The spatiotemporal richness of hummingbird wing deformations.

Animals exhibit an abundant diversity of forms, and this diversity is even more evident when considering animals that can change shape on demand. The evolution of flexibility contributes to aspects of performance from propulsive efficiency to environmental navigation. It is, however, challenging to quantify and compare body parts that, by their nature, dynamically vary in shape over many time scales. Commonly, body configurations are tracked by labelled markers and quantified parametrically through conventional measures of size and shape (descriptor approach) or non-parametrically through data-driven analyses that broadly capture spatiotemporal deformation patterns (shape variable approach). We developed a weightless marker tracking technique and combined these analytic approaches to study wing morphological flexibility in hoverfeeding Anna's hummingbirds (Calypte anna). Four shape variables explained >95% of typical stroke cycle wing shape variation and were broadly correlated with specific conventional descriptors such as wing twist and area. Moreover, shape variables decomposed wing deformations into pairs of in-plane and out-of-plane components at integer multiples of the stroke frequency. This property allowed us to identify spatiotemporal deformation profiles characteristic of hoverfeeding with experimentally imposed kinematic constraints, including through shape variables explaining <10% of typical shape variation. Hoverfeeding in front of a visual barrier restricted stroke amplitude and elicited increased stroke frequencies together with in-plane and out-of-plane deformations throughout the stroke cycle. Lifting submaximal loads increased stroke amplitudes at similar stroke frequencies together with prominent in-plane deformations during the upstroke and pronation. Our study highlights how spatially and temporally distinct changes in wing shape can contribute to agile fluidic locomotion.

Hummingbirds use distinct control strategies for forward and hovering flight.

The detection of optic flow is important for generating optomotor responses to mediate retinal image stabilization, and it can also be used during ongoing locomotion for centring and velocity control. Previous work in hummingbirds has separately examined the roles of optic flow during hovering and when centring through a narrow passage during forward flight. To develop a hypothesis for the visual control of forward flight velocity, we examined the behaviour of hummingbirds in a flight tunnel where optic flow could be systematically manipulated. In all treatments, the animals exhibited periods of forward flight interspersed with bouts of spontaneous hovering. Hummingbirds flew fastest when they had a reliable signal of optic flow. All optic flow manipulations caused slower flight, suggesting that hummingbirds had an expected optic flow magnitude that was disrupted. In addition, upward and downward optic flow drove optomotor responses for maintaining altitude during forward flight. When hummingbirds made voluntary transitions to hovering, optomotor responses were observed to all directions. Collectively, these results are consistent with hummingbirds controlling flight speed via mechanisms that use an internal forward model to predict expected optic flow whereas flight altitude and hovering position are controlled more directly by sensory feedback from the environment.

Specializations in optic flow encoding in the pretectum of hummingbirds and zebra finches.

All visual animals experience optic flow-global visual motion across the retina, which is used to control posture and movement.1 The midbrain circuitry for optic flow is highly conserved in vertebrates,2-6 and these neurons show similar response properties across tetrapods.4,7-16 These neurons have large receptive fields and exhibit both direction and velocity selectivity in response to large moving stimuli. Hummingbirds deviate from the typical vertebrate pattern in several respects.17,18 Their lentiformis mesencephali (LM) lacks the directional bias seen in other tetrapods and has an overall bias for faster velocities. This led Ibbotson19 to suggest that the hummingbird LM may be specialized for hovering close to visual structures, such as plants. In such an environment, even slight body motions will translate into high-velocity optic flow. A prediction from this hypothesis is that hummingbird LM neurons should be more responsive to large visual features. We tested this hypothesis by measuring neural responses of hummingbirds and zebra finches to sine wave gratings of varying spatial and temporal frequencies. As predicted, the hummingbird LM displayed an overall preference for fast optic flow because neurons were biased to lower spatial frequencies. These neurons were also tightly tuned in the spatiotemporal domain. We found that the zebra finch LM specializes along another domain: many neurons were initially tuned to high temporal frequencies followed by a shift in location and orientation to slower velocity tuning. Collectively, these results demonstrate that the LM has distinct and specialized tuning properties in at least two bird species.

Response properties of optic flow neurons in the accessory optic system of hummingbirds versus zebra finches and pigeons.

Optokinetic responses function to maintain retinal image stabilization by minimizing optic flow that occurs during self-motion. The hovering ability of hummingbirds is an extreme example of this behavior. Optokinetic responses are mediated by direction-selective neurons with large receptive fields in the accessory optic system (AOS) and pretectum. Recent studies in hummingbirds showed that, compared with other bird species, 1) the pretectal nucleus lentiformis mesencephali (LM) is hypertrophied, 2) LM has a unique distribution of direction preferences, and 3) LM neurons are more tightly tuned to stimulus velocity. In this study, we sought to determine if there are concomitant changes in the nucleus of the basal optic root (nBOR) of the AOS. We recorded the visual response properties of nBOR neurons to large-field-drifting random dot patterns and sine-wave gratings in Anna's hummingbirds and zebra finches and compared these with archival data from pigeons. We found no differences with respect to the distribution of direction preferences: Neurons responsive to upward, downward, and nasal-to-temporal motion were equally represented in all three species, and neurons responsive to temporal-to-nasal motion were rare or absent (<5%). Compared with zebra finches and pigeons, however, hummingbird nBOR neurons were more tightly tuned to stimulus velocity of random dot stimuli. Moreover, in response to drifting gratings, hummingbird nBOR neurons are more tightly tuned in the spatiotemporal domain. These results, in combination with specialization in LM, support a hypothesis that hummingbirds have evolved to be "optic flow specialists" to cope with the optomotor demands of sustained hovering flight.NEW & NOTEWORTHY Hummingbirds have specialized response properties to optic flow in the pretectal nucleus lentiformis mesencephali (LM). The LM works with the nucleus of the basal optic root (nBOR) of the accessory optic system (AOS) to process global visual motion, but whether the neural response specializations observed in the LM extend to the nBOR is unknown. Hummingbird nBOR neurons are more tightly tuned to visual stimulus velocity, and in the spatiotemporal domain, compared with two nonhovering species.

Phase transformation-driven artificial muscle mimics the multifunctionality of avian wing muscle.

Skeletal muscle provides a compact solution for performing multiple tasks under diverse operational conditions, a capability lacking in many current engineered systems. Here, we evaluate if shape memory alloy (SMA) components can serve as artificial muscles with tunable mechanical performance. We experimentally impose cyclic stimuli, electric and mechanical, to an SMA wire and demonstrate that this material can mimic the response of the avian humerotriceps, a skeletal muscle that acts in the dynamic control of wing shapes. We next numerically evaluate the feasibility of using SMA springs as artificial leg muscles for a bipedal walking robot. Altering the phase offset between mechanical and electrical stimuli was sufficient for both synthetic and natural muscle to shift between actuation, braking and spring-like behaviour.

Flight muscle power increases with strain amplitude and decreases with cycle frequency in zebra finches (Taeniopygia guttata).

Birds that use high flapping frequencies can modulate aerodynamic force by varying wing velocity, which is primarily a function of stroke amplitude and wingbeat frequency. Previous measurements from zebra finches (Taeniopygia guttata) flying across a range of speeds in a wind tunnel demonstrate that although the birds modulated both wingbeat kinematic parameters, they exhibited greater changes in stroke amplitude. These two kinematic parameters contribute equally to aerodynamic force, so the preference for modulating amplitude over frequency may instead derive from limitations of muscle physiology at high frequency. We tested this hypothesis by developing a novel in situ work loop approach to measure muscle force and power output from the whole pectoralis major of zebra finches. This method allowed for multiple measurements over several hours without significant degradation in muscle power. We explored the parameter space of stimulus, strain amplitude and cycle frequencies measured previously from zebra finches, which revealed overall high net power output of the muscle, despite substantial levels of counter-productive power during muscle lengthening. We directly compared how changes to muscle shortening velocity via strain amplitude and cycle frequency affected muscle power. Increases in strain amplitude led to increased power output during shortening with little to no change in power output during lengthening. In contrast, increases in cycle frequency did not lead to increased power during shortening but instead increased counter-productive power during lengthening. These results demonstrate why at high wingbeat frequency, increasing wing stroke amplitude could be a more effective mechanism to cope with increased aerodynamic demands.

Evolutionary and cardio-respiratory physiology of air-breathing and amphibious fishes.

Air-breathing and amphibious fishes are essential study organisms to shed insight into the required physiological shifts that supported the full transition from aquatic water-breathing fishes to terrestrial air-breathing tetrapods. While the origin of air-breathing in the evolutionary history of the tetrapods has received considerable focus, much less is known about the evolutionary physiology of air-breathing among fishes. This review summarizes recent advances within the field with specific emphasis on the cardiorespiratory regulation associated with air-breathing and terrestrial excursions, and how respiratory physiology of these living transitional forms are affected by development and personality. Finally, we provide a detailed and re-evaluated model of the evolution of air-breathing among fishes that serves as a framework for addressing new questions on the cardiorespiratory changes associated with it. This review highlights the importance of combining detailed studies on piscine air-breathing model species with comparative multi-species studies, to add an additional dimension to our understanding of the evolutionary physiology of air-breathing in vertebrates.

Morphology, Ecology, and Biogeography of Independent Origins of Cleaning Behavior Around the World.

Members of an ecological guild may be anticipated to show morphological convergence, as similar functional demands exert similar selective pressures on phenotypes. Nature is rife with examples, however, where such taxa instead exhibit 'incomplete' convergence or even divergence. Incorporating factors such as character displacement by other guild members or variation in ecological specialization itself may therefore be necessary to gain a more complete understanding of what constrains or promotes diversity. Cleaning, a behavior in which species remove and consume ectoparasites from "clientele," has been shown to exhibit variation in specialization and has evolved in a variety of marine habitats around the globe. To determine the extent to which specialization in this tropic strategy has affected phenotypic evolution, we examined the evolution of cleaning behavior in five marine fish families: Labridae, Gobiidae, Pomacanthidae, Pomacentridae, and Embiotocidae. We used a comparative framework to determine patterns of convergence and divergence in body shape and size across non-cleaning and cleaning members within these five clades. Highly specialized obligate cleaning, found in the Indo-Pacific and the Caribbean, evolved in the Labridae and Gobiidae at strikingly similar times. In these two regions, obligate cleaning evolves early, shows convergence on an elongate body shape, and is restricted to species of small body size. Facultative cleaning, shown either throughout ontogeny or predominately in the juvenile phase, exhibits a much more varied phenotype, especially in geographic regions where obligate cleaning occurs. Collectively, our results are consistent with varying extents of an ecological specialization constraining or spurring morphological evolution in recurrent ways across regions.

Phylo-Allometric Analyses Showcase the Interplay between Life-History Patterns and Phenotypic Convergence in Cleaner Wrasses.

Phenotypic convergence is a macroevolutionary pattern that need not be consistent across life history. Ontogenetic transitions in dietary specialization clearly illustrate the dynamics of ecological selection as organisms grow. The extent of phenotypic convergence among taxa that share a similar ecological niche may therefore vary ontogenetically. Because ontogenetic processes have been shown to evolve, phylogenetic comparative methods can be useful in examining how the scaling of traits relates to ecology. Cleaning, a behavior in which taxa consume ectoparasites off clientele, is well represented among wrasses (Labridae). Nearly three-fourths of labrids that clean do so predominately as juveniles, transitioning away as adults. We examine the scaling patterns of 33 labrid species to understand how life-history patterns of cleaning relate to ontogenetic patterns of phenotypic convergence. We find that as juveniles, cleaners exhibit convergence in body and cranial traits that enhance ectoparasitivory. We then find that taxa that transition away from cleaning exhibit ontogenetic trajectories that are distinct from those of other wrasses. Obligate and facultative species that continue to clean over ontogeny, however, maintain characteristics that are conducive to cleaning. Collectively, we find that life-history patterns of cleaning behavior are concordant with ontogenetic patterns in phenotype in wrasses.

Labrid cleaner fishes show kinematic convergence as juveniles despite variation in morphology.

Cleaning, a dietary strategy in which mucus or ectoparasites are removed and consumed off other taxa, is performed facultatively or obligately in a variety of species. We explored whether species in the Labridae (wrasses, parrotfishes) of varying ecological specialization employ similar mechanisms of prey capture. In investigating feeding on attached prey among juveniles of 19 species of wrasses, we found that patterns of biting in wrasses are influenced by the interaction between the maxilla and a feature of the premaxilla which we term the maxillary crest. Premaxillary motion during biting appears to be guided by the relative size of the crest. In many cases, this results in a 'premaxillary bite' wherein the premaxillae rapidly move anteroventrally to meet the lower jaws and deliver a protruded bite. Cleaners in the Labrichthyini tribe, however, exhibited reduced or absent maxillary crests. This coincided with a distinct kinematic pattern of prey capture in these labrichthyine cleaners, coupled with some of the fastest and lowest-excursion jaw movements. Although evidence of kinematic specialization can be found in these labrichthyines (most notably in the obligate cleaners in Labroides), we found that facultative cleaners from other lineages similarly evolved reductions in excursions and timing. Convergence in feeding kinematics is thus apparent despite varying degrees of cleaning specialization and underlying morphological features.

Effects of prey characteristics on the feeding behaviors of an apex marine predator, the California moray (Gymnothorax mordax).

Moray eels comprise a large radiation of elongate marine predators that are thought to swallow large prey whole but also circumvent gape constraints by manipulating prey into more manageable pieces. Prey manipulation behaviors include shaking, rotation, knotting, and ramming prey against another object to assist in swallowing. Most morays feed on a wide variety of prey that vary in mechanical properties such as stiffness and toughness, which could potentially affect feeding behaviors. There is little diet data informing us of the maximum prey size morays can swallow whole and whether maximum prey size differs between prey types. Our study examines feeding behaviors for the California moray (Gymnothorax mordax) in the laboratory. We recorded morays feeding on freshly thawed fish and cephalopods of varying size. We found that prey size had a strong effect on total feeding time and manipulation duration for both fish and cephalopods. While morays were observed using a diversity of prey manipulation behaviors and the durations for each of these behaviors increased with prey size, prey type had no effect on manipulation behaviors employed. Total manipulation duration, however, comprised a greater proportion of total feeding time for fish compared to cephalopods. As relative prey mass (RPM) increased for cephalopods, morays spent a greater proportion of their total feeding time transporting prey. Transport rate was higher for cephalopod prey but the relationship between RPM and transport rate was negative for both prey types. Despite this decrease in transport rate, we attribute the lower total feeding times for larger cephalopod prey compared to fish to behavioral tactics of morays. Morays used the corners of the aquaria to aid in the transport of larger cephalopod prey. We hypothesize that the deformable tissues of cephalopods and the presumably low coefficient of friction of their thawed mantles and tentacles may be difficult for the recurved teeth on the pharyngeal jaws to pierce and grip during transport.

Ontogenetic Allometry in Shape and Flexibility Underlies Life History Patterns of Labrid Cleaning Behavior.

Body shape plays a crucial role in the movement of organisms. In the aquatic environment, the shape of the body, fins, and the underlying axial skeleton reflect the ability of organisms to propel and maneuver through water. Ontogenetic changes in body shape and flexibility of the axial skeleton may coincide with shifts in ecology (e.g., changes in habitat or feeding mode). We use the evolution of cleaning behavior in the Labridae (wrasses and parrotfishes) as a case study. Cleaner fishes are species that remove and consume ectoparasites from other organisms. In many cases, cleaning involves a high degree of maneuverability, as cleaners on the hunt for parasites may continuously dart around the body of their clients. In labrids, at least 58 species are known to clean. Over two-thirds of these species, however, clean predominately as juveniles, exhibiting an ontogenetic shift away from cleaning as they enter adulthood. Using a phylogenetic comparative framework, we examined features of the axial skeleton, overall body shape, and pectoral fin shape in 31 species of labrids spread across four major clades to assess how scaling patterns in these systems are associated with the ontogeny of cleaning behavior. We find that across wrasses, the ontogeny of body shape shows evolutionary concordance with the degree of flexibility across the vertebral column. A key driver of this relationship is that species that shift away from cleaning over ontogeny show stronger positive allometry for body depth and vertebral moment of inertia than other taxa. Species that clean throughout their life histories show a more elongate body and vertebral column, and tend to maintain the combination of these characteristics over ontogeny. Cleaning behavior in labrid fishes is thus an excellent model with which to investigate morphological patterns as they relate to evolution, development, and ecology.

Cleaners among wrasses: Phylogenetics and evolutionary patterns of cleaning behavior within Labridae.

Cleaner fishes remove and consume ectoparasites and are often categorized by whether they perform this behavior: (1) predominately as juveniles, (2) facultatively throughout ontogeny, or (3) obligately. Through a literature search, we confirmed that with at least 58 species exhibiting cleaning behavior, the Labridae (wrasses, parrotfishes, and allies) contain the highest diversity of cleaner fishes. In fact, there are 3-4 times as many cleaners within labrids as there are in any other marine group. The distribution and underlying causes of this exceptional diversity have not been determined. Here, we assess the topological and temporal patterns of labrid cleaner evolution. We used maximum likelihood and Bayesian approaches to infer the phylogenetic relationships and divergence times between 320 labrid species (50.7% of nominal species). We then employed stochastic character mapping to infer how and when cleaning behavior evolved. We estimate that cleaning has independently evolved 26-30 times in the Labridae, and all such events likely occurred no earlier than in the late Miocene. Given the current sampling and pattern of transitions, we hypothesize that the majority of facultative or obligate cleaning may have evolved through heterochrony.

Linking cranial morphology to prey capture kinematics in three cleaner wrasses: Labroides dimidiatus, Larabicus quadrilineatus, and Thalassoma lutescens.

Cleaner fishes are well known for removing and consuming ectoparasites off other taxa. Observers have noted that cleaners continuously "pick" ectoparasites from the bodies of their respective client organisms, but little is known about the kinematics of cleaning. While a recent study described the jaw morphology of cleaners as having small jaw-closing muscles and weak bite forces, it is unknown how these traits translate into jaw movements during feeding to capture and remove ectoparasites embedded in their clients. Here, we describe cranial morphology and kinematic patterns of feeding for three species of cleaner wrasses. Through high-speed videography of cleaner fishes feeding in two experimental treatments, we document prey capture kinematic profiles for Labroides dimidiatus, Larabicus quadrilineatus, and Thalassoma lutescens. Our results indicate that cleaning in labrids may be associated with the ability to perform low-displacement, fast jaw movements that allow for rapid and multiple gape cycles on individually targeted items. Finally, while the feeding kinematics of cleaners show notable similarities to those of "picker" cyprinodontiforms, we find key differences in the timing of events. In fact, cleaners generally seem to be able to capture prey twice as fast as cyprinodontiforms. We thus suggest that the kinematic patterns exhibited by cleaners are indicative of picking behavior, but that "pickers" may be more kinematically diverse than previously thought.

Scaling patterns inform ontogenetic transitions away from cleaning in Thalassoma wrasses.

In fishes, cleaning is a mutualistic behavior wherein a species will remove and consume ectoparasites from other organisms. More than two-thirds of cleaner fishes display this behavior predominately as juveniles and discontinue cleaning as adults; such species are here referred to as 'facultative cleaners'. Whether allometric changes in morphological traits coincide with ontogenetic shifts away from cleaning is unknown. We tested the hypothesis that transitions away from cleaning are associated with scaling patterns in the feeding apparatus of facultative cleaners, and then compared such patterns with those exhibited by non-cleaner congeners. We measured functional traits related to feeding, such as vertical gape distance, premaxillary protrusion distance and maxillary kinematic transmission coefficient (KT) in each ontogenetic series of 11 Thalassoma wrasses (Labridae). As these fishes predominately capture prey via biting, we modeled bite force using MandibLever (v3.3) to create an ontogenetic trajectory of bite force for each species. Our results indicate that cleaner fishes in Thalassoma, as juveniles, possess jaws with low mobility that exhibit weaker bite forces. Additionally, there was remarkable consistency in the range of body lengths over which we observed significant differences between facultative cleaners and non-cleaners in bite force, vertical gape distance and premaxillary protrusion distance. Through ontogeny, facultative cleaner fishes exhibit positive allometry for a number of functionally important feeding traits, which possibly obviates the need to continue cleaning.