Effects of fertiliser applications on survival and recruitment of the apple snail, Pomacea canaliculata (Lamarck)
Introduction
Pressures to increase food production to meet a growing world population and global food demands have led to an increasing use of chemical and organic inputs in agriculture; particularly nitrogen-based chemical fertilisers (FAO, 2008). The global demand for fertilisers is forecast to grow annually by 1.9%, from around 180 million tonnes in 2012 to around 194 million tonnes by 2016 (FAO, 2012). The use of nitrogen in agriculture has been linked to sustaining agricultural productivity (Stewart et al., 2005) and due to limitations in land availability, increasing fertiliser use on existing cropland is considered the most likely path farmers will take to increase production (FAO, 2008). However, high fertiliser use has a number of negative effects on ecosystems, such as altering plant community composition (Vitousek, 1994, Tilman and Lehman, 2001); increasing greenhouse gas (nitrous oxide) emissions; and contaminating groundwater, rivers, lakes and coastal waters, causing eutrophication (Zhu and Chen, 2002, Galloway et al., 2003).
Rice (Oryza sativa L.) is the only major cereal crop that is grown in standing water, thus the use of nitrogen fertilisers during rice production is likely to have major consequences for the aquatic flora and fauna that inhabit rice ecosystems. Many aquatic organisms are susceptible to water-borne chemicals, including fertilisers, and to changes in floodwater chemistry as a result of chemical inputs (Simpson et al., 1994a). However, few studies have examined the effects of nitrogen fertilisers on aquatic organisms in rice ecosystems. Aquatic biomass, in particular green algae, followed by populations of ostracods and chironomid as well as mosquito larvae have been shown to increase following inorganic nitrogen fertiliser applications in rice fields (Simpson et al., 1994a, Simpson et al., 1994b, Sunish and Reuben, 2002, Mutero et al., 2004). Simpson et al. (1994a) indicated that benthic molluscan communities change over the course of rice crop development and that this may be associated with changing water chemistry resulting from fertiliser use. Furthermore, De La Cruz et al. (2001) demonstrated that inorganic nitrogen fertilisers cause mortality of golden apple snails (Pomacea canaliculata [Lamarck]) within a few days of application during land preparation for rice crops.
Applications of nitrogen fertilisers from land preparation to within 14 days of crop establishment, followed by one to two further applications during the rice cropping season, are common practices in rice fields in South-East Asia (Buresh et al., 2007, Palis et al., 2007). The addition of nitrogen to the rice crop initially increases photosynthesis levels and pH and reduces concentrations of dissolved oxygen in the floodwater (Mikkelsen et al., 1978; Simpson et al., 1994a). However, assimilation of nitrogen also increases plant vigor, which benefits the crop, and increases primary productivity in the aquatic environment. This includes new growth of macrophytes and algae. Increasing plant and algal productivity can also benefit aquatic herbivores by increasing food quality and availability (Horgan et al., 2014). For aquatic herbivores, nitrogen fertilisers can therefore have both negative effects through toxicity and by altering the physio-chemical properties of the water, and positive effects by increasing the production (biomass) and quality of aquatic vegetation. Because of the dynamic nature of nitrogen in aquatic agro-ecosystems like rice, including sudden peaks during application and gradual declines post-application, interactions between nitrogen fertilisers and aquatic herbivores will be complex.
The present study examines the effects of fertilisers on the survival of P. canaliculata (Lamarck) in rice systems. P. canaliculata was introduced to much of Asia, including the Philippines, during the 1980s and is considered a major pest of rice during early crop stages, but a beneficial herbivore of weeds during later crop stages (Joshi et al., 2006, Hidaka et al., 2007, Horgan et al., 2014). Previous field experiments by De La Cruz et al. (2001) indicated a reduction in rice damage from snails (missing hills) as a result of basal applications of inorganic nitrogen fertilisers, but the effects of compound fertilisers on snail mortality were largely inconclusive. Furthermore, as plants are affected by fertiliser treatments, i.e., increased growth rates, increased tolerance, and an increased capacity to compensate for damage, field experiments that monitor missing hills or other forms of damage to the crop do not clearly differentiate between the direct effects of snails on the plants and indirect effects mediated through snail mortality. Therefore, we conducted a series of controlled experiments to examine the direct effects of fertilisers on snail mortality. Furthermore, we addressed a two-phase model of snail responses to fertilisers, whereby mortality is increased soon after nitrogen application, but where survival and fitness is eventually enhanced once the excess nitrogen has been assimilated into plant tissues, creating a more favorable environment for herbivore growth and development.
Section snippets
Study species
The P. canaliculata in our experiments were collected from lowland irrigated rice fields at the International Rice Research Institute Experimental Station (henceforth IRRI), Los Baños, Philippines (14°11′N, 121°15′E). Although several Pomacea species have been introduced into Asia (and the Philippines), recent molecular analysis has indicated P. canaliculata as the most common and perhaps only apple snail species present in the Philippines (Hayes et al., 2008). Using published primers (Cooke
Experiment 1 – fertiliser (type) induced mortality
Snail mortality at the end of the experiment was affected by fertiliser type/treatment and snail size (Table 1; Fig. 1), with the highest mortality occurring among adults. Post-hoc analysis revealed a significant difference (P < 0.05) in snail mortality between the control and all four fertiliser types, but no significant difference between the four fertilisers tested (Table 1; Fig. 1). There was higher adult mortality in pots that received either complete fertiliser or urea, but similar levels
Discussion
Our study has shown that nitrogen fertilisers have lethal effects on apple snails. This confirms findings by De La Cruz et al. (2001) that nitrogen pulses in irrigated rice ecosystems initially cause a decrease in P. canaliculata survival. In our laboratory studies we found 10–60% mortality of adult snails when confined in the presence of fertiliser and in the field we found larger declines in snail numbers (18%) in fertilised plots compared to control plots. Complete fertiliser and urea
Acknowledgements
We thank Alberto Naredo, Vincent Vertudes, Reyuel Quintana, Felisa Navor and Marol Recide for their assistance in sampling and measuring snails from the field and for monitoring the field experiment at IRRI farm. We thank two anonymous reviewers for helpful comments that improved the manuscript. This study was funded by the Global Rice Science Partnership (GRiSP). ANP was funded through a training and mobility grant from the Spanish Government and administered through Becas Faro (Faro Global).
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