| Issue |
Int. J. Lim.
Volume 61, 2025
|
|
|---|---|---|
| Article Number | 7 | |
| Number of page(s) | 9 | |
| DOI | https://doi.org/10.1051/limn/2025006 | |
| Published online | 07 May 2025 | |
Research Article
Interactions between Anisus spirorbis (Planorbidae) and Galba truncatula (Lymnaeidae) in snail communities on sedimentary soils
Laboratory of Parasitology, Faculty of Pharmacy, 2 rue du Docteur Raymond Marcland, 87025 Limoges, France
* Corresponding author: gilles.dreyfuss@orange.fr
Received:
26
June
2024
Accepted:
19
March
2025
Field investigations were carried out in mid-April for two years in road ditches located in the department of Indre (central France) to determine whether there was competition between Anisus spirorbis and Galba truncatula in habitats where the two species live together. Compared to control populations, the number of A. spirorbis living in a community was 70 per cent lower in 2023 and 59 per cent lower in 2024, while the density of G. truncatula showed no significant variation. Shell diameter (A. spirorbis) or shell height (G. truncatula) did not differ significantly between community and control snails. Laboratory studies were also conducted from March to June for two years by placing juvenile, pre-adult or adult planorbids in the presence of juvenile, pre-adult or adult G. truncatula in Petri dishes for 30 days. The life stage of G. truncatula had a significant influence on the survival of A. spirorbis. In pairwise-raised snails, this survival was significantly lower for juvenile planorbids than for pre-adults. In contrast, survival of adult planorbids was slightly lower than that noted in corresponding controls, while their reproductive activity was significantly lower. This interspecific competition between A. spirorbis and G. truncatula would not be due to a limitation in food resources because food was abundant in their natural habitat or breeding dishes. It might be due to the action of mucus and/or toxicity of faecal pellets excreted by adult G. truncatula.
Key words: Anisus spirorbis / density / ditch / Galba truncatula / Lymnaeidae / Planorbidae / shell
© D. Rondelaud et al., Published by EDP Sciences, 2025
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
1 Introduction
The dwarf pond snail, also known as Galba truncatula, is well known among human and animal health professionals for its role as an intermediate host of the parasite, Fasciola hepatica. This lymnaeid enables the larval development of the fluke and therefore contributes to the transmission of this parasitosis to humans and many domestic or wild ruminants (Andrews et al., 2022). The control of G. truncatula is, in theory, relatively easy on acidic soils of Limousin (central France) because most snail habitats are located on the periphery of a surface drainage networks, have a small area and are populated only by G. truncatula (Rondelaud et al., 2009). In contrast, on the sedimentary soils of the Brenne Regional Natural Park (Brenne RNP) close to these acidic areas, the habitats of G. truncatula are often contiguous with those of other freshwater pulmonate gastropods. In winter and spring, the movements of these snails, particularly upstream, lead to an overlap in the distribution areas for G. truncatula and other gastropods. This results in the formation of communities with an extensive habitat and a width of the overlap area of up to 12 m (Rondelaud et al., 2009; Vignoles et al., 2017).
In western Europe, this type of snail community including G. truncatula is relatively common in road ditches, ponds, and open drainage ditches in swampy grasslands on sedimentary soils (Boycott, 1936; Kerney, 1999; Glöer and Diercking, 2010; Glöer, 2019). The list of pulmonate gastropods inhabiting these communities varies according to the country in which the study was conducted, the habitat type investigated and the geological nature of the subsoil (Costil et al., 2001; Bauer and Ringeis, 2002, for example). In the case of the Brenne RNP, the assemblage generally includes three species: Anisus spirorbis, G. truncatula, Omphiscola glabra with the less frequent presence of physids, namely Aplexa hypnorum or Physella acuta. According to Mouthon (1981, 1982), this group of species is characteristic of environments that dry up periodically during the summer season. Investigations carried out by our team between 2011 and 2015 in the Brenne RNP confirmed the frequency of these communities in ditches along roads or between adjacent land plots (Rondelaud et al., 2015, 2016a). In these habitats, the number of snails belonging to the overwintering generation was low: a mean density of 5.4 snails/m2 in March 2017 and 8.7/m2 in March 2018 (see Sect. 2.2.1 for the method used) in 24 communities formed by four of the above-mentioned species (unpublished data).
Several authors such as Osenberg (1989), Cross and Benke (2002) or Turner et al. (2007) have already shown that the size of a snail population in a community can be reduced by the action of one or more species that share the same habitat. Among the processes that may explain this, competition between snail species or individuals of the same species for food acquisition at a given site is most frequently cited (Byers, 2000; Turner et al., 2007; Dillon, 2010). As G. truncatula is present in most communities in the Brenne RNP, it was first necessary to assess the intensity of competition that other species may exert on this lymnaeid—or vice versa—before studying its impact on the distribution of trematode-infected G. truncatula within these communities. The American bladder snail (P. acuta) is already known to have invaded other countries globally (Wethington and Lydeard, 2007; Bousset et al., 2014; Ebbs et al., 2018) and for its effective competition with native snails that share the same habitat as it. According to the authors, this competition resulted in stunted growth and often mortality in juveniles of native species, and could go up to the exclusion of these species in the considered habitats (Brackenbury and Appleton, 1993; Cope and Winterbourn, 2004; Dobson, 2004; De Kock and Wolmarans, 2007; Zukowski and Walker, 2009). In France, some samples of P. acuta have been successfully introduced into different stations occupied by G. truncatula so that lymnaeids colonise the emerged areas of their habitats and fall prey to terrestrial predators (Rondelaud, 1978). Several experiments were also conducted by our team to study the interactions between G. truncatula and two other freshwater gastropods. The moss bladder snail (A. hypnorum) also exerted a less strong competition with G. truncatula. In pairs formed by this physid and this lymnaeid, survival of adult G. truncatula was significantly lower than that of pre-adults, while young G. truncatula had identical survival to that of controls (Rondelaud et al., 2016b). In habitats occupied by G. truncatula and O. glabra, the first species might be superseded by the second lymnaeid, which might lead to total extinction of G. truncatula (Rondelaud et al., 2005). When adults of both species are raised together in Petri dishes, mortality affected 80 per cent of G. truncatula while this was limited (< 10 per cent) in the corresponding controls after one month of breeding (Dreyfuss et al., 2014).
Unlike the two physids and O. glabra, the review of the literature did not show a report on the possible interactions between G. truncatula and A. spirorbis. As communities with these two species are relatively common in the southeast of the Brenne RNP, the two following questions arose: did competition exist between G. truncatula and A. spirorbis in the habitats where these two species lived together? What were the possible consequences of this competition on the life cycle of the lymnaeid or planorbid? To answer the first question, investigations were conducted in 2023 and 2024 in habitats inhabited by these two species to count these snails and specify the diameter or height of their shell in adults. Control habitats colonised by either species were also considered. The answer to the second question was realised in 2023 and 2024 by studying the survival of G. truncatula and A. spirorbis raised in pairs for 30 days under laboratory conditions. Controls were also established for each species with snails raised according to the same protocol.
2 Materials and methods
2.1 Stations studied
Snail investigations were carried out on a total of 15 road ditches colonised, either by a community with A. spirorbis and G. truncatula (five habitats), or by a population of planorbids or lymnaeids (five sites for each species). These ditches are located away from major roads in the municipalities of Chitray, Ciron, Luzeret, Migné, Nuret le Ferron, Rosnay, Ruffec and Thenay (Fig. 1). The area of habitats colonised by a community ranged from 5.7 to 7.5 m2 in mid-January 2023, while that of the control sites ranged from 7.2 to 9.6 m2 for A. spirorbis and from 4.1 to 6.2 m2 for G. truncatula. The bottom sediment is silt and sand, while the impermeable subsoil is usually sandstone or clay. Their capacity for water retention is low so that these ditches are very sensitive to summer dryness while they are waterlogged during the winter and spring (Parc Naturel Régional de la Brenne, 2012). In January 2023, the pH of stagnant water in ditches ranged from 6.7 to 7.8, and the level of dissolved calcium was distributed between 26 and 35 mg.L−1. In habitats colonised by A. spirorbis, G. truncatula, or a community with both species, vegetation was mainly composed of scattered clumps of rushes and plants belonging to the family Poaceae. The periphyton included many plant debris and detritus for most months of the year. Epiphytic green algae, abundant in spring on the dead leaves of trees, were also present in almost all habitats. All these ditches were not mowed during the two years of the study: 2023 to 2024.
The climate is temperate of oceanic type and is frequently swept by humid winds from the west or southwest. The average annual rainfall is about 550 mm, but can vary from one to two times from one year to the next (Parc Naturel Régional de la Brenne, 2012). The average annual temperature ranges from 10.5° to 11 °C with mild winters (Rondelaud et al., 2016a, 2016b).
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Fig. 1 Geographical location of the Indre department in central France (right map) and the municipalities (in green) on which the 15 snail habitats are located (left map). |
2.2 Field investigations
2.2.1 Experimental protocol
First, snails were surveyed in mid-April in the 15 ditches at the hottest hours of the day (13:00 to 16:00) because they were present at that time in the upper layer of the water. This period was chosen because all individuals belonging to the overwintering generation were then in the adult stage. Three quadrats of 1 m2 each, separated from each other by an interval of 1 or 2 m, were selected in each ditch. Snails were collected from each quadrat using a 20 cm diameter sieve (mesh size: 3 mm) when the depth of the water layer was greater than 10 cm, or by visual search in other cases (water depth less than 10 cm, or reduced to a film). This area was checked 30 minutes later to collect snails which could have escaped the first count. Snails were then classified according to their species and counted before being replaced in the prospected quadrat.
The diameter of the shell for planorbids and the height of the shell for lymnaeids were specified in a second step. Samples of 50 snails each were collected for each species and in each ditch in mid-April 2023 and 2024. After collection, the snails were transported to the laboratory and the height or diameter of their shell according to species was measured using a digital calliper. Snails were then returned in their natural habitat.
2.2.2 Statistics
The two parameters were the number of A. spirorbis or G. truncatula in the three quadrats selected in each ditch and the height or diameter of the shell in adults during investigations in mid-April. The values obtained for each parameter in the 15 habitats were grouped considering the snail species, the year of study and the status of the malacological stand (community, control population).
The normality of the values for each parameter was first analysed using the Shapiro-Wilk test (Shapiro and Wilk, 1965). As the distribution of these values were not normally distributed, the Kruskal −Wallis test was used to compare snail densities. This test was also used to compare the heights of adult shells for lymnaeids or shell diameters for planorbids. All analyses were carried out using R software version 4.1.2 (R Core Team, 2021).
2.3 Laboratory investigations
2.3.1 Snail groups
The life history traits of A. spirorbis, in the presence or absence of G. truncatula, were studied during two successive years (2023 to 2024). Three life stages were considered for A. spirorbis: juveniles (1–1.5 mm diameter), pre-adults (2.5–3 mm) and adults (4–4.5 mm). For G. truncatula, the shell height for the three life stages was 1.5–2, 3–4 and 5–6 mm, respectively. These dimensions were selected based on the maximum shell size in planorbids (6 mm in diameter) and lymnaeids (12 mm in height). The snails used for the experiments came from several monospecific populations living in ditches in the communes of Luzeret, Migné, Nuret le Ferron and Thenay. After their collection in the field, snails were acclimatised for 48 hours to laboratory conditions (see below). Most pre-adult and adult snails collected were then used for experiments. On the other hand, several adult snails of each species were reared in aquaria under laboratory conditions in order to obtain egg masses and, subsequently, juveniles and pre-adults for use in experiments.
Nine pairs were formed with both species (Tab. 1). Eight Petri dishes, each containing five plus five snails, were used for each pair (a total of 40 snails for A. spirorbis and 40 for G. truncatula). Control groups were set up according to the same protocol. Four dishes containing ten snails each were used for each life stage of the planorbid or lymnaeid (Tab. 1).
Four successive experiments were performed for each pair of snails and each control group according to the same protocol. Each was carried out with monospecific populations different from those used in a previous experiment. The first two trials took place from March to June 2023 and the other two over the same period in 2024.
The nine pairs of Anisus spirorbis + Galba truncatula and control groups used in laboratory studies. *, Eight Petri dishes for each pair of snails and four for each control group. The figures in this table represent a single experiment.
2.3.2 Breeding technology
Snails used in the experiments were placed in single-use Petri dishes (diameter of 14 cm) using the method that Rondelaud et al. (2007, 2014) and Dreyfuss et al. (2023) have applied to raise lymnaeids of the genus Galba. Dead leaves of herbaceous plants (usually Molinia caerulea are placed along the periphery of each container. A leaf of dried or degraded lettuce occupied the centre of each ssssssssox and is surrounded by four stems of Fontinalis antipyretica (spring moss) arranged in a rectangle around the lettuce. The spring moss ensures the oxygenation of the water while the dead leaves limit the emergence of snails and their immobilization on the dish walls. Two pieces of dead tree leaf, covered by epiphytic green algae (total area, 7 to 8 cm2) were placed in each dish in addition to lettuce because planorbids and lymnaeids frequently consume this type of plant in spring, Spring water (60 mL), with a dissolved calcium ion content of 35 mg.L−1, is added to each dish. The containers are placed in an air-conditioned room and are subjected to a constant temperature of 20° ± 1 °C and a photoperiod of 12:12 hours. The change of water and that of the food, if necessary, are carried out every day. On the 15th and 22nd day, the snails are placed in new Petri dishes prepared according to the same protocol. On the day 30, surviving planorbids and lymnaeids are counted.
In order to determine whether the presence of G. truncatula had an influence on the reproductive activity of A. spirorbis, the egg masses laid by adult planorbids or adult lymnaeids were removed from their breeding boxes when they were deposited. Egg masses provided by adults of both species in pairs: A. spirorbis + G. truncatula, and in corresponding control groups were counted each week during the four experiments conducted in 2023 and 2024.
2.3.3 Statistics
The first parameter studied was the number of live snails present in their dishes on day 30, while the second parameter was the total number of egg masses laid by A. spirorbis or G. truncatula during the 30 days of each experiment. The values obtained for each parameter in the four successive experiments were averaged, framed by a standard deviation, taking into account the species of snails and the group raised in petri dishes (pairs, controls).
The normality of values was first analysed using the Shapiro-Wilk test (Shapiro and Wilk, 1965). As the distribution of values was not normal for the first parameter, the Scheirer– Ray– Hare test, coupled with the post-hoc Steel– Dwass test (Siegel and Castellan, 1988), was used to compare the differences between the number of planorbids in pairs and the numbers of controls. In contrast, the distribution of values for the second parameter was normal and one-way analysis of variance was used to compare the differences between the numbers of egg masses laid by adult snails in pairs and those deposited by the corresponding controls. All analyses were performed using R 4.1.2 software (R Core Team, 2021).
3 Results
3.1 Field investigations
Table 2 shows the numbers of snails per m2 of habitat during the 2023 and 2024 investigations. In the control populations, the number of A. spirorbis per metre square of habitat was high with an average of 31.5 snails/m2 in 2023 and 28.7/m2 in 2024. However, in communities, the density of this species was significantly lower (2023: H = 26.78; p < 0.001; 2024: H = 19.54, p < 0.001). Compared to controls, the number of A. spirorbis in communities was 70 per cent lower in 2023 and 59 per cent lower in 2024. No clear variation in the density of snails in any population (communities, controls) was noted for G. truncatula.
The adult shell dimensions (height or diameter depending on the species) are presented in Table 3. The average diameter of the shell for A. spirorbis ranged from 5.5–5.8 mm, while the average height of the shell for G. truncatula varied from 9.9 to 11.3 mm. No significant differences between planorbid diameters or between lymnaeid heights were noted.
Number of snails per square metre of habitat in 15 ditches colonised by a community with Anisus spirorbis and Galba truncatula, or a control population in mid-April 2023 and 2024.
Adult shell dimensions in Anisus spirorbis and Galba truncatula in 15 ditches colonised by a community with both species, or a control population in mid-April 2023 and 2024. Parameter measured in adults: shell diameter in mm (A. spirorbis), shell height in mm (G. truncatula).
3.2 Laboratory investigations
3.2.1 Survival of snails
Table 4 gives the numbers of surviving planorbids in snail pairs and control groups at the end of the 1-month period. The life stage of G. truncatula had a significant influence (H = 44.86, p < 0.001) on the survival of A. spirorbis. The life stage of G. truncatula and the interaction between the life stages of both species had no clear effect on these results. In snail pairs, the survival of A. spirorbis was significantly lower for juvenile snails (p < 0.001) than for pre-adults (p < 0.01). In contrast, the survival rates of adult planorbids were slightly lower than that noted in the corresponding controls and the differences were not significant .
On day 30 of the experiment, the survival rates of G. truncatula in snail pairs were 89.7 per cent for juveniles, 94.6 per cent for pre-adults, and 97 per cent for adults (out of a total of 160 snails in each group at the beginning of the experiment). In the control groups, the respective percentages were 91.2 per cent, 96.2 per cent and 96.2 per cent out of 160 snails in each group (data not shown).
In pairs formed with adult or pre-adult G. truncatula, shells of dead juvenile planorbids were found during the first two weeks of experiment on epiphytic algae samples on which lymnaeids and planorbids fed (96 shells/206 dead juveniles: 46.6 per cent) or in close proximity (53/206: 25.7 per cent).
Number of Anisus spirorbis at the 30th day of experiment in pairs formed by A. spirorbis + Galba truncatula (40 + 40 snails, respectively, per life stage) and in controls (40 planorbids per life stage). The numbers noted for each pair of snails or each control group in the four experiments were reduced to an average with a standard deviation for a single experiment.
3.2.2 Reproductive activity during the experiments
Table 5 shows the numerical distribution of egg masses laid by 40 adult A. spirorbis over several periods of the experiment. In pairwise-raised planorbids, the mean number of these egg masses peaked at 38.4 between the 8th and 15th days before decreasing gradually afterwards to 15.1 masses between the 23rd and 30th days. In the control group, the same numerical variation was observed with a maximum of 41.2 egg masses between the 8th and 15th days, followed by a subsequent decrease at 34.2 masses between the 23rd and 30th days. Comparison of total egg mass counts on day 30 showed a significant difference (F = 27.41; p < 0.001).
In adult G. truncatula, the total number of egg masses was 134.8 ± 7.8 at day 30 in the pairwise-raised group and 148.4 ± 11.2 in the control group. No significant difference between the two groups of snails was observed.
Number of egg masses laid by 40 adult Anisus spirorbis in relation to different times of the experiment.
4 Discussion
4.1 Field observations
In the present study, the density of overwintering G. truncatula per square metre of habitat did not show a significant difference between the counts recorded in snail communities and control populations. The averages obtained (4.5–5.4 snails/m2) in these habitats on sedimentary soils fall within the range of values that Rondelaud et al. (2011) reported for road ditches on acidic soils. Unlike lymnaeids, the situation is different for planorbids. In control ditches, populations were abundant as shown in Table 2 and this result was consistent with observations that Welter-Schultes (2012, 2014) and Bichain et al. (2017) reported in habitats where A. spirorbis is the only species of freshwater pulmonate gastropod. In contrast, the density of planorbids showed a drastic decrease when this species was part of a community. Compared to the control populations, where the average density was 31.5 snails/m2 in 2023 and 28.7/m2 in 2024, the number of planorbids was, respectively, lower by 70 per cent and 59 per cent in habitats where the two species lived together. These data indicate that A. spirorbis is the species most affected by the presence of G. truncatula in a bispecific community and that competition between the two molluscs takes place at the expense of the planorbid. However, other investigations carried out in the Brenne RNP habitats showed that the mean number of adult O. glabra in April 2013 was slightly higher than that of adult A. spirorbis (40.6 ± 9.6 instead of 31.0 ± 8.3 snails, respectively) when both species live in the same site (Vignoles et al., 2015). According to these authors, there was no competition between these two snails in these bispecific communities of the Brenne. Several hypotheses can be proposed to explain the decrease in the number of planorbids when they live with G. truncatula in the same habitat. The first would be to consider this decrease in the abundance of planorbids as a consequence of global warming between the two survey periods (2012-2013, 2023-2024). According to Rondelaud et al. (2022) and Vignoles et al. (2022), heatwaves between these two periods resulted in a significant decrease in the number and abundance of both G. truncatula and O. glabra populations. The second hypothesis relates to the very nature of the habitat colonised by the community formed by A. spirorbis and G. truncatula or O. glabra. Indeed, the area of habitats with A. spirorbis and G. truncatula was generally less important and the vegetation present in the habitats or on their edges less abundant than in the sites occupied by the planorbid and O. glabra (Rondelaud, pers. obs.). However, a third hypothesis related to a reduction in the reproductive activity of A. spirorbis (Table 5) cannot be excluded due to the competition that exists between these snails in bispecific communities. The decrease in the number of egg masses during each generation of the planorbid would result in a gradual decline in the number of newborns and, consequently, in the abundance of the adult population.
In G. truncatula, the mean shell height did not differ significantly between snail communities and control populations. A same finding was observed for the average diameter of the shell in A. spirorbis. Two complementary hypotheses can be proposed may explain this similarity in shell dimensions in community and control snails for each specie. The first is to recognise that the density of each species in snail communities may be too low to exert a significant effect on shell dimensions. Indeed, several authors, such as Osenberg (1989) or Cross and Benke (2002) noted that in communities of freshwater gastropods, where interspecific competition occurred, the shell dimensions in the species under competition were lower than those in controls when the abundance of the competitive species became high in the habitat. The second hypothesis concerns the food resources (debris of dead plants, detritus, algae) present in the habitats, occupied by the mollusc communities studied. At these sites, the food for both molluscs would be sufficiently abundant and would thus allow normal growth in both species.
4.2 Laboratory observations
Conducting a study on competition between two freshwater snail species is a delicate operation because the density of snails in each species varies throughout the year depending on the type of habitat they colonise so that there is no ideal figure. Therefore, the number of molluscs to be placed in the presence of individuals of the other species is generally chosen (i) according to the volume of the rearing container and (ii) the similarity in feeding and the use of the same habitat (Connell, 1983; Schoener, 1983; Turner et al., 2007). The environment inside a Petri dish may differ considerably from natural conditions in the natural environment (Dillon, 2010). Despite this difficulty, such experiments can detect negative interactions between the two species, sometimes leading to the death of one of the partners (Turner et al., 2007).
On the 30th day of each experiment, the survival of A. spirorbis in snail pairs significantly decreased inversely with shell height in G. truncatula (Table 4). This decrease mainly affected juvenile planorbids and, to a lesser extent, pre-adults while adult survival was close to that observed for the same life stage in the control group. Since the competition of one animal species against another affected the survival, growth or reproduction of the individuals concerned (Byers, 2000; Dillon, 2010), the low values noted in juveniles and pre-adults of A. spirorbis are difficult to interpret, as only the survival of molluscs was considered in this study. These results cannot be explained solely by the limitation of food resources in Petri dishes because food was provided in abundance and the change of water and food, if necessary, was daily. It is therefore appropriate to incriminate the only G. truncatula to comment on the low survival of juvenile and pre-adult planorbids in pairs formed with adult lymnaeids. In our opinion, several hypotheses can be proposed to explain the mortality of juvenile and pre-adult planorbids in pairs formed with adult G. truncatula.
The first two assumptions relate to the mucus secreted by G. truncatula. The latter has been little studied by the authors, with the exception of mucopolysaccharides (Wilson, 1968; Kalbe et al., 2000; Georgieva et al., 2016). Mucus secreted by adult lymnaeids might lead to the death of juvenile and pre-adult A. spirorbis because of its ability to adhere strongly to the shells of this species so that the planorbids would be stuck in this mucus and would eventually die. But the presence of a protein-like water-soluble compound in G. truncatula mucus that would be cytotoxic to these juveniles and pre-adults cannot be ruled out. Such compounds with cytotoxic activity have already been reported in the mucus of two other Lymnaeidae: Lymnaea stagnalis and Stagnicola elodes, when these species were in the presence of trematode miracidia not compatible with these lymnaeids (Sapp and Roberts, 2000; Coyne et al., 2015). These two hypotheses are based on the presence of numerous dead shells of juvenile and pre-adult A. spirorbis observed on or around epiphytic algae samples.
The third assumption relates to the faecal pellets that adult G. truncatula deposited in the Petri dishes during the experiments. As juvenile planorbids and sometimes pre-adults have often been observed on these excreta, the toxicity of nitrogen compounds contained in these faecal pellets (Friedl, 1974; Camargo and Alonso, 2006; Liess, 2014; Hill and Griffiths, 2016), at least in the first days after excretion (Wotton and Malmqvist, 2001), might be the likely cause of mortality of these planorbids while adults of A. spirorbis would tolerate this toxicity when in the presence of adult G. truncatula. The presence of microcystins, which G. truncatula accumulate in its digestive gland when consuming toxic cyanobacteria (Zurawell et al., 2006; Gérard et al., 2009; Gérard and Lance, 2019; Ren et al., 2023), and/or that of the microbiota released in the faeces of the lymnaeid in its faecal pellets (Hu et al., 2024; McCann et al., 2023, 2024) are other factors to be taken into consideration. Excretion of these toxins and/or microbiota in the faeces of adult lymnaeids would be fatal for many juvenile and pre-adult planorbids when they ingest some of the material present in these pellets just after their deposit in the breeding dishes.
During the laboratory investigations, the planorbids raised in pairs exhibited a significant reduction in the number of egg masses, particularly between the 16th and 30th day of each experiment. Compared to the corresponding control groups, the number of egg masses laid between the 23rd and 30th day was almost twice as low. Several hypotheses can be proposed to interpret this result. In our opinion, the most valid would be to consider this decreased reproductive activity in A. spirorbis as an indirect consequence of the toxicity of microcystins when G. truncatula ingests these cyanobacteria. According to Gérard et al. (2008) and Lance et al. (2010), recurrent blooms of toxic cyanobacteria, usually during the summer and autumn in temperate regions, can result in a significant decrease in gastropod abundance and species richness. In addition, the presence of mirocystins alters the microbiota composition in the gastropods (Ren et al., 2023). If adult planorbids consume faecal material (microcystins, modified microbiota) from G. truncatula, it can he hypothesised that either of these constituents would cause a disruption in the functioning of snail's digestive gland and, consequently, in that of the nearby gonad, hence this late decline in the number of egg masses laid by planorbids during the experiments.
4.3 Synthesis
The fact that the survival of juvenile planorbids, and to a lesser extent, that of pre-adults are affected by the presence of adult G. truncatula is a surprising result. Indeed, previous studies carried out by our team have shown that this lymnaeid was previously the species most affected by competition when A. hypnorum, O. glabra or P. acuta are raised in pairs with G. truncatula under laboratory conditions (Rondelaud et al., 2005, 2016b; Dreyfuss et al., 2014). In the field, many populations of G. truncatula are generally located at the upstream extremities of a drainage network (Moens, 1991) or form colonies separated from those of physids or O. glabra when these molluscs live in the same road ditch or drainage swale (Vareille-Morel et al., 1999).
The present report complements the investigations that our team has conducted since 2010 in the Brenne RNP to study the relationships between freshwater gastropod species when they live in communities in periodically dried ditches. Several ecological and parasitological studies were carried out on bispecific or polyspecific communities of snails compared to monospecific populations through field investigations and laboratory experiments (Vignoles et al., 2015, 2022; Rondelaud et al., 2016a, 2016b; Dreyfuss et al., 2018). The results support the proposal of the following diagram to assess the intensity of competition between these five species of pulmonate snails:
P. acuta > A. hypnorum > O. glabra > G. truncatula > A. spirorbis.
The existence of this gradient in the intensity of interspecific competition can largely explain the low densities of individuals found in the 24 communities that our team studied in 2017 and 2018 in the Brenne RNP. Among the five species of pulmonate gastropods present in the habitats of these communities, the average density of overwintering A. spirorbis was 1.4 snails/m2 in March 2017 and 1.6/m2 in March 2018 (they are then in the adult stage), while that of G. truncatula was, respectively, 0.8 snails/m2 and 0.7/m2 (unpublished data).
5 Conclusions
In the present study, planorbids showed a significant decrease in their number when they lived in a community in the field while the density of G. truncatula did not vary significantly. Under laboratory conditions, this decrease mainly affected juveniles of A. spirorbis and, to a lesser extent, pre-adults when in the presence of adult G. truncatula. This interspecific competition is unlikely due to a limitation in food resources, as these were in abundance in snail habitats or in rearing dishes, but might be due to the action of mucus and/or the toxicity of excreta that adult G. truncatula secrete or deposit in their environment.
Acknowledgments
The authors gratefully thank A. Thomas for assistance in collecting and counting snails in the field. They also thank the anonymous reviewers for their valuable comments.
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Cite this article as: Rondelaud D, Vignoles P, Dreyfuss G. 2025. Interactions between Anisus spirorbis (Planorbidae) and Galba truncatula (Lymnaeidae) in snail communities on sedimentary soils. Int. J. Lim. 61, 7: https://doi.org/10.1051/limn/2025006
All Tables
The nine pairs of Anisus spirorbis + Galba truncatula and control groups used in laboratory studies. *, Eight Petri dishes for each pair of snails and four for each control group. The figures in this table represent a single experiment.
Number of snails per square metre of habitat in 15 ditches colonised by a community with Anisus spirorbis and Galba truncatula, or a control population in mid-April 2023 and 2024.
Adult shell dimensions in Anisus spirorbis and Galba truncatula in 15 ditches colonised by a community with both species, or a control population in mid-April 2023 and 2024. Parameter measured in adults: shell diameter in mm (A. spirorbis), shell height in mm (G. truncatula).
Number of Anisus spirorbis at the 30th day of experiment in pairs formed by A. spirorbis + Galba truncatula (40 + 40 snails, respectively, per life stage) and in controls (40 planorbids per life stage). The numbers noted for each pair of snails or each control group in the four experiments were reduced to an average with a standard deviation for a single experiment.
Number of egg masses laid by 40 adult Anisus spirorbis in relation to different times of the experiment.
All Figures
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Fig. 1 Geographical location of the Indre department in central France (right map) and the municipalities (in green) on which the 15 snail habitats are located (left map). |
| In the text | |
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