Settling cyanobacterial blooms do not improve growth conditions for soft bottom meiofauna

Journal of Experimental Marine Biology and Ecology

Volumn 368, Issue 2, 2009, Pages 138-146

  Nascimento, Francisco J A ^a   Karlson, Agnes M L ^a   Näslund, Johan ^a   Gorokhova, Elena ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Benthic pelagic coupling; Cyanobacteria; Meiofauna; Organic matter quality

Indexed keywords

ALGAL BLOOM; AMINO ACID; BENTHIC-PELAGIC COUPLING; CYANOBACTERIUM; DIATOM; EUPHOTIC ZONE; LIGNIN; MARINE SEDIMENT; MEIOFAUNA; NEMATODE; NUCLEIC ACID; OSTRACOD; PHYTOPLANKTON; SOFT-BOTTOM ENVIRONMENT; TOXIN;

ATLANTIC OCEAN; BALTIC SEA;

ALGAE; BACILLARIOPHYTA; CANDONA NEGLECTA; CYANOBACTERIA; HETEROCYPRIDEIS SORBYANA; NEMATODA; NODULARIA; NODULARIA SPUMIGENA; OSTRACODA; PARACANTHONCHUS; PARACYPRIDEIS FENNICA;

EID: 57249104713     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2008.09.014     Document Type: Article

References (78)

1. Agrawal M.K., Zitt A., Bagchi D., Weckesser J., Bagchi S.N., and von Elert E. Characterization of proteases in guts of Daphnia magna and their inhibition by Microcystis aeruginosa PCC 7806. Environ. Toxicol. 20 (2005) 314-322
2. Ahlgren G., Gustafsson I.B., and Boberg M. Fatty-acid content and chemical composition of fresh-water microalgae. J. Phycol. 28 (1992) 37-50
3. Ahlgren G., Goedkoop W., Markensten H., Sonesten L., and Boberg M. Seasonal variations in food quality for pelagic and benthic invertebrates in Lake Erken - the role of fatty acids. Freshw. Biol. 38 (1997) 555-570
4. Andersson A., Selstam E., and Hagström A. Vertical transport of lipid in seawater. Mar. Ecol. Prog. Ser. 98 (1993) 149-155
5. Ankar S., and Elmgren R. The benthic macro- and meiofauna of the Askö-Landsort area (northern Baltic proper). A stratified random sampling survey. Contributions from the Askö Laboratory (1976), University of Stockholm, Stockholm 1-115
6. Blomqvist S., and Lundgren L. A benthic sled for sampling soft bottoms. Helgol. Mar. Res. 50 (1996) 453-456
7. Blomqvist S., and Heiskanen A.S. The challenge of sedimentation in the Baltic Sea. In: Wulff F., Rahm R., and Larsson P. (Eds). A Systems Analysis of the Baltic Sea vol. 148 (2001), Springer-Verlag, Berlin 211-227
8. Boersma M., and Kreutzer C. Life at the edge: Is food quality really of minor importance at low quantities?. Ecology 83 (2002) 2552-2561
9. Bremer H., and Dennis P.P. Modulation of chemical composition and other parameters of the cell by growth rate. In: Neidhardt F.C., et al. (Ed). Escherichia coli and Salmonella: cellular and molecular biology (1996), ASM Press, Washington, D.C 1553-1569
10. Buckley L., Caldarone E., and Ong T.L. RNA-DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia 401 (1999) 265-277
11. Buffan-Dubau E., and Carman K.R. Diel feeding behavior of meiofauna and their relationships with microalgal resources. Limnol. Oceanogr. 45 (2000) 381-395
12. Burns C.W., and Xu Z.K. Utilization of colonial cyanobacteria and algae by fresh-water calanoid copepods- Survivorship and reproduction of adult Boeckella spp. Arch. Hydrobiol. 117 (1990) 257-270
13. Caldarone E.M., Clemmesen C.M., Berdalet E., Miller T.J., Folkvord A., Holt G.J., Olivar M.P., and Suthers I.M. Intercalibration of four spectrofluorometric protocols for measuring RNA/DNA ratios in larval and juvenile fish. Limnol. Oceanogr.: Methods 4 (2006) 153-163
14. Dahl U., Gorokhova E., and Breitholtz M. Application of growth-related sublethal endpoints in ecotoxicological assessments using a harpacticoid copepod. Aquat. Toxicol. 77 (2006) 433-438
15. Dalto A.G., Gremare A., Dinet A., and Fichet D. Muddy-bottom meiofauna responses to metal concentrations and organic enrichment in New Caledonia South-West Lagoon. Estuar. Coast. Shelf Sci. 67 (2006) 629-644
16. De Benardi R., and Giussanig. Are blue-green algae a suitable food for zooplankton- An overview. Hydrobiologia 200 (1990) 29-41
17. DeMott W.R., and Moxter F. Foraging on cyanobacteria by copepods - Responses to chemichal defenses and resource abundance. Ecology 72 (1991) 1820-1834
18. DeMott W.R., and Müller-Navarra D.C. The importance of highly unsaturated fatty acids in zooplankton nutrition: evidence from experiments with Daphnia, a cyanobacterium and lipid emulsions. Freshw. Biol. 38 (1997) 649-664
19. Engström J., Koski M., Viitasalo M., Reinikainen M., Repka S., and Sivonen K. Feeding interactions of the copepods Eurytemora affinis and Acartia bifilosa with the cyanobacteria Nodularia sp. J. Plankton Res. 22 (2000) 1403-1409
20. Finni T., Kononen K., Olsonen R., and Wallström K. The history of cyanobacterial blooms in the Baltic Sea. Ambio 30 (2001) 172-178
21. Gardeström J., Gorokhova E., Gilek M., Grahn M., Bengtsson B.E., and Breitholtz M. A multilevel approach to predict toxicity in copepod populations: Assessment of growth, genetics, and population structure. Aquat. Toxicol. 79 (2006) 41-48
22. Gardner W.S., Nalepa T.F., Frez W.A., Cichocki E.A., and Landrum P.F. Seasonal patterns in lipid-content of Lake-Michigan macroinvertebrates. Can. J. Fish. Aquat. Sci. 42 (1985) 1827-1832
23. Goedkoop W., and Johnson R.K. Pelagic-benthic coupling: Profundal benthic community response to spring diatom deposition in mesotrophic Lake Erken. Limnol. Oceanogr. 41 (1996) 636-647
24. Goedkoop W., Åkerblom N., and Demandt M.H. Trophic fractionation of carbon and nitrogen stable isotopes in Chironomus riparius reared on food of aquatic and terrestrial origin. Freshw. Biol. 51 (2006) 878-886
25. Goedkoop W., Demandt M., and Ahlgren G. Interactions between food quantity and quality (long-chain polyunsaturated fatty acid concentrations) effects on growth and development of Chironomus riparius. Can. J. Fish. Aquat. Sci. 64 (2007) 425-436
26. Gorokhova E. Relationships between nucleic acid levels and egg production rates in Acartia bifilosa: implications for growth assessment of copepods in situ. Mar. Ecol. Prog. Ser. 262 (2003) 163-172
27. Gorokhova E., and Kyle M. Analysis of nucleic acids in Daphnia: development of methods and ontogenetic variations in RNA-DNA content. J. Plankton Res. 24 (2002) 511-522
28. Gorokhova E., Edlund A., Hajdu S., and Zhivotova E.N. Nucleic acid levels in copepods: dynamic response to the phytoplankton bloom in the northern Baltic proper. Mar. Ecol. Prog. Ser. 349 (2007) 213-225
29. Graf G. Benthic-pelagic coupling - a benthic view. Oceanogr. Mar. Biol. 30 (1992) 149-190
30. Graneli E., Wallström K., Larsson U., Graneli W., and Elmgren R. Nutrient limitation of primary production in the Baltic Sea area. Ambio 19 (1990) 142-151
31. Gulati R.D., and DeMott W.R. The role of food quality for zooplankton: remarks on the state-of-the-art, perspectives and priorities. Freshw. Biol. 38 (1997) 753-768
32. Gustafsson O., Andersson P., Roos P., Kukulska Z., Broman D., Larsson U., Hajdu S., and Ingri J. Evaluation of the collection efficiency of upper ocean sub-photic-layer sediment traps: a 24-month in situ calibration in the open Baltic Sea using Th-234. Limol. Oceanogr.: Methods 2 (2004) 62-74
33. Heiskanen A.S., and Leppänen J.M. Estimation of export production in the coastal Baltic Sea: Effect of resuspension and microbial decomposition on sedimentation measurements. Hydrobiologia 316 (1995) 211-224
34. Hu S.I., Horng C.Y., and Cheng I.J. The use of growth and ingestion rates of Capitella sp I as the bioassay approaches to determine the sediment quality of coastal wetlands of Taiwan. J. Exp. Mar. Biol. Ecol. 297 (2003) 179-202
35. Ibiam U., and Grant A. RNA/DNA ratios as a sublethal endpoint for large-scale toxicity tests with the nematode Caenorhabditis elegans. Environ. Toxicol. Chem. 24 (2005) 1155-1159
36. Johnson R.K. Seasonal variation in diet of Chironomus plumosus (L) and Chironomus anthracinus Zett (Diptera, Chironomidae) in mesotrophic Lake Erken. Freshw. Biol. 17 (1987) 525-532
37. Kankaanpää H.T., Sipiä V.O., Kuparinen J.S., Ott J.L., and Carmichael W.W. Nodularin analyses and toxicity of a Nodularia spumigena (Nostocales, Cyanobacteria) water-bloom in the western Gulf of Finland, Baltic Sea, in August 1999. Phycologia 40 (2001) 268-274
38. Karjalainen M., Engström-Öst J., Korpinen S., Peltonen H., Paakkonen J.P., Ronkkonen S., Suikkanen S., and Viitasalo M. Ecosystem consequences of cyanobacteria in the northern Baltic Sea. Ambio 36 (2007) 195-202
39. Karlson A.M.L., Nascimento F.J.A., and Elmgren R. Incorporation and burial of carbon from settling cyanobacterial blooms by deposit-feeding macrofauna. Limnol Oceanog 53 (2008) 2754-2758
40. Korpinen S., Karjalainen M., and Viitasalo M. Effects of cyanobacteria on survival and reproduction of the littoral crustacean Gammarus zaddachi (Amphipoda). Hydrobiologia 559 (2006) 285-295
41. Koski M., Schmidt K., Engstrom-Ost J., Viitasalo M., Jonasdottir S., Repka S., and Sivonen K. Calanoid copepods feed and produce eggs in the presence of toxic cyanobacteria Nodularia spumigena. Limnol. Oceanogr. 47 (2002) 878-885
42. Laine A.O. Distribution of soft-bottom macrofauna in the deep open Baltic Sea in relation to environmental variability. Estuar. Coast. Shelf Sci. 57 (2003) 87-97
43. Lampert W. Laboratory studies on zooplancton-cyanobacteria interactions. N.Z. J. Mar. Freshw. Res. 21 (1987) 483-490
44. Larsson U., Hajdu S., Walve J., and Elmgren R. Baltic Sea nitrogen fixation estimated from the summer increase in upper mixed layer total nitrogen. Limnol. Oceanogr. 46 (2001) 811-820
45. Lehtimäki J., Moisander P., Sivonen K., and Kononen K. Growth, nitrogen fixation, and nodularin production by two Baltic sea cyanobacteria. Appl. Environ. Microbiol. 63 (1997) 1647-1656
46. Lignell R., Heiskanen A.S., Kuosa H., Gundersen K., Kuuppoleinikki P., Pajuniemi R., and Uitto A. Fate of a phytoplankton spring bloom- Sedimentation and carbon flow in the planktonic food web in the Northern Baltic. Mar. Ecol. Prog. Ser. 94 (1993) 239-252
47. Limén H., and Ólafsson E. Ostracod species-specific utilisation of sediment detritus and newly settled cyanobacteria, Aphanizomenon sp., in the Baltic Sea: evidence from stable carbon isotopes. Mar. Biol. 140 (2002) 733-738
48. Lurling M., and Beekman W. Growth of Daphnia magna males and females fed with the cyanobacterium Microcystis aeruginosa and the green alga Scenedesmus obliquus in different proportions. Acta Hydrochim. Hydrobiol. 34 (2006) 375-382
49. Mayer L.M., Schick L.L., Sawyer T., Plante C.J., Jumars P.A., and Self R.L. Bioavailable amino-acids in sediments - A biomimetic, kinetics-based approach. Limnol. Oceanogr. 40 (1995) 511-520
50. Menge B.A. Top-down and bottom-up community regulation in marine rocky intertidal habitats. J. Exp. Mar. Biol. Ecol. 250 (2000) 257-289
51. Mincks S.L., Smith C.R., and DeMaster D.J. Persistence of labile organic matter and microbial biomass in Antarctic shelf sediments: evidence of a sediment 'food bank'. Mar. Ecol. Prog. Ser. 300 (2005) 3-19
52. Modig H., van de Bund W.J., and Ólafsson E. Uptake of phytodetritus by three ostracod species from the Baltic Sea: effects of amphipod disturbance and ostracod density. Mar. Ecol. Prog. Ser. 202 (2000) 125-134
53. Montagna P.A., Blanchard G.F., and Dinet A. Effect of production and biomass of intertidal microphytobenthos on meiofaunal grazing rates. J. Exp. Mar. Biol. Ecol. 185 (1995) 149-165
54. Müller-Navarra D. Evidenve that a highly unsaturated fatty-acid limits Daphmia growth in nature. Arch. Hydrobiol. 132 (1995) 297-307
55. Müller-Navarra D.C., Brett M.T., Liston A.M., and Goldman C.R. A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403 (2000) 74-77
56. Nascimento, F.J.A., Karlson, A.M.L., Elmgren, R., 2008. Settling blooms of filamentous cyanobacteria as food for meiofauna assemblages. Limnol. Oceanogr. 53, 2636-2643.
57. Norkko J., Norkko A., Thrush S.F., and Cummings V.J. Detecting growth under environmental extremes: Spatial and temporal patterns in nucleic acid ratios in two Antarctic bivalves. J. Exp. Mar. Biol. Ecol. 326 (2005) 144-156
58. Ólafsson E., and Elmgren R. Seasonal dynamics of sublittoral meiobenthos in relation to phytoplankton sedimentation in the Baltic Sea. Estuar. Coast. Shelf Sci. 45 (1997) 149-164
59. Ólafsson E., Modig H., and van de Bund W.J. Species specific uptake of radio-labelled phyto-detritus by benthic meiofauna from the Baltic Sea. Mar. Ecol. Prog. Ser. 177 (1999) 63-72
60. Olenina I., Hajdu S., Edler L., Andersson A., Wasmund N., Busch S., Göbel J., Gromisz S., Huseby S., Huttunen M., et al. Biovolumes and size-classes of phytoplankton in the Baltic Sea. HELCOM Balt. Sea Environ. Proc. vol. 106 (2006) 1-144
61. Pääkkönen J.P., Rönkkönen S., Karjalaineno M., and Viitasalo M. Physiological effects in juvenile three-spined sticklebacks feeding on toxic cyanobacterium Nodularia spumigena-exposed zooplankton. J. Fish Biol. 72 (2008) 485-499
62. Park S., Brett M.T., Oshel E.T., and Goldman C.R. Seston food quality and Daphnia production efficiencies in an oligo-mesotrophic Subalpine Lake. Aquat. Ecol. 37 (2003) 123-136
63. Platt H., and Warwick R.M. Free-living marine nematodes. Part I. British Enoplids. In: Kermack D.M., and Barnes R.S.K. (Eds). Synopses of the British Fauna (New Series) (1983), Cambridge University Press, Cambridge 307
64. Ravet J.L., Brett M.T., and Muller-Navarra D.C. A test of the role of polyunsaturated fatty acids in phytoplankton food quality for Daphnia using liposome supplementation. Limnol. Oceanogr. 48 (2003) 1938-1947
65. Richoux N.B., Thompson R.J., Delbel D., and Parrish C.C. Seasonal and developmental variation in the lipids of Acanthostepheia malmgreni (Amphipoda) from the hyperbenthos of a cold-ocean environment (Conception Bay, Newfoundland). J. Mar. Biol. Assoc. U.K. 84 (2004) 1189-1197
66. Schmidt K., and Jonasdóttir S.H. Nutritional quality of two cyanobacteria: How rich is 'poor' food?. Mar. Ecol. Prog. Ser. 151 (1997) 1-10
67. Sivonen K., and Jones G. Cyanobacterial toxins. In: Chorus I., and Bartram J. (Eds). Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management (1999), E. & F. N. Spon, London 41-111
68. Sivonen K., Kononen K., Carmichael W.W., Dahlem A.M., Rinehart K.L., Kiviranta J., and Niemelä S.I. Occurence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and structure of the toxin. Appl. Environ. Microbiol. 55 (1989) 1990-1995
69. Svensen C., Strogyloudi E., Riser C.W., Dahmann J., Legrand C., Wassmann P., Graneli E., and Pagou K. Reduction of cyanobacterial toxins through coprophagy in Mytilus edulis. Harmful Algae 4 (2005) 329-336
70. Tallberg P., and Heiskanen A.S. Species-specific phytoplankton sedimentation in relation to primary production along an inshore-offshore gradient in the Baltic Sea. J. Plankton Res. 20 (1998) 2053-2070
71. Vance D.E., and Vance J.E. Biochemistry of lipids and membranes (1985), Benjamin Cummings
72. Vargas C.A., Escribano R., and Poulet S. Phytoplankton food quality determines time windows for successful zooplankton reproductive pulses. Ecology 87 (2006) 2992-2999
73. Vos J.H., Peeters E., Gylstra R., Kraak M.H.S., and Admiraal W. Nutritional value of sediments for macroinvertebrate communities in shallow eutrophic waters. Arch. Hydrobiol. 161 (2004) 469-487
74. Vrede T., Persson J., and Aronsen G. The influence of food quality (P : C ratio) on RNA : DNA ratio and somatic growth rate of Daphnia. Limnol. Oceanogr. 47 (2002) 487-494
75. Wagner M.M., Campbell R.G., Boudreau C.A., and Durbin E.G. Nucleic acids and growth of Calanus finmarchicus in the laboratory under different food and temperature conditions. Mar. Ecol. Prog. Ser. 221 (2001) 185-197
76. Walsby A.E. Gas vesicles. Annu. Rev. Plant Physiol. 26 (1975) 427-439
77. Walve J., and Larsson U. Blooms of Baltic Sea Aphanizomenon sp (cyanobacteria) collapse after internal phosphorus depletion. Aquat. Microb. Ecol. 49 (2007) 57-69
78. Wilson A.E., Samelle O., and Tillmanns A.R. Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnol. Oceanogr. 51 (2006) 1915-1924