Post-fire Seedling Recruitment Christopher T. Martine1 ...lubertazzi/files/Martine et al....
Transcript of Post-fire Seedling Recruitment Christopher T. Martine1 ...lubertazzi/files/Martine et al....
2005 NORTHEASTERN NATURALIST 12(3):267-286
The Biology of Corema conradii:
Natural History, Reproduction, and Observations of a
Post-fire Seedling Recruitment
Christopher T. Martine1'*, 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
Corema conradii (Torr.) Torr. ex Loud, (broom-crowberry, Ericaceae) has attracted attention from botanists because it exhibits a number of curious
characteristics. First and most importantly, it is locally rare. This low-
growing, evergreen, woody shrub occurs in small disjunct populations dis?
tributed across an area that stretches from Newfoundland to the New Jersey Coastal Plain (Clemants 1997). Although the species has a global heritage rank of G4 (uncommon but not rare), it is listed as SI (endangered) in New
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?
tion of areas that share some interesting and peculiar characteristics. These
habitats are generally heath-like, on dry, upland soils, and collectively include a number of special botanical associations that are not widespread 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].
268 Northeastern Naturalist Vol. 12, No. 3
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
of Corema conradii. Post-fire 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?
vations, ideas from conservation biology and ecology, and our own field
observations. The life cycle model suggests an important role for fire and
disturbance; details some facts and hypotheses about C. conradii life his?
tory stages, seed dispersal, and sexual reproduction; and offers some sug?
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
applied to the conservation and management of this species and the habitat
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
Massachusetts (Dunwiddie et al. 1996, Sorrie 1987), the dry bogs of Nova
Scotia (Rocheleau and Houle 2001), and the Pine Plains of New Jersey (Collins and Anderson 1994; Redfield 1884,1889). Common associates, such
as Pinus rigida P. Mill. (Pinaceae) and Arctostaphylos uva-ursi (L.) Spreng. (Ericaceae), are also well-adapted to fire (Dunwiddie 1990, Givnish 1981).
Figure 1. Corema conradii stem and staminate inflores? cence. Illustration by Rachel A. Figley, from Martine and
Figley (2002).
2005 CT. Martine, D. Lubertazzi, and A. DuBrul 269
Redfield (1884) reported that a population of Corema conradii in Isle
au Haut, ME, appeared to be almost destroyed by a fire that had occurred
a few years before his inspection of the site in 1884. Noting that the
"plant had narrowly escaped extinction," he also made the observation
that "new sprouts" emerging at this site "gave promise of good increase if
botanists give it fair treatment." This is the first published record of how
fire can seemingly destroy C. conradii plants and whole populations. Stone (1911) later corroborated Redfield's accounts with his own obser?
vations, as well as those of other botanists. The mass mortality of adult
plants described by these authors is especially evident in areas where C.
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 encountered in the
New Jersey Pine Plains. According to this account, a recent fire had
killed 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?
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 a fire
treatment to a 20- x 20-m plot to test the response of the vegetation to a fire
disturbance. Adult C. conradii plants represented 61 percent of the total
ground cover before the burn and all were killed by a fire treatment in 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
heating of seeds and a variety of other factors such as scarification of the seed
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
populations may appear to have been extirpated. A 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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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,
Menges and Kohfeldt 1995, Quintana-Ascencio et al. 2003), an area similar
in ecology to the New Jersey Pine Barrens. Ceratiola ericoides Michx.
(Florida rosemary, Ericaceae), the dominant component of the Rosemary scrub, is also well studied and exhibits numerous characteristics shared with
the closely related Corema conradii (Ceratiola, Corema, and Empetrum are
recognized by some authors as the three genera included in Empetraceae,
although their inclusion in a broadly circumscribed Ericaceae is supported
by morphology and molecular data [Anderberg et al. 2002, Kron et al. 2002, and references therein]). Like C. conradii, Ceratiola ericoides is a dioecious
shrub with seeds that germinate only after fires during which adults are
killed (Gibson and Menges 1994, Johnson 1982). The tendency for fire to
effectively "restart" a population (either by new recruitment through seed
germination or the regeneration of established plants from below-ground
structures) is a pattern common in the plant communities with which C.
conradii is associated (Givnish 1981, Kiviat 1988).
A Contemporary Observation of the Impact of Fire on Corema in the
New Jersey Pine Plains
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" to describe the "formation of stunted, twisted and
dwarfed trees and shrubs" (predominantly C. conradii, Pinus rigida and
Quercus marilandica Muenchh. [Fagaceae]) associated with dry, infertile
soil and a history of fires. Givnish (1981) reviewed the natural history of
fire-dependent communities, such as the coremal, in the New Jersey Pine
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
Corema conradii seedlings were never encountered in 1996 or during
subsequent field visits between 1997 and 2001. In June of 2001, a fire
consumed approximately 2000 acres of pine plains forest in the Warren
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
fall of 2002, we observed seedlings emerging in and around the areas
where the adult C. conradii plants had been killed (Fig. 2). This area was
revisited the following March (2003), and seedling density data were col?
lected in May of that same year. Methods
Seedling density sampling Pre-burn monitoring of the plants was not initially predicated on pre?
suming a fire was to pass through this area, nor was this work focused on
seedling germination questions. The three sampling sites used for seedling
density sampling therefore represent areas where we did not quantify any
pre-burn plot characteristics. Dead adult plants are still present and it is not
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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conradii with occasional small gaps. The fire had burned thoroughly
through this area, as there was a nearly continuous fuel layer on the ground 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 had occurred as scattered individuals and the fire could not have
burned as intensely as in Sites 1 and 2 because bare sandy gaps, which
contained no combustible fuel for a fire, were much more prevalent here.
A 10-m transect was set up through each sample site and a 0.25-m2
quadrat placed on the ground at randomly chosen locations along this line.
The following data were collected for each sample quadrat: number of
Corema conradii seedlings; percent ground cover (expressed as a cover
value between 0-4) of all constituents within the sample; distance of each
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
used to track growth and survival of individual plants and, eventually, the
frequencies of male and female individuals in each population. Maps were
drawn and digital photos were taken of each sample plot.
Results
The pre-burn density of Corema conradii in the Warren Grove, NJ, coremal burn site was not as dense as the Nantucket population (Dunwiddie
[1990] reported that the plant was the dominant pre-burn cover species). While this difference was not quantified in our study area, we compared our
seedling density data to the Nantucket population in two ways (Table 1). One comparison was simply the per plot and the total sample seedling
average. The sampling sites represented a range of pre-burn densities be?
tween sample patches. Site 1 is likely the closest approximation to the
Nantucket population as pre-burn density was relatively high for this patch. Sites 2 and 3 represent lower pre-burn densities. Our small number of
replicates and limited sampling (one site for a high, medium, and low pre- burn Corema conradii density) do show a positive correlation between
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
allow for a more realistic seedling density comparison between a larger,
continuously dense cover of pre-burn C. conradii in Nantucket and a more
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
2005 CT. Martine, D. Lubertazzi, and A. DuBrul 273
the cover), although Hudsonia ericoides L. (Golden-heather, Cistaceae)
(resprouting from rootstocks) was a notable component in some samples, where it represented as much as 50 percent of the cover. Almost all of the
C. conradii seedlings we encountered (as well as new seedlings of H.
ericoides) were in bare sand, with very few found at the edges of burned
mounds. These observations are similar to reports from the Florida Rose?
mary Scrub, where post-fire recruitment is typically concentrated in gaps
(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
the same as they have since 1996. No new seedlings are evident in any unburned sites where C. conradii is presently growing. We will continue to
monitor seedlings in our study plots to track seedling survival and plant
growth, and determine how long new seedlings will continue to appear.
Coremal 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), Gaylussacia baccata
(Wangenh.) K. Koch (Ericaceae), Kalmia latifolia L. (Ericaceae), Pinus
rigida, Quercus marilandica, and Hudsonia ericoides. None of the Corema
conradii plants we observed ever produced shoots from the rootstocks of
burned plants. Hudsonia ericoides and C. conradii were the only two woody
species present as seedlings. This post-disturbance combination of taxa was
also witnessed on the Pine Plains by Levin (1966). As the single species in our study sites to regenerate post-fire both
vegetatively and by seed, Hudsonia ericoides appeared to be the major
competitor for space with Corema conradii seedlings and had actively colonized areas previously dominated by C. conradii adults. Dunwiddie
(1990) found that Arctostaphylos uva-ursi (Ericaceae) was an equally
aggressive early colonizer in study plots in Massachusetts. He suggested that this species might dominate these sites for some time while serving
Table 1. First-year Corema conradii seedling density data from quadrats placed randomly along transects through three coremal plots located within the Warren Grove, NJ, June 2001 fire perimeter. Seedling density is given as the average number of seedlings (total seedlings / n) per 0.25 m2 and as an adjusted average that excludes quadrats with 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).
? Seedlings/0.25 m2 n Adjusted Site 1 7.75 4 7.75 (n = 4) Site 2 4.00 3 6.00 (n = 2) Site 3 1.50 4 3.00 (n = 2) All plots 4.45 11 6.13 (n = 8) Nantucket 10.08 38
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as a nursery species for C. conradii juveniles. The open sands of the Pine
Plains are a harsh microenvironment and seedlings may benefit from the
protection afforded by nursery plants. Many of the new C. conradii seed?
lings in our sites co-occur with H. ericoides in the bare white sands
between burned C. conradii mounds. Here, H. ericoides may perform the
same nursery function that Dunwiddie (1990) assigned to A. uva-ursi in
Massachusetts plots.
Discussion
Corema conradii was first discovered in New Jersey in 1831 by S.W.
Conrad, from an area once known as Pemberton Mills. John Torrey returned
to this same station around 1848 in order to collect material with which to
formally describe the species. Because the Pemberton Mills population was
entirely staminate, Torrey also visited a site discovered by Rafinesque in
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. These 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.
Source-sink populations From a metapopulation perspective, small isolated patches of Corema
conradii are likely to be small sink populations. This could have been the
case at the type locality and may explain why Redfield, more than 30
years after Torrey's type collection, was not able to find any plants at this
location (our best guess is that the type locality is at the present day intersection of New Jersey state highway 70 and county road 539). Iso?
lated patches of plants are also recorded in other accounts: Redfield
(1889:195) noted "two or three patches ... on the side of the road ...
within half a yard of the wheel-track;" Harshberger (1916:158) identified
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. 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
relatively expansive population where C. conradii was a dominant compo? 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.
2005 CT. Martine, D. Lubertazzi, and A. DuBrul 275
Sexual reproduction and metapopulation structure
Corema conradii is dioecious, a sexual condition present in only about 6
percent of the angiosperms (Renner and Ricklefs 1995). Pollination in the
species is believed to be primarily by wind (Dunwiddie 1990), and clouds of
pollen are shed when one comes into contact with male plants bearing mature flowers (C. Martine, pers. observ.). Corema conradii is the first
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
Jersey study sites, we have observed plants flowering in mid-February
(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? tant fitness constraints. If a population is composed of one or a few
individuals, is sufficiently isolated from a larger population, and contains
only males or females, plants may not be able to reproduce. A lack of
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 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
patch; because no reproduction occurs, these are sink populations. Single- sex sink scenarios, where reproductive success cannot occur for lack of
individuals of one or the other sex, have been proposed as paths to local
extinction in a number of other dioecious plant species (e.g., Nanami et
al. 1999, Osunkoya 1999, Somanathan and Borges 2000, Traveset et al.
2003, Wilson and Harder 2003).
Harshberger (1916) and Rocheleau and Houle (2001) reported very rare
occurrences of monoecy in populations in New Jersey and Quebec, respec?
tively. The occasional expression of male and female flowers on some
Corema conradii individuals could be construed as an adaptive advantage for plants found in small, isolated patches. In the case of C. conradii,
however, this appears to be nothing more than an infrequent developmental stochastic occurrence.
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
2003, we observed large aggregations of the small, dry, three-seeded 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
276 Northeastern Naturalist Vol. 12, No. 3
in low depressions or were located where water had been slowed by a dam of
mound vegetation 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 individuals at this site. An inspection of the fine litter that accumulates
within mounds of live adult plants indicated?by the presence of an abun?
dance of fruits ?which plants were reproductively active females. Such
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
populations, can be the formation of a seed bank that is stored in situ
(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
in a site through simple diffusion processes of seed dispersal, and, most
importantly, serve as a ready source of new seedlings if the adults are killed
by a disturbance. More work examining seed production is needed to deter?
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
produced. Although many of these seeds may never find a suitable site to
germinate, a few may succeed in establishing new plants a short distance
beyond the boundaries of the original population. In some instances, when
a number of fruits and seeds are carried to the same suitable place by
prevailing winds or down-slope runoff, a cluster of plants growing in the
same place can be produced, expanding the population or creating nearby outliers. Deer occasionally browse on C. conradii and could potentially
disperse seeds locally. Anthropogenic agents such as horse hooves, car?
riage wheels and vehicle tire treads appear to have been long-distance
dispersal agents for C. conradii as well, apparently moving fruits and seeds
over several kilometers from source populations. This conjecture is based
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
perhaps germination?of Corema conradii seeds. The fruits of C. conradii
are unlike those produced by its only congener, Corema album (L.) D. Don
(Empetraceae), an endangered endemic of the west coast of the Iberian
Peninsula (Calvino-Cancela 2002, Diaz-Barradas et al. 2000, Guitian et al.
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
dispersal), however, and ants of the Aphaenogaster rudis Emery species
2005 CT. Martine, D. Lubertazzi, and A. DuBrul 277
complex have been observed in Nantucket, Massachusetts transporting, stor?
ing, and discarding C. conradii fruits (Dunwiddie 1990). The investment by 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 1985, Rickson 1977). Definitive evidence for
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?
ters below ground. The P. davisi nest entrance was quite diffuse and no
colony or any workers were found while digging in this spot. Similar nest entrances and fruit arrangements were also observed at the Levin site during this same visit.
Myrmecochory is likely to play a role in the successful 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
germination. It should be noted that elaisomes do not need to confer fitness benefits that are always realized nor does this structure need to contain a cue
that stimulates a specific ant species to move its fruits (Beattie 1985). It
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 production and morphology differ throughout the range of this plant and if the variation is correlated with particular ant species.
278 Northeastern Naturalist Vol. 12, No. 3
Disturbance
Corema conradii is known to respond to fire by producing a large number of new seedlings. Mechanical disturbance is also known to stimulate
a germination response (Levin 1966). In the summer of 2003, we observed
new seedlings emerging in tire tracks that had been made at the Levin site. It
is not difficult to imagine that a species that thrives in the heath-like open?
ings that C. conradii favors could possess seeds that have become adapted for germination in disturbed, open areas. Both fire and mechanical distur?
bance appear to trigger germination.
Demography
Only one published study (Rocheleau and Houle 2001) has specifically examined the demography of a Corema conradii population. The Quebec
populations they investigated show that the mean age of nonproductive 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
C. conradii 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.
The life cycle model
The facts, observations, and hypotheses 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 seed germination rate (Nicholson and Alexander, unpubl. data), it is not
clear what elements of a burn provide the stimulus for seeds to initiate
germination. After a fire, there is an initial delay before seeds germinate.
Seedlings were not apparent in our sites until the fall of 2002, about 20
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
meristem?either root or shoot?development is occurring. Observations of
first-year seedlings in our New Jersey study site?as well as examination of
seedlings collected by Redfield in 1889 (CONN #127343)-revealed di?
minutive above-ground systems supported by below-ground systems that
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
stage is a perilous period. Adult 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
(Dunwiddie 1990, this study) then more than 90 percent of the seedlings can
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
rooting stems that contribute to the formation of a mound consisting of
living stems, a fibrous root mass, and leaf litter. The establishment of this
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.
280 Northeastern Naturalist Vol. 12, No. 3
external to the plant that is delivered via wind and water. This litter accumu?
lation?and its decomposition through time?may serve a number of eco?
logical roles. For example, it may influence nutrient dynamics, attract ants, and/or prevent other seeds from germinating in the mound. This detritus may also play a role in allelopathy, a competitor exclusion strategy reported in
the closely related Ceratiola ericoides (Fischer et al. 1994). As per our
model, the growth stage lasts from 5-10 years after germination and is
followed by the reproductive stage.
Reproduction begins when flowers are produced. Plants of Corema
conradii are still growing during this stage, but it is unclear how growth rates differ between this stage and the growth stage identified above (the
period of growth without reproduction). The transition from the growth
stage to the reproductive stage may be initiated because of the size of a plant, a variably expressed genetic timing mechanism, the environment, or a com?
bination of these factors.
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
in plants established at least 40 years ago after severe mechanical distur?
bance (Windisch 1998). Reproductively active Corema conradii individuals
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 between 25 and 35 years of age
(Dunwiddie 1990, Zaremba 1984), perhaps later in very open, sandy sites
with little or no woody competition (Windisch 1998). In the senescent stage,
reproduction slows or ceases. Senescence can occur earlier where woody
competition is greater (Windisch 1998). In the absence of a large distur?
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
the course of many years; the same pattern is exhibited by Ceratiola
ericoides 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? duction and the beginning of senescence are.
The extended senescent stage may be cut short by a very high intensity
fire, an event that can kill all or most non-reproductive or poorly performing adults (individuals still producing fruits at reduced rates) and clear the way for a new cohort of seedlings to emerge given suitable conditions afterwards.
Very high intensity fires in pine plains, such as in the June 2001 fire
analyzed in this study, typically occur after three or more decades of fire
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
Corema conradii plants do not resprout from their roots, two high intensity fires within a decade could eliminate a population that has not reached
reproductive maturity. Post-fire drought or 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 (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
severe, mixed intensity fires that allow greater survival of adult C. 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 1998).
Corema conradii biology Corema conradii favors disturbed habitats and can thrive in the sandy,
nutrient-poor soils found within and around the northeastern coast of North
America. Where it becomes established as a reproductive population, C.
conradii can become locally dominant. Copious seed production by local
populations leads to the build-up of a localized seed bank. This resource
serves as a means of regenerating a vigorous new cohort of plants when
disturbance occurs, and also serves as a source for anthropogenicly exported seeds that can lead to the formation of new small populations or isolated
plants along sand roads. Natural long-distance dispersal mechanisms in C. 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?
ering phenology should also vary substantially across the range of the
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 Recommendations
In most parts of its range, this species is of conservation concern. Corema conradii has a limited distribution within the confines of some
political boundaries, meaning the species is potentially at risk within some rare habitats or state/provincial management boundaries.
282 Northeastern Naturalist Vol. 12, No. 3
A particular motivation behind Dunwiddie's 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
suppression of fire on Nantucket, can have negative consequences for the
persistence of populations of disturbance-dependent species (Quintana- Ascencio and Menges 1996, Quintana-Ascencio et al. 2003, and references
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 post- fire 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
these conclusions were also reached by both Zaremba (1984) and Dunwiddie
(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
rarity of the species rather than its lack of regeneration. In both states, the
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, New Jersey appeared to possess a greater number of sites for Corema
conradii. It appears that many of these localities contained only a few
individuals or isolated plants along sand roads, suggesting anthropogenic
dispersal mechanisms; the decline of such occurrences is consistent with our
source-sink metapopulation model. The real concern is the status of the
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
using controlled mixed intensity prescribed burning and mechanical treat?
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 these populations to learn more about the reproductive biology of this
species, including the longevity of seed banks and the response to various
fire and disturbance regimes (Windisch 1998). Management of rare taxa
requires understanding of breeding biology and genetics, seed dispersal, and
seedling recruitment, survival, and establishment (Anderson et al. 2002, 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
these larger, southernmost populations of this fascinating species continue
to not only survive, but to thrive.
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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