Estimating the timing of growth rings in Atlantic cod otoliths using stable oxygen isotopes

A technique involving micro‐scale sampling of otolith carbonate and analyses of stable oxygen isotope composition was used to relate the zone appearance of the otolith to the seasonal temperature cycle. Otolith opacity could then be related to the timing of zone formation. Otoliths from two groups of Atlantic cod Gadus morhua held under known temperature conditions over a period of 4 and 6 years were examined. The otolith translucency followed the same pattern as the estimated temperature (from otolith δ¹⁸O values) in the yearly increments three and four, meaning that the translucent zones were deposited at the seasonal highest temperature in late summer and early autumn. The relative light intensities of otolith yearly increments five and six of older fish (deposited in the same years), however, were not significantly correlated to the estimated temperatures since increased otolith translucency also occurred at low temperatures. This might have been caused by stress in connection with gonad development or starvation during the spawning period. The results showed that this method of coupling otolith opacity and stable oxygen isotope composition can be used to estimate the timing of zone formations in otoliths.     

Phenology and North Sea cod Gadus morhua L.: has climate change affected otolith annulus formation and growth?

Timing and rate of seasonal zone formation in southern North Sea cod Gadus morhua otoliths was studied. Samples were taken from two time periods, representing low and high temperature regimes. Opaque zones were laid down between January and June, in contrast with the pattern described in other published studies. Translucent zone formation started earlier in the warmer period, corresponding to peak annual sea surface temperatures, and a period of slow body growth and low metabolic activity. Translucent zone formation, however, continued once temperatures decreased and growth rate increased. It is hypothesized that translucent zone formation is triggered at a threshold of metabolic stress, and that the combined energetic requirements of reproduction, growth and migration may maintain translucent zone formation even if feeding conditions improve. Higher temperatures had a significant negative effect on the rate of translucent zone deposition, but caused a slight increase in opaque zone formation rate. The findings of this study indicate that historical otolith collections could provide key inputs into future phenological studies to improve the understanding of climate change impacts and the dynamics of otolith structure.     

Temperature effects on otolith pattern formation in Atlantic cod Gadus morhua

The effect of food intake and temperature on otolith macrostructure and microstructure was examined experimentally in Atlantic cod Gadus morhua. Daily increment formation was validated and otolith accretion rate and optical density quantified using image analysis. Two‐week periods of starvation had no discernable effect on otolith increment width or optical density, despite having negative effects on somatic growth. In contrast, temperature had a strong positive effect on otolith accretion rate and clear effects on optical density with the otolith becoming more translucent at higher temperatures. Somatic growth, otolith accretion and otolith optical density each had a significantly different response curve to temperature. No relationship was detected between individual somatic growth rates and the accretion rate or optical properties of the otolith. The experimental manipulation of temperature‐induced otolith patterns similar to the ‘false ring’ secondary structures sometimes observed in the otoliths of wild fish. The results suggest that otolith pattern arises from a combination of temperature and seasonal effects, but not directly from individual variation in somatic growth.     

Otolith oxygen and carbon stable isotopes in wild and laboratory-reared plaice (Pleuronectes platessa)

The relationship between water temperature, growth rate, and otolith isotopic ratios was measured for juvenile plaice (Pleuronectes platessa) reared at two temperatures (11 and 17°C) and two feeding regimes (1 and 3 prey items·ml^?1). The otolith isotope ratios in individual fish ranged from ?2 to ?4 for carbon isotope ratios (δ¹³C) and from 0.2 to 1.9 for oxygen isotope ratios (δ¹⁸O). The otolith oxygen isotope ratios were significantly affected by water temperature, but not by feeding level, and there were no significant synergistic effects. The fractionation of oxygen isotopes during otolith growth was independent of individual growth rate. Carbon isotope ratios were not significantly affected by food ration or water temperature, but were related to fish growth rate. The carbon isotope ratios were negatively correlated with fish length in the colder water treatments, and tended to increase with fish length in the warm water treatments. The laboratory-determined relationship between otolith oxygen isotope ratio and water temperature was applied to individuals of five species (plaice, cod, whiting, haddock, gurnard) collected in a single trawl sample. The otolith derived temperatures often overestimated measured water temperatures. The difference between real and estimated water temperatures varied between species, and the closest fit was for field-caught plaice.     

Effect of somatic and otolith growth rate on stable isotopic composition of early juvenile cod (Gadus morhua L) otoliths

The relative amounts of the stable isotopes of carbon and oxygen in fish otoliths can be used to reveal the environmental history experienced by the fish. This requires that the relative amounts of the isotopes are deposited in equilibrium with the surrounding environment, or that the offset from this equilibrium is known and can be quantified. It is known that carbon isotopes in biogenic carbonates are a mixture of carbon from the seawater and metabolically derived carbon, but the effect of the somatic growth rate of the fish is still unclear. The possible effect of otolith growth rate and fractionation of both carbon and oxygen isotopes are also not established. We carried out a controlled laboratory experiment where we reared cod (Gadus morhua L.) larvae and early juveniles at two temperatures (6 and 10 °C) and generated different growth rates within each temperature by manipulation of prey levels. The otoliths of the resulting fish were analysed for carbon and oxygen isotopes. We found no effect of otolith precipitation rate on fractionation of either carbon or oxygen isotopes. However, there was a depletion of ¹³C in the otoliths of fish with elevated metabolism. The proportion of metabolically derived carbon in the otoliths was estimated to be 28-32%. Our results suggest that measurements of oxygen isotopes in otoliths can be a reliable tool to estimate ambient temperature since the oxygen isotopes seem to be deposited in the otoliths independently of kinetic and metabolic effects. Fractionation of carbon isotopes in otoliths on the other hand can give valuable insight into metabolism and feeding pattern of fish.     

Daily growth increments in the otoliths of Atlantic salmon parr, Salmo salar L., and the influence of environmental factors on their periodicity

Daily increments were demonstrated in the sagitta otoliths of fast- and slow- growing Atlantic salmon parr, Salmo salar L., when held under natural photoperiod and temperature. Otolith increments continued to be deposited at a daily rate when fish were held under constant light and/or temperature and on single or multiple feeding regimes. However abnormally short photoperiods of 6L: 6D induced two increments per day. The results suggest that an endogenous rhythm, synchronized lo light/dark transitions within a 24 h period, controls otolith increment deposition.     

Otolith accretion rates: Does size really matter?

This study examined the relationship between otolith size and growth in juvenile cod (Gadus morhua L.). Two groups of juvenile cod were reared under different food ration and temperature regimes to obtain fish of similar somatic size but with different sized otoliths. The two groups were subjected to alternating temperature regimes and intermediate ration levels. Large otoliths grew significantly faster than the small ones and variation between individuals was extensive. The ratio of otolith growth during cold and warm temperature exposure did not differ between groups, and the observed growth pattern is therefore not attributable to differential growth within individual temperature periods. The ratio decreased with otolith size, presumably as a result of ontogenetic decrease in otolith protein composition. These results suggest that processes coupled to the metabolic rate of the endolymphatic epithelium are the key driver behind otolith growth.     

Tracing the life history of red gurnard (Aspitrigla cuculus) using validated otolith annual rings

Back calculation, marginal increment analysis and modal progression analysis were used to trace growth processes of the red gurnard, Aspitrigla cuculus L., in the Mediterranean Sea. Three false rings appeared regularly on otoliths and were hypothesized to refer to the ontogeny on the basis of the study of the recruitment and reproduction processes of the species. The first two rings were laid down during the first pelagic period and the transformation to the bottom mode of life, respectively. The third ring corresponded to the first spawning at the end of the second year of life. The marginal increment analysis demonstrated that one opaque and one translucent zone is formed each year, the translucent ring corresponding to the period of slow growth in the winter. Temperature and salinity of Mediterranean waters below the thermocline where red gurnard live do not undergo seasonal variations. Therefore, traditional interpretation of the discontinuity patterns on otoliths related to the decrease of water temperature should be rejected for Mediterranean fish distributed on the deep shelf and slope. Discontinuities in otolith structure may be related to seasonal variation in feeding intensity as a consequence of decreases in the benthic mysids biomass and time available to find food due to reduced daylight. Future research should focus on the trophic ecology of the demersal fishes and the seasonal fluctuations of the prey resources during the year in order to assess the role of the food supply with regard to otolith growth patterns in the Mediterranean Sea.     

A century of fish growth in relation to climate change,population dynamics and exploitation

Marine ecosystems, particularly in high‐latitude regions such as the Arctic, have been significantly affected by human activities and contributions to climate change. Evaluating how fish populations responded to past changes in their environment is helpful for evaluating their future patterns, but is often hindered by the lack of long‐term biological data available. Using otolith increments of Northeast Arctic cod (Gadus morhua) as a proxy for individual growth, we developed a century‐scale biochronology (1924–2014) based on the measurements of 3,894 fish, which revealed significant variations in cod growth over the last 91 years. We combined mixed‐effect modeling and path analysis to relate these growth variations to selected climate, population and fishing‐related factors. Cod growth was negatively related to cod population size and positively related to capelin population size, one of the most important prey items. This suggests that density‐dependent effects are the main source of growth variability due to competition for resources and cannibalism. Growth was also positively correlated with warming sea temperatures but negatively correlated with the Atlantic Multidecadal Oscillation, suggesting contrasting effects of climate warming at different spatial scales. Fishing pressure had a significant but weak negative direct impact on growth. Additionally, path analysis revealed that the selected growth factors were interrelated. Capelin biomass was positively related to sea temperature and negatively influenced by herring biomass, while cod biomass was mainly driven by fishing mortality. Together, these results give a better understanding of how multiple interacting factors have shaped cod growth throughout a century, both directly and indirectly.     

Effects of temperature,starvation and photoperiod on otolith increments in larval Chinese sucker, <Emphasis Type="Italic">Myxocyprinus asiaticus</Emphasis>

Effects of water temperature, starvation and photoperiod on otolith increment formation in larval Chinese sucker, Myxocyprinus asiaticus, were examined in this study. The results demonstrated that otolith increments of larvae reared under diel temperature fluctuations were very clear and appeared with a high contrast, while those of larvae raised under constant water temperatures were vague or hard to identify. The increment deposition rates were less than 1.0/day in later stage of starvation period. Also, increment deposition was affected by cyclic regimes of water temperature fluctuations, the number of increments corresponded to the cycle times rather than the exact days larvae experienced. However, varying of feeding frequency and photoperiod did not result in any alterations of daily increment formation. Increment width increased obviously with higher rearing temperatures till several days after yolk absorption. However, the width presented an ontogenetic decline during period of endogenous nutrition and the first several days of exogenous nutrition stage. Starvation decoupled the relationship between somatic growth and otolith growth; otolith kept growing, and increment width of starved larvae was similar to those in fed individuals before 9–20 days old; the divergence of increment width from the fed larvae occurred in later stage of starvation period. It can be concluded that temperature regimes and food levels are the major factors affecting increment formation in terms of clarity, deposition rate and width, while photoperiod and feeding frequency have less influence on it.     

The influence of feeding behaviour on growth of Atlantic cod (Gadus morhua,Linnaeus, 1758) in the North Sea

The objective of this study was to resolve key mechanisms driving individual growth patterns of Atlantic cod (Gadus morhua). Growth dynamics were analysed by linking growth patterns with stomach content composition and environmental temperature. Samples were collected in August/September of the years 2009, 2010 and 2011 in the north‐eastern part of the central North Sea. Prey selection was assessed by identification of individual prey items in the stomach content to species. Ten feeding groups were identified consisting of individuals with one prey type dominating their stomach contents (≥75% by mass), of which six were used for growth analyses: “Sandeel”, “Clupeids”, “Norway pout”, “Flatfishes”, “Crustaceans” and “Brittle stars”. For each group, growth patterns were estimated based on measures of otolith growth increments. The stomach contents showed that cod as a species are opportunistic in their prey selection, but at the same time indicated that the total, broad feeding niche width of the population is dominated by individual diet specialization and that many individuals temporally show a preference for a particular prey type. The contribution of invertebrates and particularly crustaceans decreased with increasing cod size, whereas that of fish and predominantly herring increased. Prey type had a significant effect on growth, while temperature had no effect. Slowest growth was observed in the cod group preying on sandeel, while cod preying on Norway pout showed the fastest growth. No significant difference was observed between groups preying on brittle stars, crustaceans, flatfishes and herring. Growth in the year before capture did however not differ between any of these groups. Across sampling years, growth chronology patterns were similar but not significantly influenced by temperature.     

Otolith age determination for adult tilapia, Oreochromis niloticus L. from Lake Awassa (Ethiopian Rift Valley) by interpreting biannuli and differentiating biannual recruitment

Age of mature Oreochromis niloticus in Lake Awassa, Ethiopia, was estimated by analysing optical macrozones (translucent and opaque) in sagittal otoliths from fish sampled over a 12-month period. Seasonal record on the type of macrozone at the edge of otoliths suggested that two translucent macrozones associated with biannuli were formed each year; one during January and February and another during June and July. Formation of translucent macrozones coincided with minimum water temperature, spawning associated loss in condition and presumably with reduction in the quantity and quality of the food consumed by the fish. Relative marginal increment analysis showed that biannulus formation may be completed in March and in August each year. A concurrent study has confirmed a biannual recruitment in O. niloticus in Lake Awassa, from which mid-February and mid-August were taken as median hatch-dates. A procedure to assign otolith age is described which considers median hatch-dates and uses the number of biannuli in otoliths without discriminating between fish from the two recruitment cohorts. We also show a procedure to discriminate between the two cohorts by using the number of biannuli, conditions on the edge of the otolith and time of capture to assign age for the two recruitment cohorts separately.     

Variations in feed intake and growth of Baltic salmon and brown trout exposed to continuous light at constant low temperatures

Interindividual variations in feed intake and growth were studied in Baltic salmon Salmo salar and brown trout S. trutta , held under constant low temperatures of 2, 4 or 6° C and continuous light for 2 months. Rates of feed intake and growth were dependent upon rearing temperature, being lowest at 2° C and highest at 6° C. Further, feed intake and growth were initially low, but increased during the course of the experiment in both species and at all temperatures. These results suggest that acclimatization to the rearing conditions may have required several weeks. The increase in group mean feed intake with time was the result of both an increase in the proportions of fish that fed and an increase in feed intake amongst feeding fish. At the same time as feeding and growth rates increased, interindividual variations in feed intake and growth tended to decrease, suggesting that individual fish were acclimatizing to the new rearing conditions at different rates. Thus, the differences in group mean feed intake and growth rates observed at a given temperature reflected interindividual variations among fish making up the groups. This suggests that group rates of feed intake and growth are not only temperature- dependent, but that they are also highly influenced by variability among fish making up the group.     

Morphometry and composition of red drum otoliths: Changes associated with temperature,somatic growth rate,and age

• 1.1. Size and composition of sagittal otoliths from red drum, Sciaenops ocellatus (Sciaenidae), reared at various constant temperatures were compared with otoliths from wild-caught fish.
• 2.2. Uncoupling of otolith growth and somatic growth in laboratory-reared fish was evident in otolith length, area, volume, weight, density, and organic fraction.
• 3.3. Fish grown at low temperatures had significantly smaller and less dense otoliths having a greater organic content than fish of the same size grown at higher temperatures.
• 4.4. Changes in inorganic elements were poorly related to temperature in laboratory-reared fish.
• 5.5. The effect of temperature on otolith elemental composition was small relative to the effects of age and its associated physiological changes.

     

Influence of Lernaeocera branchialis (Crustacea: Copepoda) on growth rate of Atlantic cod, Gadus morhua

Influence of Lernaeocera branchialis, a hematophagous copepod, on the growth rate of Atlantic cod, Gadus morhua, was investigated in fish of various sizes. Initially, it appeared that growth, over a 16-mo period, was reduced when single or multiple infections were present. We then examined growth rate by comparing food consumption, weight gain, food conversion efficiency, and condition (k) factor over a 2-mo period and subsequently over a 4 wk in control and experimentally infected fish. Total body weight and length of each fish, controls and infected were determined before and after feeding known weights of food. Adults infected with young parasites consumed more food and gained more weight than controls, especially in the first month, but food conversion efficiency and k-factor were greater than those of controls after 2 mo, but food efficiency was still lower than in controls. In 2 groups of young infected fish, all values were consistently lower than those of uninfected fish of comparable size during the 2-mo period. Three additional trials on immature cod confirmed that infected fish consumed less food and exhibited less growth than infected controls. Our results suggest that only adult cod infected with immature parasites compensate for the infections by increasing food consumption, thus resulting in a transitory weight gain. Additionally, parasites that have completed their reproductive activities still produce subtle effects in the form of low food conversion efficiency in their hosts.     

Does water calcium content influence the distinctness of daily growth increments in the otoliths of larval whitefish (Coregonus lavaretus L.)?

In larval and juvenile whitefish ( Coregonus lavaretus L.) from Lake Constance, Germany, the otolith increments are deposited daily, whereas daily deposition could not be confirmed in larval whitefish from Lake Pyhäselkä, Finland. The calcium concentration in Lake Constance is high (around 1.3 m m ), while calcium deficiency is typical for Finnish lakes (around 0.15 m m ). Therefore, the hypothesis that the distinctness of daily otolith increments in whitefish is related to water calcium content was tested by rearing three groups of Lake Constance whitefish in water of 0.2, 1.3 and 4.7 m m Ca. The eggs were incubated in lake water (1.3 m m Ca), and the larvae were acclimated to the experimental calcium concentrations on the day of hatching. After 39 days of ad libitum- feeding with Artemia nauplii, the three groups did not differ significantly in total length, wet and dry weight, and otolith length and width. The daily increments were easily recognizable, and contrast between dark (D)- and light (L)-zones was the same in the fish of all test groups. For the experimental set-up of this study, and particularly the range of calcium concentrations tested, the hypothesis that water calcium content influences the distinctness of daily otolith increments was rejected.     

Otolith shape in juvenile cod (Gadus morhua): Ontogenetic and environmental effects

The objectives of this study were to describe the otolith shape development of cod from post-metamorphosis larvae to juveniles and to examine whether shape development is an ontogenetically determined process. Fish were reared under three different temperature regimes and two feeding levels. I examined shape by the length~width relationship of the otolith as well as the number and size of the lobes formed. Otolith size and crenulation is exclusively linked to fish size, indicating an ontogenetically determined development. Otolith shape is closely associated with the spatial development of the lobes. This process is linked with food consumption. Higher food consumption leads to a higher number of larger lobes, resulting in a more rectangular otolith. In conclusion: Otolith shape development consists of an ontogenetic component in the form of increasing size and crenulation and an environmental component impacting on the size and number of the lobes formed.     

Enhanced protein synthetic capacity in Atlantic cod (Gadus morhua) is associated with temperature-induced compensatory growth

Atlantic cod (Gadus morhua) were held either at seasonal ambient temperatures (-0.3 to 11 degrees C) or at a relatively constant control temperature (8-11 degrees C) to investigate aspects of protein synthesis during a period of compensatory growth. Protein synthesis rate, total RNA, and RNA-specific protein synthesis rate were determined in white muscle and liver when ambient temperatures were -0.3, 4.5, and 11 degrees C in February, June, and July, respectively. To allow for comparisons between treatment temperatures, fish were also acutely transferred to a comparable assay temperature in February and June. Over the transition from 4.5 to 11 degrees C (June to July), the ambient-held cod had a significant increase in size and a substantially higher growth rate relative to control-held fish over the same period, consistent with cold-induced compensatory growth. During the onset of this enhanced growth, in June when ambient temperature was approximately 4.5 degrees C, ambient-held fish elevated their capacity for protein synthesis in the white muscle and liver via elevation of the RNA content. When ambient temperature reached the same point as for the control fish (11 degrees C), the rate of white muscle protein synthesis remained higher in the ambient-held vs. that in the control-held fish, a process facilitated by elevated RNA content and greater RNA-specific rate of protein synthesis. In the liver, all measured characteristics of protein synthesis were the same for ambient and control fish in July. The latter suggests that compensatory growth may be in part explained by improved efficiency of protein synthesis.     

Respiration of juvenile Arctic cod (Boreogadus saida): effects of acclimation,temperature, and food intake

Oxygen consumption (VO₂) of juvenile Arctic cod (Boreogadus saida) was investigated at low tempera tures (six temperatures; range -0.5 to 2.7°C). Small (mean wt. 6–8 g) and large (mean wt. 14 g) fish were acclimated, or adjusted to a constant temperature (0.4°C), for 5 months and then tested for metabolic cold adaptation (elevated metabolic rates in polar fishes). Short-term (2 weeks) acclimated fish showed elevated VO₂ similar to previously established values for polar fishes, but there was no such evidence after longterm acclimation. Long-term acclimation caused VO₂ values to drop significantly (from 86.0 to 46.5 mg O₂·kg^–1·h^–1, at 0.4°C), which showed that metabolic cold adaptation was a phenomenon caused by insufficien: acclimation time for fish in respiration experiments. We also measured the effects of temperature and feeding on VO₂. A temperature increase of 2.3°C resulted in relatively large increases in VO₂ for both longand short-term acclimated fish (Q₁₀ = 6.7 and 7.1, respectively), which suggests that metabolic processes are strongly influenced by temperature when it is close to zero. Feeding individuals to satiation caused significant increases in VO₂ above pre-fed values (34–60% within 1–2 days after feeding). Respiration budgets of starved and fed Arctic cod at ambient temperatures in Resolute Bay N.W.T., Canada, were used to model annual respiration costs and potential weight loss. Low respiration costs for Arctic cod at ambient temperatures result in high growth efficiency during periods of feeding and low weight loss during periods of starvation.     

Is the marginal otolith increment width a reliable recent growth index for larval and juvenile herring?

Marginal otolith increment width analysis was performed on field‐collected larval and juvenile spring‐spawned herring Clupea harengus that experienced variable feeding conditions and high temperatures that were above the optimum for growth. Although drastic zooplankton biomass reduction had a significant effect on increment width, a delay of a few days in the otolith response was observed. More importantly, a very clear, positive temperature effect on marginal increment width was demonstrated in fish characterized by temperature independent somatic growth. These results indicate that under natural conditions it may be impossible to distinguish increment width changes related to variation in feeding conditions from changes caused by temperature fluctuations. Therefore, it was concluded that marginal otolith increment width analysis could not be used as a recent growth index ( I _G) for herring larvae and juveniles exposed to drastic temperature fluctuations. The implication of these results is significant not only for the use of marginal increments as a recent growth index, but also if growth rate backcalculation is to be used as a research method.