Table Of ContentMadrono, Vol. 58, No. 3, pp. 145-152, 2011
A COMPARISON OF THE EFFECTS OF NA2SO4 AND NACL ON THE GROWTH
OF HELIANTHUS PARADOXUS AND HELIANTHUS ANNUUS (ASTERACEAE)
M. O. Mendez' and O. W. Van Auken
Department of Biology, University of Texas at San Antonio, San Antonio, TX 78249
[email protected]
Abstract
Helicmthusparadoxus Heiser(Asteraceae, puzzle sunflower), isa federally threatened hybrid species
found in salt marshes ofwest Texas and New Mexico. Helianthus anmius L. (Asteraceae, common
sunflower)isoneoftheparent speciesand isfound throughout NorthAmerica, but it isnot present in
the inland salt marshes where H. paradoxus is found. Helianthus paradoxus has previously been
described as a halophyte, but its tolerance to Na2S04, one ofthe major salts found in its habitat, has
not been investigated. However, salinity has been identified as a major abiotic factor influencing the
limited distribution of H. paradoxus populations. In this greenhouse study, the effects of elevated
concentrations ofNa2S04 and NaCl, at equal ionic strengths (0.00, 0.09, 0.17, 0.34, and 0.51), on the
survival and dry mass ofboth H. paradoxus and H. annuuswereexamined. In the three-way factorial
experiment, the effects on dry mass observed were dependent on the species, the type ofsalt and the
ionic strength ofthe salt. Helianthusparadoxus produced more dry mass than H. annuus in both salt
treatments; however, NaCl was more inhibitory ofdry mass production for both species with plants
unable to survive the highest salt treatments. While dry mass ofH. annuus decreased with increasing
ionic strengths ofboth salts, dry mass of H. paradoxus increased by 38 to 72% in low to moderate
ionic strengths ofNa2S04 relative to the nonsalinetreatment. Both specieswere less tolerant ofNaCl
than Na2S04 with H. paradoxus seeming to have moderate and high tolerance to elevated CI" and
S04^~ ionic strength, respectively, while H. annuus had low to moderate tolerance. Greater dry mass
production in Na2S04, along with tolerance to both salts, suggests that low to moderate sulfate soil
salinity will enhance the dry mass production ofH. paradoxus.
Key Words: Halophyte, helianthus annuus, helianthusparadoxus, ionic strength, NaCl, Na2S04, salt
tolerance, sunflower.
Helianthusparadoxus Heiser (Asteraceae, puz- Ecological and ecophysiological studies of H.
zle sunflower) is a federally threatened species paradoxus have determined that this homoploid
with limited distribution in salt marshes in west hybrid species is salt tolerant, unlike its parental
Texas and New Mexico (Correll and Johnston species. Helianthus paradoxus is restricted to
1979; Poole and Diamond 1993; McDonald inland salt marshes with salt levels of approxi-
1999). Hybridization studies (Heiser 1958, 1965; mately 10 g kg-' (Poole and Diamond 1993; U.S.
Abbott 1992) and molecular analysis (Rieseberg Fish and Wildlife Service 2005; Grunstra and
et al. 1990; Rieseberg 1991; Rieseberg et al. 1991) Van Auken 2007a, b), while H. annuus and H.
have determined that H. paradoxus is a stabilized petiolaris can be found in low saline soils
hybrid species between H. annuus L. (Asteraceae, (<0.02 g kg ' soil sodium, Welch and Rieseberg
common sunflower) and H. petiolaris Nutt. 2002). Helianthus paradoxus is a better compet-
(plains sunflower). Although H. paradoxus shares itor than its progenitors in saline soils (Bush and
several morphological and ecophysiological traits Van Auken 2004). The west Texas and New
with its parental species (Rosenthal et al. 2002), it Mexico salt marshes were key habitats in
has diverged and is genetically isolated from its isolating hybrids (Abbott 1992). The parental
progenitors and considered a separate species. species are glycophytes and cannot survive the
Helianthus anuus is common throughout North same habitat as H. paradoxus, where other salt
America and grows in disturbed, heavy clay soils tolerant plants are generally present (Poole and
that are moist in the spring and dry out by mid- Diamond 1993; Lexer et al. 2003; U.S. Fish and
summer. Helianthus petiolaris is found in dry, Wildlife Service 2005). Additionally, H. para-
sandy soils in western North America, while H. doxus is capable of sequestering higher sodium
paradoxus grows in heavy, waterlogged, saline and sulfur concentrations and produces greater
soils (Van Auken and Bush 1998). leaf succulence compared to its parental species
while maintaining significantly greater fitness
when grown in elevated NaCl concentrations
(Welch and Rieseberg 2002) or in field-like highly
ist'rCy,urrTeenxtasaddAre&ssM: DIenptaerrtnmateinotnaolf BUinoilveorgsyit&y,Ch5e2m01- salIinnetshoeillcarognedsittikonnsow(nKarproepnulbaetrigoent oalf. H2.006p)a.ra-
University Boulevard, Laredo, TX 78041, USA. doxus, at the Diamond-Y Spring Preserve near
MADRONO
146 [Vol. 58
Fort Stockton, Texas, the distribution of H. Table 1. Ionic Strengths of Each Treatment
paradoxus is mainly affected by soil salinity and AND Corresponding Salt Concentrations in
soil moisture gradients when biotic factors are GKG"' Examinedin the Study.
not considered (Bush and Van Auken 1997; Van
NaCl Na2S04
Auken and Bush 1998; Bush 2006a, b). This large
desert spring and associated salt marsh has had Ionic strength (g kg-')
1.44 to 2.70 million H. paradoxus plants (Van 0.00 0 0
Auken and Bush 1998), depending on environ- 0.09 5 4.1
mental conditions. In addition, there are several 0.17 10 8.1
rare and federally endangered invertebrates 0.34 20 16.2
found in the marsh (McDonald 1999). Helianthus 0.51 30 24.3
paradoxus plants consistently establish parallel to
the drainage of Leon Creek but their proximity The objective ofthis study was to examine the
depends on seasonalclimaticconditions influencing survival, growth and the salt tolerance of H.
soil salinity levels and soil water content, both of paradoxus in elevated levels ofboth Na2S04 and
whichdecreasedramaticallyuplandfromthelowest NaCl, at equal ionic strengths. Both ofthese salts
point in the salt marsh (Van Auken and Bush 1998; are major contributors of the soil salts of the
Grunstra and Van Auken 2007a, b). When annual Diamond-Y Spring Preserve. Our experiment
rainfall is high, H. paradoxuscan be found further also included themore salt tolerant ofits parental
from the drainage compared to drier years when species, H. annuus, a known glycophyte.
plants are located closer to the drainage. The
population of H. paradoxus at the Diamond-Y Materials and Methods
Spring Preserve seems to be dependent on low to
intermediate salinity levels and intermediate Helianthusparadoxusseedswerecollected from
moisture levels; however, saHnity appears to be the Nature Conservancy's Diamond-Y Spring
the major abiotic factor affecting the local Preserve near Fort Stockton, Texas (31°00.54'N,
distribution ofH. paradoxus (Bush 2006a, b). 102°55.49'W) and stored dry at 25°C until used.
Previous studies have identified H. paradoxus Helianthus annuus seeds were purchased from
as a salt tolerant species with characteristics of Native American Seed Farm (Junction, Texas
halophytes (Welch and Rieseberg 2002; Bush and 76849) and stored dry at 4°C. Seeds of both
Van Auken 2004). However, these studies were species were cold stratified in Ziploc® storage
done with NaCl, one of the major salt compo- bags lined with paper towels, wet with deionized
nents ofthe marsh, but not Na2S04 which is also water, and maintained at 4°C in the dark for
found at high concentrations in soils of its salt 4 weeks {H. paradoxus) or 8 weeks {H. annuus).
marsh habitat (Boghici 1997). In addition, the To prevent osmotic shock, groups of seeds
effects of a limited range of salinity levels have (approximately 400 seeds for each treatment)
been examined. Chloride is generally more toxic were germinated on paper toweling saturated
than S04-^~ and even Na^ at lower concentrations with deionized water (0.00 osmotic strength) in
(Manchanda et al. 1982; Marschner 1995; Frank- plastic storage bags at 25°C. Germinated seed-
lin and Zwiazek 2004; Munns and Tester 2008); lings were transferredto equal orincreasinglevels
however, S04^" salinity can be more growth of the appropriate salt (NaCl and Na2S04 at
inhibitive than C\~ for some halophytes (Warne ionic strengths of0.00, 0.05, 0.09, 0.13, 0.17, 0.26,
et al. 1990; Egan and Ungar 1998). At the same 0.34, 0.43, and 0.51) every 2 d until placed in the
time, separating specific ion effects is difficult and final salt (NaCl or Na2S04) and ionic strength to
differential effects ofCI" and S04^" salinity on H. be tested (0.00, 0.09, 0.17, 0.34, and 0.51).
paradoxus are still unknown; consequently, the Seedlings were kept in the appropriate solution
influence of these anions on the ecological for a total of 18 days prior to transplanting to
isolation and distribution of H. paradoxus has pots in the greenhouse containing the corre-
not yet been elucidated. sponding treatment (Table 1).
Ionic strength rather than salt concentration For each species, five plants per pot with five
was used as a treatment variable in the present replicate pots per treatment (25 plants per species
study. It is used as a normalization procedure and per treatment) were grown for 62 d. Plastic pots
was required because ofdifferent numbers ofions (15 cm diameter X 15 cm height) lined with a
present in equal molar solutions ofNaCl (2 ions) Ziploc® storage bag (to retain water, salts, and
and Na2S04 (3 ions). Therefore, it was important nutrients) were filled with 1.4 kg of air-dried,
mm
to compare the two salts at concentrations that sieved (5.8 mesh screen) soil. The soil was the
allowed osmotic potential of the corresponding upper 10 cm of a low nutrient Patrick-series
treatments to be equal. Concentrations ofthe two Mollisol (clayey-over-sandy, carbonatic-thermic,
salt treatments were based on equal ionic typic calciustoll), collected from northern Bexar
strengths calculated using procedures in Barrow Co., Texas (Taylor et al. 1966; Van Auken and
(1966). Bush 1998). The soil was friable, allowing root
2011] MENDEZ AND VAN AUKEN: SALT TOLERANCE OF TWO HELIANTHUS SPECIES 147
Table 2. Three-Way ANOVA Results for the Total Dry Mass (g) of Two Species {Helianthvs
PARADOXUSAND H. ANNUUS) GROWNIN TWO SALTS (NaCLAND NA2SO4) ANDAT FiVE lONIC STRENGTHS (0.00,
0.09, 0.17, 0.34, AND 0.51). All main effects and interactions were significant. Significant interactions are
designated (* = P < 0.05; ** = p < q.qI; *** = p < o.OOl; **** = P < 0.0001).
Source" df SS F P
Species 1 4.11 35.69 <0.000l
Salt 1 14.75 128.17 <0.0001
Strength 4 5.00 43.44 <0.0001
Species X salt*** 1 1.39 12.05 0.0008
Species X strength** 4 0.55 4.78 0.0016
Sak X strength**** 4 1.67 14.50 <0.0001
Species x salt x strength* 4 0.40 3.51 0.0108
Error 80 9.21
Total 99 59.95
extraction and recovery (Bush and Van Auken determine the effects of salt type and ionic
2004). Appropriate amounts of anhydrous salts strength on the dry mass of each species, a
ANOVA
(Na2S04 or NaCl) and a single nutrient applica- three-way including interactions was
tion (0.05 g ofP fromNa2HP04 • 7H2O, 0.07 g N employed. When significance was detected with
from NH4NO3, 0.07 g ofK from KCl and 0.03 g the overall ANOVA, two-way and one-way
of S from MgS04 7H2O; Tiedemann and ANOVAs were used followed by Duncan's
•
Klemmedson 1986) were added to each pot and Multiple Range Test to examine significant
thoroughly mixed. Before seedlings were planted, differences between all possible combinations of
400 ml ofdeionized water was added to each pot. salt type and salt concentration for each species
Thereafter, soil moisture was maintained at separately. Mean mortality was calculated, but
approximately field capacity with distilled water. was not analyzed statistically.
This study was conducted in a fiberglass green-
house in which the daytime temperatures ranged Results
from approximately 26' to 38°C and light levels
were approximately 36% of full sunlight with a All H. paradoxus and H. annuus plants died in
mean photosynthetically active photon flux den- the highest ionic strengths of NaCl examined
sities of562 ± 135 fimol m"- s~' measured with a (0.34 and 0.51). However, both species demon-
Li-Cor® LI-188 integrating quantum sensor. strated 100% survivorship in the no-salt treat-
Plant survivorship was assessed at 62 d for ment. For all Na2S04 treatments, 100% of H.
each treatment combination (species X salt x paradoxus plants survived, while 100% of the H.
ionic strength). Percent survivorship is based on annuus plants survived in each of the Na2S04
the mean number oferect and green plants out of treatments except at the 0.51 ionic strength, the
five plants per replicate pot per treatment. highest Na2S04 concentration tested. Plant sur-
Shoot and root dry mass were measured at the vivorship for H. paradoxus in NaCl treatments
end oftheexperiment. For shoot dry mass, plants was 100% at the 0.09 and 0.17 ionic strengths,
from each pot were clipped at the soil surface and while 80% and 40% ofH. annuus plants survived
placed in a pre-weighed paper bag. For the ash- in these same ionic strengths, respectively.
free root dry mass, all ofthe soil and particulate Three three-way ANOVAs were used to
matter from each pot was carefully washed off analyze shoot, root, and total dry mass; however,
the roots. Roots were then wrapped in pre- only total dry mass data will be presented.
weighed aluminum foil. All plant material was Results were similar for mean shoot and root
dried in a forced air oven at 90 C to a constant dry mass (analysis not shown). The three-way
mass. After drying, roots were ashed in a ANOVA (Table 2) demonstrated a significant
programmable muffle furnace (Fisher Scientific overall species, salt, and ionic strength effect on
Isotemp®, Fisher Scientific Research, Pittsburgh, total dry mass. In addition, the three two-way
PA) at 625°C for 3 hours to obtain the ash-free interactions were significant as was the three-way
root dry mass (Bohm 1979). Total dry mass was interaction. To demonstrate more clearly the
also calculated by combining the shoot dry mass experimental results, two ofthe two-way interac-
and ash-free root dry mass per pot. tions will be presented first. Overall, H. para-
All dry mass data was analyzed using SAS doxus produced more dry mass than H. annuus in
statistical software (SAS Institute 1999) with each both salts (Fig. la, species X salt interaction).
pot as the unit ofreplication and P < 0.05 as the For both species, more dry mass was produced in
criterion for significance. Any plant mortalities the Na2S04 treatment than in the NaCl treat-
because of a treatment effect were taken into ment. In addition, ionic strength was significant
account by including a dry mass of zero. To with more dry mass in the lower treatments;
MADRONO
148 [Vol. 58
Salt IonicStrength
bFiyg.spe1c.iesTw{Hoe-lwiaanythiunstepraarcatidoonxuplsotasndofHteoltiaalndtrhyusmaansnsuu(bsa)rsa)ndas(tbh)eironeiscposntsreenvgatrhia(b0l.e00f-o0r.5(a1))sbaylts(pNecaiCels.aAndtNhrae2eS-0w4a)y
ANOVAdetermined therewere significantdifferences (P < 0.0001) between salt treatmentsandionicstrengthsfor
eachspecies. Differentlettersindicatesignificantdifferencesbetweenmeans(Duncan'sMultipleRangeTest). Lines
above the bars represent + one SD (standard deviation).
however, dry mass ofH. annuus was significantly strengths of NaCl where dry mass of H.
lower at an ionic strength of0.09 (Fig. lb, species paradoxus was 15-fold greater than H. annuus.
X ionic strength interaction). The salt X ionic
strength interaction has not been presented Discussion
because the results can be seen within the three
way interaction figure. The significant three-way Salt tolerance is the ability ofa species to grow
interaction indicated that dry mass was depen- and adjust to the presence ofa specific ion (ionic
dent on species, salt type, and ionic strength effect) or to adapt to the general effects of low
(Table 2, Fig. 2a, b). Helianthus paradoxus dry waterpotentials (osmotic effect) (Ungar 1991). In
mass was higher in Na2S04 compared to NaCl this study, a potential ionic effect and an osmotic
(Fig. 2a), with the greatest dry mass at the mid effect were investigated using NaCl and Na2S04
ionic strengths (Fig. 2a). On the other hand, H. salts at increasing ionic strengths. Both salts are
annuus dry mass was lower than H. paradoxus, found in H. paradoxus habitats at various
but H. annuus did produce more dry mass in concentrations (Boghici 1997; Van Auken and
Na2S04 compared to NaCl (Fig. 2b). In addi- Bush 1998; Lexer et al. 2003). To differentiate
tion, as the ionic strength increased dry mass of between the effects of the two salts and the CI"
H. annuus decreased. and SO4-" anions, equalionic strengthswereused
In comparison to the Na2S04 treatments, dry in the separate salt treatments (Barrow 1966).
mass ofboth species was significantly reduced in Due to greater salt tolerance of H. annuus in
NaCl at elevated ionic strengths (Duncan's NaCl and mixed salt environments compared to
Multiple Range Test, P < 0.0001, Fig. 2a, b). H. petiolaris (both purported parental species)
In the no-salt treatment, growth ofH. annuuswas (Ashraf and Tufail 1995; Welch and Rieseberg
elevated compared to H. paradoxus (not signifi- 2002; Bush and Van Auken 2004; Karrenberg
cantly). However, for all levels of salt addition, et al. 2006; DiCaterinaet al. 2007), H. annuuswas
total dry mass of H. paradoxus was greater than used as a comparative species for salt effects on
H. annuus, yet the differences were salt depen- growth ofH. paradoxus.
dent. For both species, mean total dry mass was As in previous studies, this investigation
elevated in Na2S04 at an ionic strength of 0.09 demonstrated that H. paradoxus was more salt
compared to NaCl. Dry mass of H. paradoxus tolerant than one of its parental species, H.
was 32% greater than dry mass of H. annuus in annuus, and even produced slightly more dry
this treatment. In the 0.17 to 0.51 ionic strengths mass in low saline soils compared to H. annuus
ofNa2S04, mean total dry mass ofH. paradoxus (Figs, lb, 2a, and 2b). Helianthus paradoxus
was 2- to 12-fold greater than H. annuus. Both produced 70% more dry mass than H. annuus
species produced less dry mass in NaCl treat- over all treatments (data not shown) and
ments; however, H. annuus dry mass was reduced consistently produced more dry mass in elevated
most by NaCl. Total dry mass of H. paradoxus salinity soils (Fig. 2a, b), especially in the sulfate
was 7-fold greater than H. annuus in the 0.09 treatments. Results of this greenhouse study are
NaCl treatment. This difference between species consistent with observations that H. paradoxus
in NaCl increased at the 0.17 and 0.34 ionic has greater fitness in sahne conditions than H.
2011] MENDEZ AND VAN AUKEN: SALT TOLERANCE OF TWO HELIANTHUS SPECIES 149
more tolerant than H. annuus to low to moderate
NaCl concentrations (Fig. 2). Greater dry mass
production and survivorship of H. paradoxus
plants compared to H. annuus in NaCl treatments
was also observed by Welch and Rieseberg (2002)
in corresponding NaCl treatments (100 and
200 mmol L"' [~6 and 12 g kg"'] NaCl). Plant
survivorship of H. annuus indicated that low
Na2S04 levels seem to be less inhibitive than
NaCl but significant dry mass reduction was still
observed above 0.09 ionic strength treatments.
Dry mass of H. paradoxus, on the other hand,
was enhanced by low to moderate levels of
0 0.09 0.17 0.34 0.51 Na2S04 with 38 to 72% greaterdry mass, relative
to the no-salt treatment. This corresponds to field
IonicStrength observations where H. paradoxus was most
abundant in soil salinities (mainly Na, K, Ca,
mam Na2S04 NaCI and Mg chlorides with less SO4) ranging from 5
i 1 to 12 g kg"' in the Diamond-Y Spring Preserve
(Boghici 1997; Van Auken and Bush 1998; Bush
2006b; Grunstra and Van Auken 2007a, b).
Although previous studies did not differentiate
between the effects of NaCl and Na2S04 (Welch
and Rieseberg 2002; Bush and Van Auken 2004;
Karrenberg et al. 2006; Van Auken and Bush
2006), those studies support the salt tolerance of
H. paradoxus to low concentrations of NaCl.
Results consistently demonstrated that biomass
of H. annuus was statistically reduced by NaCl
alone (Welch and Rieseberg 2002) or by low
levels of mixed salts (Na^, CI and SO4-
,
included; Bush and Van Auken 2004; Karrenberg
et al. 2006), while H. paradoxus demonstrated
lower productivity in NaCl alone and greater
growth and productivity in the presence ofSO4-
Ionicstrength
as observed in the present study. Greater salt
Fig. 2. Three-way interaction plots oftotal dry mass tolerance ofH. paradoxus to NaCl, as compared
(bars) as the response variable for (a) Heliantlius to H. annuus, has been attributed to significantly
paradoxus and (b) Heliantlius annuus. Salts were greater fitness along with Na^ accumulation, leaf
Nstar2eSng0t4hs(obflac0k.00b-a0r.)51.anAd NtharCele-w(agyrayANbaOr)VAatdeitoenri-c succulence, and water use efficiency (Welch and
mined there were significant differences (P < 0.0001) Rieseberg 2002). Because the salts were at equal
between salt treatments and ionic strengths for each ionic strengths and Na^ seems to serve as an
species. Different letters indicate significant differences osmoticum for H. paradoxus (Welch and Riese-
between means (Duncan's Multiple Range Test) within berg 2002), it can be assumed that CI is causing
a species. Lines above the bars represent + one SD reduced productivity in comparison to SO4-
.
(standard deviation). Molar concentrations of Cl~ in the soil water of
the Diamond-Y Spring Preserve are approxi-
mately 1.5 times that of molar concentrations of
annuus (Welch and Rieseberg 2002; Bush and SO4- therefore, CI- has the potential of inhib-
Van Auken 2004; Karrenberg et al. 2006), and iting g;rowth of H. paradoxus in its salt marsh
that H. annuus is not expected to be found in habitat (Boghici 1997). However, these data in
areas with elevated soil salinity where H. para- conjunction with previous salt studies (Welch and
doxus is able to grow and outcompete H. annuus Rieseberg 2002; Bush and Van Auken 2004;
and probably other non-halophytic species (Ab- Karrenberg et al. 2006) indicate that the presence
bot 2003; Van Auken and Bush 2006). of soil sulfate may have played an important
Both Helianthus spp. exhibited a specific ionic role in the selection for and adaptation of
growth inhibition at elevated levels of CI H. paradoxus to the Na-Cl -SO4- rich environ-
,
compared to S04^ and differences in salt ments. Further, poor tolerance to chloride and
,
tolerance between species were evident. For both sulfate by H. annuus has limited its establishment
species, NaCl caused plant mortahty at ionic and therefore, fitness in the H. paradoxus salt
strengths of0.34 and 0.51, yet H. paradoxus was marsh habitat.
MADRONO
150 [Vol. 58
It should be noted that in order to maintain (Harborne 1975; Tomas-Barberan et al. 1987;
equal osmotic potentials between treatments, Rajakaruna et al. 2003). A possible role of
molar concentrations ofNa^ in NaCl treatments sulphur in the salt tolerance of halophytes also
were 3.0 times that of Na2S04 treatments. includes the production ofmethylated sulfonium
Nevertheless, the molar equivalents of Na+ at compounds that accumulate in the cytosol as
0.09 and 0.17 ionic strengthswere between that of osmotically compatible organic solutes for com-
the 0.34 and 0.51 ionic strengths of Na2S04 partmentalization of Na^ and CI" in vacuoles.
where dry mass production ofH. paradoxus was These organic solutes also serve to detoxify
not inhibited. Since an inert osmotic medium sulfides in salt marsh plants (Flowers and Colmer
such as polyethylene glycol was not examined, an 2008). Flavonoid sulfates or methylated sulfoni-
osmotic effect in combination with an ionic effect umcompounds have not beenmeasured intissues
cannot be excluded (Katembe et al. 1998; Munns of H. paradoxus; however, Na2S04 tolerance of
and Tester 2008). this species together with Na^ and S04-~ accu-
In the limited studies comparing phytotoxicity mulation suggests a possible detoxification mech-
of both salts, greater toxicity to NaCl compared anism not yet identified.
to Na2S04 has been demonstrated for other salt Ecological isolation ofH. paradoxuswithin the
tolerant glycophytes and halophytes (Manchanda inland salt marshes of west Texas and New
et al. 1982; Curtin et al. 1993; Franklin and Mexico may in part depend on the elevated levels
Zwiazek 2004; Pagter et al. 2009). Chloride is of soil salinity found in soils of these habitats
more toxic to plants than sulfate possibly due to (Boghici 1997; McDonald 1999; Van Auken and
synergistic phytotoxicity effects with Na^, differ- Bush 1998, 2006; Abbott 2003). Halophytes are
ential inhibition of enzyme activity, reduction in limited to saline environments because of an
plant productivity, and imbalance of nutritional advantageous adaptation to excess salts and a
status (Greenway and Munns 1980; Manchanda reduction of competitive ability in non-saline
et al. 1982; Curtin et al. 1993; Wang et al. 1997; environments (Ungar 1991). Distribution of H.
Veira Dos Santos and Caldeira 1999; Franklin paradoxus plants appears to be dependent on low
and Zwiazek 2004). Ion toxicity is dependent on to moderate soil salinity levels at the Diamond-Y
whether the plant possesses adaptations to SpringPreservewhereNa^, CI" and S04^" arethe
tolerate the osmotic stress and to exclude and/ prevalent salts from groundwater discharge,
or compartmentalize the ion. Although not yet while Ca-^, Mg-^, and HCO3" are secondary ions
documented, it is possible that H. paradoxus (Boghici 1997; Van Auken and Bush 1998; Bush
accumulated CI alongwith Na^andmayeven be 2006b; Grunstra andVanAuken2007a, b). In the
more sensitive to C\~ compared to SO4- due to present study, H. paradoxus outperformed H.
poorcompartmentalization into vacuoles (Green- annuus in both soil salt treatments, partially
wayand Munns 1980; Flowerset al. 1986; Munns explaining the inability of H. annuus to survive
1993; Rajakaruna et al. 2003). Chloride may be the salt marsh habitat of H. paradoxus (Lexer
considered more toxic sometimes because ofpoor et al. 2003; Bush and Van Auken 2004). The
salt tolerance response and thus, high accumula- presence of salts excluded H. annuus from
tion ofCI over Na^, or in this case SO4- Toxic colonizing the salt marsh (Abbott 2003; Lexer
cytoplasmic Cr concentrations havenot ye.t been et al. 2003), while the salt tolerance of H.
determined but are assumed to be equal to or paradoxus to both NaCl and Na2S04 has allowed
slightly lower than Na^ (Flowers et al. 1986; this species to establish in the Diamond-Y Spring
Greenway and Munns 1980; Munns and Tester Preserve and other salt marsh environments in
2008). west Texas and New Mexico. Further, tolerance
Sulfate may be required for salt tolerance in H. to high concentrations of Na2S04, as demon-
paradoxus. Tissue ion concentrations were not strated by significantly greater productivity rela-
examined in this study, but previous work tive to non-saline conditions, suggests that H.
suggested that (as in other halophytes) S04^", paradoxus may experience a physiological stress
along with Na^, may be an important vacuolar response without elevated Na2S04, which is
osmoticum in plant tissue (Greenway and Munns necessary for optimum growth and perhaps
1980; Karrenberg et al. 2006; Johnston 2006). necessary for salt tolerance (Munns and Tester
Leaf sodium and sulfur concentrations were 2008). The establishment of H. paradoxus in the
shown to be inversely related to calcium, Diamond-Y Spring Preserve has been promoted j
i
magnesium, and potassium concentrations but by the selection for transgressive phenotypes
positively related to biomass and succulencein H. promoting salt tolerance (sodium exclusion,
paradoxus (Karrenberg et al. 2006). Interestingly, calcium uptake, and leaf succulence), as demon-
several studies have found a correlation between strated by H. paradoxus, along with the presence |
plants inhabiting waterlogged sulfate rich soils ofspecific ions (Na+, Ca^+, and S04^") in the salt
and the presence of vacuole stored flavonoid marsh habitat (Abbott 2003; Lexer et al. 2003;
sulfates which may serve to detoxify excess Karrenberg et al. 2006). In addition, both
sulfates alone or in combination with sodium parental species are poor competitors in field-Uke
2011] MENDEZ AND VAN AUKEN: SALT TOLERANCE OF TWO HELIANTHUS SPECIES 151
elevated soil salinity conditions, while H. para- (Asteraceae) in an inland salt marsh ofwest Texas.
dnoonxsuasliisnea pcooonrdictoimonpseti(tBourshagaainnsdt HV.anannAuuukseinn JourAnNalDoOf.AWri.dVEanvnirAounkmeennt.s16949:72.2-T3h6e. effects of
neighbors and grazing on the growth ofHelianthus
2004).
paradoxus. Southwestern Naturalist 42:416-422.
The potential for hybridization is still present AND 2004. Relative competitive ability
and environmental conditions isolating hybrid of Helianthus p.aradoxus and its progenitors, H.
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to havebeen an important factorin theiradaptive soil salinities. International Journal of Plant
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reported parent species to H. paradoxus is also and ionic relations. Soil Science Society ofAmerica
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However, environmental factors such as the soil Dicaterina, R., M. M. Guiliani, T. Rotunno, A.
conditions required for the isolation and survival De Caro, and Z. Flagella. 2007. Influence of
ofsome ofthe H. annuus X H. petiolaris hybrids salt stress on seed yield and oil quality of two
was and continues to be the saUne soils sur- sunflower hybrids. Annals of Applied Biology
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TreoxuansdinagndtheNieswolatMeedxispcroing(sAbibnotthtis 2a0r0e3a;ofLewxeestr DonoVvelaenn,osLi., AL.., DH.. RR.ieRsoebseerngt,haaln,dM.F.SLaundcwhiegz.-
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with establishment in the Na^-Cl -SO4" domi- habitats? Journal of Evolutionary Biology
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Acknowledgments Atriplex prostrata (Chenopodiaceae). Journal of
Plant Nutrition 21:2193-2205.
Some support for this project was provided by the Flowers, T. J., M. A. Hajibagheri, and N. J. W.
Nature Conservancy ofTexas, the University ofTexas Clipson. 1986. Halophytes. The Quarterly Review
at San Antonio, the Texas Department of Parks and ofBiology 61:313-337.
Wildlife, the U.S. Fish and Wildlife Service, and Dr. and T. D. Colmer. 2008. Salinity tolerance in
Loyce and Mr. William Collenback. We especially halophytes. New Phytologist 179:945-963.
thank Mr. John Karges ofthe Nature Conservancy of Franklin, J. A. and J. J. Zwiazek. 2004. Ion uptake
Texas for help and advice during various stages ofthis in Pinus banksiana treated with sodium chloride
project. and sodium sulphate. Physiologia Plantarum
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