The Spanish National Advisory Board of Mariculture (JACUMAR) developed an initiative to unify methodologies between the regions of Spain, in which they proposed the implementation of site-specific “Environmental Monitoring Plans” (EMPs). In this study, we tested the feasibility of an EMP on a fish farm in the Mediterranean Sea. The methods and tools proposed in the EMP are highly useful for environmental monitoring of aquaculture. However, spatial heterogeneity figured prominently in a univariate analysis with environmental variables and a multivariate analysis of polychaete assemblages. This variability may be due to habitat patchiness, and may therefore be solved by an improved experimental design, e.g. by adding replications for increasing statistical power. Multivariate analysis of polychaete assemblages provided accurate information about the quality of the sediment. This information could also be improved using ecological data about key polychaete families in order to avoid misleading results. Thus, the JACUMAR EMP has proved useful in providing precise information about the ecological status of marine benthic habitats, meeting the requirements of current European Directives. However, we suggest that some modifications may be required in order to account for possible misleading thresholds for environmental quality standards, spatial heterogeneity and increasing power analyses.
La Junta Nacional Asesora de Cultivos Marinos (JACUMAR) desarrolló una iniciativa para unificar metodologías entre las regiones de España, en la que propusieron la implementación de “Planes de Seguimiento Ambiental” (EMP) específicos de cada caso. En este estudio se ha evaluado la viabilidad del EMP en una granja de peces del Mediterráneo. Los métodos y herramientas propuestos en el EMP son de gran utilidad para el seguimiento ambiental de la acuicultura. Sin embargo, la heterogeneidad espacial ha jugado un papel destacado en los análisis uni-variante con variables ambientales y multi-variante de las comunidades de poliquetos. Esta variabilidad puede ser debida a la heterogeneidad de los hábitats y, por tanto, debe resolverse mejorando el diseño experimental, p.ej. añadiendo réplicas en el muestreo para aumentar la potencia estadística. El análisis multi-variante de las comunidades de poliquetos ha proporcionado información precisa sobre la calidad del sedimento. Esta información también podría mejorarse utilizando datos ecológicos sobre las principales familias de poliquetos, con el fin de evitar resultados que pudieran inducir a errores. Por todo lo anterior, el EMP propuesto por JACUMAR ha demostrado ser útil para proporcionar información precisa sobre el estado ecológico de los hábitats bentónicos marinos, cumpliendo con los requisitos de las directivas europeas actuales. Sin embargo, los resultados de este artículo sugieren la conveniencia de realizar algunas modificaciones, con el objetivo de mejorar los umbrales para los estándares de calidad ambiental, la heterogeneidad espacial y la potencia de los análisis.
The identification of indicators for the monitoring of aquaculture activities has been on the agenda of the FAO’s General Fisheries Commission for the Mediterranean in recent decades (
This approach to EMPs focuses on the interactions between aquaculture and benthic ecosystems, in particular, increases in organic enrichment (from uneaten food and fish faeces) and the sensitiveness of benthic assemblages to detecting environmental impacts (
Among all macrobenthic faunal groups, the polychaete assemblages are commonly used for the analysis of disturbances produced by organic enrichment, due to their widespread distribution in the benthos, their trophic flexibility and their quick response to disturbances (
The aim of this study was to assess the feasibility of the EMP defined by JACUMAR (
The study was carried out in 2009 in a sea bream and sea bass floating-cage farm at 25-30 m depth in Guardamar bay, southeast Spain (
Samples were collected in late summer during the period of warmest water and maximum productivity. Four zones were sampled in the vicinity of the fish farm according to the EMP (
δ15N(‰) = [(Rsample/Rstandard)–1] 103
where R=15N/14N. The standard was atmospheric N2 while the analytical precision was 0.1‰ (
Data analyses
Values of environmental variables were classified by the environmental quality standards (EQS) proposed by JACUMAR (
Environmental Quality Standards (EQS) | ||
---|---|---|
Zone A | Zone B | |
Total free sulphide (TFS) | <3000 µM <3 samples over 5000 µM | <3000 µM <50% higher than zones C |
Finest fraction | <50% higher than zones C | <25% higher than zones C |
Organic matter (OM) | <50% higher than zones C | = zones C |
pH | Between 7 and 9 | Between 7.5 and 8.5 Special case: = zones C |
Redox potential (Eh) | Zone A Special case: –50 and –100 mV higher than zone C | Between –50 and –100 mV higher than zone C Special case: = zones C |
δ15N | <6‰ or <4 units higher than zones C | = zones C |
Polychaete assemblage | <75% less families than zones C | <50% less families than zones C |
<75% dissimilarity compared to zones C | <50% dissimilarity compared to zones C |
ANOVA analysis of the environmental variables showed that total free sulphide (TFS) was the most sensitive environmental variable to the fish farming activity, showing significant differences for zone factor (
ANOVA | TFS | % Finest fraction | Organic matter | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Source of variation | df | F | P | CV | F | P | CV | F | P | CV | ||
Zone | 3 | 30.78 | 0.000*** | 81% | 1.66 | 0.252 | 10% | 1,36 | 0.322 | 6% | ||
Station (zone) | 8 | 1.43 | 0.235 | 2% | 2.65 | 0.031· | 31% | 2,29 | 0.055· | 28% | ||
Residual | 24 | 17% | 59% | 66% | ||||||||
Cochran’s C test | C=0.37631, P>0.05 | - a | C=0.35787, P>0.05 | |||||||||
Transformation | log (x+1) | arc sin (x) | log (x+1) | |||||||||
ANOVA | pH | Eh | δ15N | |||||||||
Source of variation | F | P | CV | F | P | CV | F | P | CV | |||
Zone | 3 | 0.95 | 0.461 | 0% | 5.79 | 0.021 | 52% | 0.69 | 0.585 | 0% | ||
Station (zone) | 8 | 0.44 | 0.885 | 0% | 4.19 | 0.003* | 25% | 0.66 | 0.723 | 0% | ||
Residual | 24 | 100% | 23% | 100% | ||||||||
Cochran’s C test | -a | -a | C=0.30955, P>0.05 | |||||||||
Transformation | none | none | none | |||||||||
PERMANOVA | Polychaete assemblage | Pairwise test | P | P-MC | ||||||||
Source of variation | P | CV | A - B | 0.0956 | 0.0029** | |||||||
A - C1 | 0.1034 | 0.0007*** | ||||||||||
Zone | 3 | 0.0004*** | 37% | A - C2 | 0.0977 | 0.0003*** | ||||||
Station (zone) | 16 | 0.029* | 16% | B - C1 | 0.1019 | 0.06 | ||||||
Residual | 24 | 47% | B - C2 | 0.1957 | 0.1809 | |||||||
Total | 35 | C1 - C2 | 0.1 | 0.0538 |
Despite the significant differences observed in the ANOVA analysis, TFS concentration did not exceed the permitted limits established by the EQS proposed by JACUMAR (
PERMANOVA analysis of polychaete families showed significant differences among zones in spite of the spatial variability among stations (
The MDS analysis of the polychaete assemblage structure was in agreement with the PERMANOVA results, as zones C1, C2 and B were tightly clustered, and zone A appeared to be separated in the plot. Moreover, zone A showed higher scatter between its samples (
Polychaete assemblage | |||
---|---|---|---|
Zone | Aver. Dissim. % | % nº families | EQS |
A - C1 | 83.87 | <64.63 | <75 |
A - C2 | 83.82 | <70.10 | <75 |
B - C1 | 53.97 | >17.07 | <50 |
B - C2 | 48.95 | <1.03 | <50 |
A - B | 86.53 | ||
C1 - C2 | 44.4 |
The application of EMPs proposed by JACUMAR (
The spatial variability for geochemical and biological variables is a normal consequence of benthic assemblage patchiness and irregular disturbance of the seabed by fish farming. This variability can affect the sediment mostly at a scale of metres (
Dissimilarity tests for polychaete assemblages concluded that values in zones A and B exceeded the EQS proposed by JACUMAR. In this aspect of sensitivity, polychaete assemblages at family level appeared to be a very good tool for identifying changes in the benthic ecosystem, allowing slight differences between zones to be detected even with high spatial heterogeneity. Polychaete assemblages showed higher spatial variability below the fish farm than in other zones. This increased variability has been considered to be a general feature of assemblages in stressed environments and could be due to several scenarios: changes in total cover or total number of taxa, changes in the variance-to-mean ratio for particular species, or changes in taxonomic composition (
Analysis of polychaete assemblages could be enhanced with ecological information from univariate analysis of polychaete families. Polychaetes have been well documented as bioindicators, specifically species such as
Sulphide measurements, such as TFS, are able to show variations in biogeochemical processes of the sediment due to organic enrichment (
After many years using Eh to add information on the degree of organic enrichment, some authors do not advocate its use in finfish monitoring. This is due to the problems associated with potential “poisoning” of the probes and the high variability in the Eh measures, and the difficulty of obtaining a stable reading that was also encountered in the present study (
A more exhaustive EMP with increased periodicity may be required if surveys reveal significant negative impacts. An adjustable EMP is proposed by JACUMAR for Spain, as has been done by Norway and Croatia (
Consensus about monitoring protocols is needed to ensure that data meet defined standards of quality with a known level of confidence, in order to be credible to external review and allow comparisons between places, regions and agencies. The proposed EMP of JACUMAR seems to be a very innovative approach and a reliable tool for monitoring fish farming along a scale of thousands of kilometres along the entire Spanish coast, and this kind of proposal could be considered for implementation in other European and Mediterranean countries with fish farming under similar environmental conditions. Moreover, this EMP is pioneering in adding a hypothesis test as an EQS for fish farm monitoring, and in proposing comparisons with control locations as natural background values. However, in some cases higher statistical power with regard to univariate and multivariate analysis is needed in order to accurately determine the effects of fish farming.
Therefore, before full implementation of JACUMAR EMP in Spain, it will be necessary to evaluate the need to increase spatial replication at several scales, contrasting the information obtained from various pilot cases. A revision of EQS for environmental variables will be recommended for TFS and polychaete assemblage with the addition of ecological information about their families. The use of Eh and δ15N would be unwise. Moreover, iterative EMP will be important in order to trace the progression of fish farm activity in relation to benthic environmental quality (
We are grateful to the CULMAR fish farm for giving us access and providing assistance during the study. We thank “Spanish National Plans of Aquaculture” (JACUMAR) in particular for the project “Selección de indicadores, determinación de valores de referencia, diseño de programas y protocolos de métodos y medidas para estudios ambientales en acuicultura marina”. We also thank Nick Marchant for his assistance with the English version.