A miniature bioassay for testing the acute phytotoxicity of photosystem II herbicides on seagrass

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Wilkinson, Adam D ^a,b   Collier, Catherine J ^a   Flores, Florita ^b   Mercurio, Phil ^b,c   O'Brien, Jake ^c   Ralph, Peter J ^d   Negri, Andrew P ^b  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DIURON; HERBICIDE; PHOTOSYSTEM II; WATER POLLUTANT;

ARTICLE; BIOASSAY; FLUORESCENCE IMAGING; HALOPHILA OVALIS; HYDROPONICS; LEAF SURFACE; LONG TERM EXPOSURE; NONHUMAN; OXIDATIVE STRESS; PHOTOOXIDATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYTOTOXICITY ASSAY; PLANT GROWTH; PLANT LEAF; QUANTUM YIELD; RELIABILITY; RHIZOME; RISK ASSESSMENT; SEAGRASS; SENSITIVITY ANALYSIS; TOXICITY TESTING; WATER QUALITY; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; POACEAE; PROCEDURES; SENSITIVITY AND SPECIFICITY; TOXICITY; WATER POLLUTANT;

HALOPHILA OVALIS;

BIOLOGICAL ASSAY; DIURON; DOSE-RESPONSE RELATIONSHIP, DRUG; HERBICIDES; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT LEAVES; POACEAE; SENSITIVITY AND SPECIFICITY; TOXICITY TESTS, ACUTE; WATER POLLUTANTS, CHEMICAL;

EID: 84922882969     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117541     Document Type: Article

References (49)

1. Kirkman H (1997) Seagrasses of Australia. Canberra: Department of the Environment. 36 p.
2. Marbà N, Holmer M, Gacia E, Barròn C (2006) Seagrass beds and coastal biogeochemistry. In: Larkum AWD, Orth RJ, Duarte CM, editors. Seagrasses: Biology, Ecology and Conservation. Dordrecht: Springer
3. Touchette BW (2007) Seagrass-salinity interactions: Physiological mechanisms used by submersed marine angiosperms for a life at sea. J Exp Mar Biol Ecol 350: 194-215.
4. Fourqurean JW, Duarte CM, Kennedy H, Marba N, Holmer M, et al. (2012) Seagrass ecosystems as a globally significant carbon stock. Nature Geosci 5: 505-509.
5. Costanza R, d'Arge R, de Groot R, Farber S, Grasso M, et al. (1997) The value of the worlds ecosystem services and natural capital. Nature 387: 253-260.
6. Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, et al. (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci 106: 12377-12381. doi: 10.1073/pnas.0905620106 PMID: 19587236
7. Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, et al. (2006) A Global Crisis for Seagrass Ecosystems. Bio Science 56: 987-996.
8. Fabricius KE, Logan M, Weeks S, Brodie J (2014) The effects of river run-off on water clarity across the central Great Barrier Reef. Mar Pollut Bull 84: 191-200. doi: 10.1016/j.marpolbul.2014.05.012 PMID: 24863415
9. Collier CJ, Waycott M, McKenzie LJ (2012) Light thresholds derived from seagrass loss in the coastal zone of the northern Great Barrier Reef, Australia. Ecol Indic 23: 211-219.
10. Haynes D, Ralph P, Prange J, Dennison B (2000) The impact of the herbicide diuron on photosynthesis in three species of tropical seagrass. Mar. Pollut. Bull. 41: 288-293.
11. Kennedy K, Schroeder T, Shaw M, Haynes D, Lewis S, et al. (2012) Long term monitoring of photosystem II herbicides - Correlation with remotely sensed freshwater extent to monitor changes in the quality of water entering the Great Barrier Reef, Australia. Mar. Pollut. Bull. 65: 292-305. doi: 10.1016/j.marpolbul.2011.10.029 PMID: 22154275
12. Lewis SE, Brodie JE, Bainbridge ZT, Rohde KW, Davis AM, et al. (2009) Herbicides: A new threat to the Great Barrier Reef. Environ Pollut 157: 2470-2484. doi: 10.1016/j.envpol.2009.03.006 PMID: 19349104
13. Lewis SE, Schaffelke B, Shaw M, Bainbridge ZT, Rohde KW, et al. (2012) Assessing the additive risks of PSII herbicide exposure to the Great Barrier Reef. Mar. Pollut. Bull. 65: 280-291. doi: 10.1016/j.marpolbul.2011.11.009 PMID: 22172236
14. Smith R, Middlebrook R, Turner R, Huggins R, Vardy S, et al. (2012) Large-scale pesticide monitoring across Great Barrier Reef catchments - Paddock to Reef Integrated Monitoring, Modelling and Reporting Program. Mar. Pollut. Bull. 65: 117-127. doi: 10.1016/j.marpolbul.2011.08.010 PMID: 21920563
15. Davis AM, Thorburn PJ, Lewis SE, Bainbridge ZT, Attard SJ, et al. (2013) Environmental impacts of irrigated sugarcane production: Herbicide run-off dynamics from farms and associated drainage systems. Agric Ecosyst Environ 180: 123-135.
16. Shaw M, Furnas MJ, Fabricius K, Haynes D, Carter S, et al. (2010) Monitoring pesticides in the Great Barrier Reef. Mar Pollut Bull 60: 113-122. doi: 10.1016/j.marpolbul.2009.08.026 PMID: 19818971
17. Haynes D, Muller J, Carter S (2000) Pesticide and herbicide residues in sediments and seagrasses from the Great Barrier Reef World Heritage Area and Queensland Coast. Mar. Pollut. Bull. 41: 279-287.
18. Flores F, Collier CJ, Mercurio P, Negri AP (2013) Phytotoxicity of four photosystem II herbicides to tropical seagrasses. PLoS ONE 8: e75798. doi: 10.1371/journal.pone.0075798 PMID: 24098726
19. Ralph PJ, Smith RA, Macinnis-Ng CMO, Seery CR (2007) Use of fluorescence-based ecotoxicological bioassays in monitoring toxicants and pollution in aquatic systems: Review. Toxicol Environ Chem 89: 589-607.
20. Wahedally SF, Mamboya FA, Lyimo TJ, Bhikajee M, Björk M (2012) Short-term effects of three herbicides on the maximum quantum yield and electron transport rate of tropical seagrass Thalassodendron ciliatum. TAJNAS 3: 458-466.
21. Jones RJ, Muller J, Haynes D, Schreiber U (2003) Effects of herbicides Diuron and Atrazine on corals of the Great Barrier Reef, Australia. Mar Ecol Prog Ser 251: 153-167.
22. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA-Gen Subjects 990: 87-92.
23. Osmond C, Anderson J, Ball M, Egerton J (1999) Compromising efficiency: the molecular ecology of light-resource utilization in plants. Physiol Plant Ecol: 1-25.
24. Ralph PJ (2000) Herbicide toxicity of Halophila ovalis assessed by chlorophyll fluorescence. Aquat Bot 66: 141-152.
25. Küster A, Altenburger R (2007) Development and validation of a new fluorescence-based bioassay for aquatic macrophyte species. Chemosphere 67: 194-201. PMID: 17083966
26. Schreiber U, Quayle P, Schmidt S, Escher BI, Mueller JF (2007) Methodology and evaluation of a highly sensitive algae toxicity test based on multiwell chlorophyll fluorescence imaging. Biosens Bioelectron 22: 2554-2563. PMID: 17118646
27. Magnusson M, Heimann K, Quayle P, Negri AP (2010) Additive toxicity of herbicide mixtures and comparative sensitivity of tropical benthic microalgae. Mar Pollut Bull 60: 1978-1987. doi: 10.1016/j.marpolbul.2010.07.031 PMID: 20800855
28. Waycott M, McMahon KM, Mellors JE, Calladine A, Kleine D (2004) A guide to tropical Seagrasses of the Indo-West Pacific: James Cook University, Townsville 72 p.
29. Marsh H, O'Shea TJ, Reynolds JE III (2011) Ecology and conservation of the Sirenia: dugongs and manatees: Cambridge University Press.
30. Ralph PJ, Burchett MD (1995) Photosynthetic responses of the seagrass Halophila ovalis (R. Br.) Hook. f. to high irradiance stress, using chlorophyll a fluorescence. Aquat Bot 51: 55-66.
31. Collier CJ, Villacorta-Rath C, van Dijk K-j, Takahashi M, Waycott M (2014) Seagrass proliferation precedes mortality during hypo-salinity events: a stress-induced morphometric response. PLoS ONE 9: e94014. doi: 10.1371/journal.pone.0094014 PMID: 24705377
32. Campbell SJ, McKenzie LJ, Kerville SP (2006) Photosynthetic responses of seven tropical seagrasses to elevated seawater temperature. J. Exp. Mar. Biol. Ecol. 330: 455-468.
33. Inglis GJ (2000) Variation in the recruitment behaviour of seagrass seeds: implications for population dynamics and resource management. Pac Cons Biol 5: 251.
34. Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82: 222-237.
35. van Dam JW, Negri AP, Mueller JF, Altenburger R, Uthicke S (2012) Additive pressures of elevated sea surface temperatures and herbicides on symbiont-bearing foraminifera. PLoS ONE 7: e33900. doi: 10.1371/journal.pone.0033900 PMID: 22439012
36. Bliss CI (1939) The toxicity of poisons applied jointly. Ann Appl Biol 26: 585-615.
37. Ralph PJ, Macinnis-Ng CMO, Frankart C (2005) Fluorescence imaging application: effect of leaf age on seagrass photokinetics. Aquat. Bot. 81: 69-84.
38. Schwarzschild AC, MacIntyre WG, Moore KA, Laurence Libelo E (1994) Zostera marina L. growth response to atrazine in root-rhizome and whole plant exposure experiments. J. Exp. Mar. Biol. Ecol. 183: 77-89.
39. Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 26: 648-653. PMID: 11701322
40. Negri AP, Flores F, Röthig T, Uthicke S (2011) Herbicides increase the vulnerability of corals to rising sea surface temperature. Limnol Oceanogr 56: 471-485.
41. Ralph PJ (1998) Photosynthetic response of laboratory-cultured Halophila ovalis to thermal stress. Mar. Ecol. Prog. Ser 171: 123.
42. Kahn AE, Durako MJ (2009) Photosynthetic tolerances to desiccation of the co-occurring seagrasses Halophila johnsonii and Halophila decipiens. Aquat Bot 90: 195-198.
43. Björk M, Uku J, Weil A, Beer S (1999) Photosynthetic tolerances to desiccation of tropical intertidal seagrasses. Mar Ecol Prog Ser 191: 121-126.
44. Collier CJ, Waycott M (2014) Temperature extremes reduce seagrass growth and induce mortality. Mar Pollut Bull 83: 483-490. doi: 10.1016/j.marpolbul.2014.03.050 PMID: 24793782
45. Durako MJ, Kunzelman JI, Kenworthy WJ, Hammerstrom KK (2003) Depth-related variability in the photobiology of two populations of Halophila johnsonii and Halophila decipiens. Mar Biol 142: 1219-1228.
46. Magnusson M, Heimann K, Ridd M, Negri AP (2012) Chronic herbicide exposures affect the sensitivity and community structure of tropical benthic microalgae. Mar Pollut Bull 65: 363-372. doi: 10.1016/j.marpolbul.2011.09.029 PMID: 22019103
47. GBRMPA (2010) Water quality guidelines for the Great Barrier Reef Marine Park (Revised). Great Barrier Reef Marine Park Authority, Townsville. Available: http://www.gbrmpa.gov.au/corp-site/key-issues/water-quality/water-quality-guidelines. Accessed 2014 August 28.
48. Magnusson M, Heimann K, Ridd M, Negri AP (2013) Pesticide contamination and phytotoxicity of sediment interstitial water to tropical benthic microalgae. Water Research 47: 5211-5221. doi: 10.1016/j.watres.2013.06.003 PMID: 23870432
49. Beer S, Mtolera M, Lyimo T, Björk M (2006) The photosynthetic performance of the tropical seagrass Halophila ovalis in the upper intertidal. Aquat Bot 84: 367-371.