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ICES CM 2012/G:17

Temporal trends in the trophic guild composition in fish communities: development of indicators to support the Marine Strategy Framework Directive.

Paula S. Haynes1*, Simon P.R. Greenstreet2, Deirdre Brophy1, David G. Reid3, and Samuel Shephard1.

1 Marine and Freshwater Research Centre, Department of Life Sciences, Galway-Mayo Institute of Technology, Dublin Road, Galway, Ireland 2 Marine Scotland-Science, Marine Laboratory, Aberdeen AB11 9DB, UK. 3 Marine Institute, Rinville, Oranmore, Co. Galway, Ireland

* Corresponding Author: Paula S. Haynes. Tel: 00353 85 7333058; email: [email protected]

Introduction

Fishing can change the structure of marine food webs, impairing functioning, with the removal of high target changing fish and composition at lower trophic levels (Pauly et al., 1998). The Marine Strategy Framework Directive (MSFD) requires indicators of “Abundance trends of functionally important selected groups/species” to identify Good Environmental Status, with the large fish indicator (LFI) subsequently developed to measure the proportion by weight of fish above a specified length threshold (Greenstreet et al., 2011; Shephard et al., 2011). However, this indicator measures changes in the size composition of fish communities, and not changes in the proportion of top predators. While changes in trophic composition are indicated by changes in size composition, as body size is generally related to trophic position in marine food webs, this may not always be the case. For example, in the North Sea, a decline in the size composition of fish communities did not coincide with a decline in the trophic composition; large bodied high trophic level predators were replaced by smaller bodied predators feeding at the same trophic level (Jennings et al., 2002). Hence, ecological indicators under the MSFD need to be developed which consider all components of the fish , and not simply those occupying higher trophic levels.

While previous studies have assigned fish species in a community to their respective trophic guilds based on dietary data (Greenstreet et al., 1997; Heath, 2005), size- related shifts in the diet were not considered. Fish may occupy several trophic guilds throughout their life time. Assigning species to trophic guilds only on the basis of mature- sized fish diet ignored the fact that the diets of smaller sized individuals of the same species might differ markedly, to the extent that smaller fish might be feeding at a lower trophic level or performing a different trophic function within the food web. Furthermore, by not considering fish size, the proportion of in a community may be overestimated, and the proportion of and benthivores underestimated. Accounting for size is particularly important given that there has been a global shift in fisheries landings from large piscivores to smaller planktivorous fish (Pauly et al., 1998).

The objectives of the present research were to establish a trophic guilds “look-up” table for all Northeast Atlantic fish species of every possible length, incorporating size related shifts in diet into this table, and to assess using a trophic guilds indicator as a proxy for the identification of underlying food web changes, by examining trends in the structure of trophic levels over time.

ICES CM 2012/G:17

Methods

Following an extensive review of fish feeding literature, a look-up table was constructed, in which all size classes of all species sampled by the UK West Coast Ground Fish Survey (WCGFS) in the Celtic Sea (ICES area VIIg) were assigned to, using the same four broad trophic guilds as Greenstreet et al., (1997): Pelagic planktivores, pelagic piscivores, demersal benthivores and demersal piscivores. Ontogenetic shifts in diet were accounted for, by allowing allocation to guild to change with increasing size (length), so that individuals of a particular species might be assigned to several different trophic guilds. Time series of the proportion (by ) of the sampled community representing each guild were calculated.

Results/discussion

The first three fish species of the trophic guilds look-up table are presented in Table 1. The proportion of fish by trophic guild for the Celtic Sea fish community is presented in Figure 1, where the biomass typically fluctuated annually, without any clear trend. This pattern contrasts with previously observed declines in indices of fish community size structure derived from the same data, using the LFI (Shephard et al. 2011). The LFI, found an overall reduction in the proportion of large fish (> 50cm) in the Celtic Sea. This reduction in size was not reflected by a change in the trophic guild composition of the fish community, suggesting some resilience in the trophic structure of the system. This suggests that compensatory mechanisms such as species substitutions occurred, whereby the overall abundance of functional groups remained stable, despite significant shifts in the structure and abundance of highly exploited fish species. Indicators of trophic structure might therefore be used as a proxy for the identification of underlying food web changes, prior to investigations on ecosystem . From a management perspective, it is essential to implement policies that recognise the importance of functional roles in an ecosystem, in order to try and prevent any future negative ecosystem changes.

Table 1: Trophic guilds to which Northeast Atlantic fish species were assigned based on ontogenetic switches in diet. Common name Scientific name Length (cm) below Trophic guild Angler fish Lophius piscatorius 0-5 Pelagic 6-29 Demersal benthivore 30-150 Demersal Atlantic wolfish Anarhichas lupus 1-4 Pelagic planktivore 5-150 Demersal benthivore Ballan wrasse Labrus bergylta 0-1 Pelagic planktivore 2-65 Demersal benthivore

ICES CM 2012/G:17

Figure 1: Proportion of fish by trophic guild for the Celtic Sea fish community.

References

Greenstreet, S.P.R., Bryant, A.D., Broekhuizen, N., Hall, S.J., and Heath, M.R. 1997. Seasonal variation in the consumption of food by fish in the North Sea and implications for food web dynamics. ICES Journal of Marine Science. 54 (2): 243-266. Greenstreet, S.P.R., Rogers, S.I., Rice, J.C., Piet, G.J., Guirey, E.J., Fraser, H.M., and Fryer, R.J. 2011. Development of the EcoQO for fish communities in the North Sea. ICES Journal of Marine Science. 68: 1–11. Heath, M.R. 2005. Changes in the structure and function of the North Sea fish foodweb, 1973-2000, and the impacts of fishing and climate. ICES Journal of Marine Science. 62 (5): 847-868. Heath, M.R., Rasmussen, J., Bailey, M.C., Dunn, J., Fraser, J., Gallego, A., Hay, S.J., Inglis, M., and Robinson, S. 2012. Larval mortality rates and of lesser sandeel (Ammodytes marinus) in the northwestern North Sea. Journal of Marine Systems. 93: 47-57. Jennings S., Greenstreet S.P.R., Hill L., Piet G.J., Pinnegar J.K., and Warr K.J. 2002. Long- term trends in the trophic structure of the North Sea fish community: evidence from stable isotope analysis, size-spectra and community metrics. Marine Biology. 141: 1085-1097. Shephard, S., Reid, D.G., Greenstreet, S.P.R. 2011. Interpreting the large fish indicator for the Celtic Sea. ICES Journal of Marine Science. 68 (9): 1963-1972. Pauly, D., Christensen, V., Dalsgaard, J., Froese, R. and Torres, F. Jr. 1998. Fishing down marine food webs. Science. 279: 860–863.