Pomacea canaliculata, a freshwater snail native to South America, has become widely naturalised in many countries, causing serious damage to agricultural and native ecosystems. Although climate warming is likely to expand the distribution of this species, limited information exists regarding its impact on feeding activities. In this study, we examined the effects of temperature on the feeding activity of this species and estimated the impact of climate warming on its feeding potential. The feeding activity was determined by measuring the amount of standard food (Japanese mustard spinach, komatsuna) ingested at different temperatures. It tended to increase from 15 to 25 °C but became almost stable from 25 to 35 °C. The respiration rate determined by the O2 consumption rate, showed a similar response to temperature. Based on these findings, we constructed a simple model to estimate the relative feeding activity using climatic data recorded at meteorological stations throughout the Japanese Archipelago. The model estimated that, with warming of + 2 °C, annual feeding potential (relative value) increased by 21.1% at the present northern distribution limit of this species. The effect of warming on percentage increase in feeding potential was estimated to be smaller at the southern distribution limit (9.9%), although the absolute feeding potential was larger than that at the northern sites. The model also suggested that if this species expanded its northern distribution range as a result of climate warming, it would have a high feeding potential comparable to that of the southern regions.
Pomacea canaliculata (Lamarck 1822), a freshwater snail native to the central part of South America, encompassing the Lower Paraná, Uruguay, and La Plata basins (Hayes et al. 2012), is naturalised worldwide and causes serious damage to aquatic crops, such as rice and taro (Halwart 1994; Yusa and Wada 1999; Martín et al. 2019). Additionally, snails consume various types of aquatic plants and thereby have strong negative effects on the biodiversity of aquatic ecosystems (Lach et al. 2000; Qiu and Kwong 2009; Manara et al. 2022). This species is known to have a rapid growth rate and high fecundity (Yoshida et al. 2016). Therefore, P. canaliculata is treated as an invasive alien species in Southeast and East Asia and is listed among 100 of the world’s worst invasive species (Lowe et al. 2000).
Pomacea canaliculata is expanding worldwide (Yang et al. 2022; Yin et al. 2022). One possible factor contributing to the recent expansion of the distribution range is climate warming (Lei et al. 2017; Hah et al. 2022), although other factors such as water quality and moisture may also be important in determining its distribution (Ito 2002; Qin et al. 2023). Pomacea canaliculata often fails to overwinter in temperate regions (Wada and Matsukura 2007; Yoshida et al. 2009). Several authors have proposed models to predict distribution ranges of snails in response to climate warming (Lei et al. 2017; Yin et al. 2022; Yoshida et al. 2022). Recently, Yoshida et al. (2022) presented a model for assessing the potential risk of overwintering success in P. canaliculata in Japan at a 1 km2 grid scale. These studies will be helpful in planning strategies to avoid future snail expansion.
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In areas where snails can overwinter, the damage caused by snail feeding is largely determined by density, feeding activity (feeding rate), and feeding duration (active period). Although climate warming is likely to increase feeding activity and duration, information on its impact on feeding for this species is limited.
In this study, we examined the effects of temperature on feeding and respiration rates under laboratory conditions and constructed a simple model to estimate annual feeding activity (relative rate) using climatic data recorded at meteorological stations throughout the Japanese Archipelago. Using this model, we estimated the impact of climate warming on feeding potential.
Materials and methods
Materials
Snails used in the study were collected from a paddy field located in Hyogo Prefecture, western Japan (34°49′N, 134°25′E). Mean air temperature within the region is 15.6 °C (1991–2020) recorded by the Automated Meteorological Data Acquisition System (AMeDAS), and agricultural damage by the snails has been reported in the region (Hirose et al. 1999). The snails were transported to the laboratory at Hiroshima University and individually placed in plastic containers with 0.3 L of tap water. The containers were stored in a growth box (LH-60FL12-DT; NK System, Japan) at 15 °C until the experiments. The snails were fed standard food daily (see section: Feeding activity). All measurements were completed within five months following sample collection.
Feeding activity
The effect of temperature on the feeding activity of P. canaliculata was determined by measuring the amount of standard food ingested at different temperatures (10, 15, 20, 25, 30 and 35 °C). Under experimental conditions, P. canaliculata consumes various plant species, including land plants that may not be available in its natural environment. For example, Tsushima et al. (1997) used Chinese cabbage (Brassicacae) as food in their experimental study of carotenoid metabolism. Given our study’s focus on investigating the temperature’s impact on relative rates of feeding, we selected komatsuna (Brassica campestris var. komatsuna, Japanese mustard spinach) as the standard food. This choice was based on the snails’ pronounced preference for this food, its year-round availability, and its suitable shape for measurement (thin and flat leaves).
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We used 10 snails of mature size (shell height: 2.5–3.0 cm) for each temperature in the feeding experiment. Each snail was individually placed in a plastic container containing 0.3 L of water and maintained at 25 °C for 24 h without food. Subsequently, ten containers, each housing one food-deprived snail, were placed in a growth box at each experimental temperature (10, 15, 20, 25, 30 and 35 °C). After 1 d of temperature acclimatisation, each snail was fed a piece of fresh komatsuna of known dry weight (estimated using the dry weight/leaf area (DW/LA) ratio determined for subsamples). Leaf area was measured using image analysis software, imageJ, following previously described methods (Schneider et al. 2012). Dried komatsuna was obtained by placing fresh komatsuna in a drying machine at 80 °C for 2 d. Twenty-four hours after the beginning of the feeding experiment, the leaves were retrieved to measure their dry weight. The feeding rate was obtained by subtracting the actual measured dry weight post-feeding from the pre-feeding weight estimated by DW/LA ratio.
Respiration activity
In addition to feeding activity, we measured respiration rate, an indicator of metabolic activity, in snails. We utilized the same 10 snails of mature size (shell height: 2.5–3.0 cm) for each temperature, as in the feeding experiment. We placed one snail (2.5–3.0 in shell height) in a cylindrical acrylic chamber (diameter, 10 cm; height, 5 cm) filled with oxygen-saturated water (0.27 L). The snail chamber was then placed in a temperature-regulated water bath. The dissolved oxygen in the chamber was monitored every 20 min using a dissolved oxygen meter (Multilab IDS 4010-1W; YSI, Japan). Throughout the measurement process, the water in the acrylic chamber was gently stirred using a stirring bar.
The temperature dependency of the respiration rate was assessed by measuring oxygen consumption at temperatures of 15, 20, 25, 30, and 35 °C. For this measurement, 10 snails were kept in an incubator for 1 d at each experimental temperature for acclimatisation.
Based on the results, we calculated the temperature coefficient Q10.
where v1 and v2 represent the respiration rates (oxygen consumption) at temperatures T1 and T2 (°C) (mg O2 h−1 indiv−1).
Model estimation of relative feeding activity
Based on the experimental results obtained, we constructed a simple model to estimate annual feeding activity (relative rate) using climatic data. As temperature dependence for respiration was similar to that of feeding rate (see results), the response of feeding to temperature in the range of 15–25 °C was approximated by the Q10 equation which is widely used for expressing temperature-respiration curves (Kawasaki et al. 2019; Lei et al. 2022).
The Q′10 value of feeding activity in the temperature range of 15–25 °C was expressed as
where v′1 and v′2 represent a decline in the feeding of snails at T1 and T2 (°C) (mg day−1 indiv−1), respectively. The Q′10 value serves as an index indicating the change in feeding rate.
where IT and I25 denote feeding rates at T (°C) and 25 °C, respectively. We assumed that the feeding rate was constant in the temperature range of 25–35 °C (= I25).
We used daily mean air temperatures for the last 30 years (1991–2020) recorded by the Automated Meteorological Data Acquisition System (AMeDAS) in capitals of 29 prefectures where the invasion of P. canaliculata has been reported (Yoshida et al. 2022). To investigate the impact of climate warming on the feeding potential of snails, we calculated the value assuming a warming condition of 2 °C above the present temperature.
Each value was expressed relative to the value in Hiroshima Prefecture, located in the centre of the snail distribution range.
Statistical analysis
Effects of temperature on feeding activity and respiration rate were analysed using the Tukey–Kramer test in R (version 4.2.1, R Core Team 2022). Statistical significance was set at p < 0.05.
Results
Relationship of respiration and feeding rates to temperature
Pomacea canaliculata did not exhibit any feeding activity at 10 °C (data not shown). The feeding activity increased with increasing temperature in the range 15–25 °C (Tukey-Kramar, p < 0.05) (Fig. 1a). The feeding activity at 25 °C was approximately three times that at 15 °C. There were no significant changes in the feeding activity from 25 to 35 °C (Tukey-Kramar, p > 0.05) (Fig. 1a).
Fig. 1
Effect of temperature on a feeding activity and b respiration rate of P. canaliculata under experimental conditions (n = 10). Feeding activity was determined by measuring the amount of standard food (Japanese mustard spinach, komatsuna) consumed. The respiration rate was determined by O2 consumption rate. Broken line in a indicates the temperature-feeding activity curve expressed by the model. Means with the same letter are not significantly different (Tukey-Kremer p > 0.05)
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The response of respiration to temperature was similar to that of the feeding activity. Respiration rate increased with increasing temperature in the range 15–25 °C (Tukey-Kramar, p < 0.05) (Fig. 1b). The Q10 value for respiration in this temperature range was calculated to be 3.3. No significant differences in the respiration rate were detected in the high temperature range of 25–35 °C (Tukey-Kramar, p > 0.05) (Fig. 1b).
Model estimation of relative feeding activity
According to the model, relative feeding activity varied significantly among the 29 prefectures (Fig. 2a), with the highest activity observed at the southern distribution limit (Okinawa Prefecture) and the lowest at the northern distribution limit (Ibaraki Prefecture). However, the north–south trend was unclear for the other prefectures. The relative feeding value for Okinawa Prefecture was 2.3 times larger than that of Ibaraki Prefecture.
Fig. 2
Annual feeding potential of Pomacea canaliculata in the Japanese Archipelago at a current temperature conditions and b warming condition of + 2 °C estimated by the model. Feeding potentials in the potential distribution areas (Yoshida et al. 2022) are also shown in b. We used daily mean air temperatures at the capitals of 29 prefectures in the recent thirty years (1991–2020) recorded by the Automated Meteorological Data Acquisition System (AMeDAS). Each prefecture value is relative to the annual feeding potential in Hiroshima Prefecture at the present temperature condition
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The model estimated that the total feeding potential (feeding rate) of the current distribution zone would increase by 15.9% under warming conditions (Fig. 2b). The percentage increase was larger at the northern distribution limit of Ibaraki (21.1%) than at the southern distribution limit of Okinawa (9.9%), although the annual feeding potential per individual was estimated to be larger at Okinawa (68.7 g year−1 indv−1) than at Ibaraki (32.8 g year−1 indv−1).
Additionally, we estimated the feeding potential under warming conditions at eight additional sites (prefectures) where the invasion of P. canaliculata has not been reported but falls within the potential distribution areas estimated by Yoshida et al. (2022) (Fig. 2b). The values for these prefectures ranged from 0.8 to 1.2 which were comparable to those in Kyushu and Shikoku at the present temperature condition.
Discussion
Previous studies have demonstrated that P. canaliculata is sensitive to low temperatures, with its distribution is limited by winter cold (Yoshida et al. 2009, 2022) although an ability to enhance the cold hardiness (cold acclimation) has been reported (Wada and Matsukura 2011). In our experiment, the snail exhibited no feeding activity at 10 °C, consistent with findings from a previous study (Seuffert et al. 2010).
Feeding activity sharply increased with temperature within the range of 15–25 °C, but no significant change in the activity was observed at temperatures above 25 °C. Seuffert et al. (2010) reported similar responses in feeding activity to temperature. Feeding time also increased with temperature increase within the range 15–25 °C but decreased at temperatures above 25 °C (Bae et al. 2015; Seuffert and Martín 2017).
Although respiration is not a direct indicator of feeding activity, the two are related. Previous studies conducted on gastropods in intertidal habitats have reported that a portion of the ingested energy and carbon is lost through respiration, with a respiration/feeding ratio range of 0.06–0.57 (Paine 1971; Edwards and Welsh 1982). Increases in the respiration rates of gastropods with increasing temperature have also been reported in previous studies (McMahon and Russell-Hunter 1977; Cheung 1995; Sidorov 2005). However, in our study, no significant differences in respiration rate were detected in the high temperature range of 25–35 °C. This apparent insensitivity of respiration to high temperatures may be partly explained by the absence of aerial respiration in our measurements. Pomacea species are known to obtain oxygen from both water and air (Seuffert and Martín 2010; Mardones et al. 2021). Seuffert and Martín (2010) reported that aerial respiration was increasingly important for snails at temperatures above 25 °C, and the snails could enter into a comatose state if access to air is impeded. In our respiration measurements, snails in the chambers could only perform aquatic respiration; therefore their total respiration rates might have been underestimated especially at high temperatures. Conversely, it is assumed that feeding rate response to temperature in our experiment is similar to that in natural environments because the rate was measured in the experimental condition where the snails had access to air.
Our model suggested that the feeding potential was the highest at the southern distribution limit (Okinawa Prefecture) and the lowest at the northern distribution limit (Ibaraki Prefecture). This appears to be a natural result of the model estimation which is based on the temperature responses of feeding. For other sites, however, the north–south trend was unclear. This may be partly due to the location of the meteorological stations. We used temperature data recorded at meteorological stations near the capital of each prefecture as representative values. Therefore, differences in factors such as elevation and urbanisation (heat island phenomenon) between the locations might obscure the north–south temperature gradient (Table S1).
The north–south gradient in the feeding potential became distinct under the warming condition of 2 °C, with high values at southern Kyushu (Fig. 2b). However, the percentage increase in feeding potential due to warming was higher at the northern distribution limit of Ibaraki (21.1%) than at the southern distribution limit of Okinawa (9.9%). This is largely owing to the fact that warming of 2 °C increased the number of days with mean temperatures above 25 °C in Okinawa (Table S1), whereas the feeding activity remained insensitive to this temperature range. Conversely, the warming extended the feeding span in the northern part of the distribution range (Table S1). This also applies to areas where the invasion of P. canaliculata has not been reported but is within the potential distribution areas (Yoshida et al. 2022). The feeding potential estimated for these areas (0.8–1.2) was comparable to those in Kyushu and Shikoku where serious damage in crops by the snail have been reported at present temperature conditions (Hirai 1987; Yoshida et al. 2022).
Projected future warming differs widely depending on emission scenarios and models. The warming we assumed in our estimation (2 °C) is close to the temperature that is likely to occur in mid-term, 2041–2060 based on the emission scenario SSP2–4.5 (Lee et al. 2021). Since temperatures above 35 °C are harmful to the snail (Seuffert and Martín 2017), further warming may have negative impacts on the snail. Seuffert and Martín (2024) predicted that suitable areas for P. canaliculata would reduce more than they expand globally in the next 80 years, although an increase in distribution beyond the northern areas is also predicted. Since the study area (the Japanese Archipelago) is situated in the northern areas of the distribution range, it is likely that future warming would increase the distribution range and feeding activity of the snail at least for middle-term.
Our model estimated the relative feeding potential, which was determined mainly by temperature. In reality, the effect of feeding on crops is influenced by other factors such as snail density, species, and crop cultivation schedule. Moreover, the activity is affected largely by water temperature (rather than air temperature) which is difficult to be estimated by climate models. However, our results indicate that if this species expands its northern distribution range because of climate warming, it will cause serious damage to crops in newly invaded areas evaluated in this study. Therefore, early detection and extermination of the snails in these areas are crucial in controlling this risk.
Declarations
Conflict of interest
All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.
Ethical approval
The experiments comply with the current laws of the country in which they were performed.
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