Abstract
Western sand lance Ammodytes japonicus exhibits dormancy in summer known as estivation, a distinctive ecology among teleosts. Estivation starts in early summer and continues until winter even water temperature lowered than the initiation threshold. In this study, we examined the onset of estivation in western sand lance reared under two experimental conditions of 14–25 °C-shift or 12 °C-constant. Our observations revealed that estivation in this species can be induced by intrinsic circannual rhythms other than either high or fluctuating water temperatures.
This is a preview of subscription content, log in via an institution to check access.
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request.
References
Amiya N, Matsuda E, Miyazaki Y, Nakano N, Kataoka M, Yamaji T, Amano M, Yoshinaga T (2023) Circadian rhythm and endocrinological control on the swimming and sand burrowing behaviors of Japanese sand lances Ammodytes spp. (Uranoscopiformes, Ammodytidae). Zool Sci. https://doi.org/10.2108/zs230053
Andrews MT (2019) Molecular interactions underpinning the phenotype of hibernation in mammals. J Exp Biol 222:jeb160606
Burke RL, Hussain AA, Storey JM, Storey KB (2002) Freeze tolerance and supercooling ability in the Italian wall lizard, Podarcis sicula, introduced to Long Island, New York. Copeia 3:836–842
Campbell AC, Fraser KP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an Antarctic fish: on ice for winter. PLoS ONE 3:e1743
Connor R, Lauren ER, Speers-Roesch B (2022) Inactivity and the passive slowing effect of cold on resting metabolism as the primary drivers of energy savings in overwintering fishes. J Exp Biol 222:jeb243407
Gao X, Jin C, Llusia D, Li Y (2015) Temperature-induced shifts in hibernation behavior in experimental amphibian populations. Sci Rep 5:11580
Grimpo K, Legler K, Heldmaier G, Exner C (2013) That’s hot: golden spiny mice display torpor even at high ambient temperatures. J Comp Physiol B 183:567–581
Gwinner E (1986) Synchronization of circannual rhythms. In: Bradshaw SD, Burggren W, Heller HC, Ishii S, Langer H, Randall DJ, Neuweiler G (eds) Circannual Rhythms. Zoophysiology, vol 18. Springer, Berlin, pp 49–68
Hand SC (1991) Metabolic dormancy in aquatic invertebrates. In: Castellini MA, Fiévet B, Hand SC, Motais R, Pelster B, Weber RE (eds) Advances in comparative and environmental physiology, vol 8. Springer, Berlin, pp 1–50
Hashimoto H (1991) Population ecology of the Japanese sand eel. J Fac Appl Biol Sci, Hiroshima Univ 30:135–192 ((in Japanese))
Høines ÅS, Bergstad OA (2001) Density of wintering sand eel in the sand recorded by grab catches. Fish Res 49:295–301
Inoue M (2001) Effects of water temperature on feeding and growth of juvenile Kelp Grouper, Epinephelus moara. Bull Mie Pref Fish Res Inst 9:35–38
Kuriyama I, Miyamoto A, Tanaka S, Tsuchihashi Y (2011) Influence of water temperature, dissolved oxygen and salinity on feeding of sevenband grouper Epinephelus septemfasciatus caltured with a self-feeding system. Bull Mie Pref Fish Res Inst 20:23–31
Nakagawa S, Yamaguchi Y (2022) Mammalian hibernation—the survival strategy for harsh seasons with cold and little food by hypometabolism and hypothermia. Jap J Biometeorol 58:51–56 ((in Japanese with English abstract))
Niu Y, Chen Q, Storey KB, Teng L, Li X, Xu T, Zhang H (2022) Physiological ecology of winter hibernation by the high-altitude frog Nanorana parkeri. Physiol Biochem Zool 95:201–211
Pengelley ET, Asmundson SJ, Barnes B, Aloia RC (1976) Relationship of light intensity and photoperiod to circannual rhythmicity in the hibernating ground squirrel, Citellus lateralis. Comp Biochem Physiol 53:273–277
Shima T, Miura M, Onchi H, Yokota M (2014) Demand feeding device-feeding behavior of Masu salmon Oncorhynchus masou and Japanese Whithing Sillago japonica-. Rep Mar Ecol Res Inst 18:67–70
Tomiyama M, Yanagibashi S (2004) Effect of temperature, age class, and growth on induction of in Japanese sandeel (Ammodytes personatus) in Ise Bay, central Japan. Fish Oceanogr 13:81–90
Uye S, Kuwata H, Endo T (1987) Standing stocks and production rates of phytoplankton and planktonic copepods in the Inland Sea of Japan. J Oceanogr 42:421–434
Volkoff H, Ronnestad I (2020) Effects of temperature on feeding and digestive processes in fish. Temperature 7:307–320
Winslade P (1974) Behavioural studies on the lesser sandeel Ammodytes marinus (Raitt) III. The effect of temperature on activity and the environmental control of the annual cycle of activity. J Fish Biol 6:577–586
Wright PJ, Bailey MC (1996) Time of hatching in Ammodytes marinus from Shetland waters and its significance to early growth and survivorship. Mar Biol 126:143–152
Yamada H (2011) Studies on the mechanisms of recruitment determination of Japanese sand lance Ammodytes personatus in Ise Bay. Bull Mie Pref Res 20:1–7
Yamada H, Nishimura A, Tsuchihashi Y, Kuno M (1999) Nutritional condition and reproductive potential of sand lance. Bull Jpn Soc Fish Oceanogr 62:22–29
Acknowledgements
We would like to deeply appreciate the Ikuha-Ura Fishery Cooperative, Awaji Island, Hyogo Prefecture for the great effort to collect experimental fish. Thanks are also due to Drs. Tetsuya Nishikawa, Kaori Uozumi, Minoru Tanda, and Shigeyoshi Okamoto of the Fisheries Technology Institute, Hyogo Prefectural Technology Centre for Agriculture, Forestry and Fisheries, Akashi, Hyogo, Japan for their help to maintain the experimental fish. We wish to thank two anonymous reviewers who gave us helpful comments and advices to improve our manuscript. Mr. Shiro Kagawa of the NHK Enterprises, Japan supported obtaining fish. This study was partially supported by the Japan Society for the Promotion of Science KAKENHI Grants 17K15325 to NA and 19K06195 to TY.
Author information
Authors and Affiliations
Contributions
SH and NA designed the experiments. SH performed the observations and data analysis with technical support from NN and RT. SH, NA, and TY prepared the first draft with input from MA. All authors interpreted the data and co-wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no relevant financial interests that may influence the interpretation of our results.
Ethical approval
All the experiments were conducted in accordance with the guidelines for animal experimentation of Kitasato University.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Hibino, S., Amiya, N., Nakano, N. et al. Onset of estivation in western sand lance Ammodytes japonicus is not solely triggered by elevating water temperature. J Ethol 42, 131–135 (2024). https://doi.org/10.1007/s10164-023-00805-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-023-00805-1