Abstract
We examined spatial and temporal variations in the species composition of two seagrass species, Zostera marina and Z. caespitosa, in a lagoon facing the Sea of Okhotsk. We also considered how those variations affected habitat quality for motile epifauna, especially for a commercial shrimp. A long-interval comparison between 1996 and 2013 showed that seagrass species composition in the lagoon did not vary, while their relative abundances did. A survey in 2012 revealed that the abundance of Z. caespitosa was affected by the abundance of Z. marina, water depth, and location in the lagoon. Although these seagrass species have similar aboveground morphology, differences in their fine structures were detected. Diversities of motile animals inhabiting the seagrass species were the same. Differences in seagrass utilization were observed when we focused on a commercial shrimp, Pandalus latirostris. This shrimp always preferred higher densities of shoots irrespective of the species and seasonally changed their preference for the number of leaves per shoot. They were therefore more abundant in Z. caespitosa, which had those structural characteristics. The results suggest that the management of shrimp resources could be improved by flexibly changing protected areas in accordance with the dynamics of seagrass distribution in the lagoon.
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References
Angelini C, Altieri AH, Silliman BR, Bertness MD (2011) Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. Bioscience 61:782–789
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193
Bell SS, Brooks RA, Robbins BD, Fonseca MS, Hall MO (2001) Faunal response to fragmentation in seagrass habitats: implications for seagrass conservation. Biol Conserv 100:115–123
Blandon A, Ermgassen P (2014) Quantitative estimate of commercial fish enhancement by seagrass habitat in southern Australia. Estuar Coast Shelf Sci 141:1–8
Boström C, Jackson EL, Simenstad CA (2006) Seagrass landscapes and their effects on associated fauna: a review. Estuar Coast Shelf Sci 68:383–403
Boström C, Pittman SJ, Simenstad C, Kneib RT (2011) Seascape ecology of coastal biogenic habitats: advances, gaps, and challenges. Mar Ecol Prog Ser 427:191–217
Chiba S, Goshima S (2003) Population structure and seasonal growth of the protandrous pandalid shrimp Pandalus latirostris in Notoro Lagoon, Hokkaido. Aquac Sci 51:375–383
Chiba S, Goshima S, Mizushima T (2000) Factors affecting the occurrence of early maturing males in the protandrous pandalid shrimp Pandalus latirostris. Mar Ecol Prog Ser 203:215–224
Chiba S, Yoshino K, Kanaiwa M, Kawajiri T, Goshima S (2013) Maladaptive sex ratio adjustment by a sex-changing shrimp in selective-fishing environments. J Anim Ecol 82:632–641
Christiaen B, Lehrter JC, Goff J, Cebrian J (2016) Functional implications of changes in seagrass species composition in two shallow coastal lagoons. Mar Ecol Prog Ser 557:111–121
Connolly RM, Hindell JS (2006) Review of nekton patterns and ecological processes in seagrass landscapes. Estuar Coast Shelf Sci 68:433–444
Costanza R, d’Arge R, deGroot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, Oneill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260
Duarte CM (2002) The future of seagrass meadows. Environ Conserv 29:192–206
Duffy JE (2006) Biodiversity and the functioning of seagrass ecosystems. Mar Ecol Prog Ser 557:233–250
Eriander L, Infantes E, Olofsson M, Olsen JL, Moksnes PO (2016) Assessing methods for restoration of eelgrass (Zostera marina L.) in a cold temperate region. J Exp Mar Biol Ecol 479:76–88
Gurbisz C, Kemp WM, Sanford LP, Orth RJ (2016) Mechanisms of storm-related loss and resilience in a large submersed plant bed. Estuar Coasts 39:951–966
Hamilton BM, Fairweather PG, McDonald B (2012) One species of seagrass cannot act as a surrogate for others in relation to providing habitat for other taxa. Mar Ecol Prog Ser 456:43–51
Hemminga MA, Duarte CM (2000) Seagrass ecology. Cambridge University Press, New York
Hokkaido Regional Development Bureau (1997) Survey for environmentally sustainable use of coastal area of Hokkaido, Sapporo (in Japanese)
Hori M, Suzuki T, Monthum Y, Srisombat T, Tanaka Y, Nakaoka M, Mukai H (2009) High seagrass diversity and canopy-height increase associated fish diversity and abundance. Mar Biol 156:1447–1458
Horinouchi M (2007) Review of the effects of within-patch scale structural complexity on seagrass fishes. J Exp Mar Biol Ecol 350:111–129
Hyndes GA, Kendrick AJ, MacArthur LD, Stewart E (2003) Differences in the species- and size-composition of fish assemblages in three distinct seagrass habitats with differing plant and meadow structure. Mar Biol 142:1195–1206
Jiang X, Peng J, Zhang LA, Cui CJ, Tian PP, Li XJ, Zhang XM, Gao TX (2013) Distinguishing morphologically similar Zostera species (Z. caespitosa and Z. marina) using microsatellite DNA markers on leaf fragments. Aquat Bot 107:59–62
Kamimura Y, Kasai A, Shoji J (2011) Production and prey source of juvenile black rockfish Sebastes cheni in a seagrass and macroalgal bed in the Seto Inland Sea, Japan: estimation of the economic value of a nursery. Aquat Ecol 45:367–376
Kendrick AJ, Hyndes GA (2003) Patterns in the abundance and size-distribution of syngnathid fishes among habitats in a seagrass-dominated marine environment. Estuar Coast Shelf Sci 57:631–640
Kurata H (1955) The post-embryonic development of the prawn, Pandalus kessleri. Bull Hokkaido Region Fish Res Lab 12:1–15
Larkum A, Orth RJ, Duarte C (2006) Seagrasses: biology, ecology and conservation. Springer, Dordrecht
Lee KS, Park SR, Kim YK (2007) Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. J Exp Mar Biol Ecol 350:144–175
Leopardas V, Uy W, Nakaoka M (2014) Benthic macrofaunal assemblages in multispecific seagrass meadows of the southern Philippines: variation among vegetation dominated by different seagrass species. J Exp Mar Biol Ecol 457:71–80
Malavasi S, Franco A, Riccato F, Valerio C, Torricelli P, Franzoi P (2007) Habitat selection and spatial segregation in three pipefish species. Estuar Coast Shelf Sci 75:143–150
Micheli F, Bishop MJ, Peterson CH, Rivera J (2008) Alteration of seagrass species composition and function over two decades. Ecol Monogr 78:225–244
Mizushima T (1981) Ecology and catch of the prawn, Pandalus kessleri in Zostera beds in Notsuke Bay, Hokkaido, Japan. In: Japan Soc Fish Sci (ed) Seaweed beds. Kouseisha-Kouseikaku, Tokyo, pp. 57–74 (in Japanese)
Mizushima T (1985) Relationship between the density of larva of Pandalus kessleri C. and that of Zostera marina L. J Hokkaido Fish Sci Inst 42:14–25 (in Japanese with English abstract)
Mizushima T, Takaya Y (2003) Hokkai shrimp Pandalus latirostris in Notsuke Bay, eastern Hokkaido. In: Ohtomi J, Watanabe S (eds) Crustacean resources and their diversity. Koseisha-koseikaku, Tokyo, pp 21–30 (in Japanese)
Moore EC, Hovel KA (2010) Relative influence of habitat complexity and proximity to patch edges on seagrass epifaunal communities. Oikos 119:1299–1311
Müller C, Erzini K (2017) Interspecific differences in habitat selection of syngnathids in the Ria Formosa lagoon, Portugal. Estuar Coast Shelf Sci 189:235–242
Nakaoka M (2005) Plant-animal interactions in seagrass beds: ongoing and future challenges for understanding population and community dynamics. Popul Ecol 47:167–177
Nakaoka M, Aioi K (2001) Ecology of seagrasses Zostera spp. (Zosteraceae) in Japanese waters: a review. Otsuchi Mar Sci 26:7–22
Nakaoka M, Toyohara T, Matsumasa M (2001) Seasonal and between-substrate variation in mobile epifaunal community in a multispecific seagrass bed of Otsuchi Bay, Japan. Mar Ecol PSZ N I 22:379–395
Nejrup LB, Pedersen MF (2008) Effects of salinity and water temperature on the ecological performance of Zostera marina. Aquat Bot 88:239–246
Nishino Y, Satoh T (2016) Ecology and hydrography of sea ice and the water column in Lagoon Notoro-ko during frozen period. Eco-Engineering 28:7–14
Orth RJ, Harwell MC, Bailey EM, Bartholomew A, Jawad JT, Lombana AV, Moore KA, Rhode JM, Woods HE (2000) A review of issues in seagrass seed dormancy and germination: implications for conservation and restoration. Mar Ecol Prog Ser 200:277–288
Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996
Pogoreutz C, Kneer D, Litaay M, Asmus H, Ahnelt H (2012) The influence of canopy structure and tidal level on fish assemblages in tropical Southeast Asian seagrass meadows. Estuar Coast Shelf Sci 107:58–68
Ralph PJ, Durako MJ, Enriquez S, Collier CJ, Doblin MA (2007) Impact of light limitation on seagrasses. J Exp Mar Biol Ecol 350:176–193
Ray BR, Johnson MW, Cammarata K, Smee DL (2014) Changes in seagrass species composition in northwestern Gulf of Mexico estuaries: effects on associated seagrass fauna. PLoS One 9:e107751
Robbins BD, Bell SS (2000) Dynamics of a subtidal seagrass landscape: seasonal and annual change in relation to water depth. Ecology 81:1193–1205
Shin H, Choi HK (1998) Taxonomy and distribution of Zostera (Zosteraceae) in eastern Asia, with special reference to Korea. Aquat Bot 60:49–66
Shinomiya Y, Chiba S, Kanamori M, Hashizume S, Yoshino K, Goshima S (2017) Importance of patch size variation for the population persistence of a decapod crustacean in seagrass beds. Mar Ecol Prog Ser 570:157–171
Short FT, Polidoro B, Livingstone SR, Carpenter KE, Bandeira S, Bujang JS, Calumpong HP, Carruthers TJB, Coles RG, Dennison WC, Erftemeijer PLA, Fortes MD, Freeman AS, Jagtap TG, Kamal AM, Kendrick GA, Kenworthy WJ, La Nafie YA, Nasution IM, Orth RJ, Prathep A, Sanciangco JC, van Tussenbroek B, Vergara SG, Waycott M, Zieman JC (2011) Extinction risk assessment of the world’s seagrass species. Biol Conserv 144:1961–1971
Short FT, Kosten S, Morgan PA, Malone S, Moore GE (2016) Impacts of climate change on submerged and emergent wetland plants. Aquat Bot 135:3–17
Stoner AW (1983) Distribution of fishes in seagrass meadows: role of macrophyte biomass and species composition. Fish Bull 81:837–846
Tolan JM, Holt SA, Onuf CP (1997) Distribution and community structure of ichthyoplankton in Laguna Madre seagrass meadows: potential impact of seagrass species change. Estuaries 20:450–464
Toyohara T, Nakaoka M, Aioi K (1999) Population dynamics and reproductive traits of phytal gastropods in seagrass bed in Otsuchi Bay, north-eastern Japan. Mar Ecol PSZN I 20:273–289
Tuya F, Haroun R, Espino F (2014a) Economic assessment of ecosystem services: monetary value of seagrass meadows for coastal fisheries. Ocean Coast Manag 96:181–187
Tuya F, Ribeiro-Leite L, Arto-Cuesta N, Coca J, Haroun R, Espino F (2014b) Decadal changes in the structure of Cymodocea nodosa seagrass meadows: natural vs. human influences. Estuar Coast Shelf Sci 137:41–49
Virnstein RW, Howard RK (1987) Motile epifauna of marine macrophytes in the Indian River Lagoon, Florida. 1. Comparisons among 3 species of seagrasses from adjacent beds. Bull Mar Sci 41:1–12
Watanabe Y, Kawamura T, Yamashita Y (2018) Introduction: the coastal ecosystem complex as a unit of structure and function of biological productivity in coastal areas. Fish Sci. https://doi.org/10.1007/s12562-018-1176-7
Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381
Whitfield AK (2017) The role of seagrass meadows, mangrove forests, salt marshes and reed beds as nursery areas and food sources for fishes in estuaries. Rev Fish Biol Fish 27:75–110
Zimmerman RC, Hill VJ, Gallegos CL (2015) Predicting effects of ocean warming, acidification, and water quality on Chesapeake region eelgrass. Limnol Oceanogr 60:1781–1804
Acknowledgements
We thank T. Kawajiri at the Nishi-Abashiri Fishermen’s Cooperative Association. We also thank K. Nishio at the Okhotsk Marine Research Center and members of the Laboratory of Fisheries Science at Tokyo University of Agriculture for their support in this study. We followed the privacy policy of the Hokkaido Regional Development Bureau when we cited data from their publication in this manuscript. This manuscript was improved by valuable comments of two anonymous reviewers. This work was supported by the Global Environment Research Fund (RF-1102) of the Ministry of the Environment.
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This article is sponsored by the Coastal Ecosystem Complex Project of the Ocean Resource Use Promotion Technology Development Program, the Ministry of Education, Culture, Sports, Science and Technology, Japan.
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Yusa, T., Shoji, J. & Chiba, S. Spatial–temporal variations in the composition of two Zostera species in a seagrass bed: implications for population management of a commercially exploited grass shrimp. Fish Sci 84, 261–273 (2018). https://doi.org/10.1007/s12562-018-1182-9
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DOI: https://doi.org/10.1007/s12562-018-1182-9