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Juvenile growth and survival of the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) reared at different constant temperatures
SpringerPlus volume 2, Article number: 312 (2013)
Pomacea canaliculata is a freshwater snail that cultured under certain conditions could provide interesting rewards in research and aquaculture. P. canaliculata is usually reared at 25°C, though the optimal temperature for culturing this species, that balances growth and survival rates, is so far unknown. In this work we present results of growth and survival of cohorts reared in the laboratory at different constant water temperatures (15, 20, 25, 30 and 35°C) during the pre-reproductive period.
Two different groups were recognized among the five treatments: the two lower temperatures (15 and 20°C) that showed no mortality but with very low growth rates and the treatments of 25, 30 and 35°C in which snails grew faster but displayed a reduction in survival as temperature increases. After 10 weeks, the mean shell lengths attained at 30 and 35°C were only 2–3 mm higher than that of the treatment of 25°C and were not statistically different.
Our results support using water temperatures of 25°C for the rearing of cohorts when the objective is to quickly obtain numerous large snails. Temperatures of 15 and 20°C may be appropriate if the aim is to preserve juveniles for long periods with a very low risk of mortality. The results reported here will be useful to the scheduling of laboratory trials intended for basic research, snail control or mass rearing for different applications of this species.
Pomacea canaliculata (Lamarck) is a freshwater snail belonging to the Ampullariidae family, native to subtropical and temperate South America. It naturally distributes from southern Brazil to the south of Buenos Aires Province, where it reaches its southernmost limit in Encadenadas del Oeste basin (Martín et al. 2001). The interest on the basic aspects of the biology and ecology of this species has greatly increased in the past years due to the serious troubles caused to crops and natural wetlands in invaded regions, especially in Southern and Eastern Asia. The introduction of P. canaliculata and other apple snails to new areas needs to be strongly discouraged due to their negative impacts and great invasive potential (Cowie et al. 2009; EFSA 2012). Nevertheless, in their native ranges, in already invaded areas or under rigorously confined conditions, their culture promises interesting rewards in the fields of applied and basic research and aquaculture.
Several studies were intended to adjust the culturing techniques of different species of ampullariids, such as Pomacea patula catemacensis (Baker) (Ruiz-Ramírez et al. 2005), Pomacea paludosa (Say) (Garr et al. 2011; Posch et al. 2012), Pomacea bridgesii (Reeve) (Coelho et al. 2012), Pomacea urceus (Müller) (Ramnarine 2003 2004) and Marisa cornuarietis L. (Aufderheide et al. 2006; Selck et al. 2006). There are some researches in which P. canaliculata cohorts were reared under laboratory conditions, both at room temperature (9-29°C; Estebenet and Cazzaniga 1992) and with controlled temperature (Estebenet and Cazzaniga 1992; Estoy et al. 2002; Martín and Estebenet 2002; Tamburi and Martín 2009). However, the latter were all performed at 25°C, thus there is so far no studies of the response of growth and survival of P. canaliculata to a wide temperature range.
It is widely recognized that several aspects of the life cycle of P. canaliculata, including growth, feeding, crawling, aerial respiration, reproduction and survival, depend on temperature (e.g. Estebenet and Cazzaniga 1992; Estebenet and Martín 2002; Ito 2002; Albrecht et al. 2004; Matsukura and Wada 2007; Seuffert and Martín 2009; Seuffert et al. 2010). For instance, in short duration trials the levels of general activity and feeding reached a peak in the range of 25-32°C (Heiler et al. 2008; Seuffert et al. 2010) but began to decrease above these temperatures with an associated declined of survival (Seuffert and Martín 2010). On the other hand, the activity of P. canaliculata drops rapidly to zero below 15°C (Seuffert et al. 2010). Based on the response of these traits, we hypothesized that temperatures higher than 25°C will probably promote a faster growth though also will reduce survival. The optimal temperature for culturing this species, that maximizes growth and survival rates, is so far unknown although it also depends on the specific aims of the culture. In this work we present results of growth rates and survival of P. canaliculata reared at different constant water temperatures during the pre-reproductive period (ten weeks).
Ten egg masses were collected in February 9th 2012 in El Huascar stream, (36°55′3″ S, 61°35′50″W, Buenos Aires Province, Argentina) and brought to the laboratory where they were kept in a room at 25°C. Most eggs hatched between February 14th and 22nd and the hatchlings from each egg mass were raised for 3–4 weeks in 3 L aquaria. Afterwards, a group of 120 snails was randomly selected (shell length = 5.00 ± 0.046 mm; mean ± standard error) and subgroups of 12 individuals were placed in ten plastic aquaria of 20 L (30 × 35 × 20 cm) that were maintained at five constant water temperatures with electric thermostats (15, 20, 25, 30 and 35°C; two aquaria for each temperature) under 14 h light/day photoperiod. Once a week the aquaria were brushed, the water was totally renewed and snails’ shell length (SL) was measured with a Vernier caliper to the nearest 0.1 mm; the number of live snails per aquarium was also recorded. Throughout the whole trial the snails were fed with fresh lettuce which was maintained at ad libitum levels by supplying it two to three times a week according to consume, in order to avoid bacterial growth and water fouling. No artificial aeration was provided as it affects water quality by resuspending food debris and faeces and since the aquarium dimensions and shape allowed the snails an easy access to breathe air.
For each temperature we calculated the growth rate (mm.week-1) for the phase of linear growth (first four weeks), the mean shell length after four and ten weeks, the percentage of survival (100 × number of live snails / total number of snails) at the end of the experiment and the mean survival time. Differences in these variables among treatments were analyzed with nested ANOVAs, with the aquaria being the nested factor and water temperature the main fixed factor. When homogeneity of variances was rejected by Levene’s test, the dependent variable was log-transformed and re-analyzed. If homoscedasticity was not attained by this procedure, a non-parametric test (Kruskal-Wallis) was performed. Differences among treatments in the coefficients of variation (CV,%) of shell length were compared through Levene’s tests using the individual deviations relative to the median of each treatment (Schultz 1985).
Results and discussion
The growth rate during the first four weeks varied 6.4 fold in the studied temperature range, between a minimum of 0.684 mm.week-1 at 15°C and a maximum of 4.377 mm.week-1 at 30°C (Figure 1). The values estimated for the treatments of 25 and 35°C were 3.958 and 4.264 mm.week-1, respectively. The sizes of the snails after four weeks were significantly different among treatments (F 4, 5 = 111.670; p < 0.0001), being higher for the treatments of 25, 30 and 35°C (t-tests; p < 0.0001 in all cases, after Bonferroni correction for 10 comparisons; Figures 1 and 2); there was no significant component of variance due to the different aquaria (nested factor; F 5, 102 = 1.458; p = 0.210).
After ten weeks, the maximum mean shell length (32.03 mm) was recorded in the treatment of 35°C (Figure 2), being significantly higher than the means recorded with 15 and 20°C (p < 0.0001 in both cases, after Bonferroni correction) but not different from those of 25°C (p = 0.078) and 30°C (p = 0.577). The mean shell lengths for the treatments of 25 and 30°C were 29.24 and 31.14 mm, respectively, and were not significantly different (p = 0.216). Mean survival time differed significantly among treatments (Kruskal-Wallis test: Χ2 = 9.639; p = 0.047) and was negatively correlated with water temperature (Spearman’s ρ = −0.279; p = 0.002). The percentages of survival after ten weeks for the treatments of 15 and 20°C were 100%, whereas for 25, 30 and 35°C values were 95.83, 87.50 and 79.17%, respectively (Figure 2).
On the whole, two different groups were clearly recognized among the five treatments: the two lower temperatures (15 and 20°C) that showed no mortality and very low growth rates and, on the other side, the treatments of 25, 30 and 35°C in which snails grew faster but suffered some mortality. Within the latter group of temperatures, growth rate at 30°C was higher than at 25°C, though the differences were relatively small (0.422 mm.week-1) and not statistically different; also, both mean shell lengths were not different. A higher temperature (35°C) did not increase the growth rate or the mean shell length after the first four weeks. After 10 weeks, the mean lengths attained with 30 and 35°C were only 2–3 mm higher than that of the treatment of 25°C and were not statistically different. These results, together with the lower survival registered with the two warmer temperatures, indicates that there would be no apparent benefit in culturing snails of this species at temperatures of 30°C and above. On the other hand, no snail died after 10 weeks in the treatments of 15 and 20°C though the slow growth recorded with these low temperatures would imply an undesirable long period of rearing.
The lack of a further increase in growth rate in the treatments of highest temperatures was probably related to a decrease in the time spent feeding above 25°C (Seuffert et al. 2010). Similarly, the weight growth rate of Pomacea maculata at 35°C was smaller than that between 20 and 30°C, even though in this case the feeding rate was not affected by water temperature (Gettys et al. 2008).
As time passed, the differences in size among snails of the same treatment got bigger. This was reflected in the increase of the coefficient of variation (CV) of shell length (Table 1). At the beginning of the experiment, the CV was not different among treatments (Levene’s test: F 4, 115 = 0.576, p = 0.681; mean CV: 11.25%, range: 10.3-12.3%), but at week ten it reached values that ranged from 13.3% at 20°C to 22.0% at 25 and 30°C and that were significantly different (Levene’s test: F 4, 105 = 3.365, p = 0.012). Size is sexually dimorphic in P. canaliculata (Estebenet and Martín 2003) but this probably had no influence in this size variation since none of the snails attained maturity during our ten weeks trial; under optimum conditions males and females take at least 13 weeks to mature (Tamburi and Martín 2009). A possible explanation of the differences in size recorded here is the feeding interference between individuals (Estebenet and Martín 2002). If the aim is to obtain homogeneous stocks of snails for experimentation this can be solved by using individual aquaria (Tamburi and Martín 2009) or individual plastic frame enclosures in collective aquaria (Estebenet and Cazzaniga 1998) or by rearing them at low temperatures (15-20°C).
In the present work we found that, as expected, survival and growth showed opposite responses to temperature which indicates that the optimal development of laboratory cohorts of P. canaliculata would occur at intermediate values. Until now, rearing temperatures close to 25°C have been frequently chosen for the design of laboratory experiments (e.g., Estebenet and Cazzaniga 1992; Estoy et al. 2002; Martín and Estebenet 2002; Tamburi and Martín 2009). Our results support using water temperatures of 25°C for the rearing of cohorts when the objective is to quickly obtain numerous large snails. On the other hand, temperatures of 15 and 20°C may be appropriate if the aim is to preserve juveniles for long periods with a very low risk of mortality.
The results reported here will be useful to improve the culturing techniques of P. canaliculata that will help to promote different applications of this species, such as its use as a component of high nitrate content in biological fertilizers (Vetayasuporn 2006) or as food for aquaculture (Bombeo-Tuburan et al. 1995; Lan et al. 2006) and for intensive animal farming (Kaensombath and Ogle 2005). The information obtained here will be also useful to the scheduling of laboratory trials intended for basic research, snail control (Joshi et al. 2008; Song et al. 2011) or mass rearing for ecotoxicological applications (Lo and Hsieh 2000; Coler et al. 2005; Vega et al. 2012).
Pomacea canaliculata is the apple snail that reaches the most extreme latitudes in the world, both in its native range (Martín et al. 2001) and in invaded regions (Ito 2002). In consequence, its response to low temperatures may differ from that of subtropical and tropical Pomacea spp., indicating that is necessary to be cautious in extrapolating the present results to them and also to obtain data on thermal biology at the species or population level.
Albrecht EA, Koch E, Carreño NB, Castro-Vazquez A: Control of seasonal arrest of copulation and spawning in the apple snail Pomacea canaliculata (Prosobranchia: Ampullariidae): differential effects of food availability, water temperature and day length. Veliger 2004, 47: 147-152.
Aufderheide J, Warbritton R, Pounds N, File-Emperador S, Staples C, Caspers N, Forbes V: Effects of husbandry parameters on the life-history traits of the apple snail, Marisa cornuarietis : effects of temperature, photoperiod, and population density. Invertebr Biol 2006, 125: 9-20. 10.1111/j.1744-7410.2006.00035.x
Bombeo-Tuburan I, Fukumoto S, Rodriguez EM: Use of the golden apple snail, cassava, and maize as feeds for the tiger shrimp, Penaeus monodon , in ponds. Aquaculture 1995, 131: 91-100. 10.1016/0044-8486(94)00329-M
Coelho ARA, Calado GJP, Dinis MT: Freshwater snail Pomacea bridgesii (Gastropoda: Ampullariidae), life history traits and aquaculture potential. AACL Bioflux 2012, 5: 161-168.
Coler RA, Coler RR, Felizardo EKG, Watanabe T: Applying weight gain in Pomacea lineata (Spix 1824) (Mollusca: Prosobranchia) as a measure of herbicide toxicity. Braz J Biol 2005, 65: 617-623.
Cowie RH, Dillon RT, Robinson DG, Smith JW: Alien non-marine snails and slugs of priority quarantine importance in the United States: A preliminary risk assessment. Am Malacol Bull 2009, 27: 113-132. 10.4003/006.027.0210
EFSA: Scientific Opinion on the evaluation of the pest risk analysis on Pomacea insularum , the island apple snail, prepared by the Spanish Ministry of Environment and Rural and Marine Affairs. Eur Food Safe Authority J 2012, 10(2552):57. 10.2903/j.efsa.2012.2552
Estebenet AL, Cazzaniga NJ: Growth and demography of Pomacea canaliculata (Gastropoda: Ampullariidae) under laboratory conditions. Malacol Rev 1992, 25: 1-12.
Estebenet AL, Cazzaniga NJ: Sex related differential growth in Pomacea canaliculata (Gastropoda: Ampullariidae). J Mollus Stud 1998, 64: 119-123. 10.1093/mollus/64.1.119
Estebenet AL, Martín PR: Pomacea canaliculata (Gastropoda: Ampullariidae): Life-history traits and their plasticity. Biocell 2002, 26: 83-89.
Estebenet AL, Martín PR: Shell interpopulation variation and its origin in Pomacea canaliculata (Gastropoda: Ampullariidae) from Southern Pampas, Argentina. J Mollus Stud 2003, 69: 301-310. 10.1093/mollus/69.4.301
Estoy GF, Yusa Y, Wada T, Sakurai H, Tsuchida K: Size and age at first copulation and spawning of the apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae). Appl Entomol Zool 2002, 37: 199-206. 10.1303/aez.2002.199
Garr AL, Lopez H, Pierce R, Davis M: The effect of stocking density and diet on the growth and survival of cultured Florida apple snails, Pomacea paludosa . Aquaculture 2011, 311: 139-145. 10.1016/j.aquaculture.2010.11.017
Gettys LA, Haller WT, Mudge CR, Koschnick TJ: Effect of temperature and feeding preference on submerged plants by the island apple snail, Pomacea insularum (d’Orbigny, 1839) (Ampullariidae). Veliger 2008, 50: 248-254.
Heiler KCM, Von Oheimb PV, Ekschmitt K, Albrecht C: Studies on the temperature dependence of activity and on the diurnal activity rhythm of the invasive Pomacea canaliculata (Gastropoda: Ampullariidae). Mollusca 2008, 26: 73-81.
Ito K: Environmental factors influencing overwintering success of the golden apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae), in the northernmost population of Japan. Appl Entomol Zool 2002, 37: 665-661.
Joshi RC, San Martín R, Saez-Navarrete C, Alarcon J, Sainz J, Antolin MM, Martin AR, Sebastian LS: Efficacy of quinoa ( Chenopodium quinoa ) saponins against golden apple snail ( Pomacea canaliculata ) in the Philippines under laboratory conditions. Crop Prot 2008, 27: 553-557. 10.1016/j.cropro.2007.08.010
Kaensombath L, Ogle B: Laboratory-scale ensiling of Golden Apple snails (GAS)(Pomacea spp.). Swedish University of Agricultural Sciences: MSc thesis; 2005. http://www.mekarn.org/msc2003-05/theses05/content/lamp1.pdf
Lan LM, Long DN, Micha JC: The effects of densities and feed types on the production of Macrobrachium rosenbergii (de Man) in the rotational rice–prawn system. Aquac Res 2006, 37: 1297-1304. 10.1111/j.1365-2109.2006.01562.x
Lo CC, Hsieh TT: Acute toxicity to the golden apple snail and estimated bioconcentration potential of triphenylphosphine oxide and series of related compounds. B Environ Contam Tox 2000, 65: 104-111. 10.1007/s001280000101
Martín PR, Estebenet AL: Inter-population variation of life-history traits in Pomacea canaliculata (Gastropoda: Ampullariidae) in Southwestern Buenos Aires Province, Argentina. Malacologia 2002, 44: 153-163.
Martín PR, Estebenet AL, Cazzaniga NJ: Factors affecting the distribution of Pomacea canaliculata (Gastropoda: Ampullariidae) along its southernmost natural limit. Malacologia 2001, 43: 13-23.
Matsukura K, Wada T: Environmental factors affecting the increase in cold hardiness in the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae). Appl Entomol Zool 2007, 42: 533-539. 10.1303/aez.2007.533
Posch H, Garr AL, Pierce R, Davis M: The effect of stocking density on the reproductive output of hatchery-reared Florida apple snails, Pomacea paludosa . Aquaculture 2012, 360–61: 37-40.
Ramnarine IW: Induction of spawning and artificial incubation of eggs in the edible snail Pomacea urceus (Müller). Aquaculture 2003, 215: 163-166. 10.1016/S0044-8486(02)00364-2
Ramnarine IW: Quantitative Protein Requirements of the Edible Snail Pomacea urceus (Muller). J World Aquacult Soc 2004, 35: 253-256. 10.1111/j.1749-7345.2004.tb01082.x
Ruiz-Ramírez R, Espinosa-Chávez F, Martinez-Jeronimo F: Growth and Reproduction of Pomacea patula catemacensis Baker, 1922 (Gastropoda: Ampullariidae) When Fed Calothrix sp. (Cyanobacteria). J World Aquacult Soc 2005, 36: 87-95.
Schultz BB: Levene’s Test for Relative Variation. Syst Biol 1985, 34: 449-456. 10.1093/sysbio/34.4.449
Selck H, Aufderheide J, Pounds N, Staples C, Caspers N, Forbes V: Effects of food type, feeding frequency, and temperature on juvenile survival and growth of Marisa cornuarietis (Mollusca: Gastropoda). Invertebr Biol 2006, 125: 106-116. 10.1111/j.1744-7410.2006.00045.x
Seuffert ME, Martín PR: Influence of temperature, size and sex on aerial respiration of Pomacea canaliculata (Gastropoda: Ampullariidae) from southern Pampas, Argentina. Malacologia 2009, 51: 191-200. 10.4002/040.051.0115
Seuffert ME, Martín PR: Dependence on aerial respiration and its influence on microdistribution in the invasive freshwater snail Pomacea canaliculata (Caenogastropoda, Ampullariidae). Biol Invasions 2010, 12: 1695-1708. 10.1007/s10530-009-9582-5
Seuffert ME, Burela S, Martín PR: Influence of water temperature on the activity of the freshwater snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) at its southernmost limit (Southern Pampas, Argentina). J Therm Biol 2010, 35: 77-84. 10.1016/j.jtherbio.2009.11.003
Song ZJ, Xu XM, Deng WL, Peng SL, Ding LS, Xu HH: A new dimeric iridal triterpenoid from Belamcanda chinensis with significant molluscicide activity. Org Lett 2011, 13: 462-465. 10.1021/ol102796k
Tamburi NE, Martín PR: Reaction norms of size and age at maturity of Pomacea canaliculata (Gastropoda: Ampullariidae) under a gradient of food deprivation. J Mollus Stud 2009, 75: 19-26.
Vega IA, Arribére MA, Almonacid AV, Ribeiro Guevara S, Castro-Vazquez A: Apple snails and their endosymbionts bioconcentrate heavy metals and uranium from contaminated drinking water. Env Sci Poll Res 2012, 19: 3307-3316. 10.1007/s11356-012-0848-6
Vetayasuporn S: Effects of biological and chemical fertilizers on growth and yield of shallot ( Allium cepa var . ascolonicum ) production. J Biol Sci 2006, 6: 82-86.
This work was funded with grants by CONICET (“Consejo Nacional de Investigaciones Científicas y Técnicas”, PIP 112 200901 00473) and UNS (“Universidad Nacional del Sur”, PGI 24B/144 and PGI 24B/185). MES is a postdoctoral fellow in CONICET and PRM is a researcher in CONICET.
The authors declare that they have no competing interests.
MES is the main author, has performed the experiments and wrote the manuscript. PRM has proposed the topic, supervised this work, provided ideas and contributed with the manuscript writing and revision. MES and PRM conceived and designed the study. Both authors have read and approved the final manuscript.
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Seuffert, M.E., Martín, P.R. Juvenile growth and survival of the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) reared at different constant temperatures. SpringerPlus 2, 312 (2013). https://doi.org/10.1186/2193-1801-2-312
- Shell Length
- Freshwater Snail
- Buenos Aires Province
- Apple Snail
- Mass Rear