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Redescription of Unio Tumidiformis Castro, 1885 (Bivalvia, Unionidae), an Endemism from the South-Western Iberian Peninsula

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Redescription of Unio Tumidiformis Castro, 1885 (Bivalvia, Unionidae), an Endemism from the South-Western Iberian Peninsula Journal of Natural History Vol. 43, Nos. 31–32, August 2009, 1929–1945 RedescriptionTNAH0022-29331464-5262Journal of Natural History,History Vol. 1, No. 1, May 2009: pp. 0–0 of Unio tumidiformis Castro, 1885 (Bivalvia, Unionidae), an endemism from the south-western Iberian Peninsula JoaquimJournalJ. Reis and of Natural R. Araujo History Reisa* and Rafael Araujob aUniversidade de Lisboa, Faculdade de Ciências, Centro de Biologia Ambiental, 1749-016 Lisboa, Portugal; bMuseo Nacional de Ciencias Naturales. CSIC. José Gutiérrez Abascal, 2. 28006 Madrid. Spain (Received 4 November 2008; final version received 23 April 2009) The possible occurrence of Unio crassus Philipsson, 1788 on the Iberian Peninsula has been a controversial issue since the nineteenth century. Several characters, including molecular, morphological and life cycle, show that the Iberian taxon is related to, but well differentiated from, the central European U. crassus. The valid name for this Iberian taxon is Unio tumidiformis Castro, 1885. Live populations are distributed throughout the Guadiana, Mira and Sado river basins. Unio tumidiformis can be distinguished from other Unio species by its regular oval shape, high relative height and width, strong wavy umbonal rugae, supra-cardinal tooth on the right valve, and lower glochidium height. From the potential fish hosts tested, only Squalius alburnoides (Steindachner, 1866) resulted in juvenile drop-off, suggesting some degree of specialization in the parasite–host relation- ship. The endemic nature, population status and habitat of U. tumidiformis make this species important from a conservation point of view. Keywords: freshwater mussel; Iberian Peninsula; taxonomy; endemic; conservation Introduction Recent studies on European unionoid taxonomy are developing a new perspective on the real number of taxa in this imperilled mollusc group. Molecular techniques have been very useful tools to complete the conchological and anatomical approaches Downloaded By: [Reis, Joaquim] At: 16:31 24 July 2009 historically employed to organize naiad taxonomy (Araujo et al. 2005; Graf and Cummings 2006, Araujo et al. 2009). We consider Haas (1969), the primary expert in Palaearctic unionoids, the best starting point from which to develop a new European unionoid phylogeny. Regarding the Palaearctic genus Unio, Haas considered a series of 12 “fundamental Unio species” comprising different “races” or subspecies. For his classifications, Haas (1969) largely used shell shape of the different taxa as found in the centres of their distribution areas. One of these species, Unio crassus Philipsson, 1788, was considered by Haas (1940, 1969) as comprising eight “races”: six from Europe, one from the Caucasus and one from north-eastern Asia. Araujo and Ramos (2001), Velasco et al. (2002) and Reis (2003) refer to the occurrence of U. crassus in northern Iberian rivers where Margaritifera margaritifera lives, but they do not relate them to any of the Haas (1940, 1969) “races”. Recent studies showed that these populations are not U. crassus (Reis et al., unpublished results), but correspond to an Iberian race of Unio pictorum as defined by Haas (1940, 1969). In recognition that the *Corresponding author. Email: [email protected] ISSN 0022-2933 print/ISSN 1464-5262 online © 2009 Taylor & Francis DOI: 10.1080/00222930902993724 http://www.informaworld.com 1930 J. Reis and R. Araujo Iberian and central European U. pictorum populations may not belong to the same taxon (Reis 2006), the Iberian taxon is referred hereafter as Unio cf. pictorum Unio crassus batavus Maton and Rackett, 1807 is the only U. crassus “race” to be reported from the Iberian Peninsula. The first reference to U. c. batavus in the Iberian Peninsula was made by Morelet in 1845, who identified several specimens from the Tagus (= Tejo = Tajo) and Guadiana river basins in Portugal (Morelet 1845). Later, in 1885, Castro described four new species from the rivers Sado and Tagus in Portugal (see below), which he assigned to the U. tumidus Philipsson, 1788 group, even though this species has never been reported from the Iberian Peninsula (Castro 1885). These four species were considered to be synonyms of U. c. batavus by Haas (1917, 1940, 1969). Two further species considered by Haas (1940, 1969) as U. c. batavus syno- nyms were described by Kobelt: Unio baeticus from the river Guadaira in Spain (Kobelt 1887) and Unio conimbricus from the river Mondego in Portugal (Kobelt 1893). Azpeitia (1933) considered the occurrence in Spain of three species that he thought belonged to the U. c. batavus group: U. baeticus, U. callipygus Drouët, 1893 (described from the river Guadiana) and U. jourdheuili Ray in Locard, 1882 (origi- nally described from France and cited in the river Tagus by Azpeitia in 1933). In his comprehensive revision of freshwater mussels from Portugal, Nobre (1941) did not refer to any previous citations. The Portuguese taxa reported by Morelet (1845), Castro (1885) and Locard (1899), which Haas (1940, 1969) considered to be synonymous with U. c. batavus, were referred to as Unio cf. crassus in a recent revision by Reis (2006). Herein we show that the correct name for this taxon is U. tumidiformis Castro, 1885. Recent phyl- ogenetic studies clearly support the distinction of U. tumidiformis from U. crassus (Araujo et al. 2009). Our purpose is to clarify the taxonomy of U. tumidiformis using the widest possible range of characters (i.e. molecular, morphological and anatomical). While results for the whole of Europe are still preliminary (Araujo et al., unpublished results), more concrete findings have been proposed for Iberian naiad taxonomy (Araujo et al. 2005, 2009). This paper is devoted to the revision of the systematics, taxonomy and main biological features of U. tumidiformis: shell morphology, anat- omy, distribution, reproductive season and larval stage. Downloaded By: [Reis, Joaquim] At: 16:31 24 July 2009 Material and methods Studied material To identify the historical distribution of U. tumidiformis in the Iberian Peninsula, both the literature (Morelet 1845; Bourguignat 1864; Castro 1873, 1885, 1887; Kobelt 1887, 1893; Drouët 1893; Locard 1899; Azpeitia 1933; Nobre 1941; Haas 1969; Soriano et al. 2001; Pérez-Quintero 2006; Reis 2006) and the mollusc collections at the following Museums were reviewed: Museo Nacional de Ciencias Naturales (Madrid, Spain), Museu Bocage (Lisbon, Portugal), Museu Zoológico da Universidade de Coimbra (Coimbra, Portugal), Museu do Instituto Zoológico Dr. Augusto Nobre (Porto, Portugal) and Muséum National d’Histoire Naturelle (Paris, France). Recent studied specimens came from field sampling during the last 10 years and from many gracious collaborators who sent additional material. Nearly 1000 localities were sam- pled around the Iberian Peninsula in the context of several studies, including 300 in Journal of Natural History 1931 the Guadiana basin, 250 in the Tagus basin, 80 in the Guadalquivir basin, 13 in the Sado basin, six in the Mira basin and 30 minor rivers from the south-western Iberian Peninsula (15 in Portugal and 15 in Spain). Additionally, all major Palaearctic river basins in Morocco (north of the Oum er Rbia river) were checked (30 localities), as far east as the border with Algeria. Table 1 shows the recent sampling locations from where the specimens used to study U. tumidiformis characters were collected. Recent specimens of Unio from central Europe and northern Africa at the above-mentioned collections were also studied for comparison purposes. External morphology Shell characters were studied in specimens from the Guadiana, Mira and Sado river basins (see Table 1). The shell outline, colour, umbo sculpture, when visible, and hinge characteristics as well as any distinctive feature were described. Maximum length, anterior length (measured from the anterior edge of the umbo to the anterior tip of the shell), maximum height, height at the umbo (measured from the uppermost edge of the umbo to the ventral margin of the shell along a line perpendicular to its longitudinal axis) and maximum width (Zettler 1997; Nagel 1999) were measured. Whenever necessary a binocular lens was used to aid the analyses. All relevant features were photographed. Anatomy Anatomical studies of 20 specimens were carried out paying close attention to char- acters that are considered taxonomically relevant in unionoids (Ortmann 1911; Haas 1924; Nagel 1999; Graf and Cummings 2006). To reveal the sexual strategy of the species (hermaphroditism versus dioecia), 60 specimens were histologically sectioned. Gonad samples and gill contents of gravid specimens were examined under a light microscope. Anatomical studies were conducted on living and preserved specimens from the rivers Bullaque, Estena, Guadiana, Milagro, São Pedro and Vascão (Guadiana river basin) (see Table 1). Downloaded By: [Reis, Joaquim] At: 16:31 24 July 2009 Life cycle For the characterization of the larval stage, glochidia were collected from living mus- sels in the field and in aquaria by flushing the marsupia with water, and studied using scanning electron microscopy and light microscopy. The life cycle of the species was inferred from field observations, specimen dissections, histological sections and experiments in aquaria. Studied glochidia came from 10 specimens collected from the rivers São Pedro and Vascão (Guadiana river basin, Portugal). Artificial infestations of potential host fish were carried out in aquaria following a modification of the proto- col described by Jones
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