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versión impresa ISSN 0327-9545

Biocell v.30 n.2 Mendoza mayo/ago. 2006


Facultative and obligate symbiotic associations of Pomacea canaliculata (Caenogastropoda, Ampullariidae)

I.A. Vega*, M.C. Damborenea**, C. Gamarra-Luques*, E. Koch*, J.A. Cueto, and A. Castro-Vazquez*

* Laboratory of Physiology (IHEM-CONICET), Department of Morphology and Physiology, Faculty of Medicine, National University of Cuyo .
** Invertebrate Zoology Department, Faculty of Natural Sciences and Museum, National University of La Plata , Argentina

Address correspondence to: Dr. Israel A. Vega. Fisiología Normal, Facultad de Ciencias Médicas, Universidad Nacional de Cuyo. Casilla de Correo 33. (5500) Mendoza, ARGENTINA. Fax: (+54-261) 449 4117. E-mail: /

Key words: Mollusk symbiosis. Applesnails. Endocytobiosis. Bacterial symbiosis. Eukaryotic symbiosis.

Pomacea canaliculata (Lamarck 1822) occurs mainly in lentic habitats throughout the lower Amazon basin and the Plata basin (Hylton-Scott, 1958; Martín et al., 2001). This Neotropical species has been introduced (ca. 1980) to several South East Asian countries for aquaculture, and has become a serious pest for rice and other crops (Halwart, 1994). Many Pacific islands are currently included in the invaded area (Cowie, 2002).
In a previous previous publication we have presented preliminary evidence for a symbiotic association of Pomacea canaliculata and of other Neotropical Ampullariidae with a large and pigmented prokaryotic symbiont within specific cells of the midgut gland of this snail (Castro-Vazquez et al., 2002). The current paper overviews the diversity of symbiotic associations of P. canaliculata , and updates the information on the prokaryotic symbiont, which is most likely a cyanobacterium.

What do we put in the term “symbiosis”?

The development of symbiosis theory has been a complex one, as Sapp (1994) has masterfully depicted, and this is many times reflected in a conflicting use of terms. What is now called “symbiosis” was conceptually postulated by the first time in 1868, by the Swiss botanist Simon Schwendener (1868), who interpreted the lichens as modified fungi that keep a green algae[1] “in slavery”. For this special parasitic[2] relationship, Johannes Reinke (1873) suggested the use of consortium , a word that is in use even today, and another German lichenologist, Albert Bernhard Frank (1877), coined the term Symbiotismus. [3] Even though his studies were well known and his treatise on Botany (Frank, 1892) was widely used, credit for coining the term was (and is) generally given to Heinrich Anton de Bary, who first used the term symbiosis ( Symbiose ) in his address to a joint meeting of German naturalists and physicians (de Bary, 1879). He defined it as “the living together of unlike named organisms”, and said that “parasitism, mutualism, lichenism, etc., are each special cases of that one general association for which the term symbiosis [ Symbiose ] is proposed as the collective name”.[4]
Buchner (1921) studied the microbial symbionts of aphid insects and concluded that the development of such cells, tissues and organs as the aphid mycetocytes and mycetosomes could not occur without having profoundly altered the physiology and even the habits of the hosts. This was a seed notion that symbiotic relationships are the outcome of a co-evolutive process.
Nuttall (1923) and Meyer (1925) elaborate this argument and conceived the origin of symbiosis through a preliminary stage of parasitism on the part of one of the associated organisms, and the solution of the conflicts between them, in the course of time, by their mutual adaptation. Both species have to alter their physiology and even their habitats, and –which is worst– all the process is, as normal in Evolution, open-ended: co-evolution may imply a one-to-one gene adjustment every time the host or the symbiont get some significant mutation (Ridley, 1996).
It has been early acknowledged that the difference between parasitism and mutualism might be blurred, not only in the course of evolution but also in the host's lifetime (Nuttall, 1923; Meyer, 1925). As an example of the latter, Candida albicans , a harmless inhabitant of the human skin and intestine, causes lesions when either the associated bacterial biota or the immune status of the host changes. Even cyanolichens, generally quoted as prime examples of mutualism between eukaryotic and prokaryotic organisms, do not show anything but a continuous cline of possibilities from parasitic to mutualistic interactions (Rikkinen, 2002).
For these reasons, many authors have come to use the term symbiosis as encompassing parasitic, commensal and mutualistic interactions, i.e., as a comprehensive concept that does not consider the role which the two individuals play but is based in the mere coexistence, as Frank (1877) proposed more than a century ago. More recently, the concept was extended to include some associations involving not whole cells but dietary chloroplasts (Kawaguti and Yamasu, 1965; Taylor, 1968; Greene, 1974; Trench, 1975), as found in the cells of the midgut gland in elysioid opistobranch slugs (a special case of symbiosis referred to as “kleptoplasty”, Gilyarov, 1983; see also Rumpho et al., 2000, for a recent review). A similar association has only recently been reported for the Argentinean marine slug Elysia patagonica (Muniain et al., 2001). In fact, the consequences of such acquisition of chloroplasts may bear interesting parallels with the apparently cyanobacterial-gastropod symbiosis that will be commented on later in this paper.
For the sake of clarity, we will briefly and precisely define some terms related to the concept of “symbiosis”, as they will be used in this review: (1) In a symbiotic association (sometimes, also called consortium) the largest organism is named the host, while the smaller is named the symbiont. (2) Obligate (as opposed to facultative) symbioses refer to associations involving symbionts found in all individuals of the host species. (3) Epibiosis and derived terms are used when the symbiont lives on the external parts of the host (for P. canaliculata , the periostracum and the operculum). (4) Endosymbiosis (and derived terms) refers to a consortium in which the symbiont lives within the limits of the host's body (also including cavities communicated to the exterior, as the gut and mantle cavity). (5) Endocytobiosis (and derived terms) refers to an intracellular endosymbiosis. (6) Cyanobiont refers to a cyanobacterium involved in a symbiosis.

A survey of symbiotic associations with Eukarya

Epibiotic associations

In a study on P. canaliculata individuals , collected in both lotic and lentic habitats in the surroundings of the middle Paraná river , Di Persia and Radici de Cura (1973) described a diverse community of epibiotic organisms covering the periostracum (and to a lesser extent, the operculum) of this species. Also, they demonstrated (1973) that those epibiotic community is different between dead and live snails (diversity and quantity), suggesting that the movement of the host is necessary to maintain the community of epibiotic organisms). Taxonomically equivalent communities were also observed in Pomacea insularum and Pomacea scalaris , although the epibiotic mat was thicker in P. canaliculata and P. insularum than in P. scalaris (a fact likely related to the smoother surface of the periostracum in the latter species). The composition and stratification of the epibiotic community may be outlined as follows: (1) a rather thick mat, predominantly composed by the chlorophytes Stigeoclonium sp. and Oedogonium sp. (Oedogoniaceae), together with species in the genera Spirogyra and Mougeotia (Zygonemataceae), Scenedesmus (Scenedesmaceae) and Ankistrodesmus (Oocystaceae); chlorophytes were followed in abundance by chrysophytes in the genera Gomphonema (Gomphonemaceae, living on Stigeoclonium ) and Navicula spp. (Naviculaceae); sessile ciliates ( Vorticella campanula , Vorticellidae, and Epistylis plicatilis , Epistylidae) also occur in this basal substratum were also composing the algal mat; (2) a diverse biota of motile organisms inhabiting the predominantly algal mat, including euglenophytes ( Trachelomonas spp. and Phacus spp. ), a variety of ciliates in the genera Coleps (Colepidae), Didinium (Didiniidae), Chilodonella (Chilodonellidae) and Codonella (Codonellidae), rotifers (genera Rotaria, Philodinidae, and Keratella and Brachionus , Brachionidae), nematodes (genus Actinolaimus, Actinolaimidae), leeches ( Helobdella ampullariae , Glossiphoniidae), oligochaete ( Chaetogaster limnaei , Naididae), aphanoneurans ( Aeolosoma spp. , Aeolosomatidae) and dipterans larvae ( Chironomus sp. , Chironomidae). Cazzaniga (1988) also observed an ectoproct ( Hyalinella vahiriae ) living in the suture of P. canaliculata , and Dreher Mansur et al., (2003) and Darrigran and Damborenea (2005) have recently added the exotic golden mussel Limnoperna fortunei (Mytilidae) to the list of frequently found epibionts.

Symbiotic animals in the mantle cavity

A variety of organisms have been found dwelling within the mantle cavity of P. canaliculata . However, it should be noted that their diversity (even if we include those endosymbionts in other snail's organs) does not parallel that of the epibiota, which may indicate some selectivity on either the part of the host or of the symbionts. Some possibilities of selectivity on the part of the symbionts suggest themselves, e.g. that photosynthetic organisms would not be able to survive as endosymbionts in dark environments, or that sessile organisms will not found adequate surfaces for fixation. It is also possible that the mucous secretion and the water current in the mantle cavity may be unfavorable for the settling of many organisms.

Platyhelminthes, Turbellaria:

Temnocephala iheringi (Temnocephalidae) is the most common turbellarian in the mantle cavity of P. canaliculata and it also extends to the lung. The egg capsules are always laid over the periostracum, especially at the opening of the umbilicus and in the contact zone of the peristome with the suture. T. iheringi has also been found associated to other ampullariid species ( Pomacea haustrum , Pomacea lineata , Asolene platae and Pomella megastoma , Damborenea and Cannon, 2001). This temnocephalid symbiont has been recorded from Brazil , Argentina and Uruguay , while other two species ( Temnocephala haswelli and Temnocephala rochensis ) have only been reported from Uruguay.
High prevalence values of T. iheringi (92-100%) were found in two P. canaliculata populations: Bagliardi beach, on the southwest bank of the Plata river (Damborenea, 1996) and Regatas Lake , Palermo , Buenos Aires city (Table 1). Abundance was about 14 temnocephalids per snail in the Bagliardi beach study (range: 0-167; n=303), and no significant differences in abundance were found between male and female hosts (Damborenea, 1996). Both abundance and aggregation in the mantle cavity were higher in late spring and summer (Damborenea, 1998). Although T. iheringi was also found associated to other ampullariid species (Damborenea and Cannon, 2001), stronger Aeolosoma association to P. canaliculata was apparent, since no temnocephalid worms were found in either P. scalaris (Damborenea, 1996; and Table 1) or Asolene pulchella (Table1). Nevertheless, this is not an obligate symbiosis for P. canaliculata either: in a study covering 20 habitats occupied by P. canaliculata in the province of Buenos Aires (Martín et al., 2005) T. iheringi was found in only eight sites (three out of 13 lotic habitats, and five out seven lentic habitats). No information is available regarding the functional significance of this consortium.


Platyhelminthes, Trematoda:

Several trematode larval stages have been described associated to P. canaliculata, both found in the mantle cavity (cercariae and metacercariae).
Probably related rediae were found in the connective tissue of the midgut gland and gonad (see below). The identification of trematode species is based on the adult forms, which are usually found in vertebrates. Therefore, generic or specific identification of larval stages is often impossible, unless the entire life cycle could be studied.
Two types of cercariae have been found in the mantle cavity of snails, in both streams and lakes of the Buenos Aires province: schistosomatid cercariae have been found in the Luján river and on the Bagliardi beach (Damborenea, unpublished data); and a xiphidiocercaria has also been found in the same localities (Ostrowski de Nuñez, 1979). Metacercariae have also been described in the mantle cavity ( e.g. Echinostoma parcespinosum , Martorelli, 1987). The metabolic, physiological and/or ecological interactions between these larval stages and their host are unknown.

Annulata, Hirudinea:

Five Glossiphoniid leeches have been found in the mantle cavity of Pomacea canaliculata collected on the Bagliardi beach (Plata river): Helobdella ampullariae , Helobdella triserialis , Helobdella simplex , Helobdella adiastola and Gloiobdella michaelseni (Damborenea and Gullo, 1996). As we have already mentioned, some individuals are also found on the operculum and periostracum.
All life stages of H. ampullariae (juveniles, adults and adults with both cocoons and broods) were found inside the snail, but they were never found free in the habitat (Damborenea and Gullo, 1996).
The reproductive season extends from December to June, i.e., overlapping to some extent the quiescent seasonal period of P. canaliculata , when the host is usually buried in the mud. The abundance of H. ampullariae on P. canaliculata increases with the host size: 0-1 leeches were found in juvenile snails (< 20 mm length), while up to 65 leeches were found in bigger snails, and the symbiont prevalence rose to 100%. Transmission of the symbiont probably occurs during copulation (Damborenea and Gullo, 1996). This leech has been also found as an endosymbiont to Pomella megastoma and P. insularum, Ampullariidae, and Chilina fluminea , Chilinidae (Ringuelet, 1945, 1985).
Both brooder adults and juveniles of the other four Helobdella species were only found during the spring and summer (Damborenea and Gullo, 1996), while H. ampullariae was also found in autumn and winter. No information is available of the functional significance of these consortia with P. canaliculata . They are not present in all populations of the snail, and therefore, should not be considered obligate symbiosis. The associations probably benefit the brooders and juveniles with food and protection.

Crustacea, Copepoda:

So far, only two copepod species have been described as endosymbiotic to freshwater invertebrates, and they both were found associated to Pomacea species: Ozmana haemophila (Cyclopoidea, Ozmanidae, Ho and Thatcher, 1989), which is associated to P. maculata , and O. huarpium (Gamarra-Luques et al., 2004) which is associated to P. canaliculata .
O. huarpium
was found in rather large numbers (about one hundred copepods per snail) in snails from both a cultured strain and from the locality of the strain's original stock ( Palermo , Buenos Aires City ). In spite of the large number of copepods, there was no evidence of
tissue reactions or of any harm to the host. While O. haemophila was found restricted to the haemocoel of P. maculata , and occurring in rather small numbers (1-14 copepods per snail), O. huarpium (also found in the haemocoel) predominates in the penis sheath groove, the ctenidium and the mantle cavity, figuring in these pallial organs 63-65% of total mature forms. The sex ratio of the endosymbiont is skewed to the female side in these organs, specially in male hosts. Apparently, a special female tropism of O. huarpium for the male host's pallial organs might ensure interindividual transmission of the endosymbiont, which would be mainly transmitted during copulation.
All snails were bearing O. huarpium in the original study (Gamarra-Luques et al., 2004). Interestingly, however, no copepods were found either in P. scalaris or Asolene pulchella that were collected in the Regatas lake ( Palermo , Buenos Aires city) where all P. canaliculata were infested, indicating a specificity of the consortium between P. canaliculata and O. huarpium (Table 1). However, this is not an obligate symbiosis for the snail, since no copepods have been found in P. canaliculata individuals collected in four localities other than Palermo.[5]

Aracnida, Acari:

An unionicolid species, Unionicola (Ampullariatax) ampullariae , has been reported in the mantle cavity of both P. canaliculata and P. insularum (Vidrine, 1996). Di Persia and Radici de Cura (1973) also mention that up to 14 individuals may be found in large snails, and larvae, nymphs and adults may all of them be found in the mantle cavity. We have observed that they are not present in all populations of P. canaliculata , and therefore, they do not constitute an obligate symbiosis.

Symbiotic animals in the haemocoel and connective tissue

Platyhelminthes, Trematoda:

Two redia generations of Echinostoma parcespinosum were described in the connective tissue of the digestive gland and gonad of P. canaliculata . One to three cercariae were observed inside rediae of the second generation. In this case the snail is the first intermediate host of this parasite, whose adults are found in the intestine of the rails Rallus maculatus and Rallus sanguinolentus (Martorelli, 1987).
Rediae containing immature cercariae of Dietziella egregia (whose definitive host is the white-faced ibis Plegadis chihi ) were observed just once (Digiani and Ostrowski de Nuñez, 2000). Some different but unidentified schistosomatid metacercariae have been frequently found in the pericardial cavity (Damborenea, unpublished data) and in the posterior renal cavity ( Dietziella egregia , Digiani and Ostrowski de Nuñez, 2000).
The above mentioned studies were carried out
within the native range of P. canaliculata , while Keawjam et al. (1993) have studied natural infestation of the snail in Thailand , an invaded area (Cowie, 2002). They have found three different trematode metacercariae: amphistomes (from the foot), distomes (from the heart, kidney and foot muscle), and echinostomes (from the foot). The effect of these larvae on P. canaliculata was not assessed, but the authors suggest that some alteration in the reproductive efficiency might occur.

Crustacea, Copepoda:

As we already mentioned, Ozmana huarpium is not only found in the mantle cavity but also in the haemocoel of P. canaliculata , and it was occasionally found in hollow organs as the seminal vesicle, but not in the gut. It was never found in connective tissue.

Symbiotic protists and animals in the gut


Two species of large ciliates, Parasicuophora ampullariarum and Parasicuophora corderoi have been described as inhabiting the gut of P. canaliculata (Gascón, 1975). These ciliates are not found in all populations of the host, therefore should be classified as facultative symbioses.


We have frequently observed a bdelloid rotifer (Gamarra-Luques and Castro-Vazquez, unpublished findings) in the gut content and feces of a cultured strain of P. canaliculata . This rotifer remains alive for at least several days outside the snail, i.e., in the aquarium sediments. A proper description of this association is wanting. Also, no studies of the distribution of this rotifer in the natural populations of P. canaliculata are available.


Chao et al. (1987) have reported the experimental infection of P. canaliculata by Angiostrongylus cantonensis . This worm does not occur in the native range of P. canaliculata , but it does in the invaded territories. Snails may become infected as a consequence of ingestion of nematode eggs present in rodent fecal pellets. Man is infected by ingestion of third state larvae (Jindrak, 1975). This nematode is a common causative agent of human eosinophilic meningoencephalitis, a serious and frequently epidemic disease.

Platyhelminthes, Trematoda:

One species of Paramphistomidae, Catadiscus pomaceae , has been found in the intestine of P. canaliculata from a natural population from Corrientes province, Argentina (Hamann, 1992). Other known species of Catadiscus are associated to amphibians and reptiles, and while other adult trematodes have also been recorded in other mollusks (e.g., Martorelli, 1989), this is the only record of one inhabiting the intestine of an ampullariid snail (Hamann, 1992). No information is available about the effects of this endosymbiotic trematode on P. canaliculata . Its life cycle is unknown, but considering the known life cycles of Paramphistomidae, P. canaliculata may become infested by ingesting metacercariae found on plants and other substrata.

Symbiotic associations with Bacteria

Epibiotic bacteria:

Di Persia and Radici de Cura (1973) have noted the presence of filamentous cyanobacteria of the genera Oscillatoria and Lyngbya (Oscillatoriales) living in the epibiotic community of the periostracum of P. canaliculata . They also mentioned Nostoc commune , but only in some individual snails. The same authors mention numerous “filamentous bacteria” within the predominantly algal mat (probably chains of heterotrophic coccoid and rod-like bacteria).

Extracellular endosymbiotic bacteria:

Also, as in many other mollusks (e.g. Rosenberg and Breiter, 1969), the gut of Pomacea canaliculata is colonized by numerous coccoid or rod-like heterotrophic bacteria. However, we are not aware of any attempt of identifying them in P. canaliculata , and of exploring their possible functional implications.
In the latter respect, we have recently observed (Vega et al., 2005) that Pomacea canaliculata can live on a cellulose-only diet for at least two months, which would indirectly indicate the presence of a cellulase in their gut, and that this cellulase may originate from the gut bacterial symbionts, as shown by rendelberger (1997) in a pulmonate snail.
However, it should also be mentioned that evidences for endogenous animal cellulases (first shown in the termite Reticulitermes speratus , Watanabe et al., 1998) have later been found in several species, including mollusks (e.g., Haliotis discus hannai , Suzuki et al., 2003).

An obligate endocytobiotic bacterium:

In our previous review (Castro-Vazquez et al., 2002) we suggested the existence of a symbiotic association of P. canaliculata to a large prokariont bearing chlorophyll-like pigment/s. The putative symbiotic corpuscles were found in midgut gland and feces of all P. canaliculata individuals from various places, which would indicate an obligate symbiotic association. Similar pigmented corpuscles were also found in the midgut gland and feces of P. insularum and P. scalaris, as well as in Asolene pulchella . Although the search for the presence of putative symbiotic elements in the latter species was not as thorough as that in P. canaliculata , both at the individual and population levels, it was also suggested that they would be obligate symbioses. The examination of a single individual of Marisa cornuarietis , another Neotropical ampullariid species, did show pigmented corpuscles in the midgut gland, but they did not appear to be eliminated in the feces.
Two pigmented corpuscular types within the cells of the midgut gland of P. canaliculata (identified as C and K corpuscles) appear to be morphotypes of the same organism, since transitional forms between typical C and K corpuscles can be seen in the midgut gland (Koch et al., 2005). Typical C corpuscles are rounded, 14 µm width, granule-containing bodies, which are encased in an electron dense wall. Sometimes an outer membrane could be seen detached from the external wall of C corpuscles, which may also contain some inner membranes but not true thylacoids. K corpuscles, on their part, are dark brown, either oval or club shaped bodies (36 µm length, 14 µm width) which appear made of electron dense lamellae surrounding a core of coarse globules (Castro-Vazquez et al., 2002; Koch et al., 2005). Also, seemingly nude forms of C corpuscles, i.e., without a wall but with a double membrane surrounding them, have also been shown within the gland's alveolar cells (Castro-Vazquez et al., 2002; Koch et al., 2005).
The mean corpuscular DNA content were estimated for glandular C corpuscles and found to be higher than known bacterial genome sizes, which would suggest that more than one genome copy may be present in a single corpuscle (Vega et al., 2005). Strong evidence for the bacterial nature of these corpuscles has come from the amplification of a 1500 bp DNA fragment corresponding to the bacterial 16S rRNA gene, using DNA extracted from glandular C and K corpuscles as template (Vega et al., 2005). However, DNA sequence identification of the symbiont, as those recently obtained for the cyanobacterial endocytobionts associated to the diatoms Climacodium frauenfeldianum (Carpenter and Jason, 2000) and Rhopalodia gibba (Prechtl et al., 2004) is still wanting. Nevertheless, both the size and the chlorophyll-like pigment/s of this bacterium strongly suggest that it should be a cyanobacterium in the order Chroococcales or Pleurocapsales.
It should be noted that the Cyanobacteria have been particularly successful in developing symbiotic associations during evolution, involving protists, fungi, plants and animals; however, known cyanobacterial endocytobioses are comparatively rare (Raven, 2002). In particular, cyanobacterial/animal endocytobioses have only been described in the marine sponge Siphonocalina tabernacula and in the didemnid ascidian Lissoclinum punctatum (Hirose et al., 1996, 1998). In both cases, most cyanobionts were located extracellularly in the host's tissues, while only some were found within amoebocytic, presumably phagocytic cells.
Nothing is known of the functional significance of this mollusk/bacteria endocytobiosis. Even though C corpuscles have chlorophyll-like pigment/s, it should be stressed that they would not be able to perform photosynthesis in the dark environment of the ampullariid midgut gland. Instead, chloroplasts occupying the cells of the many terminal midgut gland tubules located below the slug´s transparent dorsal mantle, are able to photosynthetically reduce carbon, and to transfer photosynthate to their host (Rumpho et al., 2000).
Transmission of the bacterial endocytobiont of P. canaliculata seems to occur vertically, i.e. it is directly transferred from mother to offspring, since pigmented corpuscles appeared in juveniles that were hatched aseptically and that were afterwards cultured in sterile media (Koch et al., 2003). So far, we have been unable to culture the endocytobiont in vitro (Koch and Castro-Vazquez, unpublished). However, since both C and K morphotypes are eliminated in large quantities in the feces, we searched for them in the environments where P. canaliculata lives. Morphologically “healthy” C corpuscles have been thus observed in the mud of limnotopes inhabited by P. canaliculata , even at the end of winter (i.e., after many months of snail quiescence). Also, they have been found in up to three years-old sediments of aquaria formerly inhabited by snails (Koch et al., 2005).

Concluding considerations

The number and diversity of endosymbiotic associations in which P. canaliculata is involved suggests that this metazoan organism does not establish a sharp distinction between self and non-self . This apparently non-stringent selectivity of P. canaliculata to host a variety of organisms poses several theoretical and practical questions: (1) Is this condition exclusive of this species, or is it shared with other ampullariid species? As we have mentioned above, a preference for P. canaliculata (as compared with P. scalaris and A. pulchella ) is shown by such varied symbionts as a temnocephalid worm ( T. iheringi ), a leech ( H. ampullariae ) and a cyclopoid copepod ( O. huarpium ). (2) Which are the trophic relations of these symbionts with their host, and with the other symbionts that may coexist in the snail?. (3) P. canaliculata has been shown susceptible to the natural infection with a symbiont, Angiostrongylus cantonensis (Keawjam et al., 1993), to which it is not exposed in its original range (Chao et al., 1987): would then be possible that other invasive species as P. lineata y P. bridgesi were able to develop new symbiotic associations in its present range, and that some of these symbioses would become a threat to man health? (4) Alternatively, as both artificial and beneficial symbioses have been developed (particularly of cyanobacteria with plants, see Gusev et al., 2002), would it be possible to utilize P. canaliculata as both an artificial and beneficial host?
A single obligate symbiosis (an endocytobiosis) of P. canaliculata with a prokariont has been described (Castro-Vazquez et al., 2002; Koch et al., 2005; Vega et al., 2005). The question of the presumptive cyanobacterial nature of this prokaryotic endocytobiont is interesting,
because known cyanobacterial endocytobioses are just a few and, so far, no one has been described in a mollusk (Vega and Castro-Vazquez, in preparation). Also, though several symbioses of mollusks with intracellular chemoautotrophic bacteria have been described (Cavanaugh, 1994; Felbeck, 1987; Shively et al., 1998; Windoffer and Giere, 1997), no symbiosis is known involving the cells of the midgut gland, except for the one presented here and for the already mentioned case of “kleptoplasty”. Since cyanobacteria may be the ancestors of both protistan and plant chloroplasts, it would be interesting that future studies will compare the obligate (apparently cyanobacterial) endocytobiosis of ampullariids with both the kleptoplasty of elysioid slugs, and with the primordial endocytobiosis from which chloroplasts originated.

[1] By 1868, the Algae were including the Cyanobacteria.

[2] The term “parasite” (and derived words) has been used in European languages since ancient times. For the Greeks, παρασιτος ( parasitos) was that who eats besides someone else, a concept akin to that of the Latin word commensal , i.e., that one who eats at the same table, or even who merely seats besides someone else; derived (and more specific) uses of παρασιτος referred to the citizens that were fed at the expense of the state, and eventually to macroscopical parasites of man and animals, in a strict biological sense.

[3] “We must bring all the cases where two different species live on or in one another under a comprehensive concept which does not consider the role which the two individuals play but is based in the mere coexistence and for which the term symbiosis [ Symbiotismus ] is to be recommended” (Frank, 1877).

[4] As for “parasitism”, “symbiosis” has also ancient roots: συµβιωτης ( symbiotes ) was said of who was living with someone else, or of who was having a favorite relation with someone. Συμβιωτικος ( symbiotikos ) was applied to anything related to life in common.

[5] The studied limnotopes where O. huarpium was looked for and not found were a fishing club near the town of Tunuyán (Mendoza), the banks of the Conlara river, near the town of Concarán (San Luis), the Bagliardi beach (on the Plata river) and the Tafí river (Tucumán).


1. Brendelberger H (1997). Bacteria and digestive enzymes in the alimentary tract of Radix peregra (Gastropoda, Lymnaeidae) Limnol Oceanogr. 42: 1635-1638.         [ Links ]
2. Buchner P (1921). Tier und pflanze in intrazellularer symbiose. Berlin : Borntraeger.         [ Links ]
3. Carpenter EJ, Janson S (2000). Intracellular cyanobacterial symbionts in the marine diatom Climacodium frauenfeldianum. J Phycol. 36: 540-544.         [ Links ]
4. Castro-Vazquez A, Albrecht EA, Vega IA, Koch E, Gamarra-Luques C (2002). Pigmented corpuscles in the midgut gland of Pomacea canaliculata and other Neotropical apple-snails (Prosobranchia, Ampullariidae): A possible symbiotic association. Biocell 26: 101-109.         [ Links ]
5. Cavanaugh CM (1994). Microbial symbiosis: patterns of diversity in the marine environment. Am Zool 34: 79-89.         [ Links ]
6. Cazzaniga NJ (1988). Hyalinella vahiriae (Ectoprocta) en la Provincia de San Juan. Revista de la Asociación de Ciencias Naturales del Litoral 19: 205-208.         [ Links ]
7. Chao D, Lin CC, Chen YA (1987). Studies on growth and distribution of Angiostrongylus cantonensis larvae in Ampullarium canaliculatus. Southeast Asian J Trop Med Public Health 18:248-252.         [ Links ]
8. Cowie RH (2002). Apple-snails (Ampullariidae) as agricultural pests: their biology, impacts and management . In: Mollusks as crop pests. Barker G.G. (ed.) CABI Publishing: Wallingford , pp. 145-192.         [ Links ]
9. Damborenea MC (1996 ). Patrones de distribución y abundancia de Temnocephala iheringi (Platyhelminthes, Temnocephalidae) en una población de Pomacea canaliculata (Mollusca Ampullariidae) . Gayana Zool 60: 1-12.         [ Links ]
10. Damborenea MC (1998). Distribution patterns of temnocephalids commensal with Crustacea and Mollusca from Argentina . Hydrobiologia 383: 269-274.         [ Links ]
11. Damborenea MC, Cannon LRG (2001). On Neotropical Temnocephala (Platyhelminthes) . J Nat Hist 35: 1103-1118.         [ Links ]
12. Damborenea MC, Gullo BS (1996). Hirudíneos asociados a la cavidad paleal de Pomacea canaliculata (Lamarck, 1822) (Gastropoda: Ampullaridae) del balneario Bagliardi, Río de la Plata , Argentina. Neotropica 42: 97-101.         [ Links ]
13. Darrigran G, Damborenea MC (2005). A bioinvasion history in South America . Limnoperna fortunei (Dunker, 1857), the golden mussel . Am Malac Bull. (in press).         [ Links ]
14. De Bary HA (1866). Morphologie und physiologie der Pilze, Flechten und Myxomiceten , 1st edition.         [ Links ]
15. Digiani MC, Ostrowski de Nuñez M (2000). Estudios preliminares sobre el ciclo biológico de Dietziella egregia (Dietz, 1909) (Digenea: Echinostomatidae) en la provincia de Buenos Aires . III Congreso Argentino de Parasitología, 1-4 Noviembre 2000, Mar del Plata. Resumen 366.         [ Links ]
16. Di Persia DH, Radici de Cura MS (1973). Algunas consideraciones acerca de los organismos epibiontes desarrollados sobre Ampullariidae . Physis B 32: 309-319.         [ Links ]
17. Dreher Mansur MC, dos Santos CP, Darrigran G, Heydrich I, Callil CT, Cardoso FR (2003). Primeros dados quali-quantitativos do mexilhao-dourado, Limnoperna fortunei (Dunker), no Delta do Jacuí, no Lago Guaíba e no Laguna dos Patos, Rio Grande do Sul, Brasil e alguns aspectos de sua invasao no novo ambiente . Rev Bras Zool. 20: 75-84.         [ Links ]
18. Felbeck H (1987). Symbiosis in the deep sea . Sci Am 256: 114-120.         [ Links ]
19. Frank AB (1877). Über die biologischen Verhältnissen des Thallus eineger Krustenflechten . Beitr Biol Pflanzen. 2: 123-200.         [ Links ]
20. Frank AB (1892). Lehrbuch der Botany. Leipzig .         [ Links ]
21. Gamarra-Luques C, Vega IA, Koch E, Castro-Vazquez A (2004). Intrahost distribution and transmission of a new species of cyclopoid copepod endosymbiotic to a freshwater snail, Pomacea canaliculata (Caenogastropoda, Ampullariidae) from Argentina . Biocell 28: 155-164.         [ Links ]
22. Gascón A (1975). Dos ciliados del género Parasicuophora parásitos de Pomacea canaliculata . Rev Biol Uruguay 3: 111-125.         [ Links ]
23. Gilyarov M (1983). Appropriation of functioning organelles of food organisms by phytophagous and predatory opisthobranch mollusks as a specific category of food utilization. Zh Obshci Biol 44: 614-620.         [ Links ]
24. Greene RW (1974). Symbiosis in sacoglossan opisthobranchs: functional capacity of symbiotic chloroplasts . Mar Biol. 7: 138-142.         [ Links ]
25. Gusev MV, Baulina OI, Gorelova OA, Lobakova ES, Korzhenevskaya TG (2002). Artificial cyanobacterium-plant symbioses . In Rai AN, Bergman B, Rasmussen U, eds., “Cyanobacteria in symbiosis”, Kluwer Academic Publishers, Dordrecht , pp. 253-312.         [ Links ]
26. Halwart M (1994). The golden apple snail Pomacea canaliculata in Asian rice farming system: present impact, and future threat . Internatl J Pest Manage. 40: 199-206.         [ Links ]
27. Hamann MI (1992). Catadiscus pomaceae sp. (Trematoda, Paramphistomidae) from Pomacea canaliculata (Lamark, 1801) (Prosobranchia, Ampullariidae) . Mem Inst Oswaldo Cruz 87: 9-14.         [ Links ]
28. Hirose E, Maruyama T, Cheng L, Lewin R (1996). Intracellular symbiosis of a photosynthetic prokaryote, Prochloron sp., in a colonial ascidian . Invertebr Biol. 115: 343-348.         [ Links ]
29. Hirose E, Maruyama T, Cheng L, Lewin R (1998). Intra- and extracellular distribution of photosynthetic prokaryotes, Prochloron sp. , in a colonial ascidian: ultrastructural and quantitative studies . Symbiosis 26: 193-198.         [ Links ]
30. Ho JS, Thatcher VE (1989). A new family of cyclopoid copepods (Ozmanidae) parasitic in the hemocoel of a snail from the Brazilian Amazon . J Nat Hist 23: 903-911.         [ Links ]
31. Hylton-Scott MI (1958). Estudio morfológico y taxonómico de los ampulláridos de la República Argentina . Rev Mus Arg Cienc Nat “B Rivadavia” e Inst Nac Invest Cienc Nat, Cienc Zool. 3: 233-333.         [ Links ]
32. Jindrak K (1975). Angiostrongyliasis cantonensis (eosinophilic meningitis, Alicata's disease). Contemp Neurol Ser 12: 133-64.         [ Links ]
33. Kawaguti S, Yamasu T (1965). Electron microscopy on the symbiosis between an elysioid gastropod and chloroplasts of a green alga . Biol J Okayama Univ 11: 57-65.         [ Links ]
34. Keawjam RS, Poonswad P, Upatham ES, Banpavichit S (1993). Natural parasitic infections of the golden apple snail, Pomacea canaliculata. Southeast Asian J Trop Med Public Health 24:170-177.         [ Links ]
35. Koch E, Vega IA, Albrecht EA, Gamarra-Luques C, Castro-Vazquez A (2003). Evidence for direct mother-offspring transmission of a possible symbiont inhabiting the midgut gland (MGG) of Pomacea canaliculata. Biocell 27: 24 (abstract).         [ Links ]
36. Koch E, Vega IA, Albrecht EA, Oortega HH, Castro-Vazquez A (2005). A light and electron microcopic study of pigmented corpuscles in the midgut gland and feces of Pomacea canaliculata (Caenogastropoda, Ampullariidae). Veliger 48:45-52.         [ Links ]
37. Martin PR, Estebenet AL, Cazzaniga NJ (2001). Factors affecting the distribution of Pomacea canaliculata (Gastropoda, Ampullariidae) along its southernmost natural limit . Malacologia 43: 13-23.         [ Links ]
38. Martin PR, Estebenet AL, Burela S (2005). Factors affecting the distribution and abundance of the commensal Temnocephala iheringi (Platyhelminthes, Temnocephalidae) among the southernmost populations of the apple snail Pomacea canaliculata (Mollusca: Ampullariidae). Hydrobiologia, (in press).         [ Links ]
39. Martorelli SR (1987). Estudios parasitológicos en biotopos lénticos de la República Argentina. IV. El ciclo biológico de Echinostoma parcespinosum Lutz, 1924 (Digenea) parásito de Rallus maculatus maculatus y Rallus sanguinolentus sanguinolentus (Aves: Rallidae). Rev Mus La Plata (N S) Zool. 14: 48-59.         [ Links ]
40. Martorelli SR (1989). Estudios parasitológicos en biotopos lénticos de la República Argentina. IV. Desarrollo del ciclo biológico monoxeno de la metacercaria progenética de Genarchella genarchella Travassos, 1928 (Digenea, Hemiuridae) parásita de Littoridina parchappei (Mollusca, Hidrobiidae) . Rev Mus La Plata (N S) Zool. 14: 109-117.         [ Links ]
41. Meyer KF (1925). The “bacterial symbiosis” in the concretion deposits of certain operculate land mollusks of the families Cyclostomatidae and Annullariidae . J Infect Dis. 36: 1-107.         [ Links ]
42. Muniain C, Marín A, Penchaszadeh PE (2001). Ultrastructure of the digestive gland from the larval and adult stages of the sacoglossan Elysia patagonica Muniain and Ortea, 1997 . Mar Biol. 139: 687-695.         [ Links ]
43. Nuttall GHF (1923). Symbiosis in animals and plants . Report of the British Association for the Advancement of Science, pp. 197-214.         [ Links ]
44. Ostrowski de Nuñez M (1979). Ungewöhnliche xiphidiocercarie aus Ampullaria canaliculata nebst Bemerkungen über Travtrema stenocotyle . Angew Parasitol 20: 46-52.         [ Links ]
45. Prechtl J, Kneip C, Lockhart P, Wenderoth K, Maier UG (2004). Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin . Mol Biol Evol 21: 1477-1481.         [ Links ]
46. Raven JA (2002). The evolution of cyanobaterial symbioses. Biol Environ Proc R Irish Acad 102 B: 3-6.         [ Links ]
47. Ridley M (1996). Evolution 2nd edition. Cambridge , Blackwell Science, Massachussetts, pp. 719.         [ Links ]
48. Reinke J (1873). Zur Kenntniss des Rhizoms von Corallorhiza und Epigogon . Flora 31: 145-209.         [ Links ]
49. Rikkinen J (2002). Cyanolichens: an evolutionary overview . In Rai AN, Bergman B, Rasmussen U, eds., “Cyanobacteria in symbiosis”, Kluwer Academic Publishers, Dordrecht , pp 31-72.         [ Links ]
50. Ringuelet R (1945). Hirudíneos del Museo de La Plata . Rev Mus La Plata (NS) Zool. 4: 95-137.         [ Links ]
51. Ringuelet R (1985). Annulata Hirudinea . En: Castellanos Z (ed). Fauna de agua dulce de la Republica Argentina (27) 1. FECIC, Buenos Aires , pp. 321.         [ Links ]
52. Rosenberg FA, Breiter H (1969). The cole of cellulolytic bacteria in the digestive processes of the shipworm. I. Isolation of some cellulolytic microorganisms from the digestive system of teredine borers and associated waters. Mater Org 4: 147-159.         [ Links ]
53. Rumpho ME, Summer EJ, Manhart JR (2000). Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol 123:29-38.         [ Links ]
54. Sapp J (1994). Evolution by association. A history of symbiosis . Oxford University Press, New York , pp. 1-254.         [ Links ]
55. Schwendener S (1868). Untersuchungen über den Flechtenthallus . Beitr wissensch Bot. 6: 195-207.         [ Links ]
56. Shively JM, van Keulen G, Meijer WG (1998). Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annu Rev Microbiol 52: 191-230.         [ Links ]
57. Suzuki K, Ojima T, Insita K (2003). Purification and cDNA cloning of a cellulase from abalone Haliotis discus hannai . Eur J Biochem 270: 771-778.         [ Links ]
58. Taylor DL (1968). Chloroplasts as symbiotic organelles in the digestive gland of Elysia viridis (Gastropoda Opistobranchia) . J Mar Biol Assoc UK . 48: 1-15.         [ Links ]
59. Trench RK (1975). Of “leaves that crawl”: functional chloroplasts in animal cells . Symp Soc Exp Biol 29: 229-265.         [ Links ]
60. Vega IA, Gamarra-Luques C, Koch E, Bussmann LE, Castro-Vazquez A (2005). A study of corpuscular DNA and midgut gland occupancy by putative symbiotic elements in Pomacea canaliculata (Caenogastropoda, Ampullariidae). Symbiosis 39: 37-45.         [ Links ]
61. Vidrine MF (1996). Najadicola and Unionicola. Gail Q. Vidrine Collectibles. Eunice, Louisiana, i-vi, pp. 1-182.         [ Links ]
62. Watanabe H, Noda H, Tokuda G, Lo N (1998). A cellulase gene of termite origin . Nature 394: 330-331.         [ Links ]
63. Windoffer R, Giere O (1997). Symbiosis of the hydrothermal vent gastropod Ifremeria nautilei (Provannidae) with endobacteria: Structural analyses and cological considerations. Biol Bull 193: 381-392.         [ Links ]

Received on April 7, 2005.
Accepted on May 30, 2005.

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