Fish Ontogeny Research Articles

The Scientific Achievements of Gordon H. Copp (1956–2023): An Unabridged Version From His Doctor of Science Portfolio

ABSTRACTThis paper outlines the scientific achievements of Gordon H. Copp (1956–2023) in fish biology and invasion science as presented in his Doctor of Science portfolio. Gordon's mentorship began during his postdoctoral research and expanded to involve students, early‐career researchers as well as prominent fish biologists in a vast number of research projects. Early in his career, Gordon was involved in the study of floodplain fish communities for which he developed a novel technique for sampling young‐of‐year (0+) fish and in the early ontogeny of fishes. Gordon's later involvement in non‐native species policy has been pivotal, from developing risk analysis schemes for freshwater fishes to advising on EU and UK regulations. Gordon's research throughout his entire career on the pumpkinseed sunfish Lepomis gibbosus as a model species highlights his focus on understanding and predicting invasiveness under varying climate conditions, contributing to a broader understanding of non‐native species impacts.

A complete study of neuroendocrine regulation of fish reproduction. 4. Migration impulse as a starting mechanism of spawning

The participation of the hypothalamo-hypophysial neurosecretory system (NS) in the initiation of anadromous fish spawning migration was established on the basis of ecological-histophysiological analysis the results of histomorphological, immunohistochemical and electron microscopic studies for the first time. Activation of the neurosecretory products synthesis in the neurosecretory cells perikaryons and their excretion into the cerebrospinal fluid of the III brain ventricle in anadromous migrants forms at the beginning of the river spawning migration, spring-spawning: Russian sturgeon, stellate sturgeon and autumn-spawning: pink salmon and chum salmon, was shown. Transport and mass accumulation of neurosecretory products in the neurohypophysis were discovered at the same time. It is concluded, that the NS impacts a complex synchronous effect, which consists: firstly, in the neurotropic effect of nonapeptide neurohormones (NPh) on behavioral centers, which causes a dominant state of CNS excitation corresponding to the “Migration impulse”; secondly, in the violation of the long-term adapted marine “Pastured” level of osmoregulation; and thirdly, in the cessation of the well-known antigonadotropic effect of NPh, which contributes the organism transition to the energyconsuming energy type of metabolism. A comparative analysis (cross-analysis) of our own and literature data confirms the commonality and points to the universality of this metabolic mechanism for different forms of migration in fish ontogeny, which allows us to consider it as the most important aromorphosis type of phylogenetic adaptations, aimed at the species biological progress achieving. In the subsequent navigational mechanisms of homing, widely covered in the world literature, the leading role is played by the luliberinergic centers of the hypothalamus. The ecological diversity of these population-level mechanisms and the presence of straing in fish allow us to consider them as specializations of microevolutionary origin. The most promising direction for the further neuroendocrinological research development seems to be the analysis of the mechanisms of imprinting in connection with the enhancement of growth and survival of juveniles in the critical salinity medium, and for the purpose of homing control (development of the commercial fish-return biotechnology management) — the mechanisms of interaction between the NS and the luliberinergic centers in the neuroendocrine complex of CNS.

Development of Schooling Behavior in Fish Ontogeny

Development of Schooling Behavior in Fish Ontogeny

Tryptophan and Cortisol Modulate the Kynurenine and Serotonin Transcriptional Pathway in the Kidney of Oncorhynchus kisutch.

Aquaculture fish are kept for long periods in sea cages or tanks. Consequently, accumulated stress causes the fish to present serious problems with critical economic losses. Fish food has been supplemented to reduce this stress, using many components as amino acids such as tryptophan. This study aims to determine the transcriptional effect of tryptophan and cortisol on primary cell cultures of salmon head and posterior kidney. Our results indicate activation of the kynurenine pathway and serotonin activity when stimulated with tryptophan and cortisol. An amount of 95% of tryptophan is degraded by the kynurenine pathway, indicating the relevance of knowing how this pathway is activated and if stress levels associated with fish culture trigger its activation. Additionally, it is essential to know the consequence of increasing kynurenic acid "KYNA" levels in the short and long term, and even during the fish ontogeny.

Thyroid hormones in development of coloration of two species of Neotropical cichlids.

Neotropical cichlids demonstrate an enormous diversity of pigment patterns, a morphological trait that plays an important role in the adaptation and speciation. It has been suggested that alterations of the activity of the thyroid axis, one of the main endocrine axes regulating fish ontogeny, are involved in the development and diversification of pigment patterns in the Neotropical cichlids. To test this hypothesis, we assessed the thyroid hormone developmental dynamics and pigment patterning, and experimentally induced hyper- and hypothyroidism at different developmental stages in convict cichlid, Amatitlania nigrofasciata, and blue-eye cichlid, Cryptoheros spilurus. We revealed that both species display a similar type of coloration development and similar reactions on changes of the thyroid hormone level, but species-specific differences in hormonal dynamics and thyroid hormone-responsiveness. These findings indicate that thyroid hormone is a necessary but not sufficient signal to induce the transition from larval to juvenile coloration, and is a component of a complex, concerted endocrine cascade that drives skin development.

Bone calcification rate as a factor of craniofacial transformations in salmonid fish: Insights from an experiment with hormonal treatment of calcium metabolism.

Adaptation to different environments can be achieved by physiological shifts throughout development. Hormonal regulators shape the physiological and morphological traits of the evolving animals making them fit for the particular ecological surroundings. We hypothesized that the artificially induced hypersynthesis of calcitonin and parathyroid hormone mutually influencing calcium metabolism could affect bone formation during early ontogeny in fish imitating the heterochrony in craniofacial ossification in natural adaptive morphs. Conducting an experiment, we found that the long-standing treatment of salmonid juveniles with high doses of both hormones irreversibly shifts the corresponding hormone status for a period well beyond the time scale for total degradation of the injected hormone. The hormones program the ossification of the jaw suspension bones and neurocranial elements in a specific manner affecting the jaws position and pharingo-branchial area stretching. These morphological shifts resemble the adaptive variants found in sympatric pelagic and demersal morphs of salmonids. We conclude that solitary deviations in the regulators of calcium metabolism could determine functional morphological traits via transformations in skeletal development.

Comparison of Taste Reception and Feeding Behavior of the Nile Tilapia Oreochromis niloticus (Cichlidae) of Different Age

Comparison of specimens of the Nile tilapia Oreochromis niloticus of two age groups did not show any significant differences. L-cysteine, L-lysine and citric acid have an attractive taste for juveniles (age 1.5 months, body length 6.5–7.0 cm, weight 5–7 g); L-cysteine and citric acid have an attractive taste for adult fish (4 months, 12–15 cm, 45–50 g). The other eight L-amino acids have an indifferent taste for fish of both age groups. Based on the data obtained and the results of other studies, a hypothetical scheme is proposed, according to which the fastest functional transformations of taste reception in fish ontogeny occur after the start of exogenous feeding of larvae and are completed before maturation. Fish of both age groups rarely re–grasp pellets flavored with taste substances, but juveniles spend much more time on pellets orosensory evaluation, up to 1.4–1.6 times. Regardless of the fish age, such an assessment requires more time if the testing of pellets ends with their ingestion. The differences may indicate an undeveloped stereotype of feeding behavior in juveniles of Nile tilapia.

Aerobic response to thermal stress across ontogeny and habitats in a teleost fish.

Near-future climate change projections predict an increase in sea surface temperature that is expected to have significant and rapid effects on marine ectotherms, potentially affecting a number of critical life processes. Some habitats also undergo more thermal variability than others, and the inhabitants therefore must be more tolerant to acute periods of extreme temperatures. Mitigation of these outcomes may occur through acclimation, plasticity or adaptation, although the rate and extent of a species' ability to adjust to warmer temperatures is largely unknown, specifically as it pertains to effects on various performance metrics in fishes that inhabit multiple habitats throughout ontogenetic stages. Here, the thermal tolerance and aerobic performance of schoolmaster snapper (Lutjanus apodus Walbaum, 1792) collected from two different habitats were experimentally assessed under different warming scenarios (temperature treatments = 30, 33, 35, 36°C) to assess vulnerability to an imminently changing thermal habitat. Larger subadult and adult fish collected from a 12 m deep coral reef exhibited a lower critical thermal maximum (CTmax ) compared to smaller juvenile fish collected from a 1 m deep mangrove creek. However, the CTmax of the creek-sampled fish was only 2°C above the maximum water temperature measured in the habitat from which they were collected, compared to a CTmax that was 8°C higher in the reef-sampled fish, resulting in a wider thermal safety margin at the reef site. A generalized linear model showed a marginally significant effect of temperature treatment on resting metabolic rate (RMR), but there were no effects of any of the tested factors on maximum metabolic rate or absolute aerobic scope. Post hoc tests revealed that RMR was significantly higher for creek-collected fish at the 36°C treatment and significantly higher for reef-collected fish at 35°C. Swimming performance [measured by critical swimming speed] was significantly lower at the highest temperature treatment for creek-collected fish and trended down with each successive increase in temperature treatment for reef-collected fish. These results show that metabolic rate and swimming performance responses to thermal challenges are somewhat consistent across collection habitats, and this species may be susceptible to unique types of thermal risk depending on its habitat. We show the importance of intraspecific studies that couple habitat profiles and performance metrics to better understand possible outcomes under thermal stress.

Biochemical composition and adenylate energy charge shifts in longfin yellowtail (Seriola rivoliana) embryos during development under different temperatures

The longfin yellowtail Seriola rivoliana is an emerging species for aquaculture diversification worldwide and production relies on fertilized eggs from captive broodstock. Temperature is the main factor that influences the developmental process and success during fish ontogeny. However, the effects of temperature on the utilization of the main biochemical reserves and bioenergetics are scarcely investigated in fish, whereas protein, lipid and carbohydrate metabolism have critical roles in maintaining cellular energy homeostasis. In this context, we aimed to evaluate metabolic fuels (protein, lipids, triacylglicerides, carbohydrates), adenylic nucleotides and derivates (ATP, ADP, AMP, IMP), and the adenylate energy charge (AEC) during embryogenesis and in hatched larvae in S. rivoliana at different temperatures. For this purpose, fertilized eggs were incubated at six constant (20, 22, 24, 26, 28 and 30 °C) and two oscillating (21⇄29 °C) temperatures. Biochemical analyses were made at blastula, optic vesicles, neurula, prehatch and hatch periods. Results indicated that the developmental period had a major influence on the biochemical composition at any temperature regime tested during the incubation. Protein content decreased only at hatching mainly due to the loss of the chorion, total lipids tended to increase at the neurula period and variations in carbohydrates depended on the particular spawn analyzed. Triacylglicerides were a critical egg fuel during hatching. The high AEC during embryogenesis and even in hatched larvae suggested an optimal energy balance regulation. The lack of critical biochemical changes from different temperature regimes during embryo development confirmed that this species exhibits a high adaptive capacity in response to constant and fluctuating temperatures. However, the timing of hatching was the most critical period of development, where biochemical components and energy utilization significantly changed. The oscillating temperatures tested may have physiological advantages without detrimental energetic effects that will require further research on larval quality after hatching.

Effects of Ethanol Preservation on Larval and Fingerling Walleye and Gizzard Shad Body Size

Characterizing larval fish dynamics helps identify factors contributing to poor or strong recruitment events and informs stocking practices. Growth is fundamental to fish ontogeny and survival, especially during critical early life stages, which can depend heavily on access to prey. However, obtaining accurate body size measurements of larval fish in the field can be challenging and often means samples must be preserved for later analysis. Importantly, this process can affect fish size. Here, we examined the effects of preservation in 95% ethanol on the total lengths (mm) and wet weights (mg) of larval and fingerling Walleye Sander vitreus and Gizzard Shad Dorosoma cepedianum collected from the field using pushed ichthyoplankton nets. We also estimated the time required for preservation effects to stabilize. Responses to preservation were similar between species, with consistent decreases in wet weights of ~40–70% depending on fish size, which took ~2 months to stabilize. Conversely, the response of total length was variable in direction, with lengths increasing or decreasing up to 5–10%. As a result, the average effect of preservation on total length was minimal (<2.5% decreases). Walleye and Gizzard Shad body size play an important role in understanding their dynamics early in life, and the effects of preservation should be considered to accurately and precisely characterize size metrics.

Multiscale analysis on otolith structural features reveals differences in ontogenesis and sex in Merluccius merluccius in the western Adriatic Sea.

Otolith biomineralization results from biochemical processes regulated by the interaction of internal (physiological) and external (environmental) factors which lead to morphological and ultrastructural variability at intra- and interspecific levels. The aim of this study was to conduct a multi-scale analysis of the sagittal otoliths of the Merlucius merlucius (European hake) from the western Adriatic Sea in order to correlate otolith features with fish ontogeny and sex. We show that otoliths of sexually undifferentiated (non-sexed) individuals having a fish body total length (TL) less than 15 cm had faster growth in length, width, area, perimeter, volume and weight and a higher amount of organic matrix compared with otoliths of sexually differentiated individuals (females and males) having a fish size range of 15–50 cm. Most importantly, with increasing fish TL, female saccular otoliths contained a higher number of protuberances and rougher surface compared with male specimens, which showed more uniform mean curvature density. The differences between females and males discovered in this study could be associated with fish hearing adaptation to reproductive behavioural strategies during the spawning season. The outcomes of this research provide insights on how size and sex-related variations in otolith features may be affected by fish ecological and behavioural patterns.

H Geoffrey Moser. Larval Fishes: Taxonomy, Distribution, and Fisheries Biology

Authors' note.—H Geoffrey Moser was one of the most influential larval-fish biologists of the past century. He was perhaps best known to ASIH members as the coeditor and motivating force behind the first ASIH Special Publication, Ontogeny and Systematics of Fishes. His other accomplishments included an extensive body of publications on larval fishes, with descriptions of development in almost 50 families and as editor of one of the most comprehensive regional identification guides for the California Current (relevant for much of the eastern Pacific and elsewhere). He co-taught courses in larval-fish identification that trained a generation of ichthyologists in that discipline. Many of those scientists have passed that skill on to younger students, continuing his legacy to the present. In addition, he was a talented illustrator and a poet. Geoff, as he was known to his colleagues and friends, passed away unexpectedly at the age of 83 on September 30, 2021. He was interviewed for this Historical Perspective by internet during the COVID-19 pandemic at his home in Bozeman, Montana, in April, 2021 by Eric Hilton and Bruce Mundy. He also provided most of the photographs. The interview was completed through questions and answers exchanged by email. Geoff was shown all of the drafts of this account. He actively contributed to it until the day before his death and approved its content.

Biotic and Abiotic Factors Affecting Feeding Success of Early Juvenile Lake Whitefish in Lakes Michigan and Huron

AbstractFeeding success is associated with increased growth and survival during early life stages for fish, and understanding the factors that influence feeding success is a critical step toward predicting future recruitment to the fishery. The goal of our study was to test whether various biotic and abiotic factors, including prey abundance, fish abundance, and water temperature, affected the feeding success of early juvenile Lake Whitefish Coregonus clupeaformis from Lakes Michigan and Huron. Higher feeding success, which was determined using residuals from average weights of consumed prey for a given length fish, was associated with more rapid growth rates in length and depended on multiple factors. Although the relationships were not overly strong, one factor that was most consistently associated with increased feeding success was available zooplankton biomass in combination with some other factor(s) such as water temperature and/or total fish or Lake Whitefish density. There was no difference in diet composition or the available zooplankton community composition among four different levels of feeding success. Feeding success measures help integrate complex environmental factors that can vary with fish ontogeny. In turn, feeding success has the potential to be an important metric for Lake Whitefish fishery management strategies that critically need to account for the myriad factors influencing survival and growth of prerecruits to the fishery.

Metazoan parasite community of Hoplias malabaricus (Characiformes, Erythrinidae) in a stream of Caatinga domain, Brazil.

We purpose to describe and characterize the structure of the parasitic community of H. malabaricus in a stream from Caatinga domain, Ceará state, Brazil. A total of 42 specimens of H. malabaricus have been collected between December 2018 and August 2019, in which, 34 specimens were parasitized by at least one parasite. A total of 1,872 parasites were recovered, of which, 157 were Urocleidoides cuiabai (prevalence = 50%), 268 Urocleidodes brasiliensis (prevalence = 71.43%), 98 Dactylogyridae gen. sp. (prevalence = 14.29%), 401 Diplostomidae gen. sp. (prevalence = 4.76%), 183 Spiroxys sp. (prevalence = 42.86%) and 765 Pindapixara tarira (prevalence = 9.52%). The respective parasite species of H. malabaricus showed a pattern of overdispersion (or aggregation) typical of the parasitehost systems, corroborating with previous studies of parasitic communities of freshwater fish in Brazil. A positive and significant correlation between the host size and abundance of U. brasiliensis was verified. The ontogeny of fish can influence the parasitic load, some larger hosts tend to host larger quantities of parasites. The parasitic levels can vary with the host sex due to the differences in the ecological and physiological interactions between male and female. However, the host sex did not show influences in the prevalence and parasitic burden. All parasite taxa in this study have not yet been reported in the Carás stream, Caatinga domain. This finding extends the geographical distribution of this parasite species, furthermore, contributing to the knowledge of the biodiversity of fish parasites in the Neotropical region.

Why body size matters: how larger fish ontogeny shapes ecological network topology

Ontogenetic development can strongly shape species interactions. Yet, rarely is stage‐structure considered when analyzing species interaction networks, particularly networks that can account for more than feeding relationships. Here, we assess 1) if body size or trophic level regulate the importance of species' ontogeny on their interactions and 2) how including relevant stage‐structure affects the topology of species interaction networks. We use a count‐based inferential method to create networks from adult and juvenile fish count data and test stage‐structure importance by comparing a model that includes stage‐structure for all species against models that include stage‐structure only for larger fishes and only for piscivorous fishes during network construction. While the inferential method we use cannot differentiate between different types of interactions, it can account for different interaction types within a network as a pairwise interaction is inferred when one species influences the abundance of another. Next, we use graphlet‐based techniques to test if including stage‐structure alters overall network topology and a linear model to measure if adult‐juvenile size differences drive interaction differences at a species‐level. We find that the model that includes stage‐structure only for larger fishes outperforms other stage‐structured models including the model with only piscivore stage‐structure, and that larger differences in body size among juveniles and adults lead to greater interaction dissimilarities. Moreover, we find topological differences between inferred networks that only include adults and those that account for the stage‐structure of larger species. Overall, our study demonstrates how stage‐structured topological changes can be measured using inferred interaction networks and illustrates how larger species' juveniles fundamentally shape the structure of stream fish communities.

Seasonal calibration of the end-cretaceous Chicxulub impact event

The end-Cretaceous Chicxulub impact triggered Earth’s last mass-extinction, extinguishing ~ 75% of species diversity and facilitating a global ecological shift to mammal-dominated biomes. Temporal details of the impact event on a fine scale (hour-to-day), important to understanding the early trajectory of mass-extinction, have largely eluded previous studies. This study employs histological and histo-isotopic analyses of fossil fish that were coeval with a unique impact-triggered mass-death assemblage from the Cretaceous-Paleogene (KPg) boundary in North Dakota (USA). Patterns of growth history, including periodicity of ẟ18O and ẟ13C and growth band morphology, plus corroborating data from fish ontogeny and seasonal insect behavior, reveal that the impact occurred during boreal Spring/Summer, shortly after the spawning season for fish and most continental taxa. The severity and taxonomic symmetry of response to global natural hazards are influenced by the season during which they occur, suggesting that post-impact perturbations could have exerted a selective force that was exacerbated by seasonal timing. Data from this study can also provide vital hindsight into patterns of extant biotic response to global-scale hazards that are relevant to both current and future biomes.

High growth performance in the early ontogeny of an amphidromous fish, Ayu Plecoglossus altivelis altivelis, promoted survival during a disastrous river spate

AbstractAlthough river floods and spates have a major influence on fish populations, few studies have examined the selective pressure on individuals and traits that favour their survival. In this study, the factors that potentially affect the survival of an amphidromous fish species, ayu Plecoglossus altivelis altivelis (Temminck &amp; Schlegel), during a major spate were examined. Using otolith analyses, ayu in the Takahashi River, Okayama, Japan, were compared before (April; n = 50) and after (September; n = 32) a spate with regard to their respective hatch‐date distributions, standard body length and age at upstream migration, age at metamorphosis, and larval and juvenile growth rates. When comparing juvenile traits, surviving adult ayu grew faster than individuals collected before the spate. These findings suggest that juvenile growth rate is a key factor for enhancing subsequent survival and highlight the importance of conserving suitable nursery habitats to enhance fish survival during future floods.

What Indicators Could be Useful to Understand the Development of Digestive Tract, During the Early Ontogeny of Teleost Fish?

What Indicators Could be Useful to Understand the Development of Digestive Tract, During the Early Ontogeny of Teleost Fish?

Zooplanktivore fish body growth responses to browning‐induced light limitation vary over ontogeny, but not with fish density

AbstractOngoing climate change is leading to browning of many lakes and coastal areas, which can impair fish body growth and biomass production. However, whether and how effects of light limitation caused by browning on fish body growth vary over early ontogeny is unknown. In this study, we set up a mesocosm experiment to test whether roach (Rutilus rutilus) body growth responses to browning depend on body size, and if findings are robust over roach densities. We also studied a potential mechanism for size‐specific responses by conducting an aquaria experiment to test if size‐specific prey selectivity in roach changes with browning. We found that roach body growth responses to browning‐induced light limitation vary over ontogeny (independent of roach density), negatively affecting body growth of young‐of‐the‐year (YOY) but not of 1‐year‐old individuals. We also show that this difference in growth response is likely a consequence of browning‐induced alterations in zooplankton community composition and variation in prey selectivity between YOY and 1‐year‐old fish. This suggests that we should account for the diverse effects of browning over fish ontogeny, mediated via altered prey composition and ontogenetic changes in prey preference, when assessing overall impacts of browning on aquatic ecosystems.

Natural toxic impact and thyroid signalling interplay orchestrates riverine adaptive divergence of salmonid fish.

Adaptive radiation in fishes has been actively investigated over the last decades. Along with numerous well-studied cases of lacustrine radiation, some examples of riverine sympatric divergence have been recently discovered. In contrast to the lakes, the riverine conditions do not provide evident stability in the ecological gradients. Consequently, external factors triggering the radiation, as well as developmental mechanisms underpinning it, remain unclear. Herein, we present the comprehensive study of external and internal drivers of the riverine adaptive divergence of the salmonid fish Salvelinus malma. In the Kamchatka River, north-east Asia, this species splits in the reproductively isolated morphs that drastically differ in ecology and morphology: the benthivorous Dolly Varden (DV) and the piscivorous stone charr (SC). To understand why and how these morphs originated, we performed a series of field and experimental work, including common-garden rearing, comparative ontogenetic, physiological and endocrinological analyses, hormonal 'engineering' of phenotypes and acute toxicological tests. We revealed that the type of spawning ground acts as the decisive factor driving the radiation of S. malma. In contrast to DV spawning in the leaf krummholz zone, SC reproduces in the zone of coniferous forest, which litter has a toxic impact on developing fishes. SC enhances resistance to the toxicants via metabolism acceleration provided by the elevated thyroid hormone expenditure. These physiological changes lead to the multiple heterochronies resulting in a specific morphology and ecology of SC. Salvelinus malma represents a notable example of how the thyroid axis contributes to the generation of diverse phenotypic outcomes underlying the riverine sympatric divergence. Our findings, along with the paleoecology data concerning spruce forest distribution during the Pleistocene, provide an opportunity to reconstruct a scenario of S. malma divergence. Taken together, obtained results with the data of the role of thyroid hormones in the ontogeny and diversification of fishes contribute a resource to consider the thyroid axis as a prime director orchestrating the phenotypic plasticity promoting evolutionary diversification under the changing environmental conditions.