Ecomechanics and the Rules of Life: a Critical Conduit Between the Physical and Natural Sciences.

Nature provides the parameters, or boundaries, within which organisms must cope in order to survive. Therefore, ecological conditions have an unequivocal influence on the ability of organisms to perform the necessary functions for survival. Biomechanics brings together physics and biology to understand how an organism will function under a suite of conditions. Despite a relatively rich recent history linking physiology and morphology with ecology, less attention has been paid to the linkage between biomechanics and ecology. This linkage, however, could provide key insights into patterns and processes of evolution. Ecomechanics, also known as ecological biomechanics or mechanical ecology, is not necessarily new, but has received far less attention than ecophysiology or ecomorphology. Here, we briefly review the history of ecomechanics, and then identify what we believe are grand challenges for the discipline and how they can inform some of the most pressing questions in science today, such as how organisms will cope with global change.

Linking ecomechanical models and functional traits to understand phenotypic diversity.

Physical principles and laws determine the set of possible organismal phenotypes. Constraints arising from development, the environment, and evolutionary history then yield workable, integrated phenotypes. We propose a theoretical and practical framework that considers the role of changing environments. This 'ecomechanical approach' integrates functional organismal traits with the ecological variables. This approach informs our ability to predict species shifts in survival and distribution and provides critical insights into phenotypic diversity. We outline how to use the ecomechanical paradigm using drag-induced bending in trees as an example. Our approach can be incorporated into existing research and help build interdisciplinary bridges. Finally, we identify key factors needed for mass data collection, analysis, and the dissemination of models relevant to this framework.

Extreme premaxillary protrusion in the king-of-the-salmon, Trachipterus altivelis.

The king-of-the-salmon, Trachipterus altivelis (Lampriformes), has an unusual set of oral jaws which allow it the ability to protrude the entire upper jaw, containing the premaxilla and the maxilla bones, to extreme distances. Here, we provide a short description of the cranial anatomy and mechanism of jaw protrusion in T. altivelis using hand-drawn illustrations (by KF), supplemented by CT-scans. We then place the protrusion abilities of T. altivelis into context by comparing anatomical jaw protrusion with protrusion from other members of the Lampriformes, other unrelated species with highly protrusile jaws, and unrelated species with more stereotypical amounts of jaw protrusion. Through these comparisons we demonstrate that T. altivelis is indeed, capable of some of the most extreme premaxillary protrusion as of yet discovered, even when taking into account the extreme morphological modifications that facilitate said protrusion. That is to say, T. altivelis can protrude the premaxilla farther than one would predict from the length of the ascending process alone.

Ontogeny of Feeding Mechanics in Smoothhound Sharks: Morphology and Cartilage Stiffness.

The diet of dusky smoothhound sharks, Mustelus canis, shifts over ontogeny from soft foods to a diet dominated by crabs. This may be accompanied by changes in the skeletal system that facilitates the capture and processing of large and bulky prey. The hyoid arch, for example, braces the jaws against the cranium, and generates suction for prey capture and intraoral transport. In this study, ontogenetic changes in the hyoid arch were investigated by quantifying size, mineralization, and stiffness to determine whether increasingly stiffer cartilages are associated with the dietary switch. Total length and length of the hyomandibula and ceratohyal cartilages over ontogeny were the proxy for body size. Cross-sectional area, percent mineralization, and second moment of area were quantified in 28 individuals spanning most of the natural size range. Mechanical compression tests were conducted to compare flexural stiffness to size. Our results show that the morphological characters tested for the hyomandibular and ceratohyal cartilages scales isometrically with length. While stiffness of the hyomandibular and ceratohyal cartilages scales isometrically with length when assessed on morphological characters alone (second moment of area), this relationship becomes allometric when mechanical properties are included (flexural stiffness). Thus, while the hyoid arch elements grow isometrically, the mechanical properties dictate a scaling relationship that dwarfs morphological characteristics. The various combinations of morphologies and ontogenetic trajectories of chondrichthyan species illustrate the tremendous flexibility that they possess in the functional organization of the feeding apparatus.

Presence of repeating hyperostotic bones in dorsal pterygiophores of the oarfish, Regalecus russellii.

Hyperostosis, excessive bone growth along bone that stems from bone, periosteum or articular or epiphyseal cartilage, occurs in at least 22 families of fishes most of which are tropical or subtropical marine species. While the presence of hyperostosis is well documented in fishes, the mechanism driving the development of the excessive bone growth is unclear. This study documented hyperostosis along the dorsal pterygiophores in both sexes of oarfish, Regalecus russellii; however, it was not present in all specimens examined. This is the second lampridiform fish with hyperostoses and the first case documented in a deeper-water, epi-mesopelagic fish. In oarfish, the majority of the dorsal pterygiophores tissues are poorly mineralized, anosteocytic bones with some fish displaying localized stiffened, hyperostotic growths near the distal edge. Oarfish lack a swim bladder so they must continuously beat their bi-directional dorsal fin to maintain position within the water column while engaged in locomotory behavior. These fishes have areas of localized, hyperostotic skeletal elements along the dorsal pterygiophores that, presumably, function as a stiffened lever system to support fin undulation. It was noted that hyperossification was not present in all fish examined and was only documented in fish with total lengths greater than 3 m.

Why does Gila elegans have a bony tail? A study of swimming morphology convergence.

Caudal-fin-based swimming is the primary form of locomotion in most fishes. As a result, many species have developed specializations to enhance performance during steady swimming. Specializations that enable high swimming speeds to be maintained for long periods of time include: a streamlined body, high-aspect-ratio (winglike) caudal fin, a shallow caudal peduncle, and high proportions of slow-twitch ("red") axial muscle. We described the locomotor specializations of a fish species native to the Colorado River and compared those specializations to other fish species from this habitat, as well as to a high-performance marine swimmer. The focal species for this study was the bonytail (Gila elegans), which has a distinct morphology when compared with closely related species from the Southwestern United States. Comparative species used in this study were the roundtail chub (Gila robusta), a closely related species from low-flow habitats; the common carp (Cyprinus carpio), an invasive cyprinid also found in low-flow habitats; and the chub mackerel (Scomber japonicus), a model high-performance swimmer from the marine environment. The bonytail had a shallow caudal peduncle and a high-aspect-ratio tail that were similar to those of the chub mackerel. The bonytail also had a more streamlined body than the roundtail chub and the common carp, although not as streamlined as the chub mackerel. The chub mackerel had a significantly higher proportion of red muscle than the other three species, which did not differ from one another. Taken together, the streamlined body, narrow caudal peduncle, and high-aspect-ratio tail of the bonytail suggest that this species has responded to the selection pressures of the historically fast-flowing Colorado River, where flooding events and base flows may have required native species to produce and sustain very high swimming speeds to prevent being washed downstream.

Functional Morphology: 'Point and Shoot' Prey Capture in Fishes.

The ability to protrude the jaws and capture elusive prey is a hallmark of fish evolution. New analyses provide insight into how jaw protrusion changed predator-prey relationships and fueled species diversification in ancient seas.

The Teleost Intramandibular Joint: A mechanism That Allows Fish to Obtain Prey Unavailable to Suction Feeders.

Although the majority of teleost fishes possess a fused lower jaw (or mandible), some lineages have acquired a secondary joint in the lower jaw, termed the intramandibular joint (IMJ). The IMJ is a new module that formed within the already exceptionally complex teleost head, and disarticulation of two bony elements of the mandible potentially creates a "double-jointed" jaw. The apparent independent acquisition of this new functional module in divergent lineages raises a suite of questions. (1) How many teleostean lineages contain IMJ-bearing species? (2) Does the IMJ serve the same purpose in all teleosts? (3) Is the IMJ associated with altered feeding kinematics? (4) Do IMJ-bearing fishes experience trade-offs in other aspects of feeding performance? (5) Is the IMJ used to procure prey that are otherwise unavailable? The IMJ is probably under-reported, but has been documented in at least 10 lineages within the Teleostei. Across diverse IMJ-bearing lineages, this secondary joint in the lower jaw serves a variety of functions, including: generating dynamic out-levers that allow fish to apply additional force to a food item during jaw closing; allowing fish to "pick" individual prey items with pincer-like jaws; and facilitating contact with the substrate by altering the size and orientation of the gape. There are no consistent changes in feeding kinematics in IMJ-bearing species relative to their sister taxa; however, some IMJ-bearing taxa produce very slow movements during the capture of food, which may compromise their ability to move prey into the mouth via suction. Despite diversity in behavior, all IMJ-bearing lineages have the ability to remove foods that are physically attached to the substrate or to bite off pieces from sessile organisms. Because such prey cannot be drawn into the mouth by suction, the IMJ provides a new mechanism that enables fish to obtain food that otherwise would be unavailable.

Suction, Ram, and Biting: Deviations and Limitations to the Capture of Aquatic Prey.

When feeding, most aquatic organisms generate suction that draws prey into the mouth. The papers in this volume are a demonstration of this fact. However, under what circumstances is suction ineffective as a feeding mechanism? Here we consider the interplay between suction, ram, and biting, and analyze the contribution of each to the capture of prey by a wide variety of species of fish. We find, not surprisingly, that ram is the dominant contributor to feeding because suction, and biting, are only effective when very close to the prey. As species utilize more strongly ram-dominated modes of feeding, they may be released from the morphological and behavioral constraints associated with the need to direct a current of water into the head. Morphological and behavioral changes that facilitate larger gapes and stronger jaws are explored here, including predators that lack a protrusile upper jaw, predators with elongate jaws, predators that rely on suspension feeding, and predators that bite. Interestingly, while the mobility of the jaws and the shape of the opening of the mouth are modified in species that have departed from a primary reliance on suction feeding, the anterior-to-posterior wave of expansion persists. This wave may be greatly slowed in ram and biting species, but its retention suggests a fundamental importance to aquatic feeding.

Heads or tails: do stranded fish (mosquitofish, Gambusia affinis) know where they are on a slope and how to return to the water?

Aquatic vertebrates that emerge onto land to spawn, feed, or evade aquatic predators must return to the water to avoid dehydration or asphyxiation. How do such aquatic organisms determine their location on land? Do particular behaviors facilitate a safe return to the aquatic realm? In this study, we asked: will fully-aquatic mosquitofish (Gambusia affinis) stranded on a slope modulate locomotor behavior according to body position to facilitate movement back into the water? To address this question, mosquitofish (n = 53) were placed in four positions relative to an artificial slope (30° inclination) and their responses to stranding were recorded, categorized, and quantified. We found that mosquitofish may remain immobile for up to three minutes after being stranded and then initiate either a "roll" or a "leap". During a roll, mass is destabilized to trigger a downslope tumble; during a leap, the fish jumps up, above the substrate. When mosquitofish are oriented with the long axis of the body at 90° to the slope, they almost always (97%) initiate a roll. A roll is an energetically inexpensive way to move back into the water from a cross-slope body orientation because potential energy is converted back into kinetic energy. When placed with their heads toward the apex of the slope, most mosquitofish (>50%) produce a tail-flip jump to leap into ballistic flight. Because a tail-flip generates a caudually-oriented flight trajectory, this locomotor movement will effectively propel a fish downhill when the head is oriented up-slope. However, because the mass of the body is elevated against gravity, leaps require more mechanical work than rolls. We suggest that mosquitofish use the otolith-vestibular system to sense body position and generate a behavior that is "matched" to their orientation on a slope, thereby increasing the probability of a safe return to the water, relative to the energy expended.

Are kissing gourami specialized for substrate-feeding? Prey capture kinematics of Helostoma temminckii and other anabantoid fishes.

Helostoma temminckii are known for a "kissing" behavior, which is often used in intraspecific interactions, and an unusual cranial morphology that is characterized by an intramandibular joint (IMJ). The IMJ is located within the lower jaw and aids in generating the eponymous kissing movement. In other teleost linages the IMJ is associated with the adoption of a substrate-grazing foraging habit. However, because of anatomical modifications of the gill-rakers, Helostoma has been considered a midwater filter-feeding species. We offered midwater, benthic, and attached food to Helostoma, Betta, and two "true" osphronemid gouramis, to ask: (1) how do food capture kinematics differ in different foraging contexts; and (2) are Helostoma feeding kinematics distinct when compared with closely related anabantoids that lack an IMJ? For all anabantoid species except Helostoma, benthic prey were captured using a greater contribution of effective suction relative to midwater prey, though Helostoma was rarely willing to feed in the midwater. Helostoma individuals produced relatively less suction than other species regardless of the food type. Helostoma produced a much larger gape and more premaxillary protrusion than other species, but also took longer to do so. We suggest that the jaw morphology of Helostoma facilitates an extremely large mouth-gape to enhance substrate-scraping. The large amplitude mouth-opening that characterizes substrate-feeding may represent a functional trade-off, whereby the enhanced ability to procure food from the substrate is accompanied by a concomitant reduction in the ability to produce suction.

The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond.

The perciform group Labroidei includes approximately 2600 species and comprises some of the most diverse and successful lineages of teleost fishes. Composed of four major clades, Cichlidae, Labridae (wrasses, parrotfishes, and weed whitings), Pomacentridae (damselfishes), and Embiotocidae (surfperches); labroids have been an icon for studies of biodiversity, adaptive radiation, and sexual selection. The success and diversification of labroids have been largely attributed to the presence of a major innovation in the pharyngeal jaw apparatus, pharyngognathy, which is hypothesized to increase feeding capacity and versatility. We present results of large-scale phylogenetic analyses and a survey of pharyngeal jaw functional morphology that allow us to examine the evolution of pharyngognathy in a historical context. Phylogenetic analyses were based on a sample of 188 acanthomorph (spiny-rayed fish) species, primarily percomorphs (perch-like fishes), and DNA sequence data collected from 10 nuclear loci that have been previously used to resolve higher level ray-finned fish relationships. Phylogenies inferred from this dataset using maximum likelihood, Bayesian, and species tree analyses indicate polyphyly of the traditional Labroidei and clearly separate Labridae from the remainder of the traditional labroid lineages (Cichlidae, Embiotocidae, and Pomacentridae). These three "chromide" families grouped within a newly discovered clade of 40 families and more than 4800 species (>27% of percomorphs and >16% of all ray-finned fishes), which we name Ovalentaria for its characteristic demersal, adhesive eggs with chorionic filaments. This fantastically diverse clade includes some of the most species-rich lineages of marine and freshwater fishes, including all representatives of the Cichlidae, Embiotocidae, Pomacentridae, Ambassidae, Gobiesocidae, Grammatidae, Mugilidae, Opistognathidae, Pholidichthyidae, Plesiopidae (including Notograptus), Polycentridae, Pseudochromidae, Atherinomorpha, and Blennioidei. Beyond the discovery of Ovalentaria, this study provides a surprising, but well-supported, hypothesis for a convict-blenny (Pholidichthys) sister group to the charismatic cichlids and new insights into the evolution of pharyngognathy. Bayesian stochastic mapping ancestral state reconstructions indicate that pharyngognathy has evolved at least six times in percomorphs, including four separate origins in members of the former Labroidei, one origin in the Centrogenyidae, and one origin within Beloniformes. Our analyses indicate that all pharyngognathous fishes have a mechanically efficient biting mechanism enabled by the muscular sling and a single lower jaw element. However, a major distinction exists between Labridae, which lacks the widespread, generalized percomorph pharyngeal biting mechanism, and all other pharyngognathous clades, which possess this generalized biting mechanism in addition to pharyngognathy. Our results reveal a remarkable history of pharyngognathy: far from a single origin, it appears to have evolved at least six times, and its status as a major evolutionary innovation is reinforced by it being a synapomorphy for several independent major radiations, including some of the most species rich and ecologically diverse percomorph clades of coral reef and tropical freshwater fishes, Labridae and Cichlidae. [Acanthomorpha; Beloniformes; Centrogenyidae; key innovation; Labroidei; Ovalentaria; pharyngeal jaws; Perciformes.].

Prey capture behavior of native vs. nonnative fishes: a case study from the Colorado River drainage basin (USA).

The Colorado River drainage basin is home to a diverse but imperiled fish fauna; one putative challenge facing natives is competition with nonnatives. We examined fishes from Colorado River tributaries to address the following questions: Do natives and nonnatives from the same trophic guild consume the same prey items? Will a given species alter its behavior when presented with different prey types? Do different species procure the same prey types via similar feeding behaviors? Roundtail chub (Gila robusta) and smallmouth bass (Micropterus dolomieu), midwater predators, and Sonora sucker (Catostomus insignis) and common carp (Cyprinus carpio), benthic omnivores, were offered six ecologically relevant prey types in more than 600 laboratory trials. Native species consumed a broader array of prey than nonnatives, and species from a given trophic guild demonstrated functional convergence in key aspects of feeding behavior. For example, roundtail chub and smallmouth bass consume prey attached to the substrate by biting, then ripping the prey from its point of attachment; in contrast, Sonora sucker remove attached prey via scraping. When presented with different prey types, common carp, roundtail chub, and smallmouth bass altered their prey capture behavior by modifying strike distance, gape, and angle of attack. Gape varied among the species examined here, with smallmouth bass demonstrating the largest functional and anatomical gape at a given body size. Because fish predators are gape-limited, smallmouth bass will be able to consume a variety of large prey items in the wild, including large, invasive crayfish and young roundtail chub-their presumptive trophic competitors.

Comparative kinematics of cypriniform premaxillary protrusion.

Premaxillary protrusion has evolved multiple times within teleosts, and has been implicated as contributing to the evolutionary success of clades bearing this adaptation. Cypriniform fishes protrude the jaws via the kinethmoid, a median sesamoid bone that is a synapomorphy for the order. Using five cypriniform species, we provide the first comparative kinematic study of jaw protrusion in this speciose order. Our goals were to compare jaw protrusion in cypriniforms to that in other clades that independently evolved upper jaw protrusion, assess the variation in feeding kinematics among members of the order, and test if variation in the shape of the kinethmoid has an effect on either jaw kinematics or the degree of suction or ram used during a feeding event. We also examined the coordination in the relative timings of upper and lower jaw movements to gain insight on the cypriniform protrusile mechanism. Overall, speed of protrusion in cypriniforms is slower than in other teleosts. Protrusion speed differed significantly among cypriniforms but this is likely not due to kinethmoid shape alone; rather, it may be a result of both kinethmoid shape and branching patterns of the A1 division of the adductor mandibulae. In the benthic cypriniforms investigated here, upper jaw protrusion contributed up to 60% of overall ram of the strikes and interestingly, these species also produced the most suction. There is relatively little coordination of upper and lower jaw movements in cypriniforms, suggesting that previous hypotheses of premaxillary protrusion via lower jaw depression are not supported within Cypriniformes. Significant variation in kinematics suggests that cypriniforms may have the ability to modulate feeding, which could be an advantage if presented with the challenge of feeding on different types of prey.

Very low pressures drive ventilatory flow in chimaeroid fishes.

Chimaera (Holocephali) are cartilaginous fishes with flexible operculi rather than external gill slits, suggesting ventilation occurs in a manner different from other fishes. We examined holocephalan ventilation morphology, behavior, and performance by anatomical investigations, high-speed video, and in vivo pressure measurements from the buccal and parabranchial cranial cavities in Hydrolagus colliei and Callorhinchus callorynchus. Ventilatory modes ranged from quiet resting breathing to rapid "active" breathing, yet external cranial movements-excepting the passive movement of the opercular flap-were always extremely subtle, and pressures generated were one to two orders of magnitude lower than those of other fishes. To explain ventilation with such minimal pressure generation and cranial motion, we propose an "accordion" model, whereby rostrocaudal movement of the visceral arches drives pressure differentials, albeit with little lateral or ventral movement. Chimaeroids have comparatively large oropharyngeal cavities, which can move fluid with a smaller linear dimension change than the comparatively smaller cavities of other fishes. Orobranchial pressures are often less than parabranchial pressures, suggesting flow in the "wrong" direction; however, the long gill curtains of chimaeroids may passively restrict backflow. We suggest that constraints on holocephalan jaw and hyoid movements were compensated for evolutionarily by novel visceral arch mechanics and kinematics.