A novel trophic cascade between cougars and feral donkeys shapes desert wetlands.

Introduced large herbivores have partly filled ecological gaps formed in the late Pleistocene, when many of the Earth's megafauna were driven extinct. However, extant predators are generally considered incapable of exerting top-down influences on introduced megafauna, leading to unusually strong disturbance and herbivory relative to native herbivores. We report on the first documented predation of juvenile feral donkeys Equus africanus asinus by cougars Puma concolor in the Mojave and Sonoran Deserts of North America. We then investigated how cougar predation corresponds with differences in feral donkey behaviour and associated effects on desert wetlands. Focusing on a feral donkey population in the Death Valley National Park, we used camera traps and vegetation surveys to compare donkey activity patterns and impacts between wetlands with and without cougar predation. Donkeys were primarily diurnal at wetlands with cougar predation, thereby avoiding cougars. However, donkeys were active throughout the day and night at sites without predation. Donkeys were ~87% less active (measured as hours of activity a day) at wetlands with predation (p < 0.0001). Sites with predation had reduced donkey disturbance and herbivory, including ~46% fewer access trails, 43% less trampled bare ground and 192% more canopy cover (PERMANOVA, R2  = 0.22, p = 0.0003). Our study is the first to reveal a trophic cascade involving cougars, feral equids and vegetation. Cougar predation appears to rewire an ancient food web, with diverse implications for modern ecosystems. Our results suggest that protecting apex predators could have important implications for the ecological effects of introduced megafauna.

Subchondral defects resembling osteochondrosis dissecans in joint surfaces of the extinct saber-toothed cat Smilodon fatalis and dire wolf Aenocyon dirus.

Skeletal disease may hamper the behavior of large predators both living and extinct. We investigated the prevalence of osteochondrosis dissecans (OCD), a developmental bone disease affecting the joints, in two Ice Age predators: the saber-toothed cat Smilodon fatalis and dire wolf Aenocyon dirus. As published cases in modern Felidae and wild Canidae are rare, we predicted that subchondral defects resembling OCD would be rare in the extinct predators. We examined limb joints in juvenile and adult S. fatalis: 88 proximal humeri (shoulder), 834 distal femora (stifle), and 214 proximal tibiae. We also examined limb joints in juvenile and adult A. dirus: 242 proximal humeri, 266 distal femora, and 170 proximal tibiae. All specimens are from the Late Pleistocene Rancho La Brea fossil locality in Los Angeles, California, USA. While the Smilodon shoulder and tibia showed no subchondral defects, subchondral defects in the Smilodon femur had a prevalence of 6%; most defects were small (<7mm); and nine adult stifles with defects also showed osteoarthritis. Subchondral defects in the A. dirus femur had a prevalence of 2.6%; most defects were large (>12mm); and five stifles further developed mild osteoarthritis. Subchondral defects in the A. dirus shoulder had a prevalence of 4.5%; most defects were small, and three shoulders developed moderate osteoarthritis. No defects were found in the A. dirus tibia. Contrary to our prediction, we found a high prevalence of subchondral defects in the stifle and shoulder of S. fatalis and A. dirus resembling OCD found in humans and other mammals. As modern dogs affected by OCD are highly inbred, this high prevalence in the fossil taxa may suggest that they experienced inbreeding as they approached extinction. The deep-time history of this disease supports the need for monitoring of animal domestication, as well as conservation, to avoid unexpected surges in OCD under conditions like inbreeding.

Computed tomography reveals hip dysplasia in the extinct Pleistocene saber-tooth cat Smilodon.

Reconstructing the behavior of extinct species is challenging, particularly for those with no living analogues. However, damage preserved as paleopathologies on bone can record how an animal moved in life, potentially reflecting behavioral patterns. Here, we assess hypothesized etiologies of pathology in a pelvis and associated right femur of a Smilodon fatalis saber-toothed cat, one of the best-studied species from the Pleistocene-age Rancho La Brea asphalt seeps, California, USA, using visualization by computed tomography (CT). The pelvis exhibits massive destruction of the right hip socket that was interpreted, for nearly a century, to have developed from trauma and infection. CT imaging reveals instead that the pathological distortions characterize chronic remodeling that began at birth and led to degeneration of the joint over the animal's life. These results suggest that this individual suffered from hip dysplasia, a congenital condition common in domestic dogs and cats. This individual reached adulthood but could not have hunted properly nor defended territory on its own, likely relying on a social group for feeding and protection. While extant social felids are rare, these fossils and others with similar pathologies are consistent with a spectrum of social strategies in Smilodon supported by a predominance of previous studies.

Iterative evolution of large-bodied hypercarnivory in canids benefits species but not clades.

Ecological specialization has costs and benefits at various scales: traits benefitting an individual may disadvantage its population, species or clade. In particular, large body size and hypercarnivory (diet over 70% meat) have evolved repeatedly in mammals; yet large hypercarnivores are thought to be trapped in a macroevolutionary "ratchet", marching unilaterally toward decline. Here, we weigh the impact of this specialization on extinction risk using the rich fossil record of North American canids (dogs). In two of three canid subfamilies over the past 40 million years, diversification of large-bodied hypercarnivores appears constrained at the clade level, biasing specialized lineages to extinction. However, despite shorter species durations, extinction rates of large hypercarnivores have been mostly similar to those of all other canids. Extinction was size- and carnivory-selective only at the end of the Pleistocene epoch 11,000 years ago, suggesting that large hypercarnivores were not disadvantaged at the species level before anthropogenic influence.

Hypercarnivorous teeth and healed injuries to Canis chihliensis from Early Pleistocene Nihewan beds, China, support social hunting for ancestral wolves.

Collaborative hunting by complex social groups is a hallmark of large dogs (Mammalia: Carnivora: Canidae), whose teeth also tend to be hypercarnivorous, specialized toward increased cutting edges for meat consumption and robust p4-m1 complex for cracking bone. The deep history of canid pack hunting is, however, obscure because behavioral evidence is rarely preserved in fossils. Dated to the Early Pleistocene (>1.2 Ma), Canis chihliensis from the Nihewan Basin of northern China is one of the earliest canines to feature a large body size and hypercarnivorous dentition. We present the first known record of dental infection in C. chihliensis, likely inflicted by processing hard food, such as bone. Another individual also suffered a displaced fracture of its tibia and, despite such an incapacitating injury, survived the trauma to heal. The long period required for healing the compound fracture is consistent with social hunting and family care (food-sharing) although alternative explanations exist. Comparison with abundant paleopathological records of the putatively pack-hunting Late Pleistocene dire wolf, Canis dirus, at the Rancho La Brea asphalt seeps in southern California, U.S.A., suggests similarity in feeding behavior and sociality between Chinese and American Canis across space and time. Pack hunting in Canis may be traced back to the Early Pleistocene, well before the appearance of modern wolves, but additional evidence is needed for confirmation.

Dietary specialization is linked to reduced species durations in North American fossil canids.

How traits influence species persistence is a fundamental question in ecology, evolution and palaeontology. We test the relationship between dietary traits and both species duration and locality coverage over 40 million years in North American canids, a clade with considerable ecomorphological disparity and a dense fossil record. Because ecomorphological generalization-broad resource use-may enable species to withstand disturbance, we predicted that canids of average size and mesocarnivory would exhibit longer durations and wider distributions than specialized larger or smaller species. Second, because locality coverage might reflect dispersal ability and/or survivability in a range of habitats, we predicted that high coverage would correspond with longer durations. We find a nonlinear relationship between species duration and degree of carnivory: species at either end of the carnivory spectrum tend to have shorter durations than mesocarnivores. Locality coverage shows no relationship with size, diet or duration. To test whether generalization (medium size, mesocarnivory) corresponds to an adaptive optimum, we fit trait evolution models to previously generated canid phylogenies. Our analyses identify no single optimum in size or diet. Instead, the primary model of size evolution is a classic Cope's Rule increase over time, while dietary evolution does not conform to a single model.

First bone-cracking dog coprolites provide new insight into bone consumption in Borophagus and their unique ecological niche.

Borophagine canids have long been hypothesized to be North American ecological 'avatars' of living hyenas in Africa and Asia, but direct fossil evidence of hyena-like bone consumption is hitherto unknown. We report rare coprolites (fossilized feces) of Borophagus parvus from the late Miocene of California and, for the first time, describe unambiguous evidence that these predatory canids ingested large amounts of bone. Surface morphology, micro-CT analyses, and contextual information reveal (1) droppings in concentrations signifying scent-marking behavior, similar to latrines used by living social carnivorans; (2) routine consumption of skeletons; (3) undissolved bones inside coprolites indicating gastrointestinal similarity to modern striped and brown hyenas; (4) B. parvus body weight of ~24 kg, reaching sizes of obligatory large-prey hunters; and (5) prey size ranging ~35-100 kg. This combination of traits suggests that bone-crushing Borophagus potentially hunted in collaborative social groups and occupied a niche no longer present in North American ecosystems.

Skeletal trauma reflects hunting behaviour in extinct sabre-tooth cats and dire wolves.

Skeletal-injury frequency and distribution are likely to reflect hunting behaviour in predatory vertebrates and might therefore differ between species with distinct hunting modes. Two Pleistocene predators from the Rancho La Brea asphalt seeps, the sabre-tooth cat, Smilodon fatalis, and dire wolf, Canis dirus, represent ambush and pursuit predators, respectively. On the basis of a collection of over 1,900 pathological elements, the frequency of traumatic injury across skeletal elements in these two species was calculated. Here we show that the frequency of trauma in the sabre-tooth cat exceeds that of the dire wolf (4.3% compared to 2.8%), implying that the killing behaviour of S. fatalis entailed greater risk of injury. The distribution of traumatic injuries also differed between the two species. S. fatalis, an ambush predator, was injured more often than expected across the lumbar vertebrae and shoulders whereas C. dirus, a pursuit predator, had higher than expected levels of injury in the limbs and cervical vertebrae. Spatial analysis was used to quantify differences in the distribution of putative hunting injuries. Analysis of injury locations discriminated true hotspots from injury-dense areas and facilitated interpretation of predatory behaviour, demonstrating the use of spatial analyses in the study of vertebrate behaviour and evolution. These results suggest that differences in trauma distribution reflect distinct hazards of each species' hunting mode.