sign in sign up
<<
Home , Fish

Not to be cited without prior reference to the Authors

ICES CM 2007/D:19

Fishing effects on fish diversity in different environmental scenarios: a comparison of case-studies in Scottish, French and Italian waters

Catherine S. Longo, Marie-Joëlle Rochet, Francesco Colloca, Graham J. Pierce, Fabrizio Serena, and Simon P. R. Greenstreet

1. The protection of species diversity has been recognised as a priority for sustainable management in international agreements (e.g. the EU CFP, 2003). Nevertheless, an appropriate indicator of the impact of on fish species diversity is still lacking. The way that fish assemblages respond to fishing exploitation in terms of diversity remains poorly understood – available studies show contradictory or inconclusive results. 2. Since many processes in marine communities are known to be size-based, including fishing effects and predation, we argue that an appropriate metric to detect fish species diversity changes should also be size-based. 3. Therefore we subdivided trawl survey data on communities into large (predator) and small (prey) size categories. We compared how large versus small fish diversity changed moving from less to more exploited areas. 4. As a working hypothesis we tested whether these changes could be explained as the effect of fishing-driven changes in trophic dynamics. 5. However, the nature of the size-based mechanisms mentioned above depends on the system considered. To understand how local factors affect the relationship between fishing disturbance and fish species diversity, we present a comparative study of 3 different European systems: the North-western North , the Bay of Biscay and the Tyrrhenian Sea. 6. Our analysis shows that fisheries induce different types of responses in large versus small fish diversity (species evenness). 7. The type of response varied between systems, but the direction of change could be only in part explained by means of trophic dynamics. Therefore, a model taking into account more variables to characterise the system is required. For example, especially when the spatial of the study is small, local characteristics such as habitat heterogeneity may be more relevant size-structuring drivers than fishing disturbance.

Keywords: ; demersal fish; fisheries; trophic interactions; Tyrrhenian Sea; Bay of Biscay; .

Contact author: Catherine S. Longo, Laboratoire d’Ecologie et Modèles pour l’halieutique (EMH), Rue de l’Ile d’Yeu, IFREMER, BP 21105, 44311, Nantes CEDEX 03, France [e-mail: [email protected]; [email protected] ].

Introduction

The protection of species diversity has been recognised as a priority for sustainable fisheries management in international agreements (e.g. the EU CFP, 2003). Nevertheless, an appropriate indicator of the impact of fishing on fish species diversity is still lacking. The main issues raised against the use of this type of indicators in the published reviews (ICES 2001; Rice & Rochet 2005; Link 2005) can be summarised as: - lack of an unambiguous relationship between cause (fishing) and effect - lack of predictability of the direction of change in diversity induced by fishing (increase? decline?) (e.g. Bianchi et al, 2000) These criticisms are symptomatic of gaps in the understanding of the mechanisms underlying the fishing disturbance-fish species diversity relationship. Many aspects of the functioning of marine communities are size-structured such as trophic dynamics and life-history traits. Often the ecological effects of fishing are size-structured as well (e.g. Kerr & Dickie, 2001). We suggest that where fisheries produce size-based effects on fish communities, and thus affect the communities’ trophic dynamics, also size-structured changes in fish diversity should be expected. Here we tested the hypothesis that different sizes respond differently to fishing pressure and thus undergo different changes in species diversity. To this end we compared the species diversity in demersal fish communities sampled during trawl surveys from heavily fished and less fished areas, separating the fish into large and small size categories. We constructed some working hypotheses to predict the size-based patterns, founded in theoretical knowledge on the relationship of fisheries with trophic dynamics (Pauly et al, 1998) and on that of trophic dynamics with species diversity (Huston, 1994). Many studies in the published literature have suggested that, in those areas where intense fishing has sensibly reduced large fish abundance, an indirect effect has been the increase of the smaller fish they prey upon (e.g. Daan et al. 2005). If fishing induces a predatory release effect in small fish, according to niche theory the most competitive species will expand at the expense of others, becoming more dominant (Huston, 1994). If this occurs, species evenness (i.e. the relative proportion of individuals among species) of small fish should be found to decline as an indirect effect of fishing. In large fish, that represent often the main target of fisheries, we assume here that the direct impact of fishing will mask any other potential indirect effects, such as changes in trophic dynamics (Rice & Kronlund, 1997). Therefore, in this case, we do not expect to observe any change in species evenness. To test these assumptions the demersal fish community was devided into size groups as follows: a ‘large’ fish group composed by the predator size range of the fish community and a ‘small’ fish group composed by the size range they are expected to prey upon, based on prey- predator size ratios available in the literature (Frœse & Pauly, 1998; Jennings et al., 2001). The increase/decline in and species evenness of ‘small’ and of ‘large’ fish found in the more exploited areas was compared against expected results described above. This trophodynamic explanation can apply to those systems where fisheries are strongly size- selective (so that small sized fish escape the fishermen and increase when their predators decline) and where the predation of large fish upon small fish is ecologically significant (so that the decline of large fish in a heavily exploited state determines a significant alteration in the predator-prey dynamics). On the other hand, in areas where fishing disturbance affects directly most fish sizes and where the percentage of piscivorous fish is low, no cascade effects should be observed. Based on this, size-structured effects of fisheries on diversity should vary depending on the degree of piscivory within the fish community and on the degree of size- selectivity of fisheries in the ecosystem considered. Therefore, to appreciate the role played by the system’s characteristics in determining the observed patterns, we repeated the hypothesis testing in areas located in 3 different European eco-regions: the North-western North Sea, the Bay of Biscay and the Tyrrhenian Sea.

Methods

Hypotheses testing design: We assume that, in heavily fished areas, there is a fisheries-mediated predatory release effect. In those areas where fisheries are size-selective, the consequences of this effect should be the declining biomass of large fish (the ‘predators’) and an increased biomass of small fish (their ‘prey’) (e.g. Daan et al 2005). We test here that this predatory release entails size-based changes in species evenness. In particular, we assume fish species evenness, in a heavily fished state, to change as follows: • in an eco-region where fisheries are size-selective and piscivory is ecologically relevant: a. small fish evenness declines b. large fish evenness shows no trend • in an eco-region where fisheries are not size-selective and piscivory is not ecologically relevant: a. small fish evenness shows no trend b. large fish evenness shows no trend To perform this test, in each eco-region selected, we 1. compared the demersal fish community in a heavily fished and a less fished state. To do so, within the area sampled by trawl surveys, we selected sub-areas that were as similar as possible in terms of habitat but differed in fishing effort intensity. 2. defined the size-categories to be analysed: To test for a predatory release effect we estimated the size-range of the fish predators that are removed by fisheries. Then, under the assumption of an opportunistic size-based (Jennings et al., 2002), we estimated the size range of fish that these predators would generally prey upon. If the ‘prey’ size-range is too small to be caught by fishermen, these will be the individuals we expect to undergo predatory release effects (Fig.1). To establish expected results for each eco-region, we 3. defined the eco-regions on a scale of “size-selectivity” of the fishing strategy, based on the legal minimum landing sizes relative to the size frequency distribution of the community. 4. determined the ”ecological relevance of piscivory” within the demersal community comparing the relative proportion of to the total biomass of the fish assemblage, but also referring to diet information in the published literature. The categories to which each case-study was assigned are shown in Tab.1. For further details on methods used see Anon. (2007a), Anon. (2007b).

The hypothesis testing within each case-study is based on the assumption that the most ecologically relevant parameter that differs between areas compared is fishing intensity. However, locating two equivalent areas in terms of habitat, but with very different levels of fishing exploitation is problematic because there is generally a high collinearity between fishing intensity and habitat type. Furthermore, wether two habitats are “sufficiently similar”, i.e. their characteristics do not differ to the extent of determining a significant difference in species diversity, is something difficult to accurately quantify. For further details on the methods applied see, respectively, for the Scottish study: Anon. (2007a), for the French: Longo & Rochet (in prep.), for the Italian: Anon. (2007b).

The data-sets: Data for demersal fish was collected during standardised monitoring surveys. Respectively the surveys were: Scotland – Scottish August Ground-fish Survey (SAGFS), covering 75 ICES within the north- western North Sea, between 1984 and 1996, performed by the Scottish FRS (see Greenstreet & Rogers, 2006 and references therein) . France – EVHOE Survey in the Grande Vasiere area of the Bay of Biscay, between 1997 and 2006, performed by IFREMER (ICES, 1991). Italy – MEDITS Survey in the Central and Tyrrhenian Sea (GSU 9) from 1996 to 2004, between 1996 and 2005, performed on behalf of the Italian Ministry of Forestry and Agriculture by the Operational Units (U.O.) “Lazio” and “Toscana Nord” (Bertrand et al., 1997). Within each survey, only hauls of the same duration were included. To avoid sampling bias due to differential catchability of species with a distinctly pelagic behaviour (e.g. Clupeids), these were excluded from the analyses. Fishing effort: As trawling represents the heaviest (Jennings and Kaiser, 1998) and most widespread impact on demersal communities in the studied areas (Jennings et al., 1999; Léauté, 1998; Tudela, 2004), information on this gear was used as proxy for fishing intensity. The spatial distribution of fisheries exploitation was used to assign areas to either ‘Low’ or ‘High’ fishing effort. Data was obtained respectively as follows: Scotland – International fishing effort data (hours fished), for the years 1990-5, was averaged for each ICES rectangle based on Jennings et al., (1999). ‘Low’ effort areas corresponded to rectangles with < 5000 h·y-1 of trawling. France – aereal survey observations from 1989-1994 (Léauté, 1998) allowed to map the spatial distribution of individual trawlers. The areas were considered to be with ‘low’ fishing effort in areas where boat density corresponded to < 20 boats per cell in a 0.25° x 0.25° grid (~ 550 Km2). Italy – a fishing effort map based on a model using fleet vessel power, base-port distance and fishermen habits was used to define the least exploited zones of the area (Corsi 1998). Biomass estimates: Fish size during the surveys was recorded by measuring individual fish length. These values were converted to weight (in grams) through weight at length relationships, available from the literature (Froese & Pauly, 2007; Jennings et al. 2001 and references therein), to obtain total biomass estimates per weight range. Species diversity estimates: Species ‘diversity’ is understood here a generic term applied to either of the components of biodiversity at the species level (such as species richness or evenness), ‘richness’ as the number of species, whereas ‘evenness’ is the diversity component measured by the distribution of individuals among species. To measure species evenness we used Pielou’s evenness index, calculated as: H’/ lnN, where N is the number of individuals, H’ is Shannon’s diversity index ( - Σ(pi* ln pi)), pi is the relative proportion of species ‘i’ ( Σpi =1)), using the Primer software (Clarke & Worwick, 1994). This index was selected because our explorations have shown that it is more robust to sample-size and sensitive to species dominance compared with other indices such as Simpson’s or some of the Hill series (Hill, 1973). Data aggregation: in each eco-region studied, to obtain a representative sample of each area type (‘low’ or ‘high’ effort), randomly selected hauls were aggregated in groups of 10 and pooled. Previosuly published work (Daan, 2001; Merigot et al., 2007) suggests that a compromise must be saught between a sufficiently large sample size and not aggregating so many hauls that new variability due to spatial heterogeneity is incorporated. Based on our explorations, 10 hauls were a compromise that could be applied to the data from all the case- studies. Statistical tests: Within each of the eco-regions studied, ANOVA tests were run separately for small and for large fish comparing biomass and species evenness, with fishing intensity level as a factor. Fishing pressure was considered to affect biomass/diversity significantly if a difference was found at the 5% confidence level. The analyses were performed using the R software (www.r-project.com).

Results and Discussion

The box-plots shown in Fig. 2, give a visual overview of the differences observed with the ANOVA tests on species evenness. For ‘small fish’ (between 8-64 g), the tests indicated a significant difference in species evenness between heavily and less exploited areas in the Italian case and in the Scottish case. For ‘large fish’ (between 256 – 4096 g) the differences were not significant in any of the cases. Tab.1 shows the direction of change that resulted significant at the 5% confidence level. Of the two northern European case-studies (Scotland, France), where fisheries is size- selective and piscivory is expected to be ecologically relevant (so much so that predation among fish is included in predictive models used for stock assessment, such as MSVPA), one area (the Scottish Sea) has shown a decline in small fish species evenness in more exploited zones, in accordance with our hypothesis, while the other (the Bay of Biscay) has shown no significant change. The latter case-study however did not show any sinificant difference in the size structure of the community between the less exploited and the more exploited zone (results not shown here). If no significant change in the predator abundance is found (the “large” size group), there is no reason to expect a predatory release to occur. Further explorations (Longo & Rochet, in prep.) have indicated that the patterns in the ‘small’ fish category are likely to be the result of differences in depth, which may be more significant than fishing in a small sized area of study. Therefore further parameters, such as spatial scale, should be taken into account when modelling the fishing disturbance-fish diversity relationship. In the Central Mediterranean, species evenness was found to be higher in the less exploited area. This result is similar to the one obtained in the Scottish case-study. Nevertheless, in the Mediterranean, piscivory of demersal fishes upon demersal prey is assumed to be hardly relevant (for detailed diet composition of the assemblage in the area see Colloca, 2003) and fisheries are scarcely selective (Tudela, 2004), thus affecting directly also these smaller size categories. It doesn’t seem likely that the same explanation can apply also to this case. Drivers other than trophic dynamics, such as habitat heterogeneity, could be responsible for this result. As observed in the French case-study, the small spatial scale may determine habitat charactreristics to be more strongly structuring factors than fishing or predation. Species evenness of larger fish did not show any significant change in any of the regions. This suggests that fishing effects are so strong that they mask any ecological dynamics (Rice & Kronlund, 1997). It may also be the indication that trawl samples are insufficient to provide sensitive measures. In fact large fish, because they are less abundant than small fish, are difficult to sample and sample-sizes become even smaller in exploited areas. Differences in species evenness may be too slight to capture with such low sampling power (see also Jennings & Dulvy, 2005). (For an overview of results see Fig.1).

Conclusions

Overall the comparison of different areas confirmed that changes in fish species diversity associated to fishing intensity can be found if diversity metrics are applied separately to “large” and “small” fish size ranges. Since studies often fail to detect such differences when applying diversity indices on the whole demersal assemblage, this may provide a more sensitive method of measuring community level fishing effects. We attempted to also provide some insight on the mechanisms involved, by defining such size ranges according to and fishing selectivity. For small fish, although patterns suggesting an indirect effects of fishing on species evenness were found in Scotland, trophic dynamics could not explain the changes observed in the other cases, suggesting that other drivers, such as fine-scale habitat heterogeneity, should also be considered to model the fishing disturbance-fish diversity relationship, at least for studies on a relatively small spatial scale. For large fish it appears that either fishing direct effects are so strong that no other processes play a relevant part in determining their ecological equilibria, or these other processes occur on a scale that is invisible given trawl survey sampling power. The parsimonious representation of the interaction between fisheries and fish diversity presented here is obviously oversimplified, however it serves the purpose of disentangling the different processes involved through an hypothesis testing method.

Fig.1. Hypothesis testing design. The size-structure of the fish community, here represented through the distribution of normalised biomass across individual fish body size (i.e. biomass size spectrum (Platt & Denman, 1977)), was subdivided for the hypothesis testing as follows: 1. the range of the fish community that is fished by trawlers (> the “minimum fished size”), 2. the portion of the fished community that preys on other fish (”piscivores”), 3. the overlapping of these two categories (“fished piscivores”) and 4. the portion that is expected to experience a predatory release effect (“prey”) in case of intense harvesting of the predators. In the text they are referred to as: “fished piscivores” = ‘Large fish’; “prey” = ‘Small fish’.

Tab. 1. Overview of changes in fish biomass and diversity going from less to more exploited areas, in each of the 3 case-studies. Arrows indicate significant differences found at the 5% level with an ANOVA test. “B” = biomass; “J’” = species evenness (Pielou’s index); “↓”= decline; “↑”= increase; “=” = no change.

System SMALL FISH LARGE FISH System characteristics B J’ B J’ Fishing Piscivory strategy Scotland Size-selective High relevant = France Size-selective High relevant = = Italy Non size- Low Not selective relevant =

a)

J’

b)

J’

Fig.2. Boxplots of demersal fish species evenness values in highly exploited (HI) and less exploited (LO) areas of French, Italian and Scottish waters. a) ‘Small fish’ = fish of 8-34 g; b) ‘Large fish’ = fish of 512- 8192 g.

References:

Anon. 2007a, ICES Working Group on Fish Ecology 2007 Report. ICES CM 2007/LRC:03. Anon. 2007b, EU Project BECAUSE Final Report. Project website: http://www1.uni-hamburg.de/BECAUSE/ Bertrand, J., Gil de Sola, L., Papacostantinou, C., Relini, G. and Souplet, A., 1997. An international bottom trawl survey in the Mediterranean: the MEDITS programme. ICES CM 1997/Y:03. Baltimore. USA. Bianchi, G., Gislason, H., Graham, K., Hill, L., Jin, X., Koranteng, K., Manickchand-heileman, S., Paya`, I., Sainsbury, K., Sanchez, F., and Zwanenburg, K. 2000. Impact of fishing on size composition and diversity of demersal fish communities. ICES Journal of Marine Science, 57: 558-571. Clarke, K.R., and Warwick, R.M. 1994. Change in marine communities: an approach to statistical analysis and interpretation. Natural Environment Research Council, UK. Colloca, F. 2003. Struttura e risorse trofiche dell'associazione ittica del margine della piattaforma continentale tirrenica. PhD thesis, University “La Sapienza”, Rome. Corsi, F. 1998. Spatial distribution of fishing effort: Modelisation through deductive modelling. In: COPEMED Workshop on the Use of GIS as an Assistance Tool for Decision Makers in Fisheries Management, Malaga (Spain), 16-19 Dec 1998. Taconet, M. & Bensch, A. (Eds.) Daan, N. 2001. A spatial and temporal diversity index taking into account species rarity, with an application to the North Sea. ICES CM 2001/T:04 Daan, N., Gislason, H., Pope, J.G. & Rice, J.C. 2005. Changes in the North Sea fish community: evidence of indirect effects of fishing? ICES Journal of Marine Science, 62: 177-188. Frœse, R., and Pauly, D. (Eds) 1998. FishBase 98: concepts, structure and data sources. International Center for Living Aquatic Management, Manila, Philippines. www..org Greenstreet, S.P.R. and Rogers, S.I. 2006. Indicators of the Health of the Fish Community of the North Sea: Identifying Reference Levels and Setting Objectives for an Ecosystem Approach to Management. ICES Journal of Marine Science, 63(4): 573-593. Hill, M.O. 1973. Diversity and evenness: a unifying notation and its consequences. Ecology 54(2): 427-432 Huston, M.A. 1994. Biological diversity. The coexistence of species on changing landscapes. Cambridge University Press, Cambridge, England. ICES. 1991. Report of the study group on the coordination of bottom trawl surveys in Sub-Areas VI, VII and VIII and Division IXa. ICES CM 1991/G: 13. ICES 2001. Report of the Working Group on Ecosystem Effects of Fishing Activities. ICES CM 2001/ACME: 09. Jennings, S., Alsvlag, J., Cotter, A.J.R., Ehrich, S., Greenstreet, S.P.R., Jarre-Teichmann, A., Mergardt, N., Rijnsdrop, A.D., Smedstad, O. 1999. Fishing effects in the northeast Atlantic shelf : patterns in fishing effort, diversity and community structure. III. International trawling effort in the North Sea: an analysis of spatial and temporal trends. Fisheries Research, 40: 125-134. Jennings, S., Pinnegar, J.K., Polunin, N.V.C., and Boon, T.W. 2001. Weak cross-species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. Journal of Ecology, 70: 934-944. Jennings, S., Warr, K. J., Mackinson, S. 2002. Use of size-based production and stable isotope analyses to predict trophic transfer efficiencies and predator-prey body mass ratios in webs. Marine Ecology Progress Series, 240: 11-20. Jennings, S. & Dulvy, N.K. 2005. Reference points and reference directions for size-based indicators of community structure. ICES Journal of Marine Science, 62: 397-404 Kerr, S.J., and Dickie, L.M. 2001. The biomass spectrum. Columbia University Press, New York, 320 pp. Léauté, J-P. 1998. Les flotilles de pêche de 1’Union Européenne dans le golfe de Gascogne vues du ciel. Oceanologica Acta, 21(2): 371-381. Link, J. 2005. Translating ecosystem indicators into decision criteria. ICES Journal of Marine Science, 62: 569-576. Longo, C. & Rochet, M.-J. 2007. Spectres de diversité par taille: un outil pour comprendre les changements de diversité specifique des poissons? Cas d’étude en Golfe de Gascogne. 9th AFH Symposium - 28-30 June, La Rochelle, France, (paper in prep.) Merigot, B.,Bertrand, J.A.,Mazouni, N.,Manté, C.,Durbec, J-P.,Gaertner, J-C. 2007. A multicomponent analysis of species diversity of groundfish assemblages on the continental shelf of the Gulf of Lions (northwestern Mediterranean Sea). Estuarine, Coastal and Shelf Science, 73: 123-136. Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., and Torres, F. 1998. Fishing down marine food webs. Science, 279: 860-863. Platt, T., & Denman, K. 1977. Organization in the pelagic ecosystem. Helgolander Wissenschaftliche Meeresuntersuchungen, 30: 575-581. Rice, J.C. & Kronlund, A.R. 1997. Community analysis and : diagnostic patterns, processes and inferences. Journal of Sea Research, 37: 301-320. Rice, J. C. & Rochet, M-J. 2005. Do explicit criteria help in selecting indicators for ecosystem-based fisheries management? ICES Journal of Marine Science, 62: 528-539. Tudela, S. 2004. Ecosystem effects of fishing in the Mediterranean: an analysis of the major threats of fishing gear and practices to biodiversity and . Studies and Reviews. General Fisheries Commission for the Mediterranean. No. 74. Rome, FAO. 2004. 44p.