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Department of Biological Sciences, Mount Holyoke College, South Hadley, Massachusetts 01075-6418 USA
Received for publication February 29, 2000. Accepted for publication May 30, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSTUDY SPECIES AND COLLECTION...MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: dormancy • germination • latitude • morphophysiological dormancy • Sarracenia • Sarraceniaceae • seed size
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSTUDY SPECIES AND COLLECTION...MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Fenner, 1983
; Thompson, 1987
), and their importance to plant fitness and are widely appreciated (e.g., Leon, 1985
; Venable, 1985, 1989
; Foster, 1986
; Lord, Westoby, and Leishman, 1995
; Venable et al., 1998
; Higgins and Richardson, 1999
). Comparative analyses of seed size (e.g., Foster, 1986
; Mazer, 1989
; Leishman, Westoby, and Jurado, 1995
; Lord, Westoby, and Leishman, 1995
; Venable et al., 1998
) and seed germination (e.g., Garwood, 1983, 1989
; Leon, 1985
) have been especially useful in illustrating not only the broad range of seed traits that occur within and among taxa, but also the environmental and phylogenetic constraints that limit variability in characters. Seed traits, including seed size, length of dormancy, germination requirements, and germination rate, often vary in parallel and are thought to comprise co-evolved complexes or life history strategies for many species (e.g., Harper, 1977
; Foster, 1986
; Venable and Brown, 1988
; Evans and Cabin, 1995
; Rees and Westoby, 1997
). These co-evolved complexes may be correlated with relatedness among species (Mazer, 1989
). Alternatively, locally strong environmental forces could decouple seed traits from phylogeny (Leishman, Westoby, and Jurado, 1995
; Lord, Westoby, and Leishman, 1995
). In this study, I examine seed size, germination, and dormancy and their covariation across a latitudinal gradient among a set of closely related species in the genus Sarracenia. An explicit goal of this study is to test whether seed traits are useful taxonomic characters for distinguishing among these species, or whether local environmental conditions that change predictably across a latitudinal gradient have resulted in geographic patterns among seed traits that are independent of an existing phylogeny of Sarracenia species.
Germination biology of carnivorous plants, including Sarracenia (the pitcher plant), has received little attention from botanists or plant ecologists (Baskin and Baskin, 1998
), although carnivorous plant collectors and enthusiasts have a rich lore of suggestions and recipes for germination of these plants (on-line Carnivorous Plant Archive at http://randomaccess.unm.edu/www/cp/cparchive.html). The lack of studies on the germination of carnivorous plants is in striking contrast to the more extensive literature on their morphological adaptations for carnivory (e.g., Darwin, 1875
; Arber, 1941
; Juniper, Robins, and Joel, 1989
) and the community of invertebrates that live within the pitcher-shaped leaves of Sarracenia, Darlingtonia (both Sarraceniaceae), and Nepenthes (Nepenthaceae) (reviews in Higley, 1885
; Bradshaw, 1983
; Fish, 1983
). Within the genus Sarracenia, the germination requirements of only one species, S. purpurea, have been carefully studied (Mandossian, 1966
; Gotsch and Ellison, 1998
). Sarracenia purpurea is the most widespread species in the genus, occurring throughout Canada and the eastern United States. The remaining species in the genus occur only in the southeastern United States, and there is no a priori reason to suspect that their germination requirements are identical to those of S. purpurea.
Relying on Mandossian's (1966)
study, Baskin and Baskin (1998)
suggested that all Sarracenia species have nondeep morphophysiological dormancy (MPD), in which the embryos are underdeveloped at dehiscence and the radicle, once developed, is prevented from emerging because of physiological inhibition (definition after Nikolaeva, 1977
; Baskin and Baskin, 1998
). Gotsch and Ellison's (1998)
observations on embryo development at time of dehiscence and germination requirements confirmed that S. purpurea seeds have nondeep MPD, but data from other species in this genus are unavailable. Several authors have observed dramatic increases in population size of southern Sarracenia species following fires (McDaniel, 1971
; Weiss, 1980
; Barker and Williamson, 1988
; Brewer, 1999
), suggesting that some southern species could require fire for germination. Even if all Sarracenia species have nondeep MPD, length of dormancy could be shorter among species growing in the southeastern United States relative to S. purpurea at the northern limits of its range. Both increases in mean temperature and decreases in number of subfreezing days could select for shorter dormancy periods among southern species (Baskin and Baskin, 1998
). To test these hypotheses, I examined the germination requirements of eight of the nine species of Sarracenia and of both subspecies (and three of the four subspecific varieties) of S. purpurea.
Seed characteristics, including seed size and germination requirements, could also be helpful in resolving systematic and phylogenetic questions within this genus. Taxonomy of Sarracenia is based principally on the morphology of the carnivorous, pitcher-shaped leaves (Macfarlane, 1908
; McDaniel, 1971
; Schnell and Krider, 1976
; Case and Case, 1976
; Naczi et al., 1999
). The Sarraceniaceae are clearly a monophyletic group (Albert, Williams, and Chase, 1992
), but recent attempts to resolve interspecific relationships using molecular techniques have provided little resolution among the species of Sarracenia (Bayer, Hufford, and Soltis, 1996
), although isozyme analysis (Godt and Hamrick, 1996, 1998a, b
) has tended to support subspecific-level distinctions proposed by earlier authors (Case and Case, 1976
; Schnell, 1979
) on morphological grounds. McDaniel (1971)
asserted that seed size was a diagnostic characteristic and could be used to distinguish among species, but presented insufficient data to test this hypothesis. I therefore also collected data on seed size, and examined interspecific relationships in seed size and germination requirements in the context of prior systematic work in Sarracenia.
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STUDY SPECIES AND COLLECTION INFORMATION |
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TOPABSTRACTINTRODUCTIONSTUDY SPECIES AND COLLECTION...MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Schnell, 1979
; Godfrey and Wooten, 1981
). Within S. purpurea, I studied germination of 11 populations of S. purpurea ssp. purpurea (Raf.) Wherry, one of S. purpurea ssp. venosa var. venosa (Raf.) Fernald, and one of S. purpurea ssp. venosa var. burkii Schnell. Seeds of the federally endangered S. oreophila (Kearney) Wherry were unavailable. All but S. purpurea ssp. purpurea are found only in the southeastern United States, where they occur in wet pine savannas, bogs, or pineland seepage slopes (Godfrey and Wooten, 1981
). Sarracenia alata occurs in southwestern Alabama, southern Mississippi, and Louisiana and extends into eastern Texas. Sarracenia leucophylla and S. psittacina both occur in southern Georgia, northern Forida, southern Alabama, and southeastern Mississippi. Sarracenia minor and S. rubra occur along the southeastern coastal plain, from southern North Carolina to the central peninsula of Florida. Sarracenia flava occurs sympatrically with S. minor and S. rubra, but extends farther northwards into southeastern Virginia. The federally endangered species Sarracenia jonesii was separated from the S. rubra complex by Case and Case (1976)
and is known from only ten populations in North and South Carolina (Godt and Hamrick, 1996
). Its identity as a distinct species is supported by isozyme studies (Godt and Hamrick, 1996
). Sarracenia purpurea is a common and widespread bog species that ranges from Newfoundland westward across Canada to Manitoba, southward along the eastern United States to Florida and Mississippi, as well as into Ohio, Illinois, Iowa, and northern Indiana.
Schnell (1979)
divided S. purpurea into two subspecies, ssp. purpurea and ssp. venosa (Raf.) Wherry. Sarracenia purpurea ssp. purpurea, the "northern" pitcher plant, grows as far south as Maryland, whereas ssp. venosa, the "southern" pitcher plant, occurs from Maryland (possibly extending north into southern New Jersey) southward. These two subspecies of S. purpurea are sympatric in southern Maryland and northern Virginia (Wherry, 1933
), although recent field observations on the degree of sympatry are lacking. Schnell later subdivided ssp. venosa into three varieties: var. venosa that occurs on the Atlantic coastal plain, var. montana Schnell & Determann that occurs in the southern Appalachian Mountains of Georgia and the Carolinas, and var. burkii that occurs on the Gulf coastal plain from the Florida panhandle westward into Louisiana (Schnell, 1993
; Schnell and Determann, 1997
). Gleason and Cronquist (1991)
rejected the subspecific and varietal designations of Schnell (1979)
, and recognized only two varieties of S. purpurea, the "northern" pitcher plant, S. purpurea var. purpurea and the "southern" pitcher plant, S. purpurea var. venosa. Most recently, isozyme analysis (Godt and Hamrick, 1998b
) has supported the subspecific designations proposed by Schnell (1979)
, and morphological analysis has been used to further elevate S. purpurea ssp. venosa var. burkii to the species level—S. rosea Naczi, Case & Case (Naczi et al., 1999
). To add insult to nomenclatural injury, Reveal (1993)
pointed out that the correct name for the northern pitcher plant should be S. purpurea var. terrae-novae de la Pylaie and that the correct name for var. venosa actually should be var. purpurea! To avoid confusion with common usage, I follow current convention here and refer to the northern pitcher plant as S. purpurea ssp. purpurea and the southern pitcher plant as S. purpurea ssp. venosa, and refer to the varieties of ssp. venosa where necessary.
I used wild-collected seeds for all species except S. jonesii and S. rubra, for which I obtained outcrossed seeds from cultivated plants. Seeds of Sarracenia flava were collected from a bog in Miramar Beach, Walton County, Florida, USA in July 1997. Seeds of Sarracenia minor were collected from a small bog in Jedborg, Dorchester County, South Carolina, USA in September 1997. Seeds of S. leucophylla were collected from another bog in Walton County, Florida in September 1997. Seeds of S. alata and S. psittacina were collected from a bog in Stone County, Mississippi, USA in November 1997. Seeds of S. rubra and S. jonesii were collected in September 1998 from outcrossed-plants grown by David Mellard in Atlanta, Georgia, USA.
For intraspecific comparisons within the widespread S. purpurea, I studied germination of seeds from 13 populations (Table 1). Wild-collected seeds of S. purpurea were obtained between September and November 1998. Latitude and longitude of each population were recorded using GPS. Elevation of each site (metres above sea level) was determined from USGS topographic maps.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONSTUDY SPECIES AND COLLECTION...MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Seed size (length, width) was determined for 200 seeds per species or population using an ocular micrometer in a Willd dissecting scope at 50x magnification. Twenty seeds per species and population were also weighed (±0.01 mg) to determine length–mass relationships.
Seeds of each species and population were tested for morphological dormancy (sensu Baskin and Baskin, 1998) by attempting to germinate freshly collected seeds. Under a laminar-flow hood, ten seeds were surface-sterilized (10% bleach solution, followed by a triple rinse with distilled water), then placed in sterile 9 cm diameter petri dishes between two sheets of sterilized filter paper and moistened with 6 mL of sterile distilled water. Petri dishes were placed on a warm (20°C) bench in high light (PAR [Photosynthetic Active Radiation] > 1000 µmol·m-2·sec-1), long-day (14 h) conditions in the Mount Holyoke College greenhouse. Seeds were checked daily for 60 d for germination (radicle emergence); 2 mL of distilled water were added to each dish every 2 d to prevent desiccation. Ten additional seeds of each species and population were dissected to examine the state of the embryo upon dispersal. Dissected embryos were stained with tetrazolium to determine viability (Lakon, 1949
). The remaining seeds were stored dry at 4°C prior to using them in the experiments involving stratification (cold and moist pretreatment) or scarification.
These seeds were then divided randomly into five germination treatments: (1) no pretreatment other than cold, dry storage (dry treatment); (2) cold, dry storage plus scarification in 1 mol/L H2SO4 for 60 sec followed by a triple rinse in distilled water (scarification treatment); (3) seeds moist-chilled at 4°C for 2 wk (short stratification treatment); (4) seeds moist-chilled at 4°C for 4 wk (intermediate stratification treatment); (5) seeds moist-chilled at 4°C for 5 wk (long stratification treatment). The dry and stratification treatments tested for the need for a period of additional embryo development, whereas the scarification treatment tested for the impermeability of the seed coat. Cold, moist stratification also is a common, dormancy-breaking treatment for seeds with MPD (Baskin and Baskin, 1998
). Because no germination occurred in the scarification treatment in 1997, this treatment was eliminated for the species from which seeds were collected and studied in fall 1998 (S. jonesii, S. rubra, all populations of S. purpurea).
For stratification, seeds were (1) surface-sterilized for 60 sec in a 10% bleach solution; (2) triple rinsed in distilled water; (3) placed in sterile 9 cm- diameter petri dishes between two sheets of sterilized filter paper; (4) moistened with 6 mL of sterile distilled water; (5) placed in a dark refrigerator at 4°C. All plating was done aseptically under a laminar-flow hood to minimize possibility of fungal or mold growth. For each treatment x species or population combination, I used five replicate plates of ten seeds. Petri dishes were placed on greenhouse benches in full sun (maximum PAR 1500 µmol·m-2·sec-1). Because germination experiments were conducted in the winter, supplemental lighting (sodium flood lights) was used to maintain a day length of 14 h. Greenhouse temperature (20°C) and relative humidity (70%) were maintained by computer controllers. Temperatures within the petri dishes were not monitored, although they probably exceeded ambient temperature. Once they were in the greenhouse, I added 2 mL of distilled water to each plate every 48 h to prevent desiccation. Plates were examined every 2 d for 34 d for evidence of radicle emergence.
Statistical analysis
Data were analyzed using ANOVA and regression procedures in Systat version 8.0 (SPSS Inc., Chicago, Illinois, USA). For interspecific comparisons, I used the Hawley Bog population of S. purpurea ssp. purpurea (chosen at random from among the northern populations) and the Appalachicola (Florida) population of S. purpurea ssp. venosa. Although Hawley Bog is not at the northern limit of the range of S. purpurea, its high elevation gives it an apparent latitude well north of its location in northwestern Massachusetts (Table 1). The Appalachicola population is assuredly a population of S. purpurea ssp. venosa, whereas the Arden Bog (Maryland) population likely is S. purpurea ssp. venosa (personal observation), but is within the zone of sympatry of the two subspecies of S. purpurea (Wherry, 1933
). All 13 populations of S. purpurea were used for the intraspecific comparisons.
Results are presented as means ± 1 SE throughout. Comparisons were made both among and within species (or populations) using a nested ANOVA design, for which the factors were species (or populations) and treatment nested within species (or populations). I compared time (days) to first observed germinant, time to 50% germination (50% of the actual number of seeds that germinated in a given species or population x treatment combination), total number of seeds germinated after 34 d, time to maximum germination, and germination rate (germinants per day, calculated as maximum number of germinants / [days to maximum germination - days to initial germination]) across species or populations (main effect in the ANOVA), and among treatments within species or populations (nested effect in the ANOVA). All data were examined to ensure that they conformed to assumptions of parametric ANOVA. Only germination rate required transformation (to their natural logarithm) prior to analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSTUDY SPECIES AND COLLECTION...MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Interspecific variability in seed size
Sarracenia species produced very small, obovate, light brown seeds that ranged from 1.2 to 2.7 mm in length (Table 2), and 0.8–1.8 mm in width. Five seed-size groups (based on seed length) were apparent, and were distinguished using Fisher's Least Significant Difference post-hoc test for multiple comparisons among means. The largest seed group consisted of S. flava and S. leucophylla and the smallest seed group consisted of S. jonesii, S. rubra, S. minor, and S. psittacina. Seeds of S. alata and the two subspecies of S. purpurea were intermediate in size, but were all statistically dissimilar in length (Table 2). Seed length and width were weakly but significantly correlated (r = 0.24, P < 1 x 10-15). Seed length and width were significant predictors of seed mass (mass in g = 0.0004 x length x width - 0.003) and this regression explained 56% of the observed variance in seed mass.
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= 2.09, SE = 0.004) and 0.6–1.7 mm in width ( = 1.18, SE = 0.002; Table 3). Seed size varied significantly among populations (F12, 3689 = 184.7, P < 0.0001; Table 3). Although intersite differences in seed size were observed, this variability did not show any relationship either with absolute latitude (r2 = 0.13, P = 0.23) or with latitude corrected for elevation (100 m elevation 
1° latitude) (r2 = 0.04, P = 0.50). Variability in seed size within S. purpurea exceeded the variability in seed size observed across all eight species studied.
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Subsequent pairwise comparisons (Fisher's Least Significant Difference test) among treatments within species illustrated that these significant effects were due to strong effects of treatment on a few species. Onset of germination was significantly accelerated by increasing stratification from 2 to 4 wk in S. minor, S. jonesii, and both subspecies of S. purpurea. Onset of germination showed further acceleration with additional stratification (6 wk) only in S. jonesii and both subspecies of S. purpurea. In contrast, onset of germination was significantly slowed with increasing stratification in S. leucophylla. Time to 50% germination was accelerated by increasing stratification from 2 to 4 wk in S. jonesii, S. rubra, and S. purpurea ssp. venosa. No further effect on time to 50% germination was found by increasing stratification time to 6 wk. Total numbers of germinated seedlings of S. flava, S. minor, and both subspecies of S. purpurea increased significantly as stratification time increased from 2 to 4 wk, but no additional enhancement was observed by increasing stratification time to 6 wk. Maximum number of S. leucophylla seedlings occurred with 4 wk stratification and was lowest in the 6-wk stratification treatment. Germination rate increased significantly between 2- and 4-wk stratification time only in S. rubra and both subspecies of S. purpurea, and only S. purpurea ssp. purpurea showed a further increase in germination rate with the 6-wk stratification period. Seed size was not correlated with germination requirements (P = 0.79, Spearman correlation test on ranked seed size group vs. ranked optimal pretreatment time [columns 3 and 5 of Table 2]).
Intraspecific variability in germination
Germination trajectories of all populations of S. purpurea are illustrated in Fig. 2 (that of S. purpurea ssp. purpurea var. burkii is in Fig. 1). Analysis of variance indicated significant differences among populations (main effect) in: time to onset of germination (F12,26 = 17.7, P < 0.001); time to 50% germination (F12,26 = 22.7, P < 0.001); maximum number of seeds germinated during the experiment (F12,26 = 19.0, P < 0.001); time to maximum germination (F12,26 = 8.6, P < 0.001); and germination rate (F12,26 = 4.6, P < 0.001). Similarly, ANOVA indicated significant differences among treatments within populations (nested effect) in: time to onset of germination (F26, 147 = 4.4, P < 0.001); time to 50% germination (F26, 147 = 3.6, P < 0.001); maximum number of seeds germinated during the experiment (F26, 147 = 16.9, P < 0.001); time to maximum germination (F26, 147 = 3.1, P < 0.001); and germination rate (F26, 147 = 3.2, P < 0.001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSTUDY SPECIES AND COLLECTION...MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Barker and Williamson, 1988
; Brewer, 1999
). Cluster analysis of the eight species and two subspecies of S. purpurea based on their average germination rates (time to onset, time to 50% germination, time to maximum germination, germination rate) illustrate strong geographic groupings (Fig. 3). The northern pitcher plant, S. purpurea ssp. purpurea, and the coastal plain species, S. rubra, clearly separate out from the rest of the species. The coastal plain species with broad ranges, S. minor, S. jonesii, S. flava, and S. purpurea ssp. venosa, form a second cluster. The three southern species occur in two clusters, one formed by S. leucophylla and S. psittacina and the other by S. alata alone. Addition of seed size data into the cluster analysis (tree not shown) maintains the tree topology, but the positions of S. flava and S. psittacina are interchanged.
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). Cluster analysis of 12 of the 13 populations of S. purpurea based on their average germination rates (time to onset, time to 50% germination, time to maximum germination, germination rate) illustrate the geographic heterogeneity in germination characteristics within this species (Fig. 4). The Appalachicola population of S. purpurea ssp. venosa (var. burkii) was not included in this cluster, as preliminary analysis indicated that it was a strong outlier in all parameters, and its inclusion in the cluster analysis resulted in virtually no discrimination among the other 12 populations. This cluster analysis, together with the data in Table 3, do not suggest that the Maryland population, identified on the basis of field characteristics as S. purpurea ssp. venosa var. venosa, is distinguishable from S. purpurea ssp. purpurea on the basis of seed size and germination characteristics.
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). Within-species variability in seed size overlaps and exceeds between-species variability in seed size, and among species, seeds of several species are similarly sized (Tables 2 and 3).
At the species level, the groupings of Sarracenia based on germination characteristics (Fig. 3) differ from a cladistic analysis of these species based on ITS-1 and ITS-2 sequences (Bayer, Hufford, and Soltis, 1996
). Their phylogenetic analysis suggested S. alata as the sister group of a large subclade composed of the other Sarracenia species. Within this subclade, they identified two monophyletic groups: one consisting of S. purpurea (probably ssp. purpurea) and S. leucophylla, and the other consisting of S. flava, S. minor, and S. psittacina. Sarracenia rubra was not assignable to either of these groups (Bayer, Hufford, and Soltis [1996
] included S. jonesii within S. rubra). Support for the existence of the two monophyletic groups, however, was not strong (bootstrap value of 36% for the S. purpurea–S. leucophylla group and 70% for the S. flava–S. minor–S. psittacina group; Bayer, Hufford, and Soltis, 1996
). Lack of congruence between germination characteristics and the molecular phylogeny of these species is consistent with the hypothesis that as Sarracenia species migrated north following the deglaciation at the end of the Pleistocence, their dormancy requirements evolved in response to the increasingly long winters associated with higher latitudes. The observed decoupling of germination ecology and seed traits from Sarracenia phylogeny also suggests that the species had diversified prior to deglaciation.
In contrast, the intraspecific groupings of populations of S. purpurea support current hypotheses concerning the relationships of the subspecies and varieties. In both the interspecific analysis (Fig. 3) and the intraspecific analysis (Fig. 4), S. purpurea ssp. venosa var. burkii is clearly separate and distinct from the other populations of S. purpurea. Naczi et al. (1999)
proposed assigning this variety to a new species, S. rosea, based on flower color, scape height, and leaf morphology. Godt and Hamrick (1998b)
, using isozymes, clearly identified this variety as distinct from other varieties and subspecies of S. purpurea. On the basis of germination properties, S. purpurea ssp. venosa var. burkii is more closely allied with other southern coastal plain species than it is to S. purpurea ssp. purpurea or to the more northern S. purpurea ssp. venosa var. venosa. Thus, these studies on morphology, isozymes, and germination all point to a clearly distinctive entity of S. purpurea along the Gulf Coast of the United States. The nesting of the Arden Bog population of S. purpurea ssp. venosa var. venosa firmly within more northerly populations of S. purpurea ssp. purpurea implies either that the distinction between these two subspecies is not useful (as suggested by Gleason and Cronquist, 1991
), that this population is actually S. purpurea ssp. purpurea, or that extensive hybridization between the subspecies has occurred in this putative zone of sympatry. Isozyme studies (Godt and Hamrick, 1998b
) suggest that S. purpurea ssp. venosa var. venosa is difficult to distinguish from S. purpurea ssp. purpurea. Further field work, common garden experiments, and genetic analysis on S. purpurea ssp. purpurea and ssp. venosa var. venosa are required to clarify their range limits and relationships.
These data illustrate that a comparative analysis of seed germination, in groups for which some phylogenetic information exists, can be used to test hypotheses about the relative strength of environmental factors and phylogeny on the evolution of seed traits. The results presented here support earlier studies that pointed to strong environmental control on seed characters (e.g., Leishman, Westoby, and Jurado, 1995
; Lord, Westoby, and Leishman, 1995
; Baskin and Baskin, 1998
). Although seed characters show some degree of covariance among species, this covariance appears to be related more to geography than to phylogeny. Additional comparative studies on phylogenetically well-known groups with broad geographical distributions are needed to determine the relative importance of local environment and phylogenetic history on early life histories of plants.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONSTUDY SPECIES AND COLLECTION...MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bradshaw, W. E. 1983 Interaction between the mosquito Wyeomyia smithii, the midge Metriocenemus knabi, and their carnivorous host Sarracenia purpurea. In J. H. Frank and L. P. Lounibos [eds.], Phytotelmata: terrestrial plants as host for aquatic insect communities, 161–189. Plexus Publishing, Medford, New Jersey, USA
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———. 1989 Tropical soil seed banks: a review. In M. A. Leck, V. T. Parker, and R. L. Simpson [eds.], Ecology of soil seed banks, 149–209. Academic Press, San Diego, California, USA
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———, and ———. 1998a Allozyme diversity in the endangered pitcher plant Sarracenia rubra ssp. alabamensis (Sarraceniaceae) and its close relative S. rubra ssp. rubra. American Journal of Botany 85: 802–810[Abstract]
———, and ———. 1998b Genetic divergence among infraspecific taxa of Sarracenia purpurea. Systematic Botany 23: 427–438[CrossRef][ISI]
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dry treatment; • scarification only; 
short stratification; 
intermediate stratification; 
long stratification
