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Ephemeroptera communities as bioindicators of the suitability of headwater streams for restocking with white-clawed crayfish, Austropotamobius pallipes
Ecological Indicators 46 (2014) 560–565
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Ephemeroptera communities as bioindicators of the suitability of headwater streams for restocking with white-clawed crayfish, Austropotamobius pallipes Joelle Jandry a , Michel Brulin b , Bernard Parinet a , Frédéric Grandjean c,∗ a
IC2MP, Equipe Eaux Géochimie Santé, Bât B1, E11 rue Marcel Doré, TSA 41105, 86073 Poitiers Cedex, France OPIE, Chemin rural n◦ 7 BP30, 78041 Guyancourt, France c Laboratoire Ecologie et Biologie des Interactions—UMR CNRS 7267 Equipe Ecologie Evolution Symbiose—Batiment B8-B35 6, rue Michel Brunet TSA 51106, F-86073 Poitiers Cedex, France b
a r t i c l e
i n f o
Article history: Received 29 November 2013 Received in revised form 3 July 2014 Accepted 6 July 2014 Keywords: Running water Restocking Bioindicators Leptophlebiidae White-clawed crayfish
a b s t r a c t Currently, the distribution of the European native white-clawed crayfish (Austropotamobius pallipes) is restricted and fragmented over its range. Many European countries have active programmes for conservation of the species, including reintroduction programmes. Here, we have studied four brooks that were restocked with crayfish coming from population rescue from the Brissionnières after a drought in summer 2009. The aim was to validate the use of Ephemeropteran communities as potential bioindicators to select brooks for crayfish restocking. Restocked brooks were surveyed in 2010 and 2012. All brooks showed chemical and physical parameters in accordance with A. pallipes requirements. Three brooks which had high Ephemeropteran richness including Leptophlebiidae species (Habrophlebia lauta and Paraleptophlebia submarginata) have been restocked successfully. No crayfish were observed during the survey in Le Peu, which had only two Ephemeropteran species tolerant of reduced water quality and had no Leptophlebiidae species. Ecological characteristics of Ephemeropteran species and the limitations of their use as bioindicators to select brook for restocking are discussed. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Reintroduction programs are powerful tools for stabilizing, reestablishing, or increasing in situ animal populations that have suffered significant declines. They can play an important role in the conservation of threatened species. The threatened white-clawed crayfish (Austropotamobius pallipes) is a good example to illustrate this. For this species, significant declines are occurring across much of its range. This species is estimated to have undergone a 50–80% decline over a 10 year period over its global range (Füreder et al., 2010). The maintenance of such a decline trend will possibly lead to the extinction on Britain, during the next 30 years (Sibley, 2004). Several factors are contributing to this decline, individually and in combination (1) habitat destruction by channelization, (2) decrease of water quality by use of agricultural chemicals, (3) the construction of ponds or lakes changing the physical and chemical parameters of brooks inhabited by indigenous crayfish, (4) direct
∗ Corresponding author. Tel.: +33 549454276. E-mail address: [email protected] (F. Grandjean). http://dx.doi.org/10.1016/j.ecolind.2014.07.005 1470-160X/© 2014 Elsevier Ltd. All rights reserved.
competition from introduced non-indigenous species, mainly Pacifastacus 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 the ONEMA (Office National des Eaux et des Milieux Aquatique) has shown that the number of A. pallipes populations has considerably declined over the last 20 years (Changeux, 2003). In Poitou-Charentes region including four departments, where 137 populations were reported in 1978, A. pallipes is now almost completely restricted to two departments, with only 45 populations recorded. This represents a decrease around 70% of the population number in 25 years, with a loss of 40% of populations in the last 6 years (Bramard et al., 2006). As a result of this decline, A. pallipes has listed in the IUCN red List of endangered species in 2010 (Füreder et al., 2010), as well as being listed as a species requiring special conservation measures in the European Union under the Species and Habitats Directive, Annex 2. Restocking of habitats with native crayfish species is among the most important current management and conservation options (Taugbol et al., 1992; Reynolds, 1997). However, a restocking
J. Jandry et al. / Ecological Indicators 46 (2014) 560–565
programe requires a set of criteria to indicate whether it will be successful. Those defined so far are related mainly to the origin of stocks and habitats (Reynolds, 1998, Reynolds et al., 2000). Because the white-clawed crayfish is considered to be a species complex (Grandjean et al., 2000a, 2002a,b; Fratini et al., 2005), it is important that the genetic composition of the crayfish used in stocking is similar to the composition originally present in the area to be restocked. In a recent review of restocking attempts, SoutyGrosset and Reynolds (2009) recommended that before restocking, a feasibility study should be done in order to (a) check the taxonomic status of individuals and confirm that there is an appropriate genetic match, and (b) choose the site of reintroduction. The suitability of the area to be restocked is assessed according to: (1) general characteristics of the catchment, (2) its physico-chemical and ecological particulars, (3) absence of non indigenous crayfish species, and likelihood of their access, and (4) absence of Aphanomyces astaci and other potential pathogenic agents. SoutyGrosset and Reynolds (2009) reported from 59 case-studies with 26 successful and 33 unsuccessful reintroductions. The most important factor by far is the absence of non-native crayfish, because A. pallipes populations cannot co-exist with non-native crayfish Souty-Grosset and Reynolds (2009). Genetic parameters may play a role in the potential of evolution of a population in the long term, the choice of suitable habitat is probably the key factor for the success of the restocking, especially when restocking concerns species that require very high quality habitats in regard to physical and chemical parameters (Grandjean et al., 2000b, 2001, 2011; Trouilhé et al., 2003, 2007, 2012). Assessment of the availability of suitable habitat is therefore a key component in planning a reintroduction. Poor assessment of site to be stocked
561
can increase the chances that the population will not survive at the site. Up to now, the selection of a brook for restocking has been based on the physicochemical characteristics of the aquatic habitats (Souty-Grosset and Reynolds, 2009) (Fig. 1). In France, A. pallipes habitats are generally small forest streams with permanent running water and with a high density of shelters such as stones, gravel and roots (Grandjean et al., 2000b, 2003; Trouilhé et al., 2007, 2012). Typically, the width of the brooks is often less than 2 m and the depth not more than 1 m. Dissolved oxygen concentrations range from 7 to 10 mg L−1 ; water temperatures do not exceed 21.8 ◦ C during summer; pH values are around 8 and waters have high conductivity ranging from 140 to 580 S cm−1 (Trouilhe´ et al., 2003, 2007). Generally, the sites for restocking are chosen based on few physical and chemical criteria and on a single field survey, in such cases these parameters have a limited value because it does not reflect the range of conditions experienced by the stream over time. In recent studies, Grandjean et al. (2011) and Trouilhé et al. (2012), showed that Ephemeropteran richness overall and the presence of mayflies of the Leptophlebiidae family are associated with the presence of A. pallipes. These two studies highlight that the presence of A. pallipes is associated with species of Ephemeroptera sensitive to organic pollution, particularly Habroleptoïdes confusa, Habrophlebia fusca, Habrophlebia lauta and Paraleptophlebia submarginata, from the family Leptophlebiidae. They reported a high Ephemeropteran diversity ranging from 4 to 8 species in brooks with A. pallipes. During, summer 2009, the most dense crayfish population (Les Brissonnières) in Vienne department was severely affected by a period of drought. Technician staff from ONEMA (the French national fisheries office) rescued 496 crayfish and moved them to
Bv
0
nne Vie Bv
Cl ai n
Poitiers
Montmorillon
Fb Ch Or
Bri Pe
bv Ga r
Fig. 1. Map on the connectivity of brooks located in Vienne department (France).
temp
e
562
J. Jandry et al. / Ecological Indicators 46 (2014) 560–565
Table 1 Details on the number of crayfish, sex ratio and carapace length introduced to four brooks. Hydrographic drainage
Gartempe Gartempe Gartempe Vienne
Brook
Ru du Peu Font-Bignoux Ru de Chambon Oranville
Introduced number
133 187 86 90
four other brooks, in the same region which were less affected by low flow during the drought. These brooks were chosen due the absence of exotic crayfish and because their physical aspects closely resembled those already seen at sites with white-clawed crayfish in this region (Ostrebski, pers. com.). These earlier findings in a field experiment provided by the actions of fisheries personnel gave us a good opportunity to test if Ephemeropteran community is a good bioindicator to select brooks for restocking attempts with the white-clawed crayfish as proposed by Grandjean et al. (2011). We address the following questions regarding Ephemeropteran community: (1) Are the presence of Leptophlebiidae family and Ephemeropteran richness are associated to restocking success (2) What are the ecological characteristics of Ephemeropteran species (3) what are the limitations of the use of the Ephemeropteran community as bioindicator brooks with crayfish and to use it to select brooks for restocking attempts in the future.
2. Material and methods 2.1. Sites for restocking Four sites (Oranville, Font-Bignoux, Ru du Peu and Ru du Chambon) used for restocking are in the upstream areas two hydrographic basins (Gartempe & Vienne belonging to the same large catchment, the Loire) and are closely related geographically to the donor population (Les Brissonières, in the hydrographic basin of Gartempe). The sites are located in Poitou-Charentes region in the western part of France. The sites have moderately fast flowing water with shade from riparian shrubs or trees (Alnus sp., Salix sp., Corylus avellana) and with a lot of refuges for crayfish (stones and in the banks).
2.2. Physical and chemical parameters The diversity of channel features and substrates (riffles, pools, gravel, cobbles and pebbles, sand) and their abundance were characterized for each site. A physical and chemical survey was carried out on 20–21 April 2010. For each site, samples of water were taken in 2 L polyethylene bottles and stored at 4 ◦ C until analysis, for the measurement of physical and chemical parameters linked to the organic matter (turbidity, TOC, TSS and UV254 nm) and dissolved oxygen, as in Trouilhe´ et al. (2007). In situ measurements of dissolved oxygen (O2 ), O2 saturation %, pH and conductivity (Cond) were recorded using a digital meter (WTW) with the appropriate probes. Water turbidity (Turb) was measured, using a HACH Pocket Turbidimeter Cat. no. 52600-00. On unfiltered samples, total organic carbon (TOC) was analysed using a Shimadzu TOC 5000A analyser, UV absorbance at 254 nm was measured with a UV–vIS spectrophotometer SAFAS DES (Double Energy System) 190. Total suspended solids (TSS) was recorded as the weight of material retained by the fibreglass filters GF/C millipore membrane.
Male
60 75 37 41
Female
73 112 49 49
Number of ind within the total size class in mm <40
40< x <80
>80
26 94 43 45
66 55 34 36
41 38 9 9
2.3. Ephemeroptera fauna The Ephemeropteran communities were identified to species level from IBGN sampling (French biotic index from macroinvertebrates fauna) according to the protocol described in Grandjean et al. (2003). Samplings took place on 15th and 16th april 2010. Only Ephemeroptera were considered and each individual was identified to species level using a Swiss identification key (Studemann et al., 1992). Jaccard’s similarity index (Jaccard, 1908) were estimated between donor site community and those found in sites selected for restocking.
2.4. Restocking The donor population of crayfish “Les Brissonières” was located in the Gartempe catchment. Crayfish were caught by hand between 22nd August to 11th September 2009. Restocking took place in the same period. Crayfish were maintained in ice box with wet vegetation in the bottom. The time between capture and stocking was not exceed three hours. For each stream, crayfish were released in lenthic part along around two hundred meters. 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 in 2010 and 2012 respectively. The survey method was by a walked transect along 500 m of the brook at night with a light. In 2010, only the number of individuals observed was reported. In 2012, crayfish were caught by hand and sex and carapace length were noted. In Le Peu brook, additional investigations were made by using 20 baited traps during three days in September 2012 to confirm absence of crayfish.
3. Results 3.1. Physical and chemical parameters The brooks of Ru du Peu, Oranville and Chambon, were physically similar in nature, with depth around 1.5 m whereas FontBignoux site was relatively shallow and narrow compared to the others with only 0.4 m of depth (Tables 2 and 3). The cobble was the dominant subtrate for all of the sites. The canopy cover was dense for most of them, ranging from 50% to 90%. The chemical parameters were recorded at the four sites were all within the range for recorded by Trouilhé et al., 2007, at sites where white-clawed crayfish were present in their extensive survey of the region.
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Table 2 Physical parameters for the four brooks selected for restocking attempts and for the donor site “Les Brissonnières”. (Values are given as percentage cover, width in meters and depth in cm). Hydrographic drainage
Brook
Width
Depth
Cobble
Gravel
Sand
Litter
Aquatic macrophyte
Canopy cover
Surrounding
Gartempe Gartempe Gartempe Vienne
Ru du Peu Font-Bignoux Ru de Chambon Oranville
2 0.4 1.5 1.3
25 12 15 30
50 40 85 85
10 40 5 5
30 20 5 5
0 0 5 5
10 0 0 0
50 70 90 90
Pasture Forested Pasture forested forested
Table 3 Values 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 april 2010.
Ch Fon Ora Peu
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 )
13.5 15.6 11.3 14.3
8.24 8.51 8.62 8.6
350 370 444 195
8.6 8.08 8.52 10.41
75 74 88 101
3.14 1.01 4.52 3.13
0.27 0.016 0.154 0.19
0.085 0 0 0
28.85 42.68 50.41 17.73
7.093 0.675 4.702 5.29
20.91 19.51 25.91 3.11
6.47 3.32 6.32 23.6
Table 4 Occurrence of Ephemeropteran species in the four sites selected for restocking and in the donor site (from Grandjean et al., 2011). Brook
Ru du Peu Font-Bignoux Ru de Chambon Oranville Brissonnières
Baetidae
Ephemerellidae
Ephemeridae
Heptagenidae
B. Rhodani
S. ignita
E. Danica
E. dispar
15 12 46 34 10
5 2 15 18 10
2
15
5 2
3.2. Ephemeropteran communities
Leptophlebiidae
R. semicolorata
E. sp
P. submarginata
4 32
25
H. confusa
3 4 15
H. fusca
4
Nb. Sp
H. lauta
2 4 6 5 8
2 13 8 8
3.3. Crayfish surveys
In sites selected for restocking, the families of Ephemeroptera identified during our quantitative sampling are recorded in Table 4, with one species recorded from each of the families Baetidae, Ephemerellidae, Ephemeridae and Heptageniidae and three species of Leptophlebiidae. Baetis rhodani were most abundant at our sampling sites and appeared in three of four sites. Ecdyonurus dispar were present in all sites, whereas one or more species of Leptophlebiidae (Habrophlebia fusca, Habrophlebia lauta and Paraleptophlebia submarginata) were only encountered at three sites. Leptophlebiidae are the most sensitive species to organic pollution and are classified in indicator group 7 in the French IBGN on the scale of biological water quality. Ecological characteristics of species are presented as supplementary data. There are some differences in Ephemeropteran richness with a total ranging from 2 species for Ru du Peu to 6 for Ru du Chambon. The Font-Bignoux and Oranville harboured 4 and 5 species respectively. The Jaccard index estimated between these sites and the donor site “Les Brissonnières” was ranged from 0.25 (Ru du Peu) to 0.625 (Ru du Chambon and Oranville) and 0.5 with Font-Bignoux.
Crayfish were recorded at three of the sites (Ru du Chambon, Oranville, and Font-Bignoux) in both 2010 and 2012 (Table 5). No crayfish were recorded in the Ru du Peu in either 2010 or 2012. Breeding of A. pallipes at the three sites was confirmed by the presence of juvenile crayfish in the size class <40 mm (Grandjean et al., 1997a,b) (Table 5). 4. Discussion The monitoring of reintroductions in 2010 and 2012 showed that three of four restocking attempts were successful with indication of crayfish reproduction (juveniles catches) at three sites three years after restocking. The success rate was of 75% for reintroductions and larger than those generally observed for the white-clawed crayfish. In general review on reintroduction of A. pallipes in Europe, Souty-Grosset and Reynolds (2009) reported from 59 study findings, that 26 reintroductions were successful and 33 unsuccessful. They underlined that more information would be needed on sites chosen for reintroduction. In most cases, no data were collected about biotic parameters but somethimes on
Table 5 Survey of brooks restocking by A. pallipes in 2010 and 2012. Brook
2010
Male
Female
number of ind. within the size class in mm <40
40< x <80
>80
Ru du Peu Font-Bignoux Ru du Chambon Oranville
0 10 15 13
0 ND ND ND
0 ND ND ND
– 2 3 2
– 5 7 7
– 3 5 4
Brook
2012
Male
Female
Ru du Peu Font-Bignoux Ru du Chambon Oranville
0 19 42 38
0 11 18 21
0 8 24 17
number of ind. within the size class in mm <40 40< x <80 – – 5 7 12 17 10 15
>80 – 7 13 13
564
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physical–chemical ones. In our study, we showed that selection of brook for restocking based only on physical–chemical parameters was not enough to guarantee the success of reintroduction. Indeed, the Ru du Peu had the physical–chemical requirements for harbouring white-clawed crayfish according to the findings of Trouilhé et al. (2003, 2007). These authors performed a long survey of chemical parameters for 2 years with twice monthly sampling from brooks with white-clawed crayfish. They reported variation of chemical parameters between locations with crayfish and free of crayfish, but these differences were impossible to characterize from only one field sampling. In a recent study comprising 29 brooks in Poitou-Charentes region, Grandjean et al. (2011) reported an association between Ephemeroptera community and A. pallipes sites. This association was based firstly on richness of mayfly species. The Ephemeropteran richness is significantly higher in sites with crayfish than sites without crayfish. They found the Ephemeropteran richness ranged from four to eight species in sites with crayfish and 2–6 in those without crayfish. In our study, the Ru du Chambon, Oranville and Font-Bignoux had 6, 5 and 4 species respectively. The Ru du Peu harboured only 2 species. Secondly, Grandjean et al. (2011) reported that the presence of A. pallipes was also associated with species from the family Leptophlebiidae which are sensitive to organic pollution, such as Habroleptoïdes confusa, Habrophlebia fusca, Habrophlebia lauta and Paraleptophlebia submarginata, Except for Ru du Peu, the sites in our study showed at least one species of Leptophebidae.
5. Ecological characteristics of ephemeropteran species and limitations of this study The nine species of mayfly collected in streams sheltering whiteclawed crayfish are all found in France, although none are listed in the Red List for France, or in a list of heritage species. Three of them, Ephemera danica, Serratella ignita and Baetis rhodani, colonise many water courses at a wide range of altitudes (data from the Inventory of Ephemeroptera of France, Brulin, 2007, 2010, 2011). The first is associated with soft substrates (sand, fine gravel) in which the fossorial larvae dig their burrows; the other two are more widespread. On the other hand, the other species are linked to running water. This is the case for the two Heptageniidae, Rhithrogena semicolorata and Ecdyonurus dispar, the latter equally at home in the epipotamon, in the gravel beds of the large rivers of the plains where the current is. The four species of Leptophlebiidae are often associated with forested brooks, usually cool, where the larvae disperse rapidly among the larger elements of the substrate, generally in gravel and small stones barely colonised by periphyton (especially for Habrolepto¨ıdes confusa), among the fine rootlets of riparian vegetation (Paraleptophlebia submarginata), or in the larger masses of decomposing vegetation—twigs, leaf litter and branches (Habrophlebia lauta or fusca). These substrates were often associated with the presence of A. pallipes which requires a high diversity of microhabitats (Nardi et al., 2005). Rootlets, gravels and stones offer shelters for juveniles and adults and leaf litter or decomposing vegetation are the most important constituent of adult diet (Scali and Gibertini, 2007). The utilisation of these species as bioindicators of the potential habitat of white-clawed crayfish is reinforced by the fact that they are well known, widespread in the national territory, and that their determination, except for Rhithrogena semicolorata, poses few problems for the larval stage. However, sampling campaigns need to be carried out at the start of Spring to collect the mature larvae, the end of their life cycle being accomplished at this time especially for H. confusa, and P. submarginata. The larvae of these two univoltine species grow slowly over the winter (Sowa, 1975), and
their summer emergence makes their collection necessary before summer sampling campaigns. Saprobic indices associated with these nine species (Moog, 2002) show for some a degree of resistance to organic pollution. Their arrangement in decreasing order of sensitivity is as follows: Habrophlebia fusca: 1.5; Habrolepto¨ıdes confusa, Paraleptophlebia submarginata: 1.6; Ephemera danica: 1.8; Rhithrogena semicolorata: 1.9; Habrophlebia lauta: 2.0; Baetis rhodani, Serratella ignita, Ecdyonurus dispar: 2.1. The species best correlated with the presence of white-clawed crayfish are chiefly three of the collected Leptophlebiidae, the waters generally characteristic of -mésosaprobes. Even if our results are based on limited restocked brooks, they seem confirm the previous work performed by Grandjean et al. (2011) based on comparison of large number of site harbouring crayfish and free of crayfish. Ephemeropteran community could be used in the selection of brooks for reintroduction of the whiteclawed crayfish in Poitou-Charentes region. This study opened new fields of research in the management and the conservation of the white-clawed crayfish in Poitou-Charentes region and throughout their native range. However, it could be interesting to assess the global community of intolerant orders towards the organic disturbance 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 grateful to the members of ONEMA Sébastien Baillargeat, and Gérard Ostrebski SD 86 (Office National de l’Eau et des Milieux Aquatiques) and Sébastien Joussemet Fédération de Pêche (86) for field assistance. We would like to thank Julian Reynolds and Stephanie Peay for useful comments on the manuscript. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.ecolind.2014.07.005. References ´ M.-C., Bachelier, E., Dumas, J.-C., Fournier, C., Bramard, M., Demers, A., Trouilhe, Broussard, E., Robin, O., Souty-Grosset, C., Grandjean, F., 2006. Distribution of indigenous and non-indigenous crayfish populations in the Poitou-Charentes region: evolution over the past 25 years. Bull. Franc¸ais Pêche Piscic. 380-381, 857–860. Brulin, M., 2007. Atlas de distribution des Éphémères de France. 1ère partie: hors Baetidae et Heptageniidae (Insecta, Ephemeroptera). Ephemera 8 (1), 1–73. Brulin, M., 2010. Atlas de distribution des Éphémères de France, 2ème partie: famille des Heptageniidae (Ephemeroptera). Ephemera 11 (2), 71–133. Brulin, M., 2011. Atlas de distribution des Éphémères de France, 3ème partie: familles des Ametropodidae et des Baetidae (Ephemeroptera). Ephemera 12 (2), 65–109. Changeux, T., 2003. Changes in crayfish distribution in metropolitan France according to the national surveys performed by the Conseil Supérieur de la Pêche from 1997 to 2001. Bull. Franc¸ais Pêche Piscic. 370-371, 15–41. Füreder, L., Gherardi, F., Holdich, D., Reynolds, J., Sibley, P., Souty-Grosset, C., 2010. IUCN 2010. IUCN Red list of Threatened Species. Version2010.4. www.iucnredlist.org Grandjean, F., Romain, D., Souty-Grosset, C., Mocquard, J.P., 1997a. Size at sexual maturity and morphometric variability in three populations of Austropotamobius pallipes pallipes according to a restocking strategy. Crustaceana 70 (1), 31–44. Grandjean, F., Romain, D., Avila-Zarza, C., Bramard, M., Souty-Grosset, C., Mocquard, J.P., 1997b. Morphometry, Size at maturity and sexual size dimorphism of the white-clawed crayfish Austropotamobius pallipes pallipes(Lereboullet) from a wild french population (Deux-Sèvres). Crustaceana 70 (4), 454–468. Grandjean, F., Harris, D.J., Souty-Grosset, C., Crandall, K.A., 2000a. Systematics of the European endangered crayfish species, Austropotamobius pallipes (Decapoda: Astacidae). J. Crustac. Biol. 20 (3), 522–529. Grandjean, F., Cornuault, B., Archambault, S., Bramard, M., Otrebsky, G., 2000b. Life history and population biology of the white-clawed crayfish, Austropotamobius
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Reynolds, J.D., Souty-Grosset, C., Gouin, N., Devaney, S., Grandjean, F., 2000. Experimental restocking of native cratfish in White lake, Co. Westmeath, Ireland. In: Rogers, D., Bickland, J. (Eds.), Crayfish Conference Leeds. Environment agency, Leeds, pp. 123–130. Scali, M., Gibertini, G., 2007. Feeding habits of the crayfish Austropotamobius pallipes (Decapoda, Astacidae) in a brook in Latium (central Italy). Ital. J. Zool. 74 (2), 157–168. Sibley, P.J., 2004. Conservation management and legislation—the UK experience. Bull. Fr. Pêche Piscic., vol.369–370. Souty-Grosset, C., Reynolds, J., 2009. Current ideas on methodological approaches in European crayfish conservation and restocking procedures. Knowl. Manag. Aquat. Ecosyst. 394-395, 01–11. Souty-Grosset, C., Holdich, D.M., Noël, P.Y., Reynolds, J.D., Haffner, P., 2006. Crayfish conservation and management. In Souty-Grosset, C., Holdich, D.M., Noël, P.Y., Reynolds, J.D., Haffner, P. (eds). Atlas of Crayfish in Europe. MNHN, Paris (Patrimoines naturels, 64): 187 pp. Sowa, R., 1975. Ecology and biogeography of mayflies (Ephemeroptera) of running waters in the Polish part of the Carpathians, 2. Life cycles. Acta Hydrobiol. 17 (4), 319–353. Studemann, D., Landolt, P., Sartori, M., Hefti, D., Tomka, I., 1992. Ephemeroptera (French version). In: Société ento-mologique suisse (ed.): Insecta Helvetica Fauna, pp. 1–174. Taugbol, T., Skurdal, J., Hastein, T., 1992. Crayfish plague and management strategies in Norway. Biol. Conserv. 63, 75–82. ´ M.C., Ricard, F., Parinet, B., Grandjean, F., Souty-Grosset, C., 2003. ManTrouilhe, agement of the white-clawed crayfish (Austropotamobius pallipes) in western France. Bull. Fr. Pêche Piscic. 370-371, 97–114. ´ M.-C., Souty-Grosset, C., Grandjean, F., Parinet, B., 2007. Physical and Trouilhe, chemical water requirements of the white-clawed crayfish (Austropotamobius pallipes) in western France. Aquat. Conserv.: Mar. Freshw. Ecosyst. 17 (5), 520–538. Trouilhé, M.-C., Freyssinel, G., Jandry, J., Brulin, M., Parinet, B., Souty-Grosset, C., Grandjean, F., 2012. The relationship between Ephemeroptera and presence of the white-clawed crayfish (Austropotamobius pallipes), Case study in the PoitouCharentes (France). Fundam. Appl. Limnol. 179 (4), 293–303.
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Ecological Indicators journal homepage: www.elsevier.com/locate/ecolind
Ephemeroptera communities as bioindicators of the suitability of headwater streams for restocking with white-clawed crayfish, Austropotamobius pallipes Joelle Jandry a , Michel Brulin b , Bernard Parinet a , Frédéric Grandjean c,∗ a
IC2MP, Equipe Eaux Géochimie Santé, Bât B1, E11 rue Marcel Doré, TSA 41105, 86073 Poitiers Cedex, France OPIE, Chemin rural n◦ 7 BP30, 78041 Guyancourt, France c Laboratoire Ecologie et Biologie des Interactions—UMR CNRS 7267 Equipe Ecologie Evolution Symbiose—Batiment B8-B35 6, rue Michel Brunet TSA 51106, F-86073 Poitiers Cedex, France b
a r t i c l e
i n f o
Article history: Received 29 November 2013 Received in revised form 3 July 2014 Accepted 6 July 2014 Keywords: Running water Restocking Bioindicators Leptophlebiidae White-clawed crayfish
a b s t r a c t Currently, the distribution of the European native white-clawed crayfish (Austropotamobius pallipes) is restricted and fragmented over its range. Many European countries have active programmes for conservation of the species, including reintroduction programmes. Here, we have studied four brooks that were restocked with crayfish coming from population rescue from the Brissionnières after a drought in summer 2009. The aim was to validate the use of Ephemeropteran communities as potential bioindicators to select brooks for crayfish restocking. Restocked brooks were surveyed in 2010 and 2012. All brooks showed chemical and physical parameters in accordance with A. pallipes requirements. Three brooks which had high Ephemeropteran richness including Leptophlebiidae species (Habrophlebia lauta and Paraleptophlebia submarginata) have been restocked successfully. No crayfish were observed during the survey in Le Peu, which had only two Ephemeropteran species tolerant of reduced water quality and had no Leptophlebiidae species. Ecological characteristics of Ephemeropteran species and the limitations of their use as bioindicators to select brook for restocking are discussed. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Reintroduction programs are powerful tools for stabilizing, reestablishing, or increasing in situ animal populations that have suffered significant declines. They can play an important role in the conservation of threatened species. The threatened white-clawed crayfish (Austropotamobius pallipes) is a good example to illustrate this. For this species, significant declines are occurring across much of its range. This species is estimated to have undergone a 50–80% decline over a 10 year period over its global range (Füreder et al., 2010). The maintenance of such a decline trend will possibly lead to the extinction on Britain, during the next 30 years (Sibley, 2004). Several factors are contributing to this decline, individually and in combination (1) habitat destruction by channelization, (2) decrease of water quality by use of agricultural chemicals, (3) the construction of ponds or lakes changing the physical and chemical parameters of brooks inhabited by indigenous crayfish, (4) direct
∗ Corresponding author. Tel.: +33 549454276. E-mail address: [email protected] (F. Grandjean). http://dx.doi.org/10.1016/j.ecolind.2014.07.005 1470-160X/© 2014 Elsevier Ltd. All rights reserved.
competition from introduced non-indigenous species, mainly Pacifastacus 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 the ONEMA (Office National des Eaux et des Milieux Aquatique) has shown that the number of A. pallipes populations has considerably declined over the last 20 years (Changeux, 2003). In Poitou-Charentes region including four departments, where 137 populations were reported in 1978, A. pallipes is now almost completely restricted to two departments, with only 45 populations recorded. This represents a decrease around 70% of the population number in 25 years, with a loss of 40% of populations in the last 6 years (Bramard et al., 2006). As a result of this decline, A. pallipes has listed in the IUCN red List of endangered species in 2010 (Füreder et al., 2010), as well as being listed as a species requiring special conservation measures in the European Union under the Species and Habitats Directive, Annex 2. Restocking of habitats with native crayfish species is among the most important current management and conservation options (Taugbol et al., 1992; Reynolds, 1997). However, a restocking
J. Jandry et al. / Ecological Indicators 46 (2014) 560–565
programe requires a set of criteria to indicate whether it will be successful. Those defined so far are related mainly to the origin of stocks and habitats (Reynolds, 1998, Reynolds et al., 2000). Because the white-clawed crayfish is considered to be a species complex (Grandjean et al., 2000a, 2002a,b; Fratini et al., 2005), it is important that the genetic composition of the crayfish used in stocking is similar to the composition originally present in the area to be restocked. In a recent review of restocking attempts, SoutyGrosset and Reynolds (2009) recommended that before restocking, a feasibility study should be done in order to (a) check the taxonomic status of individuals and confirm that there is an appropriate genetic match, and (b) choose the site of reintroduction. The suitability of the area to be restocked is assessed according to: (1) general characteristics of the catchment, (2) its physico-chemical and ecological particulars, (3) absence of non indigenous crayfish species, and likelihood of their access, and (4) absence of Aphanomyces astaci and other potential pathogenic agents. SoutyGrosset and Reynolds (2009) reported from 59 case-studies with 26 successful and 33 unsuccessful reintroductions. The most important factor by far is the absence of non-native crayfish, because A. pallipes populations cannot co-exist with non-native crayfish Souty-Grosset and Reynolds (2009). Genetic parameters may play a role in the potential of evolution of a population in the long term, the choice of suitable habitat is probably the key factor for the success of the restocking, especially when restocking concerns species that require very high quality habitats in regard to physical and chemical parameters (Grandjean et al., 2000b, 2001, 2011; Trouilhé et al., 2003, 2007, 2012). Assessment of the availability of suitable habitat is therefore a key component in planning a reintroduction. Poor assessment of site to be stocked
561
can increase the chances that the population will not survive at the site. Up to now, the selection of a brook for restocking has been based on the physicochemical characteristics of the aquatic habitats (Souty-Grosset and Reynolds, 2009) (Fig. 1). In France, A. pallipes habitats are generally small forest streams with permanent running water and with a high density of shelters such as stones, gravel and roots (Grandjean et al., 2000b, 2003; Trouilhé et al., 2007, 2012). Typically, the width of the brooks is often less than 2 m and the depth not more than 1 m. Dissolved oxygen concentrations range from 7 to 10 mg L−1 ; water temperatures do not exceed 21.8 ◦ C during summer; pH values are around 8 and waters have high conductivity ranging from 140 to 580 S cm−1 (Trouilhe´ et al., 2003, 2007). Generally, the sites for restocking are chosen based on few physical and chemical criteria and on a single field survey, in such cases these parameters have a limited value because it does not reflect the range of conditions experienced by the stream over time. In recent studies, Grandjean et al. (2011) and Trouilhé et al. (2012), showed that Ephemeropteran richness overall and the presence of mayflies of the Leptophlebiidae family are associated with the presence of A. pallipes. These two studies highlight that the presence of A. pallipes is associated with species of Ephemeroptera sensitive to organic pollution, particularly Habroleptoïdes confusa, Habrophlebia fusca, Habrophlebia lauta and Paraleptophlebia submarginata, from the family Leptophlebiidae. They reported a high Ephemeropteran diversity ranging from 4 to 8 species in brooks with A. pallipes. During, summer 2009, the most dense crayfish population (Les Brissonnières) in Vienne department was severely affected by a period of drought. Technician staff from ONEMA (the French national fisheries office) rescued 496 crayfish and moved them to
Bv
0
nne Vie Bv
Cl ai n
Poitiers
Montmorillon
Fb Ch Or
Bri Pe
bv Ga r
Fig. 1. Map on the connectivity of brooks located in Vienne department (France).
temp
e
562
J. Jandry et al. / Ecological Indicators 46 (2014) 560–565
Table 1 Details on the number of crayfish, sex ratio and carapace length introduced to four brooks. Hydrographic drainage
Gartempe Gartempe Gartempe Vienne
Brook
Ru du Peu Font-Bignoux Ru de Chambon Oranville
Introduced number
133 187 86 90
four other brooks, in the same region which were less affected by low flow during the drought. These brooks were chosen due the absence of exotic crayfish and because their physical aspects closely resembled those already seen at sites with white-clawed crayfish in this region (Ostrebski, pers. com.). These earlier findings in a field experiment provided by the actions of fisheries personnel gave us a good opportunity to test if Ephemeropteran community is a good bioindicator to select brooks for restocking attempts with the white-clawed crayfish as proposed by Grandjean et al. (2011). We address the following questions regarding Ephemeropteran community: (1) Are the presence of Leptophlebiidae family and Ephemeropteran richness are associated to restocking success (2) What are the ecological characteristics of Ephemeropteran species (3) what are the limitations of the use of the Ephemeropteran community as bioindicator brooks with crayfish and to use it to select brooks for restocking attempts in the future.
2. Material and methods 2.1. Sites for restocking Four sites (Oranville, Font-Bignoux, Ru du Peu and Ru du Chambon) used for restocking are in the upstream areas two hydrographic basins (Gartempe & Vienne belonging to the same large catchment, the Loire) and are closely related geographically to the donor population (Les Brissonières, in the hydrographic basin of Gartempe). The sites are located in Poitou-Charentes region in the western part of France. The sites have moderately fast flowing water with shade from riparian shrubs or trees (Alnus sp., Salix sp., Corylus avellana) and with a lot of refuges for crayfish (stones and in the banks).
2.2. Physical and chemical parameters The diversity of channel features and substrates (riffles, pools, gravel, cobbles and pebbles, sand) and their abundance were characterized for each site. A physical and chemical survey was carried out on 20–21 April 2010. For each site, samples of water were taken in 2 L polyethylene bottles and stored at 4 ◦ C until analysis, for the measurement of physical and chemical parameters linked to the organic matter (turbidity, TOC, TSS and UV254 nm) and dissolved oxygen, as in Trouilhe´ et al. (2007). In situ measurements of dissolved oxygen (O2 ), O2 saturation %, pH and conductivity (Cond) were recorded using a digital meter (WTW) with the appropriate probes. Water turbidity (Turb) was measured, using a HACH Pocket Turbidimeter Cat. no. 52600-00. On unfiltered samples, total organic carbon (TOC) was analysed using a Shimadzu TOC 5000A analyser, UV absorbance at 254 nm was measured with a UV–vIS spectrophotometer SAFAS DES (Double Energy System) 190. Total suspended solids (TSS) was recorded as the weight of material retained by the fibreglass filters GF/C millipore membrane.
Male
60 75 37 41
Female
73 112 49 49
Number of ind within the total size class in mm <40
40< x <80
>80
26 94 43 45
66 55 34 36
41 38 9 9
2.3. Ephemeroptera fauna The Ephemeropteran communities were identified to species level from IBGN sampling (French biotic index from macroinvertebrates fauna) according to the protocol described in Grandjean et al. (2003). Samplings took place on 15th and 16th april 2010. Only Ephemeroptera were considered and each individual was identified to species level using a Swiss identification key (Studemann et al., 1992). Jaccard’s similarity index (Jaccard, 1908) were estimated between donor site community and those found in sites selected for restocking.
2.4. Restocking The donor population of crayfish “Les Brissonières” was located in the Gartempe catchment. Crayfish were caught by hand between 22nd August to 11th September 2009. Restocking took place in the same period. Crayfish were maintained in ice box with wet vegetation in the bottom. The time between capture and stocking was not exceed three hours. For each stream, crayfish were released in lenthic part along around two hundred meters. 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 in 2010 and 2012 respectively. The survey method was by a walked transect along 500 m of the brook at night with a light. In 2010, only the number of individuals observed was reported. In 2012, crayfish were caught by hand and sex and carapace length were noted. In Le Peu brook, additional investigations were made by using 20 baited traps during three days in September 2012 to confirm absence of crayfish.
3. Results 3.1. Physical and chemical parameters The brooks of Ru du Peu, Oranville and Chambon, were physically similar in nature, with depth around 1.5 m whereas FontBignoux site was relatively shallow and narrow compared to the others with only 0.4 m of depth (Tables 2 and 3). The cobble was the dominant subtrate for all of the sites. The canopy cover was dense for most of them, ranging from 50% to 90%. The chemical parameters were recorded at the four sites were all within the range for recorded by Trouilhé et al., 2007, at sites where white-clawed crayfish were present in their extensive survey of the region.
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Table 2 Physical parameters for the four brooks selected for restocking attempts and for the donor site “Les Brissonnières”. (Values are given as percentage cover, width in meters and depth in cm). Hydrographic drainage
Brook
Width
Depth
Cobble
Gravel
Sand
Litter
Aquatic macrophyte
Canopy cover
Surrounding
Gartempe Gartempe Gartempe Vienne
Ru du Peu Font-Bignoux Ru de Chambon Oranville
2 0.4 1.5 1.3
25 12 15 30
50 40 85 85
10 40 5 5
30 20 5 5
0 0 5 5
10 0 0 0
50 70 90 90
Pasture Forested Pasture forested forested
Table 3 Values 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 april 2010.
Ch Fon Ora Peu
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 )
13.5 15.6 11.3 14.3
8.24 8.51 8.62 8.6
350 370 444 195
8.6 8.08 8.52 10.41
75 74 88 101
3.14 1.01 4.52 3.13
0.27 0.016 0.154 0.19
0.085 0 0 0
28.85 42.68 50.41 17.73
7.093 0.675 4.702 5.29
20.91 19.51 25.91 3.11
6.47 3.32 6.32 23.6
Table 4 Occurrence of Ephemeropteran species in the four sites selected for restocking and in the donor site (from Grandjean et al., 2011). Brook
Ru du Peu Font-Bignoux Ru de Chambon Oranville Brissonnières
Baetidae
Ephemerellidae
Ephemeridae
Heptagenidae
B. Rhodani
S. ignita
E. Danica
E. dispar
15 12 46 34 10
5 2 15 18 10
2
15
5 2
3.2. Ephemeropteran communities
Leptophlebiidae
R. semicolorata
E. sp
P. submarginata
4 32
25
H. confusa
3 4 15
H. fusca
4
Nb. Sp
H. lauta
2 4 6 5 8
2 13 8 8
3.3. Crayfish surveys
In sites selected for restocking, the families of Ephemeroptera identified during our quantitative sampling are recorded in Table 4, with one species recorded from each of the families Baetidae, Ephemerellidae, Ephemeridae and Heptageniidae and three species of Leptophlebiidae. Baetis rhodani were most abundant at our sampling sites and appeared in three of four sites. Ecdyonurus dispar were present in all sites, whereas one or more species of Leptophlebiidae (Habrophlebia fusca, Habrophlebia lauta and Paraleptophlebia submarginata) were only encountered at three sites. Leptophlebiidae are the most sensitive species to organic pollution and are classified in indicator group 7 in the French IBGN on the scale of biological water quality. Ecological characteristics of species are presented as supplementary data. There are some differences in Ephemeropteran richness with a total ranging from 2 species for Ru du Peu to 6 for Ru du Chambon. The Font-Bignoux and Oranville harboured 4 and 5 species respectively. The Jaccard index estimated between these sites and the donor site “Les Brissonnières” was ranged from 0.25 (Ru du Peu) to 0.625 (Ru du Chambon and Oranville) and 0.5 with Font-Bignoux.
Crayfish were recorded at three of the sites (Ru du Chambon, Oranville, and Font-Bignoux) in both 2010 and 2012 (Table 5). No crayfish were recorded in the Ru du Peu in either 2010 or 2012. Breeding of A. pallipes at the three sites was confirmed by the presence of juvenile crayfish in the size class <40 mm (Grandjean et al., 1997a,b) (Table 5). 4. Discussion The monitoring of reintroductions in 2010 and 2012 showed that three of four restocking attempts were successful with indication of crayfish reproduction (juveniles catches) at three sites three years after restocking. The success rate was of 75% for reintroductions and larger than those generally observed for the white-clawed crayfish. In general review on reintroduction of A. pallipes in Europe, Souty-Grosset and Reynolds (2009) reported from 59 study findings, that 26 reintroductions were successful and 33 unsuccessful. They underlined that more information would be needed on sites chosen for reintroduction. In most cases, no data were collected about biotic parameters but somethimes on
Table 5 Survey of brooks restocking by A. pallipes in 2010 and 2012. Brook
2010
Male
Female
number of ind. within the size class in mm <40
40< x <80
>80
Ru du Peu Font-Bignoux Ru du Chambon Oranville
0 10 15 13
0 ND ND ND
0 ND ND ND
– 2 3 2
– 5 7 7
– 3 5 4
Brook
2012
Male
Female
Ru du Peu Font-Bignoux Ru du Chambon Oranville
0 19 42 38
0 11 18 21
0 8 24 17
number of ind. within the size class in mm <40 40< x <80 – – 5 7 12 17 10 15
>80 – 7 13 13
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physical–chemical ones. In our study, we showed that selection of brook for restocking based only on physical–chemical parameters was not enough to guarantee the success of reintroduction. Indeed, the Ru du Peu had the physical–chemical requirements for harbouring white-clawed crayfish according to the findings of Trouilhé et al. (2003, 2007). These authors performed a long survey of chemical parameters for 2 years with twice monthly sampling from brooks with white-clawed crayfish. They reported variation of chemical parameters between locations with crayfish and free of crayfish, but these differences were impossible to characterize from only one field sampling. In a recent study comprising 29 brooks in Poitou-Charentes region, Grandjean et al. (2011) reported an association between Ephemeroptera community and A. pallipes sites. This association was based firstly on richness of mayfly species. The Ephemeropteran richness is significantly higher in sites with crayfish than sites without crayfish. They found the Ephemeropteran richness ranged from four to eight species in sites with crayfish and 2–6 in those without crayfish. In our study, the Ru du Chambon, Oranville and Font-Bignoux had 6, 5 and 4 species respectively. The Ru du Peu harboured only 2 species. Secondly, Grandjean et al. (2011) reported that the presence of A. pallipes was also associated with species from the family Leptophlebiidae which are sensitive to organic pollution, such as Habroleptoïdes confusa, Habrophlebia fusca, Habrophlebia lauta and Paraleptophlebia submarginata, Except for Ru du Peu, the sites in our study showed at least one species of Leptophebidae.
5. Ecological characteristics of ephemeropteran species and limitations of this study The nine species of mayfly collected in streams sheltering whiteclawed crayfish are all found in France, although none are listed in the Red List for France, or in a list of heritage species. Three of them, Ephemera danica, Serratella ignita and Baetis rhodani, colonise many water courses at a wide range of altitudes (data from the Inventory of Ephemeroptera of France, Brulin, 2007, 2010, 2011). The first is associated with soft substrates (sand, fine gravel) in which the fossorial larvae dig their burrows; the other two are more widespread. On the other hand, the other species are linked to running water. This is the case for the two Heptageniidae, Rhithrogena semicolorata and Ecdyonurus dispar, the latter equally at home in the epipotamon, in the gravel beds of the large rivers of the plains where the current is. The four species of Leptophlebiidae are often associated with forested brooks, usually cool, where the larvae disperse rapidly among the larger elements of the substrate, generally in gravel and small stones barely colonised by periphyton (especially for Habrolepto¨ıdes confusa), among the fine rootlets of riparian vegetation (Paraleptophlebia submarginata), or in the larger masses of decomposing vegetation—twigs, leaf litter and branches (Habrophlebia lauta or fusca). These substrates were often associated with the presence of A. pallipes which requires a high diversity of microhabitats (Nardi et al., 2005). Rootlets, gravels and stones offer shelters for juveniles and adults and leaf litter or decomposing vegetation are the most important constituent of adult diet (Scali and Gibertini, 2007). The utilisation of these species as bioindicators of the potential habitat of white-clawed crayfish is reinforced by the fact that they are well known, widespread in the national territory, and that their determination, except for Rhithrogena semicolorata, poses few problems for the larval stage. However, sampling campaigns need to be carried out at the start of Spring to collect the mature larvae, the end of their life cycle being accomplished at this time especially for H. confusa, and P. submarginata. The larvae of these two univoltine species grow slowly over the winter (Sowa, 1975), and
their summer emergence makes their collection necessary before summer sampling campaigns. Saprobic indices associated with these nine species (Moog, 2002) show for some a degree of resistance to organic pollution. Their arrangement in decreasing order of sensitivity is as follows: Habrophlebia fusca: 1.5; Habrolepto¨ıdes confusa, Paraleptophlebia submarginata: 1.6; Ephemera danica: 1.8; Rhithrogena semicolorata: 1.9; Habrophlebia lauta: 2.0; Baetis rhodani, Serratella ignita, Ecdyonurus dispar: 2.1. The species best correlated with the presence of white-clawed crayfish are chiefly three of the collected Leptophlebiidae, the waters generally characteristic of -mésosaprobes. Even if our results are based on limited restocked brooks, they seem confirm the previous work performed by Grandjean et al. (2011) based on comparison of large number of site harbouring crayfish and free of crayfish. Ephemeropteran community could be used in the selection of brooks for reintroduction of the whiteclawed crayfish in Poitou-Charentes region. This study opened new fields of research in the management and the conservation of the white-clawed crayfish in Poitou-Charentes region and throughout their native range. However, it could be interesting to assess the global community of intolerant orders towards the organic disturbance 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 grateful to the members of ONEMA Sébastien Baillargeat, and Gérard Ostrebski SD 86 (Office National de l’Eau et des Milieux Aquatiques) and Sébastien Joussemet Fédération de Pêche (86) for field assistance. We would like to thank Julian Reynolds and Stephanie Peay for useful comments on the manuscript. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.ecolind.2014.07.005. References ´ M.-C., Bachelier, E., Dumas, J.-C., Fournier, C., Bramard, M., Demers, A., Trouilhe, Broussard, E., Robin, O., Souty-Grosset, C., Grandjean, F., 2006. Distribution of indigenous and non-indigenous crayfish populations in the Poitou-Charentes region: evolution over the past 25 years. Bull. Franc¸ais Pêche Piscic. 380-381, 857–860. Brulin, M., 2007. Atlas de distribution des Éphémères de France. 1ère partie: hors Baetidae et Heptageniidae (Insecta, Ephemeroptera). Ephemera 8 (1), 1–73. Brulin, M., 2010. Atlas de distribution des Éphémères de France, 2ème partie: famille des Heptageniidae (Ephemeroptera). Ephemera 11 (2), 71–133. Brulin, M., 2011. Atlas de distribution des Éphémères de France, 3ème partie: familles des Ametropodidae et des Baetidae (Ephemeroptera). Ephemera 12 (2), 65–109. Changeux, T., 2003. Changes in crayfish distribution in metropolitan France according to the national surveys performed by the Conseil Supérieur de la Pêche from 1997 to 2001. Bull. Franc¸ais Pêche Piscic. 370-371, 15–41. Füreder, L., Gherardi, F., Holdich, D., Reynolds, J., Sibley, P., Souty-Grosset, C., 2010. IUCN 2010. IUCN Red list of Threatened Species. Version2010.4. www.iucnredlist.org Grandjean, F., Romain, D., Souty-Grosset, C., Mocquard, J.P., 1997a. Size at sexual maturity and morphometric variability in three populations of Austropotamobius pallipes pallipes according to a restocking strategy. Crustaceana 70 (1), 31–44. Grandjean, F., Romain, D., Avila-Zarza, C., Bramard, M., Souty-Grosset, C., Mocquard, J.P., 1997b. Morphometry, Size at maturity and sexual size dimorphism of the white-clawed crayfish Austropotamobius pallipes pallipes(Lereboullet) from a wild french population (Deux-Sèvres). Crustaceana 70 (4), 454–468. Grandjean, F., Harris, D.J., Souty-Grosset, C., Crandall, K.A., 2000a. Systematics of the European endangered crayfish species, Austropotamobius pallipes (Decapoda: Astacidae). J. Crustac. Biol. 20 (3), 522–529. Grandjean, F., Cornuault, B., Archambault, S., Bramard, M., Otrebsky, G., 2000b. Life history and population biology of the white-clawed crayfish, Austropotamobius
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