Abstract. Introduction. Narcis Prat 1, Diego Añón-Suárez 2 and Maria Rieradevall 1
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1 Aquatic Insects 2004, Vol. 26, No. 3/4, pp First Record of Podonominae Larvae Living Phoretically on the Shells of the Water Snail Chilina dombeyana (Diptera: Chironomidae / Gastropoda: Lymnaeidae) Narcis Prat 1, Diego Añón-Suárez 2 and Maria Rieradevall 1 1 Universitat de Barcelona, Barcelona, Spain; 2 Centro Regional Universitario Bariloche, Bariloche, Argentina Abstract Larvae of Podonomus albinervis Edwards, 1931 were found phoretic on Gastropoda Chilina dombeyana (Bruigière, 1789) on the shores of Lake Nahuel Huapi, in Bariloche, Argentina. Larvae were attached with mucus and some had developed a tube made of detritus on the spire of the snail shell. Adults and pupae with associated larval exuviae were found, which helped to identify the species. Approximately 10% of the snail individuals examined on the shores of the lake had chironomid larvae on their shells. Laboratory observations showed that the midge larvae leave the snail shell when the snail leaves the water, thus demonstrating the phoretic relationship. The high density of both snails and Chironomidae in the littoral habitats of the lake may explain this phoretic relationship. Keywords: Podonomus albinervis, Chilina dombeyana, phoresis, Argentina. Introduction Phoresy is defined as a special kind of commensal relationship in which one organism (the phoretic or phoront) attaches to another (the host) for a limited time period (Houck, 2003). Advantages of such behaviour may be dispersal to a new habitat and the incidental provision of substrate, shelter, or protection, but strictly speaking phoresy excludes any direct physiological benefit during transit (Houck, l. c.). Chironomid larvae have often been found living phoretically on other macroinvertebrates (e.g. Steffan, 1967a; White et al., 1980), particularly on Gastropoda (Mancini, 1979; Address correspondence to: N. Prat, Departament d Ecologia, Universitat de Barcelona, Diagonal 645, E Barcelona, Spain. nprat@ub.edu DOI: / Taylor & Francis Ltd.
2 148 N. Prat et al. Vinikour, 1982). The topic was revived as early as 1967 by Steffan (1967b) in one of the first reports of a phoretic relationship between snails and chironomids. 26 chironomid taxa are known to be commensal on freshwater invertebrates, and potential hosts include Ephemeroptera, Plecoptera, Trichoptera, Megaloptera, Hemiptera and Gastropoda (Tokeshi, 1995). The Podonominae is a Chironomidae subfamily that inhabits cold streams and brooks and is especially abundant in the northern or southernmost latitudes. The genus Podonomus is abundant in South America and close to 50 species have been found (Brundin, 1966). Its larvae are commonly associated with mosses in fast streams from the higher part of the Andes in Bolivia to the Magellan peninsula but are absent from the medium and lower part of the Amazon tributaries. Until now, no species of the family has been described as phoretic on other macroinvertebrates (Tokeshi, 1995). Material and Methods Material was collected on the shores of Lake Nahuel Huapi (40 50 S, W, 764 m a.s.l.), in the city of San Carlos de Bariloche, Patagonia, Argentina in March 1998 and February This is a large (557 km 2 ), deep (maximum depth 467 m) glacial oligotrophic lake (Pedrozo et al., 1993; Modenutti et al., 1998) with thermal stratification in summer (Quirós & Drago, 1985). Podonomus albinervis Edwards, 1931 was first described by Edwards in 1931 from the outlet of this lake. The city s lake shore is mainly composed of medium-sized rocks with some gravel and sand, and is exposed to wind. The periphyton community is composed mainly of diatoms and green algae (mainly filamentous), with a sporadic presence of blue-greens. These algae are more abundant on the lake front than at other sites in the lake because of the high nutrient input from human discharge (Baffico, 2001). The 1998 sample consisted of several individuals of the snail Chilina dombeyana (Bruigière, 1789) together with many Chironomidae larvae and pupae, including several Orthocladiinae (mainly Cricotopus) and Podonominae. The specimens were kept alive and examined in the laboratory where it was observed that the snail shells bore firmly attached midge larvae. The chironomid larvae, pupae, pupal exuviae and larval skins attached to pupae found on the shores of the lake and on the snails shells were dissected, cleaned and prepared for microscopic examination following the procedure described in Wiederholm (1983). Podonomus material collected in 1998 was: six larvae, 10 larval skins, three larval skins attached to pupae, six pupae, and one male and one female adult. All the material remains in the collection of the first author and was used to identify the species. The Edwards type material in the Natural History Museum in London (BMNH) was examined during a visit by two of the authors. The type material consisted of one uncleared male pupa and one uncleared larva and was labelled as collected in Argentina, Terr. Rio Negro, Bariloche, 6-XI-1926, ZW. Edwards, BM , pupae associated with Simulium femineum and Edwardsina nigra. As the number of larvae and snails observed in 1998 was low, in order better to determine the extent of the phoretic relationship between the snail and the midge, one hundred snails of different sizes were collected by D. Añon-Suárez in February These specimens were deposited individually in jars and taken to the laboratory for immediate observation in order to determine whether chironomids were present on the shells of the snails. Results Taxonomy All the material collected on the lake shores (larvae, pupae and adults) in March 1998 belonged to the midge species Podonomus albinervis. This species is very distinctive in its pupal and adult stages, as pointed out by Brundin (1966) in his monograph on the Podonominae of the Austral region. The BMNH type material collected by
3 Phoretic Podonominae on Water Snails 149 Edwards downstream from the outlet of Lake Nahuel Huapi (Río Negro) was examined by the authors and confirmed the species identification of the material collected in 1998 and Figures 1 6 show pictures of distinctive taxonomic characteristics of the pupae and larvae of P. albinervis from Lake Nahuel Huapi. These photographs/drawings complement the excellent taxonomic work and illustrations by Brundin (1966). The pupae and pupal exuviae fit Brundin s key (op. cit.), including the large ventral plate in the second segment, the curved hook of the seventh abdominal segment (Fig. 4), the dorsal setae arranged in a single transversal line and the length of the stalk of the thoracic horn (1/8 of the plate) (Figs. 2, 3). The number of anal setae is and 8 10 wavy setae were present in segment VIII. Some slight differences were Figures 1 7. (1 6) Podonomus albinervis: (1) pupal exuviae, dorsal view; (2) thoracic horn of pupae (lateral view); (3) idem (dorsal view); (4) abdominal segments VII and VII of pupae; (5) larval mandible; (6) larval mentum. (7) Chilina dombeyana, dorsal view.
4 150 N. Prat et al. found between the material collected in 1998 and 2003, the type material and the description provided by Brundin. Thus, the hook of segment VII is slightly less curved than in the original drawing by Brundin (1966, his fig. 170) or the type material (1 pupa) from the BMNH (compared with Fig. 4). In addition, the dorsal setae of the abdominal segments of the pupae are short and surrounded in some segments by six small tubercles, characteristic of the pupae of other Podonomus species but not described by Brundin for P. albinervis. In the samples taken on the shores of Lake Nahuel Huapi, two larval skins associated with pupae were found together with two larvae in the prepupal stage with pupal horns developed inside the last instar larvae. In all cases, the larvae were albinervis maculatus type sensu Brundin (1966). In our material, the larval head is wider in its posterior part, few setae are present in the larval body, the brush has seven setae, the brush pedestal is always dark, the epipharynx has three lobules, the third antennal segment is without rings, the antennae are short, and the medium tooth of the mentum has the same size as the first laterals (Figs. 5 and 6). A large distinctive mental brush is present. Phoresy In March 1998 only 10 snails were examined, several of which had P. albinervis larvae firmly attached. The larvae were difficult to remove and some secretion was present, although no tube of any kind was noted, unlike what has been observed for other species of Chironomidae (Mancini, 1979; Vinikour, 1982). Many other larvae were found living free in the littoral of the lake unattached to snails. In February 2003, 10 of the 100 snails examined had P. albinervis larvae attached. In this case a tube made by detritus and small sand grains was observed and this tube followed the shell spire. Some larvae were seen partially outside the tube. These larvae were probably eating algae attached to the shell surface of C. dombeyana. In the laboratory, larvae attached to the shells did not leave the Gastropoda while the snail remained submerged. When the snail leaves the water, however, the larvae abandon the shell and live freely on the bottom of the jar. In all cases a single individual larva was present on the shell and no relationship was observed between midge larval instars and shell size. No morphological adaptations of the phoretic individuals were found, as seems to be frequent in this kind of relationship (Houck, 2003). Discussion Brundin (1966) found one female of Podonomus albinervis in the littoral of Lake Nahuel Huapi and larvae and pupae of the same species in the waters of Lake Villarica in Chile, pointing out that this is the only species of Podonominae able to live in lakes. On the other hand, the snail Chilina dombeyana (Fig. 7) is exclusive to temperate South America, where it is widespread in lakes, rivers and irrigation canals (Habit et al., 1989). The species has been identified as an intermediate host of helminthid fish parasite larvae both in Chile and Argentina (Olmos & George-
5 Phoretic Podonominae on Water Snails 151 Nascimento, 1997; Revenga & Scheirnert, 1999). In Lake Nahuel Huapi, the emission of cercaria of the species Tylodelphis barilochensis (Quagiotto & Valverde, 1992) by C. dombeyana and the presence of this Trematoda on fish of the species Galaxias maculatus (Jenyns, 1842) have been reported. Galaxias maculatus may suffer blindness due to the parasite s action. This is the first record of a Podonominae phoresic on Gastropoda. The extent to which this phoresy is an obligatory or facultative relationship is unknown. Our laboratory observations suggest a facultative and temporary relationship (symphoresis according to Steffan, 1967b). P. albiventris lives temporarily on C. dombeyana, a pulmonate snail living on exposed rocks of the shore of Lake Nahuel Huapi but which may spend some time out of water. At such occasions, in the laboratory, Podonomus larvae abandoned the shell. Therefore, the relationship appears to be facultative, also in view of the large densities of unassociated Chironomidae larvae and Gastropoda in the littoral of the lake. Possible advantages of this kind of symphoresy may be access to algae growing on the shell and the transportation of larvae away from areas crowded by other larvae, preventing intraspecific competition. Acknowledgments The authors acknowledge the loan of the Edwards material and facilities provided by S. Brooks during the visit of N.P. and M.R. to the NHM London (M.R. had a Marie-Curie fellowship at that time). This paper was completed during a stay of N.P. and M.R. at the University of California, Berkeley. The authors are grateful for the Gaspar de Portolà grant provided to each by the Generalitat de Catalunya and to Prof. V. Resh for hosting them. The participation of Diego Añón-Suárez was funded by Grant B940 from the Universidad Nacional del Comahue (Argentina). One anonymous referee and the journal editor helped very much to improve the original manuscript. References Baffico GD (2001): Variations in the periphytic community structure and dynamics of Lake Nahuel Huapi (Patagonia, Argentina). Hydrobiologia 455: Brundin L (1966): Transantartic relationships and their significance as evidenced by Chironomid midges. With a monograph of the subfamilies Podonominae and Aphroteniinae and the austral Heptagyiae. Kung Sven Vetenskapsakad Handl 11: Habit E, Bertrán C, Arévalo S, Victoriano P (1989): Benthonic fauna of the Itata River and irrigation canals (Chile). Irrigation Sci 18: Houck MA (2003): Phoresy. In: Resh VH, Cardé RT, eds., Encyclopaedia of Insects. San Diego/London, Academic Press/Elsevier Science, pp Mancini ER (1979): A phoretic relationship between a chironomid larva and an operculate stream snail. Entomol News 90: Modenutti BE, Balseiro E, Dieguez MC, Queimaliños C, Albariño R (1998): Heterogeneity of fresh-water Patagonian ecosystems. Ecología Austral 8:
6 152 N. Prat et al. Olmos V, George-Nascimento M (1997): El gremio de larvas de digenea en el caracol del sur de Chile Chilina dombeyana. Qué indica la tasa metabólica de los hospedadores parasitados? Rev Chil Hist Nat 70: Pedrozo F, Chillrud S, Temporetti P, Díaz M (1993): Chemical composition and nutrient limitation in rivers and lakes of northern Patagonian Andes ( S; 71 W) (Rep. Argentina). Ver Int Verein Limnol 25: Quirós R, Drago (1985): Relaciones entre variables físicas morfométricas y climáticas en lagos patagónicos. Rev Asoc Cienc Nat Litoral 16: Revenga V, Scheirnert P (1999): Infections by Helminthid Parasites in Puyenes, Galaxias maculatus (Galaxidae, Salmoniformes) from Southern Argentina with special Reference to Tylodelphis barilochensis (Digenea, Platyhelminthes). Mem Inst Oswaldo Cruz 94: Steffan AW (1967a): Larval phoresis of Chironomidae in Perlidae. Nature 213: Steffan AW (1967b): Ectosymbiosis in Aquatic Insects. In: Henry, S.M. ed., Symbiosis. Vol II. New York/London, Academic Press, pp Tokeshi M (1995): Species interaction and community structure. In: Armitage P, Cranston PS, Pinder LCV, eds., The Chironomidae. The Biology and Ecology of Non-Biting Midges. London, Chapman and Hall, pp Vinikour WS (1982): Phoresis between the snail Oxytrema (= Elima) carinifera and aquatic insects, especially Rheotanytarsus (Diptera: Chironomidae). Entomol News 93: White TR, Weawer JSIII, Fox RC (1980): Phoretic relationships between Chironomidae (Diptera) and benthic macroinvertebrates. Entomol News 91: Wiederholm T (ed) (1983): Chironomidae of the Holartic Region Keys and Diagnoses. Part I Larvae. Ent Scand Suppl 19:
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