The Development of Form and Function in Fishes and the Question of Larval Adaptation

<em>Abstract.</em>—This review examines the transition from cutaneous to branchial respiration and ionoregulation in teleost larvae. Before gills develop, the skin is the only significant site of gas and ion exchange. The primary site of these two processes shifts from the skin to the gill as development proceeds. When the transition begins and the speed at which it occurs, both vary considerably depending on species. In general, ionoregulatory activity begins to shift to the gill before gas exchange. The transition to branchial ionoregulation also tends to proceed more rapidly than the transition to branchial respiration. The key morphological indicator of the shift in ionoregulatory activity to the gill is the appearance of large numbers of mitochondria-rich cells on gill arches. The corresponding indicator for gas exchange is the appearance of gill lamellae. For both activities, the transition occurs gradually, and even at the end of the larval period, the skin still plays an important role in both processes. This is particularly true for gas exchange. The ecological implications of the transitions and what they may mean in terms of gill evolution are discussed.

The Development of Form and Function in Fishes and the Question of Larval Adaptation

<em>Abstract</em>.—Fish embryos and larvae are developing, not static, organisms before metamorphosis or transformation to the juvenile form. The means by which embryos and larvae meet physiological challenges posed by their environments and the extent to which evolution shapes the outcome of development is only partially understood. An understanding of these issues can only be approached by coupling the development of form and function over the broad phylogenetic span of fishes. Much work has come forward that describes the development of body form and organ systems, while equally valuable, but often separate, work has emerged that describes the physiology of embryos and larvae. Far fewer composite studies that couple developing form with function are available, and fewer yet have addressed such questions as when, and in what capacity, do developing organs or organ systems function. The evolutionary question also requires a phylogenetic perspective. The reviews that follow this introduction will present current thought that reflects upon the following questions: (1) when is the onset of organ (or organ system) development, and in what physiological capacity do these systems operate among fish embryos and larvae; and (2) are there morphological and physiological specializations that are unique to embryonic and larval fishes, and what are these specializations?

The Development of Form and Function in Fishes and the Question of Larval Adaptation

<em>Abstract.</em>—Three phases of myogenesis have been identified in the myotomal muscles of larval teleosts. The commitment of embryonic slow and fast muscle lineages is determined prior to segmentation (embryonic myogenesis) and involves notochord and floorplate derived signaling pathways, which drive the adaxial cells to a slow muscle fate. The adaxial cells elongate to span the entire somite width and subsequently migrate through the myotome to form a superficial layer of slow muscle fibers. The remaining cells of the lateral mesoderm adopt the default fast muscle phenotype. The second phase of fiber expansion in the myotomes involves recruitment from discrete germinal zones for both slow and fast muscle fibers (stratified hyperplasia). Finally, myogenic precursor cells are activated throughout the myotome (mosaic hyperplasia). The progeny of these cells either fuse to form additional fibers on the surface of existing muscle fibers or are absorbed by fibers as they expand in diameter (hypertrophic growth). There is considerable species diversity with respect to the timing of innervation of the embryonic muscle fibers in relation to other developmental events, the degree of maturation of the muscle fibers at hatching, and the onset and relative importance of stratified and mosaic hyperplasia to growth during larval life. A subset of myogenic cells specified by their position in the anterior myotomes are thought to migrate out and populate the pectoral fin buds leading to the differentiation of the pectoral fin muscles. Little is known about the mechanism of formation of the unpaired fin muscles, which occurs after the differentiation of the myotomes and is often delayed until relatively late in larval life. During ontogeny, embryonic isoforms of the myofibrillar proteins are replaced by larval and adult isoforms, and the adult multiterminal pattern of slow muscle innervation gradually develops, reflecting changes in swimming style and performance as body size increases. The body length at which particular protein isoforms are switched on varies for each myofibrillar component and with temperature. In general, early larval stages show a greater reliance on aerobic metabolic pathways and a lower capacity for anaerobic glycolysis than later larval and juvenile stages. Temperature has a marked effect on the ultrastructure, number, and phenotype of larval muscle fibers. Recent evidence suggests that egg incubation temperature can influence myogenic cell commitment, producing long-term consequences for fiber recruitment and growth performance during subsequent stages of the life cycle. The ecological significance of the phenotypic plasticity of muscle growth and some potential applications to fisheries science are briefly discussed.

The Development of Form and Function in Fishes and the Question of Larval Adaptation

<em>Abstract.</em>—The swim bladder originates as an unpaired dorsal outgrowth of the posterior foregut. While in physostome fish the embryonic connection to the pharynx persists, in physoclist fishes, it is lost during early development. In most fish larvae, the swim bladder is inflated shortly after hatching, just prior to the time of first feeding. At this time, many larvae swim up and start surfacing. In this case, initial inflation of the swim bladder is achieved by gulping air, and a lack of swim bladder inflation often is accompanied by a significant reduction of viability. While this appears to be the way most physostome fish inflate their swim bladder, some species obviously are able to inflate the swim bladder without surfacing. In adult fish, gas secretion into the swim bladder requires the activity of gas gland cells, which acidify the blood and thus induce a decrease in its gascarrying capacity. In consequence, gas partial pressures increase, providing a pressure head for the diffusive transport of gas from the blood into the swim bladder. Recent studies on the European glass eel <em>Anguilla anguilla </em>suggest that, at the time of first inflation, gas gland cells may not yet be functional. Nevertheless, glass eels can inflate their swim bladder without surfacing. Although various mechanisms have been proposed to explain the inflation of the swim bladder without gulping air, a decisive answer cannot yet be presented.

The Development of Form and Function in Fishes and the Question of Larval Adaptation

<em>Abstract.</em>—The liver and bile system, as well as the exocrine pancreas, with their digestive enzymes are of fundamental importance for metabolic processes and digestion of exogenous food in developing fish. The pancreatic tissue, liver hepatocytes, the gallbladder, and bile system develop when embryos/larvae are still solely depending on endogenous yolk reserves as sources for metabolic energy and structural components. Due to the central role of the liver in different metabolic pathways, its structure clearly reflects the nutritional status and condition in feeding larvae. Stored glycogen and synthesis of lipoproteins in the liver have been reported during the endotrophic phase for different species. Bile components are synthesized in the liver and excreted at first feeding and thereby contribute to improved lipid digestion and uptake in the gut epithelium cells. The hepatic energy stores respond sensitively to nutritional changes and physiological unbalances. The exocrine pancreas is functional at the time of hatching or mouth opening, which is well documented by histological localization of zymogen granules, as well as by immunochemical and molecular detection of several pancreatic enzymes or their precursors. The later development is mainly characterized by quantitative growth, while no new structural elements develop. As in adults, fish larvae seem to possess the most important, if not all, pancreatic enzymes. Amylase, trypsinogen, chymotrypsinogen, and, more recently, phospholipase A₂ and bile salt-dependent lipase are some of the enzymes that have been detected at very early larval stages and show that fish larvae are able to digest ingested food. The developmental sequence of cell differentiation, like the synthesis of enzymes, and bile appear to be genetically programmed, while a dietary influence has been detected on both the organ structure and enzyme levels after the endotrophic phase. The shift from endogenous to exogenous stimulation occurs during the endo–exotrophic phase, and a decline or a stagnation of liver and pancreatic function is reported during this period for many pelagic marine fish larvae. Whether this is a normal development or an environmentally/dietary-caused delay in digestive functionality remains to be solved. Numerous in vitro studies have shown that the activity and secretion of pancreatic enzymes are affected in different degrees by food ration size, nutritional status, and dietary composition. The ingestion rate of food seems to regulate pancreatic responses at an earlier time than the dietary composition. Fish larvae, in general, are capable of digesting their food without being dependent upon exogenous enzymes from live prey in terms of digestive capacity.

The Development of Form and Function in Fishes and the Question of Larval Adaptation

<em>Abstract.</em>—This paper examines how allometric analysis can be used as a tool to explain morphological changes that take place during fish larval development. First, constraints to survival, growth, and continued differentiation are identified. Then, processes of growth are predicted to meet and overcome these constraints, which are mutually interrelated. The final step is to test the predictions by looking at growth of the entire animal and at separate elements belonging to particular functional systems. The reproductive strategy of producing numerous, but very small eggs, adopted by many teleosts, has major implications. In particular, the lack of reserves, the need to utilize external food early in life, and the extreme susceptibility of newly hatched larvae to predation put them under strong selective pressure to grow rapidly. Small size also means that viscous forces are much more important than they are at bigger size later in life. When energy is limited, larvae should direct available resources towards primary needs yielding the greatest return in terms of enhancing the larva’s ability to find, capture, and assimilate additional food and to avoid being eaten. We speculate that constructions for feeding, swimming, and ventilation are particularly important and should therefore grow early and at a higher rate than the body as a whole. Allometric data of a wide variety of species and taken from several functional complexes are presented to support this contention. Length dependent changing growth coefficients of head, trunk, and tail indeed show the predicted priorities in different major groups of fish. High positive allometric growth of structures involved in feeding make early larvae specialized zooplanktivorous predators.

The Development of Form and Function in Fishes and the Question of Larval Adaptation

<em>Abstract.</em>—Adult fishes sense vibrations and disturbances in the water through the auditory and mechanosensory lateral line systems. The developmentally complete systems impart certain levels of sensitivity and acuity to a fish, but fish larvae hatch with rudimentary auditory and lateral line systems that confer poor sensory performance. The structures become more elaborate during ontogeny, with attendant improvement in performance. This review summarizes the ontogenetic changes in the peripheral anatomy of these sensory systems as well as the experimental work that has been undertaken to measure the changing functionality of each. In both systems, the number of end organs increases ontogenetically, roughly in proportion to somatic growth. Improvements in sensory function coincide with, and may be attributable to, these increases in end organs. Accessory structures that enhance functionality develop late in the larval period. Problems and recent advances in methodology as applied to larval fishes are discussed.

The Development of Form and Function in Fishes and the Question of Larval Adaptation

<em>Abstract.</em>—Although the basic structure of the vertebrate retina is similar across taxa, high variability in specific features of the fish retina reflects the differences in visual microhabitat of these species. The vertebrate retina is the first step in the neural integration of visual information. A great deal of retinal function can be inferred from structure, and as these relationships continue to be revealed, we are gaining new insights into how vision is integrated by the nervous system. Among fishes, the developmental rate and acquisition of retinal structures is highly variable. While some species develop all structures early in embryogenesis, others delay acquisition of the full adult retinal complement of cells until months after hatching. Given the tight relationship between structure and function, differences in the timing of retinogenesis have implications for the visionbased survival skills of the early life history stages and for the overall ecology and fitness of the species. Although much of the observed variation may be related to altricial versus precocial life history strategies, we suggest that protracted retinal development also reflects and separates the constraints imposed by the requirements of foraging and predator avoidance. As evidenced by a typically monochromatic all-cone retina, the eye of early fish larvae is adapted for efficient foraging in bright light. At later stages, an improved ability to identify the presence of predators is acquired via addition of rod photoreceptors for low light vision, as well as multiple cone spectral channels (and regularly geometric cone mosaics) for increased contrast and motion sensitivity. The larval retina of some species exhibits further specializations, such as the pure rod retina of the eel leptocephalus and the pure green cone retina of many marine teleosts. Overall, variation in the development of the teleost retina can be viewed as a continuum from very rapid to greatly delayed. The developmental trajectory of the visual system in any given species represents a product of evolutionary history, developmental constraints, and foraging and predation pressures.