J. Phycol. 38, 265–272 (2002)
THE IMPORTANCE OF DIATOM CELL SIZE IN COMMUNITY ANALYSIS 1
Pauli Snoeijs,2 Svenja Busse, and Marina Potapova3
Department of Plant Ecology, Evolutionary Biology Centre, Uppsala University, Villavägen 14, SE-75236 Uppsala, Sweden
The large variation in size and shape in diatoms is
shown by morphometric measurements of 515 benthic
and pelagic diatom species from the Baltic Sea area.
The largest mean cell dimension (mostly the apical
axis) varied between 4.2 and 653 m, cell surface area
between 55 and 344,000 m2, and cell volume between 21 and 14.2 106 m3. The shape-related index, length to width ratio, was between 1.0 and 63.3
and the shape- and size-related index, surface area to
volume ratio, was between 0.02 and 3.13. Diatom
community analysis by multivariate statistics is usually
based on counts of a fixed number of diatom valves
with species scores irrespective of cell size. This procedure underestimates the large species for two reasons. First, the importance of a species with higher
cell volume is usually larger in a community. Second,
larger species usually have lower abundances and
their occurrence in the diatom counts is stochastic. This
article shows that co-occurring small and large diatom
species can respond very differently to environmental
constraints. Large epiphytic diatoms responded most
to macroalgal host species and small epiphytic diatoms most to environmental conditions at the sampling site. Large epilithic diatoms responded strongly
to salinity, whereas small epilithic diatoms did so less
clearly. The conclusion is that different scale-dependent responses are possible within one data set. The
results from the test data also show that important
ecological information from diatom data can be missed
when the large species are neglected or underestimated.
the global ocean production (Treguer et al. 1995),
and a carbon fixation estimate of 53.2 1015 g Cyr–1
for global terrestrial primary production (Melillo et
al. 1993). Besides their importance in the oceans, diatoms are widely distributed in almost any (semi-)
aquatic habitat. This great success of diatoms as a
group is coupled to the large variety in size and shape
among species, which provides a variety of interaction
strategies with the environment.
There is an enormous range in cell size among diatoms, which spans from small species (e.g. Stephanodiscus and Cyclotella spp.), with a minimum diameter of
ca. 3 m, a surface area of ca. 28 m2, and a cell volume of ca. 10 m3, to very large species, such as Ethmodiscus with a maximum diameter of ca. 2 mm (Hustedt 1927–1930), a surface area of ca. 34 106 m2,
and a cell volume of ca. 12.5 109 m3. When considering the photosynthetically active surface area, this
difference exceeds that between a 2-cm high grass
with 10 leaves and a 10-m high tree with 100,000
leaves. Large differences in size among species in an
ecological community pose two kinds of size-related
problems for synecological analysis. First, it is difficult
to define a “correct” weight for the different species
in a numerical analysis because differences in scale
between the message transmitter (environment) and
receiver (alga) will give asymmetry in relationships
(Allen 1977). For example, when using abundances,
the importance of the larger species is underestimated, and when using biomass, that of the smaller
species is underestimated. This problem can be partly
resolved by using (log-) transformed abundance scores.
Also, larger species are usually less abundant than
smaller ones in ecological communities because the
maximum specific growth rates in algae decrease with
increasing cell size (Raven and Geidler 1988, Mizuno
1991). Therefore, the probability of encountering large
species when recording species composition is small
and their occurrence in diatom counts is stochastic.
This may lead to false ecological interpretations. The
message that large diatoms need to be studied separately was put forward already by Hustedt (1957, p.
187), and later by Simola (1990) but has in practice
been neglected in studies on diatom assemblage or
community composition (e.g. ter Braak and van Dam
1989, Hall and Smol 1992, Anderson et al. 1995, Snoeijs 1995, Laing et al. 1999, Stevenson and Pan 1999).
Besides size, the variety in shape among diatom
species is of ecological relevance because it affects surface area to volume ratios and thereby a cell’s relative
area exposed to the environment (Lewis 1976, Chisholm 1992). This is also a variable within species; for
example, Potapova and Snoeijs (1997) showed that
Key index words: community ecology; diatoms; multivariate statistics; scale; shape; size
Abbreviations: AA, apical axis; L/W, ratio of the largest dimension (“length”) to second largest dimension
ratio (“width”); PA, pervalvar axis; psu, practical salinity units (g salt per kg water); S/V, surface area
to volume ratio; TA, transapical axis
Recent estimates for the number of extant diatom
species are about 200,000 (Mann and Droop 1996).
Diatoms contribute at least 23% to the earth’s primary production, based on a carbon fixation estimate
of 25.8 1015 g Cyr1 for diatoms, which is 43% of
1
Received 11 June 2001. Accepted 10 December 2001.
Author for correspondence: e-mail [email protected].
3 Present address: Patrick Center for Environmental Research, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, PA 19103-1195, USA.
2
265
266
PAULI SNOEIJS ET AL.
the changes in cell proportions of Diatoma moniliformis
Kützing during its life cycle fit well with annual
growth cycles, with high surface area to volume ratios
during the period of optimal growth in spring.
The aims of the present study were to summarize
size- and shape-related qualities of a large number of
diatom species from the Baltic Sea area and to test if
small and large diatom species respond differently to
environmental constraints when co-occurring in the
same diatom community.
materials and methods
Measurements of size. The valve sizes of 515 diatom taxa from
epiphytic, epilithic, sediment-associated, and pelagic diatom
communities along the Swedish coast (from the Skagerrak to
the northern Bothnian Bay) and the Gulf of Finland (see map
in Snoeijs 1995) were measured. The vast majority of the taxa
are different species, but some nominal forms and varieties are
considered separately (see Appendix in on-line version). The
term “species” is used throughout this article to denote different
taxa, including these varieties. Most studied species are illustrated
in Snoeijs (1993), Snoeijs and Vilbaste (1994), Snoeijs and Potapova (1995), Snoeijs and Kasperoviciene (1996), and Snoeijs
and Balashova (1998). The diatoms were embedded in Naphrax
(refractive index 1.74, Northern Biological Supplies Ltd., Ipswich,
UK), and dimensions were measured under a light microscope
at magnification 1000. In most cases, the two dimensions appearing most abundantly on the slides were measured. For pennate diatoms, these were usually the apical axis and the transapical axis but were sometimes the apical axis and the pervalvar
axis (PA). For centric diatoms, sometimes only measurements of
the diameter could be taken. The third dimension, most often
the PA but sometimes the transapical axis, was measured on the
permanent slides (if possible) or estimated from electron micrographs as a mean percentage of the transapical axis or the diameter. For each species, the measurements were made on 10
or 25 specimens representing one population (sample). Usually, standard deviations for small species had already stabilized
when 10 specimens were measured, but for larger species 25
specimens were necessary to obtain stable standard deviations.
Calculations of size- and shape-related parameters. The cell volume,
the cell surface area, the surface area to volume ratio (S/V) and
the ratio of the largest dimension (“length”) to second-largest dimension ratio (“width”) (L/W) were calculated from means of
the 10 or 25 measurements for each species. Cell volume and
surface area were calculated based on rectangularity, which is defined as the area enclosed by the outline of a diatom valve expressed as a proportion of the area of its enclosing rectangle
(Droop 1994). Rectangularity was measured on electron and
light micrographs. For diatoms with an uneven PA, a mean value
of the PA was used in combination with rectangularity. S/V can
be considered a combined measure of size and shape, whereas
L/W is a measure of shape only. The biovolume should not include the vacuole volume, which is larger in larger diatoms
(Sicko-Goad et al. 1985), but we did not correct for this.
Epiphyton community data. The epiphyton data set consists of
48 samples, 12 samples (4 replicates per host species) from
each of 4 sampling sites in the Gräsö area. Two sampling sites
were situated on the eastern side of the island Gräsö and were
exposed to the open Baltic Sea: Björnören S (Site 63: 60 24
50 N, 18 28 24 E) and Björnören N (Site 64: 60 24 54 N,
18 28 21 E). The other two sampling sites were situated on
the western side of Gräsö in a ca. 2-km wide channel between
the island and the mainland: Djursten (Site 68: 60 22 16 N,
18 24 11 E) and Gräsö Ferry (Site 69: 60 21 03 N, 18 27
53 E). At each site, four replicate samples were taken of each
of three filamentous macroalgal hosts, Pilayella littoralis (L.)
Kjellmann (Phaeophyta), Ceramium gobii Wærn (Rhodophyta),
and Cladophora glomerata (L.) Kützing (Chlorophyta). All samples were taken on 13 and 14 May 1990, and the sampling sites
did not vary in salinity (5 practical salinity units [psu]), exposure to wave action, or nutrient concentrations in the water.
The major environmental differences between the samples
were site location and macroalgal host. For further site descriptions and sampling procedures, see Snoeijs (1994).
The diatoms were separated into two size classes. It was difficult to decide where to place the boundary between large and
small diatoms because no distinct size groups were found
among the 515 investigated species. Therefore, an artificial distinction was made by classifying species with a mean volume
1000 m3 as “small” and species with a mean volume 1000
m3 as “large.” This limit lies at species with a minimum length
of ca. 20 m, which can be recognized and counted at magnification 200 or 400. From each sample, 250 diatom valves
were identified and counted at 1000 (Data “all species”). After this, counting was continued for small species ( 1000 m3)
only, until a total of 250 diatom valves of small species was obtained (Data “small species only”). On a separate slide with a
higher density of diatom valves, 250 valves of large species
(1000 m3) were identified and counted at magnification
200 (Data “large species only”). The relative abundances were
transformed to relative diatom cell volumes and relative diatom
surface areas. Altogether, nine epiphyte data sets were tested
with different recording scales (abundance, cell volume, surface area) and including small species only, large species only,
or both.
Epilithon community data. The epilithon data set consists of
24 samples, 4 replicate samples from each of 6 sampling sites in
the Bothnian Bay. Two sampling sites were situated in each of
three areas with different salinities, with one of the sites exposed to strong or moderate wave action and the other site little exposed to wave action: Area 10 (Holmön: Sites 147 [63 48
47 N, 21 00 46 E] and 159 [63 46 37 N, 20 49 45 E], 3.0
and 3.1 psu), Area 11 (Skellefteåhamn: Sites 171 [64 41 15 N,
21 18 44 E] and 176 [64 37 54 N, 21 17 19 E], 2.6 and 2.4
psu), and Area 13 (Rånefjärden: Sites 179 [65 46 49 N, 22
27 58 E] and 181 [65 48 44 N, 22 29 21 E], 0.9 and 0.5
psu). All samples were taken 27–31 May 1991. The major environmental differences between the sites were wave action (referred to as “more wave action” and “less wave action,” respectively) and salinity. Salinity was strongly correlated with water
silicate concentrations, but these were high everywhere and
thus never limiting for diatom growth. For further site descriptions and sampling procedures, see Busse and Snoeijs (2002).
From each sample, 250 valves of small diatom species (
1000
m3) were identified at 1000 (Data “small species only”), together with x large species (1000 m3) that came along with
these (Data “all species,” n 250 x). On a separate slide with
a higher concentration of diatom valves, 125 valves of large species were identified and counted at magnification 1000 (Data
“large species only”). Only abundance scores were used in the
analyses.
Data analysis. Multivariate statistical analysis was performed
by correspondence analysis (CA) (Jongman et al. 1987) with
the program CANOCO (ter Braak and Smilauer 1998). No data
transformations or down-weighting of rare species were applied. Dummy variables with the possible scores of either “1” or
“0” were constructed for nominal-scale variables (categories):
host–site combinations (epiphytic data) and wave action–area
combinations (epilithic data). These dummy variables were
tested passively on the results of the CA ordination by multiple
regression analysis and centroids show their relative positions
in the ordination plots. These centroids are thus in all analyses
each based on 1000 diatom valves, except for the epilithic large
diatoms for which the centroids are based on 500 valves.
results
Cell surface area. Mean cell surface areas varied between 55 m2 for Nitzschia inconspicua Grunow and
344,000 m2 for the pelagic centric diatom Coscinodiscus
wailesii Gran and Angst (Fig. 1a, Appendix). The pen-
DIATOM SIZE AND COMMUNITY ANALYSIS
nate diatom with the highest surface area was Nitzschia
scalaris (Ehrenberg) W. Smith (63,000 m2). The median cell surface area was 1093 m2, and 95% of the
species had cell surface areas between 57 and 23,000
m2 (factor 400). The species with the largest cell
surface areas were found in the genera Campylodiscus,
Coscinodiscus, Nitzschia, Pleurosira, and Rhizosolenia.
Cell volume. Mean cell volume varied between 21
m3 for Nitzschia inconspicua and 14.2 106 m3 for
Coscinodiscus wailesii (Fig. 1b, Appendix). The pennate diatom with the highest volume was Tryblionella
circumsuta (Bailey) Ralfs in Pritchard (440,000 m3).
The median cell volume was 1718 m3, and 95% of
the species had cell volumes between 31 and 113,000
m3 (factor 3600). The species with the largest volumes were found in the genera Coscinodiscus, Pleurosira, Rhizosolenia, Surirella, and Tryblionella. Of the 515
diatom species, 43% had a cell volume 1000 m3
(classified as small diatoms in this article) and 57% a
cell volume 1000 m3 (classified as large diatoms in
this article); 3% were very close to the cut-off between
the two groupings (i.e. between 900 and 1100 m3).
Surface area to volume ratio. Mean S/V varied between
0.02 m1 for Coscinodiscus wailesii and 3.13 m1 for
Nitzschia paleacea (Grunow) Grunow (Fig. 2, Appendix).
The median S/V was 0.66 m1 and 95% of the species had S/Vs between 0.2 and 2.6 m1 (factor 13).
The species with the largest S/V were small and thin
Achnanthes, Catenula, Cylindrotheca, and Nitzschia species.
Length to width ratio. Mean L/W varied between 1.0
for most centric species and 63.3 for the centric Proboscia alata (Brightwell) Sundström (Fig. 2, Appendix). The pennate diatom with the highest L/W was
Pseudonitzschia pungens (Grunow) Hasle (L/W 50).
267
The median L/W was 2.9, and 95% of the species had
L/W between 1 and 15 (factor 15). The species with
the largest L/W were large and thin Nitzschia, Proboscia, Pseudonitzschia, Rhizosolenia, Synedra, and Tabularia
species.
Shape. When considering cell shape, centrics and
small roundish pennates (e.g. Staurosira spp.) were
closest to a sphere (L/W 1.0–2.0) and thereby had
the smallest S/Vs relative to their largest dimension
(Fig. 2). When cells got thinner (L/W gets larger),
their S/Vs became larger relative to their largest dimension (L). There was no relationship between shape
or size with life form (epipelic, metaphytic, epiphytic,
epipsammic, or pelagic), except that all epipsammic
species were small and that many pelagic species were
centrics. There were diatoms of all shapes in all size
classes, with a weak trend of getting thinner with increasing length.
Community analysis of epiphyton data. The most abundant diatom taxa in the epiphyton data set are summarized in Table 1. The degree of importance of the large
taxa in the epiphyton communities depended on the
measure used to express their weight in the data set.
When expressed on the basis of abundance their importance was ca. 10% (Fig. 3a), on the basis of surface area
ca. 40% (Fig. 3b), and on the basis of volume ca. 60%
(Fig. 3c). Figure 4 shows the results of the CA analyses
using relative abundance scores. The large species
showed a pattern according to host alga with Pilayella
littoralis in the right half of the ordination, Cladophora
glomerata in the lower left quadrant, and Ceramium gobii in the upper left quadrant (Fig. 4a). No pattern
with sampling site was found for the large species.
Contrarily, the distribution of the small species was
Fig. 1. Size-related properties of 515 diatom species from the Baltic Sea area related to the mean cell length (largest mean linear dimension). (a) Mean cell surface area. (b) Mean cell volume. The thick horizontal line indicates the median where half of the
values are above and the other half below. The thin lines indicate the upper and lower limits where 95% of the values are in between.
268
PAULI SNOEIJS ET AL.
the left (Fig. 4b). In the combined data set (Fig. 4c),
the separations of both sampling site and host were
less clear than in each of the separate CA runs for
large and small species. CA analyses using relative volume or relative surface area scores resulted in less welldefined separation patterns than the relative abundance data. For example, compared with Figure 4a,
both volume- and surface-based scores placed Pilayella
(PILA) from site 68 far away from the other PILA centroids and Ceramium (CERA) and Cladophora (CLAD)
were separated from PILA, but not from each other.
Community analysis of epilithon data. The most abundant diatom species in the epilithon data set are summarized in Table 2. The mean relative abundance (
SD) of the large species varied between 2.1 1.5 and
12.2 2.2. Figure 5 shows the results of the CA analyses using relative abundance scores. The large species
showed a pattern according to the differences in salinity between the three sampling areas (Fig. 5a). The
small species separated Area 10 and Area 13 but not
Area 11 with a salinity in between Areas 10 and 13
(Fig. 5b). The combined data set (Fig. 5c) gave almost
the same results as the small species only.
Fig. 2. Illustration of the relationship between size and
shape. Mean surface area to volume ratio of 515 diatom species
from the Baltic Sea area related to the mean cell length (largest
mean linear dimension), subdivided into shape groups according
to the mean length to width ratio shown as different symbols.
not related to macroalgal host, but there was a pattern
according to sampling site with the two sites from the
eastern side of the island to the right of the ordination and those from the western side of the island to
discussion
Diatom dimensions and environmental effects. It is difficult to define a “correct” weight for the different
Table 1. Epiphyton data set, showing the diatom taxa with a relative abundance of at least 3% for at least one host/site combination.
VOL
(m3)
269
696
74
21
124
698
129
400
24
3535
1104
3156
2402
1451
1722
4178
38844
1958
11967
9525
1866
22046
2841
Diatom taxon
“Small” taxa
Diatoma moniliformis Kützing
Tabularia sp. ‘laev’
Navicula perminuta Grunow in Van Heurck
Nitzschia inconspicua Grunow
Gomphonemopsis exigua (Kützing) Medlin
Rhoicosphenia curvata (Kützing) Grunow
Tabularia waernii Snoeijs
Berkeleya rutilans (Trentepohl) Grunow
Achnanthidium cf. minutissimum (Kützing)
Czarnecki
Total abundance (%)
“Large” taxa
Ctenophora pulchella (Ralfs ex Kützing) Williams
& Round
Tabularia fasciculata (C. A. Agardh) Williams &
Round
Gomphonema olivaceum (Hornemann) Brébisson
Mastogloia smithii Thwaites
Surirella brebissonii Krammer & Lange-Bertalot
Cocconeis pediculus Ehrenberg
Navicula lanceolata (C. A. Agardh) Ehrenberg)
Licmophora gracilis var. anglica (Kützing)
H. & M. Peragallo
Diatoma vulgaris Bory
Tabularia tabulata (C. A. Agardh) Snoeijs
Surirella crumena Brébisson ex Kützing
Epithemia sorex Kützing
Epithemia turgida var. westermannii (Ehrenberg)
Grunow
Diatoma bottnica Snoeijs
Total abundance (%)
VOL Cell volume.
PILA CLAD CERA PILA CLAD CERA PILA CLAD CERA PILA CLAD CERA
63
63
63
64
64
64
68
68
68
69
69
69
56
9
8
5
5
4
3
—
67
1
7
5
—
15
3
—
45
—
9
21
4
13
1
1
55
10
7
4
2
6
4
3
63
2
11
3
—
15
2
—
58
1
4
8
1
16
3
1
76
1
3
6
—
10
—
—
71
—
4
7
—
13
—
—
65
—
2
9
—
19
—
1
74
1
6
5
—
2
—
8
80
—
6
4
—
5
1
1
73
—
3
4
—
18
1
1
1
92
1
97
4
98
1
91
—
95
—
93
—
97
—
95
1
97
—
96
1
99
—
99
58
7
2
62
16
8
39
5
3
44
17
11
26
5
3
2
2
—
2
24
1
1
59
1
1
42
6
2
33
—
17
6
3
5
2
1
4
37
3
4
23
1
4
30
18
5
16
1
8
15
3
2
3
6
2
16
—
1
71
2
2
39
2
1
38
3
44
6
—
2
—
2
22
26
—
—
32
1
11
64
—
—
9
1
—
—
—
—
—
—
—
—
—
1
—
—
—
—
4
—
—
1
—
—
—
—
3
—
1
1
—
3
—
4
5
5
4
3
1
1
—
—
—
—
6
2
—
—
2
—
—
1
—
—
—
1
1
—
—
—
1
—
—
—
—
1
97
1
2
97
3
1
95
1
—
97
1
3
97
1
3
94
—
—
93
—
—
98
1
—
97
—
—
99
1
—
100
1
—
99
DIATOM SIZE AND COMMUNITY ANALYSIS
269
Fig. 3. Proportions of the large diatom species (1000
m3) in the epiphyton communities, expressed as (a) abundance, (b) surface area, and (c) cell volume. CERA, Ceramium
gobii; CLAD, Cladophora glomerata; PILA, Pilayella littoralis. The
numbers 63, 64, 68, and 69 represent the four sampling sites.
Error bars show the SD of n 4 samples.
species in a numerical analysis because differences in
scale between an environmental variable and the algal
response will give asymmetry in relationships (Allen
1977). We show large differences in mean cell size
among 515 diatom species from benthic and pelagic
diatom communities in the Baltic Sea area. These
large differences give rise to the question of which parameter (abundance, surface area, or cell volume) is
most appropriate for use in statistical analyses between environmental factors and diatom communities. For example, when the environmental variable is
a nutrient concentration, it will interact with the cell
surface and the surface area (as a constraint for the
nutrient uptake) will be important, thus a surface-related species measure such as S/V seems appropriate
to use. In the case of water movement, cell volume
(weight) might be more appropriate, as well as in the
case of grazing where each specific grazer is coupled
to a preferred food object size. Also, colony formation
may affect the surface area exposed to the environment. Thus, different and complicated types of interactions exist within one data set. We made comparisons of the use of relative abundances, cell volume,
and surface area on the epiphyton data set and found
that the use of abundances yielded the best separation
Fig. 4. Ordination plots for three CA analyses of the epiphyton data using relative abundance scores, showing centroids
for host/site combinations (multiple regression: P 0.05). (a)
Large species only, (b) small species only, and (c) all species.
CERA, Ceramium gobii; CLAD, Cladophora glomerata; PILA, Pilayella littoralis. The numbers 63, 64, 68, and 69 represent the
four sampling sites. The eigenvalues of the ordination axes are
given between brackets.
patterns in CA. This is because the larger species receive too much weight when expressed as cell volume
or surface area and create an unbalanced data set,
even within the two separate data sets of small and
large species.
Diatom dimensions are not stable. Another factor that
makes it difficult to define a correct measure for the
different species in a numerical analysis is that diatom
dimensions are not stable. The cell volume of a diatom species depends on its genetically fixed range but
is modified by life cycle and environmental conditions. Snoeijs and Potapova (1997) showed that the
cell volume of Diatoma moniliformis varies between ca.
100 and ca. 600 m3 during the life cycle and that
highest S/V is reached at ca. 300 m3 in fast-growing
270
PAULI SNOEIJS ET AL.
Table 2. Epiphyton data set, showing the diatom taxa with a relative abundance of at least 3% for at least one area/wave exposure
combination.
VOL
(m3)
749
698
77
123
423
123
639
341
215
709
41
269
54
364
3535
6146
1722
3156
22046
1104
1451
4013
66737
1869
2498
1866
3037
6216
2402
3083
Diatom taxon
“Small” taxa
Diatoma tenuis C. A. Agardh
Rhoicosphenia curvata (Kützing) Grunow
Achnanthidium minutissimum (Kützing) Czarnecki
Fragilaria sp. (small)
Cymbella sp. (small)
Fragilaria cf. vaucheriae (Kützing) J. B. Petersen
Denticula tenuis var. crassula (Naegeli) W. & G. S. West
Berkeleya fennica Juhlin-Dannfelt
Amphora coffeaeformis (C. A. Agardh) Kützing
Brachysira vitrea (Grunow) R. Ross in B. Hartley
Fragilaria sp. (small)
Encyonopsis sp. (small)
Amphora veneta Kützing
Encyonema silesiacum (Bleisch) D. G. Mann in Round et al.
Staurosira elliptica (Schumann) Williams & Round
Diatoma moniliformis Kützing
Planothidium cf. delicatulum (Kützing) Round & Bukhtiyarova
Martyana schulzii (Brockmann) Snoeijs
Total abundance (%)
“Large” taxa
Ctenophora pulchella (Ralfs ex Kützing) Williams & Round
Cymbella helvetica Kützing
Cocconeis pediculus Ehrenberg
Gomphonema olivaceum (Hornemann) Brébisson
Epithemia turgida var. westermannii (Ehrenberg) Grunow
Tabularia fasciculata (C. A. Agardh) Williams & Round
Surirella brebissonii Krammer & Lange-Bertalot
Navicula rhynchocephala Kützing
Thalassiosira baltica (Grunow) Ostenfeld
Encyonema caespitosum Kützing
Amphora copulata (Kützing) Schoeman & Archibald
Epithemia sorex Kützing
Encyonema lacustre (C. A. Agardh) D. G. Mann in Round et al.
Rhopalodia gibba (Ehrenberg) O. Müller
Mastogloia smithii Thwaites
Mastogloia smithii var. amphicephala Grunow
Total abundance (%)
Area 10
EXP
Area 10
QUI
Area 11
EXP
Area 11
QUI
Area 13
EXP
Area 13
QUI
69
8
6
3
3
2
2
1
—
—
—
1
—
—
—
—
—
—
95
80
3
2
2
1
2
—
—
—
—
—
—
—
—
—
—
—
—
90
65
1
16
4
3
1
2
—
—
—
—
—
—
—
—
1
—
—
94
7
—
34
3
1
1
8
13
6
2
2
1
2
—
—
—
1
1
81
3
1
27
9
2
6
3
1
—
3
9
8
3
2
2
—
1
1
81
18
1
9
7
1
5
—
—
—
—
6
—
1
5
7
4
3
3
70
22
21
20
13
6
3
1
—
1
1
1
1
—
—
—
1
91
24
17
12
12
1
2
8
7
5
2
1
1
—
—
—
—
91
15
42
—
13
—
1
6
3
—
2
—
5
1
—
—
—
89
2
44
—
1
—
—
12
14
—
2
3
3
—
2
—
1
85
12
8
—
1
1
1
5
4
—
3
—
19
24
3
3
2
86
10
2
—
1
5
2
9
4
—
4
1
11
—
11
14
12
86
VOL Cell volume, EXP More exposed to wave action, QUI Less exposed to wave action.
populations. The mean volume varied between ca. 150
and ca. 300 m3 during a 3-year period with monthly
samplings. Snoeijs (1992) showed that the mean apical axis of Ctenophora pulchella (Ralfs) Williams and
Round and Tabularia cf. laevis populations in the Bothnian Bay was more than double that in Baltic Sea
proper, which also indicates that the environment (in
this case salinity) may affect size, probably by ecotypic
differentiation. To obtain stable SDs, about 25 specimens from each species should be measured, except
for the very small ones (Snoeijs 1995, Hillebrand et al.
1999). This would imply that for correct cell volume
and surface area quantification it is necessary to measure the dimensions of 25 specimens of each species in
each sample. In relation to the information obtained,
this is far too laborious.
Community analysis. We identify here the problem
that counts of a fixed number of diatom valves of large
and small species together, as currently practiced by
(palaeo-) ecologists, might neglect the important ecological information that can be obtained from the larger
species. Phytoplankton counts often include counts at
different levels of microscopic magnification (Edler
1979). However, the statistical error is still considerable
for species present with only a few scores, a problem addressed earlier by Venrick (1978). Large species usually
have low abundances, and their occurrence in diatom
counts is stochastic and thus not ecologically relevant.
Even if the stochastics are taken out by additional
counts of large diatoms that are made separately and
included in the final data set with the small diatoms
according to a large/small ratio, the ecological importance of the large diatoms will still be underestimated.
Recommendations. We recommend counts and analyses of relative abundances of large and small diatoms
separately in the same way as field layer and tree layer
are usually analyzed separately in community analysis
of terrestrial plants. This article shows that small and
large species may respond differently to the same
environmental constraints when co-occurring in the
same diatom community. Unfortunately, the limit between small and large is more difficult to define for
DIATOM SIZE AND COMMUNITY ANALYSIS
271
cies. This might suggest that counts of the larger diatoms only would be sufficient to describe community
responses. However, the results from the epiphytic
data set show that the small diatoms also respond
strongly and specifically to environmental conditions
but that these can be other environmental conditions
than the ones decisive for the distribution of the large
diatoms. Analyses of a large data set of epilithic diatom communities along the salinity gradient of the
northern Baltic Sea (Busse and Snoeijs 2002) showed
that large diatoms respond more strongly to salinity
and small diatoms to exposure to wave action.
Financial support was provided by the Swedish Research Council (VR), by the International Association for the Promotion of
Cooperation with Scientists from the Independent States of the
former Soviet Union (INTAS), and by PhD-research fellowships
to Svenja Busse from the FAZIT-Foundation of the “Frankfurter
Allgemeine Zeitung” and the Consul Karl and Dr Gabriele Sandmann Foundation (KKGS-Stiftung), Berlin, Germany. We thank
Heikki Simola (University of Joensuu, Finland) and two anonymous reviewers for critical comments on the manuscript and
the more than 40 members of the Baltic Marine Biologists Working Group 27 for cell measurements of 150 of the 515 species.
Fig. 5. Ordination plots for three CA analyses of the epilithon data using relative abundance scores, showing area/wave
action centroids (multiple regression: P 0.05). (a) Large species only, (b) small species only, and (c) all species. The eigenvalues of the ordination axes are given between brackets.
diatoms than for terrestrial plants. Our suggestion for
a limit at 1000 m3 seems appropriate. Two data sets
with similar species richness are obtained, and in each
of these the size range is small enough to allow comparisons based on simple abundance records. Our results also show that a better response to important environmental variables, such as salinity or substratum,
is obtained from the large species. This could be related to life history strategies. The smallest and largest
diatoms in diatom communities may be considered
analogues to herbs and mature forest trees in terrestrial plant communities, respectively. Following life history theories (MacArthur and Wilson 1967, Grime 1979,
Silvertown et al. 1993), small fast-growing species are
usually less specialized than large slow-growing spe-
Allen, T. F. H. 1977. Scale in microscopic algal ecology: a neglected
dimension. Phycologia 16:253–7.
Anderson, N. J., Renberg, I. & Segerström, U. 1995. Diatom production responses to the development of early agriculture in a
boreal forest lake-catchment (Kassjön, northern Sweden).
J. Ecol. 83:809–22.
Busse, S. & Snoeijs, P. 2002. Gradient responses of epilithic diatom
communities in the Bothnian Bay, northern Baltic Sea. Nova
Hedwigia 74: in press.
Chisholm, S. W. 1992. Phytoplankton size. In Falkowski, P. G. &
Woodhead, A. D. [Eds] Primary Productivity and Biochemical Cycles in the Sea. Plenum Press, New York, pp. 213–37.
Droop, S. J. M. 1994. Morphological variation in Diploneis smithii
and D. fusca (Bacillariophyceae). Arch. Protistenk. 144:249–70.
Edler, L. 1979. Recommendations for marine biological studies in the
Baltic Sea: phytoplankton and chlorophyll. Baltic Mar. Biol. 5:1–38.
Grime, J. P. 1979. Plant Strategies & Vegetation Processes. John Wiley &
Sons, New York, 222 pp.
Hall, R. I. & Smol, J. P. 1992. A weighted-averaging regression and
calibration model for inferring total phosphorus concentrations from diatoms in British Columbia (Canada) lakes. Freshw.
Biol. 27:417–34.
Hillebrand, H., Dürselen, C., Kirschel, D., Pollinger, U. & Zohary,
T. 1999. Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 35:403–24.
Hustedt, F. 1927–1930. Die Kieselalgen Deutschlands, Österreichs
und der Schweiz mit Berücksichtigung der übrigen Länder Europas sowie die angrenzenden Meeresgebiete. Dr. L. Rabenhorsts Kryptogamen-Flora 7/1. 920 pp.
Hustedt, F. 1957. Die Diatomeenflora des Flusystems der Weser
im Gebiet der Hansestadt Bremen. Abh. naturw. Ver. Bremen
34:181–440.
Jongman, R. H. G., ter Braak, C. J. F. & van Tongeren, O. F. R.
1987. Data Analysis in Community and Landscape Ecology. Pudoc,
Wageningen, 299 pp.
Laing, T. E., Pienitz, R. & Smol, J. P. 1999. Freshwater diatom assemblages from 23 lakes located near Norilsk, Siberia: a comparison with assemblages from other circumpolar treeline regions. Diatom Res. 14:285–305.
Lewis, W. M. 1976. Surface/volume ratio: implications for phytoplankton morphology. Science 192:885–7.
MacArthur, R. H. & Wilson, E. O. 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, 203 pp.
272
PAULI SNOEIJS ET AL.
Mann, D. G. & Droop, S. J. M. 1996. Biodiversity, biogeography and
conservation of diatoms. Hydrobiologia 336:19–32.
Melillo, J. M., McGuire, A. D., Kicklighter, D. W., Moore, B., Vorosmarty, C. J. & Schloss, A. L. 1993. Global climate change and
terrestrial net primary production. Nature 363:234–40.
Mizuno, M. 1991. Influence of cell volume on the growth and
size reduction of marine and estuarine diatoms. J. Phycol.
27:473–8.
Potapova, M. & Snoeijs, P. 1997. The natural life cycle in wild populations of Diatoma moniliformis (Bacillariophyceae) and its disruption in an aberrant environment. J. Phycol. 33:924–37.
Raven, J. A. & Geidler, R. J. 1988. Temperature and algal growth.
New Phytol. 110:441–61.
Sicko-Goad, L. M., Schelske, C. L. & Stoermer, E. F. 1985. Estimation of intracellular carbon and silica content of diatoms from
natural assemblages using morphometric techniques. Limnol.
Oceanogr. 29:1170–8.
Silvertown, J. W., Franco, M., Pisanty, I. & Mendoza, A. 1993. Comparative planned demography: relative importance of life-cycle
components to the finite rate of increase in woody and herbaceous perennials. J. Ecol. 81:465–76.
Simola, H. 1990. Look at the big ones. Abstracts of the 11th International Diatom Symposium, San Francisco, USA. p. 106. San Francisco State University.
Snoeijs, P. 1992. Studies in the Tabularia fasciculata complex. Diatom
Res. 7:313–44.
Snoeijs, P. [Ed.] 1993. Intercalibration and Distribution of Diatom
Species in the Baltic Sea, Volume 1. Opulus Press, Uppsala,
129 pp.
Snoeijs, P. 1994. Distribution of epiphytic diatom species composition, diversity and biomass on different macroalgal hosts along
seasonal and salinity gradients in the Baltic Sea. Diatom Res.
9:189–211.
Snoeijs, P. 1995. Effects of salinity on epiphytic diatom communi-
ties on Pilayella littoralis (Phaeophyceae) in the Baltic Sea. Ecoscience 2:382–94.
Snoeijs, P. & Balashova, J. [Eds.] 1998. Intercalibration and Distribution of Diatom Species in the Baltic Sea, Volume 5 (including
check-list). Opulus Press, Uppsala, 141 pp.
Snoeijs, P. & Kasperoviciene, J. [Eds.] 1996. Intercalibration and Distribution of Diatom Species in the Baltic Sea, Volume 4. Opulus
Press, Uppsala, 125 pp.
Snoeijs, P. & Potapova, M. [Eds.] 1995. Intercalibration and Distribution of Diatom Species in the Baltic Sea, Volume 3. Opulus Press,
Uppsala, 125 pp.
Snoeijs, P. & Potapova, M. 1997. Ecotypes or endemic species? A hypothesis on the evolution of Diatoma taxa (Bacillariophyta) in
the northern Baltic Sea. Nova Hedw. 67:303–48.
Snoeijs, P. & Vilbaste, S. [Eds.] 1994. Intercalibration and Distribution
of Diatom Species in the Baltic Sea, Volume 2. Opulus Press, Uppsala, 125 pp.
Stevenson, R. J. & Pan, Y. 1999. Assessing environmental conditions
in rivers and streams with diatoms. In Stoermer, E. F. & Smol,
J. P. [Eds] The Diatoms: Applications to the Environmental and Earth
Sciences. Cambridge University Press, Cambridge, pp. 11–40.
ter Braak, C. J. F. & Smilauer, P. 1998. CANOCO Reference Manual
and User’s Guide to CANOCO for Windows. Centre for Biometry,
Wageningen, 351 pp.
ter Braak, C. J. F & van Dam, H. 1989. Inferring pH from diatoms: a
comparison of old and new calibration methods. Hydrobiologia
178:209–23.
Treguer, P. Nelson, D. M., Van Bennekom, A. J., DeMaster, D. J.,
Leynaert, A. & Queguiner, B. 1995. The silica balance in the
world ocean: a reestimate. Science 268:375–9.
Venrick, E. L. 1978. How many cells to count? In Sournia, A. [Ed.]
Phytoplankton manual. UNESCO Monographs on Oceanographic
Methodology. United Nations Educational, Scientific and Cultural Organization, Paris, 6:167–80.