Biomechanics of biting in loggerhead shrikes: jaw-closing force, velocity and an argument for power.

Differences in the physical and behavioral attributes of prey are likely to impose disparate demands of force and speed on the jaws of a predator. Because of biomechanical trade-offs between force and speed, this presents an interesting conundrum for predators of diverse prey types. Loggerhead shrikes (Lanius ludovicianus) are medium-sized (∼50 g) passeriform birds that dispatch and feed on a variety of arthropod and vertebrate prey, primarily using their beaks. We used high-speed video of shrikes biting a force transducer in lateral view to obtain corresponding measurements of bite force, upper and lower bill linear and angular displacements, and velocities. Our results show that upper bill depression (about the craniofacial hinge) is more highly correlated with bite force, whereas lower bill elevation is more highly correlated with jaw-closing velocity. These results suggest that the upper and lower jaws might play different roles for generating force and speed (respectively) in these and perhaps other birds as well. We hypothesize that a division of labor between the jaws may allow shrikes to capitalize on elements of force and speed without compromising performance. As expected on theoretical grounds, bite force trades-off against jaw-closing velocity during the act of biting, although peak bite force and jaw-closing velocity across individual shrikes show no clear signs of a force-velocity trade-off. As a result, shrikes appear to bite with jaw-closing velocities and forces that maximize biting power, which may be selectively advantageous for predators of diverse prey that require both jaw-closing force and speed.

Comparative skeletal anatomy of salt marsh and western harvest mice in relation to locomotor ecology.

The salt marsh harvest mouse (Reithrodontomys raviventris) is an endangered species, endemic to the San Francisco Bay Estuary, that co-occurs with the more broadly distributed species, the western harvest mouse (Reithrodontomys megalotis). Despite their considerable external morphological similarities, the northern subspecies of salt marsh harvest mice have relatively longer and thicker tails than do western harvest mice, which may be related to their abilities to climb emergent marsh vegetation to avoid tidal inundation. We used micro-CT to compare post-cranial skeletal anatomy between the salt marsh and western harvest mouse, to examine whether the salt marsh harvest mouse's restriction to brackish marshes is associated with skeletal adaptations for scansorial locomotion. We found that salt marsh harvest mice exhibited a deeper 3rd caudal vertebra, a more caudally located longest tail vertebra, craniocaudally longer tail vertebrae, and a longer digit III proximal phalanx than western harvest mice. These phalangeal and vertebral characteristics are known to decrease body rotations during climbing, increase contact with substrates, and decrease fall susceptibility in arboreal mammals, suggesting that the salt marsh harvest mouse may be morphologically specialized for scansorial locomotion, adaptive for its dynamic wetland environment.

Phenotypic differentiation despite gene flow: Beak morphology, bite performance, and population genetics of Loggerhead Shrikes (Lanius ludovicianus).

Previous studies of Loggerhead Shrikes (Laniidae: Lanius ludovicianus) in North America have indicated considerable intraspecific genetic and phenotypic differentiation, but the congruence between genetic and phenotypic differentiation remains obscure. We examined phenotypic differences in beak shape and bite force among geographic groupings across a 950 km range, from the lower Imperial Valley to the upper Central Valley of California, USA. We integrated these analyses with a population genetic analysis of six microsatellite markers to test for correspondence between phenotypic and genetic differences among geographic groups. We found significant phenotypic differentiation despite a lack of significant genetic differentiation among groups. Pairwise beak shape and bite force distances nevertheless were correlated with genetic (F ST) distances among geographic groups. Furthermore, the phenotypic and genetic distance matrices were correlated with pairwise geographic distances. Takentogether, these results suggest that phenotypic differences might be influenced by neutral processes, inbreeding (as indicated by high heterozygosity deficiencies we observed), local adaptation, and/or phenotypic plasticity.

Repeated Evolution of Unorthodox Feeding Styles Drives a Negative Correlation between Foot Size and Bill Length in Hummingbirds.

AbstractDifferences among hummingbird species in bill length and shape have rightly been viewed as adaptive in relation to the morphology of the flowers they visit for nectar. In this study we examine functional variation in a behaviorally related but neglected feature: hummingbird feet. We gathered records of hummingbirds clinging by their feet to feed legitimately as pollinators or illegitimately as nectar robbers-"unorthodox" feeding behaviors. We measured key features of bills and feet for 220 species of hummingbirds and compared the 66 known "clinger" species (covering virtually the entire scope of hummingbird body size) with the 144 presumed "non-clinger" species. Once the effects of phylogenetic signal, body size, and elevation above sea level are accounted for statistically, hummingbirds display a surprising but functionally interpretable negative correlation. Clingers with short bills and long hallux (hind-toe) claws have evolved-independently-more than 20 times and in every major clade. Their biomechanically enhanced feet allow them to save energy by clinging to feed legitimately on short-corolla flowers and by stealing nectar from long-corolla flowers. In contrast, long-billed species have shorter hallux claws, as plant species with long-corolla flowers enforce hovering to feed, simply by the way they present their flowers.

Geometric morphometric analysis of the humerus in New and Old World vultures.

The vulture guild is composed of two distinct groups, Old and New World, which provide a unique insight into how morphology varies among convergent species. All vultures are considered to be large birds of prey that utilize a style of flight called thermal soaring to search and feed primarily on carrion. Even though this flight style is exhibited among all 23 species, slight variations in their skeletal morphology may relate to their differences in ecology. We hypothesized that vulture humeral morphology varies in relation to these organisms' habitat, average body mass, courtship displays, and migratory behavior. To address this hypothesis, we used three-dimensional geometric morphometrics to measure the overall shape differences of vulture humeri. Humeral morphology was found to vary most by habitat association and migratory tendency. The humeri of vultures that inhabit forested areas exhibit features that suggest increased flapping flight compared to those in open and mountainous regions. Migratory species were found to possess more robust features near the glenohumeral joint. We found these (and other features) have some utility for predicting ecology and behavior, but we suggest that further investigation into skeletal and muscular wing elements may reveal greater understanding of the habits of extinct vulture species.

Behavioral correlates of semi-zygodactyly in Ospreys (Pandion haliaetus) based on analysis of internet images.

Ospreys are renowned for their fishing abilities, which have largely been attributed to their specialized talon morphology and semi-zygodactyly-the ability to rotate the fourth toe to accompany the first toe in opposition of toes II and III. Anecdotal observations indicate that zygodactyly in Ospreys is associated with prey capture, although to our knowledge this has not been rigorously tested. As a first pass toward understanding the functional significance of semi-zygodactyly in Ospreys, we scoured the internet for images of Osprey feet in a variety of circumstances. From these we cross-tabulated the number of times each of three toe configurations (anisodactylous, zygodactylous, and an intermediate condition between these) was associated with different grasping scenarios (e.g., grasping prey or perched), contact conditions (e.g., fish, other objects, or substrate), object sizes (relative to foot size), and grasping behaviors (e.g., using one or both feet). Our analysis confirms an association between zygodactyly and grasping behavior; the odds that an osprey exhibited zygodactyly while grasping objects in flight were 5.7 times greater than whilst perched. Furthermore, the odds of zygodactyly during single-foot grasps were 4.1 times greater when pictured grasping fish compared to other objects. These results suggest a functional association between predatory behavior and zygodactyly and has implications for the selective role of predatory performance in the evolution of zygodactyly more generally.

Come on baby, let's do the twist: the kinematics of killing in loggerhead shrikes.

Shrikes use their beaks for procuring, dispatching and processing their arthropod and vertebrate prey. However, it is not clear how the raptor-like bill of this predatory songbird functions to kill vertebrate prey that may weigh more than the shrike itself. In this paper, using high-speed videography, we observed that upon seizing prey with their beaks, shrikes performed rapid (6-17 Hz; 49-71 rad s-1) axial head-rolling movements. These movements accelerated the bodies of their prey about their own necks at g-forces of approximately 6 g, and may be sufficient to cause pathological damage to the cervical vertebrae and spinal cord. Thus, when tackling relatively large vertebrates, shrikes appear to use inertia of their prey's own body against them.

Mechanical analysis of avian feet: multiarticular muscles in grasping and perching.

The grasping capability of birds' feet is a hallmark of their evolution, but the mechanics of avian foot function are not well understood. Two evolutionary trends that contribute to the mechanical complexity of the avian foot are the variation in the relative lengths of the phalanges and the subdivision and variation of the digital flexor musculature observed among taxa. We modelled the grasping behaviour of a simplified bird foot in response to the downward and upward forces imparted by carrying and perching tasks, respectively. Specifically, we compared the performance of various foot geometries performing these tasks when actuated by distally inserted flexors only, versus by both distally inserted and proximally inserted flexors. Our analysis demonstrates that most species possess relative phalanx lengths that are conducive to grasps actuated only by a single distally inserted tendon per digit. Furthermore, proximally inserted flexors are often required during perching, but the distally inserted flexors are sufficient when grasping and carrying objects. These results are reflected in differences in the relative development of proximally and distally inserted digital flexor musculature among 'perching' and 'grasping' taxa. Thus, our results shed light on the relative roles of variation in phalanx length and digit flexor muscle distribution in an integrative, mechanical context.

Nest-building behavior of Monk Parakeets and insights into potential mechanisms for reducing damage to utility poles.

The Monk Parakeet (Myiopsitta monachus) commonly uses utility poles as a substrate for building large, bulky nests. These nests often cause fires and electric power outages, creating public safety risks and increasing liability and maintenance costs for electric companies. Previous research has focused on lethal methods and chemical contraception to prevent nesting on utility poles and electrical substations. However, implementation of lethal methods has led to public protests and lawsuits, while chemical contraception may affect other than the targeted species, and must be continually reapplied for effectiveness. One non-lethal alternative, nest removal, is costly and may not be a sustainable measure if Monk Parakeet populations continue to grow. In order to identify cost-effective non-lethal solutions to problems caused by Monk Parakeet nesting, we studied their behavior as they built nests on utility poles. Monk Parakeets initiate nests by attaching sticks at the intersection of the pole and electric lines. We found that parakeets use the electric lines exclusively to gain access to the intersection of lines and pole during nest initiation, and continue to use the lines intensively throughout construction. Monk Parakeets also have more difficulty attaching sticks during the early stages of nest construction than when the nest is nearing completion. These findings suggest that intervention during the earlier stages of nest building, by excluding Monk Parakeets from electric lines adjacent to poles, may be an effective, non-lethal method of reducing or eliminating parakeets nesting on, and damaging, utility poles.

Getting a grip on tetrapod grasping: form, function, and evolution.

Human beings have been credited with unparalleled capabilities for digital prehension grasping. However, grasping behaviour is widespread among tetrapods. The propensity to grasp, and the anatomical characteristics that underlie it, appear in all of the major groups of tetrapods with the possible exception of terrestrial turtles. Although some features are synapomorphic to the tetrapod clade, such as well-defined digits and digital musculature, other features, such as opposable digits and tendon configurations, appear to have evolved independently in many lineages. Here we examine the incidence, functional morphology, and evolution of grasping across four major tetrapod clades. Our review suggests that the ability to grasp with the manus and pes is considerably more widespread, and ecologically and evolutionarily important, than previously thought. The morphological bases and ecological factors that govern grasping abilities may differ among tetrapods, yet the selective forces shaping them are likely similar. We suggest that further investigation into grasping form and function within and among these clades may expose a greater role for grasping ability in the evolutionary success of many tetrapod lineages.

In vivo bite and grip forces, morphology and prey-killing behavior of North American accipiters (Accipitridae) and falcons (Falconidae).

Raptors exhibit a diversity of strategies to procure their prey but ultimately kill using their beaks and/or talons. Thus, bite and grip forces are ecologically important variables that have direct survival implications. Whereas hawks rely primarily on their feet for killing prey, falcons tend to employ their beaks. Consequently, falcons are expected to achieve relatively greater bite forces, and hawks are expected to generate relatively greater grip forces. Force estimates predicted from musculoskeletal morphology in a previous study indicated that falcons (Falco spp.) possess greater jaw force capabilities than accipiters (Accipiter spp.) but there were no clear differences in predicted grip-force capacity outside of differences in scaling. The objective of this study was to complement those results with measurements of in vivo forces by inducing captive and wild accipiters and falcons to bite and grasp force transducers. Bite force increased isometrically in both groups whereas grip force tended toward positive allometry. After adjusting for body mass, falcons produced greater bite forces, and accipiters produced greater grip forces. Thus, previous anatomical estimates of forces predicted the expected direction and magnitude of differences in bite forces but the overall greater in vivo grip forces of accipiters deviated from the pattern obtained from biomechanical estimates. Although the scaling relationships were similar between data sets, forces generated by live birds were consistently lower than those predicted from biomechanics. Estimated and in vivo jaw and digital forces were nevertheless correlated, and therefore provide an important link between morphology and killing behavior in these raptors.

Musculoskeletal underpinnings to differences in killing behavior between North American accipiters (Falconiformes: Accipitridae) and falcons (Falconidae).

Accipiters (Accipiter spp.) and falcons (Falco spp.) both use their feet to seize prey, but falcons kill primarily with their beaks, whereas accipiters kill with their feet. This study examines the mechanistic basis to differences in their modes of dispatching prey, by focusing on the myology and biomechanics of the jaws, digits, and distal hindlimb. Bite, grip, and distal hindlimb flexion forces were estimated from measurements of physiological cross-sectional area (PCSA) and indices of mechanical advantage (MA) for the major jaw adductors, and digit and tarsometatarsal flexors. Estimated bite force, total jaw adductor PCSA, and jaw MA (averaged over adductors) tended to be relatively and absolutely greater in falcons, reflecting their emphasis on biting for dispatching their prey. Differences between genera in estimated grip force, total digit flexor PCSA, and digit MA (averaged over inter-phalangeal joints and digits) were not as clear-cut; each of these parameters scaled positively allometric in accipiters, which may reflect the scaling of both prey size, and the proportion of mammalian prey consumed by this lineage with increasing body size. Estimated tarsometatarsal force was greater in falcons than in accipiters, due to their greater MA, which may reflect selection for incurring greater forces during prey strikes. Conversely, the comparatively lower tarsometatarsal MA in accipiters reflects their capacity for greater foot speed potentially necessary for grasping elusive prey. Thus, this study elucidates how differences in jaw and hindlimb musculoskeletal morphology of accipiters and falcons are reflected in differences in their killing modes, and through differences in their force-generating capacities.