The freshwater pearl mussel [Margaritifera margaritifera (L.)](Bivalvia, Unionoida) rediscovered in Portugal and threats

to its survival

Joaquim Reisa,b

aInstituto Portugues de Malacologia, Zoomarine, E.N. 125, km 65, Guia, 8200-864 Albufeira, PortugalbInstituto da Conservacao da Natureza, Rua Filipe Folque 46, 1� 1050-114 Lisboa, Portugal

Received 13 June 2002; received in revised form 5 February 2003; accepted 12 February 2003

Abstract

The freshwater pearl mussel (Margaritifera margaritifera) was discovered in six rivers in Portugal, where it had been considered

extinct, these being the southernmost European populations, together with the river Agueda in Spain. The former distribution ofthe mussel in Portugal included suitable habitats in river basins located north and including the Vouga river basin. A severe decline,caused by pollution and river channel alteration, seems evident. The populations in rivers Cavado, Neiva and Paiva are small and

with no evidence of recent recruitment. In the rivers Mente, Rabacal and Tuela large populations were found, with evidence ofjuvenile recruitment. They are extremely important for the conservation of the species in the south of its European distribution, butare also threatened, especially in rivers Mente and Rabacal affected by two dams to be constructed in the very near future. The

conservation of the mussel in Portugal depends on extensive surveys of their actual populations and efforts for protecting them. Ifthis is achieved, Portuguese and Spanish populations of M. margaritifera together could be a stronghold for the conservation of thespecies in Europe.# 2003 Elsevier Ltd. All rights reserved.

Keywords: Margaritifera; Portugal; Europe; Distribution; Conservation; Dam

1. Introduction

The freshwater pearl mussel (Margaritifera margar-itifera) is widely distributed throughout its holarticrange, having been probably the most abundant bivalvein ancient oligotrophic rivers in the Northern Hemi-sphere (Araujo and Ramos, 2001). Today however, it isendangered in all of its range (Bauer, 1986; Lucey, 1993;Cosgrove et al., 2000; Araujo and Ramos, 2001; Cos-grove and Hastie, 2001; Young et al., 2001a). Bauer(1988) estimated a decline of over 90% in central Eur-ope populations, and only 25% of its formerly knownpopulations in southern Europe remain (Bauer, 1986).Only four of these south European populations (locatedin northern Spain) are relatively large and with juvenilespresent (Alvarez et al., 2000; Young et al., 2001a). Thecauses of this decline are various, but modification of

the river channel and pollution come at the top of thelist (Bauer, 1986; Araujo and Ramos, 2001; Young etal., 2001a). Disappearance or reduction of salmonidpopulations, the natural host for M. margaritifera glo-chidia, is another cause of its decline (Araujo andRamos, 2001; Hastie and Cosgrove, 2001). Despite thistendency, populations still occur in many Europeancountries (Araujo and Ramos, 2001), and are now pro-tected under the Habitats Directive and the Bern Con-vention. It is also listed as Endangered in the IUCN1996 Red Data Book.The freshwater pearl mussel was first recorded in

Portugal in 1845 by Morelet, who described it as a newspecies Unio tristis based on a single shell collected fromthe river Tamega. The last published data on the pre-sence of M. margaritifera in Portugal (Nobre, 1941)confirmed its occurrence in the river Tamega, as well asin other tributaries of the Douro, and in two other riv-ers (Vouga and Mira basins) further south in the coun-try. Bauer (1986) visited the Douro’s tributaries, known

0006-3207/03/$ - see front matter # 2003 Elsevier Ltd. All rights reserved.

doi:10.1016/S0006-3207(03)00086-7

Biological Conservation 114 (2003) 447–452

www.elsevier.com/locate/biocon

E-mail address: jmc.reis@clix.pt (J. Reis).

to have contained M. margaritifera populations, andfound no trace of these populations. Young et al.(2001a) stated that the freshwater pearl mussel shouldbe regarded as extinct in Portugal on the basis of theexisting evidence.This paper gives information on the occurrence of the

freshwater pearl mussel as part of a broader researchproject from the Portuguese Institute for Nature Con-servation (ICN) on all Portuguese freshwater bivalvespecies in order to conserve them.

2. Methods

2.1. Distribution and abundance

A total of 240 sites (each 100–1000 m long) covering131 rivers and streams belonging to 18 river basins werechecked for the presence of bivalves through the years2001 and 2002. Site selection was not directed just tosuitable freshwater pearl mussel habitats, and so a widevariety of freshwater habitats were surveyed. Previouslyrecorded sites (Nobre, 1941), not visited by Bauer in 1986were also checked. Surveys were conducted based on themethod described by Young et al. (2001b). All differenthabitats of the river at each site were searched using aglass-bottomed box. Densities were estimated using 50 mtransects and searches were made specifically for juve-niles by searching through the sediment at selected 1 m2

quadrats at each site. An estimate of the total number ofmussels in each river was made based on the mean den-sity between two sites, distance between the sites andmean river width. Results are expressed as number ofmussels per square metre and total population estimate.

2.2. Population structure

A random sample of mussels was removed from eachriver and all individuals measured and weighed. Themussels were then put back in their original place. Thesedata were plotted by 10 mm length categories to inferpopulation structure. Length profiles are generallyskewed to the right when compared with age profiles(Young et al., 2001c), but can be a useful first approach

to the population structure, providing evidence of recentrecruitment (Young et al., 2001b).

2.3. Habitat and water quality

At every site the river was characterized with respectto depth, substrate and current velocity and the follow-ing water parameters measured: temperature, dissolvedoxygen, conductivity and pH.

3. Results

3.1. Distribution

Freshwater pearl mussels were found in 21 sites,located in the rivers Cavado (one), Mente (one), Neiva(one), Paiva (two), Tuela (five) and Rabacal (11). Themaximum inhabited length of river was 63 km in theriver Rabacal (Table 1, Fig. 1). The rivers Mente, Tuelaand Rabacal all belong to the Tua watershed (Douroriver basin). They are almost undisturbed, with nomajor works throughout their course, no industries andvery low human population densities in the surroundingenvirons. The populations of river Rabacal and its trib-utary Mente are connected, thus forming a singlepopulation. M. margaritifera was found living togetherwith Unio crassus at one site in the river Tuela and twoin the river Rabacal (all at the downstream end of M.margaritifera occurrence). In the river Cavado, M.margaritifera was found in a 10 km stretch between theupstream limit of the reservoir of ‘‘Paradela’’ and the‘‘Alto Cavado’’ dam. These are the two upstream damsfrom a total of six major dams in the river. This stretchis well preserved, located in a low human populationdensity area and is inaccessible most of the time. In theriver Paiva, where it was known to occur at the begin-ning of the 20th century (Nobre, 1941) but regarded asextinct by Bauer (1986), freshwater pearl mussels werefound along 10 km of well preserved river length(Table 1). The river Neiva is a 36 km long coastal riverrunning directly to the Atlantic ocean. Only three mus-sels were found close to each other in >1 km of sear-ched river length.

Table 1

Abundance of freshwater pearl mussel in Portugal: buried or hidden mussels were considered in calculations

River

Cavado

Mente Neiva Paiva Tuela Rabacal

Length of river inhabited (km)

10 8 a 10 26 63

Density (mussels per m2)

b 0.16 b b 0.05–0.32 0.09–50

Total river population estimate

<100 22 000 <100 <500 50 000 1 000 000

a Only three individuals were found in close vicinity of each other.b Too few mussels to calculate density.

448 J. Reis / Biological Conservation 114 (2003) 447–452

No evidence of the presence of freshwater pearl mus-sels was found in the river Mira or the Vouga basin atthe sites given by Nobre (1941). Instead, in the Mirabasin, there were communities of Anodonta, Potomidaand Unio, as in most rivers and streams in the south,including the Tejo basin. At the site reported for theVouga Basin no mussels of any kind were found. Thiswas also the situation verified in all surveyed rivers andstreams of the littoral north of that basin. The riversSousa and Ferreira in this same area had large M. mar-garitifera populations at the beginning of the 20th cen-tury, but these were already extinct when Bauer visitedthem in 1986.

3.2. Abundance

The mussel density (Table 1) varied greatly, but wasconsiderably lower in the rivers Cavado, Neiva andPaiva where no estimate could be calculated. M. mar-garitifera was found along short stretches of these riversand was more abundant in the Paiva. The largest abun-dance was found in the river Rabacal, with densities upto 50 mussels m�2. The proportion of buried or hidden

mussels varied between zero and 34.4% of unburiedmussels (mean 15.6%). In rivers Rabacal and Tuela M.margaritifera is gradually replaced by U. crassus, whichwas found especially in slow flowing areas of theserivers.

3.3. Population structure

The populations of pearl mussel showed different sizedistributions. At Paiva and Tuela there were mostlylarge individuals (none smaller than 40 mm) indicatingdeficient recruitment, especially in the river Paiva, wherethe population structure was more skewed towards lar-ger sizes (Fig. 2). The Rabacal population had a gooddistribution of small to large individuals indicating norecruitment problems. Lengths ranged from 57 to 103mm in the Paiva, 42 to 93 mm in the Tuela and 10 to109 mm in the Rabacal. In the Mente, which is con-nected to the Rabacal, the length range of 38–81 mmindicates reasonable recruitment. Finally, at Cavado(60–76 mm) and Neiva (71–81 mm) the length rangesindicate the absence of recent recruitment. Large speci-mens are rare in southern Europe unlike in most north-

Fig. 1. The distribution of Margaritifera margaritifera in Portugal. *, no mussel (river with ancient or present population). , ancient records, no

mussels found at marked sites or rivers. *, sites with living populations.

J. Reis / Biological Conservation 114 (2003) 447–452 449

ern European populations, indicating that individualsdo not attain a long life (Bauer, 1991).

3.4. Habitat and water quality

All 21 sites showed characteristics known to beessential for the freshwater pearl mussel: clean sand,primary rocks, clear flowing water. Brown trout (Salmotrutta) are present in all sites, and are particularlyabundant in rivers Mente, Rabacal and Tuela. Musselswere found at various depths, from a few centimetres toa maximum of 2 m. They seemed to be concentrated inmoderate flow areas, often just below rapids. Data col-lected on water quality are summarized in Table 2 foreach river.

Fig. 2. Length profiles of populations of Margaritifera margaritifera from rivers Cavado, Mente, Neiva, Paiva, Rabacal and Tuela.

Table 2

Water quality parameters (mean values) in Portuguese rivers occupied

by pearl mussels

River

Temperature

(�C)

Conductivity

(ms)

pH O2

(mg/l)

O2

(%)

Cavadoa

20.8 25 6.87 8.40 103.0

Menteb

12.3 41 7.07 10.84 105.5

Neivac

20.4 74 6.73 7.30 82.0

Paivab

15.3 27 6.95 8.20 92.0

Rabacala

22.5 37 7.45 7.68 91.8

Tuelaa

20.1 65 7.63 8.15 95.6

a Sampling in July 2001.b Sampling in April 2002.c Sampling in August 2002.

450 J. Reis / Biological Conservation 114 (2003) 447–452

4. Discussion

Portugal is located at the southern limit of the fresh-water pearl mussel European distribution. M. margar-itifera may originally have been found in all tributariesof the river Douro where conditions were favourable,being replaced by other unionids in warmer rivers.Nowadays it has disappeared from all coastal tribu-taries, and thrives only in untouched interior rivers suchas the Mente, Tuela and Rabacal. However, it seemslikely that other small unsurveyed streams might stillharbour freshwater pearl mussels, as many are wellpreserved and relatively untouched.Historic and recent data indicate that the species was

common in many rivers north of the River Vouga,which might constitute its southern distribution limit inthe country. The record from river Mira (Nobre, 1941)is probably erroneous. Suitable habitats exist in somerivers of the Tejo basin, but the species was neverrecorded there. The recently described population fromthe river Agueda in Spain (Velasco et al., 2002) is theonly known population located further south than thePortuguese ones. The species must have been commonin most rivers in the northern coastal region, whererecords only exist from rivers Sousa and Ferreira, in theDouro basin (Nobre, 1941). This is nowadays Portu-gal’s most densely populated and industrialized region.Pollution and river channel alteration should be heldresponsible for the disappearance of the mussel fromthis region, as already proposed by Bauer (1986) forrivers Sousa and Ferreira. Most of the losses can beconsidered ‘‘accidental’’ as suggested by Cosgrove andHastie (2001), as there was no knowledge about pearlmussels in most rivers. The small Cavado and Neivapopulations seem to be remnant populations, survivingin unspoiled stretches of river away from major humansettlements, but their continuity is threatened in theshort term as there is no evidence of recruitment. This isa possible effect of habitat reduction and fragmentationby dam construction in the river Cavado, and pollutionin the Neiva.The cause of the reduction of the Paiva population

remains unknown as the river seems to maintain sui-table habitat for the species. This and the Aguedapopulation show signs of ageing (Velasco et al., 2002),with consequent average size much higher than thepopulations from the northern tributaries of the riverDouro (Mente, Rabacal and Tuela). The sizes andcharacteristics of the populations found in these riversmake them extremely important for the conservation ofthe species in the south of Europe, as very few arecomparable with these. In fact only four other rivers inSpain seem to house potentially healthy populations(Alvarez et al., 2000; Young et al., 2001a). Relativelyhigh densities along long stretches of the Mente, Tuelaand Rabacal, together with presence of juveniles and

pristine habitats should ensure the future of thesepopulations, but all rivers are threatened by electricalschemes in the near future. Two dams may actually beconstructed before the end of 2003 in the river Rabacaldirectly affecting stretches occupied by M. margaritiferaboth in this river and in the river Mente. These mayhave a disastrous long-term effect on the affected popu-lations, as indicated by the river Cavado example.Our results support Bauer’s (1991) observation on the

variation in longevity of freshwater pearl mussel withlatitude, those in southern rivers having a shorter lifespan. Shorter longevity is related to a series of other lifehistory traits, such as lower fertility (Bauer, 1991).Effects of habitat modification on these populations canthus act faster than in other more northern Europeanpopulations.The survival of M. margaritifera in Portugal depends

on preserving undisturbed rivers with healthy popula-tions; thus it is essential that most of these rivers andstreams are surveyed in the near future, providing thenecessary knowledge about other possible populations.Conflict resolution between river engineering projectsand pearl mussel conservation, and knowledge of thestatus of the mussel, are the keys for conservation ofthis species in Portugal, as in most of its Europeanrange (Cosgrove and Hastie, 2001). If this can beachieved, Portugal together with Galicia and Asturias innorthern Spain can be an important stronghold for theconservation of the freshwater pearl mussel in Europe.

Acknowledgements

I wish to thank the Instituto da Conservacao da Nat-ureza (ICN) for funding this project, Dr. LeonorRogado for logistic support and Dr. Marisa Quaresmafor providing informations and field help at riversMente, Rabacal and Tuela. Dr. Francisco Alvares madethe first discovery of M. margaritifera shells in the riverCavado. I wish to thank Dr. Rafael Araujo for all hishelp during this project and for useful revisions to anearly draft of the manuscript. I also thank Dr. BrianDavis and three anonymous reviewers for constructivecomments on the manuscript.

References

Alvarez-Claudio, C., Garcia-Roves, P., Ocharan, R., Cabal, J.A.,

Ocharan, F.J., Alvarez, M.A., 2000. A new record of the freshwater

pearl mussel Margaritifera margaritifera L. (Bivalvia, Unionidae)

from the river Narcea (Asturias, north-western Spain). Aquatic

Conservation: Marine and Freshwater Ecosystems 10, 93–102.

Araujo, R., Ramos, M.A., 2001. Action plan for Magaritifera mar-

garitifera in Europe. Nature and Environment 117, 29–66.

Bauer, G., 1986. The status of the freshwater pearl mussel Margar-

itifera margaritifera L. in the south of its European range. Biological

Conservation 38, 1–9.

J. Reis / Biological Conservation 114 (2003) 447–452 451

Bauer, G., 1988. Threats to the freshwater pearl mussel Margaritifera

margaritifera L. in central Europe. Biological Conservation 45, 239–

253.

Cosgrove, P.J., Hastie, L.C., 2001. Conservation of threatened fresh-

water pearl mussel populations: river management, mussel translo-

cation and conflict resolution. Biological Conservation 99, 183–190.

Cosgrove, P.J., Young, M.R., Hastie, L.C., Gaywood, M., Boon, P.J.,

2000. The status of the freshwater pearl mussel Margaritifera mar-

garitifera Linn. in Scotland. Aquatic Conservation: Marine and

Freshwater Ecosystems 10, 197–208.

Bauer, G., 1991. Plasticity in life history traits of the freshwater pearl

mussel—consequences for the danger of extinction and for con-

servation measures. In: Seitz, A., Loeschcke, V. (Eds.), Species

Conservation: A Population-Biological Approach. Birkhauser Ver-

lag, Basel, pp. 103–120.

Hastie, L., Cosgrove, P.J., 2001. The decline of migratory salmonid

stocks: a new threat to pearl mussels in Scotland. Freshwater Forum

15, 85–96.

IUCN, 1996. The 1996 IUCN Red Lists of Threatened Animals.

IUCN, Gland, Switzerland and Cambridge, UK.

Lucey, J., 1993. The distribution of Margaritifera margaritifera (L.) in

southern Irish rivers and streams. Journal of Conchology 34, 301–

310.

Morelet, A., 1845. Description des mollusques terrestres et fluviatiles

du Portugal. J. B. Bailliere, Paris.

Nobre, A., 1941. Fauna malacologica de Portugal II. Moluscos ter-

restres e fluviais. Memorias e Estudos do Museu da Universidade de

Coimbra 124, 1–278.

Velasco, J.C., Araujo, R., Bueno, R., Laguna, A., 2002. Descubierta la

poblacion europea mas meridional conocida de la madreperla de rıo

Margaritifera margaritifera L. (Bivalvia, Unionoida), en la penın-

sula Iberica (Rio Agueda, Salamanca). Iberus 20, 1–10.

Young, M.R., Cosgrove, P.J., Hastie, L.C., 2001a. The extent of, and

causes for, the decline of a highly threatened Naiad: Margaritifera

margaritifera. In: Bauer, G., Wachtler, K. (Eds.), Ecology and

Evolution of the Freshwater Mussels Unionoida. Springer-Verlag,

Berlin, Heidelberg, pp. 337–357.

Young, M.R., Cosgrove, P.J., Hastie, L.C., Henniger, B., 2001b. A

standardised method for assessing the status of freshwater mussels

in clear, shallow rivers. Journal of Molluscan Studies 67, 395–405.

Young, M.R., Hastie, L.C., al-Mousawi, B., 2001c. What represents

an ‘‘ideal’’ population profile for Margaritifera margaritifera? In:

Wasserwirtschaftsamt Hof, X., Albert-Ludwigs Unicersitat Frei-

burg, X. (Eds.), The Freshwater Pearl Mussel in Europe: Population

Status and Conservation Strategies. Wasserwirtschaftsamt Hof,

Hof, pp. 35–44.

452 J. Reis / Biological Conservation 114 (2003) 447–452