Jose Iriarte-Diaz

Quantifying the complexity of bat wing kinematics

Body motions (kinematics) of animals can be dimensionally complex, especially when flexible parts of the body interact with a surrounding fluid. In these systems, tracking motion completely can be difficult, and result in a large number of correlated measurements, with unclear contributions of each parameter to performance. Workers typically get around this by deciding a priori which variables are important (wing camber, stroke amplitude, etc.), and focusing only on those variables, but this constrains the ability of a study to uncover variables of influence. Here, we describe an application of proper orthogonal decomposition (POD) for assigning importances to kinematic variables, using dimensional complexity as a metric. We apply this method to bat flight kinematics, addressing three questions: (1) Does dimensional complexity of motion change with speed? (2) What body markers are optimal for capturing dimensional complexity? (3) What variables should a simplified reconstruction of bat flight include in order to maximally reconstruct actual dimensional complexity? We measured the motions of 17 kinematic markers (20 joint angles) on a bat (Cynopterus brachyotis) flying in a wind tunnel at nine speeds. Dimensional complexity did not change with flight speed, despite changes in the kinematics themselves, suggesting that the relative efficacy of a given number of dimensions for reconstructing kinematics is conserved across speeds. By looking at subsets of the full 17-marker set, we found that using more markers improved resolution of kinematic dimensional complexity, but that the benefit of adding markers diminished as the total number of markers increased. Dimensional complexity was highest when the hindlimb and several points along digits III and IV were tracked. Also, we uncovered three groups of joints that move together during flight by using POD to quantify correlations of motion. These groups describe 14/20 joint angles, and provide a framework for models of bat flight for experimental and modeling purposes.

In vivo bone strain and finite-element modeling of the craniofacial haft in catarrhine primates.

Hypotheses regarding patterns of stress, strain and deformation in the craniofacial skeleton are central to adaptive explanations for the evolution of primate craniofacial form. The complexity of craniofacial skeletal morphology makes it difficult to evaluate these hypotheses with in vivo bone strain data. In this paper, new in vivo bone strain data from the intraorbital surfaces of the supraorbital torus, postorbital bar and postorbital septum, the anterior surface of the postorbital bar, and the anterior root of the zygoma are combined with published data from the supraorbital region and zygomatic arch to evaluate the validity of a finite‐element model (FEM) of a macaque cranium during mastication. The behavior of this model is then used to test hypotheses regarding the overall deformation regime in the craniofacial haft of macaques. This FEM constitutes a hypothesis regarding deformation of the facial skeleton during mastication. A simplified verbal description of the deformation regime in the macaque FEM is as follows. Inferior bending and twisting of the zygomatic arches about a rostrocaudal axis exerts inferolaterally directed tensile forces on the lateral orbital wall, bending the wall and the supraorbital torus in frontal planes and bending and shearing the infraorbital region and anterior zygoma root in frontal planes. Similar deformation regimes also characterize the crania of Homo and Gorilla under in vitro loading conditions and may be shared among extant catarrhines. Relatively high strain magnitudes in the anterior root of the zygoma suggest that the morphology of this region may be important for resisting forces generated during feeding.

Innovative Approaches to the Relationship Between Diet and Mandibular Morphology in Primates

Attempts to establish relationships between mandibular morphology and either traditional dietary categories or geometric and material properties of primate diets have not been particularly successful. Using our conceptual framework of the feeding factors impacting mandibular morphology, we argue that this is because dietary categories and food geometric and material properties affect mandibular morphology only through intervening variables that are currently poorly understood, i.e., feeding behavior, mandibular loading, and stress and strain regimes. Our studies of 3-dimensional jaw kinematics in macaques and capuchins show that, although jaw movement profiles during chewing are affected by food material properties and species-level effects, patterns of jaw movements in these two species are broadly similar. However, because mandibular loading, stress, and strain regimes are determined by interactions between feeding behavior (such as jaw kinematics) and mandibular morphology, it is difficult to say whether these similarities in chewing kinematics also mean similarities in loading, stress, and strain. Comparative analyses of the scaling of daily feeding time and chew cycle duration reveal only weak support for the hypothesis that larger primates chew more than smaller primates. Consideration of these results suggests that better data are needed on the relationship between dietary categories, food material and geometric properties, the amount of time/cycles associated with different feeding behaviors (ingestion, premolar biting, mastication), and mandible stress and strain patterns if we are to understand fully relationships between mandibular morphology and diet in primates.

Kinematics of slow turn maneuvering in the fruit bat Cynopterus brachyotis

SUMMARY Maneuvering abilities have long been considered key factors that influence habitat selection and foraging strategies in bats. To date, however, very little experimental work has been carried out to understand the mechanisms that bats use to perform maneuvers. In the present study, we examined the kinematics of slow-speed turning flight in the lesser short-nosed fruit bat, Cynopterus brachyotis, to understand the basic mechanics employed to perform maneuvers and to compare them with previous findings in bats and other flying organisms. Four individuals were trained to fly in L-shaped flight enclosure that required them to make a 90 deg. turn midway through each flight. Flights were recorded with three low-light, high-speed videocameras, allowing the three-dimensional reconstruction of the body and wing kinematics. For any flying organisms, turning requires changes of the direction of travel and the reorientation of the body around the center of mass to maintain the alignment with the flight direction. In C. brachyotis, changes in body orientation (i.e. heading) took place during upstroke and preceded the changes in flight direction, which were restricted to the downstroke portion of the wingbeat cycle. Mean change in flight direction was significantly correlated to the mean heading angular velocity at the beginning of the downstroke and to the mean bank angle during downstroke, although only heading velocity was significant when both variables were considered. Body reorientation prior to changes in direction might be a mechanism to maintain the head and body aligned with the direction of travel and, thus, maximizing spatial accuracy in three-dimensionally complex environments.

Wing structure and the aerodynamic basis of flight in bats

Powered, flapping flight has evolved at least four times in the Animal Kingdom: in insects, birds, pterosaurs, and bats. Although some aspects of flight mechanics are probably common to all of these lineages, each of the four represents a unique solution to the challenges of maneuverable flapping flight at animal length scales. Flight is less well documented and understood for bats than birds and insects, and may provide novel inspiration for vehicle design. In particular, bat wings are made of quite flexible bones supporting very compliant and anisotropic wing membranes, and possess many more independently controllable joints than those of other animals. We show that the mechanical characteristics of wing skin play an important role in determining aerodynamic characteristics of the wing, and that motions at the many hand joints are integrated to produce complex and functionally versatile dynamic wing conformations.

The effect of body size on the wing movements of pteropodid bats, with insights into thrust and lift production

SUMMARY In this study we compared the wing kinematics of 27 bats representing six pteropodid species ranging more than 40 times in body mass (Mb=0.0278–1.152 kg), to determine whether wing posture and overall wing kinematics scaled as predicted according to theory. The smallest species flew in a wind tunnel and the other five species in a flight corridor. Seventeen kinematic markers on the midline and left side of the body were tracked in three dimensions. We used phylogenetically informed reduced major axis regression to test for allometry. We found that maximum wingspan (bmax) and maximum wing area (Smax) scaled with more positive allometry, and wing loading (Qs) with more negative allometry (bmax∝Mb0.423; Smax∝Mb0.768; Qs∝Mb0.233) than has been reported in previous studies that were based on measurements from specimens stretched out flat on a horizontal surface. Our results suggest that larger bats open their wings more fully than small bats do in flight, and that for bats, body measurements alone cannot be used to predict the conformation of the wings in flight. Several kinematic variables, including downstroke ratio, wing stroke amplitude, stroke plane angle, wing camber and Strouhal number, did not change significantly with body size, demonstrating that many aspects of wing kinematics are similar across this range of body sizes. Whereas aerodynamic theory suggests that preferred flight speed should increase with mass, we did not observe an increase in preferred flight speed with mass. Instead, larger bats had higher lift coefficients (CL) than did small bats (CL∝Mb0.170). Also, the slope of the wingbeat period (T) to body mass regression was significantly more shallow than expected under isometry (T∝Mb0.180), and angle of attack (α) increased significantly with body mass [α∝log(Mb)7.738]. None of the bats in our study flew at constant speed, so we used multiple regression to isolate the changes in wing kinematics that correlated with changes in flight speed, horizontal acceleration and vertical acceleration. We uncovered several significant trends that were consistent among species. Our results demonstrate that for medium- to large-sized bats, the ways that bats modulate their wing kinematics to produce thrust and lift over the course of a wingbeat cycle are independent of body size.

Whole-body kinematics of a fruit bat reveal the influence of wing inertia on body accelerations

SUMMARY The center of mass (COM) of a flying animal accelerates through space because of aerodynamic and gravitational forces. For vertebrates, changes in the position of a landmark on the body have been widely used to estimate net aerodynamic forces. The flapping of relatively massive wings, however, might induce inertial forces that cause markers on the body to move independently of the COM, thus making them unreliable indicators of aerodynamic force. We used high-speed three-dimensional kinematics from wind tunnel flights of four lesser dog-faced fruit bats, Cynopterus brachyotis, at speeds ranging from 2.4 to 7.8 m s–1 to construct a time-varying model of the mass distribution of the bats and to estimate changes in the position of their COM through time. We compared accelerations calculated by markers on the trunk with accelerations calculated from the estimated COM and we found significant inertial effects on both horizontal and vertical accelerations. We discuss the effect of these inertial accelerations on the long-held idea that, during slow flights, bats accelerate their COM forward during ‘tip-reversal upstrokes’, whereby the distal portion of the wing moves upward and backward with respect to still air. This idea has been supported by the observation that markers placed on the body accelerate forward during tip-reversal upstrokes. As in previously published studies, we observed that markers on the trunk accelerated forward during the tip-reversal upstrokes. When removing inertial effects, however, we found that the COM accelerated forward primarily during the downstroke. These results highlight the crucial importance of the incorporation of inertial effects of wing motion in the analysis of flapping flight.

The impact of bone and suture material properties on mandibular function in Alligator mississippiensis: testing theoretical phenotypes with finite element analysis.

The functional effects of bone and suture stiffness were considered here using finite element models representing three different theoretical phenotypes of an Alligator mississippiensis mandible. The models were loaded using force estimates derived from muscle architecture in dissected specimens, constrained at the 18th and 19th teeth in the upper jaw and 19th tooth of the lower jaw, as well as at the quadrate‐articular joint. Stiffness was varied systematically in each theoretical phenotype. The three theoretical phenotypes included: (i) linear elastic isotropic bone of varying stiffness and no sutures; (ii) linear elastic orthotropic bone of varying stiffness with no sutures; and (iii) linear elastic isotropic bone of a constant stiffness with varying suture stiffness. Variation in the isotropic material properties of bone primarily resulted in changes in the magnitude of principal strain. By comparison, variation in the orthotropic material properties of bone and isotropic material properties of sutures resulted in: a greater number of bricks becoming either more compressive or more tensile, changing between being either dominantly compressive or tensile, and having larger changes in the orientation of maximum principal strain. These data indicate that variation in these model properties resulted in changes to the strain regime of the model, highlighting the importance of using biologically verified material properties when modeling vertebrate bones. When bones were compared within each set, the response of each to changing material properties varied. In two of the 12 bones in the mandible, varied material properties within sutures resulted in a decrease in the magnitude of principal strain in bricks adjacent to the bone/suture interface and decreases in stored elastic energy. The varied response of the mandibular bones to changes in suture stiffness highlights the importance of defining the appropriate functional unit when addressing relationships of performance and morphology.

What does feeding system morphology tell us about feeding

Feeding is the set of behaviors whereby organisms acquire and process the energy required for survival and reproduction. Thus, feeding system morphology is presumably subject to selection to maintain or improve feeding performance. Relationships among feeding system morphology, feeding behavior, and diet not only explain the morphological diversity of extant primates, but can also be used to reconstruct feeding behavior and diet in fossil taxa. Dental morphology has long been known to reflect aspects of feeding behavior and diet but strong relationships of craniomandibular morphology to feeding behavior and diet have yet to be defined.

Sources of Variance in Temporal and Spatial Aspects of Jaw Kinematics in Two Species of Primates Feeding on Foods of Different Properties

Chewing kinematics reflects interactions between centrally generated motor signals and peripheral sensory feedback from the constantly changing oral environment. Chewing is a strongly modulated behavior that responds to differences in material properties among different type of foods and to changes in the external physical properties of the food as the bolus gets processed. Feeding, as any complex biological behavior, presents variation at multiple hierarchical levels, from among species or higher-order levels to variation among chewing cycles within a single feeding sequence. Thus, to understand the mechanics and evolution of feeding systems requires estimation of how this variation is distributed across each of these hierarchical levels, which in turn requires large sample sizes. The development of affordable, high-resolution, three-dimensional kinematic recording systems has increased our ability to collect large amounts of data on complete or near-complete feeding sequences that can be used to shed light on the mechanisms of control in vertebrate feeding. In this study, we present data on the nature and sources of variation (from species to chewing cycle levels) in kinematics of chewing in two species of primates, Cebus and Macaca, while they feed on foods of known material properties. Variation in chewing kinematics was not evenly distributed among hierarchical levels. Most of the variation was observed among chewing cycles, most likely in response to changes in the external properties of the food bolus throughout the feeding sequence. Species differences were found in duration and vertical displacement during slow-close phase suggesting that each species exhibits different power stroke dynamics. Cebus exhibited more variable gape cycles than did Macaca, in particular when eating low-toughness foods. This increased ability to temporally and spatially modulate the gape cycle may reflect increased efficiency in processing food because Cebus monkeys use fewer, but longer cycles, than does Macaca when feeding on low-toughness foods. This is due to an increase in duration of the jaw-opening phases of the gape cycle, when the tongue repositions the food bolus in the oral cavity.