Marine Pollution Bulletin 79 (2014) 34–38

Contents lists available at ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Growth, nutrient status, and photosynthetic response

to diesel-contaminated soil of a cordgrass, Spartina argentinensis
Susana Redondo-Gómez a,⇑, María C. Petenello b, Susana R. Feldman b
a
Departamento de Biología Vegetal y Ecología, Facultad de Biología, Universidad de Sevilla, Apartado 1095, 41080 Sevilla, Spain
b
Biología, Facultad de Ciencias Agrarias y CIUNR, Universidad Nacional de Rosario, Argentina

a r t i c l e i n f o a b s t r a c t

Keywords: The present study was conduced to investigate the tolerance limits of Spartina argentinensis, which occurs
Growth in inland marshes of the Chaco-Pampean regions of Argentina, to diesel-contaminated soil. A glasshouse
Diesel tolerance experiment was designed to investigate the effect of diesel fuel from 0% to 3% on growth and photosyn-
Mycorrhizal index thetic apparatus of S. densiflora by measuring gas exchange and photosynthetic pigments. We also per-
Nutrient status
formed chemical analysis of plant samples, and determined mycorrhizal index. Tiller and root
Photosynthesis
Soil contamination
biomasses declined with increasing diesel fuel concentration, as well as photosynthetic rate (A). Reduc-
tions in A could be accounted for by non-stomatal limitations. Mycorrhizal roots of S. argentinensis were
reduced by the presence of diesel fuel, but did not affect its nutritional status; in fact, most element con-
centrations increased with diesel contamination. Despite the negative effect of diesel-contaminated soil,
S. argentinensis continued growing, which could be useful management options for phytorremediation of
diesel-contaminated soils.
Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction Duncan, 1999). Therefore, is very important to identify plants

Accidental oil spills represent a serious health risk to wetland
systems throughout the world (Pezeshki et al., 2000). Diesel fuel
is a complex mixture of petroleum hydrocarbons containing every-
thing from alkanes to naphthalenes which may interfere with nor-
mal plant development. Furthermore, polycyclic aromatic
hydrocarbons (PAHs) found in diesel spills are of particular concern
as they are relatively persistent in the soil (Wang et al., 1990).
There are urgent needs to find effective technologies to clean up
contaminated soils.
Phytoremediation, the use of plants to detoxify polluted envi-
ronments, is under active investigation as a low-cost and environ-
mentally friendly technique for restoration of contaminated soils
and waters (Pilon-Smits, 2005). Plants have been shown to encour-
age organic contaminant reduction (Palmroth et al., 2002; Redon-
do-Gómez et al., 2011), principally by providing an optimal
environment for microbial proliferation in the rhizosphere (Kruger
et al., 1997). If plants can be successfully established on polluted
soils, then the plant–microbial interaction in the rhizosphere
may provide an economical method for enhancing microbial deg-
radation of complex organic contaminants. But, plants are very
sensitive and respond rapidly to diesel presence (Adam and
⇑ Corresponding author. Address: Dpto. Biología Vegetal y Ecología, Facultad de
Biología, Universidad de Sevilla, Avda. Reina Mercedes s/n, 41012 Sevilla, Spain.
Tel.: +34 95 4557165; fax: +34 95 4615780.
E-mail address: susana@us.es (S. Redondo-Gómez).
capable of growing in diesel-contaminated soils.
Spartina argentinensis Parodi is the dominant species of tempo-
rally flooded inland marsh communities of Argentina, growing in
hydro-halomorphic soils with high Na concentration in the upper
layers. These communities cover approximately three millions hect-
ares in the Chaco-Pampean regions of central Argentina (Cabrera
and Willink, 1973). Furthermore, this species has shown to be useful
for bioremediation; Redondo-Gómez et al. (2011) found that
S. argentinensis is a chromium hyperaccumulator. Nonetheless, no
studies have reported the physiological impact of diesel fuel. Consid-
ering that this species has high photosynthetic and growth rates,
resprouts after disturbance even under severe drought conditions
(Feldman et al., 2004; Feldman and Lewis, 2007), can germinate on
diesel contaminated substrates (Petenello and Feldman, 2012),
and that the closely related species, S. densiflora demonstrated high
tolerance to phenantrene (represents a class of more persistent
PAHs; Redondo-Gómez et al., 2011), it was hypothesized that
S. argentinensis could be used for diesel phytoremediation. Conse-
quently, the main objective of the present study was to evaluate
the tolerance of S. argentinensis to diesel contaminated soil. The
specific objectives were to: (1) analyze the growth of plants in exper-
imental diesel treatments ranging from 0% to 3% (v/w) diesel fuel; (2)
ascertain the extent to which effects on the photosynthetic appara-
tus, gas exchange characteristics and photosynthetic pigments
determine plant performance with diesel increasing; and (3)
examine possible role of mycorrhizal-colonization in roots of

0025-326X/$ - see front matter Ó 2014 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.marpolbul.2014.01.009
 S. Redondo-Gómez et al. / Marine Pollution Bulletin 79 (2014) 34–38
S. argentinensis and nutrient status in response to increasing external
diesel contamination in explaining effects on growth. A number of
studies (Adam and Duncan, 1999, 2003; Kechavarzi et al., 2007;
Lin and Mendelssohn, 2009; Lam, 2012; Petenello and Feldman,
2012) have investigated the effect of diesel on plant growth. How-
ever, to our knowledge, little is known about the extent to which ef-
fects of diesel on photosynthetic apparatus and nutrient status
determine plant performance.
2. Materials and methods
2.1. Plant material and stress treatments
Ripe spikes of S. argentinensis were collected in February 2012
from the glen of Ludueña stream (15 km SW Rosario, 32°450 S;
60°350 W, Santa Fe, Argentina). Caryopses were stripped from the
spikes and those containing seeds were selected and stored at
25 °C (in the dark).
Commercial diesel fuel (density, 0.875–0.900 g cm3 at 15 °C;
500 ppm S; Cetane index, 46; flashpoint, 48 °C; and viscosity,
3.5–5.0 cSt at 37.8 °C) was mixed with Vertic Argiudol soil (Roldán
series; clay 24.1%, silt 71.4% and sand 4.4%; total organic carbon
3.68%; total nitrogen 0.28%; assimilable phosphorous 44.1 ppm;
Cation Exchange Capacity 17.67; pH 6.65) from Faculty of Agricul-
tural Sciences (33°010 S; 60°530 W, Zavalla, Argentina) at 0%, 1%, 2%
and 3% (v/w), and field-moist soil was placed into polyethylene
bags. The soil–diesel mixture was allowed to stabilise for 72 h be-
fore planting. Because preliminary experiments indicated that the
use of high soil–diesel concentrations inhibited the growth of S.
argentinensis from seeds, the higher concentration of diesel fuel
was set to 3%.
In April 2012, seeds were placed in individual plastic pots
(15 cm of diameter and 20 of height) filled with 800 g of the appro-
priate soil–diesel mixture. The pots were allocated in shallow
trays; fifteen pots per tray, with one tray per diesel fuel treatment.
Trays were placed in a glasshouse (Rosario, Santa Fe, Argentina)
with controlled temperature of 21–25 °C, 40–60% relative humid-
ity and natural daylight. Pots were irrigated with tap water as nec-
essary. The possibility of adding NaCl to the culture medium was
disregarded because salt does not affect either the photosynthetic
functions or the growth of S. argentinensis.
Plants were grown for 250 days under the previously described
conditions, long enough to assess the tolerance in diesel-fuel-trea-
ted plants.
2.2. Growth analysis
Fifteen plants were harvested from each treatment at the end of
the experiment; plants were dried at 80 °C for 48 h and weighed.
The dry mass of tiller and root samples was determined.
2.3. Chemical analysis of plant samples
In accordance with protocols of Redondo-Gómez et al. (2007), at
the end of the experiment, tiller and root samples were dried at
80 °C for 48 h and ground. Tillers and roots were carefully washed
with distilled water before any further analysis. Then 0.5 g sam-
ples, taken from a mixture of the tillers or the roots belonging to
the 15 plants used for each treatment, were tripicately digested
with 6 ml HNO3, 0.5 ml HF and 1 ml H2O2. Ca, Cu, Fe, K, Mg, Mn,
P and Zn were measured by inductively coupled plasma (ICP-
AES) spectroscopy (ARL-Fisons 3410, USA). Reference materials
from Fisons certified for Ca, Cu, Fe, K, Mg, Mn, P and Zn were used
to check accuracy and precision in the analysis of total elements.
The average uncertainty of elements determination was in all cases
35
<2% (see for more details Cambrollé et al., 2008). Total N concen-
tration was determined for undigested dry samples with an ele-
mental analyser (Leco CHNS-932, Spain).
2.4. Gas exchange
Measurements were taken on random, fully expanded leaves
(n = 12) using an infrared gas analyzer in an open system (LI-6400,
LI-COR Inc., Neb., USA) after 220 d of treatment. Net photosynthetic
rate (A), intercellular CO2 concentration (Ci) and stomatal conduc-
tance to CO2 (Gs) were all determined at an ambient CO2 concentra-
tion of 360 lmol mol1, temperature of 25/28 °C, 50 ± 5% relative
humidity and a photon flux density of 1200 lmol m2 s1.
A, Ci and Gs were calculated using standard formulae from Von
Caemmerer and Farquhar (1981). Photosynthetic area was approx-
imated as the area of a trapezium.
2.5. Photosynthetic pigments concentration
Photosynthetic pigments of five tillers per treatment were
extracted using 0.05 g of fresh material in 5 ml of 80% aqueous
acetone. After filtering, 1 ml of the suspension was diluted with a
further 2 ml of acetone and chlorophyll a (Chl a), chlorophyll b
(Chl b) and carotenoid (Cx + c) contents were determined with a
Hitachi U-2001 spectrophotometer (Hitachi Ltd., Japan), using
three wavelengths (662, 645 and 470 nm). Concentrations of pig-
ments (lg g fwt1) were obtained through calculation Lichtenthal-
er (1987).
2.6. Mycorrhizal index
The mycorrhizal index, percentage of mycorrhizal short roots,
was determined by randomly examining 12 fresh roots per
soil–diesel treatment following established protocols (Vannette
and Rasmann, 2012). Fine root tissue (about 200 mg) was cleared
with 10% KOH for 10 min, acidified using 2% HCl and stained in
0.05% trypan blue in 1:1:1, water/glycerine/lactic acid. Roots were
mounted on slides and scored at 20 magnification with a Nikon
E600 (Melville, NY, USA) microscope using the magnified gridline
intersect method (McGonigle et al., 1990), with at least 100
intersections scored per sample. An intersection was considered
colonized if arbuscular mycorrhizal (AM) hyphae, arbuscules or
vesicles were present. Stained roots were also analyzed for coloni-
zation by non-AM fungi, which are distinguishable from mycorrhi-
zal hyphae by their linear hyphae and regular septa.
2.7. Statistical analysis
Statistical analysis was carried out using IBM SPSS Statistics v.
20 (IBM.corp) Pearson coefficients were calculated to assess corre-
lation between soil–diesel concentration and different variables.
Data were analyzed using a one-way analysis of variance (F-test).
Data were first tested for normality with the Kolmogorov–Smirnov
test and for homogeneity of variance with the Brown–Forsythe
test. Significant test results were followed by LSD test for identifi-
cation of important contrasts. In all cases, a significance level of
P < 0.05 was used.
3. Results
3.1. Growth analysis
Tiller and root biomasses declined with increasing diesel fuel
concentration (r = 0.75 and r = 0.72, for tiller and root bio-
masses respectively, P < 0.0001 for both; Fig. 1). Diesel fuel de-
36 S. Redondo-Gómez et al. / Marine Pollution Bulletin 79 (2014) 34–38
creased the total biomass of S. argentinensis by 65%, 89% and 92%
(with respect to plants grown without diesel oil) at 1%, 2% and
3% diesel fuel, respectively. However, Plants did not show chlorosis
at either of the treatments.
3.2. Chemical analysis of plant samples
Tissue Ca, Cu, Fe, Mn and Zn concentrations were greater in the
tillers than in roots, and tiller and root Mn (r = 0.86, P < 0.001 and
r = 0.88, P < 0.001, respectively), tiller N (r = 0.63, P < 0.05), and root
Ca (r = 0.80, P < 0.01), Cu (r = 0.72, P < 0.01), Fe (r = 0.93, P < 0.001),
Mg (r = 0.92, P < 0.001), P (r = 0.95, P < 0.001) and Zn (r = 0.85,
P < 0.001) contents increased with external diesel concentration;
while tiller Cu concentration diminished (r = 0.85, P < 0.001;
Table 1). In contrast, tiller and root K concentration showed no sig-
nificant response to increasing diesel concentration (P > 0.05). In
addition, tiller and root Cu, Mn and P contents were correlated
(Cu, r = 0.64, P < 0.05; Mn, r = 0.88, P < 0.0001; P, r = 0.73,
P < 0.01).
3.3. Gas exchange
Net photosynthetic rate (A) declined with increasing diesel con-
centration (r = 0.37, P < 0.01); and the highest A value was re-
corded at 0% diesel (ANOVA, P < 0.0001; Fig. 2A). Furthermore,
there was a significant relationship between total biomass and A
(r = 0.99, P < 0.01). In contrast, there were not relationships be-
tween stomatal conductance (Gs) and A, or Gs and diesel concen-
tration (Fig. 2B).
Moreover, intercellular CO2 concentration (Ci) increased with
increasing diesel concentration (r = 0.40, P < 0.01; Fig. 2C).
3.4. Photosynthetic pigment concentration
There was no effect of diesel treatment on chlorophyll a content
(Chl a; Fig. 3A), but chlorophyll b content (Chl b) diminished with
Fig. 1. Tiller (A) and root (B) biomasses of Spartina argentinensis grown at 0%, 1%, 2%
and 3% diesel fuel over 250 days. Values represent mean ± SE, n = 15. Different
letters indicate means that are significantly different from each other (LSD test,
P < 0.05).
increasing external diesel concentration after 250 d of treatment
(r = 0.61, P < 0.01; Fig 3B). Carotenoids (Cx + c) also showed no
relationship with diesel concentration (Fig. 3C).
3.5. Mycorrhizal index
The percentage of mycorrhizal roots declined with increasing
diesel fuel concentration (r = 0.94, P < 0.001), ranging between
77% and 7% for the control and the highest diesel concentration,
respectively (Fig. 4).
4. Discussion
Spartina argentinensis demonstrated low tolerance to diesel fuel
in the soil because its grown was lower than 50% of the control at
all diesel dosages (total biomass decreased by 65% at 1% diesel fuel)
after 250 days of exposure; the higher the level of pollution, the
more the effect. Hernández-Ortega et al. (2012) obtained similar
result for Melilotus albus; treatment of 0.75% diesel fuel reduced
its total biomass by 75% with respect to the control. Nevertheless,
residual oil concentrations in the sediment of up to 5% did not ad-
versely affect Spartina alterniflora (DeLaune et al., 1979), suggesting
the great difference in tolerance between plant species. However,
Lam (2012) recorded 60% and 15% survival of Spartina foliosa for
the crude oil and diesel treatments, respectively, possibly because
diesel refined nature and low-molecular weight make it more bio-
available to the plant. Otherwise, Lin and Mendelssohn (2009)
found that belowground biomass in the 8–16 cm subsurface sedi-
ment was affected at all diesel dosages, while live stem density
was significantly affected at oil dosages P16%. In contrast, the ef-
fect of diesel fuel in the soil on aboveground biomass of S. argentin-
ensis was more severe compared to the belowground component
(root biomass diminished by 65%, 88% and 91% and tiller biomass
by 71%, 90% and 92% at 1%, 2% and 3% diesel fuel, respectively).
Similar result was recorded for perennial ryegrass in 2.5% diesel
contaminated subsurface soil layers (Kechavarzi et al., 2007).
The declining growth of S. argentinensis in presence of diesel
contamination may be attributed to a decrease in A. Pajević et al.
(2009) also found that photosynthetic rates of willow genotypes
diminished in soil polluted with 1% diesel fuel, and explained that
inhibition of Gs in plants grown under conditions of soil contami-
nation indicated that depression of photosynthesis occurred to a
great extent at the stomatal level. In the present experiment, the
limitation to net photosynthetic rate was not because of Gs; there
is no correlation between A and Gs. Furthermore, we recorded an
increase of Ci with increasing diesel concentration, which could
be linked to a decrease in RuBisCO activity (Monnet et al., 2001;
Mateos Naranjo et al., 2008).
On the other hand, diesel dosages higher than 2% enhanced til-
ler Mn concentrations and decreased chlorophyll b contents of S.
argentinensis. Related to this, Mn (55 mg kg1) has been de-
scribed to have a toxic effect on chlorophyll content, especially
on concentrations of chlorophyll b (Macfie and Taylor, 1992). Addi-
tionally, decreased chlorophyll b contents could be partially attrib-
uted to lower tiller copper concentration in presence of diesel fuel,
as noted Peng et al. (2013). The decrease in pigment concentration
or an increase in pigment degradation could also lead to a decline
in photosynthetic functioning of S. argentinensis.
Mycorrhizal-colonization in roots of S. argentinensis was signif-
icantly reduced by the presence of diesel fuel, although mycorrhi-
zal associations were still developed. Kirk et al. (2005) noted that,
in the presence of plant roots, diesel reduced fungal colonization,
germ tube and hyphal growth; they hypothesized that diesel inter-
fered with communication between the plant and fungus as well as
having toxic effects on fungal growth. However, it did not affect the
 S. Redondo-Gómez et al. / Marine Pollution Bulletin 79 (2014) 34–38 37

Table 1
Total Ca, Cu, Fe, K, Mg, Mn, N, P and Zn concentrations for tillers and roots of Spartina alterniflora grown at 0%, 1%, 2% and 3% diesel fuel over 250 days. Values represent mean ± SE,
n = 3. Means within a diesel treatment that have different letter are significantly different from each other (LSD test, P < 0.05).

Treatment Tiller concentration

Diesel fuel (%) Ca (mg g1) Cu (mg kg1) Fe (mg kg1) K (mg g1) Mg (mg g1) Mn (mg kg1) N (mg g1) P (mg g1) Zn (mg kg1)
a c a a a a b a
0 0.09 ± 0.006 2.1 ± 0.08 76 ± 10.8 1.51 ± 0.133 0.09 ± 0.008 37 ± 2.8 11.1 ± 0.16 0.07 ± 0.006 7.5 ± 0.43a
1 0.09 ± 0.004a 1.8 ± 0.06bc 86 ± 5.5a 1.68 ± 0.007a 0.10 ± 0.002ab 37 ± 0.7a 9.9 ± 0.04a 0.07 ± 0.001a 5.6 ± 0.14a
2 0.10 ± 0.007a 1.7 ± 0.16ab 81 ± 2.4a 1.74 ± 0.039a 0.13 ± 0.004b 124 ± 5.4b 12.9 ± 0.41c 0.10 ± 0.003b 6.9 ± 0.86a
3 0.10 ± 0.010a 1.4 ± 0.11a 93 ± 3.4a 1.71 ± 0.164a 0.12 ± 0.011ab 122 ± 15.4b 12.5 ± 0.38c 0.08 ± 0.008ab 6.7 ± 0.76a
Root concentration
0 0.17 ± 0.018a 5.7 ± 0.62a 836 ± 58.5a 0.53 ± 0.016b 0.07 ± 0.04a 206 ± 15.4a 7.5 ± 0.30a 0.04 ± 0.002a 19.5 ± 2.05a
1 0.18 ± 0.024a 7.2 ± 0.66ab 1707 ± 222.2b 0.57 ± 0.007b 0.09 ± 0.007a 453 ± 61.5b 8.9 ± 0.79a 0.07 ± 0.003b 22.1 ± 2.22a
2 0.28 ± 0.014b 11.1 ± 0.76c 4933 ± 319.7c 0.46 ± 0.029a 0.11 ± 0.005b 1047 ± 73.6c 9.1 ± 0.73a 0.13 ± 0.006c 32.5 ± 1.74b
3 0.28 ± 0.020b 9.3 ± 0.71bc 5164 ± 229.6c 0.71 ± 0.016c 0.13 ± 0.006b 937 ± 66.5c 9.4 ± 0.92a 0.14 ± 0.005c 33.0 ± 2.10b

Fig. 2. (A) Net photosynthetic rate (A), (B) stomatal conductance (Gs), (C)
Fig. 3. (A) Chlorophyll a (Chl a), (B) chlorophyll b (Chl b) and (C) carotenoid (Cx + c)
intercellular CO2 concentration (Ci) in Spartina argentinensis grown at 0%, 1%, 2%
concentrations in Spartina argentinensis grown at 0%, 1%, 2% and 3% diesel fuel over
and 3% diesel fuel over 250 days. Values represent mean ± SE, n = 12. Different
250 days. Values represent mean ± SE, n = 5. Different letters indicate means that
letters indicate means that are significantly different from each other (LSD test,
are significantly different from each other (LSD test, P < 0.05).
P < 0.05).

nutrient uptake of S. argentinensis, since its element concentrations
increased with diesel contamination; except tiller Cu and K con-
centrations, which diminished and remained unchanged, respec-
tively. Thus, the role of mycorrhizal associations in nutrient
uptake of S. argentinensis was insignificant in the current study.
Hernández-Ortega et al. (2012) found that plants of Melilotus albus
treated with 0.75% diesel had reduced content of elements com-
pared to plants without the contaminant, although arbuscular
mycorrhizal fungi (AMF)-plants had greater content of microele-
ments than non-AMF plants.
When petroleum hydrocarbons contaminate soil, the added car-
bon stimulates microbial numbers and causes an imbalance in the
C:N ratio which may result in immobilization of soil nitrogen by
the microbial biomass, leaving none available for plant growth
(Xu and Johnson, 1997). Thus, studies on phytoremediation pay
particular attention to the performance of legumes versus other
38 S. Redondo-Gómez et al. / Marine Pollution Bulletin 79 (2014) 34–38
Fig. 4. Percentage of mycorrhizal roots in Spartina argentinensis grown at 0%, 1%, 2%
and 3% diesel fuel over 250 days. Values represent mean ± SE, n = 12. Different
letters indicate means that are significantly different from each other (LSD test,
P < 0.05).
plants species (Adam and Duncan, 2003). Surprisingly, tissue
nitrogen content of S. argentinensis increased with diesel pollution.
Otherwise, nitrate reductase (NRA) is an important enzymatic
activity in plants exposed to different environmental stresses
(Foyer et al., 1998; Taiz and Zeiger, 2002). In this regard,
Hernández-Ortega et al. (2012) noted that diesel induced greater
root NRA in Melilotus albus, suggesting that nitrogen assimilation
is a crucial process for plant establishment at contaminated soils.
In conclusion, diesel contamination resulted in negative effects
on the growth of S. argentinensis, which could be consequence of
reduced photosynthesis, but did not affect its nutritional status.
Despite the negative impact of the presence of diesel fuel, the
plants continued growing and did not exhibit chlorosis after
250 d of treatment; therefore, this species can be useful manage-
ment options for phytorremediation of diesel-contaminated soils.
However, the continuous exposition to diesel-contaminated soils
might affect in acute manner photosynthesis, with consequences
at the mineral balance. Thus, long-term studies will be needed in
the future.
Acknowledgements
We are grateful to the Council of the National University of
Rosario (Argentina; AGR-164) and Spanish Science and Technology
Ministry and Andalusian Council for their supports (projects
CTM2008-04453 and P11-RNM-7274, respectively).
References
Adam, G., Duncan, H.J., 1999. Effect of diesel fuel on growth of selected plant
species. Environ. Geochem. Health 21, 353–357.
Adam, G., Duncan, H., 2003. The effect of diesel fuel on common vetch (Vicia sativa
L.) plants. Environ. Geochem. Health 25, 123–130.
Cabrera, A.L., Willink, A., 1973. Biogeografía de América Latina, Serie de Biología,
Monografía No. 13. OEA, Washington, D.C..
Cambrollé, J., Redondo-Gómez, S., Mateos-Naranjo, E., Figueroa, M.E., 2008.
Comparison of the role of two Spartina species in terms of phytostabilization
and bioaccumulation of metals in the estuarine sediment. Mar. Pollut. Bull. 56,
2037–2042.
DeLaune, R.D., Patrick Jr., W.H., Buresh, R.J., 1979. Effect of crude oil on a Louisiana
Spartina alterniflora salt marsh. Environ. Pollut. 20, 21–30.
Feldman, S.R., Bisaro, V., Lewis, J.P., 2004. Photosynthetic and growth responses to
fire of the subtropical-temperate grass Spartina argentinensis Parodi. Flora 199,
491–499.
Feldman, S.R., Lewis, J.P., 2007. Effect of fire on Spartina argentinensis Parodi
demographic characteristics. Wetlands 27, 785–793.
Foyer, C.H., Valadier, M.H., Migge, A., Becker, T.W., 1998. Drought/induced effects on
nitrate reductase activity and mRNA and on the coordination of nitrogen and
carbon metabolism in maize leaves. Plant Physiol. 117, 283–292.
Hernández-Ortega, H.A., Alarcón, A., Ferrera-Cerrato, R., Zavaleta-Mancera, H.A.,
López-Delgado, H.A., Mendoza-López, M.R., 2012. Arbuscular mycorrhizal fungi
on growth, nutrient status, and total antioxidant activity of Melilotus albus
during phytoremediation of a diesel-contaminated substrate. J. Environ.
Manage. 95, S319–S324.
Kechavarzi, C., Pettersson, K., Leeds-Harrison, P., Ritchie, L., Ledin, S., 2007. Root
establishment of perennial ryegrass (L. perenne) in diesel contaminated
subsurface soil layers. Environ. Pollut. 145, 68–74.
Kirk, J.L., Moutoglis, P., Klironomos, J., Lee, H., Trevors, J.T., 2005. Toxicity of diesel
fuel to germination, growth and colonization of Glomus intraradices in soil and
in vitro transformed carrot root cultures. Plant Soil 270, 23–30.
Kruger, E.L., Anderson, T.A., Coats, J.R., 1997. Phytoremediation of contaminated
water and soil. In: Kruger, E.L., Anderson, T.A., Coats, J.R. (Eds.),
Phytoremediation of soil and water contaminants. ACS Symposium Series
664. Americam Chemical Society, Washintong D.C., pp. 2–17.
Lam, K., 2012. Alaska crude oil and diesel effects on Californian Spartina foliosa and
Spartina foliosa  alterniflora hybrid cordgrass. Oil Effects on marsh cordgrass.
Environmental Sciences Senior Thesis Symposium, UC Berkeley Environmental
Sciences. University of California at Berkeley, Berkeley, California, pp. 1–16.
Lichtenthaler, H.K., 1987. Chlorophylls and carotenoids: pigments of photosynthetic
biomembranes. Method Enzymol. 148, 350–382.
Lin, Q., Mendelssohn, I.A., 2009. Potential of restoration and phytoremediation with
Juncus roemerianus for diesel-contaminated coastal wetlands. Ecol. Eng. 35, 85–
91.
Macfie, S.M., Taylor, G.J., 1992. The effects of excess manganese on photosynthetic
rate and concentration of chlorophyll in Triticum aestivum in solution culture.
Physiol. Plant. 85, 467–475.
Mateos Naranjo, E., Redondo-Gómez, S., Cambrollé, J., Luque, T., Figueroa, M.E.,
2008. Growth and photosynthetic responses to zinc stress of an invasive
cordgrass, Spartina densiflora. Plant Biol. 10, 754–762.
McGonigle, T.P., Miller, M.H., Evans, D.G., Fairchild, G.L., Swan, J.A., 1990. A new
method which gives an objective measure of colonization of roots by vesicular-
arbuscular mycorrhizal fungi. New Phytol. 115, 495–501.
Monnet, F., Vaillant, N., Vernay, P., Coudret, A., Sallanon, H., Hitmi, A., 2001.
Relationship between PSII activity, CO2 fixation, and Zn, Mn and Mg contents of
Lolium perenne under zinc stress. J. Plant Physiol. 158, 1137–1144.
Pajević, S., Borišev, M., Nataša, N., Krstić, B., Pilipović, A., Orlović, S., 2009.
Phytoremediation capacity of poplar (Populus spp.) and willow (Salix spp.)
clones in relation to photosynthesis. Arch. Biol. Sci., Belgrade 61, 239–247.
Palmroth, M.R.T., Pichtel, J., Puhakka, J.A., 2002. Phytoremediation of sudarctic soil
contaminated with diesel fuel. Bioresour. Technol. 84, 221–228.
Peng, H., Kroneck, P.M.H., Küpper, H., 2013. Toxicity and deficiency of copper in
Elsholtzia splenden affect photosynthesis biophysics, Pigments and metal
accumulation. Environ. Sci. Technol. 47, 6120–6128.
Petenello, M.C., Feldman, S.R., 2012. Evaluation of tolerance to soils contaminated
with diesel oil in plant species with bioremediation potencial. Acta Biológica
Colombiana 17, 589–598 (in Spanish).
Pezeshki, S.R., Hester, M.W., Lin, Q., Nyman, J.A., 2000. The effects of oil spill and
clean-up on dominant US Gulf Coast marsh macrophytes: a review. Environ.
Pollut. 108, 129–139.
Pilon-Smits, E., 2005. Phytoremediation. Annu. Rev. Plant Biol. 56, 15–39.
Redondo-Gómez, S., Mateos-Naranjo, E., Davy, A.J., Fernández-Muñoz, F.,
Castellanos, E., Luque, T., Figueroa, M.E., 2007. Growth and photosynthetic
responses to salinity of the salt-marsh shrub Atriplex portulacoides. Ann. Bot.
100, 555–563.
Redondo-Gómez, S., Andrades-Moreno, L., Parra, R., Valera-Burgos, J., Real, M.,
Mateos-Naranjo, E., Cox, L., Cornejo, J., 2011. Spartina densiflora demonstrates
high tolerante to phenanthrene in soils and reduces it concentration. Mar.
Pollut. Bull. 62, 1800–1808.
Vannette, R.L., Rasmann, S., 2012. Arbuscular mycorrhizal fungi mediate below-
ground plant-herbivore interactions: a phylogenetic study. Funct. Ecol. 26,
1033–1042.
Wang, X., Yu, X., Bartha, R., 1990. Effect of bioremediation of PAH residues in soil.
Environ. Sci. Technol. 24, 1086–1089.
Xu, J.G., Johnson, R.L., 1997. Nitrogen dynamics in soils with different hydrocarbon
contents planted to barley and field pea. Can. J. Soil Sci. 77, 453–458.
Taiz, L., Zeiger, E., 2002. Plant Physiology, third ed. Sinauer Associates Inc.,
Sunderland, MI.
Von Caemmerer, S., Farquhar, G.D., 1981. Some relationships between the
biochemistry of photosynthesis and the gas exchange of leaves. Planta 153,
377–387.