Publications

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2016

A three dimensional free body analysis describing variation in the musculoskeletal configuration of the cynodont lower jaw
Evolution & Development (2016) 18:41-53
Reed DA, Iriarte-Diaz J & Diekwisch TGH

A three dimensional free body analysis describing variation in the musculoskeletal configuration of the cynodont lower jaw
Evolution & Development (2016) 18: 41-53
Reed DA, Iriarte-Diaz J & Diekwisch TGH

The evolution of the middle ear from the cynodont craniomandibular bones is one of the key mammalian innovations, and the mechanics underlying this anatomical transformation represents an intriguing paradox. Because the jaw joint of nonmammalian cynodonts was functionally coupled to the inner ear, auditory performance would favor low joint reaction forces. However, this could not be achieved at the expense of feeding performance, favoring high bite forces. The balance of these two seemingly incompatible performance criteria in the context of the morphological diversity of the cynodont lower jaw is poorly understood. Here we derive a series of equations using three dimensional free body analysis that describe the relationship between the orientation and position of the jaw elevator muscles, the position of the jaw articulation relative to the bite point, the joint reaction forces and the bite force in the lower jaw of the nonmammalian cynodont Probainognathus. These equations permit the effects of variation in each variable to be tested independently, yielding three terms that act to limit joint reaction forces without substantially impacting bite force: the reorientation of the resultant muscle force more vertically, shifting the position of the bite point medial to the jaw articulation, and elevating the jaw articulation above the level with the tooth row only when the muscles are oriented principally in the anterior direction. The predictions from our equations provide insights for functional interpretations of patterns of morphological diversity in the cynodont fossil record. They also illustrate that the musculoskeletal configuration of the cynodont lower jaw can be evolutionarily labile without negatively impacting the dual performance criteria of the auditory and feeding system.

2015

Bone strain magnitude is correlated with bone strain rate in tetrapods: implications for models of mechanotransduction
Proceedings of the Royal Society B (2015) 282: 20150321
Aiello BR, Iriarte-Diaz J, Blob RW, Butcher MT, Carrano MT, Espinoza NR, Main RP & Ross CF

Bone strain magnitude is correlated with bone strain rate in tetrapods: implications for models of mechanotransduction
Proceedings of the Royal Society B (2015) 282: 20150321
Aiello BR, Iriarte-Diaz J, Blob RW, Butcher MT, Carrano MT, Espinoza NR, Main RP & Ross CF

Hypotheses suggest that structural integrity of vertebrate bones is maintained by controlling bone strain magnitude via adaptive modelling in response to mechanical stimuli. Increased tissue-level strain magnitude and rate have both been identified as potent stimuli leading to increased bone formation. Mechanotransduction models hypothesize that osteocytes sense bone deformation by detecting fluid flow-induced drag in the bone's lacunar–canalicular porosity. This model suggests that the osteocyte's intracellular response depends on fluid-flow rate, a product of bone strain rate and gradient, but does not provide a mechanism for detection of strain magnitude. Such a mechanism is necessary for bone modelling to adapt to loads, because strain magnitude is an important determinant of skeletal fracture. Using strain gauge data from the limb bones of amphibians, reptiles, birds and mammals, we identified strong correlations between strain rate and magnitude across clades employing diverse locomotor styles and degrees of rhythmicity. The breadth of our sample suggests that this pattern is likely to be a common feature of tetrapod bone loading. Moreover, finding that bone strain magnitude is encoded in strain rate at the tissue level is consistent with the hypothesis that it might be encoded in fluid-flow rate at the cellular level, facilitating bone adaptation via mechanotransduction.

2014

What does feeding system morphology tell us about feeding?
Evolutionary Anthropology (2014) 23: 105-120
Ross CF & Iriarte-Diaz J

What does feeding system morphology tell us about feeding?
Evolutionary Anthropology (2014) 23:105-120
Ross CF & Iriarte-Diaz J

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. To understand why this might be, we review here the field of primate feeding biomechanics.

In vivo cranial bone strain and bite force in the agamid lizard Uromastyx geyri
Journal of Experimental Biology (2014) 217: 1983-1992
Porro LB, Ross CF, Iriarte-Diaz J, O’Reilly JC, Evans SE & Fagan MJ

In vivo cranial bone strain and bite force in the agamid lizard Uromastyx geyri
Journal of Experimental Biology (2014) 217: 1983-1992
Porro LB, Ross CF, Iriarte-Diaz J, O’Reilly JC, Evans SE & Fagan MJ

In vivo bone strain data are the most direct evidence of deformation and strain regimes in the vertebrate cranium during feeding and can provide important insights into skull morphology. Strain data have been collected during feeding across a wide range of mammals; in contrast, in vivo cranial bone strain data have been collected from few sauropsid taxa. Here we present bone strain data recorded from the jugal of the herbivorous agamid lizard Uromastyx geyri along with simultaneously recorded bite force. Principal and shear strain magnitudes in Uromastyx were lower than cranial bone strains recorded in Alligator but higher than those reported from herbivorous mammals. Our results suggest that variations in principal strain orientations in the facial skeleton are largely due to differences in feeding behavior and bite location, whereas food type has little impact on strain orientations. Furthermore, mean principal strain orientations differ between male and female Uromastyx during feeding, potentially due to sexual dimorphism in skull morphology.

Walking like dinosaurs: Chickens with artificial tails provide clues about non-avian theropod locomotion
PLoS ONE (2014) 9 (2): e88458
Grossi B, Iriarte-Diaz J, Larach O, Canals M & Vasquez RA

Walking like dinosaurs: Chickens with artificial tails provide clues about non-avian theropod locomotion
PLoS ONE (2014) 9 (2): e88458
Grossi B, Iriarte-Diaz J, Larach O, Canals M & Vasquez RA

Birds still share many traits with their dinosaur ancestors, making them the best living group to reconstruct certain aspects of non-avian theropod biology. Bipedal, digitigrade locomotion and parasagittal hindlimb movement are some of those inherited traits. Living birds, however, maintain an unusually crouched hindlimb posture and locomotion powered by knee flexion, in contrast to the inferred primitive condition of non-avian theropods: more upright posture and limb movement powered by femur retraction. Such functional differences, which are associated with a gradual, anterior shift of the centre of mass in theropods along the bird line, make the use of extant birds to study non-avian theropod locomotion problematic. Here we show that, by experimentally manipulating the location of the centre of mass in living birds, it is possible to recreate limb posture and kinematics inferred for extinct bipedal dinosaurs. Chickens raised wearing artificial tails, and consequently with more posteriorly located centre of mass, showed a more vertical orientation of the femur during standing and increased femoral displacement during locomotion. Our results support the hypothesis that gradual changes in the location of the centre of mass resulted in more crouched hindlimb postures and a shift from hip-driven to knee-driven limb movements through theropod evolution. This study suggests that, through careful experimental manipulations during the growth phase of ontogeny, extant birds can potentially be used to gain important insights into previously unexplored aspects of bipedal non-avian theropod locomotion.

2013

In vivo bone strain and finite element modeling of the mandible of Alligator mississippiensis
Journal of Anatomy (2013) 222 (3): 195-227
Porro LB, Metzger KA, Iriarte-Diaz J & Ross CF

In vivo bone strain and finite element modeling of the mandible of Alligator mississippiensis
Journal of Anatomy (2013) 222 (3): 195-227
Porro LB, Metzger KA, Iriarte-Diaz J & Ross CF

Forces experienced during feeding are thought to strongly influence the morphology of the vertebrate mandible; in vivo strain data are the most direct evidence for deformation of the mandible induced by these loading regimes. Although many studies have documented bone strains in the mammalian mandible, no information is available on strain magnitudes, orientations or patterns in the sauropsid lower jaw during feeding. Furthermore, strain gage experiments record the mechanical response of bone at a few locations, not across the entire mandible. In this paper, we present bone strain data recorded at various sites on the lower jaw of Alligator mississippiensis during in vivo feeding experiments. These data are used to understand how changes in loading regime associated with changes in bite location are related to changes in strain regime on the working and balancing sides of the mandible. Our results suggest that the working side mandible is bent dorsoventrally and twisted about its long-axis during biting while the balancing side experiences primarily dorsoventral bending. Strain orientations are more variable on the working side than the balancing side with changes in bite point and between experiments; the balancing side exhibits higher strain magnitudes. In the second part of this paper, we use principal strain orientations and magnitudes recorded in vivo to evaluate a finite element model of the alligator mandible. Our comparison demonstrates that strain orientations and mandibular deformation predicted by the model closely match in vivo results; however, absolute strain magnitudes are lower in the finite element model.

The evolution of locomotor rhythmicity in tetrapods
Evolution (2013) 67 (4): 1209-1217
Ross CF, Blob R, Carrier DR, Daley MA, Deban SM, Demes B, Gripper JL, Iriarte-Diaz J, Kilbourne B, Landberg T, Polk J, Schilling N & Vanhooydonck B

The evolution of locomotor rhythmicity in tetrapods
Evolution (2013) 67 (4): 1209-1217
Ross CF, Blob R, Carrier DR, Daley MA, Deban SM, Demes B, Gripper JL, Iriarte-Diaz J, Kilbourne B, Landberg T, Polk J, Schilling N & Vanhooydonck B

Differences in rhythmicity (relative variance in cycle period) between mammal, fish, and lizard feeding systems have been hypothesized to be associated with differences in their sensorimotor control systems. We tested this hypothesis by examining whether the locomotion of tachymetabolic tetrapods (birds and mammals) is more rhythmic than that of bradymetabolic tetrapods (lizards, alligators, turtles, salamanders). Species averages of intra-individual coefficients of variation in cycle period were compared while controlling for gait and substrate. Variance in locomotor cycle periods is significantly lower in tachymetabolic than in bradymetabolic animals for data sets that include treadmill locomotion, non-treadmill locomotion, or both. When phylogenetic relationships are taken into account, the non-treadmill analysis and the pooled analyses remain significant, the treadmill analysis becomes nonsignificant (but only marginally). The co-occurrence of relatively high rhythmicity in both feeding and locomotor systems of tachymetabolic tetrapods suggests that the anatomical substrate of rhythmicity is in the motor control system, not in the musculoskeletal components.

2012

Kinematic plasticity during flight in fruit bats: individual variability in response to loading
PLoS ONE (2012) 7(5): e36665
Iriarte-Diaz J, Riskin DK, Breuer KS & Swartz SM

Kinematic plasticity during flight in fruit bats: individual variability in response to loading
PLoS ONE (2012) 7(5): e36665
Iriarte-Diaz J, Riskin DK, Breuer KS & Swartz SM

All bats experience daily and seasonal fluctuation in body mass. An increase in mass requires changes in flight kinematics to produce the extra lift necessary to compensate for increased weight. How bats modify their kinematics to increase lift, however, is not well understood. In this study, we investigated the effect of a 20% increase in mass on flight kinematics for Cynopterus brachyotis, the lesser dog-faced fruit bat. We reconstructed the 3D wing kinematics and how they changed with the additional mass. Bats showed a marked change in wing kinematics in response to loading, but changes varied among individuals. Each bat adjusted a different combination of kinematic parameters to increase lift, indicating that aerodynamic force generation can be modulated in multiple ways. Two main kinematic strategies were distinguished: bats either changed the motion of the wings by primarily increasing wingbeat frequency, or changed the configuration of the wings by increasing wing area and camber. The complex, individual-dependent response to increased loading in our bats points to an underappreciated aspect of locomotor control, in which the inherent complexity of the biomechanical system allows for kinematic plasticity. The kinematic plasticity and functional redundancy observed in bat flight can have evolutionary consequences, such as an increase potential for morphological and kinematic diversification due to weakened locomotor trade-offs.

Granger causality analysis of functional connectivity of spiking neurons in orofacial motor cortex during chewing and swallowing
Engineering in Medicine and Biology Society (2012) 4587-4590. Conference proceedings
Takahashi K, Pesce L, Best M, Iriarte-Diaz J, Kim S, Coleman TP, Hatsopoulos NG & Ross CF

Granger causality analysis of functional connectivity of spiking neurons in orofacial motor cortex during chewing and swallowing
Engineering in Medicine and Biology Society (2012) 4587-4590. Conference proceedings
Takahashi K, Pesce L, Best M, Iriarte-Diaz J, Kim S, Coleman TP, Hatsopoulos NG & Ross CF
http://dx.doi.org/10.1109/EMBC.2012.6346988

Primate feeding behavior is characterized by a series of jaw movement cycles of different types making it ideal for investigating the role of motor cortex in controlling transitions between different kinematic states. We recorded spiking activity in populations of neurons in the orofacial portion of primary motor cortex (MIo) of a macaque monkey and, using a Granger causality model, estimated their functional connectivity during transitions between chewing cycles and from chewing to swallowing cycles. We found that during rhythmic chewing, the network was dominated by excitatory connections and exhibited a few “out degree” hub neurons, while during transitions from rhythmic chews to swallows, the numbers of excitatory and inhibitory connections became comparable, and more “in degree” hub neurons emerged. These results suggest that networks of neurons in MIo change their operative states with changes in kinematically defined behavioral states.

Innovative approaches to the relationship between diet and mandibular morphology in primates
International Journal of Primatology (2012) 33: 632-660
Ross CF, Iriarte-Diaz J & Nunn CL

Innovative approaches to the relationship between diet and mandibular morphology in primates
International Journal of Primatology (2012) 33: 632-660
Ross CF, Iriarte-Diaz J & Nunn CL

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 only affect mandibular morphology through intervening variables that are currently poorly understood: namely, feeding behavior and mandibular loading, stress, and strain regimes. Our studies of 3D 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 fully understand relationships between mandibular morphology and diet in primates.

A bird? A plane? No, it's a bat: An introduction to the biomechanics of bat flight
In: Evolutionary History of Bats: Fossils, Molecules and Morphology (Gunnell GF & Simmons NB, eds). Cambridge University Press (2012) p. 317-352
Swartz SM, Iriarte-Diaz J, Riskin DK & Breuer KS
Probabilistic finite element analysis of a craniofacial finite element model
Journal of Theoretical Biology (2012) 300: 242-253
Berthaume MA, Dechow PC, Iriarte-Diaz J, Ross CF, Strait DS, Wang Q & Grosee IR

Probabilistic finite element analysis of a craniofacial finite element model
Journal of Theoretical Biology (2012) 300: 242-253
Berthaume MA, Dechow PC, Iriarte-Diaz J, Ross CF, Strait DS, Wang Q & Grosee IR

We employed a probabilistic finite element analysis (FEA) method to determine how variability in material property values affects stress and strain values in a finite model of a Macaca fascicularis cranium. The material behavior of cortical bone varied in three ways: isotropic homogeneous, isotropic non-homogeneous, and orthotropic non-homogeneous. The material behavior of the trabecular bone and teeth was always treated as isotropic and homogeneous. All material property values for the cranium were randomized with a Gaussian distribution with either coefficients of variation (CVs) of 0.2 or with CVs calculated from empirical data. Latin hypercube sampling was used to determine the values of the material properties used in the finite element models. In total, four hundred and twenty six separate deterministic FE simulations were executed. We tested four hypotheses in this study: (1) uncertainty in material property values will have an insignificant effect on high stresses and a significant effect on high strains for homogeneous isotropic models; (2) the effect of variability in material property values on the stress state will increase as non-homogeneity and anisotropy increase; (3) variation in the in vivo shear strain values reported by Strait et al. (2005) and Ross et al. (2011) is not only due to variations in muscle forces and cranial morphology, but also due to variation in material property values; (4) the assumption of a uniform coefficient of variation for the material property values will result in the same trend in how moderate-to-high stresses and moderate-to-high strains vary with respect to the degree of non-homogeneity and anisotropy as the trend found when the coefficients of variation for material property values are calculated from empirical data. Our results supported the first three hypotheses and falsified the fourth. When material properties were varied with a constant CV, as non-homogeneity and anisotropy increased the level of variability in the moderate-to-high strains decreased while the level of variability in the moderate-to-high stresses increased. However, this is not the pattern observed when CVs calculated from empirical data were applied to the material properties where the lowest level of variability in both stresses and strains occurred when the cranium was modeled with a low level of non-homogeneity and anisotropy. Therefore, when constant material property variability is assumed, inaccurate trends in the level of variability present in modest-to-high magnitude stresses and strains are produced. When the cranium is modeled with the highest level of accuracy (high non-homogeneity and anisotropy) and when randomness in the material properties is calculated from empirical data, there is a large level of variability in the significant strains (CV=0.369) and a low level of variability in the modest-to-high magnitude stresses (CV=0.150). This result may have important implications with regard to the mechanical signals driving bone remodeling and adaptation through natural selection.

2011

Sources of variation in temporal and spatial aspects of jaw kinematics in two species of primates feeding on foods of different properties
Integrative and Comparative Biology (2011) 51: 307-319
Iriarte-Diaz J, Reed DA & Ross CF

Sources of variation in temporal and spatial aspects of jaw kinematics in two species of primates feeding on foods of different properties
Integrative and Comparative Biology (2011) 51: 307-319
Iriarte-Diaz J, Reed DA & Ross CF

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.

The instantaneous center of rotation of the mandible in non-human primates
Integrative and Comparative Biology (2011) 51: 320-332
Terhune C, Iriarte-Diaz J, Taylor A & Ross CF

The instantaneous center of rotation of the mandible in non-human primates
Integrative and Comparative Biology (2011) 51: 320-332
Terhune C, Iriarte-Diaz J, Taylor A & Ross CF

Kinematic analyses of mandibular movement in humans demonstrate that the mandibular instantaneous center of rotation (ICoR) is commonly located near the level of the occlusal plane and varies in its position during a chewing sequence. Few data are available regarding the location of the ICoR in non-human primates and it remains unclear how the position of the ICoR varies in association with mastication and/or gape behaviors. ICoR was quantified throughout the gape cycle in five species of non-human primates (Macaca mulatta, Cebus apella, Chlorocebus aethiops, Eulemur fulvus, Varecia variegata). The ICoR is commonly located below the mandibular condyle close to the occlusal plane and varies considerably both superoinferiorly and anteroposteriorly through the gape cycle. The path of the ICoR, and by inference condylar movement, in Macaca and Chlorocebus differs from humans whereas movement in Cebus resembles that of humans. Similarities between humans and Cebus in articular eminence and occlusal morphology may explain these similarities. The properties of food had little influence on ICoR movement parameters.

Whole-body kinematics of a fruit bat reveal the influence of wing inertia on body accelerations
Journal of Experimental Biology (2011) 214: 1546-1553
Iriarte-Diaz J, Riskin DK, Willis DJ, Breuer KS & Swartz SM

Whole-body kinematics of a fruit bat reveal the influence of wing inertia on body accelerations
Journal of Experimental Biology (2011) 214: 1546-1553
Iriarte-Diaz J, Riskin DK, Willis DJ, Breuer KS & Swartz SM

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
Journal of Anatomy (2011) 218: 59-74
Reed DA, Porro LB, Iriarte-Diaz J, Lemberg JB, Holliday CM, Anapol F & Ross CF

The impact of bone and suture material properties on mandibular function in Alligator mississippiensis: testing theoretical phenotypes with finite element analysis
Journal of Anatomy (2011) 218: 59-74
Reed DA, Porro LB, Iriarte-Diaz J, Lemberg JB, Holliday CM, Anapol F & Ross CF

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.

In vivo bone strain and finite-element modeling of the craniofacial haft in catarrhine primates
Journal of Anatomy (2011) 218: 112-141
Ross CF, Berthaume MA, Dechow PC, Iriarte-Diaz J, Porro LB, Richmond BG, Spencer M & Strait D

In vivo bone strain and finite-element modeling of the craniofacial haft in catarrhine primates
Journal of Anatomy (2011) 218: 112-141
Ross CF, Berthaume MA, Dechow PC, Iriarte-Diaz J, Porro LB, Richmond BG, Spencer M & Strait D

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.

2010

The effect of body size on the wing movements of pteropodid bats, with insights into thrust and lift production
Journal of Experimental Biology (2010) 213: 4110-4122
Riskin DK, Iriarte-Diaz J, Middleton KM, Breuer KS & Swartz SM

The effect of body size on the wing movements of pteropodid bats, with insights into thrust and lift production
Journal of Experimental Biology (2010) 213: 4110-4122
Riskin DK, Iriarte-Diaz J, Middleton KM, Breuer KS & Swartz SM

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 (bmaxMb0.423; SmaxMb0.768; QsMb0.233) 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 (CLMb0.170). Also, the slope of the wingbeat period (T) to body mass regression was significantly more shallow than expected under isometry (TMb0.180), 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.

2008

Kinematics of the slow turning maneuvering in the fruit bat Cynopterus brachyotis
Journal of Experimental Biology (2008) 211: 3478-3489
Iriarte-Diaz J & Swartz SM

Kinematics of the slow turning maneuvering in the fruit bat Cynopterus brachyotis
Journal of Experimental Biology (2008) 211: 3478-3489
Iriarte-Diaz J & Swartz SM

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. Here 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 an L-shaped flight enclosure that required them to make a 90-degree 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 previous 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.

Quantifying the complexity of bat wing kinematics
Journal of Theoretical Biology (2008) 254: 604-615
Riskin DK, Willis DJ, Iriarte-Diaz J, Hedrick TL, Kostandov M, Chian J, Laidlow DH, Breuer KS & Swartz SM

Quantifying the complexity of bat wing kinematics
Journal of Theoretical Biology (2008) 254: 604-615
Riskin DK, Willis DJ, Iriarte-Diaz J, Hedrick TL, Kostandov M, Chian J, Laidlow DH, Breuer KS & Swartz SM

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.

2006

What explains the trot-gallop transition in small mammals?
Journal of Experimental Biology (2006) 209: 4061-4066
Iriarte-Diaz J, Bozinovic F & Vasquez RA

What explains the trot-gallop transition in small mammals?
Journal of Experimental Biology (2006) 209: 4061-4066
Iriarte-Diaz J, Bozinovic F & Vasquez RA

The transition from trot to gallop in quadruped mammals has been widely hypothesized to be a strategy to minimize the energetic costs of running. This view, however, has been challenged by some experimental evidence suggesting instead that this transition might be triggered by mechanical cues, and would occur when musculoskeletal stresses reach a certain critical value. All previous experiments to test those hypotheses have used relatively large species and their results, therefore, may not be applicable to small mammals. In this study we evaluated the effect of carrying loads on the locomotor energetics and gait transitions of the rodent Octodon degus running on a treadmill. Metabolic rate and cost of transport increased about 30% with a 20% increment in body mass. This increment was higher than expectations based on other mammals, where energy consumption increases in proportion to the added mass, but similar to the response of humans to loads. No abrupt change of energy consumption between gaits was observed and therefore no evidence was found to support the energetic hypothesis. The trot–gallop transition speed did not vary when subjects were experimentally loaded, suggesting that the forces applied to the musculoskeletal system do not trigger gait transition.

Direct measurements of the kinematics and dynamics of bat flight
Bioinspiration & Biomimetics (2006) 1: S10-S18
Tian X, Iriarte-Diaz J, Middleton K, Galvao R, Israeli E, Roemer A, Sullivan A, Song A, Swartz SM & Breuer K

Direct measurements of the kinematics and dynamics of bat flight
Bioinspiration & Biomimetics (2006) 1: S10-S18
Tian X, Iriarte-Diaz J, Middleton K, Galvao R, Israeli E, Roemer A, Sullivan A, Song A, Swartz SM & Breuer K

Experimental measurements and analysis of the flight of bats are presented, including kinematic analysis of high-speed stereo videography of straight and turning flight, and measurements of the wake velocity field behind the bat. The kinematic data reveal that, at relatively slow flight speeds, wing motion is quite complex, including a sharp retraction of the wing during the upstroke and a broad sweep of the partially extended wing during the downstroke. The data also indicate that the flight speed and elevation are not constant, but oscillate in synchrony with both the horizontal and vertical movements of the wing. PIV measurements in the transverse (Trefftz) plane of the wake indicate a complex ‘wake vortex’ structure dominated by a strong wing tip vortex shed from the wing tip during the downstroke and either the wing tip or a more proximal joint during the upstroke. Data synthesis of several discrete realizations suggests a ‘cartoon’ of the wake structure during the entire wing beat cycle. Considerable work remains to be done to confirm and amplify these results.

2005

Relative size of hearts and lungs of small bats
Acta Chiropterologica (2005) 7: 65-72
Canals M, Atala C, Grossi B & Iriarte-Diaz J

Relative size of hearts and lungs of small bats
Acta Chiropterologica (2005) 7: 65-72
Canals M, Atala C, Grossi B & Iriarte-Diaz J

We estimated the heart and lung size of several species of small bats (Tadarida brasiliensis, Mormopterus kalinowski, Myotis chiloensis, Histiotus macrotus, H. montanus, Lasiurus borealis and L. cinereus) and compared these values to those of bats of larger size and other mammals. Our results confirmed that bats have the largest relative heart and lung size of all mammals. This is associated with the high energetic costs of flight. As expected, the mass-specific lung and heart sizes of small bats were larger than those of large bats. However, although relative heart mass decreased according to body mass, Mb-0.21, lung volume was nearly isometric with body mass (exponent = 0.90). This exponent was close to unity, and between exponents reported previously (0.77 and 1.06). This suggests that small bats compensate the energetic cost of flight mainly by changes in cardiovascular morphology. The relative heart mass of both, H. macrotus and H. montanus was particularly large, representing 1.71 and 2.18% of total body mass, respectively. These values correspond to 121.3 and 162.7%, respectively, of the expected values from allometric relationships. In these big-eared bats, the large hearts could be attributed to the energetic costs induced by the ears' drag.

Biomechanical and ecological relationships of wing morphology of eight Chilean bats
Revista Chilena de Historia Natural (2005) 78: 215-227
Canals M, Grossi B, Iriarte-Diaz J & Veloso C

Biomechanical and ecological relationships of wing morphology of eight Chilean bats
Revista Chilena de Historia Natural (2005) 78: 215-227
Canals M, Grossi B, Iriarte-Diaz J & Veloso C

In this study we compared the wing morphology of eight species of bats inhabiting Chile, including two previously studied species. We correlated our results with ecological information. Aspect ratio, wing span, wing area, wing loading and the second moment of area of the midshaft of the humerus were estimated for the molossid Mormopterus kalinowskii, the phyllostomidae Desmodus rotundus and the vespertilionids Histiotus montanus, Histiotus macrotus, Lasiurus borealis, and Lasiurus cinereus. The free-tailed bats T. brasiliensis and M.kalinowskii and D. rotundus, without uropatagyum, showed low wing areas, but whilst the molossids showed large aspect ratios, that of D. rotundus was only moderate. Desmodus rotundus showed the lowest wing span (relative to the expected value) and the largest wing loading. The second moment of area of the midshaft of the humerus of M. chiloensis was lower than the predicted values from allometric equations, suggesting poor resistance to bending and torsional forces. All other vespertilionids showed high second moment of area of the humerus. This may be explained by the energetically expensive form of locomotion, especially in species with high parasite power as a consequence of their long ears. The high Ih of D. rotundus can be explained by its low aspect ratio and its high body mass. A principal component analysis showed two orthogonal axes. The first correlated positively with wing loading and negatively with the mass, corrected wingspan. The second component was correlated with the aerodynamic efficiency parameter, aspect. Four functional groups, one per quadrant. were described: (1) Desmodus rotundus, with high wing loading but low corrected wing span, was in the increased agility zone, with moderate power consumption during flight; (2) the molossids were located within the high speed flight and low total power zone, showing high aerodynamic efficiency; (3) most of vespertilionids were in the zone of low speed but increased maneuverability, with relatively low aspect ratios and wing loading; (4) Lasiurus cinereus was in the zone of fast speed flight and the low aspect ratio predicts an increased agility. The functional groups (2) and (3) exploit similar habitats but with different life styles. The molossids foraging in open areas at fast flight speed and the vespertilionids foraging in more wooded areas with maneuverable and slow flight. Desmodus rotundus clearly constitute a single group that may be related to commuting flights from communal roost and their particular mode of locomotion.

2003

Past and present small mammals of Isla Mocha (Chile)
Mammalian biology (2003) 68: 365-371
Saavedra B, Quiroz D & Iriarte J

Past and present small mammals of Isla Mocha (Chile)
Mammalian biology (2003) 68: 365-371
Saavedra B, Quiroz D & Iriarte J

We describe archaeozoological and extant small mammals from Isla Mocha, an island located in south-central Chile. Species composition was compared among past and present assemblages. Also composition, as well as individual and population parameters were compared among island habitats. Specimens from archaeological sites included Oligoryzomys longicaudatus, Abrothrix sp., and Octodon pacificus, whereas Abrothrix longipilis, A. olivaceus, Oligoryzomys longicaudatus, and Geoxus valdivianus were captured. Higher richness was observed in intermediate-disturbed habitat. Body size and tail length, as well as body mass did not vary among island habitats for A. longipilis or A. olivaceus. Higher abundance was associated to less perturbed habitat.

2002

Differential scaling of locomotor performance in small and large terrestrial mammals
Journal of Experimental Biology (2002) 205: 2897-2908
Iriarte-Diaz J

Differential scaling of locomotor performance in small and large terrestrial mammals
Journal of Experimental Biology (2002) 205: 2897-2908
Iriarte-Diaz J

It has been observed that the relationship between locomotor performance and body mass in terrestrial mammals does not follow a single linear trend when the entire range of body mass is considered. Large taxa tend to show different scaling exponents compared to those of small taxa, suggesting that there would be a differential scaling between small and large mammals. This pattern, noted previously for several morphological traits in mammals, has been explained to occur as a result of mechanical constraints over bones due to the differential effect of gravity on small and large-sized forms. The relationship between maximum relative running speed (body length s-1) and body mass was analysed in 142 species of terrestrial mammals, in order to evaluate whether the relative locomotor performance shows a differential scaling depending on the range of mass analysed, and whether the scaling pattern is consistent with the idea of mechanical constraints on locomotor performance. The scaling of relative locomotor performance proved to be non-linear when the entire range of body masses was considered and showed a differential scaling between small and large mammals. Among the small species, a negative, although nearly independent, relationship with body mass was noted. In contrast, maximum relative running speed in large mammals showed a strong negative relationship with body mass. This reduction in locomotor performance was correlated with a decrease in the ability to withstand the forces applied on bones and may be understood as a necessary stress reduction mechanism for assuring the structural integrity of the limb skeleton in large species.

Biomechanic consequences of differences in wing morphology between Tadarida brasiliensis and Myotis chiloensis
Acta Theriologica (2002) 47: 193-200
Iriarte-Diaz J, Novoa FF & Canals M

Biomechanic consequences of differences in wing morphology between Tadarida brasiliensis and Myotis chiloensis
Acta Theriologica (2002) 47: 193-200
Iriarte-Diaz J, Novoa FF & Canals M

The wing morphology of bats is very diverse, and may correlate with energetic behavioural, and ecological demands. If these demands conflict, wing shape may reflect compromise solutions. In this study, we compared the wing morphology of two bats Tadarida brasiliensis (Geoffroy, 1824) and Myotis chiloensis (Waterhouse, 1828), that differ in body size, habitat, and foraging behaviour. We analyzed features of biomechanical and energetic relevance, and sought evidence of compromise solutions to energetic, ecological, and behavioural demands. We found that wing span of both species conformed to expectations based on allometric relationships, but that although the wing area of M. chiloensis did not differ from predictions, the wing area of T. brasiliensis was lower. M. chiloensis possessed an unusually low second moment of area of the humerus. Wing form of M. chiloensis is consistent with highly maneuverable flight needed to live between shrubs and wooded habitats and its low aspect ratio and low wing loading indicate a high energetic cost and a low flight speed, respectively. The low humeral second moment of area may be related to a reduction of wing mass and may result in decreased inertial power. In contrast, T. brasiliensis showed high aspect ratio and wing loading, characteristic of high speed, energetically economic flight.

Functional morphology and geographic variation in the digging apparatus of cururos (Octodontidae: Spalacopus cyanus)
Journal of Mammalogy (2002) 83: 145-152
Bacigalupe LD, Iriarte-Diaz J & Bozinovic F

Functional morphology and geographic variation in the digging apparatus of cururos (Octodontidae: Spalacopus cyanus)
Journal of Mammalogy (2002) 83: 145-152
Bacigalupe LD, Iriarte-Diaz J & Bozinovic F

We studied morphological and functional variations in jaws of coastal and mountain populations of subterranean Spalacopus cyanus inhabiting soils with contrasting hardness. We found almost no morphological differentiation between populations in the variables we measured. However, there were clear differences in incisor resistance between them. Apparently, soil hardness did not represent a selective pressure on cururos' digging apparatus. An Andean origin of this genus could explain our results.

2001

Comparison of the wing morphology of Tadarida brasiliensis (Chiroptera: Molossidae) and Myotis chiloensis (Chiroptera: Vespertilionidae) as representatives of two flight patterns
Revista Chilena de Historia Natural (2001) 74: 699-704
Canals M, Iriarte-Diaz J, Olivares R & Novoa FF

Comparison of the wing morphology of Tadarida brasiliensis (Chiroptera: Molossidae) and Myotis chiloensis (Chiroptera: Vespertilionidae) as representatives of two flight patterns
Revista Chilena de Historia Natural (2001) 74: 699-704
Canals M, Iriarte-Diaz J, Olivares R & Novoa FF

Wing morphology is related by one hand to biomechanical properties and energetics of flying, and on the other hand to ecological and behavioral aspects of flying, such as flight pattern, foraging behavior, habitat selection and size of prey. In this work we compare the wing morphology of Tadarida brasiliensis (Molossidae) and Myotis chiloensis (Vespertilionidae), as representatives of two flight patterns, and looking for trade-offs between wing morphology, ecology and behavior. Our results showed that T. brasiliensis is larger and with higher wing span than M. chiloensis, although the wing area does not differ between these bats. The latter species showed a smaller variability in body mass and cortical area of humerus, probably related with mechanic and energetic constraints. Without size effect, there were differences in the external diameter and medullar diameter of humerus, but with a similar cortical area. The humerus of T. brasiliensis is a bone of similar length, wider and with smaller cortical thickness than in M. chiloensis, which is related to a higher resistance to bending and torsional forces. The wing shape found in each bat is in agree with the life mode: slow, short and manoeuvrable flight in wooded zones of M. chiloensis and fast and long distance flight in open areas of T. brasiliensis.