Response of the green alga Oophila sp., a salamander endosymbiont, to a PSII-inhibitor under laboratory conditions

Environmental Toxicology and Chemistry

Volumn 33, Issue 8, 2014, Pages 1858-1864

  Baxter, Leilan ^a   Brain, Richard ^b   Rodriguez Gil, Jose Luis ^a   Hosmer, Alan ^b   Solomon, Keith ^a   Hanson, Mark ^c  

^a UNIVERSITY OF GUELPH   (Canada)

^b SYNGENTA CROP PROTECTION   (United States)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Algae; Atrazine; Oophila

Indexed keywords

ALGAE; DENSITY (OPTICAL); DENSITY MEASUREMENT (OPTICAL); HERBICIDES;

ALGAL POPULATIONS; CONTROLLED LABORATORIES; EFFECTIVE CONCENTRATION; LABORATORY CONDITIONS; NATURAL ENVIRONMENTS; OOPHILA; SYMBIOTIC ALGAE; TOXICITY ASSAYS;

GALLIUM ALLOYS;

ATRAZINE;

AMPHIBIAN; ATRAZINE; BIOLOGICAL DEVELOPMENT; CONCENTRATION (COMPOSITION); ENDOSYMBIONT; GREEN ALGA; GROWTH RATE; HOST-SYMBIONT INTERACTION; LABORATORY METHOD; PHOTOSYNTHESIS; POLLUTION EXPOSURE; POLLUTION TOLERANCE; TOXICITY TEST;

ALGAL GROWTH; AMBYSTOMA; AMBYSTOMA MACULATUM; ARTICLE; ASSAY; CONTROLLED STUDY; EGG; ENDOSYMBIONT; EXPOSURE; GREEN ALGA; GROWTH RATE; LABORATORY; NONHUMAN; OOPHILA; OPTICAL DENSITY; PHOTOSYSTEM II; PRIORITY JOURNAL; PROCESS OPTIMIZATION; TOXICITY TESTING;

ALGAE; AMBYSTOMA MACULATUM; CHLOROPHYTA; OOPHILA; SALAMANDROIDEA; VERTEBRATA;

ALGAE; ATRAZINE; OOPHILA;

AMBYSTOMA; ANIMALS; ATRAZINE; CHLOROPHYTA; ECOTOXICOLOGY; ENZYME INHIBITORS; HERBICIDES; LABORATORIES; OVUM; PHOTOSYSTEM II PROTEIN COMPLEX; SYMBIOSIS; WATER POLLUTANTS, CHEMICAL;

EID: 84904409840     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.2629     Document Type: Article

References (55)

1. Gilbert PW. 1942. Observations on the eggs of Ambystoma maculatum with especial reference to the green algae found within the egg envelopes. Ecology 23:215-227.
2. Gilbert PW. 1944. The alga-egg relationship in Ambystoma maculatum: A case of symbiosis. Ecology 25:366-369.
3. Kerney R, Kim E, Hangarter RP, Heiss AA, Bishop CD, Hall BK. 2011. Intracellular invasion of green algae in a salamander host. Proc Nat Acad Sci U S A 108:6497-6502.
4. Hutchison VH, Hammen CS. 1958. Oxygen utilization in the symbiosis of embryos of the salamander, Ambystoma maculatum and the alga, Oophila amblystomatis. Biol Bull 115:483-489.
5. Goff LJ, Stein JR. 1978. Ammonia: Basis for algal symbiosis in salamander egg masses. Life Sci 22:1463-1468.
6. Marco A, Blaustein AR. 2000. Symbiosis with green algae affects survival and growth of northwestern salamander embryos. J Herpetol 34:617-621.
7. Tattersall GJ, Spiegelaar N. 2008. Embryonic motility and hatching success of Ambystoma maculatum are influenced by a symbiotic alga. Can J Zool 86:1289-1298.
8. Pinder AW, Friet SC. 1994. Oxygen-transport in egg masses of the amphibians Rana sylvatica and Ambystoma maculatum: Convection, diffusion and oxygen production by algae. J Exp Biol 197:17-30.
9. Kerney R. 2011. Symbioses between salamander embryos and green algae. Symbiosis 54:107-117.
10. Graham ER, Fay SA, Davey A, Sanders RW. 2013. Intracapsular algae provide fixed carbon to developing embryos of the salamander Ambystoma maculatum. J Exp Biol 216:452-459.
11. Zamudio KR, Savage WK. 2003. Historical isolation, range expansion, and secondary contact of two highly divergent mitochondrial lineages in spotted salamanders (Ambystoma maculatum). Evolution 57:1631-1652.
12. Olivier HM, Moon BR. 2010. The effects of atrazine on spotted salamander embryos and their symbiotic alga. Ecotoxicology 19:654-661.
13. Giddings JM, Anderson TA, Hall LW Jr, Hosmer AJ, Kendall RJ, Richards RP, Solomon KR, Williams WM. 2005. Atrazine in North American Surface Waters: A Probabilistic Aquatic Ecological Risk Assessment. SETAC, Pensacola, FL, USA.
14. Forson D, Storfer A. 2006. Effects of atrazine and iridovirus infection on survival and life-history traits of the long-toed salamander (Ambystoma macrodactylum). Environ Toxicol Chem 25:168-173.
15. Kerby JL, Storfer A. 2009. Combined effects of atrazine and chlorpyrifos on susceptibility of the tiger salamander to Ambystoma tigrinum virus. EcoHealth 6:91-98.
16. Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, Sager T, Sih A, Palmer BD. 2004. Multiple stressors and salamanders: Effects of an herbicide, food limitation, and hydroperiod. Ecol Appl 14:1028-1040.
17. Boone MD, James SM. 2003. Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecol Appl 13:829-841.
18. Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, Sager T, Sih A, Palmer BD. 2003. Lethal and sublethal effects of atrazine, carbaryl, endosulfan, and octylphenol on the streamside salamander (Ambystoma barbouri). Environ Toxicol Chem 22:2385-2392.
19. Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, Mount DR, Nichols JW, Russom CL, Schmieder PK, Serrrano JA, Tietge JE, Villeneuve DL. 2010. Adverse outcome pathways: A conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29:730-741.
20. Harrison RG, Wilens S. 1969. Organisation and Development of the Embryo. Yale University Press, New Haven, CT, USA.
21. Andersen RA. 2005. Algal Culturing Techniques: A Book for All Phycologists. Elsevier Academic Press, Burlington, MA, USA.
22. US Environmental Protection Agency. 1996. Ecological effects test guidelines: OPPTS 850.5400-Algal toxicity, tiers I and II. EPA 712/C-96/164. Washington, DC.
23. ASTM International. 2012. Standard Guide for Conducting Static Toxicity Tests with Microalgae. ASTM International, West Conshohocken, PA, USA.
24. Vallotton N, Eggen RIL, Escher BI, Krayenbuhi J, Chevre N. 2008. Effect of pulse herbicide exposure on Scenedesmus vacuolatus: A comparison of two photosystem II inhibitors. Environ Toxicol Chem 27:1399-1407.
25. Geis SW, Fleming KL, Korthals ET, Searle G, Reynolds L, Karner DA. 2000. Modifications to the algal growth inhibition test for use as a regulatory assay. Environ Toxicol Chem 19:36-41.
26. Sokal RR, Rohlf FJ. 1995. Biometry: The Principles and Practice of Statistics in Biological Research, 3rd ed. W. H. Freeman, New York, NY, USA.
27. Ritz C, Streibig JC. 2005. Bioassay analysis using R. Journal of Statistical Software 12:1-22.
28. Denton DL, Fox JF, Fulk FA. 2003. Enhancing toxicity test performance by using a statistical criterion. Environ Toxicol Chem 22:2323-2328.
29. Solomon KR, Carr JA, Du Preez LH, Giesy JP, Kendall RJ, Smith EE, Van Der Kraak GJ. 2008. Effects of atrazine on fish, amphibians, and aquatic reptiles: A critical review. Crit Rev Toxicol 38:721-772.
30. DeNoyelles F, Kettle WD, Sinn DE. 1982. The responses of plankton communities in experimental ponds to atrazine, the most heavily used pesticide in the United States. Ecol 63:1285-1293.
31. Chapman PM. 2004. Indirect effects of contaminants. Mar Poll Bull 48:411-412.
32. Mayer P, Frickmann J, Christensen ER, Nyholm N. 1998. Influence of growth conditions on the results obtained in algal toxicity tests. Environ Toxicol Chem 17:1091-1098.
33. Lambrev P, Goltsev V. 2001. pH dependence of the effects of diuron, atrazine and dinoseb on the luminescent properties of thylakoid membranes. Bulgarian Journal of Plant Physiology 27:85-100.
34. Bianchini K, Tattersall GJ, Sashaw J, Porteus CS, Wright PA. 2012. Acid water interferes with salamander-green algae symbiosis during early embryonic development. Physiol Biochem Zool 85:470-480.
35. Calfee RD, Bridges CM, Little EE. 2006. Sensitivity of two salamander (Ambystoma) species to ultraviolet radiation. J Herpetol 40:35-42.
36. Guasch H, Ivorra N, Lehmann V, Paulsson M, Real M, Sabater S. 1998. Community composition and sensitivity of periphyton to atrazine in flowing waters: The role of environmental factors. J Appl Phycol 10:203-213.
37. Mayasich JM, Karlander EP, Terlizzi DE. 1986. Growth-responses of Nannochloris-oculata Droop and Phaeodactylum-tricornutum Bohlin to the herbicide atrazine as influenced by light intensity and temperature. Aquat Toxicol 8:175-184.
38. Laviale M, Prygiel J, Creach A. 2010. Light modulated toxicity of isoproturon toward natural stream periphyton photosynthesis: A comparison between constant and dynamic light conditions. Aquat Toxicol 97:334-342.
39. Rosenkrantz RT, Cedergreen N, Baun A, Kusk KO. 2013. Influence of pH, light cycle, and temperature on ecotoxicity of four sulfonylurea herbicides towards Lemna gibba. Ecotoxicology 22:33-41.
40. Baxter LR, Sibley PK, Solomon KR, Hanson ML. 2013. Interactions between atrazine and phosphorus in aquatic systems: Effects on phytoplankton and periphyton. Chemosphere 90:1069-1076.
41. Lozano RB, Pratt JR. 1994. Interaction of toxicants and communities: The role of nutrients. Environ Toxicol Chem 13:361-368.
42. Guasch H, Lehmann V, van Beusekom B, Sabater S, Admiraal W. 2007. Influence of phosphate on the response of periphyton to atrazine exposure. Arch Environ Contam Toxicol 52:32-37.
43. Tubea B, Hawxby K, Mehta R. 1981. The effects of nutrient, pH and herbicide levels on algal growth. Hydrobiologia 79:221-227.
44. Kamaya Y, Takada T, Suzuki K. 2004. Effect of medium phosphate levels on the sensitivity of Selenastrum capricomutum to chemicals. Bull Environ Contam Toxicol 73:995-1000.
45. Lewis MA. 1995. Use of fresh-water plants for phytotoxicity testing: A review. Environ Pollut 87:319-336.
46. Gala WR, Giesy JP. 1990. Flow cytometric techniques to assess toxicity to algae. In Landis WG, van der Schalie WH, eds, Aquatic Toxicology and Risk Assessment, Vol 13. ASTM International, Philadelphia, PA, USA, pp 237-246.
47. Klaine SJ, Richards P, Baker D, Naddy R, Brown T, Joab B, Casey R, Fernandez D, Overmeyer J, Benjamin R. 1997. Agrochemical fate and effects in terrestrial, aquatic and estuarine ecosystems. Proceedings, International Symposium on the Use of Nuclear and Related Techniques for Studying Environmental Behavior of Crop Protection Chemicals, Vienna, Austria, July 1-5, 1996, pp 247-264.
48. Baxter L, Brain R, Prosser R, Solomon K, Hanson M. 2013. Sensitivity of a green alga to atrazine is not enhanced by previous acute exposure. Environ Pollut 181:325-328.
49. Maule A, Wright SJL. 1984. Herbicide effects on the population-growth of some green-algae and cyanobacteria. J Appl Bacteriol 57:369-379.
50. Beale SI, Appleman D. 1971. Chlorophyll synthesis in Chlorella: Regulation by degree of light limitation of growth. Plant Physiol 47:230-235.
51. Hatfield PM, Guikema JA, Stjohn JB, Gendel SM. 1989. Characterization of the adaptation response of Anacystis nidulans to growth in the presence of sublethal doses of herbicide. Curr Microbiol 18:369-374.
52. Byer JD, Struger J, Sverko E, Klawunn P, Todd A. 2011. Spatial and seasonal variations in atrazine and metolachlor surface water concentrations in Ontario (Canada) using ELISA. Chemosphere 82:1155-1160.
53. Andrus JM, Winter D, Scanlan M, Sullivan S, Bollman W, Waggoner JB, Hosmer AJ, Brain RA. 2013. Seasonal synchronicity of algal assemblages in three Midwestern agricultural streams having varying concentrations of atrazine, nutrients, and sediment. Sci Tot Environ 458:125-139.
54. Vallotton N, Moser D, Eggen RIL, Junghans M, Chèvre N. 2008. S-metolachlor pulse exposure on the alga Scenedesmus vacuolatus: Effects during exposure and the subsequent recovery. Chemosphere 73:395-400.
55. Fedtke C. 1982. Modes of herbicide action as determined with Chlamydomonas reinhardii and coulter counting. ACS Symposium Series 181:231-250.