Community Biomass and Bottom up Multivariate Nutrient Complementarity Mediate the Effects of Bioturbator Diversity on Pelagic Production

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Caliman, Adriano ^a,d   Carneiro, Luciana S ^a,d   Leal, João J F ^a,b   Farjalla, Vinicius F ^a   Bozelli, Reinaldo L ^a   Esteves, Francisco A ^a,c  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO FEDERAL DE EDUCAÇÃO   (Brazil)

^c Núcleo de Pesquisas em Ecologia e Desenvolvimento Sócio Ambiental de Macaé ^*  (Brazil)

^d FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

DISSOLVED INORGANIC NITROGEN; NITROGEN; PHOSPHORUS; TOTAL DISSOLVED PHOSPHORUS; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPLANKTON; BENTHOS; BIODIVERSITY; BIOMASS; BIOTURBATION; COMMUNITY BIOMASS; ECOSYSTEM; NONHUMAN; NUTRIENT DYNAMICS; PELAGIC ZONE; SPECIES COMPOSITION; SPECIES DIVERSITY; SPECIES EXTINCTION; SPECIES RICHNESS; TROPHIC LEVEL;

ANIMALS; BIODIVERSITY; BIOMASS; CHIRONOMIDAE; ECOSYSTEM; GASTROPODA; GEOLOGIC SEDIMENTS; INVERTEBRATES; NITROGEN; PLANKTON; POLYCHAETA; POPULATION DYNAMICS; WATER MICROBIOLOGY;

EID: 84866315986     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044925     Document Type: Article

References (101)

1. Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, et al. (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9: 1146-1156.
2. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, et al. (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443: 989-992.
3. Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, et al. (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486: 105-108.
4. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, et al. (2012) Biodiversity loss and its impact on humanity. Nature 486: 59-67.
5. Naeem S, Duffy JE, Zavaleta E, (2012) The Functions of Biological Diversity in an Age of Extinction. Science 336: 1401-1406.
6. Duffy JE, (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Environ 7: 437-444.
7. Caliman A, Pires AF, Esteves FA, Bozelli RL, Farjalla VF, (2010) The prominence of and biases in biodiversity and ecosystem functioning research. Biodivers Conserv 19: 651-664.
8. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, et al. (2005) Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol Monogr 75: 3-35.
9. Hillebrand H, Matthiessen B, (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12: 1405-1419.
10. Reiss J, Bridle JR, Montoya JM, Woodward G, (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24: 505-514.
11. Raffaelli D, (2006) Biodiversity and ecosystem functioning: issues of scale and trophic complexity. Mar Ecol Prog Ser 311: 285-294.
12. Covich AP, Austen MC, Barlocher F, Chauvet E, Cardinale BJ, et al. (2004) The role of Biodiversity in the functioning of freshwater and marine benthic ecosystems. Bioscience 54: 767-775.
13. Palmer MA, Covich AP, Lake S, Biro P, Brooks JJ, et al. (2000) Linkages between aquatic sediment biota and life above sediments as potential drivers of biodiversity and ecological processes. Bioscience 50: 1062-1075.
14. Vaughn CC, (2010) Biodiversity Losses and Ecosystem Function in Freshwaters: Emerging Conclusions and Research Directions. Bioscience 60: 25-35.
15. Schmitz OJ, Grabowski JH, Peckarsky BL, Preisser EL, Trussell GC, et al. (2008) From individuals to ecosystem function: Toward an integration of evolutionary and ecosystem ecology. Ecology 89: 2436-2445.
16. Griffin JN, De la Haye KL, Hawkins SJ, Thompson RC, Jenkins SR, (2008) Predator diversity and ecosystem functioning: Density modifies the effect of resource partitioning. Ecology 89: 298-305.
17. Griffiths GJK, Wilby A, Crawley MJ, Thomas MB, (2008) Density-dependent effects of predator species-richness in diversity-function studies. Ecology 89: 2986-2993.
18. He JS, Wolfe-Bellin KS, Schmid B, Bazzaz FA, (2005) Density may alter diversity-productivity relationships in experimental plant communities. Basic Appl Ecol 6: 505-517.
19. Marquard E, Weigelt A, Roscher C, Gubsch M, Lipowsky A, et al. (2009) Positive biodiversity-productivity relationship due to increased plant density. J Ecol 97: 696-704.
20. Allen DC, Vaughn CC, (2011) Density-dependent biodiversity effects on physical habitat modification by freshwater bivalves. Ecology 92: 1013-1019.
21. Gamfeldt L, Hillebrand H, (2008) Biodiversity Effects on Aquatic Ecosystem Functioning- Maturation of a New Paradigm. Int Rev Hydrobiol 93: 550-564.
22. Maestre FT, Quero JL, Gotelli NJ, Escudero A, Ochoa V, et al. (2012) Plant Species Richness and Ecosystem Multifunctionality in Global Drylands. Science 335: 214-218.
23. Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, et al. (2011) High plant diversity is needed to maintain ecosystem services. Nature 477: 199-U196.
24. Gamfeldt L, Hillebrand H, Jonsson PR, (2008) Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89: 1223-1231.
25. Hector A, Bagchi R, (2007) Biodiversity and ecosystem multifunctionality. Nature 448: 188-191.
26. Bengtsson J, (1998) Which species? What kind of diversity? Which ecosystem function? Some problems in studies of relations between biodiversity and ecosystem function. Appl Soil Ecol 10: 191-199.
27. Rosenfeld JS, (2002) Logical fallacies in the assessment of functional redundancy. Conserv Biol 16: 837-839.
28. Giller PS, Hillebrand H, Berninger UG, Gessner MO, Hawkins S, et al. (2004) Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. Oikos 104: 423-436.
29. Bracken MES, Stachowicz JJ, (2006) Seaweed diversity enhances nitrogen uptake via complementary use of nitrate and ammonium. Ecology 87: 2397-2403.
30. Duffy JE, Richardson JP, Canuel EA, (2003) Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol Lett 6: 637-645.
31. Mouillot D, Villeger S, Scherer-Lorenzen M, Mason NWH, (2011) Functional Structure of Biological Communities Predicts Ecosystem Multifunctionality. PLoS One 6: 9.
32. Meysman FJR, Middelburg JJ, Heip CHR, (2006) Bioturbation: a fresh look at Darwin's last idea. Trend Ecol Evol 21: 688-695.
33. Teal LR, Bulling MT, Parker ER, Solan M, (2008) Global patterns of bioturbation intensity and mixed depth of marine soft sediments. Aquat Biol 2: 207-218.
34. Mermillod-Blondin F, Rosenberg R, (2006) Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats. Aquat Sci 68: 434-442.
35. Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, et al. (2012) What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser 446: 285-302.
36. Mermillod-Blondin F, (2011) The functional significance of bioturbation and biodeposition on biogeochemical processes at the water-sediment interface in freshwater and marine ecosystems. J N Am Benthol Soc 30: 770-778.
37. Teal LR, Parker ER, Solan M, (2010) Sediment mixed layer as a proxy for benthic ecosystem process and function. Mar Ecol Prog Ser 414: 27-40.
38. Gilbertson WW, Solan M, Prosser JI (2012) Differential effects of microorganism-invertebrate interactions on benthic nitrogen cycling. FEMS Microbiol Ecol: n/a-n/a.
39. Sundback K, Miles A, Hulth S, Pihl L, Engstrom P, et al. (2003) Importance of benthic nutrient regeneration during initiation of macroalgal blooms in shallow bays. Mar Ecol Prog Ser 246: 115-126.
40. Leal JJF, Esteves FD, Farjalla VF, Enrich-Prast A, (2003) Effect of Campsurus notatus on NH4+, DOC fluxes, O-2 uptake and bacterioplankton production in experimental microcosms with sediment-water interface of an Amazonian lake impacted by bauxite tailings. Int Rev Hydrobiol 88: 167-178.
41. Marinelli RL, Williams TJ, (2003) Evidence for density-dependent effects of infauna on sediment biogeochemistry and benthic-pelagic coupling in nearshore systems. Estuar Coast Shelf Sci 57: 179-192.
42. Emmerson MC, Solan M, Emes C, Paterson DM, Raffaelli D, (2001) Consistent patterns and the idiosyncratic effects of biodiversity in marine ecosystems. Nature 411: 73-77.
43. Caliman A, Leal JJF, Esteves FA, Carneiro LS, Bozelli RL, et al. (2007) Functional bioturbator diversity enhances benthic-pelagic processes and properties in experimental microcosms. J N Am Benthol Soc 26: 450-459.
44. Caliman A, Carneiro LS, Bozelli RL, Farjalla VF, Esteves FA, (2011) Bioturbating space enhances the effects of non-additive interactions among benthic ecosystem engineers on cross-habitat nutrient regeneration. Oikos 120: 1639-1648.
45. Bulling MT, Hicks N, Murray L, Paterson DM, Raffaelli D, et al. (2010) Marine biodiversity-ecosystem functions under uncertain environmental futures. Philos Trans R Soc Lond Ser B-Biol Sci 365: 2107-2116.
46. Godbold JA, Bulling MT, Solan M, (2011) Habitat structure mediates biodiversity effects on ecosystem properties. Proc R Soc B-Biol Sci 278: 2510-2518.
47. Ieno EN, Solan M, Batty P, Pierce GJ, (2006) How biodiversity affects ecosystem functioning: roles of infaunal species richness, identity and density in the marine benthos. Mar Ecol Prog Ser 311: 263-271.
48. Solan M, Cardinale BJ, Downing AL, Engelhardt KAM, Ruesink JL, et al. (2004) Extinction and ecosystem function in the marine benthos. Science 306: 1177-1180.
49. Waldbusser GG, Marinelli RL, Whitlatch RB, Visscher PT, (2004) The effects of infaunal biodiversity on biogeochemistry of coastal marine sediments. Limnol Oceanogr 49: 1482-1492.
50. Godbold JA, Solan M, (2009) Relative importance of biodiversity and the abiotic environment in mediating an ecosystem process. Mar Ecol Prog Ser 396: 273-282.
51. Lohrer AM, Thrush SF, Gibbs MM, (2004) Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431: 1092-1095.
52. Caliman A, Carneiro LS, Santangelo JM, Guariento RD, Pires APF, et al. (2010) Temporal coherence among tropical coastal lagoons: a search for patterns and mechanisms. Braz J Biol 70: 803-814.
53. Bozelli RL, Caliman A, Guariento RD, Carneiro LS, Santangelo JM, et al. (2009) Interactive effects of environmental variability and human impacts on the long-term dynamics of an Amazonian floodplain lake and a South Atlantic coastal lagoon. Limnologica 39: 306-313.
54. Figueiredo-Barros MP, Leal JJF, Esteves FD, Rocha AD, Bozelli RL, (2006) Life cycle, secondary production and nutrient stock in Heleobia australis (d'Orbigny 1835) (Gastropoda: Hydrobiidae) in a tropical coastal lagoon. Estuar Coast Shelf Sci 69: 87-95.
55. Mermillod-Blondin F, François-Carcaillet F, Rosenberg R, (2005) Biodiversity of benthic invertebrates and organic matter processing in shallow marine sediments: an experimental study. J Exp Mar Biol Ecol 315: 187-209.
56. Caliman A (2009) A importância da biodiversidade sobre a magnitude e estabilidade de processos regenerativos entre compartimentos aquáticos [Phd Thesis]. Rio de Janeiro: Universidade Federal do Rio de Janeiro. 140 p.
57. Esteves FA, Caliman A, Santangelo JM, Guariento RD, Farjalla VF, et al. (2008) Neotropical coastal lagoons: An appraisal of their biodiversity, functioning, threats and conservation management. Braz J Biol 68: 967-981.
58. Callisto M, Gonçalves-Junior JF, Leal JJF, Petrucio MM (1998) Macroinvertebrados bentônicos nas lagoas Imboassica, Cabiúnas, e Comprida. In: Esteves FA, editor. Ecologia das Lagoas Costeiras do Parque Nacional da Restinga de Jurubatiba e do Município de Macaé (RJ). Rio de Janeiro: Nupem/UFRJ. 479-486.
59. Alves JM, Caliman A, Guariento RD, Figueiredo-Barros MP, Carneiro LS, et al. (2010) Stoichiometry of benthic invertebrate nutrient recycling: interspecific variation and the role of body mass. Aquat Ecol 44: 421-430.
60. Graneli W, (1979) Influence of Chironomus Plumosus Larvae on the Exchange of Dissolved Substances between Sediment and Water. Hydrobiologia 66: 149-159.
61. De Haas EM, Kraak MHS, Koelmans AA, Admiraal W, (2005) The impact of sediment reworking by opportunistic chironomids on specialised mayflies. Fresh Biol 50: 770-780.
62. Figueiredo-Barros MP, Caliman A, Leal JJF, Bozelli RL, Farjalla VF, et al. (2009) Benthic bioturbator enhances CH4 fluxes among aquatic compartments and atmosphere in experimental microcosms. CanJ Fish Aquat Sci 66: 1649-1657.
63. Jolliffe PA, (2000) The replacement series. J Ecol 88: 378-385.
64. Sundareshwar PV, Morris JT, Koepfler EK, Fornwalt B, (2003) Phosphorus limitation of coastal ecosystem processes. Science 299: 563-565.
65. Farjalla VF, Enrich-Prast A, Esteves FA, Cimbleris A, (2006) Bacterial growth and DOC consumption in a tropiacal coastal lagoon. Braz J Biol 66: 383-392.
66. Solorzano L, (1969) Determination of ammonia in natural waters by phenolhypochlorite method. Limnol Oceanogr 14: 799-801.
67. Golterman HL, Clymo RS, Ohnstad MAM (1978) Methods for physical and chemical analysis of freshwater. Oxford: Blackwell Scientific Publication. 214 p.
68. Smith DC, Azam F, (1992) A simple, economical method for measuring bacterial protein syntesis rates in seawater using 3H-Leucine. Marine Microbial Food Webs 6: 107-114.
69. Simon M, Azam F, (1989) Protein-content and protein-synthesis rates of planktonic marine-bacteria. Mar Ecol Prog Ser 51: 201-213.
70. Schmid B, Hector A, Huston MA, Inchausti P, Nijs I, et al. (2002) The design and analisys of biodiversity experiments. In: Loreau M, Naeem S, Inchausti P, editors. Biodiversity and ecosystem functioning: sysnthesis and perspectives. New York: Oxford University Press. 61-78.
71. Cottingham KL, Lennon JT, Brown BL, (2005) Knowing when to draw the line: designing more informative ecological experiments. Front Ecol Environ 3: 145-152.
72. Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sunderland, Massachusetts USA: Sinauer Associates.
73. Hedges LV, Gurevitch J, Curtis PS, (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80: 1150-1156.
74. Loreau M, (1998) Separating sampling and other effects in biodiversity experiments. Oikos 82: 600-602.
75. Gurevitch J, Morrow LL, Wallace A, Walsh JS, (1992) A meta-analisis of competition in field experiments. Am Nat 140: 539-572.
76. Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD, (2010) Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Proc Natl Acad Sci U S A 107: 1443-1446.
77. Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Version 2.0. Sunderland, Massachusetts: Sinauer Associates.
78. Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. New York, USA: Springer.
79. Rangel T, Diniz-Filho JAF, Bini LM, (2006) Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Glob Ecol Biogeogr 15: 321-327.
80. Tilman D, (1999) The ecological consequences of changes in biodiversity: A search for general principles. Ecology 80: 1455-1474.
81. Moore JW, (2006) Animal ecosystem engineers in streams. Bioscience 56: 237-246.
82. Flecker AS, Feifarek BP, Taylor BW (1999) Ecosystem engineering by a tropical tadpole: Density-dependent effects on habitat structure and larval growth rates. Copeia: 495-500.
83. Maestre FT, Castillo-Monroy AP, Bowker MA, Ochoa-Hueso R, (2012) Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. J Ecol 100: 317-330.
84. Wootton JT, Emmerson M, (2005) Measurement of interaction strength innature. Annu Rev Ecol Evol Syst 36: 419-444.
85. Kristensen E, (2000) Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia 426: 1-24.
86. Aller RC, Hall POJ, Rude PD, Aller JY, (1997) Biogeochemical heterogeneity and suboxic diagenesis in hemipelagic sediments of the Panama Basin. Deep Sea Res 45: 133-165.
87. Hiddink JG, Davies TW, Perkins M, Machairopoulou M, Neill SP, (2009) Context dependency of relationships between biodiversity and ecosystem functioning is different for multiple ecosystem functions. Oikos 118: 1892-1900.
88. Peter H, Ylla I, Gudasz C, Romani AM, Sabater S, et al. (2011) Multifunctionality and Diversity in Bacterial Biofilms. PLoS One 6.
89. Peter H, Beier S, Bertilsson S, Lindstrom ES, Langenheder S, et al. (2011) Function-specific response to depletion of microbial diversity. Isme J 5: 351-361.
90. Massol F, Gravel D, Mouquet N, Cadotte MW, Fukami T, et al. (2011) Linking community and ecosystem dynamics through spatial ecology. Ecol Lett 14: 313-323.
91. Spehn EM, Hector A, Joshi J, Scherer-Lorenzen M, Schmid B, et al. (2005) Ecosystem effects of biodiversity manipulations in European grasslands. Ecol Monogr 75: 37-63.
92. Whiting GJ, Chanton JP, (1993) Primary production control of methane emission from wetlands. Nature 364: 794-795.
93. Cardinale BJ, Wrigh JP, Cadotte MW, Carroll IT, Hector A, et al. (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci U S A 104: 18123-18128.
94. Petchey OL, Gaston KJ, (2002) Functional diversity (FD), species richness and community composition. Ecol Lett 5: 402-411.
95. Stief P, Holker F, (2006) Trait-mediated indirect effects of predatory fish on microbial mineralization in aquatic sediments. Ecology 87: 3152-3159.
96. Biles CL, Solan M, Isaksson I, Paterson DM, Emes C, et al. (2003) Flow modifies the effect of biodiversity on ecosystem functioning: an in situ study of estuarine sediments. J Exp Mar Biol Ecol 285: 165-177.
97. Biles CL, Paterson DM, Ford RB, Solan M, Raffaelli DG, (2002) Bioturbation, ecosystem functioning and community structure. Hydrology and Earth System Sciences 6: 999-1005.
98. Duffy JE, Carinale BJ, France KE, McIntyre PB, Thebault E, et al. (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10: 522-538.
99. Cardinale BJ, Ives AR, Inchausti P, (2004) Effects of species diversity on the primary productivity of ecosystems: extending our spatial and temporal scales of inference. Oikos 104: 437-450.
100. Schindler DE, Scheuerell MD, (2002) Habitat coupling in lake ecosystems. Oikos 98: 177-189.
101. Ceballos G, Ehrlich PR, (2002) Mammal population losses and the extinction crisis. Science 296: 904-907.