Hydrobiologia DOI 10.1007/s10750-008-9521-y
PRIMARY RESEARCH PAPER
Ecological variation within Sellaphora species complexes (Bacillariophyceae): specialists or generalists? Aloisie Poulı´cˇkova´ Æ Jana Sˇpacˇkova´ Æ Martyn G. Kelly Æ Martin Duchoslav Æ David G. Mann
Received: 27 March 2008 / Revised: 26 June 2008 / Accepted: 7 July 2008 Ó Springer Science+Business Media B.V. 2008
M. G. Kelly Bowburn Consultancy, 11 Monteigne Drive, Bowburn, Durham DH6 5QB, UK e-mail:
[email protected]
species are ecologically differentiated with respect to trophic status, we used tools recently developed in the UK in response to the EU Water Framework Directive (WFD). Diatom samples from three substrata (plants, rocks, sediment) were taken from 22 lakes in Scotland and England, covering a gradient from oligotrophic mountain lakes to eutrophic lowland ponds. The epilithic and epiphytic diatom assemblages were used to evaluate lake trophic status according to the UK WFD assessment system and showed that there was a strong environmental gradient in the dataset. Sellaphora species occurred in the sediment-derived epipelon and their distributions were analysed in relation to the trophic gradient. A total of 28 Sellaphora phenodemes (putative species) were found, and some of them differed in their environmental demands. Two groups were distinguished: (1) a group indicating rather oligotrophic conditions and containing several demes with linear valves and subcapitate or capitate poles (referred to here as S. [pupula] cap-A, cap-B and cap-C and (2) a group occurring in eutrophic lakes and containing the recently described species S. blackfordensis, S. capitata and S. obesa, as well as S. [pupula] U ‘small lanceolate’. The data obtained are also discussed with respect to Finlay’s hypothesis on microalgal cosmopolitanism.
D. G. Mann Royal Botanic Garden, Edinburgh EH3 5LR, Scotland, UK e-mail:
[email protected]
Keywords Epipelon Diatoms Cryptic species Ecological differentiation Water Framework Directive Ubiquity hypothesis
Abstract The genus Sellaphora has become a model system for studies of the species concept, speciation and automated identification in diatoms. Three species, S. pupula, S. bacillum and S. laevissima, have proved to be complexes containing several or many species, which are difficult to distinguish morphologically but which are genetically differentiated and (where tested) reproductively isolated. Until now, however, there has been little information about the ecology of the species within this complex, except in relation to parasite sensitivity. In order to test whether semi- and pseudo-cryptic Sellaphora
Handling editor: J. Padisak A. Poulı´cˇkova´ (&) J. Sˇpacˇkova´ M. Duchoslav Department of Botany, Faculty of Science, Palacky´ University, Svobody Str. 26, 771 46 Olomouc, Czech Republic e-mail:
[email protected]
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Hydrobiologia
Introduction Diatoms play a key role in the functioning of many ecosystems and are used as bioindicators of water quality and past climates (Stoermer & Smol, 1999). Despite their significance, however, many aspects of the biodiversity, ecology and geographical distribution of diatoms are poorly understood. There is, for example, debate about whether distributions of diatoms are (Telford et al., 2006, 2007; Vyverman et al., 2007) or are not (Finlay et al., 2002; see also BaasBecking, 1934, Finlay, 2002) dispersal-limited. Finlay et al. (2002) distinguished two types of freshwater species, the first comprising cosmopolitan diatoms with broad ecological tolerance (generalists) and the second comprising diatoms with more exacting requirements (specialists), which consequently occur at only a few locations. Recent evidence from molecular data and mating experiments has shown, however, that traditional diatom morphospecies (i.e. species defined solely on the basis of a visual assessment of differences in shape, size, patterning and ultrastructure of their silica frustules) are often heterogeneous, containing several to many subtly differing taxa (Mann, 1999; Behnke et al., 2004; Mann et al., 2004; Sarno et al., 2005; Amato et al., 2007; Evans et al., 2007, 2008). Similar phenomena have been recorded among marine diatoms (Lundholm et al., 2006; Amato et al., 2007) and in many other, unrelated groups of organisms, and there can be significant differences in ecology between related cryptic species (Bruna et al., 1996; Dawson & Jacobs, 2001; Kucera & Darling, 2002; Rocha-Olivares et al., 2004, Miura et al., 2006; Fernandez et al., 2006). Sellaphora pupula (Ku¨tzing) Mereschkowsky (formerly Navicula pupula Ku¨tzing) is a common, cosmopolitan freshwater species according to the major diatom floras (e.g. Hustedt, 1930, 1927–1966; Proshkina-Lavrenko, 1950; Krammer & Lange-Bertalot, 1986). This epipelic diatom has long been known to be very variable (e.g. Hustedt, 1927–1966, p. 121; Schoeman & Archibald 1976–1980; Krammer & Lange-Bertalot 1986), and the apparently high degree of intergradation was used as an argument against splitting the species or even the recognition of varieties and forms within it. Recent research has revealed, however, that the ‘intergradation’ is deceptive. Instead, Sellaphora pupula is a complex containing many pseudo- and semi-cryptic species
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(Mann, 1984, 1989, 1999; Mann & Droop, 1996; Mann et al., 1999, 2004; Behnke et al., 2004; Evans et al., 2007, 2008). Slight differences in valve shape and size, striation pattern and stria density are markers for populations that cannot interbreed (gamodemes sensu Gilmour & Heslop-Harrison, 1954). Demes can also differ in reproductive biology and susceptibility to chytrid and oomycete parasites (Mann, 1989, 1999). Some of the demes have already been separated formally at species level, including S. pupula sensu stricto, S. auldreekie D. G. Mann et S. M. McDonald, S. blackfordensis D. G. Mann et S. Droop, S. capitata D. G. Mann et S. M. Macdonald, S. lanceolata D. G. Mann et S. Droop and S. obesa D. G. Mann et M. M. Bayer (Mann et al., 2004). More recently, new demes have been found and given provisional ‘‘nick-names’’ (e.g. ‘‘elliptical’’, ‘‘spindle’’: Evans et al., 2007, 2008; Mann et al., 2008) until they have been fully characterized by electron microscopy and by an appropriate molecular barcode. Other commonly recorded ‘species’ within Sellaphora (e.g. S. bacillum, S. laevissima, S. seminulum) have not been studied so intensively but are also heterogeneous complexes, rather than single species (Evans et al., 2008; Mann et al., 2008). Although Sellaphora pupula agg. has proved to be a valuable model system for studying the nature of species in microalgae and the biological significance of morphological variation in this complex has been demonstrated (Mann, 1999; Mann et al., 2004), there are as yet few autecological data for the demes and species within this complex. Such data would permit more sophisticated testing of models concerning microbial biogeography. Furthermore, as noted by Denys (2006), if segregate Sellaphora species do differ with respect to physical and chemical niche parameters, identifying them may aid ecological monitoring and palaeoecological reconstruction. For comparison, in the Achnanthidium minutissimum complex (for which no molecular data are yet available to corroborate fine morphological distinctions), failure to differentiate morphotypes has been shown to lead to appreciable loss of information (Denys, 2006). We therefore undertook the present study to test whether pseudocryptic species within Sellaphora species complexes have distinct niches along a lake trophic gradient, assessed via the lake trophic diatom index (LTDI), which was developed recently to aid
Hydrobiologia
ecological monitoring, e.g., in relation to the Water Framework Directive (WFD) of the European Union (Kelly et al., 2006).
Material and methods We sampled 22 lakes in Great Britain (Table 1) covering the spectrum from oligotrophic glacial mountain lakes to eutrophic lowland lakes/ponds. The investigations were carried out in October– November 2004, 2005 and 2006. The geographical positions, and basic morphometric and hydrological data of the lakes are summarized in Table 1. Samples from three types of substrata were taken at each lake. The substrata investigated were: stones (mostly boulders, C10 cm); the submerged parts of littoral macrophytes, mostly reeds (Phragmites australis (Cav.) Steud.); and fine bottom mud. Epilithon was brushed from three stones with a toothbrush into plastic bottles. Reed stalks (15 cm sections) were collected from 50 cm below the water surface in the inner part of the littoral zone and placed in plastic bags. Epiphyton was then removed by scraping with a scalpel and transferred to a plastic bottle. Sediment samples were collected using a glass tube, as described by Round (1953), and transported to the laboratory in polyethylene bottles. The mud–water mixtures were then poured into plastic boxes and allowed to stand in the dark for at least 5 h. The supernatant was then removed by suction and the mud covered with lens tissue. Under low-level illumination (*5 lmol photons m-2 s-1), epipelic algae moved up through the lens tissue and became attached to cover slips placed on top. Diatoms dried on cover slips were cleaned by heating with 30% H2O2 and after washing with deionized water mounted in Naphrax (currently available from Brunel Microscopes: http://www. brunelmicroscopes.co.uk/). Bright field (BF) light microscopy (LM: planapochromat lenses, nominal numerical aperture 1.32 or 1.4) was carried out using a Reichert Polyvar 2 photomicroscope fitted with a Polaroid DMC2 digital camera capable of 1,600 9 1,200 pixel resolution (images were captured via Optimas image analysis software version 6.2: MediaCybernetics, Silver Spring, MD 20910, USA). In some cases, background noise and specks were removed digitally by image
division (http://rbgweb2.rbge.org.uk/algae/methods/ removing_dust.htm; Bayer et al., 2001). Diatom species were identified according to Krammer & Lange-Bertalot (1986, 1988, 1991a, b) and Mann et al. (2004). Sellaphora demes were sorted and compared using digital images taken from acid-cleaned material from each lake. Phenodemes (Gilmour & Heslop-Harrison, 1954) were distinguished by sorting the images into groups in which the only variation in shape and pattern was that expected in diatoms undergoing size reduction during the life cycle, i.e. exhibiting the allometric changes documented by Geitler (1932) and Round et al. (1990, pp. 82–86). The phenodemes found during our study are documented in Figs. 3 and 4. The British Sellaphora demes have also been surveyed independently by Mann et al. (2008) and in most cases our demes correspond to theirs. Wherever this is the case, we have indicated it by adopting the same names, which are either a species name or a standardized deme name consisting of the name of the species complex (S. [pupula], S. [bacillum] or S. [laevissima]) and an informal ‘nick-name’ prefixed by ‘U’ (for ‘phenodeme’), according to the suggestions of Mann & Kociolek (1990). An example is ‘Sellaphora [pupula]’ U ‘lordly’, which means a phenotypically distinct deme called ‘lordly’, which would be identified as S. pupula using standard diatom floras, e.g. Krammer & Lange-Bertalot (1986). However, several of the demes distinguished by Mann et al. (2008) overlap each other in their morphological variation (at least in LM) and require molecular or other nonmorphological data to confirm identification. Consequently, in the present paper we were not always able to make the same distinctions as Mann et al. (2008). For example, most specimens of our S. [pupula] cap-A probably belong to Mann et al.’s S. [pupula] U ‘pseudocapitate’, but U ‘pseudocapitate’ is very similar morphologically to U ‘cf. capitate’ and can occur in the same habitat. Again, S. [pupula] cap-B, cap-C and cap-D cannot be exactly reconciled with single demes in the Mann et al. (2008) taxonomy. The essential point, however, is that the taxonomy used in the present paper was applied consistently, regardless of lake trophic status. The relative abundances of individual diatom species were estimated by counting 400 individuals from each of 66 samples. The representation of all diatom taxa from the epilithic and epiphytic samples
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Blackford Pond
Figgate Loch
Marbury Big Mere
Oss Mere
Ellesmere
Fenemere
RBG Pond
Dunsapie Loch
Rae Loch Lake of Menteith
Blake Mere
Cole Mere
Loch of Butterstone
Loch Venachar
Malham Tarn
Loch Leven
Loch Achray
Threipmuir Reservoir
Loch Voil
Loch of the Lowes
Loch of Clunie
Loch of Craiglush
1
2
3
4
5
6
7
8
9 10
11
12
13
14
15
16
17
18
19
20
21
22
08.12.04
08.12.04
08.12.04
29.09.05
11.10.05
29.09.05
08.11.06
28.10.06
29.09.05
08.12.04
21.10.05
22.10.05
08.12.04 29.09.05
12.10.04
02.12.04
23.10.05
21.10.05
21.10.05
21.10.05
27.11.04
12.10.04
Sampling date
NO 041444
NO 115437
NO 041436
NN 486197
NT 169636
NN 507068
NT 166993
SD 898668
NN 567062
NO 059453
SJ 435329
SJ 416337
NO 160446 NN 567009
NT 281731
NT 248752
SJ 446230
SJ 407345
SJ 561440
SJ 560454
NT 298736
NT 253709
Grid reference
100
48
100
126
253
84
107
381
82
96
88
91
60 17
110
15
88
98
105
78
15
75
Alt. (m a.s.l.)
13
21
16
30
5
29.5
25
4.4
33.8
7.6
11.5
13.5
4.8 23.5
3
2
2.2
18.8
2.9
8.0
3
2
Depth (m)
28
54
88
228
78
82
1373
62
417
44
27.6
8.4
13 264
1.5
0.09
9.4
46.1
9.5
10.5
1
0.8
Area (ha)
MA
MA
MA
LA
MA
LA
HA
MA
LA
MA
HA
HA
MA MA
HA
HA
HA
HA
HA
HA
HA
HA
Alkal.
7.54
7.95
7.54
6.68
n.d.
6–6.9
8.14
n.d.
6.69
8.3
7.6–8.3
7.1–8.2
n.d. 7.04
9.9
7.5
8
7.5–9.5
9.1
9.2
8.2
8.4
pH
127
198
126
31.7
n.d.
31–45
230
n.d.
43.9
139
289
121
n.d. 77
219
374
570
272
479
428
365
331
Cond. (lS cm-2)
17.95
28.34
26.77
25.87
23.76
26.60
42.44
36.52
30.45
35.99
35.31
35.14
50.30 37.32
52.41
65.28
54.03
52.18
50.73
65.73
72.43
77.39
LTDI reeds
-1
23.27
36.68
43.36
29.77
33.66
38.92
50.19
36.12
29.96
48.92
48.79
50.10
58.55 50.65
52.85
64.53
68.48
76.63
70.67
69.66
73.48
74.96
LTDI stones
H
G–H
G–H
G–H
G–H
G–H
G
G
G
G
G
G
M M
M
M
P–M
P–M
P–M
P–M
P
P
Class
Grid reference—UK Ordnance Survey (http://www.ordnancesurvey.co.uk/oswebsite/getamap/), alt.—altitude, alkal—alkalinity categories: LA \ 200 leq l ; MA 200—1,000 leq l-1; HA [ 1,000 leq l-1; cond.—conductivity, LTDI reeds/stones—trophic diatom index based on epiphyton/epilithon, water quality classes: P—poor, M—moderate, G— good, H—high; n.d.—no data
Lake
No.
Table 1 Basic geomorphological and environmental characteristics of the lakes investigated
Hydrobiologia
Hydrobiologia
were used to calculate the ‘‘LTDI stone’’ and ‘‘LTDI reed’’ (Kelly et al., 2006). This is a variant of the trophic diatom index (Kelly & Whitton, 1995), which was calibrated on a dataset of 576 samples from 177 UK lakes. The LTDI is a weighted average index that gives values that range from 0 (indicating highly oligotrophic conditions) to 100 (indicating highly eutrophic conditions). Ecological status was assessed by converting the LTDI values to Ecological Quality Ratios (EQRs), computed as (100 - observed LTDI)/ (100 - expected LTDI), where the expected LTDI is 20 for low alkalinity lakes and 25 for medium and high alkalinity lakes (Kelly et al., 2006; see Table 1 for definitions of alkalinity categories). Status class boundaries are: 0.90 (high/good), 0.63 (good/moderate), 0.44 (moderate/poor) and 0.22 (poor/bad). Multivariate statistical methods using the software package CANOCO for Windows 4.5 (ter Braak & Sˇmilauer, 2002) were used for exploratory analyses of diatom data from epipelic samples. We prepared two datasets: the first contained all diatoms except for Sellaphora, and the second contained only species of the Sellaphora complex. The first dataset was analysed via detrended correspondence analysis (DCA) because a preliminary test indicated that a unimodal approach was appropriate for the study (Lepsˇ & Sˇmilauer, 2003). The species data were square-root transformed before analysis. Environmental factors (alkalinity categorized into three categories (HA, MA, LA), altitude, lake surface area, lake depth) and trophic indices based on species composition on reeds (LTDI reed) and stones (LTDI stone) were correlated with the results of DCA to help with interpretation of the ordination results. To test whether the environmental gradient extracted from the entire community composition except for Sellaphora complex (first dataset) is a significant predictor of Sellaphora community composition (second dataset), a constrained correspondence analysis (CCA) was used with sample scores on the first axis of the DCA as an environmental variable. A Monte Carlo permutation test with 499 permutations was used to test the significance of the first constrained axis. Species-response curves for selected species of the Sellaphora complex were modelled using generalized linear models (GLM). Due to overdispersion, the presence–absence data were used and GLMs using the binomial distribution and logitlink function were calculated. Only Sellaphora
species that occurred in more than five localities were analysed. Sample scores on the first DCA axis (=trophic gradient, see results) were used as a predictor. Model complexity was evaluated by stepwise selection using the Akaike Information Criterion statistic (Lepsˇ & Sˇmilauer, 2003). Only significant response curves are reported.
Results Lake trophic status evaluation based on epilithon and epiphyton In total, 189 diatom taxa were found on stones and reeds in the 22 lakes. Species richness per sample ranged from 7 to 28 species and the most frequently observed species were Achnanthidium minutissimum (Ku¨tz.) Czarn. and Cocconeis placentula Ehrenb. Achnanthidium minutissimum was present in all samples and dominant in 13 lakes (abundance [ 50%: reeds—four samples, stones—six samples; abundance 30–49%: reeds—four samples, stones—four samples). Cocconeis placentula was present in 36 samples and dominant in three lakes (abundance 30–49%: reeds— two samples; stones—one sample; abundance 20–29%: reeds—one sample). The representation of the genus Sellaphora was negligible within epilithon and epiphyton. LTDI values from rocks and plants were highly correlated (Spearman correlation coefficient r = 0.90; P \ 0.001) and indicated a wide range of trophic conditions, ranging from oligotrophic (Loch Achray, Loch of Craiglush) to eutrophic (Blackford Pond, Figgate Loch, Dunsapie Loch). Ecological status assessments ranged from high to poor; no sites with bad status were included in the study but our experience shows that relatively few standing waters in the UK fit this category (Kelly, unpublished). Epipelic diatom distributions along the lake trophic gradient (excluding Sellaphora) In total, 157 diatom taxa were found in mud samples. Species richness ranged from 9 to 32 species per lake, the highest being recorded in Dunsapie Loch and the lowest in the Loch of the Lowes. The first and second axes of a DCA ordination of epipelic diatoms explained 10.2 and 8.5% of the
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Hydrobiologia
variance of species data. Lake characteristics (depth, area, altitude, alkalinity) and trophic level (LTDI stones, LTDI reeds) were included as supplementary factors and suggested that the first axis represented the trophic gradient, with oligotrophic lakes in the right part of the diagram and mesotrophic and eutrophic ones on the left (Fig. 1). This pattern is supported by a strong correlation of the sample scores on the first axis with trophic indices (Spearman correlation coefficient; LTDI stones: r = -0.64, P = 0.001, LTDI reeds: r = -0.71, P \ 0.001), and with lake depth (r = 0.71, P \ 0.001). A similar pattern was observed in the distribution of alkalinity categories over the ordination diagram, with low alkalinity lakes on the right and high alkalinity lakes on the left (Fig. 1). Samples from deep, oligotrophic, low alkalinity lakes (often with low pH and conductivity) were characterized by occurrence of Brachysira vitrea (Grun.) R. Ross, Tabellaria flocculosa (Roth) Ku¨tz., Pinnularia gibba Ehrenb. and P. subcapitata Greg. In contrast, epipelic assemblages in shallow, high
Fig. 1 Joint ordination diagram (DCA) of the samples (first dataset) and supplementary environmental factors. The first ordination axis (x-axis) can be interpreted as a trophic gradient. Abbreviations: Achray, Loch Achray; Blake, Blake Mere; Blackfor, Blackford Pond; Big, Marbury Big Mere; Butterst, Loch of Butterstone; Clunie, Loch of Clunie; Craig, Loch of Craiglush; Cole, Cole Mere; Dun, Dunsapie Loch; Elles, Ellesmere; Fene, Fenemere; Figgate, Figgate Loch; Leven, Loch Leven; L. Lowes, Loch of the Lowes; Ment, Lake of Menteith; Malham, Malham Tarn; Oss, Oss Mere; Rae, Rae Loch; RBGP, Royal Botanic Garden Pond; Threip, Threipmuir Reservoir; Venach, Loch Venachar; Voil, Loch Voil; alkalinity categories: LA \ 200 leq l-1; MA 200–1,000 leq l-1; HA [ 1,000 leq l-1; LTDI reed, trophic diatom index on reeds; LTDI ston, trophic diatom index on stones
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alkalinity, meso-eutrophic lakes typically included Placoneis placentula (Ehrenb.) Heinzerl., Staurosira construens (Ehrenb.) D. M. Williams et Round, Craticula cuspidata (Ku¨tz.) D. G. Mann, Navicula menisculus Schumann, Placoneis elginensis (Greg.) E. J. Cox, Staurosirella pinnata (Ehrenb.) D. M. Williams et Round, and all Amphora spp. (Fig. 2). Occurrence of Sellaphora demes on the lake trophic gradient Altogether 28 morphospecies were distinguished within Sellaphora (Table 2, Figs. 3, 4). Most lake epipelon contained several Sellaphora demes and
Fig. 2 DCA ordination of epipelic diatom species (first dataset). Only species with higher weight in the analysis are shown. Achmin, Achnanthidium minutissimum; Ampcop, Amphora copulata; Ampova, A. ovalis; Ampped, A. pediculus; Astfor, Asterionella formosa; Aulgra, Aulacoseira granulata; Bravit, Brachysira vitrea, Cocpla, Cocconeis placentula; Cracus, Craticula cuspidata; Cymcus, Cymbella cuspidata; Cymnav, Cymbella naviculiformis; Cysdub, Cyclostephanos dubius; Gomgra, Gomphonema gracile; Gompar, G. parvulum; Navcad, Navicula capitatoradiata; Navcap, N. capitata; Navcar, N. cari; Navcrt, N. cryptotenella; Navcry, N. cryptocephala; Navdec, N. decussis Oestr.; Navgre, N. gregaria; Navmen, N. menisculus; Navrad, N. radiosa; Navrhy, N. rhynchocephala; Navtrv, N. trivialis; Navven, N. veneta; Neiamp, Neidium ampliatum; Neidub, N. dubium; Pingib, Pinnularia gibba; Pinsub, P. subcapitata; Plaelg, Placoneis elginensis; Plalan, P. lanceolatum, Plapla, P. placentula, Staanc, Stauroneis anceps; Stapho, S. phoenicenteron; Stacon, Staurosira construens; Stapin, Staurosirella pinnata; Tabflo, T. flocculosa
Hydrobiologia Table 2 The occurrence of Sellaphora morphospecies Morphospecies
Abbreviation
Image
Lake
S. auldreekie
Selaul
Fig. 3m
1, 4, 5, 8, 18
S. cf. auldreekie
Selcau
Fig. 3n
1, 10
S. [bacillum] U ‘button’ S. [bacillum] U ‘oval’’
Bacbut Bacova
Fig. 4j Fig. 4k
5, 15 3–5, 12, 15, 16
S. [bacillum] U ‘radiate’
Bacrad
Fig. 4m
16
S. [bacillum] U ‘rectangular’
Bacrec
Fig. 4i
1, 6, 8, 9, 11, 13, 21
S. [bacillum] sharp
Bacsha
Fig. 4l
13, 20
S. blackfordensis
Selbla
Fig. 3a
1, 6–8, 15, 21
S. capitata
Selcap
Fig. 3b
1, 6–8, 15, 20, 21
S. [laevissima] U ‘barless capitate’
Laecap
Fig. 4n
9
S. [laevissima] fine
Laefin
Fig. 4h
5, 6, 8–10, 15, 18
S. [laevissima] U ‘very coarse’
Laecoa
Fig. 4g
4
S. obesa
Selobe
Fig. 3h
1, 5, 6, 8, 12, 13, 15, 16
S. pupula
Selpup
Fig. 4b
1, 2, 4–7, 9, 15–18 10, 11, 13, 14, 18, 19, 22
S. [pupula] cap-A
Pupcaa
Fig. 3c
S. [pupula] cap-B
Pupcab
Fig. 3d
10, 11, 13, 14, 18, 19, 21, 22
S. [pupula] cap-C
Pupcac
Fig. 3e
5, 10, 11, 14, 17, 19, 21
S. [pupula] cap-D
Pupcad
Fig. 3f
8, 16, 18
S. [pupula] U ‘grooved lanceolate’ S. [pupula] U ‘lordly’
Puplag Puplor
Fig. 4d Fig. 4c
13, 17 16
S. [pupula] U ‘mini-obese’
Pupobm
Fig. 3i
4, 5, 12, 18, 22
S. [pupula] U ‘mouse’
Pupmou
Fig. 4a
16
S. [pupula] U ‘small lanceolate’
Puplas
Fig. 4e
1, 5, 8, 15, 16, 18, 20
S. [pupula] U ‘spike’
Pupspk
Fig. 4f
4, 16
S. [pupula] ‘spindle’
Pupspi
Fig. 3l
1, 21
S. [pupula] U ‘tidy’
Puptid
Fig. 3g
17
S. [pupula] U ‘upland elliptical’
Pupelp
Fig. 3k
11, 18
S. [pupula] U ‘urban elliptical’
Pupelr
Fig. 3j
1
Simple latin binomials (e.g. S. pupula, S. blackfordensis, etc.) and deme names prefixed by ‘U’ refer to Sellaphora species and demes described and illustrated by Mann et al. (2008). Other names, not prefixed by ‘U’, refer to demes distinguished for and consistently applied in the present paper. These may comprise more than one of the demes described by Mann et al. (2008)
species, with 8–10 recorded in Blackford Pond, Dunsapie Loch, Threipmuir Reservoir, Loch Leven, Malham Tarn, and Ellesmere (Table 2). The environmental gradient extracted from the entire community (except for Sellaphora) was a significant predictor of Sellaphora community composition (CCA, Monte Carlo permutation test of the first axis, F = 2.61, P = 0.002). When Sellaphora morphospecies were plotted in the ordination space defined by epipelic taxa, clear differences in preferences were observed, with some having high scores on axis 1, suggesting a preference for oligotrophic
conditions, whereas others had low scores, apparently preferring more eutrophic conditions (Fig. 5). Some Sellaphora morphospecies were very rare in the lakes surveyed and therefore their positions in the ordination diagram may be a matter of chance. Nine of the 28 morphospecies occurred in only one lake and seven in only two lakes. Therefore, further analyses were done only with those morphospecies present in at least five lakes. GLMs for seven Sellaphora morphospecies, using the first axis of the DCA (=trophic gradient) as a predictor, were statistically significant at P = 0.05. Again, species
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Fig. 3 Sellaphora morphospecies: a, S. blackfordensis (RBG pond); b, S. capitata (Dunsapie Loch); c, S. [pupula] cap-A (Blake Mere); d, S. [pupula] cap-B (Loch Venachar); e, S. [pupula] cap-C (Loch Venachar); f, S. [pupula] cap-D (Dunsapie Loch); g, S. [pupula] U ‘tidy’(Loch Achray); h, S. obesa (Dunsapie Loch); i, S. [pupula] U ‘mini-obese’ (Cole
Mere); j, S. [pupula] U ‘urban elliptical’ (Blackford Pond); k, S. [pupula] U ‘upland elliptical’ (Threipmuir Reservoir), l, S. [pupula] ‘spindle’ (Blackford Pond); m, S. auldreekie (Ellesmere); n, S. cf. auldreekie (Blackford Pond). Scale bar = 10 lm
were differentiated with respect to trophic status, with Sellaphora cap-A, cap-B, cap-C all indicating rather oligotrophic conditions, whereas S. blackfordensis, S. capitata, S. obesa, and S. [pupula] U ‘small lanceolate’ indicated meso- and eutrophic conditions
(Fig. 6, Table 3). When the responses of Sellaphora aggregates (Sellaphora bacillum agg., S. laevissima agg. and S. pupula agg.) over the same gradient were tested, no relation to the first axis of the DCA was found for any of them (P [ 0.4).
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Fig. 4 Sellaphora morphospecies: a, S. [pupula] U ‘mouse’ (Loch Leven); b, S. pupula (Fenemere); c, S. [pupula] U ‘lordly’ (Loch Leven); d, S. [pupula] U ‘grooved lanceolate’ (Loch of Butterstone); e, S. [pupula] U ‘small lanceolate’ (Threipmuir Reservoir); f, S. [pupula] U ‘spike’ (Loch Leven); g, S. [laevissima] U ‘very coarse’ (Oss Mere); h,
S. [laevissima] fine (Lake of Menteith); i, S. [bacillum] U ‘rectangular’ (Fenemere); j, S. [bacillum] U ‘button’ (Malham Tarn); k, S. [bacillum] U ‘oval’ (Oss Mere); l, S. [bacillum] sharp (Loch of Butterstone); m, S. [bacillum] U ‘radiate’ (Loch Leven); n, S. [laevissima] U ‘barless capitate’ (Rae Loch). Scale bar = 10 lm
Discussion
are treated each as a single entity, they show broad tolerance without any response to the trophic gradient, but we now know that this disguises specialism among the component demes. Some members of the S. pupula complex (e.g. Sellaphora cap-A, -B and -C) are characteristic of oligotrophic conditions, whereas others are restricted to eutrophic waters. The latter, including S. blackfordensis, S. capitata,
Our data show that the broad ecological tolerance generally recorded for the whole S. pupula complex (e.g. in the European Diatom Database at http://crati cula.ncl.ac.uk/Eddi/jsp/) is not possessed by the individual species and demes that comprise it. If S. pupula agg., S. bacillum agg. or S. laevissima agg.
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Hydrobiologia Table 3 Generalized linear models describing response of selected Sellaphora morphospecies to the first ordination axis of DCA Morphospecies
Equation
F
P
Selbla
-1.11 - 1.44x
5.4
0.03
Selcap
-0.85 - 1.52x
6.6
0.02
Selobe
-0.86 - 2.42x
12.3
0.002
Puplas
-0.77 - 1.26x
5.3
0.03
Pupcaa
-1.09 - 1.19x
6.3
0.02
Pubcab
-0.15 + 3.80x - 1.43x2
4.9
0.02
Pupcac
-0.91 + 3.34x - 0.99x2
6.9
0.006
Binomial distribution, logit-link function; F, F values; P, Probability level; x, predictor = sample scores on the first axis of the DCA (first dataset). See abbreviations in Table 2
Fig. 5 Position of Sellaphora morphospecies (second dataset) in the ordination space (first and second axes of the DCA) defined by other epipelic diatoms (first dataset). Empty triangle, species found in fewer than three lakes; full triangle, species found in three or more lakes. For abbreviations see Table 2
Fig. 6 Species response curves (GLM using the binomial distribution and logit-link function) for selected species of the genus Sellaphora (for abbreviations see Table 2). The first ordination axis (x) of the DCA (first dataset) was used as a predictor. All visualized models are significant at P B 0.05. For regression equations see Table 3
S. obesa, and S. [pupula] U ‘small lanceolate’ (two others—S. auldreekie and S. pupula—are just below the significance level: not illustrated), often occur
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together in shallow lowland ponds in urban or fertile agricultural catchments. Thus, distinguishing these species in ecological or palaeoecological studies could provide greater precision, as suggested by Denys (2006). Although the present analysis was restricted to lakes and ponds in Britain, unpublished molecular sequence data and mating experiments (K. M. Evans and V. A. Chepurnov, personal communication) show that at least some of the ‘eutrophic’ demes also occur in the Czech Republic (S. auldreekie), Belgium (S. capitata), the Ukraine (S. capitata) and Australia (S. auldreekie, S. capitata, S. [pupula] U ‘urban elliptical’), again in similar shallow lakes. Many lakes contain several Sellaphora demes. In our dataset and also in the presence–absence survey by Mann et al. (2008), the greatest numbers of coexisting demes occurred in meso and eutrophic lakes, such as Malham Tarn or Blackford Pond. Oligotrophic lakes, such as Lochs Voil, Venachar and Achray, the Loch of Craiglush (this study) and Lochs Maree, Tulla and Lubnaig (Mann et al., 2008), generally have fewer Sellaphora species and demes. It will be interesting to see whether there is a drop-off in Sellaphora diversity if the survey is extended even further into the fertile end of the trophic spectrum. Preliminary results from 45 eutrophic to hypertrophic fishponds in the Czech Republic and records from Hungary support this presumption, since the genus Sellaphora is rare within Czech epipelic diatom assemblages (B1%; cf. 1–40% in British lakes: Poulı´cˇkova´, unpublished) and Hungarian lowland waters (B1% in 21 sites; J. Padisa´k, personal communication; van Dam et al. 2007).
Hydrobiologia
Explanations of diversity in natural communities are legion, spread between the extremes of ‘niche assembly’ (e.g. Tilman 1982) and ‘dispersal assembly’ (Hubbell 2001). Even after allowance has been made for diminution during the life cycle, Sellaphora species differ considerably in cell size. For example, among species and demes with a lanceolate valve outline there are small- (S. auldreekie and S. [pupula] U ‘small lanceolate’: Figs. 3m, 4e), medium(S. [pupula] U ‘spindle’ and S. [pupula] U ‘spike’: Figs. 3l, 4f) and large-celled (S. obesa: Fig. 3h) examples. Although the differences in each linear dimension are not great, the accompanying differences in volume and surface area: volume ratio are likely to have significant effects on cell physiology (cf. Potapova & Snoeijs, 1997; Raven & Ku¨bler, 2002). Nevertheless, it is difficult to imagine how the 8–10 Sellaphora species that occur together in lakes like Blackford Pond or Malham Tarn could coexist via niche separation, especially given that several tens of species of other diatom genera exist alongside them in the epipelon. Nor do our data give full support to the alternative extreme explanation of diversity—the neutralist view—which assumes ‘per capita ecological equivalence of all individuals of all species in a trophically defined community’ (Hubbell, 2001). In this paradigm, ‘communities are open, nonequilibrium assemblages of species largely thrown together by chance, history, and random dispersal’ and the presence or absence of species reflects ‘random dispersal and stochastic local extinction’. However, the same Sellaphora species generally occur in eutrophic lakes, whether the lakes are close together (and therefore presumably likely to share the same pool of potential immigrants) or not, and lakes of different trophic status have different Sellaphora floras. The ‘‘ubiquity hypothesis’’ (Finlay & Clarke, 1999a, b; Finlay, 2002; Finlay et al., 2002) postulates that for microorganisms ‘‘everything is everywhere’’ but ‘‘the environment selects’’. Finlay et al. (2002) suggested that diatom species can be classified into ‘specialists’, which are often rare and occur at few localities, and ‘generalists’, which have broad ecological tolerances so that suitable habitats are plentiful and local abundance is often high. Generalists will therefore be detected readily in rapid surveys of diversity, whereas specialists will be more easily missed. In both cases, however, the high
absolute abundance of diatom species in suitable habitats is suggested to ensure rapid, ubiquitous dispersal. There is already evidence that diatom dispersal is not as rapid and effective as required for the ‘‘ubiquity hypothesis’’, from comparisons of species-richness relationships along different segments of the pH range (Telford et al., 2006, 2007). Vyverman et al. (2007) have shown, using a global freshwater diatom dataset, that: (1) latitudinal gradients in local and regional genus richness are present; and (2) historical factors (colonization and extinction, dispersion and migration) explain significantly more of the observed geographical pattern in genus richness than do contemporary environmental conditions. However both these studies, like the original analysis by Finlay et al. (2002), rely on surveys undertaken with coarse-grained taxonomies that assume taxon equivalence across the areas and habitats surveyed. Our results imply that such studies are likely to overestimate the effectiveness of dispersal, because the units recorded represent sets of lineages that probably diverged from each other millions of years ago (cf. Evans et al., 2008). Finlay et al. (2002) discussed four abundant (=generalist) diatom species within a dataset based on published works, surveyed from Web of Science and the Fritsch Collection of Freshwater Algal Illustrations (http://www.fritschalgae.info/). These did not include S. pupula but did include Navicula cryptocephala Ku¨tz., Cyclotella meneghiniana Ku¨tz., Gomphonema parvulum (Ku¨tz.) Ku¨tz. and Nitzschia palea (Ku¨tz.) W. Sm. All four have been considered taxonomically complex, as reflected in the number of varieties and forms that have been described within them and the presence of cytologically and reproductively differentiated demes in Navicula cryptocephala (Geitler, 1951, 1952a, b, 1958; Poulı´cˇkova´ & Mann, 2006; VanLandingham, 1967–1978). Furthermore, Beszteri et al. (2005, 2007) have shown that Cyclotella meneghiniana is highly diverse genetically, probably containing several or many biological species. We conclude that none of the examples used by Finlay et al. (2002) to support the ubiquity hypothesis are secure taxonomically. Overall, then, it remains unclear whether any ‘generalist’ species actually exist, at least of the kind discussed by Finlay et al. (2002), and the use of morphospecies in wide-ranging ecological and biogeographical analyses needs to be cautious, unless the
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questions being asked are unsubtle. This, however, raises some interesting questions for biomonitoring, as the methods that are commonly used for environmental assessment (e.g. Atazadeh et al., 2007; Heinsalu et al., 2007, 2008; Stenger-Kova´cs et al. 2007) depend heavily on sensitivity and tolerance parameters of taxa as described in major floras and do not yet take full account of cryptic diversity. Denys’ (2006) suggestion that distinguishing these species will provide greater precision may be offset by the problems involved in ensuring consistent identification, particularly when several analysts are involved. Kelly et al. (2002) noted that some Sellaphora pupula agg. demes (‘elliptical’, ‘tidy’) were correctly distinguished by almost all the 26 analysts who participated in an on-line ring test whilst the identification rate for others (e.g. ‘pseudocapitate’) was as low as 66%. Potapova & Hamilton (2007) suggested the use of morphological groups (which did not always correspond exactly with formally recognized taxa) as a means for tackling similar problems in the Achnanthidium minutissimum complex, and practical approaches such as this will need to be explored for other species complexes if the benefits of this new knowledge are to lead to more sensitive environmental assessments. Acknowledgements The helpful comments of two anonymous reviewers are gratefully acknowledged. This research was supported by project GACR 206/07/0115 from the Czech Republic and an EU Framework 6 SYNTHESYS GB-TAF-643 award to Assoc. Prof. Aloisie Poulı´cˇkova´.
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