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10.1146/annurev.ecolsys.35.021103.105708
Annu. Rev. Ecol. Evol. Syst. 2004. 35:583?621
doi: 10.1146/annurev.ecolsys.35.021103.105708
First published online as a Review in Advance on August 5, 2004
ECOLOGY OF WOODLAND HERBS IN TEMPERATE
DECIDUOUS FORESTS?
Dennis F. Whigham
Smithsonian Environmental Research Center, Edgewater, Maryland 21037
Harvard Forest, Petersham, Massachusetts 01366; email: whighamd@si.edu
Key Words life history, reproduction, herbivory, mycorrhiza, conservation
? Abstract The diversity of woodland herbs is one of the most striking features of
deciduous forests in the temperate zone. Here I review the literature on the ecology of
woodland herbs. The review is timely because, since Paulette Bierzychudek?s seminal
review of the subject in 1982, a number of species have become rare or threatened owing
to the conversion of forests to other land uses, competition by alien plant species, and
increased abundance of native wildlife that negatively impact woodland herbs (e.g.,
white-tailed deer). Although the basic biology of woodland herbs is mostly known, few
species have been studied in detail, and we are only able to make broad generalities
about their ecology. We are especially lacking in information needed to conserve and
restore species in altered and threatened habitats.
INTRODUCTION
Woodland herbs account for most of the vascular plant species diversity in decidu-
ous forests in eastern North America (e.g., Ramsey et al. 1993, McCarthy & Bailey
1996, McCarthy 2003), Europe (e.g., Hermy et al. 1999), and Japan (e.g., Kawano
1985). This diverse group of species has long attracted the interest of naturalists,
and herbalists have used them since ancient times because many species (e.g.,
American Ginseng) contain medicinally active and therapeutic chemicals (Lewis
& Zenger 1982, Smith et al. 1996). Ecologists have also long been interested in
woodland herbs because of the wide array of life history attributes that make them
ideal research subjects. In recent years, woodland herbs have attracted attention be-
cause landscape alteration and habitat destruction caused many species to become
rare or threatened.
Species declines and losses are primarily due to the conversion of forests into
nonforest land uses and to competition from invasive species (Jolls 2003, Meekins
& McCarthy 2000), leading investigators to discuss conservation and restoration
?The U.S. Government has the right to retain a nonexclusive, royalty-free license in and to
any copyright covering this paper.
583
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584 WHIGHAM
of woodland herbs in deciduous forests (e.g., Drayton & Primack 1996, Robinson
et al. 1994, Jolls 2003). Three issues related to the population ecology of woodland
herbs have received the most attention in eastern North America: (a) Logging
(Kochenderfer & Wendel 1983, Meier et al. 1995) and (b) deer browsing (Rooney
& Dress 1997b, Waller & Alverson 1997, Rooney 2001, Bellemare et al. 2002;
Rooney & Gross 2003) both negatively impact herb diversity, and (c) clear-cut
areas abandoned to secondary succession will slow the recovery of herb diversity
(Vellend 2003).
Most studies of the ecology of woodland herbs cite the 1982 review paper by
Bierzychudek (1982a). During the intervening 20 years, additional information
has been published on a range of topics related to the biology and ecology of
woodland herbs (e.g., Gilliam & Roberts 2003). The objective of this contribution
is to update and extend the analysis provided by Bierzychudek. My hope is that
this synthesis will be useful to individuals who study woodland herbs as well as
support efforts to develop more effective research, conservation, and restoration
strategies.
The review is organized into topics that contain relevant literature citations and
an overview of the current state of knowledge. I consider the topics covered by
Bierzychudek (phenology, longevity, modes of reproduction, reproductive effort,
seed dispersal and germination, patterns of mortality, population structure and sta-
bility) and additional topics (clonality, herbivory, genetic variability, mycorrhizae,
nutrient storage and nutrient cycling, responses to disturbance) not included or
only briefly considered in the 1982 review. Jolls (2003) has also reviewed topics
considered by Bierzychudek and I have attempted to augment that material.
PHENOLOGY
Although most woodland herbs are deciduous, the range of phenological patterns
has been more fully examined, and Givnish (1983, 1987) described the diver-
sity of leaf phenology patterns in ecological and evolutionary contexts. Studies
in Japan (Kawano 1985, Uemura 1993) provide a detailed comparative analysis
of phenological patterns among woodland herbs. Uemura (1993) identified two
groups of evergreen and three groups of deciduous species, as well as wintergreen
and achlorophyllous species. Uemura?s wintergreen groups were based on leaf
longevity (one or two years). The deciduous groups, which accounted for most
species, were based on whether the species had heteroptic (i.e., plants with both
summer green and overwintering leaves), summer green, or spring green leaves.
Four wintergreen species had no leaves in the summer, and three achlorophyllous
species were in two families (Orobanchaceae and Orchidaceae). Kawano (1985)
also recognized a similar range of phenological patterns in Japan and attributed the
diversity of phenological patterns to having ?differentiated as a result of adaptive
response to woodland habitats where conspicuous periodicity in various physical
and biotic regimes predominates.?
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ECOLOGY OF HERBS OF DECIDUOUS FORESTS 585
Givnish (1983, 1987) provided rigorous analyses that supported Kawano?s com-
ments, and Neufeld & Young (2003) summarized the literature on the ecophysi-
ology of woodland herbs. Excluding winter annuals, Givnish (1987) recognized
six guilds on the basis of leaf phenology: spring ephemerals, early summer, late
summer, wintergreen, evergreen, and dimorphic. Givnish found clear differences
in leaf thickness and width between the spring ephemeral, early summer, and late
summer guilds and clear evolutionary patterns within guilds and growth forms.
Spring ephemerals had determinate growth and displayed foliage between 5?15 cm
above the ground on basal leaves or short umbrellas. Leaves close to the ground
have more efficient temperature regulation, permitting efficient use of light during
the short period between emergence and development of the tree canopy. Early
summer species had determinate growth with leaves from 10?160 cm above the
ground, displayed in a variety of umbrella-like structures that minimize shading
and maximize light capture with the lowest possible structural costs. Late sum-
mer species had indeterminate growth and displayed leaves at a greater height
(40?160 cm). Evergreen and wintergreen species and the winter phases of dimor-
phic species displayed leaves close to the ground, resulting in enhanced winter
photosynthesis (Minoletti & Boerner 1993, Tissue et al. 1995).
More recent studies support the earlier conclusions about flowering and fruiting,
especially Bierzychudek?s comment that caution needs to be applied to information
on breeding systems because the degree of compatibility or incompatibility may
vary from one location to another and geographic variability in breeding systems
should be expected. Trillium kamtschaticum in Japan (Ohara et al. 1996) and
Podophyllum peltatum in North America (Policansky 1983) are two species that
have more than one breeding system over their ranges of distribution. Northern
populations of T. kamtschaticum in Hokkaido, for example, are self-compatible and
have a high degree of genetic diversity compared with mostly self-incompatible
southern populations.
Several studies (Ashmun et al. 1982, Pitelka et al. 1985a, Collins & Pickett
1988, Givnish 1987) have shown that autumn flowering species respond positively
to light gaps and have indeterminate growth and thin, broad leaves displayed
along vertically elongating shoots. Most autumn flowering species do not develop
preformed buds, whereas most spring flowering species do (Randall 1952, as
described in Gerber et al. 1997b). Not described in the 1982 review were species
that flower in midsummer, such as Goodyera pubescens, an evergreen orchid, and
Tipularia discolor a wintergreen orchid that is leafless when it flowers (Snow &
Whigham 1989, Whigham 1990).
LONGEVITY
Not much was known about the longevity of woodland herbs in 1982, and little has
changed since then (Jolls 2003). Most woodland herbs are perennial and clonal.
Annuals (Baskin & Baskin 1998) and pseudoannuals (Baskin & Baskin 1988,
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
586 WHIGHAM
Cook 1988) that produce ramets at the ends of short-lived spacers typically live
for one year (Wijesinghe & Whigham 1997). Some species (e.g., Viola spp.) have
individuals that live between 1 and 10 years (Bender et al. 2000, 2002), and others
live for as long as 30?50 years. Clintonia borealis is an example of a clonal species
with long-lived individuals (Pitelka et al. 1985b), and Panax quinquefolia (Lewis
& Zenger 1982) and species of Trillium (Davis 1981) are examples of long-lived
nonclonal species.
For some woodland herbs, longevity cannot be easily interpreted. For example,
individuals of the nonclonal orchid Galearis spectabilis failed to produce seeds in
or near permanent plots for more than 10 years, and fewer than 5% of the individuals
originally marked are still alive (D. Whigham, unpublished data). Most individuals
appear aboveground for 1?2 years, and new plants appear each year. I suspect that
the new plants are seedlings or individuals that have persisted underground as
heterotrophic plants supported by mycorrhiza (e.g., Gill 1996, Shefferson et al.
2001), and thus establishing ages of individuals is difficult.
PATTERNS OF MORTALITY
Recent studies have provided more information on mortality. Seedling mortality
can be negatively (Syrja?nen & Lehtila? 1993) or positively (Smith 1983a) related
to density. Groups of Floerkea proserpinacoides seedlings, for example, have a
greater chance of pushing through leaf litter and surviving. Some species have low
mortality at all life history stages or mortality may be independent of age (e.g.,
Solbrig 1981). Mortality rates of most species are, however, higher for juveniles
(Meagher & Antonovics 1982b, Inghe & Tamm 1985, Matlack 1987) and smaller
plants (Pitelka et al. 1985b, Scheiner 1988, Bloom et al. 2001). In dioecious species,
mortality may (Meagher & Antonovics 1982a) or may not (Bawa et al. 1982) be
higher for females.
One would expect diseased plants to have higher mortality. Ramets of Actaea
spicata had higher mortality when infected with the smut Urocystis carcinodes,
and voles consumed infected plants at a higher rate (Wennstro?m & Ericson 1994).
Larger infected plants, however, produced more fruits because large plants may
have enough resources to allow the fungus to remain in a latent condition even
though mortality would be higher if the smut became virulent.
MODES OF REPRODUCTION
As described in the phenology section, most woodland herbs are perennials, and
the majority are clonal. Clonality has arisen separately in many groups of plants,
and many of the 21 clonal growth forms identified in the European flora (Klime?s
et al. 1997) have also been described for North American (Table 1) and Japanese
floras (Kawano 1975). However, a complete analysis of the distribution of clonal
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ECOLOGY OF HERBS OF DECIDUOUS FORESTS 587
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12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 589
growth forms among herbs in temperate forests of North America, Japan, and other
parts of Asia has not yet been done.
Further studies support Bierzychudek?s finding that although many woodland
herbs reproduce clonally, sexual reproduction is important. Kudoh et al. (1999),
for example, found that some patches of Uvularia perfoliata contained only one
genotype, indicating establishment from a single seed. A patch in a gap habitat,
in contrast, had a very high level of genetic diversity, indicating establishment of
individuals from many seeds.
In 1982, most woodland herbs were considered hermaphroditic (table 3 in
Bierzychudek 1982a). About half were self-compatible and the other half partially
or completely self-incompatible. Studies cited in Table 2 indicate that there is an
almost equal distribution between the three categories, suggesting that some level
of self-incompatibility may be more common than previously thought.
CLONALITY
Many woodland herbs are clonal and have a wide range of growth patterns (Klime?s
et al. 1997). I now consider aspects of clonality that influence current and future
growth and reproduction.
Physiological Integration
Jo?nsdo?ttir & Watson (1997) divided clonal species into four categories on the basis
of clone size and the degree of physiological integration. Using the same categories
to characterize woodland herbs, Table 3 shows that physiological integration has
been studied in few woodland herbs and most species examined form large and
highly integrated clones (Pitelka & Ashmun 1985). Patterns of physiological in-
tegration range from species such as Aster acuminatus, which form large patches
with short-lived connections and little physiological integration, to species such
as Clintonia borealis, which form large patches with long-lived connections that
are highly integrated (Ashmun et al. 1982). Clintonia borealis may be typical
of many species of spring flowering herbs, as similar patterns have been shown
for Podophyllum peltatum (Landa et al. 1992) and Aralia nudicaulis (Flanagan
& Moser 1985b). Patterns of resource sharing are complex in herbaceous species
that have a high degree of physiological integration (e.g., Hutchings & Mogie
1990, Price & Hutchings 1992). Tables 1 and 3 demonstrate, however, that too few
woodland herbs have been examined in detail to draw broad generalities regarding
physiological integration in woodland herbs.
Foraging for Resources
Foraging has been demonstrated in clonal herbs (Hutchings & de Kroon 1994),
but few species have been studied (e.g., de Kroon & Hutchings 1995, Cain et al.
1996, Wijesinghe & Whigham 2001). Wijesinghe & Hutchings (1997) suggested
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
590 WHIGHAM
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ay
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a
La
te
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ar
ch
?
Se
lf-
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tib
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sp
,A
nd
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Sc
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19
77
vi
rg
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ic
a
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rly
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ay
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im
ar
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po
lli
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r
(P
ort
ula
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)
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 591
Cl
in
to
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Pa
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lly
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ap
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ar
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87
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al
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ilia
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on
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rch
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La
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Se
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ar
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19
93
a
lb
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ilia
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a
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ic
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pr
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Se
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A
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19
93
G
er
a
n
iu
m
M
ay
Pa
rt
ia
lly
se
lf-
H
er
m
ap
hr
od
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N
o
H
al
ic
te
d
be
es
,
M
cC
al
l&
Pr
im
ac
k
19
87
m
a
cu
la
tu
m
in
co
m
pa
tib
le
fli
es
,b
u
m
bl
eb
ee
s,
(G
era
nia
ce
ae
)
be
et
le
s,
an
ts
H
ep
at
ic
a
M
ar
ch
?A
pr
il
Se
lf-
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
N
o
M
os
tly
so
lit
ar
y
M
ot
te
n
19
82
a
m
er
ic
an
a
be
es
,b
ee
fli
es
,
(R
an
un
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e)
ha
lic
tid
be
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Je
ffe
rso
n
ia
A
pr
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Se
lf-
co
m
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ap
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N
o
H
al
ic
tid
s,
ho
ne
yb
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s
Sm
ith
et
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.1
98
6
di
ph
yl
la
(fa
cu
lta
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e
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ga
m
y)
(B
erb
eri
da
ce
ae
)
Li
nn
ae
a
Ea
rly
Ju
ly
Pa
rt
ia
lly
se
lf-
H
er
m
ap
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N
o
So
lit
ar
y
be
es
,
B
ar
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&
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el
en
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m
19
87
bo
re
a
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in
co
m
pa
tib
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sy
rp
hi
ds
(C
ap
rif
oli
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(C
on
tin
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d)
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
592 WHIGHAM
TA
BL
E
2
(C
on
tin
ue
d)
Po
lli
na
to
r
Fl
ow
er
in
g
Br
ee
di
ng
lim
ite
d
Sp
ec
ie
s
pe
ri
od
C
om
pa
tib
ili
ty
sy
st
em
se
ed
se
t
In
se
ct
v
isi
to
rs
So
ur
ce
M
ai
an
th
em
um
Ea
rly
Ju
ne
Se
lf-
in
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
N
o
So
lit
ar
y
be
es
,b
ee
B
ar
re
tt
&
H
el
en
ur
m
19
87
,
ca
n
a
de
ns
e
fli
es
,s
yr
ph
id
s
M
cC
al
l&
Pr
im
ac
k
19
87
(L
ilia
ce
ae
)
M
ed
eo
la
La
te
Ju
ne
Se
lf-
in
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
Ye
s
Fl
ie
s?
B
ar
re
tt
&
H
el
en
ur
m
19
87
,
vi
rg
in
ia
na
M
cC
al
l&
Pr
im
ac
k
19
87
(L
ilia
ce
ae
)
O
xa
lis
Ea
rly
Ju
ly
Pa
rt
ia
lly
se
lf-
H
er
m
ap
hr
od
ite
Ye
s
So
lit
ar
y
be
es
,s
yr
ph
id
s,
B
ar
re
tt
&
H
el
en
ur
m
19
87
,
m
o
n
ta
na
in
co
m
pa
tib
le
(C
ha
sm
og
am
o
u
s,
fli
es
,t
hr
ip
s,
be
et
le
s
Ja
sie
ni
uk
&
Le
ch
ow
ic
z
(O
xa
lid
ac
ea
e)
cl
ei
sto
ga
m
o
u
s)
19
87
O
rc
hi
s(
=
G
al
ea
ris
)
La
te
A
pr
il?
Pa
rt
ia
lly
se
lf-
H
er
m
ap
hr
od
ite
Ye
s
B
um
bl
eb
ee
s
D
ie
rin
ge
r1
98
2
sp
ec
ta
bi
lis
ea
rly
Ju
ne
in
co
m
pa
tib
le
Po
ly
ga
m
o
di
oe
ci
ou
s
(O
rch
ida
ce
ae
)
Pa
n
a
x
Ju
ne
?A
ug
us
t
N
A
H
er
m
ap
hr
od
ite
Ye
s?
N
A
Le
w
is
&
Ze
ng
er
19
82
qu
in
qu
efo
liu
m
(A
ral
iac
ea
e)
Po
do
ph
yl
lu
m
M
ay
Pa
rt
ia
lly
se
lf-
Po
ly
ga
m
o
di
oe
ci
ou
s
Ye
s
B
um
bl
eb
ee
s
Po
lic
an
sk
y
19
83
,
pe
lta
tu
m
in
co
m
pa
tib
ili
ty
La
v
er
ty
&
Pl
ow
rig
ht
(B
erb
eri
da
ce
ae
)
19
88
Pr
im
ul
a
ve
ri
s
M
ay
Se
lf-
in
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
N
A
N
A
Le
im
u
et
al
.2
00
2
(P
rim
ula
ce
ae
)
(di
sty
lou
s)
P.
vu
lg
ar
is
M
ay
Se
lf-
in
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
Ye
s
B
ee
-fl
ie
s,
bu
m
bl
e
B
oy
d
et
al
.1
99
0
(di
sty
lou
s)
be
es
,b
u
tte
rfl
ie
s
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 593
Py
ro
la
M
id
-J
ul
y
Se
lf-
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
Ye
s
B
um
bl
eb
ee
s,
so
lit
ar
y
B
ar
re
tt
&
H
el
en
ur
m
19
87
se
cu
n
da
be
es
(P
yro
lac
ea
e)
Tr
ie
nt
al
is
Ea
rly
Ju
ne
Se
lf-
in
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
Ye
s
Sy
rp
hi
ds
B
ar
re
tt
&
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el
en
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m
19
87
bo
re
a
lis
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rim
ula
ce
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ill
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m
M
ay
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rt
ia
lly
se
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co
m
pa
tib
le
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m
ap
hr
od
ite
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o
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um
bl
eb
ee
s,
bu
tte
rfl
ie
s,
O
ha
ra
et
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99
6
ka
m
tsc
ha
tic
um
fli
es
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ilia
ce
ae
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T.
u
n
du
la
tu
m
La
te
M
ay
H
ig
hl
y
au
to
ga
m
o
u
s
H
er
m
ap
hr
od
ite
U
nc
le
ar
So
lit
ar
y
be
es
B
ar
re
tt
&
H
el
en
ur
m
19
87
O
bl
ig
at
ea
po
m
ic
tic
T.
er
ec
tu
m
M
ay
Se
lf-
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
Ye
s
D
ip
te
ra
ns
,
D
av
is
19
81
,I
rw
in
20
00
H
ig
hl
y
a
po
m
ic
tic
H
ym
en
op
te
ra
ns
,
Co
le
op
te
ra
ns
T.
gr
a
n
di
flo
ru
m
M
ay
Se
lf-
in
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
Ye
s
D
ip
te
ra
ns
,
K
al
isz
et
al
.1
99
9,
an
d
se
lf-
co
m
pa
tib
le
H
ym
en
op
te
ra
ns
,
Ir
w
in
20
00
Co
le
op
te
ra
ns
T.
n
iv
ea
le
M
ar
ch
Se
lf-
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
Ye
s
H
on
ey
be
es
,b
ee
tle
s,
N
es
om
&
La
D
uk
e
19
85
U
vu
la
ria
M
ay
Se
lf-
in
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
N
o
H
al
ic
tid
be
es
,
M
cC
al
l&
Pr
im
ac
k
19
87
se
ss
ili
fol
ia
be
et
le
,
(L
ilia
ce
ae
)
bu
m
bl
eb
ee
s
Vi
ol
a
Ea
rly
M
ay
?
Se
lf-
co
m
pa
tib
le
H
er
m
ap
hr
od
ite
N
A
B
um
bl
eb
ee
s
M
at
til
a
&
Sa
lo
ne
n
19
95
m
ira
bi
lis
en
d
o
f
(C
ha
sm
og
am
o
u
s,
(V
io
la
ce
ae
)
gr
ow
in
g
se
as
o
n
cl
ei
sto
ga
m
o
u
s)
a In
fo
rm
at
io
n
n
o
tp
ro
v
id
ed
in
o
rig
in
al
so
u
rc
e
m
at
er
ia
l.
b B
ol
d
in
di
ca
te
si
nf
or
m
at
io
n
al
so
in
B
ie
rz
yc
hu
de
k
(19
82
a).
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
594 WHIGHAM
TABLE 3 Four categories of ramet systems based on the number of ramets and the
degree of physiological integration (Jo?nsdo?ttir & Watson 1997). The number of species
found in each category is shown in the second column and the number of the species
examined that are found in woodland habitats is shown in the third column
Number Number of
of species woodland
Type of integration examined herb species
Restrictive integration in small ramet systems 4 1
Restrictive integration in large ramet systems 25 2
Full integration in small ramet systems 6 0
Full integration in large ramet systems 17 7
that species that have the potential for rapid clonal expansion respond to resource
variability differently than species with a limited potential for horizontal expan-
sion. Woodland species that typically produce preformed bulbs, corms, and short
rhizomes, for example, may be more responsive to small-scale variations in habitat
conditions than species with the potential to spread rapidly by clonal propagation.
Wijesinghe & Whigham (2001) found little evidence for nutrient foraging in two
clonal species of Uvularia, and Cain & Damman (1997) also found that nutrient
foraging might not be important in woodland herbs.
Competition
There is evidence for (e.g., Handel 1978, Hughes 1992) and against (Pitelka 1984,
Kudoh et al. 1999) intra- and interspecific competition in clonal woodland herbs.
Givnish (1982) concluded that the degree of competition depends on habitat char-
acteristics, such as the level of productivity, and that clonal species in productive
habitats can minimize interspecific competition through allelopathic interactions
or by maintaining a dense leaf cover close to the ground. Pitelka (1984) sug-
gested that clonal species that are highly integrated physiologically regulate shoot
densities to minimize intraspecific competition.
REPRODUCTIVE EFFORT
There have been several studies of patterns of biomass allocation in woodland herbs
since Bierzychudek (1982a) concluded that the only generalization that could be
made was that woodland herbs allocated less biomass to sexual reproduction than
species in grasslands or early successional habitats. Biomass of most woodland
herbs is allocated between sexual reproductive effort (SRE) and asexual propaga-
tion, referred to as vegetative reproductive effort (VRE). Both SRE and VRE have
been measured in few species. The mean variation of VRE in Aster acuminatus was
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 595
large (28.2%?35.2%) compared with 5.0%?13.4% for SRE (Pitelka et al. 1980).
VRE for Solidago caesia (8.3%?33.3%) and Aster lateriflorus (11.1%?56.3%)
was also highly variable (Gross et al. 1983). Most recent SRE data fall within
the range of values reported by Bierzychudek (1982a), but they show that SRE
can be highly variable. A highly variable SRE, for example, has been found in
the sex-switching genus Arisaema (Lovett Doust et al. 1986, Clay 1993). SREs
of staminate, carpellate, and monoecious individuals were similar (ca. 15%), but
large carpellate plants allocated 44% of the biomass to sexual reproduction, a value
much higher than the SRE reported for the species by Bierzychudek (1982a). Fac-
tors acting independently or in combination that influence SRE are light (Gross
et al. 1983, Jurik 1983, Pitelka et al. 1985a), pollination, and fruit success (Snow &
Whigham 1989). Although several authors have demonstrated that fruit and seed
production in woodland herbs is often limited (Flanagan & Moser 1985a, Davis
1986, Barrett & Helenurm 1987, Lubbers & Lechowicz 1989, Snow & Whigham
1989, Primack & Hall 1990, Robertson & Wyatt 1990, Bertin & Sholes 1993,
Agren & Willson 1992, Primack et al. 1994, Rockwood & Lobstein 1994, Irwin
2000), few studies have examined the impacts of sexual reproduction on SRE or
VRE. The most significant impacts of pollinator limitations on fruit and seed set
appear to be on future growth and reproduction (Snow & Whigham 1989, Primack
& Hall 1990, Gerber et al. 1997b, Matsumura & Washitani 2000).
SEED DISPERSAL AND GERMINATION
Bierzychudek (1982a) found that most forest herbs lack ?special dispersal mech-
anisms,? that seeds of most species require a cold treatment, and that dormancy
typically lasts less than 6 months (i.e., there is no seed bank). A review by Pickett &
McDonnell (1989) supports her conclusion, but several woodland herbs, including
weedy species, persist in the seed bank (Baskin & Baskin 1992, Baskin et al. 1993,
Leckie et al. 2000).
There have been additional studies of seed germination of woodland herbs
(e.g., Lewis & Zenger 1982; Smith 1983b; Matlack 1987; Syrja?nen & Lehtila?
1993; Traveset & Willson 1997; Baskin & Baskin 1998, 2002; Kalisz et al. 1999;
Bender et al. 2003). Germination characteristics of selected woodland herbs are
summarized in Table 4 and a larger listing can be found in table 10.18 in Baskin
& Baskin (1998). Seeds of some species are not dormant at maturation (Baskin
& Baskin 1998), but most are dormant, and a common dormancy syndrome is
morphophysiological (i.e., embryos are both morphologically and physiologically
dormant). Embryos of some species mature during a period of warm temperature
and germinate in the autumn (Baskin & Baskin 1983, Smith 1983b).
Most seed germination studies have used relatively large seeds. Some woodland
herbs (e.g., ferns, parasitic plants, and orchids), however, have very small seeds or
spores. ?Dust? seeds of terrestrial orchids are dormant when they are dispersed,
and germination is spatially and temporally variable (Rasmussen & Whigham
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
596 WHIGHAM
TA
BL
E
4
Se
ed
ch
ar
ac
te
ris
tic
so
fw
o
o
dl
an
d
he
rb
s
Se
ed
w
ei
gh
t
N
um
be
rs
ee
ds
Se
ed
Sp
ec
ie
s(
Fa
m
ily
)
(m
g)
pe
r
fr
ui
t
lo
ng
ev
ity
G
er
m
in
at
io
n
So
ur
ce
Ac
ta
ea
sp
ic
at
a
5.
9a
N
A
d
N
A
N
A
Eh
rle?
n
&
Er
ik
ss
on
20
00
(R
an
un
cu
lac
ea
e)
Al
liu
m
u
rs
in
um
5.
4a
N
A
N
A
W
in
te
ro
r
Er
ns
t1
97
9
(L
ilia
ce
ae
)
sp
rin
g
af
te
r
co
ld
tr
ea
tm
en
t
Ar
isa
em
a
tr
ip
hy
llu
m
N
A
N
A
N
A
N
A
B
ra
un
&
B
ro
ok
s1
98
7
(A
rac
ea
e)
As
ar
um
ca
n
a
de
ns
e
6.
8?
14
.2
b
2?
30
c
1
ye
ar
?
Ep
ic
ot
yl
e
do
rm
an
cy
B
as
ki
n
&
B
as
ki
n
19
86
,
(A
ris
tol
oc
hia
ce
ae
)
(ra
dic
le
gr
ow
th
Ca
in
&
D
am
m
an
19
97
,
in
au
tu
m
n,
sh
oo
t
H
ei
th
au
s1
98
1,
gr
ow
th
fo
llo
w
in
g
Sm
ith
et
al
.1
98
9a
sp
rin
g)
Ca
m
pa
nu
la
a
m
er
ic
an
a
0.
1a
20
?4
0
N
A
A
ut
um
n
o
r
sp
rin
g
G
al
lo
w
ay
20
02
(C
am
pa
nu
lac
ea
e)
de
pe
nd
in
g
o
n
ph
en
ol
og
y
o
f
m
o
th
er
pl
an
t
C.
la
tifo
lia
0.
1a
N
A
N
A
N
A
Eh
rle?
n
&
Er
ik
ss
on
20
00
Co
nv
a
lla
ria
m
a
jal
is
17
.0
a
N
A
N
A
N
A
Eh
rle?
n
&
Er
ik
ss
on
20
00
(C
on
v
al
la
ria
ce
ae
)
Fl
oe
rk
ea
pr
o
se
rp
in
ac
oi
de
s
N
A
1
Se
v
er
al
N
o
do
rm
an
cy
,
Sm
ith
19
83
b
(L
im
na
nth
ac
ea
e)
ye
ar
s
co
n
tr
ol
le
d
by
en
v
iro
nm
en
t
H
ep
at
ic
a
a
cu
til
ob
a
2.
4a
9.
9a
N
A
N
A
Sm
ith
et
al
.1
98
9b
(R
an
un
cu
lac
ea
e)
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 597
Je
ffe
rso
n
ia
di
ph
yl
la
3.
4?
36
.8
b
?
20
?4
0c
N
A
Sp
rin
g
fo
llo
w
in
g
B
as
ki
n
&
B
as
ki
n
19
89
;
(B
erb
eri
da
ce
ae
)
(E
mb
ryo
s
di
sp
er
sa
l
Sm
ith
et
al
.1
98
6,
u
n
de
v
el
op
ed
19
89
a;
H
ei
th
au
s1
98
1
w
he
n
se
ed
s)
di
sp
er
se
d
La
th
yr
us
ve
rn
u
s
12
.0
a
N
A
N
A
N
A
Eh
rle?
n
&
Er
ik
ss
on
20
00
(F
ab
ac
ea
e)
Pa
ri
sq
ua
dr
ifo
lia
4.
6a
N
A
N
A
N
A
Eh
rle?
n
&
Er
ik
ss
on
20
00
(T
ril
lia
ce
ae
)
Pa
n
a
x
qu
in
qu
efo
lia
N
A
1.
9a
2
ye
ar
s?
18
?2
2
m
o
n
th
s
Le
w
is
&
Ze
ng
er
19
82
(A
ral
iac
ea
e)
af
te
rd
isp
er
sa
l
Po
do
ph
yl
lu
m
pe
lta
tu
m
N
A
N
A
N
A
N
A
B
ra
un
&
B
ro
ok
s1
98
7
(B
erb
eri
da
ce
ae
)
Po
ly
go
na
tu
m
m
u
lti
flo
ru
m
28
.6
a
N
A
N
A
N
A
Eh
rle?
n
&
Er
ik
ss
on
20
00
(C
on
v
al
la
ria
ce
ae
)
Sa
ng
ui
na
ria
ca
n
a
de
ns
is
15
.7
a
11
.2
?3
1.
0b
N
A
N
A
Pu
dl
o
et
al
.1
98
0,
(P
ap
av
er
ac
ea
e)
H
ei
th
au
s1
98
1
H
ya
ci
nt
ho
id
es
N
A
N
A
N
A
Ju
ne
?J
ul
y.
Th
om
ps
on
&
Co
x
19
78
(=
Sc
ill
a)
n
o
n
sc
ri
pt
a
Se
ed
sr
eq
ui
re
(L
ilia
ce
ae
)
hi
gh
te
m
pe
ra
tu
re
co
n
di
tio
ni
ng
,
ge
rm
in
at
e
in
au
tu
m
n
Si
le
ne
di
oi
ca
0.
7?
1.
2b
N
A
Se
v
er
al
N
o
do
rm
an
cy
M
at
la
ck
19
87
(C
ary
op
hy
lla
ce
ae
)
ye
ar
s
(co
ntr
oll
ed
by
en
v
iro
nm
en
t)
Tr
ie
nt
al
is
41
.1
?6
4.
7c
0?
14
c
Se
v
er
al
A
ut
um
n
o
r
H
iir
sa
lm
i1
96
9
eu
ro
pa
ea
ye
ar
s
fo
llo
w
in
g
sp
rin
g
(P
rim
ula
ce
ae
)
(C
on
tin
ue
d)
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
598 WHIGHAM
TA
BL
E
4
(C
on
tin
ue
d)
Se
ed
w
ei
gh
t
N
um
be
rs
ee
ds
Se
ed
Sp
ec
ie
s(
Fa
m
ily
)
(m
g)
pe
r
fr
ui
t
lo
ng
ev
ity
G
er
m
in
at
io
n
So
ur
ce
Tr
ill
iu
m
er
ec
tu
m
4.
1a
9.
6?
21
.6
b
N
A
N
A
D
av
is
19
81
,G
un
th
er
&
(L
ilia
ce
ae
)
La
nz
a
19
89
T.
gr
a
n
di
flo
ru
m
6.
5a
N
A
N
A
N
A
G
un
th
er
&
La
nz
a
19
89
T.
ka
m
tsc
ha
tic
um
2.
9a
38
?2
16
c
N
A
N
A
O
ha
ra
&
H
ig
as
hi
19
87
,
O
ha
ra
&
K
aw
an
o
19
86
T.
n
iv
ea
le
2.
8a
31
.4
a
N
A
N
A
Sm
ith
et
al
.1
98
9a
T.
ts
ch
on
os
ki
i
3.
5a
28
?1
68
c
N
A
N
A
O
ha
ra
&
H
ig
as
hi
19
87
,
O
ha
ra
&
K
aw
an
o
19
86
T.
u
n
du
la
tu
m
5.
7a
N
A
N
A
N
A
G
un
th
er
&
La
nz
a
19
89
U
vu
la
ria
pe
rfo
lia
ta
N
A
N
A
N
A
D
ou
bl
e
do
rm
an
cy
W
eb
b
&
W
ill
so
n
19
85
,
(L
ilia
ce
ae
)
(ra
dic
le
in
fir
st
ye
ar
,
W
hi
gh
am
19
74
ep
ic
ot
yl
in
se
co
n
d)
Vi
ol
a
m
ira
bi
lis
2.
48
?2
.5
6b
17
.0
?1
9.
9b
N
A
N
A
M
at
til
a
&
Sa
lo
ne
n
19
95
(V
io
la
ce
ae
)
V.
so
ro
ri
a
7.
8?
9.
3b
20
?5
4c
U
nk
no
w
n
R
eq
ui
re
co
ld
So
lb
rig
19
81
bu
t>
1
ye
ar
tr
ea
tm
en
t,
ge
rm
in
at
e
in
sp
rin
g
a M
ea
n
b R
an
ge
o
fm
ea
n
s
c R
an
ge
d I
nf
or
m
at
io
n
n
o
tp
ro
v
id
ed
in
o
rig
in
al
so
u
rc
e
m
at
er
ia
l.
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 599
1993, 1998b; Whigham et al. 2002). Seeds of many woodland orchids will not
germinate unless an appropriate mycorrhizal fungus is present (Rasmussen 1995,
Whigham et al. 2002), but others germinate without fungi (Baskin & Baskin 1998)
and the spatial variation in fungal distribution may determine where successful
germination will occur (Rasmussen & Whigham 1998b).
To the list of seed dispersers (Table 5) can be added spiders (Gunther & Lanza
1989), yellow jackets (Zettler et al. 2001), turtles (Braun & Brooks 1987), rabbits
(Knight 1964), and both brown and black bear (Traveset & Willson 1997). Long
distance dispersal of seeds has also been documented (Willson 1993, Cain et al.
1998, Vellend et al. 2003), and hedgerows that connect forest patches provide
intermediate scale corridors for dispersal (Corbit et al. 1999). Although a variety
of vertebrates and invertebrates disperse woodland herb seeds (Handel et al. 1981,
Vellend et al. 2003), ants are the most common dispersal agent (table 10.21 in
Baskin & Baskin 1998). Interactions between ants and other animals can play
a critical role in seed dispersal (Webb & Willson 1985; Smith et al. 1989a,b;
Valverde & Silvertown 1995). Ground beetles, for example, eat elaiosomes on
Trillium seeds, resulting in lower rates of ant seed dispersal (Ohara & Higashi
1987). Seed dispersal by ants is also influenced by seed density (Smith et al.
1986), and studies of Trillium species have shown that ant-seed interactions are
very complex (Gunther & Lanza 1989, Higashi et al. 1989)
Seed dispersal distances vary widely, and data in Table 5 are probably minimum
values because no wind-dispersed species (e.g., terrestrial orchids) are included.
Mammals (Vellend et al. 2003) and birds can disperse seeds for long distances, but
movements of seeds over long distances are difficult to assess. Rodents disperse
seeds of woodland herbs (e.g., Valverde & Silvertown 1995), but they also destroy
many seeds (Smith et al. 1989a,b).
Models have also been used to test generalities and evaluate the importance
of seed dispersal and factors that influence it. Patterns of seed dispersal (Ehrle?n
& Eriksson 2000) and disturbance to the forest canopy influence woodland herb
community diversity (Fro?borg & Eriksson 1997, Valverde & Silvertown 1997b),
and dispersal of seeds away from parent plants can be beneficial (Cipollini et al.
1993) or harmful (Valverde & Silvertown 1997a).
NUTRIENT STORAGE AND NUTRIENT CYCLING
Herbs account for a relatively small amount of the biomass and nutrient standing
stocks in deciduous forests, but nutrient uptake and cycling by herbs can account
for significant amounts of total ecosystem nutrient flux (Peterson & Rolfe 1982).
The importance of herbs in nutrient cycling processes in forests is, however, un-
doubtedly related to their patterns of distribution in forests, as the distribution of
most species is strongly influenced by nutrient availability and habitat heterogene-
ity (Crozier & Boerner 1984; Gilliam 1988; Lechowicz et al. 1988; Klinka et al.
1990; Vellend et al. 2000a,b; Miller et al. 2002; Beatty 2003; Small & McCarthy
2003).
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
600 WHIGHAM
TA
BL
E
5
Se
ed
di
sp
er
sa
la
n
d
pr
ed
at
io
n
ch
ar
ac
te
ris
tic
so
fw
o
o
dl
an
d
he
rb
sa
D
isp
er
sa
l
Pe
rc
en
t
Sp
ec
ie
s
D
isp
er
sa
la
ge
nt
di
st
an
ce
(m
)
Pr
ed
at
or
pr
ed
at
io
n
So
ur
ce
Al
liu
m
u
rs
in
um
(L
ilia
ce
ae
)
G
ra
v
ity
an
d
flo
w
er
in
g
0.
19
?0
.2
7
N
A
b
N
A
Er
ns
t(
19
79
)
st
al
ks
fa
lli
ng
o
v
er
As
ar
um
ca
n
a
de
ns
e(
Ar
ist
olo
ch
iac
ea
e)
A
nt
s
M
ea
n
=
1.
54
,
R
od
en
t
Li
ttl
e
H
ei
th
au
s1
98
1,
M
ax
=
35
(P
er
o
m
ys
cu
s
to
?
50
Sm
ith
et
al
.1
98
9b
,
le
uc
op
us
)
Ca
in
&
D
am
m
an
19
97
,
Ca
in
et
al
.1
99
8
Ar
a
bi
sl
ae
vi
ga
ta
v
ar
.
G
ra
v
ity
<
0.
5
N
A
N
A
B
lo
om
et
al
.2
00
2a
la
ev
ig
at
a
(B
ras
sic
ac
ea
e)
Ar
isa
em
a
tr
ip
hy
llu
m
(A
rac
ea
e)
Tu
rt
le
(Te
rr
a
pe
ne
ca
ro
lin
a)
NA
N
A
N
A
B
ra
un
&
B
ro
ok
s1
98
7
Ca
re
x
co
m
m
u
n
is
(C
yp
era
ce
ae
)
A
nt
s,
m
at
ur
e
cu
lm
sb
en
d
0.
25
N
A
N
A
H
an
de
l1
97
8
to
w
ar
d
gr
ou
nd
C.
pl
at
yp
hy
lla
M
ay
,
flo
w
er
st
al
ks
be
nd
0.
01
?0
.2
9
N
A
N
A
H
an
de
l1
97
8
w
he
n
m
at
ur
e
C.
u
m
be
lla
ta
A
nt
s
0.
02
?0
.1
6
N
A
N
A
H
an
de
l1
97
8
Cl
ay
to
ni
a
vi
rg
in
ic
a
(P
ort
ula
ce
ce
ae
)
A
nt
s,
m
at
ur
e
in
flo
re
sc
en
ce
N
A
N
A
N
A
H
an
de
l1
97
8
re
fle
x
es
to
w
ar
d
gr
ou
nd
En
dy
m
io
n
o
n
sc
ri
pt
us
(L
ilia
ce
ae
)
Pa
ss
iv
e
ex
pu
lsi
on
o
f
M
ea
n
=
0.
40
,
N
N
A
K
ni
gh
t1
96
4
se
ed
s,
ra
bb
its
M
ax
=
0.
81
Fl
oe
rk
ea
po
se
rp
in
ac
oi
de
s(
Li
mn
an
tha
ce
ae
)
G
ra
v
ity
U
p
to
0.
05
N
on
e
N
A
St
am
p
&
Lu
ca
s1
98
3
G
er
a
n
iu
m
m
a
cu
la
tu
m
(G
era
nia
ce
ae
)
Ex
pl
os
iv
e
(e.
g.,
ba
lli
sti
c)
M
ea
n
=
3.
02
,
N
A
N
A
St
am
p
&
Lu
ca
s1
98
3
M
ax
=
4.
55
H
ep
at
ic
a
a
cu
til
ob
a
(R
an
un
cu
lac
ea
e)
A
nt
s
N
A
R
od
en
ts
Se
ed
Sm
ith
et
al
.1
98
9a
pr
ed
at
io
n
is
ra
re
Im
pa
tie
ns
ca
pe
ns
is
(B
als
am
ina
ce
ae
)
Ex
pl
os
iv
e
(e.
g.,
ba
lli
sti
c)
M
ea
n
=
0.
24
,
N
A
N
A
St
am
p
&
Lu
ca
s1
98
3,
M
ax
=
3.
5
Pr
im
ac
k
&
M
ia
o
19
92
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 601
Je
ffe
rso
n
ia
di
ph
yl
la
(B
erb
eri
da
ce
ae
)
A
nt
s
N
A
R
od
en
ts
37
?5
4
o
f
H
ei
th
au
s1
98
1;
Sm
ith
ca
ps
ul
es
pr
io
r
et
al
.1
98
6,
19
89
b
to
de
hi
sc
en
ce
Lu
zu
la
ca
m
pe
st
ri
s(
Ju
nc
ac
ea
e)
A
nt
s
1
N
A
N
A
H
an
de
l1
97
8
Pa
n
a
x
qu
in
qu
efo
liu
m
(A
ral
iac
ea
e)
G
ra
v
ity
<
0.
1
R
od
en
ts?
N
A
Le
w
is
&
Ze
ng
er
19
82
O
xa
lis
a
ce
to
se
lla
(O
xa
lid
ac
ea
e)
Ex
pl
os
iv
e
(e.
g.,
ba
lli
sti
c)
R
an
ge
:0
.6
?4
.5
N
A
N
A
B
er
g
20
00
Ph
yt
ol
ac
ca
a
m
er
ic
an
a
(P
hy
to
la
cc
ac
ea
e)
B
ird
s
>
33
N
A
N
A
H
op
pe
s1
98
8
Po
do
ph
yl
lu
m
pe
lta
tu
m
(B
erb
eri
da
ce
ae
)
Tu
rt
le
(Te
rr
a
pe
ne
ca
ro
lin
a)
NA
N
A
N
A
B
ra
un
&
B
ro
ok
s1
98
7
Pr
im
ul
a
vu
lg
ar
is
(P
rim
ula
ce
ae
)
A
nt
s(
M
yr
m
ic
a
ru
br
a
)
A
nt
s
=
0.
03
7?
N
A
N
A
Ca
ha
la
n
&
G
lid
do
n
19
85
;
ca
.
20
%
,r
o
de
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12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 603
Nutrient cycling is also related to patterns of resource allocation. The majority
of woodland herbs are perennial, and most biomass and nutrients are stored in
roots, rhizomes, bulbs, and corms (Kawano 1975, Muller 1979, Gross et al. 1983,
Piper 1989, Kawano et al. 1992). The seasonal pattern of biomass and nutrient
allocation in Allium tricoccum seems to be typical of many perennial woodland
herbs (e.g., Whigham 1974, Nault & Gagnon 1988). Early in the growing season,
carbon and nutrients stored belowground are allocated to aboveground biomass,
peaking in leaves and reproductive structures in the spring or early summer. As the
growing season progresses, nutrients are resorbed and accumulate in belowground
structures, declining in aboveground structures as leaves senesce and fruits and
seeds develop. In clonal species, belowground biomass and nutrients are allocated
to new ramets, as well as to older structures (Pitelka et al. 1980, Boerner 1986,
Benner & Watson 1989, Wijesinghe & Whigham 1997).
Nutrient resorption has been investigated in a few species. DeMars & Boerner
(1997) found significant differences in phosphorus and nitrogen resorption and
suggested that differences among species were due to phenological characteristics,
topographic differences, and nutrient and moisture availability. In Polystichum
acrostichoides, an evergreen fern, there were no seasonal differences in nutrient
resorption, indicating that leaves were maintained during the cold period to allow
the species to fix carbon whenever climatic conditions were suitable (Minoletti &
Boerner 1993).
Patterns of nutrient uptake and resorption by woodland herbs led to the ?vernal
dam hypothesis? (Muller 1979, Muller 2003) that described the ability of wood-
land herbs to immobilize nutrients in biomass that would otherwise be lost from
the ecosystem. Others (e.g., Peterson & Rolfe 1982) examined this hypothesis
and concluded that plants have the potential to immobilize nitrogen but have little
impact on other nutrients. Zak et al. (1990) evaluated the hypothesis in the con-
text of competition for nutrients between the spring geophyte Allium tricoccum
and microbes. They concluded that microbes immobilized more nitrogen than the
spring geophyte, but that microbes and A. tricoccum together retained significant
amounts of nutrients.
MYCORRHIZAE
Every woodland herb that has been examined has been shown to develop mycor-
rhizal associations, and the primary benefit to the herb partner is increased nutri-
ent uptake (e.g., Widden 1996, Whitbread et al. 1996, Lapointe & Molard 1997).
There appear to be differences in levels of mycorrhizal activity among species,
with slow growing species having lower levels of mycorrhizal infection (Brundrett
& Kendrick 1990a,b). Differences in mycorrhizal activity also occur across mois-
ture, nutrient, and successional gradients; woodland herbs in wet and nutrient-rich
habitats have lower levels of mycorrhizal activity (DeMars & Boerner 1995) and
species in late successional habitats have higher levels of vesicular, arbuscular, and
ectomycorrhizal activity (Boerner 1992, Boerner et al. 1996).
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
604 WHIGHAM
Terrestrial orchids are an interesting group because they develop mycorrhizal
associations that apparently only benefit the orchid partner (Rasmussen 1995).
Some woodland orchids are achlorophyllous (e.g., Corallorhiza sp.) and obtain
all their carbon and other nutrients from mycorrhizae, thus requiring fungal inter-
actions at all life history stages (Zelmer & Currah 1995). Mycorrhizae are also
important for woodland orchids that produce leaves but are able to persist below-
ground for one to many years without forming leaves (Mehrhoff 1989, Gill 1996,
Shefferson et al. 2001).
A variety of techniques for studying seed germination and protocorm develop-
ment in the field portend to expand our understanding of mycorrhizal interactions
in terrestrial orchids (Rasmussen & Whigham 1993, 1998a,b, 2002). Much of our
knowledge comes from laboratory studies (e.g., Rasmussen 1995), but more recent
efforts have included field-based approaches. Seeds of some species, as previously
noted, require mycorrhizae for germination, whereas interactions between seeds
and mycorrhizal fungi appear to be facultative for other species (Baskin & Baskin
1998; Rasmussen 1995, 2002; Rasmussen & Whigham 1998b; Whigham et al.
2002). Protocorms, the life history stage that follows seed germination, obtain all
their resources through mycorrhizal interactions (Rasmussen 1995, 2002). Some
woodland orchids (e.g., species of Corallorhiza) associated with fungi that form
ectomycorrhizal interactions and are indirectly parasitic on trees (Zelmer & Currah
1995).
POPULATION STRUCTURE AND STABILITY
Since 1982, there have been few age structure studies of woodland herbs, and most
have employed stage-based models to simulate age-based characteristics (e.g.,
Bierzychudek 1982b; Meagher & Antonovics 1982a,b; Hara & Wakahara 1994;
Bierzychudek 1999; Jolls 2003). Some species have been shown to have stable
population structure (Meagher & Antonovics 1982a; Inghe & Tamm 1985; Kawano
et al. 1986, 1992), but for most species, population structure is temporally variable
(Inghe & Tamm 1985, Matlack 1987, Scheiner 1988, Whitman et al. 1998) due to
variation in factors such as weather, disturbance, and levels of nutrient availability
(Whigham et al. 1993, Fro?borg & Eriksson 1997). Population size may also vary
spatially, as has been shown for the rare orchid Isotria medeoloides (Mehrhoff
1989). Population trends may also be directional. Diekmann & Dupre? (1997), for
example, found long-term declines in populations due to regional acidification and
eutrophication.
More recent publications suggest that flowering rates may be greater and more
variable than the 1%?25% range reported in the 1982 review. Flowering may
be size dependent, and once a minimum size is reached, individuals can flower
yearly independent of the level of reproductive effort (Lewis & Zenger 1982,
Mehrhoff 1989, Cain & Damman 1997). Other species switch back and forth
between flowering and nonflowering depending on the level of reproductive effort
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
ECOLOGY OF HERBS OF DECIDUOUS FORESTS 605
(Bierzychudek 1982b, Snow & Whigham 1989, Gerber et al. 1997a). Variability
in flowering also appears to be influenced by factors such as genetics (Meagher &
Antonovics 1982a), herbivory (Snow & Whigham 1989), weather (Inghe & Tamm
1985), disturbance (Whigham et al. 1993, Primack et al. 1994, Gill 1996), and
the costs of producing flowers and fruits (Snow & Whigham 1989, Whigham &
O?Neill 1991, Primack & Hall 1990, Falb & Leopold 1993, Gerber et al. 1997b).
GENETIC VARIABILITY
Relatively few studies have examined genetic variability of woodland herbs, and
even fewer studies have been based on measurements of genetic identities of plants
within or among populations. The most important conclusion thus far is that most
populations of clonally reproducing species typically contain more than one genet
(e.g., Smith et al. 2002). Patches of some species (e.g., Clintonia borealis and
Podophyllum peltatum) contain few, perhaps one or two, genets (Policansky 1983,
Pitelka et al. 1985b). Patches of other woodland herbs (e.g., Asarum canadense)
contain numerous genotypes (Eriksson 1989, Cain & Damman 1997), and genetic
substructuring has been demonstrated for clonal species (Cahalan & Glidden 1985,
Kudoh et al. 1999, Ziegenhagen et al. 2003). Some woodland herbs have both high
and low genetic diversity, depending on rates of outcrossing and seed set (Ohara
et al. 1996).
Uvularia perfoliata (Kudoh et al. 1999) is probably representative of many
clonal woodland herbs. An Uvularia patch in an area where tree gaps had previ-
ously occurred had a high level of genetic variability at small (centimeter) and large
(meter) scales. Ramets of different genets intermingled, and there was no evidence
of competition between genets. Kudoh et al. (1999) also found genetic substruc-
turing of a few genets with many ramets, and of many genets with few ramets.
They attributed this pattern to a few founder genets and subsequent establishment
of new genets from seeds that were produced from within-patch outcrossing.
RESPONSES TO DISTURBANCE
Canopy Gaps
Disturbance plays an important role in the dynamics of forests (Pickett & White
1985, Webb 1999), and a close linkage exists between canopy disturbance and
dynamics of understory vegetation (Gilliam & Roberts 2003). Collins et al. (1985)
reviewed the literature on woodland herb responses to gaps and suggested that
herbaceous species can be divided into three guilds (Table 6) and that various
physiological, morphological, and ecological responses of species could be pre-
dicted for each guild. Woodland herbs clearly respond to changes in light conditions
in canopy gaps, but microhabitat heterogeneity may be equally important (Bratton
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
606 WHIGHAM
TABLE 6 Predicted responses (first column) of woodland herbs in gap habitats
(Collins et al. 1985). The predicted responses are positive (+), none (0), or
negative (?)
Responses Sun herbs Light flexible herbs Shade herbs
Water uptake 0 + +
Nutrient uptake +/0 +/0 0
Seedling establishment + + 0/?
Leaf duration +/0 +/0 0/?
Assimilation +/0 + ?
Pollination +/0 + +
Flowering +/0 + 0/+
Seed set +/0 + 0
Clonal growth +/0 + 0/?
Architectural shift 0 + 0
Survivorship 0 + ?
1976). Pits and mounds associated with treefalls, for example, provide a high de-
gree of microhabitat variability and may have a higher species diversity and greater
herb cover than adjacent undisturbed areas (Peterson & Campbell 1993). Mounds
and logs created during treefalls are sites for colonization by woodland orchids
(Rasmussen & Whigham 1998a). Pits and mounds have also been shown to have
characteristic species assemblages, depending to a large degree on the dominant
tree species (Beatty 1984).
Although microhabitat conditions are important, changes in light quality and
quantity associated with gaps generate the greatest responses in understory herbs
because most species are light limited (Table 6). Most woodland herbs experience
increased growth and reproduction in response to increased light (Collins & Pickett
1988, Neufeld & Young 2003). Positive responses to gaps are related to gap size,
but positive responses can be partially offset by negative impacts associated with
competition (Hughes 1992).
Individual species have shown a range of responses to increased light in gaps.
Gap size has a positive influence on population size (Scheiner 1988), growth rates,
and frequency of flowering (Dahlem & Boerner 1987, Whigham et al. 1993, Griffith
1996, Wijesinghe & Whigham 1997). Recently, models have been used to evaluate
a range of species responses to gap habitats. Valverde & Silvertown (1997a, 1998)
concluded that Primula vulgaris formed metapopulations in response to gaps and
that local populations formed and became extinct in response to changing habitat
conditions associated with light gaps. Cipollini et al. (1993) and Whigham et al.
(1993) found similar results for Cynoglossum virginianum, a nonclonal wood-
land herb that persists in a vegetative state for long periods under closed canopy
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ECOLOGY OF HERBS OF DECIDUOUS FORESTS 607
conditions. When gaps form, individuals increase in size and flower until light
levels decline, eventually returning to a vegetative state.
Herbivory
Woodland herbs (e.g., ferns) produce chemicals that deter herbivores, but herbivory
appears to have a negative impact on most species (Brunet 1993). The impacts
of herbivory on growth and reproduction of woodland herbs appears to be, in
part, species dependent (Rockwood & Lobstein 1994), but other factors are also
important. Plant size (Davis 1981, Rooney & Waller 2001), sex (Delph et al.
1993), and nutritional quality (Ericson & Oksanen 1987) are important. The plant
parts attacked by herbivores (Ericson & Oksanen 1987), herbivore-feeding patterns
(Ehrle?n 1995, Matlack 1987), the phenological status of the plant (de Kroon et al.
1991, Watson 1995, Whigham & Chapa 1999), and the degree of physiological
integration in clonal species (Ashmun et al. 1982, Price et al. 1992) are also
important.
As might be expected, the greater the amount of tissue removed the greater
the impacts on growth and reproduction, but other factors (e.g., the pattern of leaf
removal) also influence plant responses to herbivory (Whigham 1990, Price &
Hutchings 1992). Perhaps most importantly, most woodland herbs do not produce
new aboveground tissues in response to herbivory, which suggests that the timing
and amount of herbivory would influence short- and long-term plant responses.
Complete or partial leaf removal can result in cessation of or decreased flowering
(Whigham 1990, Syrja?nen & Lehtila? 1993, Primack et al. 1994). Partial defoliation
can, however, also have no effect on growth and reproduction (Agren & Willson
1992).
Most herbivory studies have only considered aboveground plant parts. Herbi-
vores also consume belowground tissues (Ericson & Wennstro?m 1997). Rodent
herbivory of underground corms of Tipularia discolor, for example, had a greater
impact on the long-term dynamics of populations than any other factor (Whigham
& O?Neill 1991).
Deer browsing can result in the almost complete elimination of woodland herbs,
except for a few unpalatable species (Tilghman 1989). In addition, species that can
survive on microsites (e.g., refuges such as mounds, boulders, and logs) that are
unavailable to deer can also avoid browsing (Rooney & Dress 1997a). If species can
survive browsing, however, there is some evidence that they can recover following
elimination of deer browsing (Albert & Barnes 1987).
Waller & Alverson (1997) agreed with McShea & Rappole (1992) in concluding
that deer are keystone species with impacts well beyond reducing herb diversity in
forests. Deer browsing reduces or eliminates tree regeneration (e.g., Nomiya et al.
2002), and browsing results in the loss of bird species that specialize in the forest
understory (Casey & Hein 1983). Deer browsing can also reduce invertebrate
diversity (Miller et al. 1992), and increased deer abundance has been linked to
Lyme disease (Jones et al. 1998). The evidence seems clear that deer abundance
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
608 WHIGHAM
and management will continue to be a major threat to the diversity of woodland
herbs in forests of eastern North America.
Urbanization and Forest Conversion
Researchers have examined the fate of woodland herbs in urban settings, conclud-
ing that we may not be able to conserve the original species diversity in urban
forests (Robinson et al. 1994, Drayton & Primack 1996). Similarly, several studies
(Peterken & Game 1984, Falinski et al. 1988, Brunet 1993, Hermy et al. 1993,
Hermy 1994, Singleton et al. 2001, Bellemare et al. 2002, Vellend 2003, Verheyen
et al. 2003) have shown that it will take long periods of time, perhaps centuries,
for herb diversity to recover in forests that developed on lands that had previously
been cleared and used for agricultural production. For example, forested areas in
the Vosges Mountains that had been cleared and used to support crops, gardens,
pastures, or tree plantations had similar species diversity of woodland herbs, but
none of them were characteristic of ancient forests (Koerner et al. 1997).
Logging
Woodland herb diversity may be lower in logged forests, and it may never again
reach levels found in old-growth forests (Meier et al. 1995). Comparison of dif-
ferent logging activities showed that woodland herbs were negatively impacted by
clearcuts (Albert & Barnes 1987, Duffy & Meier 1992) and completely eliminated
by clearcutting followed by herbicide application (Kochenderfer & Wendel 1983).
Duffy & Meier (1992) concluded that it was unlikely that the herb community
would recover in the clearcut stands within normal (40?150 years) cutting cycles.
Selective logging had less of an impact on herb diversity in Canada (Reader 1987,
1988; Meier et al. 1995), and Reader & Bricker (1992) suggested that selective
logging could be used as a management tool to conserve woodland herbs.
CONCLUSIONS AND RECOMMENDATIONS
Woodland herbs include species of diverse phylogenetic origin that have evolved
a wide range of life history adaptations that allow them to persist and flourish
in an environment that is often light limited. Light is clearly the most important
factor limiting the growth and reproduction of woodland herbs, but some life
history strategies (e.g., spring ephemerals, wintergreen species, parasites, etc.) have
evolved that allow individuals to complete most of their growth and reproduction
prior to full development of the tree canopy and resultant low light conditions.
Although much more has been learned about the ecology of woodland herbs
since Bierzychudek?s (1982a) review, only a small percentage of the species have
been studied in detail, and, at best, we can still offer only broad generalizations
about the ecology of woodland herbs. What types of studies will most likely ben-
efit future efforts to understand the ecology of woodland herbs and also support
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ECOLOGY OF HERBS OF DECIDUOUS FORESTS 609
conservation and restoration efforts? Individual species will undoubtedly continue
to attract the attention of researchers, and those types of efforts should be en-
couraged. The most effective studies, however, are likely to be those that use a
synthetic approach in which functional groups (e.g., Givnish 1982, Kawano 1985)
are identified and used as the basis for testing ideas that further our understanding
of woodland herbs as well as support conservation and restoration efforts.
As indicated, only a few broad generalizations about the ecology of woodland
herbs are, however, possible because only a limited number of species and have
been studied in detail. First, it is clear that most species are adapted to take advan-
tage of canopy disturbances, which result in higher light conditions for a few years
or more and higher levels of other resources. Canopy gaps often have higher herb
diversity because they have a greater range of microhabitats (e.g., pits and mounds,
coarse wood in various stages of decomposition), but light is still the key to success
of most species. Most woodland herbs have increased growth, sexual reproduction
and asexual propagation in gaps, and seedling recruitment also appears to be more
common in gap habitats. It is difficult, however, to evaluate species responses to
gap disturbances without either long-term studies or experimental manipulations.
Matrix models offer the opportunity to explore broader questions about the range
of responses of woodland herbs to gap disturbances. To date, however, matrix mod-
els have been applied to few species, and a useful approach would be to use them
to address questions related to functional groups. The incorporation of spatially
explicit models into studies of woodland herb populations would also be useful
because of the high degree of spatial heterogeneity found in forest habitats.
A second broad generalization is that all woodland herbs are mycorrhizal. What
are the ecological consequences of mycorrhizal interactions beyond those that have
been associated with nutrient uptake? We still know very little about the impor-
tance of mycorrhizal interactions in the establishment and growth of seedlings
of woodland herbs, especially species that require mycorrhizal associations for
germination and survival.
A third generalization is that herbivores and pathogens affects the short- and
long-term dynamics of woodland herb populations. Herbivores and pathogens
probably influence woodland herbs much more than have been identified to date.
Additional studies are needed on the growth and reproductive responses of wood-
land herbs to pathogens and herbivores, especially the responses of belowground
tissues.
Conservation issues have only begun to be addressed, and future research needs
to focus on the maintenance and restoration of woodland herbs in landscapes
influenced more directly by human activities (e.g., clearcutting and fragmentation
of forests) or indirectly (e.g., deer browsing, invasion of alien species). Little
research has been conducted on management approaches that might be used to
reintroduce species into forests from which they have been eliminated.
Finally, more effort should be placed on long-term population studies of wood-
land herbs. Inevitably, long-term studies provide valuable information that can be
used to design experiments, develop realistic parameters for modeling efforts, and
12 Oct 2004 11:55 AR AR229-ES35-21.tex AR229-ES35-21.sgm LaTeX2e(2002/01/18) P1: GJB
610 WHIGHAM
open new lines of investigation. Long-term studies reveal previously unknown facts
about woodland herb ecology and the many important interactions that woodland
herbs have with other organisms. Although difficult to fund and sustain, long-term
studies have low start-up and maintenance costs and are ideal for demonstrating
ecological phenomena in teaching environments. Small colleges and universities
throughout the eastern United States own or have access to sites that would be ideal
for conducting long-term studies of woodland herbs. Datasets that expand from
year to year with relatively little effort can be very useful in teaching ecological
principles. Hopefully, this review will encourage others to start both short- and
long-term studies using this interesting group of plants as models to embellish
scientific knowledge and educate the public and future scientists.
In closing, space limitations required me to restrict the number of references
cited in the review. A larger list of relevant documents can be found at http://www.
serc.si.edu/labs/plant ecology/biblio.jsp, and additional references are in Gilliam
& Roberts (2003).
ACKNOWLEDGMENTS
The review was written while the author was a Bullard Fellow at Harvard Forest.
I extend thanks to the staff of the Harvard Forest, especially David Foster, Glen
Mozkin, and Ruth Kern for reading early versions and for discussions related to
it. I thank Matt Baker, Jerry Baskin, Candy Feller, Anne Innis, Ann Lubbers, Jay
O?Neill, Ryan King, Melissa McCormick, Glen Mozkin, Dag-Inge ?ien, Mark
Vellend, and Dushyantha Wijesinghe for comments on various drafts. The Smith-
sonian?s Environmental Sciences and Scholarly Studies programs have supported
the author?s research on woodland herbs. Smithsonian Fellowship and Visiting Sci-
entist programs provided funding for post-docs and visitors who work on woodland
herbs (Martin Cipollini, Hans de Kroon, Heidrun Huber, Hiroshi Kudoh, Melissa
McCormick, Hanne Rasmussen, Allison Snow, Dushyantha Wijesinghe, Jess Zim-
merman). The Smithsonian Work-Learn program supported many student interns
over a 20-year period. The long-term influence of Shoichi Kawano is much appre-
ciated, as are grants from the Smithsonian Institution and the Japanese government,
which have provided resources for long-term interactions between our labs. Finally,
special thanks to Jan for her support during the preparation of the manuscript.
The Annual Review of Ecology, Evolution, and Systematics is online at
http://ecolsys.annualreviews.org
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