Coexistence of Resident and Anadromous Pond Smelt, Hypomesus Nipponensis, in Lake Ogawara

Coexistence of resident and anadromous pond smelt, Hypomesus nipponensis, in Lake Ogawara

SATOSHIKATAYAMA Graduate School of Agricultural Science, Tohoku University, Sendai, 981-8555, Japan (katayama@bios. tohoku. ac.jp)

SUMMARY. Pond smelt, Hypomesus nipponensis, inhabit fresh, brackish, and oceanic waters, and support substantial commercial fisheries in Japanese lakes. Pond smelt in Lake Ogawara, northern Japan, display a bimodal body length distribution during the spawning season, despite being 0+ fish. Analyses of otolith microstructure and microchemistry were utilized to discriminate anadromous from resident individuals, and revealed that individuals smaller than 60 mm SL were resident, those between 60-80 mm were mixed resident and anadromous, and those larger than 80 mm were anadromous. Intensive research on the reproductive ecology identified spawning localities in the lake and inflowing rivers. Although only anadromous fish spawned in inflowing rivers, spawners in the lake were a mixture of anadromous and resident individuals, suggesting that anadromous and resident spawning groups share a common spawning ground. These fish spawn during almost the same period from mid March to early May. Therefore, reproductive isolation does not appear to occur, and genetic differentiation has not been found through isozyme and mtDNA analyses. The anadromous and resident life history styles appear to be ecological variations within a single population. Lastly, qualitative and quantitative contributions of migratory and non-migratory pond smelts to the next generation were examined and heterogeneity in the life history of this population was discussed.

KEYWORDS: residence, anadromy, pond smelt, alternative life history styles

INTRODUCTION throughout the year and all over the take. 2,3)

Anadromous migration has been studied mainly for salmonids. But various taxonomic groups should be examined to examine the ecology and evolution of fish migration. Pond smelt, Hypomesus nipponensis, is an osmerid species that inhabits fresh, brackish, and oceanic waters throughout the Japanese Archipelago, 1) In this paper, I present evidence of the coexistence of anadromous and resident pond smelt in the Lake Fig.1 Map showing Ogawara population and examine the qualitative and the location of Lake quantitative contributions of migratory and Ogawara. non-migratory pond smelts to the next generation.

POND SMELT AND LAKE OGAWARA

Pond smelt support substantial commercial fisheries in lakes. The production of pond smelt in Lake Ogawara ALTERNATIVE LIFE HISTORY STYLES OF accountsfor a high proportionin Japan. The lake POND SMELT covers an area of 63 km and the northern section is connected to the Pacific Ocean by the 6-km-long Recent ecological research in Lake Ogawara has Takase River (Fig. 1). revealed the co-occurrence of two size groups of pond Lake Ogawara is a brackish lake that has some smelt.4,6) The fish show a bimodal body length inflow of salt water into the lake through the Takase distribution during the spawning season from March River. The southern part of the lake has freshwater to May, in spite of being an annual species. inflow from the Shichinohe and Sadoro Rivers. Lake Analyses of otolith micro-structure and -chemistry Ogawara is almost permanently stratified. The surface were utilized to discriminate anadromous from layer is far less saline, approximately 0.6 in chlorinity, resident individuals, and revealed the coexistence of d

both life history styles within the lake.7,8) Profiles of of females shedding in spawning grounds were Sr:Ca ratios from individuals could be grouped into discriminated through otolith increment analysis. two patterns such as a resident pattern with low Sr:Ca Resident fish were hardly found in an inflowing river, ratios from the core to the edge of the otolith and an in which only anadromous fish spawned, whereas anadromous pattern with abrupt increases of Sr:Ca anadromous and resident fish shared a common ratios (Fig.2). Fish smaller than 60 mm SL were spawning ground in the lake. 15) resident, those between 60-80 mm were mixed Allozymic analysis was performed in order to resident and anadromous, and those larger than 80 mm check for genetic differentiation in the pond smelt in were anadromous. Anadromous individuals were Lake Ogawara. There is no significant difference estimated to first migrate into the sea after 40-82 among year classes, among localities, and between days post-hatch and 14.6-30.9 mm. resident and anadromous pond smelt in the lake and between its inflowing and outflowing rivers. 16) In RFLP analyses, there has been no evidence supporting genetic differentiation found so far, although two mtDNA haplotypes were detected. Therefore, reproductive isolation does not seem to occur between the two life history styles, resulting in an absence of genetic differentiation between them. This suggests that the anadromous and resident life

Fig.2 Sr:Ca ratio (•~ 10-3) profiles from a resident and an history styles are ecological variations in a single anadromous pond smelt otoliths caught in Lake Ogawara on population. April 10, 1991.

Table 1 Comparison of ecological characteristics between Analysis of the Sr:Ca profiles found that there was resident and anadromous pond smelt in Lake Ogawara no difference in body size between resident and (Average •} SD). anadromous individuals during the time of the first seaward migration of pond smelt. Also, field investigations have not yet shown significant differences of body length and age in day between sea-run migrants and residents. 5) In contrast, only the faster growing male Atlantic salmon, Salmo salar9,10) and masu salmon, Oncorhynchus masou.11,12) become precocious and resident in rivers. Oppositely, larger individuals of Arctic charr, Salvelinus alpinus migrate downstream. 13)

INTERGENERATIONAL RELATIONSHIP BETWEEN RESIDENT AND ANADROMOUS FISH

To determine whether the resident and anadromous pond smelts in Lake Ogawara are differentiated POND SMELT MIGRATION: ECOLOGY AND genetically or not, their timing and locality of EVOLTION reproduction and genetic characteristics were examined. Temporal changes in the proportion of Reproductive characteristics were compared between spent fish were compared between anadromous and resident and anadromous fish (Table 1).15)Mean resident groups. Spawning of both groups began in oocyte diameters of mature oocytes were not mid-March and peaked in April 8-12. Although significantly different between them. The eggs of anadromous fish finished spawning slightly earlier resident fish had a significantly greater water content than resident ones, both groups did not differ and a significantly lower dry weight than those of significantly in the period of peak spawning (Table anadromous fish. The relationship between fecundity 1). 14) and SL was discontinuous, with an inflection point at Spawning grounds were formed not only in the lake, 63.8 mm SL, which coincides with the distinction but also in the inflowing rivers. 4,6) Life history styles between large anadromous and small resident 35 spawners. This relationship showed that the large Hypomesus olidus (PALLAS), in Lake Ogawara, Aomori anadromousfemales have a lower fecundity at a given Pref., Japan. 3. Annual cycle of ecological elements in body size than small resident females. These results relation to production of food organisms of the fish. Tohoku J. Agr. Res. 1953; 4: 71-90. suggestthat the anadromous fish have a strategy that 3. Kawasaki T, Ito K. Conservation of the environment and values egg quality more than egg quantity in their intervention by man -A case study on Lake Ogawara. reproductiveallocation. Proceedings of 6th International Conference on the As a result of living in the sea, the anadromous fish Conservation and Management of Lakes Kasumigaura growto a larger size than resident fish. Greater growth 1995; 196-198. of anadromous fish is known for many fishes 4. Katayama S, Okata A. Pond smelt spawning in the inflowing river into Lake Ogawara. Tohoku J. Agri. Res. including the threespine stickleback, Gasterosteus 1995; 45: 87-102. aculeatus,17-19)Clupea pallasii,20)four species of the 5. Katayama S. Ecological study on pond smelt population in genus Salmo, three species of Salvelinus and one Lake Ogawara. PhD Thesis, Tohoku University, Sendai, speciesof Oncorhynchus.21)This has been interpreted, 1996. from an aspect of evolutional biology, to exceed 6. Katayama S, Omori M, Okata A. Selection on the migration cost and lead to increased fitness.22,23) spawning ground of pond smelt spawners in Lake Ogawara. Monthly Kaiyo 1996; 28: 308-314 (in Japanese). However,this may not apply directly to the migratory 7. Katayama S, Omori M, Radtke RL. Analyses of growth and non-migratory pond smelts in Lake Ogawara. processes in the Lake Ogawara pond smelt population Residentspawners have much poorer fecundity due to through the use of daily otolith increments. Env. Biol. their small body sizes, but had approximately 3.4 and Fishes 1998; 52: 313-319. 3.8 greater abundance than the anadromous spawners 8. Katayama S, Radtke RL, Omori M, Shafer DJ. in the 1993 and 1994 year classes, respectively (Fig.3). Coexistence of anadromous and resident life history styles of pond smelt, Hypomesus nipponensis, in Lake Ogawara, This suggests that two life history styles may Japan, as determined by analyses of otolith structure and contribute to the next generation almost evenly in strontium : calcium ratios. Env. Biol. Fishes 2000; 58: quantity. 195-201. Therefore, the use of two life history styles by the 9. Dalley EL, Andrews CW, Green JM. Precocious male pond smelt population in Lake Ogawara supports the Atlantic salmon parr (Salmo salar) in Insular hypothesis that heterogeneity in life history and/or Newfoundland. Can. J. Fish. Aquat. Sci. 1983; 40: 647-652. morphology provides the maximum fitness of a 10. Myers RA. Demographic consequences of precocious populationfacing temporal and geographical changes maturation of Atlantic salmon, Salmo salar. Can. J. Fish. in theirenvironment. 24,25) Aquat. Sci. 1984; 41: 1349-1353. 11. Kubo T. Notes on the phase differentiation and smolt transformation of juvenile masu salmon (Oncorhynchus masou). Scientific Reports of the Hokkaido Salmon Hatchery 1974; 28: 9-26 (in Japanese). 12. Utoh H. Study of the mechanism of differentiation between the stream resident form and the seaward migratory form in masu salmon, Oncorhynchus masou Brevoot, 1, Growth and sexual maturity of precocious masu salmon parr. Bull. Fac. Fish. Hokkaido Univ. 1976; Fig.3 Standard body size distributions of pond smelt caught 26: 321-326. during spawning period, March-May in Lake Ogawara. 13. Strand R, Heggberget T. Growth and sex distribution in an Compositions of two size groups were estimated and their anadromous population of Arctic char in Northern Norway. proportions were denoted above histograms. Trans. Am. Fish. Soc. 1994; 123: 377-384. 14. Katayama S, Sugawara Y, Omori M, Okata A. The ACKNOWLEDGEMENTS maturation and spawning processes of anadromous and resident pond smelt in Lake Ogawara. Ichthyol. Res. 1999; I wish to thank Dr. M.Omori, Tohoku University, for 46: 7-18. 15. Katayama S. Spawning grounds and reproductive traits of helpful suggestions throughout these studies on pond anadromous and resident pond smelt, Hypomesus smelt. nipponensis, in Lake Ogawara, Japan. Fish. Sci. 2001; 67: 401-407. REFERENCES 16. Katayama S, Kijima A, Omori M, Okata A. Genetic differentiation among and within local regions in the pond 1. SaruwatariT, LopezJA, Pietsch TW. A revision of smelt, Hypomesus nipponensis, Tohoku J. Agr. Res. 2001; osmeridgenus Hypomesus Gill (Teleostei:Salmoniforms), 52: 61-77. with the descriptionof a new species from the southern 17. Narver DW. Phenotypic variation in threespine KurillIslands. Species Diversity 1997; 2: 59-82. sticklebacks (Gasterosteus aculeatus) of the Chignik 2. Sato R. Biologicalobservation on the Pond smelt, River System, Alaska. J. Fish. Res. Board Can 1969; 26: 36

405-412 18. Mori S. Two morphological types in the reproductive stock of three-spined stickleback, Gasterosteus aculeatus, in Lake Harutori, Hokkaido Island. Env. Biol. Fishes 1990; 27: 21-31. 19. Snyder RJ. Migration and life histories of the threespine stickleback: evidence for adaptive variation in growth rate between populations. Env. Biol. Fishes 1991; 31: 381-388. 20. Kanno Y. On the life history of herring, Clupea pallasii Cuvier et Valenciennes, in the brackish Lake Notoro, Hokkaido. 2. The relationship between land-locked and migratory herring based on scale analysis. Bull. Fac. Fish. Hokkaido Univ. 1980; 31: 175-183 (in Japanese with English summary). 21. Hutchings JA, Morris DW. The influence of phylogeny, size and behaviour on patterns of covariation in salmonid life histories. Oikos 1985; 45: 118-124. 22. Baker RR. The evolutionary ecology of animal migration. Holmes and Meier, New York. 1978. 23. Gross, MR. Evolution of diadromy in fishes. Am. Fish. Soc. Symp. 1987; 1: 14-25. 24. Levins R. Theory of fitness in a heterogeneous environment. The fitness set and adaptive function.Amer. Nat. 1962; 891: 361-373. 25. Iwasa Y. Why does the polymorphism occur? -fitness set-. In: Ito Y (ed.). Introduction to social ecology. Tokyo Univ. Press. Tokyo. 1982; 87-105 (in Japanese).