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Science of the Total Environment 605–606 (2017) 1055–1063 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Relationship of fish indices with sampling effort and land use change in a large Mediterranean river David Almeida a, Juan Diego Alcaraz-Hernández a, Roberto Merciai a, Lluís Benejam b, Emili García-Berthou a,⁎ a GRECO, Institute of Aquatic Ecology, University of Girona, 17003 Girona, Catalonia, Spain b BETA Technology Centre, Aquatic Ecology Group, University of Vic – Central University of Catalonia, 08500 Vic, Catalonia, Spain HIGHLIGHTS GRAPHICAL ABSTRACT • Fish-based indices have been barely tested in lower reaches of large European rivers. • Two fish-based indices (EFI+ and IBICAT2b) respond significantly to land use change in the River Ebro. • EFI+ also depends on sampling effort. • Existing standard protocols should be carefully followed for ecological assess- ment using fish. article info abstract Article history: Fish are invaluable ecological indicators in freshwater ecosystems but have been less used for ecological assess- Received 15 April 2017 ments in large Mediterranean rivers. We evaluated the effects of sampling effort (transect length) on fish metrics, Received in revised form 2 June 2017 such as species richness and two fish indices (the new European Fish Index EFI+ and a regional index, IBICAT2b), Accepted 3 June 2017 in the mainstem of a large Mediterranean river. For this purpose, we sampled by boat electrofishing five sites each Available online xxxx with 10 consecutive transects corresponding to a total length of 20 times the river width (European standard re- Editor: D. Barcelo quired by the Water Framework Directive) and we also analysed the effect of sampling area on previous surveys. Species accumulation curves and richness extrapolation estimates in general suggested that species richness was Keywords: reasonably estimated with transect lengths of 10 times the river width or less. The EFI+ index was significantly Ecological status affected by sampling area, both for our samplings and previous data. Surprisingly, EFI+ values in general de- European fish index EFI + creased with increasing sampling area, despite the higher observed richness, likely because the expected values Human impact of metrics were higher. By contrast, the regional fish index was not dependent on sampling area, likely because it Index of biotic integrity does not use a predictive model. Both fish indices, but particularly the EFI+, decreased with less forest cover per- Non-native species centage, even within the smaller disturbance gradient in the river type studied (mainstem of a large Mediterra- nean river, where environmental pressures are more general). Although the two fish-based indices are very different in terms of their development, methodology, and metrics used, they were significantly correlated and provided a similar assessment of ecological status. Our results reinforce the importance of standardization of sampling methods for bioassessment and suggest that predictive models that use sampling area as a predictor might be more affected by differences in sampling effort than simpler biotic indices. © 2017 Elsevier B.V. All rights reserved. ⁎ Corresponding author. E-mail address: [email protected] (E. García-Berthou). http://dx.doi.org/10.1016/j.scitotenv.2017.06.025 0048-9697/© 2017 Elsevier B.V. All rights reserved. 1056 D. Almeida et al. / Science of the Total Environment 605–606 (2017) 1055–1063 1. Introduction of fish species occurrence and richness —key indicators in estimates of fish assemblage integrity and diversity—, whereas oversampling causes Freshwater ecosystems provide essential services to humanity (e.g. costs higher than necessary (Hughes et al., 2002). Species richness rises water provisioning, irrigation, energy production) and are thus severely monotonically with sampling area (e.g., electrofishing transect length) disrupted worldwide because of hydrologic alteration, pollution, river to an asymptotic maximum number of species (Hughes et al., 2002; fragmentation, and introduction of invasive species (Malmqvist and Meador, 2005). Typically, a smaller transect length might be expected Rundle, 2002; Nilsson et al., 2005; Gallardo et al., 2016). Consequently, to be necessary to estimate relative abundance or species composition, fresh waters are among the most threatened habitats at the global whereas larger sampling efforts are needed to accurately estimate spe- scale (Malmqvist and Rundle, 2002; Vörösmarty et al., 2010). Accurate cies richness (Dauwalter and Pert, 2003) and species abundance should assessments of the ecological status of these water resources are crucial be more proportional to sampling size. The WFD states that methods for environmental managers and to assist policy-makers in designing used for the monitoring of fish and other type parameters should con- appropriate regulations (Boulton, 1999; Carballo et al., 2009). Such en- form to the standards developed by the European Committee for Stan- vironmental assessments are often undertaken by using Indexes of Biot- dardization (CEN) or other national or international standards, which ic Integrity (IBIs), which can be based on a variety of biological ensure the provision of data of an equivalent scientific quality and com- communities from the aquatic ecosystem, such as macrophytes, benthic parability EC (European Commission) (2014)). For fish in particular, the invertebrates, diatoms or fish (Karr, 1991; Hering et al., 2006). Fish are EN 14962 European Standard (CEN, European Committee for Standard- an excellent taxonomic group to estimate ecological integrity in rivers ization, 2006) recommends electrofishing as one of the most suitable (Schiemer, 2000), as they are very sensitive to common anthropogenic methods for sampling in habitats b2 m deep of all kind of rivers. The disturbances including hydrologic alteration, habitat degradation, loss EN 14011 European Standard (CEN, European Committee for Standard- of water quality or land-use change (Casatti et al., 2009; Aparicio ization, 2003) provides detailed requirements on electrofishing, includ- et al., 2011). Fish have long lifespans and generation times and large ing that: i) for assessing species composition, abundance and age home ranges compared to most other aquatic taxa, making them structure in rivers, in general a river length of at least 20 times the more appropriate to detect disturbances at large spatial and temporal river width should be sampled; and ii) for large rivers (b30 m wide), scales, e.g. old disruptive events (Karr, 1981; Simon, 1999). where it is already known that the fish community is uniform, a length In the European Union (EU), the Water Framework Directive (WFD) of 10 times the river width may be sufficient. regulates the management of water resources and requires the Member These CEN guidelines on sampling effort have not been systematical- States to assess the ecological status of their water bodies (EC, European ly followed in Spain and elsewhere, with surveys often by wading from Commission, 2000; Schmutz et al., 2007). The WFD requires the use of the river bank during low flows and with river lengths much shorter fish among other taxonomic groups for these assessments (Hering than required by the EN 14011 standard. The effects of electrofishing ef- et al., 2006; Carballo et al., 2009; Vidal-Abarca et al., 2016). A recent re- fort in large European rivers have been barely examined (Flotemersch view of aquatic bioassessment methods in Europe showed that their re- et al., 2011) and the applicability of EFI+ and other indices in large sponse with anthropogenic pressures is less tight in rivers than in other Mediterranean rivers is largely unknown. The objectives of our study systems such as lakes or coastal waters and also weaker with fish than are: i) to evaluate the effects of sampling effort (transect length) on other taxonomic groups (Birk et al., 2012). One of the landmarks in the fish metrics, such as species richness and EFI+; and ii) to test the development of a fish-based IBI was the European Fish Index (EFI whether sampling effort affects the results of EFI+ and another regional hereafter), consisting of a multi-metric predictive model based on the fish index (IBICAT2b) in a given site. We hypothesized that: i) as cus- deviation between observed and predicted reference conditions for tomary, species richness would increase with sampling effort, but less the fish assemblages (Pont et al., 2006, 2007). A new version of this than in many other regions since local fish species richness is low in index, the EFI+, was later developed to overcome several limitations the Iberian Peninsula; and ii) IBIs such as EFI+ and IBICAT2b would (e.g. low applicability to different eco-regions within Europe, better de- be less affected than species richness by sampling effort, because they tection of anthropogenic disturbances) and thus, to provide a method also rely on other metrics (species composition and size structure). applicable across nearly the whole range of European rivers (EFI+ Consortium, 2009; Logez and Pont, 2011). However, the applicability 2. Materials and methods of EFI+ in lowland reaches of large rivers is uncertain, as few reference sites under these environmental conditions were available for the de- 2.1. Study area velopment of predictive models (De Leeuw et al., 2007; EFI+ Consortium, 2009). Because the EFI+ was developed at the European The Ebro River (NE Spain) is the second largest