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.


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.


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.)


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


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


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.


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


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


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.


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


(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.


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


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.


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


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.

Literature Cited

Anderberg, A.A., C. Rydin, and M. Kallersjo. 2002. Phylogenetic relationships in the order Ericales s.l.: Analyses of molecular data from five genes from the

plastid and mitochondrial genomes. American Journal of Botany 89:677-687.

Anderson, G.J., S.D. Johnson, P.R. Neal, and G. Bernardello. 2002. Reproductive biology and plant systematics: The growth of a symbiotic association. Taxon 51:637-653.

Beattie, A.J. 1985. The Evolutionary Ecology of Ant-Plant Mutualisms. Cambridge University Press, New York, NY. 192 pp.

Boyd, H.P. 1991. A Field Guide to the Pine Barrens of New Jersey. Plexus Publish?

ing, Medford, NJ. 423 pp. Calvino-Cancela, M. 2002. Spatial patterns of seed dispersal and seedling recruit?

ment in Corema album (Empetraceae): The importance of unspecialized dispers? es for regeneration. Journal of Ecology 90:775-784.

Clemants, S. 1997. Broom crowberry technical page. Brooklyn Botanic Garden.

Brooklyn, NY. Available at: http://www.bbg.org/sci/nymf/encyclopedia/emp/ cor0010b.htm.

Collins, B.R., and K.H. Anderson. 1994. Plant Communities of New Jersey. Rutgers University Press, New Brunswick, NJ. 287 pp.

Crawford, D.J., E. Ruiz, T.F. Stuessy, E. Tepe, P. Aqeveque, F. Gonzalez, R.J.

Jensen, G.J. Anderson, G. Bernardello, CM. Baeza, U. Swenson, and M. Silva O. 2001. Allozyme diversity in endemic flowering plant species of the Juan Fernandez Archipelago, Chile: Ecological and historical factors with implica? tions for conservation. American Journal of Botany 88:2195-2203.


Diaz-Barradas, M.C, O. Correja, M. Zunzunegui, F. Ain-Lhout, A. Clavijo, P. Silva, and S. Ferreira. 2000. Distribuigao de sexos na especie Corema album ao longo de um gradiente climatico. Revista de Biologia 18:7-22.

Dunwiddie, P.W. 1990. Rare plants in coastal heathlands: Observations on Corema conradii (Empetraceae) and Helianthemum dumosum (Cistaceae). Rhodora 96:22-26.

Dunwiddie, P.W., R.E. Zaremba, and K.A. Harper. 1996. A classification of coastal heathlands and sandplain grasslands in Massachusetts. Rhodora 98:117-145.

Fischer, N.H., G.B. Williamson, J.D. Weidenhamer, and D.R. Richardson. 1994. In search of allelopathy in the Florida scrub: The role of terpenoids. Journal of Chemical Ecology 20:1355-1380.

Gibson, D.J., and E.S. Menges. 1994. Population structure and spatial pattern in the dioecious shrub Ceratiola ericoides. Journal of Vegetation Science 5(3):337- 346.

Givnish, T.J. 1981. Serotiny, geography, and fire in the Pine Barrens of New Jersey. Evolution 35:101-123.

Guitian, P., M. Madrano, and M. Rodriguez. 1997. Reproductive biology of Corema album (L.) D. Don (Empetraceae) in the northwest Iberian Peninsula. Acta Botanica Gallica 144(1):119-128.

Harshberger, J.W. 1916. Reprint 1970. The Vegetation of the New Jersey Pine Barrens. Dover Publications, New York, NY. 329 pp.

Hawkes, C.V., and E.S. Menges. 1996. The relationship between open space and fire for species in a xeric Florida shrubland. Bulletin of the Torrey Botanical Club

123(2):81-92. Johnson, A.F. 1982. Some demographic characteristics of the Florida rosemary,

Ceratiola ericoides Michx. American Midland Naturalist 108:170-174.

Kiviat, E. 1988. The Northern Shawangunks: An Ecological Survey. Mohonk Pre?

serve, New Paltz, NY.

Kron, K.A., W.S. Judd, P.F. Stevens, D.M. Crayn, A.A. Anderberg, P.A. Gadek, C.J.

Quinn, and J.L. Luteyn. 2002. Phylogenetic classification of Ericaceae: Molecu? lar and morphological evidence. The Botanical Review 68:335-423.

Levin, M.H. 1966. Early stages of secondary succession on the Coastal Plain, New

Jersey. American Midland Naturalist 75:101-119.

Lutz, H.L. 1934. Ecological relations in the pitch pine Plains of southern New Jersey. Yale University School of Forestry Bulletin 38:1-80.

Martine, C.T., and R.A. Figley. 2002. Shrubs and Vines of New Jersey and the Mid- Atlantic States. Forest Resource Education Center, New Jersey Forest Service, Jackson, NJ. 114 pp.

Mathews, F.S. 1915. Field Book of American Trees and Shrubs. G.P. Putnam's Sons, New York, NY. 465 pp.

Menges, E.S., and J. Kimmich. 1996. Microhabitat and time since fire: Effects on

demography of a Florida scrub endemic plant. American Journal of Botany 83:185-191.

Menges, E.S., and N. Kohfeldt. 1995. Life history strategies of Florida scrub plants in relation to fire. Bulletin of the Torrey Botanical Club 122:282-297.

Nanami S., H. Kawaguchi, and T. Yamakura. 1999. Dioecy-induced spatial patterns of two codominant tree species, Podocarpus nagi and Neolitsea aciculata. Jour? nal of Ecology 87:678-687.

NatureServe. 2003. NatureServe Explorer: An On-line Encyclopedia of Life [web application]. Version 1.8. NatureServe, Arlington, VA. Available at http:// www.natureserve.org/explorer (Accessed: April 3, 2004).


New Jersey Natural Heritage Database, [unpublished]. Office of Natural Lands

Management, Division of Parks and Forestry, New Jersey Department of Envi?

ronmental Protection, Trenton, NJ.

Nicholson R., and J. Alexander. Unpublished. Germination trials with Corema conradii.

Osunkoya, O.O. 1999. Population structure and breeding biology in relation to conservation in the dioecious Gardenia actinocarpa (Rubiaceae) ?a rare shrub of North Queensland rainforest. Biological Conservation 88:347-359.

Quintana-Ascencio, P.F., and E.S. Menges. 1996. Inferring metapopulation dynam? ics from patch-level incidence of Florida scrub plants. Conservation Biology 10(4):1210-1219.

Quintana-Ascencio, P.F., E.S. Menges, and C.W. Weekley. 2003. A fire-explicit population viability analysis of Hypericum cumulicola in Florida rosemary scrub. Conservation Biology 17(2):433-449.

Redfield, J.H. 1884. Corema conradii and its localities. Bulletin of the Torrey Botanical Club 11:91-101.

Redfield, J.H. 1889. Corema in New Jersey. Bulletin of the Torrey Botanical Club 16:193-195.

Renner, S.S., and R.E. Ricklefs. 1995. Dioecy and its correlates in the flowering plants. American Journal of Botany 82:596-606.

Rickson, F.R. 1977. Progressive loss of ant-related traits of Cecropia peltata on selected Caribbean islands. American Journal of Botany 64:585-592.

Roche, S., K.W. Dixon, and J.S. Pate. 1998. For everything a season: Smoke-induced seed germination and seedling recruitment in a Western Australian Banksia woodland. Australian Journal of Ecology 23:111-120.

Rocheleau, A., and G. Houle. 2001. Different cost of reproduction for the males and females of the rare dioecious shrub Corema conradii (Empetraceae). American Journal of Botany 88:659-666.

Schemske, D.W., B.C. Husband, M.H. Ruckleshaus, C. Goodwillie, I.M. Parker, and J.G. Bishop. 1994. Evaluating approaches to the conservation of rare and endan?

gered plants. Ecology 75:584-606.

Somanathan, H., and R.M. Borges. 2000. Influence of exploitation on population structure, spatial distribution, and reproductive success of dioecious species in a

fragmented cloud forest in India. Biological Conservation 94:243-256.

Sorrie, B.A. 1987. Notes on the rare flora of Massachusetts. Rhodora 89:113-196.

Stone, W. 1911. The Plants of Southern New Jersey. Reprint 1973. Quarterman Publications, Boston, MA.

Tieu, A., K.W. Dixon, K.A. Meney, and K. Sivasithamparum. 2001. Interaction of soil burial and smoke on germination patterns in seeds of selected Australian native plants. Seed Science Research 11:69-76.

Torrey, J. 1848. An account of several new genera and species of North American

plants. Annals of the Lyceum of Natural History of New York 4:83-87.

Traveset, A., J. Gulias, N. Riera, and M. Mus. 2003. Transition probabilities from

pollination to establishment in a rare dioecious shrub species (Rhamnus ludovici

salvatoris) in two habitats. Journal of Ecology 91:427-437'.

Whelan, R.J. 1995. The Ecology of Fire. Cambridge University Press, Cambridge, UK.

Wilson, W.G., and L.D. Harder. 2003. Reproductive uncertainty and the relative

competitiveness of simultaneous hermaphroditism versus dioecy. American Naturalist 162(2):220-241.


Windisch, A.G. 1998. Department of Defense Legacy Program studies at Warren Grove Range, New Jersey: Vegetation mapping, broom crowberry survey, and restoration at Warren Grove Range and vicinity; Pine plains management at Warren Grove Range and vicinity, using prescribed fire versus mechanical dis? turbance. In Unpublished report dated June 29, 1998, and submitted to Col. Richard Masse, Air National Guard, Andrews Air Force Base, MD. The Nature

Conservancy, at New Jersey Natural Heritage Program, Trenton, NJ.

Yampolsky C, and H. Yampolsky. 1922. Distribution of sex forms in the

phanerogamic flora. Bibliotheca Genetica 3:1-62.

Zaremba, R. 1984. Corema conradii?Broom crowberry. Unpublished report of the

Massachusetts Heritage Program, Westborough, MA.

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