiation of arctoid carnivorans, the poorly known Amphicynodontidae, a group very likely related to bears. So far, the Amphicynodontidae have only been studied on the basis of their cranial and dental remains. The fossil site of Itardies (MP23, lower Oligocene), in the Quercy Phosphorites (France), have yielded hundreds of postcranial remains attributed to Am. leptorhynchus, allowing a complete analysis of its locomotor behaviour in comparison to a large sample of extant carnivorans showing diverse lifestyles. The anatomy of the forelimb of Am. leptorhynchus indicates well-developed climbing skills and grasping abilities. Thus, this early arctoid was probably living mostly in trees, moving on the ground basically for foraging as observed in small modern climbing carnivorans such as the red panda or the kinkajou, although some other climbing carnivorans can also live in rocky areas.

Testing the occurrence of convergence in the craniomandibular shape evolution of living carnivorans.

Convergence consists in the independent evolution of similar traits in distantly related species. The mammalian craniomandibular complex constitutes an ideal biological structure to investigate ecomorphological dynamics and the carnivorans, due to their phenotypic variability and ecological flexibility, offer an interesting case study to explore the occurrence of convergent evolution. Here, we applied multiple pattern‐based metrics to test the occurrence of convergence in the craniomandibular shape of extant carnivorans. To this aim, we tested for convergence in many dietary groups and analyzed several cases of carnivoran convergence concerning either ecologically equivalent species or ecologically similar species of different body sizes described in the literature. Our results validate the occurrence of convergence in ecologically equivalent species in a few cases (as well as in the case of giant and red pandas), but almost never support the occurrence of convergent evolution in dietary categories of living carnivorans. Therefore, convergent evolution in this clade appears to be a rare phenomenon. This is probably the consequence of a complex interplay of one‐to‐many, many‐to‐one, and many‐to‐many relationships taking place between ecology, biomechanics, and morphology.

Ecometrics and Neogene faunal turnover: the roles of cats and hindlimb morphology in the assembly of carnivoran communities in the New World

Cats possess some of the highest ankle gear ratios of any extant carnivorans, a feature that facilitates leaping and sprinting involved in ambush predation and scansorial lifestyles. In today's North American carnivoran communities, the high gear ratio of cats contributes to an overall high ecometric average for this trait and contributes strongly to measures of ecometric disparity at the community level. But cats were late additions to North American communities, arriving from Eurasia about 17 Ma at the end of the “cat gap”. This paper uses ecometric analysis to document changes in hindlimb functional diversity in North American carnivoran communities over the last 19 million years in order to better understand the roles of trait evolution, clade turnover, and environmental change in community assembly. To accomplish this, I look at the phylogenetic history of ankle gear ratios of cats and other carnivorans, and the history of their occupation of high gear ratio niches in North American communities. The primary focus is on the Great Plains, which experienced profound changes in vegetation and climate through this period. Across all Carnivoramorpha, including a variety of extinct clades, it was found that gear ratios range from 1.08 (with extant ursids and viverrids and extinct miacids and barbourofelids, one of the three cat groups considered in this paper, having the lowest values) to 1.46 (with extant felids, herpestids, and canids having the highest values). Using the fossil record combined with phylogenetic ancestor reconstruction, it is shown that stem carnivorans and early felids had gear ratios about halfway between these extremes, consistent with a semidigitigrade or mildly digitigrade stance that was not overly specialized for either leaping or sprinting. Barbourofelids and some machairodontines evolved lower gear ratios that emphasized mechanical efficiency over advantage. When cats first entered North American communities in the Miocene they did not occupy high gear ratio niches and, in fact, occupied some of the lowest gear ratio niches during the Barstovian, Clarendonian, and Hemphillian. A major restructuring of gear ratio distributions in North American carnivoran communities occurred during the Blancan that appears to have resulted from clade sorting processes involving the selective loss of low gear ratio groups, as well as the evolution of increased gear ratios in felids and canids.

New fossils of Amphicyonidae (Carnivora) from the middle Miocene (MN6) site of Carpetana (Madrid, Spain)

Herein, we present a study of an interesting sample of fossils of the giant amphicyonid Megamphicyon giganteus (Schinz, 1825) from the Spanish middle Miocene (MN6) site of Carpetana (Madrid city), obtained during public works for the Madrid underground in 2008. Although the dentition of this species is known from other sites, the postcranial bones are very poorly known, and the new material provides new data on the locomotor adaptations of this spectacular predator, and allows an estimation of its body mass, which would be around 600 kg. Surprisingly, despite this giant size, the morphology of both femur and tibia shows that this animal exhibited higher cursorial capacity than large extant carnivorans, such as bears, which together with a high degree of pronation/supination movement of the forearm, reveals adaptations of M. giganteus to occupy the niche of active top predator in middle Miocene ecosystems.

The effects of phylogeny, body size, and locomotor behavior on the three-dimensional shape of the pelvis in extant carnivorans.

The mammalian pelvis is thought to exhibit adaptations to the functional demands of locomotor behaviors. Previous work in primates has identified form-function relationships between pelvic shape and locomotor behavior; few studies have documented such relationships in carnivorans, instead focusing on long bones. Most work on the functional morphology of the carnivoran pelvis, in particular, has used univariate measures, with only a few previous studies incorporating a three-dimensional (3D) analysis. Here we test the hypothesis that carnivoran taxa that are characterized by different locomotor modes also differ in 3D shape of the os coxae. Using 3D geometric morphometrics and phylogenetic comparative methods, we evaluate the phylogenetic, functional, and size-related effects on 3D pelvis shape in a sample of 33 species of carnivorans. Using surface models derived from laser scans, we collected a suite of landmarks (N = 24) and curve semilandmarks (N = 147). Principal component analysis on Procrustes coordinates demonstrates patterns of shape change in the ischiopubis and ilium likely related to allometry. Phylogenetic generalized least squares analysis on principal component scores demonstrates that phylogeny and body size have greater effects on pelvic shape than locomotor function. Our results corroborate recent research finding little evidence of locomotor specialization in the pelvis of carnivorans. More research on pelvic morphological integration and evolvability is necessary to understand the factors driving pelvic evolution in carnivorans.

The possible role of predator-prey dynamics as an influence on early hominin use of burned landscapes.

Foraging in burned areas has been suggested to represent the earliest stage in the use and control of fire by early hominins. Recently burned areas offer immediate foraging benefits including increased search efficiency for high-ranked food items and decreased hunting opportunities for ambush predators. As such, they provide a triple-bonus (reduced risk from ambush, ease of terrestrial travel and higher foraging returns) for some primates. However, previous studies have not yet accounted for other types of predators e.g., coursing (endurance predators that can pursue prey over long distances) which were sympatric with hominins and may also have exploited these environments. Behavioral ecology studies on the use of burned landscapes by extant carnivores demonstrate that while some ambush predators avoid recently burned areas, coursing predators do take advantage of their immediate hunting opportunities. Research examining habitat selection by animals under the simultaneous threat of multiple predator species with different modes of hunting, and the diversity of Plio-Pleistocene carnivore guild is suggestive of two possible evolutionary scenarios in which hominins could either have selected or avoided burned areas (3-2 mya), based on whether ambush or coursing predators were perceived as presenting the greatest risk.

Carnivoran hunting style and phylogeny reflected in bony labyrinth morphometry

Carnivorans are a highly diverse and successful group of mammals, found on the top of the food chain. They originated in the Palaeocene (ca. 60 Ma) and have developed numerous lifestyles, locomotion modes and hunting strategies during their evolutionary history. Mechanosensory organs, such as the inner ear (which houses senses of equilibrium and hearing), represent informative anatomical systems to obtain insights into function, ecology and phylogeny of extant and extinct vertebrates. Using µCT scans, we examined bony labyrinths of a broad sample of various carnivoran species, to obtain new information about hunting behaviours of ancient carnivorans. Bony labyrinths were digitally reconstructed and measurements were taken directly from these 3D models. Principal component analyses generally separated various hunting strategies (pursuit, pounce, ambush and occasional), but also support their phylogenetic relationships (Canoidea vs. Feloidea). The height, width and length of all three semicircular canals show functional morphological adaptations, whereas the diameter of the canals, the height of the cochlea and particularly the angle between the lateral semicircular canal and the cochlea indicate a phylogenetic signal. The results demonstrate that the bony labyrinth provides a powerful ecological proxy reflecting both predatory habits as well as phylogenetic relationships in extinct and extant carnivorans.

Biomechanical simulations of Leptarctus primus (Leptarctinae, Carnivora), and new evidence for a badger-like feeding capability

ABSTRACTVariations in craniodental morphology have been correlated to feeding adaptations in living organisms and used as proxies for paleodiet reconstruction. Within the mammalian order Carnivora, the Miocene fossil musteloid Leptarctus has been variably interpreted as a carnivore, frugivore, herbivore, omnivore, or insectivore based on morphological comparisons with extant species. Here, we perform the first simulation of cranial biomechanics in Leptarctus primus, aiming to identify a living analogue using biomechanical capability rather than qualitative morphology. Finite element models (FEMs) of 18 extant carnivorans and two extinct outgroup taxa were used to compare known diet-biomechanics relationships with the biomechanical properties of L. primus FEMs within a phylogenetic context. Multivariate analyses of simulated bite efficiency and skull stiffness values indicate that L. primus is most similar overall to Taxidea taxus (American badger) in unilateral bite simulations. Based on biomechanical predictions, we postulate that L. primus resembled the American badger in its feeding ecology more closely than any other taxon tested and thus conclude that L. primus was dominantly a carnivore with an auxiliary feeding capability of omnivory. We also compared the L. primus FEMs with the potentially synonymous Hypsoparia bozemanensis to determine a possible range of feeding capabilities. We observed an increase in mechanical efficiency with a deepening of the zygomae of H. bozemanensis, a trait previously used to differentiate it from L. primus. Ongoing work to expand the database of cranial biomechanical simulation data across Carnivoramorpha should help to further clarify evolutionary patterns of skull biomechanical specializations in musteloids and other carnivorans.

Dental microwear textures across cheek teeth in canids: Implications for dietary studies of extant and extinct canids

Dental microwear texture analysis (DMTA) has been instrumental in reconstructing dietary ecology of extinct and extant carnivorans. Current sampling methods for canids focus on lower second molars (m2), where the grinding of flesh and bone captures dental microwear indicative of diet. However, dental microwear on other biomechanically analogous grinding facets (i.e. the talonid basin on the lower carnassial, m1) might be comparable and could help dramatically increase sample sizes of fossil specimens, as carnassials are more frequently recovered and identifiable than lower m2s. Here, we quantify the degree to which dental microwear textures between grinding facets on lower first and second molars are similar in two species of extant canids, coyotes (Canis latrans) and gray wolves (Canis lupus). Casts of paired m1s and m2s for each individual were sampled from museum collections and analyzed for three microwear parameters that correlate with diet in carnivorans: anisotropy, complexity, and textural fill volume. Within wolves, the m1 talonid and m2 are indistinguishable in all DMTA parameters. In coyotes, grinding facets of the m1 talonid and m2 are indistinguishable in complexity and textural fill volume, but anisotropy values of m1s are significantly lower than those of m2s. Differences in anisotropy between species were unlikely to be driven by biomechanical shifts in bite force between the m1 talonid and m2, but could stem from a combination of subtle morphological variation and intra-tooth variation. Overall, these data suggest that regions across molars with similar functions yield similar dental microwear textures. Finally, to demonstrate the effect of increased sample size, we show how the combination of DMTA data from lower m1 talonids and lower m2s of the hypocarnivorous Phlaocyonini canids from the John Day Formation of eastern Oregon, USA, alters the size and shape, but not position, of their reconstructed dietary “niche” space and hence interpretations about dietary behavior.

Detection of Endangered American Martens (Martes americana) in Apostle Islands National Lakeshore, Wisconsin

American martens (Martes americana) warrant concern in Wisconsin, U.S.A., for multiple reasons, including being the state's only endangered mammal and a clan animal of the Ojibwe tribes. American martens were once present throughout much of the state but were extirpated in the early 20th century through habitat loss and unregulated trapping. In the 1950s two reintroductions of martens to Stockton Island of the Apostle Islands archipelago were considered failures, with the last confirmed sighting in the archipelago in 1969. In the decades since the Stockton Island reintroduction efforts, anecdotal reports of martens have surfaced throughout the archipelago. In 2014–2016 we deployed 91 camera traps on 13 of the 21 Apostle Islands to survey the archipelago's extant carnivore species. We detected American martens at 28 of 87 functioning camera trap sites on 5 of 13 monitored islands and documented the existence of American martens in APIS in Wisconsin for the first time in over 50 y. We suggest continued research to evaluate the status of the APIS population and its potential origins to guide future conservation efforts.

Correlates between calcaneal morphology and locomotion in extant and extinct carnivorous mammals.

Locomotor mode is an important component of an animal's ecology, relating to both habitat and substrate choice (e.g., arboreal versus terrestrial) and in the case of carnivores, to mode of predation (e.g., ambush versus pursuit). Here, we examine how the morphology of the calcaneum, the 'heel bone' in the tarsus, correlates with locomotion in extant carnivores. Other studies have confirmed the correlation of calcaneal morphology with locomotion behaviour and habitat. The robust nature of the calcaneum means that it is frequently preserved in the fossil record. Here, we employ linear measurements and 2D-geometric morphometrics on a sample of calcanea from eighty-seven extant carnivorans and demonstrate a signal of correlation between calcaneal morphology and locomotor mode that overrides phylogeny. We used this correlation to determine the locomotor mode, and hence aspects of the palaeobiology of, 47 extinct carnivorous mammal taxa, including both Carnivora and Creodonta. We found ursids (bears), clustered together, separate from the other carnivorans. Our results support greater locomotor diversity for nimravids (the extinct 'false sabertooths', usually considered to be more arboreal), than previously expected. However, there are limitations to interpretation of extinct taxa because their robust morphology is not fully captured in the range of modern carnivoran morphology.

Craniodental and humeral morphology of a new species of Masrasector (Teratodontinae, Hyaenodonta, Placentalia) from the late Eocene of Egypt and locomotor diversity in hyaenodonts.

Hyaenodonta is a diverse clade of carnivorous mammals that were part of terrestrial faunas in the Paleogene of Eurasia and North America, but the oldest record for the group is Afro-Arabian, making the record there vital for understanding the evolution of this wide-spread group. Previous studies show an ancient split between two major clades of hyaenodonts that converged in hypercarnivory: Hyainailourinae and Hyaenodontinae. These clades are each supported by cranial characters. Phylogenetic analyses of hyaenodonts also support the monophyly of Teratodontinae, an Afro-Arabian clade of mesocarnivorous to hypercarnivorous hyaenodonts. Unfortunately, the cranial anatomy of teratodontines is poorly known, and aligning the clade with other lineages has been difficult. Here, a new species of the phylogenetically controversial teratodontine Masrasector is described from Locality 41 (latest Priabonian, late Eocene) from the Fayum Depression, Egypt. The hypodigm includes the most complete remains of a Paleogene teratodontine, including largely complete crania, multiple dentaries, and isolated humeri. Standard and “tip-dating” Bayesian analyses of a character-taxon matrix that samples cranial, postcranial, and dental characters support a monophyletic Masrasector within Teratodontinae, which is consistently placed as a close sister group of Hyainailouridae. The cranial morphology of Masrasector provides new support for an expanded Hyainailouroidea (Teratodontinae + Hyainailouridae), particularly characters of the nuchal crest, palate, and basicranium. A discriminant function analysis was performed using measurements of the distal humerus from a diverse sample of extant carnivorans to infer the locomotor habits of Masrasector. Masrasector was assigned to the “terrestrial” locomotor category, a result consistent with the well-defined medial trochlear ridges, and moderately developed supinator crests of the specimens. Masrasector appears to have been a fast-moving terrestrial form with a diverse diet. These specimens considerably improve our understanding of Teratodontinae, an ancient member of the Afro-Arabian mammalian fauna, and our understanding of hyaenodont diversity before the dispersal of Carnivora to the continent near the end of the Paleogene.

Palaeobiology of Hyaenodon exiguus (Hyaenodonta, Mammalia) based on morphometric analysis of the bony labyrinth.

Species of the extinct genus Hyaenodon were among the largest carnivorous mammals from the Late Eocene through Early Miocene in North America, Europe and Asia. The origin, phylogeny and palaeobiology of Hyaenodonta are still ambiguous. Most previous studies focused on teeth and dental function in these highly adapted species, which might be influenced by convergent morphologies. The anatomy of the bony labyrinth in vertebrates is generally quite conservative and, additionally, was used in functional-morphological studies. This study provides the first anatomical description of the bony labyrinth of the extinct European species Hyaenodon exiguus in comparison to selected extant carnivoran taxa discussed from a functional-morphological perspective. Hyaenodon exiguus may have occupied a hyaena-like dietary niche with a semi-arboreal lifestyle, based on the relative height, width and length of the semicircular canals of the inner ear. However, this contradicts previous functional-morphological studies focusing on the diameter of the canals, which presumably represent the signal of locomotion mode.