MARINE ECOLOGY PROGRESS SERIES Vol. 307: 247–257, 2006 Published January 24 Mar Ecol Prog Ser Tactics and demographic attributes in the European eel Anguilla anguilla in the Gironde watershed, SW France F. Daverat1,*, J. Tomás2 1Cemagref, 50 Avenue de Verdun, 33612 Cestas, France 2IMEDEA, CSIC-UIB, Miquel Marquès 21, 07190 Esporles, Balearic Islands, Spain ABSTRACT: The patterns of habitat use and their relative proportions were investigated for 270 eels Anguilla anguilla sampled in coastal areas, the estuary and the river of the Gironde watershed, by measuring Sr and Ca concentrations in the otolith. Sr:Ca values outside the elver mark discriminated residence in the same habitat until capture (freshwater, estuary, or sea) from a switch of habitat following 3 patterns: a shift from freshwater to estuarine, seasonal movements within the limits of the estuary, or a switch of habitat from brackish to freshwater (downstream nomads). Results show a gradient of residency from freshwater (100%) to estuary (44%) to the sea (24%). The most abundant (30%) alternative to residence in an estuary and its adjacent coastal site were the downstream nomads, which concentrated in coastal areas and the lower part of the estuary after leaving freshwater. Overall, up to 50% of the eels analysed had spent a period in freshwater. Fish growth rates in freshwater were lower than anywhere else in the watershed. Back-calculation of fish size- at-age showed that, of all eels passing through freshwater, residents were slow growers, while downstream nomads were fast growers. The latter migrate to the estuary at Ages 2+ and 3+, when their size is greater than estuarine residents. Results revealed that lower estuarine and marine habi- tats are colonised by yellow rather than glass eels. This suggests that competition with estuarine residents and downstream nomads prevents precocious settlement of glass eels in estuary and marine habitats. KEY WORDS: Anguilla anguilla · Catadromy · Otolith · Sr:Ca · Life-history pattern Resale or republication not permitted without written consent of the publisher INTRODUCTION The European eel Anguilla anguilla is a catadro- mous fish that spawns in the Sargasso Sea. The lar- Diadromous fish populations display a high level of vae drift with the Gulf Stream and North Atlantic life-cycle plasticity, and their populations are often Current to the continental shelf of Europe and North composed of fractions with different life histories. Par- Africa, where they metamorphose into glass eels tial migration, the phenomenon by which populations (Tesch 2003). They become pigmented elvers as are composed of migratory and resident components, they penetrate estuaries, rivers and streams, and has been investigated for a large number of salmonid complete their growth phase in a large range of habi- and other anadromous species (Jonsson & Jonsson tats (lagoons, estuaries, marshes, rivers, lakes and 1993). In the same manner, for catadromous species, streams). The growth phase lasts from 3 to 15 yr or the partition of population into ecophenotypes with more and is followed by a second metamorphosis alternative life strategies has been described mainly into silver eel. Silver eels achieve sexual maturity as for temperate eels (Tsukamoto & Arai 2001, Tzeng et they swim back to their spawning grounds in the al. 2002). Sargasso Sea. *Email: [email protected] © Inter-Research 2006 · www.int-res.com 248 Mar Ecol Prog Ser 307: 247–257, 2006 Many studies based on otolith microchemistry have The first objective of this study was to describe the hypothesised that, among a single eel population, dif- diversity of life histories of the European eels Anguilla ferent life-history tactics coexist, related to the choice anguilla encountered in the Gironde watershed and to of habitat (marine, brackish, freshwater) or a shift of calculate their relative proportions in the compart- habitat (Tzeng et al. 2000a, 2002, 2003, Tsukamoto & ments of the river basin (coastal compartment, estuar- Arai 2001, Jessop et al. 2002, Limburg et al. 2003, Mor- ine compartment and river compartment) using otolith rison et al. 2003, Arai et al. 2004, Daverat et al. 2005, microchemistry. The second objective was to evaluate Kotake et al. 2005). However, most studies are qualita- the differences in demographic attributes (age, sex, tive and only describe the occurrence of a certain tac- size, growth rate) between life-history types. Finally, tic; they do not always evaluate the proportion of the we investigated the mechanisms of segregation of pat- river basin population involved. terns of habitat use by comparing the back-calculated The partitioning of divergent life histories is amaz- size-at-age for the different groups. ingly consistent for 5 species of temperate eels: Anguilla anguilla in the Baltic Sea (Tzeng et al. 2000b), A. rostrata (Jessop et al. 2002, Morrison et al. 2003), MATERIALS AND METHODS A. japonica (Tsukamoto & Arai 2001, Tzeng et al. 2002) and the New Zealand eels A. diffenbachii and A. aus- Study site. Coastal sites: The Arcachon Bay is a large tralis (Arai et al. 2004). This partitioning reflects the bay (Fig. 1), with a wide opening to the Atlantic Ocean, separation of populations into riverine-, estuarine- and characterised by eel grass Zostera marina and Z. nana marine-resident fractions and a group of eels often meadows, where the salinity ranges between 25 and called ‘migrants’, ‘transients’, or ‘nomads’ (Tsukamoto 35 psu. The Pertuis (Fig. 1) constitutes a large shallow & Arai 2001, Daverat et al. 2005) that move from one coastal zone, that receives the influence of Gironde compartment to another once or more during their estuary panache as well as the runoff of other smaller growth phase. rivers. Islands (the main ones being Oleron and Re), A higher growth rate in a more productive environ- which provide shelter for eels, support an intensive ment is probably the main advantage of estuarine and oyster culture. The salinity in this zone varies between coastal residence (Morrison & Secor 2003). On the other 20 and 35 psu. hand, freshwater residency results in a lower mortality rate compared to marine environments (Jonsson & Jon- sson 1993). It is probable that the choice of a tactic would result in a specific demographic attribute (size-at-age, size-at-migration). However, comparison of the growth rates of migratory contingents are contradictory. Morri- son et al. (2003) showed that Anguilla rostrata estuarine residents and ‘freshwater to estuary mode’ nomads have similar growth rates, which are higher than those of freshwater residents, whereas Tzeng et al. (2002) only found significantly different growth rates between sim- ilar ecophenotypes of A. japonica for the first 5 yr of life, using retrospective growth analysis. A recent study by Kotake et al. (2005) pointed out that eels, which were collected in a Japanese bay, with different types of habi- tat use (estuarine, marine and freshwater eels) emigrate as female silver eels at the same size. The adoption of a tactic of habitat use may be influ- enced by environmental conditions, as well as by the individual’s status. Results obtained for salmonids emphasise the influence of the individual status, often associated with size at a given age (Thieriault & Dod- Atlantic Ocean son 2003). For eels moving from one compartment to another, fast growth, or larger size-at-age may favour migration. A recent finding on thyroid status related to migratory behaviour of glass eels (Edeline et al. 2004) Fig. 1. Map of the study site showing the Gironde–Garonne– suggested that physiological stress leads to precocious Dordogne watershed, the Pertuis coastal area and the Bay of settlement of eels in the estuary. Arcachon Daverat & Tomás: Tactics and demographics of Anguilla anguilla 249 Estuarine sites: The Gironde estuary (Fig. 1), the were manipulated and sacrificed according to ethics largest European estuary, is 76 km long. It varies in legislation and to minimise suffering (Anonymous width from 2 to 11 km at its widest part. Its surface area 1998). is approximately 625 km2 at high tide. The bottom of Estimation of eel maturity. A new method using the estuary is mainly a mixture of sand and mud, with external measures of morphometry (Durif et al. 2005) the sandiest part in the lower sectors and the muddiest was used to estimate the maturity of the eels, based on part in the upper sectors (Castaing 1981, Sottolichio measures of fish weight, total length, pectoral fin 1999). In the Gironde estuary, the salinity gradient length and eye diameter. These external measures varies upstream between 33 and 0 psu and changes were found to vary with hormone levels and gonado- with tide and season (Castaing 1981, Sottolichio 1999). somatic index as fish maturation progressed. In this The limit of the estuary is defined with the 0 psu salin- system of classification, maturation is described by ity front. 5 levels from Stage I (yellow eels) to Stage V (silver Riverine sites: Fish were sampled in the Garonne eels). and Dordogne Rivers, both in the tidally influenced Chemical analyses of the otolith. Sagittal otoliths part of the river (also called the tidal freshwater estu- were extracted, rinsed 3 times with Milli-Q water, ary) and in the river without tidal influence down- dried and stored until they were embedded in epoxy stream of the first dams. resin. Otoliths were ground in the sagittal plane to Field sampling. A total of 270 eels were collected expose the core (Fig. 2), polished using 1 μm diamond in the different salinity zones of the study site during paste and coated with a 3 nm layer of gold. A Cameca every season of 2001, 2002, 2003 and 2004. Two SX 100 Wavelength Dispersive X-ray Spectrometry types of fishing gear were used in this study: eels (WDS) instrument was used to analyse Sr and Ca in from the river (n = 63) and Arcachon Bay (n = 20) otoliths.