Variations of Supercooling Capacity in Intertidal Gastropods

Abstract

Winter low-temperature confines species distribution. Intertidal gastropods are distributed from tropical to polar zones, facing variable intensities and durations of low temperatures. They usually set their supercooling points (SCPs) at high subzero temperatures to stimulate freezing. However, the variations in SCP in intertidal gastropods at intraspecific and interspecific levels remain poorly understood. Here, we measured the body size, cooling rate, and SCP of nine intertidal gastropod species in China. These species were distributed in high or middle intertidal zone with different geographic distributions. The average SCPs (-4.27~-7.10 °C) and the coefficients of variation of SCP (22.6%~45.9%) were high in all species. At the intraspecific level, the supercooling capacity was positively correlated with the cooling rate. Interspecifically, the supercooling capacity was closely related to the cooling rate, and also to the species' geographical distribution. Northern high-shore species showed lower SCPs, while southern high-shore species had higher SCPs. There was no difference in SCP between widespread high- and mid-shore species. Our results indicated that the supercooling capability is potentially an adaptative response to the local winter temperatures, and the cooling rate is a factor in determining the difference in SCP at the intraspecific and interspecific levels.

Keywords: cooling rate; low temperature; molluscs; species distribution; supercooling point.

Figure 1

Sampling locations in China and winter temperatures at sampling locations. (a) Two sampling locations (Qingdao and Dongtou) of nine intertidal gastropod species. (b) The total number of occurrences of temperatures in winter (December, January, and February) over the past ten years (2011–2021) in Qingdao (blue bars) and Dongtou (orange bars).

Figure 2

Body size measurement in snails and the comparison of body size among nine species. (a) Shell diagrams indicate the measurement of length (L), width (W), and height (H). Volume (V) is calculated according to the formula below. (b) Volumes of nine intertidal gastropods with different geographic distribution ranges and tide zone (Echinolittorina malaccana, Em; Nerita yoldii, Ny; E. radiata, Er; Littoraria sinensis, Ls; Reishia clavigera, Rc; Monodonta labio, Ml; Tegula rustica, Tr; Littorina brevicula, Lb; Lunella coreensis, Lc). Box plots show median (center line within the box), first and third quartile values (lower and upper borders of the box), and the whiskers extend to 1.5× the interquartile range. The spots outside the box are outliers. Different letters indicate significant differences in volume among species (p < 0.05).

Figure 3

Example of observed changes in body temperature of a snail that was cooled from 16 °C. The supercooling point (SCP) denotes the temperature at which the snail froze. T is the temperature at which an individual reaches its supercooling point and t is the time when ice formation occurs in the body. Cooling rate is calculated based on T and t.

Figure 4

Cooling rates of nine intertidal species in the present study. Different letters indicate significant differences in cooling rate among species (p < 0.05). Species abbreviations: Echinolittorina malaccana, Em; Nerita yoldii, Ny; E. radiata, Er; Littoraria sinensis, Ls; Reishia clavigera, Rc; Monodonta labio, Ml; Tegula rustica, Tr; Littorina brevicula, Lb; Lunella coreensis, Lc.

Figure 5

Correlation between individual’s volume and cooling rate in each species. Northern, southern, and widespread species are distinguished with purple, orange, and green, respectively. Filled circles and empty circles represent high-shore individuals and mid-shore individuals, respectively. R-squared reflects the goodness of fit. The F and p values indicate whether the slope is significantly non-zero. Solid line reflects linear regression line, and dashed lines reflect the 95% confidence intervals around linear regression line. Species abbreviations: Echinolittorina malaccana, Em; Nerita yoldii, Ny; E. radiata, Er; Littoraria sinensis, Ls; Reishia clavigera, Rc; Monodonta labio, Ml; Tegula rustica, Tr; Littorina brevicula, Lb; Lunella coreensis, Lc.

Figure 6

Supercooling points (SCPs) of nine intertidal species in China. The center line in the box plot is the median value, and the whiskers extend to 1.5× the interquartile range (IQR). The spots outside the box are outliers. Different letters indicate significant differences in cooling rate among species (p < 0.05). Species abbreviations: Echinolittorina malaccana, Em; Nerita yoldii, Ny; E. radiata, Er; Littoraria sinensis, Ls; Reishia clavigera, Rc; Monodonta labio, Ml; Tegula rustica, Tr; Littorina brevicula, Lb; Lunella coreensis, Lc.

Figure 7

Relationship between cooling rate and supercooling point in each study species. The nine gastropods are northern (purple), southern (orange) and widespread (green) species, respectively, and live in high-shore (filled circle) or mid-shore (empty circle) zones. R-squared reflects the goodness of fit. The F and p values indicate whether the slope is significantly non-zero. Solid line reflects linear regression line, and dashed lines reflect the 95% confidence intervals. Species abbreviations: Echinolittorina malaccana, Em; Nerita yoldii, Ny; E. radiata, Er; Littoraria sinensis, Ls; Reishia clavigera, Rc; Monodonta labio, Ml; Tegula rustica, Tr; Littorina brevicula, Lb; Lunella coreensis, Lc.