Characterizing the effects of temperature on behavioral periodicity in golden apple snails (Pomacea canaliculata)
Introduction
Invasive species can have severe impacts on freshwater ecosystems, and their effects on native biodiversity and ecosystem function can be detrimental even in the absence of any other environmental changes (Lodge, 1993). These effects can occur over very short timescales, resulting in abrupt alterations of ecosystems in ways that are unpredictable and/or undesirable (Mooney and Hobbs, 2000).
The golden apple snail, Pomacea canaliculata, is a freshwater snail native to tropical and temperate South America that has become an invasive agricultural pest in Asian countries (Cowie et al., 2006, Halwart, 1994, Hayes et al., 2008, Wada, 2004). The colonization of golden apple snail has increased worldwide, and many countries in tropical, subtropical, and temperate regions are now threatened by the golden apple snail (Baker, 1998, Rawlings et al., 2007, Seuffert and Martín, 2009). With high growth and reproductive rates, polyphagous feeding habits, amphibious respiration, and the ability to aestivate (Cowie, 2002, Estebenet et al., 2006), the golden apple snail is highly adaptable to diverse environmental conditions (e.g., Mendoza et al., 1999). Research on the ecology and behavior of the golden apple snail is therefore urgently needed to minimize its dispersal and control its impact (Ranamukhaarachchi and Wickramasinghe, 2006).
Golden apple snails vary both the type and the periodicity of their behavior in response to environmental conditions. Water temperature, in particular, has a strong effect on their behavior (Costil and Bailey, 1998) as well as on other aspects of their biology such as growth rate, aerial respiration, reproduction, and survival (e.g., Seuffert et al., 2010). For example, golden apple snails have well-developed gills and lungs that allow them to respire both in and out of water (Seuffert et al., 2010); during sustained activity, they generally exhibit a periodic aerial respiration behavior, but the interval between aerial respirations increases at lower water temperatures (Seuffert and Martín, 2009). In addition, in cold conditions (e.g., 10 °C), golden apple snails tend to stay motionless, often while buried in mud (Damborenea, 1996, Seuffert et al., 2010). On the other hand, they tend to adopt active states such as moving, feeding, and ventilating at higher temperatures (e.g., 18 °C).
Evaluating the behavior of continuously and/or long-term monitored organisms is very complex, because the organisms exhibit varied and often non-linear responses to environmental conditions (Bae and Park, 2014). For example, aquatic organisms can exhibit behaviors such as locomotion, foraging, and resting as either direct or time-delayed responses to habitat conditions. It is also known that organisms exhibit continuity in their behavior; an organism that is moving at one moment is likely to keep its moving behavior at the next moment even though it is dependent to the observation time interval and observed environmental conditions. Markov chain can be suitable to compare the changes of behavior maintenance or behavior turnover according to different external conditions (here, different water temperatures). Because Markov chain can quantify the relationship among the behaviors based on present and next-time step, it has been widely applied to animal movement or behavior observed within the same time interval (e.g., Franke et al., 2004, Jonsen et al., 2003). Behavioral data from continuous observations also contain information regarding both the periodicity of behavior and behavioral responses to environmental conditions. Such time-dependent data can be understood using various time-series analysis methods. One such method, spectral analysis, a type of representative frequency domain analysis, has been widely applied to determine the time dependencies, trends, and cycles of animal behaviors such as movement behaviors of German cockroaches (Chon et al., 2004), adaptive search behaviors of Atlantic bluefin tuna (Newlands et al., 2004), feeding and lying behaviors of cattle (Wilson et al., 2005), aggregation behaviors of juvenile blacktip sharks (Heupel and Simpfendorfer, 2005), and behavioral responses of medaka to chemical treatments (Park et al., 2005). Spectral analysis can fit various periodic components to a time series to find periodicities in the time series data.
Until now, there has been not so much attention in the researches on long-term observation (i.e., 2 days in our study) with short-time interval (i.e., 1 min), especially in behavior observation (Bae et al., in press) in contrary to animal movement (e.g., movement tracking using GPS). It can be the starting point to figure out the relationships between behaviors of invasive species and various environmental conditions (e.g., different temperatures) for setting up the management and control methods of invasive species because animal behavior reflects the responses from external conditions. In this study, we examined the behavioral periodicity of golden apple snails at four different water temperatures. We assumed that the periodicity of behavior, the degree of behavioral consistency, and the rate of behavioral turnover from one behavior to another would depend on the water temperature. Given this assumption, we tested two hypotheses. First, the periodicity of motionless behaviors would be longer at lower water temperatures, whereas the periodicity of both motion and motionless behaviors would be shorter at higher water temperatures. Second, behavioral turnover would occur more rapidly at higher water temperatures.
Section snippets
Test organisms and behavioral observations
Golden apple snails (Pomacea canaliculata) were obtained from the Gapyeong Golden Apple Snail Farm (http://www.gpwoolunge.co.kr/), and a stock population was maintained in aquariums with dechlorinated tap water (water temperature: 25 °C ± 1 °C; L16:D8) (Matsukura et al., 2009, Takeichi et al., 2007). The behaviors of test organisms were observed in aquariums (30 cm × 30 cm) filled with water to a depth of 15 cm and with a 3 cm sediment layer at four different temperatures (15 °C, 20 °C, 25 °C, and 30 °C;
Results
The golden apple snails generally spent more time in moving behaviors such as side-crawling and bottom-crawling at higher temperatures, whereas they spent more time in motionless behaviors (i.e., clinging) at lower temperatures (Table 1, Fig. 1, Fig. 2). The time spent in clinging was significantly greater during photophase (15 °C: 42.8%, 20 °C: 20.4%, 25 °C: 19.4%, 30 °C: 5.5% of time spent) than during scotophase (15 °C: 23.3%, 20 °C: 15.8%, 25 °C: 6.8, 30 °C: 1.1%) for all experimental water
Discussion
We examined the behavioral patterns of golden apple snails at four experimental water temperatures. Snails spent more time clinging to the side of the aquarium during the photophase than during the scotophase, regardless of the water temperature (Fig. 2). A higher activity level during the scotophase has been shown by other studies to be a strategy for predator avoidance (e.g., Heiler et al., 2008, Lee and Oh, 2006). Golden apple snails also generally spawn their eggs at night, in part to
Conclusions
We studied how behavioral patterns in golden apple snails depend on the water temperature, a key factor in the ecology of this invasive freshwater pest. In order to assess the differences in behaviors at the four water temperatures studied, we analyzed behavioral consistency, periodicity, and turnover at each temperature. At lower temperatures, golden apple snails tended to maintain their behavior, for both motion and motionless behaviors. At higher temperatures, on the other hand, the snails
Acknowledgments
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (NRF-2013R1A1A2009494) and the Cooperative Research Program for Agricultural Science & Technology Development, RDA, Republic of Korea (No. PJ007420052011). We thank two anonymous reviewers for their constructive comments and help to improve the contents of this paper.
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