Research PaperEffects of glyphosate-based herbicides on survival, development and growth of invasive snail (Pomacea canaliculata)
Graphical abstract
Introduction
Glyphosate-based herbicides are among the world’s best-selling agricultural chemicals now. Since 1970s, it has widely used in over 130 countries on at least 100 crops by blocking an enzyme of 5-enolpyruvylshikimate-3-phosphate synthase that plants need to make amino acids and proteins (Casida and Durkin, 2017, Sánchez et al., 2017). Overall pesticide use steadily increased largely because of the increased use of glyphosate during the late of 2000 s (Stone et al., 2016). Furthermore, its annual global production increased by 33% from 2008 to 2014 achieving 825,000 tons (Grandcoin et al., 2017). Due to its broad-spectrum herbicidal nature and the well-development of resistant crop varieties, glyphosate-based herbicides have reached to one of the most key agricultural chemicals ever; its impact on modern agriculture practices is undisputable (Gilbert, 2013, Annett et al., 2014).
After being applied in farming, forestry, parks, public spaces and gardens, glyphosate might pose a threat to both the environment and human health. The extremely large consumption worldwide of glyphosate is contributing to its detection in various environmental matrices of water, sediment and soil (Aparicio et al., 2013, Ronco et al., 2016). The maximum level of glyphosate in surface water can reach up to 7.6 mg/L (Solomon and Thompson, 2003). Residues of this herbicide have even been found in foodstuffs, drinking water and groundwater, thereby resulting in its positive findings in human urine and breast milk (Krüger et al., 2014, Steinborn et al., 2016).
Even though glyphosate is not carcinogenic (Dost, 2016), recent scientific studies have raised concerns about its safety and there have been calls for glyphosate-containing herbicides to be banned. The debate over the potential risk of glyphosate has become protracted (EPA, 2016, Williams et al., 2016). Glyphosate caused growth inhibition, metabolic depression, reproductive toxicity, and mortality in daphnia, fish and wood frog (Avigliano et al., 2014, Navarro-Martín et al., 2014, Uren Webster et al., 2014). It is interesting to note that agriculturally relevant exposures to glyphosate herbicide benefited growth of wood frog tadpole (Lanctôt et al., 2014) and human breast cancer cells (Thongprakaisang et al., 2013). Therefore, we proposed a hypothesis that whether application of glyphosate would help benefit population growth of problematic alien invasive species.
Invasive species, the golden apple snail Pomacea canaliculata, is reported to gain successful colonization related to its inherent characteristics such as high fecundity, adaptability to harsh environmental conditions and a wide voracious appetite (Joshi and Parera, 2017). It was intentionally introduced to Southeast Asia for aquaculture as a potential food source for local consumption and export, but it has become a major agricultural pest where rice production suffered over the past decades (Byers et al., 2013). A total annual loss by golden apple snails to agriculture was estimated up to $2138 million per annum across three invaded countries of Vietnam, Philippines and Thailand (Nghiem et al., 2013). This species has been in the top 100 of the “World’s Worst Invasive Alien Species” (Luque et al., 2013). Concerns over hazard and control of the spread of golden apple snails have got much attention (Byers et al., 2013, Joshi and Parera, 2017), but little is known about influence of widely used glyphosate herbicide on the survival, development and growth of the invasive species of P. canaliculata. Whether the attacks by glyphosate would help control magnification of the golden apple snail, just as whether glyphosate can facilitate pest outbreaks is questioned; both deserve comprehensive study.
The present work was working on effects of glyphosate-based herbicides on survival, development and growth of the invasive snail P. canaliculata. The report comprises three parts: (i) in the first part an acute toxicity was conducted; (ii) in the second part a chronic assay lasted for 135 days to glyphosate exposures was taken with a focus on physiological response and metabolic rate of the snail; (ii) in the third part of the study, 11 enzymes were adopted to study cellular response of the golden apple snail against glyphosate after chronic exposure.
Section snippets
Chemicals and reagents
Chemical standard for glyphosate (C3H8NO5P) was purchased from Dr. Ehrenstorfer (98%, Germany). The glyphosate stock solution of 1000 mg/L was prepared with Milli-Q water of 18.2 MΩ cm (Millipore, Billerica, MA, USA) and stored in the dark at 4 °C. Reagents for toxicity bioassay were prepared for reconstituted moderately hard water (MHW) using the ISO 6341 recipe (ISO, 2012): 294.0 mg/L calcium chloride dihydrate (CaCl2·2H2O, 96.0%, China), 123.0 mg/L magnesium sulfate heptahydrate (MgSO4·7H2O,
Results and discussion
With the growing application of agrochemicals, their threat to the environment and even human health is receiving more attention. Glyphosate has gained its global favor due to its highly broad-spectrum effectiveness especially in the cultivation of genetically modified crops (Stone et al., 2016; Grandcoin et al., 2017). Available toxicological data not only presented its negative impact on daphnia, fish and wood frog but also showed its positive impact on the growth of tadpole and cells (
Conclusions and limitations
In the present work, effects of glyphosate on survival, development and growth of the invasive snail P. canaliculata were studied. The data suggests that glyphosate can cause acute toxicity to the snail but only at high concentrations unlikely to occur in the natural environment; long-term sublethal exposures (e.g. 20 and 120 mg/L) to glyphosate reduced uptake of food, limited growth performance and altered metabolic profiles of the snails. Glyphosate, being a chemical stressor (FBPase, ACP and
Competing interest
The authors declare no competing financial interest.
Acknowledgements
This work was funded by the Guangdong Natural Science Foundation (Grant No. 2015A030310148), the National Natural Science Foundation of China (Grant No. 31500441, 31770479), and Earthwatch Institute Hong Kong. Funding was also provided by the Science & Technology Planning Project of Guangdong Province, China (2015A020208012, 2015B0909030). A.J. Li appreciated the support from Dr. Kurunthachalam Kannan (Wadsworth Center, New York Department of Health, Albany, USA) during wiring of this paper.
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Yanggui Xu and Adela Jing Li contributed equally to this work.