Data comparison

When the results and conclusions of the studies used in this literature review were collated, several issues became apparent which made comparisons more difficult and potentially distorted. The first was that the terminology used often differed between papers and was usually not well-defined. The definitions of the habitats are a prime example of this. Most studies did not define what was meant by each habitat type, and, as such, it was not possible to tell whether 2 studies were using the same parameters to differentiate between habitat types, even if they used the same terminology. Additionally, some studies combined habitat types (such as grouping rivers and brooks together) while others kept them as separate habitats. As pointed out by De Roeck et al. (Reference De Roeck, Van Coillie, De Wulf, Soenen, Charlier, Vercruysse, Hantson, Ducheyne and Hendrickx2014) ‘The [small water body] type definitions are not unequivocal in the literature’.

Sometimes it is also difficult to determine where a particular habitat ends, as they are often connected. Peters (Reference Peters1938) discussed how one of the roadside ditches investigated was ‘not merely a ditch to drain the road but was a running stream’. This is especially true when the same water system is sampled at multiple sites, such as the same river or lake, while changes in the water table or recent rainfall could move habitats between types depending on when they were sampled. For this review, different sampling sites were treated as different habitats and so each was counted.

Another potential issue is misidentification. The identification of Galba species and the taxonomic relationships of Lymnaeid snails has historically been based on species morphology. However, many of these species are extremely morphologically similar, which makes misidentification a possibility. Bargues et al. (Reference Bargues, Artigas, Khoubbane, Flores, Glöer, Rojas-Garcia, Ashrafi, Falkner and Mas-Coma2011) revealed that a cryptic species named Lymnaea schirazensis (which has since been reclassified as Galba schirazensis) had often been confused with G. truncatula. Although there is some evidence that G. schirazensis is a potential intermediate host of F. hepatica (Celi-Erazo et al., Reference Celi-Erazo, Alda, Montenegro-Franco, Pavon, Minda-Aluisa, Calvopiña, Pointier, Hurtrez-Boussès, Cevallos, Benítez-Ortíz and Rodríguez-Hidalgo2020), at the very least successful infection is much less likely compared with G. truncatula, and thus it has likely distorted data related to the susceptibility of G. truncatula populations to infection (Bargues et al., Reference Bargues, Artigas, Khoubbane, Flores, Glöer, Rojas-Garcia, Ashrafi, Falkner and Mas-Coma2011). Misidentification of snail populations may have also distorted the geographic range of G. truncatula, especially as G. schirazensis is not the only cryptic species confused with G. truncatula. Galba neotropica (formerly Lymnaea neotropica) also has significant geographic overlap with G. truncatula (Bargues et al., Reference Bargues, Artigas, Khoubbane, Ortiz, Naquira and Mas-Coma2012), while the sub-Saharan populations of G. truncatula may be another distinct species (Mahulu et al., Reference Mahulu, Clewing, Stelbrink, Chibwana, Tumwebaze, Russell Stothard and Albrecht2019) and there are also doubts about the populations identified in Alaska and Yukon (Jabbour-Zahab et al., Reference Jabbour-Zahab, Pointier, Jourdane, Jarne, Oviedo, Bargues, Mas-Coma, Anglés, Perera, Balzan, Khallayoune and Renaud1997).

Due to these cryptic species, any study which only identified G. truncatula by morphological characteristics may have misidentified some or all the snails found during their research. However, these studies were still included in the literature review, as this study aimed to assess the overall state of assumed knowledge of the environmental preferences of G. truncatula, including the level of uncertainty surrounding these conclusions. With that said, the presence of these cryptic species does mean that any results from morphological-based studies are less reliable, especially in regions where G. truncatula is present alongside other morphologically similar lymnaeid species. The bulk of the information in this paper is from Western Europe (specifically France, Switzerland and the UK) where currently there is no record of cryptic species being misidentified as G. truncatula, though this is a risk, nonetheless. In most of the rest of this paper, results and conclusions from papers which identified G. truncatula morphologically will be compared alongside those that did do using molecular methods as if the species has been correctly identified. However, this is done with the understanding that the morphological identification may not be correct, and thus genetic identification of specimens is needed in future research to validate any findings related to the species environmental preferences. In total, 32/198 studies were confirmed to use genetic identification for every snail used during their research, while 6 only genetically identified a portion of the snails used.

Habitat preferences

All the G. truncatula habitats identified by the studies examined in this review were freshwater sources of some sort, or at least had water present for part of the year. This is not surprising given the snail's physiology. Although G. truncatula aestivation can allow the snail to survive for at least 6 months in dry conditions (Kendall, Reference Kendall1949), they will die rapidly unless appropriately sheltered from desiccation, and the egg masses they produce can dry out within 12 h (Roberts, Reference Roberts1950). However, as G. truncatula is an air breathing mollusc which must inhale air into its pulmonary cavity to respire, a suitable habitat must allow for regular access to the surface of any water body (Dreyfuss et al., Reference Dreyfuss, Vignoles, Rondelaud, Dreyfuss, Vignoles and Rondelaud2015). Furthermore, habitats will need to provide a suitable food source, with the snail's preferred natural diet being blue or green algae, which thrives on bare mud surfaces (Euzéby, Reference Euzéby1971; Dreyfuss et al., Reference Dreyfuss, Vignoles, Rondelaud, Dreyfuss, Vignoles and Rondelaud2015).

Given these requirements, it may be somewhat surprising that the habitats found across the largest number of studies were rivers, streams and ponds/pools, as shown in Fig. 2. This may imply that G. truncatula is more aquatic than previously thought, however there are a number of alternative explanations. Firstly, several studies included within this literature review were surveys of river systems (Dreyfuss et al., Reference Dreyfuss, Vareille-Morel and Rondelaud1997; Sîrbu, Reference Sîrbu2005; Pérez-Quintero, Reference Pérez-Quintero2013; Phyzhaya and Yanchurevich, Reference Phyzhaya and Yanchurevich2015; Yigezu et al., Reference Yigezu, Mandefro, Mengesha, Yewhalaw, Beyene, Ahmednur, Abdie, Kloos and Mereta2018; Abbaspour et al., Reference Abbaspour, Yaripour, Gloeer and Zamanpoore2019), and so would obviously include at least 1 river or stream habitat. Secondly, these habitats also included the banks of these watercourses, so given the snail's need for air and the common location of its food sources it seems likely that G. truncatula is found on the mud next to rivers and ponds or in the shallower water near the bank rather than in the middle of these habitats. That said, the species was also identified in a diverse range of unique habitats, such as an ‘estavelle-type outlet karst conduit-aquifer’ (Falniowski et al., Reference Falniowski, Lewarne, Rysiewska, Osikowski and Hofman2021). Though these habitats do not represent the typical water sources that G. truncatula inhabits, they nonetheless demonstrate the adaptability of the species.

Overall, habitats which were identified in more studies also tended to be counted more often on an individual basis. This indicates that similar habitats tend to be common for G. truncatula across multiple different regions. There are some differences between the 2 counts, however. In some cases, a large number of habitats were found to be inhabited by G. truncatula, but were mostly found in only a few studies. For example, Drainage Furrows were the most common habitat in the Individual Habitat count, representing 54.58% of the total habitats counted. However, 10 482 of the 10 626 Drainage Furrows recorded came from just 4 studies, all in central France (Vareille-Morel et al., Reference Vareille-Morel, Dreyfuss and Rondelaud1999; Rondelaud et al., Reference Rondelaud, Hourdin, Vignoles, Dreyfuss and Cabaret2011; Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2016, Reference Dreyfuss, Vignoles and Rondelaud2018a).

These regional differences in habitat preferences may be due to different land management causing different habitats to be available, rather than actual regional differences in snail preference. For example, Herzon and Helenius (Reference Herzon and Helenius2008) report that open drainage systems are more commonly found in the Netherlands, Poland and Finland whilst these systems have now almost all been replaced by subsurface piped systems in some countries such as Sweden. Considering the role of G. truncatula as an intermediate host for fluke parasites which infect grazing livestock, it is surprising that boggy areas of pastureland were not more commonly recorded as a habitat of G. truncatula, as the snail is often found on the surface of damp mud in waterlogged areas. However, this may be partially due to semantics as ‘Swampy/Boggy/Moist Areas’ and ‘Swampy Meadows/Wet Meadows’ may be synonymous, but were kept separate due to differences in terminology and a lack of habitat definitions as discussed in the section ‘Data Comparison’.

It is also worth noting that the most commonly recorded habitats of G. truncatula may not be the best suited for the snail, as the 2 habitat counts do not include how many snails were recorded at each habitat. As such, it is possible that some of the more common habitats were only populated by a small number of snails. These data were not collated from studies due to a large variation in defining sampling areas and how the number of snails per habitat was recorded. A few studies did compare the densities of the snail populations in different habitat types, specifically those which investigated the decline in populations in central France (Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2016, Reference Dreyfuss, Vignoles and Rondelaud2018b; Rondelaud et al., Reference Rondelaud, Vignoles and Dreyfuss2022). These studies seem to suggest that the habitats which are most frequently inhabited by G. truncatula tend to have denser populations, though it is unknown if this also applies to other regions. Occupancy can be used as a proxy for species abundance in ecological surveys, including those for which detection is imperfect (Royle et al., Reference Royle, Nichols and Kéry2005), but this presupposes that occupancy and abundance are positively and predictably related (Steenweg et al., Reference Steenweg, Hebblewhite, Whittington, Lukacs and McKelvey2018). Fuller characterization of the relationship between observed habitat patch occupancy and abundance of G. truncatula, and standardization of methods including calibration of search effort would enable fair comparison between habitats/studies and over time. It is also possible that the presence of G. truncatula within habitats is somewhat stochastic or may be driven by factors such as water movement.

Habitat selection in G. truncatula may also be driven by the presence of predator species. The terrestrial snail Zonitoides nitidus is the most well-studied predator of G. truncatula, and natural populations of Z. nitidus have prevented the formation of some experimental new colonies of G. truncatula though the rate of failure differed substantially between habitat types (Vareille-Morel et al., Reference Vareille-Morel, Rondelaud and Dreyfuss2002). This species has also been investigated as a potential control mechanism for G. truncatula, with Z. nitidus shown to eliminate or reduce G. truncatula population size within 2 years of introduction. However, new Z. nitidus populations were only sustainable in swampy meadows, and G. truncatula populations re-established within 3–8 years (Rondelaud et al., Reference Rondelaud, Vignoles, Dreyfuss and Mage2006). Using the omnivorous snail Oxychilus draparnaudi alongside Z. nitidus resulted in a more rapid elimination of G. truncatula populations (Rondelaud et al., Reference Rondelaud, Vignoles, Dreyfuss and Mage2006), and thus, introducing multiple predator species could be a more effective control mechanism.

The larva of sciomyzid flies have also been considered as a potential control method, though this has not been explored experimentally (Gormally, Reference Gormally1985, Reference Gormally1988). To fully assess whether any of these species could be used as a control method, more information is needed regarding their effectiveness and the potential impact their introduction would have on the local ecology of where they were introduced. That said, the use of predators to control mosquito populations has often been effective (Shaalan and Canyon, Reference Shaalan and Canyon2009) though less so in small, artificial habitats (Washburn, Reference Washburn1995).

Climatic preferences

As shown by Fig. 2, G. truncatula has an extensive geographic range across countries with diverse climatic conditions. The full extent of this geographic range is not certain due to misidentification (as discussed in Data Comparison). Nonetheless, the species has been genetically identified in dry climates such as the Bolivian Altiplano (Bargues et al., Reference Bargues, Angles, Coello, Artigas, Renata Funatsu, Fernando Cuervo, Buchon and Mas-Coma2021) and North Africa (Mahulu et al., Reference Mahulu, Clewing, Stelbrink, Chibwana, Tumwebaze, Russell Stothard and Albrecht2019), despite the snails need for moisture. This once again reflects the snail's adaptability and ability to colonize suitable habitats within otherwise harsh environments.

Galba truncatula can undergo aestivation in order to survive in drought conditions. While this can be an effective strategy in arid climates (Belfaiza et al., Reference Belfaiza, Moncef and Rondelaud2005), many snails die while undergoing this process, and the extent to which it is used seems to vary between populations (Goumghar et al., Reference Goumghar, Rondelaud, Dreyfuss and Benlemlih2001). It would be natural to assume that higher rates of rainfall would therefore be beneficial for G. truncatula. However, while some studies have found positive correlations between average rainfall and snail abundance (Walton and Jones, Reference Walton and Jones1926; Charlier et al., Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a, Reference Charlier, Vercruysse, Morgan, Van Dijk and Williams2014b), others have found either a negative relationship (Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2018a) or no significant correlation (Novobilský et al., Reference Novobilský, Engström, Sollenberg, Gustafsson, Morrison and Höglund2014; Roessler et al., Reference Roessler, Oehm, Knubben-Schweizer and Groll2022). These mixed results may be because the species prefers moist mud surfaces or shallow, slow-moving or still water over deep, fast-flowing watercourses (Peters, Reference Peters1938; Heppleston, Reference Heppleston1972; Rondelaud et al., Reference Rondelaud, Hourdin, Vignoles and Dreyfuss2009; Knubben-Schweizer and Torgerson, Reference Knubben-Schweizer and Torgerson2015; Olkeba et al., Reference Olkeba, Boets, Mereta, Yeshigeta, Akessa, Ambelu and Goethals2020; Jones et al., Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a). As such, too much rainfall could be detrimental to the snails as it could result in too much water being present and/or the water flowing too quickly. This is supported by some studies which have found that G. truncatula habitats are less common in areas with both extremely low or high monthly rainfall (De Kock et al., Reference De Kock, Wolmarans and Bornman2003), and that the snails are less abundant at times of the year with the lowest and highest rainfall (Relf et al., Reference Relf, Good, Hanrahan, McCarthy, Forbes and deWaal2011; Iglesias-Piñeiro et al., Reference Iglesias-Piñeiro, González-Warleta, Castro-Hermida, Córdoba, González-Lanza, Manga-González and Mezo2016).

In addition to rainfall levels, temperature can also have a major impact on the viability of snail populations. A recent literature review of lymnaeid life history (Dube et al., Reference Dube, Kalinda, Manyangadze, Mindu and Chimbari2023) found that temperatures between 10 and 25°C are generally accepted as optimal for G. truncatula fecundity and growth. The findings of this present review are broadly in agreement with this assessment. A minimum temperature of 10°C for at least part of the year is widely accepted as the minimum temperature for a viable G. truncatula population as this is the lowest temperature at which the snails produce egg masses (Roberts, Reference Roberts1950; Heppleston, Reference Heppleston1972; Valero et al., Reference Valero, Marti, Marcos, Robles and Mas-Coma1998; Charlier et al., Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a; Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2018a). Older laboratory experiments have found that G. truncatula can remain active at temperatures as low as 1.5°C (Kendall, Reference Kendall1953), however below 5°C their level of activity (including eating) is severely decreased and this exposure also reduced the number of eggs the adults produce once they are returned to room temperature (Hodasi, Reference Hodasi1976). Curiously, this second study also found that juvenile snails exposed to cold temperatures tended to rapidly consume food and experience faster growth post-exposure, resulting in snails that were slightly larger than the control group and produced more eggs. This could indicate that in climates with cold winters, reproduction in the spring is disproportionately driven by overwintering juveniles, although it is not clear whether seasonal exposure to low temperatures increases overall population growth rates.

Overall, though, most research indicates that temperatures below 10°C are suboptimal at best for G. truncatula. The impact of higher temperatures, however, is much less certain, as is the optimum temperature for the snail within its tolerance limits. Laboratory tests in the 1950s showed conflicting results, with some data showing that growth rates increased at 25°C compared to 17°C (Roberts, Reference Roberts1950) and other data indicating that 17–21°C is optimal and temperatures above 25°C are detrimental (Kendall, Reference Kendall1953). More modern laboratory studies focused on temperature were found during this review, but they examined the impact on trematode infection and growth in the snail rather than the life history of the snails themselves (Rondelaud et al., Reference Rondelaud, Titi, Vignoles, Mekroud and Dreyfuss2013; Vingnoles et al., Reference Vignoles, Titi, Rondelaud, Mekroud and Dreyfuss2014; Titi et al., Reference Titi, Rondelaud, Mekroud, Vignoles and Dreyfuss2014). As such, these studies were not included in the summary statistics.

Data from field studies are also unclear, partially due to the impact of confounding factors. For instance, most longitudinal studies show that G. truncatula abundance does not peak during the hottest months of the year. In some cases, a summer generation occurs shortly before (Charlier et al., Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a) or after (Relf et al., Reference Relf, Good, Hanrahan, McCarthy, Forbes and deWaal2011) the annual peak in temperature, while in other cases no population increase occurs during summer (Mekroud et al., Reference Mekroud, Benakha, Benlatreche, Rondelaud and Dreyfuss2002; Villavicencio et al., Reference Villavicencio, Gorochov and Vasconcellos2006; Iglesias-Piñeiro et al., Reference Iglesias-Piñeiro, González-Warleta, Castro-Hermida, Córdoba, González-Lanza, Manga-González and Mezo2016). However, the temperatures in which these population peaks occur also differ between studies. In Algeria, the highest snail abundance occurred when mean monthly temperatures reached around 20°C (Mekroud et al., Reference Mekroud, Benakha, Benlatreche, Rondelaud and Dreyfuss2002), while in Ireland the hottest period still had low snail abundance despite only reaching 15–17°C (Relf et al., Reference Relf, Good, Hanrahan, McCarthy, Forbes and deWaal2011). Temperature alone is clearly not the core driver of lower population abundance during the hottest parts of the year. Likely it is also due to the increased chance of desiccation due to lower rainfall levels and increased speed of drying out at higher temperatures.

Comparisons of the mean annual temperature of different habitats also have contradictory results. In central France, G. truncatula presence was found to have a positive correlation with temperature (Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2018a), while in South Africa it had a negative correlation (De Kock et al., Reference De Kock, Wolmarans and Bornman2003). However, the mean annual temperatures recorded in central France (<9.5 to ⩾11.5°C) straddled the border of the lowest 2 categories temperature categories in South Africa (5–10 and 10–15°C). As such, it is possible that the optimum annual temperature for G. truncatula lies around 11–12°C, but it seems more likely that the difference in correlation is due to other factors such as rainfall, habitat availability or soil type.

This could also reflect the preferences of 2 different species, given the uncertainty of G. truncatula in Sub-Saharan Africa (Mahulu et al., Reference Mahulu, Clewing, Stelbrink, Chibwana, Tumwebaze, Russell Stothard and Albrecht2019). The discrepancies in temperature preferences between different populations of snails could also be due to the snails adapting to local temperature conditions. Prior literature does seem to suggest differences in reproductive cycles and growth in lymnaeid species adapted to different climates (Dube et al., Reference Dube, Kalinda, Manyangadze, Mindu and Chimbari2023). However, no studies were found which directly compared the temperature tolerances of G. truncatula populations from different climates in lab or field observations during the searches for the present review. As such, it is unclear whether any adaptation to different climates is due to evolution or the innate ability of plasticity of the species to upregulate metabolic pathways for thermoregulation.

Temperature can also be significantly altered by local conditions, and so macroclimatic temperature measurements may not be the most accurate indicator of snail presence. Indeed, temperature readings taken closer to the soil may be a more accurate predictor of snail presence, while soil moisture and the presence of plants can also change the intensity of temperature fluctuations (Smith and Wilson, Reference Smith and Wilson1980; Roessler et al., Reference Roessler, Oehm, Knubben-Schweizer and Groll2022). Furthermore, water temperature may differ significantly from air temperature, which could help shelter G. truncatula from temperature extremes. In the Bolivian altiplano, the average air temperature stays below 10°C for most of the year, while water temperatures mostly stay above this minimum threshold (Bargues et al., Reference Bargues, Angles, Coello, Artigas, Renata Funatsu, Fernando Cuervo, Buchon and Mas-Coma2021). Water and shade may also create microclimates that shelter G. truncatula from high temperature extremes (Khallaayoune and El Hari, Reference Khallaayoune and El Hari1991), though without water temperature measurements this is less certain. Some longitudinal studies also found that G. truncatula abundance is correlated with periods of increased water temperature (Chlyeh et al., Reference Chlyeh, Dodet, Delay, Khallaayoune and Jarne2006; Rondelaud et al., Reference Rondelaud, Hourdin, Vignoles and Dreyfuss2009; Şahin and Zeybek, Reference Şahin and Zeybek2020), though Olkeba et al. (Reference Olkeba, Boets, Mereta, Yeshigeta, Akessa, Ambelu and Goethals2020) found that water temperature was significantly negatively correlated with G. truncatula presence.

Climatic conditions change with altitude, but it is unclear whether this impacts the snail, and outcomes may vary depending on the region. Most studies which focused on altitude in Europe (and 1 in Morocco) found that altitude had little to no impact on the presence of the snail (Walton, Reference Walton1918; Sturm, Reference Sturm2007, Reference Sturm2012; Georgiev and Hubenov, Reference Georgiev and Hubenov2013; Anistratenko et al., Reference Anistratenko, Furyk, Anistratenko, Degtyarenko and Anistratenko2019; Roessler et al., Reference Roessler, Oehm, Knubben-Schweizer and Groll2022). A few studies indicated that altitude may negatively impact the snail, though this may be due to other factors such as higher predation rates or a higher abundance of peatland (Rondelaud and Mage, Reference Rondelaud and Mage1990; Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2018a). In South America and sub-Saharan Africa, however, several studies identified that G. truncatula tends to be found at higher altitudes compared with other lymnaeid species (Walker et al., Reference Walker, Makundi, Namuba, Kassuku, Keyyu, Hoey, Prödohl, Stothard and Trudgett2008; Pointier et al., Reference Pointier, Noya, de Noya and Théron2009; Howell et al., Reference Howell, Mugisha, Davies, Lacourse, Claridge, Williams, Kelly-Hope, Betson, Kabatereine and Stothard2012; Malatji et al., Reference Malatji, Pfukenyi and Mukaratirwa2020; Pereira et al., Reference Pereira, Uribe and Pointier2020; Bardales-Valdivia et al., Reference Bardales-Valdivia, Bargues, Hoban-Vergara, Bardales-Bardales, Goicochea-Portal, Bazán-Zurita, Del Valle-Mendoza, Ortiz and Mas-Coma2021).

This could indicate that in tropical regions, the temperatures at lower altitudes are too high for G. truncatula, but the moderating effect of altitude on temperature allows the snail to thrive. Indeed, the species has been found at lower altitudes in Chile compared to Bolivia, which is closer to the equator (Artigas et al., Reference Artigas, Bargues, Mera y Sierra, Agramunt and Mas-Coma2011). In South Africa, De Kock et al. (Reference De Kock, Wolmarans and Bornman2003) found G. truncatula across a wide range of altitudes. However, altitude also had a significant impact on the presence of the snail, as 81.6% of collections were between 1000 and 2500 m. Strangely, the lowest altitude areas (0–1000 m) tended to have fewer habitats, but a larger number of snails collected compared with the highest altitude areas (2000–3000 m) in which the trend was reversed. This somewhat mixed result could be a result of South Africa's subtropical to temperate climate.

The varied climatic conditions of different populations of G. truncatula also reflect how the species will respond to climate change in different regions. In central France, the species has declined in recent years due to a series of heatwaves (Rondelaud et al., Reference Rondelaud, Vignoles and Dreyfuss2022; Vignoles et al., Reference Vignoles, Dreyfuss and Rondelaud2022), while in Bolivia warmer temperatures are allowing G. truncatula to colonize areas which were previously too cold (Bargues et al., Reference Bargues, Artigas, Angles, Osca, Duran, Buchon, Gonzales-Pomar, Pinto-Mendieta and Mas-Coma2020). In the UK, temperatures are staying above 10°C for a larger portion of the year, which is predicted to increase fascioliasis prevalence in livestock (Fox et al., Reference Fox, White, McClean, Marion, Evans and Hutchings2011). The impact of warmer weather can also depend on the time of year and have a mixed impact. Heppleston (Reference Heppleston1972) observed that a mild autumn allowed for an additional generation of snails, but this resulted in the premature deaths of many juvenile snails instead of overwintering, while in summer both G. truncatula growth and mortality rates increased with higher temperatures.

As climate change makes weather patterns more unpredictable, the observed effects of climate anomalies on snail populations will doubtless depend on what the key limiting factors are in different seasons and locations. When trying to predict the impacts of these weather patterns, it is important to consider the likely curvilinear relationships of G. truncatula presence and behaviour with both rainfall and temperature. As increased rainfall and temperature could easily have both a positive and negative impact on snail populations, simple correlations and linear regression, whether univariate or multivariate, might therefore be poorly suited to characterize non-monotonic temperature–abundance relationships.

Physio-chemical properties of habitats

The impact of differences in the physio-chemical properties of G. truncatula habitats on snail presence and abundance has been widely noted but mechanisms are poorly understood. The most widely reported physio-chemical property from G. truncatula habitats was water pH. The minimum and maximum pH values recorded demonstrate that G. truncatula can tolerate a wide water pH range, while the range of means (6.35–7.8) could indicate that optimum pH range is close to neutral (see Fig. 6). This aligns with research from Europe and South America (Walton and Wright, Reference Walton and Wright1926; Euzéby, Reference Euzéby1971; Bargues et al., Reference Bargues, Angles, Coello, Artigas, Renata Funatsu, Fernando Cuervo, Buchon and Mas-Coma2021), but this is far from certain given the proportion of studies which identified positive or negative associations between pH and the presence of the snail. Assessing pH preferences is also made more complicated due to potential confounding factors. For example, 1 study found G. truncatula in waters below pH 7.4, but lower pH waters in this area were polluted (Pérez-Quintero, Reference Pérez-Quintero2011), while a study in Wales suggested that the negative correlation between G. truncatula and pH could be due to more acidic soils tending to be in higher rainfall areas (Jones et al., Reference Jones, Davis, Jones, Tyson, Davies, Cutress, Brophy, Rose, Williams and Williams2021). Furthermore, Moens (Reference Moens1981) identified G. truncatula in habitats with water pH ranging from 5.4 to 8.7 but found the pH level closely aligned with that of the soil in the general region where the habitat was located. This indicates that habitat pH may have little impact on G. truncatula presence so long as the pH is within the species' tolerance limits. Only a single study was identified during this review that measured the soil pH of G. truncatula habitats (Charlier et al., Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a), which found a positive correlation between soil pH and snail abundance, though another study, found after the study searches were completed, found G. truncatula at habitats with soils ranging in pH from 4.5 to 6 (Bishop, Reference Bishop1981). This lack of data warrants further investigation into the relationship between soil pH and G. truncatula presence.

Regarding soil conditions, several papers noted that G. truncatula avoids areas of peatland (Walton, Reference Walton1918; Peters, Reference Peters1938; Heppleston, Reference Heppleston1972; Moens, Reference Moens1981; Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2018a), while only a single paper identified during the review found G. truncatula on ‘peaty soils’ (Gaasenbeek et al., Reference Gaasenbeek, Over, Noorman and De Leeuw1992). It was initially suggested that the assumed avoidance of peatland in G. truncatula was because the acid conditions would be detrimental to shell construction (Walton, Reference Walton1918; Peters, Reference Peters1938). Lower pH conditions have been found to be detrimental to shell construction in marine gastropods (Duquette et al., Reference Duquette, McClintock, Amsler, Pérez-Huerta, Milazzo and Hall-Spencer2017) and decreased abundance in terrestrial snails (Johannessen and Solhøy, Reference Johannessen and Solhøy2001), and the pH can reach as low as 3.8 in some North American peat bogs (Schwintzer and Tomberlin, Reference Schwintzer and Tomberlin1982; Craft, Reference Craft and Craft2022). As such, it is possible that acidic conditions could be one of the reasons for avoidance, particularly in more acidic peatland.

However, the acidity of peatland varies greatly depending on access to groundwater and local minerotrophic conditions, and some areas of peatland can be roughly neutral (Craft, Reference Craft and Craft2022), with these variations potentially impacting suitability for G. truncatula inhabitation. For example, a recent study of rich fen peatlands in Finland found G. truncatula in 15/19 investigated sites, where water pH was 5.8 on average (Bocharnikova, Reference Bocharnikova2024). Fens, which are fed by mineral-rich groundwater and tend to have a higher pH compared to peat bogs which are mainly fed by rainwater, may therefore be a more suitable habitat for G. truncatula. Nevertheless, G. truncatula snails were inconsistently detected by Bishop (Reference Bishop1981) in East Anglian fens, with G. truncatula snails found in fens with a soil pH of 4.5, but not in others where soil pH was as high as 7.6. As such, pH is unlikely to be the sole reason for the avoidance of peatland given the snail's wide pH tolerance.

An alternative hypothesis suggests that the avoidance of peatland may be due to a lack of food caused by an absence of suitable conditions for algal growth (Heppleston, Reference Heppleston1972). Galba truncatula has reportedly rapidly infested peatland following the application of fertilizer, possibly due to increased unicellular algal growth (Comerton and Houghton, Reference Comerton and Houghton1975), though both cyanobacteria and chlorophyceae have been identified on peatland (Hamard et al., Reference Hamard, Céréghino, Barret, Sytiuk, Lara, Dorrepaal, Kardol, Küttim, Lamentowicz, Leflaive and Le Roux2021). Whether the species present in these habitats are not favoured by G. truncatula or if the algae are not found in sufficient quantities to sustain the snail has not been investigated by any study found during this present review.

The reasons for the apparent aversion to peatland found in G. truncatula, and to what extent the snails are averse, needs further investigation. If peaty soils reduce G. truncatula numbers and fluke infection, this could act as an incentive for farmers to restore and preserve peatland habitats on their pastures. If G. truncatula are averse to peatlands or indeed to general acidic conditions, research would also be needed to establish if other snail species can inhabit these habitats and act as an intermediate host for fluke parasites as has been hypothesized by Relf et al. (Reference Relf, Good, McCarthy and de Waal2009).

The physical properties of the soil may also influence the snail's presence. Several studies have indicated that clay soils are preferred by G. truncatula (Walton, Reference Walton1918; Charlier et al., Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a; Dmitrović et al., Reference Dmitrović, Savić and Pešić2016; Vignoles et al., Reference Vignoles, Dreyfuss and Rondelaud2022). This may be because clay is easier to burrow into compared with other soils (Vignoles et al., Reference Vignoles, Dreyfuss and Rondelaud2022), as snails have also been found significantly more frequently in habitats with muddy substrata than those that were sandy or stony (De Kock et al., Reference De Kock, Wolmarans and Bornman2003). Clay soils may also allow for suitable water source habitats to form more easily, as their low hydraulic conductivity causes them to expand and water to form pools rather than easily draining away (Yu et al., Reference Yu, Loureiro, Cheng, Jones, Wang, Chia and Faillace1993; Turtola and Paajanen, Reference Turtola and Paajanen1995). Some studies have found that soils with poor drainage more broadly are positively associated with G. truncatula presence, rather than specifically those with a high clay content (Moens, Reference Moens1981; Wright and Swire, Reference Wright and Swire1984). Additionally, 1 study found that the snail was more common in loamy soils compared to clay soils (Charlier et al., Reference Charlier, Bennema, Caron, Counotte, Ducheyne, Hendrickx and Vercruysse2011), though the reasons for this are unclear.

Roessler et al. (Reference Roessler, Oehm, Knubben-Schweizer and Groll2022) also found a negative correlation between G. trunctula presence and soil depth (defined as the depth that plant roots can penetrate). This was hypothesized to be due to soil horizons formed from dense particles at a shallow depth preventing root penetration and resulting in poor drainage. Soils with high organic content may also be unfavourable for the snails, as less snail eDNA has been found in darker soils (Jones et al., Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a) and G. truncatula was found to be significantly less abundant in soils made up of decaying plant matter (De Kock et al., Reference De Kock, Wolmarans and Bornman2003). Overall, most evidence suggests poorly draining soils are beneficial for G. truncatula, but more research is needed to determine whether the snail favours specific soil types.

Salinity and conductivity may also influence the presence of G. truncatula, but the impact of these factors is not well studied and varies between studies. Conductivity was positively associated with G. truncatula presence in Austrian lakes and the Normandy Coast (Costil et al., Reference Costil, Dussart and Daguzan2001; Sturm, Reference Sturm2007), whilst the snail was only found in saline-alkali environments in Northeastern China (Wu et al., Reference Wu, Guan, Ma, Xue, Yang and Batzer2019). However, in Uganda the species had a significant negative correlation with both salinity and conductivity (Howell et al., Reference Howell, Mugisha, Davies, Lacourse, Claridge, Williams, Kelly-Hope, Betson, Kabatereine and Stothard2012), and in South Africa the species was significantly more likely to be found in freshwater than brackish water (De Kock et al., Reference De Kock, Wolmarans and Bornman2003). Research into the impact of concentration of different minerals in the water on G. truncatula is also limited. In the First River in Turkey, Calcium was found to have a positive correlation with G. truncatula abundance, and was the only mineral studied to have a significant impact on the species' abundance (Şahin and Zeybek, Reference Şahin and Zeybek2020). However, in the rift valley of Ethiopia, the occurrence of G. truncatula was positively linked with calcium concentration and negatively linked with magnesium concentration, but the minerals had the opposite impact on the snail's abundance (while nitrate was also shown to positively impact abundance) (Olkeba et al., Reference Olkeba, Boets, Mereta, Yeshigeta, Akessa, Ambelu and Goethals2020). It is not clear why this is the case, nor why the effects differ between the 2 studies. Overall, more research is needed to clarify the impact of these minerals on snail populations. While farmers may only have a limited ability to change the chemistry of the water on their land, understanding how water chemistry influences the snail will allow for more accurate risk assessments and for planning parasite control measures.

Habitat permanence, population structure and movement

Some evidence suggests that permanent habitats may be better suited for G. truncatula, as populations in temporary habitats are found less often (Moens, Reference Moens1981; De Kock et al., Reference De Kock, Wolmarans and Bornman2003) and tend to have fewer annual generations (Bargues et al., Reference Bargues, Angles, Coello, Artigas, Renata Funatsu, Fernando Cuervo, Buchon and Mas-Coma2021). Furthermore, Heppleston (Reference Heppleston1972) found that populations in permanent habitats have larger populations despite increased mortality, which could indicate that these populations can ‘afford’ more losses due to more optimal conditions. Higher concentrations of snail eDNA have been found in temporary habitats, though this may be due to evaporation concentrating the eDNA rather than an indication of more snails being present (Jones et al., Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a).

These suboptimal conditions may be due to the habitats being without moisture for prolonged periods of time, which may cause crashes in the population. In fact, permanent habitats may sometimes act as a reservoir for temporary populations. This was hypothesized to be the case in the Doukkala district of Morocco, in which there were high rates of fascioliasis in livestock despite very few snails being found (Belfaiza et al., Reference Belfaiza, Moncef and Rondelaud2005). It was thought the irrigation cycles might allow snails from a breeding population near a dam to spread through the area, expanding colonized habitats and parasite transmission. These possible cycles of population crashes are reflected in some results which found lower genetic diversity, allelic richness and effective population sizes in temporary populations, which is likely the result of more frequent genetic bottlenecks (Trouvé et al., Reference Trouvé, Degen, Renaud and Goudet2003, Reference Trouvé, Degen and Goudet2005). That said, other studies have also found a similar level of genetic diversity in populations from temporary or permanent habitats, suggesting no significant difference in the frequency of bottlenecks or population extinction events (Chapuis et al., Reference Chapuis, Trouvé, Facon, Degen and Goudet2007). The same study also found that individuals from temporary habitats mature later and are less fecund (Chapuis et al., Reference Chapuis, Trouvé, Facon, Degen and Goudet2007), which is likely because larger individuals are less susceptible to drought conditions in temporary habitats, while size had no impact on this trait in permanent habitats (Chapuis and Ferdy, Reference Chapuis and Ferdy2012).

Heppleston (Reference Heppleston1972) also observed that snails in temporary habitats exhibited a greater degree of dispersal than those from permanent habitats, though overall the snail was ‘relatively sedentary’, despite earlier laboratory tests indicating the species can move around 33 cm h⁻¹. This limited movement is also supported by population genetics which indicate very limited migration between subpopulations (Trouvré et al., Reference Trouvé, Degen and Goudet2005; Correa et al., Reference Correa, De Meeûs, Dreyfuss, Rondelaud and Hurtrez-Boussès2017). However, some field evidence shows G. truncatula can move over 100 m per month downstream (Rondelaud, Reference Rondelaud1983), or 10 m per 2 weeks upstream under favourable conditions (Rondelaud et al., Reference Rondelaud, Hourdin, Vignoles and Dreyfuss2005). This suggests that G. truncatula can move substantial distances, but only do so under certain circumstances such as when exposed to a lack of resources. However, the circumstances which cause the species to move are also poorly understood, so more research would be needed to test this hypothesis.

Questions also remain regarding the potential for G. truncatula to be transported by animals either locally or across vast geographical areas. Juhász and Majoros (Reference Juhász and Majoros2023) found that wild boars transported G. truncatula from wallowing sites on their coat whilst it has been hypothesized that Equids and Llamas may carry and transport the snail on their feet (Mas-Coma et al., Reference Bargues, Artigas, Angles, Osca, Duran, Buchon, Gonzales-Pomar, Pinto-Mendieta and Mas-Coma2020, Reference Mas-Coma, Cafrune, Funatsu, Mangold, Angles, Buchon, Fantozzi, Artigas, Valero and Bargues2021; Mera Y Sierra et al., Reference Mera Y Sierra, Neira, Bargues, Cuervo, Artigas, Logarzo, Cortiñas, Ibaceta, Lopez Garrido, Bisutti and Mas-Coma2020). As such, it is also feasible that livestock may transport the snail on their hooves, which could be an important means for G. truncatula to colonize temporary habitats on pastureland, however, no evidence of such a phenomenon was found in the literature. The ability of G. truncatula to undergo aestivation in dry mud may also allow long distance transport on the feet of livestock, with Mas-Coma et al. (Reference Mas-Coma, Valero and Bargues2009) hypothesizing that it was by this means that G. truncatula initially arrived in South America as cattle were imported to the continent from Europe from the 1400s onwards. It has also been suggested that birds can aerially distribute G. truncatula over thousands of kilometres and allow the snail to colonize remote areas such as mountains and islands, with the global distribution of G. truncatula sharing similarities with major migratory flightpaths of wetland birds (van Leeuwen, Reference van Leeuwen2012). The mode of such transport is unclear though, with transport attached to the feet or feathers most likely, although some molluscs are capable of surviving passage through the avian digestive tract (van Leeuwen, Reference van Leeuwen2012).

Snails may also be dispersed by flowing water along waterways. Hurtrez-Boussès et al. (Reference Hurtrez-Boussès, Hurtrez, Turpin, Durand, Durand, De Meeüs, Meunier and Renaud2010) found that genetic differentiation of snail populations increases with hydrographic distance along the streams, and the genetic variance between populations is lower than expected if the populations were connected by direct water flow. This could be an important consideration for combatting the spread of G. truncatula and fluke infection.

The influence of flooding on the spread of the G. truncatula is unclear. Although flooding could spread the snail a considerable distance from permanent habitats (Walton, Reference Walton1918), some researchers suggest that most of the habitats the snails are placed in are likely to be unsuitable (Peters, Reference Peters1938), and that flooding is unlikely to be the main contributor of snail dispersal into new regions (Heppleston, Reference Heppleston1972). However, flooding may also transport some G. truncatula into new suitable habitats where they can rapidly establish new colonies (Skuce et al., Reference Skuce, Van Dijk, Smith and Morgan2014). This may be especially true in the period immediately after flooding, following the creation of many temporary habitats on pastureland away from the snails' typical habitats. These temporary habitats may also last for several weeks if the pasture has poor drainage or if rainfall continues after the flooding subsides. As such, while the heavy rainfall that results in flooding could be detrimental to the snails in permanent habitats (as discussed above in ‘Climatic Preferences’), it may also allow for either the temporary or permanent expansion of the snail's range, and thus the spread of trematode infections.

There is limited research focused on the vertical movement of the snail. Research focused on a population downstream of a dam found that snails mostly followed seasonal variation of water levels, but more rarely followed daily fluctuations. However, some individuals did retreat to emerged ground when water levels rapidly increased (Hourdin et al., Reference Hourdin, Vignoles, Dreyfuss and Rondelaud2006). Preference for water depth may differ between populations, with snails from marshlands appearing to be more amphibious than those from populations in irrigation and road ditches, while infection by F. hepatica resulted in a preference for deeper water (Moukrim and Rondelaud, Reference Moukrim and Rondelaud1992). Overall, how G. truncatula moves in response to changes in water depth is poorly understood.

Radiation, shade and habitat flora

There is some evidence that high levels of shade may be detrimental for G. truncatula, although it is unclear whether some shade is beneficial. Most studies suggest that bare mud surfaces are preferential for G. truncatula, as these are good conditions for the unicellular algae on which the snail feeds (Kendall, Reference Kendall1953; Heppleston, Reference Heppleston1972). However, evidence from Spain found that G. truncatula is positively associated with daily global radiation up to 18 000 kJ (10 kJ m⁻² day⁻¹), but then declines (Iglesias-Piñeiro et al., Reference Iglesias-Piñeiro, González-Warleta, Castro-Hermida, Córdoba, González-Lanza, Manga-González and Mezo2016). This may suggest that some shade is beneficial, which aligns with findings which showed G. truncatula presence is significantly less likely for habitats located within forests but significantly more likely if they are near to forests (Roessler et al., Reference Roessler, Oehm, Knubben-Schweizer and Groll2022). Furthermore, a lack of vegetation along riverbanks was hypothesized to be the reason for smaller riverbank populations of G. truncatula compared to marshland populations (Dreyfuss et al., Reference Dreyfuss, Vareille-Morel and Rondelaud1997), while De Kock et al. (Reference De Kock, Wolmarans and Bornman2003) also found that aquatic vegetation was present at 91.6% of G. truncatula habitats (though it was only calculated to have a small impact on the likelihood of the snail's presence).

However, Jones et al. (Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a) found that while there was significantly lower levels of G. truncatula eDNA in fully shaded habitats, no significant difference was found between partially shaded and unshaded habitats, which indicates the benefits of partial shade may be more situational. This study also highlighted that farmers in many parts of the world are being encouraged to plant trees for environmental purposes. As such, understanding whether the shade provided by canopy vegetation is beneficial or detrimental to the snail could be important for farmers to strategically place trees to interrupt fluke transmission and prevent livestock infection. Careful siting of trees could also increase hydraulic connectivity and reduce soil saturation in areas of pasture acting as foci of snail populations.

Plants are also sometimes used to identify potential habitats of G. truncatula, although studies differ as to whether specific plants are associated with the presence of the snail or not. For example, rushes (family Juncaceae) have been associated with the presence of G. truncatula in a number of studies (Rondelaud et al., Reference Rondelaud, Hourdin, Vignoles, Dreyfuss and Cabaret2011; Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2018a; Jones et al., Reference Jones, Davis, Jones, Tyson, Davies, Cutress, Brophy, Rose, Williams and Williams2021, Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a), but Charlier et al. (Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a) found no significant correlation between the presence of rushes and G. truncatula. This study also found a negative correlation between the presence of G. truncatula and reeds, but a more recent study found a positive correlation (Roessler et al., Reference Roessler, Oehm, Knubben-Schweizer and Groll2022). Buttercups (genus Ranunculus) are another potential indicator, as they were commonly found at G. truncatula habitats by Charlier et al. (Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a) and Roberts, (Reference Roberts1950). It seems likely that botanical indicators of G. truncatula presence may vary substantially geographically and between habitat types.

Three of the studies in this review identified the presence of G. truncatula in watercress beds (Rondelaud and Mage, Reference Rondelaud and Mage1990; Rondelaud et al., Reference Rondelaud, Hourdin, Vignoles and Dreyfuss2005, Reference Rondelaud, Vignoles, Dreyfuss and Mage2006). Though this indicates this is an uncommon habitat of the snail, it is troubling as Nasturtium officinale (common watercress) is the main cause of human infection by F. hepatica in Western Europe (Rondelaud et al., Reference Rondelaud, Hourdin, Vignoles and Dreyfuss2005). As such, it is important that the crop is carefully monitored for the snail, and water supply regulated especially to avoid ingress of fluke eggs.

Snails from different habitats may also be adapted to consume different types of plant matter and algae based on the availability in their environment. Vignoles et al. (Reference Vignoles, Rondelaud and Dreyfuss2011) reared snails from a riverbank population on conditions optimal for those from meadows but found no significant increase in snail size compared with those in the wild habitats. It was suggested that the decaying leaves used as feed in meadows may not make up a large part of the river snails' diet, and that they might therefore have developed different food preferences. A recent metagenomic study of the gut microbiome of snails from 2 farms revealed significantly different beta diversity, which indicates that the microbiome may be adapted to different conditions (McCann et al., Reference McCann, McFarland, Megaw, Siu-Ting, Cantacessi, Rinaldi and Gobert2024). This could possibly be due to differences in the snail's diet, however the diet of these 2 populations is not known. Metagenomic studies of the gut contents of snail intermediate hosts are rare, and no genetic studies of G. truncatula diet were found during this review.

The impact of human activity

The creation and destruction of snail habitats are perhaps the most direct impacts that humans can have on the presence or abundance of G. truncatula. However, whether a certain human activity is beneficial or detrimental to the snail seems to be very situational. Artificial watercourses such as drainage ditches, drainage furrows and irrigation canals are among the most abundant habitats of G. truncatula across many different studies (Rondelaud et al., Reference Rondelaud, Hourdin, Vignoles, Dreyfuss and Cabaret2011; Charlier et al., Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a, Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2016, Reference Dreyfuss, Vignoles and Rondelaud2018a, Reference Dreyfuss, Vignoles and Rondelaud2018b; Vignoles et al., Reference Vignoles, Dreyfuss and Rondelaud2022; Jones et al., Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a). This may be because these artificial watercourses are similar to natural habitats such as streams and rivers, and thus the creation of these habitats may allow for the presence of the snail. However, in many cases these artificial habitats are part of open drainage systems and draining fields can be an effective way to destroy G. truncatula habitats (Rees, Reference Rees1942; Dreysuss et al., Reference Dreyfuss, Vignoles and Rondelaud2016, Reference Dreyfuss, Vignoles and Rondelaud2018a, Reference Dreyfuss, Vignoles and Rondelaud2018b). Furthermore, when subsurface drainage systems malfunction, they can create new habitats through subsurface effluences which can potentially hamper efforts to combat Fascioliasis (Bargues et al., Reference Bargues, Artigas, Angles, Osca, Duran, Buchon, Gonzales-Pomar, Pinto-Mendieta and Mas-Coma2020; Jones et al., Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a). As such, open drainage systems may act as an effective habitat for G. truncatula while simultaneously limiting their spread across the field by concentrating the moist habitats in 1 area. That said, large-scale interconnected artificial waterways may also allow for G. truncatula and fascioliasis to spread, as was found by Belfaiza et al. (Reference Belfaiza, Moncef and Rondelaud2005). Regular clearing of open drainage systems could be an effective method of control, as it is one of the main reasons for habitat loss of G. truncatula in central France (Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2016, Reference Dreyfuss, Vignoles and Rondelaud2018b).

Galba truncatula can also be impacted by poaching (the mechanical disturbance of soil and vegetation in wet conditions) by vehicles or livestock. Tracks created by vehicles and livestock can fill with water and thus act as habitats for the snail (Heppleston, Reference Heppleston1972; Hörweg et al., Reference Hörweg, Prosl, Wille-Piazzai, Joachim and Sattmann2011; Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2016; Jones et al., Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a). However, excessive poaching may also be detrimental for the snail. Charlier et al. (Reference Charlier, Bennema, Caron, Counotte, Ducheyne, Hendrickx and Vercruysse2011) found no G. truncatula in humid areas near water troughs, while Dreyfuss et al. (Reference Dreyfuss, Vignoles and Rondelaud2018b) found that cattle trampling has resulted in the destruction of G. truncatula habitats near vernal pools used as a water source. It is possible that the high throughput of animal traffic in these areas results in the mechanical disturbance of snail habitats, though they are also likely to be subjected to a high degree of urine and faecal deposition, a source of pollution which will increase habitat microbial load (O'Callaghan et al., Reference O'Callaghan, Kelly-Quinn, Jennings, Antunes, O'Sullivan, Fenton and Huallachain2019) which is likely to be detrimental to G. truncatula. High animal or vehicle traffic may also result in the destruction of the snail itself, as Juhász and Majoros (Reference Juhász and Majoros2023) noted that while vehicles can decrease soil drainage (which can be beneficial for G. truncatula), they can also crush the snails beneath their tires.

Mechanical gyro-crushing of rushes and other vegetation near small water sources has resulted in a decline of G. truncatula habitats in central France (Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2016, Reference Dreyfuss, Vignoles and Rondelaud2018b), possibly because the deposition of crushed plant matter on the mud surface inhibits unicellular algal growth (Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2018a, Reference Dreyfuss, Vignoles and Rondelaud2018b). It is unknown if the destruction of rushes by other means such as topping would have a similar effect, though the practice is regularly promoted as a method of fluke control (COWS, 2019). Mowing has also been found to correlate negatively with the presence of G. truncatula (Charlier et al., Reference Charlier, Soenen, De Roec, Hantson, Ducheyne, Van Coillie, De Wulf, Hendrickx and Vercruysse2014a), which may be due to the intense regeneration of plants after mowing hindering the production of the unicellular algae (Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2016).

Non-agricultural infrastructure can also impact the presence of the snail. In Bolivia, road construction disrupted fascioliasis transmission loci, but allowed the snails to be transported to new areas by livestock carried on trucks (Bargues et al., Reference Bargues, Artigas, Angles, Osca, Duran, Buchon, Gonzales-Pomar, Pinto-Mendieta and Mas-Coma2020). Additionally, unpublished data by Rondelaud (reported by Hourdin et al., Reference Hourdin, Vignoles, Dreyfuss and Rondelaud2006) shows that river habitats upstream of dams tend to be numerous with high snail population densities. Several studies have also shown that while G. truncatula can tolerate low levels of pollution, the species tends to prefer areas with less anthropogenic activity (Pérez-Quintero, Reference Pérez-Quintero2011; Phyzhaya and Yanchurevich, Reference Phyzhaya and Yanchurevich2015; Bargues et al., Reference Bargues, Angles, Coello, Artigas, Renata Funatsu, Fernando Cuervo, Buchon and Mas-Coma2021). However, this may depend on the activity as Olkeba et al. (Reference Olkeba, Boets, Mereta, Yeshigeta, Akessa, Ambelu and Goethals2020) found that car-washing, and silviculture had a positive correlation with the presence of the snail. Heavy metal pollution in Iran has been found to supress antioxidants, neurotransmitter activity and compounds used for protein synthesis (Banaee and Taheri, Reference Banaee and Taheri2019), while pesticide pollution in the same river also led to decreased antioxidant activity in the snail (Raisi et al., Reference Raisi, Reza Pourkhabbaz, Banaee, Reza Pourkhabbaz and Javanmardi2018).

Global climate change may be having a significant impact on the distribution of G. truncatula, though whether this impact is positive or negative largely depends on the region in question. However, in recent decades policymakers have encouraged farmers to preserve or create areas of biodiversity such as wetlands and woodland to preserve species and mitigate global warming (Brown, Reference Brown, Kovács, Herzon, Villamayor-Tomas, Albizua, Galanaki, Grammatikopoulou, McCracken, Olsson and Zinngrebe2021; Sidemo-Holm et al., Reference Sidemo-Holm, Ekroos and Smith2021; Collas, Reference Collas2023). The potential impact of woodland due to shade is discussed above (Jones et al., Reference Jones, Davis, Nalepa-Grajcar, Woodruff, Williams, Brophy and Jones2024a). Creating new wetlands could introduce new habitats and therefore high-risk areas for livestock infections by trematodes. For example, research by Cuthill (Reference Cuthill2020) showed that scrapes, which are small, shallow, irregular-shaped pools created on pasture as habitats for declining farmland wading birds can be rapidly colonized by G. truncatula.

As such, concerns have been raised regarding the impact of widespread farmland scrape creation on liver fluke infection risk in livestock (Jones et al., Reference Jones, Rees, Brophy, Williams, Williams, Morphew, Davis and Evans2024b). The risk of scrapes becoming a source for Fasciola infection will likely vary between farms depending on the precise location of the scrape, the environmental properties of that location and how the scrape is grazed and how the wider area is managed. However, restrictions are often placed upon the management of wetland habitats of biodiversity value. As such practices often promoted to limit fasciolosis risk including fencing, rotational grazing and drainage cannot be implemented on some wetland habitats where G. truncatula populations exist as strict conservation grazing and land management regimens are a necessity to maximize biodiversity (Martin et al., Reference Martin, Fraser, Pakeman and Moffat2013). But even in instances where new wetland habitats are fenced off, they may still impact fluke risk primarily through its hydrological effect on neighbouring grassland.

Restoring wetland habitats such as fen and peat bog near pastureland could attenuate any potential positive effects on G. truncatula due to its aversion to peat. Substantially more research is needed to assess the impacts of both afforestation and peat/wetland restoration on G. truncatula ecology and liver fluke risk, with very few longitudinal or intervention studies discovered in the present review. There are also many socio-economic dimensions of ecological restoration processes, with arguments for and against their integration with food production (Brown, Reference Brown, Kovács, Herzon, Villamayor-Tomas, Albizua, Galanaki, Grammatikopoulou, McCracken, Olsson and Zinngrebe2021; Collas, Reference Collas2023), but animal health is not usually taken into consideration. Additionally, due to the increasing demand for livestock produce, there have also been several studies investigating the viability of alternative crops for foraging (e.g. Kakabouki et al., Reference Kakabouki, Bilalis, Karkanis, Zervas, Tsiplakou and Hela2014; Lee et al., Reference Lee, Domingues, McAuliffe, Tichit, Accatino and Takahashi2021; Karydogianni et al., Reference Karydogianni, Roussis, Mavroeidis, Kakabouki, Tigka, Beslemes, Stavropoulos, Katsenios, Tsiplakou and Bilalis2022). It is unknown whether using these plants instead of traditional grasses would impact the snail's ecology.

The cost of land modification strategies must also be considered in addition to their effectiveness at preventing fluke infection. Improvements to drainage systems, changing foliage and so on may be very expensive, and thus divert resources from other investments. This will be exacerbated in lower income regions and countries, which are also more likely to have substandard sanitation infrastructure which may undermine attempted control measures and contribute to the spread of fascioliasis to humans. In the Bolivian settlement of Huacullani, children were found to be at risk because the route they took from school crossed transmission hotspots. Similar problems have impacted the control of mosquitoes in Ecuador, where a lack of sanitation has led people to store water in ways that encourage mosquito proliferation (Harris and Carter, Reference Harris and Carter2019). As such, any control measures developed will need to take local financial and infrastructure conditions into account to be successful.

Ecology and fluke transmission

Environmental conditions which impact populations of G. truncatula may also influence cycles of fluke transmission. Several studies have shown that fluke infection rates vary between habitats, with lower rates identified in river and stream populations (Schweizer et al., Reference Schweizer, Meli, Torgerson, Lutz, Deplazes and Braun2007; Rondelaud et al., Reference Rondelaud, Vignoles and Dreyfuss2016a) and in snails that inhabit habitats with fast-flowing water (Manga-Gonzalez et al., Reference Manga-Gonzalez, Gonzalez-Lanza and Otero-Merino1991). This may be due to the faster flowing water being sub-optimal for the snail or impeding the ability of the miracidia to swim to snails. Additionally, the diversity of trematode species infecting G. truncatula can also vary depending on habitat type. Rondelaud et al. (Reference Rondelaud, Vignoles and Dreyfuss2016a) found that only C. daubneyi and F. hepatica were found in G. truncatula from drainage furrows, while there was a much greater diversity in pools. Furthermore, Opisthoglyphe ranae and Haplometra cylindracea, trematode parasites of frogs, had much higher infection rates in pools than F. hepatica. It is unknown whether this is due to differing habitat preferences of the trematodes or the definitive host species being more likely to frequent different habitats. Although the intensity of co-infection of either F. hepatica and C. daubyeni in livestock has been found to be negatively correlated with the other species (Jones et al., Reference Jones, Brophy, Mitchell and Williams2017a), it is currently unclear whether habitats that encourage greater competition of trematode species have a reduced risk of transmission to definitive hosts.

Some studies have also identified a positive correlation between snail size and F. hepatica infection rates, both within (Smith, Reference Smith1984; Wislon and Denison, Reference Wilson and Denison1980) and between snail populations (Chapuis, Reference Chapuis2009). However, while there is some evidence that snails in temporary habitats and those from higher altitudes tend to be larger in size (Goumghar et al., Reference Goumghar, Rondelaud, Dreyfuss and Benlemlih2001; Chapuis et al., Reference Chapuis, Trouvé, Facon, Degen and Goudet2007), it is unknown if these populations are more susceptible to infection. Furthermore, in Galicia, Spain, it was found that while snail size was positively associated with F. hepatica infection, C. daubneyi had a negative correlation, which may be due to older snails developing resistance to C. daubneyi over time (Iglesias-Piñeiro et al., Reference Iglesias-Piñeiro, González-Warleta, Castro-Hermida, Córdoba, González-Lanza, Manga-González and Mezo2016).

Much like the population abundance of G. truncatula, fluke infection rates in the snail also undergo seasonal fluctuations which can vary from year to year due to climatic conditions. However, local conditions can also alter the impact of these weather patterns, as Novobilský et al. (Reference Novobilský, Engström, Sollenberg, Gustafsson, Morrison and Höglund2014) found that seasonal variation in the proportion of infected snails differed substantially between farms in Sweden. Several studies have identified that local factors can impact infection rates in livestock (Bennema et al., Reference Bennema, Ducheyne, Vercruysse, Claerebout, Hendrickx and Charlier2011; Charlier et al., Reference Charlier, Bennema, Caron, Counotte, Ducheyne, Hendrickx and Vercruysse2011; Jones et al., Reference Jones, Brophy, Mitchell and Williams2017a), however it is difficult to assess whether these factors have a bigger impact on the snails or the trematodes, and in some cases both may be impacted. For example, while mowing may be detrimental for G. truncatula (as discussed in ‘The Impact of Human Activity’), it may also remove metacercariae from fields and kill the free-living stages by exposing them to sunlight. That said, the infection rates within the definitive and intermediate hosts are linked. For example, Jones et al. (Reference Jones, Williams, Dalesman, Ayodeji, Thomas and Brophy2017b) found that the F. hepatica and C. daubneyi egg count in livestock faeces was the main determining factor of infection rates in G. truncatula.

That said, even snail populations with infection rates of <1 to 7% in G. truncatula are enough to cause livestock infection rates of over 30% (Khallaayoune and El Hari, Reference Khallaayoune and El Hari1991; Mage et al., Reference Mage, Bourgne, Toullieu, Rondelaud and Dreyfuss2002; Belfaiza et al., Reference Belfaiza, Moncef and Rondelaud2005). A similar pattern is also seen in human schistosomiasis infection rates (Léger et al., Reference Léger, Borlase, Fall, Diouf, Diop, Yasenev, Catalano, Thiam, Ndiaye, Emery and Morrell2020; Nwoko et al., Reference Nwoko, Kalinda and Chimbari2022), and highlights the need to not only identify the habitats where G. truncatula is present, but also where the snail is likely to interface with livestock. Currently, there is disagreement over whether F. hepatica becomes better adapted to infect local populations of G. truncatula over time (Vareille-Morel et al., Reference Vareille-Morel, Rondelaud and Dreyfuss2002; Dreyfuss et al., Reference Dreyfuss, Vignoles and Rondelaud2012; Sanabria et al., Reference Sanabria, Mouzet, Courtioux, Vignoles, Rondelaud, Dreyfuss, Cabaret and Romero2013) or is better adapted to infect new populations of snail (Gasnier et al., Reference Gasnier, Rondelaud, Abrous, Carreras, Boulard, Diez-Banos and Cabaret2000; Correa et al., Reference Correa, De Meeûs, Dreyfuss, Rondelaud and Hurtrez-Boussès2017). In either case, preventing livestock from interfacing with the snail will work to both break current cycles of infection and prevent flukes from establishing themselves in new snail populations.

Identifying which potential habitats contain G. truncatula and how far they extend across pastureland can be a time-consuming process, and sometimes the snails may be missed during malacological searches due to their small size or low populations. However, eDNA techniques have been proven highly effective at identifying the presence of G. truncatula, as well as other amphibious trematode intermediate snail hosts, even in habitats where the snails were not visually identified (Jones et al., Reference Jones, Brophy, Davis, Davies, Emberson, Rees Stevens and Williams2018, Reference Jones, Davis, Jones, Tyson, Davies, Cutress, Brophy, Rose, Williams and Williams2021, 2022; Davis et al., Reference Davis, Tyson, Cutress, Davies, Jones, Brophy, Prescott, Rose, Williams, Williams and Jones2020; Mulero et al., Reference Mulero, Toulza, Loisier, Zimmerman, Allienne, Foata, Quilichini, Pointier, Rey and Boissier2021; Rathinasamy et al., Reference Rathinasamy, Tran, Swan, Kelley, Hosking, Williamson, Knowles, Elliott, Rawlin, Spithill and Beddoe2021). This could be especially useful in identifying habitats which may contribute to the spread of fluke to livestock but are only inhabited by a small number of snails. That said, it is well established that other snail species can act as the intermediate host of F. hepatica and C. daubneyi, but it is unknown how much they contribute to the spread of these trematodes, especially given the issues with misidentification discussed in ‘Data Comparison’. More research also is needed to investigate the role of these other species in fluke transmission, particularly in environments where G. truncatula is not present.

Environmental management of snails to reduce fluke transmission

It is currently unclear whether the most common or suitable habitats of G. truncatula act as the primary transmission foci for fluke infection. Rivers and drainage furrows are the most common according to the habitat counts, but these would primarily be water sources on pastures, rather than a significant source of grazed forage. As such, it may be the case that rarer habitats recorded in this review, such as moist areas or subsoil effluences on the pastureland, contribute more to infection than those watercourse habitats on the periphery of fields as grazing livestock would consume plant matter contaminated with fluke cysts. In this instance, G. truncatula populations in these habitats would be worthy of increased focus in preventative control strategies, but this has not been systematically investigated. Farmers are often encouraged to fence off ‘wet areas’ to avoid fluke infection, but large swathes of pastureland may need to be temporarily fenced off to match the same impact as current treatment-based measures. This is especially true in flatter regions where potential habitats are likely to be more widespread (Beltrame et al., Reference Beltrame, Rose Vineer, Walker, Morgan, Vickerman and Wagener2021).

If watercourses are the primary transmission foci for infection, this could be used as an incentive for farmers to take part in schemes to preserve watercourse ecosystems. Arnott et al. (Reference Arnott, Chadwick, Harris, Koj and Jones2019) found that while funding was available for such projects under Agri-environment schemes, they only accounted for only 3% of options taken up by farmers. However, this incentive relies on whether restricting access to watercourses reduces fluke transmission to livestock. An alternative to fencing is improving better drainage in fields, as Beltrame et al. (Reference Beltrame, Rose Vineer, Walker, Morgan, Vickerman and Wagener2021) found that around 8% more drainage on UK farms could match the impact of treatment regimens. However, this strategy runs counter to the need to increase water storage on farmland to alleviate downstream flooding from increasingly frequent extreme rainfall events (Collentine and Futter, Reference Collentine and Futter2018).

If environmental measures are not a viable or affordable solution, improved treatment regimens may be a better option in the short term, though this does risk the development and spread of Anthelmintic resistance through overtreatment (Vineer et al., Reference Vineer, Morgan, Hertzberg, Bartley, Bosco, Charlier, Chartier, Claerebout, De Waal, Hendrickx and Hinney2020). However, targeted treatment regimens could be used to reduce the transmission of fluke eggs onto pastureland at the times of the year when the snails are most active. Such regimens have been shown to not only reduce infection rates of F. hepatica in livestock, but also in G. truncatula (Parr and Gray, Reference Parr and Gray2000), however, there remains potential for wildlife such as rabbits and hares to also contaminate G. truncatula habitats with F. hepatica eggs (Juhasz et al., Reference Juhasz, Chapman, Martin, Cunningham, Jones, Johnson, Walsh, Quayle, Cracknell, LaCourse and Stothard2023).

Alternatively, grazing schedules could be created so that livestock avoid fields with high-risk areas at times when infective metacercariae are most abundant. Livestock are also known to spend more time near water sources for drinking and grazing during periods of dry and warm weather (Boray, Reference Boray2007; Pandey et al., Reference Pandey, Kiker, Campbell, Williams and Coleman2009), so providing alternative water sources during these periods could lower the risk of fluke infection.

However, this strategy requires a better understanding of which factors result in high-risk areas so they can be mapped at the farm level, as has been done for other helminth livestock parasites (McFarland et al., Reference McFarland, Vineer, Chesney, Henry, Brown, Airs, Nicholson, Scollan, Lively, Kyriazakis and Morgan2022). Incorporating the preference of G. truncatula for poorly draining soils has already been shown to improve the HELF model of fluke risk (Beltrame et al., Reference Beltrame, Dunne, Vineer, Walker, Morgan, Vickerman, McCann, Williams and Wagener2018), and earlier research has suggested that mapping potential G. truncatula habitats will increase the accuracy of infection risk models (Charlier et al., Reference Charlier, Bennema, Caron, Counotte, Ducheyne, Hendrickx and Vercruysse2011). It stands to reason that gaining a greater understanding of the environmental preferences of G. truncatula will allow for a more accurate mapping of potential risk areas. However, which habitats are high risk may also depend on the livestock species, as cattle are known to favour marshier areas of pastureland than those favoured by sheep or goats (Boray, Reference Boray2007).

Watercress beds were the only habitats investigated by studies in this review in which direct plant consumption could cause human fascioliasis. However, the consumption of freshwater plants is also a major source of infection in the Bolivian altiplano, which suffers from hyperendemic human infection (Angles et al., Reference Angles, Buchon, Valero, Bargues and Mas-Coma2022). In both cases, thorough cleaning of the crops is required to ensure cysts are not ingested. However, a lack of treated water available for rural households is also a major issue for regions with hyperendemic human infection, especially as poor sanitation can result in sewage, natural water sources, pasture drainage and irrigation ditches for crops being connected, resulting in the spread of F. hepatica from G. truncatula habitats to human habitation (Angles et al., Reference Angles, Buchon, Valero, Bargues and Mas-Coma2022). As such, improvements to sanitation systems and the education of local community leaders are vital to help reduce human infection rates in these areas.