Search strategy

A systematic search of the literature on Google Scholar, PubMed, and EBSCOhost databases was conducted using the following terms and Boolean operators (OR, AND): Fasciolosis AND Temperature, Lymnaea OR Radix OR Galba OR Pseudosuccinea OR Austropeplea OR Fossaria AND growth, fecundity, AND survival at the global scale. Other search terms used were (Fascioliasis AND Temperature), (Lymnaea AND Temperature), (Galba AND Temperature), (Pseudosuccinea AND Temperature), (Fossaria AND Temperature), (Austropeplea AND Temperature) and (Radix AND Temperature), Mathematical Models AND Temperature AND Fascioliasis AND Intermediate Hosts. The identified articles were initially screened by reading the titles and abstracts. Furthermore, the selected articles’ references and bibliographic lists were searched for potential leads to additional relevant studies for inclusion. Full-text articles were retrieved and managed in the Endnote 20 reference manager (Clarivate Analytics, Philadelphia, PA, USA).

Inclusion criteria

Studies were considered for inclusion in the review if they were published in peer-reviewed scientific journals and specifically reported on (1) the effect of temperature on life history traits of IHS of Fasciola hepatica and Fasciola gigantica that cause animal and human fascioliasis; (2) the genus Lymnaea, Austropeplea, Fossaria, Galba, Radix, Pseudosuccinea; and (3) only articles written in English were considered in this study.

Exclusion criteria

Exclusion criteria were: i) studies concerning a different parasite than F. gigantica or F. hepatica; ii) studies that do not include Lymnaea sp., Fossaria sp., Galba sp., Radix sp., Austropeplea sp or Pseudosuccinea sp.; iii) articles not written in English; iv) studies reporting results outside of the scope of the review question; and v) studies not reporting on the effect of temperature on life history traits of IHS.

The systematic literature search yielded a total of one thousand two hundred twenty-seven plus seventeen reports from other sources, which included abstracts, reports, books, and theses (Fig 1). Seven hundred fifty articles were eliminated because of duplication, and three hundred articles were removed as they were deemed ineligible based on their titles and abstracts. A further one hundred and twenty articles were excluded because they did not focus on temperature despite looking at the life history traits of IHS, and thirty-nine were further dropped as they did not specifically report on temperature about the IHS Lymnaea spp, Fossaria spp, Galba spp, Austropeplea spp Pseudosuccinea spp, and Radix spp of Fasciola spp. Table 1 lists the thirty-five publications that were considered for this evaluation. The findings from the publications that met the criteria for the review were categorized into the following themes: temperature and fecundity, temperature and growth, temperature and survival, and temperature and parasite development. These are discussed below about potential changes in the disease risk with a possible rise in temperature.

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Fig 1. PRISMA diagram shows the study selection process.

https://doi.org/10.1371/journal.pntd.0011812.g001

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Table 1. Summary of laboratory experimental studies and models that assessed the effect of temperature on Lymnaea, Galba, Pseudosuccinea, Austropeplea and Radix snail species.

https://doi.org/10.1371/journal.pntd.0011812.t001

The study selection process is shown in Fig 1.

Temperature effect on IHS fecundity

Reviewed articles in Table 1, showed that temperature influence the time of sexual maturity and fertility in Lymnaeid snails [50]. In temperate Galba truncatula, reproduction rate and fecundity ceased at temperature below 5°C. In one of the experiments involving Galba truncatula, it was observed that reproduction rate and fecundity ceased at a temperature below 5°C [33,50]. In another study, it was observed that fecundity occurred under experimental conditions at temperatures as low as 10–11°C for Galba truncatula [60]. The reproduction temperature range for Galba truncatula was observed to be 10–25°C. The reproduction rate was high at 24°C for Pseudosuccinea columella, and this was also observed to tolerate cooler, warmer, and desert temperatures [66]. However, it was observed that the reproduction rate of Radix acuminata in the tropics occurred optimally at a temperature range of 16–34°C [39,40]. Furthermore, Aziz [42] and Misra [41] found that the reproduction rate of Radix luteola (Lamarck) and Radix acuminata, respectively, was higher at lower temperature ranges of 15–20°C. In subtropical regions, 5–10°C was the minimal temperature needed for Pseudosuccinea columella and Austopeplea (Lymnaea) tomentosa egg development and hatching [66]. It was observed that Lymnaea stagnalis eggs require constant temperatures between 9.9°C and 28.0°C for development and hatching [57]. Most studies found that snail reproduction increased within a certain temperature range, but fecundity was significantly reduced below and beyond that temperature range (Table 1).

Temperature effect on IHS growth

Temperature has been shown to affect IHS growth [41,42,61,62]. In temperate regions, the optimal growth rate of Lymnaea viatrix snails was at 25°C, and it declined at temperatures above 25°C [52,61]. In another study, it was noted that snail growth increased between temperatures of 15°C and 24°C for Lymnaea viridis [56]. Also, the growth rate for Lymnaea stagnalis increased with temperature, with 25°C being optimal [50]. At 20°C, most Radix peregra snails showed significantly higher growth rates [49]. In the tropics, it was observed that the rate of growth increased with temperature from 15–30°C for Radix acuminata [42]. In another experiment, it was noted that at 15–22.5°C, juvenile Galba truncatula snails became active, and their growth increased rapidly [33]. In the subtropics, temperature is particularly influential in the development of G. truncatula and F. hepatica, which require temperatures ≥10°C for growth, reproduction, and survival [62]. The studies reviewed revealed that IHS species from different regions have different thermal tolerances for growth (Table 2).

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Table 2. Summary of Table 1 shows the IHS of Fasciola spp., their preferred climate, the overall thermal tolerance range for each life history trait, and the temperature range for the development of Fasciola spp. intramolluscan larval stages.

https://doi.org/10.1371/journal.pntd.0011812.t002

Temperature effect on the survival of IHS

Several studies (Table 1) showed that lymnaeid snails do not survive at temperatures below 5°C [33] and that their survival rate is greatly reduced when temperatures get to 25–35°C. Temperatures above 30°C were lethal to developing embryos of L. tomentosa; P. columella hatched at up to 34.5°C, but at 36°C none survived [66]. In the studies carried out by Aziz and Raut [42], the survival rate of Radix acuminata in the tropics decreased between temperatures of 25°C and 30°C, while the survival rate for Lymnaea peregra in the subtropics was high at 20°C [49]. In general, IHS survival decreased with increasing temperatures.

Temperature and parasite development

In an experiment to ascertain how seasonal temperature fluctuations affect the development of Fasciola gigantica in Radix natalensis in the tropics, it was observed that at 16°C, rediae developed from the sporocyst [32]. It was noted that cercariae were shed at a minimum temperature above 16°C, and the majority of the cercariae were shed at a mean maximum temperature of 20°C [32]. In the temperate region, cercariae shedding for Fasciola hepatica took longer at low temperatures (6–8°C), and the time for the process was significantly reduced at 20°C in the temperate region [59]. No F. hepatica larval development was observed at temperatures below 15°C in P. columella [58]. The maximum development rate of F. hepatica inside G. truncatula was observed at temperatures from 23–25°C, and no larval development was observed at temperatures below 10°C [37,43,48,51,53,55,57]. Another study found that several generations of daughter rediae were observed at 10°C, that shedding occurred at 10–25°C, and that no cercariae shedding occurred at temperatures below 10°C or above 25°C [46,47,52–54,62]. It was observed in the subtropics that the infection rate rose with increasing temperatures up to 24°C and diminished with a further elevation in temperature. Infection rates were highest in G. truncatula at 16–24°C, in P. columella, and at 20°C in A (L). tomentosa and G. cubensis [67]. Most studies reviewed concluded that the optimal temperature for Fasciola development was between 10°C and 30°C.

Temperature-dependent model formulation

Numerous statistical and mathematical models have been developed to understand the dynamics of fascioliasis transmission. Most of these models synthesize information from experimental studies and extrapolate to give future projections.

Statistical models

The study by Malone et al. [36] showed that 23°C was an optimal temperature for the distribution of F. hepatica in the Ethiopian highlands. Prediction of the distribution of snails has been used to potentially indicate the risks of disease transmission. Studies by Stensgaard et al. [68] and Pedersen et al. [69] have combined aspects of temperature and Geographic Information Systems (GIS) to predict the spatial distribution of the disease. These studies indicate areas that will be suitable for both snail and parasite distribution and further suggest that variable habitats may be created due to a temperature rise.

Mathematical models

A model by Rapsch et al. [63] suggested that the risk for fascioliasis is high at high temperatures. As the development of Fasciola hepatica takes only 2–3 weeks at temperatures of 23°C–26°C, risk in this temperature range is high. It was observed that the risk of the disease caused by low land strain of F. hepatica is high at altitudes below 1800m and decreases as altitude increases [63]. The month of August was predicted to have a high fascioliasis prevalence in Switzerland as this is the with favourable temperatures for the development of the parasite. Another model by Hope-Cawdery [64] predicted that the effect of temperature on the survival of extra-mammalian stages of liver fluke occurs at a temperature range of 10–30°C. They observed the effect of temperature on survival to the completion of the intra-molluscan stage of F. hepatica, with an optimum at about 16°C. It also shows that, at low temperatures, the combination of long development times and increasing mortality rates results in a rapidly falling potential for transmission. This occurs in nature, as the presence of snails in Iceland without transmission demonstrates. Most models identified rainfall and temperature as the most important factors for the survival and development of the parasite’s free-living stages, as well as the IHS [65].

Temperature effect on fecundity of IHS

Generally, most living organisms, including snails, channel most of their resources towards their life history traits (growth, fecundity, and survival) [28]. The predicted rise in temperatures will have an effect on snail fecundity and egg development; and this will have important implications on the future distribution and population dynamics of the IHS [66]. The results of this review study suggest a positive association between temperature and snail fecundity. The study has shown that there will be a likely increase in snail population within favourable temperature range [33,50] while, rising temperatures beyond the favourable temperature range due to climate change may negatively affect the life-history traits of snails. This effect on life-history traits will potentially lead to a reduction in egg viability and or reduced survival due to changes in the allocation of resources [70]. Temperature also influences organisms’ physiological functions by altering the metabolic rates and aerobic scope of ectotherms through thermodynamic effects [71]. The concept of energy allocation maybe the case. At low temperatures, snails may not feed as much thus, energy reallocation is towards survival than reproduction [33]. According to Khallaayoune et al. [72], cooler temperatures may also affect the synchronization of reproductive events such as the timing of mating and egg-laying. Furthermore, these factors might limit the reproductive success and population growth of lymnaeid snails in temperate regions. In contrast, the results of the reviewed papers indicated that temperatures ranging from 10–25°C enhanced egg mass production in Galba truncatula [73]. Most studies suggested that within favourable temperature range, the reproductive activities of lymnaeid snails can be stimulated, leading to higher fecundity [40,42]. However, most studies also indicated that temperatures above 25°C have negative adverse effects on the fecundity and fertility of snails from temperate regions [44,66]. Heat wave temperature at 25°C was associated with Lymnaea stagnalis producing more eggs, while their immune defence was reduced [50]. The reviewed articles showed that IHS from temperate, Oceania, the Mediterranean, and subtropical regions are temperature sensitive [57,60,66]. On the other hand, IHS from the tropical regions produce more egg masses in the low-temperatures, while the opposite is true in high temperatures for those observed in the tropical regions [40–42]. Higher temperatures might have a positive effect on the reproductive events in lymnaeid snails. For example, Radix acuminata fecundity was optimal at warmer temperatures, between 15°C and 36°C [40–42]. The variations observed in optimal temperatures for fecundity vary with the snail species, size, age, and experimental protocol used. The production of egg masses at different temperatures might suggest that some IHS species are well adapted to low- or high-temperature ranges [28]. This was noted in Pseudosuccinea columella, which has adapted to subtropical and tropical climates. Most of the reviewed articles in this study on lymnaeid snails suggested that most snails’ fecundity ceased at temperatures below 5°C and over 30°C [33,46]. To guide snail control activities, it is critical to understand the optimal temperature range for fecundity for lymnaeid snails and the predicted effect of climate change on snail population dynamics.

Temperature effect on the growth of IHS

Snail growth is another important life history trait that can influence snails to invade new places and adapt to new environments. Growth affects fecundity, ability of IHS to resist trematode infections, and resource availability to the development of intramolluscan larval stages of the trematodes [28]. Snails maintained at 25°C were observed to be larger compared to snails maintained at 15°C [50]. Also, development rates are more temperature-sensitive for species from cooler habitats and terrestrial species than those from warmer habitats and aquatic habitats [70]. This is because warmer temperatures increase feeding habits and metabolic processes, which generate energy for the growth of IHS. Growth has been observed to be influenced by temperatures between the lower threshold and upper threshold temperatures (Table 2). For example, the temperature range of 10–26°C for Galba truncatula [60]. Below and above these temperatures, snail growth may be inhibited while snail mortality increases. For instance, Heppleston [74] suggested that growth was most rapid in the warm summer months, which incidentally is the period when snail mortality was greatest. For example, the optimal growth rate temperature for Lymnaea viatrix snails was 25°C, and above this temperature, the growth rate declined [61], while Venturini [52] observed the optimal growth rate temperature for the same species at 25.5°C. Warmer temperatures and low altitudes have been observed to favour the proliferation of Radix natalensis over Galba truncatula in the tropical regions of Africa and Asia [8,36]. This observation may suggest that climate change may result in the shift in the transmission dynamics of Fasciola hepatica infections by Pseudosuccinea columella which is associated with colonisation of fresh water habitats [23]. At extreme temperatures, the growth of snails declines, and death rates increase. Most of these studies showed that high temperatures within a suitable thermal threshold range promote snail growth. For example, the range of temperatures in tropical locations is 15–35°C; in temperate zones, it is 10–26°C; and in desert or arid regions, it is 18–24°C. A temperature-driven high growth rate might result in increased fecundity, higher survival rates, and the potential of the vector snails to spread fascioliasis to new areas.

Temperature effect on the survival of the IHS

The disease transmission cycle cannot be completed without the existence and survival of a compatible host [28]. The survival time of IHS is influenced by both biotic and abiotic factors. These factors include the species of the snail, habitats types, soil moisture and relative humidity, and tolerance for low- or high-altitude habitats [75]. For example, G. truncatula snails in the Andean highlands of South America adapt to the extreme environmental characteristics of very high-altitude areas [16,76,77]. In Africa, Galba truncatula has adapted to cooler, high-lands or high-altitude areas in Lesotho, South Africa [78], North African nations (Morrocco, Egypt, Tunisia), and East African nations (Ethiopia, Kenya, Uganda, Tanzania) [36], and this is the case in the high lands or altitude in Bolivia [2,77,79,80], which has enhanced the spread of Fasciola hepatica infections. These adaptation techniques include having a longer cercarial shedding period, increased cercarial production per snail, and prolonged survival of infected snails [76]. The absence of Fasciola gigantica in South America ensured fascioliasis transmission by Galba/Fossaria species [14].

Temperature may influence IHS survival; it has been observed that snails survive longer in low-temperature environments than in high-temperature habitats [73]. It has been shown that IHS exhibit phenotypic modification after infection, which affects their life span [28]. Snail survival is one of the primary requirements for trematode development and the maturation of their intramolluscan larval stages. Several IHS are observed to have different optimal temperatures to survive. For example, Radix natalensis, which is the main IHS for Fasciola gigantica in tropical and subtropical habitats, can tolerate warm temperatures in the range of 18–25°C compared to Galba truncatula, which is the IHS for Fasciola hepatica in temperate regions and prefers a cooler environment (10–25°C) [81]. On the other hand, high temperatures have also been associated with altered membrane permeability, increased accumulation of harmful metabolites, and weakened immune systems in snails [28]. This may decrease the snails’ survival chances by making them more susceptible to infection. Despite this, G. truncatula has developed an overwintering ability to withstand extremely cold environments and aestivation in unstable water bodies to resist drought periods [16,46,82]. Therefore, the survival rates of most lymnaeid snail spp. are inversely correlated to an increase in temperature.

Rising temperatures and habitat microecology factors such as soil surface temperature, air temperature, soil humidity, and soil and water pH in these regions might drive lymnaeid snails to shift their geographic distribution [4,25]. Cooler regions that were once suitable for these temperate regions may become less favourable, and extremely cold regions in the temperate regions that were previously unsuitable may become more habitable [24,77]. This can lead to changes in the distribution and abundance of lymnaeid snails, potentially affecting the overall disease transmission dynamics [65]. However, most of the studies were done on infected snails. Understanding the thermal tolerance range of both infected and non-infected snails may be important in predicting the overall effect of climate change on fascioliasis.

Temperature effect on the development of intramolluscan stages of Fasciola spp

The development of the parasite larval stages within snail hosts is temperature-dependent [83–85]. This was supported by the results of the reviewed articles in Table 1, which suggested that high temperatures within a certain favourable thermal regime by IHS promote the rapid development of Fasciola spp. intramolluscan larval stages and the emission of cercariae. Therefore, it was suggested that high temperatures shorten the prepatent stage of Fasciola spp. [12,54,60,73,85]. Temperatures below and above the optimal temperature may result in a decrease in parasite development. Furthermore, Table 2 presents the optimal temperatures for the development of intramolluscan trematode stages for each of the IHS studied. These variations may result from differences in the protocols or experimental conditions, the ability of the IHS to tolerate both warmer and colder temperatures, and many other compounding factors like the type of snail food, the mammalian source of the parasite eggs, the altitude of the isolates’ origin, and variations in daily and seasonal temperatures [85–87]. Despite the variations in optimal temperatures for the development of Fasciola spp inside their IHS, it was observed that the development rates of helminth eggs and early larval stages increase with rising temperatures below the maximal development threshold, of which temperatures above this might stop parasite development [61]. However, the risk of disease transmission decreases at temperatures above 30°C, as IHS dies at this thermal regime due to desiccation [61,63]. It was further noted that the development of Fasciola spp within their intermediate hosts might be affected by the species involved and by the rate at which they adapt to the new environment created by climate change. There was concordance between the presence of G. truncatula or F. hepatica and R. natalensis or F. gigantica, suggesting that the determining factor in the distribution of F. hepatica and F. gigantica is not temperature per se but rather the presence of an intermediate host in which each species can reproduce efficiently [88]. Additionally, the development of parasites within a host is significantly impacted by the strong immunological response of IHS against Fasciola infections. For example, Pseudosuccinea columella in Cuba has been found to have some immune response or resistance against F. hepatica infections [22].

Disease models

Several statistical models have been developed in the past to predict how climatic factors, specifically temperature and rainfall, affect parasite abundance [24]. As the temperature at which infection is carried out increases, there is a proportional increase in parasitization of IHS [51]. However, these models were developed under historic climate conditions or for a specific geographic location, and thus are not well suited to predicting how infection epidemiology might shift in situations of global climatic change [89]. Hence, an answer to it is the development of a mechanistic model. To develop it, data from the fieldwork must be combined with the data from experimental studies on the effect of temperature on host-parasite interactions.

Statistical models

Statistical models have been utilized to better understand the risk factors for fascioliasis and to discover correlations between various disease transmission factors. These models identify optimal areas for snail and parasite distribution. The results also imply that when temperatures rise, variable ecosystems may emerge. Furthermore, regression techniques have been regarded as useful to species distribution modeling since they are concerned with demonstrating correlations between the dependent variable, which can be binary, counts, or ordinal, and the independent or explanatory variables [90,91]. Regression approaches have been utilized in the research of fascioliasis to explain the geographical variation of infections throughout several areas of investigation [92]. The use of geographic information systems (GIS) and remote sensing (RS) technology in epidemiological research and the control of zoonotic diseases has increased over the last few decades [93]. Fascioliasis is a suitable candidate for the application of RS and GIS in epidemiology because it is strongly influenced by the environment, particularly the habitat of the intermediate host. Temperature is an essential element that might limit the development of fascioliasis and the creation of new snail habitats, according to models developed by Pedersen et al. [69]. Further iterative GIS analysis by Malone et al. [36] suggested that soil acidity regime in Southwestern Sudan and Uganda (<5.5 pH) may be unsuitable for lymnaeid snail hosts of F. hepatica and or those tropical thermal regimes with an average annual mean temperature above 23°C, as unsuitable for Galba truncatula. The average annual mean temperature of 23°C or above was found to correspond to areas below the reported 1200 m elevation limit of F. hepatica in Ethiopia [36].

Mathematical models

Rapsch et al. [63] and Fox et al. [24] predicted that changes in the global temperature may have an impact on both the snails’ geographic distribution and the abundance of Fasciola spp. However, the research by De Kock et al. [78] shows that temperature, altitude, type of waterbody, and, to a lesser extent type of substratum, are critical factors that may greatly affect the geographical distribution of G. truncatula. Although models based on temperature and rainfall have been developed to estimate fluke abundance, these models usually use data from the season during which the transmission is known to occur [89]. These models are not reliable in predicting changes in the seasonality of infection. Most previous models identified rainfall and temperature as the key drivers in the transmission of fasciolosis [94,95]. However, current models incorporate GIS and remote sensing (RS) in mapping the suitable habitats for IHS and the distribution and abundance of IHS species in a particular area. The highest risk for the development of eggs was defined at 30°C where development only takes 8–10 days. However, the risk of the disease transmission decreased at a temperature above 30°C, as eggs die at this thermal regime. Rapsch et al. [63] observed that at low temperatures like 10°C the fascioliasis risk is low because the development of the eggs takes up to 6 months. In another case, a model predicted that the occurrence of G. truncatula decreases with the increase in temperature, whilst the distribution of R. natalensis increases with the rising temperature, but within its thermal tolerable range [23]. The main key drivers of fascioliases in the global database were rainfall and potential evapotranspiration across the entire globe [24,96]. As a result, the resulting equation for generating the index was modified to allow for the assessment of fascioliasis risk from either F. hepatica or F. gigantica, as both species thrived in East Africa [36]. In East Africa, risk index maps were developed for both species. The computed risk score showed geographic variation in the transmission patterns of both fascioliasis species. Places with higher soil moisture content were riskier than those with lower soil moisture content [36].

Potential future research areas

The impact of climate change on fascioliasis is complex due to the multitude of factors that may be at play [97]. While temperature can influence the spread of fascioliasis, the availability of food, parasite, compatible host, the ability of the pathogen to utilize a variety of host snails [11,98], and water sources for the snails and the presence of other climatic and human-related factors may also play a role [99]. For instance, higher humidity levels and changes in water availability could modify the transmission dynamics and spread of the parasite [6]. Furthermore, changes in host species composition may cause the disease’s natural distribution to expand or constrict. Overall, the potential impact of climate change on fascioliasis is uncertain, and more research is needed to fully predict the effects of climate change on fascioliasis transmission. Furthermore, more research into the impact of the various factors that may be involved should be conducted to gain a better understanding of the complex transmission dynamics of fascioliasis.

There is a need to understand the effect of temperature on all the development stages of the snail-parasite system as well as the survival rates of IHS over time [83,100]. The tolerance of successive snail generations at various temperature regimes may also need to be assessed. This is because the parameters employed in disease models based on the performance of a single generation may change as snails adjust to greater temperatures over time. To achieve this, the use of experimental data coupled with field studies may prove valuable in observing the changes in the environment. Temperature-driven experiments based on infected and non-infected snails may assist in understanding the life history trials and disease transmission dynamics of fascioliasis and other snail-borne diseases that may be affected most by climate-driven rise in temperature. The use of geographic information systems (GIS) in models will also assist in projecting the areas that can be future disease hot spots owing to the rise in temperature. Furthermore, this review revealed that many studies on fascioliasis have focused on F. hepatica, which thrives in temperate climates and subtropical developed countries, and less on F. gigantica, which is most prevalent in tropical regions of the developing world. The review also exposed that few experimental studies explore the effect of temperature on life history traits of fascioliasis intermediate host snails in Africa. No mechanistic model has been developed to forecast how future temperature increases will affect the dynamics of fascioliasis transmission in Africa.