Corresponding author: Alberto Romero-Blanco ( alberto.romerob@hotmail.com ) Academic editor: Jaimie T.A. Dick
© 2019 Alberto Romero-Blanco, Álvaro Alonso.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Romero-Blanco A, Alonso Á (2019) Tolerance assessment of the aquatic invasive snail Potamopyrgus antipodarum to different post-dispersive conditions: implications for its invasive success. NeoBiota 44: 57-73. https://doi.org/10.3897/neobiota.44.31840
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The New Zealand mudsnail (NZMS) Potamopyrgus antipodarum (Gray, 1843) (Tateidae, Mollusca) is a successful invasive species able to alter the functioning of the invaded ecosystems. However, to arrive and establish in new aquatic ecosystems, this snail must survive to the overland translocation through aerial exposure and must tolerate the new physical and chemical conditions of the recipient ecosystem. In this study, we simulated different conditions for the NZMS invasion by combining two air exposure treatments (0 and 20 h) with different physical and chemical conditions of the rehydration water (low and normal water temperatures and normal and high water conductivities). Mortality, behavior and neonate production were compared across treatments. Air exposure caused a high percentage of mortality but survivors tolerated the subsequent abiotic conditions. Low temperatures and high conductivities altered the behavior of adult snails, increasing significantly their reaction time (i.e. time to start normal movement). This may have negative consequences for the survival of this species under natural conditions. Finally, these conditions did not affect significantly the production of neonates. These results supported that the surviving NZMS to a brief period of air exposure possess the ability to acclimate to contrasting abiotic conditions with a potential establishment of new populations and that survivors can reproduce in different abiotic conditions after an air exposure period.
Air exposure, conductivity, mortality, neonate production, New Zealand mudsnail, temperature
Biological invasions are considered one of the main forms of global change (
Exotic invasive freshwater mollusks represent a threat to the functioning of the invaded ecosystems and to native species (
The New Zealand mudsnail (NZMS), Potamopyrgus antipodarum (Gray, 1843), is a prosobranch native of New Zealand and an invasive species in many aquatic ecosystems around the world (
The impacts caused on invaded ecosystems by NZMS are mostly due to its elevated population density. For example,
The NZMS may tolerate a wide range of physical and chemical conditions. Some authors (
The aim of this study was to assess the effect of a period of air desiccation (= aerial passive translocation) and two subsequent physical and chemical factors (temperature and conductivity) on the mortality, behavior and reproduction of Potamopyrgus antipodarum. We hypothesized that the period of air desiccation would decrease the ability of this snail to tolerate the subsequent abiotic conditions. Therefore, the mortality, behavior and reproduction of the NZMS would be affected negatively. This study can provide new data about what environmental conditions the NZMS needs to establish and multiply successfully in recipient ecosystems with different properties than those of the original ecosystem.
Animals for this experiment were collected from a laboratory population kept in two 60-l glass aquaria with control water (moderately hard USEPA: 96 mg NaHCO3, 60 mg CaSO4*2H2O, 4 mg KCl, 122.2 mg MgSO4*7H2O/l of deionized water), enriched with calcium carbonate (10 mg de CaCO3/l of deionized water) (
Six treatments were established (Table
Physical and chemical properties of desiccation treatments and their respective controls. In the treatment code “D” means “desiccation” and “C” means “control” (not subjected to desiccation); the number indicates target water temperature and “cond” indicates high conductivity. C18: normal temperature and normal conductivity control; D18: desiccation treatment with normal temperature and normal conductivity; C10: low temperature and normal conductivity control; D10: desiccation treatment with low temperature and normal conductivity; C-cond18: high conductivity and normal temperature control; D-cond18: desiccation treatment with high conductivity and normal temperature.
Treatment code | Desiccation period (hours) | Water temperature (°C) | Conductivity (μS/cm) |
---|---|---|---|
C18 | 0 | 18 | 300 |
D18 | 20 | 18 | 300 |
C10 | 0 | 10 | 300 |
D10 | 20 | 10 | 300 |
C-cond18 | 0 | 18 | 3000 |
D-cond18 | 20 | 18 | 3000 |
Two climatic chambers (ANSONIC®VAC0732) were used to attain the target temperatures (18 °C and 10 °C) (Table
After the air exposure period, snails were translocated to USEPA water with the physical and chemical properties showed in Table
Measures of conductivity, dissolved oxygen and temperature of water were monitored every 1–2 weeks for 50 days by randomly selecting three glass vessels of each desiccation treatment and each control. A digital conductivimeter (TDS&EC meter, GHB) was used to measure the water temperature and conductivity and a portable oxymeter (OXI 45+, CRISON Instruments) to measure the dissolved oxygen concentration. The air temperature and the relative humidity of climatic chambers were measured every 3 hours using two climate recorders (LOG32, DOSTMANN electronic GmbH, Germany).
Selected endpoints were three parameters related with animal fitness (Table
Summary of the analyzed parameters, the variables of each parameter and the statistical analysis applied.
Parameters | Variables | Comparisons | Statistical analysis |
---|---|---|---|
Mortality | Cumulative percentage of dead adults at day 50 after rehydration | Controls | Kruskal-Wallis test |
Desiccation treatments – Controls | Mann-Whitney U tests | ||
Desiccation treatments | One-way ANOVA | ||
Behavior | Reaction time | – | Mixed ANOVA and post hoc test (Student t pairwise with Bonferroni correction) |
Cumulative number of immobile adults at day 50 after rehydration | Desiccation treatments – Controls | Mann-Whitney U tests | |
Desiccation treatments | Kruskal-Wallis test | ||
Reproduction | Total number of neonates per live adult at day 7 after rehydration | Desiccation treatments – Controls | Mann-Whitney U tests |
Desiccation treatments | Kruskal-Wallis test | ||
Cumulative number of total, dead and live neonates at day 50 after rehydration | Desiccation treatments – Controls | Mann-Whitney U tests | |
Desiccation treatments | Kruskal-Wallis test |
For each variable based on the cumulative number, two comparisons were made: the three controls were compared with their respective desiccation treatments through three Mann-Whitney U tests and desiccation treatments were compared among them through a Kruskal Wallis test or through a one-way ANOVA. Table
Three kinds of comparisons were performed to study the influence of treatments (desiccation treatments and controls) on the cumulative percentage of mortality of adults (Table
A mixed ANOVA was performed to study the influence of time and treatments (desiccation treatments and controls) on the reaction time of the NZMS between 8–50 days after rehydration (Table
The effect of treatments (desiccation treatments and controls) on the total number of neonates at 7 days after rehydration was studied through the ratio between the total number of neonates and the number of live adults of each replicate. Differences in the total number of neonates between the desiccation treatments and their controls were studied through the Mann-Whitney U test (Table
To decrease type I errors in multiple testing, a p-value of 0.01 was chosen. Surviving individuals of the same replicates were averaged during their individualization to avoid pseudoreplication (Fig.
The data underpinning the analysis reported in this paper are deposited at Figshare, https://doi.org/10.6084/m9.figshare.7708052.v1
Overall, values of dissolved oxygen were relatively high in all treatments (> 8.5 mg O2/l; n = 12 measures for each treatment), air temperature (mean ± SD) in climatic chambers was 17.6 ± 2.04 °C at normal temperature and 11 ± 0.73 °C at low temperature (n = 389 measures in each climatic chamber) and the mean water conductivity (± SD) was 2811.5 ± 177.1 μS/cm in the treatments with high conductivity and 303.4 ± 43.7 μS/cm in the treatments with normal conductivity (n = 15 measures for each treatment).
Only the 16.1% of total snails of the desiccation treatments survived after the period of exposure to air at 7 days of rehydration. Cumulative percentage of mortality at day 50 after rehydration was significantly higher in the desiccation treatments than in their respective controls (p < 0.01; Mann-Whitney U test). By contrast, differences in the cumulative percentage of mortality were non-significant between desiccation treatments (F(2,18) = 0.68, p = 0.52, η2 = 0.07 [effect size]; ANOVA) (Fig.
Mean (± SD) of the cumulative percentage of mortality in each desiccation treatment at day 50 after rehydration (n = 15 observations). No significant differences were found between the desiccation treatments (p > 0.01; ANOVA).
The influence of time and treatments on the reaction time is shown in Figure
Mean reaction time (in seconds) of individuals of each treatment for each observation time between 8 and 50 days after rehydration (n = 11 observations). SD has been removed for clarity. Time affected significantly the reaction time (p < 0.05; mixed ANOVA). The interaction between time and treatments did not caused significant differences (p > 0.05; mixed ANOVA). Letters in right indicate significant differences in reaction time between treatments (p < 0.001; Student t pairwise with Bonferroni correction).
Summary of results of mixed ANOVA assessing the influence of time and treatments on reaction time.a
Source of variation | Degrees of freedomb | F | p | Effect size |
---|---|---|---|---|
Within subject | ||||
Time | 5.8/163.4 | 2.82 | 0.010 | 0.07 |
Time × Treatment | 29.2/163.4 | 1.14 | 0.300 | 0.14 |
Between subjects | ||||
Treatment | 5/28 | 9.71 | <0.001 | 0.27 |
On the other hand, no significant differences were found neither in the cumulative number of immobile individuals between controls and their respective desiccation treatments (p > 0.01 in all cases; Mann-Whitney U test) nor between desiccation treatments (χ2 = 1.24, p = 0.54; Kruskal-Wallis) (data not shown).
Figure
Mean (+ SD) of the total number of produced neonates per live adult in each treatment at 7 days after rehydration (n = 1 observation). Numbers indicate live adults of each treatment. No significant differences were found between desiccation treatments nor between controls and desiccation treatments (p > 0.01; Kruskal-Wallis and Mann-Whitney U test).
Figure
Mean (+ SD) of the cumulative number of total neonates (A), dead neonates (B) and live neonates (C) registered at day 50 after rehydration (n = 6 observations). No significant differences were found between treatments (p > 0.01; Mann-Whitney U test and Kruskal-Wallis test). Mean (SD has been removed for clarity) of the cumulative number per observation time of total neonates (D), dead neonates (E) and live neonates (F) registered between 8 and 50 days after rehydration (n = 6 observations).
This study confirmed that the NZMS is able to survive and reproduce under contrasting physical and chemical conditions after a short-term desiccation period. These conditions can be found in new regions where the NZMS can arrive after a brief period of exposure to air. We found a higher mortality than expected after a short air exposure period. For instance,
A higher number of individuals died in the desiccation treatments as compared to controls. This result confirmed our initial hypothesis and it coincides with those of other studies (
Treatments affected the NZMS behavior in different ways. The high conductivity increased the reaction time. The desiccation process had little influence in this regard. Thus, high conductivity could have negative effects on the acclimatization of the mudsnail to the recipient ecosystems, because this effect may make access to resources difficult and impair the escape from potential predators. Low temperatures also caused a significant increase in the reaction time. Moreover, other authors have already confirmed that low temperatures affect negatively other life history traits, such as reproduction, in this mollusk (
Regarding reproduction, we found that neonates tolerated the new environmental conditions (temperature and conductivity) after rehydration. Neither high conductivities nor low temperatures reduced the number of neonates, in contrast to other authors who reported that low temperatures slow down the NZMS embryonic development and production (
Neonates showed a wide tolerance to temperatures and conductivities. Embryos are protected against air exposure since they are housed in a brood pouch carried by adult females until they are fully formed and functional (
The invasive success of the NZMS resides in various functional traits shared with other invasive species, such as fast growth rate, high fecundity rate, early sexual maturity, asexual reproduction, a tolerance to wide ranges of abiotic conditions, and a high phenotypic plasticity, among others (
This research was funded by Universidad de Alcalá (CCG2016/EXP-054) and by the IMPLANTIN project (GCL2015-65346-R) of the Ministerio de Economía, Industria y Competitividad of Spain. We want to extend our sincere gratitude to Alberto Jiménez Valverde for his advice on the statistical analysis section. We give special thanks to Pilar Castro, Luis Mariano González and Elizabeth Rivero for suggesting corrections and improvements for the English usage for this manuscript.