Embryonic development of the bullseye puffer Sphoeroides annulatus (Tetraodontidae): A morphofunctional approach to ontogenetic steps

The embryonic development of the bullseye puffer, Sphoeroides annulatus, was characterized on the basis of the theory of saltatory ontogeny. This theory predicts a correlative relationship between the ontogeny-type in an altricial-precocial spectrum and the habitat that a species occupies within an unstable-stable environmental spectrum. Because S. annulatus inhabits a variety of unstable environments along a wide latitudinal range, the hypothesis that this species presents one of the most altricial embryonic developments among tetraodontids was tested. Based on major developmental events that marked the ontogenetic thresholds nine embryonic steps were identified. Developmental features such as small adhesives eggs, lack of vitelline circulation, small free embryos swimming up at hatching guided by positive phototaxis, and small first-feeding larvae actively swam in the water column, suggest that S. annulatus belongs to the reproductive guild of the nonguarders-lithopelagophils. Moreover, a comparative analysis of the developmental sequences, egg size, and first-feeding larvae size between tetraodontids confirms the hypothesis of this study and supports the evolutionary principle of the altricial-precocial spectrum postulated in the theory of saltatory ontogeny.     

Early development of the rainbow darter,Etheostoma caeruleum,according to the theory of saltatory ontogeny

Synopsis The early development of rainbow darter, Etheostoma caeruleum, was examined from an ecological perspective. Steps and thresholds of ontogeny to completion of body squammation are defined, and related to environmental factors. Rainbow darter eggs are about 2 mm diameter, considerably larger than those of related logperch (Percina caprodes). The embryonic vitelline respiratory plexus is much more extensive. The pelagic interval characteristic of logperch and ancestral percids is eliminated and onset of exogenous feeding is delayed. The larger larvae of the rainbow darter can begin feeding directly on aquatic insects, and complete their life cycle in streams. Therefore, shifts in the timing of important thresholds (e.g. exogenous feeding) are ecologically important. Furthermore, early maturation and/or delayed bone and scale formation may be responsible for reductions in the lateralis system and scalation in this and other darter species.     

Behavioural response of Kootenai white sturgeon (Acipenser transmontanus,Richardson, 1836) early life stages to gravel,pebble, and rubble substrates: guidelines for rearing substrate size

Guidelines for creating rearing substrate for sturgeon early life stages are needed for restoration programmes creating habitats for spawning and rearing of early life stages. To determine the effects of rock size on motile early life stages, experiments were conducted in artificial streams to observe the behaviour of free embryos and larvae of Kootenai River white sturgeon (Acipenser transmontanus) relative to rock size. Most (≥90%) of the free embryos in replicate test streams with 100% gravel, 100% pebble, or 100% rubble hid under rocks, with few moving downstream. There was no difference in downstream movement of free embryos among rock treatments, therefore all rock types provided cover habitat. Similarly, in rock mixture tests, with a variable percentage of pebble, small rubble, or large rubble in different tanks, even fewer free embryos moved downstream. With increasing age, larvae increasingly used the open bottom and velocity refuges downstream of or alongside rocks of any size while drift feeding. Downstream movement of larvae in both rock regime tests was affected by rock size, with significantly reduced movement relative to increasing abundance of large rock (rubble). However, in all rock mixtures, free embryos (and later, larvae when they stopped dispersing) preferred the smallest rock size available (pebble; P = 0.0001). This suggests a strong innate preference of both life stages for small substrate that is likely related to increased survival. A rock mixture of 10% gravel (16–32 mm diameter) and 30–40% pebble (diameter, 30–60 mm) should provide adequate rearing substrate for free embryos and early‐larvae. The remaining 50–60% should be mixed rubble and boulders for spawning and egg rearing.     

Microsatellite markers for the endangered Roanoke logperch, Percina rex (Percidae) and their potential utility for other darter species

The Roanoke logperch (Percina rex Jordan and Evermann), an endangered fish, occurs in only six watersheds in the Roanoke and Chowan river drainages of Virginia, USA. The species’ population genetic structure is poorly known. We developed 16 microsatellite markers that were reliably scorable and polymorphic P. rex. Markers were also screened in seven other darter species of the genus Percina. Most markers exhibited successful amplification and polymorphism in several species. These markers may therefore prove useful for population genetic studies in other darters, a diverse but highly imperiled group.     

Ecological and evolutionary consequences of early ontogenies of darters (Etheostomatini)

Synopsis The ecological classification of fishes into reproductive guilds is based on the premises that (1) reproductive styles and early ontogeny are closely related, and (2) both are correlated with the ecology of a species. A comparison of early ontogenies of logperch (Percina caprodes), rainbow darter (Etheostoma caeruleum), and fantail darter (E. flabellare) confirmed these premises, and provided possible explanations for diversity within the Etheostomatini. Young logperch have limited vitelline circulation, hatch while still poorly developed, and therefore must drift from oxygen rich lotic habitats to lentic habitats where small planktonic prey are available. Young rainbow and fantail darters have extensive vitelline plexuses, are well developed at transition to first feeding, and begin feeding on aquatic insects. Thus there is no necessity for a drift interval. As a result, the latter species are adapted for stream life. Interspecific differences in reproductive styles and early ontogenies may have contributed to speciation of darters by allowing partitioning of breeding sites and food resources for young. In addition, reduced drift dispersal and small stream habitation may have indirectly contributed to speciation by reducing genetic exchange among populations.     

Early Development of the Sofie, Chondrostoma toxostoma

The developmental biology of embryos, larvae and juveniles of sofie, Chondrostoma toxostoma, reared from artificial insemination, was examined under controlled laboratory conditions, using both in-vivo and preserved specimens. The complete remodelling process (metamorphosis) was described and interpreted according to the theory of saltatory ontogeny, providing a model within which the highly complex ecological niche and behaviour (habitat use, diet, etc.) of the free embryos and larvae can be evaluated. The sofie ova were relatively opaque and the free embryos presented a small yolksac. Consequently, the free embryo steps were short and the free embryos emerged rapidly from the substratum. The circulatory system appeared early and was simple, which suggests that sofie free embryos require well oxygenated water. The remodelling of the mouth from a superior to inferior position characterised changes in the sofie's diet during early life history, which is typical of the genus. Differences in development relative to the nase, C. naus, are discussed.     

Distribution and Relative Size of the Swim Bladder in Percina, With Comparisons to Etheostoma, Crystallaria, and Ammocrypta (Teleostei: Percidae)

The distribution of the swim bladder was examined in 20 species representing all four genera (Percina, Etheostoma, Crystallaria, and Ammocrypta) of darters (Etheostomatini). Including data on species examined in other studies, swim bladders have been found in 15 of 17 species of Percina, but were absent in Crystallaria asprella, Ammocrypta pellucida, and the 18 species of Etheostoma examined. Relative swim bladder length in Percina was shown to be positively correlated with body size. Although not statistically significant, swim bladder size also correlates with habitat (riffle, run, or pool) and swimming behavior (midwater or benthic).     

HETEROCHRONY AND DEVELOPMENTAL INNOVATION: EVOLUTION OF FEMALE GAMETOPHYTE ONTOGENY IN GNETUM,A HIGHLY APOMORPHIC SEED PLANT

Seed plant female gametophytes are focal points for the evolutionary modification of development. From a structural perspective, the most divergent female gametophytes among all seed plants are found in Gnetum, a clade within Gnetales. Coenocytic organization at sexual maturity, absence of defined egg cells (free nuclei are fertilized), lack of centripetal cellularization, and postfertilization development of embryo-nourishing tissues are features of the female gametophytes of Gnetum unparalleled among seed plants. Although the female gametophyte of Gnetum retains the three basic phases of somatic development common to female gametophytes of plesiomorphic seed plants (free nuclear development, cellularization, cellular growth), the timing of fertilization has been accelerated relative to the rate of somatic development. As a consequence, the female gametophyte of Gnetum matures sexually (is fertilized) at a juvenile (compared with the ancestral somatic ontogeny) and free nuclear stage of somatic development, thereby precluding differentiation of egg cells. Unlike progenetic animals, where truncation of somatic ontogeny evolves in tandem with acceleration in the timing of sexual maturation, the female gametophyte of Gnetum completes the entire ancestral somatic ontogeny after precocious sexual maturation. This results in the evolution of postfertilization development of embryo-nourishing female gametophyte tissues, a phenomenon unique among seed plants. Nonheterochronic developmental innovations have also played important roles in the evolution of the female gametophyte of Gnetum. Centripetal cellularization, which is always associated with the phase change from coenocytic to cellular organization among plesiomorphic seed plant female gametophytes, is lacking in Gnetum. Instead, during early phases of development, apomorphic free nuclear organization is coupled with a highly anomalous pattern of cellularization. Stage-specific innovations during early development in the female gametophyte of Gnetum do not affect plesiomorphic aspects of later phases of development. Thus, a complex array of heterochronic and nonheterochronic developmental innovations have played critical roles in the ontogenetic evolution of the highly apomorphic female gametophyte of Gnetum.     

Early ontogeny of Adinia xenica (Pisces,Cyprinodontiformes): 1. The development of embryos in hiding

Synopsis Examination of living and stained preserved embryos of the fundulid Adinia xenica from the intertidal salt marshes of the northern Gulf of Mexico, revealed a saltatory pattern of development. Embryonic structures indicate an ability to tolerate low oxygen conditions, primarily by extensive vascularization of the large yolksac and pericardial headfold, and capillaries covering the entire body. Adhesive fibres of the chorion hold the egg to the chosen substrate, away from anoxic sediments. Prior to hatching most embryos enter a resting interval of up to four weeks, with a mean duration of 8 days (in the laboratory). Growth ceases, development is limited to some skeletal calcification, and metabolic rate, as indicated by bradycardia and yolk resorption, is greatly reduced. This step distributes hatching and recruitment over time in a variety of environmental conditions. Hatching is considered to result from a variable summation of internal and external factors; ease of its induction increases during the resting interval. Upon hatching most embryos are well developed and ready to feed exogenously, there being essentially no free-embryo phase. The considerable individual variation in timing and relative order of some ontogenic events may provide opportunities for environmentally induced heterochronies and thus assist A. xenica to develop in a range of habitats and conditions. Reproductive style includes hiding the eggs in protected locations, and a fractional spawning pattern. Consideration of this plus morphological adaptations, egg size and adhesivity places A. xenica in the reproductive guild of brood-hiding cavity spawners.     

Ontogenetic shifts in habitat use by the endangered Roanoke logperch (Percina rex)

1. Conservation of the federally endangered Roanoke logperch (Percina rex, Jordan and Evermann) necessitates protection of habitat that is critical for all age classes. We examined habitat use patterns of individual logperch to determine: (1) if age classes of logperch in the Nottoway and Roanoke Rivers exhibit habitat selectivity, (2) if age classes differ in habitat use, and (3) if ontogenetic patterns of habitat use differ between the Roanoke and Nottoway river populations. 2. In the summers of 2000 and 2001, we observed 17 young‐of‐year (YOY) logperch [<4 cm total length (TL)], 13 subadult logperch (4–8 cm TL), and 49 adult logperch (>8 cm TL) in the upper Roanoke River, and 40 subadult and 39 adult logperch in the Nottoway River, Virginia. 3. All size classes of Roanoke logperch demonstrated habitat selectivity and logperch used a wide range of habitats in the Roanoke and Nottoway rivers during ontogeny. Habitat use by logperch varied among age classes and between rivers. 4. In the Roanoke River, adult and subadult logperch primarily preferred run and riffle habitat, often over gravel substrate. Subadults were found in lower water velocities and slightly more embedded microhabitats than adults. YOY logperch were found in shallow, stagnant backwaters and secondary channels. In the Nottoway River, both adult and subadult logperch were found over sand and gravel in deep, low‐velocity pools and runs. Subadults were observed in slightly more silted, lower velocity habitat than adults. Shifts in habitat use were more distinct between age classes in the Roanoke River than the Nottoway River. 5. Successful conservation of this species will involve sound understanding of spatial variation in habitat use over logperch life history and preservation of the ecological processes that preserve required habitat mosaics.     

Patterns of diversification in a North American endemic fish,the Blackbanded Darter (Perciformes,Percidae)

The coastal plain of the south‐eastern United States shows multiple biogeographic patterns of plant and animal dispersal; however, few freshwater fish taxa span these biogeographic barriers. Percina nigrofasciata, the Blackbanded Darter (Teleostomi: Percidae), is a small, benthic, freshwater fish species with an extensive range in the south‐eastern United States. Recently, two species have been elevated from within P. nigrofasciata: P. crypta and P. westfalli, but their ranges have not been established. We broadly sampled across the south‐eastern United States, encompassing the range of P. nigrofasciata sensu lato. We reconstruct the phylogeny of Percina using both mitochondrial and nuclear markers. Eighty‐four specimens of Percina nigrofasciata were sampled for the mitochondrial gene cytochrome b (1,119 bp) to form a base phylogeny. The nuclear marker S7‐I1 was subsampled across populations to detect instances of hybridization. Phylogenetic relationships with other members of the genus Percina were assessed through Bayesian inference. Our results suggest that Percina nigrofasciata sensu stricto occurs from the Lake Pontchartrain Basin in Louisiana to the rivers of the Mobile Basin with little genetic structuring throughout its range. Percina westfalli occurs from the Apalachicola River drainages to the Atlantic Slope from the Savannah River to the St. Johns River. We find that P. crypta is not genetically distinct from P. westfalli in the Chattahoochee and Flint Rivers. Possible ancestral hybridization occurred between the P. nigrofasciata and P. westfalli in the panhandle of Florida between Mobile Bay and the Apalachicola River.     

Habitat use and feeding behavior of thirteen species of benthic stream fishes

Synopsis The densities, habitat use, and feeding behaviors of 13 fish species belonging to the benthic invertebrate-feeding guild were studied by snorkeling at three localities in the Little River of eastern Tennessee, U.S.A. Resource partitioning occurred by habitat, feeding behavior and time of activity. Differences were also found at the generic level.Cottus was a nocturnal feeder, whereasPercina andEtheostoma were, for the most part, diurnally active.Percina moved about rapidly and spent most of its time above the bottom. In contrast,Etheostoma varied considerably in the amount of time spent under cover, spent little time above the bottom, and exhibited low levels of swimming activity. Nearly all species sought cover at night, suggesting they may be particularly sensitive to predation at night. Species with small adult sizes (Etheostoma, Cottus andP. evides) were concentrated in shallow water habitats, whereas species with large adult sizes (Percina) were more abundant in deep water habitats. The habitat use data are consistent with the hypothesis that size-selective predation by centrarchid bass may cause smaller fish to avoid deep water areas. Large species should have a lower risk of predation due to their size and behavior.     

Alternative life histories of the genusLucania: 2. Early ontogeny ofL. goodei,the bluefin killifish

Synopsis This is the second of three papers devoted to the interpretation of morphological development in altricial and precocial species within the genus Lucania. The focus of this paper was the early life history of the bluefin killifish,Lucania goodei. Reproductively mature specimens were collected in the run below Newport Spring, north of St. Marks National Wildlife Refuge in northwest Florida. These specimens were transported to the laboratory, where they served as brood stock for specimens described in this study. Offspring were reared under controlled conditions and were described according to the theory of saltatory ontogeny, which gives a sampling design based on morphological, rather than chronological, progression. The morphological development of these offspring is described on the basis of detailed illustrations, photomicrographs, and measurements of mensural and meristic characters. This account of early ontogeny, in combination with a corresponding study on the early ontogeny of the rainwater killifish,L. parva (Crawford & Balon 1994a), establishes the empirical basis for an altricial-precocial life history model (Crawford & Balon 1994b).     

The function of the caudal keel inPercina (Percidae)

Synopsis Unique to darters of the subgenusOdontopholis ofPercina andPercina (Imostoma)antesella is the development of a caudal keel in breeding males. The keel is a semicircular extension of the ventral surface of the caudal peduncle and anterior lower caudal fin. The reproductive behavior of species ofPercina implies an adaptive function related to the burial and fertilization of eggs. The caudal keel appears to serve as a plow-share which, in conjunction with an elongated anal fin, facilitates the transfer of sperm from the male's genital opening to eggs buried in the substrate by the female.     

Embryo and early larval stages of the Humboldt Current krill Euphausia mucronata (Crustacea: Euphausiacea)

The Humboldt Current krill, Euphausia mucronata (Crustacea: Euphausiacea), is an endemic and keystone species in the food web of this highly productive eastern border current ecosystem. The morphology and ontogeny of E. mucronata is known from calyptopis I to the adult phase, but the embryonic and early‐life stages (nauplius and metanauplius) of this broadcast spawning species are unknown. We describe the morphology and development time of these life stages to complete the knowledge of its life cycle. Embryos were obtained from purple‐gonad gravid females collected off Dichato, central Chile, during November 2012. Eight gravid females (mean=16 mm total length) were incubated in seawater at 12°C under laboratory conditions. The average development time from single‐cell embryos to the metanauplius stage was 2.2 d and hatching occurred between 20 and 25 h. The average growth rate was 0.35 mm d^?1 from the late limb bud to the metanauplius stage (range=0.21–0.48 mm d^?1). Embryos of E. mucronata had a mean chorion diameter of 0.460 mm, embryo diameter of 0.343 mm, and perivitelline space of 0.056 mm. Our biological information reported here constitutes a baseline for future ecological studies on distribution and temporal variability of spawning activity and reproductive strategies of E. mucronata in the highly variable and productive Humboldt Current ecosystem.     

Ontogeny of gene expression in Pomoxis (pisces: Centrarchidae)

The regulation of gene expression during embryogenesis was investigated in white and black crappie (Pomoxis spp.) and their reciprocal interspecific F₁ hybrids. The schedule of morphological development and the timing of isozyme expression were compared among the two species and both reciprocal maternal half-sibling F₁ hybrids. Although absolute rates of morphological development differed in response to incubation temperature, relative rates of morphological development (normalized to the onset of retinal pigment deposition) were similar among all crosses. Furthermore, these relative rates were similar to those previously documented for other centrarchid species. To assess differences in ontogenetic patterns of gene expression among the crosses, we examined expression for 39 enzymeencoding loci. Expression was not detected in the embryos for 16 loci due to low or nonexistent activity. Enzymatic activity from eight other loci were continuously detected throughout embryogenesis as a result of maternal enzyme in the egg. However, 15 loci initiated expression during the early development period investigated (fertilization through yolk sac absorption). We observed temporal variability in expression of these 15 loci among the crosses, either in the form of differential expression between parental species or as disturbances in the ontogeny of expression in interspecific hybrids. Such variability in expression suggests that some of the gene regulating mechanisms have diverged since Pomoxis species shared a common ancestral genome. © 1994 Wiley-Liss, Inc.     

Early ontogeny of white sucker,Catostomus commersoni,with steps of saltatory development

Synopsis Frequent and detailed observations of arbitrary stages revealed a saltatory pattern of development in the early ontogeny of fluvial spawning white sucker. Considered as adaptations for respiration were: i) expansion of the surface area of the yolk through a change in yolk shape, ii) the presence of carotenoid pigment in the yolk, iii) a large caudal vein sinus, iv) coverage of the yolk surface with capillaries of bilaterally paired vitelline plexi, and v) a large pair of vitelline veins. The ability to swim developed slowly and well after hatching. Young suckers would therefore spend most of the eleutheroembryonic phase in the interstices of the rock substrate of the spawning ground. The change from a benthic to pelagic mode of existence occurred with swimbladder inflation and before the start of exogenous feeding.     

Development of the visual system of anchovy larvae,Engraulis anchoita: A microanatomical description

During the early ontogeny of fish larvae, the accurate development of the visual system plays a key role, because it is involved in locating food, orientation, selection of favorable habitat, and evasion of predators. The structure of the eye of the fish is typical of vertebrates, with some modifications related to the aquatic environment. In the present work, we describe the development of the larval eye of Engraulis anchoita for the first time. Larvae were collected at the Permanent Station of Environmental Studies (EPEA) in coastal waters of the Southwestern Atlantic Ocean during research cruises in 2015 and 2016. We describe the histology of the retina layers, determine the beginning of the functionality of the eye, and discuss a possible synchronization with the development of the digestive tract. This study provides information about the biology of E. anchoita, the most abundant fish species in the southwestern Atlantic Ocean. Also, recent studies have shown responses of the retina and other tissues to the increase in environmental acidity. Therefore, results of this study are also discussed with respect to the possible effect of acidification on the larvae of this species. The continuity of the time series developed at the EPEA will allow monitoring the effect of long-term environmental and biological variables on the early ontogeny of anchovy in the context of climate change. The high commercial fishing potential of E. anchoita due to its high abundance, as well as its essential role in the trophic web of other commercially valuable fishing resources of Argentina, reinforce the need to continue deepening knowledge about this species. Research highlights:

• Eyes of Engraulis anchoita larvae are functional from early larval stages.
• At hatching, the retina is formed by only few layers from which the other layers differentiates during ontogeny.
• Focal distance increases with larval growth.

     

The parachute function of the hull in eggs of Mopalia kennerleyi (Chitonida: Mopaliidae), and swimming of its larvae through ontogeny

Free‐spawning species of chitons produce eggs enclosed in a coating known as the hull. In Chitonida, several studies have shown that the hull helps to direct sperm to specific areas of the egg surface, facilitating fertilization. One study has found evidence that this structure also serves to reduce the sinking rates of the eggs. To clarify how the presence of the hull modifies sinking rates in chiton eggs, here we compare sinking speeds and densities of eggs of Mopalia kennerleyi with and without the hull. Sinking rates of eggs with the hull were approximately one‐third of those without it. This structure acts as a flotation device because it has a density very close to that of seawater, and it increases the effective diameter and therefore the drag on the negatively buoyant egg. Since there is limited knowledge about morphology and behavior of chiton larvae, we also analyzed changes during ontogeny in behavior, swimming speeds, and body shape of larvae of M. kennerleyi. Over time, the larvae decreased their upward swimming tendency and preferred to stay near the bottom, and their bodies became elongated and dorso‐ventrally compressed. These changes may be related to preparation for settlement and metamorphosis. Further studies of these subjects are required in chitons, since movement of early stages, as eggs/embryos sinking or larvae swimming in the water column, may affect their survival.     

Ontogenetic modulation of branch size,shape, and biomechanics produces diversity across habitats in the Bursera simaruba clade of tropical trees

Organismal size and shape inseparably interact with tissue biomechanical properties. It is therefore essential to understand how size, shape, and biomechanics interact in ontogeny to produce morphological diversity. We estimated within species branch length‐diameter allometries and reconstructed the rates of ontogenetic change along the stem in mechanical properties across the simaruba clade in the tropical tree genus Bursera, measuring 376 segments from 97 branches in nine species in neotropical dry to rain forest. In general, species with stiffer materials had longer, thinner branches, which became stiffer more quickly in ontogeny than their counterparts with more flexible materials. We found a trend from short stature and flexible tissues to tall statures and stiff tissues across an environmental gradient of increasing water availability, likely reflecting a water storage–mechanical support tradeoff. Ontogenetic variation in size, shape, and mechanics results in diversity of habits, for example, rapid length extension, sluggish diameter expansion, and flexible tissues results in a liana, as in Bursera instabilis. Even species of similar habit exhibited notable changes in tissue mechanical properties with increasing size, illustrating the inseparable relationship between organismal proportions and their tissue mechanics in the ontogeny and evolution of morphological diversity.