Abstract
Species of the free-burrowing amphipod genus, Urothoe, are common on open sandy beaches. On intertidal sandflats, some species are associated with burrows or tubes of large infauna. How this link is formed and persisting under sheltered conditions was examined. On an intertidal sandflat in mid-western Kyushu, Japan, U. carda co-occurred with the deep burrow-dwelling callianassid shrimp, Nihonotrypaea harmandi, along a 300-m transect between tide marks. Amphipods resided in the surface 5-cm sediment outside shrimp burrows, as confirmed by sediment coring and burrow casting. In summers 1980 and 1981, the shrimp and amphipod populations were confined to the upper shore at mean densities of 182 and 701 inds m−2, respectively. In winter to spring, when the sediment surface mixing was caused by seasonal wind-induced waves, the amphipod but not the shrimp expanded down to the lowest shore. Later, by 1983, the shrimp increased mean density by 2.5 times and now also ranged to the lowest shore. In the summers of 1984, 2010, and 2015, the amphipod expanded to the lowest shore as well, with small variations in population size. Three marked changes in substrate properties were associated with shrimp inhabitation: thicker oxidized layer (proxy for oxygenated layer) in the sediment column; looser surface sediment, as evaluated with vane shear strength; and coarser and better-sorted surface sediment with less mud content. At least the former two changes were attributable to shrimp bioturbation, which could provide the amphipod with more permeable and softer substrates, leading to the formation of facultative commensalism.
Similar content being viewed by others
References
Aller RC, Dodge RE (1974) Animal-sediment relations in a tropical lagoon: Discovery Bay, Jamaica. J Mar Res 32:209–232
Amos CL, Van Wagoner NA, Daborn GR (1988) The influence of subaerial exposure on the bulk properties of fine-grained intertidal sediment from Minas Basin, Bay of Fundy. Estuar Coast Shelf Sci 27(1):1–13. https://doi.org/10.1016/0272-7714(88)90028-5
Bally R (1983) Intertidal zonation on sandy beaches of the west coast of South Africa. Cah Biol Mar 24:85–103. https://doi.org/10.1016/0272-7714(88)90028-5
Barnard JL, Karaman GS (1991) The families and genera of marine gammaridean Amphipoda (except marine Gammaroidea). Part 2. Rec Aust Mus Suppl 13(2):419–866. https://doi.org/10.3853/j.0812-7387.13.1991.367
Bousfield EL (1970) Adaptive radiation in sand-burrowing amphipod crustaceans. Chesap Sci 11(3):143–154. https://doi.org/10.2307/1351237
Buchanan JB, Kain JM (1971) Measurement of the physical and chemical environments. In: Holme NA, McIntyre AD (eds) Methods for the study of marine benthos. Blackwell, Oxford, pp 30–58
Callaway R (2006) Tube worms promote community change. Mar Ecol Prog Ser 308:49–60. https://doi.org/10.3354/meps308049
Dale RK, Miller DC (2008) Hydrologic interactions of infaunal polychaetes and intertidal groundwater discharge. Mar Ecol Prog Ser 363:205–215. https://doi.org/10.3354/meps07455
Fenchel TM, Riedl RJ (1970) The sulfide system: a new biotic community underneath the oxidized layer of marine sand bottoms. Mar Biol 7(3):255–268. https://doi.org/10.1007/BF00367496
Fernandez-Gonzalez V, Fernandez-Jover D, Toledo-Guedes K, Valero-Rodriguez JM, Sanchez-Jerez P (2014) Nocturnal planktonic assemblages of amphipods vary due to the presence of coastal aquaculture cages. Mar Environ Res 101:22–28. https://doi.org/10.1016/j.marenvres.2014.08.001
Fincham AA (1970) Amphipods in the surf plankton. J Mar Biol Assoc UK 50(1):177–198. https://doi.org/10.1017/S0025315400000709
Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 48:452–458. https://doi.org/10.1038/bmt.2012.244
Lackschewitz D, Reise K (1998) Macrofauna on flood delta shoals in the Wadden Sea with an underground association between the lugworm Arenicola marina and the amphipod Urothoe poseidonis. Helgoländer Meeresunters 52(2):147–158. https://doi.org/10.1007/BF02908744
Manning RB, Tamaki A (1998) A new genus of ghost shrimp from Japan (Crustacea: Decapoda: Callianassidae). Proc Biol Soc Wash 111(4):889–892
McLachlan A (1978) A quantitative analysis of the meiofauna and the chemistry of the redox potential discontinuity zone in a sheltered sandy beach. Estuar Coast Shelf Sci 7(3):275–290. https://doi.org/10.1016/0302-3524(78)90110-X
McLachlan A, Turner I (1994) The interstitial environment of sandy beaches. PSZN I Mar Ecol 15(3–4):177–211. https://doi.org/10.1111/j.1439-0485.1994.tb00053.x
Pillay D, Branch GM (2011) Bioengineering effects of burrowing thalassinidean shrimps on marine soft-bottom ecosystems. Oceanogr Mar Biol Annu Rev 49:137–192
Posey MH (1986) Changes in a benthic community associated with dense beds of a burrowing deposit feeder, Callianassa californiensis. Mar Ecol Prog Ser 31:15–22
Riddle MJ (1988) Cyclone and bioturbation effects on sediments from coral reef lagoons. Estuar Coast Shelf Sci 27:687–695. https://doi.org/10.1016/0272-7714(88)90075-3
Sassa S, Watabe Y (2007) Role of suction dynamics in evolution of intertidal sandy flats: field evidence, experiments, and theoretical model. J Geophys Res 112:F01003. https://doi.org/10.1029/2006JF000575
Sassa S, Watabe Y (2008) Threshold, optimum and critical geoenvironmental conditions for burrowing activity of sand bubbler crab, Scopimera globosa. Mar Ecol Prog Ser 354:191–199. https://doi.org/10.3354/meps07236
Sassa S, Watabe Y (2009) Persistent sand bars explained by geodynamic effects. Geophys Res Lett 36:L01404. https://doi.org/10.1029/2008GL036230
Sassa S, Watabe Y, Yang S, Kuwae T (2011) Burrowing criteria and burrowing mode adjustment in bivalves to varying geoenvironmental conditions in intertidal flats and beaches. PLoS One 6(9):e25041. https://doi.org/10.1371/journal.pone.0025041
Sassa S, Yang S, Watabe Y, Kajihara N, Takada Y (2014) Role of suction in sandy beach habitats and the distributions of three amphipod and isopod species. J Sea Res 85:336–342. https://doi.org/10.1016/j.seares.2013.06.005
Sudo H (1988) Diurnal rhythms in predatory fish and amphipod prey. In: Hanyu I, Tabata M (eds) Daily rhythmic activities in aquatic animals. Kouseisha-Kouseikaku, Tokyo, pp 117–183 (in Japanese)
Takeuchi S, Tamaki A (2014) Assessment of benthic disturbance associated with stingray foraging for ghost shrimp by aerial survey over an intertidal sandflat. Cont Shelf Res 84:139–157. https://doi.org/10.1016/j.csr.2014.05.007
Takeuchi S, Takahara Y, Agata Y, Nasuda J, Yamada F, Tamaki A (2013) Response of suspension-feeding clams to natural removal of bioturbating shrimp on a large estuarine intertidal sandflat in western Kyushu, Japan. J Exp Mar Biol Ecol 448:308–320. https://doi.org/10.1016/j.jembe.2013.07.018
Tamaki A (1984) Structural characteristics of an intertidal sand flat in Tomioka Bay, Amakusa, west Kyushu. Publ Amakusa Mar Biol Lab Kyushu Univ 7:125–150
Tamaki A (1985) Inhibition of larval recruitment of Armandia sp. (Polychaeta: Opheliidae) by established adults of Pseudopolydora paucibranchiata (Okuda) (Polychaeta: Spionidae) on an intertidal sand flat. J Exp Mar Biol Ecol 87(1):67–82. https://doi.org/10.1016/0022-0981(85)90193-5
Tamaki A (1987) Comparison of resistivity to transport by wave action in several polychaete species on an intertidal sand flat. Mar Ecol Prog Ser 37:181–189
Tamaki A (1994) Extinction of the trochid gastropod, Umbonium (Suchium) moniliferum (Lamarck), and associated species on an intertidal sandflat. Res Popul Ecol 36(2):225–236. https://doi.org/10.1007/BF02514939
Tamaki A, Ingole B (1993) Distribution of juvenile and adult ghost shrimps, Callianassa japonica Ortmann (Thalassinidea), on an intertidal sandflat: intraspecific facilitation as a possible pattern-generating factor. J Crustac Biol 13(1):175–183. https://doi.org/10.1163/193724093X00543
Tamaki A, Kikuchi T (1983) Spatial arrangement of macrobenthic assemblages on an intertidal sand flat, Tomioka Bay, west Kyushu. Publ Amakusa Mar Biol Lab Kyushu Univ 7:41–60
Tamaki A, Suzukawa K (1991) Co-occurrence of the cirolanid isopod Eurydice nipponica Bruce & Jones and the ghost shrimp Callianassa japonica Ortmann on an intertidal sand flat. Ecol Res 6:87–100. https://doi.org/10.1007/BF02353872
Tamaki A, Suzukawa K (1997) Life history and zonation dynamics of the cirolanid isopod, Eurydice nipponica Bruce & Jones, on an intertidal sandflat in western Kyushu, Japan. Crustac Res 26:83–102. https://doi.org/10.18353/crustacea.26.0_83
Tamaki A, Takeuchi S (2016) Persistence, extinction, and recolonization of an epibenthic gastropod population on an intertidal sandflat: 35-y contingent history of a key species of the benthic community in metapopulation and metacommunity contexts. J Shellfish Res 35(4):921–967. https://doi.org/10.2983/035.035.0419
Tamaki A, Ueno H (1998) Burrow morphology of two callianassid shrimps, Callianassa japonica Ortmann, 1891 and Callianassa sp. (= C. japonica: de Man, 1928) (Decapoda: Thalassinidea). Crustac Res 27:28–39. https://doi.org/10.18353/crustacea.27.0_28
Tamaki A, Ingole B, Ikebe K, Muramatsu K, Taka M, Tanaka M (1997) Life history of the ghost shrimp, Callianassa japonica Ortmann (Decapoda: Thalassinidea), on an intertidal sandflat in western Kyushu, Japan. J Exp Mar Biol Ecol 210(2):223–250. https://doi.org/10.1016/S0022-0981(96)02709-8
Tudhope AW, Scoffin TP (1984) The effects of Callianassa bioturbation on the preservation of carbonate grains in Davies Reef lagoon, Great Barrier Reef, Australia. J Sediment Petrol 54:1091–1096
Vader W (1978) Associations between amphipods and echinoderms. Astarte 11:123–134
Volkenborn N, Polerecky L, Wethey DS, DeWitt TH, Woodin SA (2012) Hydraulic activities by ghost shrimp Neotrypaea californiensis induce oxic–anoxic oscillations in sediments. Mar Ecol Prog Ser 455:141–156. https://doi.org/10.3354/meps09645
Wada M, Urakawa T, Tamaki A (2016) Dynamics of bacterial community structure on intertidal sandflat inhabited by the ghost shrimp Nihonotrypaea harmandi (Decapoda: Axiidea: Callianassidae) in Tomioka Bay, Amakusa, Japan. Gene 576(2):657–666. https://doi.org/10.1016/j.gene.2015.10.017
Wardiatno Y, Shimoda K, Koyama K, Tamaki A (2003) Zonation of congeneric callianassid shrimps, Nihonotrypaea harmandi (Bouvier, 1901) and N. japonica (Ortmann, 1891) (Decapoda: Thalassinidea), on intertidal sandflats in the Ariake-Sound estuarine system, Kyushu, Japan. Benthos Res 58(1):51–73. https://doi.org/10.5179/benthos1996.58.1_51
Woodin SA, Wethey DS, Volkenborn N (2010) Infaunal hydraulic ecosystem engineers: cast of characters and impacts. Integr Comp Biol 50(2):176–187. https://doi.org/10.1093/icb/icq031
Wynberg RP, Branch GM (1994) Disturbance associated with bait-collection for sandprawns (Callianassa kraussi) and mudprawns (Upogebia africana): long-term effects on the biota of intertidal sandflats. J Mar Res 52(3):523–558. https://doi.org/10.1357/0022240943077019
Yamada F, Kobayashi N (2007) Intertidal multiple sand bars in a low-energy environment. J Waterw Port Coast Ocean Eng 133(5):343–351. https://doi.org/10.1061/(ASCE)0733-950X(2007)133:5(343)
Yamada A, Somiya R, Ikeda N, Tamaki A (2017) The complete mitochondrial genome of the burrowing ghost shrimp, Nihonotrypaea harmandi (Bouvier, 1901), (Crustacea, Decapoda, Axiidea, Callianassidae)—a validation of the genus and species classifications. Mitochondrial DNA B Resour 2(1):238–239. https://doi.org/10.1080/23802359.2017.1318676
Yu OH, Soh HY, Suh H-L (2002) Seasonal zonation patterns of benthic amphipods in a sandy shore surf zone of Korea. J Crustac Biol 22(2):459–466. https://doi.org/10.1163/20021975-99990253
Zipperle A, Reise K (2005) Freshwater springs on intertidal sand flats cause a switch in dominance among polychaete worms. J Sea Res 54(2):143–150. https://doi.org/10.1016/j.seares.2005.01.003
Acknowledgements
We thank K. Hayashi, T. Hasegawa, S. Miyabe, H. Ueno, H. Kimura, Y. Tanaka, C. Matsumoto, Y. Sato, T. Nakagawa, and K. Watanabe for help in the field work. The water-depth data were provided by Hydrographic and Oceanographic Department, Japan Coast Guard. We appreciate constructive comments from the three reviewers.
Funding
This study was partly supported by the Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research JP26440244 to AT and JP15H02265 to SS.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Responsible Editor: M. Hüttel.
Reviewed by S. Woodin and undisclosed experts.
Rights and permissions
About this article
Cite this article
Tamaki, A., Kagesawa, T., Takeuchi, S. et al. Facultative commensalism of a free-burrowing urothoid amphipod with a deep burrow-dwelling callianassid shrimp in intertidal sand. Mar Biol 165, 36 (2018). https://doi.org/10.1007/s00227-018-3296-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-018-3296-0