Experimental demonstration of viability for the endangered giant pearlmussel Margaritifera auricularia (: Unionoida) in its natural habitat

Cristian R. ALTABA and Miguel A. LÓPEZ

Altaba, C.R. and López, M.A. 2001. Experimental demonstration of viability for the endangered giant pearlmussel Margaritijera auricularia (Bivalvia: Unionoida) in its SHNB natural habitat. Bol/. Soco Hist. Nat. Balears, 44: 15-21. ISSN 0212-260X. Palma de Mallorca.

The giant pearlmussel Margaritijera auricularia is a critically endangered , sur­ viving in natural habitats only in the lower Ebro (Catalonia, ). The viability of this population was assessed by addressing whether the adults are producing larvae, if any host exists in the area, and what recruitment is actually taking place. AII adults monitored released larvae during Spring, showing that they are fertile hermaphrodites. SOCIETAT O'HISTORIA Artificial infections of a wide array of were performed under controlled condi­ NATURAL DE LES BALEARS tions, and it was found that the only host is the freshwater blenny fluviatilis, which lives in the same habitat and is also endangered. Young individual s were located, the smallest one with an age just aboye 2 years. It appears that this population is inde­ ed viable, although it needs urgent and effective conservation action. Keywords: species interactions, limnology, conservatioll, Ebro, Margaritifera auricula­ ria, Salaria fluviatilis.

VIABlLITAT DE LA NÁIADE AMENA<;:ADA Margaritijera auricularia (BIVALVIA: UNIONOIDA) AL SEU HÁBITAT NATURAL. La n¡lÍade Margaritijera auricularia és una especie que es troba en perill crític, i que sobreviu en hilbitats naturals únicament al curs inferior de l'Ebre (Catalunya, Espanya). La viabilitat d'aquesta població ha estat avaluada investigant si els adults estan produint larves, si hi ha cap peix hoste a l'area, i si té lloc un reclutament efectiu. Tots els adults que foren objecte de seguiment allibe­ raren larves a la primavera, demostrant així que són hermafrodites fertils. Es realitzaren infeccions artificials d'un ampli ventall de peixos sota condicions controlades, i es deter­ mina que I'únic hoste és la bayosa de riu (Salariafluviatilis), que viu al mateix habitat i es troba igualment amena<;:ada. Es localitzaren individus joves, el més petit deis quals tenia una edat just per damunt deis dos anys. Aquesta població, dones, sembla del tot viable, encara que necessita mesures de conservació urgents i efectives. Paraules clau: interacions entre especies, limnologia, conservació, Ebre, Margaritifera auricularia, Salaria fluviatilis.

Cristian R. ALTABA and Miguel A. LÓPEZ, lmtitut Mediterrani d'Estudis Avan¡:ats (CSlC-UlB), 07071 Palma de Mallorca. E-mail: [email protected]. Actual adress: CRA Conselleria de Medi Ambient, Govern de les llles Balears, carrer Reina Constan¡:a s/n, 07006 Palma de Mallorca and MAL Departament d'Ecologia, Facultat de Biologia, Universitat de Barcelona, Avda. Diagonal 242, 08017 Barcelona.

Recepció del manuscrit: 28-des-OO; revisió acceptada: 06-jun-01. 16 Boll. SOCo Rist. Nat. BaZears, 44 (2001)

Introduction In the lower Ebro there are sites where the local density of M. auricularia is fairly high One of the most endangered species in (Altaba, 1997). This suggests that the limiting is the giant pearlmussel Margaritifera factor must be in the larval stages of its complex auricuZaria (Spengler, 1793), a very large fresh­ life history, which involves a parasitic stage on water mussel that lives only in big rivers. Its ori­ the gills of certain fishes. Indeed, it has been ginal range extended throughout Western Europe shown in other species of Margaritifera that the and North , but this species now survives local density of young and adult pearlmussels only in the Ebro river and adjacent channels in depends mainly on' the density of available host Spain (Altaba, 1990; 1992; 1997; 2000; Primack, fishes (Johnson & Brown, 1998; Cunjak & 1998). Initially, only recently dead specimens McGladdery, 1991). Thus, identifying the host were located (Altaba, 1990; 1993). Later on, fishes for such a species has important conse­ during public works in the lower Ebro in quences for its conservation (Neves et al., 1985; Catalonia (Lorán, 1993), a sampling project of Neves & Widlak, 1987). Based on indirect evi­ freshwater bivalves allowed the finding of live dence, it was hypothesized that Acipenser sturio individuals and the assessment of their distribu­ (Common Sturgeon) could be the host of M. auri­ tion (Altaba, 1996a). cularia (Altaba, 1990). However, most of the The lower Ebro has experienced impor­ living specimens in the Ebro were certainly not tant changes in hydrology as a consequence of carried by this fish, because its upstream migra­ dam construction, water diversion, and pollu­ tion was halted by the Xerta weir centuries ago. tion (Ibáñez et al., 1996). However, it still Furthermore, overfishing caused its disappearan­ keeps many of the features of a wild big river, ce 30 years ago (Fernández & Farnós, 1999). such as graveI shallows, and it harbors a thri­ In order to test the viability of M. auricu­ ving native fauna. This is clearly shown by the Zaria in the lower Ebro it was necessary to assess abundance of freshwater mus seIs belonging to whether the adults are producing larvae, if any several species. As a result of a large-scale host fish exists in the area, and what recruitment intensive sampling, it was possible to evaluate is actually taking place. The first question was the size and distribution of their populations addressed by monitoring adults in the wild, the (Altaba, 1997; 2000). In contrast, the fish fauna second was tested through experimental infesta­ of the lower Ebro, which originally was compo­ tions on a wide array of fishes, and the third sed of only 14 species, has been enriched in involved exhaustive searches in the fieId. A recent years through the introduction of at least detailed account of the laboratory work will be 13 exotics, several of which have become exce­ published elsewhere (López & Altaba, 2000, in edingly successful, displacing the native ones press), and only the relevant findings are reported (Sostoa & Lobón-Cervia, 1989; Elvira, 1995; here together with the results of field work. 1996; 1997). However, the question remained of whet­ her the population of Margaritifera auricularia Material and methods in the lower Ebro is indeed viable. This is a highly relevant issue, because outside of this The live specimens that were found during natural habitat there has been no recruitment for public works in the river were translocated into decades. The relie demes living further upstream trays filled with cobbles and suspended in the flo­ and in adjacent channels in Aragon have suffered wing water from a stable surface. In this manner, from rampant pollution and massive siltation. they could be monitored daily, independently of These factors may be responsible for those water leve!. No further manipulation of the ani­ demes being composed of only very old speci­ mals took place, and the release of glochidia larvae mens (Altaba, 1997; 2000; Álvarez Halcón et al., was followed by visual inspection. The larvae used 2000). in the following experiments were collected with a c. I? Alrllbll af/(I M .A. LlÍp i';'. Villbilirr ofM({/gllririfáll al/ricl/llIrill ill ir.\' IIlIrl/mlllllbiwr 17

sy rin ge I'ro m Ihe shell 's edge. placed in a larger inl o Ihe g ill ~. Inrecled I¡sh were kepl in closed­ conl aim:r. and rapidl y carried \O Ihe laboraloly circuil I¡¡nb al Ihe Cmrre d 'Aqiii(,I/If/(/'{/ (I RTA ) FI'll Ill Ma rch 10 J une 2()()(). ,1 IOlal 0 1' 176 I¡ s­ racilili es in Ih e Ebro Delta . The bOl\olll 0 1' Ihese hes belongin g lo 16 spee ies we re in !'ccled. Thi s la n'" wa~ ,cparaled by a Illcsh. and all p a rt i c k ~ on includ ed X which are naliVl: 10 Ihe lower Ehro il we re siphoned. sieved and inspecled every day. (AI/g l/illo IIlIg l/illll. Bllr/m.\' g m l'lI.I'ii. 8 l1rhl/.1 The search 1'01' yo un g age c1a, se~ in Ih e I¡ eld 11I1II.I'i. CllIl/ld/'li,l'{()/l11I {()X(}.I'{(}lllll. Cohiri.l· 11II11/1Ii­ wa s carri ed oul by careru l Illanual i ll ~pec l ioll 0 1' m /(/ . S(/I(/ri(/ pl/I·i(/rili.\'. Li:ll llllmrll and MI/g il selecled area,. There i, a lillliled Ilulllber 0 1' , il e~ (,i'I¡f/llII/.I ). and X which are in lroduced exo li e~ inhabiled by M . (/ l/ri('l/llIrill. 'o il \\ a~ con~ i tk red (¡\ ('i/}('I/ H'r h(/l'ri. I-Ilhl//'lIl/,I' a llJII/'llIl.l . C(/rll.l.l'il/s inappropriale 10 proceed \"" ilh any ,alllplill g Ihal (/ 11 1'11111 .1. Crpril/I/.\' (·{I/·IJio. G(}hio gohio. could be deslrucli ve 01' Ihe n

Fig, 1. al 1 ~ lI l') ' ICe! gloc1l1llia nI' M"rg"rifi/á" III/ri('/I/"r;" ill lile lil" II lell l' oi" a S"/,,r;a fl""úlf;!i, gd!. h ) JU\'cllilc, relc a\cd i"roll\ Iheir ho,\. " i"l er le" lhall OIlC e!a~ (li" i"rec lifc. Fig. / . ,,) G/"I/III1/" d,' I:t rg"nlikr" :J uricu laria l'1I( 'i\lfll.\ tll, JilllllU'II/\ d 'lIl/" /¡rlil/'/II111 dI' S""'ri,, IlU\ ,aldi, . /J) ./11 ""111/' "/¡'''l'l'lIf' d,,/ \('11 IIllIf". de,!,,'," dt' ,,/(,1/\' ¡/'WJ diu de l'ldtl lIillrl·. 18 Boll. SOCo Hist. Nat. Balears, 44 (2001)

due to the constructton of a power station at the individual found measures only 5.74 mm in length Xerta weir. InitiaHy, aH adult bivalves in this area (Fig. 2). According to the annual rings present were recovered and translocated to safe sites, but (and the application of an unpublished growth no young specimens were found. When this site equation for the population), its age is just aboye 2 was dry a second, more thorough search was per­ years. The shape of this specimen is reminiscent formed. of the adult's, although the umbos are conside­ rably more central, and the val ves are quite flat.

Results Discussion The production of glochidia larvae was observed in all the adult individuals monitored. The results obtained point all in one direc­ They were released, gradually but almost conti­ tion: the studied population is a viable one. The nuously, in dense masses, which became slowly finding that all adults produce larvae strongly washed away through the dilution of the hyaline suggests that they are hermaphroditic, a condi­ mucus containing the larvae. The time of release tion that has occasionally been reported in other extended from March to June, and every indivi­ margaritiferids (Smith, 1976; Ziuganov et al., dual was productive for at least two months. 1994). It also shows that the precautions taken The glochidia adhered readily to the gills of during the handling of the pearlmussels were most fishes. However, after a few days they were adequate to mitigate the possible stress response rejected by the vast majority of individual fishes. (Waller et al., 1995). Furthermore, together with Juveniles were recovered from only one potential the activity demonstrated by the glochidia, it host species, the Freshwater Blenny, Salaria flu­ indicates that these specimens are in good repro­ viatilis. The infection of this species was readily ductive condition. effected, although not all attached glochidia beca­ The finding of a natural host is crucial. me encysted by the host's epithelium. Later on, Remarkably, Salaria fluviatilis is found in the numerous encysted larvae were visible on the gill same microhabitat as Margaritifera auricularia: filaments. The cysts appear as pustules with a dia­ sites with swift current passing over a bottom of meter of 0.2 mm (Fig. la). FinaHy, juveniles were coarse (decimetric) consolidated gravels (Altaba, recovered (Fig. lb). The parasitic stage lasted 1997). Other species of Margaritilera live in from over 40 to just 26 days similar habitats (Stober, 1972; Vanotte & The juveniles of Margaritifera auricularia Minshall, 1982). Moreover, only from this fish are very small (l7S /.lm in diameter). Their shape could juveniles reach such a microhabitat in a big is almost spherical, with a long and almost straight river before being carried away by the current. hinge. Their color is whitish, with a faint tinge of Indeed, S. fluviatilis is an ambush predator living golden in the hyaline shell. The shell surface is in burrows, and lays and takes care of the eggs on rough, and the glochidial shell is clearly visible as the underside of boulders (Coté et al., 1999; a hump at the apical parto The edge starts a fast Perdices et al., 2000). growth just after release, clearly visible as a sharp The attached glochidia were often shed protruding margin after a few hours. The foot is quite fast by non-hosts, suggesting that a strong cylindridoid club-shaped, clearly enlarged near immune response is involved (Fustish & the tipo No cilia were visible, and there were no Millemann, 1978; Meyers et al., 1980; Bauer, signs of any ability to move reptating. However, 1987). No sign of such a response was obser­ the movements of the foot were fast, suggesting ved in the host species, even if the number of that these juveniles are able to burrow readily. larvae on the gills decreased with time, as hap­ Young specimens were found in the field pens in related bivalve species (Young & only in the exposed area. They were already dead, Williams, 1984). Several workers have repor­ and the soft parts were rotten inside. The smallest ted a narrow host specificity for margaritiferids c. 1? AllOho ami M .A. L(ípe:. Viohi/il\' (JI" Margarilil"ero ol/ricL/lorio ill il.\· I/alurol Ilt/bital 19

(Bauer. 1987: Zjuganov 1.' 1 01. , 1990: ez lin 1.' 1 shoa ls by agri culture ancJ se lllcllleJ1l S along ri ver al.. 1994 : John so n & Brown, 1998). allhough banks. ancJ finally by pollulion. In acJcJi ti on. Ihe in ri ve rs harboring a ri ch fi sh fauna lhere see ms fres hwa ler Illollusca n faun as of th e lO be a wider va riation in res islance across I"ish M ed ilerranea n region as a whole are endangercd spec ies (Murphy, 1942: Awakura, 1968: cJu e to w icJ cspread habi tat dcs lruction ( Itaba. M eyers & Millemann . 1977). The fairly large 1996b). nUlllber 01" le,led fi sh spec ies 1IUppOW, Ihe The kn owledge obtainccJ onlhe viabilily 0 1" hypoth es is lhat M. ouricl/lorio is hos t-s pec ific lhe Mwgarilif"e ra ol/ ricl/laria popu lation in lhe on S. .fll/I'i(/Iili.l". lower Ebro shoulcJ be usecl to prolllote its consc r­ Live young individuals of M ClIg orilifértl va lion urgent ly ancJ efficicntly. It should be al/ ricl/loria had nol bee n repon ed anywhere I"or incorporatecl into a souncl rccovery progralll decades. The early and only record s were I"rolll (e.g .. Beas ley & Robel1 s. 1999). which shoul d bc channels adjace nt lO Ihe Ebro in Arago n. wherc focusecl bOlh on lhe stri ct proleclion of ils habi ­ lhey ha ve nol been found aga in (Hans. 19 17: lars. and on rea ring juvenile pea rllllusse ls in C¡~P ­ Ciria, 1920: Iva rez Halcón 1.' 1 al.. 2000). This livity for reinlroducl ion lO th e w ilcl . Clearly, lhe new finding shows Ihat rec ruillllent is not onl y surviva l of lhis spec ies is now inlilllalely linkcd possible. bUI Ih al it is aC lualy laking place. wilh prescrvalion 0 1" Ihe lowcr Ebro. As in Ihe case 0 1" Illany oth er fres hwater biva lve, (Boga n. 1993 ), lhe decline and ncar cx linclion nf Margariliféro al/rieL/luria was cau ­ Acknowledgements sed by a co rnbination of faclors (Altaba, 1990: 2000: Prilllack. 1998). Its host fi sh is an endang­ We are grmefullo J.A . Alcover. 1. Doadrio. erecl spec ics (Elvira. 1996: Perdi ces el al., 2000). E. alvel, B. Ivira. D . Furones . L. M . Gon/úlcJ:. ConsicJ cring lhe hosl-spec ific rclationship repor­ B. Heredia, V. López. S. M onl scrral. G.X. Pom, . lecJ here. Ihe ori gin al c1i slriblllion of Salaria jlu­ e. Ponse ll, N. Pra l. J. M. Querall. A . de Sosloa I'ioli/is Illay havc been co nsicJcrabl y larger th at al and D. Vinyole,. This projecl has bee n supponed prese nl. Thus. Ihe cJi sa ppea ran ce of bOlh il1lerac ­ by lhe pani sh Minislry of the Env ironlllenl. ling spcc ic> woulcJ have occurred lhrough lhe Perlllits wcre provided by Ihc Depan alllenl de bui lcJin g 0 1" weirs ancJ cJalll s, by lhe cJeslrLI cti on 0 1" M edi Ambienl of lhe Gencralilal de Cma lunya.

Fig.2. Yllun g , p ~ci lll e n 01' MI/I :~lI rit if{'/"a C/ l/ricI/I C/ ria t"ound receml y dcad in

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