Variable niche size of the giant mangrove whelk Terebralia palustris (Linnaeus, 1767) in a subtropical estuary

Hydrobiologia

Volumn 803, Issue 1, 2017, Pages 265-282

  Raw, Jacqueline L ^a   Perissinotto, Renzo ^a   Bird, Matthew S ^a   Miranda, Nelson A F ^a   Peer, Nasreen ^a  

^a NELSON MANDELA METROPOLITAN UNIVERSITY   (South Africa)

Author keywords

Deposit feeder; Isotopic niche; SIBER; Subtropical mangrove; Trophic niche width

Indexed keywords

DEPOSIT FEEDER; DIET; ESTUARY; GASTROPOD; ISOTOPIC ANALYSIS; LEAF LITTER; MANGROVE; NICHE; NICHE PARTITIONING; PHYTOBENTHOS; STABLE ISOTOPE; SUBTROPICAL REGION; TROPHIC LEVEL;

GASTROPODA; RHIZOPHORACEAE; TEREBRALIA PALUSTRIS;

EID: 85018728480     PISSN: 00188158     EISSN: 15735117     Source Type: Journal    
DOI: 10.1007/s10750-017-3223-2     Document Type: Article

References (103)

1. Alfaro, A. C., 2008. Diet of Littoraria scabra, while vertically migrating on mangrove trees: gut content, fatty acid, and stable isotope analyses. Estuarine, Coastal and Shelf Science 79: 718–726.
2. Alongi, D. M., 1994. Zonation and seasonality of benthic primary production and community respiration in tropical mangrove forests. Oecologia 98: 320–327.
3. Alongi, D. M., 1998. Coastal Ecosystem Processes. CRC, Boca Raton.
4. Alongi, D. M., 2009. Paradigm shifts in mangrove biology. In Perillo, G. M. E., E. Wolanski, D. R. Cahoon & M. M. Brinson (eds), Coastal Wetlands: An Integrated Ecosystem Approach. Elsevier, Amsterdam: 615–640.
5. Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.
6. Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PRIMER+ for PERMANOVA: Guide to Software and Statistical Methods. PRIMER-E Ltd., Plymouth.
7. 13C in the Mondego Estuary food web: seasonal variation in producers and consumers. Marine Environmental Research 67: 109–116.
8. Balvanera, P., A. B. Pfisterer, N. Buchmann, J.-S. He, T. Nakashizuka, D. Raffaelli & B. Schmidt, 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 9: 1146–1156.
9. Bearhop, S., C. E. Adams, S. Waldron, R. A. Fuller & H. MacLeod, 2004. Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73: 1007–1012.
10. Begg, G. W., 1980. The Kosi System: aspects of its biology, management and research. In Bruton, M. N. & K. H. Cooper (eds), Studies on the Ecology of Maputaland. Rhodes University and the Natal Branch of the Wildlife Society of Southern Africa, Durban: 358–373.
11. Bligh, E. G. & W. J. Dyer, 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37: 911–917.
12. Bosire, J. O., F. Dahdouh-Guebas, J. G. Kairo, J. Kazungu, F. Dehairs & N. Koedam, 2005. Litter degradation and CN dynamics in reforested mangrove plantations at Gazi Bay, Kenya. Biological Conservation 126: 287–295.
13. Bouillon, S., N. Koedam, A. Raman & F. Dehairs, 2002. Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests. Oecologia 130: 441–448.
14. Bouillon, S., F. Dahdouh-Guebas, A. V. V. S. Rao, N. Koedam & F. Dehairs, 2003. Sources of organic carbon in mangrove sediments: variability and possible ecological implications. Hydrobiologia 495: 33–39.
15. Bouillon, S., N. Koedam, W. Baeyens, B. Satyanarayana & F. Dehairs, 2004a. Selectivity of subtidal benthic invertebrate communities for local microalgal production in an estuarine mangrove ecosystem during the post-monsoon period. Journal of Sea Research 51: 133–144.
16. Bouillon, S., T. Moens, I. Overmeer, N. Koedam & F. Dehairs, 2004b. Resource utilization patterns of epifauna from mangrove forests with contrasting inputs of local versus imported organic matter. Marine Ecology Progress Series 278: 77–88.
17. Bouillon, S., R. M. Connolly & S. Y. Lee, 2008. Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. Journal of Sea Research 59: 44–58.
18. Brenna, J. T., T. N. Corso, H. J. Tobias & R. J. Caimi, 1997. High-precision continuous-flow isotope ratio mass spectrometry. Mass Spectrometry Reviews 16: 227–258.
19. Bui, T. H. H. & S. Y. Lee, 2014. Does ‘You are what you eat’ apply to mangrove grapsid crabs? PLoS ONE 9: e89074.
20. Cahoon, L. B., J. E. Nearhoof & C. L. Tilton, 1999. Sediment grain size effect on benthic microalgal biomass in shallow aquatic ecosystems. Estuaries 22: 735–741.
21. Cannicci, S., D. Burrows, S. Fratini, T. Smith III, J. Offenberg & F. Dahdouh-Guebas, 2008. Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review. Aquatic Botany 89: 186–200.
22. Claessen, D., C. Van Oss, A. de Roos & L. Persson, 2002. The impact of size-dependent predation on population dynamics and individual life history. Ecology 83: 1660–1675.
23. Clarke, K. R. & R. N. Gorley, 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E: Plymouth Marine Laboratory, Plymouth.
24. Clarke, K. R. & R. M. Warwick, 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd ed. PRIMER-E: Plymouth Marine Laboratory, Plymouth.
25. Cloern, J. E. & A. D. Jassby, 2008. Complex seasonal patterns of primary producers at the land–sea interface. Ecology Letters 11: 1294–1303.
26. DeNiro, M. J. & S. Epstein, 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42: 495–506.
27. DeNiro, M. J. & S. Epstein, 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45: 341–351.
28. Doi, H., E. Kikuchi, S. Takagi & S. Shikano, 2006. Selective assimilation by deposit feeders: experimental evidence using stable isotope ratios. Basic and Applied Ecology 7: 159–166.
29. Ehleringer, J. R., N. Buchmann & L. B. Flanagan, 2000. Carbon isotope ratios in belowground carbon cycle processes. Ecological Applications 10: 412–422.
30. Emmerson, W. D. & L. E. McGwynne, 1992. Feeding and assimilation of mangrove leaves by the crab Sesarma meinerti de Man in relation to leaf-litter production in Mgazana, a warm-temperate southern African mangrove swamp. Journal of Experimental Marine Biology and Ecology 157: 51–53.
31. Feller, I. C., C. E. Lovelock, U. Berger, K. L. McKee, S. B. Joye & M. C. Ball, 2010. Biocomplexity in mangrove ecosystems. Annual Review of Marine Science 2: 395–417.
32. Feulner, G. R., 2000. The large mangrove mud creeper Terebralia palustris (Linnaeus, 1767) in non-mangrove environments in southeastern Arabia. Tribulus 10: 15–26.
33. Finke, D. L. & W. E. Snyder, 2008. Niche partitioning increases resource exploitation by diverse communities. Science 321: 1488–1490.
34. Flint, R. W. & R. D. Kalke, 1986. Niche characterization of dominant estuarine benthic species. Estuarine, Coastal and Shelf Science 22: 657–674.
35. 15N) of mangroves and lichens in an oligotrophic, microbially-influenced ecosystem. Biogeosciences 5: 1693–1704.
36. Fox, J. & S. Weisberg, 2014. An {R} Companion to Applied Regression. 2.1-3 Edn. Sage, Thousand Oaks.
37. Fratini, S., S. Cannicci & M. Vannini, 2000. Competition and interaction between Neosarmatium smithi (Crustacea: Grapsidae) and Terebralia palustris (Mollusca: Gastropoda) in a Kenyan mangrove. Marine Biology 137: 309–316.
38. Fratini, S., S. Cannicci & M. Vannini, 2001. Feeding clusters and olfaction in the mangrove snail Terebralia palustris (Linnaeus) (Potamididae: Gastropoda). Journal of Experimental Marine Biology and Ecology 261: 173–183.
39. Fratini, S., V. Vigiani, M. Vannini & S. Cannicci, 2004. Terebralia palustris (Gastropoda; Potamididae) in a Kenyan mangal: size structure, distribution and impact on the consumption of leaf litter. Marine Biology 144: 1173–1182.
40. Fratini, S., M. Vannini & S. Cannicci, 2008. Feeding preferences and food searching strategies mediated by air- and water-borne cues in the mud whelk Terebralia palustris (Potamididae: Gastropoda). Journal of Experimental Marine Biology and Ecology 362: 26–31.
41. Gladstone-Gallagher, R. V., C. J. Lundquist & C. A. Pilditch, 2014. Response of temperate intertidal benthic assemblages to mangrove detrital inputs. Journal of Experimental Marine Biology and Ecology 460: 80–88.
42. Guest, M. & R. Connolly, 2004. Fine-scale movement and assimilation of carbon in saltmarsh and mangrove habitat by resident animals. Aquatic Ecology 38: 599–609.
43. Hammerschlag-Peyer, C. M., L. A. Yeager, M. S. Araújo & C. A. Layman, 2011. A hypothesis-testing framework for studies investigating ontogenetic niche shifts using stable isotope ratios. PLoS ONE 6: e27104.
44. Hart, E. A. & J. R. Lovvorn, 2003. Algal vs. macrophyte inputs to food webs of inland saline wetlands. Ecology 84: 3317–3326.
45. Herbon, C. M. & I. Nordhaus, 2013. Experimental determination of stable carbon and nitrogen isotope fractionation between mangrove leaves and crabs. Marine Ecology Progress Series 490: 91–105.
46. Houbrick, R. S., 1991. Systematic review and functional morphology of the mangrove snails Terebralia and Telescopium (Potamididae; Prosobranchia). Malacologia 33: 289–338.
47. 34S signals. Marine Ecology Progress Series 227: 145–155.
48. Imgraben, S. & S. Dittmann, 2008. Leaf litter dynamics and litter consumption in two temperate South Australian mangrove forests. Journal of Sea Research 59: 83–93.
49. Jackson, A. L., R. Inger, A. C. Parnell & S. Bearhop, 2011. Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80: 595–602.
50. Jacob, U., K. Mintenbeck, T. Brey, R. Knust & K. Beyer, 2005. Stable isotope food web studies: a case for standardized sample treatment. Marine Ecology Progress Series 287: 251–253.
51. Knoppers, B., 1994. Aquatic primary production in coastal lagoons. In Kjerfve, B. (ed.), Coastal Lagoon Processes. Elsevier, Amsterdam.
52. Komiyama, A., J. E. Ong & S. Poungparn, 2008. Allometry, biomass, and productivity of mangrove forests: a review. Aquatic Botany 89: 128–137.
53. Kon, K., H. Kurokura & K. Hayashizaki, 2007. Role of microhabitats in food webs of benthic communities in a mangrove forest. Marine Ecology Progress Series 340: 55–62.
54. Kon, K., H. Kurokura & P. Tongnunui, 2011. Influence of a microhabitat on the structuring of the benthic macrofaunal community in a mangrove forest. Hydrobiologia 671: 205–216.
55. Kyle, R. & C. Ward, 1995. Kosi Bay Nature Reserve, South Africa: Information Sheet for the Site Designated to the List of Wetlands of International Importance in Terms of the Convention on Wetlands of International Importance, Especially as Waterfowl Habitat.
56. Layman, C. A., D. A. Arrington, C. G. Montana & D. M. Post, 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42–48.
57. Lee, S. Y., 1998. Ecological role of grapsid crabs in mangrove ecosystems: a review. Marine and Freshwater Research 49: 335–343.
58. Lee, S. Y., J. H. Primavera, F. Dahdouh-Guebas, K. McKee, J. O. Bosire, S. Cannicci, K. Diele, F. Fromard, N. Koedam, C. Marchand, I. Mendelssohn, N. Mukherjee & S. Record, 2014. Ecological role and services of tropical mangrove ecosystems: a reassessment. Global Ecology and Biogeography 23: 726–743.
59. Levin, L. A., D. F. Boesch, A. Covich, C. Dahm, C. Erseus, K. C. Ewel, R. T. Kneib, A. Moldenke, M. A. Palmer, P. Snelgrove, D. Strayer & J. M. Welawski, 2001. The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4: 430–451.
60. Liu, W., J. Zhang, G. Tian, H. Xu & X. Yan, 2013. Temporal and vertical distribution of microphytobenthos biomass in mangrove sediments of Zhujiang (Pearl River) Estuary. Acta Oceanologica Sinica 32: 82–88.
61. Loreau, M. & W. Ebenhoh, 1994. Competitive-exclusion and coexistence of species with complex life-cycles. Theoretical Population Biology 46: 58–77.
62. Mackey, A. P. & G. Smail, 1996. The decomposition of mangrove litter in a subtropical mangrove forest. Hydrobiologia 332: 93–98.
63. Mazumder, D. & N. Saintilan, 2010. Mangrove leaves are not an important source of dietary carbon and nitrogen for crabs in temperate Australian mangroves. Wetlands 30: 375–380.
64. Mazumder, D., R. J. Williams, D. Reid, N. Saintilan & R. Szymczak, 2008. Variability of stable isotope ratios of glassfish (Ambassis jacksoniensis) from mangrove environments in southeast Australia and implications for choosing sample size. Environmental Bioindicators 3: 114–123.
65. Mazumder, D., R. J. Williams, L. Wen, N. Saintilan & C. T. Walsh, 2016. Impoundment constraint of fish niche diversity in a temperate Australian river. Hydrobiologia. doi:10.1007/s10750-015-2630-5.
66. McCutchan, J. H., W. M. Lewis, C. Kendall & C. C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378–390.
67. Middelburg, J., 2014. Stable isotopes dissect aquatic food webs from the top to the bottom. Biogeosciences 11: 2357–2371.
68. Miranda, N. A. F. & R. Perissinotto, 2012. Stable isotope evidence for dietary overlap between alien and native gastropods in coastal lakes of northern KwaZulu-Natal, South Africa. PLoS ONE 7: e31897.
69. Morrisey, D. J., A. Swales, S. Dittmann, M. A. Morrison, C. E. Lovelock & C. M. Beard, 2010. The ecology and management of temperate mangroves. Annual Review of Oceanography and Marine Biology 48: 43–160.
70. Newell, R. I. E., N. Marshall, A. Sasekumar & V. C. Chong, 1995. Relative importance of benthic microalgae, phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia. Marine Biology 123: 595–606.
71. Newsome, S. D., C. Martinez del Rio, S. Bearhop & D. L. Phillips, 2007. A niche for isotopic ecology. Frontiers in Ecology and the Environment 5: 429–436.
72. Nishihira, M., M. Kuniyoshi & K. Shimamura, 2002. Size variation in Terebralia palustris (Gastropoda: Potamididae) of Irimote Island, southern Japan, and its effect on some population characteristics. Wetlands Ecology and Management 10: 243–247.
73. Nozais, C., R. Perissinotto & S. Mundree, 2001. Annual cycle of microalgal biomass in a South African temporarily-open estuary: nutrient versus light limitation. Marine Ecology Progress Series 223: 39–48.
74. Oakes, J. M., R. M. Connolly & A. T. Revill, 2010. Isotope enrichment in mangrove forests separates microphytobenthos and detritus as carbon sources for animals. Limnology and Oceanography 55: 393–402.
75. Ólafsson, E., S. Buchmayer & M. W. Skov, 2002. The East African decapod crab Neosarmatium meinerti (de Man) sweeps mangrove floors clean of leaf litter. Ambio 31: 569–573.
76. Pagliosa, P. R., M. S. Oortman, A. S. Rovai & E. J. Soriano-Sierra, 2016. Is mangrove planting insufficient for benthic macrofaunal recovery when environmental stress is persistent? Ecological Engineering 95: 290–301.
77. Pape, E., A. Muthumbi, C. P. Kamanu & A. Vanreusel, 2008. Size-dependent distribution and feeding habits of Terebralia palustris in mangrove habitats of Gazi Bay, Kenya. Estuarine, Coastal and Shelf Science 76: 797–808.
78. Pearman, P. B., A. Guisan, O. Broennimann & C. F. Randin, 2008. Niche dynamics in space and time. Trends in Ecology and Evolution 23: 149–158.
79. Penha-Lopes, G., S. Bouillon, P. Mangion, A. Macia & J. Paula, 2009. Population structure, density and food sources of Terebralia palustris (Potamididae: Gastropoda) in a low intertidal Avicennia marina mangrove stand (Inhaca Island, Mozambique). Estuarine, Coastal and Shelf Science 84: 318–325.
80. Perissinotto, R., C. Nozais & I. Kibirige, 2002. Spatio-temporal dynamics of phytoplankton and microphytobenthos in a South African temporarily-open estuary. Estuarine, Coastal and Shelf Science 54: 363–374.
81. Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320.
82. Phillips, D. L., R. Inger, S. Bearhop, A. L. Jackson, J. W. Moore, A. C. Parnell, B. X. Semmens & E. J. Ward, 2014. Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92: 823–835.
83. Pianka, E. R., 1976. Competition and niche theory. In May, R. M. (ed.), Theoretical Ecology, Principals and Practices. W. B. Saunders Co., Philadelphia: 114–141.
84. Pohlert, E. R., 2014. The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR). http://CRAN.R-project.org/package=PMCMR
85. Polis, G. A. & D. R. Strong, 1996. Food web complexity and community dynamics. American Naturalist 147: 813–846.
86. Post, D. M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718.
87. R Development Core Team, 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
88. Rajkaran, A. & J. B. Adams, 2011. Mangrove forests of Northern Kwa-Zulu Natal: sediment conditions and population structure of the largest mangrove forests in South Africa. West Indian Ocean Journal of Marine Science 10: 25–38.
89. Raw, J. L., R. Perissinotto, N. A. F., Miranda & N. Peer, 2017. Feeding dynamics of Terebralia palustris (Gastropoda: Potamididae) from a subtropical mangrove ecosystem. Molluscan Research. doi:10.1080/13235818.2017.1323370
90. Raw, J. L., R. Perissinotto, R. H. Taylor, N. A. F. Miranda & N. Peer, 2014. Decline of Terebralia palustris in South African mangroves. African Journal of Marine Science 36: 517–522.
91. Schellekens, T., A. M. de Roos & L. Persson, 2010. Ontogenetic diet shifts result in niche partitioning between two consumer species irrespective of competitive abilities. American Naturalist 176: 625–637.
92. Slim, F. J., M. A. Hemminga, C. Ochieng, N. T. Jannink, E. C. de la Moriniere & G. van der Velde, 1997. Leaf litter removal by the snail Terebralia palustris (Linnaeus) and sesarmid crabs in an East African mangrove forest (Gazi Bay, Kenya). Journal of Experimental Marine Biology and Ecology 215: 35–48.
93. Steinke, T. D., A. Rajh & A. J. Holland, 1993. The feeding behaviour of the red mangrove crab Sesarma meinerti de Man, 1887 (Crustacea: Decapoda: Grapsidae) and its effect on the degradation of mangrove leaf litter. South African Journal of Marine Science 13: 151–160.
94. Steinke, T. D., R. A. Lubke & C. J. Ward, 2003. The distribution of algae epiphytic on pneumatophores of the mangrove, Avicennia marina, at different salinities in the Kosi System. South African Journal of Botany 69: 546–554.
95. Tomlinson, P. B., 1999. The Botany of Mangroves. Cambridge University Press, Cambridge.
96. Turner, T. F., M. L. Collyer & T. J. Krabbenhoft, 2010. A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91: 2227–2233.
97. 13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46: 2061–2066.
98. 15N enrichment: a meta-analysis. Oecologia 136: 169–182.
99. 14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Marine Biology 142: 1009–1018.
100. Werner, E. E. & J. F. Gilliam, 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics 15: 393–425.
101. Wiens, J. J., D. D. Ackerly, A. P. Allen, B. L. Anacker, L. B. Buckley, H. V. Cornell, E. I. Damschen, T. Jonathan Davies, J.-A. Grytnes, S. P. Harrison, B. A. Hawkins, R. D. Holt, C. M. McCain & P. R. Stephens, 2010. Niche conservatism as an emerging principle in ecology and conservation biology. Ecology Letters 13: 1310–1324.
102. Wright, C. I., P. Lindsay & J. A. G. Cooper, 1997. The effect of sedimentary processes on the ecology of the mangrove-fringed Kosi Estuary/Lake system, South Africa. Mangroves and Salt Marshes 1: 79–94.
103. Yang, L. H., J. L. Bastow, K. O. Spence & A. N. Wright, 2008. What can we learn from resource pulses? Ecology 89: 621–634.