Jennifer A. Ress
A Dissertation
Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of
DOCTOR OF PHILOSOPHY
May 2012
Committee:
Rex L. Lowe, Advisor
John T. Chen Graduate Faculty Representative
George S. Bullerjahn
Jeffrey R. Johansen
Daniel M. Pavuk
ii ABSTRACT
Rex Lowe, Advisor
The ecology and adaptations of aerial algal communities from selected areas in North
America were examined. First, morphological adaptations to desiccation as well as microhabitat preference of diatoms were explored from the Great Smoky Mountains National Park (GSMNP).
Reduced size as an adaptation against desiccation was not supported by the data, with aerial diatoms being longer than had been previously shown in the literature. However, a reduction in the amount of open area on the valve face as an adaptation against desiccation was supported by the data. Second, aerial algal communities from the GSMNP and the Lake Superior region were compared and contrasted. Factors structuring algal communities in each region were examined and similarities and differences were identified between the two regions. These regions were not found to support unique aerial algal communities. Third, bryophyte-algal associations were investigated from a cliff face in O’ahu, HI. Algal species were examined for fidelity to bryophyte species within this site. There was no relationship found between algal species and bryophyte species, however, there was a relationship between algal species and both aspect and light levels. Finally, desiccation tolerance of algal communities was studied through a laboratory experiment. Changes in algal community composition were examined after exposure to different periods of desiccation. Overall, algal community composition was not found to change as a result of exposure to different periods of desiccation. This dissertation explored algal communities from understudied aerial and explored factors that structure and influence community composition. iii DEDICATION
To my son, Alexander,
I am so excited to watch you and be there with you as you begin your own exploration
of the world.
iv ACKNOWLEDGMENTS
First and foremost, I want to thank my husband, Evan Thomas, for his constant support and encouragement throughout this project. Not only did Evan provide much needed emotional support, but he also provided logistical support throughout the project. Evan was always ready to help me brainstorm, aid in fieldwork, and review my manuscripts time and time again. I also thank him for setting aside work on his own dissertation during the last year of my program to allow me more time to complete my work. Without his support and self-sacrifice, I would not have been able to complete this work. I also want to thank my parents, Robert and Judith Ress, for their support and encouragement throughout this process.
I want to thank my advisor, Dr. Rex Lowe, for his guidance and support throughout my graduate career. I want to thank Rex for allowing me the independence to pursue and coordinate this project. Rex has helped me grow and develop as a researcher which has allowed me to become a more knowledgeable and confident scientist. I would also like to thanks my committee, Dr. George Bullerjahn, Dr. Jeff Johansen, Dr. Dan Pavuk, and Dr. John Chen, for their guidance and time.
This work was funded in part by a Sigma Xi Grant-in-Aid of research. v
TABLE OF CONTENTS
Page
INTRODUCTION: ALGAL COMMUNITIES FROM AERIAL HABITATS ...... 1
CHAPTER I. MORPHOLOGICAL ADAPTATIONS AND HABITAT PREFERENCE OF
AERIAL DIATOMS
Introduction...... 6
Study Area...... 8
Methods...... 8
Results...... 10
Cell Length...... 11
Biovolumes ...... 12
Proportion Of Areolar Area ...... 13
Microhabitat Preference ...... 14
Discussion ...... 15
CHAPTER II. CONTRAST AND COMPARISON OF AERIAL ALGAL COMMUNITIES
FROM TWO DISTINCT REGIONS
Introduction...... 19
Study Area...... 20
Methods...... 22
Results ...... 23
Discussion...... 26
CHAPTER III. BRYOPHYTES AND ASSOCIATED ALGAL COMMUNITIES FROM AN
EXPOSED CLIFF FACE ON O'AHU (HAWAI’I, USA) vi
Introduction...... 30
Study Area...... 31
Methods...... 32
Results ...... 33
Discussion...... 35
CHAPTER IV. DESICCATION TOLERANCE OF AQUATIC AND PSEUDOAERIAL
ALGAE
Introduction...... 39
Study Area...... 40
Methods...... 41
Results...... 43
Cell Density Data ...... 43
Site 1 ...... 45
Site 3 ...... 45
Site 5 ...... 46
Community Composition Data ...... 47
Site 1 ...... 47
Site 3 ...... 48
Site 5 ...... 48
Non-Metric Multidimensional Scaling ...... 49
Site 1 ...... 49
Site 3 ...... 49
Site 5 ...... 50 vii
Discussion...... 50
CONCLUSIONS AND FUTURE DIRECTIONS…...... 54
LITERATURE CITED ...... 57
TABLES...... 64
CHAPTER I...... 64
CHAPTER II...... 91
CHAPTER III...... 115
CHAPTER IV...... 122
FIGURES...... 135
CHAPTER II...... 135
CHAPTER III...... 144
CHAPTER IV...... 154
viii
LIST OF TABLES
Table Page
CHAPTER I:
1 Site information for aerial and aquatic samples collected from the Great Smoky
Mountains National Park including site identification number, location, habitat
type, microhabitat type, pH, GPS coordinates, light level (µmols-1 m-2 per µA) (*
indicates average value of light levels measured at different times of day), aspect,
sponge weight change (g), and moisture category; Light, aspect, sponge weight
change and moisture category were recorded only from aerial habitats...... 65
2 Aerial taxa with the highest relative abundances with the range in length measured
for each taxon ...... 71
3 Taxa occurring with >1% relative abundance in populations from aerial habitats
with differing moisture availabilities (1=dry, 2=damp, 3=wet, 4=very wet)...... 72
4 Aquatic taxa with the highest relative abundances with the range in length measured
for each taxon...... 74
5 Median, maximum, and minimum lengths of diatom communities from both aerial
and aquatic populations; * indicates significance ...... 75
6 Median lengths of taxa shared between aerial and aquatic habitats, and median
lengths of taxa unique to aerial and aquatic habitats; * indicates significance ...... 76
7 Median lengths for taxa present in both aerial and aquatic habitats; * indicates
significance……...... 77
8 Median, maximum, and minimum cell lengths of diatoms from aerial habitats with
different moisture availabilities (1=dry, 2=damp, 3=wet, 4=very wet) ...... 78 ix
9 Pairwise Wilcoxon rank sum tests of cell length between diatom populations from
different moisture categories; * indicates significance (Bonferroni correction factor
α = 0.0125 used for pairwise comparisons) ...... 79
10 Median lengths in each moisture category (1=dry, 2=damp, 3=wet, 4=very wet) for
taxa with the highest relative abundances in the aerial habitats; Kruskal-Wallis
nonparametric analysis of variance result with post hoc pairwise Wilcoxon rank sum
tests for taxa occurring in three or more moisture categories, Wilcoxon rank sum
test for taxa occurring in only two moisture categories; * indicates significance
(Bonferroni correction factor α = 0.0167used for post hoc pairwise comparisons).... 80
11 Median, maximum, and minimum biovolumes for both aerial and aquatic
populations; * indicates significance ...... 81
12 Median biovolumes of taxa shared between aerial and aquatic habitats, and
median biovolumes of taxa unique to aerial and aquatic habitats; * indicates
significance………… ...... 82
13 Median biovolumes for taxa present in both aerial and aquatic habitats; * indicates
significance…...... 83
14 Median, maximum, and minimum biovolumes of diatoms from aerial habitats with
different moisture availabilities (1=dry, 2=damp, 3=wet, 4=very wet) ...... 84
15 Pairwise Wilcoxon rank sum tests of biovolume between different moisture
categories; * indicates significance (Bonferroni correction factor α = 0.0125 used
for pairwise comparisons) ...... 85
16 Median biovolumes in each moisture category (1=dry, 2=damp, 3=wet, 4=very
wet) for taxa with the highest relative abundances in the aerial habitats; Kruskal- x
Wallis nonparametric analysis of variance result with post hoc pairwise Wilcoxon
rank sum tests for taxa occurring in three or more moisture categories, Wilcoxon
rank sum test for taxa occurring in only two moisture categories; * indicates
significance (Bonferroni correction factor α = 0.0167used for post hoc pairwise
comparisons) ...... 86
17 Median percent open area of diatoms from aerial habitats with different moisture
availabilities (1=dry, 2=damp, 3=wet, 4=very wet)...... 87
18 Pairwise Wilcoxon rank sum tests of percent open area between different moisture
categories; * indicates significance (Bonferroni correction factor α = 0.0125 used for
pairwise comparisons) ...... 88
19 List of common species frequently encountered in bryophytic samples. A species was
considered common if it occurred in >20% of the samples ...... 89
20 List of common species frequently encountered in epilithic samples. A species was
considered common if it occurred in >20% of the samples ...... 90
CHAPTER II:
1 Taxa list for the two regions Lake Superior (LSR) and Great Smoky Mountains
National Park (GSMNP); an “X” indicates presence of taxon in region ...... 92
2 List of common taxa frequently encountered across Lake Superior region samples.
A taxon was considered common if it occurred in >20% of the samples ...... 102
3 Taxa occurring with >1% relative abundance in populations from aerial habitats
with differing moisture availabilities (1=dry, 2=damp, 3=wet, 4=very wet)...... 103
4 Aquatic taxa with the highest relative abundances with the range in length measured
for each taxon...... 104 xi
5 Median, maximum, and minimum lengths of diatom communities from both aerial
and aquatic populations; * indicates significance ...... 105
6 Median lengths of taxa shared between aerial and aquatic habitats, and median
lengths of taxa unique to aerial and aquatic habitats; * indicates significance ...... 106
7 Similarity percentages analysis displaying taxa contributing to the separation of
Great Smoky Mountains National Park samples forming groups GSMNP 1 and
GSMNP 2 in non-metric multidimensional scaling ordination (Figure 1). Table
includes the average relative abundance of each taxon in each group, the average
dissimilarity (AD) of each taxon between groups, the ratio Average
Dissimilarity/Standard Deviation (AD/SD) for each taxon, the percent contribution
of each taxon to the overall separation between groups, and the cumulative percent
dissimilarity between groups……...... 107
8 Similarity percentages analysis displaying taxa contributing to the separation of
groups Great Smoky Mountains National Park 2 (GSMNP 2) and Lake Superior
region (LSR) in non-metric multidimensional scaling ordination (Figure 1). Table
includes the average relative abundance of each taxon in each group, the average
dissimilarity (AD) of each taxon between groups, the ratio Average
Dissimilarity/Standard Deviation (AD/SD) for each taxon, the percent contribution
of each taxon to the overall separation between groups, and the cumulative percent
dissimilarity between groups ...... 108
9 Pairwise Wilcoxon rank sum tests of cell length between diatom populations from
different moisture categories; * indicates significance (Bonferroni correction factor
α = 0.0125 used for pairwise comparisons) ...... 109 xii
10 Mean relative abundance of taxa for the two moisture categories Dry and Very Wet
for the Lake Superior Region (LSR) ...... 110
11 Mean relative abundance of taxa for the two moisture categories Dry and Very Wet
for the Great Smoky Mountains National Park (GSMNP) ...... 112
12 Species diversity for each moisture category (Dry, Damp, Wet, Very Wet) in both
the Lake Superior region (LSR) and the Great Smoky Mountains National Park
(GSMNP)…...... 114
CHAPTER III:
1 List of common taxa frequently encountered across all samples from Nu'uanu Pali.
A taxon was considered common if it occurred in >20% of the samples ...... 116
2 ANOSIM results of factor Aspect calculated from the Bray-Curtis Similarity
Matrix of species data; * indicates significance (Bonferroni correction factor
α = 0.017 used for pairwise comparisons) ...... 117
3 ANOSIM results of factor Light calculated from the Bray-Curtis Similarity
Matrix of species data; * indicates significance (Bonferroni correction factor
α = 0.017 used for pairwise comparisons) ...... 118
4 Similarity percentages analysis displaying taxa contributing to the separation of
groups S (South) and N (North) in non-metric multidimensional scaling ordination
(Figure 3). Table includes the average relative abundance of each taxon in each
group, the average dissimilarity of each taxon between groups, the ratio Average
Dissimilarity/Standard Deviation for each taxon, the percent contribution of each
taxon to the overall separation between groups, and the cumulative percent
dissimilarity between groups ...... 119 xiii
5 Similarity percentages analysis displaying taxa contributing to the separation of
groups High (high light) and Low (low light) in non-metric multidimensional
scaling ordination (Figure 4). Table includes the average relative abundance of
each taxon in each group, the average dissimilarity of each taxon between groups,
the ratio Average Dissimilarity/Standard Deviation for each taxon, the percent
contribution of each taxon to the overall separation between groups, and the
cumulative percent dissimilarity between groups ...... 120
6 Similarity percentages analysis displaying taxa contributing to the separation of
groups High (high light) and Moderate (moderate light) in non-metric
multidimensional scaling ordination (Figure 4). Table includes the average relative
abundance of each taxon in each group, the average dissimilarity of each taxon
between groups, the ratio Average Dissimilarity/Standard Deviation for each taxon,
the percent contribution of each taxon to the overall separation between groups,
and the cumulative percent dissimilarity between group ...... 121
CHAPTER IV:
1 Site information for each location sampled in the Great Smoky Mountains National
Park for algal populations utilized in the desiccation experiment ...... 123
2 A. Median Total Cell Density (cells/cm2) of the populations (included all health
categories) for the establishment, control, and treatment groups in each site; B.
Percent change in cell density from the establishment period for each treatment;
C. Percent change for each treatment from the two week to the four week sampling
period; D. Percent change from control to the four week treatments ...... 124
3 Taxa Median cell densities (cells/cm2) of the common healthy taxa in all xiv
populations from Site 1; A taxon was considered common if it occurred in >20%
of the samples...... 125
4 Taxa with the greatest median cell densities (cells/cm2) in all populations from
Site 1; Health categories include: H=Healthy, HI=Heavily Impaired, D=Dead ...... 127
5 Median cell densities (cells/cm2) of the common healthy taxa in all populations
from Site 3; A taxon was considered common if it occurred in >20% of the
samples……...... 128
6 Taxa with the greatest median cell densities (cells/cm2) in all populations from
Site 3; Health categories include: H=Healthy, HI=Heavily Impaired, D=Dead ...... 129
7 Median cell densities (cells/cm2) of the common healthy taxa in all populations
from Site 5; A taxon was considered common if it occurred in >20% of the
samples……...... 130
8 Taxa with the greatest median cell densities (cells/cm2) in all populations from Site
5; Health categories include: H=Healthy, MI=Moderately Impaired, D=Dead ...... 131
9 Median relative abundance of the dominant common healthy taxa in all
populations from Site 1; A taxon was considered dominant if it occurred with a
median relative abundance > 1% in >3 samples ...... 132
10 Median relative abundance of the dominant common healthy taxa in all
populations from Site 3; A taxon was considered dominant if it occurred with a
median relative abundance > 1% in >3 samples ...... 133
11 Median relative abundance of the dominant common healthy taxa in all
populations from Site 5; A taxon was considered dominant if it occurred with a
median relative abundance > 1% in >3 samples ...... 134 xv
LIST OF FIGURES
Figure Page
CHAPTER II:
1 Non-metric multidimensional scaling plot categorized by region (GSMNP=Great
Smoky National Park and LSR=Lake Superior region) of species data for samples
of aerial algal communities. Samples from the GSMNP formed two distinct
clusters and were coded differently (GSMNP 1, GSMNP 2) to illustrate the
separation ...... 136
2 Non-metric multidimensional scaling plot categorized by moisture categories of
species data for samples of aerial algal communities from the Lake Superior region
and the Great Smoky Mountains National Park ...... 137
3 Non-metric multidimensional scaling plot categorized by moisture of species data
for samples of aerial algal communities from the Great Smoky Mountains
National Park region ...... 138
4 Non-metric multidimensional scaling plot categorized by moisture categories
of species data for samples of aerial algal communities from the Lake Superior
region……...... 139
5 Non-metric multidimensional scaling plot categorized by region (GSMNP=Great
Smoky National Park and LSR=Lake Superior region) of division data for samples
of aerial algal communities ...... 140
6 Bubble plot of samples from NMDS ordination displaying relative abundance of xvi
each division in each sample from the Lake Superior region and the Great Smoky
Mountains National Park (green =Chlorophyta, yellow=Bacillariophyta,
red=Cyanophyta). Each sample is represented by a bubble and corresponds to
the abundance of each division within that sample. Samples represented by one
bubble were comprised of taxa from only one division, while samples represented
by bubbles within bubbles were comprised of taxa from more than one division;
abundance corresponds to size of bubble...... 141
7 Bubble plot of samples from NMDS ordination displaying relative abundance of
each division in each sample from the Great Smoky Mountains National Park (green
=Chlorophyta, yellow=Bacillariophyta, red=Cyanophyta). Each sample is
represented by a bubble and corresponds to the abundance of each division within
that sample. Samples represented by one bubble were comprised of taxa from only
one division, while samples represented by bubbles within bubbles were comprised
of taxa from more than one division; abundance corresponds to size of bubble ...... 142
8 Bubble plot of samples from NMDS ordination displaying relative abundance of
each division in each sample from the Lake Superior region (green =Chlorophyta,
yellow=Bacillariophyta, red=Cyanophyta). Each sample is represented by a bubble
and corresponds to the abundance of each division within that sample. Samples
represented by one bubble were comprised of taxa from only one division, while
samples represented by bubbles within bubbles were comprised of taxa from more
than one division; abundance corresponds to size of bubble ...... 143
xvii
CHAPTER III:
1 Non-metric multidimensional scaling plot categorized by bryophyte (Anoectangium
euchloron, Campylopus umbellatus, Hyophila involuta, Hymenostylium
recurvirostrum var. cylindricum, Macromitrium emersulum, Philonotis turneriana,
Vesicularia perviridis, Weissia ovalis, and Liverwort) for species data of aerial
algal community samples from Nu'uanu Pali ...... 145
2 Non-metric multidimensional scaling plot categorized by moisture category for
species data of aerial algal community samples from Nu'uanu Pali ...... 146
3 Non-metric multidimensional scaling plot categorized by aspect (S=south, N=
north, W= west) for species data of aerial algal community samples from Nu'uanu
Pali…………...... 147
4 Non-metric multidimensional scaling plot categorized by light (high, moderate,
low) for species data of aerial algal community samples from Nu'uanu Pali ...... 148
5 Non-metric multidimensional scaling plot categorized by bryophyte (Anoectangium
euchloron, Campylopus umbellatus, Hyophila involuta, Hymenostylium
recurvirostrum var. cylindricum, Macromitrium emersulum, Philonotis turneriana,
Vesicularia perviridis, Weissia ovalis, and Liverwort) for division data of aerial
algal community samples from Nu'uanu Pali ...... 149
6 Non-metric multidimensional scaling plot categorized by moisture category for
division data of aerial algal community samples from Nu'uanu Pali ...... 150
7 Non-metric multidimensional scaling plot categorized by aspect (S=south, N=
north, W= west) for division data of aerial algal community samples from Nu'uanu
Pali...... 151 xviii
8 Non-metric multidimensional scaling plot categorized by light (high, moderate,
low) for division data of aerial algal community samples from Nu'uanu Pali ...... 152
9 A. Non-metric multidimensional scaling plot (NMDS) for species data of aerial
algal community samples from Nu'uanu Pali; B. Bubble plot of samples from
NMDS ordination displaying relative abundance taxa from the Division
Bacillariophyta in each sample; the larger the bubble the greater the abundance; C.
Bubble plot of samples from NMDS ordination displaying light measurements
from each sample; the larger the bubble the greater the light level; D. Bubble plot
of samples from NMDS ordination displaying moisture levels from each sample;
the larger the bubble the greater the amount of moisture ...... 153
CHAPTER IV:
1 Plot of median algal cell densities of the populations (included all health categories)
for the establishment, control, and treatment groups from Site 1 ...... 155
2 Box Plot of median cell densities of the populations (included all health categories)
for the establishment, control and treatment groups from Site 3 ...... 156
3 Box Plot of median cell densities of the populations (included all health categories)
for the establishment, control and treatment groups from Site 5 ...... 157
4 Non-metric multidimensional scaling plot of species data for samples of algal
communities from Site 1 categorized by treatment ...... 158
5 Bubble plot of samples from NMDS ordination displaying total cell density in
each sample from Site 1. Each sample is represented by a bubble and corresponds
to the total cell density within that sample; the larger the bubble the greater the
density ...... 159 xix
6 Non-metric multidimensional scaling plot of species data for samples of aerial
algal communities from Site 3 categorized by treatment ...... 160
7 Bubble plot of samples from NMDS ordination displaying total cell density in
each sample from Site 3. Each sample is represented by a bubble and corresponds
to the total cell density within that sample; the larger the bubble the greater the
density...... 161
8 Non-metric multidimensional scaling plot of species data for samples of aerial
algal communities from Site 5 categorized by treatment ...... 162
9 Bubble plot of samples from NMDS ordination displaying total cell density in
each sample from Site 5. Each sample is represented by a bubble and corresponds
to the total cell density within that sample; the larger the bubble the greater the
density ...... 163
1
INTRODUCTION: ALGAL COMMUNITIES FROM AERIAL HABITATS
Algal communities are known to colonize non-aquatic habitats including exposed bedrock (Omelon et al. 2006; Pentecost 1992), soil (Johansen et al. 1981; Hayek and Hulbary
1956), terrestrial bryophytes (Van de Vijer et al. 2003; van Kerckvoorde 2000), tree bark (Wylie and Schlichting 1973), and anthropogenic structures (Lee and Wee 1982; Schlichting 1975).
Moisture can originate from a groundwater seep, precipitation, humidity, or waterfall spray and can be highly variable, ranging from perennially moist to mostly dry. Categories have been developed for these algae based on habitat type. Petersen (1935) described three main categories, euaerial, pseudoaerial, and terrestrial. Algae which inhabit elevated objects receiving only atmospheric moisture are termed euaerial. Pseudoaerial algae inhabit areas that receive fairly constant moisture supplied from a groundwater seep, surface runoff, or waterfall spray.
Terrestrial algae inhabit soils.
Algae from aerial habitats have been an area of research interest for more than 100 years
(Petersen 1928; Fritsch 1907; West and West 1894). Despite this fact, much less attention has been paid to these habitats compared to aquatic habitats. The majority of the research that has been performed on aerial habitats has been primarily floristic work with little focus on the ecology of these communities (McMillan and Rushforth 1985; Schlichting 1975; Dodd and
Stoermer 1962). However, in more recent years, the focus has begun to shift toward attempting to understand the ecology of these communities (Furey et al. 2007; Lowe et al. 2007; Van de
Vijver and Beyens 1997; Camburn 1983). Moisture has been found to play a significant role in structuring the algal communities that inhabit these areas (Casamatta et al. 2002; Beyens 1989;
Camburn 1983). Typically, species diversity has been shown to increase with increasing moisture availability (Casamatta et al. 2002; Camburn 1983). Moisture has also been shown to 2 play an important role in the colonization of aerial habitats. Pentecost (1992) cleared aerial habitats of the existing algal communities to observe recolonization rates. The driest site had very little recolonization after 10 years while the wettest site supported a thick algal mat within less than a year.
Algae have developed methods to cope with the variable environment of aerial habitats.
Variables such as moisture and temperature can change greatly on a day-to-day basis and even during the course of one day. Algal communities can experience frequent and prolonged periods of desiccation in aerial habitats. Different algal species have developed adaptations to sequester and retain moisture as well as limit moisture loss, and these mechanisms include reduced size and morphological changes in diatoms as well as mucilage production.
Cells of diatom populations from aerial habitats are typically smaller than those found in aquatic habitats (Patrick 1977; Round 1957). Van de Vijver and Beyens (1997) found that valve length of the diatom Pinnularia borealis Ehrenberg was significantly smaller in aerial populations from drier mosses compared to those from wetter mosses. In addition, diatoms have developed adaptations to fluctuating moisture availabilities in aerial habitats. Diprora haenaensis Main, from a pseudoaerial habitat in Kaua’i (Hawaiian Islands), possesses thickened cell walls as a potential mechanism for retaining moisture (Main 2003). There are diatoms known to produce internal valves, such as Hantzschia spp. and Melosira dickiei (Thwaites)
Kützing, as another moisture retaining strategy (Round et al. 1990; Dodd and Stoermer 1962).
Reductions in the number of areolae, as seen in the genus Diadesmis Kützing, and occlusion of areolae with silica, as seen in genera such as Nupela Vyverman and Compere and
Chamaepinnularia Lange-Bertalot and Krammer, have also been proposed to be possible adaptations for moisture conservation (Lowe 2010; Lowe et al. 2007). 3
Many algal species inhabiting aerial habitats are known to produce extracellular mucilage which aides in water retention (Gerrath 2003; Potts 1999; Shephard 1987; Patrick 1977). This mucilage can contain a considerable amount of moisture. Boney (1980) found a 97.5-98.8% total weight loss from Mesotaenium chlamydosporum De Bary colonies after a three day period in a desiccator. Shephard (1987) found that mucilage produced by Gloeocystis spp. lasted longer during periods of desiccation when compared to water. Mucilage production is common in aerial cyanobacterial genera, such as Nostoc Vaucher ex Bornet and Flahault, Gloeothece Nägeli,
Gloeocapsa Kützing, and Aphanocapsa Nägeli. Many aerial green algae produce mucilage as well, including colonial forms such as Coccomyxa Schmidle and Gloeocystis Nägeli and desmids such as Mesotaenium Nägeli and Spirotaenia Brébisson. There are also some diatom genera capable of producing mucilaginous sheaths, such as Encyonema Kützing and Frustulia
Rabenhorst. Other algal species that do not produce their own mucilage may form associations with species that do produce mucilage. Boney’s (1980) investigations into Mesotaenium chlamydosporum colonies revealed a variety of other algal species and invertebrates living within the mucilage. Johansen et al. (1983) found that mucilage producing cyanobacteria and green algae are the first colonizers on moist rock faces, and once these establish, other algal species begin to colonize the mucilage.
Another variable, solar radiation, can be much more intense in aerial habitats resulting in the production of internal or external protective pigments. Common protective pigments in cyanobacteria include the UV-A absorbing pigment scytonemin and the UV-B absorbing pigments mycrosporine amino acids (MAA). Scytonemin, which accumulates in the extracellular mucilage, has been shown to be produced by both Nostoc commune Vaucher and
Chlorogloeopsis sp. (Cyanophyta) only when exposed to UV-A (Ehling-Schulz et al. 1997; 4
Garcia-Pichel et al. 1992). Ehling-Schulz et al. (1997) demonstrated that an extracellular MAA accumulates in Nostoc commune only when exposed to UV-B.
Algal cells have been found to be transported by wind, water, and animals, such as birds, as well as by humans (Kristiansen 1996). Wind is likely to be the primary dispersal mechanism of algae into aerial habitats due to the limited contact humans and animals have with these areas.
The same adaptations to survival in aerial environments by algae, such as tolerance to desiccation and to solar radiation, also aid in the survival of wind dispersal. The ability of algal cells to not only be transported by wind but to also survive this mode of dispersal allows for the colonization of new aerial habitats.
Studies into airborne algae have shown that the majority of species present in air samples are soil algae (Sharma et al. 2006; Rosas et al 1987; Brown et al. 1964). Airborne algal samples have shown variability across different climates. Chlorophytes were found to dominate air samples in temperate regions (Tiberg 1987; Schlichting 1964), while air samples from tropical regions were found to be dominated by cyanobacteria (Sharma et al. 2006, Schlichting 1969).
The concentration and diversity of algal cells present in the atmosphere have been shown to vary throughout the year. Maximum concentrations of algal cells have been found to occur during the summer (Tiberg 1984). The greatest algal diversity in the atmosphere has been found to occur during different seasons in different geographical locations, for example during the summer in
India (Sharma et al. 2006) and Michigan (Schlichting 1964) and during the winter in Texas
(Schlichting 1964). Sharma et al. (2006) found that some genera exhibited seasonal variation in their presence in the atmosphere, while others were present year round. Schlichting (1964) found algae were more commonly collected from the atmosphere on cloudy to partly-cloudy days when UV levels were lower. A greater abundance and diversity of algae in the atmosphere 5 has been reported from semiarid regions where winds lift dust and associated algal cells into the atmosphere (Schlichting 1969). However, Schlichting (1974) stated that regions with abundant soil and aerial algae may also result in high abundance and diveristy of atmospheric algae.
In this dissertation, I examined the ecology and adaptations of aerial algal communities from selected areas in North America. The first chapter explored morphological adaptations to desiccation as well as microhabitat preference of diatoms. In the second chapter, I contrasted communities from the Great Smoky Mountains National Park (GSMNP) and the Lake Superior region. I examined factors structuring communities in each region, and examined similarities and differences between the two regions. The third chapter focused on bryophyte-algal associations from a cliff face in O’ahu, HI. I determined if particular algal species demonstrated fidelity with the same bryophyte species within this site. In the fourth chapter, I investigated desiccation tolerance of algal communities from a laboratory experiment. By conducting a laboratory experiment on natural aerial and aquatic algal communities from GSMNP, I examined changes to community composition after exposure to desiccation.
6
CHAPTER 1: MORPHOLOGICAL ADAPTATIONS AND HABITAT PREFERENCE OF AERIAL DIATOMS
Introduction
Algal communities are commonly found inhabiting non-aquatic habitats. The algal communities in these aerial habitats can be subject to harsh environmental conditions such as an inconsistent availability of moisture, extreme heat, and high levels of ultraviolet radiation.
Moisture availability and temperature can change daily and may even fluctuate during the course of one day. Algal communities can experience frequent and prolonged periods of desiccation, and moisture availability has been found to be an important factor regulating the algal communities in these habitats (Casamatta et al. 2002; Beyens 1989; Camburn 1983). Aerial algae have evolved methods to cope with the temporal drying of these habitats. One adaptation of diatoms to life in aerial habitats is a reduction in size. In general, diatoms from aerial populations have been found to be smaller than those from aquatic populations (Patrick 1977;
Round 1957). In aerial populations, the valve lengths of Pinnularia borealis Ehrenberg was found to decrease as moisture levels decreased (Van de Vijver and Beyens 1997). Patrick (1977) proposed that reduction in cell size allowed diatoms to withstand desiccation and the associated osmotic stress. Other adaptations to life in these habitats exposed to fluctuating moisture availability are the production of internal valves, reduction in the number of areolae, and occlusion of areolae with silica (Lowe 2010; Lowe et al. 2007; Round et al. 1990; Dodd and
Stoermer 1962). These adaptations aid in the retention of internal moisture as osmotic pressures increase.
Three types of aerial algal communities, euaerial, pseudoaerial, and terrestrial, are grouped by habitat type (Petersen 1935). Euaerial habitats only receive atmospheric moisture, pseudoaerial habitats receive a fairly constant supply of moisture from sources such as a 7 groundwater seep or spray from a waterfall, and terrestrial habitats are soil habitats which can be further divided based on moisture availability. Diatoms from euaerial and pseudoaerial habitats were examined to identify possible adaptations to the aerial environment. Diatoms from these habitats were compared to diatoms from aquatic habitats in order to determine if there were morphological differences between communities. I expected that overall cell length and biovolume of diatom communities from aerial habitats would be smaller than that of aquatic communities, and I anticipated that cell length and biovolume would decrease with decreasing moisture availability within the aerial communities. As cell size decreases, thus decreasing surface area and decreasing areolar area, moisture conservation may become easier for taxa inhabiting aerial habitats, especially the drier aerial habitats. As for species that occurred in both habitats or across moisture availabilities, I expected that the cell length and biovolume would also decrease with decreasing moisture availability. In addition, as moisture availability decreased, I expected that the amount of open area on the valve face, areolar area, would decrease. Reducing the areolar area on the valve face may allow cells to conserve moisture and combat the osmotic stress encountered during periods of desiccation thus allowing these cells to survive in drier habitats or habitats that experience fluctuations in moisture availability.
Diatom species were also evaluated on their fidelity to microhabitat substrate within aerial habitats. There have been several studies examining the diatom communities associated with bryophytes from aerial habitats (Alfinito et al. 1998; Van de Vijver and Beyens 1997; Lowe and Collins 1973; Dodd and Stoermer 1962). However, these studies did not investigate microhabitat preference of aerial diatoms. The present study examined whether individual diatom species were preferentially found associated with bryophytes versus exposed rock. I expected to find a preference by some diatom species for bryophytic habitats over epilithic 8 habitats due to the ability of bryophytes to trap and retain moisture. This trapped moisture could allow diatom community development in areas where otherwise it might not be possible due to lack of available moisture.
Study Area
The Great Smoky Mountains National Park (GSMNP) is located across the Tennessee-
North Carolina state line and covers approximately 2,000 km². Elevations range from 267 m to
2025 m. One of the largest tracts of deciduous, temperate, old-growth forest in North America is found in the park.
Methods
The aquatic diatom flora was examined from lotic samples collected in GSMNP from
2003 to 2005 (Table 1). Collecting expeditions to the GSMNP by Bowling Green State
University and John Carroll University groups occurred on five separate occasions, October
2003, May 2004, July 2004, October 2004, and May to August 2005. The aerial diatom flora was examined from samples collected in the GSMNP from June and July, 2007 (Table 1).
Moisture availability was assessed for each aerial collection at the time of sampling. As a method to estimate moisture levels, a piece of sponge was placed on each rock face for five or ten seconds. The difference in weight of the sponge was recorded for each site, and four moisture categories (1=dry, 2=damp, 3=wet, 4=very wet) were created from these measurements for the purpose of statistical analysis. Weight change less than 0.1 g was considered dry and assigned to moisture category 1, weight change between 0.1-0.5 g was considered damp and assigned to moisture category 2, weight change between 0.5-1.0 g was considered wet and assigned to moisture category 3, and weight change greater than 1.0 g was considered very wet and assigned to moisture category 4. Samples were preserved in at least 2% glutaraldehyde. 9
Diatoms were cleaned in boiling nitric acid and air dried onto 18 X 18 mm, no.1 cover glass. Permanent diatom mounts for light microscope (LM) analysis were made using Naphrax mounting medium. Samples were analyzed with an Olympus BX51 Photomicroscope with high resolution Nomarski DIC optics. Cover glasses, mounted on specimen stubs and sputter-coated with 10nm gold/palladium alloy, were analyzed on a high resolution Hitachi S-2700 scanning electron microscope (SEM). Algae were identified to the lowest taxonomic level possible using standard references. References consisted of: Geitler (1932), Krammer and Lange-Bertalot
(1986), Krammer and Lange-Bertalot (1988), Krammer and Lange-Bertalot (1991a), Krammer and Lange-Bertalot (1991b), Komárek and Anagnostidis (1999), Potapova et al. (2003), Wehr and Sheath (2003), Komárek and Anagnostidis (2005), Thomas et al. (2009), and Furey (2011).
In order to examine differences in cell size between habitats, diatom valve lengths were measured from 19 aquatic samples and 20 aerial samples (Appendix A). For each sample, a minimum of 600 cells were identified and relative abundances calculated. Measurements were taken from 100 cells in each sample. The taxonomic composition of those 100 cells corresponded to the calculated relative abundance for each taxon. Cell biovolumes were also calculated for each sample using formulas published in Hillebrand et al. (1999). Wilcoxon rank sum test was used to examine differences in overall cell length and biovolume between habitats.
Species shared between habitats were identified, and those with sufficient population size were analyzed for differences in cell length and biovolume. For the aerial communities, Kruskal-
Wallis nonparametric analysis of variance was used to examine differences in overall cell length and biovolume among moisture categories. Post hoc Wilcoxon rank sum tests with Bonferroni correction were used to reveal significant differences between moisture categories. 10
SEM images were utilized to examine the proportion of open area from puncta relative to valve area. Utilizing the same 19 aquatic samples and 20 aerial samples, overall valve area and total open area on the valve face was measured and the proportion of open area was calculated.
The first fifteen cells from each sample encountered in the SEM were photographed for measurement. Images were imported into Spot® imaging program where the measurement tool was calibrated and utilized to obtain measurements. The formulas utilized to calculate valve area were derived from Hillebrand et al. (1999). The “region area” tool was used to measure the area of highly irregular valves. This tool allowed for the tracing of the valve outline and calculated the area created within the boundaries. Openings on the valve face, areolae, and the total area of these openings were calculated and the proportion of open area was calculated for each cell.
Wilcoxon rank sum test was used to examine differences in the proportion of open area between habitats. For the aerial communities, Kruskal-Wallis nonparametric analysis of variance was used to examine differences in the proportion of open area among moisture categories. Post hoc
Wilcoxon rank sum tests with Bonferroni correction were used to reveal significant differences between moisture categories.
To address microhabitat substrate preference, a total of 40 samples were analyzed, 20 were from bryophytic communities and 20 were from epilithic communities. A minimum of 600 valves were counted. Taxa occurring in more than eight samples were analyzed for microhabitat preference. Wilcoxon rank sum test was used to examine differences in the relative abundances of these taxa between microhabitats.
Results
A total of 155 taxa were identified from aerial habitats and 199 from aquatic habitats. Of the taxa identified, 76 taxa were present in both habitats. The most abundant taxa in the aerial 11 populations were Cymbella gracilis (Ehrenberg) Kützing (14.77%), Achnanthidium minutissimum (Kützing) Czarnecki (8.52%), and Eunotia bigibba Kützing (8.27%) (Table 2).
Species abundance was variable across populations from different levels of moisture availability
(Table 3). Populations from moisture category 1, the driest habitats, were dominated by Eunotia paludosa var. paludosa (23.99%), Diadesmis contenta (17.66%), and Diadesmis perpusilla
(16.97%). The most abundant taxa in populations from moisture category 2 were C. gracilis
(17.99%) and Eunotia bigibba (16.15%), while the most abundant in populations from moisture category 3 were C. gracilis (31.25%) and A. minutissimum (9.07%). Three taxa dominated populations from moisture category 4, the wettest habitats, which included Eunotia subarcuatoides (20.54%), E. bigibba (17.49%), and A. minutissimum (16.93%). The aquatic populations were dominated by two taxa, A. minutissimum (14.59%) and Rossithidium pusillum
(Grunow) Round & Bukhtiyarova (11.11%) (Table 4). In addition to A. minutissimum, two other taxa, Diatoma mesodon and Nupela lapidosa, were present with high relative abundances in both habitats.
Cell Length
Diatom cells from populations in aquatic habitats were significantly shorter than those from aerial habitats (p<0.0001) (Table 5). The median length of aquatic diatoms was 16.15µm compared to 19.11µm for aerial diatoms. Diatoms from aquatic populations had a greater range in cell length as well as having the largest cells. Examining the cell length of the taxa shared between habitats, the cells of aquatic populations were significantly shorter than those of aerial populations (Table 6). However, taxa unique to each habitat were found to be significantly shorter in aerial populations than those in aquatic populations. Thirteen taxa were examined for differences in median length between habitats (Table 7). Six taxa were found to be significantly 12 shorter in aerial habitats. These taxa included A. minutissimum, Diadesmis contenta, Eunotia incisa, Fragilaria capucina var. gracilis, Frustulia rhomboides var. saxonica, and N. lapidosa.
One species, Eunotia minor, was found to be significantly longer in aerial habitats. There was no difference in cell length in the remaining five taxa.
In the aerial habitats, the overall median cell length decreased with decreasing moisture availability (Table 8). Cell length was found to be significantly shorter in moisture category 1 compared to the other categories, but there was no difference detected between the remaining categories (Table 9). Upon examining the taxa with the highest relative abundances, the response to decreasing moisture availability was variable among species (Table 10). The cell length of C. gracilis, D. mesodon, E. bigibba, and Eunotia tenella was significantly shorter in populations with less available moisture. However, cell lengths for both A. minutissimum and
Diadesmis perpusilla were significantly longer in populations with less moisture. Cell length fluctuated among moisture categories for D. contenta and N. lapidosa, but this could be a result of small sample size in some of the moisture categories for each species.
Biovolumes
Aquatic diatoms had significantly smaller biovolume than aerial diatoms (p<0.0001)
(Table 11). The median biovolume of aquatic diatoms was 141.75µm3 compared to 164.13µm3 for aerial diatoms. Cells with the maximum biovolume were from aerial populations.
Comparing the biovolume of taxa shared between habitats, the cells from aquatic populations had a significantly smaller volume than those from aerial populations (Table 12). There was no difference in the biovolume of taxa unique to each habitat. Of the thirteen taxa examined for differences in biovolume between habitats, seven were found to be significantly smaller in aerial populations (Table 13). These taxa included A. minutissimum, D. contenta, D. mesodon, E. 13 incisa, F. capucina var. gracilis, F. rhomboides var. saxonica, and N. lapidosa. There was no difference in biovolume for the remaining taxa.
In the aerial habitats, the overall median biovolume was variable across the different moisture categories (Table 14). Cell biovolume was the smallest in populations with the lowest moisture availability, and biovolume was shown to be significantly smaller in these populations compared to populations with greater moisture levels (Table 15). Upon examining the taxa with the highest relative abundances, the response to decreasing availabilities of moisture was variable among species (Table 16). The biovolume of C. gracilis, D. mesodon, E. bigibba, and
E. tenella was significantly smaller in populations with less available moisture. However, biovolume for D. perpusilla was significantly larger in populations with less moisture.
Biovolume fluctuated among moisture categories for D. contenta and N. lapidosa which may be due to small sample size in some of the moisture categories. Biovolume also fluctuated for A. minutissimum among the moisture categories, however, small sample size was not an issue for this species.
Proportion Of Areolar Area
Diatoms from aerial habitats were found to have significantly less open area on the valve face compared to diatoms from aquatic habitats (p<0.0001). The median percent areolar area of aerial diatoms was 0.89% compared to 2.48% for aquatic diatoms. Only a small number of cells were measured from each sample, so there was insufficient data to compare percent areolar area for one species between habitats.
In the aerial habitats, the median percent areolar area was variable across the different moisture categories (Table 17). Percent areolar area was significantly greater in moisture category 1 compared to the three remaining moisture categories (Table 18). Due to the small 14 number of cells measured from each sample, there was insufficient data to compare percent areolar area for one species across different moisture availabilities.
Microhabitat Preferences
Forty-four genera and 229 taxa were identified from both bryophytic and epilithic microhabitats combined. There were 163 taxa identified from the bryophytic microhabitats, of which 85 were unique taxa. Forty-one genera were identified from bryophytic communities with six genera unique to this microhabitat. Genera unique to the bryophytic microhabitat included
Aulacoseira Thwaites, Placoneis Mereschkowsky, Stauroneis Ehrenberg, Staurosirella Williams and Round, Synedra Ehrenberg, and Tryblionella W. Smith. There were 144 taxa identified from the epilithic microhabitats, of which 66 were unique taxa. Thirty-eight genera were identified from the epilithic communities. There were three unique genera identified from the epilithic microhabitat and included Hantzschia Grunow, Kobaysiella Lange-Bertalot, and Tabellaria
Ehrenberg ex Kützing.
From the bryophytic habitats, twenty-six taxa were considered common occurring in
>20% of the samples (Table 19). Taxa with the highest average relative abundances included F. rhomboides var. saxonica (7.26%), E. paludosa var. paludosa (7.66%), D. contenta (5.41%), and
A. minutissimum (5.16%). From the epilithic habitats, twenty-six taxa were considered common occurring in >20% of the samples (Table 20). Taxa with the highest average relative abundances included C. gracilis (10.98%), A. minutissimum (8.61%), E. perpusillum (8.60%), F. rhomboides var. saxonica (7.66%). Of the common taxa identified in each microhabitat, thirteen taxa were found to be common to both (Tables 19-20). These taxa consisted of A. minutissima, Adlafia bryophila, Chamaepinnularia mediocris, D. contenta, D. perpusilla, E. paludosa var. paludosa, 15
F. rhomboides var. saxonica, Gomphonema parvulum morphotype 2, Meridion circulare,
Navicula angusta, Nitzschia sp1, N. lapidosa, and Planothidium lanceolata.
Seventeen taxa were identified as occurring in more than eight samples and were compared for microhabitat preference. These taxa included A. minutissimum, C.mediocris,
Navicula keeleyi, D. contenta, D. perpusilla, E. bigibba, E. exigua, E. paludosa var. paludosa, F. rhomboides var. saxonica, Navicula angusta, Nitzschia sp.1, Nitzschia sp.2, N. lapidosa, Nupela neglecta, Orthoseira roeseana, P. lanceolata, and Psammothidium marginulata. There was no difference in median relative abundance for any of the taxa except D. contenta which was found to have a significantly greater median relative abundance in bryophytic communities (5.45%) compared to epilithic communities (0.32%) (p=0.0097). Upon examining the taxa unique to each microhabitat, these taxa were rare occurring in less than six samples, most occurring in two or less.
Discussion
Diatom cell length and biovolume were found to be greater in populations from aerial habitats compared to populations from aquatic habitats. The longest cells were identified from the aquatic populations, however, aquatic populations were dominated by small taxa, such as A. minutissimum, R. pusillum, and Eolimna minima (Table 4). Abundances of moderately sized diatoms (20-60µm) were greater in aerial populations compared to aquatic populations (Tables 3,
4). These results contradict the findings by Round (1957) that aerial taxa are very small, usually
<20µm. Examining individual species did reveal that most species found across habitats were shorter in length and had a smaller volume in aerial populations (Tables 7, 13). Round (1957) did find that Pinnularia viridis had a much smaller size range in the aerial communities he examined. Taxa present in both habitats were found to have significantly greater cell length in 16 aerial populations while the cell length of taxa unique to each habitat was found to be significantly greater in aquatic populations (Table 6). Of the shared taxa, aquatic populations were dominated by smaller taxa which drove down the overall cell size. Taxa identified as unique to aerial habitats had a shorter cell length supporting findings by Round (1957).
In aerial habitats, diatom populations were found to be the shortest with the smallest biovolume in the driest habitats (Tables 8, 14). The length and biovolume of most species examined were found to be smaller as moisture levels decreased. This coincides with the findings of Van de Vijver and Beyens (1997) where the valve length of Pinnularia borealis was significantly smaller in aerial populations from drier habitats. There were two taxa, A. minutissimum and D. perpusilla, that did increase in length as moisture levels decreased (Table
10). As more taxa are examined, the response of cell length to decreases in moisture may in fact be revealed to not be a predictable response but be a species dependant response.
Diatoms from aerial habitats were found to have less open area on the valve face compared to diatoms from aquatic habitats. This reduction in open area on the valve face in aerial habitats could potentially provide protection against the osmotic stress encountered during periods of drying. However, percent open area of cells in the aerial populations was greater in communities from the driest habitats (moisture category 1) compared to the three other moisture categories. In fact, the percent open area for moisture category 1 was not different from the percent open area for the aquatic populations. This finding is counterintuitive to the idea that a reduction in the areolar area on the valve face is an adaptation against desiccation. D. contenta and D. perpusilla were present with high abundances in the aerial habitats with the lowest moisture availabilities (Table 3). Preliminary results from this study showed that both D. contenta and D. perpusilla had considerably large percent areolar areas (median value 2.86% and 17
4.95%, respectively) compared to other taxa. This suggests that these taxa may possess a mechanism other than a reduction in open area on the valve face for protection against desiccation. There were a limited number of cells measured from the aerial populations which could be contributing to the overall high percent open area for the populations from the driest habitats. Other abundant taxa from moisture category 1 such as E. paludosa var. paludosa and
Eunotia curtagrunowii had much less open area on the valve face. Cells of E. paludosa var. paludosa had small, unoccluded puncta with a median open area of 1.97%, and the puncta of cells of E. curtagrunowii were mostly occluded with a median open area of 0.01%. More research into this issue is needed in order to determine whether the overall percent open area does decrease with decreasing moisture availabilities.
There does not appear to be a microhabitat preference among aerial diatoms. Only one species, D. contenta, was present with significantly higher abundances in bryophytic communities compared to epilithic communities. This species was also most abundant in the driest aerial communities, and SEM analysis did reveal that the percent open area on the valve face was relatively high for this species. These finding may suggest that bryophytes do allow for some protection against desiccation. However, there was no microhabitat preference seen in D. perpusilla which was also found to have high abundances in the driest habitats as well as have a large amount of open area on the valve face.
Most of the taxa unique to either microhabitat were present in only one or two samples making determinations of microhabitat preference difficult. If a greater number of samples were analyzed, patterns in microhabitat preference may become more apparent. Currently, this study suggests that microhabitat based on substrate type does not play an important role in the species composition of these communities and instead suggests that certain taxa, if adapted to the aerial 18 environment, can survive on any substrate. Moisture availability, desiccation regime, or algal community composition may have a greater influence on the presence/absence and abundance of diatom taxa.
19
CHAPTER 2: CONTRAST AND COMPARISON OF AERIAL ALGAL COMMUNITIES FROM TWO DISTINCT REGIONS
Introduction
The ecology of aerial algal communities has been understudied and is presently not well understood. Most of the research on aerial habitats has been floristic in nature, focusing on the description and identification of species that are present in these areas (McMillan and Rushforth
1985; Lowe and Collins 1973; Dodd and Stoermer 1962). The majority of ecological studies that have been performed on aerial algae are on bryophytic diatom communities mainly in the Arctic and Antarctic (Van de Vijver et al. 2008; van Kerckvoorde et al. 2000; Van de Vijver and
Beyens 1997; Beyens 1989). There have been limited ecological studies of aerial communities from the northern temperate zone (Furey et al. 2007; Lowe et al. 2007; Camburn 1983; Camburn
1982), however, there have been many studies focusing on cryptogamic soil crust communities
(Johansen et al. 1993; Johansen and St. Clair 1986; Johansen and Rushforth 1985; Johansen et al.
1984). These ecological studies do demonstrate the significant impact of moisture in these habitats. Moisture availability can be quite variable in these habitats due to the often ephemeral water sources. Sources for water in aerial habitats include groundwater seeps, precipitation, humidity, or waterfall spray. In addition to creating moisture variability across aerial habitats, moisture can vary daily or seasonally within a particular habitat. This fluctuation in moisture can influence the species inhabiting these areas. Species diversity can also be affected by moisture and has been shown to increase as moisture availability increases (Casamatta et al. 2002;
Camburn 1983; Johansen et al. 1983).
There has been no published research directly comparing aerial algal floras between geographic regions. While moisture may exert the greatest influence on community composition within a geographic area, other factors may become more influential when examining 20 community composition between different regions. Variables such as pH, geology, and climate may play a role in structuring the general flora of the area while moisture may influence local variability. The Great Smoky Mountains National Park (GSMNP) and the land surrounding
Lake Superior in the Upper Peninsula (UP) of Michigan and Ontario, Canada, are abundant in aerial algal habitats. Natural habitats created from stream cuts, waterfall spray, and exposed bedrock, in addition to habitats created by road cuts all provide potential areas for aerial algal communities to develop. I examined both the ecology of habitats within each region as well as compared the overall flora between the two regions.
I anticipated that the overall aerial algal communities would differ between the two study areas. While there may be some cosmopolitan taxa present across the two regions, I believed that the overall flora from the Lake Superior region (LSR) would be distinct from that of the
GSMNP. I expected these two areas to support distinct aerial algal flora due to environmental differences such as climate, geology, and pH. Within the study areas, I expected to see community similarities related to available moisture.
Study Areas
The area of the UP is 42,610 km² and it lies between 45° and 47° north latitude.
Elevations range from 179 m to 603 m. The UP belongs to the Western Great Lakes forests ecoregion of the temperate hardwood and broadleaf forest biome. The UP is part of the physiographic region known as the Canadian Shield. The Canadian land surrounding Lake
Superior also belongs to the Canadian Shield. The Canadian Shield is mainly comprised of igneous rock covered with a thin soil layer resulting in many areas of exposed bedrock. The north shore of Lake Superior lies at 49° north latitude and is within the boreal forest biome.
Both of these areas are within the cool temperate zone. These two locations will be collectively 21 referred to as the LSR for the remainder of this manuscript. The Köppen climate classification for the LSR is a humid continental climate characterized by variable weather conditions and a large range in seasonal temperatures. Precipitation is greatest during the summer months in this climate.
The GSMNP is located across the Tennessee-North Carolina state line and covers approximately 2,000 km². Elevations range from 267 m to 2025 m. The park lies at 35° north latitude. The GSMNP belongs to the Appalachian-Blue Ridge Forest ecoregion of the temperate hardwood and broadleaf forest biome. One of the largest tracts of deciduous, temperate, old- growth forest in North America is found in the park. The GSMNP belongs to the physiographic region known as the Blue Ridge Mountains and is within the warm temperate zone. The Köppen climate classification for the GSMNP is a humid subtropical climate which is distinguished by relatively mild winters and warm summers. This climate type experiences high levels of humidity and precipitation that is fairly evenly distributed throughout the year. However, the large variability in elevation within the GSMNP results in significantly variable climate with increasing precipitation and decreasing temperatures as elevation increases (Shanks 1954).
Air pollution has been a documented problem in the GSMNP for several decades. The burning of fossil fuels has resulted in acid precipitation from the atmospheric deposition of sulphur dioxide and nitrogen oxides. The annual precipitation in the GSMNP is five to ten times more acidic than natural rain (National Park Service 2005). This acid precipitation results in the buildup of sulfate and nitrate in the soils as well as the release of aluminum and other toxic metals from the soil (Driscoll et al. 2001; Castro and Morgan 2000).
22
Methods
Potential aerial habitats within the LSR were identified from topographic maps; these areas were explored and samples were collected when suitable habitat was identified. A total of
42 samples were collected from the LSR in July and August, 2006. Habitats similar to those found in the LSR were targeted in the GSMNP and a total of 75 samples were collected from in
June and July, 2007. Descriptions of the habitat as well as physical and chemical variables, including pH, moisture levels, light levels, and aspect were recorded for each site. The pH was measured using EMD colorpHast pH-indicator strips (range: 2.5 to 10 pH units; sensitivity of 0.2 to 0.3 pH units) in order to provide an estimate of differences in the acidity of sampling locations. As a method to estimate moisture levels, a piece of sponge was placed on each rock face for five or ten seconds, depending upon moisture content of the habitat. The difference in weight of the sponge after removal from the substrate was recorded for each site. The light levels for the LSR were measured using a Licor light meter (LI-189). A Quantum light meter
(model QMSS) was used in the GSMNP. Each site was geo-referenced (Garmin GPS unit) where global positioning system signals were available (Coordinate datum NAD83). Samples were preserved in at least 2% glutaraldehyde.
Samples were analyzed with an Olympus BX51 Photomicroscope with high resolution
Nomarski DIC optics, and digital images were recorded with a Spot® camera attached to the microscope and a computer. A minimum of 600 algal units were counted from each sample, and the non-diatom algae were identified from this material. Diatoms counted in each sample were identified from cleaned permanent mounts. Permanent mounts were made by boiling an aliquot of each sample in nitric acid, air drying the cleaned material onto cover glasses, and mounting the material in Naphrax. Algae were identified to the lowest taxonomic level possible using 23 standard references. References consisted of: Geitler (1932), Krammer and Lange-Bertalot
(1986), Krammer and Lange-Bertalot (1988), Krammer and Lange-Bertalot (1991a), Krammer and Lange-Bertalot (1991b), Komárek and Anagnostidis (1999), Potapova et al. (2003), Wehr and Sheath (2003), Komárek and Anagnostidis (2005), Thomas et al. (2009), and Furey (2011).
Relative abundances of each taxon were calculated for each sample. Rare taxa were removed from the combined data set prior to statistical analysis. Taxa that did not occur in at least one site with a relative abundance of 2% were considered rare and removed from the data set. This reduced the total number of taxa from 365 to 191. Four moisture categories were created from the sponge measurements for the purpose of statistical analysis. The four categories included dry, damp, wet, and very wet. Weight change less than 0.1 g was considered dry, weight change between 0.1-1.0 g was considered damp, weight change between 1.0-5.0 g was considered wet, and weight change greater than 5.0 g was considered very wet. Algal community patterns were explored via non-metric multidimensional scaling (NMDS) of Bray
Curtis similarities of log transformed data. An analysis of similarities (ANOSIM) was used to determine significance among the clusters identified in the NMDS ordinations. Taxa contributing to the clusters were identified through similarity percentages (SIMPER).
Results
Of the total samples collected in the LSR, twenty random samples were analyzed. Of the samples analyzed, pH ranged from 5.2 to 8.8 and light levels ranged from 002-1385 µmol m-2 s-1.
Sixty-six algal genera and 238 taxa were identified, of which 170 were unique to the LSR (Table
1). Of these taxa, the majority were identified from three divisions, the Cyanophyta,
Bacilliariophyta and Chlorophyta, with average relative abundances of 56.1%, 33.7%, and 9.5% respectively. Taxa belonging to the Chrysophyta comprised an average relative abundance of 24 less than 0.5%. In the LSR, nineteen taxa were considered common occurring in >20% of the samples (Table 2). Of these, Achnanthidium minutissimum, Aphanocapsa cf. fusco-lutea,
Leptolyngbya sp. 2, Limnothrix sp. 1, Pseudanabaena cf. minima occurred in >40% of the samples. Taxa with the highest average relative abundances included Leptolyngbya cf. subtilissima (8.0%), Gloeothece tepidariorum (4.4%), Leptolyngbya sp. 2 (4.3%), and Mougeotia spp. (4.0%) (Table 2).
In the GSMNP, twenty random samples were analyzed from the samples collected. Of the samples analyzed, pH ranged from 3.0 to 7.9 and light levels ranged from 001-780 µmol m-2 s-1. Fifty-five algal genera and 190 taxa were identified, of which 122 were unique to the
GSMNP (Table 1). These taxa were identified from three divisions, the Cyanophyta,
Bacilliariophyta and Chlorophyta, with average relative abundances of 64.5%, 19.0%, and 14.3% respectively. Thirteen taxa were considered common in the GSMNP, occurring in >20% of the samples (Table 3). Of these, A. minutissimum, Leptolyngbya sp. 2, and P. cf. minima occurred in
>35% of the samples. Taxa with the highest average relative abundances included Nostoc sphaericum (6.6%), P. cf. minima (5.9%), Leptolyngbya sp. 2 (5.4%), and A. minutissimum
(3.2%) (Table 3).
The algal communities from both the GSMNP and LSR were dominated by cyanobacteria with mean relative abundances over 50%. More than half of the commom taxa, eleven of nineteen, in the LSR were cyanobacteria (Table 2), but less than half of the common taxa, five of thirteen, in the GSMNP were cyanobacteria (Table 3). Just over half of the common taxa in the GSMNP were diatoms (Table 3).
Of the common taxa found in each region, seven taxa were found to be common to both regions (Table 2-3). These taxa consisted of A. minutissimum, A. cf. fusco-lutea, L. cf. 25 subtilissima, Leptolyngbya sp. 2, N. sphaericum, P. cf. minima, and unknown coccoid
Chlorophyte sp.1. The majority of these taxa were present with high relative abundances in the samples from each region with the exception of A. cf. fusco-lutea and L. cf. subtilissima with mean relative abundances of 0.6% and 1.2% respectively in the GSMNP, and unknown coccoid
Chlorophyte sp.1 with a mean relative abundance of 0.3% in the LSR.
In the LSR, there were 22 taxa with a mean relative abundance greater than 1% with five taxa unique to the LSR region (Table 4). There were 26 taxa in the GSMNP with a mean relative abundance greater than 1%, and of these taxa, 11 were unique to the GSMNP (Table 5). In each region, over 50% of the taxa with a mean relative abundance over 1% were cyanophytes.
The NMDS ordination of the community data did not show distinct separation between the two regions (Figure 1). However, there was separation in the GSMNP samples, forming two distinct groups with the LSR samples bisecting those groups (Figure 1). The results from the
ANOSIM revealed a significant difference between the GSMNP 1 and GSMNP 2 (p-value
0.001) groups as well as between the GSMNP 2 and LSR groups (p-value 0.001) (Table 6).
Eleven taxa contributed to approximately 50% of the dissimilarity between the two GSMNP groups (Table 7), while seventeen taxa contributed to approximately 50% of the dissimilarity between the GSMNP 2 and LSR groups (Table 8). There was some clustering in the NMDS ordination based on moisture availability with separation between the two extreme moisture categories (Figure 2). The results from the ANOSIM did not show that a significant difference existed among the moisture categories (Table 9). The lack of significance among the moisture categories was possibly due to the relatively loose clustering of sites within each moisture category. There were no patterns detected for any of the remaining physical and chemical data. 26
The NMDS ordination for each of the regions did demonstrate separation when the data were categorized by moisture (Figures 3-4). For both the LSR and GSMNP community data, separation was seen between the two extreme moisture categories. However, the ANOSIM found no significant difference among the moisture categories for either region (Table 9). The lack of significance among moisture categories was most likely due to the small sample size within each category. For both regions, there were few to no diatoms present in moisture category 1, while diatoms comprised over 60% mean relative abundance in moisture category 4 for the LSR and over 50% for the GSMNP (Table 10-11). Species diversity was highly variable across all samples from each region (Table 12). There was no significant difference found among the species diversity of the communities from the different moisture categories for each region (LSR p>0.38, GSMNP p>0.06).
In order to explore broad scale patterns, data were consolidated from species to division for each sample. The NMDS ordination of the division data showed no clustering based on region (Figure 5). A bubble plot created from the NMDS ordination did reveal a pattern for the three divisions, Cyanophyta, Chlorophyta, and Bacillariophyta, across all samples (Figure 6).
The samples formed a triangular pattern in the plot, with each tip of the triangle representing high relative abundance for one of the three divisions. Upon examining the uncategorized physical and chemical data, no variable could explain the pattern seen in the plot. Similar patterns were seen in the bubble plots for each region (Figure 7-8), but again, the physical and chemical data could not explain the patterns.
Discussion
Aerial algal communities from both the LSR and GSMNP were dominated by cyanobacteria, with mean relative abundances greater than 50%. Cyanobacteria have been found 27 to dominate communities in aerial habitats (Matthes-Sears 1999; Alfinito et al. 1998; Broady
1989). Cyanobacteria are also often found to be the first algal colonizers in aerial habitats
(Johansen et al. 1983; Hayren 1940; Diels 1914). The tolerance of many cyanobacterial taxa to wide ranges of moisture and light may contribute to their dominance (Whitton and Potts 2000;
Wynn-Williams 2000; Matthes-Sears 1999). It has been shown that cyanobacteria are able to survive and recover more quickly from desiccation than other algae (De Winder et al. 1989).
Moisture availability can vary greatly in aerial habitats with algal communities experiencing either sporadic or frequent periods of desiccation. The unpredictability of moisture availability in many aerial habitats creates a major stress upon algae that colonize these areas. The ability of cyanobacteria to begin colonizing new aerial habitats before other algal groups combined with their tolerance to desiccation give them a competitive advantage in these habitats.
The aerial algal flora of the GSMNP as a whole was not distinct from that of the LSR.
However, the NMDS ordination did identify two distinct communities within the GSMNP when analyzing the entire data set of both regions (Figure 1). The GSMNP 1 group had higher mean relative of abundances of cyanobacterial taxa while the GSMNP 2 group had higher mean relative abundances of chlorophytes and diatoms (Table 9). Cyanobacteria are commonly found to dominate extremely dry habitats while the numbers of diatom taxa increase with increasing moisture availability (Casamatta et al. 2002; Pentecost 1992). Moisture availability did contribute to the separation of the two GSMNP groups, with the driest sites within GSMNP 1 and the wettest sites within GSMNP 2 (Figure 2). However, there were sites in both GSMNP groups with intermediate levels of moisture.
Research conducted by Matthes-Sears et al. (1999) found no effects of moisture on algal community composition but attributed this finding to the small range in moisture variability 28 across their study site. Despite the relatively wide range in moisture availabilities in the present study, NMDS ordinations for the LSR-GSMNP combined, the LSR, and the GSMNP community data only revealed separation between the two extreme moisture categories (Figures 2-4). This is possibly due to the fact that algal community composition has a distinct response to extremes of moisture availability while intermediate moisture levels illicit variable responses. Cyanobacteria dominated the “dry” sites while diatoms were almost completely absent (Table 10-11). The absence or near absence of diatoms from aerial habitats with low levels moisture is common
(Casamatta et al. 2002; Pentecost 1992). Species diversity was not found to increase with increasing moisture as has been shown in other studies (Casamatta et al. 2002; Camburn 1983;
Johansen et al. 1983).
The physical and chemical characteristics of the LSR and GSMNP were not significantly different enough to lead to distinct algal communities for each region. The range of pH in each region overlapped, and the light levels measured in the GSMNP overlapped the lower range of those measured in the LSR. However, the absence of measured light levels from the higher ranges in the GSMNP could possibly be due to the time of day the measurements were taken.
Light exposure at a site depends upon the aspect as well as vegetation cover, and it may have been more revealing to measure maximum light exposure in a 24 hour period for each site. Also, measuring ultraviolet light levels may provide insight into aerial algal community composition and species distribution.
There were taxa that were unique to each region, but these taxa were present in such low abundances that they did not contribute much to the community composition. Many of the taxa that were present in higher abundance were present in both the LSR and GSMNP communities.
Species dispersal may play a role in similarities seen between the community compositions of 29 these regions. Algae have been shown to be easily transported by the wind (Brown et al. 1964).
Taxa that can withstand desiccation have the potential to survive aerial transport. Many algal taxa from aerial habitats produce extracellular mucilage which allows them to withstand periods of desiccation (Gerrath 2003; Potts 1999; Shephard 1987; Patrick 1977). UV radiation can also impact the survival of cells in aerial transport. The ability of cyanobacteria to not only withstand desiccation but also to produce photoprotective pigments gives them a competitive advantage for longer distance aerial transport (Ehling-Schulz et al. 1997; Garcia-Pichel et al. 1992, De Winder et al. 1989).
The similarity of microhabitats between the LSR and GSMNP combined with the aerial dispersal of algal cells potentially contributed to the overall similarity of these aerial algal communities. Johansen et al. (1983) found that mucilage producing cyanobacteria and green algae are the first colonizers on moist rock faces, and once established, other species begin to colonize the mucilage. Many of the more abundant taxa from these regions are mucilage producing cyanobacteria which may have a greater potential to survive aerial dispersal and colonize aerial habitats in both regions. Once these establish, more localized species that cannot survive long distance transport can begin to colonize these communities.
30
CHAPTER 3: BRYOPHYTES AND ASSOCIATED ALGAL COMMUNITIES FROM AN EXPOSED CLIFF FACE ON O'AHU (HAWAI’I, USA)
Introduction
Bryophytes are common components of aerial habitats and many studies have described the algal flora associated with bryophytes in these habitats (Alfinito et al. 1998; Van de Vijver and Beyens 1997; Lowe and Collins 1973; Dodd and Stoermer 1962). Two major bryophyte groups include mosses and liverworts and can be distinguished by gametophyte symmetry and leaf arrangement (Schofield 1985; Crum and Anderson 1981). The moss gametophyte is radially symmetric, and leaves are spirally arranged around a stem. Liverworts typically have a dorsiventral gametophyte, and take one of two forms, thallose or leafy. Leaves are typically arranged in two lateral rows and lack costae. Due to the ectohydric nature of most bryophytes, water is held and transported externally through capillary action (Schofield 1985). The overlapping leaves, leaf bases, paraphyllia, papillae, and rhizoids all act to trap water (Schofield
1985; Proctor 1982). This trapped water is not only critical to the survival of the bryophyte, but also provides water to the associated algal inhabitants.
Clearly, the ability of bryophytes to retain moisture makes them an important microhabitat for aerial algae. Furthermore, research has indicated that moisture is an important factor in structuring algal communities of aerial habitats (Casamatta et al. 2002; Beyens 1989;
Camburn 1983). Other research into these communities has shown a relationship between moisture levels in bryophytes and associated algal species (Van de Vijver et al. 2008; Van de
Vijver and Beyens 1999; Van de Vijver and Beyens 1997; Beyens 1989). However, the majority of the research into bryophyte-algal associations has focused on only a portion of the algal community present. Many studies focus on either the associated diatoms or the cyanobacteria
(van Kerckvoorde et al. 2000; Van de Vijver and Beyens 1999; Van de Vijver and Beyens 1997; 31
Nakatsubo and Ohtani 1991; Beyens 1989) with little work being done on the entire associated algal community (Alfinito et al. 1998, Ohtani and Kanda 1987, Ohtani 1986). Also, most of the research into these associations has been conducted in polar ecosystems, such as the work of Van de Vijver et al. 2008, Van de Vijver and Beyens 1999, Alfinito et al. 1998, Beyens 1989, and
Broady 1989, with very little research from other ecosystems, such as temperate or tropical. This lack of analysis on the entire community associated with aerial bryophytes leads to an incomplete picture of algal community patterns that are associated with bryophytes.
The objective of this study was to examine bryophytes and their associated algal communities from a cliff face in O'ahu, Hawai’i. The variability in moisture and sun exposure on the exposed rock of this cliff provided habitat for a diverse bryophyte flora. I anticipated that different bryophyte species would support distinct algal communities due to variable microhabitats between bryophyte species. The differing bryophyte morphologies should influence their ability to retain moisture which I then expected would influence the algal community composition. This is the first comprehensive study on algal-bryophyte associations in tropical aerial habitats.
Study Area
The state of Hawai’i is in the central Pacific Ocean and consists of hundreds of islands across a 2400 km2 area. O'ahu is the second oldest and third largest of the Hawai’ian Islands, with a total area over 1500 km2. Maximum elevation on the island is 1220 m. Two volcanoes,
Wai'anae and Ko'olau, formed the island and are oriented parallel to each other from the northwest to the southeast. Nu'uanu Pali is a cliff face located in the southern part of the Ko'olau
Mountain at an elevation of 366 m. Due to the tropical climate, there are only two seasons; the rainy season from November to March and the dry season from April to October. 32
Methods
Bryophytes, and associated algal communities, were collected in February and March,
2008. Descriptions of the habitat as well as physical and chemical factors, including pH, moisture levels, light levels, and aspect were recorded for each site. The pH was measured using
EMD colorpHast pH-indicator strips (range: 2.5 to 10 pH units; sensitivity of 0.2 to 0.3 pH units) in order to provide an estimate of differences in the acidity of sampling locations. As a method to estimate moisture levels, a piece of sponge was placed on each rock face for five or ten seconds, depending upon moisture content of the habitat. The difference in weight of the sponge before and after deployment was recorded for each site. Light levels were measured using a
Quantum light meter (model QMSS). Samples were preserved in at least 2% formalin.
Samples were analyzed with an Olympus BX51 Photomicroscope with high resolution
Nomarski DIC optics. From a subsample diatoms were cleaned in 30% hydrogen peroxide and potassium dichromate crystals and air dried onto cover glasses. Permanent diatom mounts for light microscope (LM) analysis were made using Naphrax mounting medium. A minimum of
600 algal units were counted from each sample. Diatoms were identified from the cleaned permanent mounts. Digital images were recorded with a camera (Spot®) attached to the microscope and a computer. Algae were identified to the lowest taxonomic level possible using standard references. References consisted of: Geitler (1932), Krammer and Lange-Bertalot
(1986), Krammer and Lange-Bertalot (1988), Krammer and Lange-Bertalot (1991a), Krammer and Lange-Bertalot (1991b), Komárek and Anagnostidis (1999), Potapova et al. (2003), Wehr and Sheath (2003), and Komárek and Anagnostidis (2005). Bryophytes were identified to species when possible by Mashuri Waite (University of Hawai’i at Mānoa, Honolulu, HI). 33
Taxa that did not occur in at least one site with a relative abundance of 2% were considered rare were removed from the data set prior to statistical analysis. This reduced the total number of taxa from 239 to 125. Moisture categories were created from the sponge measurements for the purpose of statistical analysis. Five moisture categories were created from the sponge measurements for the purpose of statistical analysis. The five categories included dry, damp to the touch, damp, wet, and very wet. Samples that were completely dry were considered dry, samples that were damp to the touch with no change in sponge weight were considered damp to the touch, weight change less than 0.1 g was considered damp, weight change between 0.1-1.0 g was considered wet, and weight change greater than 1.0 g was considered very wet. Three light categories, which included low, moderate, and high were also created to aid in statistical analysis. Light levels less than 100 µmol m-2 s-1 were classified as low, light levels between 100-
200 µmol m-2 s-1 were classified as moderate, and light levels greater than 200 µmol m-2 s-1 were classified as high. Algal community patterns were explored via non-metric multidimensional scaling (NMDS) of Bray Curtis similarities of log transformed data. An analysis of similarities
(ANOSIM) was used to determine significance among the clusters identified in the NMDS ordinations. Taxa contributing to the clusters were identified through similarity percentages
(SIMPER).
Results
Site pH remained consistent across the cliff face at 6.5. Light levels were highly variable among sites, ranging from 005-1208 µmol m-2 s-1. From the 32 samples collected, ten categories of bryophytes were identified; one category included the unidentified liverworts, the remaining categories were composed of the nine identified moss species. Fifty-five algal genera and 239 taxa were identified from the bryophytes of Nu'uanu Pali. Of these taxa, the majority were 34 identified from two divisions, the Cyanophyta and Bacilliariophyta, with relative abundances of
86.5% and 11.9% respectively. The remaining taxa identified belonged to the divisions
Chlorophyta and Chrysophyta.
Twenty-nine taxa were considered common occurring in >20% of the samples (Table 1).
Of these, Cyanosarcina spp., Denticula kuetzingii Grunow, Diadesmis contenta (Grunow) D.G.
Mann, Diadesmis sp. 2, Diadesmis sp. 4, Diadesmis sp. 10, Gloeothece tepidariorum (A. Braun)
Lagerheim, Pseudanabaena cf. minima, and Pseudanabaena sp. 2 occurred in >50% of the samples. Taxa with the highest average relative abundances included G. tepidariorum (10.5%),
Scytonema ocellatum Lyngbye (5.8%), and P. cf. minima (4.5%) (Table 1).
NMDS ordination of the community data did not reveal strong clustering based on the categories bryophyte or moisture (Figs 1-2). The ordination did show two distinct clusters based on aspect, a cluster south-facing (SFC) and a north/west-facing cluster (NFC/WFC) (Fig. 3).
The results from the ANOSIM revealed a significant difference between the SFC and NFC (p- value 0.001), however, there was not a significant difference between the SFC and WFC (Table
2). The lack of significance between the SFC and WFC is most likely due to the extremely small sample size of the west facing group. Nineteen taxa contributed to nearly 50% of the dissimilarity between the NFC and SFC (Table 4). The main taxa contributing to the separation of these clusters included G. tepidariorum with a greater relative abundance in the north facing cluster, and S. ocellatum, Aphanocapsa muscicola (Meneghini) Wille, and P. cf. minima with greater relative abundance in the south facing cluster (Table 4).
Two clusters were also identified in NMDS based on light, a high light cluster (HLC) and a moderate/low light cluster (MLC/LLC) (Fig. 4). ANOSIM results indicated a significant difference between high light and low light (p-value 0.001) as well as between high light and 35 moderate light (p-value 0.001) (Table 3). Nineteen species contributed about 50% of dissimilarity between the HLC and LLC (Table 5). The main taxa contributing to the separation of these clusters included G. tepidariorum with a greater relative abundance in the LLC, and S. ocellatum, A. muscicola, and P. cf. minima with greater relative abundance in the HLC (Table 5).
Approximately 50% of the dissimilarity between the HLC and MLC was determined by thirteen taxa (Table 6). The main taxa contributing to the separation of these clusters included
Gloeocapsa caldariorum Rabenhorst and G. tepidariorum with a greater relative abundance in the MLC and S. ocellatum and A. muscicola with greater relative abundance in the HLC (Table
6).
To examine more broad scale patterns, the community data were consolidated to relative abundances for each division in the samples. The NMDS ordination on these data showed no clustering based on the categories bryophyte or moisture (Figs 5-6). Patterns are evident in the ordination based on both aspect and light (Figs 7-8). To further explore these patterns, bubble plots were created. There were no patterns detected for any of the divisions except the diatoms.
A gradient of increasing relative abundance was apparent when examining the diatom data (Fig.
9b). The raw, uncategorized data for moisture and light were used to create bubble plots for these variables to compare against the gradient observed for the diatoms (Fig 9c-d). This, however, did not reveal any obvious patterns for each variable to explain the gradient seen in the diatom data.
Discussion
The algal communities associated with the bryophytes of Nu'uanu Pali were dominated by cyanobacteria with a mean relative abundance of 86.5%. Of the 29 common taxa, more than half were cyanobacteria while the remaining taxa were diatoms which constituted a small 36 proportion of each community (Table 1). In studies that have examined the entire aerial algal community associated with bryophytes, cyanobacteria were found to dominate (Alfinito et al.
1998; Broady 1989). Ohtani (1986) found that diatoms were absent from communities inhabiting bryophytes which experience extreme desiccation. The dominance of cyanobacteria inhabiting aerial bryophytes is most likely due to fact that cyanobateria are more tolerant to desiccation which can be a common occurrence. De Winder et al. (1989) demonstrated cyanobacteria not only survive desiccation, but they are also able to recover more quickly from desiccation than other algae.
There was no relationship found between bryophyte species and the associated algal community. Alfinito et al. (1998) also found no association between the algal community and moss species in the Antarctic. There was also no relationship found between moisture and algal community composition. This finding contradicts several studies that did in fact find a relationship between moisture and community composition (Van de Vijver et al. 2008; Van de
Vijver and Beyens 1999; Van de Vijver and Beyens 1997; Beyens 1989). These studies, however, only examined the diatoms and not the entire algal community. By only examining a portion of the algal community, true patterns may be missed and the relationship between bryophytes and associated algal communities will not be completely understood.
Relationships were identified between both aspect and light with algal community composition. These two factors are interrelated due to the fact that the south facing habitats receive direct light from the sun, while the north facing habitats do not receive direct sunlight.
The bryophytes and algae inhabiting the south facing side of the cliff experience a much harsher environment in regards to moisture and photooxidative stress. Despite the high humidity, the intense heat of the sun results in daily desiccation of these organisms. Bryophytes inhabiting the 37 north facing side of the cliff have the potential of holding on to any moisture from precipitation or humidity because they do not experience the drying effects of the sun. Even small, hard to quantify moisture trapped within the bryophyte could create a refuge for algae to inhabit. This can explain the difference in algal community composition from seemingly equally dry bryophytes from differing aspects along the cliff face.
Alfinito et al. (1998) found that different algal species inhabited different locations of the moss, the surface versus the axial area, and suggested that the axial area may hold a thin film of water while the surface of the tuft was dry which lead to the difference in the taxa present.
Alfinito et al. (1998) found that mucilaginous cyanobacteria formed gelatinous layers on the surface of the moss tufts while other forms of cyanobacteria, diatoms and chlorophytes were located within the bryophytes. The production of mucilage serves to protect the cells during periods of desiccation by storing water and reducing osmotic stress on the cells (Gerrath 2003;
Potts 1999; Shepard 1987; Patrick 1977). Broady (1982, 1987) also noted cyanobacterial mats, comprised of species of Nostoc and Oscillatoriacean filaments, forming along the outer surface of bryophytes which were replaced by other forms, such as the diatom Pinnularia borealis and the desmid Actinotanium cucurbita, in the moist surficial depressions of the bryophyte cushions.
The present study did not examine where algal cells were colonizing the bryophytes. This would be an interesting avenue to pursue and may show that those species which produce less/no mucilage inhabit areas where the moss morphology retains moisture. Moss morphology has been examined as a refuge from disturbance in aquatic systems (Knapp and Lowe 2009), however, the research by Alfinito et al. (1998) did not pursue the idea that the morphology may be a refuge from desiccation, only giving it a cursory glance. This approach may better explain 38 algal community composition patterns in aerial habitats rather than homogenizing all the species within the bryophyte.
The lack of association of any one environmental variable to the pattern of distribution seen for diatoms along the cliff face of Nu'uanu Pali suggests that it is the combination of variables which influence distribution. The diatoms were almost completely absent in the south facing samples (compare Fig 7 to Fig 9b). This potentially could be due to the exposure of the south facing habitats to greater amounts of solar radiation. Cyanobacteria are known to produce protective pigments that accumulate both intracellularly and extracellularly. Both the UV-A absorbing pigment scytonemin and the UV-B absorbing pigments mycrosporine amino acids accumulate in the extracellular mucilage. The absence of such compounds in diatoms may explain their near absence from the south facing samples.
To fully understand algal community composition and distribution in aerial habitats, the entire community must be included in analysis. Patterns detected while only examining part of the overall community may be incorrectly attributed a particular variable which may not hold true once the entire community is examined. Interactions between different algal species as well as with habitat variables may be missed if the entire community is not studied.
39
CHAPTER 4: DESICCATION TOLERANCE OF AQUATIC AND PSEUDOAERIAL ALGAE
Introduction
The impact of desiccation on aquatic algal communities has been the focus of much research (Mosisch 2001; Benenati et al. 1998; Peterson 1987; Evans 1959). However, there has been no published research on the effects desiccation has on aerial algal communities. These habitats receive moisture from a variety of sources such as groundwater seeps, precipitation, humidity, or waterfall spray and can experience occasional to frequent episodes of drying, depending upon sun intensity, wind exposure and levels of precipitation. An aerial habitat which receives moisture from groundwater seeps, surface runoff, and waterfall spray is termed pseudoaerial (Petersen 1935). Pseudoaerial habitats typically receive a constant moisture supply, however, algae present in these communities must still be able to tolerate and survive periods of low or no moisture. In aerial habitats, research has focused on the comparison of communities from different microhabitats with varying moisture levels in which moisture has been shown to be an important factor in structuring the communities (Casamatta et al. 2002;
Beyens 1989; Camburn 1983). Taxa adapted to aerial habitats have been found in aquatic systems, however, they occur infrequently and do not form populations as large as they would in aerial communities (Patrick 1977).
There has been a considerable amount of research into the mechanisms developed by algae to survive desiccation. The reduction in cell size as moisture levels decrease is one such mechanism that is commonly seen in diatoms. In general, diatom cells from aerial populations have been found to be smaller than diatoms from aquatic populations (Van de Vijver and Beyens
1997; Patrick 1977; Round 1957). Diatoms have also developed adaptations to fluctuating moisture availabilities that can be common in aerial habitats. The thickening of cell walls and 40 the production of internal valves are methods by which diatoms can retain moisture (Main 2003;
Round et al. 1990; Dodd and Stoermer 1962). Another adaptation against desiccation is the production of extracellular mucilage. Mucilage production is common in aerial cyanobacteria and green algae, and, in addition, some diatom genera produce mucilaginous sheaths. This mucilage can contain a considerable amount of moisture which can store moisture and reduce the osmotic stress on algal cells during periods of desiccation (Gerrath 2003; Potts 1999; Shepard
1987; Boney 1980). Extracellular mucilage can also be a refuge for other taxa that do not produce mucilage (Boney 1980). Much attention has been focused on the survivability of the cyanobacterium Nostoc commune which has been shown to be extremely tolerant to desiccation, surviving close to 100 years in a dry state (Potts 2000; Cameron 1962). Studies into N. commune have revealed that this species produces a unique protein which aides in desiccation tolerance
(Scherer and Potts 1989).
In order to understand the role of moisture in shaping pseudoaerial algal communities an experiment was performed on algal communities from the Great Smoky Mountains National
Park (GSMNP). This experiment examined the effects of desiccation on structuring algal communities by observing potential shifts in dominant taxa. I anticipated that an increase in desiccation pressure would push these communities towards a dominance of taxa more adapted to desiccation, especially taxa that have the ability to produce extracellular mucilage. Also, as moisture levels decreased, I predicted there would be an overall decrease in cell density in these populations.
41
Study Area
The GSMNP straddles the Tennessee-North Carolina state line and covers approximately
2,000 km². Elevations range from 267 m to 2025 m. One of the largest tracts of deciduous, temperate, old-growth forest in North America is found in the park.
Methods
Samples were collected from six locations within the GSMNP, three pseudoaerial locations and three stream locations (Table 1). Pseudoaerial habitats receiving moisture from groundwater seeps and in close proximity to stream locations were selected for sampling. At each location, two samples were collected, a composite pseudoaerial sample and a composite stream sample. Each of these samples was homogenized and 1 ml of this slurry was placed on the top of a 63.5mm x 63.5mm x 12.5mm sandstone tile. Each tile was placed in a covered Petri dish with sufficient Z8 medium (Kotai 1972) to cover the bottom of the Petri dish but not cover the tile. The porous nature of the sandstone tiles would allow for moisture and nutrients to wick into the tile to create a most surface for algal colonization as well as supply nutrients for the community. The tiles were kept in a room with windows and exposed to ambient light conditions without exposure to direct sunlight. The communities were given one month (4 weeks) for establishment and the medium was changed weekly. At the end of this establishment period, three tiles were removed from each site for community analysis prior to experimentation and to serve as the control.
The communities were exposed to periods of drying and rehydration in order to identify changes in community structure due to desiccation as well as determine which taxa were desiccation resistant. The desiccation treatments consisted of 6, 24, 168 hours and 1 month, with six replicates for each of the 6, 24, 168 hour treatments and three replicates for the 1 month 42 treatments. The control treatment remained consistently moist. The 6, 24, 168 hour treatments underwent the specified number of hours dehydration, followed by a period of rehydration. The
6 and 24 hour treatments were rehydrated for 24 hours before the next dehydration event. The
168 hour treatment was rehydrated for 168 hours. For dehydration, the tiles were moved to a dry
Petri dish and covered to allow for a slow drying process. Rehydration was accomplished by placing tiles back in a Petri dish with the Z8 medium and allowing the medium to saturate the tile. Three tiles from each sample were removed from the 6, 24, 168 hour treatments after the second week. The experiment ran for a total of four weeks. At the end of the fourth week, three tiles from each sample were removed from the control treatment and the 6, 24, 168 hour treatments. The 1 month treatment was rehydrated once and sampled after 9 days.
Samples were analyzed with an Olympus BX51 Photomicroscope with high resolution
Nomarski DIC optics. An aliquot was removed from each sample to create permanent diatom mounts in order to photo-document and identify the diatoms in each sample prior to community analysis. The diatoms were cleaned in boiling nitric acid and air dried onto cover glass.
Permanent diatom mounts were made using Naphrax mounting medium, and digital images were recorded with a camera (Spot®) attached to the microscope and a computer. An aliquot of 0.01 ml was drawn from each sample and loaded into a Palmer-Maloney nannoplankton counting chamber, and a minimum of 600 algal units were counted from each sample at 400X magnification. Algae were identified to the lowest taxonomic level possible using standard references. References consisted of: Geitler (1932), Krammer and Lange-Bertalot (1986),
Krammer and Lange-Bertalot (1988), Krammer and Lange-Bertalot (1991a), Krammer and
Lange-Bertalot (1991b), Komárek and Anagnostidis (1999), Potapova et al. (2003), Wehr and
Sheath (2003), Komárek and Anagnostidis (2005), Thomas et al. (2009), and Furey (2011). The 43 health of each identified algal cell was also recorded. Cell health was evaluated by examining the protoplasmic content. Five categories were utilized to describe the health of each cell. Cells with >90% of their normal protoplasm (sensu Cox 1996) were considered “Healthy”. A slight reduction in cell protoplasm (60-90% of normal protoplasm) was considered “Slightly
Impaired”. Cells with a moderate reduction in protoplasm (30-59% of normal protoplasm) were classified as “Moderately Impaired”. A large reduction in protoplasmic content (1-29% of normal protoplasm) was classified as “Heavily Impaired”. Cells with no protoplasmic content were classified as “Dead”.
Cell densities (cells/cm2) were calculated for each sample. Kruskal-Wallis nonparametric analysis of variance was used to examine differences in total cell density among samples. Post hoc Wilcoxon rank sum tests with Bonferroni correction were used to reveal significant differences between samples.
Algal community patterns were explored via non-metric multidimensional scaling
(NMDS) of Bray Curtis similarities of log transformed data. An analysis of similarities
(ANOSIM) was used to determine significance among the clusters identified in the NMDS ordinations. Similarity percentages analysis (SIMPER) was used to identify taxa responsible for patterns identified in NMDS.
Results
Algal communities collected from stream locations did not establish on the tiles, and thus were not included in the analysis.
Cell Density Data
Median total cell density (included all cell health categories) decreased as a result of desiccation across all three sites (Table 2A, Figure 1-3). In Site 1, there was a 50% or greater 44 decrease in median cell density across all desiccation treatments, with 83% loss in density in the
1 month treatment (Table 2B). The control did experience a decline in cell density by week 4 with a 40% loss in median total density. Change in median total cell density in each treatment was variable over time. The 6 hour treatment saw an increase in cell density from week 2 to week 4, while both the 24 hour and 168 hour treatments experienced a continued decline in cell density for the duration of the experiment (Table 2C). A significant difference in the median cell densities was detected for Site 1 (p=0.0029), however, post hoc testing did not reveal significance among any of the pairwise comparisons. The lack of significance among pairwise comparisons was due to the small sample size within each category.
There was a drastic decrease in cell density across all desiccation treatments of Site 3 with a minimum of 89% decrease in median total density (Table 2B). The control also experienced a severe decrease in cell density with a 92% decrease at 4 weeks. While the three desiccation treatments for Site 3 experienced a dramatic decline in cell density by week 2, all three treatments showed at least a doubling of the median total cell density by week 4 (Table
2C). Significance among the median total cell densities within Site 3 were identified (p=0.0467), however, but as in Site 1, there was no significance detected by the post hoc testing due to small sample size.
The desiccation treatments of Site 5 had a 74% or more decrease in median total cell density (Table 2B). Cell density also decreased in the control by 4 weeks with an 80% decline in median total density. The desiccation treatments experienced differences in the change of median total cell density over time. The 6 hour and 168 hour treatments saw an increase in cell density from week 2 to week 4, while the 24 hour treatment experienced a continued decline in cell density (Table 2C). Analysis revealed a significant difference in the median cell densities in 45
Site 5 (p=0.0218), yet because of small sample size, post hoc testing did not reveal significance among any of the pairwise comparisons.
Site 1
Twenty-five healthy taxa were considered common, occurring in >20% of the samples
(Table 3). More than half of the common taxa belonged to the Cyanophyta, and these taxa occurred with the greatest cell densities. The remaining common taxa belonged to the
Bacilliariophyta and Chlorophyta. Common taxa which showed a substantial decline in density from the establishment population included Aphanocapsa muscicola, Chroococcus texax,
Gloeocapsa atrata, Leptolyngbya cf. subtilissima, Limnothrix spp., Nostoc cf. microscopicum,
Nostoc sp. 1, and Pseudanabaena cf. minima. The cell densities for each of these taxa remained fairly constant across all desiccation treatments.
Examining the taxa from each treatment with the greatest median cell densities, the data revealed that L. cf. subtilissima – H had the highest median cell density in all samples (Table 4).
A. muscicola – H was found to have the second highest median cell density in all samples except for the 4 week – 6 hour sample. The cell densities for these two taxa had a variable response to desiccation pressure during the two week sampling period, but the cell densities did decrease with increasing desiccation pressure for the remainder of the experiment. The taxa with subsequent highest median cell densities began to vary greatly across samples.
Site 3
Seventeen healthy taxa were considered common, occurring in >20% of the samples
(Table 5). Cyanophytes comprised over half of the common taxa and occurred with the greatest densities. The remaining common taxa belonged to the Bacilliariophyta and Chlorophyta. Taxa that exhibited a large decrease in cell density from the establishment period included A. 46 minutissimum, A. muscicola, Aphanothece pallida, Unknown Cyanobacterial Filament,
Chroococcus pallidus, and L. cf. subtilissima. Cell density was fairly constant across all desiccation treatments for the taxa A. minutissimum, A. muscicola, A. pallida, Unknown
Cyanobacterial Filament, and C. pallidus. There was a doubling of cell density in two treatments for L. cf. subtilissima, the 2 week- to 4 week-6 hour treatment and the 2 week- to 4 week-24 hour treatment.
Examining the taxa from each treatment with the greatest median cell densities, the data revealed that L. cf. subtilissima – H had the highest median cell density in all samples (Table 6).
A. muscicola – H was found to have the second highest median cell density in all samples except for the 4 week – 168 hour sample. The cell densities for these two taxa had a variable response to desiccation pressure in the two week samples, but the cell densities did decrease with increasing desiccation pressure in the four week samples. The remainder of the taxa with highest median cell densities began to vary greatly across samples.
Site 5
Sixteen healthy taxa were considered common, occurring in >20% of the samples (Table
7). Over half of the common taxa were Cyanophytes which occurred with the greatest cell densities. The remaining common taxa belonged to the Bacilliariophyta. The taxa Aphanothece castagnei, Gloeothece tepidariorum, L. cf. subtilissima, Nitzschia sp. 1, N. cf. microscopicum, and Nostoc sp. 1 exhibited a substantial decrease in cell density from the establishment period.
A. muscicola exhibited a considerable decrease in cell density from the establishment period except in the two most extreme desiccation periods. The density of A. muscicola in the 4 week-
168 hour treatment was almost the same as that of the establishment period and in the 1 month treatment nearly doubled from the establishment period. 47
Examining the taxa from each treatment with the greatest median cell densities, Nostoc sp. 1 – H had the highest median cell density in all treatments except for the 4 week – 24 hour treatment (Table 8). The cell density for Nostoc sp. 1 – H increased with increasing desiccation pressure and time (except in the 4 week-24 hour treatment). N. cf. microscopicum - H had the highest median cell density in the establishment and the 4 week – 24 hour treatment. The cell density for N. cf. microscopicum - H remained fairly consistent across all treatments with slightly higher densities in the 4 week treatments compared to the 2 week treatments. The cell densities for the remaining taxa were quite variable across the samples.
Community Composition Data
Data were analyzed to determine how the relative proportion of healthy taxa in the community changed with differing degrees of desiccation pressure. Median relative abundances were calculated for the common healthy taxa, and taxa which were present in three or more samples at a relative abundance greater than 1% were considered to be dominant.
Site 1
Despite a decrease in overall cell density, the proportion of many of the dominant taxa remained constant across treatments (Table 9). Taxa that constituted a high proportion of the population in the establishment population which remained consistently high in the desiccation treatments included A. muscicola, C. tenax, L. cf. subtilissima, and Limnothrix spp.. The taxa G. atrata, P. cf. minima, and Nostoc cf. microscopicum experienced a decrease in relative abundance in the desiccation treatments from the establishment period. However, P. cf. minima did have an increase in relative abundance of 166% in the 2 week-6 hour treatment. Nostoc cf. microscopicum also experienced one instance where the relative abundance increased, an increase of 132% in the 4 week-6 hour treatment. G. tepidariorum and Leptolyngbya 48
"Albertano/Kovacik-green" experienced an increase in relative abundance in the desiccation treatments compared to the establishment population with both comprising larger proportions of the population in the 1 month treatment. A. muscicola and C. tenax also comprised more of the population in the 1 month treatment compared to the establishment population.
Site 3
The establishment population was dominated by two taxa, A. muscicola and L. cf subtilissima, contributing to nearly 75% of the overall population of healthy cells (Table 10).
The proportion of these two taxa remained consistently high in the desiccation treatments as well. A. muscicola did experience a marked increase in abundance in the 2 week-6 hour treatment (171%) compared to the establishment population.
Site 5
There was more variability in the response of the taxa from this site than the other two sites (Table 11). The proportion of Nostoc sp. 1 increased in abundance in the desiccation treatments compared to the establishment population remaining consistently high across all treatments. N. cf. microscopicum exhibited a large decrease in relative abundance due to desiccation pressure. A. castagnei was present in the establishment population and the 4 week- control as well as the 2 week-6 hour treatment population, however, it was absent from all remaining treatment populations. A. muscicola showed a variable response to desiccation, with slight increases in relative abundance in all treatments from the 2 week sampling period, absence from the 4 week- 6 hour and 4 week-24 hour treatments, and a dramatic increase in the 4 week-
168 hour (over 8-fold) and 1 month (nearly 10-fold) treatments.
49
Non-Metric Multidimensional Scaling
Site 1
The NMDS ordination revealed shifts in the algal population as it was exposed to differing periods of desiccation (Figure 4). The algal communities shifted away from the establishment population following a linear pattern along an increasing desiccation gradient.
There was also a population shift from the 2 week sampling period to the 4 week sampling period. Within these two sampling periods there still was evidence of a desiccation gradient which became stronger by the 4 week sampling period. ANOSIM indicated that there were significant differences in the desiccation periods (Global R 0.607, p=0.001). Significance could not be detected among the pairwise comparisons due to the small sample size and the high number of comparisons resulting in a low alpha once the Bonferroni correction was applied.
The overall pattern seen in the NMDS ordination was driven by the loss of cell density as desiccation pressure increased (Figure 5). However, the loss of cell density did not account for the separation between the different sampling periods. Taxa identified by the SIMPER analysis as those driving the clusters among treatments were used to create bubble plots to determine taxon specific response to desiccation pressure (plots not shown). There were no taxon specific patterns revealed by these plots.
Site 3
The NMDS ordination revealed that there was no response to differing periods of desiccation by the algal population (Figure 6). The communities did shift away from the establishment community; however, there were no patterns for any of the treatments. This linear shift away from the establishment population followed a gradient of decreasing total cell density (Figure 7). 50
Site 5
The NMDS ordination did not reveal a strong response in the algal population as it was exposed to differing periods of desiccation (Figure 8). There was a shift in the control population away from the establishment period. The desiccation populations also shifted away from the establishment population. The 6 hour treatment showed a population shift and a tighter clustering pattern from the 2 week sampling to the 4 week sampling. The 24 hour treatment showed a similar pattern to that of the 6 hour treatment with population shifts in a different direction. There was no pattern detected for the 168 hour treatments from either sampling period. ANOSIM indicated that there were significant differences in the desiccation periods
(Global R 0.434, p=0.001). As in Site 1, significance could not be detected among the pairwise comparisons due to the small sample size and the high number of comparisons.
The overall pattern seen in the NMDS ordination was driven by an increasing loss of cell density (Figure 9). However, cell density did not decrease with increasing desiccation pressure.
Bubble plots created from the SIMPER analysis did not reveal any taxon specific patterns for this community (plots not shown).
Discussion
The pseudoaerial algal communities were dominated by cyanobacteria comprising the majority of the common taxa for all three sites. Cyanobacteria typically dominate communities of aerial habitats which can be attributed to their tolerance of wide ranges in moisture availability
(Whitton and Potts 2000; Matthes-Sears 1999; Alfinito et al. 1998; Broady 1989). In addition to wide tolerances to moisture availability, cyanobacteria have been shown to survive desiccation and recover more quickly from desiccation than other algae (De Winder et al. 1989).
Extracellular mucilage produced by many cyanobacteria protects the cells during periods of 51 desiccation by storing water and reducing osmotic stress on the cells (Gerrath 2003; Potts 1999;
Shepard 1987). Many of the dominant cyanobacterial taxa from all three sites, including the taxa with the highest cell densities, produce extracellular mucilage.
The exposure of aerial algal communities to periods of desiccation led to a decrease in overall cell density. However, there was not a consistent decline in total density with increasing desiccation pressure (Table 2, Figures 1-3). Cell densities fluctuated across desiccation treatments and over time. Some populations experienced an increase in cell density from the two week sampling period to the four week sampling period for a particular treatment (i.e., 6 hour treatment from all three sites) which could be evidence of an acclimation to the desiccation pressure by the algal community. A community may undergo an initial period of cell loss as a response to the initial exposure to changes in moisture availability, but over time the community may begin to stabilize.
As with total cell density, the species level response to desiccation was more variable during the two week sampling period, and often the 6 hour treatment experienced the greatest decline in density. By the four week sampling period, taxa typically exhibited the expected response of decreasing density with increasing desiccation pressure (i.e., L. cf. subtilissima and
A. muscicola in Site 1). Many taxa also exhibited an increase in cell density in a particular treatment from the two week to the four week sampling period. This again may indicate an acclimation to the new moisture regime by these species.
The taxa that contributed to the greatest cell densities in these algal communities did not vary due to desiccation (Tables 4, 6, 8). There was a loss of cell density for these taxa from desiccation, but the taxa that were most abundant in the community before desiccation remained the most abundant once exposed to desiccation. The algal populations used in this experiment 52 were composite samples from each site which included microhabitats with varying amounts of water. However, the populations that formed on the tiles received only moisture from the saturated tiles and the humidity within the Petri dishes. Consequently, the taxa adapted to survive in low moisture situations were most likely to establish the communities used for this experiment. This is evident in the relatively high numbers of heavily impaired and dead diatoms in the establishment population of Site 3 and Site 5 (Tables 6, 8). Despite the fact that diatoms have been shown to have adaptations against desiccation, diatoms typically prefer wet habitats
(Van de Vijver et al. 2008). Stream diatoms have been shown to have a low tolerance to desiccation (Mosisch 2001; Peterson 1987), and as moisture levels decrease in aerial habitats, the diversity and abundance of aerial diatoms have been found to decrease (Beyens 1989; Ohtani
1986). Healthy diatoms were still present in the desiccated communities (Tables 3, 5, 7) possibly taking refuge in the extracellular mucilage produced by the cyanobacteria which dominated the communities.
There were taxa shared between the different algal populations, and the response of the shared taxa to desiccation was not always consistent. For example, the taxon A. muscicola was present in all three sites, but the response to desiccation was variable (Tables 3, 5, 7). In Site 1 and 3, there was a decrease in cell density with increasing desiccation pressure and time (except for large decrease in density for the 2 week-6 hour treatment in Site 1). For site 5, the density did decrease, however, in the two most extreme desiccation periods, 4 week-168 hour and 1 month, the density increased with a higher density in the 1 month treatment than the establishment. Variable responses by the same taxa in different populations lend support to the idea that response to desiccation is more of a community level response than an individual 53 species response. The response of a particular species to desiccation may depend upon the composition of the community and the manner in which the other species respond.
The NMDS ordinations for each site revealed different responses to desiccation from each algal population. The algal population from Site 1 experienced a population shift along a gradient of increasing desiccation pressure. There was a community shift in the population from
Site 3, but there was no difference in the response to different desiccation periods. The population from Site 5 did exhibit community shifts in response to different desiccation periods, however, there were different responses from the community to the different periods of desiccation. These results indicate that the response to desiccation can be highly variable in different algal communities and the same community can potentially have different reactions to different amounts of desiccation pressure.
In the natural environment, not all aerial habitats experience a predictable desiccation pattern. This unpredictability can lead to algal communities that are in a state of constant flux.
The instability of the algal community can allow for less dominant taxa to take hold within the community. This can also allow for new taxa to colonize the community which otherwise would not be able to compete within the community.
54
CONCLUSIONS AND FUTURE DIRECTIONS
The goal of this dissertation was to explore factors structuring algal communities in aerial habitats and investigate adaptations to this environment. The ecology of aerial algal communities has received little attention, thus leaving major gaps in the understanding of these communities. The results from the compilation of work in this dissertation have begun to shed some light onto the ecological aspects of these communities. Two major hypotheses on aerial algae have come from the limited ecological research; first, moisture plays an important role in structuring these communities (Casamatta et al. 2002; Beyens 1989; Camburn 1983), and second, aerial diatoms are smaller than aquatic diatoms due to the extreme nature of aerial habitats (Patrick 1977; Round 1957). In this dissertation, the role of moisture in structuring aerial algal communities was not found to fully support findings in the literature. In both
Chapter 2 and Chapter 3, there was not a clear relationship between moisture availability and algal community composition in natural aerial habitats. There was a relationship between moisture availability and the algal division present. In the driest sites, aerial algal communities were dominated by cyanobacteria, and as moisture levels increased, the abundance of diatoms and green algae also increased. The dominance of cyanobacteria in the driest sites can be attributed to their ability to survive periods of desiccation and quickly recover from desiccation
(De Winder et al. 1989). In Chapter 4, algal community composition did not change once communities were exposed to different periods of desiccation in a laboratory experiment. These communities experienced a loss in cell density due to desiccation, however, taxa that were dominant in the establishment populations remained dominate in the desiccated communities.
Aerial diatoms were not found to be smaller than aquatic diatoms contradicting findings in the literature. In Chapter 1, adaptations to the aerial environment were examined in diatoms 55 from aerial communities in the GSMNP. Reduced size of aerial diatoms was not supported by the data, with aerial diatoms being longer than had been previously shown in the literature.
Aquatic populations from the GSMNP were found to be dominated by small diatoms, such as
Achnanthidium minutissimum and Rossithidium pusillum, while aerial communities were dominated by moderate sized diatoms including Cymbella gracilis and Eunotia bigibba. A reduction in the amount of open area on the valve face as an adaptation against desiccation was also investigated in Chapter 1. Diatoms from aerial habitats were found to have proportionally less open area on the valve face compared to aquatic diatoms. The reduction in open area on the valve face provides an advantage to cells by provide protection against the osmotic stress encountered during periods of drying.
Environmental factors such as nutrient availability and UV-levels were not examined in any of the study areas. Nutrient availability may play a role in shaping the communities composition of aerial algae due to possible nutrient limitation in these habitats (Johansen 1999).
As moisture levels vary with aerial habitats, nutrient levels should also vary. Comparing nutrient levels among aerial habitats and monitoring fluctuations in nutrient availabilities within habitats will help clarify the role nutrients play in structuring these algal communities. Due to the exposure to high levels of solar radiation in many aerial habitats, UV-levels are also an important factor to consider. Aerial algal communities exposed to high levels of solar radiation must have mechanisms, such as the production of photoprotective pigments, to protect their cells. Certain species may be excluded from aerial habitats that receive high levels of solar radiation. These and other environmental variables will vary seasonally within each aerial habitat, possibly causing seasonal shifts in the community composition. Monitoring aerial habitats throughout an entire season, both the algal community and the environmental variables, can also help explain 56 how the environment shapes these communities. Additional aspects of aerial algal communities such as interspecies interactions and species positioning within algal mats also need to be explored in more detail. Non-mucilage producing algae may rely upon species that produce large amounts of mucilage to provide protection against desiccation. These associations may be found to be species specific or indiscriminate associations. Furthermore, examining species positioning within the algal mat may help to explain how the community survives periods of desiccation. Investigating these factors may provide additional insight into patterns seen in aerial algal communities.
57
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64 TABLES
Chapter I 65
Table 1. Site information for aerial and aquatic samples collected from the Great Smoky Mountains National Park including site identification number, location, habitat type, microhabitat type, pH, GPS coordinates, light level (µmol m-2s-1) (* indicates average value of light levels measured at different times of day), aspect, sponge weight change (g), and moisture category; Light, aspect, sponge weight change and moisture category were recorded only from aerial habitats.
Sponge Weight GPS Light (µmol Change Moisture Site ID Location Habitat Microhabitat pH Coordinates m-2s-1) Aspect (g) Category Newfound Gap N 35.520° 07062901 Road Aerial Bryophyte 5 W 83.308° 010 59° NE 0.01 1 Newfound Gap N 35.578° 07062903 Road Aerial Epilithon 4.7 W 83.346° 022* 76° E 0.6 3 Newfound Gap N 35.578° 07062904 Road Aerial Epilithon 4.7 W 83.346° 015* 114° E 0.18 2 Road to Clingmans N 35.563° 07062913 Dome Aerial Bryophyte 4.7 W 83.494° 923* 78° E 3.5 4 Road to Clingmans N 35.563° 07062914 Dome Aerial Epilithon 4.3 W 83.494° 715* 107° E 5.86 4 N 35.637° 07070101 Whiteoak Sink Aerial Bryophyte 7.5 W 83.748° 004* 202° S 0.05 1 N 35.627° 07070107 Whiteoak Sink Aerial Epilithon 7.4 W 83.745° 001 298° W 0.59 3 N 35.627° 07070108 Whiteoak Sink Aerial Epilithon 7.4 W 83.745° 001 298° W 0.57 3 Schoolhouse N 35.627° 07070109 Gap Trail Aerial Bryophyte 4 W 83.728° 005 179° S 0.01 1 66
Sponge Weight GPS Light (µmol Change Moisture Site ID Location Habitat Microhabitat pH Coordinates m-2s-1) Aspect (g) Category N 35.660° 312° 07070114 Meigs Falls Aerial Bryophyte 5.8 W 83.660° 003 NW 0.02 1 N 35.660° 326° 07070115 Meigs Falls Aerial Epilithon 6.1 W 83.660° 003 NW 0.29 2 Juney Wank N 35.466° 07070301 Falls Aerial Bryophyte 5 W 83.435° 003 120° SE 0.48 2 Tom Branch N 35.467°W 07070302 Falls Aerial Bryophyte 5.3 83.430° 004* 298° W 0.87 3 Indian Creek N 35.473° 07070303 Falls Aerial Bryophyte 4.7 W 83.428° 018* 101° E 0.13 2 Indian Creek N 35.473° 07070304 Falls Aerial Epilithon 4.7 W 83.429° 018* 94° E 0.02 1 Little Creek N 35.506° 07070305 Falls Aerial Bryophyte 5 W 83.456° 014* 152° SE 0.34 2 Road to N 35.454° 07070403 Nowhere Aerial Epilithon 5.5 W 83.482° 028* 282° W 0.84 3 Road to N 35.454° 07070404 Nowhere Aerial Bryophyte 4.7 W 83.483° 112* 282° W 2.22 4 Road to N 35.456° 212° 07070407 Nowhere Aerial Epilithon 3 W 83.493° 445* SW 0.6 3 Road to N 35.456° 07070408 Nowhere Aerial Bryophyte 3.9 W 83.493° 464* 269° W 0.47 2 Road to N 35.457° 218° 07070410 Nowhere Aerial Epilithon 3.9 W 83.509° 135* SW 1.16 4 67
Sponge Weight GPS Light (µmol Change Moisture Site ID Location Habitat Microhabitat pH Coordinates m-2s-1) Aspect (g) Category Road to N 35.455° 07070412 Nowhere Aerial Bryophyte 3.9 W 83.525° 178* 21° N 0.52 3 N 35.677° 07070503 Laurel Falls Aerial Bryophyte 3.9 W 83.593° 004* 186° S 0.09 1 N 35.677° 07070504 Laurel Falls Aerial Epilithon 4.7 W 83.593° 005* 271° W 0.96 3 Spruce Flats N 35.634° 07070505 Falls Aerial Bryophyte 5 W 83.682° 002* 281° W 0.39 2 Spruce Flats N 35.634° 07070506 Falls Aerial Epilithon 6.5 W 83.683° 010* 281° W 0.53 3 Indian Flats N 35.592° 07070508 Falls Aerial Bryophyte 4.5 W 83.633° 003* 30° NE 7.66 4 Newfound Gap N 35.639° 238° 07070806 Road Aerial Epilithon 5 W 83.474° 150* SW 0.83 3 Newfound Gap N 35.639° 07070807 Road Aerial Bryophyte 5.3 W 83.474° 085* 283° W 5.11 4 Newfound Gap N 35.644° 07070808 Road Aerial Epilithon 5 W 83.508° 018* 44° NE 0.58 3 N 35.620° 07070901 Ft Harry Falls Aerial Epilithon 4.7 W 83.471° 002* 255° W 10.58 4 N 35.620° 238° 07070903 Ft Harry Falls Aerial Epilithon 4.7 W 83.471° 008* SW 0.38 2 N 35.620° 07070904 Ft Harry Falls Aerial Bryophyte 3.9 W 83.471° 009* 348° N 0.66 3 68
Sponge Weight GPS Light (µmol Change Moisture Site ID Location Habitat Microhabitat pH Coordinates m-2s-1) Aspect (g) Category N 35.620° 314° 07070905 Ft Harry Falls Aerial Epilithon 4.7 W 83.471° 103* NW 0.4 2 N 35.620° 07070906 Ft Harry Falls Aerial Bryophyte 4.7 W 83.471° 006* 74° E 1.79 4 N 35.639° 07071201 Alum Cave Trail Aerial Bryophyte 3.9 W 83.444° 002* 274° W 0.14 2 N 35.639° 07071202 Alum Cave Trail Aerial Epilithon 3.6 W 83.444° 239* 144° SE 0.23 2 N 35.647° 07071203 Alum Cave Trail Aerial Epilithon 3.6 W 83.439° 009* 132° SE 0.37 2 N 35.651°W 07071205 Alum Cave Trail Aerial Bryophyte 3.9 83.436° 066* 128° SE 4.66 4 N 35.651° 07071207 Alum Cave Trail Aerial Epilithon 3.9 W 83.437° 097* 131° SE 0.95 3
Twentymile N 35.467° - - - - GSM 10/15/03-1C Creek Aquatic Epilithon 4.7 W 83.878°
Twentymile N 35.467° - - - - GSM 10/15/03-1E Creek Aquatic Epilithon 4.7 W 83.878°
N 35.473° - - - - GSM 10/16/03-8 Hazel Creek Aquatic Epilithon 4.7 W 83.721°
Cooper Road N 35.616° - - - - GSM 5/16/04-7 Trail Aquatic Epilithon 5 W 83.928°
N 35.448° - - - - GSM 10/22/04-J2A Pilkey Creek Aquatic Epilithon 4.7 W 83.666° 69
Sponge Weight GPS Light (µmol Change Moisture Site ID Location Habitat Microhabitat pH Coordinates m-2s-1) Aspect (g) Category
N 35.610° - - - - GSM 5/16/05-J4C Abrams Creek Aquatic Epilithon 6.8 W 83.931°
Toms Creek N 35.764° - - - - GSM 5/17/05-J4C Tributary Aquatic Epilithon 4.7 W 83.192°
Little Pigeon N 35.728° - - - - GSM 6/13/05-2B River Aquatic Epilithon 5.3 W 83.406°
Mouth of N 35.555° - - - - GSM 8/1/05-1 Abrams Creek Aquatic Epilithon 5.7 W 83.998°
Lower Tabcat N 35.524° - - - - GSM 8/1/05-3 Creek Aquatic Epilithon 5.5 W 83.993°
GSM 5/19/04- N 35.707° - - - - PF2A Ramsay Prong Aquatic Bryophyte 5 W 83.324°
Little Pigeon N 35.720°W - - - - GSM 6/13/05-4A River Aquatic Bryophyte 5.5 83.389°
N 35.570° - - - - GSM 6/15/05-6A Bradley Fork Aquatic Bryophyte 5.5 W 83.310°
N 35.707° - - - - GSM 6/17/05-J5 Camel Gap Trail Aquatic Bryophyte 5.3 W 83.324°
N 35.610° - - - - GSM 7/6/05-3 Kephart Prong Aquatic Bryophyte 4.9 W 83.369°
N 35.603° - - - - GSM 7/8/05-3 Snake Branch Aquatic Bryophyte 5 W 83.100°
N 35.674° - - - - GSM 7/11/05-2 Little River Aquatic Bryophyte 5 W 83.658° 70
Sponge Weight GPS Light (µmol Change Moisture Site ID Location Habitat Microhabitat pH Coordinates m-2s-1) Aspect (g) Category
N 35.662° - - - - GSM 7/11/05-7 Meigs Creek Aquatic Bryophyte 4.8 W 83.661°
N 35.622° - - - - GSM 7/27/05-L2 Pinkroot Branch Aquatic Bryophyte 5.6 W 83.744°
Maddron Bald N 35.730° - - - - GSM 8/10/05-9 Trail Aquatic Bryophyte 3.9 W 83.247°
71
Table 2. Aerial taxa with the highest relative abundances with the range in length measured for each taxon.
Relative Length Range Abundance (µm) Achnanthidium minutissimum 8.52 5.22-17.06 Cymbella gracilis 14.77 15.32-34.38 Diadesmis contenta (Grunow ex Van Heurck) Mann in Round, Crawford & Mann 4.07 5.00-24.80 Diadesmis perpusilla (Grunow) Mann in Round, Crawford & Mann 4.64 10.77-15.69 Diatoma mesodon Kützing 2.35 11.12-20.15 Diploneis boldtiana Cleve 2.03 14.89-25.16 Eunotia bigibba 8.27 11.96-40.64 Eunotia paludosa var. paludosa Grunow 5.11 11.38-55.73 Eunotia subarcuatoides Alles, Norpel & Lange-Bertalot 4.20 12.15-55.80 Eunotia tenella (Grunow) Hustedt 3.06 8.07-48.70 Nupela lapidosa (Krasske) H. Lange-Bertalot 3.85 9.41-24.32
72
Table 3. Taxa occurring with >1% relative abundance in populations from aerial habitats with differing moisture availabilities (1=dry, 2=damp, 3=wet, 4=very wet).
Moisture Category 1 Moisture Category 2 Moisture Category 3 Moisture Category 4 Rel. Rel. Rel. Rel. Species Abun. Species Abun. Species Abun. Species Abun. Eunotia paludosa var. paludosa 23.99 Cymbella gracilis 17.99 Cymbella gracilis 31.25 Eunotia subarcuatoides 20.54 Achnanthidium Diadesmis contenta 17.66 Eunotia bigibba 16.15 minutissimum 9.07 Eunotia bigibba 17.49 Achnanthidium Achnanthidium Diadesmis perpusilla 16.97 minutissimum 8.25 Nupela lapidosa 8.41 minutissimum 16.93 Adlafia bryophila Fragilaria capucina var. (Petersen) Moser, Lange- perminuta (Grunow) Bertalot & Metzeltin 7.91 Diploneis boldtiana 6.86 Eunotia tenella 6.45 Lange-Bertalot 6.65 Eunotia curtagrunowii Nörpel-Schempp & Lange- Bertalot 6.36 Diatoma mesodon 6.83 Nitzschia sp.2 3.92 Eunotia tenella 5.64 Diadesmis virginiana Diatomella balforiana Lange-Bertalot 3.59 Greville 3.26 Eunotia minor 3.74 Nupela lapidosa 4.16 Achnanthes coarctata Frustulia rhomboides (Brébisson ex W. Smith) var. saxonica Fragilaria capucina Eunotia papilioforma Grunow 3.28 (Rabenhorst) De Toni 3.20 var. gracilis 2.77 Furey, Johansen & Lowe 3.88 Eunotia rhomboidea Navicula keeleyi Patrick 2.20 Hustedt 2.91 Caloneis undulata 2.59 Eunotia incisa 3.00 Psammothidium marginulatum (Grunow) Nupela neglecta Ponader, Eunotia minor Bukhtiyarova et Lowe & Potapova 1.85 (Kützing) Grunow 2.59 Round 2.51 Fragilaria virescens 2.52 Orthoseira roeseana Brachysira brebissonii Navicula (Rabenhorst) O'Meara 1.81 R. Ross 1.95 cryptocephala Kützing 2.40 Meridion circulare 2.44 Eunotia musicola var. Eunotia cf. compacta tridentula Nörpel & Hustedt 1.66 Navicula sp.4 1.81 Lange-Bertalot 2.32 73
Moisture Category 1 Moisture Category 2 Moisture Category 3 Moisture Category 4 Rel. Rel. Rel. Rel. Species Abun. Species Abun. Species Abun. Species Abun. Diadesmis cf. gallica var. gallica 1.54 Nitzschia sp.2 1.79 Diadesmis perpusilla 2.17 Navicula angusta 1.84 Caloneis tenuis (Gregory) Krammer in Krammer & Eunotia incisa Eunotia exigua Lange-Bertalot 1.47 Diadesmis perpusilla 1.73 Gregory 1.67 (Brébisson) Rabenhorst 1.72 Pinnularia borealis Melosira dickiei Ehrenberg 1.43 Nupela lapidosa 1.55 (Thwaites) Kützing 1.49 Diatoma mesodon 1.64 Achnanthidium exiguum (Grunow) Cymbella minuta Hilse 1.04 Eunotia valida Hustedt 1.36 Czarnecki 1.41 Fragilaria sp.1 1.56 Tabellaria flocculosa Nitzschia sp.1 1.04 (Roth) Kützing 1.31 Navicula keeleyi 1.41 Eunotia sp.17 1.52 Fragilaria capucina var. gracilis (Østrup) Hustedt 1.28 Nitzschia sp.4 1.20 Meridion circulare Eunotia varioundulata (Greville) Agardh 1.28 Nörpel-Schempp 1.18 Fragilaria capucina var. rumpens Gomphonema mehleri (Kützing) Lange- Camburn 1.23 Bertalot 1.05 Encyonema silesiacum (Bleisch in Rabenhorst) Mann 1.17 Navicula angusta Grunow 1.17
74
Table 4. Aquatic taxa with the highest relative abundances with the range in length measured for each taxon.
Relative Abundance Length Range (µm) Achnanthidium minutissimum 14.59 5.93-20.85 Diatoma mesodon 3.08 10.45-20.88 Eolimna minima (Grunow) Lange-Bertalot 6.89 6.24-13.31 Eunotia incisa 6.25 10.60-43.92 Fragilaria capucina var. gracilis 2.76 28.03-48.43 Meridion circulare 2.64 13.26-48.78 Navicula cryptotenella Lange-Bertalot in Krammer & Lange-Bertalot 2.12 19.32-35.84 Nupela lapidosa 3.87 8.50-25.86 Planothidium lanceolatum (Brébisson ex Kützing) Lange-Bertalot 6.02 8.50-26.75 Rossothidium pusillum 11.11 5.38-21.89
75
Table 5. Median, maximum, and minimum lengths of diatom communities from both aerial and aquatic populations; * indicates significance
Aerial Aquatic Median Length (µm) 19.11 16.15 p<0.0001* Maximum Length (µm) 82.65 112.42 Minimum Length (µm) 5 5.38
76
Table 6. Median lengths of taxa shared between aerial and aquatic habitats, and median lengths of taxa unique to aerial and aquatic habitats; * indicates significance
Shared Taxa Unique Taxa Habitat Median Length (µm) Median Length (µm) Aerial 19.10 18.95 Aquatic 15.24 20.74
p-value <0.0001* 0.0227*
77
Table 7. Median lengths for taxa present in both aerial and aquatic habitats; * indicates significance.
Taxa Aerial Aquatic p-value Median Length (µm) Median Length (µm) Achnanthidium minutissimum 10.61 11.25 0.0080* Diadesmis contenta 9.2 10.37 0.0093* Navicula keeleyi 15.2 15.2 0.6402 Diatoma mesodon 13.09 13.61 0.1573 Eunotia exigua 11.8 12.13 0.3324 Eunotia incisa 17.19 19.495 0.0286* Eunotia minor 35.43 24.19 0.0013* Eunotia papilioforma 23.52 24.445 0.3606 Fragilaria capucina var. gracilis 22.62 38.495 <0.0001* Frustulia rhomboides var. saxonica 43.425 54.79 0.0002* Meridion circulare 26.56 27.815 0.9275 Navicula angusta 41.135 40.57 0.865 Nupela lapidosa 15.295 20.19 <0.0001*
78
Table 8. Median, maximum, and minimum cell lengths of diatoms from aerial habitats with different moisture availabilities (1=dry, 2=damp, 3=wet, 4=very wet).
Median Cell Length Maximum Cell Minimum Cell Moisture Category (µm) Length (µm) Length (µm) 1 17.15 64.94 5.00 2 19.39 58.2 6.05 3 19.74 82.65 6.03 4 20.1 65.27 5.22
79
Table 9. Pairwise Wilcoxon rank sum tests of cell length between diatom populations from different moisture categories; * indicates significance (Bonferroni correction factor α = 0.0125 used for pairwise comparisons).
Pairwise Comparisons p-Value 1, 2 <0.0001* 1, 3 <0.0001* 1, 4 <0.0001* 2, 3 0.3515 2, 4 0.204 3, 4 0.023
80
Table 10. Median lengths in each moisture category (1=dry, 2=damp, 3=wet, 4=very wet) for taxa with the highest relative abundances in the aerial habitats; Kruskal-Wallis nonparametric analysis of variance result with post hoc pairwise Wilcoxon rank sum tests for taxa occurring in three or more moisture categories, Wilcoxon rank sum test for taxa occurring in only two moisture categories; * indicates significance (Bonferroni correction factor α = 0.0167used for post hoc pairwise comparisons).
Achnanthidium Cymbella Diadesmis Diadesmis Diatoma Eunotia Eunotia Nupela minutissimum gracilis contenta perpusilla mesodon bigibba tenella lapidosa Median Median Median Length Median Median Length Median Median Length Median Moisture Category (µm) Length (µm) Length (µm) (µm) Length (µm) Length (µm) (µm) Length (µm) 1 10.57 13.2 2 12.14 19.62 10.66 12.73 12.96 19.5 19.48 3 10.03 21.98 8.93 11.34 13.07 14.30 4 10.50 15.24 23.27 15.04 17.71 Kruskal-Wallis / Wilcoxon Rank Sum 0.0010* <0.0001* <0.0001* 0.0012* 0.0003* 0.0210*
Post hoc Wilcoxon Rank Sum Pairwise Comparisons 1, 2 0.2945 1, 3 <0.0001* 2, 3 0.0005* 0.0002* 2, 4 0.0026* 3, 4 0.5064
81
Table 11. Median, maximum, and minimum biovolumes for both aerial and aquatic populations; * indicates significance.
Aerial Aquatic Median Biovolume (µm3) 164.13 141.75 p<0.0001* Maximum Biovolume (µm3) 21135.81 16599.27 Minimum Biovolume (µm3) 9.15 9.70
82
Table 12. Median biovolumes of taxa shared between aerial and aquatic habitats, and median biovolumes of taxa unique to aerial and aquatic habitats; * indicates significance.
Shared Taxa Unique Taxa Habitat Median Biovolume (µm3) Median Biovolume (µm3) Aerial 164.69 162.51 Aquatic 137.93 143.62
p-value <0.0001* 0.0630
83
Table 13. Median biovolumes for taxa present in both aerial and aquatic habitats; * indicates significance.
Taxa Aerial Aquatic p-value Median Length (µm) Median Length (µm) Achnanthidium minutissimum 34.16 36.62 0.0109* Diadesmis contenta 48.24 60.92 0.0065* Navicula keeleyi 169.96 205.04 0.4361 Diatoma mesodon 611.92 725.99 0.0316* Eunotia exigua 47.25 53.96 0.1758 Eunotia incisa 282.44 369.5 0.0048* Eunotia minor 921.73 763.28 0.0964 Eunotia papilioforma 726.9878 650.0545 0.1677 Fragilaria capucina var. gracilis 71.92 184.52 <0.0001* Frustulia rhomboides var. saxonica 974.34 2141.14 <0.0001* Meridion circulare 234.18 334.52 0.1836 Navicula angusta 555.17 632.74 0.2187 Nupela lapidosa 190.28 288.65 <0.0001*
84
Table 14. Median, maximum, and minimum biovolumes of diatoms from aerial habitats with different moisture availabilities (1=dry, 2=damp, 3=wet, 4=very wet).
Moisture Median Biovolume Maximum Biovolume Minimum Category (µm3) (µm3) Biovolume (µm3) 1 113.74 15234.06 13.74 2 237.66 21135.81 9.15 3 149.84 18253.56 15.06 4 239.31 7772.14 12.37
85
Table 15. Pairwise Wilcoxon rank sum tests of biovolume between different moisture categories; * indicates significance (Bonferroni correction factor α = 0.0125 used for pairwise comparisons).
Pairwise Comparisons p-Value 1, 2 <.0001* 1, 3 0.0041* 1, 4 <.0001* 2, 3 <.0001* 2, 4 0.2642 3, 4 <.0001*
86
Table 16. Median biovolumes in each moisture category (1=dry, 2=damp, 3=wet, 4=very wet) for taxa with the highest relative abundances in the aerial habitats; Kruskal-Wallis nonparametric analysis of variance result with post hoc pairwise Wilcoxon rank sum tests for taxa occurring in three or more moisture categories, Wilcoxon rank sum test for taxa occurring in only two moisture categories; * indicates significance (Bonferroni correction factor α = 0.0167used for post hoc pairwise comparisons).
Achnanthidium Cymbella Diadesmis Diadesmis Diatoma Eunotia Eunotia Nupela minutissimum gracilis contenta perpusilla mesodon bigibba tenella lapidosa Median Median Median Median Median Median Median Median Moisture Biovolume Biovolume Biovolume Biovolume Biovolume Biovolume Biovolume Biovolume Category (µm3) (µm3) (µm3) (µm3) (µm3) (µm3) (µm3) (µm3) 1 46.64 162.51 2 37.54 140.81 77.69 155.62 574.97 460.82 355.07 3 25.85 175.35 33.80 113.11 53.86 148.49 4 38.06 904.05 605.18 65.56 270.75 Kruskal-Wallis / Wilcoxon Rank Sum <0.0001* <0.0001* <0.0001* <0.0001* 0.0180* <0.0001* 0.0129*
Post hoc Wilcoxon Rank Sum Pairwise Comparisons 1, 2 0.0033* 0.4393 1, 3 0.0010* <0.0001* 2, 3 0.0002* 0.0058* <0.0001* 2, 4 0.6356 3, 4 0.0002*
87
Table 17. Median percent areolar area of diatoms from aerial habitats with different moisture availabilities (1=dry, 2=damp, 3=wet, 4=very wet).
Moisture Median Percent Category Areolar Area 1 2.44 2 0.52 3 0.66 4 0.81
88
Table 18. Pairwise Wilcoxon rank sum tests of percent open area between different moisture categories; * indicates significance (Bonferroni correction factor α = 0.0125 used for pairwise comparisons).
Pairwise Comparisons p-Value 1, 2 <.0001* 1, 3 <.0001* 1, 4 <.0001* 2, 3 0.5816 2, 4 0.739 3, 4 0.5558
89
Table 19. List of common species frequently encountered in bryophytic samples. A species was considered common if it occurred in >20% of the samples.
Percent of Sites Mean Relative Taxon Present Abundance Achnanthidium exiguum 20 0.51 Achnanthidium minutissimum 40 5.16 Adlafia bryophila 20 3.03 Caloneis bacillum (Grunow) Cleve 35 0.41 Chamaepinnularia mediocris (Krasske) Lange-Bertalot 25 0.83 Naviucla keeleyi 30 1.74 Diadesmis contenta 50 5.41 Diadesmis perpusilla 20 3.61 Eolimna minima (Grunow in Van Heurck) H. Lange- Bertalot 25 0.56 Eunotia bigibba 30 5.30 Eunotia exigua 30 1.88 Eunotia paludosa var. paludosa 25 7.66 Eunotia tenella 25 5.03 Eunotia varioundulata 20 0.95 Frustulia rhomboides var. saxonica 40 7.26 Gomphonema parvulum morphotype 2 Kützing sensu Thomas et al. 20 0.28 Meridion circulare 20 1.00 Microcostatus krasskei (Hustedt) J.R. Johansen & J.C. Sray 35 1.67 Navicula angusta 35 0.66 Nitzschia sp. 1 25 0.69 Nupela lapidosa 35 3.67 Nupela neglecta 30 2.54 Orthoseira roeseana 35 0.78 Pinnularia subcapitata Gregory 20 0.71 Planothidium lanceolata 25 0.51 Psammothidium subatomoides (Hustedt) Bukhtiyarova 20 0.08
90
Table 20. List of common species frequently encountered in epilithic samples. A species was considered common if it occurred in >20% of the samples.
Percent of Sites Mean Relative Taxon Present Abundance Achnanthidium minutissimum 70 8.61 Adlafia bryophila 20 0.10 Chamaepinnularia mediocris 20 0.99 Cocconeis placentula Ehrenberg 20 0.15 Cymbella gracilis 30 10.98 Diadesmis contenta 35 0.81 Diadesmis perpusilla 30 1.42 Diatoma mesodon 20 0.08 Encyonema perpusillum 20 8.60 Encyonema silesiacum 20 0.31 Eunotia minor 20 1.24 Eunotia paludosa var. paludosa 30 1.45 Fragilaria capucina var. gracilis 25 1.69 Frustulia rhomboides var. crassinervia (Brébisson) Ross 25 0.30 Frustulia rhomboides var. saxonica 45 7.66 Gomphonema montanum 20 0.38 Gomphonema parvulum morphotype 1 Kützing sensu Thomas et al. 30 0.36 Gomphonema parvulum morphotype 2 20 0.23 Gomphonema sp. 4 20 0.07 Meridion circulare 20 0.17 Navicula angusta 50 0.78 Nitzschia sp. 1 25 0.51 Nitzschia sp. 2 30 3.41 Nupela lapidosa 35 0.43 Planothidium lanceolata 20 0.16 Psammothidium marginulata 25 0.77
91 TABLES
Chapter II
92
Table 1. Taxa list for the two regions Lake Superior (LSR) and Great Smoky Mountains National Park (GSMNP); an “X” indicates presence of taxon in region.
Taxa LSR GSMNP
Achnanthes coarctata (Brébisson ex W. Smith) Grunow in Cleve & Grunow X X Achnanthidium minutissimum (Kützing) Czarnecki X X Achnanthidium biasolettianum (Grunow in Cleve & Grunow) Round & Bukhtiyarova X Achnanthidium sp.5 X Amphora coffeaeformis (Agardh) Kützing X Amphora pediculus (Kützing) Grunow in Schmidt et al. X Aphanocapsa cf. fusco-lutea Hansgirg X X Aphanocapsa muscicola (Meneghini) Wille X X Aphanocapsa sp.1 X X Aphanocapsa sp.2 X Aphanocapsa sp.3 X Aphanocapsa sp.4 X Aphanocapsa sp.5 X Aphanocapsa sp.6 X Aphanothece castagnei (Brébisson) Rabenhorst X Aphanothece cf. pallida (Kutzing) Rabenhorst X Aphanothece pallida (Kutzing) Rabenhorst X Aphanothece sp.1 X Aphanothece sp.2 X Aphanothece sp.3 X Aphanothece sp.4 X Brachysira brebissonii R. Ross in Hartley X Brachysira sp.1 X Brachysira vitrea (Grunow) R. Ross in Hartley X Caloneis bacillum (Grunow) Cleve X X Caloneis cf. silicula (Ehrenberg) Cleve X Caloneis sp.5 X Caloneis undulata (Gregory) Krammer in Krammer & Lange-Bertalot X Calothrix sp.1 X X Calothrix sp.2 X X Calothrix sp.3 X X Calothrix sp.4 X Calothrix sp.5 X Calothrix sp.6 X 93
Taxa LSR GSMNP
Cavinula lapidosa (Krasske) Lange-Bertalot in Lange-Bertalot & Metzeltin X X cf. Euglena sp. X cf. Microspora sp. X cf. Spondylosium sp. X Chamaepinnularia sp.1 X X Chroococcus cf. varius A. Braun in Rabenhorst X Chroococcus cohaerens (Brébisson) Nägeli X Chroococcus helveticus Nägeli X X Chroococcus pallidus (Nägeli) Nägeli X X Chroococcus sp.1 X Chroococcus sp.2 X Chroococcus sp.3 X Chroococcus sp.4 X X Chroococcus sp.5 X Chroococcus turicensis (Nägeli) Hansgirg X Chroococcus varius A. Braun in Rabenhorst X X Cladophora sp.1 X X Closterium cf. exile West & G.S.West X Closterium sp.2 X Cocconeis placentula Ehrenberg X Cosmarium abbreviatum Raciborski X Cosmarium caelatum Ralfs X Cosmarium cf. holmiense var. integrum P.Lundell X Cosmarium cf. pyramidatum Brébisson ex Ralfs X Cosmarium cf. quadrifarium var. octastichum (Nordstedt) Kurt Förster X Cosmarium costatum var. subhexalobum Boldt X Cosmarium punctulatum Brebisson X Cosmarium sp.1 X Cosmarium sp.4 X Cosmarium sp.6 X Cyanosarcina sp.1 X Cylindrospermum sp.1 X Cylindrospermum sp.2 X Cylindrospermum sp.3 X Cylindrospermum sp.4 X X Cylindrospermum sp.5 X Cylindrospermum sp.6 X 94
Taxa LSR GSMNP Cymbella delicatula Kützing X Cymbella minuta Hilse in Rabenhorst X Cymbella sp.1 X X Cymbella sp.2 X Cymbella sp.3 X X Cymbella sp.4 X Cymbella sp.7 X Cymbella sp.8 X Cymbella sp.9 X Cymbella sp.10 X X Cymbella sp.12 X Cymbella sp.13 X Diadesmis contenta (Grunow ex Van Heurck) Mann in Round, Crawford & Mann X X Diadesmis perpusilla (Grunow) Mann in Round, Crawford & Mann X X Diatoma hiemale (Lyngbye) Heiberg X Diatoma mesodon Kützing X X Diploneis cf. oblongella (Nägeli) Cleve-Euler in Cleve-Euler & Osvald X X Diploneis sp.1 X Diploneis sp.2 X X Epithemia cf. argus var. alpestris X Epithemia sp.1 X Epithemia sp.2 X Eunotia billii Lowe & Kociolek X Eunotia girdle sp.1 X Eunotia girdle sp.2 X Eunotia minor (Kützing) Grunow X Eunotia musicola var. tridentula (Grunow) Nörpel et Lange-Bertalot X Eunotia rhomboidea Hustedt X Eunotia sp.1 X Eunotia sp.2 X Eunotia sp.4 X Eunotia sp.5 X X Eunotia sp.6 X Eunotia papilioforma Furey, Johansen, and Lowe X Eunotia varioundulata Nörpel-Schempp X
Pseudostaurosira brevistriata (Grunow in Van Heurck) Williams & Round X Fragilaria capucina Desmazières X X 95
Taxa LSR GSMNP Fragilariforma virescens (Ralfs) Williams & Round X X Frustulia rhomboides (Ehrenberg) De Toni X Frustulia rhomboides var. crassinervia (Brébisson in W. Smith) Ross X X Frustulia rhomboides var. saxonica (Rabenhorst) De Toni X Frustulia sp.4 X Frustulia weinholdii Hustedt X Geissleria ignota (Krasske) Lange-Bertalot & Metzeltin X Gloeothece cf. fusco-lutea Nägeli X Gloeothece sp.1 X Gloeothece sp.5 X Gloeothece tepidariorum (A.Braun) Lagerheim X X Gomphonema acuminatum Ehrenberg X Gomphonema angustum Agardh X Gomphonema bohemicum Reichelt & Fricke in Schmidt et al. X Gomphonema celatum E.W. Thomas & J.P. Kociolek in Thomas et al. X Gomphonema girdle sp.2 X Gomphonema montanum Schumann X X Gomphonema parvulum morphotype 1 Kützing sensu Thomas et al. X Gomphonema parvulum morphotype 2 Kützing sensu Thomas et al. X X Gomphonema sp.3 X Gomphonema sp.4 X Gomphonema sp.8 X Gomphonema truncatum Ehrenberg X Green Filament sp.1 X Green Filament sp.2 X Green Filament sp.4 X Green Filament sp.5 X Green Filament sp.6 X Green Filament sp.7 X Green Filament sp.8 X Green Filament sp.9 X Gyrosigma sp.1 X Hantzschia amphioxys (Ehrenberg) Grunow in Cleve & Grunow X Leibleinia sp.1 X Leptolyngbya cf. "Albertano/Kovacik-green" X
Leptolyngbya cf. gracillima (Zopf ex Hansgirg) Anagnostidis & Komárek X Leptolyngbya cf. subtilissima (Kützing ex Hansgirg) Komárek X X 96
Taxa LSR GSMNP Leptolyngbya sp.1 X X Leptolyngbya sp.2 X X Leptolyngbya sp.4 X X Leptolyngbya sp.5 X Leptolyngbya sp.6 X Leptolyngbya sp.7 X Leptolyngbya sp.8 X Leptolyngbya sp.9 X X Limnothrix sp.1 X X Limnothrix sp.2 X X Luticola goeppertiana (Bleisch in Rabenhorst) Mann in Round, Crawford & Mann X Lyngbya sp.1 X Lyngbya sp.2 X Mallomonas sp.1 X Mastogloia grevellei W.Smith in Gregory X Mastogloia smithii Thwaites in W. Smith X X Melosira dickiei (Thwaites) Kützing X X Meridion circulare (Greville) Agardh X X Micrasterias truncata Ralfs X Microcostatus krasskei (Hustedt) J.R. Johansen & J.C. Sray X Monoraphidium sp.1 X Mougeotia spp. X X Navicula angusta Grunow X X Navicula bryophila Boye Petersen X Navicula minima Grunow in Van Heurck X X Navicula radiosa Kützing X Navicula schmassmanii Hustedt X Navicula sp.4 X Navicula sp.9 X Navicula sp.10 X Navicula sp.14 X Navicula sp.15 X Navicula sp.18 X Navicula sp.19 X Navicula sp.20 X Navicula sp.21 X Navicula sp.22 X Navicula sp.23 X 97
Taxa LSR GSMNP Navicula veneta Kützing X X Netrium digitus (Erenberg) Itzigsohn and Rothe X Netrium oblongum (De Bary) Lutkemuller var. brevis W. West X X Netrium sp.3 X Nitzschia sp.1 X X Nitzschia sp.2 X Nitzschia sp.3 X X Nitzschia sp.4 X Nitzschia sp.5 X Nitzschia sp.6 X X Nitzschia sp.7 X Nitzschia sp.8 X Nitzschia sp.9 X Nitzschia sp.10 X Nitzschia sp.11 X Nitzschia sp.12 X Nitzschia sp.13 X Nostoc borneti Gain X Nostoc cf. entophytum Bornet & Flahault X Nostoc microscopicum Carmichael ex Bornet & Flahault X Nostoc minutum Desmazières ex Bornet & Flauhault X Nostoc palludosum Kützing ex Bornet & Flahault X Nostoc sp.1 X Nostoc sp.2 X Nostoc sp.3 X Nostoc sp.4 X Nostoc sp.5 X Nostoc sp.6 X Nostoc sp.7 X Nostoc sp.8 X Nostoc sp.9 X Nostoc sp.10 X Nostoc sp.11 X Nostoc sp.12 X Nostoc sp.13 X Nostoc sp.14 X Nostoc sp.15 X Nostoc sp.16 X 98
Taxa LSR GSMNP Nostoc sp.17 X Nostoc sphaericum Vaucher ex Bornet & Flahault X X Nupela lapidosa (Krasske) H. Lange-Bertalot X Nupela neglecta Ponader, Lowe & Potapova in Potapova et al. X X Oedogonium sp.1 X X Oocystis sp.1 X Orthoseira roseana (Rabenhorst) O'Meara X X Oscillatoria rupicola Hansgirg ex Gomont X X Oscillatoria sp.1 X X Oscillatoria sp.2 X Oscillatoria sp.3 X Oscillatoria sp.4 X Oscillatoria sp.5 X Oscillatoria sp.6 X Oscillatoria sp.7 X Phacus sp.1 X Phormidium cf. lusitanicum (Sampaio) Anagnostidis X Phormidium cf. pseudocortianum (Starmach) Anagnostidis X Phormidium sp.1 X Phormidium sp.2 X Phormidium sp.3 X Phormidium sp.4 X Phormidium sp.5 X Phormidium sp.6 X Phormidium sp.7 X Phormidium sp.8 X Phormidium sp.9 X Phormidium sp.10 X Phormidium sp.11 X Phormidium sp.12 X Phormidium sp.13 X Phormidium sp.14 X Phormidium sp.15 X Phormidium sp.16 X Phormidium sp.17 X X Phormidium sp.18 X Pinnularia divergens W.Smith X Pinnularia divergentissima (Grunow in Van Heurck) Cleve X X 99
Taxa LSR GSMNP Pinnularia girdle sp.1 X Pinnularia girdle sp.2 X Pinnularia rupestris Hantzsch in Rabenhorst X Pinnularia sp.4 X Pinnularia sp.8 X Pinnularia stomatophora (Grunow in Schmidt et al.) Cleve X Pinnularia subcapitata Gregory X Placoneis placentula (Ehrenberg) Mereschkowsky X Planothidium lanceolatum (Brébisson ex Kützing) Lange-Bertalot X X Planothidium frequentissimum (Lange-Bertalot in Krammer & Lange-Bertalot) Lange-Bertalot X Psammothidium helveticum (Hustedt) Bukhtiyarova et Round X Psammothidium marginulatum (Grunow) Bukhtiyarova et Round X Psammothidium montanum (Krasske) Mayama in Mayama, S., Idei, M., Osada, K. & T. Nagumo X Psammothidium subatomoides (Hustedt) Bukhtiyarova & Round X Pseudanabaena cf. minima (G.S.An) Anagnostidis X X Pseudanabaena sp.1 X Pseudanabaena sp.2 X X Pseudanabaena sp.3 X X Pseudanabaena sp.4 X Pseudanabaena sp.5 X Pseudanabaena sp.6 X Pseudanabaena sp.7 X Pseudanabaena sp.8 X Pseudanabaena sp.9 X X Pseudanabaena sp.10 X Pseudanabaena sp.11 X Rhoicosphenia abbreviata (C.Agardh) Lange-Bertalot X Rhopalodia gibba (Ehrenberg) Otto Müller X Rossithidium cf. pusilla (Grunow) Round et Bukhtiyarova X Scenedesmus sp.1 X Scytonema sp.1 X Scytonema sp.2 X
Sellaphora cf. pupula var. aquaeductae (Krasske) E.Y.Haworth & M.G.Kelly X Sellaphora cf. seminulum (Grunow) D.G.Mann X Sellaphora laevissima (Kützing) D.G. Mann X X Sellaphora pupula (Kützing) Mereschkowsky X 100
Taxa LSR GSMNP Spirogyra sp.1 X Stauroneis anceps Ehrenberg X Stigonema sp.1 X Stigonema sp.2 X Stigonema sp.3 X Surirella linearis W.Smith X Synedra acus Kützing X X Tabellaria ventricosa Kützing X X Tryblionella littoralis (Grunow) D.G.Mann X X Unknown coccoid Chlorophyte sp.1 X X Unknown coccoid Chlorophyte sp.2 X Unknown coccoid Chlorophyte sp.3 X Unknown coccoid Chlorophyte sp.4 X Unknown coccoid Chlorophyte sp.5 X Unknown coccoid cyanobacterium sp.1 X Unknown coccoid cyanobacterium sp.2 X Unknown coccoid cyanobacterium sp.3 X Unknown coccoid cyanobacterium sp.4 X Unknown coccoid cyanobacterium sp.5 X Unknown coccoid cyanobacterium sp.7 X Unknown coccoid cyanobacterium sp.8 X Unknown coccoid cyanobacterium sp.9 X Unknown coccoid cyanobacterium sp.10 X Unknown coccoid cyanobacterium sp.11 X Unknown coccoid cyanobacterium sp.12 X Unknown coccoid cyanobacterium sp.13 X Unknown coccoid cyanobacterium sp.14 X Unknown filamentous cyanobacterium sp.1 X Unknown filamentous cyanobacterium sp.2 X Unknown filamentous cyanobacterium sp.3 X Unknown filamentous cyanobacterium sp.4 X Unknown filamentous cyanobacterium sp.5 X Unknown filamentous cyanobacterium sp.6 X Unknown filamentous cyanobacterium sp.7 X Unknown pennate girdle sp.1 X Unknown pennate girdle sp.2 X Unknown pennate girdle sp.3 X Unknown pennate girdle sp.4 X 101
Taxa LSR GSMNP Unknown pennate girdle sp.5 X Unknown pennate girdle sp.6 X Unknown pennate girdle sp.7 X Unknown pennate girdle sp.8 X Unknown pennate girdle sp.9 X Unknown pennate girdle sp.10 X Unknown pennate girdle sp.11 X Unknown pennate girdle sp.12 X Unknown pennate girdle sp.13 X Unknown pennate girdle sp.14 X Unknown pennate girdle sp.15 X Unknown pennate girdle sp.16 X Unknown pennate girdle sp.17 X Unknown pennate girdle sp.18 X Unknown pennate girdle sp.19 X Unknown pennate girdle sp.20 X Unknown pennate girdle sp.21 X Unknown pennate girdle sp.22 X Unknown pennate girdle sp.23 X Unknown pennate girdle sp.24 X Unknown pennate girdle sp.25 X Unknown pennate girdle sp.26 X Unknown pennate girdle sp.27 X Unknown pennate girdle sp.28 X Unknown pennate girdle sp.29 X Unknown pennate girdle sp.30 X Zygnema sp.1 X
102
Table 2. List of common taxa frequently encountered across Lake Superior region samples. A taxon was considered common if it occurred in >20% of the samples.
Percent of Sites Mean Relative Taxon Present Abundance Achnanthidium minutissimum 40 2.6 Aphanocapsa cf. fusco-lutea 40 2.0 Aphanocapsa sp. 1 30 0.5 Caloneis bacillum 20 0.5 Chroococcus pallidus 20 2.2 Chroococcus varius 25 0.9 Diadesmis perpusilla 25 3.2 Gloeothece tepidariorum 20 4.4 Leptolyngbya cf. subtilissima 25 8.0 Leptolyngbya sp. 2 40 4.3 Limnothrix sp. 1 60 2.8 Meridion circulare 20 3.0 Mougeotia spp. 30 4.0 Navicula radiosa 20 0.4 Nostoc palludosum 20 0.4 Nostoc sphaericum 20 2.4 Pseudanabaena cf. minima 85 3.2 Rhopalodia sp. 1 20 0.8 Unknown coccoid Chlorophyte sp.1 25 0.3
103
Table 3. List of common taxa frequently encountered across Great Smoky Mountain National Park samples. A taxon was considered common if it occurred in >20% of the samples.
Percent of Mean Relative Taxon Sites Present Abundance Achnanthidium minutissimum 40 3.2 Aphanocapsa cf. fusco-lutea 20 0.6 Fragillaria capucina 20 1.9 Frustulia rhomboides var. crassinervia 25 0.2 Frustulia rhomboides var. saxonica 25 2.2 Leptolyngbya cf. subtilissima 25 1.2 Leptolyngbya sp. 2 35 5.4 Navicula angusta 20 0.7 Nitzschia sp. 1 20 0.4 Nostoc sphaericum 20 6.6 Pinnularia sp. 1 20 0.3 Pseudanabaena cf. minima 50 5.9 Unknown coccoid Chlorophyte sp. 1 20 2.2
104
Table 4. Taxa which occurred at a mean relative abundance > 1% in the Lake Superior region (LSR) compared with the mean relative abundance in the Great Smoky Mountains National Park (GSMNP).
Mean Relative Abundance Mean Relative Abundance LSR GSMNP Leptolyngbya cf. subtilissima 8.0 1.2 Diatoma hiemale 5.2 0 Gloeothece tepidariorum 4.4 0.3 Leptolyngbya sp. 2 4.3 5.4 Mougeotia spp. 4.0 4.3 Spirogyra sp. 1 4.0 0 Orthoseira roseana 3.6 0.3 Diadesmis perpusilla 3.2 0.4 Pseudanabaena cf. minima 3.2 5.9 Meridion circulare 3.0 0.6 Limnothrix sp. 1 2.8 1.6 Achnanthidium minutissimum 2.6 3.2 Oscillatoria rupicola 2.4 0.4 Nostoc sphaericum 2.4 6.6 Aphanocapsa muscicola 2.2 1.1 Chroococcus pallidus 2.2 0.1 Nostoc microscopicum 2.1 0 Aphanocapsa cf. fusco-lutea 2.0 0.6 Epithemia cf. argus var. alpestris 1.4 0 Leptolyngbya sp. 6 1.3 0 Nitzschia sp. 1 1.1 0.4 Diatoma mesodon 1.0 0.2
105
Table 5. Taxa which occurred at a mean relative abundance > 1% in the Lake Superior region (LSR) compared with the mean relative abundance in the Great Smoky Mountains National Park (GSMNP).
Mean Relative Abundance Mean Relative Abundance LSR GSMNP Nostoc sphaericum 2.4 6.6 Pseudanabaena cf. minima 3.2 5.9 Cladophora spp. 0.2 5.7 Leptolyngbya sp. 2 4.3 5.4 Cylindrospermum sp. 4 0.9 4.8 Mougeotia spp. 4 4.3 Aphanocapsa sp. 2 0 4.3 Achnanthidium minutissimum 2.6 3.2 Phormidium sp. 16 0 3.1 Phormidium sp. 1 0 3.1 Leptolyngbya sp. 8 0 2.7 Aphanocapsa sp. 1 0.5 2.6 Green Filament sp. 4 0 2.4 Unknown coccoid Chlorophye sp. 1 0.3 2.2 Frustulia rhomboides var. saxonica 0 2.2 Stigonema sp. 1 0 2.1 Fragillaria capucina 0.5 1.9 Aphanothece cf. pallida 0 1.6 Limnothrix sp. 1 2.8 1.6 Leptolyngbya sp. 1 0.1 1.5 Cylindrospermum sp. 6 0 1.5 Nostoc sp. 17 0 1.5 Aphanothece sp. 2 0 1.4 Leptolyngbya cf. subtilissima 8 1.2 Aphanocapsa muscicola 2.2 1.1 Leptolyngbya sp. 9 1 1.1
106
Table 6. ANOSIM results for region (LSR=Lake Superior region and GSMNP=Great Smoky Mountains National Park) calculated from the Bray-Curtis Similarity Matrix; * indicates significance (Bonferroni correction factor α = 0.017 used for pairwise comparisons).
Global R p-value Region 0.261 0.001*
Pairwise Comparison R Statistic p-value GSMNP 1, GSMNP 2 0.446 0.001* GSMNP 1, LSR 0.12 0.077 GSMNP 2, LSR 0.287 0.001*
107
Table 7. Similarity percentages analysis displaying taxa contributing to the separation of Great Smoky Mountains National Park samples forming groups GSMNP 1 and GSMNP 2 in non-metric multidimensional scaling ordination (Figure 1). Table includes the average relative abundance of each taxon in each group, the average dissimilarity (AD) of each taxon between groups, the ratio Average Dissimilarity/Standard Deviation (AD/SD) for each taxon, the percent contribution of each taxon to the overall separation between groups, and the cumulative percent dissimilarity between groups.
Groups GSMNP 1 & GSMNP 2 Average dissimilarity between groups = 98.96 GSMNP 1 Avg. GSMNP 2 Avg. Rel. Species Rel. Abundance Abundance AD AD / SD % Contribution Cum. % Nostoc sphaericum 14.71 0 7.52 0.54 7.6 7.6 Pseudanabaena cf. minima 12.64 0.46 6.4 0.47 6.47 14.06 Leptolyngbya sp. 2 9.09 2.32 5.44 0.45 5.5 19.56 Cylindrospermum sp. 4 10.53 0.06 5.36 0.35 5.41 24.97 Cladophora spp 0 10.43 5.33 0.38 5.39 30.36 Mougeotia spp 0 7.86 3.97 0.34 4.02 34.38 Aphanocapsa sp. 2 0 7.74 3.9 0.31 3.94 38.32 Phormidium sp. 1 6.83 0 3.5 0.35 3.54 41.86 Phormidium sp. 16 6.84 0 3.47 0.35 3.51 45.37 Leptolyngbya sp. 8 5.92 0 3.01 0.37 3.04 48.41 Achnanthidium minutissimum 0.01 5.73 2.93 0.49 2.96 51.37
108
Table 8. Similarity percentages analysis displaying taxa contributing to the separation of groups Great Smoky Mountains National Park 2 (GSMNP 2) and Lake Superior region (LSR) in non-metric multidimensional scaling ordination (Figure 1). Table includes the average relative abundance of each taxon in each group, the average dissimilarity (AD) of each taxon between groups, the ratio Average Dissimilarity/Standard Deviation (AD/SD) for each taxon, the percent contribution of each taxon to the overall separation between groups, and the cumulative percent dissimilarity between groups.
Groups GSMNP 2 & LSR Average dissimilarity between groups = 96.79 GSMNP 2 Avg. LSR Avg. Rel. Species Rel. Abundance Abundance AD AD / SD % Contribution Cum. % Mougeotia spp. 7.86 4.01 5.62 0.45 5.8 5.8 Cladophora spp. 10.43 0.19 5.44 0.38 5.62 11.42 Leptolyngbya cf. subtilissima 0.06 7.99 4.1 0.4 4.24 15.66 Aphanocapsa sp. 2 7.74 0 3.93 0.32 4.07 19.72 Achnanthidium minutissimum 5.73 2.64 3.63 0.65 3.75 23.48 Leptolyngbya sp. 2 2.32 4.3 3.02 0.44 3.12 26.59 Diatoma hiemale 0 5.18 2.65 0.29 2.74 29.33 Gloeothece tepidariorum 0.06 4.37 2.25 0.32 2.32 31.65 Green Filament sp. 4 4.4 0 2.24 0.32 2.31 33.97 Unknown coccoid Chlorophyte sp. 1 3.97 0.34 2.14 0.42 2.21 36.17 Orthoseira roseana 0.46 3.64 2.07 0.26 2.14 38.32 Spirogyra sp. 1 0 3.98 2.06 0.32 2.13 40.45 Frustulia rhomboides var. saxonica 3.93 0 2.01 0.61 2.07 42.52 Stigonema sp. 1 3.78 0 1.95 0.47 2.01 44.54 Meridion circulare 1.04 3 1.94 0.42 2 46.54 Fragilaria capucina 3.49 0.5 1.93 0.47 1.99 48.53 Diadesmis perpusilla 0.64 3.2 1.88 0.42 1.94 50.47
109
Table 9. ANOSIM results of the category moisture for LSR-GSMNP Combined (LSR=Lake Superior region and GSMNP=Great Smoky Mountains National Park), the LSR, and the GSMNP calculated from the Bray-Curtis Similarity Matrix.
Global R p-value LSR-GSMNP Combined 0.075 0.131 LSR 0.038 0.299 GSMNP 0.126 0.114
110
Table 10. Mean relative abundance of taxa for the two moisture categories Dry and Very Wet for the Lake Superior Region (LSR).
Moisture Moisture Category Very Category Dry Wet Gloeothece tepidariorum 14.48 Diatoma hiemale 20.71 Leptolyngbya cf. subtilissima 13.54 Spirogyra sp. 1 15.91 Oscillatoria rupicola 10.62 Orthoseira roseana 14.49 Nostoc microscopicum 9.04 Diatoma mesodon 4.14 Pseudanabaena cf .minima 6.71 Meridion circulare 3.91 Aphanocapsa muscicola 3.59 Phormidium sp. 10 3.87 Limnothrix sp. 2 3.30 Diadesmis perpusilla 3.69 Leptolyngbya sp. 4 3.13 Nitzschia sp. 1 2.70 Scytonema sp. 1 2.79 Nitzschia sp. 9 2.21 Aphanocapsa cf. fusco-lutea 2.75 Phormidium cf. lusitanicum 2.03 Aphanothece sp. 3 2.65 Fragilaria capucina 2.02 Unknown coccoid cyanobacterium sp. 4 2.63 Melosira dickiei 1.78 Nostoc minutum 2.57 Achnanthidium sp. 2 1.31 Limnothrix sp. 1 2.56 Achnanthidium minutissimum 1.28 Calothrix sp. 3 2.35 Rhoicosphenia sp. 1 1.22 Nostoc sphaericum 1.97 Mougeotia spp. 1.09 Pseudanabaena sp. 9 1.64 Sellophora sp. 1 1.03 Unknown coccoid Chlorophyte Leptolyngbya sp. 2 1.57 sp. 1 1.02 Chroococcus cf. varius 1.36 Navicula radiosa 0.92 Phormidium cf. Pseudanabaena sp. 2 1.30 pseudocortianum 0.80 Unknown coccoid cyanobacterium sp. 14 1.27 Synedra sp. 1 0.79 Aphanocapsa sp. 1 1.24 Caloneis sp. 4 0.75 Cyanosarcina sp. 1 1.07 Gyrosigma sp. 1 0.75 Leptolyngbya sp. 5 1.04 Pseudanabaena cf. minima 0.73 Chroococcus varius 0.95 Phormidium sp. 11 0.60 Leptolyngbya cf. "Albertano/Kovacik-green" 0.91 Nitzschia sp. 7 0.57 Aphanocapsa sp. 3 0.80 Leptolyngbya sp. 9 0.50 Nostoc Borneti 0.68 Unknown pennate sp. 24 0.49 Nostoc palludosum 0.52 Aphanocapsa sp. 1 0.47 Phormidium sp. 6 0.08 Limnothrix sp. 1 0.43 Mallomonas sp. 0.07 Triblionella sp. 1 0.42
111
Moisture Moisture Category Very Category Dry Wet Chroococcus sp. 4 0.04 Eunotia sp. 1 0.41 Chroococcus helveticus 0.03 Unknown pennate sp. 23 0.39 Leptolyngbya sp. 2 0.36 Achnanthes coarctata 0.31 Cymbella sp. 1 0.30 Nitzschia sp. 5 0.30 Amphora pediculus 0.27 Diploneis cf. oblongella 0.25 Leptolyngbya cf. subtilissima 0.25 Fragilaria brevistriata 0.24 Zygnema sp. 1 0.21 Gomphonema acuminatum 0.21 Caloneis bacillum 0.16 Cymbella delicatula 0.16 Calothrix sp. 1 0.12 Cocconeis placentula 0.12 Frustulia rhomboides var. crassinervia 0.12 Gomphonema sp. 3 0.09 Surrirella sp. 1 0.09 Nitzschia sp. 3 0.06 Scenedesmus spp. 0.06 Gomphonema montanum 0.06 Tabellaria ventricosa 0.06 Navicula sp. 1 0.03 Chroococcus helveticus 0.03 Gomphonema parvulum morphotype 2 0.03 Gomphonema sp. 1 0.03 Rhopalodia sp. 1 0.03 Diadesmis contenta 0.03 Navicula sp. 2 0.02 Navicula sp. 3 0.02
112
Table 11. Mean relative abundance of taxa for the two moisture categories Dry and Very Wet for the Great Smoky Mountains National Park (GSMNP).
Moisture Moisture Category Very Category Dry Wet Cylindrospermum sp. 4 23.68 Achnanthidium minutissimum 14.91 Pseudanabaena cf. minima 22.52 Stigonema sp. 1 10.38 Unknown coccoid Chlorophyte Nostoc sphaericum 18.23 sp. 1 8.79 Aphanocapsa sp. 1 10.47 Fragilaria capucina 8.64 Nostoc sp. 17 7.28 Aphanothece cf. pallida 8.09 Leptolyngbya sp. 9 4.04 Aphanothece sp. 2 4.85 Leptolyngbya sp. 1 2.93 Leptolyngbya sp. 2 4.29 Calothrix sp. 3 1.84 Nupela lapidosa 4.06 Leptolyngbya cf. subtilissima 1.57 Eunotia sp. 23 3.68 Pseudanabaena sp. 3 1.35 Fragilariaforma virescens 3.11 Aphanocapsa sp. 6 1.29 Tabellaria ventricosa 2.84 Unknown coccoid cyanobacteria sp. 8 1.08 Navicula angusta 2.53 Pseudanabaena sp. 4 0.67 Meridion circulare 2.50 Aphanothece pallida 0.49 Eunotia musicola var. tridentula 2.38 Leptolyngbya sp. 2 0.26 Cymbella sp. 7 2.30 Aphanocapsa muscicola 0.18 Achnanthidium subatomoides 1.42 Gomphonema parvulum Diadesmis perpusilla 0.14 morphotype 2 1.35 Tabellaria ventricosa 0.12 Girdle sp. 1 1.34 Frustulia rhomboides var. crassinervia 0.04 Diatoma mesodon 1.09 Orthoseira roseana 0.04 Pseudanabaena sp. 9 1.08 Oscillatoria sp. 4 0.58 Unknown coccoid cyanobacteria sp. 10 0.57 Eunotia rhomboidea 0.57 Gomphonema parvulum morphotype 1 0.55 Frustulia rhomboides var saxonica 0.53 Aphanocapsa cf. fusco-lutea 0.49 Stigonema sp. 3 0.49 Frustulia rhomboides var. crassinervia 0.48 Pseudanabaena cf. minima 0.47
113
Moisture Moisture Category Very Category Dry Wet Brachysira brebissonii 0.45 Gomphonema montanum 0.35 Nitzschia sp. 1 0.24 Oscillatoria sp. 1 0.23 Leptolyngbya sp. 9 0.19 Cymbella sp. 1 0.12 Cymbella sp. 10 0.08 Melosira dickiei 0.08 Eunotia sp. 5 0.04
114
Table 12. Species diversity for each moisture category (Dry, Damp, Wet, Very Wet) in both the Lake Superior region (LSR) and the Great Smoky Mountains National Park (GSMNP).
LSR GSMNP Shannon-Weiner Moisture Shannon-Weiner Moisture Category Index Category Index Dry 1.95 Dry 1.59 Dry 1.59 Dry 0.91 Dry 1.60 Dry 0.26 Dry 1.69 Dry 0.56 Damp 2.55 Damp 0.56 Damp 0.88 Damp 2.57 Damp 1.72 Damp 1.33 Damp 1.74 Damp 1.35 Damp 2.22 Damp 1.50 Damp 0.97 Damp 3.20 Damp 3.09 Damp 1.05 Wet 2.39 Damp 0.85 Wet 2.15 Damp 1.41 Wet 2.67 Damp 2.54 Wet 1.72 Damp 0.69 Very Wet 2.01 Wet 0.26 Very Wet 0.95 Very Wet 2.44 Very Wet 2.11 Very Wet 1.94 Very Wet 0.87 Very Wet 2.66 Very Wet 2.66 Very Wet 1.45
115 TABLES
Chapter III 116
Table 1. List of common taxa frequently encountered across all samples from Nu'uanu Pali. A taxon was considered common if it occurred in >20% of the samples.
Percent of Sites Mean Relative Taxon Present Abundance Aphanocapsa muscicola 25.0 3.1 Aphanothece castagnei 28.1 3.2 Aphanothece pallida 40.6 3.4 Caloneis molaris 21.9 0.3 Cyanosarcina spp. 93.8 3.5 Denticula kuetzingii 53.1 1.1 Diadesmis contenta 56.3 0.5 Diadesmis sp.10 53.1 1.3 Diadesmis sp.2 75.0 0.7 Diadesmis sp.4 59.4 1.4 Diadesmis sp.6 25.0 0.2 Gloeothece tepidariorum 75.0 10.5 Gloeocapsa caldariorum 34.4 3.9 Leptolyngbya cf. "Albertano/Kováčik-green" 46.9 3.5 Leptolyngbya cf. rivulariarum 34.4 3.0 Limnothrix sp.5 25.0 1.2 Nitzschia sp.4 34.4 0.7 Nostoc sp.15 25.0 1.5 Nostoc sp.24 37.5 2.7 Oscillatoria rupicola 31.3 0.6 Phormidium cf. numidicum 1 28.1 0.4 Phormidium cf. numidicum 2 21.9 0.8 Pinnularia borealis 28.1 0.1 Pinnularia sp.2 28.1 0.1 Pseudanabaena cf. minima 56.3 4.5 Pseudanabaena sp.2 62.5 1.1 Rhopalodia rupestris 37.5 2.3 Scytonema ocellatum 28.1 5.8 Tolypothrix sp.1 31.3 2.4
117
Table 2. ANOSIM results of factor Aspect calculated from the Bray-Curtis Similarity Matrix of species data; * indicates significance (Bonferroni correction factor α = 0.017 used for pairwise comparisons).
Global R p-value Aspect 0.707 0.001*
Pairwise Comparison R Statistic p-value S, N 0.88 0.001* S, W 0.61 0.028 N, W 0.085 0.347
118
Table 3. ANOSIM results of factor Light calculated from the Bray-Curtis Similarity Matrix of species data; * indicates significance (Bonferroni correction factor α = 0.017 used for pairwise comparisons).
Global R p-value Light 0.504 0.001*
Pairwise Comparison R Statistic p-value High, Low 0.871 0.001* High, Moderate 0.775 0.001* Low, Moderate 0.077 0.189
119
Table 4. Similarity percentages analysis displaying taxa contributing to the separation of groups S (South) and N (North) in non-metric multidimensional scaling ordination (Figure 3). Table includes the average relative abundance of each taxon in each group, the average dissimilarity of each taxon between groups, the ratio Average Dissimilarity/Standard Deviation for each taxon, the percent contribution of each taxon to the overall separation between groups, and the cumulative percent dissimilarity between groups.
Groups S & N Average dissimilarity between groups = 91.29 Average Group S Average Group N Dissimilarity / Relative Average Relative Average Standard Percent Cumulative Abundance Abundance Dissimilarity Deviation Contribution Percent Gloeothece tepidariorum 0 13.59 4.91 1.84 5.38 5.38 Scytonema ocellatum 22.28 1.27 4.7 1.31 5.15 10.53 Aphanocapsa muscicola 11.62 0.8 3.28 1.09 3.6 14.13 Pseudanabaena cf. minima 0.4 5.64 2.83 1.12 3.1 17.23 Cyanosarcina spp. 0.49 4.5 2.63 2.03 2.88 20.11 Mesataenium sp.1 3.88 0 2.42 1.14 2.65 22.76 Aphanothece pallida 3.25 3.76 2.33 0.93 2.55 25.32 Leptolyngbya cf. "Albertano/Kovácik-green" 2.79 3.37 2.23 0.99 2.44 27.76 Leptolyngbya cf. rivulariarum 0 4.14 2.2 0.81 2.41 30.16 Gloeocapsa caldariorum 0 5.31 2.13 0.78 2.33 32.49 Nostoc sp.18 6.26 1.22 1.98 0.65 2.17 34.66 Aphanothece castagnei 2.63 3.17 1.93 0.73 2.11 36.77 Tolypothrix sp.1 1.58 2.89 1.88 0.76 2.06 38.83 Scytonema Schmidtii 6.07 0 1.81 0.62 1.99 40.82 Nostoc sp.24 0 3.45 1.79 0.84 1.96 42.78 Rhopalodia rupestris 0 3.26 1.73 0.77 1.89 44.67 Nostoc sp.15 1.58 1.66 1.64 0.86 1.8 46.47 Limnothrix sp.1 1.57 0.74 1.54 0.9 1.68 48.16 Diadesmis sp.4 0 1.78 1.5 0.93 1.64 49.8 120
Table 5. Similarity percentages analysis displaying taxa contributing to the separation of groups High (high light) and Low (low light) in non- metric multidimensional scaling ordination (Figure 4). Table includes the average relative abundance of each taxon in each group, the average dissimilarity of each taxon between groups, the ratio Average Dissimilarity/Standard Deviation for each taxon, the percent contribution of each taxon to the overall separation between groups, and the cumulative percent dissimilarity between groups.
Groups High & Low Average dissimilarity between groups = 91.81 Average Group High Group Low Dissimilarity / Average Relative Average Relative Average Standard Percent Cumulative Abundance Abundance Dissimilarity Deviation Contribution Percent Gloeothece tepidariorum 0 15.26 5.2 1.83 5.67 5.67 Scytonema ocellatum 22.28 0.91 4.83 1.31 5.26 10.92 Aphanocapsa muscicola 11.62 0.29 3.33 1.07 3.62 14.54 Pseudanabaena cf. minima 0.4 6.86 3.25 1.25 3.54 18.08 Cyanosarcina spp. 0.49 4.69 2.66 1.88 2.9 20.98 Mesataenium sp.1 3.88 0 2.44 1.14 2.66 23.64 Leptolyngbya cf. "Albertano/Kovácik-green" 2.79 4.22 2.43 1.03 2.64 26.29 Rhopalodia rupestris 0 4.02 2.09 0.9 2.28 28.56 Nostoc sp.18 6.26 1.51 2.02 0.64 2.2 30.76 Leptolyngbya cf. rivulariarum 0 3.74 1.96 0.71 2.14 32.89 Tolypothrix sp.1 1.58 3.25 1.89 0.73 2.06 34.96 Scytonema Schmidtii 6.07 0 1.83 0.62 2 36.95 Aphanothece pallida 3.25 2.76 1.83 0.68 2 38.95 Nostoc sp.24 0 2.78 1.73 0.87 1.89 40.84 Aphanothece castagnei 2.63 2.25 1.64 0.63 1.79 42.63 Limnothrix sp.1 1.57 1.01 1.6 0.92 1.75 44.38 Diadesmis sp.4 0 2.06 1.52 0.85 1.66 46.03 Nostoc sp.15 1.58 1.27 1.52 0.79 1.66 47.69 Denticula kuetzingii 0 1.48 1.52 1.2 1.66 49.35 121
Table 6. Similarity percentages analysis displaying taxa contributing to the separation of groups High (high light) and Moderate (moderate light) in non-metric multidimensional scaling ordination (Figure 4). Table includes the average relative abundance of each taxon in each group, the average dissimilarity of each taxon between groups, the ratio Average Dissimilarity/Standard Deviation for each taxon, the percent contribution of each taxon to the overall separation between groups, and the cumulative percent dissimilarity between groups.
Groups High & Moderate Average dissimilarity between groups = 90.30 Average Group High Group Moderate Dissimilarity / Average Relative Average Relative Average Standard Percent Cumulative Abundance Abundance Dissimilarity Deviation Contribution Percent Gloeocapsa caldariorum 0 14.5 5.44 3.31 6.02 6.02 Scytonema ocellatum 22.28 1.72 4.45 1.33 4.92 10.94 Gloeothece tepidariorum 0 9.58 4.36 2.47 4.83 15.77 Aphanocapsa muscicola 11.62 1.66 3.16 1.14 3.5 19.27 Aphanothece pallida 3.25 4.95 3.05 1.6 3.38 22.65 Diadesmis sp.10 0 4.28 2.99 1.81 3.32 25.97 Aphanothece castagnei 2.63 5.87 2.7 1.02 2.99 28.96 Mesataenium sp.1 3.88 0 2.33 1.14 2.58 31.54 Cyanosarcina spp. 0.49 3.44 2.25 2.18 2.49 34.03 Leptolyngbya cf. rivulariarum 0 3.98 2.22 0.93 2.46 36.49 Leptolyngbya cf. "Albertano/Kovácik-green" 2.79 2.43 2.01 1.03 2.23 38.71 Nostoc sp.24 0 5 1.98 0.82 2.2 40.91 Pseudanabaena cf. minima 0.4 2.97 1.96 1.04 2.17 43.08
122 TABLES
Chapter IV 123
Table 1. Site information for each location sampled in the Great Smoky Mountains National Park for algal populations utilized in the desiccation experiment.
GPS Location Habitat Coordinates pH Bedrock Geology Rock outcrop north of N 35° 37.410 Anakeesta Site 1 bridge on Highway 441 Pseudoaerial W 083° 24.618 5.8 Formation N 35° 37.436 Anakeesta Site 2 Walker Camp Prong Stream W 083° 24.641 4.2 Formation Rock outcrop on N 35° 37.302 Anakeesta Site 3 Highway 441 Pseudoaerial W 083° 25.438 4.7 Formation N 35° 37.268 Anakeesta Site 4 Walker Camp Prong Stream W 083° 25.420 5.0 Formation Rock outcrop east of tunnel on Laurel Creek N 35° 38.987 Site 5 Road Pseudoaerial W 083° 42.919 5.0 Metcalf Phyllite N 35° 38.987 Site 6 Laurel Creek Stream W 083° 42.912 5.0 Metcalf Phyllite
124
Table 2. A. Median Total Cell Density (cells/cm2) of the populations (included all health categories) for the establishment, control, and treatment groups in each site; B. Percent change in cell density from the establishment period for each treatment; C. Percent change for each treatment from the two week to the four week sampling period; D. Percent change from control to the four week treatments.
A. Median Total Cell Densities (cells/cm2) 2 weeks - 2 weeks - 2 weeks - 4 weeks - 4 weeks - 4 weeks - 4 weeks - Establishment 6 hour 24 hour 168 hour Control 6 hour 24 hour 168 hour 1 Month Site 1 24852.61 9550.63 12533.84 8132.91 14889.03 10375.31 8639.60 6259.97 4346.66 Site 3 43480.19 1716.10 1770.56 2667.94 3374.91 4791.91 4227.28 2795.53 1969.23 Site 5 63057.49 9578.09 12849.68 14634.42 12432.39 16391.71 7924.66 16086.09 12700.45
B. Percent Change from Establishment Site 1 -62 -50 -67 -40 -58 -65 -75 -83 Site 3 -96 -96 -94 -92 -89 -90 -94 -95 Site 5 -85 -80 -77 -80 -74 -87 -74 -80
C. Percent Change between 6 hour, 24 hour, 168 hour Treatments at 2 weeks to 4 weeks Site 1 92 -45 -30 Site 3 279 239 105 Site 5 58 -62 110
D. Percent Change from Control to 6 hour, 24 hour, 168 hour Treatments at 4 weeks Site 1 -44 -72 -138 Site 3 142 125 83 Site 5 76 -57 129
125
Table 3. Median cell densities (cells/cm2) of the common healthy taxa in all populations from Site 1; A taxon was considered common if it occurred in >20% of the samples.
2 Week - 2 Week - 2 Week - 4 Week - 4 Week - 4 Week - 4 Week - 1 Establishment 6 Hour 24 Hour 168 Hour Control 6 Hour 24 Hour 168 Hour Month Achnanthidium minutissimum (Kützing) Czarnecki 0 16.20 0 18.46 17.91 29.44 0 0 0 Aphanocapsa cf. parietina Nägeli 0 0 169.01 956.58 143.16 569.05 137.32 55.99 395.99 Aphanocapsa muscicola (Meneghini) Wille 3744.31 1361.57 2448.45 1661.60 2413.33 1243.66 739.42 712.90 724.01 Aphanocapsa sp. 4 0 0 0 0 0 484.51 519.09 267.51 0 Aphanothece castagnei (Brébisson) Rabenhorst 277.88 178.21 0 404.55 268.67 41.46 347.44 233.74 63.16 Unknown Cyanobacterial Fil. 1424.41 0 320.41 18.81 31.06 0 0 46.75 30.94 Caloneis sp. 1 0 16.20 14.08 0 26.30 12.71 11.58 9.84 13.40 Chroococcus tenax (Kirchner) Hieronymus 975.08 371.91 436.61 364.61 683.68 457.73 535.55 495.95 323.01 Diadesmis sp. 1 51.88 31.42 25.89 13.29 26.30 0 0 0 0 Diatom girdle sp. 2 231.48 29.75 32.93 66.29 47.32 94.57 21.65 35.06 13.61 Diatom girdle sp. 3 42.57 13.34 23.32 44.47 0 41.46 18.98 15.69 7.02 Euastrum sp. 1 42.75 59.51 46.64 53.16 26.30 41.46 44.37 35.67 14.04 Gloeocapsa atrata Kützing 2326.27 555.10 396.42 265.78 411.96 381.45 266.19 140.24 224.11 Gloeothece tepidariorum (A.Braun) Lagerheim 470.26 208.27 471.20 298.32 501.52 521.31 324.27 271.97 365.15 Gomphonema montanum Schumann 382.54 32.40 75.18 22.10 122.71 99.75 46.32 44.58 19.77 Green Filament sp. 1 63.56 29.75 0 11.05 245.42 0 50.63 0 0 Leptolyngbya "Albertano/Kovacik-green" 288.96 226.81 395.81 187.83 409.04 171.43 226.99 71.34 191.15 Leptolyngbya cf. subtilissima (Kützing ex Hansgirg) Komárek 10626.31 2419.40 3015.66 2149.53 3080.75 2530.25 2212.02 1836.88 1146.54 Limnothrix spp. 876.39 340.21 536.33 478.41 262.95 206.08 219.71 276.42 77.24 Nitzschia sp. 1 63.76 62.84 116.59 29.65 105.18 114.00 109.86 46.75 14.04 126
2 Week - 2 Week - 2 Week - 4 Week - 4 Week - 4 Week - 4 Week - 1 Establishment 6 Hour 24 Hour 168 Hour Control 6 Hour 24 Hour 168 Hour Month Nostoc cf. microscopicum Carmichael ex Bornet & Flahault 3571.48 145.73 0 507.35 429.49 1284.20 328.91 115.92 230.80 Nostoc sp.1 2344.90 405.02 238.62 88.95 143.29 191.68 293.50 170.54 59.56 Pseudanabaena cf. minima (G.S.An) Anagnostidis 3194.46 1344.66 605.62 146.18 1056.77 356.26 324.27 71.34 158.19 Pinnularia sp. 1 20.81 16.20 0.00 14.06 0 14.25 0 8.00 0 Tetracyclus rupestris (Braun ex Rabenhorst) Grunow in Van Heurck 191.27 74.38 61.01 44.20 154.72 139.86 44.37 35.67 7.02
127
Table 4. Taxa with the greatest median cell densities (cells/cm2) in all populations from Site 1; Health categories include: H=Healthy, HI=Heavily Impaired, D=Dead.
4 week - Est. Control 1 Month Leptolyngbya cf. Leptolyngbya cf. Leptolyngbya cf. subtilissima - H 8246.43 subtilissima - H 3080.75 subtilissima - H 1146.54 Aphanocapsa Aphanocapsa Aphanocapsa muscicola - H 3744.31 muscicola - H 2413.33 muscicola - H 610.92 Nostoc cf. Pseudanabaena cf. Gloeothece microscopicum - H 3571.48 minima - H 1056.77 tepidariorum - H 365.15 Pseudanabaena cf. Chroococcus tenax minima - H 3194.46 - H 683.68 Chroococcus tenax - H 323.01 Gloeocapsa atrata - Tetracyclus Nostoc cf. H 2326.27 rupestris - D 631.09 microscopicum - H 230.8 2 week - 2 week - 2 week - 6 hour 24 hour 168 hour Leptolyngbya cf. Leptolyngbya cf. Leptolyngbya cf. subtilissima - H 2419.4 subtilissima - H 3015.66 subtilissima - H 2149.53 Aphanocapsa Aphanocapsa Aphanocapsa muscicola - H 1361.57 muscicola - H 2448.45 muscicola - H 773.41 Pseudanabaena cf. Pseudanabaena cf. minima - H 1344.66 minima - H 605.62 Limnothrix spp. - H 478.41 Gloeocapsa atrata - Limnothrix spp. - Tetracyclus rupestris - H 555.1 H 536.33 HI 419.85 Chroococcus tenax - Gloeothece H 371.91 tepidariorum - H 471.2 Chroococcus tenax - H 364.61 4 week - 4 week - 4 week - 6 hour 24 hour 168 hour Leptolyngbya cf. Leptolyngbya cf. Leptolyngbya cf. subtilissima - H 2530.25 subtilissima - H 2212.02 subtilissima - H 1836.88 Nostoc cf. Aphanocapsa Aphanocapsa microscopicum - H 1284.2 muscicola - H 739.42 muscicola - H 712.9 Aphanocapsa Chroococcus tenax muscicola - H 1243.66 - H 535.55 Chroococcus tenax - H 495.95 Tetracyclus rupestris Tetracyclus - HI 559.45 rupestris - D 502.8 Aphanocapsa sp.3 - H 385.67 Gloeothece Aphanocapsa sp.4 tepidariorum - H 521.31 - H 343.3 Limnothrix spp. - H 276.42
128
Table 5. Median cell densities (cells/cm2) of the common healthy taxa in all populations from Site 3; A taxon was considered common if it occurred in >20% of the samples.
2 Week - 2 Week - 2 Week - 4 Week - 4 Week - 4 Week - 4 Week - 1 Establishment 6 Hour 24 Hour 168 Hour Control 6 Hour 24 Hour 168 Hour Month Achnanthidium minutissimum 421.12 5.65 4.13 32.52 121.48 41.85 90.25 142.41 64.28 Aphanocapsa muscicola 4842.83 535.45 216.21 230.77 406.68 500.65 428.96 276.68 383.57 Aphanothece castagnei 218.39 70.12 0 124.41 47.60 0 49.08 65.62 22.33 Aphanothece pallida (Kützing) Rabenhorst) 962.39 0 35.06 25.64 91.95 0 179.05 142.41 43.83 Unknown Cyanobacterial Fil. 453.16 84.44 55.51 45.43 38.68 28.61 42.13 27.01 5.59 Chroococcus pallidus Nägeli 403.88 11.50 16.51 12.39 40.02 35.44 31.39 4.07 52.59 Cosmarium sp. 1 0 3.79 3.51 4.13 5.33 0 5.23 12.77 2.39 Diatom girdle sp. 1 165.93 36.93 5.33 6.71 13.25 9.66 0 0.00 0 Gomphonema montanum 94.98 1.92 2.34 4.63 15.84 35.76 10.46 12.21 0 Gomphonema parvulum morphotype 1 Kützing sensu Thomas et al. 115.40 18.94 6.79 9.29 47.53 23.11 8.74 40.19 14.15 Gomphonema sp. 3 0 23.37 5.84 0 0 21.46 0 12.77 0 Leptolyngbya cf. subtilissima 20735.37 1204.38 1113.17 1809.69 2128.46 2503.23 2261.10 1446.89 1200.82 Nitzschia sp. 1 157.92 19.79 29.22 46.46 42.25 35.76 56.18 53.59 6.95 Phormidium cf. corium (C.Agardh) Kützing 0 38.32 47.62 20.65 15.84 0 77.24 0.00 14.90 Pseudanabaena cf. minima 201.94 17.24 37.22 41.03 32.17 0 56.18 8.93 23.37 Pseudanabaena sp. 2 230.79 28.27 3.51 9.29 50.32 57.22 42.82 31.37 17.63 Unknown Coccoid Chlorophyte 0 5.65 1.75 4.13 0 7.15 5.23 0 6.95
129
Table 6. Taxa with the greatest median cell densities (cells/cm2) in all populations from Site 3; Health categories include: H=Healthy, HI=Heavily Impaired, D=Dead.
4 Week - Est. Control 1 Month Leptolyngbya cf. Leptolyngbya cf. Leptolyngbya cf. subtilissima – H 20735.37 subtilissima - H 2128.46 subtilissima - H 1200.82 Aphanocapsa Aphanocapsa Aphanocapsa muscicola – H 4842.83 muscicola - H 406.68 muscicola - H 383.57 Achnanthidium Achnanthidium Achnanthidium minutissimum – D 2684.61 minutissimum - D 232.39 minutissimum - H 64.28 Achnanthidium Achnanthidium Chroococcus minutissimum – HI 1052.79 minutissimum - H 121.48 pallidus - H 52.59 Gomphonema Aphanothece pallida parvulum Aphanothece – H 894.87 morphotype 1 - D 106.37 pallida - H 43.83 2 Week - 2 Week - 2 Week - 6 Hour 24 Hour 168 Hour Leptolyngbya cf. Leptolyngbya cf. Leptolyngbya cf. subtilissima - H 1204.38 subtilissima - H 1113.17 subtilissima - H 1412.44 Aphanocapsa Aphanocapsa Aphanocapsa muscicola - H 258.67 muscicola - H 216.21 muscicola - H 230.77 Unknown Achnanthidium Cyanobacterial Achnanthidium minutissimum - D 87.64 Filament - H 55.51 minutissimum - D 185.85 Unknown Cyanobacterial Achnanthidium Filament - H 64.28 minutissimum - D 49.67 Nitzschia sp1 - H 46.46 Gomphonema Unknown parvulum morphotype Phormidium cf. Cyanobacterial 1 – D 48.06 corium - H 45.58 Filament - H 45.43 4 Week - 4 Week - 4 Week - 6 Hour 24 Hour 168 Hour Leptolyngbya cf. Leptolyngbya cf. Leptolyngbya cf. subtilissima - H 2503.23 subtilissima - H 2261.1 subtilissima - H 1446.89 Aphanocapsa Aphanocapsa Achnanthidium muscicola - H 500.65 muscicola - H 428.96 minutissimum - D 293.8 Achnanthidium Achnanthidium Aphanocapsa minutissimum - D 303.41 minutissimum - D 166.03 muscicola - H 276.68 Unknown Gomphonema Cyanobacterial parvulum Achnanthidium Filament sp. 2 - H 146.48 morphotype 1 - D 113.6 minutissimum - H 142.41 Gomphonema parvulum morphotype Aphanothece pallida Aphanothece 1 – D 125.55 - H 78.47 pallida - H 142.41
130
Table 7. Median cell densities (cells/cm2) of the common healthy taxa in all populations from Site 5; A taxon was considered common if it occurred in >20% of the samples.
2 Week - 2 Week - 2 Week - 4 Week - 4 Week - 4 Week - 4 Week - 1 Establishment 6 Hour 24 Hour 168 Hour Control 6 Hour 24 Hour 168 Hour Month Aphanocapsa muscicola 1359.91 274.64 374.31 353.11 264.83 0 0 1315.67 2451.03 Aphanothece castagnei 1922.48 881.96 189.10 372.73 887.10 0 0 511.63 523.13 Aphanothece pallida 0 259.76 350.61 156.94 0 0 0 390.46 0 Chroococcus pallidus 313.09 125.55 17.53 115.64 82.62 184.09 12.48 48.73 80.38 Chroococcus tenax 183.09 80.76 57.33 39.23 63.38 50.59 44.71 97.45 78.47 Diadesmis girdle sp. 1 437.59 91.55 27.01 160.21 44.14 262.16 37.45 171.65 44.77 Diatom girdle sp. 3 0 54.93 27.01 127.00 51.88 101.18 87.39 42.13 26.16 Eunotia girdle sp. 4 153.80 13.73 0 28.91 15.28 0 0 17.61 52.31 Gloeothece tepidariorum 496.13 80.10 0 82.60 0 50.59 0 194.91 104.63 Leptolyngbya cf. subtilissima 999.69 160.21 140.24 195.66 53.76 29.13 0 365.45 241.15 Meridion circulare (Greville) Agardh 153.56 0 35.06 0 63.38 0 17.48 24.52 0 Nitzschia sp. 1 915.47 247.18 298.01 251.75 158.45 151.78 145.30 176.05 31.39 Nostoc cf. microscopicum 24530.90 1177.03 1402.42 1055.20 1000.48 1821.30 1687.76 956.34 1098.56 Nostoc sp. 1 11260.27 3336.88 4926.00 4904.30 3392.62 5388.02 1657.83 4757.17 3315.78 Nupela sp. 1 62.02 11.44 17.53 22.89 0 39.86 12.48 0 20.10 Nupela sp. 2 84.22 22.89 17.53 57.82 80.78 48.47 37.45 88.03 27.46
131
Table 8. Taxa with the greatest median cell densities (cells/cm2) in all populations from Site 5; Health categories include: H=Healthy, MI=Moderately Impaired, D=Dead.
4 Week - Est. Control 1 Month Nostoc cf. microscopicum – H 24530.9 Nostoc sp. 1 - H 3392.62 Nostoc sp. 1 - H 3315.78 Nostoc sp. 1 - H 11260.27 Nupela sp. 2 - D 1433.79 Nupela sp. 2 - D 1124.72 Nostoc cf. microscopicum - Nitzschia sp. 1 - D 2197.13 Nitzschia sp. 1 - D 1009.71 H 1098.56 Aphanothece Nostoc cf. Aphanocapsa castagnei - H 1922.48 microscopicum - H 1000.48 muscicola - H 1004.78 Diadesmis girdle sp. Nitzschia sp. 1 - Nupela sp. 2 - D 1674.42 1 - D 735.64 MI 549.28 2 Week - 2 Week - 2 Week - 6 Hour 24 Hour 168 Hour Nostoc sp. 1 - H 3336.88 Nostoc sp. 1 - H 4926 Nostoc sp. 1 - H 4904.3 Nostoc cf. Nostoc cf. microscopicum - H 1177.03 microscopicum - H 1402.42 Nupela sp. 2 - D 1098.56 Nostoc cf. microscopicum - Nupela sp. 2 - D 631.67 Nupela sp. 2 - D 771.33 H 1055.2 Diadesmis girdle sp. Nitzschia sp. 1 - D 474.08 1 - D 525.91 Nitzschia sp. 1 - D 647.37 Aphanothece Diadesmis girdle castagnei - H 423.4 Nitzschia sp. 1 - D 499.76 sp. 1 - D 434.85 4 Week - 4 Week - 4 Week - 6 Hour 24 Hour 168 Hour Nostoc cf. Nostoc sp. 1 - H 5388.02 microscopicum - H 1687.76 Nostoc sp. 1 - H 4757.17 Nostoc cf. microscopicum - H 1821.3 Nostoc sp. 1 - H 1657.83 Nupela sp. 2 - D 1569.38 Nostoc cf. microscopicum - Nitzschia sp. 1 - D 1456.43 Nitzschia sp. 1 - D 592.39 H 956.34 Nupela sp. 2 - D 1369.04 Nupela sp. 2 - D 525.33 Nitzschia sp. 1 - D 882.77 Diatom girdle sp. 3 – Diatom girdle sp. 3 - Aphanocapsa D 733.58 D 324.14 muscicola - H 792.23
132
Table 9. Median relative abundance of the dominant common healthy taxa in all populations from Site 1; A taxon was considered dominant if it occurred with a median relative abundance > 1% in >3 samples.
2 Week - 2 Week - 2 Week - 4 Week - 4 Week - 4 Week - 4 Week - 1 Establishment 6 Hour 24 Hour 168 Hour Control 6 Hour 24 Hour 168 Hour Month Aphanocapsa cf. parietina 0 0 0 2.4 0 1.0 0 0 1.8 Aphanocapsa muscicola 12.2 16.3 18.6 9.5 14.3 10.2 7.9 9.3 14.1 Aphanothece castagnei 1.1 1.8 0 1.8 0 0 0 0 1.4 Chroococcus tenax 3.7 3.9 4.1 4.4 4.2 4.4 6.4 7.8 7.4 Gloeocapsa atrata 9.4 6.9 2.7 3.3 3.4 3.7 3.1 1.8 5.2 Gloeothece tepidariorum 1.9 2.2 3.8 3.7 4.4 5.0 3.8 3.7 8.4 Leptolyngbya "Albertano/Kovacik-green" 0.5 2.3 3.2 2.3 2.7 1.3 0.8 1.2 4.5 Leptolyngbya cf. subtilissima 27.5 26.0 29.3 22.7 20.9 24.4 25.6 29.3 23.7 Limnothrix spp. 3.5 3.4 3.6 5.9 2.0 1.2 2.6 4.4 1.8 Nostoc cf. microscopicum 9.4 1.1 0 2.3 2.9 12.4 0.9 1.8 4.8 Nostoc sp. 1 2.5 0.0 1.2 0.9 1.2 0.7 1.1 2.5 1.2 Pseudanabaena cf. minima 8.2 13.6 6.2 1.8 9.0 3.7 3.8 1.1 3.7
133
Table 10. Median relative abundance of the dominant common healthy taxa in all populations from Site 3; A taxon was considered dominant if it occurred with a median relative abundance > 1% in >3 samples.
2 Week - 2 Week - 2 Week - 4 Week - 4 Week - 4 Week - 4 Week - 1 Establishment 6 Hour 24 Hour 168 Hour Control 6 Hour 24 Hour 168 Hour Month Achnanthidium minutissimum 0.8 0.3 0.2 1.0 2.1 0.5 1.4 3.2 3.3 Aphanocapsa muscicola 12.1 20.7 7.8 11.3 12.1 10.4 11.6 8.3 15.4 Aphanothece pallida 1.7 0.0 0.0 0.0 1.2 0.0 2.3 3.9 2.5 Unknown Cyanobacterial Fil. 0.5 1.6 3.2 1.7 0.0 0.6 1.0 0.3 0.0 Chroococcus pallidus 1.9 1.0 0.6 0.5 0.8 0.5 0.7 0.0 1.9 Leptolyngbya cf. subtilissima 60.5 49.2 62.9 52.9 62.3 52.2 56.9 51.8 45.1 Nitzschia sp. 1 0.4 1.1 1.7 1.4 1.3 0.7 1.3 1.9 0.3 Phormidium cf. corium 0.0 0.0 2.8 0.8 0.5 0.0 1.8 0.0 1.3 Pseudanabaena cf. minima 0.0 1.5 0.5 2.5 0.5 0.0 1.3 0.0 0.0 Pseudanabaena sp. 2 1.0 1.6 0.0 0.3 0.9 1.2 0.7 0.5 0.6
134
Table 11. Median relative abundance of the dominant common healthy taxa in all populations from Site 5; A taxon was considered dominant if it occurred with a median relative abundance > 1% in >3 samples.
2 Week - 2 Week - 2 Week - 4 Week - 4 Week - 4 Week - 4 Week - 1 Establishment 6 Hour 24 Hour 168 Hour Control 6 Hour 24 Hour 168 Hour Month Aphanocapsa muscicola 0.8 2.9 1.1 2.4 2.1 0 0 6.7 7.9 Aphanothece castagnei 3.0 4.4 0 0 3.6 0 0 0 0 Diadesmis girdle sp. 1 0.3 1.0 0.2 1.1 0.4 0 0.3 1.0 0.2 Leptolyngbya cf. subtilissima 1.6 1.7 1.1 0.6 0.4 0 0 1.9 1.9 Nitzschia sp. 1 1.6 2.5 2.3 1.7 1.3 0.9 1.8 1.2 0.2 Nostoc cf. microscopicum 38.9 10.9 10.9 10.3 8.0 11.1 21.3 5.9 7.0 Nostoc sp. 1 16.7 26.3 36.6 34.7 23.6 32.9 26.0 30.8 26.1
135 FIGURES
Chapter II 136
Figure 1. Non-metric multidimensional scaling plot categorized by region (GSMNP=Great Smoky National Park and LSR=Lake Superior region) of species data for samples of aerial algal communities. Samples from the GSMNP formed two distinct clusters and were coded differently (GSMNP 1, GSMNP 2) to illustrate the separation.
137
Figure 2. Non-metric multidimensional scaling plot categorized by moisture categories of species data for samples of aerial algal communities from the Lake Superior region and the Great Smoky Mountains National Park.
138
Figure 3. Non-metric multidimensional scaling plot categorized by moisture of species data for samples of aerial algal communities from the Great Smoky Mountains National Park region.
139
Figure 4. Non-metric multidimensional scaling plot categorized by moisture categories of species data for samples of aerial algal communities from the Lake Superior region.
140
Figure 5. Non-metric multidimensional scaling plot categorized by region (GSMNP=Great Smoky National Park and LSR=Lake Superior region) of division data for samples of aerial algal communities.
141
Figure 6. Bubble plot of samples from NMDS ordination displaying relative abundance of each division in each sample from the Lake Superior region and the Great Smoky Mountains National Park (green =Chlorophyta, yellow=Bacillariophyta, red=Cyanophyta). Each sample is represented by a bubble and corresponds to the abundance of each division within that sample. Samples represented by one bubble were comprised of taxa from only one division, while samples represented by bubbles within bubbles were comprised of taxa from more than one division; abundance corresponds to size of bubble.
142
Figure 7. Bubble plot of samples from NMDS ordination displaying relative abundance of each division in each sample from the Great Smoky Mountains National Park (green =Chlorophyta, yellow=Bacillariophyta, red=Cyanophyta). Each sample is represented by a bubble and corresponds to the abundance of each division within that sample. Samples represented by one bubble were comprised of taxa from only one division, while samples represented by bubbles within bubbles were comprised of taxa from more than one division; abundance corresponds to size of bubble.
143
Figure 8. Bubble plot of samples from NMDS ordination displaying relative abundance of each division in each sample from the Lake Superior region (green =Chlorophyta, yellow=Bacillariophyta, red=Cyanophyta). Each sample is represented by a bubble and corresponds to the abundance of each division within that sample. Samples represented by one bubble were comprised of taxa from only one division, while samples represented by bubbles within bubbles were comprised of taxa from more than one division; abundance corresponds to size of bubble.
144 FIGURES
Chapter III 145
Figure 1. Non-metric multidimensional scaling plot categorized by bryophyte (Anoectangium euchloron, Campylopus umbellatus, Hyophila involuta, Hymenostylium recurvirostrum var. cylindricum, Macromitrium emersulum, Philonotis turneriana, Vesicularia perviridis, Weissia ovalis, and Liverwort) for species data of aerial algal community samples from Nu'uanu Pali.
146
Figure 2. Non-metric multidimensional scaling plot categorized by moisture category for species data of aerial algal community samples from Nu'uanu Pali.
147
Figure 3. Non-metric multidimensional scaling plot categorized by aspect (S=south, N= north, W= west) for species data of aerial algal community samples from Nu'uanu Pali.
148
Figure 4. Non-metric multidimensional scaling plot categorized by light (high, moderate, low) for species data of aerial algal community samples from Nu'uanu Pali.
149
Figure 5. Non-metric multidimensional scaling plot categorized by bryophyte (Anoectangium euchloron, Campylopus umbellatus, Hyophila involuta, Hymenostylium recurvirostrum var. cylindricum, Macromitrium emersulum, Philonotis turneriana, Vesicularia perviridis, Weissia ovalis, and Liverwort) for division data of aerial algal community samples from Nu'uanu Pali.
150
Figure 6. Non-metric multidimensional scaling plot categorized by moisture category for division data of aerial algal community samples from Nu'uanu Pali.
151
Figure 7. Non-metric multidimensional scaling plot categorized by aspect (S=south, N= north, W= west) for division data of aerial algal community samples from Nu'uanu Pali.
152
Figure 8. Non-metric multidimensional scaling plot categorized by light (high, moderate, low) for division data of aerial algal community samples from Nu'uanu Pali.
153
Figure 9. A. Non-metric multidimensional scaling plot (NMDS) for species data of aerial algal community samples from Nu'uanu Pali; B. Bubble plot of samples from NMDS ordination displaying relative abundance taxa from the Division Bacillariophyta in each sample; the larger the bubble the greater the abundance; C. Bubble plot of samples from NMDS ordination displaying light measurements from each sample; the larger the bubble the greater the light level; D. Bubble plot of samples from NMDS ordination displaying moisture levels from each sample; the larger the bubble the greater the amount of moisture. 154 FIGURES
Chapter IV 155
Figure 1. Box Plot of median algal cell densities of the populations (included all health categories) for the establishment, control, and treatment groups from Site 1.
156
Figure 2. Box Plot of median cell densities of the populations (included all health categories) for the establishment, control and treatment groups from Site 3.
157
Figure 3. Box Plot of median cell densities of the populations (included all health categories) for the establishment, control and treatment groups from Site 5.
158
Figure 4. Non-metric multidimensional scaling plot of species data for samples of algal communities from Site 1 categorized by treatment.
159
Figure 5. Bubble plot of samples from NMDS ordination displaying total cell density in each sample from Site 1. Each sample is represented by a bubble and corresponds to the total cell density within that sample; the larger the bubble the greater the density.
160
Figure 6. Non-metric multidimensional scaling plot of species data for samples of aerial algal communities from Site 3 categorized by treatment.
161
Figure 7. Bubble plot of samples from NMDS ordination displaying total cell density in each sample from Site 3. Each sample is represented by a bubble and corresponds to the total cell density within that sample; the larger the bubble the greater the density.
162
Figure 8. Non-metric multidimensional scaling plot of species data for samples of aerial algal communities from Site 5 categorized by treatment.
163
Figure 9. Bubble plot of samples from NMDS ordination displaying total cell density in each sample from Site 5. Each sample is represented by a bubble and corresponds to the total cell density within that sample; the larger the bubble the greater the density.