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

Volumn 342, Issue 2, 2007, Pages 292-312

  Shimoda, Katsumasa ^a   Aramaki, Yosuke ^a   Nasuda, Jun ^a   Yokoyama, Hisashi ^b   Ishihi, Yuka ^b   Tamaki, Akio ^a  

^a NAGASAKI UNIVERSITY   (Japan)

^b FISHERIES RESEARCH AGENCY   (Japan)

Author keywords

Benthic microalga; Boulder beach; Callianassid shrimp; Estuary; Food source; Intertidal sandflat; Phytoplankton; Seaweed; Stable isotope

Indexed keywords

CARBON ISOTOPE; CRUSTACEAN; FOOD SELECTION; FOOD WEB; HABITAT SELECTION; HABITAT TYPE; ISOTOPIC ANALYSIS; NITROGEN ISOTOPE; PHYTOPLANKTON; SPECIES-AREA RELATIONSHIP;

ARIAKE BAY; ASIA; EURASIA; FAR EAST; JAPAN; KYUSHU;

CALLIANASSIDAE; DECAPODA (CRUSTACEA); NIHONOTRYPAEA; NIHONOTRYPAEA HARMANDI; NIHONOTRYPAEA JAPONICA; NIHONOTRYPAEA PETALURA; SARGASSUM; THALASSINIDEA; ULVA COMPRESSA;

EID: 33847326875     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2006.11.003     Document Type: Article

References (85)

1. Abed-Navandi D., and Dworschak P.C. Food sources of tropical thalassinidean shrimps: a stable-isotope study. Mar. Ecol. Prog. Ser. 291 (2005) 159-168
2. Abed-Navandi D., Koller H., and Dworschak P.C. Nutritional ecology of thalassinidean shrimps constructing burrows with debris chambers: the distribution and use of macronutrients and micronutrients. Mar. Biol. Res. 1 3 (2005) 202-215
3. Atkinson R.J.A., and Taylor A.C. Aspects of the physiology, biology and ecology of the thalassinidean shrimps in relation to their burrow environment. Oceanogr. Mar. Biol. Ann. Rev. 43 (2005) 519-575
4. Berkenbusch K., and Rowden A.A. Ecosystem engineering - moving away from 'just-so' stories. N. Z. J. Ecol. 27 1 (2003) 67-73
5. Boon P.I., Bird F.L., and Bunn S.E. Diet of the intertidal callianassid shrimps Biffarius arenosus and Trypea australiensis (Decapoda: Thalassinidea) in Western Port (southern Australia), determined with multiple stable-isotope analyses. Mar. Freshw. Res. 48 6 (1997) 503-511
6. Cahoon L.B. The role of benthic microalgae in neritic ecosystems. Oceanogr. Mar. Biol. Ann. Rev. 37 (1999) 47-86
7. Cifuentes L.A., Sharp J.H., and Fogel M.L. Stable carbon and nitrogen isotope biogeochemistry in the Delaware estuary. Limnol. Oceanogr. 33 5 (1988) 1102-1115
8. Cividanes S., Incera M., and López J. Temporal variability in the biochemical composition of sedimentary organic matter in an intertidal flat of the Galician coast (NW Spain). Oceanol. Acta 25 1 (2002) 1-12
9. Coelho V.R., and Rodrigues S.A. Trophic behaviour and functional morphology of the feeding appendages of the laomediid shrimp Axianassa australis (Crustacea: Decapoda: Thalassinidea). J. Mar. Biol. Assoc. U.K. 81 3 (2001) 441-454
10. Coelho V.R., and Rodrigues S.A. Setal diversity, trophic modes and functional morphology of feeding appendages of two callianassid shrimps, Callichirus major and Sergio mirim (Decapoda: Thalassinidea: Callianassidae). J. Nat. Hist. 35 10 (2001) 1447-1483
11. Coelho V.R., Williams A.B., and Rodrigues S.A. Trophic strategies and functional morphology of feeding appendages, with emphasis on setae, of Upogebia omissa and Pomatogebia operculata (Decapoda: Thalassinidea: Upogebiidae). Zool. J. Linn. Soc. 130 4 (2000) 567-602
12. Couch C.A. Carbon and nitrogen stable isotopes of meiobenthos and their food resources. Estuar. Coast. Shelf Sci. 28 4 (1989) 433-441
13. Dworschak P.C. Feeding behaviour of Upogebia pusilla and Callianassa tyrrhena (Crustacea, Decapoda, Thalassinidea). Invest. Pesq. 51 1 (1987) 421-429
14. Dworschak P.C. The burrows of Callianassa candida (Olivi 1972) and C. whitei Sakai 1999 (Crustacea: Decapoda: Thalassinidea). In: Bright M., Dworschak P.C., and Stachowitsch M. (Eds). The Vienna School of Marine Biology: A Tribute to Jörg Ott (2002), Facultas Universitätsverlag, Vienna 63-71
15. Dworschak P.C. Biology of Mediterranean and Caribbean Thalassinidea (Decapoda). In: Tamaki A. (Ed). 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 (2004), Nagasaki University, Nagasaki 15-22
16. Dworschak P.C. Global diversity in the Thalassinidea (Decapoda): an update (1998-2004). Nauplius 13 1 (2005) 57-63
17. Dworschak P.C., and Ott J.A. Decapod burrows in mangrove-channel and back-reef environments at the Atlantic Barrier Reef, Belize. Ichnos 2 4 (1993) 277-290
18. Dworschak P.C., Koller H., and Abed-Navandi D. Burrow structure, burrowing and feeding behaviour of Corallianassa longiventris and Pestarella tyrrhena (Crustacea, Thalassinidea, Callianassidae). Mar. Biol. 148 4 (2006) 1369-1382
19. Felder D.L. Diversity and ecological significance of deep-burrowing macrocrustaceans in coastal tropical waters of the Americas (Decapoda: Thalassinidea). Interciencia 26 10 (2001) 440-449
20. Flach E., and Tamaki A. Competitive bioturbators on intertidal sand flats in the European Wadden Sea and Ariake Sound in Japan. In: Reise K. (Ed). Ecological Studies. Ecological Comparisons of Sedimentary Shores vol. 151 (2001), Springer, Berlin 149-171
21. 13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib. Mar. Sci. 27 (1984) 13-47
22. Gearing J.N., Gearing P.J., Rudnick D.T., Requejo A.G., and Hutchins M.J. Isotopic variability of organic carbon in a phytoplankton-based, temperate estuary. Geochim. Cosmochim. Acta 48 5 (1984) 1089-1098
23. Griffis R.B., and Chavez F.L. Effects of sediment type on burrows of Callianassa californiensis Dana and C. gigas Dana. J. Exp. Mar. Biol. Ecol. 117 3 (1988) 239-253
24. Griffis R.B., and Suchanek T.H. A model of burrow architecture and trophic modes in thalassinidean shrimp (Decapoda: Thalassinidea). Mar. Ecol. Prog. Ser. 79 1-2 (1991) 171-183
25. Hailstone T.S., and Stephenson W. The biology of Callianassa (Trypaea) australiensis Dana 1852 (Crustacea, Thalassinidea). Univ. Queensl. Pap., Dep. Zool. 1 (1961) 259-285
26. Hart E.A., and Lovvorn J.R. Algal vs. macrophyte inputs to food webs of inland saline wetlands. Ecology 84 12 (2003) 3317-3326
27. Herman P.M.J., Middelburg J.J., Widdows J., Lucas C.H., and Heip C.H.R. Stable isotopes as trophic tracers: combining field sampling and manipulative labelling of food resources for macrobenthos. Mar. Ecol. Prog. Ser. 204 (2000) 79-92
28. Ishihi Y., Yamada Y., Ajisaka T., and Yokoyama H. Distribution of stable carbon isotope ratio in Sargassum plants. Fish. Sci. 67 2 (2001) 367-369
29. Kang C.K., Sauriau P.G., Richard P., and Blanchard G.F. Food sources of the infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-Oléron Bay, as determined by analyses of carbon and nitrogen stable isotopes. Mar. Ecol. Prog. Ser. 187 (1999) 147-158
30. Kang C.K., Kim J.B., Lee K.S., Kim J.B., Lee P.Y., and Hong J.S. Trophic importance of benthic microalgae to macrozoobenthos in coastal bay systems in Korea: dual stable C and N isotope analyses. Mar. Ecol. Prog. Ser. 259 (2003) 79-92
31. Kendall C. Tracing nitrogen sources and cycling in catchments. In: Kendall C., and McDonnell J.J. (Eds). Isotope Tracers in Catchments Hydrology (1998), Elsevier Publishers B.V., Amsterdam 519-575
32. Kimura H., Harada K., Hara K., and Tamaki A. Enzymatic approach to fungal association with arthropod guts: a case study for the crustacean host, Nihonotrypaea harmandi, and its foregut fungus, Enteromyces callianassae. P.S.Z.N.: Mar. Ecol. 23 (2002) 157-183
33. Kubo K., Shimoda K., and Tamaki A. Egg size and clutch size in three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan. J. Mar. Biol. Assoc. U.K. 86 1 (2006) 103-111
34. Kurata K., Minami H., and Kikuchi E. Stable isotope analysis of food sources for salt marsh snails. Mar. Ecol. Prog. Ser. 223 (2001) 167-177
35. Kwak T.J., and Zedler J.B. Food web analysis of southern California coastal wetlands using multiple stable isotopes. Oecologia 110 2 (1997) 262-277
36. Lucas C.H., Banham C., and Holligan P.M. Benthic-pelagic exchange of microalgae at a tidal flat. 2. Taxonomic analysis. Mar. Ecol. Prog. Ser. 212 (2001) 39-52
37. MacGinitie G.E., and MacGinitie N. Natural History of Marine Animals. 2nd ed. (1968), McGraw-Hill, New York
38. MacIntyre H.L., Geider R.J., and Miller D.C. Microphytobenthos: the ecological role of the 'secret garden' of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19 2 A (1996) 186-201
39. Macko S.A., and Ostrom N.E. Pollution studies using stable isotopes. In: Lajtha K., and Michener R.H. (Eds). Stable Isotopes in Ecology and Environmental Science (1994), Blackwell Scientific Publishers, Oxford 45-62
40. Manning R.B., and Tamaki A. A new genus of ghost shrimp from Japan (Crustacea: Decapoda: Callianassidae). Proc. Biol. Soc. Wash. 111 4 (1998) 889-892
41. McClelland J.W., and Valiela I. Linking nitrogen in estuarine producers to land-derived sources. Limnol. Oceanogr. 43 4 (1998) 577-585
42. Michener R.H., and Schell D.M. Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha K., and Michener R.H. (Eds). Stable Isotopes in Ecology and Environmental Science (1994), Blackwell Scientific Publishers, Oxford 138-157
43. Murphy R.C., and Kremer J.N. Benthic community metabolism and the role of deposit-feeding callianassid shrimp. J. Mar. Res. 50 2 (1992) 321-340
44. Nakatsuka T., Handa N., Wada E., and Wong C.S. The dynamic changes of stable isotopic ratios of carbon and nitrogen in suspended and sedimented particulate organic matter during a phytoplankton bloom. J. Mar. Res. 50 2 (1992) 267-296
45. Nickell L.A., and Atkinson R.J.A. 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 (1995) 181-197
46. Nickell L.A., Atkinson R.J.A., and Pinn E.H. Morphology of thalassinidean (Crustacea: Decapoda) mouthparts and pereiopods in relation to feeding, ecology and grooming. J. Nat. Hist. 32 5 (1998) 733-761
47. Ohno M., Terawaki T., and Honda M. Ecology of Sargassum and creation of artificial seaweed bed in the southern Japan. Bull. Coast. Oceanogr. 27 2 (1990) 127-135 (in Japanese with English abstract)
48. Page H.M. Importance of vascular plant and algal production to macro-invertebrate consumers in a southern California salt marsh. Estuar. Coast. Shelf Sci. 45 6 (1997) 823-834
49. Parsons T.R., Maita Y., and Lalli C.M. A Manual of Chemical and Biological Methods for Seawater Analysis (1984), Pergamon Press, Oxford
50. Pinn E.H., Atkinson R.J.A., and Rogerson A. Particle size selectivity and resource partitioning in five species of Thalassinidea (Crustacea: Decapoda). Mar. Ecol. Prog. Ser. 169 (1998) 243-250
51. Pinn E.H., Atkinson R.J.A., and Rogerson A. The diet of two mud-shrimps, Calocaris macandreae and Upogebia stellata (Crustacea: Decapoda: Thalassinidea). Ophelia 48 3 (1998) 211-223
52. Pinn E.H., Nickell L.A., Rogerson A., and Atkinson R.J.A. Comparison of gut morphology and gut microflora of seven species of mud shrimp (Crustacea: Decapoda: Thalassinidea). Mar. Biol. 133 1 (1999) 103-114
53. Pinn E.H., Nickell L.A., Rogerson A., and Atkinson R.J.A. Comparison of the mouthpart setal fringes of seven species of mud-shrimp (Crustacea: Decapoda: Thalassinidea). J. Nat. Hist. 33 10 (1999) 1461-1485
54. Riera P., and Richard P. Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine bay of Marennes-Oléron. Estuar. Coast. Shelf Sci. 42 3 (1996) 347-360
55. Riera P., Stal L.J., Nieuwenhuize J., Richard P., Blanchard G., and Gentil F. Determination of food sources for benthic invertebrates in a salt marsh (Aiguillon Bay, France) by carbon and nitrogen stable isotopes: importance of locally produced sources. Mar. Ecol. Prog. Ser. 187 (1999) 301-307
56. 15N of size-fractionated plankton at a coastal station in the northern Baltic proper. Mar. Ecol. Prog. Ser. 203 (2000) 47-65
57. Schlacher T.A., and Wooldridge T.H. Origin and trophic importance of detritus-evidence from stable isotopes in the benthos of a small, temperate estuary. Oecologia 106 3 (1996) 382-388
58. Shimoda K., and Tamaki A. Burrow morphology of the ghost shrimp Nihonotrypaea petalura (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan. Mar. Biol. 144 4 (2004) 723-734
59. SPSS. SPSS Base 11.5J (2002), SPSS Japan Inc., Tokyo (In Japanese)
60. Stamhuis E.J., Reede-Dekker T., Van Etten Y., De Wiljes J.J., and Videler J.J. Behaviour and time allocation of the burrowing shrimp Callianassa subterranea (Decapoda, Thalassinidea). J. Exp. Mar. Biol. Ecol. 204 1-2 (1996) 225-239
61. Stamhuis E.J., Dauwe B., and Videler J.J. How to bite the dust: morphology, motion pattern and function of the feeding appendages of the deposit-feeding thalassinid shrimp Callianassa subterranea. Mar. Biol. 132 1 (1998) 43-58
62. Stamhuis E.J., Videler J.J., and De Wilde P.A.W.J. Optimal foraging in the thalassinidean shrimp Callianassa subterranea: improving food quality by grain size selection. J. Exp. Mar. Biol. Ecol. 228 2 (1998) 197-208
63. Stapleton K.L., Long M., and Bird F.L. Comparative feeding ecology of two spatially coexisting species of ghost shrimp, Biffarius arenosus and Trypaea australiensis (Decapoda: Callianassidae). Ophelia 55 3 (2002) 141-150
64. Suetsugi T., Fujita K., Suwa Y., and Yokoyama K. Influence of sediment transport on topography and bed material change at river mouth estuary. Tech. Note Natl. Inst. Land Infrastruc. Manage. 32 (2002) 1-169 (in Japanese)
65. Sullivan M.J., and Moncreiff C.A. Edaphic algae are an important component of salt marsh food-webs: evidence from multiple stable isotope analyses. Mar. Ecol. Prog. Ser. 62 1-2 (1990) 149-159
66. Suzuki R., and Ishimaru T. An improved method for the determination of plankton chlorophyll using N,N-dimethylformamide. J. Oceanogr. Soc. Jpn. 46 (1990) 190-194
67. Tamaki A. Comparison of resistivity to transport by wave action in several polychaete species on an intertidal sand flat. Mar. Ecol. Prog. Ser. 37 (1987) 181-189
68. Tamaki A. Extinction of the trochid gastropod, Umbonium (Suchium) moniliferum (Lamarck), and associated species on an intertidal sandflat. Res. Popul. Ecol. 36 2 (1994) 225-236
69. Tamaki A. A rebuttal to Sakai (2001): "A review of the common Japanese callianassid species, Callianassa japonica and C. petalura (Decapoda, Thalassinidea)". Crustaceana 76 1 (2003) 115-124
70. Tamaki A., and Harada K. Alongshore configuration and size of local populations of the callianassid shrimp Nihonotrypaea harmandi (Bouvier, 1901) (Decapoda: Thalassinidea) in the Ariake-Sound estuarine system, Kyushu, Japan. Crustac. Res. 34 (2005) 65-86
71. Tamaki A., and Suzukawa K. Co-occurrence of the cirolanid isopod Eurydice nipponica Bruce and Jones and the ghost shrimp Callianassa japonica Ortmann on an intertidal sand flat. Ecol. Res. 6 (1991) 87-100
72. Tamaki A., and Ueno H. Burrow morphology of two callianassid shrimps, Callianassa japonica Ortmann, 1891 and Callianassa sp. (= C. japonica: de Man, 1928) (Decapoda: Thalassinidea). Crustac. Res. 27 (1998) 28-39
73. Tamaki A., Ingole B., Ikebe K., Muramatsu K., Taka M., and Tanaka M. 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 (1997) 223-250
74. Tamaki A., Itoh J., and Kubo K. Distributions of three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) in intertidal habitats along an estuary to open-sea gradient in western Kyushu, Japan. Crustac. Res. 28 (1999) 37-51
75. Tezaki K., Iwataki M., Matsuoka K., and Mizushima K. Species composition and seasonal changes of phytoplankton occurring in Ariake Sound (2003-2004). Bull. Fac. Fish., Nagasaki Univ. 86 (2005) 1-10 (in Japanese with English abstract)
76. Underwood G.J.C., and Kromkamp J. Primary production by phytoplankton and microphytobenthos in estuaries. In: Nedwell D.B., and Raffaelli D.G. (Eds). Advances in Ecological Research. Estuaries vol. 29 (1999), Academic Press, San Diego, CA 93-153
77. 14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Mar. Biol. 142 5 (2003) 1009-1018
78. Wainright S.C., and Fry B. Seasonal variation of the stable isotopic compositions of coastal marine plankton from Woods Hole, Massachusetts and Georges Bank. Estuaries 17 3 (1994) 552-560
79. Wardiatno Y., Shimoda K., Koyama K., and Tamaki A. 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 (2003) 51-73
80. Watanabe Y., Kawamura Y., and Handa T. Porphyra (or nori) aquaculture and nutrient condition in the Ariake Bay, Japan. Bull. Coast. Oceanogr. 42 (2004) 47-54 (in Japanese with English abstract)
81. Yamada F., and Kobayashi N. Annual variations of tidal level and mudflat profile. J. Waterw. Port Coast. Ocean Eng. 130 3 (2004) 119-126
82. Yokoyama H., and Ishihi Y. Feeding of the bivalve Theora lubrica on benthic microalgae: isotopic evidence. Mar. Ecol. Prog. Ser. 255 (2003) 303-309
83. Yokoyama H., Higano J., Adachi K., Ishihi Y., Yamada Y., and Pichitkul P. Evaluation of shrimp polyculture system in Thailand based on stable carbon and nitrogen isotope ratios. Fish. Sci. 68 4 (2002) 745-750
84. Yokoyama H., Tamaki A., Harada K., Shimoda K., Koyama K., and Ishihi Y. Variability of diet-tissue isotopic fractionation in estuarine macrobenthos. Mar. Ecol. Prog. Ser. 296 (2005) 115-128
85. Yokoyama H., Tamaki A., Koyama K., Ishihi Y., Shimoda K., and Harada K. Isotopic evidence for phytoplankton as a major food source for macrobenthos on an intertidal sandflat in Ariake Sound, Japan. Mar. Ecol. Prog. Ser. 304 (2005) 101-116