Parasitology International 55 (2006) 143 – 145 www.elsevier.com/locate/parint
Phyllodistomum folium (Trematoda: Gorgoderidae) infecting zebra mussels (Dreissena polymorpha) in the Ebro River, Spain Miguel A. Peribáñez a,⁎, María L. Elrío a , María J. Gracia a , Daniel Fernández de Luco a , Juan A. Castillo a , Javier Lucientes a , Imanol Cia b b
a Departamento de Patología Animal, Universidad de Zaragoza, Miguel Servet, 177, Zaragoza-50013, Spain Departamento de Medio Ambiente y Ciencias del Suelo, Universidad de Lleida, Av. Alcalde Rovira Roure, 191, Lleida-25198, Spain
Received 15 June 2005; received in revised form 31 October 2005; accepted 21 December 2005 Available online 28 February 2006
Abstract Zebra mussels (Dreissena polymorpha) were first found in the Ebro River (Spain) in Ribaroja reservoir, in the summer of 2001. This paper reports a study to detect parasites in this bivalve species. From September 2003 to August 2004, a total of 1380 zebra mussels were collected and dissected or sectioned in paraffin and haematoxylin and eosin staining. We observed the presence of Phyllodistomum folium (Olfers, 1816) in two hosts (prevalence 0.14%). Sporocysts containing metacercariae were located within the gill lamellae. One of the mussels was collected in January and the other one in July. In both cases the shell length was N 2 cm. P. folium had not been previously reported in Spain and D. polymorpha is its only known intermediate host. It represents a new invasive species in this river basin, presumably introduced together with the zebra mussels. © 2006 Elsevier Ireland Ltd. All rights reserved. Keywords: Dreissena polymorpha; Phyllodistomum folium; Spain; Ebro River; Digenea
1. Research note The zebra mussel, Dreissena polymorpha, is a freshwater bivalve native to the drainage basins of the Black and Caspian Seas, which has now spread throughout the waterways in Europe and the eastern U.S. The growth of zebra mussel populations may result in both environmental and economic problems as water treatment facilities may experience fouling and loss of intake heads [1,2]. Very little research has been conducted on zebra mussels parasites and it is not sufficient to investigate the diversity, distribution or pathology caused by endosymbionts on the mussels, as was pointed out in a review on natural enemies of zebra mussels [3]. However, during the last decade a series of articles have contributed to a better understanding of the relationship between zebra mussels and its endosymbionts [4–13].
⁎ Corresponding author. Tel.: +34 976761561; fax: +34 976761612. E-mail address:
[email protected] (M.A. Peribáñez). 1383-5769/$ - see front matter © 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.parint.2005.12.002
Zebra mussels were first detected in Spain during the summer 2001, in the lower Ebro River [14]. It was then that we planned to carry out a study on parasites of this exotic bivalve species. It is known that, when invading new habitats, D. polymorpha may introduce up to nine nonindigenous species [5]. Several hundred of zebra mussels were collected in the Ebro River from September 2003 to December 2004 for dissection or histopathological investigation. In this study, we noted the presence of Phyllodistomum folium (Olfers, 1816) (Gorgoderidae) for the first time in Spain as a consequence of the introduction of zebra mussels. The river stretch studied extends from Ribaroja reservoir, close to the dam, to Ascó wharf (is it length, i.e. 25.5 km). A total of 1380 zebra mussels were collected from September 2003 to August 2004 (Table 1). The bivalves were classified in three categories according to the length of their shell: b1 cm; 1–2 cm and N2 cm. All of them were opened for dissection or fixed in 10% buffered formalin. The fixed mussels were embedded in paraffin and routine sections of 5 μm were obtained and stained with
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Table 1 Survey of mussels (Dreissena polymorpha) collected (by size and month) Sampling Dissection date Mussel size
Total Histological sections Mussel size
b1 cm 1–2 cm N2 cm Sep 03 Nov 03 Jan 04 May 04 Jun 04 Jul 04 Aug 04 Total
38 mussels not classified by size 16 79 0 66 0 59 0 13 48 50 0 16 64 283
Total
b1 cm 1–2 cm N2 cm 38
40 75 56 10 50 23 254
135 141 115 23 148 39 639
0 0 6 0 0 13 19
111 101 77 12 61 29 391
76 66 71 14 73 31 331
186 167 155 26 134 73 741
haematoxylin and eosin. Dissected mussels and histological sections were checked to detect the presence of parasites using light microscopy. Only one helminth species was identified in the bivalves examined. Two mussels (prevalence 0.14%) were infected with larval stages of P. folium. The presence of the parasites (Fig. 1) was macroscopically detected after opening both mussels. In both cases, they were also processed by histological techniques. One of the mussels was collected in January and the other one in July. In both cases the shell length was N 2 cm (2.6 and 2.9 cm). During dissection of bivalves, a few dozen of flat elongate whitish/yellowish sporocysts were macroscopically observed in both mussels (Fig. 1). We also observed metacercariae located inside these sporocysts (Fig. 2). As in previous histological reports [9], we could observe that sporocysts were located within branchial sinuses, deforming the gill lamellae (Fig. 2) and no other organs were infected. Parenchymatous cells and developing metacercariae could be detected inside the sporocysts. The most developed metacercariae were C-shaped and one or both suckers were observed (Fig. 3). P. folium is the only helminth species we found parasitizing zebra mussel in the Ebro River. It had not been reported previously in Spain. Phyllodistomes exhibit a close morphological similarity and a great intraspecific variability [12,15].
Fig. 1. P. folium sporocysts in the gills with the typical flat elongate shape. SP: sporocysts.
Fig. 2. P. folium sporocysts between the inner and outer epithelium of the deformed gill lamellae. Developing metacercariae in the sporocysts. ME: metacercaria; SW: sporocyst wall.
The taxonomic status of adult phyllodistomes is unclear. However, in our study, it was possible to identify species specificity as, in this genus, P. folium is the only valid species confirmed as a zebra mussel parasite [9,12]. Furthermore, histological photomicrographs of key morphological features and the precise location (sporocyst located only within branchial sinuses, i.e., the spaces between the inner and outer epithelium of gill lamellae) previously reported [9] have been very useful for species confirmation. Molloy et al. [3] listed seven families of trematodes as parasites of zebra mussels, although infections with the Sanguinicolidae, Plagiorchiidae, and Brachylaemidae have been considered extremely rare [3,9]. Besides, we have not found any specimen belonging to the Bucephalidae, Echinostomatidae or Aspidogastridae which are families commonly recorded parasitizing zebra mussels in Europe. Karatayev et al. [5] also found only one species of parasite in recently colonized
Fig. 3. P. folium sporocyst containing, developing c-shaped metacercaria. ME: metacercaria; SU: sucker; SW: sporocyst wall.
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lakes in Belarus, whereas older zebra mussel populations proved to have the highest number of alien species. We detected a prevalence of infection in zebra mussel by P. folium as low as 0.14%, which agrees with data reported by other authors. Phyllodistomum infection is not common in zebra mussel populations and, where present, prevalence tends to be lower than 1% [3,10]. In a recent investigation into several thousand mussels all over Europe, only eleven specimens were confirmed to be infected by P. folium [9] whereas in Belarus, prevalences ranged between 0.3% and 2% [5]. Acknowledgements The authors would like to thank the members of “Grupo Especial de Actividades Subacuáticas de la Guardia Civil” for diving in the Ebro River and collecting the mussels for this study, and also to the Spanish Electric Company “Endesa” for financial help. References [1] Karatayev AY, Burlakova LE, Padilla DK. The effects of Dreissena polymorpha (Pallas) invasion on aquatic communities in eastern Europe. J Shellfish Res 1997;16:187–203. [2] Strayer DL. Effects of alien species on freshwater mollusks in North America. J N Am Benthol Soc 1999;18:74–98. [3] Molloy DP, Karatayev AY, Burlakova LE, Kurandina DP, Laruelle F. Natural enemies of zebra mussels: predators, parasites, and ecological competitors. Rev Fish Sci 1997;5:27–97. [4] Burlakova LE, Karatayev AY, Molloy DP. Field and laboratory studies of zebra mussel (Dreissena polymorpha) infection by the ciliate Conchophthirus acuminatus in the Republic of Belarus. J Invertebr Pathol 1998;71:251–7.
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