Respiration rates of herring larvae at different salinities and effects of previous environmental history

Metabolic rates of early life history stages of marine fishes show considerable inter-individual differences and are highly influenced by extrinsic factors like temperature or food availability. Measuring oxygen uptake rates is a proxy for estimating metabolic rates. Still, the relationship between respiration rates and ambient or previous salinity conditions as well as parental and developmental acclimation to changes in salinity is largely unexplored. In the present study, we conducted experiments to investigate salinity effects on the routine metabolic rates (RMR) of euryhaline Atlantic herring (Clupea harengus) larvae at three levels of salinity: low (6 psu), intermediate (16 psu) and high (35 psu) reflecting ecological relevant conditions for its populations in the Atlantic and Baltic Sea. The larvae originated from different genetic backgrounds and salinity adaptations to account for cross-generation effects on metabolic rates. Closed respirometry carried out over 24 h on individual fish larvae generally confirmed near isometric respiration rates at all salinity regimes, with rates being 15.4% higher at 6 psu and 7.5% higher at 35 psu compared to 16 psu conditions. However, transgenerational acclimation to different salinity regimes of parents had no effect on the salinity specific metabolic rates of their offspring. Our study demonstrates the ability of herring to cope with a wide range of salinity conditions, irrespective of parental environmental history and genetic origin. This phenotypic plasticity is considered to be one of the main contributing factors to the success of herring as a widely distributed fish species in the North Atlantic and adjacent waters.acceptedVersio

Análisis del ciclo celular en células del cerebro como índice de crecimiento en larvas de bacalao a diferente condiciones de alimento y temperatura

The percentage of cells dividing in a specific tissue of individual larvae can be estimated by analyzing DNA per cell by flow cytometry. An experimental test was carried out with cod (Gadus morhua) larvae, with brain as the target tissue, to validate this technique as an appropriate growth index for larval fish. Standard length (SL), myotome height, and %S-phase (% of cells in the S-phase of the cell-division cycle) variability were analyzed, with temperature (6 and 10°C), food level (high- and no-food) and larval developmental stage (first feeding, pre-metamorphosis and post-metamorphosis) as independent factors. Cod larvae grew faster (in SL) and presented a higher %S-phase under high-food conditions. Larval SL increased with temperature in rearing and experimental tanks. However, there was a significant interaction between temperature and food in the %S-phase. There were no significant differences in the %S-phase between 6 and 10°C at high-food levels. We suggest that this result is a consequence of temperature-dependency of the duration of the cell cycle. In the absence of food, larvae at 10ºC had a lower %S-phase than larvae at 6°C, which may be related to increased metabolic costs with increasing temperature. Considering the effect of temperature, the mean % S-phase explained 74% of the variability in the estimated standard growth rate.El porcentaje de células en divisón en un determinado tejido de una larva de pez se puede estimar analizando la cantidad de ADN por célula mediante citometría de flujo. Se realizó un experimento con larvas de bacalao (Gadus morhua), analizando células de cerebro, para validar esta técnica como índice de crecimiento en larvas de peces. Se analizó la variabilidad de la longitud estándar (SL), la altura del tronco medida en el ano, y el %S (% de células en fase S del ciclo celular), con temperatura (6 y 10ºC), nivel de alimento (alto y sin alimento) y estado de desarrollo larvario (comienzo de la alimentación, pre-metamorfosis y post-metamorfosis) como factores independientes. Las larvas de bacalao crecieron más rápido (en SL) y presentaron mayor %S bajo condiciones de nivel alto de alimento. La SL larvaria incrementó con la temperatura. Sin embargo, se observó una interacción significativa entre temperatura y alimento sobre %S. No hubo diferencias significativas en %S entre 6 y 10ºC en condiciones de nivel alto de alimento. Sugerimos que este resultado es consecuencia de una termo-dependencia en la duración del ciclo celular. En ausencia de alimento, las larvas a 10ºC presentaron %S más bajos que las larvas a 6ºC, lo que puede estar relacionado con un incremento de los costes metabólicos a mayor temperatura. Considerando el efecto de la temperatura, el %S medio explicó el 74% de la variabilidad de la tasa de crecimiento específica estimada.

Development stage distribution as a proxy for feeding success and growth for first feeding Norwegian spring spawning herring larvae

The estimation of growth rates in young herring larvae (Clupea harengus) in the field can be difficult because the primary increments in the otoliths may not be discernible or formed at a daily level. Likewise, the estimation of mortality rates of fish larvae in the field is very difficult to achieve, especially in a rigorous quantitative manner. In this study, the authors suggest the use of a stage‐based proxy of feeding success, growth and potential survival or mortality risk of field‐caught larvae. The stage‐based proxy is derived based on observations from previous laboratory studies where larvae successfully completing start‐feeding on external food sources will advance through the early development stages, whereas those that do not (unsuccessful larvae) remain and accumulate in the development stage preceding first feeding. The relative occurrence of larvae in the early development stages is therefore expected to reflect feeding conditions of the larvae, with higher ratios of unsuccessful larvae indicative of poor feeding success and higher mortality risk. Using field data on Norwegian spring spawning herring, the authors document that the relative occurrence of larvae in the late non‐feeding stage is significantly higher at lower average zooplankton concentrations, in line with the predictions of the authors that this novel approach of using a stage‐based proxy could be a useful indication of feeding success, growth and mortality in the field. Further, there was a significant interaction effect with ambient temperature, with the ratio being higher at low zooplankton concentrations at higher temperatures. This study also suggests that these findings are not population specific as the same accumulation of non‐feeding larvae in the late non‐feeding stage was observed in laboratory‐reared larvae of both autumn and spring spawning herring populations.publishedVersio

Effects of temperature on tissue-diet isotopic spacing of nitrogen and carbon in otolith organic matter

Reconstruction of the trophic position of a fish can be performed by analysing stable nitrogen and carbon isotopes in otolith protein. However, ambient temperature may affect the tissue–diet isotopic spacing of stable isotopes from diet to predator tissue and bias estimates of trophic position. To test this, otolith protein, heart and muscle tissue from a rearing experiment with juvenile cod held at different temperatures (4, 7, 10 and 14°C) were analysed. There was no significant effect of temperature on otolith δ15N, whereas muscle and heart exhibited a slight decrease in δ15N values with increasing temperature corresponding to maximum of 0.6‰ over the 10°C range. By contrast, the otolith protein δ13C values at 4 and 7°C were significantly higher than for 10 and 14°C, suggesting an approximate 1‰ increased tissue–diet enrichment at the lower temperatures. Temperature had no significant effect on muscle and heart δ13C values. Considering the annual mean variation in ocean temperatures, our results indicate that the trophic signals recorded in the otoliths will reflect changes in diet isotope values with little bias from the ambient temperature experienced by the fish.publishedVersio

Comparison of Otolith Microstructure of Herring Larvae and Sibling Adults Reared Under Identical Early Life Conditions

Atlantic herring (Clupea harengus) is a euryhaline species, occupying fully marine habitats (35 psu) in the North Atlantic, as well as brackish waters (<20 psu) such as in the adjacent Baltic Sea. We co-reared Atlantic purebreds and Atlantic/Baltic F1 hybrids in two salinity regimes (16 and 35 psu) in a common garden experiment for 3 years until their first maturity. This setup enabled for the first time a direct comparison between adults and their larval siblings at respective salinity regimes in terms of larval growth indicated by otolith microstructure. We validated that otolith microstructure analysis of adult otoliths is reflecting the experienced otolith growth during the larval stage. No major selection in terms of otolith growth had taken place during the juvenile stage, except for one experimental group. Surviving adult Atlantic purebreds reared at 16 psu had higher otolith growth compared to their larval stages. The validation that otolith microstructure analyses of adult herring can reliably be extracted and used to examine larval growth even after several years adds strong support for further use of such analyses. Among the parental generation, Baltic herring had a faster initial otolith growth than Atlantic herring. The growth of their laboratory-reared F1 progeny was intermediate compared to their parents. In general, larval growth of both Atlantic purebreds and Atlantic/Baltic hybrids reared in 16 psu was significantly larger than for those herring reared at 35 psu. There was no significant difference in larval growth between Atlantic purebreds and Atlantic/Baltic hybrids reared at 35 psu, but hybrid larval growth was significantly higher compared to larval growth of Atlantic purebreds at 16 psu. This was not reflected at the adult stage where purebreds were ultimately larger than hybrids (Berg et al., 2018). This indicates the influence and importance of environmental and genetic factors throughout the life of Atlantic herring, along with genetic contributions to phenotypic variability.publishedVersio

¿Qué pueden decirnos las distribuciones de talla dentro de cohortes sobre los procesos ecológicos en larvas de peces?

Marine fish larvae are subject to variable environments, which is probably reflected in their growth and survival rates. Mortality rates are generally high and size-dependent. At the species level, these mortality rates are usually accompanied by correspondingly high growth rates. Here we provide examples from experimental studies with Atlantic cod (Gadus morhua) and Atlantic herring (Clupea harengus) larvae, in which multiple cohorts were followed over time. Body size, prey concentrations, and temperature are shown to influence growth rates. We present a method based on cumulative size distributions (CSDs) for visualizing variability of sizes within cohorts over time. Analysis of CSDs revealed size-selective mortality and variations among populations in size- and temperature-dependent growth throughout ontogeny. We found that cod larvae consistently exhibit higher growth rates than herring larvae. While cod larvae may have an advantage over herring larvae when food availability is high, herring were more able to survive at low food concentrations than cod. Cod and herring seem to represent two growth strategies: cod larvae are relatively small at hatching and a high growth rate appears to be a prerequisite for success, whereas herring larvae are initially large, but grow more slowly.Las larvas de peces marinos están sujetas a ambientes variables que probablemente se reflejan en sus tasas de crecimiento y supervivencia. las tasas de mortalidad son generalmente altas y dependientes de la talla. A nivel de especies, estas tasas de mortalidad están usualmente acompañadas de tasas de crecimiento altas. en este trabajo mostramos ejemplos a partir de estudios experimentales con larvas de bacalao atlántico (Gadus morhua) y arenque atlántico (Clupea harengus), en los que se siguieron cohortes múltiples a lo largo del tiempo. Se muestra como la talla del cuerpo, la concentración de presas y la temperatura influyen en la tasa de crecimiento. Presentamos un método basado en distribuciones de frecuencias de talla acumuladas (DTAs) para visualizar la variabilidad en tallas dentro de las cohortes a lo largo del tiempo. el análisis de DTAs reveló mortalidad selectiva por talla, y variaciones entre poblaciones en el crecimiento dependiente de la talla y la temperatura a través de la ontogenia. encontramos que las larvas de bacalao mostraron consistentemente mayores tasas de crecimiento que las de arenque. Mientras las larvas de bacalao pueden tener una ventaja sobre las de arenque cuando la disponibilidad de presas es alta, las de arenque son más capaces de sobrevivir a bajas concentraciones de comida. Bacalao y arenque parecen representar dos estrategias de crecimiento; las larvas de bacalao son relativamente pequeñas a la eclosión y una alta tasa de crecimiento parece un prerrequisito para el éxito, mientras que las de arenque son inicialmente más largas, pero crecen más lentamente

Genetic factors have a major effect on growth, number of vertebrae and otolith shape in Atlantic herring (Clupea harengus)

Atlantic herring, Clupea harengus, have complex population structures. Mixing of populations is known, but the extent of connectivity is still unclear. Phenotypic plasticity results in divergent phenotypes in response to environmental factors. A marked salinity gradient occurs from Atlantic Ocean (salinity 35) into the Baltic Sea (salinity range 2–12). Herring from both habitats display phenotypic and genetic variability. To explore how genetic factors and salinity influence phenotypic traits like growth, number of vertebrae and otolith shape an experimental population consisting of Atlantic purebreds and Atlantic/Baltic F1 hybrids were incubated and co-reared at two different salinities, 16 and 35, for three years. The F1-generation was repeatedly sampled to evaluate temporal variation. A von Bertalanffy growth model indicated that reared Atlantic purebreds had a higher maximum length (26.2 cm) than Atlantic/Baltic hybrids (24.8 cm) at salinity 35, but not at salinity 16 (25.0 and 24.8 cm, respectively). In contrast, Atlantic/Baltic hybrids achieved larger size-at-age than the wild caught Baltic parental group. Mean vertebral counts and otolith aspect ratios were higher for reared Atlantic purebreds than Atlantic/Baltic hybrids, consistent with the differences between parental groups. There were no significant differences in vertebral counts and otolith aspect ratios between herring with the same genotype but raised in different salinities. A Canonical Analysis of Principal Coordinates was applied to analyze the variation in wavelet coefficients that described otolith shape. The first discriminating axis identified the differences between Atlantic purebreds and Atlantic/Baltic hybrids, while the second axis represented salinity differences. Assigning otoliths based on genetic groups (Atlantic purebreds vs. Atlantic/Baltic hybrids) yielded higher classification success (~90%) than based on salinities (16 vs. 35; ~60%). Our results demonstrate that otolith shape and vertebral counts have a significant genetic component and are therefore useful for studies on population dynamics and connectivity.publishedVersio

Early life growth is affecting timing of spawning in the semelparous Barents Sea capelin (Mallotus villosus)

Capelin (Mallotus villosus) is a forage fish and a key species in the Barents Sea (BS). The BS capelin are semelparous and hence only spawn once along the north coasts of Norway and Russia before they die. The age at spawning ranges from 2 to 5 years and the spawning season peaks in March/April but starts in February and lasts until June, and the causes of the variability in timing of spawning are not well understood. Here, we aimed to find out whether early growth is associated with the timing of spawning in BS capelin, both on the individual and population level, and if there is an association between early life growth and the spatial distribution at the nursery areas and feeding grounds. For the analysis, we used an extensive dataset comprising >150 000 otolith growth zone measurements carried out during surveys from 1976 to 2019 both from the spawning and feeding areas. The data from the feeding area showed that capelin with good first-year growth were found in the productive north-west part of the Barents Sea at both age 1 and 2, while capelin with relatively poor first-year growth were typically found in the south-east Barents Sea. The data from the spawning area showed on the individual level that capelin with good first-year growth tend to spawn both at a younger age and earlier in the season. The capelin spawning late in the season were also generally smaller than early spawners. On the population level, a contradictory pattern was observed where the proportion of maturing capelin at age 2 and 3 was negatively correlated with first-year growth indicating that the great variability in year-class strength masks the general effect found at the level of individual fish. Furthermore, first-year growth was positively associated with the abundance of 1-year-old capelin indicating that rapid growth early in life enhances recruitment. On the other hand, first-year growth was strongly negatively correlated with third-year growth suggesting an increased effect of density-dependent growth with age and/or compensatory growth, or reduced growth linked to earlier maturation. In sum, our results show that the first-year growth affects growth, maturation processes, and timing of spawning later in life, thus potentially strongly influencing capelin population dynamics.publishedVersio

Egg buoyancy variability in local populations of Atlantic cod (Gadus morhua)

http://dx.doi.org/10.1007/s00227-012-1984-8Previous studies have found strong evidences for Atlantic cod (Gadus morhua) egg retention in fjords, which are caused by the combination of vertical salinity structure, estuarine circulation, and egg specific gravity, supporting small-scaled geographical differentiations of local populations. Here, we assess the variability in egg specific gravity for selected local populations of this species, that is, two fjord-spawning populations and one coastal-spawning population from Northern Norway (66–71°N/10–25°E). Eggs were naturally spawned by raised broodstocks (March to April 2009), and egg specific gravity was measured by a density-gradient column. The phenotype of egg specific gravity was similar among the three local populations. However, the associated variability was greater at the individual level than at the population level. The noted gradual decrease in specific gravity from gastrulation to hatching with an increase just before hatching could be a generic pattern in pelagic marine fish eggs. This study provides needed input to adequately understand and model fish egg dispersal

Tracking oocyte development and the timing of skipped spawning for north-east Arctic haddock (Melanogrammus aeglefinus)

The present study tracked oocyte development over 9 months and noted incidences of ‘skipping’, i.e., adults terminating their upcoming reproductive cycle, in field-caught north-east Arctic (NEA) haddock (Melanogrammus aeglefinus), currently the largest stock of this species. Applications of advanced image and histological techniques revealed the presence of cortical alveoli oocytes (CAO), which prevailed as the most advanced oocyte phase for 4–5 months. This new finding of an extended and early appearance of CAOs in this gadoid was supported by that vitellogenesis first started to appear 3 months later. The subsequent oocyte growth trajectories indicated that larger individuals [total length (TL) = 70 cm] typically spawn in the order of 3 weeks earlier than the smaller ones (TL = 40 cm). The spawning season appeared stretched over about 3 months. The majority of skipping females arrested oocyte growth at the CAO phase followed by atretic reabsorption. Compared to those individuals maturing for the spawning season, ‘skippers’ generally exhibited lower body condition, characterized also by relatively lower liver sizes at the time of the main spawning season. This study demonstrated well-developed skipping dynamics, but also that the CAO period, i.e., when skipping takes place, may be exceedingly long in this commercially valuable gadoid and that its reproductive cycle in many ways deviates from that of the data-rich, sympatric NEA cod (Gadus morhua).publishedVersio