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Ecological Indicators 46 (2014) 560–565

Contents lists available at ScienceDirect

Ecological Indicators

jo ur nal ho me page: www.elsev ier .com/ locate / ecol ind

phemeroptera communities as bioindicators of the suitability ofeadwater streams for restocking with white-clawed crayfish,ustropotamobius pallipes

oelle Jandrya, Michel Brulinb, Bernard Parineta, Frédéric Grandjeanc,∗

IC2MP, Equipe Eaux Géochimie Santé, Bât B1, E11 rue Marcel Doré, TSA 41105, 86073 Poitiers Cedex, FranceOPIE, Chemin rural n◦7 BP30, 78041 Guyancourt, FranceLaboratoire Ecologie et Biologie des Interactions—UMR CNRS 7267 Equipe Ecologie Evolution Symbiose—Batiment B8-B35 6, rue Michel Brunet TSA 51106,-86073 Poitiers Cedex, France

r t i c l e i n f o

rticle history:eceived 29 November 2013eceived in revised form 3 July 2014ccepted 6 July 2014

eywords:unning waterestocking

a b s t r a c t

Currently, the distribution of the European native white-clawed crayfish (Austropotamobius pallipes) isrestricted and fragmented over its range. Many European countries have active programmes for con-servation of the species, including reintroduction programmes. Here, we have studied four brooks thatwere restocked with crayfish coming from population rescue from the Brissionnières after a drought insummer 2009. The aim was to validate the use of Ephemeropteran communities as potential bioindi-cators to select brooks for crayfish restocking. Restocked brooks were surveyed in 2010 and 2012. Allbrooks showed chemical and physical parameters in accordance with A. pallipes requirements. Three

ioindicatorseptophlebiidae

hite-clawed crayfish

brooks which had high Ephemeropteran richness including Leptophlebiidae species (Habrophlebia lautaand Paraleptophlebia submarginata) have been restocked successfully. No crayfish were observed duringthe survey in Le Peu, which had only two Ephemeropteran species tolerant of reduced water quality andhad no Leptophlebiidae species. Ecological characteristics of Ephemeropteran species and the limitationsof their use as bioindicators to select brook for restocking are discussed.

. Introduction

Reintroduction programs are powerful tools for stabilizing, re-stablishing, or increasing in situ animal populations that haveuffered significant declines. They can play an important role inhe conservation of threatened species.

The threatened white-clawed crayfish (Austropotamobius pal-ipes) is a good example to illustrate this. For this species, significanteclines are occurring across much of its range. This species is esti-ated to have undergone a 50–80% decline over a 10 year period

ver its global range (Füreder et al., 2010). The maintenance of such decline trend will possibly lead to the extinction on Britain, duringhe next 30 years (Sibley, 2004).

Several factors are contributing to this decline, individuallynd in combination (1) habitat destruction by channelization, (2)

ecrease of water quality by use of agricultural chemicals, (3) theonstruction of ponds or lakes changing the physical and chemicalarameters of brooks inhabited by indigenous crayfish, (4) direct

∗ Corresponding author. Tel.: +33 549454276.E-mail address: frederic.grandjean@univ-poitiers.fr (F. Grandjean).

ttp://dx.doi.org/10.1016/j.ecolind.2014.07.005470-160X/© 2014 Elsevier Ltd. All rights reserved.

© 2014 Elsevier Ltd. All rights reserved.

competition from introduced non-indigenous species, mainly Paci-fastacus leniusculus, Orconectes limosus and Procambarus clarkii (5)crayfish plague carried by American crayfish.

In France, Spain and Italy, A. pallipes mainly occur in headwaters(Souty-Grosset et al., 2006). A national survey conducted by theONEMA (Office National des Eaux et des Milieux Aquatique) hasshown that the number of A. pallipes populations has considerablydeclined over the last 20 years (Changeux, 2003).

In Poitou-Charentes region including four departments, where137 populations were reported in 1978, A. pallipes is now almostcompletely restricted to two departments, with only 45 popu-lations recorded. This represents a decrease around 70% of thepopulation number in 25 years, with a loss of 40% of populations inthe last 6 years (Bramard et al., 2006).

As a result of this decline, A. pallipes has listed in the IUCN redList of endangered species in 2010 (Füreder et al., 2010), as well asbeing listed as a species requiring special conservation measuresin the European Union under the Species and Habitats Directive,

Annex 2.

Restocking of habitats with native crayfish species is amongthe most important current management and conservation options(Taugbol et al., 1992; Reynolds, 1997). However, a restocking

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J. Jandry et al. / Ecologica

rograme requires a set of criteria to indicate whether it wille successful. Those defined so far are related mainly to the ori-in of stocks and habitats (Reynolds, 1998, Reynolds et al., 2000).ecause the white-clawed crayfish is considered to be a speciesomplex (Grandjean et al., 2000a, 2002a,b; Fratini et al., 2005), its important that the genetic composition of the crayfish used intocking is similar to the composition originally present in the areao be restocked. In a recent review of restocking attempts, Souty-rosset and Reynolds (2009) recommended that before restocking,

feasibility study should be done in order to (a) check the taxo-omic status of individuals and confirm that there is an appropriateenetic match, and (b) choose the site of reintroduction. The suit-bility of the area to be restocked is assessed according to: (1)eneral characteristics of the catchment, (2) its physico-chemicalnd ecological particulars, (3) absence of non indigenous cray-sh species, and likelihood of their access, and (4) absence ofphanomyces astaci and other potential pathogenic agents. Souty-rosset and Reynolds (2009) reported from 59 case-studies with6 successful and 33 unsuccessful reintroductions.

The most important factor by far is the absence of non-nativerayfish, because A. pallipes populations cannot co-exist withon-native crayfish Souty-Grosset and Reynolds (2009). Geneticarameters may play a role in the potential of evolution of a pop-lation in the long term, the choice of suitable habitat is probablyhe key factor for the success of the restocking, especially whenestocking concerns species that require very high quality habitats

n regard to physical and chemical parameters (Grandjean et al.,000b, 2001, 2011; Trouilhé et al., 2003, 2007, 2012). Assessmentf the availability of suitable habitat is therefore a key componentn planning a reintroduction. Poor assessment of site to be stocked

BvVienne

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Fig. 1. Map on the connectivity of brooks lo

ators 46 (2014) 560–565 561

can increase the chances that the population will not survive atthe site. Up to now, the selection of a brook for restocking has beenbased on the physicochemical characteristics of the aquatic habitats(Souty-Grosset and Reynolds, 2009) (Fig. 1).

In France, A. pallipes habitats are generally small forest streamswith permanent running water and with a high density of shel-ters such as stones, gravel and roots (Grandjean et al., 2000b, 2003;Trouilhé et al., 2007, 2012). Typically, the width of the brooks isoften less than 2 m and the depth not more than 1 m. Dissolved oxy-gen concentrations range from 7 to 10 mg L−1; water temperaturesdo not exceed 21.8 ◦C during summer; pH values are around 8 andwaters have high conductivity ranging from 140 to 580 �S cm−1

(Trouilhe et al., 2003, 2007). Generally, the sites for restocking arechosen based on few physical and chemical criteria and on a sin-gle field survey, in such cases these parameters have a limitedvalue because it does not reflect the range of conditions experi-enced by the stream over time. In recent studies, Grandjean et al.(2011) and Trouilhé et al. (2012), showed that Ephemeropteranrichness overall and the presence of mayflies of the Leptophlebi-idae family are associated with the presence of A. pallipes. These twostudies highlight that the presence of A. pallipes is associated withspecies of Ephemeroptera sensitive to organic pollution, particu-larly Habroleptoïdes confusa, Habrophlebia fusca, Habrophlebia lautaand Paraleptophlebia submarginata, from the family Leptophlebi-idae. They reported a high Ephemeropteran diversity ranging from4 to 8 species in brooks with A. pallipes.

During, summer 2009, the most dense crayfish population (LesBrissonnières) in Vienne department was severely affected bya period of drought. Technician staff from ONEMA (the Frenchnational fisheries office) rescued 496 crayfish and moved them to

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cated in Vienne department (France).

562 J. Jandry et al. / Ecological Indicators 46 (2014) 560–565

Table 1Details on the number of crayfish, sex ratio and carapace length introduced to four brooks.

Hydrographicdrainage

Brook Introduced number Male Female Number of ind within the totalsize class in mm

<40 40< x <80 >80

Gartempe Ru du Peu 133 60 73 26 66 41

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Gartempe Font-Bignoux 187

Gartempe Ru de Chambon 86

Vienne Oranville 90

our other brooks, in the same region which were less affectedy low flow during the drought. These brooks were chosen duehe absence of exotic crayfish and because their physical aspectslosely resembled those already seen at sites with white-clawedrayfish in this region (Ostrebski, pers. com.). These earlier findingsn a field experiment provided by the actions of fisheries personnelave us a good opportunity to test if Ephemeropteran communitys a good bioindicator to select brooks for restocking attempts withhe white-clawed crayfish as proposed by Grandjean et al. (2011).

e address the following questions regarding Ephemeropteranommunity: (1) Are the presence of Leptophlebiidae family andphemeropteran richness are associated to restocking success (2)hat are the ecological characteristics of Ephemeropteran species

3) what are the limitations of the use of the Ephemeropteran com-unity as bioindicator brooks with crayfish and to use it to select

rooks for restocking attempts in the future.

. Material and methods

.1. Sites for restocking

Four sites (Oranville, Font-Bignoux, Ru du Peu and Ru duhambon) used for restocking are in the upstream areas two hydro-raphic basins (Gartempe & Vienne belonging to the same largeatchment, the Loire) and are closely related geographically to theonor population (Les Brissonières, in the hydrographic basin ofartempe). The sites are located in Poitou-Charentes region in theestern part of France. The sites have moderately fast flowingater with shade from riparian shrubs or trees (Alnus sp., Salix sp.,

orylus avellana) and with a lot of refuges for crayfish (stones andn the banks).

.2. Physical and chemical parameters

The diversity of channel features and substrates (riffles, pools,ravel, cobbles and pebbles, sand) and their abundance were char-cterized for each site. A physical and chemical survey was carriedut on 20–21 April 2010.

For each site, samples of water were taken in 2 L polyethyleneottles and stored at 4 ◦C until analysis, for the measurement ofhysical and chemical parameters linked to the organic matter (tur-idity, TOC, TSS and UV254 nm) and dissolved oxygen, as in Trouilhet al. (2007). In situ measurements of dissolved oxygen (O2), O2aturation %, pH and conductivity (Cond) were recorded using aigital meter (WTW) with the appropriate probes. Water turbidityTurb) was measured, using a HACH Pocket Turbidimeter Cat. no.2600-00. On unfiltered samples, total organic carbon (TOC) wasnalysed using a Shimadzu TOC 5000A analyser, UV absorbance

t 254 nm was measured with a UV–vIS spectrophotometer SAFASES (Double Energy System) 190. Total suspended solids (TSS) was

ecorded as the weight of material retained by the fibreglass filtersF/C millipore membrane.

75 112 94 55 3837 49 43 34 941 49 45 36 9

2.3. Ephemeroptera fauna

The Ephemeropteran communities were identified to specieslevel from IBGN sampling (French biotic index from macroinverte-brates fauna) according to the protocol described in Grandjean et al.(2003). Samplings took place on 15th and 16th april 2010. OnlyEphemeroptera were considered and each individual was identi-fied to species level using a Swiss identification key (Studemannet al., 1992).

Jaccard’s similarity index (Jaccard, 1908) were estimatedbetween donor site community and those found in sites selectedfor restocking.

2.4. Restocking

The donor population of crayfish “Les Brissonières” was locatedin the Gartempe catchment. Crayfish were caught by hand between22nd August to 11th September 2009. Restocking took placein the same period. Crayfish were maintained in ice box withwet vegetation in the bottom. The time between capture andstocking was not exceed three hours. For each stream, cray-fish were released in lenthic part along around two hundredmeters.

Table 1 shows the number of individuals, released at each sites,their sex and size class (size recorded as total length).

2.5. Restocking surveys

Two surveys were carried out between 20th and 30th August in2010 and 2012 respectively. The survey method was by a walkedtransect along 500 m of the brook at night with a light. In 2010, onlythe number of individuals observed was reported. In 2012, crayfishwere caught by hand and sex and carapace length were noted. In LePeu brook, additional investigations were made by using 20 baitedtraps during three days in September 2012 to confirm absence ofcrayfish.

3. Results

3.1. Physical and chemical parameters

The brooks of Ru du Peu, Oranville and Chambon, werephysically similar in nature, with depth around 1.5 m whereas Font-Bignoux site was relatively shallow and narrow compared to theothers with only 0.4 m of depth (Tables 2 and 3).

The cobble was the dominant subtrate for all of the sites. Thecanopy cover was dense for most of them, ranging from 50% to90%.

The chemical parameters were recorded at the four sites were allwithin the range for recorded by Trouilhé et al., 2007, at sites wherewhite-clawed crayfish were present in their extensive survey of theregion.

J. Jandry et al. / Ecological Indicators 46 (2014) 560–565 563

Table 2Physical parameters for the four brooks selected for restocking attempts and for the donor site “Les Brissonnières”. (Values are given as percentage cover, width in metersand depth in cm).

Hydrographic drainage Brook Width Depth Cobble Gravel Sand Litter Aquatic macrophyte Canopy cover Surrounding

Gartempe Ru du Peu 2 25 50 10 30 0 10 50 PastureGartempe Font-Bignoux 0.4 12 40 40 20 0 0 70 Forested PastureGartempe Ru de Chambon 1.5 15 85 5 5 5 0 90 forestedVienne Oranville 1.3 30 85 5 5 5 0 90 forested

Table 3Values of physical and chemical parameters; Ch = Ru du Chambon; Fon = Font-Bignoux; Ora = Oranville and Peu = Ru du Peu. Chemical survey was carried out on 20–21 april2010.

Temp (◦C) pH Cond(�S cm−1)

O2 (mg L−1) % O2 Turb (NTU) UV 254 nm NH4 (mg L−1) TSS (mg L−1) TOC(mg L−1)

Cl (mg L−1) SO4

(mg L−1)

Ch 13.5 8.24 350 8.6 75 3.14 0.27 0.085 28.85 7.093 20.91 6.47Fon 15.6 8.51 370 8.08 74 1.01 0.016 0 42.68 0.675 19.51 3.32Ora 11.3 8.62 444 8.52 88 4.52 0.154 0 50.41 4.702 25.91 6.32Peu 14.3 8.6 195 10.41 101 3.13 0.19 0 17.73 5.29 3.11 23.6

Table 4Occurrence of Ephemeropteran species in the four sites selected for restocking and in the donor site (from Grandjean et al., 2011).

Brook Baetidae Ephemerellidae Ephemeridae Heptagenidae Leptophlebiidae Nb.Sp

B. Rhodani S. ignita E. Danica E. dispar R. semicolorata E. sp P. submarginata H. confusa H. fusca H. lauta

Ru du Peu 15 5 2Font-Bignoux 12 2 2 2 4

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Ru de Chambon 46 15

Oranville 34 5 18

Brissonnières 10 15 2 10

.2. Ephemeropteran communities

In sites selected for restocking, the families of Ephemeropteradentified during our quantitative sampling are recorded in Table 4,

ith one species recorded from each of the families Baetidae,phemerellidae, Ephemeridae and Heptageniidae and three speciesf Leptophlebiidae. Baetis rhodani were most abundant at ourampling sites and appeared in three of four sites. Ecdyonurusispar were present in all sites, whereas one or more species ofeptophlebiidae (Habrophlebia fusca, Habrophlebia lauta and Par-leptophlebia submarginata) were only encountered at three sites.eptophlebiidae are the most sensitive species to organic pollu-ion and are classified in indicator group 7 in the French IBGN onhe scale of biological water quality. Ecological characteristics ofpecies are presented as supplementary data.

There are some differences in Ephemeropteran richness with aotal ranging from 2 species for Ru du Peu to 6 for Ru du Cham-on. The Font-Bignoux and Oranville harboured 4 and 5 species

espectively.

The Jaccard index estimated between these sites and the donorite “Les Brissonnières” was ranged from 0.25 (Ru du Peu) to 0.625Ru du Chambon and Oranville) and 0.5 with Font-Bignoux.

able 5urvey of brooks restocking by A. pallipes in 2010 and 2012.

Brook 2010 Male Fe

Ru du Peu 0 0 0

Font-Bignoux 10 ND NDRu du Chambon 15 ND NDOranville 13 ND ND

Brook 2012 Male Fe

Ru du Peu 0 0 0

Font-Bignoux 19 11 8

Ru du Chambon 42 18 24Oranville 38 21 17

4 3 4 13 64 8 5

25 15 8 8

3.3. Crayfish surveys

Crayfish were recorded at three of the sites (Ru du Chambon,Oranville, and Font-Bignoux) in both 2010 and 2012 (Table 5). Nocrayfish were recorded in the Ru du Peu in either 2010 or 2012.

Breeding of A. pallipes at the three sites was confirmed by thepresence of juvenile crayfish in the size class <40 mm (Grandjeanet al., 1997a,b) (Table 5).

4. Discussion

The monitoring of reintroductions in 2010 and 2012 showedthat three of four restocking attempts were successful with indica-tion of crayfish reproduction (juveniles catches) at three sites threeyears after restocking. The success rate was of 75% for reintroduc-tions and larger than those generally observed for the white-clawedcrayfish. In general review on reintroduction of A. pallipes inEurope, Souty-Grosset and Reynolds (2009) reported from 59 study

findings, that 26 reintroductions were successful and 33 unsuc-cessful. They underlined that more information would be neededon sites chosen for reintroduction. In most cases, no datawere collected about biotic parameters but somethimes on

male number of ind. within the size class in mm

<40 40< x <80 >80

– – – 2 5 3 3 7 5 2 7 4

male number of ind. within the size class in mm<40 40< x <80 >80– – –5 7 7

12 17 13 10 15 13

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64 J. Jandry et al. / Ecologica

hysical–chemical ones. In our study, we showed that selectionf brook for restocking based only on physical–chemical parame-ers was not enough to guarantee the success of reintroduction.ndeed, the Ru du Peu had the physical–chemical requirementsor harbouring white-clawed crayfish according to the findings ofrouilhé et al. (2003, 2007). These authors performed a long surveyf chemical parameters for 2 years with twice monthly samplingrom brooks with white-clawed crayfish. They reported variationf chemical parameters between locations with crayfish and freef crayfish, but these differences were impossible to characterizerom only one field sampling.

In a recent study comprising 29 brooks in Poitou-Charentesegion, Grandjean et al. (2011) reported an association betweenphemeroptera community and A. pallipes sites. This associ-tion was based firstly on richness of mayfly species. Thephemeropteran richness is significantly higher in sites with cray-sh than sites without crayfish. They found the Ephemeropteranichness ranged from four to eight species in sites with crayfishnd 2–6 in those without crayfish. In our study, the Ru du Cham-on, Oranville and Font-Bignoux had 6, 5 and 4 species respectively.he Ru du Peu harboured only 2 species. Secondly, Grandjean et al.2011) reported that the presence of A. pallipes was also associatedith species from the family Leptophlebiidae which are sensitive

o organic pollution, such as Habroleptoïdes confusa, Habrophlebiausca, Habrophlebia lauta and Paraleptophlebia submarginata, Exceptor Ru du Peu, the sites in our study showed at least one species ofeptophebidae.

. Ecological characteristics of ephemeropteran speciesnd limitations of this study

The nine species of mayfly collected in streams sheltering white-lawed crayfish are all found in France, although none are listedn the Red List for France, or in a list of heritage species. Three ofhem, Ephemera danica, Serratella ignita and Baetis rhodani, colonise

any water courses at a wide range of altitudes (data from thenventory of Ephemeroptera of France, Brulin, 2007, 2010, 2011).he first is associated with soft substrates (sand, fine gravel) inhich the fossorial larvae dig their burrows; the other two areore widespread. On the other hand, the other species are linked to

unning water. This is the case for the two Heptageniidae, Rhithro-ena semicolorata and Ecdyonurus dispar, the latter equally at homen the epipotamon, in the gravel beds of the large rivers of thelains where the current is. The four species of Leptophlebiidaere often associated with forested brooks, usually cool, where thearvae disperse rapidly among the larger elements of the substrate,enerally in gravel and small stones barely colonised by periphytonespecially for Habroleptoıdes confusa), among the fine rootlets ofiparian vegetation (Paraleptophlebia submarginata), or in the largerasses of decomposing vegetation—twigs, leaf litter and branches

Habrophlebia lauta or fusca). These substrates were often associ-ted with the presence of A. pallipes which requires a high diversityf microhabitats (Nardi et al., 2005). Rootlets, gravels and stonesffer shelters for juveniles and adults and leaf litter or decomposingegetation are the most important constituent of adult diet (Scalind Gibertini, 2007).

The utilisation of these species as bioindicators of the poten-ial habitat of white-clawed crayfish is reinforced by the fact thathey are well known, widespread in the national territory, and thatheir determination, except for Rhithrogena semicolorata, poses fewroblems for the larval stage. However, sampling campaigns need

o be carried out at the start of Spring to collect the mature larvae,he end of their life cycle being accomplished at this time espe-ially for H. confusa, and P. submarginata. The larvae of these twonivoltine species grow slowly over the winter (Sowa, 1975), and

ators 46 (2014) 560–565

their summer emergence makes their collection necessary beforesummer sampling campaigns.

Saprobic indices associated with these nine species (Moog,2002) show for some a degree of resistance to organic pollu-tion. Their arrangement in decreasing order of sensitivity is asfollows: Habrophlebia fusca: 1.5; Habroleptoıdes confusa, Paralep-tophlebia submarginata: 1.6; Ephemera danica: 1.8; Rhithrogenasemicolorata: 1.9; Habrophlebia lauta: 2.0; Baetis rhodani, Serratellaignita, Ecdyonurus dispar: 2.1. The species best correlated withthe presence of white-clawed crayfish are chiefly three of thecollected Leptophlebiidae, the waters generally characteristic of�-mésosaprobes.

Even if our results are based on limited restocked brooks, theyseem confirm the previous work performed by Grandjean et al.(2011) based on comparison of large number of site harbouringcrayfish and free of crayfish. Ephemeropteran community couldbe used in the selection of brooks for reintroduction of the white-clawed crayfish in Poitou-Charentes region. This study opened newfields of research in the management and the conservation of thewhite-clawed crayfish in Poitou-Charentes region and throughouttheir native range. However, it could be interesting to assess theglobal community of intolerant orders towards the organic disturb-ance like Plecoptera, Trichoptera and some families of Coleoptera.

Acknowledgments

This study was funded by the CPER (Contrat de Plan Etat Region)Programme Transversal Eau, University of Poitiers. We are grate-ful to the members of ONEMA Sébastien Baillargeat, and GérardOstrebski SD 86 (Office National de l’Eau et des Milieux Aquatiques)and Sébastien Joussemet Fédération de Pêche (86) for field assis-tance. We would like to thank Julian Reynolds and Stephanie Peayfor useful comments on the manuscript.

Appendix A. Supplementary data

Supplementary data associated with this article can befound, in the online version, at http://dx.doi.org/10.1016/j.ecolind.2014.07.005.

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