Revisiting the cost of carnivory in mammals

Predator–prey relationships play a key role in the evolution and ecology of carnivores. An understanding of predator–prey relationships and how this differs across species and environments provides information on how carnivorous strategies have evolved and how they may change in response to environmental change. We aim to determine how mammals overcame the challenges of living within the marine environment; specifically, how this altered predator–prey body mass relationships relative to terrestrial mammals. Using predator and prey mass data collected from the literature, we applied phylogenetic piecewise regressions to investigate the relationship between predator and prey size across carnivorous mammals (51 terrestrial and 56 marine mammals). We demonstrate that carnivorous mammals have four broad dietary groups: small marine carnivores (< 11 000 kg) and small terrestrial carnivores (< 11 kg) feed on prey less than 5 kg and 2 kg, respectively. On average, large marine carnivores (> 11 000 kg) feed on prey equal to 0.01% of the carnivore's body size, compared to 45% or greater in large terrestrial carnivores (> 11 kg). We propose that differences in prey availability, and the relative ease of processing large prey in the terrestrial environment and small prey in marine environment, have led to the evolution of these novel foraging behaviours. Our results provide important insights into the selection pressures that may have been faced by early marine mammals and ultimately led to the evolution of a range of feeding strategies and predatory behaviours.     

The evolution of encephalization in caniform carnivorans

A weighted-average model, which reliably estimates endocranial volume from three external measurements of the neurocranium of extant taxa in the mammalian order Carnivora, was tested for its applicability to fossil taxa by comparing model-estimated endocranial volumes to known endocast volumes. The model accurately reproduces endocast volumes for a wide array of fossil taxa across the crown radiation of the Carnivora, three stem carnivoramorphan taxa, and Pleistocene fossils of two extant species. Applying this model to fossil taxa without known endocast volumes expanded the sample of fossil taxa with estimated brain volumes in the carnivoran suborder Caniformia from 11 to 60 taxa. This then allowed a comprehensive assessment of the evolution of relative brain size across this clade. An allometry of brain volume to body mass was calculated on phylogenetically independent contrasts for the set of extant taxa, and from this, log-transformed encephalization quotients (logEQs) were calculated for all taxa, extant, and fossil. A series of Mann-Whitney tests demonstrated that the distributions of logEQs for taxa early in caniform evolutionary history possessed significantly lower median logEQs than extant taxa. Median logEQ showed a pronounced shift around the Miocene-Pliocene transition. Support tests, based on likelihood ratios, demonstrated that the variances of these distributions also were significantly lower than among modern taxa, but logEQ variance increased gradually through the history of the clade, not abruptly. Reconstructions of ancestral logEQs using weighted squared-change parsimony demonstrate that increased encephalization is observed across all major caniform clades (with the possible exception of skunks) and that these increases were achieved in parallel, although an "ancestor-descendant differencing" method could not rule out drift as a hypothesis. Peculiarities in the estimated logEQs for the extinct caniform family Amphicyonidae were also investigated; these unusual patterns are likely due to a unique allometry in scaling brain to body size in this single clade.     

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.     

Skeletal allometry and interlimb scaling patterns in mustelid carnivorans

To address the effects of an evolutionary increase in body size on long bone skeletal allometry, scaling patterns relating body mass, bone length, limb length, midshaft diameters, and cross-sectional properties of the humerus and femur were analyzed for four species of scansorial mustelids. Humeral and, to a lesser extent, femoral allometry is consistent with expectations of elastic similarity: bone and limb length scale with negative allometry on body mass while bone robusticity (cross-sectional parameters against bone length) scales with strong positive allometry. Differences between fore- and hindlimb scaling patterns, however, are observed, with size-dependent increases in forelimb length and humeral strength and robusticity exceeding those of the hindlimb and femur. It is hypothesized that this greater fore- than hindlimb lengthening results in postural modifications that serve to straighten the hindlimb of larger bodied scansorial mustelids relative to smaller mustelids. Straightening of hindlimb joints would more precisely align the long axis of the femur with peak (vertical) ground reaction forces, thereby accounting for the reduction in relative bending stresses acting on the femur compared to the humerus. J. Morphol. 235:121–134, 1998. © 1998 Wiley-Liss, Inc.     

Extinction and replacement among predatory mammals in the North American late Eocene and Oligocene: Tracking a paleoguild over twelve million years

Changes in taxonomic and morphologic diversity within the paleoguild of predatory mammals were explored within a mammalian chronofauna spanning a twelve million year interval, from the latest Eocene to the end of the Oligocene of North America (36–24 ma). The timespan encompassed a modest extinction event among terrestrial mammals (circa 34 ma) followed by a period of relative stability. Morphological diversity was assessed with estimates of body mass, relative tooth size, and tooth shape. Principal component, nearest‐neighbor, and minimum‐spanning‐tree analyses were used to compare morphological diversity and species packing within predator paleoguilds in the mid‐Chadronian (37–34 ma), Orellan (34–32), Whitneyan (32–29.5), and early Arikareean (29.5–24) land mammal ages. Species richness of predators throughout the interval was relatively constant, fluctuating between 15 and 18 total taxa. Moreover, despite significant differences in taxonomic composition and a modest extinction event among terrestrial mammals, morphological diversity within the paleoguild was very similar in the Chadronian and Orellan. In the Whitneyan and especially the early Arikareean, the diversity of feeding adaptations among species declined slightly, largely due to the loss of several highly specialized meat‐eaters (creodonts, nimravids) and the addition of small omnivores (canids).     

Postcranial element shape and function: assessing locomotor mode in extant and extinct mustelid carnivorans

Assessment of locomotor modes in fossil taxa must often be made on the basis of heavily fragmented postcranial material. Previous authors have used quantitative methods to determine locomotor function from whole postcranial elements. The goals of this project were to assess the ability of element shape to discern between locomotor modes through landmark analysis, and to apply the results to assessment of fossils. Results suggest that element shape is a good predictor of function, but that different elements have different predictive capacities for each locomotor mode. Additionally, a relationship between size and shape exists that appears to drive morphological differentiation in the group. Finally, data from the extant sample were applied to fossil material of the extinct Plio-Pleistocene taxon Trigonictis . The results suggest that the locomotor mode of Trigonictis was generalized and probably an intermediate between the half-bound locomotion found in weasels and ferrets and the scansorial locomotion of martens and fishers.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 150 , 895–914.     

Costs of carnivory in the common bladderwort,Utricularia macrorhiza

Summary Carnivorous plants are usually restricted to nutrient-poor environments, suggesting that there is a cost to caputuring animals that is offset by the benefits of carnivory only under unusual circumstances. One such cost could involve a reduced photosynthetic capacity associated with the growth and maintenance of prey-capture organs. This hypothesis is tested using the common bladderwort, Utricularia macrohiza, which bears numerous distinct prey-capture bladders. Measurements of the photosynthetic and respiration rates of leaves and bladders were incorporated into growth models to estimate the growth rates of plants with and without bladders. Comparisons were made in three lakes which differed in nutrient status and in which plants exhibited marked differences in their densities of prey-capture bladders. Overall, photosynthetic rates for leaves were approximately twice those for bladders while respiration rates did not differ significantly between tissues. Calculations incorporating these values indicate that plants producing both bladders and leaves would grow to as little as 21% or as much as 83% of plants that produced leaves alone. Comparisons among lakes led to the rejection of the hypothesis that plants from some lakes are able to produce more bladders per leaf because bladders differ in their photosynthetic productivity.     

Pathologic tooth deformities in modern and fossil chondrichthians: a consequence of feeding-related injury

Deformed teeth are found as rare components of the dentitions of both modern and fossil chondrichthians. Tooth deformities occur as bent or twisted tooth crowns, missing or misshaped cusps, atypical protuberances, perforations, and abnormal root structures. Deformed tooth files consisting of unusually overlapped or small teeth, or teeth misaligned in the jaw also occur in modern forms, but deformed tooth files generally are not recognizable in fossils due to post-mortem dissociation of teeth and jaws. A survey of 200 modern lamniform and carcharhiniform sharks as well as literature sources indicate that such deformities are produced by feeding-related injury to the tooth-forming tissue of the jaws, particularly by impaction of chondrichthian and teleost fin and tail spines. Tooth counts for several late Cretaceous genera, based on material recovered from coastal plain sites from New Jersey to Alabama, suggest that the frequency of occurrence of deformed teeth in a species varies from about 0.015% in Squalicorax kaupi to about 0.36% in Paranomotodon sp. Tooth counts for modern lamniform and carcharhiniform sharks yield a comparable range in frequency of tooth deformities. Variation in frequency of tooth deformity may reflect interspecific differences in feeding behavior and dietary preferences. There is no suggestion in our data of any strong patterns of temporal variation in tooth deformity frequency, or of patterns ­reflecting chondrichthian phylogenetic history and evolution. Skeletal components of the probable prey of the Cretaceous species are preserved in the same horizons as the deformed teeth, and also are found within co-occurring chondrichthian coprolites.     

What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats

1. Understanding the trophic status of consumers in freshwater habitats is central to understanding their ecological roles and significance. Tadpoles are a diverse and abundant component of many freshwater habitats, yet we know relatively little about their feeding ecology and true trophic status compared with many other consumer groups. While many tadpole species are labelled herbivores or detritivores, there is surprisingly little evidence to support these trophic assignments. 2. Here we discuss shortcomings in our knowledge of the feeding ecology and trophic status of tadpoles and provide suggestions and examples of how we can more accurately quantify their trophic status and ecological significance. 3. Given the catastrophic amphibian declines that are ongoing in many regions of the planet, there is a sense of urgency regarding this information. Understanding the varied ecological roles of tadpoles will allow for more effective conservation of remaining populations, benefit captive breeding programmes, and allow for more accurate predictions of the ecological consequences of their losses.     

Dietary habits of the deep-sea flatfish Lepidorhombus boscii in north-eastern Mediterranean waters

Stomach content analysis of four-spotted megrim Lepidorhombus boscii in the oligotrophic Aegean Sea revealed that specimens with fully filled stomachs were rarely encountered. The overall dietary breadth of the species appeared to increase in winter and spring, when stomachs fullness was reduced. The species exhibited a relatively high trophic diversity and could be considered a euryphagous carnivore preying mainly upon crustaceans. Decapod natants, namely Processa canaliculata and Alpheus glaber , dominated in terms of per cent mass, while mysids, represented mainly by Lophogaster typicus , were the most important dietary component in terms of per cent number. Isopods, amphipods and decapod brachyurans were also frequently encountered among stomach contents. Fishes were only ingested by larger specimens (>180 mm total length, L _T); mouth gape dimensions increasing in larger specimens, enabled them to consume larger organisms. Discriminant function analysis showed that size and then sex of predators had the highest weight in discriminating the dietary groups produced by cluster analysis. Resource partitioning along the trophic dimension seemed to exist among smaller males and females (<110 mm L _T), which also presented significant differences in their mouth gape dimensions. The study of the diel feeding pattern of the species demonstrated that foraging activity took place day and night, while observed qualitative differences might partly reflect variations in prey availability on a 24 h basis.     

Effect of feeding method on intake and behaviour of individually reared beef heifers fed a concentrate diet from 115 to 185 kg of body weight

A total of eight Simmental heifers (114 ± 3.2 days old and weighing 118 ± 3.8 kg BW) were used to study the effects of feeding method on intake and animal behaviour in a crossover design experiment. Treatments consisted of feeding concentrate and chopped barley straw as (1) choice (CH; concentrate and straw in separate feedbunks) or (2) total mixed ration (TMR; concentrate and straw in one feedbunk). Feeds were offered on an ad libitum basis, but always maintaining a concentrate to straw ratio of 90 to 10. The experiment was performed in two 21-day periods, and sampling was carried out in the last week of each period. At the end of each period, treatment was changed for heifers; hence, the final number of animals per treatment was eight. Intake was recorded over 7 consecutive days. BW was recorded at the beginning and the end of the experiment and on day 21 of each experimental period. Barley straw was coarsely chopped with a chopping machine. Once chopped, all the straw was handled for particle size separation using the 2-screen Penn State Particle Separator and only material of more than 8 mm was used to feed the heifers. Animal behaviour was video-recorded for 24 h on day 2 and day 6 of each experimental period. Concentrate intake and total dry matter intake of heifers fed with the CH feeding method were higher (P < 0.01 and P < 0.05) than when fed with TMR (5.1 and 5.3 v. 4.7 and 5.0 kg dry matter (DM)/day, respectively). Conversely, barley straw was consumed in higher amounts in heifers fed with the TMR feeding method (0.3 v. 0.2 kg DM/day, respectively; P = 0.001). The total NDF intake was similar in both treatments. In contrast, NDF intake from barley straw and physically effective NDF intake were higher in heifers fed with the TMR feeding method than when fed with CH. Feeding method used to feed heifers did not affect the consumption of the different kinds of barley straw particles and eating and drinking behaviours but affected ruminating behaviour. Heifers fed TMR spent more time ruminating than heifers fed concentrate and barley straw separately (376 v. 287 min/day, respectively; P < 0.01). TMR as the feeding method in intensive beef production systems could be a good approach to promote roughage intake.     

Activity, feeding behaviour and diet of Ogcocephalus vespertilio in southern west Atlantic

The Brazilian batfish Ogcocephalus vespertilio is a nocturnal and early morning predator on bottom invertebrates, staying stationary and hidden in rock holes, crevices or among bottom rocks during the day. While active, it searches for prey walking along the bottom with the help of its specialized paired fins, with the illicium protracted and oscillating or exploring the substrate. The prey are either snapped up from the bottom, after visual detection, or dug out with use of the mouth and rostrum. It feeds on crustaceans (hermit crabs, true crabs, shrimps, amphipods, porcelain crabs, isopods and mysid shrimps), molluscs (snails, sea slugs and clams), polychaete worms (mostly Errantia) and echinoderms (sea urchins and brittle stars).     

Spatial and temporal ecological diversity amongst Eocene primates of France: evidence from teeth

Diet is of paramount importance in the life of a primate. It is also highly variable, as potential food sources vary in spatial distribution and availability over time. The fossil record, due to its fragmentary nature, offers few possibilities to assess the dietary range of a given primate across its spatial and temporal distribution. Here we focus on three taxa, Leptadapis magnus (Adapidae, Adapiformes), Necrolemur cf. antiquus (Microchoeridae, Omomyiformes), and Pseudoloris parvulus (Microchoeridae, Omomyiformes). These taxa occur at different localities of the Late Eocene in the south of France ranging from MP16 (Robiac, Lavergne; 39 Ma), MP17a (La Bouffie, Euzet, Fons 4; 38 Ma) to MP17b (Perrière; 37 Ma). Diets of fossil taxa are assessed here by dental microwear analysis using a comparative database of 11 species of living strepsirhines. On the whole, leaves were a preferred food for the large-bodied Leptadapis (4-5 kg). However, the diet of this taxon varied from a mix of leaves and fruit at La Bouffie, a closed tropical rain forest environment, to a strictly leaf-eating one in the more open environment of Perrière. Based on body mass (200-350 g) and dental microwear patterns, Necrolemur had a mainly fruit-based diet, perhaps supplemented by insects. However, the comparison of the different localities reveals the dietary range of this small-bodied omomyiform which seems to vary between insects and a much softer diet. Pseudoloris had a diet strictly based on insects. Contrary to Leptadapis or Necrolemur, its diet seems to have been confined to insects whatever the locality considered.     

Reversible carnivory in Oxytricha bifaria: a peculiar ecological adaptation

The adaptive significance of the giant form of Oxytricha bifaria has been studied. It proved to be a carnivorous phase of a bacterivorous ciliate, rather than a cannibalistic one. By such a dramatic reversal in the feeding behavior O. bifaria, a primary consumer, can reversibly become a secondary one.     

Pleistocene migration routes into the Americas: Human biological adaptations and environmental constraints

Theories about the routes and timing of human entry into the Americas during the Late Pleistocene usually involve models of lowered sea levels and ice‐free land in Beringia, supported by locations and dates of archeological sites in Northeastern Asia and Northwestern America. Recently, paleoecological reconstructions made possible by advances in geochronology and climatology have received attention. Now morphological adaptations and environmental constraints that affect human activities and physiology need to be considered. Physical accessibility to an area, important as it is, does not alone determine a migration route. In considering any route, anthropologists need to ask: What would it have been like to live in this environment? Did it provide an amenable climate that supported human health and comfort? Between 16,000 and 11,000 cal BP, did this route provide enough food resources and enough hours of sunlight for people with an Upper Paleolithic technology to make a living? We discuss these questions and show ways in which the coastal‐entry model is superior to the interior route through Beringia and an ice‐free corridor.     

Morphology,diet, and stable carbon isotopes: On the diet of Theropithecus and some limits of uniformitarianism in paleoecology

Geladas were long supposed to be the only living primates feeding almost entirely on graminoids and accordingly display dramatic dental and manual adaptive traits. A recent study of Theropithecus gelada, the first in a relatively undisturbed habitat, revealed a more diverse diet, also incorporating large quantities of forbs. The peculiar adaptive traits of T. gelada are also observed in extinct Theropithecus as early as 3.7 Ma. Stable carbon isotopic data of extinct Theropithecus from eastern Africa indicate that specimens older than 3 Ma consumed a significant proportion of C₃ plants (on average ca. 40% of total food intake) whereas specimens younger than 2 Ma consumed more C₄ plants (on average ca. 80%). Recent paleobotanical evidence suggests that C₃ herbaceous plants were still present in non‐negligible proportions in Plio‐Pleistocene lowland tropical ecosystems. Together, the shared morphological adaptive traits of extant and extinct Theropithecus and the varied diets of extant T. gelada suggest that the paleodiets of Theropithecus may have been dominated by herbaceous plants, comprising both C₃ forbs and graminoids and C₄ graminoids. The changes in stable carbon isotopes could correspond to a replacement of C₃ plants by C₄ plants within the herbaceous strata rather than a shift from C₃ woody vegetation to C₄ graminoids. This synthesis highlights the need for a more exhaustive knowledge of the ecology of extant species to achieve meaningful paleodietary and paleoenvironmental reconstructions. A strong selectivity for food resources that are rare in the landscapes (as in T. gelada) should also be considered when interpreting stable carbon isotopes of extinct African mammals (and notably hominids).