Effect of stingray (Hemitrygon akajei) foraging on a ghost shrimp population (Nihonotrypaea harmandi) on an intertidal sandflat, western Kyushu, Japan
Akio Tamaki A B , Kazuyuki Harada A , Yoshinobu Sogawa A and Seiji Takeuchi AA Graduate School of Fisheries and Environmental Sciences, Nagasaki University, Bunkyo-machi 1-14, Nagasaki 852-8521, Japan.
B Corresponding author. Email: tamaki@nagasaki-u.ac.jp
Marine and Freshwater Research 71(9) 1128-1148 https://doi.org/10.1071/MF19265
Submitted: 29 July 2019 Accepted: 25 November 2019 Published: 31 January 2020
Abstract
Callianassid shrimp residing in deep burrows have large bioturbating effects on marine soft-bottom communities. A few predators that excavate deep pits could have substantial effects on shrimp populations, as well as knock-on effects. Processes and consequences of such effects on shrimp populations are poorly understood. On a 300-m-wide intertidal sandflat area between tide marks in western Kyushu between 1989 and 1994, shrimp population densities were stable, reaching >1300 individuals m–2. Dasyatid stingray feeding pits reaching depths up to 20 cm occurred abruptly in large numbers in 1994, after which shrimp densities decreased yearly to hundreds of individuals per square metre in 2001. The densities of ray feeding pits formed per day were monitored every or every other spring tide between 2000 and 2001. Schools of rays were enclosed during submerged times and their body sizes recorded alive to determine size-frequency distribution. The body-size frequency distributions of shrimp were compared among the gut contents of several rays, ray feeding pits and intact sandflat. Reductions in the shrimp density per ray feeding bout compared with the density on the intact sandflat were recorded. A model of daily predation at different seasonal rates was used to simulate the yearly change in shrimp density. The result was consistent with the actual change.
Additional keywords: bioturbation, spatial scale, top-down forcing.
References
Ajemian, M. J., and Powers, S. P. (2013). Foraging effects of cownose rays (Rhinoptera bonasus) along barrier islands of the northern Gulf of Mexico. Journal of Experimental Marine Biology and Ecology 439, 119–128.| Foraging effects of cownose rays (Rhinoptera bonasus) along barrier islands of the northern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Ajemian, M. J., Powers, S. P., and Murdoch, T. J. T. (2012). Estimating the potential impacts of large mesopredators on benthic resources: integrative assessment of spotted eagle ray foraging ecology in Bermuda. PLoS One 7, e40227.
| Estimating the potential impacts of large mesopredators on benthic resources: integrative assessment of spotted eagle ray foraging ecology in Bermuda.Crossref | GoogleScholarGoogle Scholar | 22802956PubMed |
Atkinson, R. J. A., and Taylor, A. C. (2005). Aspects of the physiology, biology and ecology of thalassinidean shrimps in relation to their burrow environment. Oceanography and Marine Biology – an Annual Review 43, 173–210.
Cadée, G. C. (2001). Sediment dynamics by bioturbating organisms. In ‘Ecological Studies, Vol. 151. Ecological Comparisons of Sedimentary Shores’. (Ed. K. Reise.) pp. 127–148. (Springer-Verlag: Berlin, Germany.)
Costa, T. L. A., Thayer, J. A., and Mendes, L. F. (2015). Population characteristics, habitat and diet of a recently discovered stingray Dasyatis marianae: implications for conservation. Journal of Fish Biology 86, 527–543.
| Population characteristics, habitat and diet of a recently discovered stingray Dasyatis marianae: implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Cross, R. E., and Curran, M. C. (2000). Effects of feeding pit formation by rays on an intertidal meiobenthic community. Estuarine, Coastal and Shelf Science 51, 293–298.
| Effects of feeding pit formation by rays on an intertidal meiobenthic community.Crossref | GoogleScholarGoogle Scholar |
D’Andrea, A. F., Lopez, G. R., and Aller, R. C. (2004). Rapid physical and biological particle mixing on an intertidal sandflat. Journal of Marine Research 62, 67–92.
| Rapid physical and biological particle mixing on an intertidal sandflat.Crossref | GoogleScholarGoogle Scholar |
Dumbauld, B. R., and Bosley, K. M. (2018). Recruitment ecology of burrowing shrimps in US Pacific coast estuaries. Estuaries and Coasts 41, 1848–1867.
| Recruitment ecology of burrowing shrimps in US Pacific coast estuaries.Crossref | GoogleScholarGoogle Scholar |
Dumbauld, B. R., Holden, D. L., and Langness, O. P. (2008). Do sturgeon limit burrowing shrimp populations in Pacific Northwest Estuaries? Environmental Biology of Fishes 83, 283–296.
| Do sturgeon limit burrowing shrimp populations in Pacific Northwest Estuaries?Crossref | GoogleScholarGoogle Scholar |
Dworschak, P. C., Felder, D. L., and Tudge, C. C. (2012). Chapter 69. Infraorders Axiidea de Saint Laurent, 1979 and Gebiidea de Saint Laurent, 1979 (formerly known collectively as Thalassinidea). In ‘Treatise on Zoology – Anatomy, Taxonomy, Biology. The Crustacea. Complementary to the Volumes Translated from the French of the Traité de Zoologie [founded by P.-P. Grassé], Volume 9 Part B. Eucarida: Decapoda: Astacidea p.p. (Enoplometopoidea, Nephropoidea), Glypheidea, Axiidea, Gebiidea, and Anomura’. (Eds F. R. Schram, J. C. von Vaupel Klein, J. Forest, and M. Charmantier-Daures.) pp. 109–219. (Brill: Leiden, Netherlands.)
Ebert, D. A., and Cowley, P. D. (2003). Diet, feeding behavior and habitat utilisation of the blue stingray Dasyatis chrysonota (Smith, 1828) in South African waters. Marine and Freshwater Research 54, 957–965.
| Diet, feeding behavior and habitat utilisation of the blue stingray Dasyatis chrysonota (Smith, 1828) in South African waters.Crossref | GoogleScholarGoogle Scholar |
Felder, D. L. (1979). Respiratory adaptations of the estuarine mud shrimp, Callianassa jamaicense (Schmitt, 1935) (Crustacea, Decapoda, Thalassinidea). The Biological Bulletin 157, 125–137.
| Respiratory adaptations of the estuarine mud shrimp, Callianassa jamaicense (Schmitt, 1935) (Crustacea, Decapoda, Thalassinidea).Crossref | GoogleScholarGoogle Scholar |
Felder, D. L. (2001). Diversity and ecological significance of deep-burrowing macrocrustaceans in coastal tropical waters of the Americas (Decapoda: Thalassinidea). Interciencia 26, 440–449.
Flach, E., and Tamaki, A. (2001). Competitive bioturbators on intertidal sand flats in the European Wadden Sea and Ariake Sound in Japan. In ‘Ecological Studies, Vol. 151. Ecological Comparisons of Sedimentary Shores’. (Ed. K. Reise.) pp. 149–171. (Springer-Verlag: Berlin, Germany.)
Gilliam, D., and Sullivan, K. M. (1993). Diet and feeding habits of the southern stingray Dasyatis americana in the central Bahamas. Bulletin of Marine Science 52, 1007–1013.
Grant, J. (1983). The relative magnitude of biological and physical sediment reworking in an intertidal community. Journal of Marine Research 41, 673–689.
| The relative magnitude of biological and physical sediment reworking in an intertidal community.Crossref | GoogleScholarGoogle Scholar |
Gray, A. E., Mulligan, T. J., and Hannah, R. W. (1997). Food habits, occurrence, and population structure of the bat ray, Myliobatis californica, in Humboldt Bay, California. Environmental Biology of Fishes 49, 227–238.
| Food habits, occurrence, and population structure of the bat ray, Myliobatis californica, in Humboldt Bay, California.Crossref | GoogleScholarGoogle Scholar |
Grubbs, R. D., Carlson, J. K., Romine, J. G., Curtis, T. H., McElroy, W. D., McCandless, C. T., Cotton, C. F., and Musick, J. A. (2016). Critical assessment and ramifications of a purported marine trophic cascade. Scientific Reports 6, 20970.
| Critical assessment and ramifications of a purported marine trophic cascade.Crossref | GoogleScholarGoogle Scholar | 26876514PubMed |
Hall, S. J., Raffaelli, D., and Thrush, S. F. (1994). Patchiness and disturbance in shallow water benthic assemblages. In ‘Aquatic Ecology: Scale, Pattern and Process’. (Eds P. S. Giller, A. G. Hildrew, D. G. Raffaelli.) pp. 333–375. (Blackwell Scientific Publications: Oxford, UK.)
Harada, K., and Tamaki, A. (2004). Assessment of the predation impact of the stingray Dasyatis akajei (Müller & Henle, 1841) on the population of the ghost shrimp Nihonotrypaea harmandi (Bouvier, 1901) on an intertidal sandflat (preliminary report). In ‘Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments – from Individual Behavior to Their Role as Ecosystem Engineers’. (Ed. A. Tamaki.) pp. 81–85. (Nagasaki University: Nagasaki, Japan.)
Heithaus, M. R., Frid, A., Vaudo, J. J., Worm, B., and Wirsing, A. J. (2010). Unraveling the ecological importance of elasmobranchs. In ‘Sharks and Their Relatives II’. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 611–637. (CRC Press: Boca Raton, FL, USA.)
Hines, A. H., Whitlatch, R. B., Thrush, S. F., Hewitt, J. E., Cummings, V. J., Dayton, P. K., and Legendre, P. (1997). Nonlinear foraging response of a large marine predator to benthic prey: eagle ray pits and bivalves in a New Zealand sandflat. Journal of Experimental Marine Biology and Ecology 216, 191–210.
| Nonlinear foraging response of a large marine predator to benthic prey: eagle ray pits and bivalves in a New Zealand sandflat.Crossref | GoogleScholarGoogle Scholar |
Howard, J. D., Mayou, T. V., and Heard, R. W. (1977). Biogenic sedimentary structures formed by rays. Journal of Sedimentary Petrology 47, 339–346.
Jacobsen, I. P., and Bennett, M. B. (2013). A comparative analysis of feeding and trophic level ecology in stingrays (Rajiformes; Myliobatoidei) and electric rays (Rajiformes: Torpedinoidei). PLoS One 8, e71348.
| A comparative analysis of feeding and trophic level ecology in stingrays (Rajiformes; Myliobatoidei) and electric rays (Rajiformes: Torpedinoidei).Crossref | GoogleScholarGoogle Scholar | 23936503PubMed |
Kanazawa, T. (2003). The fishing distribution and food of the Japanese stingray (Dasyatis akajei) in the Ariake Sea of the water temperature descending term. Bulletin of Fukuoka Marine Technology Research Center 13, 149–152.
Kiszka, J. J., Heithaus, M. R., and Quod, J.-P. (2015). Stingrays as possible facilitators for foraging trevallies in a nearshore sandflat. Marine Biodiversity 45, 625–626.
| Stingrays as possible facilitators for foraging trevallies in a nearshore sandflat.Crossref | GoogleScholarGoogle Scholar |
Kodama, K., Oyama, M., Lee, J.-H., Kume, G., Yamaguchi, A., Shibata, Y., Shiraishi, H., Morita, M., Shimizu, M., and Horiguchi, T. (2010). Drastic and synchronous changes in megabenthic community structure concurrent with environmental variations in a eutrophic coastal bay. Progress in Oceanography 87, 157–167.
| Drastic and synchronous changes in megabenthic community structure concurrent with environmental variations in a eutrophic coastal bay.Crossref | GoogleScholarGoogle Scholar |
Kristensen, E., Penha-Lopes, G., Delefosse, M., Valdemarsen, T., Quintana, C. O., and Banta, G. T. (2012). What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Marine Ecology Progress Series 446, 285–302.
| What is bioturbation? The need for a precise definition for fauna in aquatic sciences.Crossref | GoogleScholarGoogle Scholar |
Martinell, J., de Gibert, J. M., Domènech, R., Ekdale, A. A., and Steen, P. P. (2001). Cretaceous ray traces? An alternative interpretation for the alleged dinosaur tracks of La Posa, Isona, NE Spain. Palaios 16, 409–416.
| Cretaceous ray traces? An alternative interpretation for the alleged dinosaur tracks of La Posa, Isona, NE Spain.Crossref | GoogleScholarGoogle Scholar |
Martins, A. P. B., Heupel, M. R., Chin, A., and Simpfendorfer, C. A. (2018). Batoid nurseries: definition, use and importance. Marine Ecology Progress Series 595, 253–267.
| Batoid nurseries: definition, use and importance.Crossref | GoogleScholarGoogle Scholar |
Meysman, F. J. R., Middelburg, J. J., and Heip, C. H. R. (2006). Bioturbation: a fresh look at Darwin’s last idea. Trends in Ecology & Evolution 21, 688–695.
| Bioturbation: a fresh look at Darwin’s last idea.Crossref | GoogleScholarGoogle Scholar |
Moser, M. L., Patten, K., Corbett, S. C., Feist, B. E., and Lindley, S. T. (2017). Abundance and distribution of sturgeon feeding pits in a Washington estuary. Environmental Biology of Fishes 100, 597–609.
| Abundance and distribution of sturgeon feeding pits in a Washington estuary.Crossref | GoogleScholarGoogle Scholar |
Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P., and Peterson, C. H. (2007). Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.
| Cascading effects of the loss of apex predatory sharks from a coastal ocean.Crossref | GoogleScholarGoogle Scholar | 17395829PubMed |
Myrick, J. L., and Flessa, K. W. (1996). Bioturbation rates in Bahía La Choya, Sonora, Mexico. Ciencias Marinas 22, 23–46.
| Bioturbation rates in Bahía La Choya, Sonora, Mexico.Crossref | GoogleScholarGoogle Scholar |
Navia, A. F., Mejía-Falla, P. A., López-García, J., Giraldo, A., and Cruz-Escalona, V. H. (2016). How many trophic roles can elasmobranchs play in a marine tropical network? Marine and Freshwater Research 68, 1–12.
O’Shea, O. R., Thums, M., van Keulen, M., and Meekan, M. (2012). Bioturbation by stingrays at Ningaloo Reef, Western Australia. Marine and Freshwater Research 63, 189–197.
| Bioturbation by stingrays at Ningaloo Reef, Western Australia.Crossref | GoogleScholarGoogle Scholar |
O’Shea, O. R., Thums, M., van Keulen, M., Kempster, R. M., and Meekan, M. G. (2013). Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. Journal of Fish Biology 82, 1805–1820.
| Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs.Crossref | GoogleScholarGoogle Scholar | 23731138PubMed |
Peterson, C. H., Fodrie, F. J., Summerson, H. C., and Powers, S. P. (2001). Site-specific and density-dependent extinction of prey by schooling rays: generation of a population sink in top-quality habitat for bay scallops. Oecologia 129, 349–356.
| Site-specific and density-dependent extinction of prey by schooling rays: generation of a population sink in top-quality habitat for bay scallops.Crossref | GoogleScholarGoogle Scholar | 28547190PubMed |
Pillay, D., and Branch, G. M. (2011). Bioengineering effects of burrowing thalassinidean shrimps on marine soft-bottom ecosystems. Oceanography and Marine Biology – an Annual Review 49, 137–192.
| Bioengineering effects of burrowing thalassinidean shrimps on marine soft-bottom ecosystems.Crossref | GoogleScholarGoogle Scholar |
Posey, M. H. (1986). Predation on a burrowing shrimp: distribution and community consequences. Journal of Experimental Marine Biology and Ecology 103, 143–161.
| Predation on a burrowing shrimp: distribution and community consequences.Crossref | GoogleScholarGoogle Scholar |
Reidenauer, J. A., and Thistle, D. (1981). Response of a soft-bottom harpacticoid community to stingray (Dasyatis sabina) disturbance. Marine Biology 65, 261–267.
| Response of a soft-bottom harpacticoid community to stingray (Dasyatis sabina) disturbance.Crossref | GoogleScholarGoogle Scholar |
Ripple, W. J., Estes, J. A., Schmitz, O. J., Constant, V., Kaylor, M. J., Lenz, A., Motley, J. L., Self, K. E., Taylor, D. S., and Wolf, C. (2016). What is a trophic cascade? Trends in Ecology & Evolution 31, 842–849.
| What is a trophic cascade?Crossref | GoogleScholarGoogle Scholar |
Robertson, A. I. (1977). Ecology of juvenile King George whiting Sillaginodes punctatus (Cuvier & Valenciennes) (Pisces: Perciforms) in Western Port, Victoria. Australian Journal of Marine and Freshwater Research 28, 35–43.
| Ecology of juvenile King George whiting Sillaginodes punctatus (Cuvier & Valenciennes) (Pisces: Perciforms) in Western Port, Victoria.Crossref | GoogleScholarGoogle Scholar |
Saglam, H., Orhan, A. K., Kutlu, S., and Aydin, İ. (2010). Diet and feeding strategy of the common stingray Dasyatis pastinaca (Linnaeus, 1758) on the Turkish coast of southeastern Black Sea. Cahiers de Biologie Marine 51, 37–44.
Shimoda, K., Wardiatno, Y., Kubo, K., and Tamaki, A. (2005). Intraspecific behaviors and major cheliped sexual dimorphism in three congeneric callianassid shrimp. Marine Biology 146, 543–557.
| Intraspecific behaviors and major cheliped sexual dimorphism in three congeneric callianassid shrimp.Crossref | GoogleScholarGoogle Scholar |
Shimoda, K., Aramaki, Y., Nasuda, J., Yokoyama, H., Ishihi, Y., and Tamaki, A. (2007). Food sources for three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan, as determined by carbon and nitrogen stable isotope analysis. Journal of Experimental Marine Biology and Ecology 342, 292–312.
| Food sources for three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan, as determined by carbon and nitrogen stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |
Snelson, F. F., Williams-Hooper, S. E., and Schmid, T. H. (1988). Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia 1988, 729–739.
| Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons.Crossref | GoogleScholarGoogle Scholar |
Somiya, R., and Tamaki, A. (2017). Unraveling mating behavior for Axiidea (Crustacea: Decapoda): burrow-dwelling callianassid shrimp in intertidal sandflat. Journal of Experimental Marine Biology and Ecology 486, 305–313.
| Unraveling mating behavior for Axiidea (Crustacea: Decapoda): burrow-dwelling callianassid shrimp in intertidal sandflat.Crossref | GoogleScholarGoogle Scholar |
Stokes, M. D., and Holland, N. D. (1992). Southern stingray (Dasyatis americana) feeding on lancelets (Branchiostoma floridae). Journal of Fish Biology 41, 1043–1044.
| Southern stingray (Dasyatis americana) feeding on lancelets (Branchiostoma floridae).Crossref | GoogleScholarGoogle Scholar |
Suzuki, K., Yamaguchi, K., Kadowaki, T., Kadowaki, S., Matsumoto, H., and Nakamura, M. (2018). Predatory characteristics of the red stingray Dasyatis akajei for the commercially important clams in the Hii River system. Laguna 25, 31–38.
Takeuchi, S., and Tamaki, A. (2014). Assessment of benthic disturbance associated with stingray foraging for ghost shrimp by aerial survey over an intertidal sandflat. Continental Shelf Research 84, 139–157.
| Assessment of benthic disturbance associated with stingray foraging for ghost shrimp by aerial survey over an intertidal sandflat.Crossref | GoogleScholarGoogle Scholar |
Takeuchi, S., Takahara, Y., Agata, Y., Nasuda, J., Yamada, F., and Tamaki, A. (2013). Response of suspension-feeding clams to natural removal of bioturbating shrimp on a large estuarine intertidal sandflat in western Kyushu, Japan. Journal of Experimental Marine Biology and Ecology 448, 308–320.
| Response of suspension-feeding clams to natural removal of bioturbating shrimp on a large estuarine intertidal sandflat in western Kyushu, Japan.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A. (1984). Structural characteristics of an intertidal sand flat in Tomioka Bay, Amakusa, west Kyushu. Publications from the Amakusa Marine Biological Laboratory, Kyushu University 7, 125–150.
Tamaki, A. (1987). Comparison of resistivity to transport by wave action in several polychaete species on an intertidal sand flat. Marine Ecology Progress Series 37, 181–189.
| Comparison of resistivity to transport by wave action in several polychaete species on an intertidal sand flat.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A. (1994). Extinction of the trochid gastropod, Umbonium (Suchium) moniliferum (Lamarck), and associated species on an intertidal sandflat. Researches on Population Ecology 36, 225–236.
| Extinction of the trochid gastropod, Umbonium (Suchium) moniliferum (Lamarck), and associated species on an intertidal sandflat.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., and Ingole, B. (1993). Distribution of juvenile and adult ghost shrimps, Callianassa japonica Ortmann (Thalassinidea), on an intertidal sand flat: intraspecific facilitation as a possible pattern-generating factor. Journal of Crustacean Biology 13, 175–183.
| Distribution of juvenile and adult ghost shrimps, Callianassa japonica Ortmann (Thalassinidea), on an intertidal sand flat: intraspecific facilitation as a possible pattern-generating factor.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., and Kikuchi, T. (1983). Spatial arrangement of macrobenthic assemblages on an intertidal sand flat, Tomioka Bay, west Kyushu. Publications from the Amakusa Marine Biological Laboratory, Kyushu University 7, 41–60.
Tamaki, A., and 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. Journal of Shellfish Research 35, 921–967.
| 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.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., and Ueno, H. (1998). Burrow morphology of two callianassid shrimps, Callianassa japonica Ortmann, 1891 and Callianassa sp. (=C. japonica: de Man, 1928) (Decapoda: Thalassinidea). Crustacean Research 27, 28–39.
| Burrow morphology of two callianassid shrimps, Callianassa japonica Ortmann, 1891 and Callianassa sp. (=C. japonica: de Man, 1928) (Decapoda: Thalassinidea).Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., Miyamoto, S., Yamazaki, T., and Nojima, S. (1992). Abundance pattern of the ghost shrimp Callianassa japonica Ortmann (Thalassinidea) and the snake eel Pisodonophis cancrivorus (Richardson) (Pisces, Ophichthidae) and their possible interaction on an intertidal sand flat. Benthos Research 43, 11–22.
| Abundance pattern of the ghost shrimp Callianassa japonica Ortmann (Thalassinidea) and the snake eel Pisodonophis cancrivorus (Richardson) (Pisces, Ophichthidae) and their possible interaction on an intertidal sand flat.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., Tanoue, H., Itoh, J., and Fukuda, Y. (1996). Brooding and larval developmental periods of the callianassid ghost shrimp, Callianassa japonica (Decapoda: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom 76, 675–689.
| Brooding and larval developmental periods of the callianassid ghost shrimp, Callianassa japonica (Decapoda: Thalassinidea).Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., Ingole, B., Ikebe, K., Muramatsu, K., Taka, M., and Tanaka, M. (1997). Life history of the ghost shrimp, Callianassa japonica Ortmann (Decapoda: Thalassinidea), on an intertidal sandflat in western Kyushu, Japan. Journal of Experimental Marine Biology and Ecology 210, 223–250.
| Life history of the ghost shrimp, Callianassa japonica Ortmann (Decapoda: Thalassinidea), on an intertidal sandflat in western Kyushu, Japan.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., Nakaoka, A., Maekawa, H., and Yamada, F. (2008). Spatial partitioning between species of the phytoplankton-feeding guild on an estuarine intertidal sand flat and its implication on habitat carrying capacity. Estuarine, Coastal and Shelf Science 78, 727–738.
| Spatial partitioning between species of the phytoplankton-feeding guild on an estuarine intertidal sand flat and its implication on habitat carrying capacity.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., Saitoh, Y., Itoh, J., Hongo, Y., Sen-ju, S., Takeuchi, S., and Ohashi, S. (2013). Morphological character changes through decapodid-stage larva and juveniles in the ghost shrimp Nihonotrypaea harmandi from western Kyushu, Japan: clues for inferring pre- and post-settlement states and processes. Journal of Experimental Marine Biology and Ecology 443, 90–113.
| Morphological character changes through decapodid-stage larva and juveniles in the ghost shrimp Nihonotrypaea harmandi from western Kyushu, Japan: clues for inferring pre- and post-settlement states and processes.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., Kagesawa, T., Takeuchi, S., Ohashi, H., Yang, S., and Sassa, S. (2018a). Facultative commensalism of a free-burrowing urothoid amphipod with a deep burrow-dwelling callianassid shrimp in intertidal sand. Marine Biology 165, 36.
| Facultative commensalism of a free-burrowing urothoid amphipod with a deep burrow-dwelling callianassid shrimp in intertidal sand.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., Itoh, J., Hongo, Y., Takeuchi, S., and Takikawa, T. (2018b). Normal delayed establishment of a semilunar brooding and larval release cycle in the course of the reproductive season of the ghost shrimp population on a warm temperate intertidal sandflat. Journal of Shellfish Research 37, 529–570.
| Normal delayed establishment of a semilunar brooding and larval release cycle in the course of the reproductive season of the ghost shrimp population on a warm temperate intertidal sandflat.Crossref | GoogleScholarGoogle Scholar |
Tamaki, A., Itoh, J., Takeuchi, S., and Takikawa, T. (in press). Semilunar postlarval settlement periodicity ensuing from semilunar larval release cycle in the Nihonotrypaea harmandi (Crustacea, Decapoda, Axiidea, Callianassidae) population on an intertidal sandflat in an open marine coastal embayment. Population Ecology , POPE12042.
| Semilunar postlarval settlement periodicity ensuing from semilunar larval release cycle in the Nihonotrypaea harmandi (Crustacea, Decapoda, Axiidea, Callianassidae) population on an intertidal sandflat in an open marine coastal embayment.Crossref | GoogleScholarGoogle Scholar |
Taniuchi, T., and Shimizu, M. (1993). Dental sexual dimorphism and food habits in the stingray Dasyatis akajei from Tokyo Bay, Japan. Nippon Suisan Gakkaishi 59, 53–60.
| Dental sexual dimorphism and food habits in the stingray Dasyatis akajei from Tokyo Bay, Japan.Crossref | GoogleScholarGoogle Scholar |
Thompson, R. K., and Pritchard, A. W. (1969). Respiratory adaptations of two burrowing crustaceans, Callianassa californiensis and Upogebia pugettensis (Decapoda, Thalassinidea). The Biological Bulletin 136, 274–287.
| Respiratory adaptations of two burrowing crustaceans, Callianassa californiensis and Upogebia pugettensis (Decapoda, Thalassinidea).Crossref | GoogleScholarGoogle Scholar |
Thrush, S. F., Pridmore, R. D., Hewitt, J. E., and Cummings, V. J. (1991). Impact of ray feeding disturbances on sandflat macrobenthos: do communities dominated by polychaetes or shellfish respond differently? Marine Ecology Progress Series 69, 245–252.
| Impact of ray feeding disturbances on sandflat macrobenthos: do communities dominated by polychaetes or shellfish respond differently?Crossref | GoogleScholarGoogle Scholar |
Thrush, S. F., Pridmore, R. D., Bell, R. G., Cummings, V. J., Dayton, P. K., Ford, R., Grant, J., Green, M. O., Hewitt, J. E., Hines, A. H., Hume, T. M., Lawrie, S. M., Legendre, P., McArdle, B. H., Morrisey, D., Schneider, D. C., Turner, S. J., Walters, R. A., Whitlatch, R. B., and Wilkinson, M. R. (1997). The sandflat habitat: scaling from experiments to conclusions. Journal of Experimental Marine Biology and Ecology 216, 1–9.
| The sandflat habitat: scaling from experiments to conclusions.Crossref | GoogleScholarGoogle Scholar |
Tillett, B. J., Tibbetts, I. R., and Whithead, D. L. (2008). Foraging behavior and prey discrimination in the bluespotted maskray Dasyatis kuhlii. Journal of Fish Biology 73, 1554–1561.
| Foraging behavior and prey discrimination in the bluespotted maskray Dasyatis kuhlii.Crossref | GoogleScholarGoogle Scholar |
VanBlaricom, G. R. (1982). Experimental analyses of structural regulation in a marine sand community exposed to oceanic swell. Ecological Monographs 52, 283–305.
| Experimental analyses of structural regulation in a marine sand community exposed to oceanic swell.Crossref | GoogleScholarGoogle Scholar |
Wada, M., Urakawa, T., and 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, 657–666.
| Dynamics of bacterial community structure on intertidal sandflat inhabited by the ghost shrimp Nihonotrypaea harmandi (Decapoda: Axiidea: Callianassidae) in Tomioka Bay, Amakusa, Japan.Crossref | GoogleScholarGoogle Scholar | 26497271PubMed |
Wardiatno, Y., and Tamaki, A. (2001). Bivariate discriminant analysis for the identification of Nihonotrypaea japonica and N. harmandi (Decapoda: Thalassinidea: Callianassidae). Journal of Crustacean Biology 21, 1042–1048.
| Bivariate discriminant analysis for the identification of Nihonotrypaea japonica and N. harmandi (Decapoda: Thalassinidea: Callianassidae).Crossref | GoogleScholarGoogle Scholar |
Wardiatno, Y., Shimoda, K., Koyama, K., and 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 Research 58, 51–73.
| 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.Crossref | GoogleScholarGoogle Scholar |
Weitkamp, L. A., Wissmar, R. C., and Simenstad, C. A. (1992). Gray whale foraging on ghost shrimp (Callianassa californiensis) in littoral sand flats of Puget Sound, U.S.A. Canadian Journal of Zoology 70, 2275–2280.
| Gray whale foraging on ghost shrimp (Callianassa californiensis) in littoral sand flats of Puget Sound, U.S.A.Crossref | GoogleScholarGoogle Scholar |
Yamaguchi, A. (2005). On the yearly catch variation of rays in Ariake Sound. Report of Japanese Society for Elasmobranch Studies 41, 8–12.
Yamahira, K., Kikuchi, T., and Nojima, S. (1996). Age specific food utilization and spatial distribution of the puffer, Takifugu niphobles, over an intertidal sand flat. Environmental Biology of Fishes 45, 311–318.
| Age specific food utilization and spatial distribution of the puffer, Takifugu niphobles, over an intertidal sand flat.Crossref | GoogleScholarGoogle Scholar |