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Migratory Behaviors in Masu Salmon (Oncorhynchus Masou) and the Influence of Endocrinological Factors

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Migratory Behaviors in Masu Salmon (Oncorhynchus Masou) and the Influence of Endocrinological Factors Aqua-BioScience Monographs, Vol. 5, No. 2, pp. 29–65 (2012) www.terrapub.co.jp/onlinemonographs/absm/ Migratory Behaviors in Masu Salmon (Oncorhynchus masou) and the Influence of Endocrinological Factors Arimune Munakata Department of Biology Miyagi University of Education Aoba-ku, Sendai, Miyagi 980-0845, Japan e-mail: [email protected] Abstract Received on April 1, 2011 In the freshwater phase of their lifecycle, masu salmon (Oncorhynchus masou) comprise Accepted on September 22, 2011 two different phenotypes. A portion of the juveniles (migratory form) exhibit downstream Online published on November 20, 2012 migratory behavior after smoltification. However, some masu salmon (non-migratory form) such as precociously mature males live continuously in their natal rivers throughout their Keywords lifetime. The coexistence of migratory and non-migratory forms within the species indi- • cortisol cates that this salmon can be effectively used as a model fish to illuminate both inhibitory • downstream migration and stimulatory physiological control mechanisms of migratory behaviors. In masu salmon, • masu salmon it was found that sex steroid hormones inhibit the occurrence of downstream swimming • Oncorhynchus masou behavior, the initial step in seaward migration. Moreover, after the commencement of • Pacific salmon • sex steroid hormone downstream migration, sex steroid hormones induced the upstream swimming and subse- • spawning quent spawning behaviors. These findings indicate that sex steroid hormones influence • testosterone the occurrence of the downstream and upstream swimming behavior in the resulting rheo- • upstream migration taxis fashion (negative and positive, respectively). In contrast to sex steroid hormones, it was also found that cortisol, which is involved substantially in smoltification, stimulates the downstream swimming behavior. These findings indicate that the occurrence of sea- ward migration is controlled competitively by sex steroid hormones (sexual maturation) and smolt-inducing factors such as cortisol, in masu salmon and potentially other Pacific salmon. 1. Introduction and Kobayashi 2010). Most of the non-migratory forms will live continuously in their natal rivers throughout Salmonids (family Salmonidae) consist of four gen- their lives (Fig. 1). Regardless of these life history era, Hucho, Salvelinus, Salmo, and Oncorhynchus types, most salmonids will spawn in freshwater envi- (Neave 1958; Norden 1961; Murata et al. 1993). These ronments, mainly in their natal rivers (Fig. 1) (Quinn salmonids originally inhabited tributaries from high- 2005). From these phenomena, salmonids are consid- through mid-latitude areas in the northern hemisphere ered to be of freshwater (fluvial) fish origin and their (Quinn 2005). It is also known that a large part of migratory behaviors by and large start from the rivers salmonids (in quantity: the number of species and (Fig. 1). biomass) are anadromous, and these fish (i.e., migra- Among the four genera of salmonids, two genera tory form) regularly exhibit downstream migratory Hucho and Salvelinus are considered evolutionally behavior from the rivers to the sea (or lakes), after the ancient groups, based on the phylogenic analyses occurrence of parr to smolt transformation (i.e., (Norden 1961; Murata et al. 1993). Genus Hucho in- smoltification) (Fig. 1). However, many species capa- habit only the northern Eurasia continent and genus ble of anadromy also have phenotypes that are full- Salvelinus inhabit northern Eurasia and the American time residents of freshwater habitats (i.e., non- continent (Quin 2005). On the other hand, genus Salmo migratory forms) and display neither smoltification nor (i.e., Atlantic salmon) and Oncorhynchus (i.e., Pacific downstream migratory behavior to the sea (Munakata salmon), which are considered evolutionally new © 2012 TERRAPUB, Tokyo. All rights reserved. doi:10.5047/absm.2012.00502.0029 30 A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012 River Sea Pink and chum salmon Oncorhynchus (Pacific salmon) Migrants Evolution Masu salmon Non-migrants-m Salmo (Atlantic Salmon) Salvelinus Hucho Fig. 1. Schematic drawing that illustrates the diversity of distance covered by non-migratory and migratory forms for four salmonid genera (shown in the order of the evolutional age). In genus Hucho, most fish live continuously in their natal rivers. In genus Salvelinus and Salmo, some fish mi- grate to the sea after smoltification. In genus Oncorhynchus, most juveniles perform long distance seaward migration for several years. On the other hand, in masu salmon (O. masou), a portion of the fish perform seaward migration for a year after smoltification, while an equivalent portion of them stay in the rivers similar to genera Hucho, Salvelinus, and Salmo. groups, are widely distributed in the rivers and tribu- taries around the north Atlantic and Pacific Oceans, respectively (Groot and Margolis 1991). Fig. 2. Photographs of masu salmon (Oncorhynchus masou). In regard to migratory behaviors, the majority of fish (a) precocious male non-migrants, (b) immature parr non- in the genus Hucho and Salvelinus live continuously migrants, (c) pseudo smolt, (d) smolt migrants, and (e) adult in their natal river systems throughout their lifetime, smolt migrants that migrated back from the sea. as non-migratory forms (Fig. 1). If at all existent, the proportions of the migratory forms are much smaller, and their temporal and spatial ranges of migratory movements are shorter and narrower, respectively, than that mainly inhabits Japanese rivers (i.e., western Pa- those in other salmonids such as Atlantic and Pacific cific Ocean), some yearling (1+) fish live continuously salmon. On the other hand, in Pacific salmon such as in their natal rivers similar to the ancient salmonid pink (O. gorbuscha) and chum (O. keta) salmon, which genera including genus Hucho and Salvelinus are considered evolutionally the newest species, most (Machidori and Kato 1984; Kato 1991; Kiso 1995) juveniles undergo long distance seaward migration (Figs. 1, 3). In masu salmon, however, a portion of the (e.g., from Japanese streams to the Bering Sea) which 1+ juveniles exhibit downstream migratory behavior will continue for several years (Groot and Margolis after the occurrence of smoltification, as do other Pa- 1991). Their temporal and spatial ranges of migratory cific salmon such as pink and chum salmon. In masu movements are considerably longer and broader than salmon, such differentiations in lifecycles regularly in other salmonid species. Based on these wide differ- occur within the same population from the same riv- ences in migratory patterns among salmonid genera ers, especially in the northern regions of their habitat from different evolutional time periods, it is inferred (e.g., northern Honshu through Hokkaido) (Machidori that the proportions of migratory forms increased, and and Kato 1984; Kato 1991; Kiso 1995). subsequently the temporal and spatial ranges of mi- Taking the lifecycles of masu and other salmonids gration became longer and broader, respectively, into consideration, the proportion of non-migratory and through the evolutionary processes (Fig. 1). migratory forms seem to vary, not only among differ- In masu salmon (O. masou) (Fig. 2), a Pacific salmon ent salmonid genera, but also within the same genus doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved. A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012 31 River Sea Feeding Immature SmoltS Dow Spawning Precocious migration male Feeding Non-migrants ( year) Upstream migration Homing migration Fig. 3. Lifecycles of masu salmon (Oncorhynchus masou). In masu salmon, some immature juveniles (migratory form) dis- play the downstream migratory behavior after they have transformed from parr to smolt (smoltification). However, some juveniles (non-migratory form) such as precociously mature males (precocious males) will live continuously in their natal rivers throughout their lifetime. The lifecycle (migratory behavior, seaward migration) of migrants consists of downstream migration, feeding, homing, upstream migration, and spawning. On the other hand, the lifecycle of non-migrants consists of downstream movement within a river, stream residence, upstream movement, and spawning. (e.g., Pacific salmon). Since both the non-migratory precocious males) (Machidori and Kato 1984; Kiso and migratory forms appear within the same species, 1995). On the other hand, most of migratory forms are it is hypothesized that the masu salmon possesses both sexually immature male and female smolts, as observed evolutionarily ancestral (i.e., fluvial) and modern (i.e., in other Pacific salmon (Quinn 2005). These phenom- anadromous) characteristics of migratory behaviors. In ena thus indicated that “sexual maturation” is one of Japanese streams, the non-migratory form of masu the key physiological factors that regulate the occur- salmon is called “yamame” meaning mountain girl, and rence of seaward migration. Furthermore, since most the representative migratory form is called “sakura- of the downstream migrants undergo smoltification masu”, meaning cherry blossoms. Why do only a por- before their seaward migration, it was hypothesized tion of masu salmon juveniles exhibit the ocean-bound that some physiological factors which are closely re- migratory behaviors, whereas the rest do not? lated to the smoltification stimulatory regulate the oc- In this monograph, an overview of the migratory currence of downstream migratory
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