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Reproductive Biology |
2Department of Biology, Grinnell College, Grinnell, Iowa 50112-1690 USA; 3Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853-2701 USA
Received for publication September 15, 2000. Accepted for publication March 27, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: autogamy • bee-pollination • Clarkia xantiana • pollination • reproductive assurance • self-pollination
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Wyatt, 1983, 1986, 1988
). A significant factor expected to contribute to this trend is natural selection for reproductive assurance (Jain, 1976
; Lloyd, 1979, 1980, 1992
; Holsinger, 1996
; Schoen, Morgan, and Bataillon, 1996
). According to this reproductive assurance hypothesis, selection favors increased self-pollination in situations in which pollinator service strongly limits reproduction, due to mate and/or pollinator scarcity (Darwin, 1876
; Baker, 1955, 1967
). Once self-pollination has evolved, via selection for reproductive assurance and/or other reasons, the environmental conditions responsible for mate and/or pollinator limitation would also be expected to make establishment of self-pollinating populations more likely than establishment of outcrossing populations (Baker, 1955, 1967
). Thus, the value of reproductive assurance is expected to contribute to the evolutionary origin of self-pollination and to affect the geographic distributions of populations that differ in breeding system.
The main support for the significance of reproductive assurance to date has come from comparative tests of predictions about the availability of pollinating agents and mates. Compared to sites where outcrossing populations occur, sites where derived self-pollinating populations occur would be expected to have, in animal-pollinated taxa, lower pollinator density and pollinator visitation rate. Some studies have noted that self-pollinating populations are common in habitats where pollinators appear to be scarce or where flowering occurs at times of pollinator scarcity (e.g., Schemske, 1978
; Motten, 1982
; Piper, Charlesworth, and Charlesworth, 1986
). Other studies have shown that the frequency of self-fertile taxa is higher on oceanic islands than on mainland areas (e.g., Baker, 1955, 1967
; Barrett, 1996
). The latter pattern might suggest that self-pollinating populations are more likely to evolve (or establish) in situations in which the pollinators of outcrossing taxa are absent or in which population sizes are small, such as after long-distance dispersal to oceanic islands (Baker, 1955, 1967
). Very few studies, however, have quantified and documented pollinator and/or mate scarcity where self-pollinating populations occur vs. where related outcrossing populations occur (Barrett, Morgan, and Husband, 1989
; Ramsey and Vaughton, 1996
).
If comparatively low plant densities were found in self-pollinating populations, then it also would be significant if there were evidence of positive density dependence of pollinator visitation, pollen deposition, and seed production in the same systems. Such density dependence would be expected to reinforce the benefits of reproductive assurance in low-density situations. Numerous studies have shown that plant density increases pollinator visitation and pollen deposition (e.g., Lloyd, 1965
; Thomson, 1981
; Wyatt, 1986
; Burdon, Jarosz, and Brown, 1988
; Barrett, Morgan, and Husband, 1989
; Allison, 1990
; Widén, 1993
; Bosch and Waser, 1999
) and/or more direct components of reproductive success (e.g., Allison, 1990
; Kunin, 1993, 1997
; Widén, 1993
; Roll et al., 1997
; Pannell and Barrett, 1998
; Bosch and Waser, 1999
; Steffan-Dewenter and Tscharntke, 1999
). Studies of these patterns have seldom been carried out, however, in studies of the evolution of self-pollination (Ramsey and Vaughton, 1996
; Eckert and Schaefer, 1998
).
Thus, although various lines of indirect evidence support the reproductive assurance hypothesis, thorough examinations of the idea within a single system are rare, and the significance of reproductive assurance in the evolution and ecology of self-pollination remains uncertain (Holsinger, 1996, 2000
; but see Fishman and Wyatt, 1999
). It is critical to combine quantitative studies of mate availability, pollinator availability and visitation, and pollination success in order to identify the ecological circumstances that may generate selection for reproductive assurance in a particular case.
The California annual Clarkia xantiana ssp. xantiana A. Gray (Onagraceae) represents a promising model system for the study of the transition between outcross- and self-pollination. The principal pollinators of C. xantiana are solitary and semisocial bees from at least six families; among these are several bee species known to specialize on Clarkia pollen for offspring provisioning (McSwain, Raven, and Thorpe, 1973
; M. A. Geber and V. M. Eckhart, personal observation). Flowers of Clarkia xantiana ssp. xantiana are strongly protandrous and have stigmas that extend several millimeters beyond the anthers (Moore and Lewis, 1965
; Eckhart and Geber, 1999
; Runions and Geber, 2000
); these are character states associated with outcrossing in Clarkia (Holtsford and Ellstrand, 1992
). In contrast, flowers of C. xantiana ssp. parviflora (Eastw.) Harlan Lewis comb. nov. display little or no protandry or anther–stigma separation (Moore and Lewis, 1965
; Lewis and Raven, 1992
; Eckhart and Geber, 1999
; Runions and Geber, 2000
). In this subspecies, dehisced anthers and receptive stigmas are often in contact at, or sometimes before, anthesis (Eckhart and Geber, 1999
; M. A. Geber and V. M. Eckhart, personal observation). In greenhouse cultivation and in nature, ssp. parviflora self-pollinates by autonomous autogamy (sensu Lloyd, 1992
); though it is self-compatible, ssp. xantiana does not exhibit autogamy (M. A. Geber and V. M. Eckhart, personal observation). Cytogenetic and allozyme evidence indicates that ssp. parviflora was derived from the outcrossing subspecies (Moore and Lewis, 1965
; Gottlieb, 1984
). Breeding system correlates with geography and environment. Subspecies xantiana occurs mainly in relatively mesic grasslands and oak–pine woodlands in the western section of the species' range in central and southern California, while subspecies parviflora occurs mainly in relatively arid shrublands and pinyon–juniper woodlands in the eastern section of the range; the two subspecies co-occur in a narrow band in the center, mainly along the North Fork of the Kern River (Eckhart and Geber, 1999
; see Fig. 1).
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; Lewis and Lewis, 1955
; Vasek, 1968
), and numerous studies have investigated reproductive evolution and ecology in the genus (e.g., Moore and Lewis, 1965
; Vasek, 1968
; McSwain, Raven, and Thorpe, 1973
; Vasek and Harding, 1976
; Vasek and Weng, 1988
; Holtsford and Ellstrand, 1992
; Jones, 1994
; Sherry and Lord, 1996
; Groom, 1998
; Runions and Geber, 2000
; Travers and Mazer, 2000
). Despite this attention, no previous studies have carried out a quantitative evaluation of the reproductive assurance hypothesis in Clarkia. Our objective in this paper is to evaluate critical aspects of the reproductive assurance hypothesis in C. xantiana. If selection for reproductive assurance contributed to the evolution of autogamy and/or if reproductive assurance has affected the distributions of outcrossing and self-pollinating populations, then one would expect autogamous populations to experience lower densities of mates and pollinators and lower rates of pollinator visitation than outcrossing populations. One also might expect positive density dependence of pollinator visitation and pollen receipt within populations. Here we address the following questions: (1) Are measures of mate availability (i.e., the density of plants and flowers) lower in autogamous populations than in outcrossing populations? (2) Are measures of pollinator service (i.e., pollinator density and pollinator visitation rate) lower in autogamous populations than in outcrossing populations? (3) Does pollinator visitation increase with plant density and flower density? (4) Does pollen deposition (in outcrossing populations) increase with plant density?
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In the western region is an "Outcrossing Zone," where only C. xantiana ssp. xantiana populations occur. In the central region is a "Contact Zone," where both subspecies occur, sometimes at the same sites. Finally, an "Autogamous Zone" to the east defines a region where only C. xantiana ssp. parviflora populations occur. In addition to studying populations within these zones, we also studied one outlying population of each subspecies (Fig. 1). For analytical purposes, we classified the outlying ssp. xantiana population as belonging to the Outcrossing Zone and the outlying ssp. parviflora population as belonging to the Autogamous Zone.
Pollinator assemblage
We successfully collected bees foraging on C. xantiana at nine sites in the Outcrossing Zone, five in the Contact Zone, and two in the Autogamous Zone. These numbers are not proportional to search effort in each zone; we searched for pollinators at several additional sites in the Autogamous Zone but failed to locate any pollinators. Pollinator sampling was not standardized by person-hours and consequently cannot be used to estimate pollinator abundance directly. Instead we used the data for qualitative comparisons of the composition of pollinator assemblages among zones and between subspecies.
Plant and flower densities
We estimated plant and flower density at 36 populations: 10 in the Outcrossing Zone; 16 in the Contact Zone (9 where ssp. xantiana was flowering and 7 where ssp. parviflora was flowering); and 10 in the Autogamous Zone. We made these estimates by counting all C. xantiana plants and flowers in ten systematically dispersed, 0.79-m2 quadrats at each site and then calculating means for each site. Flowering time differs between the subspecies, with ssp. parviflora flowering 2–4 wk earlier than ssp. xantiana where they co-occur (Moore and Lewis, 1965
; Eckhart and Geber, 1999
). Consequently, sampling dates in the Contact Zone were substantially (and necessarily) earlier for ssp. parviflora populations than for ssp. xantiana populations.
Pollinator density, visitation rate, and response to plant density
We scored pollinator activity once at 30 of the above 36 sites, between the hours of 0830 to 1630 Pacific Daylight Time. At each site, we placed a 0.79-m2 quadrat frame at ten haphazardly selected locations and counted the number of plants and flowers enclosed within the frame. We did not position quadrats systematically because, in this case, we needed to ensure that at least one plant was included in the quadrat so that we could observe pollinator activity. We observed each quadrat for 5 min, and we scored the number of pollinators that entered the frame and the number of plants and flowers visited by each pollinator. Only insects that clearly contacted anthers and/or stigmas during their flower visit were considered pollinators; all such insects observed were foraging for nectar and/or pollen. We did not count flying insects that entered the frames but were not observed to forage on C. xantiana in the population, as it could not be determined with certainty whether these insects were potential pollinators. Using these data, we estimated the number of actively foraging pollinators per unit time per unit area (a pollinator density estimate) and the number of visits per plant per unit time (a pollinator visitation rate estimate). We also estimated plant and flower density within each quadrat, which made it possible to assess the effects of these features on pollinator visitation rate.
Plant density and pollen deposition
We estimated density effects on pollen receipt in a population of C. xantiana ssp. xantiana in the Contact Zone. At the beginning of June, we emasculated a single, male-phase flower on each of 35 haphazardly selected individuals. The majority of focal individuals possessed only a single open flower at the time. For each focal plant, we recorded the mean distance to the nearest two neighboring plants. Density (d) is expected to relate to mean nearest-neighbor distance (r) as d = 1/4r2 (Clark and Evans, 1954
). On 5 June, after stigmas became receptive but before flowers began to wilt, we located and collected focal flowers' stigmas on 32 of the 35 experimental plants. These stigmas we stored dry in waxed-paper envelopes for 6 wk, and then we used a dissecting microscope to count C. xantiana pollen grains on each stigma. As emasculation prevented the deposition of autogamous pollen, any pollen found on stigmas represented pollinator-mediated deposition from other flowers or plants. The number of seeds per fruit observed in natural populations of C. xantiana ssp. xantiana reaches a maximum of 
35 (out of an average of 55 ovules per ovary) (D. A. Moeller, Cornell University, unpublished data). Thus, a conservative minimum estimate of the pollen grains required to achieve maximum seed set is 35.
Statistical analysis
To evaluate subspecies and geographic variation in mate and pollinator availability, we first classified sites according to the subspecies investigated there (xantiana or parviflora) and the zone in which it occurred (Outcrossing, Contact, or Autogamous). Thus, there were four categories: ssp. xantiana in the Outcrossing Zone (XO), ssp. xantiana in the Contact Zone (XC), ssp. parviflora in the Contact Zone (PC), and ssp. parviflora in the Autogamous Zone (PA). As the distributions of these variables were nonnormal and had heterogeneous variances, we made pairwise comparisons among zone–subspecies categories using the nonparametric Mann-Whitney U test.
We used parametric statistics for other analyses. The pollen deposition data we analyzed by log10-transforming the variables and then regressing pollen grain number per stigma on the mean distance to the two nearest neighbors (which is related inversely to density as indicated above). We used nested analysis of covariance to assess the effects of flower density and plant density on pollinator visitation rate, while accounting also for effects of zone (considered a fixed factor) and for variation among sites nested within zones (considered a random factor). To generate the F test for the zone effect, we divided the zone mean square by the mean square of the nested factor. As tests for heterogeneity of slopes revealed no significant interactions between zone and the covariates, interaction terms were dropped from the analysis of covariance models.
The analyses of pollinator responses to plant density and flower density required care in design and interpretation. Continuous variables in these analyses were nonnormal (see above). The distributions of residuals closely approached normality, but did not quite achieve it. Therefore, significance tests should be taken as approximate. (Residuals did not correlate with predicted values, however, which would have been a more serious problem.) Another caveat arose from the fact that plant and flower densities varied among zones (i.e., the fact that a treatment variable affected covariates in analysis of covariance; see Neter and Wasserman, 1974
, chapter 22). Because overlap in densities among zones was substantial, this problem (akin to multicollinearity in multiple regression) was minor. Nevertheless, as it may have reduced the power to detect the zone effect, the significance tests for zone should be considered conservative. It also was the case that at five study sites in the Contact Zone where the two subspecies co-occurred (though only one subspecies was in flower on our sampling date), estimates of plant density may have inadvertently included nonflowering individuals of the other subspecies. We therefore analyzed the effect of plant density on per-plant visitation rate (visits per plant per 5-min interval) only in the Outcrossing and Autogamous zones. Finally, because the four zone–subspecies categories do not represent a clear one-way classification suitable for ANOVA, we analyzed the effect of flower density on per-plant visitation rate over the unambiguous one-way classification of geography alone, pooling the ssp. xantiana and ssp. parviflora sites in the Contact Zone. We carried out all statistical analyses with Minitab versions 12 and 13 (MINITAB, 2000
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Visitation rates varied in a somewhat different fashion than pollinator density. Visitation rate on a per-plant basis declined from 0.28 ± 0.06 visits · plant–1 · 12 h–1 for XO to 0.24 ± 0.09 visits · plant–1 · 12 h–1 for XC to 0.14 ± 0.07 visits · plant–1 · 12 h–1 for PC to 0.02 ± 0.01 visits · plant–1 · 12 h–1 for PA. Category PA was significantly lower than the two sets of outcrossing populations, but not significantly lower than the PC category (Fig. 2). For visitation rate on a per-flower basis, the ssp. parviflora populations in the Contact Zone had the highest values (0.19 ± 0.09 visits · flower–1 · 12 h–1 compared to 0.14 ± 0.03 visits · flower–1 · 12 h–1, 0.14 ± 0.06 visits · flower–1 · 12 h–1, and 0.02 ± 0.01 visits · flower–1 · 12 h–1 for the XO, XC, and PA categories, respectively; Fig. 2). As in the case of visitation rate on a per-plant basis, category PA was significantly lower than both sets of outcrossing populations, but not significantly different from the PC category (Fig. 2).
Density and pollinator visitation
Densities of plants and flowers significantly affected pollinator visitation. For every ten plants per 0.79 m2 quadrat (i.e., for every increase in density by 12.7 plants/m2), pollinator visits increased by 0.85 visits · plant–1 · 5 min–1 (Table 2), and for every ten flowers per quadrat, visits increased by 0.58 visits · plant–1 · 5 min–1 (Table 3). Among-zone variation was significant in the analysis of visits per plant (Table 2; least-squared means: 0.155 visits · plant–1 · 5 min–1 in the Outcrossing Zone and 0.003 visits · plant–1 · 5 min–1 in the Autogamous Zone), but, despite substantial variation among least-squared means, not significant in the analysis of visits per flower (Table 3; least-squared means: 0.068 visits · flower–1 · 5 min–1 in the Outcrossing Zone, 0.046 visits · flower–1 · 5 min–1 in the Contact Zone, and 0.003 visits · flower–1 · 5 min–1 in the Autogamous Zone).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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). There also was significant geographic variation among outcrossing populations, with densities higher in the Contact Zone.
A second significant pattern was that pollinator density and pollinator visitation rate were relatively low in autogamous populations, significantly lower in the region where only autogamous populations occur than in outcrossing populations. (Surprisingly, the highest mean visitation rate on a per-flower basis was found in selfing populations in the Contact Zone.) This finding confirmed the expectation that pollinators are more scarce and/or pollinator service less dependable where self-pollinating populations occur (see also Barrett, Morgan, and Husband, 1989
; Ramsey and Vaughton, 1996
). The Autogamous Zone also was distinctive in the composition of its pollinator assemblage; no Clarkia specialist pollinators were found there.
Low pollinator availability estimates in self-pollinating populations could have had several causes, not all of which would indicate a genuine scarcity of pollinators. For example, pollinator scarcity in the Autogamous Zone could have been an artifact of low plant and flower densities in the region (Fig. 2), as pollinators were found to avoid within-population patches with low plant and flower densities (Tables 2, 3). The finding that zone effects on visitation rate remained significant after adjusting for the effect of plant density, however, suggests that pollinator densities were genuinely low in the Autogamous Zone. If this were not the case, then we would have expected the visitation differences between the Outcrossing and Autogamous zones to be explained completely by density differences between zones.
Another possibility is that low pollinator visitation in autogamous populations arose from pollinator avoidance of the less conspicuous, and presumably less rewarding, self-pollinating subspecies. Though we suspect that such pollinator discrimination may occur, we would argue that this factor is unlikely, by itself, to have accounted for the observed pattern. If it had, then pollinator discrimination should have been equally (or especially) strong where the subspecies co-occur, but self-pollinating populations in the Contact Zone exhibited intermediate levels of pollinator visitation that did not differ significantly from those of outcrossing populations (Fig. 2). If pollinator avoidance of ssp. parviflora were responsible for low visitation rates, we also would not have expected to collect similar sets of pollinators on outcrossing and selfing populations in the Contact Zone (Table 1). (It remains possible that a quantitative study may reveal differences between the subspecies' pollinator assemblages in the Contact Zone.)
This study provided two other kinds of evidence that reproductive assurance might have been important in the evolution and ecology of selfing. First, increases in local plant and flower density increased rates of pollinator visitation. Many studies have found similar density dependence of pollinator service (see above references); the present finding is significant because it was made in the context of a study of the evolution of self-pollination (Barrett, Morgan, and Husband, 1989
; Eckert and Schaefer, 1998
). A caveat is that increased pollinator visitation may also increase the deposition of self-pollen (Snow et al., 1996
). Second, this study verified that pollen deposition declined with increasing isolation of individuals in C. xantiana. Similar findings appear in numerous studies (see above references). For example, Groom (1998)
found that pollen receipt on stigmas declined with distance to nearest neighbors in small patches of a congener, Clarkia concinna. While density dependence of these forms is not necessary or sufficient to create selection for reproductive assurance, it would be expected to strengthen such selection.
Taken together, this research suggests that reproductive assurance has been significant in the evolutionary ecology of self-pollination in C. xantiana by influencing the evolutionary origin of autogamy in C. xantiana and/or the contemporary geographic distributions of self-pollinating and outcrossing populations. At least three sets of outstanding questions remain.
The first set concerns how the observed variation in mate density, pollinator visitation, and pollen deposition translates into variation in seed production. In other words, how much reproductive assurance does autogamous self-pollination provide? Related work on C. xantiana suggests that autogamy confers substantial reproductive assurance. In experimental populations of transplanted outcrossing and autogamous plants in all three zones, supplemental hand-pollination significantly increased fruit set and/or seed set in the Autogamous Zone, but not in the others (M. A. Geber and V. M. Eckhart, unpublished data). Experimental emasculation of flowers (Schoen and Lloyd, 1992
; Eckert and Schaefer, 1998
; and references therein) in natural autogamous populations would provide an independent means to quantify the reproductive assurance that autogamy provides.
The second set of questions concerns the action of other factors that can affect the evolution of self-fertilization. For example, alleles that enforce self-pollination should possess a selective advantage when rare, as they can be transmitted both through self-pollination and (depending on the level of pollen discounting, defined as reduction in success of outcross pollen donation associated with self-pollination) through outcross pollen donation; alternative alleles enforcing outcrossing can only be transmitted via outcrossing with other outcrossing individuals (Fisher, 1941
; Holsinger, Feldman, and Christiansen, 1984
; Lande and Schemske, 1985
; Schemske and Lande, 1985
; Lloyd, 1992
; Holsinger, 1996, 2000
; Schoen, Morgan, and Bataillon, 1996
). In C. xantiana, is this advantage of selfing, plus the benefit of reproductive assurance, sufficient to outweigh the costs of inbreeding depression expected to accompany self-pollination (Charlesworth and Charlesworth, 1987
; Husband and Schemske, 1996
)? Quantification of these benefits and costs (or special analyses of population genetic structure [see Schoen, Morgan, and Bataillon, 1996
]) are necessary to quantify the contribution of selection for reproductive assurance to breeding system evolution in C. xantiana.
The final questions concern the geography of breeding-system evolution in C. xantiana. Moore and Lewis (1965)
speculated that C. xantiana ssp. parviflora arose at the edge of the range of its outcrossing progenitor through catastrophic selection for early flowering and self-pollination in exceptional drought years. The discovery that most of the range of C. xantiana ssp. parviflora lies outside the range of C. xantiana ssp. xantiana was made only recently (Eckhart and Geber, 1999
). Did autogamy evolve (or, if it has evolved more than once, did it tend to evolve) at the periphery of the outcrossing subspecies' range (in which case the Contact Zone represents primary contact) or in allopatry (in which case the Contact Zone represents secondary contact)? Did autogamy evolve mainly via selection for reproductive assurance in allopatry, or did autogamy evolve—for that reason or others—on the periphery of the outcrossing subspecies' range and then subsequently allow colonization of arid regions that support lower population densities, fewer pollinators in general, and no specialist pollinators? Although the current findings alone cannot answer these questions definitively, ongoing molecular studies of population structure and phylogenetics in C. xantiana should add resolution.
A final note of interest is that low mate availability and low pollinator service were most evident in self-pollinating populations that appear to occur outside the range of specialist pollinators abundant elsewhere. It may be worth considering further the role of geographic variation in pollinator assemblages in the evolution and ecology of plant breeding systems.
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FOOTNOTES |
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4 Author for reprint requests (e-mail: eckhart{at}grinnell.edu
).
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LITERATURE CITED |
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