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Morphology and systemat
Memoirs of the New York
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Journal ofthe Torrcv BolcllJicu! Society n5(4J, 2008, pp. 4'11·-4'16
Differential soil seed bank longevity of Paederia foetida L., an invasive woody vine, across three habitats in Florida I Hong Liul,2 University of Florida, IFAS, Fort Lauderdale Research and Education Center, Ft. Lauderdale,
Florida 33314
Robert W. PembertonU.S. Department of Agriculture, Agricultural Research Service, Invasive Plant Research Laboratory, Ft. Lauderdale, Florida 333 I 4 LIU, H. (University of Florida, IFAS, Fort Lauderdale Research and Education Center, Ft. Lauderdale, Florida 33314) AND R. W. PEMBERTON (U.S. Department of Agriculture, Agricultural Research Service, Invasive Plant Research Laboratory, Ft. Lauderdale, Florida 33314). Differential soil seed bank longevity of an invasive woody vine (Paederiafoetida L.) across three habitats in Florida. J. Torrey Bot. Soc. 135: 491 496. 2008.-Knowledge on seed bank longevity is especially important in understanding population dynamics of invasive species and critical in determining the intensity and length of control efforts. In this study we determined the soil seed bank longevity of Paederiafoetida across three main natural habitats that P. foetida occur in Florida (the interior of a mixed mesic forest, a forest edge, and an open grassland). A native of eastern Asia, P. foe/ida is invasive in natural and human created habitats in the southern United States and Hawaii. We placed multiple bags with known number of fruits (diaspores) in four stations on the soil surface in each habitat and retrieved the bags once a year for three years. Our data demonstrated that P. foetida forms a short term persistent seed bank and seeds may remain viable for more than one year in the soil seed bank. The decline of soil seed bank was significantly slower in the forest interior than in forest margin and grassland. In the forest interior, 38% of the seeds remained viable for one year, but only 2% remained viable in the forest edge and open grassland habitats. The percentages of viable seeds dropped to 4.7%,0.4%, and 0% after two years in the soil seed banks in the forest interior, the forest edge, and the open habitat, respectively. After three years, only 0.3%, 0.1%, and 0% of seeds were found viable in these three habitats, respectively. Even though very small proportions of seeds survived three years, given that the annual fruit production of P. foetida is typically large and that it only takes a minimum of two viable seeds to start a new reproducing population for this self-incompatible species, we recommend post adult plant elimination monitoring for two years in open habitat, but up to four years in forest areas. Key words: invasive species, Paederia foetida, skunk vine, seed longevity, soil seed bank.
Seed bank longevity is a vital component of plant population dynamics (Cook 1980, Fen ner 1992, Silvertown and Charlesworth 2001). A long term seed bank offers a buffer, spatially and temporally, to plant populations, which can be extremely important in conser vation and restoration of plant communities (Fenner 1992, Leek and Graveline 1979, Ogden and Rejmanek 2005), including rare and endangered species (Quintana-Ascencio et al. 2003, Liu et al. 2005, Meyer et al. 2006). However, persistent seed banks pose challeng es to weed management in agricultural fields 1 The authors thank the Hillsborough River State Park for permission to conduct our research. 2 Current affiliation; Department of Environmen tal Studies, Florida International University and Fairchild Tropical Botanic Garden, Coral Gables, Miami, FL 33I 56. 3 Author for correspondence: E-mail: Robert.
[email protected] Received for publication May 5, 2008, and in revised form August 29, 2008.
(Priestley 1986, Murdoch and Ellis 1992), as well as of invasive plants in natural areas (Lonsdale et al. 1988, Krinke et al. 2005, Shen et al. 2006, Naumann and Young 2007). Knowledge of seed bank longevity is especially important in understanding the population dynamics of invasive species and critical in determining the intensity and length of man agement (Lonsdale et al. 1988). Skunk vine (Paederia foetida L. s. str., non sensu auctt.) is a woody perennial vine native to Asia (Puff 1991). It is recognized as a Category I weed by the Florida Exotic Pest Plant Council, a classification that identifies the most invasive introduced plants in Florida (Langeland and Craddock Burks 1998). The weed is mostly found in central and northern Florida (Gann and Gordon 1998) and has sporadically naturalized in the southern Unit ed States from Texas to North Carolina, (Pemberton and Pratt 2002). It is currently spreading in both Florida and the southern United States. Paederia foetida also is a
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JOURNAL OF THE TORREY BOTANICAL SOCIETY
problem weed in Hawaii, occurring in natural and agricultural areas, particularly areas with horticultural plantings (Pemberton and Pratt 2002). This invasive vine is capable of smoth ering canopy trees as well as understory vegetation. The invasion of skunk vine into diverse native habitats in Florida has led to displacement of native flora, including endan gered Justicia cooleyi Monachino & Leoard (Gann and Gordon 1998, Langeland and Craddock Burks 1998). The main reproductive mode of the species is sexual reproduction (i.e., seeds). The goal of this study is to determine the seed bank longevity of skunk vine. This information can guide land managers to decide whether and how long they need to be concerned with seed banks during their control management efforts in different hab itats. Material and methods. STUDY SPECIES. Pae deria foetida is a member of the Paederiae of the Rubiaceae (Puff 1991), and not closely related to Florida native plants. Plants have axillary or laterally branched double scorpioid cymes. The cylindrical or bell-shaped flowers produce nectar and are pollinated by both introduced honey bees and native pollinators in Florida (Liu et 'al. 2006). The Florida populations are self-incompatible and flower from May to August, during the summer (wet) season. It takes about five months for fruit to mature (Liu and Pemberton, unpublished data). Mature fruits are 4-7 mm greenish brown, round berry with one or two seeds each (Puff 1991, Langeland and Craddock Burks 1998), seeds are ca. 3.5-5.5 X 3.5 mm (Puff 1991). The dispersal mechanism is unknown. However, the thin layer of fleshy endocarp surrounding the seeds may encour age dispersal by animals. EXPERIMENTAL SEED BANK. We collected fresh mature fruits from multiple plants in the Hillsborough River State Park, Hillsbor ough County, in west central Florida, in early November 2004. Experimental seed bank stations were established in three distinct habitats where Paederia foetida plants have become naturalized in the park. These habitats include the interior of a mixed mesic forest dominated by Liquidambar styraciflua L., Magnolia grandiflora L., and Taxodium dis tichum L., the forest edge, and an adjacent open grassland composed of Stenotaphrum
•
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secumdatum, (Walter) Kuntze monoculture. In each of the three habitats, four seed bank stations, spaced 20 m apart, were established. The center of each station was marked with 20 em long camping nails with orange plastic tops. Canopy cover at each station center was measured using a concave spherical densitom eter (Rumble and Anderson 1996), Seed bags (lOx 10 em) were constructed using nylon window screen material with mesh size (0.1 X 0.1 em) fine enough to hold the seeds, but coarse enough to allow penetration of soil and fine litter. Fruits used for the seed bank experiment were from a random mixture of collections from four different plants naturally occurred in the study area. The bags were sealed with hot-glue gun along the edges after 50 visually sound, but otherwise randomly selected fresh fruits were added, placed at the soil surface, and covered lightly with ground litter in the plot. These bags were tied to the center nail with thin metal wires, and became more deeply buried over time by litter fall and soil disturbance by wild animals. Since the fruit, rather than individual seed, is the dispersal unit (i.e., a diaspore), we used fruits as units of the seed bank experiments. We placed six seed bags at each station and a total of 72 bags (6 bags X 4 stations X 3 habitats) for the experiment on November 22, 2004. Two bags from each station were retrieved at the end of year one (December 8, 2005), end of year two (November 15, 2006), and end of year three (Jan 22, 2008). To estimate the initial number of viable seeds in each bag, four samples were randomly select ed, each with 50 visually sound fruits from four different plants used in the field seed bank experiment. We quantified the number of viable seeds by visual assessment (i.e., selecting intact seeds) and with a chemical test. We cut each seed to expose the embryo, and then soaked the cut seeds in 0.1 % solution of 2,3,5 triphenyl-2H-tetrazolium chloride (TIC) for 24 hrs in room temperature. Embryos turning red or reddish pink were considered viable (Kearns and Inouye 1993). Viability of re trieved seeds was evaluated the same way. We also estimated the number of germinated seeds by counting the number of live seedlings (which were found in bags retrieved after the first year), and the number of large seed coat fragments. Geminated seeds will leave cracked seed coat behind and therefore large fragments of seed coats are good proxy of recently
2008]
LIU A"t'
geminated seeds. Ho' as dead seeds disint means that the nun estimated by this number and the met timate the actual nut For this reason we statistics of these germinated seeds wit parisons among habi DATA ANALYSIS. used to determine th canopy cover (trans square root functic Tukey's tests were u comparisons. Repe was used to deter number of viable s one, two, and three The average number bags retrieved at ea time in terval was us square root transfo variance assumption ed as missing data the analyses. Since Sphericity was signil of Sphericity was v results with Greenl which does not assu: Differences in the n bag among the thi interval were anaf OVA. Linear regres proportion of viab formed with root number of years i habitat. The open were combined for' had similar rates 01 SPSS 13.0 (SPSS, 4 analyses. Results. The thre cantly in canopy c( 271.76, P < 0.001). cover (an average 0 (with 68% canopy higher canopy COv! habitat (with < lo/c randomly selected 4.4 (mean:::'::: std. d. start of the expe recover all four see, I
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mtze monoculture. In tats, four seed bank -art, were established. on was marked with Is with orange plastic ich station center was /e spherical densitom 'son 1996). Seed bags istructed using nylon with mesh size (0.1 X hold the seeds, but -enetration of soil and for the seed bank t random mixture of :erent plants naturally area. The bags were along the edges after otherwise randomly : added, placed at the i lightly with ground bags were tied to the tal wires, and became time by litter fall and animals. than individual seed, , a diaspore), we used ed bank experiments. at each station and a gs X 4 stations X 3 tent on November 22, I each station were ear one (December 8, (November 15, 2006), (Jan 22, 2008). To ber of viable seeds in were randomly select Ily sound fruits from I in the field seed bank ified the number of :essment (i.e., selecting chemical test. We cut ie embryo, and then 1.1 % solution of 2,3,5 1 chloride (TTC) for :ure. Embryos turning ere considered viable }93). Viability of re ted the same way. We er of germinated seeds ier of live seedlings igs retrieved after the ber of large seed coat eds will leave cracked refore large fragments d proxy of recently
493
LIU AND PEMBERTON: SEED BANK LONGEViTY OF PAEDERJA
geminated seeds. However, seed coats as well as dead seeds disintegrate with time, which means that the number of geminated seeds estimated by this method is a minimum number and the method can greatly underes timate the actual number of geminated seeds. F or this reason we only reported the basic statistics of these minimum numbers of germinated seeds without any statistical com parisons among habitats. DATA ANALYSIS. One-way ANOVA was used to determine the differences in the mean canopy cover (transformed with arcsine and square root function) among the habitats. Tukey's tests were used for pairwise post-hoc comparisons. Repeated-measures ANOVA was used to determine the differences in number of viable seeds at the end of year one, two, and three across the three habitats. The average number of viable seeds of the two bags retrieved at each seed station and each time interval was used as a replicate and was square root transformed to satisfy the equal variance assumption. Missing bags were treat ed as missing data and were not included in the analyses. Since the Mauchly's Test of Sphericity was significant (i.e., the assumption of Sphericity was violated), we used the test results with Greenhouse-Geisser adjustment, which does not assume Sphericity (Field 2000). Differences in the number of viable seeds per bag among the three habitats at each time interval were analyzed using one-way AN OVA. Linear regression was performed on the proportion of viable seeds remained (trans formed with root function of 4) and the number of years in seed bank within each habitat. The open and forest edge habitats were combined for the regression because they had similar rates of viability loss (see below). SPSS 13.0 (SPSS, Chicago) was used for the analyses.
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FIG. I. Average proportions of viable Paederia foetida seeds (square root transformed) in the fresh (indicated by 0 in the x-axis), one-, two-, three-year old experimental seed banks across three habitats in Central Florida. Note that the forest edge and open habitats have nearly identical profiles. The error bars indicate standard deviations.
edge habitat. However, one station each in the forest interior and open grass habitat disap peared during the three years seed retrieval period. The number of viable seeds decreased 230.685, significantly with time (MS FI.83,12.8 = 702.291, P < 0.001). However, the rate of viability loss was significantly different across the three habitats (MS for interaction between time and habitat = 6.876, F3 .7 , 12 .8 = 20.93, P < 0.001) (Fig. 1). Specifi cally, significantly more seeds survived after one and two years in the soil seed bank in the forest interior than in either the forest edge or the open grass habitats. There were 27 :±: 6.5 or 38% viable seeds per bag at the end of year one in the forest interior, significantly more than that in the forest edge (1.2 :±: 1.0 viable seeds or 2%) or in the open grassland habitat (1.1 :±: 1.3 viable seeds or 2%) (one-way ANOVA, MS = 700.24, F 2 ,8 = 52.879, P < 0.001). There were 3.3 :±: 3.7 (4.7%), 0.3 :±: 0.5 (0.4%), and 0 viable seeds at the end of the second year in the forest interior, the forest edge, and the open habitat, respectively. At the end of the third year there were 0.2 :±: 0.3, 0.1 :±: 0.3, and 0 viable seeds in the forest interior, forest edge, and the open habitat, respectively. The differences in the number of viable seeds Results. The three habitats differed signifi per bag at the end of second and third years cantly in canopy cover (MS = 1.512, F 2 , 9 = across habitats were not significant (MS = 271.76, P < 0.001). Forest interior had higher 10.74, F2 ,7 = 2.693, P = 0.136; and MS = cover (an average of 86%) than did forest edge 0.32, F2 ,7 = 0.453, P = 0.653, respectively). (with 68% canopy cover), and forest edge had The linear regressions on the proportion of higher canopy cover than did open grassland viable seeds (transformed with root function habitat (with < 1% canopy cover). Samples of of 4) and the number of years in seed banks randomly selected 50 fruits contained 70.5 :±: were significant for the open and forest edge 4.4 (mean z; std. deviation) viable seeds at the habitats «proportion of viable seeds)"""(l/4) = start of the experiment. We were able to 0.927 - 0.480 • years, r 2 = 0.844, P < 0.001), recover all four seed bank stations in the forest as well as for the forest interior habitat
?
494
JOURNAL OF THE TORREY BOTANICAL SOCIETY
«proportion of viable seeds)**(1I4) = 1.037 0.307 * years, r' = 0.924, P < 0.001). Based on these estimated relationships, it takes nearly one year to have a 95% reduction of the seed bank in the open or forest edge habitats, but nearly two years in the forest interior habitat. All habitats pooled, the total number of viable seed were 188 (13.8% of the estimated 1470 seeds) at the end of year one, 22, (1.6% of the 1400 seeds) at the end of the year two, and 2 (0.2% of the 1190 seeds) at the end of year three. The variation in total number of initial viable seeds was due to missing bags. In the open grass habitat, the number of germinated seeds found in the bags were 5.1 ::':: 5.9 (mean rt std. dev.) at the end of the first year, 6.5::':: 7.7 at the end of the second year, and 3 ::':: 2.0 at the end of the third year. In the forest edge habitat, the number of germinated seeds were 16.4 ::':: 15.5, 13.9 ::':: 9.5, and 14.4 ::':: 6.4 at the end of each of the three years, respectively. In the forest interior, the number of germinated seed were 10.2 ::':: 4.2,6.2::':: 7.1, and 10.8 ::':: 11.1, in each of the three years respectively. Germinating seeds and seedlings were found at the end of the first year but not in subsequent years.
Discussion. The majority of Paederia foetida seeds do not live past the first year after they reach maturity. However, small proportions of the seeds can retain viability for up to three years, especially seeds in the forest interior areas. Germination is one main reason for the reduction of our experimental seed banks. Although the average detectable numbers of germinated seeds was small (7 to 23% percent of the initial seed bank), germination account ed for a minimum of 60% of the reduction in some stations. The three habitats differed significantly in canopy covers, with forest interior having the highest cover, followed by forest edge and open grass habitat. Although germination behavior of P. foetida was not studied, the greater light availability in the latter two habitats may have induced higher germination rates of P. foetida than in the forest interior, a behavior found in many other species (Baskin and Baskin 1998). This could explain the differential seed bank longevity across the three habitats. In addition, less temperature fluctuations in the forest interior relative to the forest edge and open habitats may have also inhibited germination.
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Seed predation could be another factor for seeds to lose their viability and to disappear from the soil seed bank. Twenty six percent of the fresh seeds were found damaged by an unidentified weevil and its larvae. These seed predators could continue causing damage once the seeds are in the soil. Fungi could infest seed damaged by insects. However, it is not known what percentages of the seeds were lost due to seed predation or disease. Finally, reduction in the seed bank may be a result of an inherent aging process in the seed of this species. Our study showed that Paederia foetida is capable of forming limited short term persis tent seed banks (1 yr < persistence < 4 yrs). This trait is not unique among introduced invasive species. For examples, the majority of alien invasive plants in western Europe have either transient (longevity < 1 yr) or short term persistent (1-4 yrs) seed banks (Thomp son, et al. 1995). In the United States, one invasive woody vine (Celastrus orbiculatus Thumb.) has a transient seed bank, while another (Polygonum perfoliatum L.) has a short term persistent seed bank (Van Clef and Stiles 2001). An invasive tropical shrub, Mimosa pigra L. was found to have transient or short term persistent seed bank depending on site and burial depth (Lonsdale et al. 1988). While a persistent seed bank could buffer local population from extinction, it could dampen population growth in good years (Venable and Brown 1988), by prohibiting seed germination in those good years and subjecting seeds to prolonged exposure to predation, pathogen attack or deep burial (Sarukhan 1974). These penalties could be detrimental to introduced species that often need to increase population size quickly from a few founding individuals. Paederia foetida may avoid these potential penalties by having the majority of seeds germinated within the first year, while allow ing for a limited persistent seed bank that can quickly emerge in response to new distur bance. A transient seed bank is considered an adaptation to relatively stable and predictable environments, while a persistent seed bank is an adaptation to environments subject to unpredictable disturbance (Baskin and Baskin 1989, Thompson 2000). Paederia foetida is found in a wide range of habitats in Florida, from mixed mesic forest. to forest edge, to open habitats. It also grows in citrus groves
2008]
LIU ANI
and around houses. So mixed mesic forest, an others are subject t human or environmen' er, the seed bank bel1 Florida are not neces: ida, because of the : plant's arrival in Flori. Asia, P. foetida also habitats, including 02 banks, as well as hum as edges of agricultura urban and rural area common, it usually , environments they li Florida (Liu and Pern possible that P. foeti« bank longevity acre depending on disturb: In conclusion, giv monitoring period to I from the seed bed elimination of the : foetida) may be eft However, we advise h forest interior areas f elimination treatment ery of P. foetida due' the seed bed. Even tl tions of seeds survive, annual fruit produ typically large. A sn produced tens of clr cluster can contain 11 obs.) and it only ta viable seeds to st: population given tha self-incompatible (Li Liter:
J. M. AND C. C dormancy and gerr bank ecology, p. 5: Parker, and R. L. Si seed banks. Acaden BASKIN, C. C. AND J Ecology, biogeogra mancy and germin Diego, CA. COOK, R. 1980. The p. 107-129. In O. 1 and evolution in 1 Monographs Vol. Press, Berkeley, CP FENNER, M., ed. 19 Regeneration in PI: national, Wallingfc
BASKIN,
t
[VOL. 1:15
)e another factor Cor ity and to disappear l'wenty six percent at ind damaged by an ts larvae. These seed causing damage once . Fungi could infest . However, it is not of the seeds were lost or disease. Finally, k may be a result of s in the seed of this t Paederia foetida is sd short term persis persistence < 4 yrs).
: among introduced iples, the majority of vestern Europe have y < I yr) or short seed banks (ThompUnited States, one
"elastrus orbiculatus t seed bank, while
foliatum L.) has a ed bank (Van Clef asive tropical shrub, nd to have transient eed bank depending .onsdale et al. 1988). nk could buffer local m, it could dampen j years (Venable and mg seed germination subjecting seeds to oredation, pathogen rukhan 1974). These iental to introduced increase population ounding individuals. -oid these potential majority of seeds st year, while allow t seed bank that can nse to new distur k is considered an
able and predictable
.sistent seed bank is mments subject to (Baskin and Baskin
Paederia foetida is
habitats in Florida, , to forest edge, to )WS in citrus groves
2008]
f
I
LIU AND PEMBERTON: SEED BANK LONGEVITY OF PAEDERIA
and around houses. Some habitats, such as the mixed mesic forest, are relatively stable, while others are subject to more unpredictable human or environmental disturbance. Howev er, the seed bank behaviors of P. foetida in Florida are not necessarily adaptive in Flor ida, because of the relative recency of the plant's arrival in Florida. In its native range in Asia, P. foetida also occurs in a variety of habitats, including natural areas along river banks, as well as human disturbed areas such as edges of agricultural fields and on fences in urban and rural areas, and while it can be common, it usually does not dominate the environments they live like they can do in Florida (Liu and Pemberton, pel's. obs.). It is possible that P. foetida also has variable seed bank longevity across its native habitat, depending on disturbance regime. In conclusion, given our data, a short monitoring period to detect seedlings emerging from the seed bed (i.e., two years post elimination of the adult population of P. foetida) may be effective for open areas. However, we advise land managers to monitor forest interior areas for up to four years after elimination treatments for the possible recov ery of P. foetida due to germination of seed in the seed bed. Even though very small propor tions of seeds survived beyond three years, the annual fruit production of P. foetida is typically large. A small patch of plants can produced tens of clusters of fruits, and each cluster can contain hundreds of berries (pel's. obs.) and it only takes a minimum of two viable seeds to start a new reproducing population given that P. foetida in Florida is self-incompatible (Liu et al. 2006).
Literature cited BASKIN,.T. M. AND C. C. BASKIN. 1989. Physiology of dormancy and germination in relation to seed bank ecology, p. 53-66. In M. A. Leek, V. T. Parker, and R. L Simpson [eds.], Ecology of soil seed banks. Academic Press, San Diego, CA. BASKIN, C. C. AND .T. M. BASKIN. 1998. Seeds: Ecology. biogeography, and evolution of dor mancy and germination, Academic Press, San Diego, CA. COOK, R. 1980. The biology of seed in the soil, p. 107-129. Tn O. T. Solbrig [ed.], Demography and evolution in plant populations. Botanical Monographs Vol. 15. University of California Press, Berkeley, CA. FENNER, M., ed. 1992. Seeds: the Ecology of Regeneration in Plant Communities. CAB Inter national, Wallingford, U.K. 373 p.
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FIELD, A. 2000. Discovering statistics using SPSS for Windows. SAGE Publications, London, UK. GAc.N. G. AND D. GORDON. 1998. Pacdcria [oetida (skunk vine) and P. cruddasiana (sewer vine): Threats and management strategies. Nat. Areas .T. 18: 169-174. KEARNS, C. A. AND D. W. INOUYE. 1993. Techniques for Pollination Biologists. University of Colo rado Press, Niwot, CO. 583 p. KRINKE, L., L. MORAVcovA, P. PYSEK, V. .TAROSIK,.T. PERGI., AND 1. PERGLOVA. 2005. Seed bank of an invasive alien, Heracleum mantegazzianum, and its seasonal dynamics. Seed Sci. Res. 15: 239-248. LANGELAND, K. A. AND K. CRADDOCK BURKS, eds. 1998. Identification and Biology of Non-native Plants in Florida's Native Areas. University of Florida, Gainesville, FL. LECK, M. A. AND K . .T. GRAVELINE. 1979. The seed bank of a freshwater tidal marsh. Am. .T. Bot. 66: 1006-1015. LIU, H., E. MENGES, AND P. F. QUINTATA-AsCENCIO. 2005. Population viability analysis of Chamae crista keyensis-Stochastistic model simulations on the effect of different fire regimes. Ecol. Appl. 15: 210-221. LIU, H., R. W. PEMBERTON, AND P. STILING. 2006. Reproductive biology and pollination of skunk vine (Paederia foetidai, an exotic invasive species of Florida. J. Torrey Bot. Soc. 133: 304-311. LONSDALE, W. M., K. L. S. HARLEY, AND .T. D. GILLETT. 1988. Seed bank dynamics in Mimosa pigra, an invasive tropical shrub. .T. Appl. Ecol. 25: 963-976. MEYER, S. E., D. QUINNEY, AND .T. WEAVER. 2006. A stochastic population model for Lepidium papil liferum (Brassicaceae), a rare desert ephemeral with a persistent seed bank. Am. J. Bot. 93: 891-902. MURDOCH, A. .T. AND R. H. ELLIS. 1992. Longevity, viability, and dormancy, p. 193-229. In M. Fenner [ed.], Seeds: the ecology of regeneration in plant communities. CAB International, Wall ingford, U.K. NAUMANN,.T. C. AND D. R. YOUNG. 2007. Relation ship between community structure and seed bank to describe successional dynamics of an Atlantic Coast maritime forest . .T. Torrey Bot. Soc. 134: 89-98. OGDEN, J. A. E. AND M. REJMANEK. 2005. Recovery of native plant communities after the control of a dominant invasive plant species, Foeniculum vulgare: Implications for management. BioI. Conserv. 125: 427~39. PFMBERTON, R. W. AND P. D. PRATT. 2002. Skunk vine (Paederia foetida), p. 343-351. In R. Van Driesche, B. Blossey, M. Hoddle, S. Lyon, and R. Reardon [eds.], Biological Control of Invasive Plants in the Eastern United States. US Forest Service Forest Health Technology Enterprise Team-2002-04, Morgantown, WV. PRIESTLEY, D. A. 1986. Seed aging-Implications for seed storage and persistence in the soil. Com stock Publishing Associates, Ithaca, NY. 304 p. PUFF, C. 1991. Revision of the genus Paederia in Asia, p. 207-289. In C. Puff [ed.], The Genus Paederia L. (Rubiaceae-Paederieae): A Multidis ciplinary Study. Opera Botanica Be1gica 3.
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