Alice C. Gibb

Ontogeny of Performance in Vertebrates

When competing for food or other resources, or when confronted with predators, young animals may be at a disadvantage relative to adults because of their smaller size. Additionally, the ongoing differentiation and growth of tissues and the development of sensory‐motor integration during early ontogeny may constrain performance. Because ectothermic vertebrates show different growth regimes and energetic requirements when compared to endothermic vertebrates, differences in the ontogenetic trajectories of performance traits in these two groups might be expected. However, both groups of vertebrates show similar patterns of changes in performance with ontogeny. Evidence for compensation, resulting in relatively high levels of performance in juveniles relative to adults, appears common for traits related to locomotor and defensive behaviors. However, there is little evidence for compensation in traits associated with feeding and foraging. We suggest that this difference may be due to different selective regimes operating on locomotor versus feeding traits. As a result, relatively high levels of locomotor performance in juveniles and relatively high levels of feeding performance in adults are observed across a wide range of vertebrate groups.

TROPHIC POLYMORPHISM AND BEHAVIORAL DIFFERENCES DECREASE INTRASPECIFIC COMPETITION IN A CICHLID, HERICHTHYS MINCKLEYI

Resource polymorphisms, or morphological variations related to resource use, are common in fishes and are thought to be a possible step in speciation. This study experimentally tests the hypothesis that fitness (as estimated by growth rates) is increased by the presence of multiple trophic morphotypes (or morphs) within a population. Cage experiments were used to quantify the intraspecific competitive interactions between morphs of the polymorphic cichlid Herichthys minckleyi in Cuatro Cienegas, Mexico. Results sug- gest that competition is reduced between morphs in mixed-morph treatments relative to equal-density single-morph treatments. Field studies revealed that the morphs feed in dif- ferent microhabitats and use different feeding behaviors within these microhabitats. These results suggest that the polymorphism is maintained in the population because it decreases competition between the morphs, and that differences in feeding behavior facilitate resource partitioning.

Mudskipper pectoral fin kinematics in aquatic and terrestrial environments

SUMMARY Mudskippers use pectoral fins for their primary mode of locomotion on land and pectoral fins in conjunction with the axial musculature and caudal fin to move in water. We hypothesized that distinct pectoral fin movements enable effective locomotion in each environment. Additionally, we made three functional predictions about fin movements during locomotion on land versus water: the pectoral fin is depressed more on land than in water; the pectoral fin will have greater changes in fin area between propulsive and recovery phases in water versus land; anterior and posterior excursions will be greater on land than in water. Locomotion was recorded in each environment using a high-speed digital-imaging system and kinematic variables were calculated from digitized landmark points. Variables were analyzed using principal components analysis and matched pairs t-tests. Mudskippers produce distinct kinematic patterns across environments (P<0.003), although only some of our predictions were supported. The magnitude of fin depression is the same across habitats. However, depression occurs during the propulsive phase on land (by –0.60 cm), whereas during the propulsive phase in water the fin is elevated (by +0.13 cm). We were unable to support the hypothesis that fin orientation differs between environments. Lastly, anterior extension of the fin is greater on land (1.8 cm, versus 1.3 cm in water), creating a larger stride length in this environment. We posit that the mudskipper pectoral fin may facilitate stability in water and thrust production on land, and suggest that the robust fin morphology of the goby lineage may predispose species within this group to terrestrial locomotion.

Functional Morphology and Biochemical Indices of Performance: Is there a Correlation Between Metabolic Enzyme Activity and Swimming Performance?

Abstract Comparative physiologists and ecologists have searched for a specific morphological, physiological or biochemical parameter that could be easily measured in a captive, frozen, or preserved animal, and that would accurately predict the routine behavior or performance of that species in the wild. Many investigators have measured the activity of specific enzymes in the locomotor musculature of marine fishes, generally assuming that high specific activities of enzymes involved in aerobic metabolism are indicators of high levels of sustained swimming performance and that high activities of anaerobic metabolic enzymes indicate high levels of burst swimming performance. We review the data that support this hypothesis and describe two recent studies we have conducted that specifically test the hypothesis that biochemical indices of anaerobic or aerobic capacity in fish myotomal muscle correlate with direct measures of swimming performance. First, we determined that the maximum speed during escapes (C-starts) for individual larval and juvenile California halibut did not correlate with the activity of the enzyme lactate dehydrogenase, an index of anaerobic capacity, in the myotomal muscle, when the effects of fish size are factored out using residuals analysis. Second, we found that none of three aerobic capacity indices (citrate synthase activity, 3-hydroxy-o-acylCoA dehydrogenase activity, and myoglobin concentration) measured in the slow, oxidative muscle of juvenile scombrid fishes correlated significantly with maximum sustained speed. Thus, there was little correspondence between specific biochemical characteristics of the locomotor muscle of individual fish and whole animal swimming performance. However, it may be possible to identify biochemical indices that are accurate predictors of animal performance in phylogenetically based studies designed to separate out the effects of body size, temperature, and ontogenetic stage.

Development of the Escape Response in Teleost Fishes: Do Ontogenetic Changes Enable Improved Performance?*

Teleost fishes typically first encounter the environment as free‐swimming embryos or larvae. Larvae are morphologically distinct from adults, and major anatomical structures are unformed. Thus, larvae undergo a series of dramatic morphological changes until they reach adult morphology (but are reproductively immature) and are considered juveniles. Free‐swimming embryos and larvae are able to perform a C‐start, an effective escape response that is used evade predators. However, escape response performance improves during early development: as young fish grow, they swim faster (length‐specific maximum velocity increases) and perform the escape more rapidly (time to complete the behavior decreases). These improvements cease when fish become juveniles, although absolute swimming velocity (m s−1) continues to increase. We use studies of escape behavior and ontogeny in California halibut (Paralichthys californicus), rainbow trout (Oncorhynchus mykiss), and razorback suckers (Xyrauchen texanus) to test the hypothesis that specific morphological changes improve escape performance. We suggest that formation of the caudal fin improves energy transfer to the water and therefore increases thrust production and swimming velocity. In addition, changes to the axial skeleton during the larval period produce increased axial stiffness, which in turn allows the production of a more rapid and effective escape response. Because escape performance improves as adult morphology develops, fish that enter the environment in an advanced stage of development (i.e., those with direct development) should have a greater ability to evade predators than do fish that enter the environment at an early stage of development (i.e., those with indirect development).

Thrash, Flip, or Jump: The Behavioral and Functional Continuum of Terrestrial Locomotion in Teleost Fishes

Moving on land versus in water imposes dramatically different requirements on the musculoskeletal system. Although many limbed vertebrates, such as salamanders and prehistoric tetrapodomorphs, have an axial system specialized for aquatic locomotion and an appendicular system adapted for terrestrial locomotion, diverse extant teleosts use the axial musculoskeletal system (body plus caudal fin) to move in these two physically disparate environments. In fact, teleost fishes living at the waters edge demonstrate diversity in natural history that is reflected in a variety of terrestrial behaviors: (1) species that have only incidental contact with land (such as largemouth bass, Micropterus) will repeatedly thrash, which can roll an individual downhill, but cannot produce effective overland movements, (2) species that have occasional contact with land (like Gambusia, the mosquitofish, which evade predators by stranding themselves) will produce directed terrestrial movement via a tail-flip jump, and (3) species that spend more than half of their lives on land (like the mudskipper, Periopthalmus) will produce a prone-jump, a behavior that allows the fish to anticipate where it will land at the end of the flight phase. Both tail-flip and prone jumps are characterized by a two-phase movement consisting of body flexion followed by extension-a movement pattern that is markedly similar to the aquatic fast-start. Convergence in kinematic pattern between effective terrestrial behaviors and aquatic fast starts suggests that jumps are an exaptation of a neuromuscular system that powers unsteady escape behaviors in the water. Despite such evidence that terrestrial behaviors evolved from an ancestral behavior that is ubiquitous among teleosts, some teleosts are unable to move effectively on land-possibly due to morphological trade-offs, wherein specialization for one environment comes at a cost to performance in the other. Indeed, upon emergence onto land, gravity places an increased mechanical load on the body, which may limit the maximum size of fish that can produce terrestrial locomotion via jumping. In addition, effective terrestrial locomotor performance may require a restructuring of the musculoskeletal system that directly conflicts with the low-drag, fusiform body shape that enhances steady swimming performance. Such biomechanical trade-offs may constrain which teleost species are able to make the evolutionary transition to life on land. Here, we synthesize the current knowledge of intermittent terrestrial locomotion in teleosts and demonstrate that extant fishes represent an important model system for elucidating fundamental evolutionary mechanisms and defining the physiological constraints that must be overcome to permit life in both the aquatic and terrestrial realms.

Locomotor behavior across an environmental transition in the ropefish, Erpetoichthys calabaricus

SUMMARY Many amphibious organisms undergo repeated aquatic to terrestrial transitions during their lifetime; limbless, elongate organisms that make such transitions must rely on axial-based locomotion in both habitats. How is the same anatomical structure employed to produce an effective behavior across such disparate habitats? Here, we examine an elongate amphibious fish, the ropefish (Erpetoichthys calabaricus), and ask: (1) how do locomotor movements change during the transition between aquatic and terrestrial environments and (2) do distantly related amphibious fishes demonstrate similar modes of terrestrial locomotion? Ropefish were examined moving in four experimental treatments (in which the water level was to lowered mimic the transition between environments) that varied from fully aquatic to fully terrestrial. Kinematic parameters (lateral excursion, wavelength, amplitude and frequency) were calculated for points along the midline of the body and compared across treatments. Terrestrial locomotion in the ropefish is characterized by long, slow, large-amplitude undulations down the length of the body; in contrast, aquatic locomotion is characterized by short-wavelength, small-amplitude, high-frequency undulations that gradually increase in an anterior to posterior direction. Experimental treatments with intermediate water levels were more similar to aquatic locomotion in that they demonstrated an anterior to posterior pattern of increasing lateral excursion and wave amplitude, but were more similar to terrestrial locomotion with regard to wavelength, which did not change in an anterior to posterior direction. Finally, the ropefish and another elongate amphibious fish, the eel, consistently exhibit movements characterized by ‘path following’ when moving on land, which suggests that elongate fishes exhibit functional convergence during terrestrial locomotion.

Trophic Apparatus in Cyprinodontiform Fishes: Functional Specializations for Picking and Scraping Behaviors

Cyprinodontiforms are a diverse and speciose order that includes topminnows, pupfishes, swordtails, mosquitofishes, guppies, and mollies. Sister group to the Beloniformes and Atheriniformes, Cyprinodontiformes contains approximately twice the number of species of these other two orders combined. Recent studies suggest that this group is well suited to capturing prey by “picking” small items from the water surface, water column, and the substrate. Because picking places unusual performance demands on the feeding apparatus, this mode of prey capture may rely upon novel morphological modifications not found in more widespread ram‐ or suction‐based feeding mechanisms. To assess this evolutionary hypothesis, we describe the trophic anatomy of 16 cyprinodontiform species, selected to broadly represent the order as well as capture intrageneric variation. The group appears to have undergone gradual morphological changes to become increasingly specialized for picking and scraping behaviors. We also identify a suite of functional characters related to the acquisition of a novel and previously undescribed mechanism of premaxillary protrusion and retraction, including: modification of the “premaxillomandibular” ligament (which connects each side of the premaxilla to the ipsilateral mandible, or lower jaw), a novel architecture of the ligaments and bony elements that unite the premaxillae, maxillae and palatine bones, and novel insertions of the adductor muscles onto the jaws. These morphological changes to both the upper and lower jaws suggest an evolutionary trend within this group toward increased reliance on picking individual prey from the water column/substrate or for scraping encrusting material from the substrate. We propose that the suite of morphological characters described here enable a functional innovation, “picking,” which leads to novel trophic habits. J. Morphol., 2009.

Sustained periodic terrestrial locomotion in air-breathing fishes.

While emergent behaviours have long been reported for air-breathing osteichthyians, only recently have researchers undertaken quantitative analyses of terrestrial locomotion. This review summarizes studies of sustained periodic terrestrial movements by air-breathing fishes and quantifies the contributions of the paired appendages and the axial body to forward propulsion. Elongate fishes with axial-based locomotion, e.g. the ropefish Erpetoichthys calabaricus, generate an anterior-to-posterior wave of undulation that travels down the axial musculoskeletal system and pushes the body against the substratum at multiple points. In contrast, appendage-based locomotors, e.g. the barred mudskipper Periophthalmus argentilineatus, produce no axial bending during sustained locomotion, but instead use repeated protraction-retraction cycles of the pectoral fins to elevate the centre of mass and propel the entire body anteriorly. Fishes that use an axial-appendage-based mechanism, e.g. walking catfishes Clarias spp., produce side-to-side, whole-body bending in co-ordination with protraction-retraction cycles of the pectoral fins. Once the body is maximally bent to one side, the tail is pressed against the substratum and drawn back through the mid-sagittal plane, which elevates the centre of mass and rotates it about a fulcrum formed by the pectoral fin and the ground. Although appendage-based terrestrial locomotion appears to be rare in osteichthyians, many different species appear to have converged upon functionally similar axial-based and axial-appendage-based movements. Based on common forms observed across divergent taxa, it appears that dorsoventral compression of the body, elongation of the axial skeleton or the presence of robust pectoral fins can facilitate effective terrestrial movement by air-breathing fishes.

Functional significance of intramandibular bending in Poeciliid fishes

Substrate-feeding teleosts show multiple, independent evolutionary acquisitions of intramandibular bending (bending within the lower jaw)—a behavior that likely enhances performance when feeding on attached or encrusting food items. However, intramandibular bending has only been quantified for marine teleosts. Here, we examine substrate feeding in eight species from the order Cyprinodontiformes and quantify movements produced by the anterior jaws of four target species selected from the family Poeciliidae to represent a variety of trophic strategies. Intramandibular bending, defined here as bending between the dentary and angular–articular bones of the lower jaw, is not present in some poeciliids (i.e. Gambusia affinis), nor is it present in outgroup cyprinodontiforms (i.e. Fundulus rubrifrons). However, intramandibular bending is present in certain poeciliids (i.e. Poecilia sphenops), and can exceed 90°. Such jaw bending enables the production of a gape angle that approaches 120°, which likely allows the fish to maximize contact between the toothed tips of the jaws and the substrate during the bite. Intramandibular bending in poeciliid species is associated with specific trophic shifts: the greater the intramandibular bending in a given species, the more attached algae (periphyton) reported in its diet. This result supports the hypothesis that intramandibular bending enhances performance when feeding on encrusting food items. We predict that additional examples of functional convergence are likely to be documented in freshwater teleosts as more herbivorous species are examined, and we propose that intramandibular bending represents an excellent model system in which to examine the functional processes that underlie convergent evolution.