CONCEPTS FOR CHARACTERIZING SPAWNING BIOMASS OF THE ...

Vie et milieu - life and environment, 2007, 57 (4) : 201-211

CONCEPTS FOR CHARACTERIZING SPAWNING BIOMASS OF THE EUROPEAN EEL (ANGUILLA ANGUILLA) IN CATCHMENTS T. ROBINET 1, 2*, A. ACOU 3, P. BOURY 4, E. FEUNTEUN 5 UMR CNRS-MNHN 5178 Biologie des Organismes Marins et Ecosystèmes, Muséum National d’Histoire Naturelle, Ichtyologie, 43 rue Cuvier, 75005 Paris, France 2 Fish Pass, Bureau Expert Gestion Piscicole, 8 allée de Guerlédan, 350135 Chantepie, France 3 ERT 52 Biodiversité Fontionnelle, Université de Rennes 1, Campus de Beaulieu, Av. du Gal Leclerc, France 4 Centre de Recherche sur les Ecosystèmes Littoraux Anthropisés (CRELA), UMR 6217 CNRS-Université de La Rochelle, Bâtiment Curie, Rue Enrico Fermi, 17000 La Rochelle, France 5 UMR CNRS-MNHN 5178 Biologie des Organismes Marins et Ecosystèmes, Laboratoire Maritime et Musée de la Mer de Dinard, 17 Av. Georges V, 35801 Dinard, France * address for correspondence: [email protected] 1

SILVER EELS ESCAPEMENT SPAWNING BIOMASS MORTALITY INDICATORS

Abstract. – Silver eels biomass production is a primary management target to be urgently achieved for starting the restoration of the European eel (Anguilla anguilla) population. An assessment of the proportion of individuals actually escaping from catchments – and able to reproduce – compared to a theoretical pristine production under no human intervention, is of critical importance for preserving this resource, and EU urges Member States to implement such tools now. This preliminary approach, developed during the EU program INDICANG, proposes to clarify some of the basic concepts needed to implement assessment tools for a characterization of the production of spawning biomass in a catchment. These concepts rely mostly on the influence of the catchment context (conditions for the eel growth) on the biomass of future spawners produced, and on the notion of breeding potential (production potential of future spawners, because year-to-year effective downstream migration is unpredictable from the structure of the local eel stock). In order to allow its implementation in data-poor catchments, this assessment does not aim to be fully quantitative, but to give a semi-quantitative estimation of the silver eel potential production. After being reduced by coefficients of anthropogenic mortality (fisheries, hydroelectric turbines, dams and reservoirs), this breeding potential should give a reference value for defining the future management targets and their monitoring. « Review of the available information on the status of the stock and fisheries of the European eel supports the view that the population as a whole has declined in most of the distribution area, that the stock is outside safe biological limits and that current fisheries are not sustainable. Recruitment is at a historical minimum and most recent observations do not indicate recovery. The level observed since 1990 is below 20% of the level observed not more than three generations ago. » (FAO EIFAC/ICES 2006)

Introduction Following the decline reported for the European eel population throughout its whole continental distribution area (Dekker et al. 2003a), the EIFAC/ICES Working Groups on Eel came progressively to the point that the first management target should be the silver stage, i.e. the maturing eels on the onset of their seaward spawning migration (Dekker 2003ab, FAO EIFAC/ICES 2006), designated as future spawners or emigrants. To give a chance for the eel population to restore, EIFAC/ICES experts estimated that a minimum escapement rate of 40 % SPR (Spawners Per Recruit) should be attained. This means that the present SPR of a catchment should represent at least 40% (in biomass) of the pristine SPR, likely to be produced by a catchment without any human

perturbations1. Following these advices, EU urges all the Member States to implement tools for assessing the spawners production and all the mortality causes that can affect the eel local population2 (Council Regulation EC 1100/2007, Council of the European Union 2007). The article 4 (point 4) states that “the objective of each Eel Management Plan shall be to reduce anthropogenic mortalities so as to permit with high probability the escapement to the sea of at least 40 % of the silver eel biomass 1

Without any human perturbations (no human-induced mortal-

ity on any eel stage and natural habitats), and with a pristine recruitment level of glass-eels in the estuary. 2 The term ‘local population’ is used to designate all eels present in the catchment. Of course this is not a true population in the reproductive sense.

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relative to the best estimate of escapement that would have existed if no anthropogenic influences had impacted the stock.” At first sight, this situation looks uncomplicated: in each river catchment (the management unit), managers have to assess the biomass of silver eels that do emigrate to the sea (designated as the escapement), i.e. the biomass of future spawners produced by the catchment minus the natural and man-induced mortality on the silver stage. Behind this easy picture, however, lie insurmountable problems linked to the very singular biology of eels. Actually, because the silver eel migration behaviour is triggered by the local hydroclimatic conditions, year-to-year effective downstream migration in a catchment is simply unpredictable. Therefore, the assessment of the yearly silver eels production can only be done based on the eel stock present in the catchment (Feunteun 2002). On the other hand, EU asks an objective in biomass, and, given the marked sexual dimorphism in eels, the assessment of the yearly silver eel production has to integrate the sexratio of the silver eels produced, based on the local population parameters. Can one sex-ratio be better than another? Since a group behaviour for reproduction has been observed in captivity, it is assumed that one male can fecund several egg clutches (Van Ginneken et al. 2005b in A. anguilla, Dou et al. 2007 in A. japonica), but, even if a sex-ratio dominated by females seems more to favour the breeding potential than a sex-ratio dominated by males, this kind of debate is not serious without any strong population model. For this reason, the only admitted objective to recover the European eel population is to recover a certain level of silver eel production. This paper proposes to clarify some of the basic concepts needed to implement assessment tools for a characterization of the future spawners production: the influence of the catchment context (influencing the eel growth) on the biomass of future spawners produced, and the notion of breeding potential (potential production of future spawners). Then is presented a range of existing methods to assess either the eel breeding potential in a catchment or the real instantaneous production of spawning biomass. Growth and silver metamorphosis After having grown for years in – or nearby – continental freshwaters, the yellow eels, not mature yet, undergo their metamorphosis (silvering) to prepare for the marine migration towards oceanic spawning areas (Pankhurst 1982abc, Pankhurst & Lythgoe 1982, Fontaine 1994). Silvering, named in reference to the pigmentation of the eel skin adapted to marine pelagic life (dark back and silvery belly), is characterized by the appearance of three external marks (Acou et al. 2005, Durif et al. 2005): (1) a contrasted pigmentation between the back usually dark

(increase of dorsal melanin) and the belly usually whitesilver (increase of the ventral purine); (2) a complete lateral line, with visible neuromasts; (3) an ocular hypertrophy, increasing the Pankhurst index (Pankhurst 1982a) up to 8.0 (Pankhurst & Lythgoe 1982). An eel is called a silver eel once these 3 criteria are met. We can add that the pectoral fins are usually oversized and turn silver-golden (Durif et al. 2005), but this is difficult to measure in the field. The silver metamorphosis outstands the end of the growing stage, and is accompanied by a shift of the energy allocation from growth to reproduction, that induces a spectacular maturation of the female gonads. In Anguilla anguilla, the gonad somatic ratio raises from 0.3 in yellow eels to a mean of 1.7 in silver eels (Dufour 1985, Acou et al. 2003, Durif et al. 2005). The ability to spawn, however, is not acquired as long as the eel stays in continental waters, since its gonadotropic function is blocked until the eel reaches the ocean (Kah et al. 1989). Lipid reserves play a major role in migration, because the eel is supposed to stop feeding definitely at silvering, and allocates all of its energy to swim and reproduce. Lipids stored at the onset of the seaward migration should be a priori enough for the eel to cover 5,000-6,000 km without re-feeding (Van Ginneken & Van den Thillart 2000, Van Ginneken et al. 2005a), even if a 6,000 km trip would burn 40-60% of its energy stocks (Van den Thillart et al. 2004). In this diadromous fish, silvering leads to chloride cells (Na+/K+) modifications in gills, comparable to smoltification in salmonids, but more flexible in time, and under cortisol control (Epstein et al. 1971, Fontaine et al. 1995). Up to this day, despite this substantial knowledge on the silvering process, neither internal (age, length) nor environmental factors have been shown to initiate the silver metamorphosis (EELREP 2005). For instance, Vøllestad et al. (1986) hypothesized that water temperature acts as a long-term factor that controls the period of physiological preparation of the migration such as the silver metamorphosis. To date, this hypothesis was not confirmed to our knowledge. Nevertheless, Vøllestad (1992) has examined the geographic variations in biological parameters of silver eels from various sites in Europe and northern Africa, and outlined some relationships between the latitude of the habitat, and the eel size and age at silvering for both sexes: - whatever the latitude of the growth habitat, there is a tight correlation between the mean age at silvering of males and those of females, and the same for the mean size at silvering; - the mean age at silvering is strongly conditioned by the growth rate in both sexes, the latter being related to the latitude; - on the other hand, the mean size (not age) at silvering is not influenced by the growth rate, but possibly by the distance to the spawning area.

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concepts for eel spawning biomass

Therefore, the latitude (distance to the spawning area) of the growth habitat and its position in the watershed (Krueger & Oliveira 1997, 1999) seem to be prime factors that control the timing of silvering. The biological process involved in the adjustment of the residence time in continental waters probably integrates the cumulated mortality rate in continental waters, the distance to the spawning area, and the growth rate in the different available habitats (Chisnall & Hayes 1991, Feunteun et al. 2003, Laffaille et al. 2005). Sex determination and density threshold Studies of A. anguilla karyology found 38 chromosomes (N = 2n) with a ZW sex chromosome system (reviewed in Devlin & Nagahama 2002, Lecomte-Finiger 2003). However, it is admitted that juveniles initially possess a bipotential intersexual gonad that develops directly into an ovary or testis (Colombo & Grandi 1990, 1995, 1996, Beullens et al. 1997). On each side of the Atlantic ocean (A. anguilla and A. rostrata), a high imbalance in sex-ratios has been observed, several consecutive years in the same catchments (Krueger & Oliveira 1999). In such a global panmictic populations (Avise et al. 1986, Van Ginneken & Maes 2005), these observations claim for an environmental sex determination (ESD, Krueger & Oliveira 1999). ESD has been confirmed by several works in the field or in laboratories (Helfman et al. 1987, Holmgren 1996, Holmgren & Mosegaard 1996, Krueger & Oliveira 1997, Costa et al. 2008). An eel density above a certain threshold stresses the elvers (the sexually undifferentiated juvenile eels). This stress extends the sexual non-differentiation period, inducing usually an evolution of the undifferentiated gonads (ovotestis) toward male gonads (testis). This leads to a numerical dominance of males in densely populated habitats. Conversely, a low density of eels (i.e. no stress condition) induces an early development of ovaries, and leads to a numerical dominance of females. For the European eels the growth strategy is fundamentally different between sexes. Males reach a sufficient amount of energetic reserves very early, at 3-5 years (length ≤ 45 cm). They can undertake their sexual maturation early because their fertility is not linked to their length. Females, which must stock lipids for vitellogenesis, have to grow longer, from 4-8 years to sometimes much more according to the growth context (length ≥ 45 cm, Colombo et al. 1984, Acou et al. 2003, Haro 2003, Bevacqua et al. 2006). This difference in growth between sexes induces different growth durations, and therefore different turnovers (or residence times) between catchments producing mostly one sex or another. ESD seems to occur after one year, and before the third year in river (reviewed in Lambert & Rochard 2007). At this age (1.5-4 years including the marine life, LecomteFiniger 1992), as they undergo their ESD, most elvers

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remain in the lower part of the catchment (Apprahamian 1988, Krueger & Oliveira 1999). Thus, the global sex-ratio of a catchment might reflect mainly the eel densities in its lower part, more than those of the whole system (Krueger & Oliveira 1999, Lambert 2005). Because some juveniles can reach the upstream zones right away after their freshwater entrance (Ibbotson et al. 2002, Feunteun et al. 2003), ESD induces a heterogeneous sex-ratio along the river system, with males downstream and females upstream. In the downstream fisheries, silver males are caught earlier in the season than females, probably because, assuming that males and females emigration starts at the same time, males reside closer to the estuary than females (Haro 2003). In the literature appear some relationships between the eel global density and sex-ratio of the outgoing silver eels. The cited works correspond to small catchments, so the presented densities are assumed to affect elvers during their ESD. In rivers with a density of more than 500-1000 eels/ha (Frémur: 3900 eels/ha or 110-170kg/ha, Acou et al. (2007); Esva: 1000-5000 eels/ha or 90-159 kg/ha, Lobòn-Cervia et al. 1995), silver eels produced are majored by males (94.7 % and > 99 % for the Frémur and Esva, respectively), whereas when density is lower than 500 eels/ha (Imsa: 116 eels/ha or 3.5 kg/ha, Vøllestad & Jonsson 1988; Oir: 300 eels/ha or 35-45 kg/ha, Acou et al. 2007a), silver eels produced are mostly females (> 90 % and about 80 % for the Imsa and Oir Rivers, respectively). Because the local density of eel controls the sex-ratio, Vøllestad (1990) recommends to set up yellow eel fisheries on the Imsa River, to decrease the mean local density, and to maximize the biomass produced in silver eels (i.e. females). Moreover, the negative relationship between the female sex-ratio and population density seems to be a common phenomenon among temperate eel species. For A. rostrata, the proportion of females is a linear function of the eel density (% females = 66.91 – 221.14*density, with density expressed in eels/100 m 2, Han & Tzeng 2006). With the supposed threshold values we found in the literature for A. anguilla (previously detailed), 500 eels/ha and 1000 eels/ha would produce a sex-ratio of 0.55 (dominated by females) and 0.45 (dominated by males) respectively, that would corroborate a density threshold of density of c. 500-1000 eels/ha for the sex-ratio determination in European eels. Juveniles, when they arrive in an estuary, can settle therein or swim actively upstream (Legault 1996, Feunteun et al. 2003), but this colonization process can be obstructed. For a given estuarine recruitment, the catchment configuration drives local eel densities: obstacles to upstream migration make the elvers density very high just below them. Then, inexorably, obstacles to upstream migration tend to produce a majority of small silver males (Feunteun et al. 1998, Costa et al. 2008). On the other hand, lakes or large ponds decrease the local density,

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favouring the production of large silver females (Parsons et al. 1977, Oliveira et al. 2001, Laffaille et al. 2006). Eel candidates to emigration It is not possible today to point out precisely which stimuli induce the seaward migration behaviour. However, it is admitted that a massive downstream migration of silver eels is usually associated with specific hydrological factors in the catchment, like floods combined with cold water temperatures (Vøllestad et al. 1994, EELREP 2005), unavoidably themselves linked to some others like air temperature, rainfalls and lunar cycle (reviewed in Tesch 1977, Vøllestad et al. 1986). The massive emigration period is thought to differ with latitude, but this period corresponds, at 45-50° N, to the end of autumn or the beginning of winter (Deelder 1954, 1970, Durif 2003). However, in North Africa, silver eel fisheries also operate from the end of autumn to the end of winter (Feunteun unpubl data). A significant rise in the water temperature can break the migration process, and even reverse the silvering physiological process (EELREP 2005). The downstream migration corresponds to specific water conditions (Haro 2003). If these conditions are not met during autumn and winter, eels candidate to emigration are probably constrained to wait in the catchment for favourable water conditions in the following year. A minority of them can even regress to the yellow stage (Feunteun et al. 2000). Thus, with dry winter conditions, unfavourable for emigration, the quantity of emigrating silver eels does not reflect the real potential of silver eels of the catchment. Furthermore, if the weather alters the prediction of silver eel run, the physical characteristics of the river also play a role. Silver eels can run large distances quickly: several observations relate that tagged silver eels have been recaptured the day after their tagging up to 60 km from the upstream tagging location (on the Loire River, unpubl data from the authors). However, individual tagging experiments showed that a silver eel, if it cannot reach the sea at once, usually migrates about 380 km downstream and then stops downstream migration until the next year (EELREP 2005). Therefore, in the largest rivers, it can take several years for a silver eel to reach the estuary from the most upstream reaches. These facts, in turn, complicate the prediction of silver eels annual yield in catchments. There is a general agreement among eel specialists that the quantity of silver eels that emigrate yearly from a large catchment is simply not possible to predict (Lambert 2005, Lambert & Rochard 2007). In small catchments, estimates of silver eel production assume a one-to-one relation between pre-migrant eels and escapement of silver eels in the consecutive autumn (Acou et al. 2007a). However, the time required for an eel to complete its silvering process remains highly variable. Preliminary results based on mark-recapture

experiments showed that migration rate of pre-migrant eels ready to migrate vary greatly each year (from 0 to 100%) among and between catchments according to catchment contexts – particularly the presence of obstacles – and hydrological conditions (Feunteun et al. 2000, Acou 2006). As a consequence, considering that silver eels that turn back to the yellow stage are anecdotic, the assumption of the one-to-one relation between pre-migrant eels and escapement of silver eels could lead to biased estimates of production. As a result, instead of trying to estimate the actual annual production of spawners in a catchment, eel managers shall focus on the annual quantity of eels candidate to emigration, that will not necessarily emigrate at once. Breeding potential The breeding potential represents the quantity of silver eels that would undertake the seaward emigration each year with optimal hydroclimatic conditions. However, the breeding potential does not represent the quantity of silver eels that do escape from the river basin, because of specific mortality in the silver stage. This mortality is a direct function of the catchment context, which is related for instance to the presence of hydroelectric turbines, of silver eel fisheries, of drinking water reservoirs and related water management, over-mortality due to high densities below obstacles and death by pollution. In this catadromous fish, that colonizes rivers from the ocean, the downstream context that triggers eel density, and subsequently the sex-ratio, is formed by two fundamental factors: the fluvial recruitment (high or low) and the accessibility to the upstream zones. Fig. 1 presents four theoretical catchment configurations that induce different sex-ratio patterns in the future spawners. These factors structure factually the eel sedentary population downstream and upstream from the obstacles, and inevitably have direct repercussions on the production of silver eels. Based on some factors such as the obstacles position, the potential for eels to pass through them and colonize upstream zones, and the mortality rate of silver eels passing through them during their seaward migration, McCleave (2001) modelled the number of females produced in catchments in Maine (USA). This modelling approach clearly showed that the first factor to take into account to improve the breeding potential of a catchment is the obstacles position. It controls the surface of accessible habitats and the succession of low and high eel densities in the catchment, mostly in the downstream area when they occur there, and therefore it triggers sex-ratio for the sedentary yellow eels and the subsequent silver eels. It also affects the number of silver eels produced because of a density-dependent mortality (Vøllestad & Jonsson 1988, Lambert & Rochard 2007). These observations lead to consider the longitudinal profile of eel density as the prime descriptor of an eel population to assess

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Fig. 1. – Temporary or impassable obstacles to upstream migration can induce locally high densities due to the accumulation of migrant elvers, and therefore marked disparities in the longitudinal population structure (Aprahamian 1988, White & Knights 1997, Costa et al. 2007). Here are presented the eel density profiles according to different catchment contexts (1 to 4) and levels of fluvial recruitment (1: high or 2: low). The dashed line represents the density threshold that controls sex-ratio. The sex is determined during the very first years of continental life (reviewed in Lambert & Rochard 2007), and upstream migration is, for most eels, under the control of density (Feunteun et al. 2003). In this way, relationships will be simple in open catchments (1.1, 1.2, 3.1, 3.2). In obstructed catchments, a high recruiment below an impassable obstacle will induce high downtream densities and therefore a sex-ratio biased by males in 2.1 and 4.1, whereas a low recruitment in the same catchment context will induce a more balanced sex-ratio in 2.2 and 4.2. Sex-ratios are not biased toward females in the upper parts of 2.1 and 4.1, despite they are below the density threshold, because ESD occurred in the downstream parts for most eels. Rel Abund: relative abundance; m: sex-ratio biased by males; f: sex-ratio biased by females; Ø: no eels.

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Fig. 2. – Different types of breeding potential that should be observed, corresponding to the different catchment contexts previously described (Fig. 1). Here the breeding potentials are expressed by both mean density (N.ha-1) of the eel stock and mean weight of silver eels (that reflects sex-ratio due to the sexual dimorphism between silver males and females, here symbolized by a dashed line around 200 g). Above the density threshold (here symbolized by a dashed line around 1000 eels.ha-1), sex-ratio will be dominated by males. Catchments 1.1, 2.1, and 4.1 are typical ‘males catchments’ (sex-ratio biased by males), whereas 1.2, 3.1 and 3.2 are typical females catchments’. In pristine conditions (i.e. without any anthropogenic activities), breeding potentials shall naturally be triggered by the river length and the recruitment level.

the catchment’s breeding potential. However, if it usually takes 3 to 5 years to produce a male, it takes at least 4 to 10 years to produce a female (as little as 4 years in the Mediterranean lagoons, Acou et al. 2003; to an average of 8-9 years in the river Loire, unpubl data from the authors). The difference in the maturation time (i.e. population turnover), and the subsequent extramortality as the residence time extends, can induce large differences in the quantity of silver eels produced. Feunteun et al. (2000) estimated that between 5 and 12 % of the yellow eels in the Frémur catchment start the silvering each winter. A catchment dominated at 99 % by males produces much more silver eels in number than a 99 % females catchment. On the other hand, females are much heavier than males, so the biomass of silver eels produced from a ’males catchment’ should tend to be of the same

order of magnitude than those from a ’females catchment’. An interesting application of these views are the two neighbouring coastal catchments, Frémur and Oir Rivers, at the same latitude in western France but with different catchment contexts in term of obstacles to upstream migration (Acou et al. 2007). The Frémur (60 km2), highly impacted with seven major dams or obstructions along 17 km of mainstream, produced mainly males between 2000 and 2002 (94.7 % of males; males: N = 1521 ± 233, biomass = 160 ± 47 kg; females : N = 286 ± 103, biomass = 31 ± 15 kg). The less impacted Oir (85 km2), on which the circulation towards upper reaches is more or less free, produced in the same period mainly males close to the estuary, and females all along the upstream watercourse (for the whole catchment: 20 % of males; males: N = 95 ±

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23, biomass = 26 ± 6 kg; females: N = 378 ± 57, biomass = 103 ± 14 kg). They correspond respectively to breeding potentials of types 2.1-2.2 and 1.1-1.2 in Fig. 2, depending on the year-to-year recruitment level. However, the trophic status of these two streams might also play a role in the sex-ratio control. Estimation of the breeding potential This section and the following propose an overview of the methods available to estimate or to measure the spawning biomass of eels candidate to emigration in continental rivers. Methods for assessing directly the biomass of silver eels that should emigrate each year (based on eye diameters of the sedentary eel population) or that do emigrate (silver eel mark-recapture and fisheries data) are presented. These methods have to be sensitive to changes in the production level of silver eels, in order to give some feed-back of the management actions, to be adaptable to different types of catchments, transposable at different scales, from headwater streams to large rivers, and costeffective. The breeding potential estimate can be based on the following points: (i) because it modifies the population turnover in continental waters, and thus the total mortality cumulated with time, sex-ratio is required to the expression of the biomass of breeding potential; (ii) sex-ratio of the future spawners is directly under density control; (iii) the mean weight at silvering is pertinent to characterize the sex-ratio of spawners, because of the pronounced sexual dimorphism; and (iv) the silvering rate defines the proportion of eels candidate to emigration among the total eel stock in the catchment. Three steps are then needed: 1°- Build a consensual abacus (graph) for the relationship between the mean weight at silvering and the mean density of eels present in the catchment; 2°- Place on this abacus the mean density of eels in the catchment, that gives an idea of the mean weight at silvering in the catchment; 3°- Calculate the biomass of silver eels candidate to emigration, by modelling the silvering dynamic within the population in place (based on the size-class structure, the mortality rate and the emigration rate), or by fixing a consensual silvering rate; the breeding potential at the year y (By, in kg) is: By = dy * sy * r * wy * F’y with dy the mean density of eels in the catchment at the year y (eels/ha), sy the water surface of accessible habitats at the same year (ha), r the mean silvering rate (%), wy the mean weight at silvering at the year y (kg) and F’y the total mortality on the silver stage at the same year (F’y ≤ 1). The breeding potential is a result of the catchment context in which elvers recruit, that drives the longitudinal density profile of sedentary eels along the river axis. In this way, Fig. 2 represents the different breeding potential

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by types, that are rationally distributed along a gradient of sedentary stock mean densities. Breeding potentials that correspond to a mean density around the threshold (1000 eels.ha -1) are very close from each other on silver eel mean weight and pre-migrant biomass (N = density * mean weight * water surface, not figured), although they refer to different catchment contexts (2.2, 3.1, 4.1, 4.2). Field measurements A census of the existing methods for the abundance assessment of the eel spawning biomass enables, after the habitats proportions assessed, to identify two main categories (Table I), corresponding to various data availabilities on the migrating and/or on the sedentary stage. In most cases, data concern only the sedentary stock (data produced no 2 and 3 in Table I, with relatively low information level), or when professional or scientific fisheries are present, the assessment is a direct survey of the downstream migration (3 methods with high information level). On the sedentary eels The silvering metamorphosis starts during summertime and ends – for external traits – in autumn. Pre-migrant eels are easily identified by measuring eyes diameter (horizontal and vertical diameters on the same eye) to the nearest 0.2 mm with a standard caliper. When a precise measure is not possible in the field, the silvering can be roughly assessed by a simple check of the simultaneous presence of three external signs of silvering (colour, lateral line and large eyes, Acou et al. 2005, Durif et al. 2005). When possible, an electrofishing campaign in autumn, during the low-water period, can give an estimation of pre-migrants proportion among the sedentary eel population (eels > 200 mm in size, Laffaille et al. 2005). These pre-migrants compose the breeding potential in the sampled parts of the catchment. The accuracy of this estimation is quite acceptable in shallow waters (Feunteun et al. 2000), but not in deep waters, where the largest eels live and are difficult to sample (Laffaille et al. 2003). The number of eels candidate to emigration in the whole catchment can be extrapolated from the proportion of silver eels (pre-migrants) within a local population sampled in autumn. Two methods can be applied, with unequal efficiency: (i) the number of sedentary eels in the catchment is estimated by a catch-mark-recapture experiment; (ii) the number of sedentary eels is estimated by type of habitat with a multiple-pass electrofishing with removal (Nelva et al. 1979), combined with total water surface of the habitat concerned in the whole catchment (Feunteun et al. 2000, Cucherousset et al. 2007). The efficiency of the first method has been proved in small catchments (Feunteun et al. 2000), whereas the second is much more difficult to apply because it depends on the quality

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Table I. – A panel of available methods to assess the eel breeding potential in a catchment.

of eel-habitat models which themselves depend on the quantity of information from the field. However, the number of eels candidate to emigration in the catchment and their characteristics (sex-ratio, mean weight, body condition), the so-called breeding potential, can be assessed. This estimation aims at providing indices for pre-migrant eels, assuming that they reflect the real number of candidates to emigration, but also their sex-ratio, despite the larger fish abundance might be underestimated since they inhabit in deeper water masses. Nevertheless, as mentioned above, these methods cannot predict the number of silver eels that will finally emigrate to the sea, since this run is triggered by unpredictable climatic factors (for details see paragraph eels candidates to emigration). On the migrating eels Three methods are available, based on the assessment of the quantity of silver eels that do emigrate towards the sea, for the catchment portion upstream from the fisher-

ies, and for the time period of the study: - The exhaustive survey: survey of traps that intercept silver eels during migration (wolf traps) or other devices on dams, obstacles, thresholds or mill grids, allowing to catch almost all silver eels passing through (Vøllestad & Jonsson 1988, Feunteun et al. 2000). Experimental fixed fisheries can also be implemented to estimate the abundance of migrating silver eels. These surveys allow to quantify the production of silver eels from parts of the catchment higher than the trap devices, and during the implementation period. - The escapement assessment: catch-mark experiments can be carried out in professional or experimental fisheries. The number of running silver eels is then estimated by classic estimators (Caron et al. 2000), based on the recapture rate of the tagged silver eels among all the migrating silver eels. Such experiments need to be repeated several times with different flow conditions, in order to build up a water flow – silver eels run model. - The relative abundance survey: expressed in Catch per Unit of Effort (CPUE) of silver eels, can be assessed

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with professional fishermen logbooks, official catch reports or experimental surveys. Relative abundance measures that can be linked to the number of silver eels estimated at a given date with Peterson’s method (Caron et al. 2000). Conclusion Obviously, an estimation of the breeding potential based on the sedentary stock cannot be accurate, especially when the sampling effort to assess eel density is much too low compared to the catchment’s size (usually < 1 % of the water surface), and in large water surfaces (e.g. large rivers, lakes, marshes). However, in the European eel management context, an estimation of the present breeding potential in a catchment, even imprecise, is of great interest. On the other hand, the catchment context also comprises all chemical aggressions (water and sediment pollution) that can compromise the future reproductive success of eels. The “spawners quality” reflects the probability for eels to carry out a successful reproduction (sexual maturation, migration to the spawning areas, reproduction, embryos survival included). This quality is depressed by human impacts like pollution or pathogenic threats, and is potentially a reduction of the quantity of efficient spawners (Robinet & Feunteun 2002, Acou et al. 2008). For implementing a correct management plan, it would be opportune to check out the quality of silver eels that emigrate, and to apply a reduction coefficient to the escapement potential, in proportion with the probable decrease of their reproduction success. This aim is not attainable yet, however, in regard of recent works in this direction (Corsi et al. 2005). A cknowledgements .- This study was supported by the INDICANG INTERREG IIIb Program (web site at http://www. ifremer.fr/indicang). The authors would like to thank the two anonymous reviewers who improved the manuscript.

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