Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Broad scale variation in seagrass benthic macrofaunal assemblages along the coast of Japan


Broad scale studies in seagrass benthic macrofauna are important for future regional marine conservation. We examined spatial variation in the community structure of seagrass-associated benthic macroinvertebrates collected by sediment coring in 2010 at six seagrass sites of Japan covering the latitudinal range of 24°–43°N. Total species richness and ES(50) at site level did not show clear site variations and relationship with latitude. At core level, site variations of mean species richness, ES(50), Simpson diversity and abundance showed inconsistent pattern, but with more cases of statistically significant association with latitude. Variations were generally influenced by the seagrass species, often among subtropical species, among temperate Zostera species, and between Zostera and subtropical species. Finally, the community composition differed significantly across all sites and community similarity decreased rapidly with geographic distance, with only 5% similarity retained at the distance of 400 km. The dissimilarity among sites was higher with the similar distance compared to other types of coastal communities such as rocky intertidal assemblages, which is associated with minor occurrence of species with broad distributional range.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46

  2. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

  3. Asakura A, Suzuki H (1987) Zoogeographical aspects of rocky-intertidal molluscan fauna of the Pacific coasts of Japan. Mar Biol 95:75–81

  4. Barton K (2016) MuMIn: Multi-Model Inference. R package version 1.15.6.

  5. Bell JD, Westoby M (1986) Variation in seagrass height and density over a wide spatial scale: Effects on common fish and decapods. J Exp Mar Bio Ecol 104:275–295

  6. Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) (2014) Community ecology and conservation. Sinauer Associates, Inc, USA

  7. Blanchette CA, Melissa Miner C, Raimondi PT, Lohse D, Heady KEK, Broitman BR (2008) Biogeographical patterns of rocky intertidal communities along the Pacific coast of North America. J Biogeogr 35:1593–1607

  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

  9. Briggs JC (1966) Zoogeography and evolution. Evolution (N Y) 20:282–289

  10. Briggs JC (1995) Global biogeography. Elsevier, Amsterdam

  11. Buzas MA, Culver SJ (1999) Understanding regional species diversity through the log series distribution of occurrences. Divers Distrib 5:187–195

  12. Charney N, Record S (2012) vegetarian: Jost Diversity Measures for Community Data

  13. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial

  14. Clarke A, Lidgard S (2010) Spatial patterns of diversity in the sea: Bryozoan species richness in the North Atlantic. J Anim Ecol 69:799–814

  15. Coates M (1998) A comparison of intertidal assemblages on exposed and sheltered tropical and temperate rocky shores. Glob Ecol Biogeogr Lett 1:115–124

  16. Duarte CM (2002) The future of seagrass meadows. Environ Conserv 29:192–206

  17. Duffy JE, Reynolds PL, Boström C, Coyer JA, Cusson M, Donadi S, Douglass JA, Eklöf JS, Engelen AH, Eriksson BK, Fredriksen S, Gamfeldt L, Gustafsson C, Hoarau G, Hori M, Hovel K, Iken K, Lefcheck JS, Moksnes P-O, Nakaoka M, O’Connor MI, Olsen JL, Richardson JP, Ruesink JL, Sotka EE, Thormar J, Whalen MA, Stachowicz JJ (2015) Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative-experimental approach. Ecol Lett 18:696–705

  18. Ellingsen KE, Gray JS (2002) Spatial patterns of benthic diversity: is there a latitudinal gradient along the Norwegian continental shelf? J Anim Ecol 71:373–389

  19. Fox J, Monette G (1992) Generalized collinearity diagnostics. J Am Stat Assoc 87(417):178–183

  20. Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks.

  21. Fukuta A, Kamimura Y, Hori M, Nakaoka M, Noda T, Yamashita Y, Otake T, Shoji J (2017) Offshore currents explain the discontinuity of a fish community in the seagrass bed along the Japanese archipelago. Fish Ocea 26(1):65–68

  22. Green EP, Short FT (2003) World atlas of seagrasses. In: Green EP, Short FT (eds) University of California Press

  23. Hemminga MA, Duarte CM (2000) Seagrass ecology. Cambridge University Press

  24. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometric J 50(3):346–363

  25. Ishihara MI, Suzuki SN, Nakamura M, Enoki T, Fujiwara A, Hiura T, Hoshino D, Homma K, Hoshizaki K, Ida H, Ishida K, Itoh A, Kaneko T, Kubota K, Kuraji K, Kuramoto S, Makita A, Masaki T, Namikawa K, Niiyama K, Noguchi M, Nomiya H, Ohkubo T, Saito S, Sakai T, Sakimoto M, Sakio H, Shibano H, Sugita H, Suzuki M, Takashima A, Tanaka N, Tashiro N, Tokuchi N, Center Yakushima Forest Environment Conservation, Yoshida T, Yoshida Y (2011) Forest stand structure, composition, and dynamics in 34 sites over Japan. Ecol Res 26:1007–1008

  26. Jost L (2006) Entropy and diversity. Oikos 113:363–375

  27. Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439

  28. Kirkman H, Kirkman JA (2002) The management of seagrasses in Southeast Asia. Bull Mar Sci 71:1379–1390

  29. Kurihara T (2007) Spatiotemporal variations in rocky intertidal malacofauna throughout Japan in the 1970s and 1980s. Mar Biol 153:61–70

  30. Kurihara T, Takami H, Kosuge T, Chiba S, Iseda M, Sasaki T (2011) Area-specific temporal changes of species composition and species-specific range shifts in rocky-shore mollusks associated with warming Kuroshio Current. Mar Biol 158:2095–2107

  31. Larkum WD, Orth RJ, Duarte CM (eds) (2006) Seagrasses: biology, ecology and conservation. Springer, Dordrecht (The Netherlands)

  32. Legendre P, Legendre L (1998) Numerical ecology, 2nd English. Elsevier

  33. Lidgard S (1990) Growth in encrusting cheilostone bryozoan. II. Circum-Atlantic distribution pattern. Palaeobiology 16:304–321

  34. Momota K, Nakaoka M (2017) Influence of different types of sessile epibionts on the community structure of mobile invertebrates in an eelgrass bed. PeerJ 5:e2952

  35. Muraoka D, Shimizu D, Shirafuji N, Tamaki H, Noda T, Hamaguchi M, Fujinami Y, Matsumoto Y (2016) Impact and recovery process of the Great East Japan Earthquake and the following tsunami on Zostera meadows. Nippon Suisan Gakkaishi 82:142

  36. Nakaoka M (2005) Plant-animal interactions in seagrass beds: ongoing and future challenges for understanding population and community dynamics. Popul Ecol 47:167–177

  37. Nakaoka M, Aioi K (2001) Ecology of seagrasses Zostera spp. in Japanese water, a review. Otsuchi Mar Sci 26:7–22

  38. Nakaoka M, Noda T (2004) Special feature: multiple spatial scale approaches in population and community ecology. Popul Ecol 46:103–104

  39. 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 22:379–395

  40. Nakaoka M, Kouchi N, Aioi K (2003) Seasonal dynamics of Zostera caulescens: relative importance of flowering shoots to net production. Aquat Bot 77:277–293

  41. Nakaoka M, Ito N, Yamamoto T, Okuda T, Noda T (2006) Similarity of rocky intertidal assemblages along the Pacific coast of Japan: effects of spatial scales and geographic distance. Ecol Res 21:425–435

  42. Nakaoka M, Hori M, Tanaka Y, Mukai H (2013) Seagrass bed ecosystem. 2008–2012 Summary Report of Monitoring Sites 1000 Coastal Area Survey (Rocky Intertidal, Tidal Flats, Seagrass Beds, Algal Beds). Biodiversity Center of Japan, Nature Conservation Bureau, Ministry of the Environment, Japan, pp 31–47

  43. Nakaoka M, Lee K-S, Huang X, Almonte T, Bujang JS, Kiswara W, Ambo-Rappe R, Yaakub SM, Prabhakaran MP, Abu Hena MK, Hori M, Zhang P, Prathep A, Fortes MD (2014) Regional comparison of the ecosystem services from Seagrass Beds in Asia. In: Nakano S, Yahara T, Nakashizuka T (eds) Integrative observations and assessments. Springer, pp 367–393

  44. Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J Biogeogr 26:867–878

  45. Nishimura S (1974) Biogeographical aspects of the sea shore animals. In: Nishimura S, Yamamoto T (eds) The Sea Shore Life. HOIKUSHA Publishing Co., Ltd, Tokyo, pp 126–131

  46. Nishimura S (ed) (1992) Guide to seashore animals of Japan with color pictures and keys, vol I. HOIKUSHA Publishing Co., Ltd, Osaka

  47. Nishimura S (ed) (1995) Guide to seashore animals of Japan with color pictures and keys, vol II. HOIKUSHA Publishing Co., Ltd, Osaka

  48. Nychka D, Furrer R, Paige J, Sain S (2015) Fields: tools for spatial data. doi:10.5065/D6W957CT. R package version 8.4-1.

  49. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2013) vegan: Community Ecology Package

  50. Okuda T, Noda T, Yamamoto T, Ito N, Nakaoka M (2004) Latitudinal gradient of species diversity: multi-scale variability in rocky intertidal sessile assemblages along the Northwestern Pacific coast. Popul Ecol 46:159–170

  51. Okutani T (ed) (2000) Marine Mollusks in Japan. University of Tokyo Press, Tokyo

  52. 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

  53. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  54. Rex MA, Stuart CT, Hessler RR, Allen JA, Sanders HL, Wilson GDF (1993) Global-scale latitudinal patterns of species diversity in the deep-sea benthos. Nature 365:636–639

  55. Rohde K (1992) Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65:514–527

  56. Rosenberg R, Blomqvist M, Nilsson HC, Cederwall H, Dimming A (2004) Marine quality assessment by use of benthic species-abundance distributions: a proposed new protocol within the European Union Water Framework Directive. Mar Pollut Bull 49:728–739

  57. RStudio Team (2016) RStudio: Integrated Development for R. RStudio, Inc., Boston, MA.

  58. Ruesink J, Stachowicz JJ, Reynolds P, Boström C, Cusson M, Douglass J, Eklöf J, Engelen A. Hori M, Hovel K, Iken K, Moksnes P-O, Nakaoka M, O’Connor M, Olsen J, Sotka E, Whalen M, Duffy E (2017) Form-function relationships in a marine foundation species depend on scale: a shoot to global perspective from a distributed ecological experiment. Oikos

  59. Sanford E (2014) The Biogeography of Marine Communities. In: Bertness MD, Bruno JF, Silliamn BR, Stachowicz JJ (eds) Marine ecology and conservation. Sinauer Associates, Suntherland

  60. Shimabukuro H, Hori M, Yoshimitsu T, Tokunaga N, Inokari T, Sasaki K, Nakaoka M, Kawane M, Yoshida G, Hamaguchi M (2012) Genetic differentiation of annual Zostera marina L. growing in Kagoshima Bay, Kagoshima, Japan based on an analysis using microsatellite markers. Nippon Suisan Gakkaishi 78:204–211

  61. Short FT, Wyllie-Echeverria S (1996) Natural and human-induced disturbance of seagrasses. Environ Conserv 23:17–27

  62. Short F, Carruthers T, Dennison W, Waycott M (2007) Global seagrass distribution and diversity: a bioregional model. J Exp Mar Bio Ecol 350:3–20

  63. Soininen J, Lennon JJ, Hillebrand H, Lennon J (2007) A multivariate analysis of beta diversity across organisms and environments. Ecology 88:2830–2838

  64. Stehli FG, McAlester AL, Helsley CE (1967) Taxonomic diversity of recent bivalves and some implications for geology. Geol Soc Am Bull 78:455–466

  65. Tamaki H, Tokuoka M, Nishijima W, Terawaki T, Okada M (2002) Deterioration of eelgrass, Zostera marina L., meadows by water pollution in Seto Inland Sea, Japan. Mar Pol Bull 44(11):1253–1258

  66. Underwood AJ, Chapman MG, Connell SD (2000) Observations in ecology: you can’t make progress on processes without understanding the patterns. J Exp Mar Bio Ecol 250:97–115

  67. Unsworth RKF, Cullen LC (2010) Recognising the necessity for Indo-Pacific seagrass conservation. Conserv Lett 3:63–73

  68. VanDerWal J, Shoo LP, Johnson CN, Williams SE (2009) Abundance and the environmental niche: environmental suitability estimated from niche models predicts the upper limit of local abundance. Am Nat 174:282–291

  69. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York (ISBN 0-387-95457-0)

  70. Virnstein RW, Nelson WG, Lewis FG, Howard RK (1984) Latitudinal patterns in seagrass epifauna: do patterns exist, and can they be explained? Estuaries 7:310–330

  71. Warwick RM (1997) The ecology of soft- bottom habitats: Matching spatial patterns with dynamic processes. J Exp Mar Bio Ecol 2:216:ix

  72. Watanabe M, Nakaoka M, Mukai H (2005) Seasonal variation in vegetative growth and production of the endemic Japanese seagrass Zostera asiatica: a comparison with sympatric Zostera marina. Bot Mar 48:266–273

  73. 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

  74. Witman JD, Etter RJ, Smith F (2004) The relationship between regional and local species diversity in marine benthic communities: a global perspective. Proc Natl Acad Sci USA 101:15664–15669

  75. WoRMS Editorial Board (2015) World register of marine species. VLIZ. Accessed 20 July 2015. doi:10.14284/170

  76. Yamada K, Hori M, Tanaka Y, Hasegawa N, Nakaoka M (2007) Temporal and spatial macrofaunal community changes along a salinity gradient in seagrass meadows of Akkeshi-ko estuary and Akkeshi Bay, northern Japan. Hydrobiologia 592(1):345–358

  77. Yamada K, Hori M, Tanaka Y, Hasegawa N, Nakaoka M (2010) Contribution of different functional groups to the diet of major predatory fishes at a seagrass meadow in northeastern Japan. Estuar Coast Shelf Sci 86(1):71–82

  78. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. In: Gail M, Krickeberg K, Samet JM, Tsiatis A, Wong W (eds) Spring, New York, NY, p 574

Download references


We are grateful to M. Ito and other Hokkaido University students who provided laboratory assistance. We also thank K. Sudo, for providing additional information regarding environmental data; K. Momota, T. Takuya and M. Hashimoto for support in the identification of amphipod samples; K. Watanabe and F. Cabactulan for technical assistance. The data set was obtained from the Monitoring Sites 1000 Coastal Area Survey by the Ministry of the Environment, Japan. This study is partially supported by the Environment Research and Technology Development Fund (S-9 Integrative Observations and Assessments of Asian Biodiversity, and S-15 Predicting and Assessing Natural Capital and Ecosystem Services (PANCES)) of the Ministry of the Environment, Japan.

Author information

Correspondence to Masahiro Nakaoka.

Electronic supplementary material

About this article

Verify currency and authenticity via CrossMark

Cite this article

Leopardas, V., Hori, M., Mukai, H. et al. Broad scale variation in seagrass benthic macrofaunal assemblages along the coast of Japan. Ecol Res 33, 105–117 (2018).

Download citation


  • Abundance and species diversity
  • Latitudinal gradient
  • Macroecology
  • Regional variation
  • Similarity–distance relationship