Vasconcelos RP, Reis-Santos P, Tanner S, Maia A, Latkoczy C, Gunther D, Costa MJ, Cabral H (2008) Evidence of estuarine nursery origin of five coastal fish species along the Portuguese coast through otolith elemental fingerprints. Estuarine, Coastal and Shelf Science 79, 317-327. (original) (raw)
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Identifying the relative importance of estuaries as effective nurseries for marine fish juveniles is essential to understand the processes defining the life cycle and structure of these species’ meta-populations and raises scientific interest due to the ecological and economical importance of directly associated functions and resources. In the present work, some of the main Portuguese estuaries (Minho, Douro, Ria de Aveiro, Mondego, Tejo, Sado, Mira, Ria Formosa and Guadiana) and commercially important fish species acknowledged for their use of these estuaries as putative nurseries (Solea solea, Solea senegalensis, Platichthys flesus, Diplodus vulgaris and Dicentrarchus labrax) were analysed following an integrative, multi-metric and multi-species approach. Estuaries were ranked by natural vulnerability and anthropogenic pressures through the development of a multi-metric index; with ecological impacts and end-points of pressure sources conceptually identified. Sites identified in different estuaries as important for juveniles, for one or several species, varied in fish density and habitat quantity, which together defined the potential export of juveniles. The variability in environmental characteristics of these sites highlighted species’ resilience to potential changes in estuaries. Habitat quality, measured with RNA:DNA and Fulton (K) condition indices, showed species-specific patterns of variation amongst estuaries. Juvenile contamination by trace elements was reduced and, in general, similar amongst estuaries. Otolith elemental fingerprints were validated as natural tags to discriminate estuaries individually; with specific patterns requiring fingerprint application to be made independently. These tags allowed the retrospective identification of the estuaries where marine adults spent their juvenile period and revealed the differential effective contribution of estuaries to adult subpopulations, which also differed amongst species. Combined results of all metrics identified differences in the relative importance of estuaries as nurseries and effective juvenile habitats for the analysed species and revealed some agreement between potential and effective export estimates from individual estuaries.
Chemical composition of otoliths may provide valuable information in establishing connectivity between nursery grounds and marine coastal stocks. Juveniles of the commercially important fish species Solea solea, S. senegalensis, Platichthys flesus, Diplodus vulgaris and Dicentrarchus labrax were captured in 8 estuarine nursery grounds along the Portuguese coast in July 2005. Concentrations of Li, Na, Mg, K, Mn, Ni, Cu, Zn, Sr, Cd, Ba and Pb were determined in whole juvenile otoliths using solution-based inductively coupled plasma mass spectrometry. Significant differences in the concentration of several elements were found between estuaries and species using ANOVA and MANOVA. Linear discriminant function analysis classified otolith fingerprints between estuaries for all species with good cross-validated results. Depending on the species, 70.2 to 92.0% of individuals were correctly assigned to their estuary of origin, with discrimination success varying with species, estuaries and number of estuaries in the analysis. Since accurate classification of juvenile fish to their nursery estuary was achieved, fingerprint analysis can be used as a natural habitat tag in assigning adult fish to their estuarine nursery. Ultimately the connectivity between Portuguese estuarine nursery grounds and coastal areas may be estimated, with possible implications for future fisheries and coastal management plans.
Otolith chemical composition differed between juveniles of five fish species (Solea solea, Solea senegalensis, Platichthys flesus, Diplodus vulgaris and Dicentrarchus labrax) in nursery areas of six estuaries along the Portuguese coast (Douro, Ria de Aveiro, Mondego, Tejo, Sado and Mira). Spatially consistent patterns in the concentration of some elements were responsible for differences between species. Discrimination of estuaries using data from all species simultaneously averaged 447% of correctly classified cases, whilst discrimination of species averaged 76.2%. Moreover, species-related patterns in otolith fingerprints were highlighted when comparing species for each estuarine nursery area, with intra estuarine species discrimination averages ranging from 86.2 to 1000%. Similarities in the otolith elemental fingerprints were larger between species with close phylogeny and ecology, particularly between flatfish and perciform species. In addition to the differences in physiological regulation of species, specific microhabitat use in a common environment was suggested as a relevant factor for the differentiation of otolith chemistry among species occurring in the same locations. Despite positive results in specific estuaries, variation in otolith composition limited the use of species as proxies to classify others to their system of origin.
Connectivity between estuarine fish nurseries and coastal adult habitats can be affected by variations in juvenile growth and survival. Condition indices are renowned proxies of juvenile nutritional status and growth rates and are valuable tools to assess habitat quality. Biochemical (RNA:DNA ratio) and morphometric (Fulton’s condition factor K) condition indices were determined in juveniles of Solea solea, Solea senegalensis, Platichthys flesus, Diplodus vulgaris and Dicentrarchus labrax collected in putative nursery areas of nine estuaries along the Portuguese coast (Minho, Douro, Ria de Aveiro, Mondego, Tejo, Sado, Mira, Ria Formosa and Guadiana) in the Spring and Summer of two consecutive years (2005 and 2006) with distinct climatic characteristics. Individual condition showed significant variation amongst species. The combined use of both condition indices highlighted the low correlation between them and that RNA:DNA had a higher sensitivity. RNA:DNA varied between years but overall the site relative patterns in condition were maintained from one year to the other. Higher RNA:DNA values were found in Spring than in Summer in most species. Intra-estuarine variation also occurred in several cases. Species specific trends in the variability of condition amongst estuaries were highlighted. Some estuaries had higher juvenile condition for more than one species but results did not reveal an identical trend for all species and sites, hindering the hypotheses of one estuarine nursery promoting superior growth for all present species. Significant correlations were found between condition indices, juvenile densities and environmental variables (water temperature, salinity and depth) in the estuarine nurseries. These influenced juvenile nutritional condition and growth, contributing to the variability in estuarine nursery habitat quality. Management and conservation wise, interest in multi-species approaches is reinforced as assessments based on a single species may not reflect the overall nursery habitat quality.
Natural or anthropogenic induced variations in estuaries and the dynamics of marine fish populations potentially promote differences in connectivity between estuaries and marine areas, i.e. in their importance as nursery grounds. Within this context, an integrated assessment of the differential nursery function of the main estuaries along the Portuguese coast for commercial fish species common sole Solea solea, Senegalese sole Solea senegalensis, flounder Platichthys flesus and sea bass Dicentrarchus labrax was performed through several indicators based on available data. Contribution of individual estuaries to marine subpopulations was measured with potential metrics (juvenile density, habitat quantity, juvenile number and habitat quality within estuaries) and effective metrics (estuarine source of young adults in marine environment measured via otolith elemental fingerprints). The relationship between the two types of metrics was also assessed. Estuaries identified as important nursery and/or effective juvenile habitat (EJH) differed with species and no single estuary was best for all, highlighting species-specific regulation of nursery function. Multiple species assessment of nursery and EJH function differed among estuaries. Management and conservation of estuaries should focus on sites with higher contributions to adult subpopulations of multiple species. The importance of defining precise scientific and management objectives was emphasized by the different rankings of estuaries obtained with nursery or EJH criteria. Potential and effective contribution of estuaries were not significantly correlated, but in a quantitative analysis juvenile densities and number of juveniles seem related with effective contribution in some species. An agreement between potential and effective contributions of estuaries is concurrent with the acknowledged minor role of juvenile stage processes in regulation of recruitment to adult subpopulations.
Analysing the estuarine use patterns of juveniles of marine migrant fish species is vital for identifying important sites for juveniles as well as the basic environmental features that characterize these sites for different species. This is a key aspect towards understanding nursery function. Various estuarine systems along the Portuguese coast (Minho, Douro, Ria de Aveiro, Mondego, Tejo, Sado, Mira, Ria Formosa and Guadiana) were sampled during Spring and Summer 2005 and 2006. Juveniles of commercially important marine fish species Solea solea, Solea senegalensis, Platichthys flesus, Diplodus vulgaris and Dicentrarchus labrax, predominantly 0-group individuals, were amongst the most abundant species and had distinct patterns of estuarine use as well as conspicuous associations with several environmental features. Juvenile occurrence and density varied amongst estuaries and sites within them, and differed with species. Sites with consistently high juvenile densities were identified as important juvenile sites (i.e. putative nursery grounds). Through generalized linear models (GLM), intra-estuarine variation in occurrence and density of each of the individual species was largely explained by environmental variables (temperature; salinity; depth; percentage of mud in the sediment; presence of seagrass; importance of intertidal areas; relative distance to estuary mouth; macrozoobenthos densities; and latitude). Decisive environmental factors defining important sites for juveniles varied depending on the system as a result of different environmental gradients, though there were common dominant features for each species regardless of the estuary considered. Analysed environmental variables in the GLM also accounted for inter-estuarine variation in species’ occurrence and density. In several estuaries, the identified important juvenile sites were used by many of these species simultaneously and may be of increased value to both management and conservation. Overall, the variability in site features amongst estuaries highlighted the tolerance of these species to different available environmental conditions and provided fundamental information for future spatially explicit modelling of their distribution. This should ultimately enable the prediction of species response to habitat alterations.
Organic and inorganic pollution can impact organisms directly and affect condition, growth and survival of juvenile fish which use estuaries as nurseries, and thereby affect marine adult populations quantitatively and qualitatively. Trace element contamination (Cu, Zn, Cd, Pb) in juveniles of commercial fish Solea solea, Solea senegalensis, Platichthys flesus, Diplodus vulgaris and Dicentrarchus labrax collected in putative nurseries of the main Portuguese estuaries (with diverse intensities and sources of anthropogenic pressures) was determined via atomic absorption spectrometry. Contamination was significantly different among species. Similar levels of contamination were found among estuaries, except for D. vulgaris. Cu and Zn concentrations ranged from 1.0 to 2.1 and 14 to 59 µg g-1 muscle dry weight respectively; while Cd and Pb concentrations were very low. The results indicate that juvenile migration to off-shore habitats is associated with low export of contamination, and no particular estuary increases the potential contamination of adult stocks. This knowledge is of the utmost importance in view of the ecological and economical value of these species and their use of estuarine areas as nurseries.
Otolith elemental signatures (Li:Ca, Mg:Ca, Mn:Ca, Cu:Ca, Sr:Ca, Ba:Ca and Pb:Ca) of age-0 juveniles of flounder Platichthys flesus and sea bass Dicentrarchus labrax, collected from estuarine systems along the Portuguese coast in 2006 and 2009 were used as baseline signatures to identify the estuarine nursery of age-3+ and 2+ coastal fish matching the juvenile year classes. Otolith elemental signatures were determined via Laser Ablation Inductively Coupled Plasma Mass Spectrometry, and successfully identified the estuarine origin of the majority of coastal fish to characterized baseline estuaries. Relative contributions of individual estuaries to coastal areas, quantified using maximum likelihood estimation, varied over time for the two year classes analysed. Yet, some general patterns were discernible in terms of important estuaries and those with minor or negligible contributions. Assigned nursery origins varied among species and suggested large scale movements along the coast. For P. flesus the main source for recruits changed between year classes from Ria de Aveiro (69 %) to the Douro estuary (59 %). The Mondego estuary, located near the latitudinal limit of P. flesus occurrence contributed moderate numbers to coastal populations. The Tejo estuary was the most important estuary for D. labrax in both years (55 and 50 %), whilst the Ria de Aveiro hardly contributed to sea bass coastal populations (<2 %). Ultimately, knowledge of which estuaries replenish coastal adult populations, and fisheries both local and distant, is essential for effective management and conservation of these species and their estuarine juvenile habitats.
The chemical composition of fish otoliths can provide valuable information for determining the nursery value of estuaries to adult populations of coastal fishes. However, understanding temporal variation in elemental fingerprints at different scales is important as it can potentially confound spatial discrimination among estuaries. Otolith elemental ratios (Li:Ca, Mg:Ca, Mn:Ca, Cu:Ca, Sr:Ca, Ba:Ca and Pb:Ca) of Platichthys flesus and Dicentrarchus labrax, from several estuaries along the Portuguese coast in two years and three seasons (spring,summer and autumn) within a year, were determined via Laser Ablation Inductively Coupled Plasma Mass Spectrometry. Elemental fingerprints varied significantly among years and seasons within a year but we achieved accurate classifications of juvenile fish to estuarine nursery of origin (77-96% overall cross-validated accuracy). Although elemental fingerprints were year-specific, variation among seasons did not hinder spatial discrimination. Estuarine fingerprints of pooled seasonal data were representative of the entire juvenile year class and attainedhigh discrimination (77% and 80% overall cross-validated accuracy for flounder and sea bass, respectively). Incorporating seasonal variation resulted in up to an 11% increase in correct classification of individual estuaries, in comparison to seasons where accuracies were lowest. Overall, understanding the implications of temporal variations in otolith chemistry for spatial discrimination is key to establish baseline data for connectivity studies.
Statistical models are key for estimating fish distributions based on environmental variables, and validation is generally advocated as indispensable but seldom applied. Generalized Linear Models were applied to distributions of juvenile Solea solea, Solea senegalensis, Platichthys flesus and Dicentrarchus labrax in response to environmental variables throughout Portuguese estuaries. Species-specific Delta models with two sub-models were used: Binomial (presence/absence); Gamma (density when present). Models were fitted and tested on separate data sets to estimate the accuracy and robustness of predictions. Temperature, salinity and mud content in sediment were included in most models for presence/absence; salinity and depth in most models for density (when present). In Binomial models (presence/absence), goodness-of-fit, accuracy and robustness varied concurrently among species, and fair to high accuracy and robustness were attained for all species, in models with poor to high goodness-of-fit. But in Gamma models (density when present), goodness-of-fit was not indicative of accuracy and robustness. Only for Platichthys flesus were Gamma and also coupled Delta models (density) accurate and robust, despite some moderate bias and inconsistency in predicted density. The accuracy and robustness of final density estimations were defined by the accuracy and robustness of the estimations of presence/absence and density (when present) provided by the sub-models. The mismatches between goodness-of-fit, accuracy and robustness of positive density models, as well as the difference in performance of presence/absence and density models demonstrated the importance of validation procedures in the evaluation of the value of habitat suitability models as predictive tools.