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Role of Phytotoxin Tolerators
and Hyperaccumulators in
Plant Community Ecology
Chuck Casper
BZ 572 Phytoremediation
12/4/2012
http://www.ndsu.edu/pubweb/famulari
_research/commonSearch.php?plant
_letter=R
Presentation outline
1) Plant community development
a) differences on phytoxic sites
2) Mechanisms influencing plant community dynamics
a) Plant-Plant interactions (+ and -)
b) Regeneration and reproduction
i) seed dispersal mode
ii) reproduction method
http://www.downtoearth.org.in/content/just-forest
http://www.rustyparts.com
Metals and organic compounds alter
successional dynamics
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Many articles report significant differences in the initial colonization of bare ground on contaminated and
uncontaminated sites
“Pioneer” species differ
Rate of colonization or succession slowed, even inhibited on contaminated sites
Perhaps evidence for multiple stable states theory
http://www.iteachbio.com/Life%20Science/life.htm
Early seral or “pioneer” species
The first species to colonize site devoid of vegetation, thought to
facilitate other species, ameliorate conditions to allow
establishment of future species
 Phytotoxic compounds inhibited invasion by Chinese Tallow,
willow, rattlebrush, and salt cedar which are typical early seral or
pioneer species. (Olson and Fletcher 2000)
 Grasses planted for restoration were weak, died when soil
eroded, did not spread to bare unrestored plots
 Unintroduced grasses were more vigorous and spreading
 2 reasons plants can not colonize bare tailings
1) substrate lacks the appropriate microbiota such as
mycorrhizae
2) vegetative reproduction is much slower than by seed
Ryszka and Turnau 2007
Plant community characteristics
40 years post-disturbance urban brownfield contaminated w/ As,
Cd, Cr, Cu, Pb, Zn, V
 Betula populifolia, Populus deltoides occurred on areas of
increasing soil metal load
 Other species like emergent marshes restricted to areas with
low soil metal loads
 B. populifolia, P. deltoides accumulate Zn in leaf tissue at
extremely high levels
 Leaf litter re-deposits Zn, creates potential feedback loop
maintaining dominance by B. populifolia and P. deltoides
Gallagher et al. 2008, Gallagher et al. 2011
Pb/Zn tailing 1-30 years old in Poland
 Highest grass diversity on oldest plots
Ryszka and Turnau 2007
Pb/Zn tailings in China
 4 separate community types, with diversity increasing with time
Wang et al. 2011
Community Composition
Former industrial sludge basin contaminated by PAHs in Texas
 The three most prominent species based on area of ground
covered were mulberry tree (36%), Bermuda grass (19%),
and sunflower (9%), accounting for 64% of the total cover on
the basin (known accumulators)
 Composition much different from disturbed but
uncontaminated site
Olson and Fletcher 2000
Site polluted with Pb, Cd, Zn and sulphur dioxide since 15th
century
 Species number increased with distance from pollution
source (proxy for time)
 Willow were the only woody species present at the most
degraded plots (known accumulator)
Regvar et al. 2006
Composition cont’d
River valley in Spain w/ high pH (2.3 avg) and heavy metal
concentration, mining over 5,000 years (Fe, Cu, Zn, As, and Pb)
 Species richness decreases as degradation stage advances
 Flora comprised of Fe, Cu, Zn, Ni, and Pb excluders
Rufo and de la Fuente 2010
Rio Tinto, Spain
http://tourismplacesworld.blogspot.com/2011/06/acid-lake-rio-tinto-in-spain.html
Comparison of
hydrocarbon
contaminated site
with
uncontaminated
site
Robson et al. 2004
Robson et al. 2004
Altered development trajectory
After 20 years of natural and artificial rehabilitation of Pb/Zn
minelands (China) naturally invaded species were mostly
herbaceous (69.4% of total) especially from Poaceae and
Asteraceae families
 Succession theory predicted different community type
Li et al. 2007
Pb/Zn mine waste in Wisconsin
 Species composition changes with mine age, but successional
change in vegetative cover is minimal
 The relative proportion of open and closed turf communities
does not change significantly with time
Kimmerer 1989
Croplands unsuitable b/c heavy metal contamination in China
 One species pioneers and dominates croplands up to 13 years
after abandonment
Zhang et al. 2012
Slowed or inhibited succession
Rio Tinto, Spain
 In unaltered areas vegetation progresses toward steady plant
community or climax vegetation while slowed or inhibited on
altered sites
Rufo and de la Fuente 2010
Abandoned mine sites France, high levels of Zn, Pb, Cd, As, TI
 700 year old, 100 year old, and 10 year old sites
 Oldest site still not colonized by trees even though
surrounded by Castanea sativa (chestnut) forest
 In other nearby sites such as abandoned vineyards, bare soil
is colonized by annuals and eventually trees
within a century
Escarre et al. 2011
Question 1
 How is succession or plant community development different
on phytotoxin contaminated sites?
Positive interactions
Soils highly polluted with Zn, Cd, and Pb
 + interaction b/t Fabaceae anthyllis, and two grasses
 F. anthyllis regeneration highest when planted w/ grass
 grass cover provides shade facilitating F. anthyllis germination
 Facilitation is critical to early succession in this area, phytostabilization is
most effective when legumes and grasses planted together.
Frerot et al. 2006
Zn and Pb tailings 1-30 years old in Poland
 Unintroduced grasses were more
vigorous, spread faster, produced
more litter
 Facilitation- Natural colonizers promote
development of soil organic matter, a
crucial factor in establishment of other
plants
Ryszka and Turnau 2007
http://www.flickriver.com/photos/stationalpinejosephfou
rier/sets/72157603314028697/
Positive interactions cont’d
Increased application of heavy metals altered competition
 Increased uptake of Zn by one species reduced the negative
effect of that metal on the target species
 Highest concentration of Ni mitigated competive effect of
Salix caprea on Carex angustifolia
 Salix caprea attenuated negative effect of Zn on Centaurea
flava
 Medium Zn application enhanced competitive ability of Salix
caprea on Carex angustifolia
 Could improve remediation capacity with species mixtures
instead of monocultures
 Niche space filled
Koelbener et al. 2008
Facilitation
Selenium hyperaccumulators
 Higher soil Se concentration limits growth of Se sensitive
species-reduces competition
 Facilitate Se tolerant species through reduced herbivory
(El Mehdawi et al. 2011)
http://www.wildflower.org
http://www.ehleringer.net
Regeneration and reproduction
Site polluted with Pb, Cd, Zn and sulphur dioxide since 15th
century
 Grasses propagated and colonized mostly vegetatively not via
seed.
Regvar et al. 2006
 Self pollinating species more common on contaminated sites
 Seed dispersal via birds is lower, birds less likely to visit sites
with low plant cover
Robson et al. 2004
Pb/Zn tailings
 Colonization depended
on rhizome strategy
Wang et al. 2011
Question 2
 What reproductive strategy is common on disturbed sites
contaminated with phytotoxins?
Conclusions
 Phytotoxin contamination=altered
developmental trajectories
 Succession slowed or inhibited
 Community composition is different,
http://www.greateryellowstonescience.org/topics/scien
diversity lower
cemanagement/tools/thresholds
 Facilitation more likely a driver than competition
 Evidence for multiple stable
states theory?
 Better understanding of
ecology of contaminated sites
can yield more effective
phytoremediation strategies
http://www.williamscreekmgt.com/gallery/installation/keyston
e-enterprise-park-phytoremediation
References
Bizecki-Robson, D., Knight, J.D., Farrell, R.E., Germida, J.J. 2004. Natural revegetation of hydrocarbon-contaminated soil in semi-arid
grasslands. Canadian Journal of Botany. 82, 22-30
Escarre, J., Lefebvre, C., Raboyeau, S., Dossantos, A., Gruber, W., Marel, J.C.C., Frerot, H., Noret, N., Mahieu, S., Collin, C., Van Oort, F.
2011. Heavy Metal Concentration Survey in Soils and Plants of the Les Malines Mining District (Southern France)
Implications for Soil Restoration. Water Air and Soil Pollution. 216, 485-504
El Mehdawi, A.F., Quinn, C.F., Pilon-Smits, E.A.H. 2011. Selenium Hyperaccumulators Facilitate Selenium-Tolerant Neighbors via
Phytoenrichment and Reduced Herbivory. Current Biology 21, 1440-1449
El Mehdawi, A.F., and Pilon-Smits,E. A.H. 2012. Ecological aspects of plant selenium hyperaccumulation. Plant Biology 14, 1-10
Frerot, H., Lefebvre, C., Gruber, W., Collin, C., Dos Santos, A., Escarre, J. 2006. Specific interactions between local metallicolous plants
improve the phytostabilization of mine soils. Plant and Soil. 282, 53-65
Gallagher, F.J., Pechmann, I., Bogden, J.D., Grabosky, J., Wies, P. 2008. Soil metal concentrations and vegetative assemblage
structure in an urban brownfield. Environmental Pollution, 153, 351-361
Gallagher, F.J., Pechmann, I., Holzapfel, C., Grabosky, J. 2011. Altered vegetative assemblage trajectories within and urban brownfield.
Environmental Pollution. 159, 1159-1166
Kimmerer, R.W. 1989. Environmental Determinants of Spatial Pattern in the Vegetation of Pb-Zn Mines in Southwestern Wisconsin.
American Midland Naturalist. 121, 134-143
Koelbener, A., Ramseier, D., Suter, M., 2008. Competition alters plant species response to nickel and zinc. Plant Soil. 303, 241-251
Li, M.S., Luo, Y.P., Su, Z.Y. 2007. Heavy metal concentrations in soils and plant accumulation in a restored manganese mineland in
Guangxi, South China. Environmental Pollution. 147, 168-175
Olson, P.E., and Fletcher, J.S. 2000. Ecological Recovery of Vegetation at a Former Industrial Sludge Basin and its Implications to
Phytoremediation. Environmental Science and Pollution Research. 7, 195-204
Regvar, M., Vogel-Mikus, K., Kugonic, N., Turk, B., Batic, F. 2006. Vegetational and mycorrhizal successions at a metal polluted site: I
ndications for the direction of phytostabilization? Environmental Pollution. 144, 976-984
Rufo, L., and de la Fuente, V. 2010. Successional Dynamics of the Climatophile Vegetation of the Mining Territory of the Rio Tinto Basin
(Huelva, Spain): Soil Characteristics and Implications for Phytoremediation. Arid Land Research and Management. 24, 301327
Ryszka, P., and Turnau, K., 2007. Arbuscular mycorrhiza of introduced and native grasses colonizing zinc wastes: implications for
restoration practices. Plant Soil. 298, 219-229
Wang, J., Zhang, C.B., Ke, S.S., Qian, B.Y. 2011. Different spontaneous plant communities in Sanmen Pb/Zn mine tailings and their effects
of mine tailing physico-chemical properties. Environmental Earth Science. 62, 779-786
Zhang, C., Lie, G., Xue, S., Xiao, L., Ma, H., 2012. Rhizosphere Characteristic of Available Trace Elements During the Succession on
Abandoned Croplands in the Loess Plateau, China. Soil Science. 177, 619-627