Supporting Material

Supporting Material

Does the cost of adaptation to extremely stressful environments diminish over time? A literature synthesis on how plants adapt to heavy metals and pesticides

Evolutionary Biology

Justin SH Wan1 a, Clara K Pang a, and Stephen P Bonser a

a Evolution and Ecology Research Centre

School of Biological, Earth and Environmental Sciences

UNSW Australia

Sydney 2052

Australia

-

1 Author for Correspondence

Table S1

Data and references for: a) the assessment of costs for resistance to heavy metal (n = 34), resistance to triazine and P450 mechanism (n = 21), and other herbicides (n = 22) and; b) the assessment of benefits vs. costs for heavy metal (n = 38), and herbicides (n = 12).

a)

Heavy metal stress
Species / Family / Stressors / Log-time (yr.) / Performance trait / Life history / Effect size / Var. / References
Agrostis stolonifera / Poaceae / Cu / 1.85 / Root length / Perennial / -0.23 / 0 / Wu et al. 1975
Anthoxanthum odoratum / Poaceae / NaCl / 1.60 / Dry weight / Perennial / 0.22 / 0.001 / Kiang 1982
Anthoxanthum odoratum / Poaceae / Pb, Zn / 2.45 / Dry weight / Perennial / -1.20 / 0.003 / Hickey and McNeilly 1975
Chloris barbata / Poaceae / Cd, Hg, Zn / 1.43 / Root length / Perennial / -0.52 / 0.001 / Patra et al. 1994
Cynodon dactylon / Poaceae / Cu, Pb, Zn / 1.64 / Root length / Perennial / 0.33 / 0.012 / Shu et al. 2002
Deschampsia cepitosa / Poaceae / Ni, Pb / 0.78 / Root length / Perennial / 0.32 / 0.001 / Cox and Hutchinson 1980
Festuca rubra / Poaceae / Pb, Zn / 1.90 / Root length / Perennial / -0.02 / 0 / Karataglis 1982
Holcus lanatus / Poaceae / As / 2.15 / Root length / Perennial / -0.13 / 0.002 / McNair and Cumbes 1987
Spartina densiflora / Poaceae / As,Cu,Pb,Zn / 2.30 / Growth rate / Perennial / 0.38 / 0.038 / Mateos-Naranjo et al. 2011
Typha latifolia / Poaceae / Cu,Ni,Zn / 2.60 / Dry weight / Perennial / -0.35 / 0.015 / Ye et al. 1997
Typha latifolia / Poaceae / Cd,Pb,Zn / 2.30 / Dry weight / Perennial / -0.45 / 0.018 / Ye et al. 1997
Typha latifolia / Poaceae / Cd,Pb,Zn / 1.51 / Dry weight / Perennial / -0.37 / 0.021 / Ye et al. 1997
Cytisus striatus / Fabaceae / As / 1.85 / Root length / Perennial / -0.21 / 0.012 / Bleeker et al. 2003
Kummerowia stipulacea / Fabaceae / Cu,Pb,Zn / 3.48 / Reproductive mass / Annual / -0.62 / 0.012 / Gan et al. 2013
Elsholtzia argyi / Lamiaceae / Cu, Pb / 1.77 / Dry weight / Annual / 0.01 / 0.003 / Islam et al. 2010
Crepidorhopalon (Lindernia) tenuis / Linderniaceae / Co, Cu / 1.96 / Dry weight / Annual / -0.41 / 0.026 / Faucon et al. 2012
Paspalum distichum / Poaceae / Cu.Pb,Zn / 1.57 / Root length / Perennial / -0.38 / 0.002 / Shu et al. 2002
Paspalum distichum / Poaceae / Cu,Pb,Zn / 1.64 / Root length / Perennial / -0.52 / 0.002 / Shu et al. 2002
Mimulus guttatus / Phrymaceae / Cu / 2.14 / Dry weight / Annual / -0.35 / 0.001 / Harper et al. 1997
Plantago lanceolata / Plantaginaceae / Cu,Pb,Zn / 2.18 / Root length / Perennial / -0.08 / 0.015 / Pollard 1980
Plantago lanceolata / Plantaginaceae / Pb, Zn / 2.11 / Dry weight / Perennial / -1.61 / 0.003 / Hickey and McNeilly 1975
Armeria maritima / Plumbaginaceae / Pb, Zn / 2.11 / Inflorescence diameter / Perennial / -0.16 / 0.063 / Abratowska et al. 2012
Armeria maritima / Plumbaginaceae / Cu / 1.96 / Pollen fecundity / Perennial / -0.10 / 0.007 / Vekemans and Lefèbvre 1997
Armeria maritima / Plumbaginaceae / Pb, Zn / 3.30 / Pollen fecundity / Perennial / -0.30 / 0.003 / Vekemans and Lefèbvre 1997
Armeria maritima / Plumbaginaceae / Cu / 2.72 / Pollen fecundity / Perennial / -0.15 / 0.003 / Vekemans and Lefèbvre 1997
Armeria maritima / Plumbaginaceae / Pb, Zn / 2.17 / Pollen fecundity / Perennial / -0.15 / 0.004 / Vekemans and Lefèbvre 1997
Rumex japonicus / Polygonaceae / Cu / 3.48 / Dry weight / Perennial / -0.29 / 0.001 / Ke et al. 2007
Rumex dentatus / Polygonaceae / Cu / 3.48 / Reproductive mass / Annual / -0.15 / 0 / Huang et al. 2011
Rumex acetosa / Polygonaceae / Pb, Zn / 2.11 / Dry weight / Perennial / -1.51 / 0.008 / Hickey and McNeilly 1975
Salix caprea / Saliceae / Cd, Zn / 2.48 / Leaf dry weight / Perennial / -0.20 / 0.009 / Puschenreiter et al. 2010
Acer rubrum / Sapindaceae / Cu, Ni / 2.00 / Dry weight / Perennial / 0.32 / 0.013 / Kirkey et al. 2012
Silene vulgaris / Caryophyllaceae / Cu / 2.69 / Dry weight / Perennial / -1.25 / 0.045 / Lolkema et al. 1986
Betula pubescens / Betulaceae / Cu,Ni,SO2 / 1.89 / Plant height / Perennial / -0.11 / 0 / Eränen et al. 2008
Betula papyrifera / Betulaceae / Cu, Ni / 2.00 / Dry weight / Perennial / 0.61 / 0.042 / Kirkey et al. 2012
Herbicide stress / (Triazine, atrazine) / * P450 mechanism
Species / Family / Stressors / Time (year) / Performance trait / Life history / Effect size / Var. / References
Lolium rigidum / Poaceae / * diclofop-methyl , ACCase / 39 / Dry weight under competition / Annual / -0.25 / 0.004 / Vila-Aiub et al. 2009
Lolium rigidum / Poaceae / * APP, CHD, diclofop-methyl / 23 / Dry weight / Annual / -0.00 / 0.013 / Vila-Aiub et al. 2005
Lolium rigidum / Poaceae / * Atrazine, chlorotoluron / 17 / Fresh weight / Annual / -0.12 / 0.005 / Burnet et al. 1993
Lolium rigidum / Poaceae / * Atrazine, amitrole / 10 / Fresh weight / Annual / -0.07 / 0.002 / Burnet et al. 1993
Phalaris paradoxa / Poaceae / Triazine / 8 / Growth rate / Annual / 0.06 / 0 / Schonfeld et al. 1987
Amaranthus hybridus / Amaranthaceae / Triazine / 20 / Reproductive mass / Annual / -0.13 / 0.002 / Jordan 1996
Amaranthus hybridus / Amaranthaceae / Triazine / 24 / Reproductive mass / Annual / -0.11 / 0.001 / Jordan 1996
Amaranthus hybridus / Amaranthaceae / Triazine / 28 / Reproductive mass (intersp. competition) / Annual / -0.93 / 0.115 / Gassman and Futuyma 2004
Amaranthus rudis / Amaranthaceae / Triazine / 13 / Dry weight / Annual / -0.74 / 0.01 / Anderson et al. 1996
Amaranthus retroflexus / Amaranthaceae / Atrazine / 0.01 / Seed number / Annual / -0.13 / 0.121 / Weaver and Warwick 1982
Amaranthus powellii / Amaranthaceae / Atrazine / 3 / Seed number / Annual / -0.06 / 0.063 / Weaver and Warwick 1982
Chenopodium album / Amaranthaceae / Atrazine / 5 / Reproductive mass (intrasp. competition) / Annual / -0.30 / 0.004 / Warwick and Black 1981
Chenopodium album / Amaranthaceae / Atrazine / 5 / Reproductive mass / Annual / 0.00 / 0.006 / Warwick and Black 1981
Senecio vulgaris / Asteraceae / Triazine / 0.01 / Reproductive mass / Annual / -0.55 / 0.006 / Warwick 1980
Senecio vulgaris / Asteraceae / Triazine / 19 / Reproductive mass / Annual / -0.61 / 0.019 / Warwick 1980
Senecio vulgaris / Asteraceae / Triazine / 13 / Dry weight / Annual / -0.67 / 0.001 / Holt and Radosevich 1983
Senecio vulgaris / Asteraceae / Atrazine / 21 / Dry weight / Annual / -0.30 / 0.011 / Conard and Radosevich 1979
Datura stramonium / Solanaceae / Triazine / 3 / Reproductive mass / Annual / -0.66 / 0.046 / Williams et al. 1995
Solanum nigrum / Solanaceae / Triazine / 17 / Germination rate (high temp.) / Perennial / 0.49 / 0.001 / Kremer and Lotz 1998
Herbicide stress / (Other herbicides)
Species / Family / Stressors / Time (year) / Performance trait / Life history / Effect size / Var. / References
Hordeum leporium / Poaceae / Paraquat / 12 / Dry weight / Annual / -0.41 / 0.001 / Purba et al. 1996
Lolium rigidum / Poaceae / Paraquat / 15 / Dry weight / Annual / -0.09 / 0.002 / Powles et al. 1998
Lolium rigidum / Poaceae / Diclofop-methyl / 2 / Germination rate (high temp.) / Annual / -0.05 / 0 / Dastoori et al. 2012
Eleusine indica / Poaceae / Paraquat, glufosinate / 5 / Fresh weight / Annual / 0.02 / 0.003 / Seng et al. 2010
Eleusine indica / Poaceae / Glyphosate / 5 / Germination rate (high temp.) / Annual / 1.46 / 0.073 / Ismail et al. 2002
Echinochloa crus-galli / Poaceae / Clomazone / 3 / Dry weight / Annual / 0.07 / 0.009 / Bagavathiannan et al. 2011
Echinochloa crus-galli / Poaceae / Propanil / 8 / Growth rate / Annual / 0.02 / 0.01 / Bagavathiannan et al. 2011
Echinochloa crus-galli / Poaceae / Propanil, cyhalfop-butyl / 30 / Fresh weight / Annual / 0.24 / 0 / Rahman et al. 2010
Echinochloa crus-galli / Poaceae / Propanil / 30 / Germination rate / Annual / 0.03 / 0.004 / Marambe and Amarasinghe 2002
Amaranthus tuberculatus / Amaranthaceae / Glyphosate / 10 / Dry weight / Annual / 0.19 / 0.001 / Zelaya and Owen 2005
Kochia scoparia / Amaranthaceae / Dicamba, fluroxypyr / 12 / Dry weight / Perennial / -0.11 / 0.077 / Menalled and Smith 2007
Kochia scoparia / Amaranthaceae / Sulfonylurea / 10 / Total leaf area / Perennial / -0.15 / 0.019 / Christoffoleti et al. 1997
Kochia scoparia / Amaranthaceae / Sulfonylurea / 1 / Dry weight / Perennial / -0.23 / 0.076 / Thompson et al. 1994
Kochia scoparia / Amaranthaceae / Sulfonylurea / 1 / Dry weight / Perennial / -0.07 / 0.049 / Thompson et al. 1994
Kochia scoparia / Amaranthaceae / Sulfonylurea / 5 / Germination rate (low temp.) / Perennial / 0.88 / 0.021 / Dyer et al. 1993
Xanthium strumarium / Asteraceae / ALS / 35 / Dry weight / Annual / -0.14 / 0.011 / Crooks et al. 2005
Conyza canadensis / Asteraceae / ALS / 4 / Seed number / Annual / -0.54 / 0.08 / Davis et al. 2009
Conyza canadensis / Asteraceae / Glyphosate / 6 / Seed number / Annual / -1.82 / 0.59 / Davis et al. 2009
Conyza canadensis / Asteraceae / ALS, glyphosate / 6 / Seed number / Annual / 0.90 / 0.12 / Davis et al. 2009
Lactuca serriola / Asteraceae / Chlorsulfuron, imazapyr / 12 / Leaf area / Annual / 0.35 / 0.006 / Mallory-Smith et al. 1990

b)

Metal Stress
Species / Family / Time
(log yr.) / Trait / Benefit index (B) / Cost index(C) / Net Benefit
(B – C) / Reference
Agrostis tenuis / Poaceae / 2.78 / Root length / 0.75 / -0.06 / 0.81 / McNeilly and Bradshaw 1982
Betula pubescens / Betulaceae / 1.89 / Plant height / 0.22 / 0.11 / 0.1 / Eränen et al. 2008
Thlaspi caerulescens / Brassicaceae / 2.18 / Fruit number / 0.91 / 0.54 / 0.37 / Dechamps et al. 2008
Agrostis tenuis / Poaceae / 2.90 / Survival at 7 weeks / 1 / -0.24 / 1.24 / McNeilly 1968
Agrostis tenuis / Poaceae / 2.46 / Root length / 0.18 / -0.01 / 0.19 / Karataglis 1980
Agrostis tenuis / Poaceae / 2.34 / Root length / 0.68 / 0.02 / 0.66 / Karataglis 1980
Agrostis stolonifera / Poaceae / 1.85 / Root length / 0.9 / 0.2 / 0.69 / Wu et al. 1975
Agrostis capillaris / Poaceae / 1.98 / Dry weight / 0.36 / 0.09 / 0.27 / Dueck et al. 1987
Anthoxanthum odoratum / Poaceae / 1.60 / Reproductive mass / 0.28 / -0.25 / 0.53 / Kiang 1982
Bromus rubens / Poaceae / 1.40 / Dry weight / 0.64 / 0.29 / 0.35 / Preston 1993
Calamagrostis epigejos / Poaceae / 1.73 / Dry weight / 0.37 / 0.58 / -0.21 / Lehmann and Rebele 2004
Chloris barbata / Poaceae / 1.43 / Root length / 0.09 / 0.41 / -0.32 / Patra et al. 1994
Cynodon dactylon / Poaceae / 1.64 / Root length / 0.59 / -0.38 / 0.97 / Shu et al. 2002
Deschampsia cepitosa / Poaceae / 0.78 / Root length / 0.76 / -0.38 / 1.14 / Cox and Hutchinson 1980
Elymus repens / Poaceae / 1.73 / Dry weight / 0.26 / -0.34 / 0.6 / Lehmann and Rebele 2004
Festuca rubra / Poaceae / 1.90 / Root length / 0.74 / 0.02 / 0.72 / Karataglis 1982
Festuca rubra / Poaceae / 2.18 / Dry weight / 0.18 / 0 / 0.18 / Ayazloo and Bell 1981
Holcus lanatus / Poaceae / 2.15 / Root length / 0.74 / 0.12 / 0.61 / MacNair and Cumbes 1987
Holcus lanatus / Poaceae / 2.18 / Dry weight / 0.38 / -0.14 / 0.52 / Ayazloo and Bell 1981
Nardus stricta / Poaceae / 1.98 / Dry weight / 0.08 / 0.2 / -0.12 / Dueck et al. 1987
Phleum pratense / Poaceae / 1.45 / Dry weight / -0.13 / 0.08 / -0.21 / Clapperton and Reid 1994
Spartina densiflora / Poaceae / 2.30 / Growth rate / 0.43 / -0.46 / 0.89 / Mateos-Naranjo et al. 2011
Typha latifolia / Poaceae / 2.60 / Leaf elongation / 0.6 / 0.22 / 0.38 / Ye et al. 1997
Typha latifolia / Poaceae / 2.30 / Leaf elongation / 0.45 / 0.23 / 0.22 / Ye et al. 1997
Typha latifolia / Poaceae / 1.51 / Leaf elongation / 0.59 / 0.08 / 0.5 / Ye et al. 1997
Cytisus striatus / Fabaceae / 1.85 / Root length / 0.77 / 0.19 / 0.58 / Bleeker et al. 2003
Kummerowia stipulacea / Fabaceae / 3.48 / Seed number / 0.74 / 0.27 / 0.47 / Gan et al. 2013
Elsholtzia argyi / Lamiaceae / 1.77 / Dry weight / 0.25 / -0.01 / 0.26 / Islam et al. 2010
Crepidorhopalon tenuis / Linderniaceae / 1.96 / Dry weight / 0.82 / 0.34 / 0.48 / Faucon et al. 2012
Paspalum distichum / Poaceae / 1.57 / Root length / 0.6 / 0.35 / 0.25 / Shu et al. 2002
Paspalum distichum / Poaceae / 1.64 / Root length / 0.35 / 0.39 / -0.04 / Shu et al. 2002
Mimulus guttatus / Phrymaceae / 2.10 / Root length / 0.92 / 0.1 / 0.82 / MacNair et al. 1993
Mimulus guttatus / Phrymaceae / 2.14 / Dry weight / 0.3 / 0.18 / 0.11 / Harper et al. 1997
Plantago lanceolata / Plantaginaceae / 2.18 / Root length / 0.53 / 0.07 / 0.46 / Pollard 1980
Rumex japonicus / Polygonaceae / 3.48 / Dry weight / 0.34 / 0.25 / 0.09 / Ke et al. 2007
Rumex dentatus / Polygonaceae / 3.48 / Reproductive mass / 0.43 / 0.1 / 0.33 / Huang et al. 2011
Betula papyrifera / Betulaceae / 2.00 / Dry weight / 0.07 / 0.46 / -0.39 / Kirkey et al. 2012
Silene cucubalus / Caryophyllaceae / 2.69 / Dry weight / 0.36 / 0.71 / -0.35 / Lolkema et al. 1986
Herbicide stress
Species / Family / Time / Trait / Benefit index (B) / Cost index(C) / Net Benefit
(B – C) / Reference
Lolium rigidum / Poaceae / 17 / Fresh weight / 0.72 / 0.12 / 0.6 / Burnet et al. 1993
Lolium rigidum / Poaceae / 15 / Dry weight / 0.85 / 0.09 / 0.76 / Powles et al.1998
Lolium rigidum / Poaceae / 10 / Fresh weight / 0.64 / 0.07 / 0.58 / Burnet et al. 1993
Eleusine indica / Poaceae / 5 / Fresh weight / 0.43 / -0.02 / 0.44 / Seng et al. 2010
Avena fatua / Poaceae / 30 / Dry weight / 1 / -0.12 / 1.12 / O'Donovan et al. 1994
Echinochloa crus-galli / Poaceae / 30 / Fresh weight / 0.86 / -0.27 / 1.13 / Rahman et al. 2010
Echinochloa crus-galli / Poaceae / 30 / Dry weight / 0.9 / 0 / 0.9 / Marambe and Amarasinghe 2002
Amaranthus tuberculatus / Amaranthaceae / 10 / Dry weight / 0.39 / -0.17 / 0.55 / Zelaya and Owen 2005
Chenopodium album / Amaranthaceae / 7 / Dry weight / 0.64 / -0.02 / 0.66 / Marriage and Warwick 1980
Conyza canadensis / Asteraceae / 4 / Seed number / 1 / 0.42 / 0.58 / Davis et al. 2009
Conyza canadensis / Asteraceae / 6 / Seed number / 1 / 0.84 / 0.16 / Davis et al. 2009
Lactuca serriola / Asteraceae / 12 / Leaf area / 0.9 / -0.3 / 1.19 / Mallory-Smith et al. 1990

Table S2