Facultative commensalism of a free-burrowing urothoid amphipod with a deep burrow-dwelling callianassid shrimp in intertidal sand
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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.
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.
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.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- Aller RC, Dodge RE (1974) Animal-sediment relations in a tropical lagoon: Discovery Bay, Jamaica. J Mar Res 32:209–232Google Scholar
- 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 30–58Google Scholar
- 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 CrossRefGoogle Scholar
- Manning RB, Tamaki A (1998) A new genus of ghost shrimp from Japan (Crustacea: Decapoda: Callianassidae). Proc Biol Soc Wash 111(4):889–892Google Scholar
- 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 CrossRefGoogle Scholar
- Pillay D, Branch GM (2011) Bioengineering effects of burrowing thalassinidean shrimps on marine soft-bottom ecosystems. Oceanogr Mar Biol Annu Rev 49:137–192Google Scholar
- 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)Google Scholar
- 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 CrossRefGoogle Scholar
- Tamaki A (1984) Structural characteristics of an intertidal sand flat in Tomioka Bay, Amakusa, west Kyushu. Publ Amakusa Mar Biol Lab Kyushu Univ 7:125–150Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 7:41–60Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 54:1091–1096Google Scholar
- Vader W (1978) Associations between amphipods and echinoderms. Astarte 11:123–134Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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) CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar