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22001166 SOUTHEASTERN NATURALIST 1V5o(3l.) :1450,3 N–4o1. 43
Organic-matter Retention and Macroinvertebrate
Utilization of Seasonally Inundated Bryophytes in a
Mid-order Piedmont River
James Wood1,*, Meryom Pattillo1, and Mary Freeman2
Abstract - There is increased understanding of the role of bryophytes in supporting invertebrate
biomass and for their influence on nutrient cycling and carbon balance in aquatic
systems, but the structural and functional role of bryophytes growing in seasonally inundated
habitats is substantially less studied. We conducted a study on the Middle Oconee River,
near Athens, GA, to assess invertebrate abundance and organic-matter retention in seasonally
inundated patches of the liverwort Porella pinnata, a species that tends to be submerged
only when water levels in rivers are substantially above base flow. Aquatic invertebrate
utilization of these seasonally inundated habitats has rarely been investigated. Macroinvertebrate
biomass, insect density, and organic-matter content were significantly greater in
patches of P. pinnata than on adjacent bare rock. Bryophyte biomass explained additional
variation in organic matter, insect biomass, and density. The most abundant insects in P. pinnata
patches were Dipterans and Plecopterans. Our results suggest an important structural
role of seasonally inundated bryophyte habitats in riverine ecosystems.
Introduction
Macrophytes (aquatic vascular plants, bryophytes, and large algae) play important
roles in lotic ecosystems. Macrophytes influence the abundance of aquatic
invertebrates by providing protection from predators and increasing resource
availability (Glime 1994, Grubaugh and Wallace 1995, Lodge 1991, Nelson and
Scott 1962, Suren 1992). However, macrophytes are more often represented as
components of the floodplain rather than structural components within the channel.
Stream macrophytes influence stream metabolism directly via photosynthesis and
respiration, and these plants sequester and cycle nutrients from the water column,
trap organic material, and provide habitat for epiphytic algae (Arscott et al. 1998,
McWilliam-Hughes et al. 2009, Mulholland et al. 2000).
The roles of bryophytes in streams are best summarized by the Stream Bryophyte
Group (1999) and Glime (2015). Bryophytes have been shown to support
higher abundances and biomass of aquatic invertebrates than periphyton-covered
rocks (Heino and Korsu 2008, Parker and Huryn 2006). For example Lee and Hershey
(2000) report higher abundances of Natarsia (Chironomidae, chironomids),
Ephemerella (mayflies) and Brachycentrus and Rhyacophila (caddisflies) in bryophytes
compared to bryophyte-free areas in a long-term study of Alaska’s Kuparuk
River. High macroinvertebrate-biomass and abundance in bryophytes is likely
1University of Georgia River Basin Center, Athens, GA 30602. 2 USGS Patuxent Wildlife
Research Center, Athens, GA 30602. *Corresponding author - Wood@uga.edu.
Manuscript Editor:Nathan Dorn
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due to several factors. Bryophytes are often chemically defended, resulting in low
herbivory pressure and low rates of incidental ingestion of invertebrates by herbivores
(Parker et al. 2007, Suren and Winterbourn 1992). These non-vascular plant
taxa are hypothesized to protect invertebrates from predators such as fish and large
predatory invertebrates, and to facilitate niche partitioning of submerged habitats
(Niesiołowski 1980). Bryophytes can also retain organic matter, which can increase
the resources available to invertebrates (Harvey et al. 1997, Suren 1991).
Most studies of riverine bryophytes have been conducted in far-northern latitudes
(Englund et al. 1997, Slavik et al. 2004) or southern latitudes (Suren 1996),
while mid-latitudes, e.g., the piedmont region of North America, have received
comparatively little attention. Piedmont rivers in the southeastern US are often
sand-bottomed, interspersed with rock outcroppings, shoals, and stable woody material
where bryophytes often proliferate. Most piedmont rivers experience seasonal
fluctuations in discharge and regularly reach bank-full conditions. One common
bryophyte found on rocks and wood in seasonally inundated habitats in eastern North
America is the liverwort Porella pinnata L. (Breil 1977). Bryophyte studies have
generally focused on mosses, and few studies have investigated the relationship between
liverworts and invertebrates. Furthermore, few studies have measured aquatic
invertebrate use of bryophytes in seasonally inundated habitats, including roots and
rock faces that are within the channel but above base-flow conditions. Whereas seasonal
inundation of the floodplain enhances resources and habitat for stream biota
(Junk et al. 1989), increased discharge within the river channel temporarily inundates
bryophytes that could be subsequently inhabited by aquatic organisms. We predicted
that P. pinnata would provide substantially better invertebrate habitat than bare rock
and would function as a trap for organic matter under high-flow conditions. To test
this prediction, we quantified invertebrate biomass and abundance, and the mass of
organic matter in bryophytes growing in seasonally inundated habitats in the Middle
Oconee River, a mid-order river located in Athens, GA.
Site Description
The aim of this study was to assess invertebrate utilization and organic-matter
retention by bryophytes, especially the liverwort Porella pinnata in the Middle
Oconee River near Athens, GA (Fig. 1). The Middle Oconee River is a 6th-order
piedmont river in the Altamaha River drainage, GA, with a late-winter median flow
between 14 cms and 17 cms (~500–600 cfs). The river channel alternates between
slow-flowing, sand-bottomed pools and faster-flowing bedrock shoals with cobbled
riffles. Like most piedmont rivers in the southeastern US, past agricultural practices
and mill dams have left the channel incised, with steep banks and large amounts
of sediment deposited on the historical floodplain (Jackson et al. 2005). Deciduous
trees, including Acer rubrum L. (Red Maple), Platanus occidentalis L. (Sycamore),
and Ligustrum sinense Lour. (Chinese Privet), are the dominant riparian vegetation.
Rock outcrops and submerged woody debris are common, especially at bends in
the rivers. Porella pinnata grows abundantly on rock outcroppings and tree roots
that are seasonally submerged along the river channel (Fig. 2). The primary study
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2016 Vol. 15, No. 3
Figure 1. Map showing the Oconee River basin in Athens–Clarke County, GA. The study
reach on the Middle Oconee River (bold line) flows southeast past the city of Athens (black
star) before its confluence with the North Oconee River to form the Oconee River.
Figure 2. Photograph of rock outcrop in the Middle Oconee River, Athens, GA. showing the
epilithic liverwort Porella pinnata extending above and below the water line. Bryophytes
cover a substantial area within the river channel, often growing attached to tree roots and
rocks in seasonally inundated locations.
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species was Porella pinnata (hereafter Porella), but we also opportunistically
sampled adjacent patches of the moss Sematophyllum demissum (Wils.) Mitt.
Methods
We collected all samples along an 11-km section of the Middle Oconee River between
Ben Burton Park and the State Botanical Garden of Georgia on 8 and 9 March
2015. We took samples from submerged rock faces and boulders within the channel
approximately every 1.5 km, measured water velocity and turbidity, and collected
water samples at each sampling location. We took water samples back to the lab and
determined conductivity and pH. We obtained macroinvertebrate samples by placing
a short section of PVC pipe (area = 58.056 cm2) attached to a polyethylene collection
bag securely against the rock face between 1 and 20 cm below the water surface.
Keeping pressure on the sampler to prevent loss of sample material, we forced a
modified plastic putty knife between the sampler and the rock, and scraped the sample
material into the bag. We paired each Porella sample with a control sample taken
at similar depth from a submerged bare rock-face (i.e., rock faces without bryophyte
or other macrophytes), usually within 1 m of the bryophyte-sample point and stored
both samples in the lab on ice. We collected a total of 10 Porella–control pairs; 3
samples of Sematophyllum, 1 of Porella, and 1 additional unpaired control-sample
from bare rock were also collected opportunistically from the same section of river.
We collected these additional samples due to uncertainty about our ability to collect
adequate replicates during our sampling trip because of difficulties in accessing submerged
rock faces during high-flow conditions, to increase our sample size, and to
increase the diversity of bryophytes sampled in the study.
In the laboratory, we vigorously washed bryophyte samples under running
water, and collected macroinvertebrates and sediments from the rinse water in a
60-μm-mesh sieve. We examined the washed bryophyte material under a microscope
to detect any remaining invertebrates, then dried the samples at 60 °C for 48
h, and weighed them to obtain dry mass. Invertebrates and organic matter (OM)
(DM) were subsequently stored in polyethylene bags, preserved in 70% ethanol,
and dyed with Rose Bengal. We sorted invertebrates from OM and bryophytes under
a dissecting microscope and identified insect taxa to family and non-insect taxa
to Class (Oligochaeta) or Subclass (Copepoda). We used family-level length–mass
relationships to estimate dry mass from published regressions for insects; Class and
Subclass estimates were used for non-insect taxa (Benke et al. 1999). We expressed
invertebrate biomass as total DM divided by the sampling area. We dried all OM
and sediments at 60 °C for 48 h, weighed, ashed in a muffle furnace at 500 ºC for
4 h, and reweighed samples. We calculated ash-free dry mass (AFDM, mg per cm2
of sampling area) as DM minus ash mass.
To test the effect of Porella on invertebrates, we conducted paired-sample
analyses for invertebrate biomass, total insect biomass, Diptera biomass, and
biomass of the combined orders of Ephemeroptera, Plecoptera, and Trichoptera
(EPT). We separately tabulated insect (total, EPT, Diptera), Oligochaeta, and
Copepoda densities for Sematophyllum, Porella, and control (rock) habitats. We
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employed Wilcoxon signed ranks to compare Porella and control samples because
our data had a non-normal distribution and we used linear regression to compare
the relationships between bryophyte biomass (Porella only, and Sematophyllum
and Porella combined), invertebrate biomass, insect densities, and organic matter
AFDM. To improve normality of regression residuals, we transformed values by
taking either natural logarithms or square roots of predictor and response variables.
In order to put our results into a larger context, we obtained insect density
(abundance per unit area) and biomass estimates for the lotic macrophyte Podostemum
ceratophyllum Michx. (Hornleaf Riverweed) from Grubaugh and Wallace
(1995:Table 6) by subtracting estimates for non-insect taxa from total macroinvertebrate
values. Grubaugh and Wallace (1995) expressed insect biomass as AFDM g
m-2; thus, we converted our insect DM estimates to AFDM g m-2 using published values
for % ash for insect families or orders (Diptera) (Benke et al. 1999). To facilitate
comparisons, we converted our estimated insect abundances to individuals m-2.
Results
Discharge for the Middle Oconee River during sampling was approximately
14.5 cms (510 cfs) as measured by US Geological Survey gage 02217500. Physiochemical
measurements (mean ± 1 SE) were: turbidity (NTU) = 15 ± 1.0, pH = 6.8
± 0.01, and specific conductance at 25 ºC = 89.8 ± 0.35 μS cm-1. Water temperature
was 7 ºC at the Georgia State Botanical Gardens on 8 March 2015. Water velocity
at sample locations ranged from 0.01 to 0.37 m s-1 (mean = 0.11 ± 0.02 m s-1).
Our samples included 7 insect families in 4 orders: Diptera (Chironomidae,
Ceratopogonidae), Ephemeroptera (Heptageniidae, Baetidae, Ephemerellidae),
Plecoptera (Perlodidae), and Trichoptera (Hydropsychidae); we identified Class
Oligochaeta and Subclass Copepoda (Table 1). Invertebrate biomass and density, expressed
as the mean ± 1 SE, varied substantially between Porella and control samples.
Table 1. Mean invertebrate biomass (DM g m-2 ± 1 SE) and density (individuals m-2 ± 1 SE) from all
sampled surfaces in the Middle Oconee River in March 2015. Sampled habitat included Porella pinnata
(n = 11), Sematophyllum demissum (n = 3), and adjacent rock faces without bryophyte coverage
(Control, n = 11).
Habitat/
variable Diptera Ephemeroptera Plecoptera Trichoptera Oligochaeta Copepoda
Control
Biomass 0.02 ± 0.01 0.03 ± 0.03 less than 0.01 ± less than 0.01 0.00 ± 0.00 0.01 ± 0.01 less than 0.01 ± less than 0.01
Density 548.1 47.0 31.1 0.0 438.4 234.9
± 106.0 ± 24.6 ± 21.0 ± 0.0 ± 164.8 ± 186.2
Porella
Biomass 0.10 ± 0.03 0.16 ± 0.07 0.69 ± 0.21 0.08 ± 0.06 less than 0.01 ± 0.01 less than 0.01 ± less than 0.01
Density 3084.8 234.9 438.4 78.3 735.6 78.3
± 719.4 ± 84.6 ± 94.0 ± 48.5 ± 324.4 ± 78.3
Sematophyllum
Biomass 0.39 ± 0.28 less than 0.01 ± less than 0.01 0.21 ± 0.16 0.99 ± 0.98 0.01 ± less than 0.01 less than 0.01 ± less than 0.01
Density 8267.9 114.8 459.3 344.5 3789.4 57.4
± 3287.8 ± 57.4 ± 151.9 ± 263.1 ± 1337.9 ± 30.0
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In comparisons of paired samples, total invertebrate biomass was 14.6 times
larger in Porella samples than in the controls (Porella = 0.088 mg cm-2 ± 0.020,
control = 0.006 mg cm-2 ± 0.003, V = 53, P < 0.01; Fig. 3a). Total insect biomass
was almost 18 times greater in Porella compared with control samples (Porella =
0.088 mg cm-2 ± 0.020, control = 0.005 mg cm-2 ± 0.003, V = 53, P < 0.01; Fig. 3b),
and the biomass of EPT taxa was nearly 16 times greater in Porella than in controls
(Porella = 0.080 mg cm-2 ± 0.020, control = 0.003 mg cm-2 ± 0.003, V = 44, P =
0.01, Fig. 3c). The average dipteran biomass was 4 times greater in Porella, but the
difference between Porella and the controls was not statistically significant (P ≤
Figure 3. Box and whisker plots of invertebrate biomass (dry mass, mg cm-2) and organic
matter (AFDM mg cm-2) for submerged bare-rock faces (control) and mats of Porella pinnata
in the Middle Oconee River, Athens, GA. Wilcoxon signed ranks analysis was conducted
on 10 paired Porella and control samples, (a) invertebrate biomass (P < 0.01), (b) insect
biomass (P < 0.01), (c) biomass of insect orders Ephemeroptera, Plecoptera and Trichoptera
(EPT) (P = 0.01), and (d) organic matter mass (P < 0.01). Upper edge of box = 3rd quartile,
dark line within the box = median, lower edge of box = 1st quartile, and the whiskers indicate
the range * the interquartile range. Circles represent outliers .
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0.05) due to considerable variation between sites (Porella = 0.008 mg cm2 ± 0.002,
control = 0.002 mg cm-2 ± 0.001, V = 45, P = 0.08; data not shown).
Insect families were unevenly distributed between samples from different
habitats. Diptera was the most abundant order in all sampled habitats (Table 1)
occurring in 91% of the control samples and 100% of the bryophyte samples. We
detected Plecopterans in 72% of all Porella samples, and Trichopterans in 36% of
all the bryophyte samples and 2 out of the 3 Sematophyllum samples. We recorded
Oligochaetes in 85% of all bryophyte samples (Porella and Sematophyllum combined)
and 73% of all control samples.
In paired samples, average insect density was 5 times higher in Porella than in
controls (Porella = 0.324 cm-2 ± 0.055, control = 0.064 cm-2 ± 0.064, V = 55, P less than
0.01; Fig. 4a); EPT taxa density was nearly 10 times higher in Porella than in control
samples (Porella =0.065 cm-2 ± 0.012, control = 0.007 cm-2 ± 0.004, V = 36,
Figure 4. Box and whisker
plots of insect density
(individuals per cm-2) for
submerged bare-rock faces
(control) and Porella pinnata
mats in the Middle Oconee
River, Athens, GA. Wilcoxon
signed ranks analysis
was conducted on 10 paired
Porella and control samples,
(a) total insect (P < 0.01), (b)
EPT (P < 0.01), and (c) Diptera
(P < 0.01). Upper edge
of box = 3rd quartile,dark
line within the box = median,
lower edge of box =
1st quartile, and the whiskers
indicate the range * the interquartile
range. The circle
represents an outlier.
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P = 0.01; Fig. 4b), and dipterans were over 4.5 times more abundant in Porella
samples compared with control samples (Porella = 0.258 cm-2 ± 0.057, control =
0.057 cm-2 ± 0.011, V= 45, P < 0.01; Fig. 4c). Trapped organic matter averaged 1.82
mg AFDM cm-2 ± 0.413 in the paired Porella samples; the control samples held significantly
less material (0.550 mg AFDM cm-2 ± 0.180, V = 45, P < 0.01; Fig. 3d).
Density data from the few samples of Sematophyllum we collected suggest it might
support even higher densities of insects (Table 1) and organic matter (average for 3
unpaired samples = 5.03 mg AFDM cm-2) than Porella.
Total invertebrate biomass and insect biomass significantly increased with increasing
bryophyte biomass (invertebrate biomass: Porella and Sematophyllum
combined, square-root transformed, adjusted R2 = 0.50, F1, 12 =12.61, P < 0.01;
Porella only, adjusted R2 = 0.35, F1, 9 = 6.38, P = 0.03 (data not shown); insect biomass:
Porella and Sematophyllum combined, square-root transformed, adjusted R2 =
0.48, F1, 12 = 13.12, P < 0.01; Porella only, untransformed, adjusted R2 = 0.35, F1, 9 =
6.84, P = 0.03; Fig. 5a). Insect density significantly increased with total bryophyte
Figure 5. Simple linear
regression relationships
between bryophyte biomass
and (a) total insect
biomass (DM mg cm-2),
(b) insect density (individuals
cm-2), and (c)
organic matter (AFDM
mg cm-2). Porella pinnata
is represented as
circles, Sematophyllum
demissum is shown as
triangles. All lines represent
significant relationships
(P < 0.05).
Correlations using all
bryophyte samples are
shown by a solid line (n
= 14), and Porella only
correlations are shown
with a dashed line (n
= 11). Untransformed
data are shown in all
graphs; statistical analyses
were performed on
transformed data.
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biomass, but the trend was not significant with Porella only (Porella and Sematophyllum
combined, untransformed, adjusted R2 = 0.50, F1, 12 = 13.54, P < 0.01;
Porella only, natural log-transformed, adjusted R2 = 0.16, F1, 9 = 2.91, P = 0.12;
Fig. 5b). Retained organic matter significantly increased with bryophyte biomass
(Porella and Sematophyllum combined, natural log-transformed, adjusted R2 = 0.37,
F1, 12 = 8.55, P = 0.01; Porella only, natural log-transformed, adjusted R2 = 0.45, F1, 9 =
8.55, P = 0.01; Fig. 5c).
We found an average of 1.1 AFDM g m-2 of insect biomass and 4983 individuals
m-2 in our seasonally inundated bryophyte habitats (Porella and Sematophyllum
samples combined). In comparison, using summaries reported by Grubaugh
and Wallace (1995), we calculated insect biomass and abundance in Hornleaf
Riverweed patches in the Middle Oconee River as 13.8 AFDM g m-2 and 41,800
individuals m-2.
Discussion
We found significantly higher invertebrate biomass, density, and organic matter
in Porella than on adjacent bare rock faces. Bryophyte biomass was significantly
correlated with invertebrate biomass, invertebrate density, and organic-matter
mass. The results from this study support the conclusion that inundated bryophytes
provide important aquatic invertebrate habitat in the Middle Oconee River.
Previous studies have shown that insect biomass can be up to 8 times larger in bryophyte-
patches compared to bryophyte-free patches (Brusven et al. 1990, Parker and
Huryn 2006, Stream Bryophyte Group 1999); thus, our finding of almost 15 times
more invertebrate biomass and nearly 18 times more insect biomass in Porella than
in control samples does not appear unreasonable. Although our sampling methods
may not have captured large and highly mobile taxa such as crayfish and odonates,
our results indicate that the presence of bryophytes, even in small amounts (less than 5 mg
cm-2), may have a substantial positive impact on the invertebrate community.
Invertebrates may congregate in bryophytes near the water’s surface to prepare
for emergence, access OM and epiphytic algae (Stream Bryophyte Group 1999),
or gain protection from fish and other large predators (Glime 2015). Bryophytes
may also provide a place for drifting insects to anchor and extract themselves from
high flow-velocity areas. Additionally, bryophyte coverage that extends above and
below the water line may provide a relatively homogenous, resource-rich habitat
for invertebrates as the water level fluctuates. Although the organic matter that
bryophytes retain is presumably of higher palatability and nutritional quality compared
to the bryophytes themselves, some direct consumption of bryophytes has
also been reported (Suren and Winterbourn 1991) and may be another reason that
invertebrates colonize bryophytes. Our data support the conclusion that bryophytes
in seasonally inundated habitats play a structural role in this piedmont river, providing
habitat with increased resource availability compared to adjacent rock faces,
and support the findings of other studies that indicate that bryophytes play important
roles in riverine ecosystems (Parker et al. 2007; Suren 1991, 1992; Suren and
Winterbourn 1991).
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Interestingly, our estimates suggest that seasonally inundated bryophytes can
support insect abundance and biomass on the order of 10% of that supported by
Podostemum ceratophyllum, a perennially submerged benthic macrophyte noted
for supporting extremely high rates of secondary production (Grubaugh and Wallace
1995, Hutchens et al. 2004, Nelson and Scott 1962). Using estimates presented
in Grubaugh and Wallace (1995) from the Middle Oconee River at approximately
the same time of year, we found that seasonally submerged bryophytes (Porella
and Sematophyllum) contained about 8% of the insect biomass and 12% of the
abundance reported in Podostemum. Whereas Podostemum has been recognized as
ecologically important in eastern rivers due to its prevalence and role in structuring
the benthic community (Hutchens et al. 2004), our data indicate that bryophytes
can enhance insect abundance in seasonally inundated habitats, a habitat type where
Podostemum does not occur.
How much bryophytes actually influence habitat and resource availability in
mid-order rivers depends on the extent of bryophyte coverage at different water
levels and possibly on what type of bryophyte species are present. Our results
suggest that Sematophyllum might contain as much or more macroinvertebrate biomass
and organic matter as Porella, but our small sample-size reduces our ability
to make conclusive statements. Sematophyllum often grows lower within the river
channel and may be submerged for a longer period, thereby giving more time for
colonization by invertebrates and accumulation of organic material. Thus, shifts
in the composition of the bryophyte community, such as those encountered with
stream-flow regulation (Englund et al. 1997) may shift resource availability to
aquatic invertebrates and subsequently the invertebrate communities’ utilization of
these habitats.
Our data add to the small but growing body of evidence that bryophytes play important
roles in stream and riverine ecosystems, and provides new support for the notion
that seasonally inundated bryophytes are utilized by aquatic invertebrates. The
loss of bryophytes during stream-channel restoration has been cited as a reason for
only minimal changes in macroinvertebrate biodiversity after channel-restoration
efforts (Louhi et al. 2011, Muotka and Laasonen 2002) and the use of bryophytes in
stream-channel restoration efforts may be valuable. Bryophyte communities within
the river channels are stratified, in part on the frequency and duration of inundation
(Englund et al. 1997, Kimmerer and Allen 1982); thus, bryophytes could be considered
in the development of management plans to ensure that appropriate ecological
flow-requirements are established (Poff et al. 2010). Although periodic connections
between the river channel and floodplain can increase resource availability
to stream biota (Junk et al. 1989), the role of seasonally submerged bryophytes in
providing additional resources to stream biota still remains understudied. Our data
suggest that flows that provide seasonal habitat-connectivity to bryophytes growing
within the channel can reasonably be considered when assessing the impacts of flow
regulation. Furthermore, management actions that prevent the seasonal inundation
of bryophytes could reduce macroinvertebrate habitat, thereby reducing resources
available to higher trophic levels.
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Acknowledgments
We thank Alan Covich and 2 anonymous reviewers for their helpful suggestions on
the manuscript. We are grateful to Jon Skaggs for his help with field and laboratory work,
Phillip Bumpers for assistance with R, and Kelly Peterson for her help with figures. We
also appreciate The American Bryological and Lichenological Society-Anderson and Crum
Award, and the Society of Freshwater Science-Boesel-Sanderson Fund, for their support of
this research. Additional support was provided by the UGA Outdoor Recreation Center. Use
of trade, product, or firm names does not imply endorsement by t he US Government.
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