Elsevier

Ecological Informatics

Volume 29, Part 2, September 2015, Pages 130-138
Ecological Informatics

Characterizing the effects of temperature on behavioral periodicity in golden apple snails (Pomacea canaliculata)

https://doi.org/10.1016/j.ecoinf.2015.02.004Get rights and content

Highlights

  • We compared the behavioral periodicity of golden apple snails (GAS) at various temperatures.

  • GAS tended to maintain their pre-existing behavior at lower temperatures.

  • Behavioral periodicity was shorter at higher temperatures.

  • A combination of DCA and spectral analysis was able to differentiate response behaviors between different temperatures.

  • Behavioral turnover was characterized using cross-spectral analysis and Markov chain analysis.

Abstract

The golden apple snail (Pomacea canaliculata), an invasive freshwater species in Asia, has become a serious agricultural pest. Water temperature is one of the most important environmental factors influencing the survival, growth rate, reproduction and behavior of freshwater snails. For this reason, the behavioral periodicity of golden apple snails was examined at different water temperatures (15 °C, 20 °C, 25 °C, and 30 °C). We classified the snails' behaviors into 12 pre-defined categories each minute for 2 days at each temperature. Five dominant behavioral categories (clinging to the side of the aquarium [clinging], clinging with sprawling out its antennae [clinging-NM], crawling on the bottom of the aquarium, crawling on the side of the aquarium and feeding) were selected for further analyses. Spectral analysis and cross-spectral analysis were applied to determine the periodicity of these behaviors. Snails spent less time in moving during photophase than scotophase at all temperatures. Behavioral periodicity was much longer at lower temperatures, for both motion and motionless behaviors except clinging-NM. Detrended correspondence analysis based on periodogram values clearly characterized the differences in behavior at the various temperatures. Behavioral turnover, assessed by cross-spectral analysis, was faster at higher temperatures, and Markov chain analysis supported this result by finding a lower probability of maintaining the current behavior at higher temperatures.

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.

References (55)

  • M.J. Bae et al.

    Modeling behavior control of golden apple snails at different temperatures

    (2014)
  • G.H. Baker

    The golden apple snail, Pomacea canaliculata (Lamarck) (Mollusca: Ampullariidae), a potential invader of fresh water habitats in Australia

  • R. Best et al.

    Overview of movement analysis and gait features

  • F. Blayo et al.

    Data analysis: how to compare Kohonen neural networks to other techniques?

  • G.C. Carter et al.

    A coherence and crossspectral estimation program

  • W.I. Choi et al.

    Geographical variation in the population dynamics of Thecodiplosis japonensis: causes and effects on spatial synchrony

    Popul. Ecol.

    (2011)
  • T.-S. Chon et al.

    Implementation of computational methods to pattern recognition of movement behavior of Blattella germanica (Blattaria: Blattellidae) treated with Ca2 + signal inducing chemicals

    Appl. Entomol. Zool.

    (2004)
  • K. Costil et al.

    Influence of water temperature on the activity of Planorbarius corneus (Pulmonata, Planorbidae)

    Malacologia

    (1998)
  • R.H. Cowie

    Apple snails (Ampullariidae) as agricultural pests: their biology, impacts and management

  • R.H. Cowie et al.

    What are apple snails? Confused taxonomy and some preliminary resolution

  • M.C. Damborenea

    Patrones de distribución y abundancia de Temnocephala iheringi (Platyhelminthes, Temnocephalidae) en una población de Pomacea canaliculata (Mollusca: Ampullariidae)

    Gayana, Zool.

    (1996)
  • A.L. Estebenet et al.

    Conchological variation in Pomacea canaliculata and other South American Ampullariidae (Caenogastropoda, Architaenioglossa)

    Biocell

    (2006)
  • R.P. Francesconia et al.

    Effects of environmental temperature on the circadian periodicity of hepatic enzymes in mice

    J. Interdiscipl. Cycle

    (1970)
  • N.F. Guler et al.

    Classification of EMG signals using PCA and FFT

    J. Med. Syst.

    (2005)
  • M. Halwart

    The golden apple snail Pomacea canaliculata in Asian rice farming systems: present impact and future threat

    Int. J. Pest Manag.

    (1994)
  • K.A. Hayes et al.

    Out of South America: multiple origins of non-native apple snails in Asia

    Divers. Distrib.

    (2008)
  • K.C.M. Heiler et al.

    Studies on the temperature dependence of activity and on the diurnal activity rhythm of the invasive Pomacea canaliculata (Gastropoda: Ampullariidae)

    Mollusca

    (2008)
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