Advertisement

Symbiosis

, Volume 77, Issue 1, pp 23–39 | Cite as

Phylogeny of the egg-loving green alga Oophila amblystomatis (Chlamydomonadales) and its response to the herbicides atrazine and 2,4-D

  • Mohini Nema
  • Mark L. Hanson
  • Kirsten M. Müller
Article

Abstract

The spotted salamander (Ambystoma maculatum) shares a unique endosymbiotic relationship with the unicellular green alga, Oophila amblystomatis. Despite studies isolating and identifying O. amblystomatis in salamander eggs, the taxonomic identity of the alga remains a point of ongoing debate. In this study, the nuclear SSU rRNA gene was used to characterize two well-supported Oophila clades that include lineages identified from past studies in addition to new isolates from the current study. These two clades do not form a monophyletic group and, furthermore, O. amblystomatis appears to be paraphyletic with numerous other chlamydomonad algae. To gain further insight into the biogeographic variation of the host A. maculatum, the mitochondrial ND4 and control gene regions were examined and the phylogeography was observed to be similar to that noted in the literature. Additionally, the response of O. amblystomatis to atrazine and 2,4-dichlorophenoxyacetic acid following 96 h exposure and a 96 h recovery phase was characterized, as this is a plausible mechanism by which the development of the host salamander could be impaired by herbicides. At the 96 h growth rate, no-observed-effect concentrations were 64 μg/L and 30 mg/L for atrazine and 2,4-D, respectively. We observed full recovery ofO. amblystomatis at these concentrations within 96 h. These data suggest that atrazine and 2,4-D do not pose a significant risk to the symbiotic algae, or, indirectly, to the host salamander. In conclusion, we recommend a revision of the current taxonomy of O. amblystomatis, and demonstrate the need for species identification and thorough phylogenetic reconstruction in toxicity testing to accurately inform risk assessment.

Keywords

2,4-D Ambystoma Atrazine Nuclear SSU rRNA gene Oophila Phylogeny 

Notes

Acknowledgements

This research was supported by the Natural Sciences and Engineering Research Council (NSERC) Discovery Grant to KM and MH. Thanks to Leilan Baxter at the University of Guelph for her help with sampling and providing support with experiments. Thanks also to Craig Schneider at Trinity College, Connecticut for his insight on O. amblystomatis and its type specimen, which was integral to this study. We would finally like to acknowledge the two anonymous reviewers for taking their time to review our manuscript and provide helpful comments that contributed to the improvement of this manuscript.

Supplementary material

13199_2018_564_MOESM1_ESM.pdf (42 kb)
ESM 1 (PDF 42.1 kb)
13199_2018_564_MOESM2_ESM.pdf (46 kb)
ESM 2 (PDF 46 kb)
13199_2018_564_MOESM3_ESM.pdf (68 kb)
ESM 3 (PDF 68 kb)
13199_2018_564_MOESM4_ESM.pdf (56 kb)
ESM 4 (PDF 56 kb)
13199_2018_564_MOESM5_ESM.pdf (65 kb)
ESM 5 (PDF 65.2 kb)
13199_2018_564_MOESM6_ESM.pdf (95 kb)
ESM 6 (PDF 94.9 kb)
13199_2018_564_MOESM7_ESM.pdf (96 kb)
ESM 7 (PDF 96 kb)
13199_2018_564_MOESM8_ESM.pdf (96 kb)
ESM 8 (PDF 95.8 kb)
13199_2018_564_MOESM9_ESM.pdf (75 kb)
ESM 9 (PDF 74.6 kb)
13199_2018_564_MOESM10_ESM.pdf (81 kb)
ESM 10 (PDF 81.1 kb)
13199_2018_564_MOESM11_ESM.pdf (82 kb)
ESM 11 (PDF 82.1 kb)

References

  1. Andersen RA (ed) (2005) Algal culturing techniques. ElsevierGoogle Scholar
  2. Arèvalo E, Davis SK, Sites JW (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in Central Mexico. Syst Biol 43:387–418CrossRefGoogle Scholar
  3. Austin JD, Lougheed SC, Neidrauer L, Chek AA, Boag PT (2002) Cryptic lineages in a small frog: the post-glacial history of the spring peeper, Pseudacris crucifer (Anura: Hylidae). Mol Phylogenet Evol 25:316–329CrossRefGoogle Scholar
  4. Backhaus T, Faust M, Scholze M, Gramatica P, Vighi M, Grimme LH (2004) Joint algal toxicity of phenylurea herbicides is equally predictable by concentration addition and independent action. Environ Toxicol Chem 23:258–264CrossRefGoogle Scholar
  5. Baxter L, Brain R, Rodríguez-Gil JL, Hosmer A, Solomon K, Hanson M (2014) Response of the green alga Oophila sp., a salamander endosymbiont, to a PSII-inhibitor under laboratory conditions. Environ Toxicol Chem 33:1858–1864CrossRefGoogle Scholar
  6. Baxter L, Brain RA, Hosmer AJ, Nema M, Müller KM, Solomon KR, Hanson ML (2015) Effects of atrazine on egg masses of the yellow-spotted salamander (Ambystoma maculatum) and its endosymbiotic alga (Oophila amblystomatis). Environ Pollut 206:324–331CrossRefGoogle Scholar
  7. 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 85:470–480CrossRefGoogle Scholar
  8. Bishop CD, Miller AG (2014) Dynamics of the growth, life history transformation and photosynthetic capacity of Oophila amblystomatis (Chlorophyceae), a green algal symbiont associated with embryos of the northeastern yellow spotted salamander Ambystoma maculatum (Amphibia). Symbiosis 63:47–57CrossRefGoogle Scholar
  9. Blanck H (1984) Species dependent variation among aquatic organisms in their sensitivity to chemicals. Ecol Bull:107–119Google Scholar
  10. Boedeker C, Eggert A, Immers A, Wakana I (2010) Biogeography of Aegagropila linnaei (Cladophorophyceae, Chlorophyta): a widespread freshwater alga with low effective dispersal potential shows a glacial imprint in its distribution. J Biogeogr 37:1491–1503Google Scholar
  11. Boivin A, Amellal S, Schiavon M, Van Genuchten MT (2005) 2, 4-Dichlorophenoxyacetic acid (2, 4-D) sorption and degradation dynamics in three agricultural soils. Environ Pollut 138:92–99CrossRefGoogle Scholar
  12. Brain RA, Arnie JR, Porch JR, Hosmer AJ (2012) Recovery of photosynthesis and growth rate in green, blue–green, and diatom algae after exposure to atrazine. Environ Toxicol Chem 31:2572–2581CrossRefGoogle Scholar
  13. Buchheim MA, Chapman RL (1991) Phylogeny of the colonial green flagellates: a study of 18S and 26S rRNA sequence data. BioSystems 25:85–100CrossRefGoogle Scholar
  14. Buchheim MA, Turmel M, Zimmer EA, Chapman RL (1990) Phylogeny of Chlamydomonas (Chlorophyta) based on Cladistic analysis of nuclear 18S RNA sequence data. J Phycol 26:689–699CrossRefGoogle Scholar
  15. Buchheim MA, Lemieux C, Otis C, Gutell RR, Chapman RL, Turmel M (1996) Phylogeny of the Chlamydomonadales (Chlorophyceae): a comparison of ribosomal RNA gene sequences from the nucleus and the chloroplast. Mol Phylogenet Evol 5:391–402CrossRefGoogle Scholar
  16. 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(8):1155–1160CrossRefGoogle Scholar
  17. Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Divers Distrib 9:111–121CrossRefGoogle Scholar
  18. Church SA, Kraus JM, Mitchell JC, Church DR, Taylor DR (2003) Evidence for multiple Pleistocene refugia in the postglacial expansion of the eastern tiger salamander, Ambystoma tigrinum tigrinum. Evolution 57:372–383CrossRefGoogle Scholar
  19. Collins FS, Holden I, Setchell WA (1905) Phycotheca Boreali-Americana A collection of dried specimens of the algae of North America Fascile XXVI: 1267Google Scholar
  20. D’Amen M, Vignoli L, Bologna MA (2007) The effects of temperature and pH on the embryonic development of two species of Triturus (Caudata: Salamandridae). Amphibia-Reptilia 28:295–300CrossRefGoogle Scholar
  21. Davidson C, Shaffer HB, Jennings MR (2002) Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declines. Conserv Biol 16:1588–1601CrossRefGoogle Scholar
  22. Demchenko E, Mikhailyuk T, Coleman AW, Pröschold T (2012) Generic and species concepts in Microglena (previously the Chlamydomonas monadina group) revised using an integrative approach. Eur J Phycol 47:264–290CrossRefGoogle Scholar
  23. Driscoll CT, Driscoll KM, Mitchell MJ, Raynal DJ (2003) Effects of acidic deposition on forest and aquatic ecosystems in New York state. Environ Pollut 123:327–336CrossRefGoogle Scholar
  24. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefGoogle Scholar
  25. Ellesat KS, Yazdani M, Holth TF, Hylland K (2011) Species-dependent sensitivity to contaminants: an approach using primary hepatocyte cultures with three marine fish species. Mar Environ Res 72:216–224CrossRefGoogle Scholar
  26. Fairchild JF, Ruessler DS, Haverland PS, Carlson AR (1997) Comparative sensitivity of Selenastrum capricornutum and Lemna minor to sixteen herbicides. Arch Environ Contam Toxicol 32:353–357CrossRefGoogle Scholar
  27. Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685–695CrossRefGoogle Scholar
  28. Gilbert PW (1942) Observations on the eggs of Ambystoma maculatum with especial reference to the green algae found within the egg envelopes. Ecology 23:215–227CrossRefGoogle Scholar
  29. Gilbert PW (1944) The alga-egg relationship in Ambystoma maculatum, a case of symbiosis. Ecology 25:366–369CrossRefGoogle Scholar
  30. Gilliom RJ, Barbash JE, Crawford CG, Hamilton PA, Martin JD, Nakagaki N, Wolock DM et al. (2006) Pesticides in the nation's streams and ground water, 1992–2001 (no. 1291). Geological survey (US)Google Scholar
  31. Glozier NE, Struger J, Cessna AJ, Gledhill M, Rondeau M, Ernst WR, Murray JL et al (2012) Occurrence of glyphosate and acidic herbicides in select urban rivers and streams in Canada 2007. Environ Sci Pollut Res 19:821–834CrossRefGoogle Scholar
  32. Goff LJ, Stein JR (1978) Ammonia: basis for algal symbiosis in salamander egg masses. Life Sci 22:1463–1468CrossRefGoogle Scholar
  33. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4.6.2: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224CrossRefGoogle Scholar
  34. 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 216:452–459CrossRefGoogle Scholar
  35. Hanson ML, Wolff BA, Green JW, Kivi M, Panter GH, Warne MSJ, Ågerstrand M, Sumpter JP (2017) How we can make ecotoxicology more valuable to environmental protection. Sci Total Environ 578:228–235CrossRefGoogle Scholar
  36. Harrison RG, Wilens S (1969) Organization and development of the embryoGoogle Scholar
  37. Hoffmann M, Hilton-Taylor C, Angulo A, Böhm M, Brooks TM, Butchart SH, Chanson KE, Collen B, Cox NA, Darwall WR (2010) The impact of conservation on the status of the world’s vertebrates. Science 1194442Google Scholar
  38. Hoham RW, Bonome TA, Martin CW, Leebens-Mack J (2002) A combined 18S rDNA and rbcL phylogenetic analysis of Chloromonas and Chlamydomonas (Chlorophyceae, Volvocales) emphasizing snow and other cold-temperature habitats. J Phycol 38:1051–1064CrossRefGoogle Scholar
  39. Holzinger A, Dablander A, Gärtner G (2014) Investigations of cell morphology and reproduction in Macrochloris radiosa Ettl and Gärtner (Stephano-sphaerinia, Chlorophyta) by light-and WUDQVPLVVLRQ electron microscopy. Algological studies (Stuttgart, Germany: 2007) 144:95Google Scholar
  40. Hopkins WA (2007) Amphibians as models for studying environmental change. ILAR J 48:270–277CrossRefGoogle Scholar
  41. Hutchison VH, Hammen CS (1958) Oxygen utilization in the symbiosis of embryos of the salamander, Ambystoma maculatum and the alga, Oophila amblystomatis. Biol Bull 115:483–489CrossRefGoogle Scholar
  42. IBM Corp. Released (2015) IBM SPSS statistics for windows, Version 23.0. Armonk: IBM CorporationGoogle Scholar
  43. Jang H, Ehrenreich IM (2012) Genome-wide characterization of genetic variation in the unicellular, green alga Chlamydomonas reinhardtii. PLoS One 7:e41307CrossRefGoogle Scholar
  44. Kerney R (2011) Symbioses between salamander embryos and green algae. Symbiosis 54:107–117CrossRefGoogle Scholar
  45. Kerney R, Kim E, Hangarter RP, Heiss AA, Bishop CD, Hall BK (2011) Intracellular invasion of green algae in a salamander host. Proc Natl Acad Sci 108:6497–6502CrossRefGoogle Scholar
  46. Kim E, Lin Y, Kerney R, Blumenberg L, Bishop C (2014) Phylogenetic analysis of algal symbionts associated with four North American amphibian egg masses. PLoS One 9:e108915CrossRefGoogle Scholar
  47. Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method." PAM application Notes 1Google Scholar
  48. Lemieux C, Vincent AT, Labarre A, Otis C, Turmel M (2015) Chloroplast phylogenomic analysis of chlorophyte green algae identifies a novel lineage sister to the Sphaeropleales (Chlorophyceae). BMC Evol Biol 15:1CrossRefGoogle Scholar
  49. Leung J, Witt JD, Norwood W, Dixon DG (2016) Implications of Cu and Ni toxicity in two members of the Hyalella azteca cryptic species complex: mortality, growth, and bioaccumulation parameters. Environ Toxicol Chem 35:2817–2826CrossRefGoogle Scholar
  50. Lewis LA, Landberg T (2014) Evolutionary diversity of the symbiotic salamander algae, Oophila (Chlorophyta). Unpublished abstractGoogle Scholar
  51. Lin Y, Bishop CD (2015) Identification of free-living Oophila amblystomatis (Chlorophyceae) from yellow spotted salamander and wood frog breeding habitat. Phycologia 54:183–191CrossRefGoogle Scholar
  52. Lockert CK, Hoagland KD, Siegfried BD (2006) Comparative sensitivity of freshwater algae to atrazine. Bull Environ Contam Toxicol 76:73–79CrossRefGoogle Scholar
  53. Mann RM, Hyne RV, Choung CB, Wilson SP (2009) Amphibians and agricultural chemicals: review of the risks in a complex environment. Environ Pollut 157:2903–2927CrossRefGoogle Scholar
  54. Mayden RL (1985) Biogeography of Ouachita highland fishes. Southwest Nat 30:195–211CrossRefGoogle Scholar
  55. Mayden RL (1987) Pleistocene glaciation and historical biogeography of North American central highland fishes. Quaternary environments of Kansas. Kansas Geol Surv Guidebook Series 5:141–151Google Scholar
  56. McKnight ML, Shaffer HB (1997) Large, rapidly evolving intergenic spacers in the mitochondrial DNA of the salamander family Ambystomatidae (Amphibia: Caudata). Mol Biol Evol 14:1167–1176CrossRefGoogle Scholar
  57. Muto K, Nishikawa K, Kamikawa R, Miyashita H (2017) Symbiotic green algae in eggs of Hynobius nigrescens, an amphibian endemic to Japan. Phycol Res 65:171–174CrossRefGoogle Scholar
  58. Nakada T, Misawa K, Nozaki H (2008) Molecular systematics of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18S rRNA phylogenetic analyses. Mol Phylogenet Evol 48:281–291CrossRefGoogle Scholar
  59. Nakada T, Shinkawa H, Ito T, Tomita M (2010) Recharacterization of Chlamydomonas reinhardtii and its relatives with new isolates from Japan. J Plant Res 123:67–78CrossRefGoogle Scholar
  60. Nema M, Müller K (2016) Investigating the Phylogeography of the yellow spotted salamander, Ambystoma maculata, and taxonomic identity of its algal symbiont, Oophila amblystomatis. Poster presented at the 51st Annual Meeting of the Phycological Society of America. July 24-28, 2016. John Carroll University, Cleveland, OhioGoogle Scholar
  61. Newcomb HR, Regosin JV, Rodrigues DM, Reed JM, Windmiller BS, Romero LM (2003) Impacts of varying habitat quality on the physiological stress of spotted salamanders (Ambystoma maculatum). Anim Conserv 6:11–18CrossRefGoogle Scholar
  62. Olivier HM, Moon BR (2010) The effects of atrazine on spotted salamander embryos and their symbiotic alga. Ecotoxicology 19:654–661CrossRefGoogle Scholar
  63. Orr H (1888) Note on the development of amphibians, chiefly concerning the central nervous system: with additional observations on the hypothysis, mouth and the appendages and skeleton of the head. J Cell Sci 2(115):483–489Google Scholar
  64. Pflieger WL (1970) A distributional study of Missouri fishes. University of Kansas publications, museum of natural history. Map 20:225–570Google Scholar
  65. Phillips CA (1994) Geographic distribution of mitochondrial DNA variants and the historical biogeography of the spotted salamander, Ambystoma maculatum. Evolution 48:597–607CrossRefGoogle Scholar
  66. Pinder A, Friet S (1994) Oxygen transport in egg masses of the amphibians Rana sylvatica and Ambystoma maculatum: convection, diffusion and oxygen production by algae. J Exp Biol 197:17–30Google Scholar
  67. Pough FH, Wilson RE (1977) Acid precipitation and reproductive success of Ambystoma salamanders. Water Air Soil Pollut 7:307–316CrossRefGoogle Scholar
  68. Pröschold T, Marin B, Schlösser UG, Melkonian M (2001) Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152:265–300CrossRefGoogle Scholar
  69. Prosser RS, Brain RA, Hosmer AJ, Solomon KR, Hanson ML (2013) Assessing sensitivity and recovery of field-collected periphyton acutely exposed to atrazine using PSII inhibition under laboratory conditions. Ecotoxicology 22:1367–1383CrossRefGoogle Scholar
  70. Prosser RS, Brain RA, Andrus JM, Hosmer AJ, Solomon KR, Hanson ML (2015) Assessing temporal and spatial variation in sensitivity of communities of periphyton sampled from agroecosystem to, and ability to recover from, atrazine exposure. Ecotoxicol Environ Saf 118:204–216CrossRefGoogle Scholar
  71. Räsänen K, Laurila A, Merilä J (2002) Carry-over effects of embryonic acid conditions on development and growth of Rana temporaria tadpoles. Freshw Biol 47:19–30CrossRefGoogle Scholar
  72. Reemtsma T, Jekel M (eds.) (2006) Organic pollutants in the water cycle: properties, occurrence, analysis and environmental relevance of polar compounds. John Wiley & SonsGoogle Scholar
  73. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suiteGoogle Scholar
  74. Rioboo C, González O, Herrero C, Cid A (2002) Physiological response of freshwater microalga (Chlorella vulgaris) to triazine and phenylurea herbicides. Aquat Toxicol 59:225–235CrossRefGoogle Scholar
  75. Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22CrossRefGoogle Scholar
  76. Rocha-Olivares A, Fleeger JW, Foltz DW (2004) Differential tolerance among cryptic species: a potential cause of pollutant-related reductions in genetic diversity. Environ Toxicol Chem 23:2132–2137CrossRefGoogle Scholar
  77. Rodríguez-Gil JL, Brain R, Baxter L, Ruffell S, McConkey B, Solomon K, Hanson M (2014) Optimization of culturing conditions for toxicity testing with the alga Oophila sp.(Chlorophyceae), an amphibian endosymbiont. Environ Toxicol Chem 33:2566–2575CrossRefGoogle Scholar
  78. Rodriguez-Gil JL, Prosser R, Poirier D, Lissemore L, Thompson D, Hanson M, Solomon KR (2017) Aquatic hazard assessment of MON 0818, a commercial mixture of alkylamine ethoxylates commonly used in glyphosate-containing herbicide formulations. Part 1: species sensitivity distribution from laboratory acute exposures. Environ Toxicol Chem 36:501–511CrossRefGoogle Scholar
  79. Schultz N (2016) The symbiotic green algae, Oophila (Chlamydomonadales, Chlorophyceae): a heterotrophic growth study and taxonomic history. Master’s ThesisGoogle Scholar
  80. Shoup S, Lewis LA (2003) Polyphyletic origin of parallel basal bodies in swimming cells of chlorophycean green algae (Chlorophyta). J Phycol 39:789–796CrossRefGoogle Scholar
  81. Solomon KR, Baker DB, Richards RP, Dixon KR, Klaine SJ, La Point TW, Hall LW et al (1996) Ecological risk assessment of atrazine in North American surface waters. Environ Toxicol Chem 15:31–76CrossRefGoogle Scholar
  82. Soltis DE, Morris AB, McLachlan JS, Manos PS, Soltis PS (2006) Comparative phylogeography of unglaciated eastern North America. Mol Ecol 15:4261–4293CrossRefGoogle Scholar
  83. Song Y (2014) Insight into the mode of action of 2, 4-dichlorophenoxyacetic acid (2, 4-D) as an herbicide. J Integr Plant Biol 56:106–113CrossRefGoogle Scholar
  84. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786CrossRefGoogle Scholar
  85. Turmel M, Gutell RR, Mercier JP, Otis C, Lemieux C (1993) Analysis of the chloroplast large subunit ribosomal RNA gene from 17 Chlamydomonas taxa: three internal transcribed spacers and 12 group I intron insertion sites. J Mol Biol 232:446–467CrossRefGoogle Scholar
  86. United States Environmental Protection Agency [USEPA] (1996) Ecological effects test guidelines: OPPTS 850.5400 —Algal toxicity, tiers I and II. EPA 712/C/96/164 (1996). Washington, DCGoogle Scholar
  87. Van Der Kraak GJ, Hosmer AJ, Hanson ML, Kloas W, Solomon KR (2014) Effects of atrazine in fish, amphibians, and reptiles: an analysis based on quantitative weight of evidence. Crit Rev Toxicol 44:1–66CrossRefGoogle Scholar
  88. Wehr JD, Sheath RG, Kociolek JP (Eds.) (2015) Freshwater algae of North America: ecology and classification. ElsevierGoogle Scholar
  89. Wille N (1909) VII Abteilung. Chlorophyceae. Syllabus der Pflanzenfamilien Band 6. (Engler, A. Eds) Berlin: Verlag von Gebrüder BorntraegerGoogle Scholar
  90. Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, Melkonian M, Becker B (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11:1CrossRefGoogle Scholar
  91. Wong PK (2000) Effects of 2, 4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll–a synthesis of Scenedesmus quadricauda Berb 614. Chemosphere 41:177–182CrossRefGoogle Scholar
  92. Xue C (2014) An examination of the phylogenetic diversity of green algae (Chlorophyceae) that symbiose with spotted salamanders (Ambystoma maculatum) in the egg stage. Master’s ThesisGoogle Scholar
  93. Zamudio KR, Savage WK (2003) Historical isolation, range expansion, and secondary contact of two highly divergent mitochondrial lineages in spotted salamanders (Ambystoma maculatum). Evolution 57:1631–1652CrossRefGoogle Scholar
  94. Zhu J, Patzoldt WL, Radwan O, Tranel PJ, Clough SJ (2009) Effects of photosystem-II-interfering herbicides atrazine and bentazon on the soybean transcriptome. Plant Genome-US 2:191–205CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of BiologyUniversity of WaterlooWaterlooCanada
  2. 2.Department of Environment and GeographyUniversity of ManitobaWinnipegCanada

Personalised recommendations