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Lygodium microphyllum (Old World Climbing Fern) is one of the most problematic weeds in south Florida, invading numerous habitats from mangroves to pine flatwoods natural ecosystems. Much of the research efforts on L. microphyllum has been focused on reproductive potential, spore release, growth under different environmental conditions, belowground rhizome dormancy and survival strategies that describes its invasiveness. However, the role of an important mutualistic association with arbuscular mycorrhizal fungi (AMF) in the competitive ability and successful invasion of L. microphyllum by enhancing nutrient uptake has not been previously considered. Analysis of field root and soil samples from the ferns introduced and native range as well as a 7-week growth chamber experiment were done to determine the level of mycorrhizal colonization in the roots of L. microphyllum and the dependency on mycorrhizal fungi for growth and phosphorus (P) uptake. The field root samples showed that L. microphyllum was heavily colonized by AMF in relatively drier conditions, which are commonly found on some Florida sites compared to more common wetter sites where the fern is found in its native Australia. The results from the growth chamber experiment showed that the mycorrhizal treatment plants had significantly higher relative growth rate and biomass compared to the non-mycorrhizal plants. Similarly, L. microphyllum was highly dependent on the mycorrhizal fungi for growth and P uptake. Our results suggest that AMF play a significant role in vegetative reproduction and likely enhance the invasiveness of L. microphyllum in south Florida natural areas.
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1 23
Symbiosis
ISSN 0334-5114
Symbiosis
DOI 10.1007/s13199-014-0272-4
Mycorrhizal symbiosis and Lygodium
microphyllum Invasion in South Florida—
a biogeographic comparison
Pushpa G.Soti, Krish Jayachandran,
Matthew Purcell, John C.Volin & Kaoru
Kitajima
1 23
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Mycorrhizal symbiosis and Lygodium microphyllum Invasion
in South Floridaa biogeographic comparison
Pushpa G. Soti &Krish Jayachandran &Matthew Purcell &
John C. Volin &Kaoru Kitajima
Received: 8 September 2013 /Accepted: 13 February 2014
#Springer Science+Business Media Dordrecht 2014
Abstract Lygodium microphyllum (Old World Climbing
Fern) is one of the most problematic weeds in south Florida,
invading numerous habitats from mangroves to pine
flatwoods natural ecosystems. Much of the research efforts
on L. microphyllum has been focused on reproductive poten-
tial, spore release, growth under different environmental con-
ditions, belowground rhizome dormancy and survival strate-
gies that describes its invasiveness. However, the role of an
important mutualistic association with arbuscular mycorrhizal
fungi (AMF) in the competitive ability and successful inva-
sion of L. microphyllum by enhancing nutrient uptake has not
been previously considered. Analysis of field root and soil
samples from the ferns introduced and native range as well as
a 7-week growth chamber experiment were done to determine
the level of mycorrhizal colonization in the roots of
L. microphyllum and the dependency on mycorrhizal fungi
for growth and phosphorus (P) uptake. The field root samples
showed that L. microphyllum was heavily colonized by AMF
in relatively drier conditions, which are commonly found on
some Florida sites compared to more common wetter sites
where the fern isfound in its native Australia. The results from
the growth chamber experiment showed that the mycorrhizal
treatment plants had significantly higher relative growth rate
and biomass compared to the non-mycorrhizal plants.
Similarly, L. microphyllum was highly dependent on the my-
corrhizal fungi for growth and P uptake. Our results suggest
that AMF play a significant role in vegetative reproduction
and likely enhance the invasiveness of L. microphyllum in
south Florida natural areas.
Keywords Arbuscular mycorrhizal fungi (AMF) .Inorganic
phosphorus .Relative growth rate (RGR) .Mycorrhizal
dependency .Exotic pest plant
1 Introduction
Lygodium microphyllum (Old World Climbing Fern), native
to the wet tropics of Old World and subtropics of Africa, Asia,
Australia and Oceania (Pemberton and Ferriter 1998), is one
of the most problematic weeds in south Florida. It invades
many freshwater and moist habitats and is common in cypress
swamp, pine flatlands, wet prairies, sawgrass marshes, man-
grove communities, and the Everglades tree islands
(Pemberton and Ferriter 1998). L. microphyllum, with its
ability to form dense mats, spreads very rapidly and dominates
both understory and overstory native wetland habitats. It has
the ability to grow in varying hydrological (Gandiaga et al.
2009), nutrient (Volin et al. 2010) and light gradients (Volin
et al. 2004). It is estimated to occupy 183,080 acres in the
entire South/Central Florida region (Ferriter and Pernas 2006)
and a model developed by Volin et al. (2004) shows that, in the
absence of aggressive control measures, L. microphyllums
infestations could exceed the current combined coverage of
the top five most invasive species in Florida by 2014.
Managing L. microphyllum has been a significant challenge
for land resource managers and researchers due to its extensive
rapid invasion in natural areas of south Florida. Much of the
P. G . S o t i :K. Jayachandran (*)
Department of Earth and Environment, Florida International
University, 11200 SW 8th Street, Miami, FL 33199, USA
e-mail: jayachan@fiu.edu
M. Purcell
USDA ARS Australian Biological Control Laboratory, Brisbane,
Queensland, Australia
J. C. Volin
Department of Natural Resources and the Environment, University
of Connecticut, Storrs, CT, USA
K. Kitajima
Department of Biology, University of Florida, Gainesville, FL, USA
Symbiosis
DOI 10.1007/s13199-014-0272-4
Author's personal copy
research work previously performed on L. microphyllum focus-
es on reproductive potential, spore release, belowground rhi-
zome dormancy and survival strategies investigating its inva-
siveness (Lott et al. 2003). Volin et al. (2010) have suggested
that the belowground microbial community can influence the
establishment of L. microphyllum in south Florida and contrib-
ute to its invasiveness. Thus the role of belowground biota in
invasions by exotic plants cannot be overlooked, in particular,
the role of arbuscular mycorrhizal fungi (AMF) deserves
consideration.
Most vascular plants form symbiotic associations with
AMF, and many plants are highly dependent on this associa-
tion for their growth and survival (Smith and Read 2008).
AMF are obligate symbionts of plants; approximately 95 % of
all vascular plants can form AMF associations (Fitter and
Moyersoen 1996). Read (1991) stated that the mycorrhizal
association is the most ubiquitous and abundant form of
terrestrial symbiosis, and AMF are considered the most com-
mon type of mycorrhizae which dominates grasslands, crop-
lands, tropical forests, and desert communities. They occur
naturally in most soils and their important ecosystem function
is to assist in the acquisition of soil mineral nutrients (Dighton
2003). Arbuscular mycorrhizal fungi are known to benefit
plants by improving plant phosphorus (P) uptake (Fitter
1990; Gao et al. 2007) and also potentially enhance defense
against soil born pathogens (Azcón-Aguilar and Barea 1997).
South Florida soils are poor in P because of the binding of P
with Ca in alkaline soils and to certain extent Al or Fe in acidic
soils. AMF can facilitate P uptake by increasing 1) diffusion
rate into plant roots; 2) P concentration at the root
surface; and 3) the rate of P dissociation from the
surface of soil particles (Bolan 1991). Elements other
than P, such as N, Cu and Zn, also experience enhanced
uptake through AMF (Gildon and Tinker 1983;Gao
et al. 2007). It has been estimated that external hyphae
of AMF can contribute up to 80 % of the P, 10 % of the N,
10 % of the K, 25 % of the Zn, and 60 % of the Cu absorbed
by plants (Li et al. 1991; Marschner and Dell 1994; DeLuca
et al. 2002). Mycorrhizal fungi help overcome the nutrient
deficiency by extending their external hyphae to areas
of soil beyond the depletion zone and increasing the
absorptive surface of the root. However, Smith and
Read (2008) have reported that host plant species do
not equally benefit from AMF and some plants acquire
more nutrients from AMF than others. Furthermore if the
symbiotic relationship is non-host specific competing plant
species could be interconnected by AMF hyphal networks
(Grime et al. 1987; Newman 1988)thuscreatinganimbalance
in the nutrient distribution. This imbalance could interfere the
competitive interaction between native and exotic species by
promoting growth of the invasive species and inhibiting
growth of the native plant species (Fumanal et al. 2006;
Callaway et al. 2008).
Populations and symbiotic efficiency of AMF are reported
to be highly influenced by the various environmental factors
including climatic conditions, soil physical and chemical con-
ditions such as nutrient status, pH, salinity, organic matter etc.
While the climatic conditions of southeastern Queensland,
Australia, the native range of L. microphyllum, is similar to
the invaded areas of south Florida (Volin et al. 2010), the soil
physic-chemical properties are significantly different in these
two locations (Soti et al. unpublished data). Australian soils
are reported to be old highly weathered, deeply leached and
highly acidic (ABS 2012), in contrast, Florida soils are rela-
tively young,sandy and slightly acidic. There are considerable
numbers of studies on the soil pH influence on the root
mycorrhizal colonization, and it is reported that mycorrhizal
fungi are sensitive to highly acidic soils (Clark 1997;Postma
et al. 2007). Thus, in this study, we characterized the root
colonization by AMF in L. microphyllum under field condi-
tions in both its native Australia and its introduced environ-
ment in Florida. We also further explored the influence of
AMF on the growth and biomass allocation strategy of
L. microphyllum in growth chambers. The objectives of this
study were to: 1) evaluate the mycorrhizal status of natural
populations of L. microphyllum in both Australia and Florida;
2) determine the effect of AMF on the reproductive and
biomass allocation strategy of L. microphyllum; and, 3) eval-
uate the dependency of L. microphyllum on AMF for growth
and phosphorus uptake. We hypothesized that the south
Florida population of L. microphyllum would have a higher
degree of mycorrhizal colonization compared to the
Australian population because of the difference in soil char-
acteristics. We also hypothesized that L. microphyllum is
highly dependent on AMF for increased biomass accumula-
tion and P uptake.
2Methods
2.1 Experiment 1: degree of mycorrhizal colonization
in L. microphyllum
Roots and rhizosphere soil samples (for nutrient analysis and
spore extraction) of wild L. microphyllum were collected from
different locations in south Florida and Australia to assess the
mycorrhizal fungal root colonization and presence of AMF
spores. The locations (Fig. 1), sampling date and the soil
characteristics in each of the locations are given in Table 1.In
each location, six random sites, few meters apart, were select-
ed. Within each site, 100 fine root samples from 56 fully
grown adult plants were collected and mixed to make a com-
posite sample. Root tip samples were placed in 70 % ethanol
immediately until further processing following the method
described in McGonigle et al. (1990). These roots were cut
into 1.5 cm fragments, cleared in 15 % KOH at 70 °C for 4 h,
P.G. Soti et al.
Author's personal copy
rinsed twice with water, bleached with ammoniated H
2
O
2
,and
acidified with 1 N HCl. Once the roots were cleared, staining
was done using 0.05 % Trypan blue in acidic glycerol at 80 °C
for 20 min. At least 50 root fragments were selected randomly
for each site and the percentage of colonization were examined
with a dissecting microscope at 3060 × magnification. The
portions that showed the presence of mycorrhizal fungi were
mounted on slides in lactic acid and further examined at 100
400 X magnification to analyze the presence of mycorrhizal
structures (hyphae, vesicles, and arbuscules).
Fig. 1 Sampling sites in Florida (top)andAustralia(bottom)
A biogeographic comparison
Author's personal copy
The wet sieving and decanting technique was used to
enumerate the mycorrhizal spores in the soil (Gerdemann
and Nicolson 1963). The soil samples were mixed to homo-
geneity. Fifty grams of the soil sample were then mixed with
water and passed through a series of sieves allowing heavy
soil particles to settle for a few seconds. The sievate retained
on the sieves was washed and centrifuged with water to
remove floating organic debris and the supernatant was
discarded. The pellet in the bottom was re-suspended in a
50 % sucrose solution, and centrifuged for 1 min at 2,000
RPM to separate the spores from denser soil components.
Immediately after centrifugation, spores in the sucrose super-
natant were rinsed in a fine sieve to remove the sucrose. The
spores were then washed into a filter paper for vacuum filtra-
tion. The sporeson the filter paper were counted under a stereo
microscope.
2.1.1 Analysis of soil properties
At each sampling site, six 1 m × 1 m plots were selected
randomly and soil sample was collected from the 1015 cm
deep zone at all four corners and the center of each plot with a
soil corer (ø 18 mm) and mixed homogeneously into one bulk
sample for each plot. The samples were collected to a depth of
1015 cm. The soil samples from south Florida were
transported to the laboratory in a cooler; the central Florida
and Australian samples were stored at 4 °C and were shipped
overnight. The soil samples for the chemical and physical
properties were air dried and passed through a 2 mm sieve.
They were then ground to fine powder with a mortar and
pestle, and stored at room temperature in air-tight containers
for further analysis of nutrients. The soil pH was measured
with a pH meter, (soil solution ratio 1:1 in water), texture was
measured by the hydrometer method, percentage of carbon
and nitrogen was measured with a TruSpec Carbon/Nitrogen
Analyzer (Leco Corporation, USA), total organic matter was
measured based on the standard loss on ignition method
(500 °C, 5 h; Storer 1984), for the measurement of total P,
soil samples (0.25 g, finely ground) were ashed (500 °C),
digested in 2 ml HCL (6N) and 10 ml HNO
3
,andthen
analyzed with an UV spectrophotometer (Shimadzu
Scientific Instruments) (total P and some other variables were
not measured for samples collected in 2006).
2.2 Experiment 2: mycorrhizal dependency
of L. microphyllum
2.2.1 Plant material
Experimental plants were grown from spores collected from
an infestation in Jonathan Dickinson State Park, Florida, fol-
lowing the method used by Lott et al. (2003). The spores of
L. microphyllum were disinfected with 1 % bleach and trans-
ferred to Petri dishes that contained Parker-Thomson Medium.
The plates were placed in an incubator set at 2527 °C for
10 weeks and were watered with sterile DI water every week.
After 10 weeks, individual gametophytes were transferred to
fresh Petri dishes. When the sporelingsroots and leaves
developed, 50 plants were transplanted to small pots previ-
ously filled with sterile sand. These 50 plants were placed in a
Tabl e 1 Site information and the degree of mycorrhizal colonization
Site Coordinates Soil texture pH SOM % No. of spores/
10 g dry soil
Sampling date Deg. of colonization (%)
[minmax]
Tree Tops Park, FL, US 26° 40.04N, 80° 16
45.88W
Sandy loam 5.56 39.7±1.6 29± 7 Dec, 2010 79±3.0 [6585]
Jonathan Dickinson, FL, US 27°037.33N, 80°7
20.28W
Sand 6.02 4.30±0.9 19± 5 Dec, 2010 74±2.2 [6788]
Big Cypress Seminole Indian
Reservation, FL, US
Approximately,
26°17N, 80°54W
Sand 4.99 * * Late Oct, 2006 31 ± 7.8 [16.049.5]
Everglades National Park FL 25° 4537.0548N,
80° 4025.3554W
Sand * * * July, 2013 61± 2.8 [4967]
Polk County, FL 28° 234.03N, 81°
4441.30W
Clay 5.77 8.65 23± 5 June, 2012 68± 2.5 [5977]
Daintree Ferry, Queensland,
AU
16°1525.57S,
145°243.94E
Silt loam 4.43 8.07±1.2 12± 6 June, 2011 27± 1.4 [2433]
Logan Reserve, Queensland,
AU
27°404.16S, 153°16
0.44E
Sandy clay
loam
4.55 35.5±2.9 15± 3 June, 2011 28± 1.3 [2532]
Nudgee, Queensland, AU 27°2231.12S, 153°
5'39.42E
Loam 4.01 11.45±1.9 10 ±5 June, 2011 27 ±0.6 [2529]
SE Brisbane, Queensland, AU 27°40.36S,
153°16.60E
Sandy loam 5.55 6.83 * February, 2006 24.0 ±2.7 (3) [19.528.9]
Near Amity Point, Stradbroke
Island, Queensland, AU.
Approximately,
27.4°S, 153.4°E
Sand * * * February, 2006 30.2±6.5 (5) [7.444.7]
Mean values ± standard error, Soil organic matter (SOM), number of samples (N), * values not determined
P.G. Soti et al.
Author's personal copy
growth chamber for approximately 4 weeks. The plants were
kept very moist, and were watered with half strength
Hoaglands nutrient solution as needed. Plants were then
transferred to 2.5 L pots filled with the top soil collected from
aL. microphyllum infested site located in the Tree Tops
County Park, Davie, Florida. The potting soil was sterilized
in an autoclave to kill mycorrhizal fungal spores to ensure the
experimental plants remained free of mycorrhizal fungi.
2.2.2 Growth chamber experiment
A 7-week growth chamber (Percival Scientific, with irradi-
ance= 500 μmol m
2
s
1
, photoperiod = 12 h and temperature
27 °C) experiment was done to determine the mycorrhizal
dependency of L. microphyllum. The experiment consisted of
two treatments: mycorrhizal treatment and non-mycorrhizal
treatment with eight replicate pots per treatment. In the my-
corrhizal treatment plants received mycorrhizal inoculum; the
top soil collected from the field directly under
L. microphyllum while a systemic fungicide was added every
3 weeks in the non-mycorrhizal treatment plants to prevent
any kind of mycorrhizal contamination during the experiment.
The non-mycorrhizal plants received 50 ml of microbial wash
to provide similar microflora except the mycorrhizal fungi.
The microbial wash was prepared by filtering the field soil
slurry through a 25 μm filter paper, which removed the
mycorrhizal fungi spores in the soil but allowed the other soil
microorganisms to pass through (Johnson 1993). Three hun-
dred mg of the systemic fungicide Benomyl was applied in
100 ml of water per pot (50 mg/kg growth medium); this
fungicide is reported to effectively reduce the mycorrhizal
colonization in roots without significant impact on the plants
(Fitter and Nichols 1988; Hetrick et al. 1992). Plants were
watered to saturation once per week and received 250 ml of
half strength Hoaglands solution weekly, modified by the
addition of phosphorus as inositol hexaphosphate (Marler
et al. 1999). This form of phosphorus is not directly available
to plants for uptake, and requires alteration in the soil by
mycorrhizal fungi, soil microbes, or root exudates (DeLucia
et al. 1997).
2.2.3 Measurements
Two harvests were conducted during this study: at time 0 (the
transplanting day), and after 50 days. The allometric relation-
ship between stem length and total mass (R
2
=0.87) from the
time 0 harvest was developed to estimate the initial plant mass
of the experimental plants and to calculate the relative growth
rate (RGR) (see Gandiaga et al. 2009). The RGR (mg g
1
d
1
)
was calculated for individual plants used for the experiment,
where RGR = [ln (final dry mass)-ln (initial dry mass)]/days
(Evans 1972). After each harvest, roots, stem, and leaves
(pinnae) were separated from each plant and the leaf area
was measured with the leaf area meter to calculate the specific
leaf area (SLA). The separated plant parts were oven-dried (at
7C)toconstantmassandweighedtodeterminetheleaf
mass ratio (LMR), stem mass ratio (SMR), rhizome mass ratio
(RhiMR), and root mass ratio (RMR); differences in the mean
growth parameters between the treatments and relative growth
rate (RGR). The roots were washed with water. Twenty 1-cm
root pieces were collected from each plant before drying to
quantify the AMF colonization in the roots. Root and shoot
dry mass were measured after oven-drying for 1 week at
65 °C. Leaf samples (0.25 g, finely ground) were ashed
(500 °C), digested in 2 ml HCL (6N) and 10 ml HNO
3
,and
then analyzed with an UV spectrophotometer (Shimadzu
Scientific Instruments, US) for total phosphorus (P) concen-
tration. The percentage of carbon and nitrogen in the leaves
was measured with a TruSpec Carbon/Nitrogen Analyzer
(Leco Corporation, US) and the C/N ratio was calculated.
Dependency of shoot P uptake and growth of plants on
AMF was calculated using the formulae from Plenchette
et al. (1983), where+M represents inoculated plants and M,
fungicide treated plants:
Dependency of P uptake ¼P content þMðÞPcontentMðÞ
PcontentþMðÞ 100
Dependency of growth ¼Total dry mass þMðÞTotal dry mass MðÞ
Total dry mass þMðÞ 100
2.2.4 Statistical analyses
Data for the soil and mycorrhizal colonization (experiment 1)
were analyzed with one-way analysis of variance (ANOVA)
to compare the means of the pH, total P, total N and soil
organic matter from different sites. Correlation analysis was
done to determine the influence of soil pH and organic matter
on the degree of mycorrhizal colonization.
For the green house experiment (experiment 2), after the
harvest at 50 days, regression analysis was done to examine
A biogeographic comparison
Author's personal copy
the influence of initial plant mass on RGR and its
morphological, allocational and physiological determi-
nants as it has been reported frequently (e.g.
Mcconnaughay and Coleman 1999; Volin et al. 2002;
Kruger and Volin 2006). Regression analysis indicated
that RGR was negatively correlated to initial plant mass
(p<0.001). Additionally, RhMR and SLA at final har-
vest were all significantly related (P<0.05) to final plant
mass. Therefore, each was normalized for variation in plant
mass using analysis of covariance. All of the variables
in mycorrhizal and non-mycorrhizal treatments were
then compared with two-treatment t- test for signifi-
cance at p0.05. Regression analysis was also used to
assess relationships between RGR and its principal deter-
minants. All the parameters were analyzed with SAS Version
9.2 software.
3Results
3.1 Degree of mycorrhizal colonization and influence of soil
factors
A wide variety of different fungal structures such as
extraradical hyphae, vesicles, and arbuscules were visi-
ble in root samples from all sites. The total percentage
of roots colonized by arbuscular mycorrhizal fungi in
the Florida plants in some cases were up to three times
that of the Australian plants (Table 1). In Florida, the
range was from 31 to 79 %, while in Australia the
range was much narrower, 2729 %. Mycorrhizal spores
were present in the rhizosphere soil samples from all
sites; spore abundance was highest in Tree Tops Park in
south Florida, while the lowest abundance of spores at
Nudgee in Australia.
Tree Tops Park, the south Florida site had slightly higher
total P in the soil but this difference was not significantly
different (Fig. 2a). However there was a significant difference
in the total C and N among the different sites (Fig. 2a, b). Tree
Tops Park in Florida and Logan in Australia had significantly
higher percentage of C and N compared to the other
sites. The south Florida soil samples were slightly acid-
ic, ranging from 5.49 at Tree Tops Park to 6.22 at
Jonathan Dickinson Park. However, the Australian soil
samples were highly acidic ranging from 3.97 at Nudgee to
4.7 at Logan. Soil organic matter was significantly higher in
the Tree Tops and Logan than at Jonathan Dickinson, Nudgee
and Daintree (Table 1).
Correlation analysis shows that the degree of colonization
to be significantly positively correlated with soil pH (r=0.86,
p<0.001); N% (r=0.45, p=0.026); and C % (r= 0.43, p=
0.0177) while there was no significant correlation with soil
organic matter (r=0.02, p=0.35).
3.2 Mycorrhizal dependency
As expected, in the non-mycorrhizal treatment, beno-
myl application significantly suppressed the mycorrhi-
zal colonization of L. microphyllum roots. After
50 days, root colonization rate was high in the mycor-
rhizal treatment (>75 %), but low (<5 %) in the non-
mycorrhizal treatment. Different fungal structures were ob-
served in host plant roots including hyphae, vesicles as well as
arbuscules.
0
0.2
0.4
0.6
0.8
1
1.2
Tree Tops Jonathan
DickinsonD
Polk County Logan Nudgee Daintree
Total P (mg/g)
Sites
a
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
1.8
Tree Tops Jonathan
DickinsonD
Polk County Logan Nudgee Daintree
Total Nitrogen (%)
Sites
b
c
0
5
10
15
20
25
30
Tree Tops Jonathan
DickinsonD
Polk County Logan Nudgee Daintree
Total Carbon (%)
Sites
Fig. 2 Means (± SE) of soil nutrients: atotal soil phosphorus (mg/g); b
total soil nitrogen %; ctotal soil carbon (%)
P.G. Soti et al.
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The mycorrhizal plants had greater total P uptake in shoots
compared to the non-mycorrhizal plants. The mycorrhizal
dependency index for growth was 67 %, and 64 % for P
uptake. Relative growth rate of mycorrhizal treated plants
was 29 % greater (p=0.01) than the RGR of the non-
mycorrhizal plants (Table 2). Correspondingly, the mean bio-
mass of the L. microphyllum plants inoculated with mycorrhi-
zal fungi was also significantly greater (by 66 %) (p=0.001)
than the non-mycorrhizal plants (Table 2).
There was no significant difference in SMR (p=0.15) or
LMR (p=0.99) between the two treatments (Table 2). On the
other hand, allocation to rhizomes (RhiMR) (p=0.001) was
significantly different between treatments, resulting in greater
rhizome allocation for mycorrhizal plants compared to un-
treated. In contrast, mycorrhizal plants tended to allocate less
to roots than non-mycorrhizal plants (p=0.08).
The mycorrhizal treatment increased the leaf area of the
plants nearly four-fold (p=0.0001) and SLA was significantly
greater (p=0.003) (24 %) in the presence of mycorrhizal fungi
compared to non-mycorrhizal plants. There was no significant
difference (p=0.83) in the average P concentration in the
leaves of the mycorrhizal and non-mycorrhizal plants.
However, the total P per plant (3,291 μg) of the mycorrhizal
plants was significantly higher (p=0.0001) than the non-
mycorrhizal plants.
4 Discussion and conclusion
While our study was limited to a very few sampling sites, our
results do suggest that L. micorphyllum has a strong symbiotic
relationship with mycorrhizal fungi, and the degree of mycor-
rhizal colonization is generally higher in the invaded regions
of south Florida than in the plants native range in Australia.
Detailed information on the mycorrhizal status of the
coexisting species is not available but the high degree of
mycorrhizal colonization may assist in absorption and com-
petition for nutrients in the ferns introduced environment,
especially on sandy sites with low water holding capacity.
This could inturn provide a competitive advantage over native
Florida plants. However, others have found that that many
invasive plants do not associate with mycorrhizal fungi (see
Pringle et al. 2009). Plants such as Alliaria petiolata,
Centaurea diffusa, etc. have been found to use alternative
mechanisms to disrupt existing symbiotic relationships by
secreting lethal biochemicals in the introduced range, resulting
in the reduced growth and competitiveness of native plants
(Callaway and Aschehoug 2000;Callawayetal.2008).
Our results suggest that the differences observed in the root
colonization by mycorrhizal fungi could be the result of the
difference in the soil physico-chemical properties (Turner
et al. 2000) such as soil texture, pH, and nutrients. Our results
show that soil pH is positively correlated with mycorrhizal
colonization, indicating that the low soil pH of the Australian
soil may influence the degree of mycorrhizal colonization and
the number of spores associated with L. microphyllum, other
research have shown species-specific responses of AMF to
soil pH (Porter et al. 1987; Gemma et al. 1989). It is widely
reported that abundance of mycorrhizal fungi declines in
response to N and P fertilization (see Treseder 2004). In
contrast, our results indicate a positive correlation between
mycorrhizal colonization and soil nitrogen. Similar results
have also been reported by (Persson and Ahlstrom 1991;
Heijne et al. 1992). We did not determine the mycorrhizal
fungal species in our study but there is substantial variation in
the environmental effects on different mycorrhizal fungal
species, this variation could explain in part the contradictory
results seen in our study. Likewise, there was a significantly
positive correlation between the root mycorrhizal status and
soil C%, this result supports the existing assumption that
mycorrhizal fungi have a significant contribution to soil car-
bon storage (Treseder and Allen 2000).
In addition, the four sites in Florida with high AMF colo-
nization appear to be drier compared to the four Australian
sites and the one Florida Big Cypress Seminole Indian
Reservation site. These latter sites are characterized by peri-
odic inundation that may or may not occur on an annual basis,
while the four drier Florida sites are not inundated for any
appreciable amount of time. Relationship between flooding
and AMF colonization seen in our study could explain in part
the lowered growth rate of L. microphyllum in flooded condi-
tions compared to the drought and field conditions seen by
Gandiaga et al. (2009). Additionally, Rickerl et al. (1994);
Stevens and Peterson (1996); and Miller and Sharitz (2000)
have found a strong relationship between mychorrizal coloni-
zation and site hydrology, and this potential relationship for
L. microphyllum needs to be explored further.
Tabl e 2 Effect of arbuscular mycorrhizal fungi inoculation on plant
growth parameters and on leaf content of biolimiting elements (P and N)
Variable Mycorrhizal Non mycorrhizal P value
Final biomass(g) 1.99±0.37 0.68±0.17 0.0001
RGR mg g
1
day
1
75.13±0.01 53.88±0.01 0.000
SMR 0.17±0.03 0.20±0.05 0.15
RMR 0.18±0.05 0.24±0.08 0.08
RhiMR 0.24±0.04 0.14±0.04 0.001
LMR 0.42±0.02 0.42±0.02 0.99
SLA 505± 64 383.6± 85 0.003
Leaf area (cm
2
) 414± 112 109.7±40.7 0.0001
Total P per plant (μg) 3,291 ±615 1,129±279 0.0001
C/N ratio 1.7± 0.1 1.6 ±0.1 0.21
mean values (± SD) of the study variables: relative growth rate (RGR),
stem mass ratio (SMR), root mass ratio (RMR), rhizome mass ratio
(RhiMR), leaf mass ratio (LMR), specific leaf area (SLA) after growing
7 weeks in a growth chamber: analyzed by (two sample ttest, p<0.05)
A biogeographic comparison
Author's personal copy
We found that L. microphyllum can attain high RGR under
suitable environmental conditions. A high RGR for invasive
species has been reported for many different species (Burns
2004; James and Drenovsky 2007; Soti and Volin 2010).
From an ecological perspective, high RGR can lead to the
rapid occupation of a large space, which could be advanta-
geous for exotic invasive plants (Grime and Hunt 1975). In
our study, RGR in L. microphyllum was highly enhanced by
the presence of mycorrhizal fungi. Mycorrhizal plants pro-
duced almost three times more biomass than non-mycorrhizal
plants. Increased growth and development in mycorrhizal
plants compared to non-mycorrhizal plants has also been
found in several different species (Smith and Read 2008;
Guadarrama et al. 2004; Liu et al. 2005; Pezzani et al.
2006). On the other hand, Philip et al. (2001)observed
that colonization by AMF of Lythrum salicaria decreased
plant biomass both aboveground and belowground.
Likewise Botham et al. (2009) observed that the AMF
inoculated Fragaria virginiana plants showed no differ-
ence in biomass accumulation and growth rate compared
to control plants.
The mycorrhizal treatment plants had significantly
higher SLA compared to the non mycorrhizal plants.
The difference in the SLA between the two treatments
could lead to higher RGR in the mycorrhizal plants.
Although we did not measure photosynthesis in this study,
Gandiaga et al. (2009) found that SLA together with
photosynthesis were the major determinants of growth in
L. microphyllum plants grown under different hydrological
conditions. Other studies, using different species, have also
found that mycorrhizal plants had higher leaf area, leaf
area ratio and SLA compared with control plants
(Waschkies et al. 1994;CaglarandBayram2006).
The enhanced ability of a plant to take up phosphorus from
low P soils is considered to be the major contributing factor
for mycorrhizal dependency (Hall 1975; Smith & Read 2008).
Increased P uptake by the extraradical mycelia of mycorrhizal
fungi in the roots may allow L. microphyllum to absorb more
nutrients leading to larger shoots and more extensive roots,
compared to non-mycorrhizal plants. This relationship would
potentially convey a competitive growth advantage in the
ferns introduced range in Florida as this region is conspicuous
for its P-limiting growth environment (McCormic et al. 1999).
Previous research has shown that AMF increase plant uptake
of phosphate (Bolan 1991), micronutrients (Burkert and
Robson 1994), nitrogen (Barea 1991), and act as antagonists
against some plant pathogens (Duponnois et al. 2005).
Moreover, it has been demonstrated that plants inoculated
with AMF utilize more soluble phosphate from rock phos-
phate than non-inoculated plants (Antunes and Cardoso
1991). The current study supports these results since the mean
P uptake per plant was significantly greater in the mycorrhizal
plants than in the non mycorrhizal plants.
In conclusion, it is clear that L. microphyllum can form a
very strong symbiotic relationship with AMF in its introduced
environment in Florida. It is likely that this relationship is
strongly influenced by site hydrological conditions, but this
hypothesis needs to be tested in future research, especially
when the Florida Everglades is undergoing a major hydrolog-
ical shift as an effort for restoration. The enhanced mycorrhi-
zal fungi are also likely responsible for the greater P uptake
and biomass accumulation in the control study. Symbiotic
relationships such as found in our study, are highly beneficial,
and likely enhance the aggressive growth characteristic of this
exotic pest plant in its de novo environment. Further field
experiments and survey of sites incorporating varying degrees
of inundation are necessary to better evaluate the potential role
of mycorrhizal fungi in the growth of this highly invasive
species in south Florida natural areas. A detailed analysis of
the fungal species is also necessary to determine whether
degree of colonization is dependent on the AMF community
assemblage in each of these sites.
Acknowledgments This research was supported by the Dissertation
Evidence Acquisition Fellowship, to Pushpa Soti from the Graduate
School, Florida International University. Helpful comments on the man-
uscript were made by, Suzanne Koptur, Michael Sukop and Florentin
Maurrasse. We would also like to thank Dr. Jennifer Richards for sharing
the root samples collected at Everglades National Park (permit number
EVER-2012-SCI-0050), and Ms. Cheryl Millet at The Nature Conser-
vancy for her help in sample collection in central Florida.
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... In the invaded regions of South Florida L. microphyllum displays most of the ecological characteristic associated with successful invasive plants (Westbrooks 1998): it has the ability to grow in varying hydrological (Gandiaga et al. 2009), nutrient (Volin et al. 2010), and light conditions (Volin et al. 2004). It tolerates a wide range of soil pH (Soti et al. 2014(Soti et al. , 2015, and has a strong symbiotic relationship with arbuscular mycorrhizal fungi (AMF) (Soti et al. 2014). Comparative analysis of soil samples from both its native range and invaded region have shown that L. microphyllum, which had adapted to close-to-neutral soils in Florida, grows in highly acidic soils in its native range in Australia (Soti et al. 2014). ...
... In the invaded regions of South Florida L. microphyllum displays most of the ecological characteristic associated with successful invasive plants (Westbrooks 1998): it has the ability to grow in varying hydrological (Gandiaga et al. 2009), nutrient (Volin et al. 2010), and light conditions (Volin et al. 2004). It tolerates a wide range of soil pH (Soti et al. 2014(Soti et al. , 2015, and has a strong symbiotic relationship with arbuscular mycorrhizal fungi (AMF) (Soti et al. 2014). Comparative analysis of soil samples from both its native range and invaded region have shown that L. microphyllum, which had adapted to close-to-neutral soils in Florida, grows in highly acidic soils in its native range in Australia (Soti et al. 2014). ...
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... A taxa de colonização micorrízica correlacionou-se positivamente (r=0,97) com o pH do solo. Segundo Soti et al. (2014), o nível de colonização micorrízica das raízes está relacionado com o pH do solo, de modo que se verifica maior grau de colonização micorrízica em solos com pH 5,5 a 6,0. ...
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O presente estudo teve como objetivo avaliar a ocorrência e diversidade de fungos micorrízicos arbusculares (FMAs) em plantios de cacau-cabruca localizados na região do Sul da Bahia. Inicialmente, foram realizadas coletas de amostras de solo e raízes de plantas de cacaueiro, em dois períodos climáticos (seco e chuvoso), em seis áreas de cacau-cabruca. Nas amostras, foram realizadas: avaliação da densidade de esporos, caracterização química do solo, identificação taxonômica das espécies e avaliação da taxa de colonização micorrízica das raízes. Com exceção da área 1, que apresentou maior densidade de esporos no período chuvoso, a maior densidade de esporos foi registrada nas amostras de solo coletadas no período seco. Não houve interferência do período de coleta sobre a taxa de colonização das raízes das plantas de cacau. Foram identificadas um total de 26 espécies de fungos micorrízicos arbusculares, sendo registrada maior riqueza de espécies nas áreas 2 (11 espécies), com predominância dos gêneros Glomus e Acaulospora. Houve correlação positiva significativa entre taxa de colonização das raízes e os teores de Mg e pH do solo. Palavras-chave: micorrização, Theobroma cacao L., identificação taxonômica. Arbuscular mycorrhizal fungi in the cacaueiro I culture: Occurrence and diversity in cocoa-cabruca systems. The present study aimed to evaluate the occurrence and diversity of arbuscular mycorrhizal fungi (AMFs) in cocoa-cabruca plantations located in the southern region of Bahia. Initially, samples were collected from soil and roots of cacao plants, in two climatic periods (dry and rainy), in six areas of cacao-cabruca. In the samples, were carried out: evaluation of spore density, chemical characterization of the soil, taxonomic identification of the species and evaluation of the rate of mycorrhizal colonization of the roots. With the exception of area 1, which showed the highest spore density in the rainy season, the highest spore density was recorded in soil samples collected in the dry period. There was no interference from the collection period on the rate of colonization of the roots of cocoa plants. A total of 26 species of arbuscular mycorrhizal fungi were identified, with greater species richness recorded in areas 2 (11 species), with predominance of the genera Glomus and Acaulospora. There was a significant positive correlation between root colonization rate and soil Mg and pH levels.
... A taxa de colonização micorrízica correlacionou-se positivamente (r=0,97) com o pH do solo. Segundo Soti et al. (2014), o nível de colonização micorrízica das raízes está relacionado com o pH do solo, de modo que se verifica maior grau de colonização micorrízica em solos com pH 5,5 a 6,0. ...
... The plant tissue samples were dried in an oven at 60 C for one week and finely ground using a mortar and pestle. (2), 81e90 [1]. ...
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Higher foliar nitrogen concentration in plants is often attributed to higher biomass assimilation and subsequently higher plant growth rate. To understand the underlying mechanism of extensive growth rate of an invasive plant, Old World climbing fern (Lygodium microphyllum), we analyzed the leaf tissue samples from the native and invaded habitats. In each habitat we selected 3 different locations with varying habitat characteristics (soil type, land use history and coexisting vegetation). Plant aboveground tissue collected from each site were analyzed for macro and micro nutrients. Total C and N were measured with a Truspec CN Analyzer. Total Ca, Fe, Mg, K, Mn, and P in plant tissue samples were measured using inductively coupled plasma mass spectrometry (ICP -MS). Here we present the difference in foliar nutrient concentration of invasive plant species in their native habitats and invaded habitats.
... Among other factors contributing to its successful expansion is a symbiotic association with arbuscular mycorrhizal fungi (AMF) that promotes growth rate compared to plants without the symbiosis (Soti et al., 2014). Moreover, L. microphyllum is highly dependent on the mycorrhizal fungi for growth and phosphorus uptake. ...
Chapter
Ferns have evolved over millions of years and have become adapted to a wide variety of environments. However, with changing climate variables including increased temperature, varying patterns of precipitation, and other forcing functions related to climate change, some fern species may not be sufficiently adaptive to survive. This chapter contains a review of the literature, information on fern life cycles, adaptability, and likely threats due to climate change with recommendations for further research and policies related to their conservation.
... Among other factors contributing to its successful expansion is a symbiotic association with arbuscular mycorrhizal fungi (AMF) that promotes growth rate compared to plants without the symbiosis ( Soti et al., 2014). Moreover, L. microphyllum is highly dependent on the mycorrhizal fungi for growth and phosphorus uptake. ...
Chapter
This chapter explores the possible effects of changing climate on the adaptability and survival of ferns, with a review of the current literature and recommendations for further research and policy decisions related to conservation of ferns and preservation of their varied habitats.
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Understanding of mechanisms through which arbuscular mycorrhizal fungi (AMF) facilitate establishment and growth of exotic species is important in invasion ecology. We have poor understanding of mechanisms that mediate positive or negative impact of AMF to exotic or native species. We ask whether the quantitative and or qualitative differences in the AMF colonization to exotic Flaveria bidentis and native Setaria viridis provide competitive advantage to the invader over native species. Flaveria bidentis, a native of South America, is an aggressive invader in North China. Native S. viridis is widely distributed in farmlands, roadsides and wastelands, and also found in Flaveria bidentis invaded areas. We hypothesize that exotic species alter AMF composition, which facilitate the establishment and growth of exotic species and reduces the competitiveness of native species. Experiments were carried out to: (i) quantify AMF colonization in roots of field-grown F. bidentis or S. viridis, (ii) isolate DNA sequences of AMF species from roots and soils of exotic F. bidentis and native S. viridis to carry out phylogenetic studies, and (iii) study the effect of AMF Rhizophagus intraradices spores on the physiological performance traits of both exotic F. bidentis and native S. viridis. Our results suggest that certain AMF clones had higher colonization (85%) in roots of F. bidentis than S. viridis (21.1%). AMF-inoculation (130 spores per 100 g soil) enhanced the net photosynthetic rate in the native S. viridis when grown in monoculture but reduced its net photosynthetic rate when grown in competition with exotic F. bidentis. A lower corrected index of relative competition intensity in exotic F. bidentis, and higher levels of foliar nutrient accumulation was observed in response to AMF inoculation than native S. viridis. We show that higher AMF colonization in F. bidentis provides competitive advantage over native S. viridis. This study is important because it establishes the impact of AMF colonization on physiological and ecological performance of the invader.
Article
Aims: The cordgrass Spartina alterniflora is one of the highly successful invasive plants in coastlines worldwide. Although the S. alterniflora invasion is threatening mangroves and the increasing heavy metal pollution of oceans and coasts are of growing concerns, especially in China, the effects of S. alterniflora invasion on the enrichment of sedimental heavy metals in mangrove wetlands are not known. The objectives of this study are to determine the effects of S. alterniflora invasion on enrichment of sedimental heavy metals in the mangrove wetland and the underlying mechanisms. Methods: We investigated differences in the contents of sedimental heavy metals, including As, Cd, Cr, Cu, Ni, Pb, Zn, and Mn, for two pairs of comparisons (unvegetated shoal vs S. alterniflora monoculture and Avicennia marina monoculture vs A. marina + S. alterniflora mixture), and their relationships with environmental factors in Zhanjiang Mangrove National Natural Reserve, Guangdong, China. Important findings: Spartina alterniflora invasions in mangrove wetlands increased the contents of sedimental heavy metals, with the effects being significant on Cr, Ni, Cu, Zn, and Mn. The intermediate level of pollution was only detected in the sedimental Cd. The presence of S. alterniflora resulted in enrichment in the sedimental heavy metals in the mangrove wetland in Zhanjiang, but not to the degree of concerns for contaminations. The contents of sedimental organic matter, total C, total N, total S and total K were strongly related to the contents of sedimental heavy metals in the invaded mangrove wetland. Ultimately, the dense above-and below-ground architectures of the invasive S. alterniflora likely play a predominant role in causing enrichment of sedimental heavy metals.
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Studies have documented the flora, fauna, and soils of ground-water fed wetlands, but very little is known about their plant-mycorrhizal associations. This study was designed to determine the presence of arbuscular mycorrhizal (AM) fungi in several wetland plant species associated with fens in west central Ohio, USA. Roots of wetland plant species collected at four sites had mycorrhizal fungal colonization levels ranging from O to 61.5%. Mycorrhizal associations occurred in plants of all wetland categories (OBL, FACW, FAC). We propose that these peatland have lower nutrient availability than some other wetlands and thus may be more dependent on these root fungi for nutrient uptake. Mycorrhizal fungi may be an important consideration in the functional restoration of ground-water driven wetland systems.
Book
The roots of most plants are colonized by symbiotic fungi to form mycorrhiza, which play a critical role in the capture of nutrients from the soil and therefore in plant nutrition. Mycorrhizal Symbiosis is recognized as the definitive work in this area. Since the last edition was published there have been major advances in the field, particularly in the area of molecular biology, and the new edition has been fully revised and updated to incorporate these exciting new developments. . Over 50% new material . Includes expanded color plate section . Covers all aspects of mycorrhiza . Presents new taxonomy . Discusses the impact of proteomics and genomics on research in this area.
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Most investigations of floristic diversity have involved studies 1-15 of natural vegetation. Progress using these approaches has been limited because some potentially important factors are not amenable to precise field measurement or manipulation. Here we describe an alternative research strategy in which communities were allowed to develop in turf microcosms providing factorial combinations of soil heterogeneity, grazing and mycorrhizal infection, all of which are capable in theory6,10,13,16-19 of promoting diversity. Both grazing and mycorrhizas increased diversity markedly by raising the biomass of the subordinate species relative to that of the canopy dominant. The effect of grazing is shown to be due to the differential sensitivity of the canopy dominant to defoliation. Export of assimilate from canopy to subordinate species through a common mycelial network is likely, together with enhancement of mineral nutrient capture, to be involved in the beneficial effect of mycorrhizas. No major effects of soil heterogeneity upon diversity were detected.
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The effects of five VAM fungi (Glomus etunicatum, Glomus caledonium, Glomus clarum, Glomus mosseae, and mixed inoculum) on the nutritional status of four grapevine rootstocks (420 A, 41 B, 1103 P, and 'Rupestris du Lot') were investigated. One-year-old grapevine rootstock cuttings were rooted in perlite and transferred to black polyethylene bags filled with fumigated growing medium. A 40 g mycorrhizal soil band was used for each inoculation. The percentage of VAM inoculation, leaf area, N, P, K, and total sucrose contents of the leaves were determined. Ten months after inoculation, grapevine rootstocks were colonized by the VAM fungi at frequencies ranging from 47.0 to 64.1 %. Inoculations with G. etunicatum and G. clarum significantly increased the leaf areas of 41 B, 420 A, and 1103 P rootstocks. The VAM fungi increased leaf P, but not N and K concentrations. Leaf total sucrose concentrations of the grapevine rootstocks were increased two- to four -fold with certain inoculums compared with the control.
Chapter
It has become clear that microbial activity must be considered a key component among those conferring “soil fertility,” i.e., the ability of a given soil to support plant development and nutrition (Pauli, 1967). The major components interacting to determine “soil fertility” are depicted in Figure 1. Accordingly, “fertility” can be considered an inherent property of a given soil. However, the plant itself is able to modify soil fertility in two different ways. One is based on the “rhizosphere effect” exerted by the plant, which can alter the fluxes of energy and the supply of substrates for soil microorganisms. The other way is based on the inherently different growth rates and metabolism of the different plant species that are known to “change” the capacity of the soil to provide each particular plant with nutrients (Hayman, 1975).
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Estimations have been made of the maximum potential relative growth-rate (Rmax) attained in the exponential phase by 132 species of flowering plants including representatives from each of the dry terrestrial habitats of the Sheffield region. The period of growth between two and five weeks after germination was studied in a standardized, productive environment and fitted growth-curves were used to derive various growth-analysis parameters. Woody species exhibited a bias towards low values of Rmax and a similar trend was evident among fine-leaved grasses. Annual plants were most frequent in the high Rmax category. Grasses and forbs included a wide range of growth-rates and in both, high values of Rmax were associated with a variety of growth forms. With the exception of the woody plants and the biennial herbs, Anthriscus sylvestris and Heracleum sphondylium, all the species of low Rmax examined were species which as seedlings and mature plants tend to be small in stature. The possibility that Rmax is of adaptive significance in the field was tested by examining the frequency of species of low or high Rmax in vegetation samples from a range of habitat types. In several disturbed and/or productive habitats fast-growing species were predominant and species of low Rmax were virtually or completely absent. The reverse was true of several stable, unproductive habitats. Species of moderate Rmax were ubiquitous. The adaptive significance of Rmax and its contribution to the determination of herbaceous vegetation are explored by recognizing three primary strategies in herbaceous plants. In the `competitive' strategy, high Rmax coincides with tall stature, extensive lateral spread and the tendency to accumulate leaf litter, all characteristics which facilitate the exclusive occupation of productive, undisturbed habitats. The `ruderal' strategy also involves high Rmax but here it is associated with a short life-history in which much photosynthate is directed into seeds. The potential for rapid growth allows such plants an opportunist exploitation of disturbed habitats. The third strategy, that of the `stress-tolerant' plant, is characterized by a low potential relative growth-rate and small stature. Maximum potential relative growth-rate thus appears to be of general significance in the determination of vegetation composition, but in individual habitats this composition is also considered to be dependent upon additional plant characteristics.