Seeking the true time: Exploring otolith chemistry as an age-determination tool

Fish otoliths' chronometric properties make them useful for age and growth rate estimation in fisheries management. For the Eastern Baltic Sea cod stock (Gadus morhua), unclear seasonal growth zones in otoliths have resulted in unreliable age and growth information. Here, a new age estimation method based on seasonal patterns in trace elemental otolith incorporation was tested for the first time and compared with the traditional method of visually counting growth zones, using otoliths from the Baltic and North seas. Various trace elemental ratios, linked to fish metabolic activity (higher in summer) or external environment (migration to colder, deeper habitats with higher salinity in winter), were tested for age estimation based on assessing their seasonal variations in concentration. Mg:Ca and P:Ca, both proxies for growth and metabolic activity, showed greatest seasonality and therefore have the best potential to be used as chemical clocks. Otolith image readability was significantly lower in the Baltic than in the North Sea. The chemical (novel) method had an overall greater precision and percentage agreement among readers (11.2%, 74.0%) than the visual (traditional) method (23.1%, 51.0%). Visual readers generally selected more highly contrasting zones as annuli whereas the chemical readers identified brighter regions within the first two annuli and darker zones thereafter. Visual estimates produced significantly higher, more variable ages than did the chemical ones. Based on the analyses in our study, we suggest that otolith microchemistry is a promising alternative ageing method for fish populations difficult to age, such as the Eastern Baltic cod.     

How old are you—Evaluation of age reading methods for the invasive round goby (Neogobius melanostomus,Pallas 1814)

In the Baltic, the first observation of the round goby (Neogobius melanostomus, Pallas 1814) was made in 1990. Within the past decade the species became invasive and spread rapidly throughout the Baltic Sea. Studies about the fishes potential impacts on resident species promote the need for an increasing knowledge of their basic stock structures such as growth rates, longevity and mortality, which all rely on accurate estimates of age. Former studies on the round goby have used several different age reading techniques. In this study, we compared three standard otolith preparation methods for ageing and present the best procedure for the invasive round goby. The results showed significant differences in age estimates of the same fish between the different preparation methods and between readers. The estimation of the first annulus, the first year, was the most problematic. The overall agreement was lowest when reading the whole otoliths while the best performance was achieved with sectioned and stained preparation method. Depending on method used the growth estimates also differed. The results question comparability between previous studies and highlight the importance of harmonised aging procedures for the round goby for obtaining correct estimates of population parameters such as growth rate, age at maturity, and longevity.     

Otolith annulus validation and variables influencing false annuli formation in dorsal spines of saugeye

Marginal increment analysis is a common technique for validating formation of a single annual growth ring on an ageing structure. False annuli can form on ageing structures when environmental variables affect growth of a fish, potentially resulting in age estimation bias. Therefore, validating ageing structures is essential to ensure that accurate and precise age estimates are collected when assessing fish population dynamics. Saugeye (Sander vitreus, [Mitchill, 1818]) and S. Canadensis, [Griffith and Smith, 1834]) are highly valued sport fish that are stocked across the Midwest United States. Using marginal increment analysis, we confirmed that a single annulus was formed yearly in otoliths of juvenile saugeye, however two annuli formed in dorsal spines in a single year. Timing of the first annulus formation in both otoliths and dorsal spines was completed after a slow growth period during winter (otoliths forming in April; dorsal spines forming in March). The second annulus (false annulus) that formed during August in dorsal spines did not form in otoliths. To understand what environmental factors may influence the false annulus to form, we collected monthly water temperatures and percent empty stomachs of juvenile saugeye. The highest water temperatures of the year occur during July and August, which resulted in saugeye seeking thermal refuge and affecting feeding habits. Mean monthly temperature and percent empty stomachs were positively correlated, so during times of high temperatures foraging rates declined, suggesting the formation of false annulus on dorsal spines of juvenile saugeye. This study demonstrates how thermal stress affected accuracy of non‐lethal aging structures and further emphasizes the need for age validation studies prior to using non‐lethal ageing structures to estimate age for a particular species from different aquatic systems.     

Diet composition and food consumption rate of harbor porpoises (Phocoena phocoena) in the western Baltic Sea

Stomach content composition and prey‐specific consumption rates of juvenile and adult harbor porpoises (Phocoena phocoena) were estimated from a data set including 339 stomachs collected over a 32 yr period (1980–2011) in the western Baltic Sea. The stomach contents were mainly hard parts of fish prey and in particular otoliths. The bias originating from differential residence time of otoliths in the stomachs was addressed by use of a recently developed approach. Atlantic cod and herring were the main prey of adults, constituting on average 70% of the diet mass. Juvenile porpoises also frequently consumed gobies. Here, the mass contribution by gobies was on average 25%, which was as much as cod. Other species such as whiting, sprat, eelpout, and sandeels were of minor importance for both juveniles and adults. The diet composition differed between years, quarters, and porpoise acquisition method. Yearly consumption rates for porpoises in the western Baltic Sea were obtained in three scenarios on the daily energy requirements of a porpoise in combination with an estimate including the 95% CLs of the porpoise population size. Cod of age groups 1 and 2 and intermediate‐sized herring suffered the highest predation from porpoises.     

The diet of whiting Merlangius merlangus in the western Baltic Sea

The diet of whiting Merlangius merlangus in the western Baltic Sea was investigated and compared to the diet in the southern North Sea. Clupeids were important prey in both areas, but especially in the western Baltic Sea where they constituted up to 90% of the diet of larger individuals. Gobies, brown shrimps and polychaetes were the main prey of juveniles in the western Baltic Sea, while a wider range of species were consumed in the North Sea. The shift to piscivory occurred at smaller sizes in the western Baltic Sea and the fish prey consumed was proportionately larger than in the southern North Sea. Estimates of prey abundance and food intake of M. merlangus are required to evaluate its predatory significance in the western Baltic Sea, but its diet suggests that it could be just as significant a fish predator here as in the southern North Sea.     

Age and growth of the round goby Neogobius melanostomus in the Gulf of Gdańsk several years after invasion. Is the Baltic Sea a new Promised Land?

The ages of 8 to 23·5 cm total length (L(T)) round goby Neogobius melanostomus collected monthly during 2006 and 2007 in the Gulf of Gdańsk (Baltic Sea) ranged from 2 to 6 years, with age class 4+ years dominant. Males were larger at age than females. The fastest growth occurred in the first 2 years of life in both sexes. Females were heavier at a given L(T) than males, but only for fish > c. 15 cm. A strong relationship between N. melanostomus otolith size and fish size was found, with no difference between males and females, and a significant relationship between fish growth rate and otolith growth rate, which enabled backcalculation of growth rates. Marginal increment width analysis confirmed the periodicity of annual ring formation in otoliths and showed that the most intense opaque zone formation occurs in July to August, while hyaline zone formation starts as early as September to October. It was concluded that the N. melanostomus that have colonized the southern Baltic Sea exhibit the largest size and longest life span ever recorded for this species.     

New data on the longevity of coastal cod Gadus morhua Linnaeus, 1758 in the White Sea

The cod, Gadus morhua, is a common and abundant demersal fish in the White Sea coastal zone. The published data on the maximum age of White Sea cod still requires additional documentation, because some authors have noted difficulties in age determination by otoliths of large specimens. To obtain accurate data on the longevity of this species in the White Sea, an image analysis of thin‐sections of otoliths was made for age estimation. Research surveys in the Chupa Inlet and adjacent waters of the Kandalaksha Bay were conducted in June to August from 2007 to 2013. The five largest specimens of a total of 3564 captured fish were selected for age determination. Age of these largest individuals ranged between 7 and 12 years, total length and weight varied from 60.2 to 77.0 cm and from 2.4 to 6.1 kg, respectively. According to the data, maximal White Sea cod longevity is greater than in previously published data, and demonstrates similar longevity to conspecifics from the Baltic and North seas, whereas its life cycle is much shorter than cod from the Northeast Arctic, Iceland, Greenland, Newfoundland and Labrador stocks.     

Age estimation and validation for South Pacific albacore Thunnus alalunga

Validated estimates of age are presented for albacore Thunnus alalunga, sampled from a large part of the south‐western Pacific Ocean, based on counts of annual opaque growth zones from transverse sections of otoliths. Counts of daily increments were used to estimate the location of the first opaque growth zone, which was completed before the first assumed birthday. The periodicity of opaque zones was estimated by marginal increment analysis and an oxytetracycline mark–recapture experiment. Both validation methods indicated that opaque zones formed over the austral summer and were completed by autumn to winter (April to August). The direct comparison of age estimates obtained from otoliths and dorsal‐fin spines of the same fish indicated bias, which was assumed to be due to poor increment clarity and resorption of early growth zones in spines, resulting in imprecise age estimates. As such, age estimates from otoliths are considered to be more accurate than those from spines for T. alalunga. This is consistent with results for a growing number of tropical and temperate tuna Thunnini species. It is recommend that validated counts of annual growth zones from sectioned otoliths is used as the preferred method for estimating age‐based parameters for assessment and management advice for these important stocks.     

Evaluating the effectiveness of teeth and dorsal fin spines for non‐lethal age estimation of a tropical reef fish,coral trout Plectropomus leopardus

This study investigated whether teeth and dorsal fin spines could be used as non‐lethal methods of age estimation for a vulnerable and highly valued tropical fisheries species, coral trout Plectropomus leopardus. Age estimation of individuals from 2 to 9 years old revealed that dorsal spines represent an accurate ageing method (90% agreement with otoliths) that was more precise [average per cent error (APE) = 4·1, coefficient of variation (c.v .) = 5·8%] than otoliths (APE = 6·2, c.v . = 8·7%). Of the three methods for age estimation (otoliths, dorsal spines and teeth), spines were the most time and cost efficient. An aquarium‐based study also found that removing a dorsal spine or tooth did not affect survivorship or growth of P. leopardus. No annuli were visible in teeth despite taking transverse and longitudinal sections throughout the tooth and trialling several different laboratory methods. Although teeth may not be suitable for estimating age of P. leopardus, dorsal spines appear to be an acceptably accurate, precise and efficient method for non‐lethal ageing of individuals from 2 to 9 years old in this tropical species.     

An assessment of otoliths,dorsal spines and scales to age the long‐finned gurnard,Lepidotrigla argus,Ogilby, 1910 (Family: Triglidae)

Sagittal otoliths, dorsal spines and scales were critically assessed as structures to potentially determine the age of the long‐finned gurnard, Lepidotrigla argus. Counts were made of opaque growth increments and a readability score was assigned to each structure. Comparisons of growth increment counts were made between structures and between readings. All three structures showed some degree of readability and quantifiable growth increments, but this varied within fishes and between structures. Initial results showed that whole otoliths were more suitable to determine age estimates than dorsal spines and scales. Scales were considered unsuitable due to between reading ageing bias, variation in age estimates between structures, low precision and poor readability for this species. Dorsal spines showed evidence of loss of growth increments due to hollowing of the vascular core, which resulted in underestimation of older individuals in comparison to whole otoliths. Further analysis showed that growth increment counts from whole otoliths were lower for older individuals in comparison to sectioned otoliths. It is suggested that this is because of decreased clarity of growth increments towards the outer margin of whole otoliths in older individuals; this problem was not present with sectioned otoliths. It was concluded that sectioned otoliths were a more suitable structure from which to estimate age of L. argus than were whole otoliths, dorsal spines and/or scales.     

The use of otolith microstructure to estimate age in adult Atlantic cod Gadus morhua

Transverse sections of otoliths from Atlantic cod Gadus morhua from the Baltic Sea revealed narrow growth increments. The widths of these increments corresponded to daily increments from fish with known otolith growth rates and were therefore assumed to be daily increments. They exhibited a distinct pattern with increasing distance from the primary primordium. A series of zones with clearly distinguishable increments, first with increasing then with decreasing widths in a dome‐shaped pattern, were separated by zones where no regular increment structure was visible. Increment width seemed to be tightly coupled to the annual cycle in environmental temperature at a depth of 30–60 m, where G. morhua predominantly reside. Between 135 and 200 increments occurred within the different zones, with a non‐significant trend towards lower increment numbers and widths with distance from the primary primordium of the otolith. Increment formation apparently ceased at temperatures < 5–6° C, but growth during the cold months corresponded closely with estimated growth rates. The increment patterns seemed to reflect annual cycles in environmental temperature, and the count of the increment cycles may thus be a promising tool for the determination of the true age of Baltic G. morhua.     

Age and growth of grey triggerfish Balistes capriscus from trans-Atlantic populations

Anthropogenic factors that negatively impact reef fishes can include changes in life-history patterns of fisheries-targeted species. Understanding these impacts on growth and population age structure is essential in the management of exploited populations of fishes. This is the first study to directly compare age and growth for a major fisheries species between east and west populations of a transatlantic reef fish. The main goal of this study was to document age and growth in grey triggerfish Balistes capriscus from coastal waters of Ghana in the Gulf of Guinea (GOG) and compare those with the previous growth studies from that region and with the western Atlantic population. A secondary objective of this study was to evaluate the use of otoliths to age triggerfish and to provide a preliminary comparison with spine-derived age estimates. The results obtained from this study provided an updated understanding of the growth and age structure of the eastern B. capriscus population in GOG. The authors documented that shifts in population attributes occurred for B. capriscus after its major decline in abundance. The differences in physical and biotic characteristics of the East and West Atlantic regions and the differences in collection methods of samples make direct comparisons of growth parameters difficult. Nonetheless, overall differences in maximum sizes and ages were apparent; the western Atlantic population had a larger maximum size and older maximum age. The authors also documented that sagittal otoliths can be used to provide age estimates for triggerfish species, and otoliths as an ageing structure had better between-reader precision compared to dorsal spines.     

Changes in endosteal cell layer number of long bones are not appropriate for ageing birds: Evidence from Baltic razorbills (Alca torda Linnaeus, 1758)

Estimating the age of birds by counting the number of cell layers within the circumferential lamellae of the bone cortex gave promising results in some species (e.g., fulmar Fulmarus glacialis; shag Phalacrocorax aristotelis) but was not confirmed for others (e.g., Canada goose Branta canadensis; sandhill crane Grus canadensis). Moreover, different results were received for different bones from the same individual and the factors influencing these results have not been identified. We have evaluated the ageing method for a non-migratory population of razorbills (Alca torda) from Baltic Sea colonies by examining humeri from 38 razorbills recorded dead on the Polish coastal zone of the Baltic Sea. Only humeri of 19 birds showed clearly defined borders between the osteonal matrix and the endosteal bone. Razorbills were divided into three age categories by bill ornament (juveniles, immature, adults) and showed a trend towards a gradual loss of cell layers in the endosteal bone with increasing age, where median values totalled 8.5, 7 and 6 layers respectively. Our results indicate that counting the number of cell layers within the circumferential lamellae of the bone cortex is not a reliable methodology for ageing razorbills.     

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.     

Differentiation of western and eastern Baltic Sea cod stocks (Gadus morhua) by means of stable isotope ratios in muscles and otoliths

Stable isotope analysis of Baltic Sea cod from the Bornholm Sea (ICES‐SD 25) and western Baltic (Belt Sea, ICES‐SD 22) revealed significant differences in the δ¹⁵N and δ¹³C values of the dorsal muscle, as well as in the δ¹⁸O values of otoliths. The method pledges to become especially appropriate to the Baltic due to the high variability in oxygen isotope ratios associated with its estuarine nature.     

Validation of age readings from otoliths of juvenile roundnose grenadier, Coryphaenoides rupestris, a deep-water macrourid fish

Validation of the ageing of deep-water fish is difficult and there are only a few instances where the rings on the otoliths have been shown to be laid down annually. Roundnose grenadier have been fished commercially in the North Atlantic since the 1960s and the adult fish have frequently been aged by counting the rings in otoliths or scales. All the ageing was done on the assumption that the rings in the otoliths or scales were annual. Between 1975 and 1992, the Scottish Association for Marine Science carried out seasonal trawling surveys in the Rockall Trough using a fine-meshed trawl, and collected otoliths from a wide size range of roundnose grenadier. An examination of the growing edge of otoliths from juvenile fish from these collections suggests that the rings in the otoliths are laid down annually. The broader, opaque zones which represent the growth phase were dominant between September and March. The thinner, hyaline zones were dominant between April and July. The apparent delay in the growth phase compared with most shallow-water species is discussed in relation to the availability of mesopelagic prey.     

Age determination in common carp <Emphasis Type="Italic">Cyprinus carpio</Emphasis>: history,relative utility of ageing structures,precision and accuracy

The common carp Cyprinus carpio is one of the most widely-distributed freshwater fishes in the world. Due to its value for conservation and fisheries in several native/translocated areas of distribution and its detrimental effects on the aquatic ecosystem in most invasive areas, robust age-based population dynamics models are required for successful management of this species. The present study provides a global review of age determination in carp, including a historical account of ageing methods, an assessment of the relative utility of ageing structures, and an evaluation of precision and accuracy (i.e. validation) of age estimates. Historically, scales were by far the most widely-employed structure, followed by the operculum, otolith, dorsal spine, vertebra and fin ray. However, in countries where carp is categorised as ‘high risk’ of impact, use of alternative structures to the scale was predominant. Causal criteria analysis showed scales and opercula to provide inconsistent evidence for successful annulus identification/counting, whereas consistent evidence was found for otoliths, dorsal spines, vertebrae and (pectoral) fin rays. Precision was always above reference thresholds for scales, whereas for otoliths, dorsal spines and fin rays was in several cases below. Accuracy was addressed sporadically and mostly in high-risk countries. It is suggested that dorsal spines or pectoral fin rays should be used in lieu of scales as non-lethal ageing structures, and otoliths (or vertebrae, pending more research) otherwise, and that validation should always be attempted as part of the set-up of more appropriate ageing protocols and use of correct terminology.     

Tetracycline marks visible in Baltic cod Gadus morhua otoliths stored for 40 years

Baltic cod Gadus morhua otoliths marked with oxytetracycline (OTC) in 1974–1975 had been sectioned and the sections stored in paper envelopes at room temperature in dry, dark conditions. After 40 years of storage, the historic OTC marks were still clearly visible showing that OTC is suitable for long‐term chemical marking of otoliths. They were, however, noticeably paler than marks in recently recaptured and archived Baltic G. morhua otoliths, chemically tagged with tetracycline at similar dosage to the historic otoliths.