Abstract
Teleosts are the largest and most diverse group of vertebrates. Although a complex variety of environmental cues influence and time their behaviour and physiology, seasonality is prevalent in many groups and has been particularly studied in salmonids where photoperiodic effects on juvenile development (smoltification) and reproductive physiology (e.g. spawning) are well characterized. This chapter considers evidence for processing of photoperiodic information via local regulation of thyroid hormone availability in the saccus vasculosus, a circumventricular organ located on the ventral side of the brain behind the pituitary gland. As this structure is not present in all photoperiodic teleosts, the chapter also discusses the role of the optic tectum, as this region expresses photoreceptors and melatonin receptors. Unlike mammals, fish (like birds) display decentralized control of photoperiodic responses, as multiple tissues may possess the cellular machinery to respond independently.
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References
Baggerman B (1972) Photoperiodic responses in the stickleback and their control by a daily rhythm of photosensitivity. Gen Comp Endocrinol 3:466–476. https://doi.org/10.1016/0016-6480(72)90177-3
Berge ÅI, Berg A, Barnung T, Hansen T, Fyhn HJ, Stefansson SO (1995) Development of salinity tolerance in underyearling smolts of Atlantic salmon (Salmo salar) reared under different photoperiods. Can J Fish Aquat Sci 52(2):243–251. https://doi.org/10.1139/f95-024
Clark RW, Henderson-Arzapalo A, Sullivan CV (2005) Disparate effects of constant and annually-cycling daylength and water temperature on reproductive maturation of striped bass (Morone saxatilis). Aquaculture 249:497–513. https://doi.org/10.1016/j.aquaculture.2005.04.001
Cowan M, Azpeleta C, López-Olmeda JF (2017) Rhythms in the endocrine system of fish: a review. J Comp Physiol B 187:1057–1089. Springer Berlin Heidelberg. https://doi.org/10.1007/s00360-017-1094-5
Cyr DG, Bromage NR, Duston J, Eales JG (1988) Seasonal patterns in serum levels of thyroid hormones and sex steroids in relation to photoperiod-induced changes in spawning time in rainbow trout, Salmo gairdneri. Gen Comp Endocrinol 69:217–225. https://doi.org/10.1016/0016-6480(88)90008-1
Duston J, Bromage N (1986) Photoperiodic mechanisms and rhythms of reproduction in the female rainbow trout. Fish Physiol Biochem 2:35–51
Duston J, Bromage N (1991) Circannual rhythms of gonadal maturation in female rainbow trout (Oncorhynchus mykiss). J Biol Rhythm 6(1):49–53
Eriksson L-O, Lundqvist H (1982) Cirannual rhythms and photoperiod regulation of growth and smolting in Baltic salmon (Salmo salar L.). Aquaculture 28:113–121
Falcón J, Besseau L, Magnanou E, Herrero MJ, Nagai M, Boeuf G (2011) Melatonin, the time keeper: biosynthesis and effects in fish. Cybium 35(1):3–18. http://www.yies.pref.yamanashi.jp/env-phy/gyouseki/59.pdf\npapers3://publication/uuid/9D60D6E4-9E07-4B47-BD1A-7CC3EFEDEAB5
Falcón J, Bolliet V, Collin JP (1996) Partial characterization of serotonin N-acetyltransferases from northern pike (Esox lucius, L.) pineal organ and retina: effects of temperature. Pflugers Arch Eur J Physiol 432(3):386–393. https://doi.org/10.1007/s004240050149
Fleming MS, Maugars G, Lafont A-G, Rancon J, Fontaine R, Nourizadeh-Lillabadi R, Weltzien F-A, Yebra-Pimentel ES, Dirks R, McCormick SD, Rousseau K, Martin P, Dufour S (2019) Functional divergence of thyrotropin beta-subunit paralogs gives new insights into salmon smoltification metamorphosis. Sci Rep 9(4561):1–15. https://doi.org/10.1038/s41598-019-40019-5
Handeland SO, Imsland AK, Björnsson BT, Stefansson SO (2013) Long-term effects of photoperiod, temperature and their interaction on growth, gill Na+ , K+-ATPase activity, seawater tolerance and plasma growth-hormone levels in Atlantic salmon Salmo salar. J Fish Biol 83:1197–1209. https://doi.org/10.1111/jfb.12215
Huang TS, Ruoff P, Fjelldal PG (2010) Effects of continuous light on daily levels of plasma melatonin and cortisol and expression of clock genes in pineal gland, brain, and liver in Atlantic salmon postsmolts. Chronobiol Int 27(9–10):1715–1734. https://doi.org/10.3109/07420528.2010.521272
IUCN (2019) The IUCN red list of threatened species 2019–2
Jobling M, Johnsen HK, Pettersen GW, Henderson RJ (1995) Effect of temperature on reproductive development in Arctic charr, Salvelinus alpinus (L.). J Therm Biol 20(1):157–165. https://doi.org/10.1016/0306-4565(94)00044-J
Kavaliers M (1982) Seasonal and Circannual rhythms in behavioral thermoregulation and their modifications by Pinealectomy in the white sucker, Catostomus commersoni. J Comp Physiol 146:235–243
Kurokawa T (1990) Influence of the date and body size at smoltification and subsequent growth rate and photoperiod on desmoltification in underyearling masu salmon (Oncorhynchus masou). Aquaculture 86:209–218
Lall SP, Tibbetts SM (2009) Nutrition, feeding, and behavior of fish. Vet Clin North Am - Exot Anim Pract 12(2):361–372. Elsevier Ltd. https://doi.org/10.1016/j.cvex.2009.01.005
Ligo M, Abe T, Kambayashi S, Oikawa K, Masuda T, Mizusawa K, Kitamura S, Azuma T, Takagi Y, Aida K, Yanagisawa T (2007) Lack of circadian regulation of in vitro melatonin release from the pineal organ of salmonid teleosts. Gen Comp Endocrinol 154:91–97. https://doi.org/10.1016/j.ygcen.2007.06.013
Lorgen M, Casadei E, Król E, Douglas A, Birnie MJ, Ebbesson LOE, Nilsen TO, Jordan WC, Jørgensen EH, Dardente H, Hazlerigg DG, Martin SAM (2015) Functional divergence of type 2 Deiodinase Paralogs in the Atlantic Salmon. Curr Biol 25:936–941. https://doi.org/10.1016/j.cub.2015.01.074
Maeda R, Shimo T, Nakane Y, Nakao N, Yoshimura T (2015) Ontogeny of the saccus vasculosus, a seasonal sensor in fish. Endocrinology 156(11):4238–4243. https://doi.org/10.1210/en.2015-1415
McCormick SD, Björnsson BT, Sheridan M, Eilerlson C, Carey JB, O’Dea M (1995) Increased daylength stimulates plasma growth hormone and gill Na+, K+- ATPase in Atlantic salmon (Salmo salar). J Comp Physiol B 165:245–254. https://doi.org/10.1007/BF00367308
McCormick SD, Hansen LP, Quinn TP, Saunders RL (2011a) Movement, migration, and smolting of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55(S1):77–92. https://doi.org/10.1139/d98-011
McCormick SD, Shrimpton JM, Zydlewski JD (2011b) Temperature effects on osmoregulatory physiology of juvenile anadromous fish. Global Warming Cambridge University Press. https://doi.org/10.1017/cbo9780511983375.012
Migaud H, Davie A, Taylor JF (2010) Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. J Fish Biol 76(1):27–68. https://doi.org/10.1111/j.1095-8649.2009.02500.x
Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, Uesaka M, Kimijima M, Hashimoto R, Arai N, Suga T, Kosuge K, Abe T, Maeda R, Senga T, Amiya N, Azuma T, Amano M, Abe H, Yamamoto N, Yoshimura T (2013) The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun 4:1–7. https://doi.org/10.1038/ncomms3108
Nishi K (1979) A daily rhythm in the photosensitive development of the ovary in the bitterling, Rhodeus ocellatus ocellatus. Bull Fac Fish Hokkaido Univ 30(2):109–115
Pankhurst NW, Purser GJ, Van Der Kraak G, Thomas PM, Forteath GNR (1996) Effect of holding temperature on ovulation, egg fertility, plasma levels of reproductive hormones and in vitro ovarian steroidogenesis in the rainbow trout Oncorhynchus mykiss. Aquaculture 146:277–290. https://doi.org/10.1016/S0044-8486(96)01374-9
Prat F, Zanuy S, Bromage N, Carrillo M (1999) Effects of constant short and long photoperiod regimes on the spawning performance and sex steroid levels of female and male sea bass. J Fish Biol 54:125–137
Raible F, Tessmar-raible K (2017) An overview of monthly rhythms and clocks. Front Neurol 8(May):1–14. https://doi.org/10.3389/fneur.2017.00189
Randall CF, Bromage NR (1998) Photoperiodic history determines the reproductive response of rainbow trout to changes in daylength. J Comp Physiol - A Sensory, Neural, Behav Physiol 183(5):651–660. https://doi.org/10.1007/s003590050288
Ravi V, Byrappa V (2018) The divergent genomes of Teleosts. Annu Rev Anim Biosci 6:47–68
Sæther B-S, Johnsen HK, Jobling M (1996) Seasonal changes in food consumption and growth of Arctic charr exposed to either simulated natural or a 12: 12 LD photoperiod at constant water temperature. J Fish Biol 48:1113–1122. https://doi.org/10.1006/jfbi.1996.0114
Sassone-Corsi P, Whitmore D, Foulkes NS (2000) Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404(6773):87–91. https://doi.org/10.1038/35003589
Schugardt C, Kirschbaum F (2004) Control of gonadal maturation and regression by experimental variation of environmental factors in the mormyrid fish, Mormyrus rume proboscirostris. Environ Biol Fish 70:227–233
Shewmon (2007) Environmental manipulation of growth and sexual maturation in yellow perch. Perca flavescens 38(3):383–394
Shimmura T, Nakayama T, Shinomiya A, Fukamachi S, Yasugi M, Watanabe E, Shimo T, Senga T, Nishimura T, Tanaka M, Kamei Y, Naruse K, Yoshimura T (2017) Dynamic plasticity in phototransduction regulates seasonal changes in color perception. Nat Commun 8(1):1–7. Springer US. https://doi.org/10.1038/s41467-017-00432-8
Soivio A, Muona M (1988) Desmoltification of heat-accelerated Baltic Salmon (Salmo salar) in brackish water. Aquaculture 71:89–97
Stefansson SO, Berge ÅI, Gunnarsson GS (1998) Changes in seawater tolerance and gill Na+,K+-ATPase activity during desmoltification in Atlantic salmon kept in freshwater at different temperatures. Aquaculture 168:271–277. https://doi.org/10.1016/S0044-8486(98)00354-8
Strand JET, Hazlerigg D, Jørgensen EH (2018) Photoperiod revisited: is there a critical day length for triggering a complete parr – smolt transformation in Atlantic salmon Salmo salar? J Fish Biol 93:440–448. https://doi.org/10.1111/jfb.13760
Sundararaj BI, Vasal S (2011) Photoperiod and temperature control in the regulation of reproduction in the female catfish Heteropneustes fossilis. J Fish Res Board Canada 33(4):959–973. https://doi.org/10.1139/f76-123
Takeuchi Y, Hada N, Imamura S, Hur S, Bouchekioua S, Takemura A (2015) Existence of a photoinducible phase for ovarian development and photoperiod-related alteration of clock gene expression in a damsel fish. Comp Biochem Physiol Part A 188:32–39. https://doi.org/10.1016/j.cbpa.2015.06.010
Tamai TK, Young LC, Whitmore D (2007) Light signaling to the zebrafish circadian clock by Cryptochrome 1a. PNAS 104(37):14712–14717
Taranger GL, Haux C, Stefansson SO, Hansen T, Bjornsson T (1998) Abrupt changes in photoperiod affect age at maturity, timing of ovulation and plasma testosterone and oestradiol-17 b profiles in Atlantic salmon, Salmo salar. Aquaculture 162:85–98
Thorarensen H, Clarke WC (1989) Smoltification induced by a “skeleton” photoperiod in underyearling coho salmon (Oncorhynchus kisutch). Fish Physiol Biochem 6(1):11–18. https://doi.org/10.1007/BF01875600
West AC, Bechtold D (2015) The cost of circadian desynchrony: evidence, insights and open questions. BioEssays:777–788. https://doi.org/10.1002/bies.201400173
West AC, Wood SH (2018) Science direct seasonal physiology: making the future a thing of the past. Curr Opin Psychol 5:1–8. https://doi.org/10.1016/j.cophys.2018.04.006
Wootton RJ, Smith C (2015) Reproductive biology of teleost fishes. Wiley
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West, A.C., Hazlerigg, D.G., Grenier, G. (2020). Calendar Timing in Teleost Fish. In: Ebling, F.J.P., Piggins, H.D. (eds) Neuroendocrine Clocks and Calendars. Masterclass in Neuroendocrinology, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-030-55643-3_7
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