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Population Biology |
2Department of Plant Biology, 2502 Plant Sciences Building, University of Georgia, Athens, Georgia 30602 USA; 3Departments of Plant Biology and Genetics, 2502 Plant Sciences Building, University of Georgia, Athens, Georgia 30602 USA
Received for publication January 7, 2003. Accepted for publication November 20, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: allozymes • Araliaceae • conservation • genetic diversity • ginseng • harvest • medicinal plant • Panax quinquefolius
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Laurance, 1999
; Pimm et al., 2001
; Vance, 2002
), potentially leading to extinction (Frankel and Soule, 1981; Shaffer, 1981
; Menges, 1991
; Ellstrand and Elam, 1993
; Mills and Smouse, 1994; Frankham, 1995
; Lande, 1995
). Human activities can also change the level and pattern of genetic diversity in native plant species, leading to loss of genetic diversity that may ultimately reduce the evolutionary potential of a species to respond to environmental changes (Ellstrand and Elam, 1993
). Population fragmentation, isolation, and lowered population densities may also modify patterns of gene exchange, reducing pollen and seed movement between sites and possibly increasing inbreeding within sites. For many species, genetic diversity is directly related to population size (Godt et al., 1996
; Godt and Hamrick, 2001
), and levels of genetic diversity may affect individual fitness and potential population persistence (Newman and Pilson, 1997
; Fischer and Matteis, 1998
).
American ginseng roots are widely collected in the United States for sale in herbal medicines as a cure-all or panacea. Although ginseng can be cultivated, wild roots are considered more potent and are therefore more valuable. Wild roots may sell for U.S. $1105 per kilogram (approximately $500 per lb) (Robbins, 1998
). The market for American ginseng has fluctuated throughout the 20th century, but has steadily increased since the 1960s. Currently, population status data are not incorporated into national management programs for Panax quinquefolius or into federal decisions regarding export of wild roots (Robbins, 2000
). Collection of wild roots less than 5 yr of age, however, is prohibited by the federal government, a measure designed to allow plants an opportunity to reproduce before harvest.
Recent trends suggest that harvest pressure on wild sources of medicinal plants is increasing (Nantel et al., 1996
; Sheldon et al., 1996; Robbins, 1998
; Laurance, 1999
). Research suggests that populations of wild-collected herbs are falling below minimum viable sizes and are going extinct due to collection pressures (Lewis, 1988
; Nantel et al., 1996
; Sheldon et al., 1996). Because the majority of medicinal plant species are not cultivated, most material for herbal remedies originates in native forests (Pearce, 1997
; Sheldon et al., 1997
). The current pressure on populations of wild-harvested plants forces the question of how nontimber forest products persist within a landscape of forest fragmentation and habitat loss. Foremost is the question of how evolutionary and demographic processes of wild-collected species are altered by harvesting.
We conducted a genetic survey of Panax quinquefolius to estimate the level and distribution of genetic diversity among populations in southeastern Appalachian forests. American ginseng is representative of the economic and cultural value of wild medicinal plants. Our sampling was designed to determine whether the genetic composition of ginseng is affected by harvest pressure by including populations protected from harvest and those where collecting is permitted. We also obtained demographic information from protected and unprotected populations in an effort to determine the ecological impact of harvest on American ginseng. Also, information is lacking on population densities, levels of genetic variation, and the distribution of this economically valuable herb (Robbins, 2000
). Appalachian hardwood forests, where most wild ginseng populations occur, are also threatened with continued habitat alteration as a result of suburbanization and logging.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and is reported to have a mixed-mating breeding system (Carpenter and Cottam, 1982; Lewis and Zenger, 1982
; Schlessman, 1985
). American ginseng reproduces exclusively by seed after a pre-reproductive period of approximately 3 yr and does not grow from roots clonally (Lewis and Zenger, 1982
; Nantel et al., 1996
). Green fruits first appear in July and August and mature and redden on the plant from August to November. In an effort to maintain natural population sizes, U.S. Fish and Wildlife regulations require ginseng collectors to harvest only ginseng large enough to reproduce (three- and four-leaf plants) and to plant seeds from harvested individuals within the same population.
Plant material
To determine the genetic structure of P. quinquefolius populations, allozyme variation was analyzed via starch gel electrophoresis. During 1999 and 2000, leaf samples were collected from 21 wild populations that occurred in national parks, national forests, and on private land from Georgia to West Virginia, for a total of 1307 plants (Fig. 1). Eight populations were protected, meaning that harvesting has not been permitted since 1940. Thirteen unprotected populations occurred in areas where permits are issued for limited ginseng harvest (Table 1). Poaching likely occurs in both protected and unprotected populations. We collected a few leaflets from a compound leaf of each plant. All plants within a contiguous patch, usually considered a population, were sampled.
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; Charron and Gagnon, 1991
; Anderson et al., 1993
). Small plants are also often considered juveniles, because reproduction is usually delayed until plants have at least three leaves (Lewis and Zenger, 1982
; Charron and Gagnon, 1991
; Anderson et al., 1993
). Significant differences in the proportion of plants in each size class and the proportion of reproductive individuals (with fruits or flowers) in each size class for protected and unprotected populations was determined with chi- square tests for marginal homogeneity (JMP, SAS, 1996
). For a more detailed approach to understanding genetic diversity and demography, we compared average within-population genetic diversity among plants in the different size classes. Categories were grouped to include enough individuals for meaningful comparisons of genetic diversity; hence, the number of leaves was used to assign plants to two size classes: small (one- and two-leaf plants) and large plants (plants with three, four, or more leaves).
Allozyme analysis
Sampled leaf material was kept on ice and returned to the University of Georgia within 48 h. There it was crushed with mortar and pestle and a bit of sea sand in a phosphate-polyvinylpyrrolidone extraction ("camellia") buffer to stabilize the enzymes (Wendel and Parks, 1982
). Enzyme extracts were absorbed onto chromatography paper wicks and stored at –70°C until analysis. We consistently resolved seven enzyme systems (abbreviation, number of loci): fluorescent esterase (FE, 1), isocitrate dehydrogenase (IDH, 2), malate dehydrogenase (MDH, 2), menedione reductase (MNR, 2), phosphoglucoisomerase (PGI, 4), triose phosphate isomerase (TPI, 3), and UTP-glucose-1-phosphate (UGPP, 2).
Genetic diversity analysis
Genetic diversity parameters were estimated using a computer program developed by M. D. Loveless and A. F. Schnabel and by POPGENE (Yeh et al., 1997
). Gene and genotype frequencies were estimated for each population, as well as genetic diversity statistics at the population, between protected and unprotected populations, and species (pooled) levels (Hedrick, 1985
; Hamrick and Godt, 1989
). Standard population genetic parameters, reported for making comparisons with published allozyme literature, include percent polymorphic loci (P), mean number of alleles per locus (A) and per polymorphic locus (AP), effective number of alleles per locus (Ae), observed heterozygosity (Ho), and expected heterozygosity (He). Deviations from Hardy-Weinberg expectations within each population were tested with Wright's (1922) F statistic for each polymorphic locus. The level of significance for comparison between observed and expected heterozygosity was determined by a chi-square test (Li and Horvitz, 1953).
Genetic structure
Interpopulation genetic structure was estimated with Nei's (1973
, 1977
) genetic diversity statistic, GST, which estimates the proportion of genetic variation among populations at polymorphic loci. Genetic diversity statistics were calculated for each locus and averaged over all loci. Significant differences in allele frequencies among populations were determined with chi-square tests of polymorphic loci, where 
2 = 2N GST (a – 1), with df = (a – 1)(n – 1), a is the number of alleles at the locus, and n is the number of populations (Workman and Niswander, 1970). Each pair of populations was used to calculate genetic distance measures (Nei, 1972
), and the hypothesis of isolation by distance was tested using the program IBD (Isolation by Distance; Bohonak, 2002
). We assessed the level of significance by a Mantel test for matrix correlation between the pairwise value for FST/(1 – FST) and log geographic distance for each population pair (Rousset, 1997
).
Indirect estimates of gene flow were obtained with Wright's (1951) method, using GST as equivalent to FST. The estimated number of migrants per generation, Nm, was calculated as Nm = (1 – GST)/4GST. A second measure of Nm was determined from the mean frequency of alleles found in single populations, i.e., "private alleles" (Slatkin, 1985; Barton and Slatkin, 1986
).
Effects of harvest pressure
The effect of harvest pressure on populations was estimated by comparing levels of genetic diversity between populations for which collection permits were issued (unprotected populations) and populations that have been protected from harvest for more than 60 yr (protected). Genetic diversity statistics were calculated as described earlier. Significant differences in diversity statistics between protected and unprotected populations were determined with an unpaired two-tailed Student t test. The test for significant differences in expected heterozygosity (He) was performed on jackknifed values (Weir and Cockerham, 1984
). Finally, evidence for a recent bottleneck as a result of harvest pressure was determined with Cornuet and Luikart's (1997) BOTTLENECK analysis program. A sign test and Wilcoxon test were used to determine whether there was a significant excess in expected heterozygosity (He) with regard to expected equilibrium gene diversity (Heq) computed from the observed number of alleles for each population. The power of each test depended on the number of polymorphic loci and sample size (Cornuet and Luikart, 1997; Luikart et al., 1997
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Genetic diversity within size classes
When genetic diversity was compared between small (one- and two-leaved plants) and large plants (three- and four-leaved plants) within populations, small plants within populations had significantly greater average allelic richness (P < 0.01; Table 4). Larger plants also maintained significantly higher average genetic diversity (He) than small ones.
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Genetic distance among populations ranged from 0.444 between populations GA5 and WV19 and 0.002 between NC15 and NC14 and between GA5 and GA4. We found a significant correlation in pairwise FST/(1 – FST) and log geographic distance (P < 0.0001 from 10 000 randomizations, reduced major axis regression r2 = 0.285), indicating significant isolation by distance. Historical levels of gene flow (Nm) among populations were estimated to be 1.15 from six private alleles with an estimated mean frequency of 0.057. In contrast, Wright's method of estimating gene flow produced a mean Nm of 0.26.
Effect of harvest pressure
Genetic diversity varied between protected and unprotected populations (Table 3). Average He for protected populations was 0.076, significantly higher (P < 0.005) than the 0.070 in unprotected populations. There was no significant difference in mean P, AP, Ae, or allelic richness, indicating that differences among protected and unprotected populations were due to loss of rare alleles resulting from bottlenecks and genetic drift. There was also a significant difference in He between populations of different sizes, but in this case, smaller populations (n < 80) had significantly higher He, 0.080 (P < 0.0001), than large populations (He = 0.057; Table 3). Small populations (14) had a mean ± SD of 43 ± 15 individuals and large populations (7) had 101 ± 11 individuals. Populations of both sizes were found in protected and unprotected areas.
Genetic structure in protected and unprotected populations
Genetic structure was greater among unprotected populations (GST = 0.491) than among protected populations (GST = 0.167; Table 3), suggesting that unprotected populations may have experienced genetic bottlenecks as a result of consistent harvest pressure. All 10 polymorphic loci had significant heterogeneity in allele frequency among unprotected populations, whereas among protected populations eight of 10 polymorphic loci had significant differences in allele frequencies.
The striking difference in genetic structure might be due to our sampling scheme in which protected populations were sampled across a smaller geographic range than were unprotected populations. However, when the unprotected West Virginia populations were deleted from the analysis, GST among unprotected populations remained close to 50% (0.478). Therefore, even when corrected for spatial scale, variation in allele frequencies among unprotected populations produced a high level of genetic structure.
Three of 13 unprotected populations had indications of a recent bottleneck (Table 5) based on both sign and Wilcoxon tests, whereas none of the eight protected populations had significant evidence for a recent bottleneck with these tests. A sign test for the number of significant results determined that there were significantly fewer occurrences of a recent bottleneck among protected populations than would be expected at random (P = 0.0078). Therefore, there was no evidence of recent bottleneck among protected populations.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Although populations are infrequent and patchy, P. quinquefolius has a wide geographic range throughout eastern North America and would be expected to maintain moderate to high levels of genetic diversity. The breeding system of P. quinquefolius is reportedly mixed selfing and outcrossing (Lewis and Zenger, 1982; Schlessman, 1985
; Schluter and Punja, 2002
), and seed dispersal mechanism is unknown. Indeed, genetic diversity in American ginseng (He = 0.159) is between the He values for short-lived perennial species with mixed mating systems (0.172) and predominately selfing species (0.135) (Hamrick and Godt, 1996
).
Comparisons of observed (Ho) and expected (He) heterozygosity within populations of P. quinquefolius had a significant excess of homozygosity. This result may be due to nonrandom mating among related individuals or to the mixed mating system reported for this species. It is possible that reductions in population size due to habitat fragmentation or harvest increased selfing or mating among closely related plants resulting in a higher proportion of homozygous individuals within populations. It is also possible that deviations from expected heterozygosity were from sampling over several small subpopulations and treating them as one population (i.e., a Wahlund effect; Hartl and Clark, 1998
). Plants within a few wild American ginseng populations were scattered throughout mountain coves and drainages, so we may have collected from more than one subpopulation when collecting leaves. We find this scenario unlikely considering an excess in homozygosity was observed at loci in all of the populations, regardless of the area sampled. Further analysis of the fine-scale genetic structure within populations of P. quinquefolius may resolve this question (Cruse-Sanders and Hamrick, unpublished manuscript).
Genetic structure
Genetic diversity within American ginseng was highly structured among populations, with approximately 50% of the total genetic variation found among populations. The genetic structure estimated for populations of P. quinquefolius was greater than that reported for other plant species with similar life history strategies and was most similar to the mean calculated for annual plants with predominantly selfing mating systems (0.553) (Hamrick and Godt, 1996
).
Genetic structure can be used to infer historical rates of gene movement among populations, although the results must be interpreted with caution (Brossart and Prowell, 1998
; Sork et al., 1999
; Whitlock and McCauley, 1999
). Gene flow (Nm) among populations was estimated to be 1.15 based on Slatkin's (1985) private allele method. Alternatively, levels of gene flow based on Wright's (1951) method averaged 0.26. These estimates suggest that historical rates of gene flow have been too low to counteract the effects of genetic drift (Wright, 1931). We found significant evidence for isolation by distance within this species, which indicates population division and divergent evolution throughout the range of American ginseng.
Genetic structure in this study (Table 3) was greater than that reported based on RAPD data among cultivated (GST = 0.18) and natural (GST = 0.28) populations of American ginseng in Canada (Schluter and Punja, 2002
). There are at least two possible explanations. First, genetic structure in this study was estimated from populations sampled over a larger geographic range. Furthermore, harvesting from wild populations was banned in Canada in 1989 (Nantel et al., 1996
). If high genetic structure among populations in the United States is, at least in part, a result of harvesting, the lower genetic structure among populations in Quebec may reflect a release from harvest pressure. This hypothesis is supported by the relatively low genetic structure among protected populations from this study (GST = 0.167).
Comparison with genetic diversity of more northern populations also suggests an effect of post-glacial dispersal resulting in loss of alleles and lower He in the more northern populations. This pattern has been noted for other Appalachian species such as Helonias bullata (Godt et al., 1995
). However, this pattern is only suggestive for ginseng since our sampling design is not adequate to fully describe geographic variation throughout the entire range of the species.
Demographic impacts of harvest
The size class structure of ginseng plants is different between protected and unprotected populations. Protected populations maintain a higher proportion of older, potentially reproductive plants than unprotected populations. Furthermore, we found a significant difference in proportions of reproductive individuals in protected and unprotected populations. In unprotected populations, small plants (one- or two-leaf plants) were more likely to have flowers or fruits compared to protected populations. Our results suggest that reproductive parameters can change with a demographic shift in a harvested population, which can lead to a significant drop in population growth rate. Hackney and Mcgraw (2001) found that small, less dense populations of American ginseng produced few seeds per flower and per plant, possibly due to reduced pollinator efficiency. Our findings suggest that this effect could be amplified due to a shift in age class structure with harvest. If unprotected populations have fewer flowering plants than expected based on census size, a drop in reproductive output and lower population growth rate could result.
Within populations, we found that large (three- and four- leaved) plants maintain significantly higher expected heterozygosity than small (one- and two-leaved) plants. This observation could be due to higher survival of more heterozygous individuals through time. Alternatively, this may represent a generational change in overall genetic diversity. Based on previous demographic work with P. quinquefolius, large plants are the oldest and reproductively mature individuals within populations (Schlessman, 1985
; Anderson et al., 1993
; Nantel et al., 1996
). Larger (reproductive) plants might not be randomly mating or have low fecundities as a result of low postharvest population densities. Furthermore, if larger, older individuals reproduce prior to harvest, it is possible that a proportion of their seeds does not germinate or is taken from the population to be planted elsewhere, resulting in low recruitment. This is likely, considering anecdotal information that ginseng diggers routinely move seeds and roots among locations to ensure that ginseng plants are found in locations they regularly harvest (V. Nazarea, University of Georgia, personal communication).
A compounding effect results when the age class distribution in harvested populations is altered, leading to long-term evolutionary effects. Based on studies of herbarium specimens, McGraw (2001)
found a significant decrease in ginseng plant stature over 150 years and concluded that the decrease resulted from the sustained harvest of large plants. Our results suggest that there is also a genetic effect of harvest on populations that compounds the harvest pressure imposed on the largest, and presumably most reproductively viable plants within populations of American ginseng.
Documented changes in plant size and genetic diversity in American ginseng populations point to possible negative evolutionary consequences of harvest. Ratner and Lande (2001)
provided a theoretical analysis of the evolutionary and demographic implications of size-selective harvesting in populations and found that harvest could lead to significant changes in the average size of individuals within populations. Although, in the short term, demographic effects may be of immediate conservation importance (Schemske et al., 1994
), the evolutionary effects of selective harvesting can exacerbate the demographic consequences of collecting.
Genetic diversity in protected and unprotected populations
Trends in genetic diversity from this study indicate that protected populations harbor significantly higher levels of genetic diversity (He) than unprotected populations. Although other measures of genetic diversity, P, AP, Ae, did not differ significantly between the two types of populations, the greater He indicates that allele frequencies at loci are more even in protected populations. These differences could be due to the current harvesting status of these populations, but there could also have been an association between protected populations and the history of the forested site where the population was found. If protected populations were more likely to be found in pristine habitats and unprotected populations in more disturbed, fragmented habitats, the pattern in genetic diversity might be due to historical bottleneck or drift in low-quality habitats as well as harvest practices (J. M. Cruse-Sanders, unpublished data).
The most noteworthy difference between protected and unprotected populations was the level of genetic structure among populations within each group. Significant variation in allele frequencies and high genetic structure, especially among unprotected populations, is consistent considering the effect harvesting has on populations. As mature plants are collected from the population, allele frequencies should change among populations and genetic structure should increase. This suggests that many populations throughout the range of the species may have experienced reduced effective population sizes due to habitat disturbance and/or harvesting. When populations become small, genetic drift causes different alleles to become fixed in different populations leading to increased genetic structure.
We found no evidence for recent population bottlenecks among any of the protected populations. The lack of evidence for a bottleneck in some populations may be because a bottleneck did not occur or that it is older than this method can detect. Additionally, as has been noted, our populations are not in Hardy-Weinburg equilibrium, which violates the assumptions of the BOTTLENECK program (Cornuet and Luikart, 1997). Therefore, results of this analysis should be interpreted with caution, although they do support our findings of possible negative evolutionary impacts of harvesting (i.e., reduced genetic diversity and increased genetic structure).
Conservation implications
An effective conservation strategy would protect populations throughout the range of ginseng to maximize the maintenance of genetic diversity, because almost 50% of the total genetic diversity occurs among unprotected populations. Schoen and Brown (1991)
pointed out that species with higher GST values also have more variation in genetic diversity parameters (P, He, etc.) than species with less genetic structure. This makes it difficult to predict levels of genetic diversity for specific populations (Schoen and Brown, 1991
) and to develop effective conservation strategies (Ceska et al., 1997
). For P. quinquefolius, our results highlight the need for empirical studies to identify populations with higher levels of genetic diversity and unique alleles.
Conservation recommendations resulting from this study include prohibiting certain populations of American ginseng from being harvested because protected populations generally maintained more genetic diversity than unprotected populations. Demographic research on ginseng in Quebec and in Great Smoky Mountain National Park (GSMNP) set the minimum viable population size at 172 plants (Nantel et al., 1996; Gagnon, 1999
), yet when populations in GSMNP were censused, only two populations met that criterion (Rock et al., 1999
). Nonetheless, protected populations within GSMNP generally harbor more genetic diversity than populations in adjacent harvested areas. Continued harvesting could have long-term negative conservation implications and evolutionary consequences. Based on our results indicating that older plants maintained more genetic diversity, we recommend that conserving a proportion of the largest (oldest) plants in each population would best protect the reproductive fitness and evolutionary potential of the species.
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FOOTNOTES |
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4 Present address: Rancho Santa Ana Botanic Garden, 1500 N. College Avenue, Claremont, CA 91711 USA. E-mail: jennifer.cruse-sanders{at}cgu.edu
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pi2), where pi is the frequency of the ith allele; allelic richness (AR); observed proportion of heterozygotes (Ho); expected proportion of heterozygotes (He). See