Table 1.

Summary of laboratory studies, field studies and models that assessed the effect of temperature on Bulinus and Biomphalaria snail species between 1980 and 2016.

Author (Reference)	Objective	Snail Species Studied	Methods	Outcome
Appleton and Eriksson [36]	To determine the influence of fluctuating above-optimal temperature regimes on the fecundity of Bi. pfeifferi	Biomphalaria pfeifferi	Laboratory experiment	Snails with the shell height of 1.5–2.5 mm did not produce egg masses and had the least survival rate. Fecundity was observed to reduce when snails were exposed to temperature above 27 °C.
Dagal et al. [37]	To determine the effect of some physico-chemical factors (temperature, pH and salinity) on the hatchability of egg masses and survival of juvenile and adult snails	Bulinus (Physopsis) abyssinucus	Laboratory experiment	No eggs hatched at 5, 10 or 15 °C. The mean survival rate of snails at 5 and 10 °C was zero. Best egg hatching temperature was 25 and 30 °C. No eggs hatched at 35 °C. Maximal snail survival time was observed at temperatures between 20 and 35 °C. No snail survived at 40 °C.
El-Emam and Madsen [38]	To compare the effect of temperature on the growth, survival and fecundity of Bu. truncatus and Bi. alexandrina	Biomphalaria alexandrina and Bulinus truncatus	Laboratory experiment	Minor differences in the shell height of Bi. alexandrina and Bu. truncatus maintained at 26 °C and 28 °C. The survival of Bi. alexandrina and Bu. truncatus greatly reduced at 10 °C and 33 °C. For both snail species, the net reproductive rate was optimum at 26 °C.
Joubert et al. [39]	To determine the survival of Bu. africanus (Krauss), Bu. globosus and Bi. pfeifferi at constant high temperatures of 34 °C to 40 °C	Bulinus africanus (Krauss), Bulinus globosus (Morelet) and Biomphalaria pfeifferi (Krauss)	Laboratory experiment	Marked increase in the survival of Bu. globosus observed at 36 °C and 34 °C. The survival time of Bu. globosus at 34 °C was almost four times longer than the survival of Bu. africanus and Bi. pfeifferi. Higher temperatures were more favourable for Bu. globosus than Bu. africanus and Bi. pfeifferi.
Kubiriza et al. [40]	To compare the performance (survival, growth, hatchability and reproduction) of Bu. nyassanus to other Bulinus spp. when exposed to different constant temperatures	Bulinus nyassanus (Smith, 1877)	Laboratory experiment	No significant differences in the growth of snails maintained at 25, 28 and 31 °C but slowest at 22 °C. No significant differences in the survival rate of snails at 25, 28 and 31 °C. However, it was observed to be optimal at 25 °C. No significant differences in the mean number of eggs laid across temperatures. The net reproductive rate was greatly reduced at 22 °C compared to the other three temperatures.
McCreesh et al. [41]	To determine the effects of water temperature on the mortality, fecundity, and growth rates of Bi. sudanica	Biomphalaria sudanica	Laboratory experiment	Water temperature strongly affected snail fecundity. Optimal snail fecundity (maximum mean number of eggs/snail/week) was observed at 21.6 °C. Very low and very high temperatures reduced snail survival. Least snail mortality was observed at 19 °C. No clear relationship between water temperature and snail growth. However, for the small and medium sized snails, fastest growth was observed at 23.1 °C and 23.3 °C, respectively.
Pflüger et al. [42]	To evaluate the effect of temperature on the development rate of Schistosoma haematobium development in Bulinus snails	Bulinus truncatus	Laboratory experiment	High snail mortality observed among snails maintained at 17 and 33 °C. Surviving snails did not develop cercariae. The minimum prepatent period of 17–19 days and 17–20 days observed among snails maintained at 30–31 °C and 32 °C, respectively. Longest prepatent period of 106–113 days observed among snails maintained at 18 °C. A hyperbolic function developed to determine the relationship between temperature and the length of the prepatent period estimated 15.3 °C as the temperature threshold at which parasite development within the Bu. truncatus theoretically comes to a standstill.
Pflüger [43]	To determine the effect of temperature on the length of the prepatent period in infected Bi. glabrata snails	Biomphalaria glabrata	Laboratory experiment	Nearly all snails maintained at 16 °C died during the prepatent period. At this temperature, the prepatent period approximated to take more than 130 days. Minimum prepatent period of 15 days observed among snails maintained at 32 and 33 °C. A hyperbolic function developed to determine the relationship between temperature and the length of the prepatent period estimated 14.2 °C as the temperature threshold at which parasite development within the Bi. glabrata theoretically comes to a standstill.
Mofolusho and Benson [44]	To access the influence of acclimatization (to laboratory conditions) on the fecundity and fertility of field collected Bi. pfeifferi	Biomphalaria pfeifferi (Krauss, 1848)	Laboratory experiment	The mean number of eggs per egg mass in laboratory bred snails was higher than in acclimatized field collected snails. The survival rate of acclimatized snails is lower than that of laboratory bred snails.
Joubert et al. [45]	To determine the survival of Bu. africanus (Krauss), Bu. globosus (Morelet) and Bi. pfeifferi (Krauss) at constant low temperatures (0 °C to 8 °C)	Bulinus africanus (Krauss), Bulinus globosus (Morelet) and Biomphalaria pfeifferi (Krauss)	Laboratory experiment	Snail survival reduced with a reduction in temperature. Lower temperatures more unfavourable for Bi. pfeifferi than Bu. africanus or Bu. globosus.
Barbosa et al. [46]	To determine the effect of seasonal temperature variation on egg production during the year	Biomphalaria glabrata	Laboratory experiment	The snail reproductive rate was observed to vary inversely with temperature. Snail reproductive rate was highest when temperature was around 19.9 °C. The reproductive rate as affected reduced as temperature rose to 24 °C during summer. The number of eggs per mass was observed to be maximal when temperature was around 22 °C observed during autumn.
O’keeffe [47]	To evaluate the effect of seasonal climatic changes on the natural populations of Bu. globosus	Bulinus globosus	Field experiment	The snail intrinsic growth rate reduces with rise in temperature beyond 28.5 °C. The per capita recruitment rate of snails increased with temperature. It was maximal at 20.6 °C, beyond which it started reducing.
Woolhouse and Chandiwana [48]	To determine the factors that influence the abundance of Bu. globosus in space and time for a critical assessment of the possible effectiveness of different snail control strategies	Bulinus globosus	Field experiment	Snails maintained in cages at 14–16 °C, 21–22 °C and 22.5–23.5 °C. Growth rate increased with rise in temperature.
Mangal et al. [49]	To determine the impact of temperature on the worm burden and prevalence of schistosomiasis for optimal disease control strategies	Non specific Biomphalaria spp.	Modelling	The mean worm burdens maximal at 30 °C and reduces sharply at 35 °C. Schistosomiasis prevalence was stable in the temperature range of 20–35 °C. Parasite survival optimum at 20 °C thus more effective to carry out disease control measures during times of increased parasite survival.
McCreesh and Booth [50]	To simulate all temperature-sensitive stages of S. mansoni and the life cycle of its intermediate host snail Bi. pfeifferi	Biomphalaria pfeifferi	Modelling	Model developed for transmission sites such as rivers and lakes. In the lake and river scenarios, infection among humans was modelled to be high at 15–19 °C and 20.5–25 °C, respectively. Outside the temperature range of 14.0–31.5 °C, snail survival reduces greatly. The prepatent period reduces with increasing time. For example, it reduces from 130 days at 14.0 °C to 18 days at 32 °C. In the lake and river scenarios, temperature ranges above 15–18 °C and 15–20 °C, respectively led to a reduction in the number of infected snails.
Ngarakana-Gwasira et al. [51]	To develop an epidemiological model for improved predictions of the impact of climatic factors on the dynamics and variation of schistosomiasis intensity in Zimbabwe	Non-specific snail species	Modelling	The temperature ranges of 18–28 °C was observed to be ideal for schistosomiasis transmission. The optimal schistostosoma transmission temperature was around 23 °C. This was supported by the reproductive number which increased linearly with temperature and reached it maximum at 23 °C. Thereafter, it started reducing. Infection among snails higher at 22 °C compared to temperature of 20 °C and 25 °C while it dies out at 30 °C.