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Systematics and Phytogeography |
Duke University, Department of Biology, Box 90338, Durham, North Carolina 27708 USA
Received for publication February 27, 2003. Accepted for publication June 6, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: endophytes • Jamaica • liverworts • North Carolina, USA • phylogeny • Xylaria • Xylariaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). New species are continually being described from cultural and molecular studies of plant tissue, and endophyte biology is a burgeoning field in mycology. (A Biological Abstracts search for "endophyt*" in the title retrieved 923 papers from 1990 through January 2003.) These studies indicate that the breadth of endophyte diversity and ecology is just beginning to be discovered (Arnold et al., 2000
).
Many groups of fungi exist as endophytes, though most are ascomycetes. Well-known examples are Clavicipitaceae (e.g., Epichloe) species that inhabit grasses (Poaceae). Endophytic associations with Epichloe have been shown to be mutualistic: the plant receives protection from herbivory through fungal toxins, and the fungus receives host tissue as a nutritive source, along with seed-mediated dispersal of mycelia (reviewed in Clay, 1988
). However, the ecology and distribution of most groups of endophytic fungi remain poorly known.
Endophytic Xylariaceae have been documented in conifers, monocots, dicots, ferns, and lycopsids (Brunner and Petrini, 1992
). One hypothesis for the role of Xylariaceae endophytes holds that the fungus is a quiescent colonizer and will later decompose cellulose and lignin when the plant begins to senesce (Petrini et al., 1995
; Whalley, 1996
). However, growing evidence suggests that some xylariaceous fungi may exist solely as endophytes (Rogers, 2000
; J. D. Rogers, Washington State University, personal communication). No obvious benefit to living host plants has been documented for Xylariaceae.
Liverworts are nonvascular, spore-bearing plants, or "bryophytes." Though these plants have long been known to form associations with fungi (see Boullard [1988
] and Read et al. [2000
] for review), few liverwort endophytes have been identified with certainty. Duckett and Read (1995)
grew ascomycetes from 11 British liverworts and through cross-inoculation experiments with angiosperms concluded that the fungi were likely Hymenoscyphus ericae (D. J. Read) Korf and Kernan (Leotiaceae), the ascomycete that forms mycorrhizae with the flowering plant family Ericaceae. This species was also identified from an Antarctic liverwort [Cephaloziella exilifora (Taylor) Stephani (Cephaloziellaceae)] based on DNA sequences from the nuclear ribosomal internal transcribed spacer (ITS) (Chambers et al., 1999
). It is unclear whether Xylariaceous endophytes previously isolated from "bryophytes," as listed in Petrini and Petrini (1985)
, included any liverworts. Endophytes of some liverwort species are restricted to the rhizoids, while those of other liverwort species can be detected growing within the thallus. Most rhizoid-associated endophytes are thought to be ascomycetes, while those within thalli are thought to be basidiomycetes or Glomalean fungi (Boullard, 1988
). The resemblance of these associations to vascular plant mycorrhizae have led some to label them as mutualistic, though the nature of the symbiosis remains poorly understood (Read et al., 2000
).
The goal of this study was to characterize the endophytic communities of six common liverworts collected in Jamaica and North Carolina, USA. The study consisted of three parts: (1) morphological observations of the fungal infection, (2) identification of the endophytes based on nrDNA similarity and phylogeny, and (3) ecological comparisons of the endophytes with related fungal species.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Cultures
Cultures were established following a modified version of the procedure from Arnold et al. (2000)
, in which contamination from surface fungi was minimized by submersion of the plant tissue in a 5% bleach solution for 2 min, followed by submersion in 70% ethanol for 2 min. Liverwort fragments were plated on sterile potato dextrose agar or malt extract agar using aseptic technique. Pure living cultures of all fungi are vouchered at DUKE and will be submitted to a public culture collection pending morphological identification.
Molecular methods
Total genomic DNA was extracted from cultured fungi using the method of Doyle and Doyle (1987)
. The ITS 1, 5.8s, and ITS 2 regions of nrDNA were amplified using the primers ITS 1 and ITS 4 (White et al., 1990
), and the 18S region was amplified using the primers NS 1 and NS 8 (White et al., 1990
). Polymerase chain reactions (PCR) were performed using a Perkin Elmer 480 (Perkin Elmer, Norwalk, Connecticut, USA) with 35 cycles of 94° for 1 min, 50° for 30 s, and 72° for 1 min, with an additional 7-min extension at 72° after cycling. The PCR amplicons were purified using Qiaquick spin-columns (Qiagen, Valencia, California, USA) according to manufacturer protocols.
Sequencing PCR utilized Big Dyes v.2.0 (Applied Biosystems, Foster City, California, USA) and an ABI Prism 3700 (Applied Biosystems). Additional internal 18S primers NS 1.5, NS 2, NS 4 (White et al., 1990
), and BMB-BR (Lane et al., 1985
) were used to improve sequencing results. All sequences have been submitted to GenBank (see Supplemental Data accompanying the online version of this article).
Analyses
Preliminary identifications of fungal ITS sequences were obtained using the GenBank BLAST (Altschul et al., 1997
) sequence similarity search with all filters removed. The closest matches were used to identify the major group of fungi to which each sequence belonged and to guide GenBank sampling for 18S phylogenetic analyses.
Alignments of ITS and 18S sequences and GenBank accessions were performed manually using Se-Al version 1 (A. Rambaut, University of Oxford, Oxford, UK). Regions that could not be unambiguously aligned were excluded from further analysis. The alignments are available upon request from the authors.
Aligned ITS sequences were analyzed using equally weighted parsimony implemented in PAUP 4.0b10 (Swofford, 2002
). A branch and bound search was conducted, with gaps scored as missing data. Trees were mid-point rooted.
Aligned 18S sequences were analyzed using equally weighted parsimony and maximum likelihood using PAUP. Heuristic parsimony searches were conducted using 100 random addition replicates with MulTrees and steepest descent in effect. Gaps were scored as missing data. Parsimony bootstrap support values were calculated using 100 full heuristic searches with 10 random additions per replicate (Felsenstein, 1985
). The maximum likelihood substitution model for 18S was determined by calculating the likelihood for 56 models and comparing them using likelihood ratio tests, implemented in Modeltest 3.06 (Posada and Crandall, 1998
). The best model was Tamura-Nei with equal base frequencies and among-site rate heterogeneity specified by a gamma shape parameter. The likelihood searches were conducted using 100 random addition replicates. Bayesian analyses were conducted on the aligned data set using MrBayes 2.01 (Huelsenbeck and Ronquist, 2001
) using a model of equal base frequencies with six substitution types and a gamma shape parameter. Four simultaneous Markov chain Monte Carlo searches were run for 1 000 000 generations and trees were sampled every 100 generations. Plots of the likelihoods from each sample were made to determine the number of generations until stationarity was achieved, in order to identify the posterior probability tree set.
All 18S phylogenies produced from parsimony, likelihood, and Bayesian analyses were rooted with the sequence for Coprinus (a basidiomycete). Coprinus was chosen because it is part of the sister group to the ascomycetes and could be easily aligned with our endophyte sequences.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Molecular analyses
The ITS and 18S sequences were obtained from all cultures except one Bazzania isolate. The total number of sequences being compared for endophytes of Bazzania is thus 16. Amplification of 18s was unsuccessful for Plagiochila and Trichocolea cultures; results of only ITS data are therefore presented for these specimens.
The ITS sequence similarity searches
Based on BLAST results from ITS sequences, all of the endophytes isolated from Bazzania were inferred to belong to the Xylariales (see Supplementary Data accompanying the online version of this article for detailed BLAST results); 14 were closely matched to sequences from Xylariaceae. Of these xylariaceous endophytes, 10 were closely matched to sequences from Xylaria. Endophytes from two Odontoschisma cultures were also closely matched to sequences from Xylariaceae, one of which returned the same list of BLAST results as six of the Bazzania isolates. All endophytes from Metzgeria, Plagiochila, and Trichocolea were closely matched to sequences from Xylaria. The identity of one Odontoschisma isolate could not be determined using similarity searches, because the top matches were unidentified fungi. The Calypogeia isolate was closely matched to sequences from the Hypocreaceae.
Phylogenetic analyses
Ten ITS sequences from cultured endophytic fungi (nine Bazzania, one Odontoschisma) returned very close BLAST matches for xylariaceous endophytes cultured from angiosperms (Guo et al., 2000
). Two of these (from Bazzania) could not be evaluated further using ITS, because the BLAST hits were "unidentified xylarialean endophyte(s)" (AF153741, AF153742, AF153743). A data matrix was compiled including the remaining eight liverwort endophyte sequences and their closely matched endophyte sequences from GenBank. Five additional non-endophyte Xylaria sequences were included in order to provide a phylogenetic context for the endophytes. Parsimony searches on this matrix resulted in two most parsimonious trees (68 parsimony-informative characters, consistency index [CI] = 0.77). All endophytes clustered together, and liverwort and angiosperm sequences were separated by only 1–7 nucleotide substitutions at the tips of the tree (Fig. 2). The tree shown is intended only to show the similarity among endophytes, not to infer relationships among species of Xylaria.
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). Parsimony searches conducted on 18S data resulted in 31 000 most parsimonious trees (318 parsimony-informative characters, CI = 0.80). The maximum likelihood search yielded one tree. The Bayesian analysis reached stationarity at 441 000 generations, resulting in a total of 5600 trees in the posterior probability distribution. The strict consensus parsimony tree, the likelihood tree, and the 95% majority rule Bayesian tree were congruent and differed only slightly in their topologies. The Bayesian tree with posterior probability confidence values and parsimony bootstrap support values is shown in Fig. 3.
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). Eleven of the Bazzania endophyte sequences group with high support in the Xylaria/Poronia/Anthostomella clade. One Metzgeria and two Odontoschisma endophytes also fall within this group. One of the endophytes isolated from Odontoschisma is sister to an endophyte isolated from Bazzania (C8 and F3, respectively). One isolate from Bazzania (F16) is strongly supported as sister to a Daldinia (Xylariaceae) sequence obtained from GenBank. One Odontoschisma endophyte (C6), which could not be identified based on ITS, is highly supported as a close relative of the Ophiostomataceae. The fungus from Calypogeia (C1) is strongly supported as a member of the Hypocreaceae.
Relationships of two Bazzania endophytes (F15 and F17) are ambiguous, but they clearly belong within the Xylariales and are closely related to one another (Fig. 3). They share a large insertion of 140 nucleotides (nt) 530 nt from the 5' end (not included in phylogenetic analyses). This insertion is also present in F16 and the Hypoxylon haematostroma sequence, but is absent from all other sequences in this analysis. It is not present in the Daldinia fissa sequence obtained from GenBank, although that sequence is closely related to F16 on the basis of nucleotide substitutions. Based on these data, it seems likely that H. haematostroma, Daldinia fissa, and the two Bazzania isolates are closely related to one another, but their inter-relationships are not resolved by this analysis.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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presented a phylogenetic analysis of Xylaria ITS sequences (18 taxa, 12 Xylaria), but other studies including substantial xylariaceous taxa have focused on identifying endophyte sequences (e.g., Guo et al., 2000
; Collado et al., 2002
; this study). Results from this study support previous analyses and highlight the need for further phylogenetic examination of this group. Xylaria may be nonmonophyletic: X. cubensis may be more closely related to Daldinia (Lee et al., 2000
), and 18S sequences from Rosellinia, Anthostomella, and Poronia group within the Xylaria clade (Collado et al., 2002
; this study). It appears that the Amphisphaeriaceae/Hyponectriaceae clade is most closely related to taxa that have been classified in the Xylariaceae (Kang et al., 2002
; this study). In general, no published molecular analysis provides convincing evidence that Xylariaceae, or any of its genera, is monophyletic. Much further study is needed in this ecologically complex group and should include a broad sampling of both endophytic and nonendophytic taxa.
The results of these molecular analyses suggest that endophytic Xylaria in liverworts and angiosperms are closely related. The ITS sequences from four Bazzania isolates are nearly identical to three endophytic Xylaria from Livistona chinensis (Arecaceae); two Bazzania isolates and one Odontoschisma are nearly identical to each other (Fig. 2). Such a pattern is not unprecedented. In studies of endophytic Xylaria using isozyme electrophoresis, Brunner and Petrini (1992)
found that 17 of 32 endophytic Xylaria from different hosts formed a unique cluster. Together, these results indicate the presence of a large group of closely related Xylaria that are endophytic, but that have very broad host ranges. At present, closely related or identical Xylaria isolates have been identified from hosts belonging to three plant divisions and two continents.
To examine the frequency and phylogeny of Xylaria as liverwort endophytes, we are currently conducting a survey of xylariaceous endophytes across the phylogenetic spectrum of liverworts.
The role of Xylaria in endophytic symbioses
One hypothesis for the role of endophytic Xylaria posits that the fungi are simply waiting for their host to senesce (or perhaps to hasten it), at which time they can begin decomposition of cell wall materials (Petrini et al., 1995
; Whalley, 1996
). Endophytes employing this strategy would have an advantage over competing saprophytes, having "claimed" the tissue before decomposition begins. Studies on endophytic Biscogniauxia (Xylariaceae) in living oak tissue have shown that the same species is present in higher abundance on decaying twigs (Collado et al., 2001
). However, data from studies examining fungal species composition in plant tissue before and after senescence do not support this hypothesis for all Xylaria. In a study of Schefflera (Araliaceae), Laessoe and Lodge (1994)
found different species of Xylaria occurring in living as compared to decomposing leaves. Bayman et al. (1998)
found different species of Xylaria in the living leaves of Manilkara (Sapotaceae) than in the fallen leaves. In some oak different species of Xylaria occur in living and dead twigs. In beech, the same species of Xylaria was isolated at much lower frequency in decaying branches compared to healthy tissue (Griffith and Boddy, 1990
). One alternative explanation for the role of xylarias that can be isolated as endophytes, but are not found decomposing the host plant, is that the fungus alternates between host taxa: one within which it exists as a cryptic endophyte and another on which it is saprophytic or pathogenic (Rogers, 2000
; J. D. Rogers, personal communication). Such a pattern of host switching is seen in Nemania serpens (Carroll, 1999
) and is thought to be common in Xylaria (Rogers, 2000
). This lifestyle has been categorized as "foraging" (Carroll, 1999
). Another explanation is that the endophytes exist only as endophytes, having become specialized to this environment (Rogers, 2000
; J. D. Rogers, personal communication).
Comparative studies involving liverworts and their xylariaceous fungi have not been performed, thus it is unknown whether endophytic Xylaria also serve as decomposers of the host tissue. However, their endophytes may likely be foragers or endophytic specialists because liverworts have no vascular tissue, thus they possess no wood and little cellulose to decompose compared to other plants; further, only a single record exists of a xylariaceous fungus producing fruiting bodies on liverwort substrate (Oudemans, 1919
). Finally, endophytic Xylaria isolated from liverworts in this study appear to be more closely related to endophytes isolated from other plants than they are to saprophytic species.
Could some Xylaria be mutualists?
Endophytic Xylaria have several characteristics that are associated with mutualism and not latent saprophytism. Based on a review of empirical studies of antagonistic interactions between endophytes and grazers, insects, and microbial pathogens, Carroll (1988)
outlined five general characteristics of endophyte mutualisms: (1) the endophyte is ubiquitous in a given host, geographically widespread, and causes minimal disease symptoms in the host plant; (2) vertical transmission or efficient horizontal transmission of the fungus occurs; (3) the fungus grows throughout host tissue, or, if confined to a particular organ, a high proportion of such organs are infected; (4) the fungus produces secondary metabolites likely to be antibiotic or toxic; and (5) the endophyte is taxonomically related to known herbivore or pathogen antagonists. Each of these characteristics as they apply to Xylaria are addressed in the following sections.
Host specificity and geographic range
Endophytic Xylaria occur on a broad diversity of plant hosts. Species delimitation based on cultures of endophytic Xylaria is difficult because of a lack of diagnostic characters. However, Xylaria have been isolated from Euterpe, Trachycarpus, and Livistona (Arecaceae; Rodrigues, 1994
; Taylor et al., 1999
; Guo et al., 2000
); Quercus and Fagus (Fagaceae); Betula, Corylus, and Alnus (Betulaceae); Acer (Sapindaceae); Fraxinus (Oleaceae); Rhizophora and Bruguiera (Rhizophoraceae); Avicennia (Avicenniaceae); Pinus and Picea (Pinaceae); and Nicotiana (Solanaceae) (Brunner and Petrini, 1992
); Manilkara (Sapotaceae; Lodge et al., 1996
; Bayman et al., 1998
); Lepanthes (Orchidaceae; Bayman et al., 1997
); Casuarina (Casuarinaceae; Bayman et al., 1998
); Schefflera (Araliaceae; Laessoe and Lodge, 1994
); Heisteria (Olacaceae) and Ouratea (Ochnaceae) (Arnold et al., 2000
); and liverworts (present study). In addition, the group of endophytic Xylaria identified in this study appears to be cosmopolitan in their distribution. Endophytic Xylaria have also been isolated from vascular plants in Europe (Brunner and Petrini, 1992
; Taylor et al., 1999
), Malaysia (Brunner and Petrini, 1992
), the Brazilian Amazon (Rodrigues, 1994
), Puerto Rico (Laessoe and Lodge, 1994
; Lodge et al., 1996
; Bayman et al., 1997
, 1998
), China (Taylor et al., 1999
; Guo et al., 2000
), Japan (Brunner and Petrini, 1992
), and Panama (Arnold et al., 2000
). Nearly identical ITS sequences (
3% divergent) were obtained from liverworts collected in Jamaica, North Carolina, and published sequences from China (Guo et al., 2000
).
Dispersal and transmission of endophytes
There is some evidence that Xylaria can be vertically transmitted through seeds as in other mutualistic endophytes: Xylaria was reported in seeds of Casuarina (Bayman et al., 1998
). However, given their global range, horizontal transmission by conidia or spores must also be effective.
Tissue specificity and abundance of infection sites
Endophytic Xylaria show moderate tissue specificity within their host plant. Some appear to be restricted to bark (Griffith and Boddy, 1990
), while others are found primarily within vascular tissue or in the leaf veins (Rodrigues, 1994
). In this study, endophytes were found in only the rhizoids of some of the liverworts. This pattern of endophyte infection has often been reported in hepatics (Pocock et al., 1984
; Duckett and Read, 1991
; Duckett et al., 1991
; Williams et al., 1994
; Duckett and Read, 1995
; Chambers et al., 1999
). In most culture studies of leaf endophytes, Xylaria is abundant in plant tissue (e.g., Rodrigues, 1994
), and in this study of plants with rhizoids, fungi were seen in nearly every rhizoid examined. Further examination using staining techniques is needed to fully address the question of tissue specificity in liverwort endophytes.
Secondary metabolites and related pathogen antagonists
The production of secondary compounds that are toxic to herbivores or pathogens is a common characteristic of many endophytic mutualisms and also provides the basis for selection favoring the symbiosis in the host plant (Carroll, 1988
). In vitro studies of endophytic Xylaria have shown that they actively produce secondary metabolites (Brunner and Petrini, 1992
), and these may also be produced when the fungus inhabits living plant tissues. Such metabolites include antifungal and antibiotic compounds (Brunner and Petrini, 1992
; Petrini et al., 1995
). The secondary compounds of the xylariaceous endophyte, Muscodor albus, were experimentally shown to inhibit the growth of a broad range of plant and human pathogenic bacteria and fungi (Strobel et al., 2001
). There has been no research on how these important compounds may affect host ecology.
Accumulating evidence suggests that relationships between endophytic Xylaria and their hosts are complex. Much further study of endophytic Xylaria is needed to fully understand their ecology. Transplant and inoculation experiments are also needed to address the question of whether Xylaria is a mutualistic, antagonistic, or commensalistic endophyte. We are currently attempting to conduct inoculation experiments with liverworts and their endophytic Xylaria in order to examine the effect of the fungus on host fitness.
Endophytes in the Hypocreales and the Ophiostomatales were also found growing within liverworts in this study. These fungi are well known for their interactions with vascular plants, fungi, and insects (e.g., Claviceps and Cordyceps, Ophiostoma and Fusarium). Their detection within liverworts is an intriguing area for future examination.
Possible ecological links between vascular plants, fungi, and liverworts
Duckett and Read (1995)
suggested that the same species of ascomycetous fungi that forms ericoid mycorrhizae can also be found in the rhizoids of liverworts. They were able to synthesize the ericoid-type mycorrhiza in axenic plants using inoculum from liverworts. The combined results of this and the present study indicate that liverworts and angiosperms may serve as alternative hosts for particular fungi. Further, if endophyte links between these plants occur in nature, the potential for nutrient exchange and recycling among plants exists. The possibility of such a complex ecological web invites further study.
Patterns in liverwort–fungal associations
It is unclear whether liverwort endophytes are species- or habitat-specific. While endophytes in Cephaloziella exilifora appear to be the same in Antarctica and Australia (Chambers et al., 1999
), different ascomycetes were isolated from Calypogeia mulleriana in the UK (Duckett and Read, 1995
) and North America (present work). In addition, an hepatic-specific ascomycetous endophyte, Mniaecia jungermanniae (Nees ex Fr.) Boud. (Leotiaceae), has been documented from numerous liverworts, including C. mulleriana (Raspe and De Sloover, 1998
). Results of the present study indicate that multiple endophytes infect the same liverwort individual and are suggestive that the same species of Xylaria and/or its close relatives have a wide host range. We are currently examining geographic patterns of endophyte diversity in another widespread temperate liverwort, Scapania undulata (L.) Dum. (Scapaniaceae).
Evolution of the fungus–land plant association
It has been suggested that the evolution of the fungus–plant mutualism was a crowning event in the evolutionary history of these two groups of eukaryotes, enabling them to colonize and dominate terrestrial habitats (e.g., Pirozynski and Malloch, 1975
). The relationship between liverworts and Xylaria is likely to be a relatively new one, because although liverworts are one of the basal-most lineages of land plants (Nickrent et al., 2000
), the clade containing Xylaria is more recently derived (Berbee and Taylor, 2001
). Nevertheless, the morphology of their association may be suggestive of what these early plant–fungal associations looked like. Additional liverwort–fungal associations deserve further examination. For instance, the complex thalloid liverworts (Marchantiidae) reportedly contain endophytic Glomales (Boullard, 1988
), which indeed may have evolved during the period when plants were invading land.
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FOOTNOTES |
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2 E-mail: christine.davis{at}duke.edu
.
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