Downstream migration patterns of one-year-old hatchery-reared European sturgeon (Acipenser sturio)

Journal of Experimental Marine Biology and Ecology 430-431 (2012) 68–77

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Journal of Experimental Marine Biology and Ecology

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Downstream migration patterns of one-year-old hatchery-reared Europeansturgeon (Acipenser sturio)

M.L. Acolas a,⁎, E. Rochard a, C. Le Pichon b, E. Rouleau a

a IRSTEA, UR EPBX, Estuarine Ecosystems and Migratory Fish, 50 avenue de Verdun, 33612 Cestas cedex, Franceb IRSTEA, UR HBAN, 1 rue Pierre-Gilles de Gennes, CS10030, 92761 Antony cedex, France

⁎ Corresponding author. Tel.: + 33 5 57 89 09 93; faxE-mail address: marie-laure.acolas@irstea.fr (M.L. Ac

a b s t r a c t

Article history:Received 5 August 2011Received in revised form 21 June 2012Accepted 25 June 2012Available online 21 July 2012

Keywords:Acoustic telemetryEstuarySpatial analysisTrajectory

Acoustic telemetry was used to quantify the behaviour of 94 hatchery-reared European sturgeon (27–38 cmin fork length) released in their native watershed. The study took place between July and December 2008 andbetween April and May 2009 in the tidal part of the Gironde system (south-west France) from freshwater tomesohaline estuary. Survival rate for the first month was estimated at 87% and the individual trajectory of 82fish was characterised. The mean distance covered per fish was 104 km, the mean ground swimming speedwas 0.7 ms−1 and no diel influence was highlighted. Three main downstream migration patterns werehighlighted with a first group of individuals settling in the freshwater part of the system, a second group cov-ering medium distances (105 km) and displaying fairly straight movement to reach the upstream estuary,and a third group of very active fish with repeated up and downmovements into the mesohaline estuary cov-ering two times more distances. We suspect that these patterns correspond to different exploratory behav-iours and salinity tolerances among individuals of the same size and cohort. According to our experiment,both the downstream freshwater part of the rivers and the upstream estuary represent important habitatsfor this age class. The direction of individual trajectory indicates that most of the fish displaying upstreamand downstream movements gradually shifted downstream between 1 and 6 months after their release.

1. Introduction

Diadromous fish populations display various migratory tactics (Gross,1987; McDowall, 1988) that can be observed between species (i.e. catad-romous vs anadromous species) orwithin one specieswhere there can bepartial migrations (Jonsson and Jonsson, 1993; Tsukamoto and Arai,2001) and there is a high level of variability within these tactics(Klemetsen et al., 2003). To understand the impact of these migratoryfish tactics on life histories, it is essential to study fish movements. Tele-metry has been successfully used to study habitat use (Blanchfield et al.,2009; Dick et al., 2009; Espinoza et al., 2011), migration behaviour(Acolas et al., 2004; Fernandes et al., 2010; Hedger et al., 2010; Lacroixet al., 2004) and environmental influence on migration (Childs et al.,2008;Davidsen et al., 2009). Telemetry studies are particularlywell suitedto the examination of endangered species as individuals are released toswim freely in their natural environment (Simpfendorfer et al., 2010).

Sturgeons are particularly vulnerable species, given their longlifespan with late maturity, intense fishing pressure, and threats totheir habitats (Billard and Lecointre, 2001; Rochard et al., 1990).Among sturgeons, seven species are anadromous including the

: + 33 5 57 89 08 01.olas).

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European sturgeon, Acipenser sturio, listed as critically endangered(IUCN) with only one remaining population in the Gironde system(Lepage and Rochard, 1995). Actions to protect this species have beenimplemented since early 1980s with conservation actions to limit inci-dental captures and poaching, and to improve the protection of thehabitats and later the building of an ex-situ stock (Williot et al., 1997).A European action plan relying particularly on the stocking ofhatchery-reared young fish was implemented recently (Rosenthal etal., 2007). Due to the low number of individuals in the population, afirst stocking action occurred in 1995 (Lochet et al., 2004) and since2007, 135000 juveniles have been released. Data from the fate ofthese fish in the natural environment are needed to optimize the con-servation program (Acolas et al., 2011a).

Among anadromous sturgeons, migration has mainly been stud-ied on adults to document reproduction migrations (Benson et al.,2007; Heublein et al., 2009) and marine migration (Edwards et al.,2007; Lindley et al., 2008; Ross et al., 2009). Studies on juvenile inthe field have mainly concerned large juveniles (above 60 cm longor greater than 2 years of age) such as the Gulf sturgeon (Acipenseroxyrinchus desotoi) (Harris et al., 2005; Sulak et al., 2009), thegreen sturgeon (Acipenser medirostris) (Lindley et al., 2011) or thewhite sturgeon (Acipenser transmontanus) (Parsley et al., 2008).Knowledge is poorly developed in our understanding of habitat useand migration tactics in juveniles, and telemetry studies on released

69M.L. Acolas et al. / Journal of Experimental Marine Biology and Ecology 430-431 (2012) 68–77

fish could improve our understanding of sturgeon life histories andstocking program sustainability (Gessner et al., 2006).

Only one telemetry study has been carried out on European sturgeon(Lepage et al., 2005; Taverny et al., 2002). Usingmanual acoustic tracking,the authors documented movements in the mesohaline sector of the Gi-ronde estuary and showed that fish exhibited low amplitudemovements(below10 km) following the tidal cycle and that thesewere concentratedclose to feeding areas. However, this study was based on 16 fish of4–5 years old (82–122 cm in total length), and in the field, very fewdata on fish of less than 2 years old are available (Rochard et al., 2001).The main biological data on European sturgeon were collected in theGironde basin (Acolas et al., 2011b;Williot et al., 1997) and onlymonitor-ing by scientific sampling or declarations by fishermen were available tostudy downstream migration patterns (Castelnaud et al., 1991; Rochardet al., 2001). These authors have described seasonal back and forthmove-ments between the estuary and the sea before the fish definitively leavethe estuary but movements of the younger fish between freshwater andthe estuary remained unknown.

We studied downstream migration patterns of one-year-oldhatchery originated fish using passive and manual tracking. Our objec-tives were (1) to estimate early survival of hatchery-reared sturgeonreleased into the natural environment, (2) to characterise their move-ments, (3) to test if there is a diel effect onmovements and (4) to identifyif one or several downstream migration patterns can be described.

2. Materials and methods

2.1. Fish origin and tagging

European sturgeon were born and reared in the IRSTEA (previouslynamed Cemagref) experimental station at Saint Seurin sur Isle (45°01′01.14″N; 0°00′55.24″E). Juvenile sturgeons were produced by a broodstock of wild adults acclimatized to hatchery conditions since the1980s (Williot et al., 1997). In 2007 the juveniles produced originatedfrom the assisted reproduction of one female and two males whereasjuveniles from 2008 were produced from two females and threemales. Thus juveniles in our telemetry study were composed of a mix-ture of different genetic origins. Those juveniles were fed on a naturaldiet (chironomids) until they reached a suitable size for tagging. Onemonth before tagging they were raised in a 2 m square tank suppliedwith amixed of underground and river water from the Isle River (an af-fluent of the Dordogne River). Fish were exposed to natural photoperi-od but tanks were covered with fine mesh to provide low luminosityconditions. Current was provided via a pump about 2 h per day totrain the fish before release.

At the hatchery, a total of 46 fishwere tagged in 2008 (cohort 2007)at 1 year old and 48fishwere tagged in 2009 (cohort 2008) at 9 monthsold. Both cohorts had the same rearing conditions. Themean fork lengthand weight were respectively 32 cm±(standard deviation) 1.6 and193 g±30 in 2008 and 31 cm±3.1 and 165 g±53 in 2009 (Table 1).Fish were individually tagged with Vemco Ltd tags: V9-6L (2.9 g inair) for 86 fish in 2008 and 2009 and V9P-1L (3.6 g in air) for 8 fish in2008. The tag weight versus fish weight ratio was on average 1.95±0.36% (Winter, 1983). In 2008, the lifespan of the tags was 6 months(signal emitted every 50/130 s) and in 2009 it was 2 months (signalemitted every 15/45 s).

Table 1Fish characteristics per release date. Data are presented as mean (±standarddeviation).

Cohort Date of release Number of fish Fork length (cm) Weight (g)

2007 7 July 2008 14 33.5 (2.1) 204.4 (35.4)21 July 2008 13 31.9 (0.6) 172.6 (7.7)28 August 2008 19 33.0 (1.5) 199.1 (31.4)

2008 6 April 2009 25 32.9 (3.0) 197.1 (56.3)27 April 2009 23 28.9 (0.9) 131.7 (14.1)

The tagging procedure followed standard recommendations (Bridgerand Booth, 2003; Wagner et al., 2011). Fish were anaesthetised with0.5 ml of clove oil diluted in ethanol (dilution at 10%) for 10 L of waterand placed in a V-shape support. During surgery, a less concentratedanaesthetic solution (60% of the initial concentration) was providedthrough the gills. The ventral part of the fish was dried using a sterilecompress, then disinfected with diluted oxygenated water (10%),and an incision of about 2 cmwas made on the ventral midline behindthe pectoral fins. The acoustic tag, disinfected beforehand with ethanoland dried, was inserted and the incision was closed with 2 sutures tiedwith a surgeon's knot (24 mm needle mounted on a sterile Ethicon ab-sorbable monofilament). At the end of the surgery, a hydrophobic anti-fungal cream was applied. External tagging (Hallprint Ltd) was carriedout to identify each fish in case of incidental recapture by fishermen.Preliminary tests on 32 juvenile European sturgeons of similar sizehave demonstrated that the tagging procedure did not affect eithergrowth or swimming capacity (challenge in a swimming tunnel) ofthis species up to 49 days after tagging (Acolas, unpublished results).Fish were released in the river between 1 and 3 weeks after tagging.

2.2. Study site

The study site is located in south-west France (Fig. 1). The Ga-ronne and Dordogne Rivers form the Gironde estuary which has asurface area of 646 km2. It is 14 km at the widest point and about72 km in length. The Gironde estuary depth varies between 2 and30 m. The study site can be divided according to a salinity gradientinto a freshwater part (upstream Dordogne River, downstream Dor-dogne and Garonne Rivers), an oligohaline part, a mesohaline part,and a polyhaline part at the mouth of the estuary (Fig. 1). In 2008,the study was carried out between July and December and in 2009between April and May. Environmental parameters (salinity, turbidity,oxygen level and temperature) for the 2 years were recorded at threesites (Fig. 1 and Table 2) by permanent recording stations (MAGEST,Automated monitoring network of the Gironde-Garonne-Dordognesystem, University of Bordeaux). In the estuary, the main human activ-ities are navigation, artisanal fisheries and energy production (nuclearpower plant). Water velocity can reach 5 ms−1 in the estuary andwater flow variations during the study period in the Dordogne andthe Garonne River are shown in Fig. 2.

2.3. Acoustic telemetry survey

All fish were released by small groups (Table 1) at the same site inthe Dordogne River (Fig. 1) at five different dates between 7th July2008 and 27th April 2009 (Fig. 2). The release site corresponds to a his-torical reproduction site (Jego et al., 2002) in freshwater near the limitof the tidal influence. Both passive andmanual trackingwere used to as-sess fish movement. Detection tests for both types of receivers (passiveand manual) were carried out in the different parts of the study area(freshwater, upstream and median estuary) at different dates andtidal cycles and theminimum andmaximum detection ranges were es-timated. In 2008 and 2009, respectively 31 and 39 passive receivers(VR2W, Vemco Ltd) were deployed and distributed along the studysite to record tagged fish passages (Fig. 1). Each passive receiver loca-tion was GPS referenced and the passive receivers' detection distancewas evaluated between 200 and 400 m in diameter independently ofthe area salinity characteristics. The arrays of receivers were distributedlongitudinally and transversely, avoiding the navigation channel andthe main fishery areas. By the end of the study, 17 receivers (2008)and 9 receivers (2009) were lost or damaged. Manual tracking (VR28,Vemco Ltd) was carried out mainly in the freshwater area. For manualtracking, the distance detection was evaluated at 800 m in freshwaterwhereas it decreased to 100 m in the upstream and in the medianestuary. In addition to a low detection range in the estuary, manualtracking was very time consuming (Cooke et al., 2005) and thus we

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GaronneRiver

Dordogne River

Girondeestuary

AtlanticOcean

Release site

Upstream River

Median Estuary

(Mesohaline sector>5 & <18‰)

Upstream Estuary

(Oligohaline sector>0.5 & <5‰)

Downstream River

(Freshwater)

2008 hydrophone position

2009 hydrophone position

Environmentalparametersmeasurement sites

Downstream Estuary

(Polyhaline sector >18& <30‰)

#######

# # # #

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Limit of tidalinfluence

Fig. 1. Study site located in the south west of France. The system studied corresponds to the downstream parts of the Dordogne and the Garonne Rivers and to the upstream andmedian Gironde estuary.

70 M.L. Acolas et al. / Journal of Experimental Marine Biology and Ecology 430-431 (2012) 68–77

focused on passive tracking to cover a large area between freshwaterand mesohaline estuary.

2.4. Data analysis

A database was constructed based on the passive andmanual track-ing detections of all the fish (24308 detections in total of which lessthan 0.3% corresponded to manual tracking). The database gathersfish identity, each date and time of detections and the correspondingcoordinates (each fishwas located spatially and temporally). Passive re-ceivers were installed in transversal lines and those lines were about10 km far apart longitudinally (Fig. 1). Using R software (R, 2006), we

Table 2Environmental parameters recorded by year at three sites in the Dordogne River (1), the GThe locations of the three sites are shown in Fig. 1. The table gives the mean value (minimNTU: Nephelometric Turbidity Unit.Sensor reference for turbidity: LIQUISYS-M CUM 253, MAX-WCUS31 (©Endress+Hauser).Sensor reference for dissolved oxygen: LIQUISYS-M COM 253, cos4 (©Endress+Hauser).Sensor reference for conductivity and temperature: LIQUISYS-M CLM 253, INDUMAX-H CLS

Sites Salinity (‰) Turbidity (NTU)

20081 Dordogne 0.11 (0.0–0.3) 616.24 (0.0–99982 Garonne 1.58 (0.0–8.1) 1962.29 (0.1–99993 Gironde 5.63 (0.1–16.0) 1055.47 (25.0–999

20091 Dordogne 0.10 (0.05–0.16) 44.57 (7.0–202.02 Garonne 0.15 (0.14–0.17) 78.30 (26.0–2563 Gironde 1.86 (0.14–8.03) 1073.03 (122.0–99

implemented a method to smooth trajectories in the case of multipledetections of the same fish at the same time by several receivers withoverlapped detection range. Presence data were smoothed with atime period of 3 min which corresponds to the time needed for a30–40 cm fish to cross 200 m (e.g. minimal distance between two re-ceivers on a line) and smoothing was based on weighted means of thenumber of signal receptions at each receiver (Simpfendorfer et al.,2002).

From this database, using the R software and the ADEhabitat pack-age (Calenge, 2006), the class “ltraj” (Calenge et al., 2009) was used tocharacterise fish trajectories. In particular, it calculates the Euclideandistances and the time interval between consecutive locations, this

aronne River (2) and the median estuary (3).um–maximum).

52 (©Endress+Hauser).

Oxygen (%) Temperature (°C)

) 85.35 (79.7–89.0) 15.50 (4.5–26.0)) 77.74 (50.9–87.1) 16.00 (8.6–25.7)9) 90.67 (72.8–113.9) 17.79 (5.7–25.0)

) 93.47 (84.3–105.5) 13.58 (9.9–17.5).0) 82.34 (78.5–88.7) 13.86 (13.3–15.4)39.0) 83.23 (69.5–99.1) 14.87 (12.6–17.7)

3 s-1)

Dordogne

Garonne

Fig. 2. Water flow variations and dates of fish release. The arrows highlight the date of release.

Upstream River

Downstream River

Upstream Estuary

Median Estuary

D1 D2 D4 6DD5

Dotted lines represent consecutive upstream and downstream movements

Fig. 3. Diagram of the spatial distribution categories. Upstream and downstream riversas well as upstream and median estuary are localized in Fig. 1. Distribution 1 (D1) cor-responds to fish that were located only in the upstream River, distribution 2 (D2) cor-responds to fish that were located in the upstream and the downstream parts of theRiver. Distributions 3 (D3) and 4 (D4) correspond to fish that were located up to theupstream estuary, respectively, without and with back and forth movements. Distribu-tions 5 (D5) and 6 (D6) correspond to fish that were located up to the median estuaryrespectively without and with back and forth movements.

basic unit of the trajectory being called “burst” (Calenge et al., 2009).Because fish traveled in the estuary and in the river, we chose to replacein each “burst” Euclidean distances by hydrographic distances (i.e. dis-tances following the river course). They were calculated between twoconsecutive position estimates using ArcGIS 9.3 and Anaqualand 2.0, afreeware for calculating hydrographic distances between points or pat-ches along a river, either upstream, downstream or in both directions(Le Pichon et al., 2006). Each “burst”was then characterised by its direc-tion: upstream, downstream, lateral and “no movement”. No move-ment corresponds to two consecutives positions of the same fishlocated within the detection range of one receiver (precision 400 m).Next, a movement table was produced to collate “bursts” (n=8770)with the associated hydrographic distance, time interval, and direction.By organising the data in this way, different parameterswere calculatedto characterise individual trajectories. For “bursts” that occurred in lessthan 24 h, total hydrographic distance covered (the sumof all distancesmeasured) was calculated per fish for the whole study period. For“bursts” that occurred in less than 1 h, the rate of movement ROM(i.e. ground swimming speed=hydrographic distance/time) was cal-culated and the mean ROMwas calculated per fish. Nycthemeral effect(i.e. day night differences) was tested on these two variables with aWilcoxon paired test. For bursts below or equal to 1 h and burstsbelow or equal to 24 h, the proportion of movements in each directionand the mean hydrographic distance covered in each direction was cal-culated. For both time periods, night and day distances covered per di-rectionwere compared using non-parametric Kruskal–Wallis (KW) testfollowed by a post hoc non-parametricmultiple comparison test (Steel–Dwass).

For each fish, we described six spatial distributions in thewatershed(Fig. 3): fish that were located only in the upstream part of the Dor-dogne river (distribution 1, D1);fish thatwere located only in the fresh-water downstream part (either Dordogne or Garonne river, D2); fishthat were located up to the upstream estuary without (D3) or with(D4) back and forth movements within the freshwater area; and fishthat reached the median estuary in a straight trajectory (D5) or withback and forth movements (D6).

Each fish was then characterised by its total hydrographic distancecovered, its rate of movement (ROM), its spatial distribution and itsdate of release. A multiple correspondence analysis (MCA) was carriedout followed by a Hierarchical Ascendant Classification (HAC) clusteranalysis (usingWard criterion) in order to identify downstreammigra-tion behavioural patterns of 77 fish out of the 94 released fish for whichwe were able to characterise each variable. The quantitative variables

were divided into classes, the qualitative variables were grouped andthe number of fish for each class or group is shown in Table 3. The ad-vantage of theMCA is that it discriminates groups and they can be com-pared with a KW test followed by a post hoc non-parametric multiplecomparison Steel–Dwass test.

3. Results

Of the 94 fish released, 7 were never detected and 5 had a very lowdetection rate. This corresponds to 12.7% of the tagged fish which maybe dead or which could have had a tag failure. Analyses were thencarried out on 82 fish. The mean number of detections per fish was289±486.

3.1. Nychtemeral effect and trajectory orientation

No significant differences were detected between night and day ei-ther in hydrographic distance covered or in ROM (respectively,Wilcoxon test, N=82, p-value=0.052 and N=77, p-value=0.304).Themean hydrographic distance covered per fish for the whole studiedperiod was 104.6 km±76.7 (minimum/maximum value: 4.3 km/345.1 km). The mean ROMwas 0.72 ms−1±0.9 (minimum/maximumvalue: 0/6 ms−1). “Bursts” that occurred in less than 1 h represent79% of the total trajectories. During this time period, 12.6% of the

Table 3Qualitative and quantitative variables included in the Multiple Correspondence Analy-sis. Classification groups are described and the number of individuals per group isgiven. For spatial distribution variable, each classification group is described in Fig. 3.

Variables Classification groups Number of individuals

Date of release(qualitative variable)

7 July 2008 1221 July 2008 1028 August 2008 86 April 2009 2427 April 2009 23

Spatial distribution(qualitative variable)

Upstream river 8Downstream river 6Upstream estuary 7Upstream estuarya 6Median estuary 14Median estuarya 36

Rate of movement (ROM) (ms−1)(quantitative variable)

[0–0.15] 23[0.15–0.3] 29[0.3–0.45] 15[0.45–0.6] 5[0.6–0.9] 5

Total distance covered (m)(quantitative variable)

[0–80000] 12[80000–120000] 13[120000–160000] 25[160000–200000] 11[200000–440000] 16

a Indicates trajectories with back and forth movements.

movements were downstream (mean distance 224.9 m±304.9), 5.7%were lateral (72.5 m±74.4), 13.9% were upstream (mean 202.3 m±234.4) and 67.6% corresponded to nomovement. The hydrographic dis-tances covered differed significantly according to orientation (KWchi-squared=280.7, df=5, p-valueb10−2); with lateral distance sig-nificantly smaller than downstream and upstream movements, whiledownstream and upstream distances did not differ significantly. Dayand night distances did not differ regardless of the direction (Fig. 4A).“Bursts” that occurred in less than 24 h represent 96.5% of the total tra-jectories. During this time period, 18.9% of themovements were down-stream (mean 4271.8 m±6350.7), 5.0% were lateral (102.5 m±381.1), 15.3% were upstream (mean 1389.3 m±3180.8) and 60.7%corresponded to no movement. The distances covered differed signifi-cantly according to orientation (KW chi-squared=499.2, df=5,

Day down

Night down

Night up

Day up

Day lateral

Night lateral

Fig. 4. Distance covered according to direction and nychtemere for basic units of the trnon-significant differences; ***: a significant difference p-valueb0.001.

p-valueb10−2) with lateral distance smaller than upstream and down-streammovements and upstreammovement smaller than downstreammovements. Day and night distances did not differ regardless of thedirection (Fig. 4B).

3.2. Patterns identified using MCA and cluster analysis

Using MCA and cluster analysis, four patterns were identified(Fig. 5). The first axis accounted for 59% of the variance and the secondaxis 43%. Each variable tested was represented for each pattern with abox plot (Fig. 6). The distance covered was significantly different forall patterns (pKW=2.49∗10−11) (Fig. 6A). The ROM was not signifi-cantly different for the different patterns (pKW=0.08), although pat-tern 3 presents very high values compared to the other patterns(Fig. 6B). Concerning the date of release, pattern 3 was significantly dif-ferent from all the other patterns (for all pSteel.Dwassb0.01)whereas pat-terns 1, 2 and 4 were not significantly different (1:2 pSteel.Dwass=0.39,1:4 pSteel.Dwass=0.86, 2:4 pSteel.Dwass=0.59) (Fig. 6C). The spatial distri-bution was highly significantly different between patterns 1 and 2 andall the other patterns (pSteel.Dwassb0.01) but itwas not very different be-tween patterns 3 and 4 (pSteel.Dwass=0.05) (Fig. 6D). Based on this anal-ysis, Figs. 7 and 8 illustrate the different patterns of downstreammigration. The first pattern is characterised by fish that stay in freshwa-ter covering a short distance (37.2 km±21.3). The second pattern con-cerns fish of all release dates and of different distribution patterns, fromdownstream freshwater residence to residence in an oligohaline sectorwith orwithout back and forthmovements into the freshwater area andfish thatmigrate directly to themedian estuary. They covered a relative-lymoderate distance (105.2 km±16.6). The third pattern concernsfishreleased in April 2009 and mainly at the end of the month when thewater flow in the rivers was increasing (Fig. 2). The distance coveredwas relatively high (165.0 km±69.8) and concerns fish that presenteda rapid downstreammigration to the median sector of the estuary. Thefourth pattern concerns fish of all release dates that covered very hightotal distances (199.1 km±77.2). This represents spatial distributionwith movement straight towards the median zone of the estuary anddistribution patterns with back and forth movements between thefreshwater area and the oligohaline sector and between the oligohalineand the mesohaline sector.

Day down

Night down

Night up

Day up

Day lateral

Night lateral

ajectory below or equal to 1 h (A) and trajectory below or equal to 24 h (B). NS:

Pattern 1

Pattern 4

Pattern 3

Pattern 2

ilarit

Axis 1 (59%)

Pattern 1 Pattern 2 Pattern 3 Pattern 4

Fig. 5. Multiple correspondence analysis plot (panel A) and cluster analysis result (Ward dendrogram) (panel B) with the four groups of individuals identified by an ellipse.

4. Discussion

4.1. Methodological aspects

Data were obtained for 87.3% of the released fish. For some individ-uals tag failures were suspected because they were not detected infreshwater by manual tracking soon after their release but it was notpossible to distinguish this from avian predation (herons are presenton the site). This percentage could be interpreted as a proxy of the sur-vival rate that could be obtained after 1 month when fish reared in thehatchery over a period of 1 year are released into the wild. In this typeof study, it was a challenge tomaintain the fixed receivers in a high cur-rent velocity area and some receivers were lost during the study, thusreducing the area of detection. In the river and in the estuary the re-ceivers were positioned along a transversal line in such a way thattheir detection ranges overlapped slightly. For safety reasons this con-figuration was not possible in the navigation channel or main fishingareas. Due to the design of this experiment, inherent in the configura-tion of the working site, we probably underestimated the distance

covered per fish; however, the objective was to draw a general patternof the downstream migration on a large scale. To cover such a longstudy area (150 km between the release site and the farthest array) atan individual level, we believe that passive acoustic tracking was thebest choice.

Our analysis gathers data from two consecutive years. In order totake into account potential bias due to the analysis over 2 years, thedate of releasewas included in theMCA analysis. One of the four groupsidentified concerns mainly individuals from one release date and it canbe explained by high water flow just after that release. This is thereforea particular case, observed due to specific environmental conditions.The other three groups include fish from the different release dateswhich allow a safe interpretation of those patterns.

4.2. Diel effects

In our study, no diel effects on ROM, on total distance covered oron distance covered taking in account the direction of the move-ment, were observed. This is in accordance with previous findings

tial d

pKW<0.01

pKW p10.0< KW<0.01

pKW=0.08

Pattern 1 Pattern 2 Pattern 3 Pattern 4 Pattern 1 Pattern 2 Pattern 3 Pattern 4

Fig. 6. Box plot of variables used in the multiple correspondence analysis for each pattern identified. The p-value of the Kruskal–Wallis test is indicated at the top left corner of eachbox plot. NS: non-significant difference between groups using the Steel–Dwass post hoc test.

in the field for older European sturgeon (Taverny et al., 2002) whereno difference between day and night ground swimming was noted.However, controlled experiments on three-month-old (Charleset al., 2009) and on one-year-old (Staaks et al., 1999) European stur-geons showed that their activity seems to increase at night. This dif-ference could be explained by the high turbidity of the estuary whichwould reduce the fish perception of day and night (Bramblett andWhite, 2001). There could also be an ontogenic evolution of dayand night perception because diel influence has been reported inmany sturgeon species, mainly for young stages, like larvae in Russiansturgeon (Acipenser gueldenstaedtii) (Kynard and Horgan, 2002) or inwhite sturgeon (A. transmontanus) (Kynard and Parker, 2005) that are

Upstream River

Downstream River

Upstream Estuary

Median Estuary

Pattern 2 N=14Pattern 1 N=13

Dotted lines rep

Fig. 7. Diagram of the four downstream migration patterns identified by the multiple corresnumber of fish per pattern. Pattern 1 represents trajectories of fish that frequent only theexcept fish that were located up to the median estuary with back and forth movements. Ptrajectory up to the median estuary. Pattern 4 gathers fish that present spatial distribution

more active at night or in Atlantic sturgeon where habitat use differedbetween night and day (Gessner et al., 2009).

4.3. Trajectory orientation

Our spatial analysis enabled us to quantify the orientation of thesturgeon movements. In general, few and small lateral movement dis-tances were observed compared to upstream and downstream move-ments. In the estuary, water current is orientated downstream andupstream and the lack of lateral movement may be explained by a ten-dency on part of the fish to follow the water current for main move-ments in order to limit energy expenditure (Taverny et al., 2002). A

istance covered

Pattern 3 N=18 Pattern 4 N=38

resent consecutive upstream and downstream movements

pondence analysis. Spatial distributions are identified for each pattern. N indicates theRiver part. Pattern 2 gathers fish that present the entire spatial distribution encounterattern 3 gathers fish that present only one spatial distribution: a straight downstreamup to the estuary with back and forth movements.

DowstreammovementLateralmovement

Pattern 3 Pattern 4

0 5 10

Pattern 1 Pattern 2

±2.5 Kilometers

Upstreammovement

River channeland estuary

Fig. 8. Illustration of one fish trajectory for each downstream migration pattern identified. Patterns 1, 2, 3 and 4 are defined in Fig. 7.

high proportion of records corresponded to no movements, whichmeans that fish were staying within the detection area of a receiver.This type of behaviour may correspond to resting or feeding in fishthat resist thewater current in order to stay in their area of interest. Re-sistance to the current has already been observed in experimental con-ditions during swimming endurance trials in other species of sturgeonsuch as shovelnose sturgeon (Scaphirhynchus platorynchus) (Adams etal., 1997, 1999) and in European sturgeon as well (Acolas, unpublishedresults). Fish settle on the substrate, maintaining their position by usingtheir pectoral fins. They can alternate swimming and positioning them-selves on the bottom with very low caudal undulation and this couldsave energy. The downstream and upstream movements recordedwould then correspond mainly to foraging behaviour.

For movements that occurred in less than 1 h, the distance coveredupstream and downstream was similar. For these short time move-ments,fish seem to carry out someup and downmovements of low am-plitude (about 200 m) whereas for movements in less than 24 h, thedistance covered in a downstream direction was three times greaterthan the upstream distance. This difference may be explained by envi-ronmental factors, which can be relatively stable during less than 1 hbut highly variable in a 24-hour period with 2 tidal cycles and associat-ed salinity variation. These upstream and downstreammovements in ashort period of time which become clearly downstream orientated(although still with some upstream movement) support the initial

hypothesis of a downstreammigration with back and forthmovementsshifting progressively downstream.

4.4. Downstream pattern interpretation

Four downstream patterns were highlighted in our study. ROM aswell as the total distance covered could be interpreted as a measure offish activity. ROM did not vary between the four patterns observed,however the distance covered was very different. If total distance cov-ered is long and if back and forthmovements are described in the spatialdistribution, fish can be considered as very active and having an explor-atory behaviour. On the other hand, if the distance is very short thismeans that fish may settle in an area and do not have an exploratorybehaviour.

Among the patterns highlighted (Figs. 7 and 8), pattern 4 could beinterpreted as very active with long distances covered and lots of backand forth movements during the downstreammigration to the medianestuary. This behaviour applies to most of the fish (45%) and could beconsidered as an exploratory behaviour with progressive downstreammigration. In contrast, pattern 1 corresponds to fish that did not explorethe estuary but settled in the freshwater area. These fish would havefound enough food and a suitable area not far from their release siteand did not display a high exploratory behaviour. Chironomids thatwere provided as food at the hatchery were available in the freshwater

part of the system as well as oligochetes but in the saline part, mainlyoligochetes and polychetes prey were available. The different patternsmay be linked to this food distribution. Part of the hatchery reared indi-vidualsmay not easily change diet (Ersbak andHaase, 1983) and choosean area where known prey are available (Pattern 1) whereas otherswere able to alternate diets and colonize a larger area (Pattern 4). Pat-tern 2 would therefore be intermediate with fish of different diet, cov-ering a medium distance and displaying a fairly straight movement toreach the oligohaline or the mesohaline estuary with very few largeback and forth movements. Pattern 3 could be interpreted as relatingto a period of high river discharge. Fish leave the freshwater area quick-ly to reach the median estuary and some fish move back and forth be-tween the oligohaline and the mesohaline estuary. This downstreambehaviour linked to a rapid change of river environmental conditionhas already been observed in Gulf sturgeon when temperatures ofriver water dropped suddenly (Sulak et al., 2009). Whatever the pat-tern, the mean ground swimming speed was similar. This means thatall fish have a similar swimming capacity, probably because of theirsimilar size and weight at release. If all fish follow the water current,as suggested above, it could also explain the homogeneity of the meanground swimming speed.

These different behaviours may be explained by different salinitytolerances among individuals. Fish in pattern 1may not support salinityvariation in the estuary,fish in pattern 2may includefish of different sa-linity tolerances and fish in pattern 4 may become progressively accli-mated to the different salinity of the estuary thanks to back and forthmovements between freshwater and median estuary. Although notwell documented due to the limited sampling in the natural environ-ment, different salinity tolerance has been reported in the literature be-cause only some individuals leave the river for the estuary during theirfirst winter (Magnin, 1962; Rochard et al., 2001). One-year-old fish(27 cm) have been localized in the upper estuary by the end of theirfirst winter and by the end of their second winter, marine incursioncan be observed for a few individuals, with fish of over 15 monthsbeing highly tolerant to salinity variation (Rochard et al., 2001). In ourexperiment, we demonstrate that fish over 9 months old can enterthe upstream and the median estuary during their first spring (April)and that they tolerate the associated salinity (up to 8‰ in 2009 and16‰ in 2008 for one-year-old fish). However, our results suggest thatthe osmoregulation capacity may not be the same for fish of the samesize and cohort. Fish stocked originated from different genetic crossingand we can suspect that osmoregulation and genetic origin may belinked.

Fish were born in a hatchery so we could have suspected a generalhomogeneous behaviour but they present different patterns of explor-atory behaviour and were located in area of different salinity whichmay illustrate phenotypic variability. Moreover, all fish were releasedat similar size and the different patterns expressed indicate that theremay not be any simple size-dependent link in migration pattern.According to our experiment, both the downstream freshwater part ofthe rivers and the upstream estuary represent important habitats forthis age class. The observed variability in movement patterns can beinterpreted as advantageous with fish that originated from hatcherypresenting adaptation capacity to the natural environment which mayenhance their survival and their performances (movements, habitatselection). These patterns may not be different than those of wild con-specifics as demonstrated in other species (Mann et al., 2011). Unfortu-nately nowild European sturgeons of this age class are present anymorein the wild to carry out a comparative study.

4.5. Conclusion–Perspectives

This is the first study on European sturgeon of less than 2 years old inthe wild. Our experiments have highlighted three main downstreammigration patterns that could be explained by a gradient in exploratorybehaviour, different prey availability, and by different salinity tolerances

within the same age class. Taking the different patterns together supportsthe idea that hatchery-reared European sturgeons can exhibit two maintypes of trajectory for downstreammigration. First, as supposedprevious-ly, they can show a gradual downstream migration towards the oceanwith upstream–downstream back and forth movements and second,some individuals can have a straight downstream migration, at least asfar as the median estuary. To complete these findings, we plan to carryout further experiments on habitat preference and on the tidal influencein downstream migration. The high survival rate obtained, the differentexploratory behaviours observed that may be linked to prey distributionor preference or to salinity tolerance support the idea that those hatcheryreared fish still present adaptive capacity which is encouraging for suchstocking programs.

Acknowledgments

We wish to thank the European Union (FEDER), the “Région Aqui-taine” and the Adour-Garonne Water Agency for their financial sup-port and the association of the Commercial fishermen (CNPMEM)who helped in providing information to the fishermen.

We wish to thank Olivier Delaigue from Cemagref, UR HBAN forhis work on writing the R script. We also wish to thank the staffs ofthe hatchery who took care of the juveniles before release: P. Chèvre,L. Jacob, J. St Sevin, D. Mercier, M. Pelard, and R. Fraty. [RH]

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Downstream migration patterns of one-year-old hatchery-reared European sturgeon (Acipenser sturio)

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