Fast Detection of Nutrient Limitation in Macroalgae and Seagrass with Nutrient-Induced Fluorescence

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  den Haan, Joost ^a   Huisman, Jef ^a   Dekker, Friso ^a   ten Brinke, Jacomina L ^b   Ford, Amanda K ^a   van Ooijen, Jan ^c   van Duyl, Fleur C ^c   Vermeij, Mark J A ^a,d   Visser, Petra M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^d CARMABI FOUNDATION   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; CHLOROPHYLL A; NITRATE; PHOSPHATE;

ARTICLE; BENTHOS; CHLOROPHYLL FLUORESCENCE; CORAL REEF; CULTURE MEDIUM; EUTROPHICATION; FRESHWATER ENVIRONMENT; INCUBATION TIME; LOBOPHORA VARIEGATA; MACROALGA; NONHUMAN; NUTRIENT LIMITATION; NUTRIENT LOADING; PHOTOSYNTHESIS; PHYTOPLANKTON; PLANT LEAF; SEAGRASS; STARVATION; THALASSIA TESTUDINUM; ULVA;

CARIBBEAN REGION; CHLOROPHYTA; ENVIRONMENT; FLUORESCENCE; SEAWATER; SEAWEED; SPECTROMETRY, FLUORESCENCE; STARVATION;

ALGAE; ANTHOZOA; LOBOPHORA VARIEGATA; THALASSIA; THALASSIA TESTUDINUM; ULVA; ULVA LACTUCA;

EID: 84879827213     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068834     Document Type: Article

References (44)

1. Smith VH, Tilman GD, Nekola JC, (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100: 179-196.
2. Howarth R, Chan F, Conley DJ, Garnier J, Doney SC, et al. (2011) Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front Ecol Environ 9: 18-26.
3. Brauer VS, Stomp M, Huisman J, (2012) The nutrient-load hypothesis: patterns of resource limitation and community structure driven by competition for nutrients and light. Am Nat 179: 721-740.
4. Paerl HW, (1988) Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnol Oceanogr 33: 823-847.
5. Bell PRF, (1992) Eutrophication and coral reefs- some examples in the Great Barrier Reef Lagoon. Water Res 26: 553-568.
6. Smith VH, Joye SB, Howarth RW, (2006) Eutrophication of freshwater and marine ecosystems. Limnol Oceanogr 51: 351-355.
7. Fong P, Donohoe RM, Zedler JB, (1994) Nutrient concentration in tissue of the macroalga Enteromorpha as a function of nutrient history: an experimental evaluation using field microcosms. Mar Ecol-Prog Ser 106: 273-281.
8. Lapointe BE, (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol Oceanogr 42: 1119-1131.
9. Beardall J, Young E, Roberts S, (2001) Approaches for determining phytoplankton nutrient limitation. Aquat Sci 63: 44-69.
10. Townsend SA, Schult JH, Douglas MM, Skinner S, (2008) Does the Redfield ratio infer nutrient limitation in the macroalga Spirogyra fluviatilis? Freshw Biol 53: 509-520.
11. Larned ST, (1998) Nitrogen- versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae. Mar Biol 132: 409-421.
12. Armitage AR, Frankovich TA, Heck KL, Fourqurean JW, (2005) Experimental nutrient enrichment causes complex changes in seagrass, microalgae, and macroalgae community structure in Florida Bay. Estuaries 28: 422-434.
13. Teichberg M, Fox SE, Aguila C, Olsen YS, Valiela I, (2008) Macroalgal responses to experimental nutrient enrichment in shallow coastal waters: growth, internal nutrient pools, and isotopic signatures. Mar Ecol-Prog Ser 368: 117-126.
14. Burkepile DE, Hay ME, (2009) Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Mar Ecol-Prog Ser 389: 71-84.
15. Shelly K, Holland D, Beardall J (2010) Assessing nutrient status of microalgae using chlorophyll a fluorescence. In: Suggett DJ, Borowitzka MA, Prášil O, editors. Chlorophyll a fluorescence in aquatic sciences: methods and applications. Heidelberg: Springer. 223-235.
16. Turpin DH, Weger HG, (1988) Steady-state chlorophyll a fluorescence transients during ammonium assimilation by the N-limited green alga Selenastrum minutum. Plant Physiol 88: 97-101.
17. Wood MD, Oliver RL, (1995) Fluorescence transients in response to nutrient enrichment of nitrogen- and phosphorus-limited Microcystis aeruginosa cultures and natural phytoplankton populations: a measure of nutrient limitation. Aust J Plant Physiol 22: 331-340.
18. Beardall J, Berman T, Heraud P, Omo Kadiri M, Light BR, et al. (2001) A comparison of methods for detection of phosphate limitation in microalgae. Aquat Sci 63: 107-121.
19. Holland D, Roberts S, Beardall J, (2004) Assessment of the nutrient status of phytoplankton: a comparison between conventional bioassays and nutrient-induced fluorescence transients (NIFTs). Ecol Indic 4: 149-159.
20. Petrou K, Doblin MA, Smith RA, Ralph PJ, Shelly K, et al. (2008) State transitions and nonphotochemical quenching during a nutrient-induced fluorescence transient in phosphorus-starved Dunaliella tertiolecta. J Phycol 44: 1204-1211.
21. Huot Y, Babin M (2010) Overview of fluorescence protocols: theory, basic concepts, and practice. In: Suggett DJ, Borowitzka MA, Prášil O, editors. Chlorophyll a fluorescence in aquatic sciences: methods and applications. Heidelberg: Springer. 31-74.
22. Maxwell K, Johnson GN, (2000) Chlorophyll fluorescence- a practical guide. J Exp Bot 51: 659-668.
23. Kohler KE, Gill SM, (2006) Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32: 1259-1269.
24. Grasshoff K, Ehrhardt M, Kremling K, editors (1983) Methods of seawater analysis, second edition. Weinheim, Verslag Chemie. 419 p.
25. Helder W, De Vries RTP, (1979) An automatic phenol-hypochlorite method for the determination of ammonia in sea- and brackish waters. Neth J Sea Res 13: 154-160.
26. Murphy J, Riley JP, (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27: 31-36.
27. Kromkamp J, Barranguet C, Peene J, (1998) Determination of microphytobenthos PSII quantum efficiency and photosynthetic activity by means of variable chlorophyll fluorescence. Mar Ecol-Prog Ser 162: 45-55.
28. Fujita RM, (1985) The role of nitrogen status in regulating transient ammonium uptake and nitrogen storage by macroalgae. J Exp Mar Biol Ecol 92: 283-301.
29. Luo MB, Liu F, Xu ZL, (2012) Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot 100: 18-24.
30. Genty B, Briantais J-M, Baker NR, (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87-92.
31. Geider RJ, La Roche J, Greene RM, Olaizola M, (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate or iron starvation. J Phycol 29: 755-766.
32. Lippemeier S, Hintze R, Vanselow KH, Hartig P, Colijn F, (2001) In-line recording of PAM fluorescence of phytoplankton cultures as a new tool for studying effects of fluctuating nutrient supply on photosynthesis. Eur J Phycol 36: 89-100.
33. Enríquez S, Borowitzka MA (2010) The use of the fluorescence signal in studies of seagrasses and macroalgae. In: Suggett DJ, Borowitzka MA, Prášil O, editors. Chlorophyll a fluorescence in aquatic sciences: methods and applications. Heidelberg: Springer. 187-208.
34. Patriquin D, (1972) The origin of nitrogen and phosphorus for growth of the marine angiosperm Thalassia testudinum. Mar Biol 15: 35-46.
35. Touchette BW, Burkholder JM, (2000) Review of nitrogen and phosphorus metabolism in seagrasses. J Exp Mar Biol Ecol 250: 133-167.
36. Young EB, Beardall J, (2003) Rapid ammonium- and nitrate-induced perturbations to chl a fluorescence in nitrogen-stressed Dunaliella tertiolecta (Chlorophyta). J Phycol 39: 332-342.
37. Shelly K, Higgins T, Beardall J, Wood B, McNaughton D, et al. (2007) Characterising nutrient-induced fluorescence transients (NIFTs) in nitrogen-stressed Chlorella emersonii (Chlorophyta). Phycologia 46: 503-512.
38. Schaffelke B, Klumpp DW, (1998) Nutrient-limited growth of the coral reef macroalga Sargassum baccularia and experimental growth enhancement by nutrient addition in continuous flow culture. Mar Ecol-Prog Ser 164: 199-211.
39. Schaffelke B, Klumpp DW, (1998) Short-term nutrient pulses enhance growth and photosynthesis of the coral reef macroalga Sargassum baccularia. Mar Ecol-Prog Ser 170: 95-105.
40. Schaffelke B, (1999) Short-term nutrient pulses as tools to assess responses of coral reef macroalgae to enhanced nutrient availability. Mar Ecol-Prog Ser 182: 305-310.
41. Mumby PJ, Foster NL, Fahy EAG, (2005) Patch dynamics of coral reef macroalgae under chronic and acute disturbance. Coral Reefs 24: 681-692.
42. Nugues M, Bak R, (2008) Long-term dynamics of the brown macroalga Lobophora variegata on deep reefs in Curaçao. Coral Reefs 27: 389-393.
43. Diaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, et al. (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PloS ONE 4: e5239.
44. Cheal AJ, MacNeil MA, Cripps E, Emslie MJ, Jonker M, et al. (2010) Coral macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29: 1005-1015.