SIVER, PETER A.. AND JOSEPHINE S. HAMER. Multivariate

Limnol.
Oceanogr., 34(2), 1989, 368-381
Q 1989, by the American Society of Limnology
and Oceanography,
Inc.
Multivariate statistical analysis of the factors controlling the
distribution of scaled chrysophytes
Peter A. Siver
Department of Biological and Environmental
Sciences,
Western Connecticut State University, Danbury 068 10
Josephine S. Hamer
Department
of Mathematics,
Western Connecticut
State University
Abstract
A total of 332 collections from 62 water bodies was analyzed for scaled chrysophytes with
electron microscopy and correlated with limnological
characteristics. The pH and specific conductance were the most important factors controlling
the distribution
of scaled chrysophytes;
temperature and total phosphorus were of lesser importance.
A mean of nine and seven taxa per collection were recorded at a pH of 5.5-6.0 and a specific
conductance ~40 $S, respectively. Significantly fewer taxa per collection were found as the pH
lowered below 5.5 or raised above 6.0 or as the specific conductance increased above 40 $S. Similar
distributional
patterns were found for the genera Mallomonas, Synura, and Spiniferomonas.
A two-factor principal component model explained 70% of the total variance within the data
set (n = 1,355). The first principal component explained 80 and 83% of the total variance within
the pH and specific conductance variables. The pH and specific conductance also dominated the
first principal component for each genus and for 23 of the 25 species tested. A cluster analysis,
using within-group linkages, produced five groups of organisms that differed primarily with respect
to their distribution along a pH gradient.
Despite the importance of scaled chrysophytes in many freshwater systems, very little is known about the roles that different
environmental
factors play in governing
their distribution
(Smol et al. 1984; Kristiansen 1986). Until recent years, the scaled
chrysophytes had long been considered to
be primarily restricted to cold, oligotrophic
conditions
(Kristiansen
and Takahashi
1982). Although some taxa are true indicators of oligotrophic water bodies or are
restricted to cool temperatures, such characteristics cannot be used to describe the
group as a whole (Kristiansen
1986). Despite the growing volume of information on
the ecology of scaled chrysophytes, much of
it remains scattered and is only qualitative
in nature; there have been very few largescale ecological studies (Kristiansen 1986).
Members of the class Chrysophyceae
(Hibberd 1976) that bear siliceous scales are
placed into one of two families, the Mallomonadaceae or the Paraphysomonadaceae (Preisig and Hibberd 1983). Based on
biochemical and ultrastructural
characteristics, Andersen (1987) proposed that the
silica-scaled Mallomonadaceae be removed
from the class Chrysophyceae (sensu Hibberd 1976) and placed into a new class, the
Synurophyceae. In this paper, references to
scaled chrysophytes refer to genera classified in the Paraphysomonadaceae
(e.g.
Spiniferomonas and Chrysosphaerella) as
well as those transferred by Andersen ( 1987)
to the Synurophyceae (e.g. Mallomonas and
Synura).
Acknowledgments
We extend special thanks to Jim Roman0 and Alan
Wachtell at the University
of Connecticut for use pf
and assistance with SEM facilities, Regina Jones for
help with fieldwork, and Mary Jane Spring for help
with the illustrations. We also thank three anonymous
reviewers.
This work was supported in part by grants to Peter
A. Siver from the 1J.S. Dept. of Interior (14-08-0001.
G1412-04) and the CSU-AAUP
(1986-1988).
368
Recently, scaled chrysophytes have become integral components of paleolimnological efforts focused on reconstructing past
pH conditions in order to establish trends
in lake water acidification
patterns (Smol
1986; Davis and Smol 1986; Charles and
Smol 1988). Such efforts rely on the assumption that lake water pH is the primary
369
Factors controlling chrysophytes
Table 1. The number of collections (N) made within different range intervals (I) for pH, specific conductance,
water temperature, and total phosphorus levels. The midpoint (MP) values given were used to determine the
weighted means for individual taxa. The intervals described here were also used in Figs. l-4 and in the ANOVA
results presented in Table 2.
<5
25 -=z5.5
~5.5 < 6
26 -=L6.5
26.5 -=c7
17 < 7.5
27.5 < 8
28 < 8.5
-8.5
Temp
Sp cond. (/.tS)
PH
I
MP
N
4.75
5.25
5.75
6.25
6.75
7.25
7.75
8.25
8.75
22
6
35
67
71
42
22
19
15
MI’
I
120
>20
>40
>60
>80
>loo
>120
>140
>160
>180
5
I
I
I
40
60
80
100
zs 120
5 140
5 160
r 180
10
30
50
70
90
110
130
150
170
190
factor controlling the distribution of species
used in the pH inference models. Initial evidence indicates that pH is an important parameter involved in governing the distribution of scaled chrysophytes (Smol et al.
1984; Roijackers and Kessels 1986; Charles
and Smol 19SS), but many more data are
needed, especially at the species and subspecies levels, to verify the importance of
pH (Kristiansen 1986). Our purpose here is
to investigate the relative importance of pH,
temperature, specific conductance, and total
phosphorus levels in controlling the distribution of 25 common taxa of scaled chrysophytes.
Materials and methods
A total of 332 samples (293 from Connecticut
and 39 from the Adirondack
Mountain
region of New York) from 62
bodies of water (45 from Connecticut and
17 from the Adirondacks) was collected between September 1983 and October 1986
and analyzed with electron microscopy for
the presence of scaled chrysophytes. Four
major environmental
variables, temperature, pH, specific conductance, and total
phosphorus, known to influence the distribution of phytoplankton
species, were used
to characterize each sample; data were analyzed for 299 of the samples (Table 1). Missing data for six total phosphorus measurements were replaced with the mean value
for the given lake. The 299 samples (not the
lakes) were used to analyze the number of
taxa of scaled chrysophytes per collection
I
N
29
117
46
25
17
23
12
6
10
14
53
>3 I 6
>6 5 9
>9 5 12
>12 I 15
>15 4 18
>18 I 21
;;;
5 24
TP (pg-P liter-‘)
(“C)
MP
N
1.5
4.5
7.5
10.5
13.5
16.5
19.5
22.5
25.5
34
33
30
22
22
25
61
38
34
I
510
>lO I 20
>20130
>30 I 40
>40
MP
N
5
15
25
35
45
90
97
47
29
30
for each of the four environmental variables
(see Figs. l-4) and in the principal component analyses (PCA, see below). Complete
data sets for additional variables were not
available.
Sixteen of the Connecticut lakes were
sampled at least twice during spring, summcr, fall, and winter; the remaining 29 bodies of water were sampled at least once during each of the respective seasons. Ten of
the Adirondack lakes were sampled at least
once during each of the spring, summer, and
fall seasons; the remaining seven were sampled at most twice (details described by Siver 19886). We caution the reader that we
are analyzing the distribution
of taxa with
respect to environmental
variables and not
comparing among lakes. Details of water
chemistry and the distributions
of species
for individual lakes can be found elsewhere
(Siver 1987, 1988a,b).
Horizontal plankton net samples (lo-grn
mesh) and water samples were taken at a
depth of 2 m from the center of the lake or
at a 0.5-m depth along shore. Bodies of water
inaccessible by boat were sampled at specific sites along shore. For a given lake, samples were always collected at the same site.
Water samples were taken with a horizontal
Van Dorn bottle. For collections from under an ice cover, plankton net samples were
made by pouring water through the net.
Water temperature, pH, specific conductance, and total phosphorus levels were
measured in situ or from water taken at the
time of collection; methods for analyses were
370
Siver and Hamer
as described by Siver (1988b). Samples for
pH determination
were allowed to equilibrate with air. At certain times of year (e.g.
thermal stratification)
integrated samples,
instead of discre te samples, may have yielded additional taxa, but they were not used
because a correlation with a specific set of
temperature, pH, specific conductance, and
total phosphorus data would not have been
possible. Thus, in this study, only collections from discrete depths, correlated with
specific chemical data from that depth, were
used.
A portion of each water sample was con
centrated with centrifugation
for 8 min a,
2,000 rpm and used for analysis of scaled
chrysophytes with scanning electron microscopy (SEM). Plankton net samples were
often useful in facilitating species identification by providing larger quantities of material. Portions (1 ml) of each net and water
sample were dried onto separate pieces of
aluminum foil, rinsed twice with distilled
water, trimmed, mounted onto an aluminum stub with Apiezon wax, coated with
gold for 4.5 min with a Polaron sputter coater, and observed with a Coates and Welter
field emission SEM (15-2 1 kV).
Weighted mean values of pH, water temperature, specific conductance, and total
phosphorus were calculated for 25 taxa with
the equation
weighted factor mean
n
,= I
n
i=l
where Pi is frequency of occurrence of the
taxon in the ith interval (Table 1), X, is midpoint of the ith interval, and n is number
of intervals. Calculations of weighted mean
pH values were made directly from pH
measurements (geometric mean of hydrogen ion concentrations) (see Middleton and
Rovers 1986).
Categories for pH, originally defined by
Hustedt (1939) to describe the distributions
of diatom taxa, have been used in a similar
fashion for species of scaled chrysophytes
(Takahashi 1978; Roijackers and Kessels
1986; Kristiansen 1986). By observing frequency distributions with respect to pH and
weighted mean pH values, each of 25 scaled
chrysophyte taxa was assigned to a specific
Hustcdt category (see Table 7).
Analysis of variance (ANOVA) was used
to determine differences in the number of
taxa found per collection among intervals
for each environmental
factor; this determination was done for all taxa as a group
as well as for the genera Mallomonas, Synura, and Spinijkomonas. Principal component analysis (PCA) was used to extract
a two-factor model that explained the maximal percentage of the total variability within data sets for all taxa; the genera MaZZowonas, Synura, and Spiniferomonas; and
,ach of 25 species. Standardized measurements of pH, specific conductance, water
temperature, and total phosphorus were used
to construct the covariance matrices for the
PCA. Log,, transformations
were also used
in PCA for several of the more common
species; since the results were not considerably different from those found without
the transformation,
they were not reported.
Analyses for individual
species (or subspecific taxa) were done for only those organisms found in 15 or more of the collections.
Data for three rare species (Mallomonas canina, Mallomonas hindonii, and Mailomonas pugio), all found under similar environmental
conditions
(e.g. the same
localities), were combined for statistical
analysis; too few records existed for any one
of these species. Cluster analysis, with average within-group linkages (Niirusis 1985),
was used to group the 25 taxa into naturally
occurring assemblages. Differences between
groups were measured with squared Euclidean distance values according to the equation
distance = (Xi - 1q)2 + (Yi - Y,)2
where X, and Xj are the mean first principal
component scores for the ith and jth groups
and Yi and Yj are the mean second principal
component scores for the ith andjth groups.
The ANOVA,
PCA, and cluster analysis
were done on a VAX 8550 computer with
SPSSX (version 3.0) statistical programs
(Nijrusis 1985).
Results
Number of taxa per collection-Total
phosphorus
(TP) content
and water tem-
371
Factors controlling chrysophytes
ALL
SPECIES
1
I”
I
C
SYNURA
D
I
SPINIFEROMONAS
5
0
0
5
15
25
35
TOTAL
>40
5
PHOSPHOROUS
I5
( yg - P LITER
25
>40
-’ 1
Fig. 1. The mean number of species of scaled chrysophytes found per collection
phosphorus. The definition of each range is given in Table 1.
perature had little effect on the number of
scaled chrysophyte taxa per collection (Figs.
1 and 2). For each range of TP tested, no
significant differences in the number of taxa
per collection were found for all species, as
well as for the genera Mallomonas, Synura,
or Spiniferomonas (Fig. 1). Likewise, no differences in the number of scaled chrysophyte taxa, Mallomonas species, or Spiniferomonas species were found among the
nine categories of water temperatures tested.
Significantly
fewer species of Synura and
Spin@&-omonaswere found, however, above
2 1” or below 6°C respectively (Fig. 2 and
Table 2).
The pH and specific conductance had significant effects on the number of scaled
chrysophyte taxa per collection (Figs. 3 and
4). A mean of nine species of scaled chrysophytes per collection was recorded between
a pH range of 5.5 and 6.0 (Fig. 3A). Fewer
taxa were found as the pH increased above
6.0; fewer than two taxa per collection were
35
for different
ranges of total
found above pH 8.0 (Fig. 3A). Likewise, the
number of taxa per collection was reduced
significantly in waters with a pH < 5.5, but
four-five taxa per collection were still present. The same pattern was found for the
genera Mallomonas and Synura (Fig. 3B,
C). No differences in the number of species
of Spiniferomonas were found between pH
values of 5 and 8, but significantly
fewer
species were found below pH 5 and above
pH 8 (Fig. 3D and Table 2).
An average of seven species of scaled
chrysophytes per collection was found for
all samples from waters with specific conductance values ~40 PS (Fig. 4A). Significantly fewer species per collection were recorded as the specific conductance increased
above 40 pS; fewer than two taxa per collection were found in waters above 160 PLS
(Table 2). A similar trend was found for
species of Mallomonas, Synura, and Spiniferomonas (Fig. 4B, C, D). For each genus
and for all scaled chrysophytes, slightly few-
No R.H. on this page!! . . .
MALLOMONAS
ALL SPECIES
6
I
.4
0
1.5
19.5
135
7.5
25.5
TEMPERATURE
Fig. 2.
As Fig. I, but for different
RANGE (“C )
ranges of water temperature.
ALL SPECIES
8
6
6.75
775
SPINIFEROMONAS
D
SYNURA
8.75
4.75
575
pH RANGE
Fie. 3.
As Fig. 1, but for different
ranges of pH.
675
775
8.75
Factors controlling chrysophytes
Table 2. Results of ANOVA for the number of taxa
found per collection based on modified categories of
pH, specific conductance, and water temperature. The
criteria defining each modified category are listed below. (Asterisks: *- significant at 0.05 level; **-significant at 0.01 level.)
Taxon
PH
Sp cond.
Temp
1,2**
3**
3**
3**
3*
4**
5**
Total
Mallomonas
Synura
Spiniferomonas
Category criteria: 1 -pH
5 5 vs. pH >5<8; 2-pH
>518 vs. pH 2 8;
3-flS 5 40 vs. pS > 40; 4--“C 5 21 vs. “C > 21; 5--“C 5 6 vs. “C
z 6.
er species per collection were found in bodies ofwater with specific conductance values
~20 PS when compared to those between
21 and 40 $S (Fig. 4).
Principal component analysis-A
twofactor model with PCA explained 70% of
the total variance within the data set for all
scaled chrysophytes (n = 1,35 5); a similar
percentage of the total variance was explained with a two-factor model for the genera Mallomonas (7 lo/o), Synura (67%), and
373
Spiniferomonas (7 1%) (Table 3). In each instance, the first PC was strongly dominated
by both pH and specific conductance. Considering this model, for all species, the first
PC explained 83 and 80% of the total variance of specific conductance and pH (Table
3); similar results were found for the genera
Mallomonas and Spiniferomonas.
Although the first PC was still dominated by
pH and specific conductance for Synura, a
slightly lower percentage (-70%) of the total variance was explained. The second PC
was dominated by either temperature (Mallomonas), total phosphorus (Synura), or
both (Spiniferomonas and all species).
Similar results of PCA were found for individual taxa of Mallomonas, Synura, and
Spiniferomonas (Tables 4, 5, and 6). Between 6 1 and 83% of the total variance in
the data sets were explained by a two-factor
model for all 25 taxa. Except for Mallomonas galeiformis and Mallomonas acaroides v. muskokana, pH and specific conductance strongly dominated the first PC
(Tables 4-6). There were many instances
ALL SPECIES
MALLOMONAS
3
6
.
0
0
IO
50
90
I30
170
CONDUCTIVITY
Fig. 4.
As Fig. 1, but for different
IO
50
90
(JJS )
ranges of specific conductance.
13Q
170
Siver and Hamer
374
analysis for the scaled chrysophyte genera Mallomonas, Synura,
The percentage (% 2: F) of the total variation within each data set
explained by a two-factor model is presented. The variables that dominate (dom. var.) each of the first (PC 1)
and second (PC 2) principal components, as well as the percentage of the variation (% S2) within those variables
explained by the respective PC are given.
Table 3. Results of principal
component
Spin$?romonas, and all species collectively.
PC I
-Taxon
No. cases
O/oz s-2
Mallomonas
724
71
Synura
380
67
Spiniferomonas
252
71
1,355
70
All species
Dom.
PC 2
% s*
Cond.
PH
PH
Cond.
Dom.
86
77
70
68
85
83
83
80
PH
Cond.
Cond.
PH
var.
% s2
Temp
72
TP
99
TP
Temp
Temp
TP
64
50
62
51
the first PC for only M. galeijbrmis and M.
acaroides v. muskokana; total phosphorus
never dominated the first PC.
For individual
taxa the second PC was
usually dominated by water temperature,
tota.l phosphorus, or both. Water tempera-
where > 80% of the total variance in the pH,
specific conductance, or both were accounted for by the first PC; for four species, e.g.
Spin$eromonas coronacircumspina, 90% or
more of the variance was explained. Water
temperature was a dominant variable for
Table 4.
var.
As Table 3, but for species of Malfomonas.
-
=
-
-~
-=
PC 1
-Taxon
No. cases
% z s
Dom.
var.
M. canina/pugiolhindonii
15
83
PH
Cond.
M. tonsurata
48
82
M. porlae-ferreae
15
- 80
M. crassisquama
96
77
M. pseudocoronata
29
77
M. acaroides v. acaroides
15
77
PH
Cond.
Cond.
PH
PH
Cond.
Cond.
PH
PH
Cond.
M. punctifera
25
76
PH
Cond.
M. heterospina
21
76
M. corymbosa
15
76
M. akrokomos
71
74
M. galeiformis
28
73
PH
Cond.
Cond.
PH
Cond.
PH
Cond.
Temp
156
72
M. acaroides v. muskokana
37
70
M. hamata
86
69
M. caudata
PH
Cond.
Temp
PH
PH
Cond.
PC 2
% s2
87
77
90
87
85
82
84
81
88
70
83
76
84
62
83
71
86
58
90
68
75
62
84
84
74
68
85
72
Dom.
var.
--% s2
80
TP
Temp
Temp
TP
Temp
TP
TP
72
73
64
66
63
81
Temp
91
Temp
99
TP
Temp
Temp
67
53
74
Temp
94
Temp
91
TP
PH
TP
Temp
TP
Cond.
TP
64
64
60
58
66
58
78
375
Factors controlling chrysophytes
Table 5. As Table 3, but for species of Synura.
PC 2
PC 1
Taxon
No. cases
S. uvella
29
% z s2
Dom.
83
PH
var.
Cond.
S. spinosa
68
72
PH
Cond.
S. petersenii
156
71
PH
Cond.
S. echinulata
S. sphagnicola
65
38
66
PH
61
Cond.
Cond.
PH
ture strongly dominated
the second PC for
Mallomonas pseudocoronata (9 1O/o),Mallomonas acaroides v. acaroides (99%), Mallomonas heterospina (74%), Mallomonas
corymbosa (94%) Mallomonas akrokomos
(9 lo/o), and Synura echinulata (87%) (Tables
4 and 5). Total phosphorus strongly dominated the second PC for Synura spinosa
(94%), Synura petersenii (96%) and Spiniferomonas bourrellyi (99%) (Tables 5 and
6).
Cluster analysis of taxa-A cluster analysis using within-group
linkages and based
on the first and second principal component
scores produced five clusters (Fig. 5). The
clusters differed, and were generally well
distinguished when projected onto an ordination plot, by their mean pH and specific
conductance values (Fig. 6 and Table 7).
Taxa within group 1 had weighted mean pH
and specific conductance values ranging
from 6.0 to 6.9 and 33 to 59 PS and were
either acidophilous or pH-indifferent
in na-
O/os2
Dom.
var.
% 5-2
88
77
86
67
78
71
72
50
65
39
TP
61
TP
94
TP
96
Temp
87
TP
Temp
65
53
ture (Table 7). Species of group 1 had
weighted mean temperature values commonly found during spring and fall months
and moderate levels of TP. Group 2 comprised taxa with the lowest weighted mean
pH, specific conductance, and TP values
(Table 7). Except for Mallomonas punctifera, all species in group 2 were acidobiontic
in nature and commonly found in waters
with pH < 5.5. Although M. punctzjera disappeared below a pH of about 5.5, it was
an acidophilous species restricted to localities with a pH <7 and low in specific conductancc. Both M. punctijera and AL acaroides v. muskokana were warm-water
species.
Mallomonas tonsurata, the only species
in group 3, had high weighted pH, specific
conductance, temperature, and TP means
(Table 7); it clearly separated from the other
clusters on its PC scores (Figs. 5 and 6).
Species within group 4 had weighted mean
pH values ranging from 6.0 to 6.5 and pre-
Table 6. As Table 3, but for species of Spinijkomonas.
PC I
Taxon
S. bilacunosa
No. casts
27
% z s
82
Dom.
var.
Cond.
PH
S. coronacircumspina
27
75
Cond.
PH
S. bourrellyi
34
73
Cond.
PH
S. trioralis
S. serrata
102
30
70
PH
70
Cond.
Cond.
PH
PC2
% L1’2
92
76
94
93
83
81
81
80
75
72
Dom.
var.
% s2
TP
Temp
Temp
TP
TP
76
64
57
54
99
TP
Temp
TP
Temp
61
56
64
62
Siver and Hamer
376
Taxon
Group
AVERAGE
WITHIN-GROUP
DISPERSION AS PERCENT OF TOTAL
--S. uvella
C. longispina
Sp. serrata
S. petersenii
Sp. bourrellyi
S. spinosa
Sp. bilacunosa
M. crassisquama
M. caudata
Sp. coronacircumspina
CM. tonsurata
M. akrokomos
a. v. acaroides
M. portae-ferreae
5P--l-
-
Fig. 5. Result of a cluster analysis for 25 taxa of scaled chrysophytes based on their distributions with respect
to pH, specific conductance, water temperature, and total phosphorus in 62 bodies of water. The mean values
of the first and second principal component scores were used as the clustering variables. Five naturally occurring
clusters (groups) are recognized. Weighted mean, pH, specific conductance, temperature, and total phosphorus
values fdF all-25 taxa are-given in Table 7.
ferred relatively low specific conductance
values and low to moderate phosphorus
Levels (Table 7). Mallomonas heterospina,
with the lowest weighted mean temperature,
did not join group 4 until the within-group
dispersion (Niirusis 1985) was 75%; the dispersion between the other three taxa within
group 4 was much less (Figs. 5 and 6). Group
5 comprised species with weighted mean pH
and specific conductance values above 7.1
and 8 1 PS and high levels of TP; all taxa in
group 5 were alkalibiontic
or alkaliphilous
in nature (Table 7).
Discussion
In recent years great emphasis has been
placed on analyzing stratigraphic profiles of
siliceous microalgal populations from lake
sediments in order to reconstruct historical
lake water conditions (e.g. Bradbury 1975;
Battarbee 1986; Munch 1980; Davis et al.
1983; Davis and Anderson 198 5; Charles
and Norton 1986; Smol et al. 1986). The
bulk of this research has focused on the reconstruction of past pH conditions in order
to establish trends in lake water acidity
caused by naturally occurring events, disturbances to the watershed, or acid deposition (Davis and Smol 1986). Diatoms have
been used in most studies, but scaled
chrysophytes have become an increasingly
integral part OF such paleolimnological
efforts (Smol 1986; Charles and Smol 1988;
Davis and Smol 1986).
Kristiansen (1986) listed three prerequisites for an organism to be a useful biolog-
377
Factors controlling chrysophytes
5-
___--- __--- - ia,
'2
\
I
'\ '\
'\\\ El
j
\ '\
II
\\
\\
I
“\d
0
-5--iO-15-20
I
IO
I
20
FIRST
I
30
PRINCIPAL
'\\
,
40
I
50
COMPONENT
\
'\\
I
60
@j
I
70
SCORE
Fig. 6. Ordination plot of 25 species of scaled chrysophytes on the first and second principal component
axes. Five clusters (groups), each defined by dashed lines, are as determined by the cluster analysis presented
in Fig. 5. The numbers refer to the species number given in Table 7. The taxa are primarily separated along the
first PC axis according to their wcightcd mean pH and specific conductance values. Symbols reflect the weighted
mean pH for each taxon (O-pH
< 6; O-6 I pH < 7; O-pH
2 7).
ical indicator: it must be taxonomically well
defined; it must be easily identifiable and
not be confused with other taxa; and it must
be distributed within a “narrow ecological
spectrum.” In addition, it is essential that
the occurrence of the organism in a given
body of water be primarily related to and
controlled by the environmental
factor in
question (e.g. pH). Thus, the relative importance of lake water acidity vs. other parameters in determining the distribution
of
a given species should be known before its
use as an indicator for pH.
Since the 1960s when electron microscopy became a standard tool in identifying
species of scaled chrysophytes, the results
from many studies have collectively documented the distributions of taxa in lake regions throughout the world. Although many
of these works lack critical environmental
data, a few have provided valuable insight
into the importance of pH as a factor regulating the distribution
of scaled chrysophytes. Takahashi (1967) concluded that differences in pH were more important than
water temperature in controlling the distribution of species. Kristiansen (1975) pro-
vided pH and temperature frequency distribution records for species of Synura and
concluded that some taxa were more commonly found in acidic (e.g. Synura sphagnicola) or alkaline (e.g. Synura uvella) waters
although others (e.g. S. petersenii) were indifferent to pH. Similarly, Takahashi (1978)
arranged 33 species of scaled chrysophytes
into the pH categories of Hustedt (1939).
Kristiansen (1985) reported the presence of
33 species in a highly eutrophic lake with a
pH range from 8.2 to 9.1; because many of
the taxa had not previously been reported
at such a high pH, yet had been reported
from habitats as low as pH 4-5, he (Kristiansen 1986) stressed that caution must be
exercised in using species as indicators of
PH.
None of the above-cited works dealing
with living populations
addressed, using
proper statistical methods, the relative importance of pH as compared to other environmental
parameters in controlling the
distribution
of scaled chrysophytes. In the
present study, PCA was used to demonstrate that lake water pH or pH in combination with specific conductance was in-
378
Siver and Hamer
Table 7. Weighted mean pH, specific conductance, temperature, and total phosphorus values for 25 taxa
separated into five groups by cluster analysis. The cluster analysis used within-group linkages and was based on
the first and second principal component scores for each taxon. The pH categories are according to Hustedt’s
(1939) system (ACB-acidobiontic;
ACF-acidophilous;
IND-pH-indifferent;
ALKF-alkaliphilous;
ALKBalkalibiontic).
Species No. correspond to the numbers on Fig. 6.
Species
No.
Hustedt
46
29
38
28
39
37
31
13
36
35
9
C. longispina
S. spinosa
Sp. bourrel[vi
S. petersenii
Sp. serrata
Sp. bilacunosa
S. uvella
M. caudata
Sp. coronacircumspina
Sp. trioralis
M. crassisquama
Group
ACF
ACF
ACF
ACF/IND
ACF
IND
IND
IND
IND
IND
IND
52
51
6
30
4
M. pugio/caninalhindonii
M. acaroides v. muskokana
S. sphagnicola
S. echinulata
M. punctifera
1
2
5
7
8
---
Taxon*
--~-~
12
3
11
53
PH
Sp cond. @S)
Temp (“C)
TP
(pg-P liter-‘)
--
1
6.0
6.1
6.1
6.2
6.4
6.5
6.6
6.7
6.7
6.7
6.9
40
41
41
45
33
47
53
54
59
56
57
14.8
11.3
13.8
12.6
15.3
19.5
17
15
17.4
17.2
15
16
17
17
17
18
18
20
17
14
19
19
Group 2
ACB
ACB
ACB
ACB/ACF
ACF
4.9
5.3
5.3
5.9
5.9
37
28
30
40
32
14
20
14
15
20
11
12
8
17
16.8
M. tonsurala
Group 3
ALKF/ALKB
7.6
83
17
28
M. hamata
A4. heterospina
M. galeiformis
M. akrokomos
Group 4
ACB/ACF
ACF
ACF
1ND
6.0
6.3
6.3
6.5
36
60
29
50
13.7
6
18.5
12
13
17
11
17
M.
M.
AL
M.
Group 5
ALKF
ALKF
ALKF
ALKB
7.1
7.3
7.7
8.1
86
81
99
112
15
19
15.6
14.1
21
17
25
24.5
* Chrysosphaerella-C.;
portae-ferreae
pseudocoronata
corymbosa
acaroides v. acaroides
Synura-S.;
Spinl~~rornonas-Sp.;
--
~--
Mallomonas-M.
strumental in controlling the occurrence of
taxa at the class, genus, species, and subspecies levels; water temperature and TP
played secondary roles in governing the
distributions
of taxa. Perhaps water temperature and TP are more instrumental in
controlling when, and to what degree, a population of a given species develops in a given
lake.
Such a conclusion is supported by two
additional studies where multivariate
statistical procedures were used on large data
sets of scaled chrysophytes. In a study of
scaled chrysophytes in 50 bodies of water
from the Netherlands, Roijackers and Kessels (1986) found that the first PC was
strongly dominated by pH and accounted
for 57% of the total variance in the data set.
The second PC, identified as water temperature, accounted for an additional 35% of
the variance. Roijackers and Kessels ( 1986)
concluded that pH was the more important
variable for determining
the presence of
scale-bearing taxa in a given body of water,
whereas water temperature controlled biomass levels. In an excellent study using reciprocal averaging, Smol et al. (1984) examined the relationships
between scaled
chrysophyte assemblages in surficial sediments and 17 characteristics for 38 lakes in
the Adirondack Mountains of New York.
They found that the first reciprocal averaging axis was highly correlated with pH (r
= 0.79) and pH-related parameters.
Factors controlling chrysophytes
379
in studies where electron microscopy is not
There is little question that pH is instrumental in governing the distributions
of used. For example, in electron microscopic
work, Siver (1988a) found species of Spiniscaled chrysophyte taxa. The effects that
factors which covary with pH play in the feromonas in 40% of the 113 collections
Skogstad
distribution of this algal group, however, are from localities in Connecticut;
( 19 86) observed populations of Spiniferofor the most part unknown. It is possible
monas in 23 of 27 localities from southern
that one or more of the covarying parameters exerts equal or greater influence on the Norway. Similarly, Nicholls (1984) reportdistribution
of a given species used as an ed the occurrence of Spimj?eromonas triorah from 40% of all collections from Onindicator organism for pH. In this situation,
and
pH inference would be correct only if the tario lakes. Despite the common
worldwide distribution
of the genus Spinicorrelation between the controlling factor(s)
and pH remained constant (Davis and Smol feromonas, it has not been recorded in many
1986). Yet pH and specific conductance were studies (e.g. Schindler and Holmgren 197 1;
Duthic and Ostrofsky 1974; Arvola 1986;
significantly correlated in collections from
Connecticut
lakes. Thus, additional
re- Kwiatkowski and Roff 1976). A similar case
can be made for many species of Mallosearch is needed to further explore the relmonas and Synura. The underestimation of
ative importance of pH, specific conducsilica-bearing
taxa in light microscopic
tance, and other possible covarying factors
studies is due, in part, to the poor preserin controlling the distributions of individual
vation of cells and the resultant disarticuspecies. Culture and field experiments will
lation of the siliceous coat (Wee 1983; Taybe instrumental in answering this question.
lor et al. 1986).
Since pH and specific conductance dominated the first PC for most species of scaled
It is well known that the acidification of
chrysophytes, it was not surprising that these lakes results in a major reduction in the
factors were most significant in controlling
species richness and diversity of phytothe number of species present in a given
plankton communities
(e.g. Hornstrom et
body of water. In general, the largest numal. 1973; Hendrey et al. 1976; Almer et al.
ber of taxa would most often be found in
1974, 1978; Yan and Stokes 1978; Eloranta
acidic bodies of water with a pH > 5.5 and
1986). The largest reduction in species richspecific conductance ~40 pS. Water temness is usually recorded from pH 6 to 5. The
perature and TP concentrations were usu- most striking change is the virtual disapally of secondary importance in controlling
pearance of most planktonic species of diathe occurrence of individual species and had toms and blue-greens at a pH between 5.5
little effect on the number of species found
and 5. In our study the reduction in the
per collection. Such an observation sup- number of species of scaled chrysophytes
ports the “new” idea that chrysophytes are below a pH of 5-5.5 was significant but less
not restricted to oligotrophic habitats (Krisdramatic than that reported for the Baciltiansen 198 5, 1986) and cold tcmperaturcs
lariophyceae and Cyanophyceae.
Species
(Kristiansen and Takahashi 1982).
within groups 3 and 5 were alkalibiontic
or
Most phytoplankton
studies that do not alkaliphilous,
rarely found below a pH of
incorporate electron microscopy rarely re- 6.3 and never recorded below pH 5.5. The
cord more than a few species of scaled maximal frequencies of occurrences for the
chrysophytes in a given sample. Since it was acidophilous
and pH-indifferent
species
common to find more than seven species within groups 1 and 4 were generally beper sample, it is safe to conclude that the tween pH 5.5 and 6.5; except for Malloimportance of scaled chrysophytes in phymonas hamata, however, each taxon within
toplankton floras is often underestimated.
groups 1 and 4 either disappeared or had a
By electron microscopy, many species of significantly reduced occurrence below pH
scaled chrysophytes have been shown to be 5.5. Except for M. punctzjkra, which also
very common in nature (Takahashi 1978; disappeared below a pH of 5, all taxa within
Kristiansen
1986; Roijackers and Kessels group 2 and M. hamata were as common
1986). but thev are seldom if ever reported
or had maximal frequencies of occurrence
I
380
Siver and Hamer
below pH 5.5. In general, taxa within groups
3 and 5 were restricted to more hard-water
habitats and not found in the same lakes as
species within group 2.
The slight reduction in number of taxa
per collection at < 20 PS was due to the fact
that most of the samples with a pH < 5 also
had specific conductance values ~20 pS.
When the collections with a pH ~5 were
removed from the data set, no decrease in
the number of species in samples at <20 PS
was observed.
Many of the most commonly reported
species of scaled chrysophytes that are found
over wide ranges of environmental
conditions clustered into group 1. For example,
S. petersenii (Nicholls and Gerrath 1985;
Siver 1987), Mallomonas crassisquama
(Siver and Skogstad 1988), and Spinij&omonas trioralis (Nicholls 1984; Siver 1988a)
are generally regarded as the most commonly occurring species within their respective genera; each of these species and
Mallomonas caudata, the most abundant
taxon in this study, clustered into group 1.
Most taxa for which water temperature
dominated either the first or second PC had
fairly restricted distributions with respect to
temperature. Maliomonas galellformis and
A!I. acaroides v. muskokana, the only species
for which water temperature dominated the
first PC, were both strictly warm-water
forms. Synura echinulata, not found during
the warmer summer months, had maximal
occurrence between 6” and 20°C. Mallomonas heterospina and A4 akrokomos were
most often found at low temperatures, M.
pseudocoronata during spring and summer
months, and M. corymbosa during spring
and fall. Mallomonas acaroides v. acaroides
had a variable occurrence with respect to
water temperature.
Synura sphagnicola, known to be a warmwater species (Asmund 1968; Kristiansen
1975; Siver 1987), was found only during
summer and early fall months. Because it
was also restricted to bodies of water low
in TP, however, it is not surprising that both
temperature and TP controlled the second
PC.
In summary, the lake water pH is instrumental in controlling
the distribution
of
scaled chrysophyte taxa at the species and
subspecies levels. Thus, this organismal
group represents an excellent biological indicator for pH.
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Submitted: 2 I March 1988
Accepted: 15 July 1988
Revised: 15 December I988