Return of adult anadromous allis shad (Alosa alosa L.) in the river Seine, France: A sign of river recovery?

RIVER RESEARCH AND APPLICATIONS

River. Res. Applic. 25: 788–794 (2009)

Published online 22 January 2009 in Wiley InterScience

SHORT COMMUNICATION

RETURN OF ADULT ANADROMOUS ALLIS SHAD (ALOSA ALOSA L.)IN THE RIVER SEINE, FRANCE: A SIGN OF RIVER RECOVERY?

J. BELLIARD,a* J. MARCHAL,b,c J.-M. DITCHE,d E. TALES,a R. SABATIEb,c and J.-L. BAGLINIEREb,c

a Hydrosystems and Bioprocesses Research Unit, Cemagref, Parc de Tourvoie, BP 44 92163 Antony cedex, Franceb INRA, UMR 985 Ecology and Ecosystems Health, F- 35000 Rennes, France

c Agrocampus Ouest, UMR 985 F-35000 Rennes, Franced Office National de l’Eau et des Milieux Aquatiques, Delegation interregionale Nord, Picardie, Ile-de-France, Haute Normandie, Basse

Normandie, 3, rue Sainte Marie 60200 Compiegne, France

(www.interscience.wiley.com) DOI: 10.1002/rra.1221

ABSTRACT

In the past, the diadromous fish fauna of the river Seine comprised 11 native species. From the second part of the 19th century, theprogressive modification of the river for navigation purposes and the increase of domestic and industrial pollution led to ageneral decline of migratory stocks and the extinction of several species. Among them, allis shad (Alosa alosa) was previouslywidespread in the Seine basin, but disappeared at the beginning of the 20th century. In July 2004, several individuals of shadwere observed in the river Seine upstream of Paris (410 km from the sea), one of them was identified as an allis shad that hadclearly spawned (thin fish and large scale erosion). A second allis shad was caught in a more downstream location (180 km fromthe sea) in November 2007 and a spawning mark was found on scales demonstrating clear evidence of reproduction. Recentoccurrences of this species are discussed in relation to the present conditions of water quality and migration in the Seinewatershed and recent evolution of the species’ distribution in the northwestern part of France. Copyright # 2009 John Wiley &Sons, Ltd.

key words: migration facilities; water quality; diadromous fishes; restoration

Received 18 April 2008; Revised 3 October 2008; Accepted 27 October 2008

HISTORICAL CONTEXT

Like other west-European rivers, the river Seine has a naturally impoverished freshwater fish fauna because of the

relative isolation of the basin with respect to the Ponto-Caspian ice refuge. The native fish fauna of the river Seine

originally included about 20 strictly freshwater fish species (Belliard et al., 1995). Conversely, it was relatively rich

in diadromous species, with 11 species recorded (Table I) (Beguer et al., 2007).

Little is known about the historical evolution of migratory fishes in the Seine Basin prior to the 19th century. In

the early 19th century, many species were already declining: catches of European sturgeon had become

exceptional, whereas Salmon spawning was only recorded in two modest tributaries of the Seine, the Andelle River

and the Cure River (Euzenat et al., 1992), indicating early extinction of this species in most of the Seine basin. By

comparison, allis shad was one of the most widely spread migratory species in the Seine basin in the first part of the

19th century. At this time, allis shad migrated upstream the Seine River to Cote d’Or (Ray, 1851), the Yonne River

to Auxerre (Moreau, 1881), and the Aisne River via the Oise River to the Ardennes (Euzenat et al., 1992) (Figure 1).

At the end of the 18th century it also occurred in the Eure River, and the Marne River, and its tributary the Ornain

River (Keith et al., 1992). Allis shad was intensely exploited by commercial fisheries in the lower river Seine:

between 1874 and 1884, several dozen tons of fish were captured by fisheries in the Rouen region (Euzenat et al.,

1992).

*Correspondence to: J. Belliard, Hydrosystems and Bioprocesses Research Unit, Cemagref, Parc de Tourvoie, BP 44 92163 Antony cedex,France. E-mail: [email protected]

Copyright # 2009 John Wiley & Sons, Ltd.

Table I. Diadromous fish species historically present in the Seine River

Allis shad Alosa alosa L. E�

Twaite shad Alosa fallax Lacepede E rSmelt Osmerus eperlanus L. E rEuropean sturgeon Acipenser sturio L. ESea lamprey Petromyzon marinus L. E�

River lamprey Lampetra fluviatilis L.Atlantic salmon Salmo salar L. E�

Sea trout Salmo trutta L. E rEuropean eel Anguilla anguilla L.Flounder Platichthys flesus L.Thin-lipped grey mullet Liza ramada Risso

E: species considered as extinct at the end of the 20th century (from Belliard et al., 1995), r: recent evidences of recovery (observation ofreproductions/presence of juveniles).�Recent observations of adults.

RETURN OF ALLIS SHAD IN THE RIVER SEINE 789

The decline of migratory stocks, particularly allis shad, was much greater in the second half of the 19th century

(Rochard et al., 2007). This is attributed, primarily, to the construction of weir and lock systems for navigation

purposes on the Seine and its main tributaries, and, secondly, to the construction of dams in headwater catchments

in order to regulate flow. The Poses weir, the barrier now closest to the sea (Figure 1) was built in 1850, and was

seconded in 1864 by the Martot weir (now destroyed), just downstream of it. Although it was relatively easy for fish

to cross these early navigation weirs, channel modification for navigation intensified from 1879 onwards, including

Figure 1. Historical distribution of allis shad in the Seine basin and location of the captures in 2004 and 2007; actual navigation weirs locateddownstream or just upstream the capture sites are indicated

Copyright # 2009 John Wiley & Sons, Ltd. River. Res. Applic. 25: 788–794 (2009)

DOI: 10.1002/rra

790 J. BELLIARD ET AL.

construction of several larger weirs that had a greater impact on fish migration (Mouchel et al., 1998). In 1886, the

extension of the Poses weir modified the last natural reach of the lower river Seine. Captures of allis shad in lower

river Seine dramatically decreased following this extension and, in 1897, ‘no more than 20 fish were caught during

the entire season’ (Gadeau de Kerville, 1897).

In the last part of the 19th century, several attempts to equip weirs with fish passes were undertaken, to improve

atlantic salmon migration (Euzenat et al., 1992). In addition, between 1888 and 1894, the artificial spawning of allis

shad has been developed to support the declining populations (Vincent, 1894), but this did not stop the decline of the

species (Roule, 1920; Quignard and Douchement, 1991).

The 20th century was marked by the successive extinctions of several migratory species. In the 1920s, allis shad

was occasionally observed in the estuarine part of the river Seine, and it appeared that there were no longer any

viable population of this species (Roule, 1920). In 1961, allis shad was considered as extinct in the Seine basin

(Spillmann, 1961).

The construction of navigation weirs greatly contributed to the extinction of allis shad and most other

diadromous species. But, domestic and industrial pollution had also adversely affected these species (Euzenat et al.,

1992; Rochard et al., 2007). At the end of the 19th century, high levels of pollution occurred downstream from Paris

as a result of direct discharge of sewage into the river (Mouchel et al., 1998). The water quality of the Seine

progressively worsened until the 1960s, to the point that long reaches downstream from Paris and in the estuary

were devoid of oxygen during much of the year (Boet et al., 1999). Thus, the level of pollution was so high that it

prevented colonization of the river Seine by migratory fishes.

Since the beginning of the 1970s, the water quality of the river has clearly improved (Figure 2), allowing the

return of nine migratory species in the lower Seine (Rochard et al., 2007) (Table I).

RECENT RECORDS OF ALLIS SHAD

In July 2004, anglers caught several fish resembling shad in the river Seine around Bois-le-Roi, upstream from Paris

(Figure 1). The site of capture was situated in a reach used for commercial navigation (deep, slow-flowing river,

about 100 m wide) just downstream from the lock of Vives-Eaux, located approximately 410 km from the sea.

Figure 2. Longitudinal variations of the dissolved oxygen concentration in the river Seine in May for different years


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Table II. Characteristics of the two allis shads caught in the river Seine in July 2004 and November 2007

Individual from July 2004 Individual from November 2007

Total length (mm) 513 570Fork length (mm) 459 500Total mass (g) 556 1280Gonad mass (g) 16 3.5Number of gill rakers on the first gill arch 116 112Number of dorsal fin rays IV/15 IV/15Number of anal fin rays III/21 III/21Number of ventral scutes 35 36Number of scales in longitudinal row About 80 About 75


Only one specimen was preserved, frozen and identified. It was 513 mm in total length and was identified as an

allis shad according specific morphological and meristic characteristics (Bagliniere and Sabatie, 2001; Alexandrino

et al., 2006): ventral sharp keel, no lateral line, tightly packed gill comb and 116 gill rakers on the first gill arch

(Table II). Its scales were irregularly arranged longitudinally. This characteristic is noted by Mennesson-Boisneau

and Boisneau (1990) as a mean to distinguish allis shad from twaite shad, the latter presenting a very regular

arrangement of scales.

Considerable erosion of scale edges highly suggests that the fish had sexually matured and had spawned. Fish

was probably 4 or 5 years old but age estimation was made difficult owing to scale erosion. It was a male and the

gonadic index (105 MG/L3F with MG¼Mass of gonads (g) and LF¼ fork length (mm)) was of 0.0165, corresponding

to the range usually observed for males after spawning (Mennesson-Boisneau and Boisneau, 1990). The post-

spawning stage was confirmed by the thinness of the fish (556 g for 513 mm total length). Using the length to mass

relationships established for Loire populations, the total mass of a similar-sized male during pre-spawning

migration would be 1062 g on average (Mennesson-Boisneau et al., 2000a). This corresponds to a loss of 48% of

the initial mass which is a ratio consistent with observations of live allis shads after spawning (Mennesson-

Boisneau et al., 2000b).

In November 2007, another shad was caught by a professional fisherman near the village of Venables, in a gravel

pit connected to the river Seine. This site is located approximately 180 km from the sea, a few kilometres upstream

from the Poses weir. Here the Seine is around 250 m wide, with a large navigated main channel and many side arms

and gravel pits connected to it.

The number of gill rakers (112) on the first gill arch and the irregular arrangement of scales clearly indicated that

this fish was another allis shad (see Table II for the fish characteristics). It was a female of 570 mm long with a total

mass of 1280 g. According to scale analysis, the fish was 5þ years old (Figure 3). A clear spawning mark on scales

indicated that it spawned in 2007. Plus growth on the edge of the scales after the spawning mark indicated that the

fish had grown after spawning. Such post-reproduction growth in freshwater has been previously observed for allis

shad on the river Mayenne, a slow flowing canalized tributary of the river Loire (Mennesson-Boisneau et al.,

2000b).

DISCUSSION

The occurrence of an adult allis shad in 2004 upstream from Paris is of interest because this species was considered

to be extinct in the river Seine. No allis shad had been observed as far upstream in the Seine basin for over a century.

The second observation in 2007 and the recent counting of several shads at the Poses weir in 2008 (Ditche personal

communication.) indicate probably an early sign of a possible natural re-colonization of the catchment by the

species.

The recent occurrence of adult allis shads in the river Seine may be explained by various factors. Since 1970s,

water quality had considerably improved due to the increasing number and performance of wastewater treatment


DOI: 10.1002/rra

Figure 3. Scale of the allis shad caught in November 2007. A spawning mark is clearly visible


plants (Figure 2). Previously, the very low dissolved oxygen concentrations in the downstream part of the estuary

probably impeded the re-colonization of most migratory species. Nowadays, from March to June, which is the

period of shad migration, the oxygen amount is generally higher than 6 and 8 mg.L�1 (respectively in the lower part

and medium part—upstream Paris—of the river Seine) (Figure 2) corresponding to conditions in accordance with

ecological requirements for shad migration and spawning.

In contrast, facilities allowing fish to pass over navigation weirs along the river Seine have not been recently

improved. Currently, only the three downstream weirs are equipped with fish passes, which were built more than

15 years ago. Presumably, weirs without fish passes prevent fish from migrating upstream, except during high flow

periods when they are lowered. However, fish can also use locks for their upstream migration. Visual observations

(Lebel et al., 1999) and radio-tracking operations (Guillard and Colon, 2000) in the river Rhone proved that the

Rhodanian twaite shad (similar in size to allis shad) use navigation locks. For the Seine catchment, the year 2004

was rather dry, and discharge remained below mean monthly flow values during the migration period of allis shads

(Figure 4). Because of this low flow, locks may have provided running waters that attracted allis shad and enabled

them to migrate far upstream into the river Seine. An alternative hypothesis would be that the relatively high

discharge in preceding months (January–beginning of February in 2004) may have enabled early migration of allis

shad. However, this hypothesis does not totally agree with the known observations on the start of shad migration in

northern rivers (usually in March–April) (Bagliniere et al., 2003). Regarding the 2007 catch, migration conditions

were probably better because of higher flow conditions during March.

The captures of adult allis shads described are concomitant with the renewed occurrence of other migratory

species in the Seine estuary and parts of the Seine River network. Since 2000, a large increase of smelt has been

observed (Rochard et al., 2007). Spawning of sea trout has been recorded in estuarial tributaries (Andelle River)

and Atlantic salmon were caught by fishermen and in scientific samples (Rochard et al., 2007; Bagliniere and

Porcher, unpublished data) and recorded at the Poses dam fish pass.

These captures also coincide with a regional regain of allis shad in northwestern France. Some individuals have

recently been observed in some coastal streams in Brittany and Normandy, such as the the Vire or the Orne which


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Figure 4. Daily discharge (years 2004 and 2007) and mean monthly discharge (35 years) in the Seine in Paris


are close to the river Seine (Bagliniere et al., 2003; Rochard et al., 2007). Furthermore, recent studies on the

distribution and richness of diadromous fish assemblages in Western Europe have shown that climatic change might

be favourable to the development of an allis shad population in the Seine watershed (Beguer et al., 2007; Rochard

et al., 2007).

In conclusion, it seems that there are currently favourable conditions enabling the return of migratory fishes in

the Seine basin. However, a sustainable return of allis shad in particular will depend on (1) facilities enabling fish to

pass navigation weirs, as they generally migrate hundreds kilometres upstream to spawn, and (2) the occurrence and

restoration of suitable spawning grounds as most of them were probably destroyed when the main channel was

modified for navigation.

ACKNOWLEDGEMENTS

We thank Mr Dedecker, G. Bonifassi and the staff of the ONEMA (SD 27 and SD 77) for providing us with the

specimens examined and related information and Natasha Shields and Crane Rogers for English improvement on

the manuscript. Discharge data source: Banque Hydro—Ministere de l’Ecologie, de l’Energie et du Developpe-

ment durable et de l’Amenagement du territoire. G. Leroy (DDE 76), M. Sarraza (Agence de l’Eau Seine-

Normandie) and W. Thomas (Service Navigation de la Seine) kindly provided water quality data.

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Return of adult anadromous allis shad (Alosa alosa L.) in the river Seine, France: A sign of river recovery?