2005
NORTHEASTERN
NATURALIST
The
Natural
Biology
History,
T. Martine1'*,
Seedling
conradii:
and
Reproduction,
Post-fire
Christopher
of Corema
12(3):267-286
Observations
of a
Recruitment
David Lubertazzi1,
and Andrew
DuBrul2
Abstract - Corema conradii (broom-crowberry, Ericaceae) is a rare dioecious shrub
that reaches the southern extent of its range in New Jersey. A hot fire burned through
one of the most extensive New Jersey populations of this state-endangered species
during the summer of 2001, resulting in mortality of nearly all plants in the burned
areas. Significant seedling recruitment occurred in the fall of 2002, followed by an
even greater seedling emergence the following year. Fire is known to be an important
stimulus for seed germination in this species, and fire events are an important
component of the life cycle. We report data on seedling emergence as well as present
ecological and biological observations of Corema conradii in the unusual coremal
habitat of the New Jersey Pine Barrens, and suggest a life cycle model for this
understudied species.
Introduction
Ericaceae)
(Torr.) Torr. ex Loud, (broom-crowberry,
has attracted attention from botanists because it exhibits a number of curious
it is locally rare. This lowFirst and most importantly,
characteristics.
Corema
conradii
growing, evergreen, woody shrub occurs in small disjunct populations dis?
to the New Jersey
tributed across an area that stretches from Newfoundland
Coastal Plain (Clemants 1997). Although the species has a global heritage
in New
rank of G4 (uncommon but not rare), it is listed as SI (endangered)
York and New Jersey, S2 (imperiled) in Quebec, S3 (vulnerable) in Massa?
chusetts and Prince Edward Island, and SX (extirpated) in New Brunswick
(NatureServe
2003). Second, across its range it occurs in an unusual collec?
These
tion of areas that share some interesting and peculiar characteristics.
and
on
are generally
heath-like,
dry, upland soils,
collectively
that are not widespread
include a number of special botanical associations
habitats
on a local or regional scale. Third, this species is notable in being dioecious
(Fig. 1), a sexual condition present in an estimated 6 percent of all an?
giosperms (Renner and Ricklefs 1995).
Published accounts of Corema conradii have not comprehensively
gen?
eralized its biology,
although a recent NatureServe
report (2003) for the
species reviews much of what is known. Aside from this report, our current
understanding
of the species
is found
in a widely
scattered
literature
that
'Department of Ecology and Evolutionary Biology, University of Connecticut, Unit
3043, 75 North Eagleville Road, Storrs, CT 06269-3043. 2Science Department,
Florence Township Memorial High School, 500 East Front Street, Florence, NJ
08518. Corresponding author - [email protected].
Vol. 12, No. 3
NortheasternNaturalist
268
details natural history observations,
offers anecdotes, and lacks much quan?
titative data. Our intent is to present information about the biology of this
species and ideas that we hope will serve as an impetus for more careful
quantitative data collection and experimentation.
We begin by discussing the role fire disturbances play in the life history
Post-fire
of Corema conradii.
seedling
emergence
appears to be a key
event in the life cycle of most populations
of this plant, and we next detail
new observations
of seedling emergence from a recently burned population
found in New Jersey. A life cycle model for C. conradii is then presented.
This model is built by synthesizing
scientific studies, natural history obser?
and our own field
vations, ideas from conservation
biology and ecology,
The life cycle model suggests an important role for fire and
observations.
about C. conradii life his?
disturbance; details some facts and hypotheses
and offers some sug?
tory stages, seed dispersal, and sexual reproduction;
gestions about data that can be gathered and examined to test some of our
ideas. Lastly, we outline how the life cycle model can be both tested and
and management
of this species and the habitat
applied to the conservation
in which it occurs.
Fire, Seedling
Germination,
and Adult
Plant Death
Throughout its range, Corema conradii primarily occurs in habitats his?
torically prone to fire (Clemants 1997), such as the low shrub heathlands of
et al. 1996, Sorrie 1987), the dry bogs of Nova
Massachusetts
(Dunwiddie
and Houle 2001), and the Pine Plains of New Jersey
Scotia (Rocheleau
Common associates, such
(Collins and Anderson 1994; Redfield 1884,1889).
as Pinus rigida P. Mill. (Pinaceae) and Arctostaphylos
uva-ursi (L.) Spreng.
(Ericaceae),
are also well-adapted
to fire (Dunwiddie
1990, Givnish
1981).
1. Corema
Figure
conradii
stem and
staminate
inflores?
cence. Illustration by
Rachel
A. Figley,
and
from Martine
Figley (2002).
CT. Martine, D. Lubertazzi, and A. DuBrul
2005
269
of Corema conradii in Isle
Redfield (1884) reported that a population
au Haut, ME, appeared to be almost destroyed by a fire that had occurred
of the site in 1884. Noting that the
a few years before his inspection
he also made the observation
had
extinction,"
narrowly escaped
"plant
that "new sprouts" emerging at this site "gave promise of good increase if
give it fair treatment." This is the first published record of how
plants and whole populations.
seemingly
destroy C. conradii
Redfield's
Stone (1911) later corroborated
accounts with his own obser?
vations, as well as those of other botanists. The mass mortality of adult
botanists
fire
can
evident in areas where C.
plants described by these authors is especially
conradii is abundant and a dominant component of the ground cover. This
is the type of population
that Redfield (1889) published observations
on
when he reported another post-fire seedling emergence
in the
encountered
New
to this account,
a recent fire had
Jersey Pine Plains. According
all of the adult plants in a previously
undocumented
C. conradii
station just west of the village of Cedar Bridge. In their place an abun?
killed
dance
of new seedlings
had arisen. Fire, it seemed, was the antecedent to
a mass, eruptive seed germination
event.
Driven by a concern over the lack of juvenile plants found in a Nantucket
Island, MA, Corema conradii population, Dunwiddie (1990) applied
treatment to a 20- x 20-m plot to test the response of the vegetation to
disturbance.
Adult C. conradii plants represented 61 percent of the
ground cover before the burn and all were killed by a fire treatment in
a fire
a fire
total
April
1987. By July of 1988, the site contained 40 C. conradii seedlings per square
meter. Dunwiddie noted that more seedlings emerged in October of that same
year, but did not provide additional quantitative data.
Nicholson
and Alexander (unpublished
manuscript) examined how the
a
of
seeds
and
of
other
such as scarification of the seed
factors
heating
variety
coat influence germination rates of Corema conradii seeds. Their experiments
revealed no significant treatment effects on seed germination rates. Although
it was not used as an independent treatment by these workers, smoke may be
important in stimulating seed germination in this species (P. Nicholson, Smith
College Botanic Garden, pers. comm.). Aerosol smoke is known to trigger
seed germination in fire-dependent plant species native to Australia and South
Africa (P. Nicholson,
Smith College Botanic Garden, pers. comm.; Roche et
al. 1998; Tieuetal.
2001).
To summarize, populations
of Corema conradii that experience
an in?
tense fire show a number of common responses. One immediate response is
the death of the adult plants. This culling can be so effective
that local
have
to
been
A
populations may appear
extirpated.
longer-term response is
the emergence of many new seedlings in the years immediately
following an
intense
fire. The stimulus that fire provides to cue?or
condition?the
seeds
to germinate is not known. One consequence
of mass mortality in adult
plants and the subsequent emergence of a new cohort of juvenile plants is the
production of uniformly aged subpopulations.
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Vol. 12, No. 3
Fire-driven population dynamics are not unusual for species associated
with landscapes that have evolved with fire. This has been particularly well
documented and studied in fire-prone vegetative associations
from western
Australia and western North America (Whelan 1995). Much work has also
been done by Menges and colleagues
on fire dynamics in the Florida scrub
community
(e.g., Hawkes and Menges 1996, Menges and Kimmich 1996,
et al. 2003), an area similar
Menges and Kohfeldt 1995, Quintana-Ascencio
in ecology
to the New Jersey Pine Barrens. Ceratiola
ericoides
Michx.
the dominant component
of the Rosemary
(Florida rosemary, Ericaceae),
shared with
scrub, is also well studied and exhibits numerous characteristics
the closely
related Corema
conradii (Ceratiola,
Corema, and Empetrum are
some
authors
as
the
three
recognized
by
genera included in Empetraceae,
in
their
inclusion
a
Ericaceae is supported
circumscribed
broadly
although
and
molecular
data
et
al.
2002, Kron et al. 2002,
by morphology
[Anderberg
and references therein]). Like C. conradii, Ceratiola ericoides is a dioecious
shrub with seeds
that germinate only after fires during which adults are
(Gibson and Menges 1994, Johnson 1982). The tendency for fire to
"restart" a population (either by new recruitment through seed
effectively
of established
or the regeneration
germination
plants from below-ground
killed
structures) is a pattern common in the plant communities
conradii is associated (Givnish 1981, Kiviat 1988).
A Contemporary
Observation
with which
of the Impact of Fire on Corema
Pine Plains
C.
in the
New Jersey
The Pine Plains of New Jersey is one of the most extensive pygmy forests
in the world, occurring over two adjacent areas that are locally termed the
West Plains and the East Plains (see page 12-13 in Boyd 1991 for a brief
description of New Jersey Pine Plains localities). Harshberger (1916) coined
the term "coremal"
dwarfed
to describe
the "formation
of stunted, twisted and
C. conradii, Pinus rigida and
(predominantly
Muenchh. [Fagaceae])
associated
with dry, infertile
trees and shrubs"
Quercus marilandica
soil and a history of fires. Givnish (1981) reviewed the natural history of
such as the coremal, in the New Jersey Pine
communities,
fire-dependent
Barrens. Corema conradii occurs in openings in this forest, typically grow?
ing in low, rounded mounds of one or a few individual plants that can reach
over two meters in diameter (C. Martine, pers. observ.).
Several scattered patches of Corema conradii found in the Stafford Forge
Fish and Wildlife Area, which includes portions of the East Plains, were
initially examined in 1996 by C. Martine and A. DuBrul. This area contained
a patchwork of dense dwarf forest with contiguous tree cover, areas where
trees were less densely spaced and did not form a continuous canopy, and
treeless areas of various sizes (from a few meters to tens of meters wide) and
shapes. The latter two types of areas were where C. conradii could be found
growing. In some of the open sites, the species dominated the ground cover,
at least within the limited extent of that particular patch.
2005
CT. Martine, D. Lubertazzi, and A. DuBrul
271
were never encountered
in 1996 or during
Corema conradii seedlings
field visits between
1997 and 2001. In June of 2001, a fire
subsequent
2000 acres of pine plains forest in the Warren
consumed
approximately
Grove Bombing Range and the Stafford Forge Fish and Wildlife Area (W.
Bien, Warren Grove, NJ, pers. comm.). This burn killed many of the adult
C. conradii within the sites where the plants were being monitored. In the
in and around the areas
fall of 2002, we observed
seedlings
emerging
where the adult C. conradii plants had been killed (Fig. 2). This area was
March (2003), and seedling density data were col?
revisited the following
lected in May of that same year.
Methods
Seedling density sampling
Pre-burn monitoring
of the plants was not initially predicated on pre?
a
fire
was
to
suming
pass through this area, nor was this work focused on
seedling germination
questions. The three sampling sites used for seedling
therefore
density sampling
represent areas where we did not quantify any
characteristics.
Dead adult plants are still present and it is not
pre-burn plot
difficult to estimate pre-burn percent coverage of Corema conradii. Each
of the sample sites was an open treeless site (as per the description above).
Site 1 was an area where the dominant pre-fire ground cover was C.
Fig. 2. Cluster of fifteen Corema conradii seedlings ca. 18 months after the fire
(Leaves are 2-3 mm in length). (Photo by D. Lubertazzi.)
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272
Vol. 12, No. 3
with occasional
small gaps. The fire had burned thoroughly
this
as
there
was
a nearly continuous fuel layer on the ground
area,
through
both in and around this plot. In Site 2, C. conradii was less dominant and
there was less available fuel for the fire in the immediate area, but the fire
still burned severely enough to kill all of the adult plants. In Site 3, C.
conradii
conradii
had occurred
as scattered
individuals
and the fire could not have
as intensely
as in Sites 1 and 2 because bare sandy gaps, which
fuel for a fire, were much more prevalent here.
contained no combustible
burned
A 10-m
transect
was set up through each sample site and a 0.25-m2
the
on
quadrat placed
ground at randomly chosen locations along this line.
The following
data were collected
for each sample quadrat: number of
as a cover
Corema conradii seedlings;
percent ground cover (expressed
within the sample; distance of each
value between 0-4) of all constituents
new seedling from the edge of the nearest burned C. conradii mound; and
height, width, and exact location of each seedling. The latter data will be
the
used to track growth and survival of individual plants and, eventually,
of male and female individuals in each population. Maps were
frequencies
drawn and digital photos
were taken of each sample plot.
Results
The pre-burn density of Corema conradii in the Warren Grove, NJ,
burn site was not as dense as the Nantucket population (Dunwiddie
[1990] reported that the plant was the dominant pre-burn cover species).
coremal
was not quantified in our study area, we compared our
data
to
the Nantucket population in two ways (Table 1).
seedling density
One comparison was simply the per plot and the total sample seedling
While this difference
average. The sampling sites represented a range of pre-burn densities be?
to the
tween sample patches. Site 1 is likely the closest approximation
Nantucket population as pre-burn density was relatively high for this patch.
Our small number of
Sites 2 and 3 represent lower pre-burn densities.
replicates and limited sampling (one site for a high, medium, and low prebetween
burn Corema conradii density) do show a positive correlation
seedling density and pre-burn adult density. The seedling data per-plot is
lower than the Nantucket population.
The per-plot and overall seedling data for the coremal was also adjusted by
eliminating quadrats within which no seedlings were found. These samples did
have dead Corema conradii adults in their vicinity, but such quadrats were
generally not as close to, or as surrounded by, dead adults that were likely to
serve as seed sources prior to the burn. Despite this post-hoc adjustment to
between a larger,
allow for a more realistic seedling density comparison
dense cover of pre-burn C. conradii in Nantucket and a more
continuously
patchy, less dominant coverage in the New Jersey coremal, the per plot and
overall seedling densities remain much lower than Dunwiddie's (1990) data.
In most of our samples, the dominant ground cover was either bare sand
or burned Corema conradii mound (each at times exceeding
75 percent of
273
CT. Martine, D. Lubertazzi, and A. DuBrul
2005
L. (Golden-heather,
ericoides
Cistaceae)
although Hudsonia
in some samples,
was
a
notable
from
rootstocks)
component
(resprouting
where it represented as much as 50 percent of the cover. Almost all of the
we encountered
of H.
C. conradii
(as well as new seedlings
seedlings
were in bare sand, with very few found at the edges of burned
ericoides)
the cover),
are similar to reports from the Florida Rose?
mounds. These observations
in gaps
mary Scrub, where post-fire recruitment is typically concentrated
(Hawkes and Menges 1996).
In the fall of 2003, more new Corema conradii seedlings were observed
in our study plots. The fire clearly stimulated seedling germination over two
subsequent years. Non-burned patches in areas near the burned plots remain
are evident in any
the same as they have since 1996. No new seedlings
will continue to
sites
where
conradii
is
We
unburned
C.
presently growing.
in our study plots to track seedling survival and plant
monitor seedlings
growth,
and determine
how long new seedlings
will continue
to appear.
habitat fire recovery
By the summer of 2003, nearly all of the woody species present before
the fire had resprouted from belowground
structures. The most common of
these include Vaccinium pallidum Ait. (Ericaceae),
baccata
Gaylussacia
K. Koch (Ericaceae),
Kalmia latifolia L. (Ericaceae),
Pinus
(Wangenh.)
Coremal
and Hudsonia ericoides. None of the Corema
rigida, Quercus marilandica,
conradii plants we observed ever produced shoots from the rootstocks of
burned plants. Hudsonia ericoides and C. conradii were the only two woody
combination of taxa was
species present as seedlings. This post-disturbance
also witnessed on the Pine Plains by Levin (1966).
As the single species in our study sites to regenerate
post-fire both
and by seed, Hudsonia
ericoides
vegetatively
appeared to be the major
for space with Corema conradii
and had actively
seedlings
areas previously
dominated
by C. conradii adults. Dunwiddie
uva-ursi
was an equally
(1990) found that Arctostaphylos
(Ericaceae)
in study plots in Massachusetts.
He suggested
aggressive
early colonizer
competitor
colonized
that this species
might
dominate
these
sites for some
time while
serving
Table 1. First-yearCorema conradii seedling density data from quadratsplaced randomlyalong
transects through three coremal plots located within the Warren Grove, NJ, June 2001 fire
perimeter.Seedling density is given as the averagenumberof seedlings (total seedlings / n) per0.25
m2 and as an adjustedaverage that excludes quadratswith no seedlings. Seedling emergence data
for a Nantucket population (Dunwiddie 1990) is also listed. The adjusted average is given to
provide a fairer comparison between the New Jersey Pine Plains and Nantucket seedling emer?
gence events (see text).
?
Site 1
Site 2
Site 3
All plots
Nantucket
Seedlings/0.25 m2
7.75
4.00
1.50
n
4
3
4
4.45
11
10.08
38
Adjusted
7.75 (n = 4)
6.00 (n = 2)
3.00 (n = 2)
6.13 (n = 8)
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274
Vol. 12, No. 3
as a nursery species for C. conradii
Plains are a harsh microenvironment
The open sands of the Pine
juveniles.
and seedlings
may benefit from the
protection afforded by nursery plants. Many of the new C. conradii seed?
with H. ericoides
in the bare white sands
lings in our sites co-occur
between burned C. conradii mounds. Here, H. ericoides may perform the
same nursery
Massachusetts
function
that Dunwiddie
(1990)
assigned
to A. uva-ursi
in
plots.
Discussion
Corema
conradii was first discovered
in New Jersey in 1831 by S.W.
an
area
from
once
known
as
Pemberton
Mills. John Torrey returned
Conrad,
to this same station around 1848 in order to collect material with which to
formally describe the species. Because the Pemberton Mills population was
in
by Rafinesque
entirely staminate, Torrey also visited a site discovered
Cedar Bridge where he made collections
of an entirely pistillate population
in which no fruit set was apparent. In the protologue associated with the two
syntypes (Conrad's ca. 1831 Pemberton Mills specimen and Torrey's ca.
1848 Cedar Bridge specimen), Torrey (1848) described the species as occur?
ring in small patches of individual plants. These collection records illustrate
one of the two ways in which plants of this species are distributed across the
landscape. Corema conradii can occur in widely isolated patches that con?
tain a few plants as well as in more expansive aggregations
of many plants.
latter populations
can range from an array of individual plants and
plant clumps spread over a larger area to places where C. conradii is the
dominant species over many hectares.
These
Source-sink
populations
From a metapopulation
small isolated patches of Corema
perspective,
This could have been the
conradii are likely to be small sink populations.
case
at the type locality and may explain why Redfield,
more than 30
after
was
able
to
find
not
collection,
years
Torrey's type
any plants at this
location
best
is
that
the
is
at
the present day
(our
guess
type locality
intersection
of New Jersey state highway 70 and county road 539). Iso?
in other accounts:
Redfield
patches of plants are also recorded
three
...
the
side
the
noted
"two
or
on
of
road ...
(1889:195)
patches
within half a yard of the wheel-track;"
identified
Harshberger (1916:158)
scattered occurrences
"along the road in the Lower Plain;" and Stone
(1911) described various plant patches in his synopsis of the distribution
of the species in New Jersey.
lated
Redfield (1889), revisiting the area around Pemberton Mills a second
time, was able to locate what could be considered a large source population
of Corema conradii. The site description
details a locally abundant and
where
C.
conradii
was a dominant compo?
relatively expansive population
nent of the flora. This and other similar populations (as in Redfield 1884) are
what could serve as the source of seeds for the sink populations.
CT. Martine, D. Lubertazzi, and A. DuBrul
2005
275
structure
and metapopulation
is dioecious, a sexual condition present in only about 6
in the
(Renner and Ricklefs 1995). Pollination
percent of the angiosperms
1990), and clouds of
species is believed to be primarily by wind (Dunwiddie
pollen are shed when one comes into contact with male plants bearing
mature flowers (C. Martine, pers. observ.).
Corema conradii is the first
Sexual
reproduction
Corema conradii
native woody species to bloom in the Pine Plains, and this early flowering
suggests that the pool of potential insect pollinators is limited. In our New
in mid-February
Jersey study sites, we have observed plants flowering
(2004) and mid-March (2003). Dunwiddie (1990) reported flowering occur?
ring as early as January in Nantucket.
The dioecious
sexual system exhibited
by Corema conradii suggests
that small, isolated patches of the species could be subject to some impor?
If a population
is composed
of one or a few
constraints.
is sufficiently
isolated from a larger population,
and contains
A lack of
or females,
plants may not be able to reproduce.
gene flow out of the patch (no pollen reaching female plants outside an
all male patch) or the lack of success in producing
seeds (unfertilized
tant fitness
individuals,
only males
female
flowers in an all female patch) results in zero fitness. The eventual
death of the adult plants in such an area would mark the extirpation of the
occurs, these are sink populations.
patch; because no reproduction
Singlesex sink scenarios,
where reproductive
success cannot occur for lack of
of one or the other sex, have been proposed as paths to local
of other dioecious
plant species (e.g., Nanami et
al. 1999, Osunkoya
and Borges 2000, Traveset et al.
1999, Somanathan
2003, Wilson and Harder 2003).
individuals
extinction
in a number
Harshberger (1916) and Rocheleau
occurrences of monoecy in populations
of
tively. The occasional
expression
Corema conradii individuals
could be
and Houle (2001) reported very rare
in New Jersey and Quebec, respec?
male
and female
flowers
on some
construed
as an adaptive advantage
In the case of C. conradii,
for plants found in small, isolated patches.
however, this appears to be nothing more than an infrequent
stochastic occurrence.
developmental
Seed production,
seed banks, and seed dispersal
In the summer of 2003, we visited a site (39?45'00"N,
74?23'32"W;
hereafter referred to as the Levin study site [it is known locally as the old
FA A Tower site]) described by Levin (1966) that has sustained a vigorous
Corema conradii population for at least 40 years. In this area, C. conradii
mounds currently dominate the ground cover and these plants are separated
from their nearest neighbors by small patches of open sand and/or black tar
lichen (Placynthiella
uliginosa (Schrad.) Coppins & P. James). In July of
we
observed large aggregations
of the small, dry, three-seeded
2003,
drupes
of the species on the ground in the Levin site. Heavy summer rains can cause
sheet flow of water on coastal plain soils and in some areas it was apparent
that the piles of fruits observed were moved there by water; these were either
NortheasternNaturalist
276
in low depressions
mound vegetation
Vol. 12, No. 3
or were located where water had been slowed
by a dam of
and had deposited C. conradii fruits and other detritus.
Fruit piles contained from a few hundred to many thousand fruits.
We are certain that these fruits were more than likely produced by
of the fine litter that accumulates
individuals
at this site. An inspection
the presence of an abun?
of live adult plants indicated?by
were
active females.
Such
plants
reproductively
within
mounds
dance
of fruits ?which
plants were also found to bear a small number of unabscised fruits.
One result of this copious fruit production, provided our observations
from the Levin study site are indicative
of other large Corema conradii
can be the formation of a seed bank that is stored in situ
populations,
(Dunwiddie
1990). This store of seed can allow for the recruitment of new
individuals into the population, lead to an increase of the plant's dominance
of seed dispersal, and, most
in a site through simple diffusion processes
a
new
serve
as
source
of
ready
seedlings if the adults are killed
importantly,
work
seed
a
disturbance.
More
examining
production is needed to deter?
by
mine the spatial and temporal arrangement of seeds found in the litter and
soil where large populations of C. conradii exist.
The abundant production
of many small fruits also provides greater
opportunity for at least some propagules to be dispersed out of the popula?
tion by environmental
agents. Strong winds and heavy rains could easily
transport the small drupes a number of meters from sites where seeds are
Although many of these seeds may never find a suitable site to
new plants a short distance
germinate, a few may succeed in establishing
the
boundaries
of
the
beyond
original population. In some instances, when
a number of fruits and seeds are carried to the same suitable place by
produced.
runoff, a cluster of plants growing in the
prevailing winds or down-slope
same place can be produced, expanding the population or creating nearby
browse on C. conradii and could potentially
outliers. Deer occasionally
agents such as horse hooves, car?
disperse seeds locally. Anthropogenic
wheels and vehicle tire treads appear to have been long-distance
dispersal agents for C. conradii as well, apparently moving fruits and seeds
This conjecture is based
from source populations.
over several kilometers
riage
on the many small isolated patches or individuals
plants of C. conradii
documented
historically
along sand roads extending kilometers beyond the
Pine Plains (Windisch 1998).
Myrmechochory
may also play an important role in the dispersal?and
Corema conradii seeds. The fruits of C. conradii
germination?of
perhaps
are unlike those produced by its only congener, Corema album (L.) D. Don
endemic of the west coast of the Iberian
an endangered
(Empetraceae),
et al. 2000, Guitian et al.
Peninsula (Calvino-Cancela
2002, Diaz-Barradas
1997), in that they are not only "scarcely larger than a pin-head" (Mathews
1915) but devoid of the fleshiness associated with bird dispersal. The fruits
do bear elaisomes
(fleshy or oily appendages typically associated with ant
and ants of the Aphaenogaster
rudis Emery species
however,
dispersal),
2005
CT. Martine, D. Lubertazzi, and A. DuBrul
277
complex have been observed in Nantucket, Massachusetts
transporting, stor?
and
C.
conradii
fruits
The
investment by
(Dunwiddie
ing,
1990).
discarding
the plant in elaisomes suggests there is some fitness advantage to be realized
by the plant for this energy expenditure, or these structures would otherwise
not be produced (Beattie
evidence
for
1985, Rickson
1977). Definitive
short-distance
fruit/seed dispersal by ants is yet to be found, as is evidence
that C. conradii possesses
a non-anthropogenic
method for long-distance
dispersal. Traits allowing for wide dispersal are typically present in dioe?
cious species (Wilson and Harder 2003, Yampolsky
and Yampolsky
1922).
The larger, more fleshy fruits of the dioecious Corema album are known to
be moved over long distances by sea gulls and other birds (Calvino-Cancela
2002). No such evidence exists for the same mechanism in C. conradii.
In July 2003, we observed minor workers of the ant species Pheidole
davisi Wheeler collecting pieces of Corema conradii leaves and transporting
them into a soil nest entrance at the Levin site. Collection of C. conradii leaf
material
by ants has not been previously reported, and the reasons behind it
are unclear. Many fruits were found scattered about the nest entrance and it
was not clear if these were discarded from the nest or if these had been
brought to the nest entrance, but never brought into the nest. Digging into
this nest revealed
two fruits and a few pieces of leaf material a few centime?
ground. The P. davisi nest entrance was quite diffuse and no
or any workers were found while digging in this spot. Similar nest
ters below
colony
entrances
and fruit arrangements
were also observed
at the Levin site during
this same visit.
is likely to play a role in the successful
Myrmecochory
germination of
some seeds that survive to become reproductive
adults, but it is not known
how dependent
Corema conradii is on this mode of seed dispersal and
It should be noted that elaisomes do not need to confer fitness
germination.
benefits
that are always realized nor does this structure need to contain a cue
a specific ant species to move its fruits (Beattie 1985). It
that stimulates
could be that such a structure simply increases the probability that a seed is
brought to another place and this movement either leads to increased germi?
nation rates or improves seedling growth in the environment
the seed is
moved to. Being moved underground may be an important component, along
with fire/disturbance,
of successful seed germination. Ants might also even?
tually place the fruits in ant waste dumps where nutrient levels are higher
relative to the surrounding soil.
It is now known that two different ant species in two different locations
will move Corema conradii
fruits. This interaction
needs to be better
studied within and among sites in different geographical
areas. Neither the
Pheidole
species we observed in New Jersey nor the Aphaenogaster
spe?
cies in Massachusetts
occur in the northern range of C. conradii. It would
also be interesting
to examine
if elaisome
and morphology
production
differ throughout the range of this plant and if the variation is correlated
with particular ant species.
Vol. 12, No. 3
NortheasternNaturalist
278
Disturbance
Corema conradii is known to respond to fire by
number of new seedlings. Mechanical disturbance is also
a germination response (Levin 1966). In the summer of
new seedlings emerging in tire tracks that had been made
a large
producing
known to stimulate
2003, we observed
at the Levin site. It
to imagine that a species that thrives in the heath-like open?
favors could possess seeds that have become adapted
that
C.
conradii
ings
for germination in disturbed, open areas. Both fire and mechanical distur?
is not difficult
bance appear to trigger germination.
Demography
Only one published study (Rocheleau
of a Corema
examined the demography
and Houle
2001)
has specifically
The Quebec
population.
that the mean age of nonproductive
conradii
show
they investigated
populations
adult plants was ca. 6 years, that reproductive plants averaged ca. 16 years of
age, and the oldest individuals in the population were close to 40 years old.
Dunwiddie (1990) estimated that the oldest plants in his Nantucket popula?
tion were around the same age, or older. Zaremba (1984), based on rates of
annual shoot growth and woody tissue production, estimated the lifespan of
at about 50 years. Since individual plants can live this long, a
sink population where the adult plants are not killed by a disturbance can be
extant for half a century.
C. conradii
The life cycle model
and hypotheses
The facts, observations,
presented can be synthesized
into a life cycle model for this plant (Fig. 3). The cycle begins with the
germination of new seeds following a disturbance.
Seeds of Corema conradii generally germinate in sandy, nutrient poor
soils. At a finer microhabitat level, germination is also favored by a recent
disturbance.
While fire is known to precede the highest field-population
and Alexander,
rate (Nicholson
seed germination
unpubl. data), it is not
clear what elements of a burn provide the stimulus for seeds to initiate
After a fire, there is an initial delay before seeds germinate.
were
not apparent in our sites until the fall of 2002, about 20
Seedlings
months after the fire. It is not known if seeds are dormant after being cued to
grow, if this lag time is spent in producing root structures, or if this time is
possibly divided between latent periods of no growth and time where active
germination.
is occurring. Observations
root or shoot?development
well as examination
in
our
New
site?as
Jersey study
seedlings
in
collected
Redfield
1889
(CONN #127343)-revealed
by
meristem?either
first-year
of
of
di?
seedlings
minutive above-ground
systems that
systems supported by below-ground
were generally deeply rooted with numerous branches. Root system forma?
tion appears to be an important and early step in seedling establishment.
Once a seedling is established,
it begins the growth phase. This juvenile
is
a
Adult
stage
perilous period.
plants can occur at a density of 1-3
individuals per m2; if this is compared with an initial 30-40 seedlings per m2
2005
CT. Martine, D. Lubertazzi, and A. DuBrul
279
1990, this study) then more than 90 percent of the seedlings can
(Dunwiddie
perish in this stage.
Successful
seedlings
ramify and spread, extending their branches both
outward and upward from a single, central stem. Vertical growth reached a
maximum height of ca. 50 cm in populations
studied by Rocheleau
and
Houle (2001), although this may be a site-dependent
character. Other popu?
lations of C. conradii maintain lower maximum heights (e.g., Nantucket: ca.
30 cm, Dunwiddie
1990). Horizontal growth usually does not exceed more
than 3-5 m in diameter (Zaremba 1984).
The spreading habit of the maturing plant is supported by adventitiously
of
rooting stems that contribute to the formation of a mound consisting
of this
living stems, a fibrous root mass, and leaf litter. The establishment
mound may be crucial to the success of an individual. Mounds consist of a
dense configuration
of overlapping
and intertwined branches that trap and
collect
organic
material
shed by the plant, as well as organic
matter and soil
Fig. 3. Life cycle model for Corema conradii in the New Jersey Pine Plains. Bold
arrows trace the course of an idealized single-population cycle in which disturbance
occurs following seed bank build-up, thereby killing adult plants and triggering a
mass replacement germination of seedlings. Deviations from this cycle might include
a) Major disturbance during the juvenile growth stage prior to seed bank build-up,
leading to local extirpation without replacement; b) Export of seeds to form a new
seed bank facing the same possibilities as that of the source population; and c)
Absence of major disturbance, leading to a lack of disturbance-induced replacement
as adults eventually senesce and die.
NortheasternNaturalist
280
external
Vol. 12, No. 3
to the plant that is delivered via wind and water. This litter accumu?
its decomposition
serve a number of eco?
through time?may
roles. For example, it may influence nutrient dynamics, attract ants,
lation?and
logical
and/or prevent other seeds from germinating in the mound. This detritus may
a competitor exclusion
also play a role in allelopathy,
strategy reported in
the closely related Ceratiola
ericoides
(Fischer et al. 1994). As per our
and is
model, the growth stage lasts from 5-10 years after germination
by the reproductive stage.
begins when flowers
Reproduction
followed
Plants of Corema
are produced.
are still growing during this stage, but it is unclear how growth
rates differ between this stage and the growth stage identified above (the
The transition from the growth
period of growth without reproduction).
stage to the reproductive stage may be initiated because of the size of a plant,
conradii
a variably expressed genetic
bination of these factors.
timing mechanism,
the environment,
or a com?
The reproductive stage lasts for about 10-25 years or more, depending on
how open the habitat remains and perhaps range-wide genotypic variation.
For example, abundant fruit production continued at the very open Levin site
distur?
at least 40 years ago after severe mechanical
in plants established
active Corema conradii individuals
bance (Windisch 1998). Reproductively
produce a profusion of flowers, and female plants can produce an abundance
of fruits. It is not known if plants produce flowers every year during the
reproductive stage.
Plants are thought
to enter senescence
25 and 35 years of age
later in very open, sandy sites
between
1990, Zaremba 1984), perhaps
(Dunwiddie
with little or no woody competition (Windisch 1998). In the senescent stage,
can occur earlier where woody
slows or ceases. Senescence
reproduction
is greater (Windisch
1998). In the absence of a large distur?
competition
bance, plants may persist in this final stage for more than two decades.
Branches die off in the center of the mound while new growth continues to
be formed only on the periphery. This leads to the formation of a ring of
living stems around a central dead patch that slowly increases in size over
of many years; the same pattern is exhibited
by Ceratiola
in Rosemary scrub in the absence of disturbance (C. Martine, pers.
observ.). Although flower and fruit production continue at a reduced rate
during this phase, it is not known how tightly coupled the decline of repro?
are.
duction and the beginning of senescence
The extended senescent stage may be cut short by a very high intensity
the course
ericoides
or poorly performing
fire, an event that can kill all or most non-reproductive
fruits
at
reduced
still producing
adults (individuals
rates) and clear the way
to
suitable
conditions afterwards.
for a new cohort of seedlings
emerge given
in
in
such
as
the June 2001 fire
fires
pine plains,
Very high intensity
in
after
three
or
more
decades of fire
this
occur
analyzed
study, typically
exclusion (Windisch 1998). If a fire regenerates a new cohort of plants in a
population, it is not clear what happens if that population is again struck by a
2005
CT. Martine, D. Lubertazzi, and A. DuBrul
281
fire before
plants mature, set seed, and replenish the seed bank. Because
conradii plants do not resprout from their roots, two high intensity
fires within a decade could eliminate
a population
that has not reached
Post-fire
or
reproductive
maturity.
drought
subsequent intense fires might
limit seedling recruitment in some cases. The expansive C. conradii popula?
tion west of Cedar Bridge described by Redfield (1889) is now largely gone
Corema
(New Jersey Natural Heritage Database [unpublished]),
suggesting the tenu?
ous nature of seedling recovery after an intense population-replacing
fire
(Windisch 1998).
The New Jersey Pine Plains historically
burned at about 10-year inter?
vals on average (Lutz 1934) during Redfield's
era when Corema conradii
was much
more abundant. Short fire intervals such as this produce less
mixed intensity
fires that allow greater survival
of adult C.
severe,
conradii plants in open sandy microsites,
as well as the creation or expan?
sion of open habitats that allow recruitment
of C. conradii
from seed
banks (Windisch
Corema
1998).
conradii
biology
conradii favors
Corema
disturbed
habitats
and can thrive in the sandy,
coast of North
nutrient-poor soils found within and around the northeastern
America. Where it becomes established
as a reproductive
conradii
populations
serves as
disturbance
seeds
C.
population,
locally dominant. Copious seed production by local
leads to the build-up of a localized
seed bank. This resource
a means of regenerating
a vigorous new cohort of plants when
occurs, and also serves as a source for anthropogenicly
exported
can lead to the formation of new small populations
or isolated
can become
that
in C.
plants along sand roads. Natural long-distance
dispersal mechanisms
conradii have not been demonstrated to date. Seeds germinating away from
the source population are probably more likely to form small sink popula?
tions than to form a new source population.
One interesting aspect of the disjunct distribution of Corema conradii is
the potential change in associated
ant species that may occur in moving
northward from New Jersey to Quebec. These changes could be associated
with differences
in elaisome structures, their chemical constituents,
or the
level of investment in ant food rewards among different populations.
Flow?
should also vary substantially
across the range of the
ering phenology
species. The most intriguing differences
may be found in the populations
occurring on the Shawangunk Ridge in Ulster County, NY?the
only local?
ity known for this species that is not on the Atlantic Coastal Plain.
Management
In most
Corema
parts of its range,
conradii has a limited
political boundaries, meaning
rare habitats or state/provincial
Recommendations
this
concern.
species is of conservation
distribution
within the confines of some
the species is potentially at risk within some
management boundaries.
282
NortheasternNaturalist
Vol. 12, No. 3
behind Dunwiddie's
A particular motivation
study (1990), as well as
ongoing work near his site (R. Freeman, Nantucket Conservation Foundation,
pers. comm.), was the advanced age of most plants found in the Nantucket
populations, coupled with a dearth of new recruitment associated with histori?
cal fire suppression. Human-induced
changes in disturbance regimes, like the
can
have negative consequences
of
fire
on
for the
Nantucket,
suppression
of
of
disturbance-dependent
species (Quintanapersistence
populations
et al. 2003, and references
Ascencio and Menges 1996, Quintana-Ascencio
therein). The solution proposed on Nantucket was to reestablish the fire
ecology of the area with a controlled burning program. Our feeling is that an
effective fire management program should include careful research and postfire monitoring to better understand the life cycle of the species. Our model
represents a general outline of the life history of this plant and points out the
many holes existing in our understanding of even the basic biology of this plant.
Burning of any Corema conradii sites should occur in a piecemeal, rather
than wholesale, manner. Burning parts of a population or site over a number
of years, rather than a full scale burning effort at one time, is likely to lead to
a better understanding
of the interactions among the plants, seedling emer?
gence, and fire. This will also mitigate the negative influence of burns that,
for whatever reason, do not lead to an abundant recruitment event. Many of
were also reached by both Zaremba (1984) and Dunwiddie
these conclusions
(1990), and are ideas strongly supported by our life cycle model.
In New Jersey and New York, where Corema conradii is endangered,
concern about the species has perhaps been centered more on the overall
In both states, the
rarity of the species rather than its lack of regeneration.
species is limited to a few stable populations containing either an abundance
of plants or an abundance of groups of plants. Corema conradii is abundant
enough locally that it is a dominant cover plant within some of these areas.
In the past, according to the early natural history notes about this plant,
a greater number of sites for Corema
Jersey appeared to possess
contained
It appears that many of these localities
conradii.
only a few
individuals
or isolated plants along sand roads, suggesting
anthropogenic
dispersal mechanisms; the decline of such occurrences is consistent with our
New
model. The real concern is the status of the
source-sink
metapopulation
extant, major source populations. Because major areas of the Pine Plains that
support extant populations of C. conradii have not burned for 30 to 60 years,
most populations are at risk for exposure to high intensity wildfire and the
high mortality and uncertain recruitment responses associated with it. Man?
agement should be designed to maintain the rare Pine Plains community and
most of the existing C. conradii plants while stimulating new recruitment by
treat?
using controlled mixed intensity prescribed burning and mechanical
ments to reduce fuel loads and restore historic fire regimes (Windisch 1998).
Mechanical creation of clusters of small, sandy openings peripheral to the C.
conradii population can also be done to establish new habitats for coloniza?
tion, expand the population boundary, and reduce the risk of high intensity
2005
CT. Martine, D. Lubertazzi, and A. DuBrul
283
fire (Windisch
1998). It is also important to continue to monitor and study
to learn more about the reproductive
of this
populations
biology
the
and
of
seed
banks
the
to
various
species, including
longevity
response
these
of rare taxa
1998). Management
regimes (Windisch
and
of
seed
genetics,
dispersal, and
requires understanding
breeding biology
et al. 2002,
survival, and establishment
(Anderson
seedling recruitment,
Crawford et al. 2001, Schemske et al. 1994). We plan to continue our work
in the New Jersey Pine Plains to test the ideas presented here with hope that
fire and disturbance
these larger, southernmost
populations
to not only survive, but to thrive.
of this fascinating
species
continue
Ackowledgments
We thank Walter Bien, Justin Smith, Nathan Figley, Bill Figley, and R. Peter
DuBrul for field assistance as well as Robynn Shannon, Greg Anderson, Kevin
Bardelski, Rachael Freeman, Paul Neal, Brigid O'Donnell, Krissa Skogen, Walt
Bien, Andrew Windisch, and an anonymous reviewer for helpful discussion and/or
editorial comments. Funding was provided by the Russell and Betty DeCoursey,
James A. Slater, and Lawrence R. Penner Funds to the Department of Ecology and
Evolutionary Biology and The Connecticut State Museum of Natural History. We
appreciate the New Jersey Air National Guard's 177th Fighter Wing for granting
access to sites within the boundaries of the Warren Grove Range, Bass River
Township. With each step in the sand and each observation committed to paper, we
are further connected and indebted to the likes of J. Torrey, N.L. Britton, J.H.
Redfield, J.W. Harshberger, and W. Stone.
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