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REPORT Resource quantity, not resource heterogeneity, maintains plant diversity M. Henry H. Stevens* and Walter P. Carson Program in Ecology and Evolution, Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, U.S.A. *Correspondence and present address: Department of Botany, 316 Pearson Hall, Miami University, Oxford, OH 45056 USA. E-mail: [email protected] Abstract Resource heterogeneity has often been proposed to explain the maintenance of plant species diversity and patterns of species diversity along productivity gradients. Resource heterogeneity should maintain biodiversity by preventing competitive exclusion because different species are superior competitors in different parts of a heterogeneous environment. In natural systems, however, resource heterogeneity covaries with average resource supply rate, making the effect of heterogeneity difficult to isolate. Using a novel experimental approach, we tested the independent effects of resource heterogeneity and average supply rate on plant species diversity. We show that the average supply rate of the most limiting resource controlled species diversity, whereas heterogeneity of this resource had virtually no effect. These findings also suggest that biodiversity declines with increasing productivity because at high enough levels of productivity one resource may always be driven to sufficiently short supply to exclude many species. Keywords Assemblage level thinning, enemy free space, heterogeneity, productivity gradient, resource ratio, species diversity, species richness. Ecology Letters (2002) 5: 420–426 INTRODUCTION Spatial heterogeneity of one or more limiting resources should prevent competitive exclusion and maintain high species richness (Hardin 1960; MacArthur 1970; Grubb 1977; Ricklefs 1977; Tilman 1982; Palmer 1994; Crawley 1997; Nicotra et al. 1999; Kassen et al. 2000). Several general theoretical models of local species interactions (MacArthur 1970; Levin 1976; Tilman 1982; Abrams 1988; Pacala & Tilman 1994) make at least two robust predictions: (1) spatial heterogeneity of limiting resources governs the number of co-occurring species (i.e. species richness), and (2) species habitat requirements and the relative abundance of different microhabitat types determine species relative abundances. In contrast, a wide variety of other hypotheses suggest that species richness is determined by the average supply rates of the most limiting resources (Preston 1962; MacArthur & Wilson 1963; Wright 1983; Rosenzweig & Abramsky 1993; Abrams 1995; Hurtt & Pacala 1995; Srivastava & Lawton 1998; Grace 1999; Stevens & Carson 1999b; Morin 2000; Hubbell 2001). Although critical differences exist within this group of hypotheses, each predicts that: (1) species richness will increase with increasing resource and energy availability, and (2) the most abundant species in the species pool may dominate any particular site by chance alone. For the remainder of this paper, we will refer to these two sets of predictions as the heterogeneity hypothesis and the energy hypothesis. Here we test the heterogeneity hypothesis and the energy hypothesis by measuring the relative importance of spatial heterogeneity and the average supply rate of light in governing a widespread but paradoxical pattern: plant species richness falls as soil resource availability and productivity rise (Grime 1973; Tilman 1982; Rosenzweig & Abramsky 1993; Tilman & Pacala 1993; Waide et al. 1999; Gough et al. 2000; Gross et al. 2000; Mittelbach et al. 2001). The resolution to this paradox appears to lie with how light availability covaries with productivity (Tilman & Pacala 1993; Huston & DeAngelis 1994). As soil resources rise, and plant communities become more productive, light availabil- ity in the understorey declines. Understorey light availability probably governs species richness because all individuals of both canopy species and understorey specialists must survive and grow in the understorey at some point in their ontogenies (Grubb 1977; Harper 1977). Heterogeneity- related hypotheses assume that species specialize in different light levels (e.g. Ricklefs 1977; Pacala et al. 1996; Kobe 1999) or different ratios of light and soil resources (Tilman 1982; Ecology Letters, (2002) 5: 420–426 Ó2002 Blackwell Science Ltd/CNRS

Resource quantity, not resource heterogeneity, maintains plant diversity

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R E P O R TResource quantity, not resource heterogeneity,

maintains plant diversity

M. Henry H. Stevens* and Walter

P. Carson

Program in Ecology and

Evolution, Department of

Biological Sciences, University

of Pittsburgh, Pittsburgh, PA

15260, U.S.A.

*Correspondence and present

address: Department of Botany,

316 Pearson Hall, Miami

University, Oxford, OH 45056

USA. E-mail:

[email protected]

Abstract

Resource heterogeneity has often been proposed to explain the maintenance of plant

species diversity and patterns of species diversity along productivity gradients. Resource

heterogeneity should maintain biodiversity by preventing competitive exclusion because

different species are superior competitors in different parts of a heterogeneous

environment. In natural systems, however, resource heterogeneity covaries with average

resource supply rate, making the effect of heterogeneity difficult to isolate. Using a novel

experimental approach, we tested the independent effects of resource heterogeneity and

average supply rate on plant species diversity. We show that the average supply rate of

the most limiting resource controlled species diversity, whereas heterogeneity of this

resource had virtually no effect. These findings also suggest that biodiversity declines

with increasing productivity because at high enough levels of productivity one resource

may always be driven to sufficiently short supply to exclude many species.

Keywords

Assemblage level thinning, enemy free space, heterogeneity, productivity gradient,

resource ratio, species diversity, species richness.

Ecology Letters (2002) 5: 420–426

I N T R O D U C T I O N

Spatial heterogeneity of one or more limiting resources

should prevent competitive exclusion and maintain high

species richness (Hardin 1960; MacArthur 1970; Grubb

1977; Ricklefs 1977; Tilman 1982; Palmer 1994; Crawley

1997; Nicotra et al. 1999; Kassen et al. 2000). Several general

theoretical models of local species interactions (MacArthur

1970; Levin 1976; Tilman 1982; Abrams 1988; Pacala

& Tilman 1994) make at least two robust predictions:

(1) spatial heterogeneity of limiting resources governs the

number of co-occurring species (i.e. species richness), and

(2) species habitat requirements and the relative abundance

of different microhabitat types determine species relative

abundances. In contrast, a wide variety of other hypotheses

suggest that species richness is determined by the average

supply rates of the most limiting resources (Preston 1962;

MacArthur & Wilson 1963; Wright 1983; Rosenzweig &

Abramsky 1993; Abrams 1995; Hurtt & Pacala 1995;

Srivastava & Lawton 1998; Grace 1999; Stevens & Carson

1999b; Morin 2000; Hubbell 2001). Although critical

differences exist within this group of hypotheses, each

predicts that: (1) species richness will increase with

increasing resource and energy availability, and (2) the most

abundant species in the species pool may dominate any

particular site by chance alone. For the remainder of this

paper, we will refer to these two sets of predictions as the

heterogeneity hypothesis and the energy hypothesis.

Here we test the heterogeneity hypothesis and the energy

hypothesis by measuring the relative importance of spatial

heterogeneity and the average supply rate of light in

governing a widespread but paradoxical pattern: plant

species richness falls as soil resource availability and

productivity rise (Grime 1973; Tilman 1982; Rosenzweig

& Abramsky 1993; Tilman & Pacala 1993; Waide et al. 1999;

Gough et al. 2000; Gross et al. 2000; Mittelbach et al. 2001).

The resolution to this paradox appears to lie with how light

availability covaries with productivity (Tilman & Pacala

1993; Huston & DeAngelis 1994). As soil resources rise, and

plant communities become more productive, light availabil-

ity in the understorey declines. Understorey light availability

probably governs species richness because all individuals of

both canopy species and understorey specialists must

survive and grow in the understorey at some point in their

ontogenies (Grubb 1977; Harper 1977). Heterogeneity-

related hypotheses assume that species specialize in different

light levels (e.g. Ricklefs 1977; Pacala et al. 1996; Kobe 1999)

or different ratios of light and soil resources (Tilman 1982;

Ecology Letters, (2002) 5: 420–426

�2002 Blackwell Science Ltd/CNRS

Tilman & Pacala 1993) and each predicts that light

heterogeneity should govern species richness. Energy-

related hypotheses (Preston 1962; MacArthur & Wilson

1963; Wright 1983; Rosenzweig & Abramsky 1993; Hurtt &

Pacala 1995; Oksanen 1996; Grace 1999; Stevens & Carson

1999b; Hubbell 2001) do not necessarily rely on assump-

tions about species specializations and predict that the

average supply rate of light should govern species richness.

We used a novel experimental approach to test the

independent contribution of light heterogeneity to plant

species richness (Stevens 1999). After establishing an

experimental productivity gradient in an herbaceous plant

community, we used shade frames to manipulate independ-

ently understorey light heterogeneity, and the average supply

rate of understorey light. This allowed us, for the first time,

to test whether light heterogeneity governs species richness

along productivity gradients. This also allowed us to test the

key underlying assumption of whether species specialize in

low-light environments.

M E T H O D S

In 1995, we sprayed with herbicide and ploughed an

abandoned agricultural field in north-western Pennsylvania,

USA. We fertilized 192 plots (4 · 4 m, each separated by

1 m) at four different rates for 3 years (1996–8) (Osmoco-

teTM slow release fertilizer, 18–6–12 NPK, at rates of 0, 8, 16

and 32 g N m)2 year)1). By 1997, the field was dominated

by several Solidago spp., Agropyron repens and Milium effusum

(Stevens 1999). In free-standing vegetation without shade

frames, our soil resource gradient created patterns widely

observed in other studies of herbaceous plant productivity

gradients: as soil resources rise, above-ground biomass

increases, and species richness, average understorey light

supply rate, and understorey light spatial heterogeneity fall

(e.g. Grime 1973; Al-Mufti et al. 1977; Tilman 1987; Stevens &

Carson 1999b; Stevens 1999).

Six designs of shade frames (Fig. 1) (1 m W · 0.75 m

H · 3 m L) provided three levels of spatial heterogeneity at

each of two average supply rates when placed over growing

vegetation (‘‘heterogeneity’’ and ‘‘average supply rate’’ are

the standard deviation and mean of a spatial array of point

light measurements) (Table 1). We selected the levels of

supply rate and heterogeneity to represent the range of each

observed in free-standing vegetation at the above levels of

fertilizer (Table 1). Over a two-year period (1997, 1998), the

shade frames took the place of the canopies formed by the

tallest plants (e.g. Euthemia graminifolia, Solidago altissima). As

plants grew taller throughout the growing season, they were

guided around the opaque outside walls of the shade frames,

so that tall plants did not cast shade in the 30 · 150 cm

sample plots (Fig. 1) and confound the shade treatments. At

the beginning of the 1997 growing season, one shade frame

was placed in each of the 192 plots fertilized with one of

four levels of soil fertilizer (above) resulting in 24 unique

treatment combinations (n ¼ 8). The shade frames did not

Uniform Continuum Gap

Schematic 2-D overviewsof shade frame types

3m

1 m

Mo

der

ate-

Lig

ht

(30%

)

3m

Lo

w-L

igh

t(2

%)

3-D frame insurroundingvegetation

Sample plot(gray)

50cm

30 cm

Figure 1 The six shade frame types cre-

ated three levels of light heterogeneity at

each of two levels of average light supply

rate (see Table 1). In this schematic, the

degree of shading indicates shade cloth

opacity (density) with black areas trans-

mitting < 1% of ambient light and white

(no shade cloth) transmitting 100%

ambient light. Shade frames were orien-

tated north–south and placed over

growing vegetation. Ramets over 50 cm

tall were guided around the outside,

plastic-sheet walls of the frames. Plants

were sampled in three contiguous

30 · 50 cm subplots, and light was

sampled at 150 1.0 cm intervals along the

dashed transect.

Resource quantity and plant diversity 421

�2002 Blackwell Science Ltd/CNRS

substantially affect other environmental variables, and they

controlled light heterogeneity independently of average

supply rate of light and soil resources (Stevens 1999). The

size of the sample plots and the scale of the spatial

heterogeneity was proportional to the size of individuals

(Fig. 1), so that many small individuals or a fraction of the

largest clonal individuals could occupy a patch of a given

light availability. Thus, the spatial scale of the heterogeneity

was proportionally similar to most canopy gaps found in

forest and old-fields (Goldberg & Gross 1988; Canham et al.

1990; Kelly & Canham 1992). The spatial patterns of the

spectrum neutral shade cloth (PAK Unlimited, Inc.,

Cornelia, Georgia, USA) mimicked levels of light hetero-

geneity observed in free-standing vegetation at the same

levels of fertilizer addition (Stevens 1999). Even though the

vast majority of these species spread clonally, we removed

the shade frames at the end of the 1997 growing season to

allow natural colonization by seed. Frames were replaced at

the beginning of the following growing season.

We measured percentage PAR (photosynthetically active

radiation, lmol photons m)2 s)1) at 150 points spread out

at 1 cm intervals along the length of a 30 · 150 cm sample

plot centred under each frame (Fig. 1). We used two

Quantum point sensors (LiCorr, Inc., Lincoln, NE), one

15 cm above the soil surface, the other above the

vegetation, and converted PAR readings to percentage

transmittance by the canopy (percentage PAR transmitted).

We used the mean and standard deviation (Tilman 1982;

p. 103) to quantify average supply rate and heterogeneity of

light in each sample plot. We derived species richness and

relative abundance from estimates of percentage cover of

each species in each sample plot. We recorded all light and

cover data so that, within each 30 · 150 cm sample plot,

three contiguous 30 · 50 cm subplots could be analysed

separately, resulting in 576 subplots used for analyses where

specifically indicated below.

To test the direct effects of light heterogeneity, average

light supply rate, and average supply rate of soil resources,

we regressed ln(species richness) on the ln(SD[percent-

age PAR]), ln(mean[percentage PAR], and ln(g N m)2 + 2),

each measured directly for each 30 · 150 cm sample plot.

To test whether species were common in low-light plots

because they were regionally common, or because they

preferred low-light conditions, we regressed species’ fre-

quencies of occurrence in low-light plots on (1) species’

frequencies of occurrence in moderate-light plots and

(2) their observed resource ratios in the moderate-light

plots (all variables log transformed). Unlike other measures

of abundance (e.g. density, biomass), each species’ frequency

of occurrence (i.e. the number of plots in which a species is

present/total number of plots) is precisely the contribution

of each species to overall mean species richness, and the

sum of all species frequencies equals mean species richness

(Palmer & van der Maarel 1995; Stevens & Carson 1999a).

We calculated each species’ resource ratio as the mean of

(subplot percentage PAR)/(g N applied m)2 + 2), using

only data from the moderate-light shade frames. Thus, the

resource ratio used for each species in this study should be

considered a ‘‘realized resource ratio’’.

To test the assumption that species had different

resource requirements, we used ECOSIM software (Gotelli

& Entsminger 2001) to test whether mean electivity

overlap was smaller than expected by chance, using the 15

species that occurred in at least 50 of the 576 30 · 50 cm

subplots. Electivity overlap takes resource abundance into

account, and is preferred to niche overlap (cf. Silvertown

et al. 1999) when resources vary in abundance (Lawlor

1980; Gotelli & Graves 1996). This analysis retained each

species’ niche breadth and reshuffled zero abundance

values (randomization algorithm 3, Gotelli & Graves

1996). We calculated the mean percentage PAR transmitted

in each subplot, and pooled each of these means into one

Table 1 Average supply rate and heterogeneity of light in shade frames (n ¼ 32/type) and in free-standing vegetation (n ¼ 12/level) along

the experimental productivity gradient (mean[standard error]). Light under shade frames was independent of fertilizer level

Frame type Av. Supply rate (mean) Heterogeneity (SD)

High – Gap 0.34 (0.013) 0.306 (0.021)

High – Cont. 0.36 (0.015) 0.151 (0.012)

High – Unif. 0.38 (0.011) 0.060 (0.0072)

Low – Gap 0.021 (0.00062) 0.072 (0.0095)

Low – Cont. 0.025 (0.0014) 0.059 (0.0054)

Low – Unif. 0.018 (0.0023) 0.005 (0.00058)

Free-standing vegetation ( g N m)2 year)1)

0 0.23 (0.022) 0.130 (0.014)

8 0.092 (0.019) 0.056 (0.014)

16 0.031 (0.011) 0.029 (0.012)

32 0.010 (0.0030) 0.006 (0.0012)

422 M.H.H. Stevens and W.P. Carson

�2002 Blackwell Science Ltd/CNRS

of seven categories of light levels (0–5%, 5–15%, 15–25%,

25–35%, 35–45%, 45–55%, and > 55%; higher light levels

were exceedingly rare). The seven light categories and

four soil fertility categories resulted in 28 different

resource combinations. Other combinations, including

fewer resource combinations (moderate vs. low light) and

more combinations (10 light levels · 4 soil fertilizer levels)

achieved the same qualitative result.

R E S U L T S A N D D I S C U S S I O N

Average supply rate of light, and not light heterogeneity,

governed species richness. The decline in average supply

rate of light caused a substantial decline in plant species

richness that was independent of the effects of soil resource

availability and light heterogeneity (Fig. 2a; partial

R2 ¼ 0.402***). In contrast, the increase in soil resources

(partial R2 ¼ 0.056*) and the decline in light heterogeneity

(partial R2 ¼ 0.004 NS) caused much smaller declines in

richness (Figs 2b.c). The results agree with results obtained

in previous years (Stevens 1999), and they provide no

support for a role of light heterogeneity in influencing

species richness.

Species composition in the species-poor, low-light plots

was best predicted by species’ relative abundances in the

moderate-light plots and not by species’ habitat preferences.

Specifically, species’ frequencies of occurrence in moderate-

light plots explained 37% of the variability in species’

frequencies in low-light plots (Fig. 3a), whereas species’

light : nitrogen ratios explained only 6% of the variability

(Fig. 3b). These results favour the energy hypothesis, where

random assembly from the species pool generates local

neighbourhoods, and total density in each local community

determines local species richness (Hurtt & Pacala 1995;

Stevens & Carson 1999a; Hubbell 2001). In addition, most

species occurred most often in similar light : nitrogen

conditions, and this also is consistent with the energy

hypothesis. Specifically, mean pairwise electivity overlap

(similar to niche overlap, Lawlor 1980; Gotelli & Graves

1996) was substantially greater than expected by chance

(observed mean electivity overlap ¼ 0.516, bootstrapped

mean ¼ 0.441, P < 0.001), and this broad overlap was

consistent among several levels of habitat resolution (see

Methods). These findings provide no support for the

assumptions that underlie the heterogeneity hypothesis.

The above support for the energy hypothesis is consistent

with a variety of possible mechanisms. First and foremost,

decreasing understorey light availability generally causes a

large decrease in stem density (Stevens & Carson 1999b),

and consequently richness should decrease by chance alone

(‘‘More Individuals’’ hypothesis, Preston 1962; Rosenzweig

& Abramsky 1993; Srivastava & Lawton 1998). Assuming

that not all species exist in every plot, different species will

disappear from different plots, and many species will ‘‘win

by default’’ because the best low-light specialists are not

present everywhere (Hurtt & Pacala 1995). The effect of

increasing productivity is to exacerbate this ‘‘winning by

default’’, and is not related directly to specialization in any

particular light level. Further, any strict interspecific hier-

archy can be weakened by positive indirect effects (Miller

1994), by large within-population variability in resource

requirements (Clements 1929; Linhart & Grant 1996), or by

equally strong intraspecific effects (Brokaw & Busing 2000;

Hubbell 2001).

Our conclusions may apply to other light-limited plant

communities because the plant community used in

this experiment shares many characteristics with other

Partial R 2 = 0.056***-2

-1

0

1

2

-4 -3 -2 -1 0 1 2 3

Fertilizer

b

Partial R 2 = 0.402***

-2

-1

0

1

2

-4 -3 -2 -1 0 1 2 3

Light Quantity

a

Partial R 2 = 0.004*

-2

-1

0

1

2

-4 -3 -2 -1 0 1 2 3

Light Heterogeneity

c

Sp

ecie

s ri

chn

ess

Average Light Supply Rate

Figure 2 Effects of (a) average light supply rate (units ¼ log[mean

PAR]), (b) fertilizer (units ¼ log[g N m)2 + 1]) and (c) light het-

erogeneity (units ¼ log[SD PAR]) on species richness (log[no. of

spp. 0.45 m)2 + 1]) (multiple R2 ¼ 0.824***; Type III sums of

squares on all factors, *P < 0.05, ***P < 0.001). The above partial

regression plots plotted all variables as residuals of the labelled

variable, given the two factors not shown in the plot (Neter et al.

1996). As a result, these partial regression plots obscure the clus-

tering of light supply rate treatments (low, high) and heterogeneity

treatments (uniform, continuum, gap) that would be apparent in a

simple scatter plot.

Resource quantity and plant diversity 423

�2002 Blackwell Science Ltd/CNRS

light-limited plant communities. As in virtually all other

communities, the community used here had already

undergone a sorting process, where some potential

community members (e.g. annuals) had been largely

excluded. As in other plant communities (e.g. Bazzaz

1996; Pacala et al. 1996), this community exhibited no

stable equilibrium prior to experimental treatments. As

with species in other communities, the herbaceous species

in this community undoubtedly differed significantly in

many ways (Grime et al. 1988) including physiological

responses to variation in light levels (Latham 1992; Kobe

et al. 1995; Larcher 1995; Kobe 1999). Herbaceous

perennials also commonly exhibit a large degree of

genetic variation within populations (Thomas & Bazzaz

1993; Geber & Dawson 1997) and local adaptation

(Linhart & Grant 1996). Thus it is not clear that the

community used in this experiment differs from other

communities in ways that would prevent generalization

to other communities where light is limiting (Bazzaz

1996).

Lastly, our results and those of other studies along

productivity gradients (Leibold 1996; Bohannan & Lenski

2000) suggest that the average abundance of a single

resource that limits most species in a community also

controls species richness. Favoured explanations for why

species diversity declines with increasing productivity

appear to depend on the system where the pattern occurs

(Waide et al. 1999; Mittelbach et al. 2001). In terrestrial

plant assemblages, increasing soil resource supply rates

increase above-ground biomass, which causes declines in

another key resource, light. In our study, it was the decline

in average light supply rate that drove down species

richness along our soil fertility gradient. In aquatic systems,

increasing the inorganic nutrients increases predation rates,

and this increase in predation can drive down prey species

richness (Leibold 1996; Bohannan & Lenski 2000). If we

envision a set of conditions that reduces the effects of

predation, this set of conditions could constitute a resource

that we call predator-free space (Holt 1977; Jeffries &

Lawton 1984; Holt & Lawton 1994). One species may be a

superior competitor for predator-free space when it

‘‘consumes’’ this resource by supporting higher predator

abundances than other species, and reduces remaining

predator-free space to such an extent that other species fail

to persist (Holt & Lawton 1994). The decline in species

richness observed along productivity gradients in both

terrestrial and aquatic systems thus results from a decline

in the average supply rate of the most limiting resource,

whether that resource is light or predator-free space. The

symmetry of the effect of predators and competitors on a

population is an old idea (MacArthur 1970), and it now

promises to unify explanations for the loss of diversity

along productivity gradients in different ecological systems.

We suggest that reducing the resource that limits most

species, not the resource most limiting to total ecosystem

productivity, will cause species richness to decrease as well.

We propose that such a relatively simple idea, analogous to

Liebig’s law of the minimum, has been overlooked in

previous explanations for the complexity of ecological

systems.

A C K N O W L E D G E M E N T S

We thank A. E. K. Long and other research interns for

technical assistance, and J. Fox, M. Leibold, Z. Long,

T. E. Miller, P. J. Morin, and O. Petchey for comments.

Supported by NSF grant DEB 9903912 to W. P. Carson,

NSF grant DEB 9806427 to P. J. Morin and T. M.

Casey, the New Jersey Agricultural Experiment Station,

University of Pittsburgh, and Pymatuning Laboratory of

Ecology (Pymatuning Laboratory publication number

110).

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Moderate-Light Freq. of Species i

-1.0

-0.5

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1.0

Lo

w-L

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t F

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cy o

f S

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-1.0 -0.5 0.0 0.5 1.0

Resource Ratio of Species i

a bPartial R2 = 0.34 Partial R 2 = 0.06

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Editor, A. Troumbis

Manuscript received 11 December 2001

First decision made 11 January 2002

Manuscript accepted 19 February 2002

426 M.H.H. Stevens and W.P. Carson

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