Table Of ContentTHE NAUTILUS 12S(l):22-27, 2014 Page 22
The freshwater mussel collection (Bivalvia: Unionida) of the
Miiseo Nacional de Ciencias Naturales (Madrid, Spain)
Maria Dolores Bragado Arthur E. Bogan
Rafael Araujo’ North Carolina State Musenin ofNatural Sciences
Mu.seo Nacional de Ciencias Naturales, CSIC 11 WestJones Street
Jose Cntierrez Abascal 2 Raleigh. NC 27601 USA
28006 Madrid, .SPAIN [email protected]
[email protected],s
[email protected]
Javier de Andres
Mnseo Nacional de Ciencias Naturales, CiSlCi
Jose (intierrez Abascal 2
28006 Madrid, SPAIN
[email protected],sic.es
ABSTRACT INTRODUCTION
A review of the freshwater mussel collection housed at the Biological specimen collections, conserved in natural
Mnseo Nacional de Ciencias Naturales of Madrid (Spain) history museums and other institutions, provide a rich
(MNCN) including complete specimen data for the 3,270 lots source of data essential for numerous areas of research
is provided. The 10,009 specimens (single valves not included) including biogeographv to phenological or evolutionary
represent species from five continents and Oceania, with studies. These collections comprise samples collected
342 species in 110 genera belonging to 6 currently recog- during the period of accelerated anthropogenic habitat
nized families ofthe Order Unionida. This collection contains
42.9 % and 60.7 % of the total currentlv recognized unionoid destruction, climate warming and freshw'ater habitat
species and genera respectively. There are 152 lots with 30 spe- destruction. These specimens and their associated data,
cies from Africa, 1,359 lots containing 245 species from the document baseline conditions before the major impact
Americas, 125 lots including 55 species from Asia, 1,472 lots ofthese factors (Nicholson, 1991; Allmon, 1994; Shaffer,
representing 18 European species and 28 lots of7 species from Fislier and Davidson, 199S; Lister et ah, 2011; Suarez
Oceania. The Iberian Peninsula has the greatest representation and Tsutsui, 2004). Museum collections are essential for
with 1,233 lots (114 Margaiitiferidae and 1,119 Unionidae). the future documentation of the abundance and dis-
'afmhie a3l9colhootls-porfesNeorrvtehd cAoflrlieccatinonmuisnscellusd,esa4n5d6rleotpsreosfenEtusroapesaign- gtorailb,utiitoins onfecsepsescaiieyst(oLicpusr,at2e01ex1i)s.tIinngosrpdeecritmoenaschainedvetltiheiisr
tnihfeisceantarecaosn.teWmeporaalsroypcroelsleecnttioannohfisftroersihcwadteesrcrimputsisoenlsoffrtohme corresponding data in museums and make sure this data
collecdon, with special emphasis on the South and Central is well organized and available for scientists (Solem at ah,
American mussels collected by the Comision Cientlfica del 19S1) and others on the World Wide Web.
Pacifico (1862-1866), aTid updated data on the presence The objective of this paper is to update the data
of threatened and endangered species following the Endan- associated watli each lot (taxonomic, faunistic, storage,
gered Species .Act (USA) and the Habitats Directive (Europe). number of specimens, etc.) in the fre.shwater mussel
According to the IntemadoTuil Union for the Conservation of collection (order Unionida) (Bouchet and Rocroi, 2010;
Nature [lUCN] Red Ust, there are 30 % of the Vulnerable Carter et ah, 2011) of the Mnseo Nacional de Ciencias
species, 36 % of the EndaTigered species, 44,5 % ofthe Crid- Naturales (Madrid, Spain) (MNCN), providing a com-
cally Etidangered and tlie .'34.5 % oftodays E.xtinct freshwater prehensive overview of this material, as well as docu-
mussels represented.
menting the association of classic studies on taxonomy
and tlistribution with the specimens. Drv specimens mav
be used for studies on shell ultrastructure, trace ele-
ment analyses, sclerochronologv or climate change,
while alcohol-preserved specimens can be the source
ofanatomical and molecular markers used in systematic,
' Correspondingauthor phylogenetic or ev'olutionarv research. We present an
M.D. Bragadoet al., 2014 Page 23
historical description of this collection, with special gastropods (Hidalgo, 1879). The freslnvater bivalves
emphasis on the freshwater nmssels collected by the were studied bv Isaac L('a (1792-1886) (Lea, 1866a, b,
“Comision Cientifica del Pacifico”, a natural histor\' 1867, 1869a, li) and Eritz Haas (Haas, 1886-1969), w'ho
expedition made between 1862 and 1866, and provide pulilished "Ndtjades del viaje al Pacifico" (Haas, 1916).
updated data on the presence of Threatened, Endan- Of the 60 new' mollusk spi'cies described from th('
gered and Extinct species following the lUCN Red material collected by the Comision, 18 w'(>re freslnvater
List, the United States Endangered Species Act and liivalves: 2 were described bv Hidalgo (CaK'o, 1994),
the Habitats Directive. 14 by Lea (1866a, b, 1867, i869a, b) and 2 bv Haas
The mollusk collection of the MNCiN houses (1916). Tlie 14 species describc'd by Lea (1866a, b,
aroimd 10(),()()() lots of the eight known mollnsk 1867, 1869a, b) lacked exact locality data, reporting
classes: Solenogastra, Caudofoveata, Polyplacophora, only South or Central America, but w'ere proliablv
Monoplacophora, Gastropoda, Cephalopoda, Bivalvia, collected bv Paz in the Uruguav River (Salto Oriental,
and Scaphopoda. Although specimens have been col- Uruguay) and were sent to Lea at the end of the (‘xpe-
lected from around the world, the best represented dition (Haas, 1916). It was uncertain if Lea’s tvpes
MNCN
areas are the Iberian Peninsula, Philippines, Cuba, were included in the or in the Lea collection
E(juatorial Guinea, and South America. The terres- at tlie USNM (Smithsonian Institution, Washington, DC)
trial mollusk collections from the Philippines, Cuba (Haas, 1916).
and Pajuatorial Guinea are probably among the best
in the world. There is an important historical repre-
sentation of the South and Central American fauna RESULTS
coming from the Comision Cientifica del Pacifico.
The core historical material of the collection is Detailed locality, taxonomic and historical on all the
MKCN
from three Spanish malacologists: Paz (P. M. Paz y freshw'ater mussel (Unionida) lots in the collec-
Membiela, 1808-1874) wath 40,000 specimens represent- tion can be found at the Global Biodiversitv Information
ing 12,000 species anrl subspecies, Hidalgo Gonzalez Eacility (GBIE). There are 1(),()()9 specimens (single
(J.
Hidalgo, 1839-1923) with 8,000 species, and Azpeitia valves not included) in 3,270 lots representing 342 spe-
(E. Azpeitia, 1859-1934) with 80,000 specimens of cies of 110 genera belonging to the currently recognized
8,171 species (6,594 gastropods and 1,577 bivalves) 6 families: Margaritiferidae, Uniouidae, Mycetopodidae
(Barreiro, 1992). Other historical material comes (= Mulleriidae), Etheriidae, Iridinidae and Ilyriidae
from the founder of the Museum, P. Eranco Davila (Bouchet and Rocroi, 2010; Carter et ah, 2011). The
(1711-1786), and from M. Graells (1809-1898), who collection contains representative lots and specimens
w'as director of the museum betw'een 1845 and 1867. of 60.7 % and 42.9 % of the total nnmber of described
More recently, the collections have growm with the unionoid genera anti species respectively (Graf and
additions of A. Ortiz de Zarate (1887-1964) with Cummings, 2007; Bogan, 2008) (Table 1). There are
4,500 lots, A. Cohos (1922-1998) with 4,390 lots, and 587 alcohol-preserved lots and 2,683 diy lots. Among
Conde with approximately 20,000 lots. The type these specimens are glochidia, optical microscopical
J.
collection incliuling primary and secondary types, con- slides ofsoft parts and shell thin sections.
tains 1,192 lots corresponding to 946 taxa, all are com- Summarizing the geographical information on speci-
puterized, arranged in tiixonomic order, and housed mens in the unionoid collection (Table 2), there are
in all steel cabinets with metal drawers that meet con- 134 lots without locality information, including the
servation standards and are locked (Templado et ah, continent of origin. The area represented by the most
1993; Villena et ah, 1997). Currently, only 50% of the specimens is Europe, with 18 species (including the
general collection is computerized. exotic Siruinodonia ivoodiana (Lea, 1834)) in 1,472 lots,
The Comision Cientifica del Pacifico (the Comision) and 29 lots without country identification. The largest
collected 38,755 specimens belonging to 816 different number of lots comes from the Iberian Peninsula, w'ith
species (Almagro, 1866). Most ofthem were collected by 1,233 lots (114 Margaritiferidae and 1,119 Uniouidae):
the President of the Comision, (P. M. Paz y Membiela), 1,131 from Spain and 102 from Portugal. During the
and by E P. Martinez y Saez, but other members of tlie past 12 years (Soriano et ah, 2001), the Iberian material
expedition like Jimenez de la Espada, Isem and Almagro in the family Uniouidae in the collection has grow'ii b\’
also collected mollusks. Zameron, Barreiros, Philippi 754 lots. Other European lots by countiv are: Albania
and Richardson donated 767 specimens of 43 species, (3), Austria (7), Belgium (11), England (14), Croatia (6),
and 37 specimens of 19 species were purchased (Almagro, Czech Republic (l), Denmark (1), Estonia (2), Erance
1866). All of the Comision specimens were studied by (69), Einland (1), Germany (37), Greece (32), Hungaiv-
Martinez y Saez, who was responsible for mollusks (7), Ireland (5), Italy (58), Latrta (2), Netherlands (1),
during the expedition, and by j. Gonzalez Hidalgo Poland (11), Romania (2), Russia (12), Slovakia (10),
(Hidalgo, 1900; Galvo, 1994). Martinez y Saez and Slovenia (4) and Sw'itzerland (5). Of the 152 African
Hidalgo wrote the three volumes set Mohiscos del viaje lots, 42 come from Morocco, 19 from Egypt, 18 from
al Pacifico, which included marine bivalves (Martinez, Senegal and 18 from Tunisia; tlie rest come from Algeria
1869), terrestrial gastropods (Hidalgo, 1872) and marine (1), Burkina Easo (3), Buiundi (7), Dem(x.'ratic Republic
)
Page 24 THE NAUTILUS, Vol. 128, No. 1
I'ablc 1. 4otal numher of genera anti .species in families of fresliwater mussels in the MNCN collection in comparison with the
whole described taxa. * W'e consider all the li\ing Margaritiferidae belonging to the genus Mnroaritifera. (1) Graf & Cummings
(2007). (2) Bogan (2008).
Species Genera Described Described Described
MNCN MNCN
species (1 species (2) genera (2)
Ltheriidae I 1 4 1 1
1lyriidae 34 9 71 83 17
Iridinidae 12 6 43 41 6
.Margaritiferidae I* 12 12 3
i
Mycetopodidae 24 36 39 12
i
UnioTiidae 264 86 674 621 142
'rO'I'AL 342 110 840 797 181
of tlie Congo (6), Etliiopia (1), Gabon (1), Guinea (1), the Comision Cientffica al Pacffico (1862-1866), which
Ivoix,' Coast (2), Lil)ya (2), Mauritania (1), Niger (1), included tlie Parana and Amazon basins, Chile and
Nigeria (1) and Soutli Africa (6). Tlie alcoliol-preserv'ed the Pacific coast of Ecuador. The information about
collection, witli 456 European and 39 lots of North tliese specimens comes from tliree different sources:
African naiads is one of the most significant conteinpo- (1) Almagro (1866, page 162) published the list of the
ran’ collections of freshwater inns.sels for these areas. freshwater mussels collected in the Comision, detailing
There are 1,358 American lots, which include 973 from tlie localities (15), number of species (44), number of
the United States of America, and 53 lots from Ctiha, specimens (300) and the name of the collectors. (This
44 collected hv Poey already included in the Piiz v information w'as based on specimens exhibited after the
Memhiela collection (Barreiro, 1992), and tlie aforemen- Comision Expedition); (2) Lea (1866a, b; 1867, 1869a,
tioned specimens collected hv the Comision Cientffica al b) described 14 new' species from South America, pro-
Pacffico (.see below). The nnmher of lots by countiw cured by Paz during the Comision but failed to include
is: Argentina (14), Bolivia (4), Brazil (60), Canada (2), any reference as to the origin of the specimens. Fol-
Chile (17), Colombia (2), Ecuador (18), Guatemala low'ing Lea (1866a), some of the material sent by Paz
(1), Me.xico (10), Nicaragua (S), Paraguay (1), Peni (3), was preserv'ed in alcohol; (3) Haas (1916), who, during
Uniguay (103) and \Tnezuela (1). There are 78 North his obliged stay in Spain due to the unfavorable politi-
American lots wdthout a countn’ listed. The best repre- cal climate in Germany (Haas, 1915), w'as invited to
MNCN
sented Asiatic countries, with a total of 125 lots, are the where he studied the mussels collected
Japan with 33 and Ghina with 21. Other A.siatic lots during the Comision. Haas (1916) listed 32 different
by counti'v are: Cambodia (1), Philippines (8), India (15), ta.xa from the Comision collection, two he described as
Indonesia (5), Irac] (6), Israel (2), Laos (3), Malaysia new' species (Diplodon hidalgoi and Mijcetopoda holivari).
(1), Myanmar (2), Singapore (2), Sri Lanka (2), Taiwan He addeda summarx’organizingthe species byriverbasin
(1), Tliailand (7), Turkey (9) and \ietnam (7). There and included some biogeographic remarks and observa-
MNCN
are 28 lots from Oceania, 8 from Australia and 20 from tions. Most of this material is in the collection
New Zealand. and has the original Haas label (Fig. 1). In his paper,
Haas mentioned that some specimens were sent by Paz
to Lea, who published several new species based on this
IIISTOBICAL OVER\4EW material (Lea, lS66a, b, 1867, 1869a, b) and Lea did not
return part of it. This included four types of species
Among the freslnvater mussel historical material, it is Lea described, and Haas supposed they w'ere in the
important to document the presence of mid-nineteenth Lea collection at the United States National Museum,
centniT specimens collected in South America hv Washington, DC (Haas, 1916).
Table 2. Number of lots in families of freshwater mussels at the MNCN mollusc collection. In brackets the corresponding
numher of species.
Africa America Asia Europe Oceania Unassigned
Ktheriidae 6(1) 1
llvriidae 142 (26) 28(7) 4
Iridinidae 41 (12) I (1)
Margaritiferidae 3(1) 4(2) 3(2) 136 (3) 4
Mycetopodidae 148 (23)
Unionidae 102 (16) 1,064 (193) 122 (53) 1,336 (15) 125
TOTAL 152 (30) 1,359 (245) 125 (55) 1,472 (18) 28 (7) 134
Ml). Bragado et al., 2014 Page 25
also sent by Paz to Lea and it was present in the Lea
collections in the Smithsonian Institution, Wa.shington,
DC. This was an error by Haas (1916) because Simpson
(1914) did not cite P;i/. as donor but the name of Prof
Orton; therefore, the type' spe'cimen of this species at
tlie Smithsonian (USNM 25429) did not come from P;iz
l)ut from Dr. C. Strebc'l (Craf and Cummings, 2013).
Otlier material from the Comision can be' feMinel at the
Senckenberg Museum e)f Frankfurt (Haas, 1916; Zilch,
1967; Graf anel Cummings, 2013).
The hvo species described by Hielalge), Castalia
crosseana Hielalge), 1865 anel Castalia jrazi Hielalge),
1868, luwe been sy'ne)nvmizee! uneler Castalia ainhigua
Lamarck, 1819 anel Rhipidodonta hi/laea (Orbignv,
1835) by Be)nnette) (1965) anel Siine)ne (2006), rexspec-
tively. One specimen of each was sent by Hielalge) te) the
Figure 1. Handwriting of P’ritz Haa.s on the labels of the Senckenberg Museum (Frankfurt am Main, Germany)
Coinision specimens. (Haas, 1916). SyTie)nymized by Haa.s (1969) are the tvve)
species described by himself (Hais, 1916), Diplodon
hidalgoi and Mijcetopoda bolivari, as Rhipidodonta
We located 51 lot.s of mussels collected by the charniana (Orbigny, 1835) anel Mijcetopodella falcata
(loniision (Table 3. Freshwater mussels from the (Higgins, 1868).
MNCN
Comision Cienti'fica al Pacifico in the mollusk It is worth ne)ting the presence of senne specimens
collection. Posted online at http://nautilus.shellinuseum from the Comisiehi preserved in fluiels (currently in
.org); they include 223 specimens ol 22 species belong- 70% ethane)!) at the MNCN ce)llectie)n that were
ing to 2 different families. We verified that the specimens probably e)verloe)keel by Haas (1916): 7 specimens of
sent to Lea by Piiz were indeed absent; at least those Anodontites trapesialis (Lamarck, 1819), 6 specimens
corresponding to the following seven species described by of Anodontites trapezea (Spix and Wagner, 1827) anel
Lea (1866a, 1869) are not in tlie MNCN. We have found 2 specimens e)f Diplodon delodontiis (Lamarck, 1819).
them at the mollusk collection of the Smitlisonian Institu- The remaining 208 specimens are all elry.
tion, National Museum of Natural History (Washington, \¥e ne)te some differences in the number e)f speci-
USA): Unio ampidlaceus Lea, 1866. Tvpe: USNM 85614 mens recordeel by Almagro (1866), Haas (1916) anel this
(=Diplodou wijmanii (Lea, I860)), Unio Jocelhis Lea, paper. Fe)r instance, regarding Anodontites patagonica
USNM
1866. Type: 85189 {=Rlupidodonta variahilis (Lamarck, 1819), Haas (1916) cite^d two le)ts at the
(Maton, 1811)), Unio parens Lea, 1866. Ty|3e: USNM MNCN, one lot e)f 3 specimens from Rie) ele la Plata
85198 {=R]iij)idodorita cJiarniana (Orbigny, 1835)), Unio and anotlier le)t with 2 specimens fre)m Miguelete River,
aaitirostris Lea, 1866. Type: USNM 85930 {—Diplodon and we have fe)unel only one lot, labelleel as Ri'o de la
parallelopipedon (Lea, 1834)), Unio appriinus Lea, 1866. Plata, but with 6 specimens, four of them with “Rio de
USNM
Ty|:)e: 85167 {=Diplodon wtpmmii (Lea, I860)), la Plata” written insiele the shell. This may!)e e.xplained
Unio mgososidcaius Lea, 1866. Type: USNM 84392 because se)me material may have been lost or mixed
{=P(ichijnaias mgososidcata (Lea, 1866)), and Unio during the last 150 years, or because the data from
nifofuscns Lea, 1865. Type: USNM 84101 (—RJiipidodonta Almagro (1866) might not be accurate. Almagro’s book
grata (Lea, I860)). Another part of the Paz material yvas wTitten in the last year of the Comision, so the
is separated between the Smithsonian and the MNCN historical number ofspecies and corresponding number
(Table 3. Freshwater mussels from the Comision of specimens may be ine,xact. Another reason could be
MNCN
Cientifica al Pacifico in the mollusk collec- the loaning or gifting of specimens between different
tion, posted online at http://nautilus.shellmuseum.org): collections and/or the loss of old labels, as occurred
Unio paraguaijensis Lea, 1866. Ty|ie: USNM 85068 among the Paz, Hidalgo, and Azpeitia collections. We
i=Diplodon delodontiis (Lamarck, 1819)), Unio peadlaris have not found the specimens from Montevideo, Negro
Lea, 1866. Type: USNM 85190 (= Diplodon wijuuinii Riy^er, Aguano and (3tavalo (Almagro, 1866).
(Lea, I860)), "Unio finnus I^ea, 1866. Type: USNM 85113 Some years after the end of the Comision, Paz sent
(= Diplodon delodontiis (Lamarck, 1819)),Monocondijlaea Ix'a his collection of North American freshyvater mollusks
USNM
lentifomiis Leti, 1866.Type: 86335{—Monocondijlaea for expert identification (ACN()252/()()2; ACN()259/()13).
comentesensis (Orbigny, 1835)), Monocondijlaea pazii Lea returned the identified specimens (451 gastropods
Lea, 1866. Ty|3e: USNM 86342 {—Monocondijlaea and 287 bivalves) in 6 parcels to La Habana (Cuba),
niinuana (Orbigny, 1835)) and Anodorita pazii Lea, yvhere thev yvere shipped again to Cadiz (Spain) arriving
1866. Type: USNM 86703 {—Anodontites trapezea (Spix on 12 July 1872. On 22 August 1872 they yvere moved
and Wagner, 1827)). HcUis (1916), cited Simpson (1914), by train to Madrid yvhere they arrived oti 4 September.
noting the tyjie of Anodorita napoensis Lea, 1868 was One year later, in 1873, the Paz mollusk collection.
PagOe 26 THE NAUTILUS, Vol. 128,’ No. 1
Table 4. Niiinlierolfreshwater iiiussels species included in the lUCN in the MNCN collection. Numbertotal ofspecies included
in each categors' in brackets.
Nearthreatened Viilnera!)le Endangered Criticallyendangered Extinct
America 35 (40) 7(14) 10 (34) 24 (50) 10(27)
Africa 0(1) 0(9) 3(5) 2(4) 0 (2)
Asia 0(2) 0(6) 3(9) 1 (8)
Europe 1 (1) 3(4) 2(2) 1 (1)
Oceania
TOTAL 36 (44) 10(33) 18 (50) 28 (63) 10 (29)
including this material, was sold to tlie Museo Nacional 169specimens ofM. auricularia in 68 lots, 67from Spain
de Ciendas Natiirales (Barreiro, 1992). and 1 from France, probably the largest collection of
this species in the world (Araujo and Ramos, 2000),
69 lots of M. niargaritifeni, 3 lots of the North African
ENDANGERED SPECIES M. marocana, 3 of M. inonodonfa, 1 of M. dahurica,
2 of M. laevis ant! 1 lot of the Asiatic M. laosensis.
Freshwater bix'alves are among the most imperiled Margaritifera laosensis is (]iiite rare in collections and
animal groups on tlie planet, declining due to pollution, has only recently been collected alive in the northern
modified or disturbed habitat and reduced numbers region of the Lao People’s Democratic Republic
of host fish (Lydeard et ah, 2004; Strayer et ah, 2004). (S. Schneider, Personal Communication).
In cases of imperiled fauna, the role of natural histoiw
collections is essential, being the last repositories where
scientists can study extinct or endangered species ACKNOWLEDCMENTS
(Nicliolson, 1991; Shaffer, Fisher and Davidson, 1998).
The MNCN collection has 82 % ofall the Near Threat- C. Bogan, J. Smith, H. Leslie, A. Garcia-Valdecasas,
ened freshwater bivalve species, 30 % ofthe Vulnerable and K.S. Cummings reviewed earlier drafts of the
species, 36 % of the Endangered species, 44.5 % of the manuscript.
%
Critically Endangered and 34.5 ofthe today’s Extinct
naiads recognized by the International Union for the
LITERATURE CITED
Consemition of Nature (lUCN) (Table 4). It also lias
nearly 60 % ofthe North American Endangered species ACN()252/()()2. 1872. Archivo del Museo Nacional de Cieiicias
(Endangered Species Act) and numerous lots of all Natiirales, 16pp.
the European species protected under the Habitats ACN()259/013. 1872-187.3. Archivo del Museo Nacional de
M
Directive: arrantifera margantifera, M. auricularia, Ciencias Natiirales. E.xpediente relative a la confusion
U. elongatiihis, and U. crassus (Tables 5, 6; Table 6. surgidaenelenviode Rafael Arangoal MuseodeCiencias
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