Kim L. Coffey

RESEARCH ARTICLE ABSTRACT: Seed germination phenology studies are important tools for determining whether seeds exhibit dormancy and what environmental conditions trigger germination. Within longleaf pine (Pinus palustris Miller) ecosystems of the southeastern United States Coastal Plain, little is known about dor­ mancy patterns and germination cues of the suite of native species composing the. diverse fire-maintained ground cover vegetation. We used two methods to determine if several dominant or functionally important herbaceous species were capable of forming a persistent soil seed bank, including: (1) a germination • phenology study and (2) a buried seed bag study. Results indicate that within species studied from three common families (Asteraceae, 2 species; Fabaceae, 8 species; and Poaceae, 3 species), species within Seed Germination the Fabaceae family seem most capable of forming long-term persistent seed banks. Although most of the Poaceae and Asteraceae species examined exhibited little dormancy in the germination phenology study, evidence from the buried seed bag study indicates that several species may form transient or even Strategies of Species short-term persistent seed banks under favorable conditions. The absence of evidence of persistent seed banking potential for several dominant species examined in this study suggests that seed reintroduction With Restoration will likely be a necessary component in restoration efforts in longleaf pine ecosystems. Index terms: hard seed coat, restoration, seed bank, seed dormancy, seed germination Potential in a Fire- Maintained Pine INTRODUCTION terns, it is difficult to obtain propagated Savanna native seedlings, and where plant materials An understanding of how environmental are available, the cost is prohibitively high cues elicit germination and the role of for large-scale restoration (Holliday 2001, persistent seed banks is useful in develop­ Coffey and Kirkman 2004). Ki m l. Coffey 1,2 ing species reintroduction strategies in a l. Katherine Kirkman restoration context. Seeds of most temper­ Germination phenology studies are an ef­ Joseph W. Jones Ecological Research ate species have some form of primary fective tool for understanding conditions Center, Ichauway dormancy and may display annual cycles required for germination and detecting Route 2 Box 2324 in germination requirements in response seed dormancy (Baskin and Baskin 1998). Newton, GA 39870 USA to seasonal changes in temperature and Although numerous studies have addressed precipitation (Parker et al. 1989, Baskin dormancy characteristics in perennial her­ and Baskin 1998). These responses vary baceous plants, little is known about spe­ • widely among species and are difficult cific germination requirements, transient to predict. Information pertaining to the « 1 year) versus short-term persistent (1-5 presence of a seed bank, which affects year) and long-term persistent (>5 year) both the potential recovery and rate of seed-banking potential (Bakker et al. 1996, recovery of the ground cover following Thompson et al. 1998), and long-term seed disturbance, can provide insights into the viability of species found in the critically seed pool available for natural recruitment endangered fire-dependent longleaf pine over time (Bakker et al. 1996, Bekker et (Pinus palustris Mill.) savannas of the al. 1998a). Seed banks are particularly southeastern United States Coastal Plain important for disturbed sites where the (Glitzenstein et al. 2001). surroundil1g .1aJ.1dscape. has geel1. s~ye.rely altered and no longer serves as a source Restoration efforts in longleaf pine eco­ of propagules for dispersal. systems have focused predominantly on establishment of longleaf pine only, Seed dormancy and germination data particularly through plantations on old I Corresponding author: are also necessary for developing field fields (e.g., longleaf pine seedlings planted [email protected] establishment and· nursery production through the USDA's Conservation Reserve 2 Current address: techniques for native species restoration Program, [Holliday 2001]). Although rec­ Mecklenburg County efforts. Such information is especially rel­ ognition of the functional importance of Division of Natural Resources 9401 Plaza Road Extension evant to grassland and savanna ecosystem native ground cover has led to increased Charlotte, North Carolina 28215 USA restoration where re-establishment of a interest in herbaceous species reintroduc­ diverse perennial ground cover is usually tions, commercial sources of seed native to dependent on seed germination rather than longleaf pine ecosystems are unavailable, Natural Areas Journal 26:289-299 outplanting propagated seedling material. and many key questions remain unan­ For most grassland and savanna ecosys- swered regarding growth and establishment

Volume 26 (3), 2006 Natural Areas Journal 289 of these native species (Pfaff and Gonter Although the technique of charting seed­ In some grasslands (e.g., Konza prairie), 1996, Glitzenstein et al. 2001). ling emergence from soil cores has been dominant grass species rely primarily on widely used to assess seed bank potential vegetative reproduction rather than regen­ Ground cover vegetation of longleaf pine (Roberts 1981, Benoit et al. 1989, Leck eration through a large and persistent seed ecosystems is dominated by perennial 1989, Gross 1990), the application of this bank (Abrams 1988). Grime et al. (1981) and presumably long-lived species (Drew approach to a spatially diverse vegetation found a high percentage of both annual and et al' 1998, Mitchell et al' 1999), and no cover, such as the species-rich longleaf pine perennial grasses capable of germinating evidence of a strong role of seed bank­ ecosystem, is probably limited (Roberts immediately, also suggesting the lack of a ing has been documented for longleaf 1981, Gross 1990, Cohen etal. 2004). Het­ long-term persistent seed bank. In general, pine-wiregrass upland vegetation. Cox et erogeneity among soil samples, even when grasses contribute less to the seed bank than al. (2004) have suggested that potential composited over large areas, may suggest composites and other forbs (Roberts 1981), seed banking occurred in longleaf pine that the sampling effort is inadequate to and perennial grasses are less likely to be sandhills, where species richness increased capture seed from numerous species, and present in the seed bank than annual grasses following ground chopping, presumably potentially those species targeted for res­ (Abrams 1988, Rice 1985), as short-lived due to breaking up soil crust and exposing toration. Such studies can verify the seed species commonly have more persistent dormant seeds. Varner et al. (2000) noted bank potential of some species, but they seeds (Thompson et al. 1998). the recovery of native herbaceous ground do not necessarily address the seed bank cover species after fire was reintroduced potential of specific dominant components Numerous legume species have seeds that into the Flomaton Natural Area, a longleaf of the native ground cover of the longleaf exhibit physical dormancy in the form pine site in Alabama, from either long-term pine ecosystem. of an impermeable seed coat (Quinlivan survival of individual perennial plants or 1971; Rolston 1978; Baskin and Baskin the presence of a persistent seed bank. Asteraceae (composites), Poaceae (grass­ 1989, 1998). This dormancy mechanism Maliakal et al. (2000) found evidence of es), and Fabaceae (legumes) families delays germination from time of seed a soil seed bank in longleaf pine-wire­ dominate the flora of the longleaf pine maturity until environmental conditions grass flatwoods in peninsular Florida, but ecosystem. They comprise the primary become favorable to promote softening of concluded that the seed bank and existing structural and functional components the seed. This hard seed coat may not be vegetation were dissimilar, suggesting a in upland, fire-maintained longleaf pine present immediately at maturity, as some low potential vegetation recovery from ecosystems. Native grasses, particularly species will readily germinate prior to be­ the seed bank. Species recruited in this warm-season C4 species, are dominant ing collected and stored (Pfaff and Gonter seedling emergence study were generally ground cover species and are desirable 1996, Glitzenstein et al. 2001). However, "weedy" species or species representing for restoration due to their importance in hard-seededness is commonly induced historical ecological conditions (Maliakal reintroducing fuel for fire management, soon after maturity (Pfaff and Gonter 1996) et al. 2000). The study was conducted although little information is available and likely results in moisture reduction for only four months, and dormant seeds regarding their dormancy except for weedy within the seed (Quinlivan 1971). Such (those that would represent a persistent soil or commercially valuable species (Simpson physically dormant seeds can persist in the seed bank) would not have been detected; 1990). Legumes are also abundant ground seed bank for long periods of time (Hull therefore, an assessment of persistent seed cover species (Martin et al. 1975, Hainds 1973, Lewis 1973, Roberts and Boddrell bank potential is somewhat inconclusive. et al. 1999), and are believed to contribute 1985) until environmental conditions favor Similarly, without differentiation between nitrogen to an environment where nitrogen germination. transient and persistent seed banks, Jenkins is volatilized by frequent fires (Boring et (2003) found that species represented in the al. 1990, Hendricks and Boring 1999). Ad­ Several mechanisms may contribute to dor­ seed bank of a longleaf pine flatwoods site ditionally, legumes provide important food mancy break, including daily temperature versus a restoration site in central Florida and cover for wildlife (Hainds et al. 1999, fluctuations (Rice 1985), relative humidity differed from each other and from the Yarrow and Yarrow 1999). Composites (Cushwa et al. 1968, Rolston 1978), and representative vegetation located in the represent one of the most abundant and high temperatures potentially associated study plot area. In another recent seedling diverse families in longleaf pine ecosys­ with fire (Cushwa et al. 1968, Martin et emergence study comparing seed banks of tems (Drew et al. 1998), contributing to al. 1975). McKeon and Mott (1982) found longleaf pine flatwoods to disturbed areas, the exceptionally high species diversity that the highest soil surface temperatures Cohen et al. (2004) found that species in­ of this ecosystem. In addition, numerous occurred immediately before the rainy sea­ dicative of flatwoods flora germinated from composite species are considered desirable son and postulated a mechanism for some soil cores; however, most germinants were for ground cover restoration because they species that ensured germination prior to wetland species that have been observed are aesthetically prominent and important precipitation and favorable growing condi­ in other seed bank studies (Kirkman and as forage, host, or nectar plants for native tions. Peak germination season is often the Sharitz 1993, Poi ani and Dixon 1995) birds, butterflies, and insects (Byre 1997, same from year to year for a given species rather than dominant ground cover species Taron 1997, Yarrow and Yarrow 1999). (Baskin and Baskin 1998). typical to longleaf pine savannas.

290 Natural Areas Journal Volume 26 (3), 2006 This study was designed to test for seed animal-transported seeds). Seed from 13 recounting. Daily weather conditions on­ dormancy and seed banking potential of frequently occurring species was hand-col­ site (Newton, GA) were monitored using several functionally and compositionally lected at maturity on Ichauway during the information on the Georgia Automated important ground cover species in longleaf growing seasons of 2001-2003. Environmental Monitoring Network (www. pine ecosystems. Specific questions ad­ griffin.peachnet.edu/bae). Flats remained dressed include: (1) Do seeds of common Following collection, all seed was stored under shade cloth through April 2004, perennial ground cover species exhibit dor­ inside at room temperature (23°C, with when the project was terminated. mancy?, (2) What phenological conditions controlled humidity) until the study was promote seed germination?, and (3) Which initiated. Species planted included three Low precipitation occurred in spring 2002, of the selected species have the potential dominant grasses [Aristida stricta Michx., and we altered the watering schedule begin­ to form persistent soil seed banks? Sorghastrum secundum (Elliott) Nash, and ning in May to 15 minutes daily to prevent Sporobolusjunceus (P. Beauv.) Kunth], two dessication of seeds and new germinants. commonly occurring composites [Solidago This cycle coincided with the typical MATERIALS AND METHODS odora Aiton and Vernonia angustifolia period of afternoon thunderstorms, which Michx.], and eight legumes [Centrosema would have provided natural moisture, but Study site virginianum (L.) Benth., Desmodium were absent during drought years. Water­ ciliare (Muhl. ex Willd.) DC., D. stric­ ing schedule returned to weekly the first This study was conducted on Ichauway, the tum (Pursh) DC., Lespedeza angustifolia week in October 2002. This same watering privately owned reserve of the Joseph W. (Pursh) Elliott, L. hirta (L.) Hornem., Mi­ scheme was applied in 2003. Jones Ecological Research Center, in the mosa quadrivalvis L., Orbexilum lupinellus lower Gulf Coastal Plain of southwestern (Michx.) Isley, and Tephrosia viriginiana Upon termination of the project in April Georgia. The 11,600 ha property consists of (L.) Pers.]' More legume species were 2004, we attempted to recover seed remain­ approximately 7000 ha of mature longleaf selected for study due to their restoration ing in the flats. We were unable to recover pine forest, and nearly half of this area value for wildlife food and cover. Spe­ any grass or composite seeds from the soil; has intact native ground cover. Frequent cies nomenclature follows Wunderlin and however, hard-seeded legume seeds were prescribed surface fires have been used Hansen (2003). recovered and tested for gerrninability. To to manage the site since the early 1900s. recover seed, soil was dried in a drying oven Dominant soils are primarily Ultisols. Standard seedling flats (28 cm x 54 cm x at 41°C for 24 hours, and sieved twice (2 The region receives approximately 132 6 cm) were filled with a mixture of Fafard mm followed by 1 mm sieve opening) to cm of rainfall per year, and average daily 3B-mix potting soil and sand (4: 1 ratio), isolate seeds. Retrieved legume seeds were temperatures are 11- °C in winter and 27 and thoroughly watered. Potting soil was counted, scarified using a straight razor °C in summer. used instead of native soil to eliminate to break the hard seed coat (C. Baskin, the presence of non-target native seeds, pers. comm.), and placed on moist filter and sand was added to aid in drainage. paper in Petri dishes to test for viability Experiment 1: germination phenology Three replications of300 seeds per species based on germination. Because viable were placed in flats (one species per flat; legume seed readily germinates after the Species selected for this study are pe­ three flats per species; N=900 total seeds seed coat is broken (pers. observation of rennials common to frequently burned, per species) and randomly alTanged on numerous trials), we used germination rate undisturbed longleaf pine savannas and outside benches under greenhouse shade to indicate viability rather than the more represent three major families with impor­ cloth (63% shade). Shade cloth decreased labor-intensive method using a 1% solution tant functional and compositional roles as extreme heat conditions and diffused of2,3,5-triphenyl-2H-tetrazolium chloride described earlier. Seed from these species raindrop impactonthesoilsurface.Seed._ (Moore.J973) to stain viable.seeds. Soft - was-absenr-iIf previbus-seedbanlcstudies - of the 13 study species was spread over and moldy seed was considered non-viable (L.K. Kirkman, unpubl. data), leading us the soil in flats in December 2001. Seed (Baskin and Baskin 1998, Bekker et al. to question the role of seed banking in was lightly pressed by hand onto the soil 1998b). Moldy seed was removed from the some common species within longleaf pine to ensure soil contact without complete dishes· as discovered and seed that did not ecosystems. While there are hundreds of burial, mimicking natural seedfall. Flats germinate after three weeks was tested for species to examine, species were selected were watered using untreated well water firmness, indicating viability. Firm seeds for this initial study based on seed avail­ once weekly for 15 minutes using automati- were retained until germination occurred ability and their propagation potential in cally timed overhead sprinklers, and were or were discarded when they became native nursery seed production for restora­ exposed to ambient outdoor temperatures moldy or soft. tion purposes. Furthermore, our goal was and light/dark periods. Germinants were to examine some of the most common monitored weekly throughout the study, species in a few major plant families and Experiment 2: buried seed bags with radicle or coleorhiza protrusion as the to select those representing varied disper­ germination critelion. Once scored, gerrni­ sal mechanisms (e.g., wind, gravity, and To determine seed-banking potential, we nants were removed from the flat to prevent

Volume 26 (3), 2006 Natural Areas Journal 291 initiated a long-term study using buried trosema virginianum, Desmodium strictum, Aristida stricta and Sorghastrum secundum bags, projected for completion in 2018. Lespedeza angustifolia, L. hirta, Mimosa seeds in Petri dishes frequently develop This study utilizes data collected during quadrivalvis, and Tephrosia virginiana), mold that destroys seed prior to germina­ the first three sample periods (2001-2005). and two composites (Solidago odora and tion (pers. observation), so rather than Ten thousand seeds (100 bags per species; Vernonia angustifolia) was collected and conducting germination tests for these 100 seeds per bag) of each of 11 of the 13 buried on Ichauway from 2001-2003. An species, they were tested for viability us­ species in the phenology study described insufficient quantity of Desmodium ciliare ing a 1 % solution of 2,3,5-triphenyl-2H­ earlier (Table 1) were placed in nylon and Orbexilum lupinellus seed (two of the tetrazolium chloride (Moore 1973). Seed mesh bags (6.5 cm x 7 cm; mesh size 100 species used in the germination phenology from all other species that were not prone microns). Sand was added to each bag experiment) prevented burial experiments to mold attack was placed on moist filter (9.0-9.5 g) to keep seeds from clumping with these two species. Bags were strung paper in Petri dishes (seed from one bag together, and each bag was sewn shut. Bags onto galvanized wire strands through a per dish), maintained in a greenhouse, wa­ were strung on 18-gauge galvanized wire, small hole punched near the edge of the tered daily, and monitored for germination. with enough room between bags to avoid bag seam and the strands of bags were Prior to germination tests, seed coats of overlap in the soil (approximately 10 cm buried to a depth of 5 cm. Each strand all legume seeds recovered were scarified apart). Multiple species were placed on was attached to a tagged metal curly stake using a straight razor to break the imperme­ each strand (number of species per strand above ground. Twenty bags of each species able seed coat (C. Baskin, pers. comm.). varied with number of species buried each were removed in the winter at one and Composite and grass seed was not treated year) to avoid total loss of a single species two years post-burial (N=2000 seeds per in any way prior to tetrazolium or germina­ in the event of soil disturbance. species per year). Species buried in 2001 tion tests. Germinants were removed and were also tested at four years post-burial. recorded daily until three weeks passed Seed bags (N=100 bags per species) were Each curly stake with attached wire strand without germination, at which point the buried within an open, frequently-burned was lifted with a trowel inserted beneath trials were concluded. Soft seed was also 68-year-old slash pine (P. elliottii Englem.) the wire to loosen bags from soil. All bags removed and considered non-viable. All plantation that is, over several decades, were brought into the lab for processing. results are based on the total number of being gradually restored to a longleaf The remaining bags will be retrieved dur­ seeds that germinated or stained (indicat­ pine canopy. Seed of three grass species ing the winter at four, eight, and 16 years ing viable seed) out of the total number of (Aristida stricta, Sorghastrum secundum, post-burial. seeds per species buried each year (N =2000 andSporobolusjunceus), six legumes (Cen- per species per year).

Table 1. Percent seed germination (number of seed germinated or stained with Tetrazolium out of possible 2000 seeds per year). a = seed bag burial in 2001; b = seed bag burial in 2002; C = seed bag burial in 2003; NA = no data available; * = all germination occurred in year one.

% germination % germination % germination in flats from seed bags from seed bags (mean± SE) Family SEecies 1 year after burial 2 years after burial 2 years in flats Asteraceae Solidago odora b 34 12 66 ± 4.34* Asteraceae Vernonia angustifolia b 5 <1 15 ± 1.28* Fabaceae Centrosema virginianum c 14 10 72 ± 0.19 Fabaceae Desmodium ciliare NA NA 93 ± 2.61 Fabaceae D. strictum b 2 0 91 ± 0.89 Fabaceae Lespedeza angustifolia b 82 74 69 ± 2.50 Fabaceae L. hirta b 90 89 83 ± 5.61 Fabaceae Mimosa quadrivalvis c 56 51 31±1.87 Fabaceae Orbexilum lupinellus NA NA 58 ± 4.41

Fabaceae Tephrosia virginiana b 61 50 73 ± 1.09 Poaceae Aristida stricta a 0 0 57 ± 7.12* Poaceae Sorghastrum secundum a 26 34 17 ± 2.89* Poaceae Sporobolusjunceus b 1 <1 30 ± 0.56*

292 Natural Areas Journal Volume 26 (3), 2006 RESULTS we examined germinated throughout the 28 within families. Among grass species months of the study. Germination response buried in seed bags in 2001 (species with to changing environmental conditions in four years of buried bag data available), Germination phenology February and March can be seen most clear­ Aristida stricta showed no sign of a soil ly in two species, Centrosema virginianum seed bank while Sorghastrum secundum Seed from all grass and composite species and Tephrosia virginiana (Figure Id), al­ still had 9% seed viability after four years germinated within the first six months of though Orbexilum lupinellus and Mimosa of burial. Only 1 % of Sporobolus junceus the study, though germination rates were quadrivalvis (Figure Ie) exhibit a similar seeds recovered in year one were viable highly variable among species (Figures pattern. For Lespedeza angustifolia and L. and even fewer following two years of la andlb). hirta, little germination occurred during burial (Table 1). In composite species, 12% the first spring (2002) following warming of Solidago odora seed remained viable Legume germination varied widely among temperatures, but by January of 2003 and after two years of burial, whereas <1 % of the eight species, but distinct seasonal again in 2004, germination rates sharply Vernonia angustifolia seed remained viable patterns were identified among groups of increased following coldest temperatures, during this period (Table 1). species, particularly among congeners. with lows averaging near freezing (0 0c) Seed from both Desmodium ciliare and D. in both years (Figure If). With the exception of Desmodium strictum, strictum had total germination rates above seed oflegume species remained viable for 90%, the majority of which occurred dur­ at least one year after burial (Table 1). Over ing the first year (Figure lc), suggesting Recovery of seeds in buried seed 70% of both species of Lespedeza seed that these legume species do not exhibit bags was recovered and germinated following the strong physical dormancy attributed to two years of burial. Tephrosia virginiana an impermeable seed coat found in many Seed viability based on buried bag extrac­ seed had a lower recovery rate, but of legume species. All other legume species tions over time varied considerably, even those recovered, 50% germinated after

- Aristida stricta 600r------~ 40 --v-- Sorghastrum secundum - Sporobolus junceus 500 30 ~

~Q) 0- 400 E .$ .fB 20 E c: :J CI:I c: E '§ 300 '2 Q) 'E '0 OJ c: =!:I: 10 CI:I E 200 ------:J- E '§ E o c: 100 CI:I Q) E

O~L-~~~~~~~~~~~_*_*_+_+_+~~~_.~_.~~~~~ D J F M A M J J A SON D J F M A M J J A S 0 ND J F M A 2002 2003 2004

Figure La, Monthly germination patterns of grass species in seedling flats - germination only within the first six months of the study. Maximum and minimum mean monthly temperatures are represented by gray background lines.

Volume 26 (3), 2006 Natural Areas Journal 293 two years. Centrosema virginianum and with the largest fluctuation between high from buried seed of Sorghastrum secundum Mimosa quadrivalvis both appear to have and low temperatures (24°C difference and Solidago odora indicates that these hard seed coats with viable seed persist­ between average high and average low species can persist in the soil for at least ing for at least two years in the seed bank temperatures). Our finding that Desmodium two years, and in the case of Sorghastrum (Table 1). species lacked the hard seed coat present secundum, a limited number of viable seeds in Lespedeza and other legume species has were present (9%) four years post-burial. also been reported elsewhere (Cushwa et Although we were unable to directly ad­ DISCUSSION al. 1968, Martin et al. 1975). Species with dress the fate of seeds in flats, we offer hard seed coats are likely capable ofform­ the following alternative explanations for This study indicates that at least a short­ ing long-term persistent seed banks, and these differing results. The discrepancy in term persistent soil seed bank (two years) continuation of the buried seed bag portion the data between seedling flats and buried is present for some species in longleaf of this study will yield long-term data on seed bags could indicate that non-dormant pine-wiregrass savannas, whereas, other this subject. Greater seed longevity of le­ seed is inhibited from germinating due to species have little or no seed dormancy. gumes than of grasses and forbs has also a light requirement unavailable because of Although we recognize that our results been demonstrated in storage and in buried depth of seed bag burial (Baskin and Baskin are limited to only a few of the many seed bags (Hull 1973). Admittedly, in our 1989, Qi et al. 1996), yet is still capable of ground cover species in this species-rich study, fewer species of grasses and forbs forming a seed bank. If exposure to light ecosystem, the germination patterns within were examined than of legumes, limiting is necessary for germination, seed of these the three major plant families studied ap­ broad generalizations across families. species would be considered non-dormant, pear to have similarities to other grassland and germination phenology results and ecosystems (Grime et al. 1981, Rabinowitz While all germination of grass and com­ buried seed bag results would then be 1981, Freeman 1998, StCicklin and Fischer posite seed placed on the soil surface in consistent in terms of dormancy absence. 1999). Germination of legume species this study occurred within the first year, In addition, we also acknowledge that there tested in this study appeared to be triggered suggesting non-dormant seed or at most a was a potential loss of seed from the soil by exposure to cold winter temperatures transient seed bank, contrasting evidence surface of the seedling flats during the first followed by warming trends in the spring

600r------~ --- Solidago odora - 40 -- Vernonia angustifolia E 30 ~ -~ Q) c.. E 2 20 E :::l E ·c ·E "C 10 ffi c :::l E .~ E o c m E

DJFMAMJJASONDJFMAMJJASONDJFMA 2002 2003 2004

Figure l.b. Monthly germination patterns of composite species in seedling flats - germination only within the first six months of the study. Maximum and minimum mean monthly temperatures are represented by gray background lines.

294 Natural Areas Journal Volume 26 (3), 2006 year due to either wind or rain displacing found that environmental conditions for 1978, Baskin and Baskin 1989). Although small seed, or even predation by animals. the seed bank (represented in our study by perennial species of longleaf pine ecosys­ This could be of particular importance in buried seed bags) during the "no-growth" tems, such as Lespedeza, persist through the case of Sorghastrum secundum, where season affected the seed response at ger­ frequent fire, fire exposes seeds in soil to evidence from buried seed bags contradicts mination. By retrieving bags in winter higher temperatures and higher amplitudes that from the flats and suggests a strong every year, we might not be able to fully of temperature fluctuation (Grime 1989), possibility of at least some seed persisting address seasonal effects on dormancy and leading in some cases to germination. for four years. Future studies should in­ germinability. clude covering seedling flats with screening Long-lived seeds constitute a buffer against material (a method used to prevent rodent Different germination patterns were also risks of local extinction due to stochastic seed predation) (Greene and Curtis 1950) observed between buried seed bags and processes (Stocklin and Fischer 1999). to eliminate the possibility of seed loss seed placed in flats in both Lespedeza spe­ Such buffering capacity suggests that veg­ prior to study conclusion. cies. These results could be due to specific etation subjected to frequent disturbance light requirements associated with burial benefits from producing a persistent seed Even though data from Aristida stricta (Qi et al. 1996), as discussed earlier. An­ bank (Thompson et al. 1998); however, seed in our studies suggests that this spe­ other possible explanation is thatLespedeza this adaptive advantage does not neces­ cies is unlikely to form a persistent seed seed placed in flats experienced larger daily sarily apply to fire-maintained longleaf bank, other field studies suggest that at temperature fluctuations or higher daily pine vegetation, where most species are least short-term (two year) seed persistence temperatures than seed buried in the soil, perennials that sprout back from below­ may occur in the soil (Seamon 1998, Mul­ leading to increased germination of seed ground perennating organs after fire. Once ligan and Kirkman 2002, Cox et al. 2004). closer to the soil surface (Cushwa et al. established, individuals of these species Thus, it may not be possible to entirely 1968). Disturbances that decrease canopy presumably persist for many years (Kirk­ generalize our experimental conditions to vegetation, exposing seeds in the soil to man et al. 2001), and long-lived adult field conditions, perhaps concerning timing more extreme temperature conditions, plants are generally unlikely to form a of precipitation events or even prolonged trigger seed coat softening and induce ger­ persistent seed bank (Rees 1994). This drought conditions. Espinar et al. (2005) mination of hard-seeded species (Rolston situation resembles a stable community

600~------~ - Desmodium ciliare 40 -- D. strictum ..-, () 500 JY~'''''' ~ ~ 30 .....:::I ~ Q) c.. 400 / \ 1\ ~ E .sl 20 E -Eco :::I r:: E '§ 300 j~V (~\\J '2 Q) 'E Cl r \ A "C r:: -:j:j:- ..... __ 1- __ (. _ . _\ __ .. 1a-co ------E 200 :::I E .~ E 100 ~ V 0 r::co Q) E

0~~~~~~*=~~-9~~~4-~~-+~~~+-~~~-+~ DJ FMAMJ JASONDJ FMAMJ JASONDJ FMA 2002 2003 2004

Figure I.c. Monthly germination patterns of Desmodillm species in seedling flats - most germination occurred within year one of the study. Maximum and minimum mean monthly temperatures are represented by gray background lines.

Volume 26 (3), 2006 Natural Areas Journal 295 that is more likely to favor a transient seed perspective will require know ledge of seed some dominant species also confirms that bank (Thompson et al. 1998). In this type longevity traits of a greater percentage of seed reintroduction will likely be necessary of savanna community, variable environ­ the total flora over a long time period. for restoration of many dominant grasses mental conditions suitable for seedling and forbs in longleaf pine ecosystems establishment are likely associated with The presence of persistent seed banks has where seed dispersal into the site over time precipitation events and microsite varia­ direct implications for restoration areas by is not an option. tions that provide adequate moisture, as providing propagules of an initial suite of well as with fire that removes aboveground native ground cover species in disturbed ACKNOWLEDGMENTS competition for light. The combination of areas, particularly in areas where propagule periodic recruitment events and persistent dispersal from neighboring high-quality The authors acknowledge the assistance of vegetation likely balance the necessity sites is limited or non-existent. However, S. Baumann, K. Bell, 1. Biggs, J. Bowen, of a persistent seed bank for popUlation the limited amount of viable seed of several D. DeBruyne, R. DeMots, E. Leonard, K. survival. Furthermore, regular removal of dominant species in the seed bank sug­ Mawhinney, H. Norden, E. O'Brien, K. aboveground biomass with frequent fire in gests that these species have alternative Schmitt, E. Schuett, and S. Wheeler with longleaf pine ecosystems does not promote mechanisms for long-term persistence seed collection and seed bag processing. the introduction of weedy annual species in agriculturally undisturbed areas, such R. Mitchell provided helpful comments (Drew et al. 1998), which do tend to form as re-sprouting or asexual/vegetative regarding the manuscript. The Robert W. persistent seed banks (Bekker et al. 1998b). reproduction associated with plant longev­ Woodruff Foundation provided funding for Thus, the degree of seed bank persistence ity (Abrams 1988, Jenkins 2003, Laughlin this study to the Joseph W. Jones Ecological in longleaf pine grassland communities 2003). Based on results from these studies, Research Center at Ichauway. can probably be viewed as intermedi­ it appears unlikely that many of the study ate between temperate deciduous forest species produce seed capable of forming communities and highly disturbed lands persistent seed banks. This lack of long­ Kim Coffey is a Natural Resources Coor­ (Bekker et al. 1998b). Validation of this term persistent seed banking potential in dinator in Charlotte, N.c. Her interests

200 ---+-- Centrosema virginianum 40 ----9-- Tephrosia virginiana

U -0 p""';""", - \ /"fi'Y"""\ 30 .a~ 150 ~ Q) 0- E \ / \ r ~ 20 E jg ::l c: /~~\ V ('"""\ ~J E a1 c: 100 '2 \ • I I \ 'E 'E.... Q) \ ,-1 \ "0c: C) 10 a1 =1:1: E \ ~ \ l~ ::l E 'x 50 a1 E V V 0 c: a1 Q) E

O~~~-LLJ~~~~~~LL~~~~~~~~ DJFMAMJJASONDJFMAMJJASONDJFMA 2002 2003 2004

Figure l.d. Monthly germination patterns of Celltrosema virgilliallllm and Tephrosia virgillialla in seedling flats - germination occurred throughout the study period, with pronounced seasonal patterns. Note different scale on y-axis is different from other figures. Maximum and minimum mean monthly temperatures are represented by gray background lines.

296 Natural Areas Journal Volume 26 (3), 2006 200 Orbexilum /upinel/us 40 ----';'- Mimosa quadriva/vis .u--- 30 -~ 150 .....::::s /\ ~ !!! (I) I/ 0.. I E I .....(I) en 20 E .....c: ::::s en E c: 100 '2 'E r \V J --J 'E '- (I) "0 Ol I \;-. , \ 10 c: =I:f: :;r"''1/ en E ~ ) \ / ::::s 50 E "N .~ V V 0 E c:en (I) E 0 D J FMAMJ JASOND JFMAMJJASOND JFMA 2002 2003 2004

Figure I.e. Monthly germination patterns of Mimosa qlladrivalvis and Orbexilllm lllpinellus in seedling flats - germination occurred throughout the study period, with subtle seasonal patterns. Maximum and minimum mean monthly temperatures are represented by gray background lines.

include herbaceous species diversity and Neerlandica 45:461-490. 145-153 in S.C. Nodvin and T.A. Waldrop, restoration and preservation of native Baskin, C.C., and J.M. Baskin. 1989. Physiol­ eds., Fire and the environment: ecological ground cover and associated rare plant ogy of dormancy and germination in relation and cultural perspectives. Proceedings of an International Symposium, Knoxville, Tenn. species. This work was conducted while to seed bank ecology. Pp. 53-66 in MA. General Technical Report SE-69, U.S. De­ she was employed as a research techni­ Leck, Y.T. Parker, and RL. Simpson, eds., Ecology of Soil Seed Banks. Academic partment of the Interior, Park Service, U.S. cian at the J. W. Jones Ecological Research Press, San Diego, Calif. Department of Agriculture, Forest Service, Center. Southeastern Forest Experiment Station, Baskin, C.C., and J.M. Baskin. 1998. Seeds: Asheville, N.C. Ecology, Biogeography, and Evolution of Katherine Kirkman is an Associate Scien­ Dormancy and Germination. Academic Byre, V.J. 1997. Birds. Pp. 327-337 in S. tist with the 1. W. Jones Ecological Research Press, San Diego, Calif. Packard and C.P. Mutel, eds., The Tallgrass Restoration Handbook. Island Press, Wash- Center. Her research interests are in main­ Bekker, R.M., I.C. Knevel, J.B.R Tallowin, tenance andRstoration ofthe_biodiversity -- --E.M,b;-Troost,and IP.Bakker.1998a.Soil _i~gton,12·C--"______ofnative ground cover in the longleafpine nutrient input effects on seed longevity: a Coffey, KL., and L.K Kirkman. 2004. Native ecosystem and associated wetlands. burial experiment with fen-meadow species. ground covers partners: re-establishing Functional Ecology 12:673-682. native ground cover in longleaf pine sa­ vannas (Georgia). Ecological Restoration Bekker, RM., J.H.J. Schaminee, J.P. Bakker, 22:288-289. and K Thompson. 1998b. Seed bank char­ LITERATURE CITED acteristics of Dutch plant communities. Acta Cohen, S., R Braham, and P. Sanchez. 2004. Botanica Neerlandica 47: 15-26. Seed bank viability in disturbed longleaf pine sites. Restoration Ecology 12:503- Abrams, M.D. 1988. Effects of burning regime Benoit, D.L., N.C. Kenkel, and P.B. Cavers. 515. on buried seed banks and canopy coverage in 1989. Factors influencing the precision of a Kansas tallgrass prairie. The Southwestern soil seed bank estimates. Canadian Journal Cox, A.C., D.R Gordon, J.L. Slapcinsky, and Naturalist 33:65-70. of Botany 67:2833-2840. G.S. Seamon. 2004. Understory restoration in longleaf pine sandhills. Natural Areas Bakker, J.P., P. Poschlod, RI. Strykstra, RM. BOling, L.R, J.J. Hendricks, andM.B. Edwards. Journal 24:4-14. Bekker, and K Thompson. 1996. Seed 1990. Loss, retention, and replacement of ni­ banks and seed dispersal: important top­ trogen associated with site preparation burn­ Cushwa, C.T., R.E. Martin, and R.L. Miller. ics in restoration ecology. Acta Botanica ing in southern pine-hardwood forests. Pp. 1968. The effects of fire on seed gerrni-

Volume 26 (3), 2006 Natural Areas Journal 297 600 -r------j --- Lespedeza angustifolia 40 ---- Lespedeza hirta 6 500 ~ 30 ~ ::I li! Q) 400 a. E JB 2 c: 20 ro E c: ::I E '§ 300 'c Q) C) 'E =1:1:: 10 -g ro 200 E ::I E .~ o E 100 c: ro Q) E

DJFMAMJJASONDJFMAMJJASONDJFMA 2002 2003 2004

Figure l.f. Monthly germination patterns of Lespedeza species in seedling fiats - germination occurred after exposure to warm summer temperatures followed by cold winter temperatures. Maximum and minimum mean monthly temperatures are represented by gray background lines.

nation. Journal of Range Management Grime, J.P. 1989. Seed banks in ecological Georgia Wildlife Press, Covington. 21 :250-254. perspective. Pp. xv-xxii in M.A. Leck, Y.T. Hull, Jr., A.C. 1973. Germination of range plant Drew, M.B., L.K Kirkman, andA.K Gholson, Parker, and RL. Simpson, eds., Ecology seeds after long periods of uncontrolled Jr. 1998. The vascular flora of Ichauway, of Soil Seed Banks. Academic Press, San storage. Journal of Range Management Baker County, Georgia: a remnant long­ Diego, Calif. 26:198-200. leaf pine/wiregrass ecosystem. Castanea Grime, J.P., G. Mason, A.V. Curtis, J. Rodman, Jenkins, A.M. 2003. Seed banking and ve­ 63:1-24. S.R Band, M.A.G. Mowforth, A.M. Neal, sicular-arbuscular mycorrhizae in pasture Espinar, J.L., L.Y. Garcia, and L. Clemente. and S. Shaw. 1981. A comparative study of restoration in central Florida. M.S. thesis, 2005. Seed storage conditions change the germination characteristics in a local flora. University of Florida, Gainesville. Journal of Ecology 69:1017-1059. germination pattern of clonal growth plants Kirkman, L.K., R.I. Mitchell, RC. Helton, and in Mediterranean salt marshes. American Gross, KL.1990.Acomparison of methods for M.B. Drew. 2001. Productivity and species Journal of Botany 92:1094-1101. estimating seed numbers in the soil. Journal richness across an environmental gradient Freeman, c.c. 1998. The flora of the Konza of Ecology 78:1079-1093. in a fire-dependent ecosystem. American Prairie - a historical review and contempo­ Hainds, M.J., R.J. Mitchell, B.J. Palik, L.R. Journal of Botany 88:2119-2128. rary patterns. Pp. 69-80 inA.K Knapp, J.M. Boring, and D.H. Gjerstad. 1999. Distribu­ Kirkman, L.K., and RR. Sharitz. 1993. Veg­ Briggs, D.C. Hartnett and S.L. Collins, eds., tion of native legumes (Leguminoseae) in etation disturbance and maintenance of Grassland Dynamics - Long-term Ecologi­ frequently burned longleaf pine (Pinaceae)­ diversity on intermittently flooded Carolina cal Research in Tallgrass Prairies. Oxford wiregrass (Poaceae) ecosystems. American bays in South Carolina. Ecological Applica­ University Press, New York. Journal of Botany 86:1606-1614. tions 4: 177 -188. Glitzenstein, J.S., D.R Streng, D.D. Wade, and Hendricks, J.I., and L.R. Boring. 1999. Nz-fixa­ Laughlin, D.C. 2003. Lack of native propagules J. Brubaker. 2001. Starting new populations tion by native herbaceous legumes in burned in a Pennsylvania, USA, limestone prairie of longleaf pine ground-layer plants in the pine ecosystems of the southeastern United seed bank: futile hopes for a role in eco­ outer coastal plain of South Carolina, USA. States. Forest Ecology and Management logical restoration. Natural Areas Journal Natural Areas Journal 21:89-110. 113:167-177. 23: 158-164. Greene, H.C., and J.T. Curtis. 1950. Germina­ Holliday, P.P. 2001. Going, going ... saving the Leck, M.A. 1989. Wetland seed banks. Pp. tion studies of Wisconsin prairie plants. longleaf pine ecosystem before it's gone. Pp. 283-305 in M.A. Leck, V. T. Parker, and RL. American Midland Naturalist 43:186-194. 55-66 in J.R Wilson, ed., The Fire Forest. Simpson, eds., Ecology of Soil Seed Banks.

298 Natural Areas Journal Volume 26 (3), 2006 Academic Press, San Diego, Calif. ogy of Soil Seed Banks. Academic Press, Rolston, M.P. 1978. Water impermeable seed Lewis, J. 1973. Longevity of crop and weed San Diego, Calif. dormancy. The Botanical Review 44:365- seeds: survival after 20 years in soil. Weed Pfaff, S., and M.A. Gonter. 1996. Florida 396. Research 13:179-191. native plant collection, production and Seamon, G. 1998. A longleaf pine sandhill Maliakal, S.K, E.S. Menges, and J.S. Denslow. direct seeding techniques: interim report. restoration in Northwest Florida. Restoration 2000. Community composition and regen­ U.S. Department of Agriculture, Natural and Management Notes 16:46-50. eration of Lake Wales Ridge wiregrass Resources Conservation Service, Plant Simpson, G.M. 1990. Seed Dormancy in flatwoods in relation to time-since-fire. Materials Center, Brookville, Fla. Grasses. Cambridge University Press, Journal of the Torrey Botanical Society Poiani, KA., and P.M. Dixon. 1995. Seed Cambridge, U.K 127:125-138. banks of Carolina bays: potential con­ StOcklin, J., and M. Fischer. 1999. Plants with Martin, R.E., R.L. Miller, and C.T. Cushwa. tributions from surrounding landscape longer-lived seeds have lower local extinc­ 1975. Germination response oflegume seeds vegetation. American Midland Naturalist tion rates in grassland remnants 1950-1985. subjected to moist and dry heat. Ecology 134:140-154. Oecologia 120:539-543. 56:1441-1445. Qi, M., M.K Upadhyaya, and R. Turkington. Taron, D.J. 1997. Insects. Pp. 305-318 in S. McKeon, G.M., and lJ. Mott. 1982. The effect 1996. Dynamics of seed bank survivorship Packard and C.F. Mutel, eds., The Tallgrass of temperature on the field softening of hard of meadow salsify (Tragopogon pratensis) Restoration Handbook. Island Press, Wash­ seed of Stylosanthes humilis and S. hamata in populations. Weed Science 44:100-108. ington, D.C. a dry monsoonal climate. Australian Journal Quinlivan, B.J. 1971. Seed coat impermeability Thompson, K, J.P. Bakker, R.M. Bekker, and of Agricultural Research 33:75-85. in legumes. The Journal of the Australian J.G. Hodgson. 1998. Ecological correlates Mitchell, R.I., L.K Kirkman, S.D. Pecot, C.A. Institute of Agricultural Science 37:283- of seed persistence in soil in the north­ Wilson, B.J. Palik, and L.R Boring. 1999. 295. west European flora. Journal of Ecology Patterns and controls of ecosystem func­ Rabinowitz, D. 1981. Buried viable seeds in a 86:163-169. tion in longleaf pine - wiregrass savannas. North American tall-grass prairie: the resem­ Varner, J.M., J.S. Kush, and RS. Meldahl. 2000. r. Aboveground net primary productiv­ blance of their abundance and composition Ecological restoration of an old-growth ity. Canadian Journal of Forest Research to dispersing seeds. Oikos 36:191-195. longleaf pine stand utilizing prescribed fire. 29:743-751. Rees, M. 1994. Delayed germination of seeds: Pp. 216-219 in W.K Moser and C.F. Moser, Moore, RP. 1973. Tetrazolium staining for a look at the effects of adult longevity, the eds., Fire and forest ecology: innovative assessing seed quality. Pp. 347-366 in W. timing of reproduction, and population silviculture and vegetation management, Tall Heydecker, ed., Seed Ecology. George, Al­ age/stage structure. American Naturalist Timbers Fire Ecology Conference Proceed­ len, and Unwin, London. 144:43-64. ings, No. 21. Tall Timbers Research Station, Mulligan, M.K, and L.K Kirkman. 2002. Rice, K.I. 1985. Responses of Erodium to Tallahassee, Fla. Burning influences on wiregrass (Aristida varying microsites: the role of germination Wunderlin, R.P., and B.F. Hansen. 2003. Guide beyrichiana) restoration plantings: natural cueing. Ecology 66:1651-1657. to the vascular plants of Florida. University seedling recruitment and survival. Restora­ Roberts, H.A. 1981. Seed banks in soils. Ad­ Press of Florida, Gainesville, Fla. tion Ecology 10:334-339. vances in Applied Biology 6:1-55. Yarrow, G.K, and D.T. Yarrow. 1999. Managing Parker, V.T., RL. Simpson, and M.A. Leck. Roberts, H.A., and J.E. Boddrell. 1985 Seed Wildlife. Sweetwater Press, Birmingham, 1989. Pattern and process in the dynamics survival and seasonal pattern of seedling Ala. of seed banks. Pp. 367-384 in M.A. Leck, emergence in some Leguminosae. Annals V.T. Parker, and RL. Simpson, eds., Ecol- of Applied Biology 106:125-132.

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