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Systematics and Phytogeography |
2Harvard University, Harvard Forest, P.O. Box 68, Petersham, Massachusetts 01366 USA; 3Department of Biological Science, Florida State University, Tallahassee, Florida 32306 USA; 4Department of Biology, University of Vermont, Burlington, Vermont 05405 USA
Received for publication February 9, 2004. Accepted for publication August 3, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: carnivorous plants • geography • morphology • phylogeography • Sarracenia purpurea • Sarracenia rosea
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Schlichting and Pigliucci, 1998
). Morphological variation and geographical separation among populations are also prerequisite to the formation of subspecies and species (Losos and Glor, 2003
). Phylogeographic analysis can be used to illuminate the interplay of climate, geographical history, and evolutionary dynamics in generating new taxa (Avise et al., 1987
; Templeton et al., 1995
; Arbogast and Kenagy, 2001
).
The North American pitcher plants in the genus Sarracenia exemplify the joint roles of these processes. All of the species are sympatric in the southeastern United States, a hot spot for biological diversity in North America (Peet and Allard, 1993
; Donovan et al., 2000
; Maskas and Cruzan, 2000
). Since the end of the Pleistocene glaciation ca. 10 000 yrs ago, one species, Sarracenia purpurea L., has rapidly extended its range much further north, and its range now spans more than 30° of latitude and 70° of longitude. Pitcher morphology varies greatly, both within and among species, reflecting differences among sites in growing conditions (Ellison and Gotelli, 2002
; Schnell, 2002
) as well as genetic differentiation (Godt and Hamrick, 1999
).
Sarracenia purpurea sensu lato (sensu Gleason and Cronquist, 1991
) is a long-lived, rosette-forming, perennial carnivorous plant that grows in sphagnum bogs, poor fens, seepage swamps, and pine savannas of the eastern United States and Canada (Schnell, 2002
). Its broad geographic range includes the entire coastal plain of the eastern United States (the Florida panhandle to Cape Cod), New England and the northern United States westward through the Great Lakes region, and all of Canada east of the Continental Divide (Schnell, 2002
; Buckley et al., 2003
). Not surprisingly, there is pronounced morphological variability in S. purpurea across its range, and botanists have named two subspecies based on quantitative and qualitative differences in pitcher morphology (Schnell, 1979
, 2002
).
The two subspecies of S. purpurea, S. purpurea subsp. purpurea and S. purpurea subsp. venosa, are distinguished by the shape of the pitcher hood, the ratio of pitcher length to the diameter of the pitcher opening, the presence or absence of hairs on the outside of the pitcher, and flower color (Schnell, 2002
). The size and shape of pitchers, however, can change dramatically in response to local environmental conditions (Mandossian, 1966
; Ellison and Gotelli, 2002
), and flower color is variable. Hence, Gleason and Cronquist (1991)
did not accept the subspecies distinction and considered these two subspecies to be only geographic varieties.
The geographic boundary separating S. purpurea subsp. purpurea and S. purpurea subsp. venosa occurs in southern Delaware and northern Maryland and is defined by the southernmost extent of the Pleistocene glaciation: S. purpurea subsp. purpurea grows in formerly glaciated areas, whereas S. purpurea subsp. venosa grows only in unglaciated areas. Historical biogeography suggests that S. purpurea subsp. purpurea is derived from S. purpurea subsp. venosa, the former having colonized northern latitudes after glaciation. Furthermore, allozyme analysis suggests that S. purpurea subsp. venosa and its varieties are more genetically similar to each other than any of them are to S. purpurea subsp. purpurea (Godt and Hamrick, 1999
).
A disjunct group of populations of S. purpurea subsp. venosa occurs on the Florida panhandle. This population has been described as a separate variety, S. purpurea subsp. venosa var. burkii Schnell (Schnell, 1993
), but based on pitcher morphology, flower color, and height of the flower scape, Naczi et al. (1999)
proposed that it be considered an entirely separate species, S. rosea Naczi, Case & Case. Further, allozyme analysis illustrates that S. purpurea subsp. venosa var. burkii is genetically distinct from both S. purpurea subsp. purpurea and S. purpurea subsp. venosa. Covariance of environmental conditions and morphology has not been assessed for either S. purpurea subsp. venosa or S. purpurea subsp. venosa var. burkii, in contrast to the detailed work on the covariance between environmental conditions and morphology of S. purpurea subsp. purpurea (Mandossian, 1966
; Ellison and Gotelli, 2002
). Taxonomic distinctions that are made based on morphology and do not account for the entire range of variability in a taxon may lead to its being split unnecessarily into multiple taxa.
We characterized patterns of variation in vegetative morphology of S. purpurea subsp. purpurea, S. purpurea subsp. venosa, and S. purpurea subsp. venosa var. burkii throughout their range in North America. We used these data, along with detailed environmental measurements, to partition morphological variation among geographic/climatic and environmental factors. We asked three questions:
) that S. purpurea subsp. venosa var. burkii be considered a separate species, S. rosea?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Because we sampled after plants had flowered, we did not collect data on flower color or shape.
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At each site, we laid a 1-m-wide belt transect across the longest axis of the Sarracenia population. If this axis was longer than 100 m, we used a 100-m transect centered on this axis. This transect was then divided into 20 equally spaced marks (maximum of 5 m apart), and the nearest pitcher plant to each mark was identified. For each of these 20 plants, we measured the maximum diameter of the rosette. For the first (largest) pitcher of the current year, we measured (±1 mm) the pitcher length, diameter of the pitcher mouth, the thickness of the pitcher lip, the maximum width of the pitcher, and the width of the wing (keel); see Ellison and Gotelli (2002)
for an illustration of these measurements. The thickness of the lip of the pitcher and the ratio of pitcher length to mouth diameter have been used as key characters to distinguish among S. purpurea subsp. purpurea, S. purpurea subsp. venosa, and S. purpurea subsp. venosa var. burkii (Naczi et al., 1999
; Schnell, 2002
).
Because size and shape of S. purpurea subsp. purpurea pitchers are known to vary with light and vegetation cover (Mandossian, 1966
), we visually estimated percentage cover of vegetation in a 1-m2 quadrat centered on each plant. Because there was no consistent set of co-occurring species across the range of S. purpurea, we distinguished percentage cover of functional groups: trees, shrubs, terrestrial or aquatic forbs, graminoids, ferns, lycopods, Sphagnum, other bryophytes, fungi, and lichens.
Relative wing width of pitchers (wing width/total pitcher width) previously has been correlated with pore-water nitrogen concentrations (Ellison and Gotelli, 2002
). Therefore, we examined covariance between pitcher morphology and nutrient concentrations in pore water. We took five pore-water samples, evenly spaced across the sample transect. Fifty-mL water samples were extracted using clean Tygon tubing from 50 cm long x 2.5 cm diameter capped and perforated PVC tubes that were sunken into the peat. For each sample, we measured pH and calcium (mg/L) with Orion ion-sensitive electrodes (Thermo Electron Corp, Woburn, Massachusetts, USA), and phosphate (PO4-P), nitrate (NO3-N), and ammonium (NH4-N) (all in mg/L) spectrophotometrically using US-EPA standard methods (Bledzki and Ellison, 1998
; Clesceri et al., 1998
). Pore-water samples were not taken in eight southern sites, due to insufficient water availability in the drier sandy soils.
Some data reduction was performed prior to analysis. First, because the unit of interest was the site (N = 39 sites), the relationships between morphology and geographic, environmental, and climatic variables were based on means at each site (of N = 20 plants or vegetation samples per site; N = 5 pore-water samples per site). Because of correlations among climatic variables, among vegetation variables, and among pore-water chemical variables, we performed principal component analysis (PCA) to generate two principal axes that accounted for the majority of variance of each of these sets of predictor variables. All variables were standardized (transformed into standard-deviation units, or Z scores) prior to performing the PCA (Gotelli and Ellison, 2004
). We also extracted two principal axes describing pitcher size and shape using PCA on the (similarly standardized) morphological variables measured for each pitcher. We separately analyzed two morphological variables used to separate the subspecies of S. purpurea (the width of the pitcher lip and the pitcher length:mouth diameter ratio) and the morphological ratio known to co-vary with pore-water nitrogen concentration (relative wing width).
All morphological variables (principal axis scores or the three distinct variables) were regressed on the environmental predictor variables. Stepwise multiple regression and Akaike's information criterion (AIC: Burnham and Anderson, 2002
) were used to identify the best-fitting model and the variables that best predicted pitcher morphology.
Our first two questions addressed geographic and environmental correlates of morphological variability without regard to taxonomic distinctions. Therefore, we initially analyzed the data without classifying the observations according to infraspecific designations. These analyses illustrate patterns of covariance between morphological traits and climate, vegetation, and pore-water chemistry across the entire geographic range of S. purpurea.
Our third question asked if observed patterns of morphological variation were concordant with identification of infraspecific taxa by other authors based on morphology. To address this question, we used one-way analysis of variance (ANOVA) to test whether plant morphology (both the principal axis scores and the three distinct morphological variables) differed consistently among S. purpurea subsp. purpurea, S. purpurea subsp. venosa, and S. purpurea subsp. venosa var. burkii. In these ANOVAs, taxonomic designation was considered a fixed factor. A priori contrasts were used to test (a) whether S. purpurea subsp. venosa var. burkii differed from the two S. purpurea subspecies and (b) whether the two subspecies of S. purpurea differed from each other. Last, an analysis of covariance (ANCOVA) was used to determine if morphological differences among infraspecific taxa remained after accounting for covariance between morphological and environmental variables. All data analyses were done using S-Plus version 6.1 (Insightful Corporation, Seattle, Washington, USA).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Data for pore-water chemistry were available for 31 of the 39 sites, and the first two principal axes accounted for 61% of the variation in water chemistry among those sites (Table 2). The first principal axis reflected ammonium and calcium availability (sites with high concentrations of these two ions had large values on this axis), whereas the second principal axis reflected pH and phosphate concentrations (sites with high pH and high PO4 concentrations had large values on this axis). The first principal axis also was correlated with the latitude (r = 0.60), illustrating the well-known increase in nitrogen deposition rates at higher latitudes (Ollinger et al., 1993
).
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The inclusion of either or both of the principal axes of climate as covariates in the analysis of variance (i.e., an ANCOVA) on plant morphology does not alter our conclusions. Sarracenia purpurea subsp. venosa var. burkii still separates out from the two subspecies of S. purpurea (P = 0.004 for the a priori contrast), and the two subspecies of S. purpurea are not distinguishable (P = 0.86 for the a priori contrast).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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There is some indication that available nutrients may also alter the amount of tissue in the pitcher wing relative to the width of the pitcher itself. Sites with high levels of ammonium and calcium tend to have plants with larger wings and narrower pitchers than do sites with lower levels of these nutrients, although most of the variation among sites remains unexplained. This pattern is consistent with the hypothesis of Givnish et al. (1984)
that relative allocation of resources to carnivorous structures results from the "costliness" of producing carnivorous structures. Pitchers with relatively large wings are photosynthetically more efficient than those with relatively small wings (Ellison and Gotelli, 2002
) and predominate when more nutrients are available.
Our data illustrate that there is no obvious way to distinguish these subspecies on morphological grounds alone, supporting Gleason and Cronquist's (1991)
treatment of these subspecies as simple geographic varieties of S. purpurea. The two principal morphological characters used to distinguish S. purpurea subsp. purpurea from S. purpurea subsp. venosa, the ratio of pitcher length to mouth diameter and the thickness of the pitcher lip (Schnell, 2002
), do not differ between northern and southern populations of S. purpurea. Because the two varieties co-occur in the mid-Atlantic states where their ranges overlap, introgression and hybridization are possible (Godt and Hamrick, 1999
). Additional genetic analysis (e.g., DNA sequencing) and field investigations of hybridization between S. p. purpurea and S. p. venosa are needed to resolve their taxonomic status definitively.
Our data do clearly support the differentiation of S. purpurea subsp. venosa var. burkii from S. purpurea, however. Sarracenia purpurea subsp. venosa var. burkii differs not only in the morphological characters measured here, but also in pitcher and flower color (Naczi et al., 1999
), height of the flower scape (Naczi et al., 1999
), and seed size and germination characteristics (Ellison, 2001
).
Overall, these conclusions are consistent with earlier results of allozyme analysis (Godt and Hamrick, 1999
). Sarracenia purpurea subsp. venosa var. burkii is genetically quite distinct from the recognized infraspecific taxa of S. purpurea. Sarracenia purpurea subsp. venosa and S. p. purpurea are genetically similar, and the allozyme data, which suggest that S. purpurea subsp. venosa is derived relative to S. purpurea subsp. purpurea, are at odds with the geographic distribution, which suggests that S. purpurea subsp. purpurea is a postglacial derivative of S. purpurea subsp. venosa. Godt and Hamrick (1999)
, also point out that the genetic grouping of S. purpurea subsp. venosa (and S. purpurea subsp. venosa var. montana) with S. purpurea subsp. purpurea is not consistent with a taxonomic system that places S. purpurea subsp. venosa var. burkii into S. purpurea subsp. venosa.
It could be argued that the observed differences between S. purpurea subsp. venosa var. burkii and S. purpurea simply reflect correlated habitat factors because the southern populations are in the warmest sites (Fig. 3A) and are intermediate in precipitation (Fig. 2A). However, including either or both of the principal axes of climate as covariates into an ANCOVA does not alter our conclusions. Sarracenia purpurea subsp. venosa var. burkii remains distinctive from S. purpurea, and the subspecies of S. purpurea are not separable morphologically. Overall, these results support the recognition of Sarracenia purpurea subsp. venosa var. burkii as the distinct species S. rosea (Naczi et al., 1999
). Recognition of its status as a distinct species also would facilitate protection of the rare S. rosea (Godt and Hamrick, 1999
). The comprehensive geographic analysis described herein is a useful tool for understanding morphometric variation and its information value for taxonomic studies.
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FOOTNOTES |
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5 E-mail: aellison{at}fas.harvard.edu
6 Present address: Bioprotection and Ecology Division, P. O. Box 84, Lincoln University, Canterbury, New Zealand
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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  G. Ne'eman, R. Ne'eman, and A. M. Ellison Limits to reproductive success of Sarracenia purpurea (Sarraceniaceae) Am. J. Botany, November 1, 2006; 93(11): 1660 - 1666. [Abstract] [Full Text] [PDF]
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