Abstract
Casting is one of the most effective methods for investigating the morphology of invertebrate burrows. However, this method is sometimes problematic, especially for studies of gravely sea floor habitats. This is because the cast often traps coarse-grained sediments (pebbles and shell fragments) on its surface, which interferes with investigation of the burrow morphology. In this study we used a combination of burrow casting and computed tomography (CT) scanning of a cast to determine the lumen morphology of the burrow of the strahlaxiid shrimp Neaxius acanthus (Decapoda: Axiidea) inhabiting a gravely intertidal flat in southwestern Japan. The images created using the CT data enabled us to accurately observe the morphology of the shrimp burrow, and to identify burrow associates including the galeommatoidean bivalve Barrimysia cumingii and the phenacolepadid gastropod Phenacolepas sp. The images also showed the position of the shrimp and its burrow associates within the burrow lumen. The combination of in situ burrow casting and CT scanning will aid the interpretation of the ecology of infauna in various seafloor settings.
References
Amon DJ, Sykes D, Ahmed F, Copley JT, Kemp KM, Tyler PA, Young CM Glover AG (2015) Burrow forms, growth rates and feeding rates of wood-boring Xylophagaidae bivalves revealed by micro-computed tomography. Front Mar Sci 2:10. doi:10.3389/fmars.2015.00010
Aoyama J, Shinoda A, Sasai S, Miller MJ, Tsukamoto K (2005) First observations of the burrows of Anguilla japonica. J Fish Biol 67:1534–1543. doi:10.1111/j.1095-8649.2005.00860.x
Atkinson RJA, Froglia C, Arneri E, Antolini B (1997) Observations on the burrows and burrowing behaviour of Squilla mantis (L.) (Crustacea: Stomatopoda). Mar Ecol 18:337–359. doi:10.1111/j.1439-0485.1997.tb00446.x
Curran HA, Martin AJ (2003) Complex decapod burrows and ecological relationships in modern and Pleistocene intertidal carbonate environments, San Salvador Island, Bahamas. Palaeogeogr Palaeoclimatol Palaeoecol 192:229–245. doi:10.1016/S0031-0182(02)00687-9
Dufour SC, Desrosiers G, Long B, Lajeunesse P, Gagnoud M, Labrie J, Archambault P Stora G (2005) A new method for three-dimensional visualization and quantification of biogenic structures in aquatic sediments using axial tomodensitometry. Limnol Oceanogr Methods 3:372–380. doi:10.4319/lom.2005.3.372
Dworschak PC (1987) Burrows of Solecurtus strigilatus (Linné) and S. multistriatus (Scacchi). Senckenbergiana maritima 19:131–147
Dworschak PC (2015) Methods collecting Axiidea and Gebiidea (Decapoda): a review. Ann Naturhist Mus Wien B 117:5–21
Dworschak PC, Ott JA (1993) Decapod burrows in mangrove-channel and back-reef environments at the Atlantic Barrier Reef, Belize. Ichnos 2:277–290. doi:10.1080/10420949309380103
Dworschak PC, Rodrigues SDA (1997) A modern analogue for the trace fossil Gyrolithes: burrows of the thalassinidean shrimp Axianassa australis. Lethaia 30:41–52. doi:10.1111/j.1502-3931.1997.tb00443.x
Dworschak PC, Felder DL, Tudge CC (2012) Infraorders Axiidea de Saint Laurent, 1979 and Gebiidea de Saint Laurent, 1979 (formerly known collectively as Thalassinidea). In: Schram FR, von Vaupel Klein JC (eds) Treatise on Zoology-Anatomy, Taxonomy, Biology. The Crustacea, Volume 9 Part B. Brill, Leiden, pp. 109–219
Gibert JM de, Muñiz F, Belaústegui Z, Hyžný M (2013) Fossil and modern fiddler crabs (Uca tangeri: Ocypodidae) and their burrows from SW Spain: ichnologic and biogeographic implications. J Crustacean Biol 33:537–551. doi:10.1163/1937240X-00002151
Goto R, Ishikawa H (2016) Borniopsis mortoni sp. n. (Heterodonta: Galeommatoidea: Galeommatidae sensu lato), a new bivalve commensal with a synaptid sea cucumber from Japan. ZooKeys 615:33–45. doi:10.3897/zookeys.615.8125
Goto R, Kato M (2012) Geographic mosaic of mutually exclusive dominance of obligate commensals in symbiotic communities associated with a burrowing echiuran worm. Mar Biol 159:319–330. doi:10.1007/s00227-011-1810-8
Goto R, Kawakita A, Ishikawa H, Hamamura Y, Kato M (2012) Molecular phylogeny of the bivalve superfamily Galeommatoidea (Heterodonta, Veneroida) reveals dynamic evolution of symbiotic lifestyle and interphylum host switching. BMC Evol Biol 12:172. doi:10.1186/1471-2148-12-172
Goto R, Ohsuga K, Kato M (2014) Mode of life of Anomiostrea coralliophila Habe, 1975 (Ostreidae): a symbiotic oyster living in ghost-shrimp burrows. J Mollus Stud 80:201–205. doi:10.1093/mollus/eyt052
Goto R, Ishikawa H, Hamamura Y (2016a) The enigmatic bivalve genus Paramya (Myoidea: Myidae): symbiotic association of an East Asian species with spoon worms (Echiura) and its transfer to the family Basterotiidae (Galeommatoidea). J Mar Biol Ass UK. doi:10.1017/S0025315416000758
Goto R, Ishikawa H, Hamamura Y (2016b) Symbiotic Association of the Bivalve Tellimya fujitaniana (Galeommatoidea) with the Heart Urchin Echinocardium cordatum (Spatangoida) in the Northwestern Pacific. Zool Sci 33:434–440. doi:10.2108/zs150215
Goto R, Ishikawa H, Hamamura Y (2016c) Morphology, Biology, and Phylogenetic Position of the Bivalve Platomysia rugata (Heterodonta: Galeommatoidea), a Commensal with the Sipunculan Worm Sipunculus nudus. Zool Sci 33:441–447. doi:10.2108/zs160009
Henmi Y, Itani G (2014a) Laboratory quantification of burrow utilization by the symbiotic varunid crab Sestrostoma toriumii. Plankton Benthos Res 9:203–206. doi:10.3800/pbr.9.203
Henmi Y, Itani G (2014b) Burrow utilization in the goby Eutaeniichthys gilli associated with the mud shrimp Upogebia yokoyai. Zool Sci 31:523–528. doi:10.2108/zs140055
Itani G, Kato M (2002) Cryptomya (Venatomya) truncata (Bivalvia: Myidae): association with thalassinidean shrimp burrows and morphometric variation in Japanese waters. Venus 61:193–202
Itani G, Uchino T (2003) Burrow morphology of the goby Taenioides cirratus. J Mar Biol Ass UK 83:881–882. doi:10.1017/S0025315403007975h
Kinoshita K (2002) Burrow structure of the mud shrimp Upogebia major (Decapoda: Thalassinidea: Upogebiidae). J Crustacean Biol 22:474–480. doi:10.1163/20021975-99990255
Kinoshita K, Itani G (2005) Interspecific differences in the burrow morphology between the sympatric mud shrimps, Austinogebia narutensis and Upogebia issaeffi (Crustacea: Thalassinidea: Upogebiidae). J Mar Biol Ass UK 85:943–947. doi:10.1017/S0025315405011926
Kinoshita K, Wada M, Kogure K, Furota T (2008) Microbial activity and accumulation of organic matter in the burrow of the mud shrimp, Upogebia major (Crustacea: Thalassinidea). Mar Biol 153:277–283. doi:10.1007/s00227-007-0802-1
Kinoshita K, Itani G, Uchino T (2010) Burrow morphology and associated animals of the mud shrimp Upogebia yokoyai (Crustacea: Thalassinidea: Upogebiidae). J Mar Biol Ass UK 90:947–952. doi:10.1017/S0025315410000214
Kneer D (2006) The role of Neaxius acanthus (Thalassinidea: Strahlaxiidae) and its burrows in a tropical seagrass meadow, with some remarks on Corallianassa coutierei (Thalassinidea: Callianassidae). Master thesis. Freie Universität, Berlin
Kneer D, Asmus H, Vonk JA (2008) Seagrass as the main food source of Neaxius acanthus (Thalassinidea: Strahlaxiidae), its burrow associates, and of Corallianassa coutierei (Thalassinidea: Callianassidae). Estuar Coast Shelf Sci 79:620–630. doi:10.1016/j.ecss.2008.05.013
Kneer D, Monniot F, Stach T, Christianen MJ (2013) Ascidia subterranea sp. nov.(Phlebobranchia: Ascidiidae), a new tunicate belonging to the A. sydneiensis Stimpson, 1855 group, found as burrow associate of Axiopsis serratifrons A. Milne-Edwards, 1873 (Decapoda: Axiidae) on Derawan Island, Indonesia. Zootaxa 3616:485–494. doi:10.11646/zootaxa.3616.5.5
Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta GT (2012) What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser 446:285–302. doi:10.3354/meps09506
Laverock B, Smith CJ, Tait K, Osborn AM, Widdicombe S, Gilbert JA (2010) Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediments. ISME J 4:1531–1544. doi:10.1038/ismej.2010.86
Lohrer AM, Thrush SF, Gibbs MM (2004) Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:1092–1095. doi:10.1038/nature03042
Nara M, Akiyama H, Itani G (2008) Macrosymbiotic association of the myid bivalve Cryptomya with thalassinidean shrimps: Examples from modern and Pleistocene tidal flats of Japan. Palaeogeogr Palaeoclimatol Palaeoecol 261:100–104. doi:10.1016/j.palaeo.2008.01.001
Nickell LA, Atkinson RJA (1995) Functional morphology of burrows and trophic modes of three thalassinidean shrimp species, and a new approach to the classification of thalassinidean burrow morphology. Mar Ecol Prog Ser 128:181–197. doi:10.3354/meps128181
Nickell LA, Atkinson RJA, Hughes DJ, Ansell AD, Smith CJ (1995) Burrow morphology of the echiuran worm Maxmuelleria lankesteri (Echiura: Bonelliidae), and a brief review of burrow structure and related ecology of the Echiura. J Nat Hist 29:871–885. doi:10.1080/00222939500770311
Pemberton GS, Risk MJ, Buckley DE (1976) Supershrimp: deep bioturbation in the Strait of Canso, Nova Scotia. Science 192:790–791. doi:10.1126/science.192.4241.790
Pervesler P, Dworschak PC (1985) Burrows of Jaxea nocturna Nardo in the Gulf of Trieste. Senck Marit 17:33–53
Rodríguez-Tovar FJ, Seike K, Curran HA (2014) Characteristics, distribution patterns, and implications for ichnology of modern burrows of Uca (Leptuca) speciosa, San Salvador Island, Bahamas. J Crustacean Biol 34:565–572. doi:10.1163/1937240X-00002263
Rosenberg R, Davey E, Gunnarsson J, Norling K, Frank M (2007) Application of computer-aided tomography to visualize and quantify biogenic structures in marine sediments. Mar Ecol Prog Ser 331:23–34. doi:10.3354/meps331023
Seike K, Curran HA (2014) Burrow morphology of the land crab Gecarcinus lateralis and the ghost crab Ocypode quadrata on San Salvador Island, The Bahamas: comparisons and palaeoenvironmental implications. Span J Palaeontol 29:61–70
Seike K, Nara M (2007) Occurrence of bioglyphs on Ocypode crab burrows in a modern sandy beach and its palaeoenvironmental implications. Palaeogeogr Palaeoclimatol Palaeoecol 252:458–463. doi:10.1016/j.palaeo.2007.05.003
Seike K, Nara M (2008) Burrow morphologies of the ghost crabs Ocypode ceratophthalma and O. sinensis in foreshore, backshore, and dune subenvironments of a sandy beach in Japan. J Geol Soc Japan 114:591–596. doi:10.5575/geosoc.114.591
Seike K, Jenkins RG, Watanabe H, Nomaki H, Sato K (2012) Novel use of burrow casting as a research tool in deep-sea ecology. Biol Lett 8:648–651. doi:10.1098/rsbl.2011.1111
Seike K, Kitahashi T, Noguchi T (2016) Sedimentary features of Onagawa Bay, northeastern Japan after the 2011 off the Pacific coast of Tohoku Earthquake: sediment mixing by recolonized benthic animals decreases the preservation potential of tsunami deposits. J Oceanogr 72:141–149. doi:10.1007/s10872-015-0297-1
Vonk JA, Kneer D, Stapel J, Asmus H (2008) Shrimp burrow in tropical seagrass meadows: an important sink for litter. Estuar Coast Shelf Sci 79:79–85. doi:10.1016/j.ecss.2008.03.003
Wetzel A (2010) Deep-sea ichnology: observations in modern sediments to interpret fossil counterparts. Acta Geol Pol 60:125–138
Ziebis W, Forster S, Huettel M, Jørgensen BB (1996) Complex burrows of the mud shrimp Callianassa truncata and their geochemical impact in the sea bed. Nature 382:619–622. doi:10.1038/382619a0
Acknowledgements
We thank Tomoko Okamoto (Gifu University) for her assistance in the fieldwork, and Tomoyuki Komai (Natural History Museum and Institute, Chiba) for identification of Neaxius acanthus, and two anonymous referees for their comments, which helped improve the manuscript. This study was undertaken through the cooperative research program of the Center for Advanced Marine Core Research (CMCR), Kochi University (Acceptance Number 15A026).
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This study was partially funded by the Japan Society for the Promotion of Science (JSPS) Research Fellowship for Young Scientists to RG.
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Seike, K., Goto, R. Combining in situ burrow casting and computed tomography scanning reveals burrow morphology and symbiotic associations in a burrow. Mar Biol 164, 59 (2017). https://doi.org/10.1007/s00227-017-3096-y
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DOI: https://doi.org/10.1007/s00227-017-3096-y