The Effects of Rhizome Severing and Nutrient Addition on Growth and Biomass Allocation in Diphasiastrum digitatum

10 Pages·2000·6 MB·English

by  Carrie A Railing

A
American
Fern
Journal 90(2]:77-86
(2000)
The Rhizome
and
Effects of Severing Nutrient
Addition on Growth and Biomass
Allocation
in
Diphasiastrum
digitatum
McCarthy*
Carrie A. Railing and Brian
C.
OH
Department of Environmental and Plant Biology, Ohio University, Athens, 45701, U.S.
—
Abstract. The effects of severing and fertilization on ramets of Diphasiastrum digitatum in an
Ohio hardwood forest were examined to determine the extent of young ramet integration. The
extent of integration was measured by overall vigor, and by architectural biomass, and growth
variables. Vigor decreased with any plant manipulation. Likewise, measured architectural and
all
biomass variables were smaller in manipulated treatments. Similar negative effects in growth and
biomass were seen with severing or fertilization, while a combination of both showed a further
decrease in growth variables compared to either of the individual treatments. Severing reduced
growth and biomass fifty percent compared to the control, indicating that integration is important
in young multi-module ramet development. The results are consistent with other studies sug-
gesting clonal lycopods are highly integrated and emphasizes the importance of integration in
young and
ramets of D. digitatum for survival growth.
modules,
Clonal plants are constructed of basic units, called that are iterated
throughout the development of a clone and can potentially function as inde-
pendent members (ramets] of a genetic individual (genet) (Harper, 1977). The
between modules
existence of connections ramets or of a clone inherent to
is
These underlying vascular connections the move-
architecture. facilitate
its
ment and sharing of plant substances (Pitelka and Ashmun, 1985), and thereby
permit the clone to function as a physiologically integrated system (Watson
among
and Casper, 1984). As long as connections persist modules, there a
is
movement and Ashmun,
potential for resource (Marshall, 1990; Pitelka 1985).
However, great deal of variation in the degree of integration within and
a
among has been demonstrated and Watson,
clonal plant species (Jonsdottir
may
clonal plants vary in their longevity and/or function-
1997). Specifically,
moved
of connections (months to decades), the substances that are (min-
ality
hormones), and
carbohydrates, photoassimilates, the direction
nutrients,
erals,
Hutch-
of flow, whether acropetal, basipetal, or bidirectional (see references in
ings and Bradbury, 1986; Jonsdottir and Watson, 1997; Klimes et 1997;
al.,
Ashmun,
and
Marshall, 1990; Pitelka 1985).
Such physiological integration can be a major factor influencing survival of
any
clonal plants that retain ramet connections for period of time (Eriksson
Ashmun,
and Watson, and
and 1990; Jonsdottir 1997; Pitelka 1985).
Jerling,
by ramets such
Adaptive advantages incurred participating in integration in-
and and
clude successful establishment survival, accelerated maturity, local-
recovery (Caraco and Kelly, 1991; Hutchings and Bradbury, 1986;
ized
stress
and Ashmun, The
and Watson, 1997; Pitelka 1985). significance of
Jonsdottir
where
these adaptive features are seen in cases disintegration, or fragmenta-
78 ME
J
occur,
through
mental
Ashmun,
However
1985). fragmentation
this or disintegration occurs, has
it
consequences on
the growth, biomass and
overall survival of the plant in ques-
most which
tion, of remain unexplored number
relatively
in
a of clonal plant
species (Charpentier
et 1998).
al.,
Although
physiological
integration in clonal plants has
attracted a great deal
of attention in recent years (see references in Marshall and
Price, 1997;
Jons-
and
dottir Watson, 1997; and Ashmun,
Pitelka most
1985), studies have
fo-
cused on angiosperms
rather than lower plants such Exam-
as pteridophytes.
ining the clonal patterns and processes
of integration in pteridophytes
offers
not only complete view
a of the plant kingdom, but also an evolutionary
offers
view
of integration
in lineages of clonal plants have many
that existed in hab-
and
geologic time
itats periods
(Dyer, 1979). In particular, few studies have
investigated
the extent of physiological integration in lower plants such
as
lycopods
(Callaghan,
1980; Carlsson Headley
1990;
et al., et 1985; ig88a;
al.,
1988b) and
those that do concern lycopods common
involve
relatively few,
species that do not reside in North America. Diphasiastrum
digitatum
(Dillen-
American
that
Watson
Lau and
1997; Young,
1988). Previous examination
of
this species' physiolog-
ical integration has focused on
the survival of older modules (Lau and Young,
whereas
1988), generalized
studies of clonal plants indicate younger
that
ra-
mets
Bradbury
we
In this study, examine
the effects of severing and
nutrient addition on
newly
developing ramet growth
Diphasiastrum
in digitatum
in order
to deter-
mine
the general
extent of physiological and how
its integration determine
to
directly responds
it to disintegration from the parent clone and
to a localized
We
increase
in nutrients. hypothesize
during
that early development,
artifi-
cially severing rhizome connections
to the parent will
significantly decrease
the vigor, growth, and biomass of young ramets. Furthermore, we
hypothesize
adding
that nutrients
to the edaphic environment
sterile
characteristic of D.
ramets
Methods
and
Materials
Organism.—
Diphasiastrum
(Wagner and
Beitel, 1996) forms
that
e growth. This
evergreen
oerennial
dis
form
dimorphic
fan-like, and
(vegetative
reproductive) and
vertical shoots adven-
• ' «-^fc 1 # _ « _
common
(Wagner and
8
RAILING & MCCARTHY: RHIZOME
79
hardwood
including and
habitats, conifer forests as well as open shrubby areas
(Cody and Wagner and Many members
Brltton, 1989; and
Beitel, 1996). of
this
other closely related genera in the temperate region are characterized as weedy
and grow
believed
are to in relatively conditions
infertile soil (Page, 1979;
Tryon and
Tryon,
1982).
The
span most
life of vertical shoots is approximately four to six years (Pri-
mack, 1973; Railing and McCarthy, unpublished Rhizome
connections
data).
may
some
persist for time before decaying and thereby separating previously
connected ramets. This type of vegetative reproduction has been noted more
as
common
than sexual reproduction (Primack, 1973) in Diphasiastrum
digita-
most
tum, reasoned because
likely so of the unsuccessful or poor spore
ger-
mination witnessed gametophyte
in cultures, rather than in nature (Roberts
and
Herty, 1934; Whittier, 1981; 1998).
—
Study Run
Area. Strouds State Park (SRSP) located in Athens County,
is
Ohio 39^20'N and 82^5'W
at (latitude) (longitude), in the southeastern
foothills
was
of the state. In the early twentieth century, the area disturbed by grazing
and As most
timbering activities. such, of the forests are considered be even-
to
aged second-growth. What now known SRSP was
as acquired conser-
is for
vation purposes in the late 1940's and early 1950's by the State of Ohio and
became The
eventually a state park in 1959. park spans over 1100 ha on Ap-
man
palachian Ohio's unglaciated Allegheny plateau, and centered around
a
is
Dow
made
watershed, Lake. The topography consists of a number of steep
and ravines believed be remnants meltways.
hills to of glacial Soils in this
region of Ohio are classified as Inceptisols (Brady, 1984) and conditions
soil
throughout the park are characterized as being moderately deep to deep, well-
drained, and mostly loamy (typic hapludalfs), originating from sandstone,
silt-
and
stone, shale, limestone parent material (National Cooperative Soil Survey,
1985). Precipitation relatively evenly distributed throughout the year and
is
cm
ranges from 5—10 per month, with July being the wettest month and Oc-
Mean
tober the driest. temperatures (high/low) are 29/18 C for July and 2/—
C
January (Midwestern Climate
for Center, 1999).
The vegetation of SRSP primarily deciduous cover and can be
is forest clas-
mixed mesophytic (^cer Aesculus octandra, Fagus
sified as spp., grandifolia,
and Liriodendron tulipifera) in the lowlands and mixed oak or oak-hickory in
uplands [Quercus and Caryo
the alba, Q. rubra, Q. velutina glabra, C. ovata),
A
number
of white pine plantations [Pinus strobus) are also present in the
(<10%
park of vegetation), having been planted by conservation corps
for
watershed protection. There are also sporadic old-fields, grassy meadows, and
maintained The herbaceous woodlands
turf grass habitats. layer of the large-
is
upon and
ly dependent the overstory vegetation there considerable diversity
is
and
of both microhabitats species (Payne, 1957; Greer ah, 1997).
et
—
Field Methods. Ten Diphasiastrum digitatum patches were located within
m
1-2
SRSP. In June 1998, 4 apical rhizome tips, approximately apart, were
haphazardly located around the perimeter of each patch. Rectangular quadrats
X
(0.25 2 m) were established around each of the four rhizome tips such that
VOLUME NUMBER
AMERICAN FERN JOURNAL:
80 90 2 (2000)
m
the rhizome was situated 0.5 into the quadrat along the longest dimension.
Quadrats within each patch were randomly assigned to one of four treatment
groups. The treatment group (Cj served as the control, and remained un-
first
Rhizomes
manipulated throughout the duration of the experiment. in the sec-
ond treatment group were severed their entrance into the rectangular
(S) at
quadrat. Quadrats assigned the third treatment group were treated with
to (F]
a standard 10-10-10 inorganic (Dragon All Purpose Plant Food) a
fertilizer at
prescribed monthly rate (ca. 100 g fertilizer per m^) for perennials. Rhizomes
in the fourth treatment group (SF] were subject to both severing and fertiliza-
tion treatments. Other above ground vegetation within quadrats was clipped
and were
treatments applied after quadrat establishment in June 1998.
made
In August 1998 vigor observations were in situ before excavating all
rhizomes. Rhizomes were assigned to one of three vigor categories that were
based on health and color. High vigor (HI) indicated a rhizome or ramet with
high health and a green to bright green color, similar to the rest of original
its
patch. Moderate vigor (MD) and low vigor (LO) referred to a ramet that dis-
played moderate health and green yellow color and poor health with yellow
to
brown
Excavated ramets were subsequently measured,
to color, respectively.
oven dried at 80 for ca. 48 hours and weighed. Data were collected to reflect
**C
growth and biomass
patterns since the treatment application. Variables
initial
examined upon ramet collection include total growth length (cm), number of
new
mean
and and and
shoots roots initiated, internode shoot length (cm),
aboveground (internode and shoot) biomass each ramet.
for
(g)
—
A
Analytical Methods. (Chi-Square Goodness-of-Fit was used
G-test Test)
among
to analyze the homogeneity of vigor categories treatment groups (Sokal
and Rohlf, 1995) with the null hypothesis that there are no differences in ramet
among
frequency the twelve possible classes treatment/vigor combina-
(i.e.,
G
anDroximate
tions). In order for to better the chi-sauare statistic, the Wil-
and
(1995).
(MANOVA)
Multivariate Analysis of Variance
significant treatment effects across growth and biomass parameters mea-
all
A
Lambda
sured using the Wilk's randomized com-
test statistic (Hintze, 1997).
MANOVA
was employed
plete block design using treatment group as a fixed
and random
effect patch as a effect. Data sets were checked for normality, equal
and Omnibus
variance, equality of covariance using the D'Agostino
test
Modified-Levene and
Equal- Variance
test,
MANOVA.
he assumptions Those
of
failini
transfer
mations.
Planned comparisons (Dowdy and Wearden, were used
(a priori) 1991) to
among
test for significant differences treatment groups according to the three
We
hypotheses. used the first hypothesis (HJ to test for significant differences
between and
the control all other treatments (C vs. S,F,SF), the second (H^) to
test for differences between treatment types (S vs. F) and the third (HJ to test
RHIZOME
81
Table
Observed
frequency of ramets within each treatment group according vigor category,
1. to in-
when
cluding G-lest (Chi-Square Goodness-of-Fit) results. Note that the cell element marked with an
G = >
P
asterisk removed, 14.8 and 0.1.
is
Vigor Category
MD
LO
Treatment Group HI
9*
Control (C)
I
Sever
(S) 5 5
6
Fertilize (F) 3
1
Sever and 4
Fertilize (SF) 6
G
= <
P
24.9, 0.01
for an additive effect of treatment types (SF vs. S,F). The above planned com-
were used on
parisons only those
variables significantly contributing
to treat-
MANOVA.
ment
within the All analyses mentioned above
effect statistical
NCSS
were conducted using software (Hintze, 1997) with an alpha
statistical
used
of 0.05 to test hypotheses.
Results
The results of the G-test used for the vigor study indicated that significant
<
among
combinations
differences (P 0.01) vigor-treatment existed (Table
1),
thereby rejecting the overall null hypothesis and indicating that Diphasiastrum
How-
digitatum ramets within vigor categories did a treatment
reflect effect.
—
upon examination, one (Treatment C HI may be
ever, closer class vigor) driv-
ing the significance in this analysis (Table In an exploratory procedure, the
1),
was removed from
aforementioned class the analysis to test for significant dif-
among The
ferences the remaining other classes. resultant G-Test indicated
homogeneous
that the classes were then (Table Hence, the control group
1).
and any
displayed the highest vigor, perturbation (treatments S, F, SF) of the
and reducing moderate
ramets affected their health coloring, vigor to either the
(MD) poor (LO)
or categories.
=
among
no
Although there are significant (P 0.347) differences patches for
among
measured
the variables (Table there are significant differences
treat-
2),
ANOVAs
=
ment groups Individual one-way each of the growth
(P 0.044). for
MANOVA
and biomass variables in the analysis indicate that shoot biomass,
new new
and
growth, shoots initiated roots initiated are the specific var-
total
among
iables measured that reflect significant differences treatment groups
power no
with high (Table 3). In addition, relatively little to significant differ-
mean among
ences in internode and shoot height treatment groups were wit-
nessed (Table However, confidence in this finding low due to the minimal
3). is
power meet
statistical in the respective F-tests. In order to the multicollinearity
MANOVA,
assumption of both above ground biomass and internode biomass
were dropped from the analysis and examined seperately using one-
variables
=
way ANOVAs. Above ground biomass and internode biomass
(P 0.004) (P
=
among
treatment groups
did significantly (Table
0.002) differ
3).
82 FERN JOURNAL: VOLUME NUMBER
90
Table
(MANOVA)
2. Multivariate Analysis of Variance among
test for differences treatments and
patches across all variables measured. Above-ground biomass and intcmode biomass were
variables
re-
moved
meet
to multicollinearity assumption.
Wilk's
Source Lambda
dfl df2
F-ratio P-value
Treatment
0.306
18 63 L81
0.044
Patch
0.125 54 117 L09
0.347
Overall, the plants any manipulated
in group 50%
or SF] displayed
(S, F, a
more
or decrease in growth and biomass The
(Fig. planned comparison
1). first
C
was
[H,: vs. S,F,SF) significant across examined <
variables
all (P 0.01] with
any
manipulation
of the rhizomes leading
to a decrease in the measured
var-
iables There was no
(Fig. 1). significant difference between treatment types
for
variables by
all as indicated the second planned comparison
S
(H2: vs.
F).
Results of the third planned comparison SF
{H3: vs. S,F) indicate that only the
new
-
shoots initiated (P 0.03) and new roots = showed
initiated (P 0.08) an
treatment
Discussion
The
showed
fact that severing
a decrease in growth and biomass compared
ramets
show
dependency upon
parental connections and
are therefore highly
inte-
number
losperms
biomass
in severed versus non-severed ramets (Ashmun
1982; Charpen-
et
al.,
Watson
ever, the severity of such disintegration often depends upon the and
size age
of the ramet severed from
the parent clone
ramet
(Hartnett
and Watson
Jonsdottir
when
comparing
the current study using younger,
interconnected
ramets
to
ramets
1988) the effects of severing are essentially the same. This
suggests that the
increased hardship by
likely incurred younger ramets when
not seen
those
is
ramets
and Watson
Jonsdottir
(1997} classify Diphasiastrum
digitatum
as displaying
integration
full in large clonal fragments, and
in turn place
other pteridophytes
and
angiosperms
within
this category. Bracken
{Pteridium aquilinum
(L.)
number
growth
of
digitatum
more
grow by means
that
of a perennating,
indeterminate rhizome
Werth
Experiments
1993). aimed
originally method
finding
at a
of controlling bracken
RAILING McCarthy: rhizome
& severing
83
ANOVA
Table
Results of one-way
3. tests for variables significantly contributing treatment
to effect
MANOVA.
ANOVAs
in previous Asterisks denote one-way two
for variables originally omitted from
MANOVA.
MS
Variable Measured
df P Power
F-ratio
Above-Ground Biomass
(g)* 3 0.28 5.71 0.004 0.82
Intemode Biomass
(g)* 3 0,57 6.33 0.002
0.86
Shoot Biomass
(g) 3 1.69 6.92 0.001 0.89
Growth
Total (cm)
3 0.37 4.69 0.009
0.73
Mean
Internode Length (cm)
3 0.51 0.10 0.959
0.06
Mean
Shoot Height (cm)
3 0.50 2.69 0.066
0.47
New
Number
Shoots
3 9.90 8.36 0.001
0.95
Number New
Roots
3 0.34 5.67 0.004
0.82
have
revealed that severing bracken rhizomes does not ehcit the same severe
and
concerning D. digitatum (Lau and Young,
1988). In seasonally-timed,
fact,
re-
above and below ground
petitive cutting of rhizomes, well above ground
as as
fronds bracken needed
of is to significantly affect respiration and assimilate
and
translocation ultimately reducing the plant's spread within an area (Low-
reaffirms the
anoth
dophyte.
Comparisons between
the physiological integration of the mayapple [Podo-
phyllum and
peltatum, L.) D. digitatum are also useful as these two herbs often
occupy
similar habitats in the eastern deciduous and
forest are frequently
found growing near each other. Although the P. peltatum tends to have a great-
er degree of lateral spread than D, digitatum, both are extensive integrators
and
(Jonsdottir Watson, 1997) that reproduce mainly through
vegetative pro-
cesses, and thereby are severely affected by severing treatments
that interfere
with acropetal transport younger ramet fragments However,
to in particular.
ramet
ment severed and Watson
(Tonsdottir
ramets
same
reduction growth
in
^
^^ s^
comparison suggests that Dipbasiastrum digitatum dependent upon
integra-
is
tion at any scale within a ramet, indicating that integration an adaptive
is trait,
possibly because of the resource-poor environments inhabits (Jonsdottir and
it
Watson.
19971.
treatment
TOWth
treatment group (S) compared to the control group This resuh does not
(C).
and
Upon
biomass Diphasiastrum
of digitatum. closer examination of the experi-
may
mental methods, the nitrogen source within the fertilizer be a possible
The
explanation. fertilizer used within the current experiment delivered ni-
ammonium
two and
trogen in forms: nitrogen f3.91%l urea nitropen ffi.n9%V
84 AMERICAN FERN VOLUME
JOURNAL:
60 o
Hi** 1.25
^
v:
o
2 a
40
a
-H
0.75
o -H
o
o "So
CQ
20
<
0.25
V)
12
0.4
o
0.3
8
B
-H
o
0.2
4
o
0.1
CO
4
0.8
CiO
o a>
3 is
0.6
o
E
2
0.4
C
1
0.2
C
S F SF C
S F SF
Treatment Group
Treatment Group
Mean
Fig. values (± standard growth and
1. 1 error) of biomass variables under each
of four
=
treatment conditions (A B = C = D =
control, severed, fertilized, severed and
fertilized). Sig-
nificance levels for each of the three planned comparisons, ***
(H,, H^, HJ, are denoted as such:
= P < 0.001, = P < 0.01, P < 0.05,+ = P <
0.1.
A
number
of studies suggest
that nitrate is the ideal deliverable form of
nitro-
gen ammonium
in whereas and
fertilizers, urea forms can
negatively
affect
some
health of
plants, particularly in combination with lower edaphic pH
Ma
ammonium
further
ammonium
accumulation
of
ammonium
plants
accompanied by
plant and
wilting, chlorosis, necrosis of above-ground
parts
(Cao and Kpodar
Tibbitts, 1998; symptoms ammonium
1992). Similar
et of
al.,
were
toxicity observed
in this study for the two treatment groups receiving
and
fertilizer (F SF).
For most
the
part, studies concerning
physiological integration in lycopod
species have focused on documenting
strictly water and/or movement
nutrient
and
storage throughout the organism (Callaghan, 1980; Headley
et 1985;
al.,
I I V I _^^ ^^H fl « H 1 F S ^r 1 ^ ^m ^H ^ ^H ^M "^h
further
ramet
lycopod
or clonal plant
survival in addition determining and
to short
long-
plant
architectural
examinations would
lend
greatlv to the
RAILING & MCCARTHY: RHIZOME SEVERING DIPHASIASTRUM ATUM
IN DIGIT
85
understanding
of the presence of clonal plants throughout evolutionary and
ecological
history.
Acknowledgments
This study was funded in part by the Department of Environmental and Plant Biology Ohio
at
We
would Madden
University, Athens, Ohio. like to thank Robert and Teresa Dennis help
for their
work and
in field data collection.
Literature Cited
AsHMUN, Thomas, and
J.W., R.J. L.F. Pitelka. 1982. Translocation of photoassimilates between
sister ramets in two rhizomatous forest herbs. Ann. Bot. 49:403-415.
Brady, N.C. 1984. The nature and property Macmillan Publishing Company, New
of soils, York.
Callaghan,
T.V. 1980. Age-related patterns of nutrient allocation in Lycopodium annotinum from
Swedish Lapland. Strategies of growth and population dynamics of tundra plants Oikos
5.
35:373-386.
Cao, W., and T.W. Tibbits. 1998. Response of potatoes to nitrogen concentrations differ with ni-
trogen forms. Plant Nutr. 21:615-623.
J.
On
Caraco, T., and C.K. Kelly. 1991. the adaptive value of physiological integration in clonal
Ecology 72:81-93.
plants.
Carlsson, B.A., I.S, JoNSUOTTiR, B.M. Svensson and T.V. Callaghan. 1990. Aspects of clonaltiy
in the arctic:a comparison between Lycopodium annotinum and Carex bigelowii. Pp. 131-
151 in van Groenendael and H. de Kroon, eds. Clonal growth in plants: regulation and
J.
SPB Academic The
function. Publishing. Hague, Netherlands.
Charpentier, a., Mesleard, and Thompson. 1998. The effects of severing on the clonal
F. J.D.
growth and clonal architecture of Scirpus maritimus. Oikos 83:107-116.
Cody, W.J., and D.M, Britton. 1989. Ferns and fern allies of Canada. Research Branch, Agriculture
Canada. Ottawa, Canada.
A
D'Agostino, R.B., A. Belanger, and R.B. D'Agostino 1990. suggestion for using powerful
Jr.
and informative tests of normality. American Statistician 44:316-321.
New
Dowdy, S., and S. Wearden. 1991. Statistics for research, edition 2. John Wiley and Sons,
York.
Dyer, A.F. 1979. The experimental biolog}' of ferns. Academic Press, New^ York.
Eriksson, O., and L. Jerling. 1990. Hierarchical selection and risk spreading in clonal plants. Pp.
79-94 in van Groenendael and H. de Kroon, eds. Clonal growih in plants: regulation and
J.
SPB Academic The
function. Publishing. Hague, Netherlands.
ammonium
Feng, and A.V. Barker. 1992. Ethylene evolution and accumulation by tomato
J.,
plants with various nitrogen forms and regimes of acidity (Part Plant Nutr. 15:2457-
I).
J.
2469.
Greer, G.K., R.M. Lloyd, and B.C. McCarthy. 1997. Factors influencing the distribution of pte-
Ohio hardwood
ridophytes in a southeastern forest. Torrey Bot. Soc. 124:11-21.
J.
New
Harper, 1977. Population biology of plants. Academic Press, York.
J.L.
among
Hartnett, D.C, and F.A. Bazzaz. 1983. Physiological integration intraclonal ramets in
Solidago canadensis Ecology 64:779—788.
L.
Headley, A.D., T.V. Callaghan, and Lee. 1985. The phosphorous economy of the evergreen
J.A.
tundra plant Lycopodium annotinum. Oikos 45:235-245.
Headley, A.D., T.V. Callaghan, and J.A. Lee. 1988a. Phosphate and nitrate movement in the
New
clonal plants Lycopodium annotinum L. and Diphasiastrum complanatum Holub.
(L.)
110:487-495.
Phytol.
Headley, A.D.. T.V. Callaghan, and Lee. 1988b. Water uptake and movement in the clonal
J.A.
New
Lycopodium annotinum and Diphasiastrum complanatum Holub.
plants L. (L.) Phytol.
110:497-502.
NCSS Number
Hintze, 1997. 6.0 Users Manual. Cruncher Statistical Systems, Inc. Kaysville, UT.
J.L.
86 FERN
Bradbury
BioScience 36:178-182.
JoNSDdTTiR, and M.A. Watson.
I.S., 1997. Extensive physiological
integration:an adaptive
in
trait
resource-poor environments? Pp. 109-136 in H. de Kroon and van Groenendael, The
eds.
J.
and
ecology- evolution of clonal plants. Backhuys
Publishers. Leiden, Netherlands.
KlimeS, L., Klimesova, R. Hendriks, and van Groenendael.
1997. Clonal plant
J. architechture:
J.
a comparative analysis of form and function. Pp. 1-29 in H. de Kroon and van Groenendael,
J.
and
eds. Tlie ecology evolution of clonal plants. Backhuys
Publishers. Leiden,
Netlierlands.
Kpodar, RM.,
Latche, and ammonium
J.C. G. Cavalie. 1992, Effects of nitrogen on
nutrition
max
soybean
[Glycine L. Merr) photosynthetic carbon metabolism. Agronomie
12:265-275.
Lau, and Young.
R.R., D.R. 1988. hifluence
of physiological on
integration survivorship and water
relations in a clonal herb. Ecology 69:215-219.
A
Lowday,
1986. comparison
J.E. of the effects of cutting with those of the herbicide asulam on
the control of bracken. Pp. 359-367 Smith and
in R.T. Taylor, eds. Bracken: land
J.A. ecology^,
and
use control technology Parthenon
Publishing, Carnforth, England.
Lowday,
R.H. Marks, and Some
Nevison.
J.E., G. 1983. of the effects of cutting bracken [Pteridium
aquilinum Kuhn)
(L.) at different times during the summer. Environ. Manaeem 17*373-
}.
380.
M.\GALHAES, and D.M. Huber. Ammonium
1989.
J.R., assimilation
in different plant species as
pH
by
affected nitrogen form and
control in solution culture. Pert. Res. 21:1-6.
Marshall,
C. 1990. Source-sink
relations of interconnected ramets. Pp. 23-41 van Groenen-
in
J.
and
dael H. de Kroon. Clonal growth and
in plants: regulation SPB Academic
function.
The
Publishing. Hague,
Netherlands.
Marshall, C, and
E.A.C.
Price. 1997. and
Sectoriality imphcations
its for physiological integra-
tion. Pp. 79-107 in H. de Kroon and van
Groenendael. The and
eds. ecology evolution
of
J.
clonal Backhuys
plants.
Publishers. Leiden, Netherlands.
Midwestern
Climate
Center. 1999. chmate summary
Historical
for Zanesville, Ohio,
http://
mcc.sws.uiuc.edu/
National
Cooperative
Soil Survey.
1985. Soil survey of Athens County Ohio. U.S. Government
Printing Office, Washington, DC.
Page, The
C.N. 1979.
diversity of ferns: an ecological perspective. Pp. 9-56 The
in A.F. Dyer,
ed.
experimental New
biology Academic
of ferns. Press, York.
A
Parks, and Werth.
J.C, C.R. 1993. study of spatial features of clones in a population of bracken
fern, Pteridium aquilinum
(Dennstaedtiaceae). Amer. Bot. 80:537-544.
J.
A
Payne, W.W.
1957. floristic study of the Athens State Forest, Athens County, Ohio. Masters
Ohio
thesis. University, Athens.
Pitelka, L.R, and Ashmun.
J.W. 1985. Physiology and integration of ramets
in clonal plants. Pp.
399-435
in J.B.C. Jackson, L.W. Buss, and R.E. Cook, eds. Population biology and
evolution
New
of clonal organisms. Yale University Haven,
Press, CT.
Primack, Growth
R.B. 1973.
patterns of five species oi Lycopodium. Amer. Fern
63:3-7,
J.
Roberts, and
E.A., S.D. Herty. 1934. Lycopodium complanatum
var. flabelliforme Fernald:
its
anatomy and method
a of vegetative propagation. Amer.
Bot. 21:688-697.
J.
SoKAL, and
Rolph,
R.R., F.J. 1995. Biometry, edition 3. W.H. Freeman and Company, New
York.
Tryon, and
R.M., Tryon. and
A.F. 1982. Ferns
allied plants with special
reference
to tropical
New
America.
Springer-
Verlag, York.
Wagner,
and
J.H. J.M. Beitel. 1996. Lycopodiaceae. Pp.18-37
Jr.. in Flora of North America Ed-
Committee,
itorial eds. Flora North America
of north of Mexico, Vol. Oxford University
2.
New
Press, York.
Watson,
A.M., and
B.B. Casper. 1984. Morphogenetic
constraints on
patterns of carbon
distri-
bution Ann.
in plants. Rev. Ecol. Syst. 15:233-258.
Whittier, D.R
1981. Gametophytes of Lycopodium
digitatum (formerly complanatum
L. var.
fla-
grown
belliforme) as in axenic cuhure.
Bot. Gaz. 142:519-524.
Whittier, D.R
1998. Germination
of spores of the Lycopodiaceae
in axenic cuhure. Amer. Fern
I
88:106-113.