Campylodiscus clypeus in inland saline lakes

Campylodiscus clypeus (Ehrenb.) Ehrenb. in inland saline lakes L. R. Carvalho1, 2, P. A. Sims2, R. W. Battarbee1, E. J. Cox2 & S. Juggins3 1

Address for correspondence: Environmental Change Research Centre, Department of Geography,

University College London, 26 Bedford Way, London WC1H 0AP, UK. 2

Department of Botany, The Natural History Museum, Cromwell Road, London SW7 5BD, UK.

3

Department of Geography, University of Newcastle, Newcastle-upon-Tyne, UK.

Abstract

This paper is concerned with Campylodiscus clypeus in recognition of Urve Miller's interest in this taxon and her contribution to the study of shoreline displacement, a stage of Baltic sea level change characterised by C. clypeus. This species has also frequently been recorded from inland saline lakes, where the dominant anions are often carbonate and sulphate, rather than chloride. Diatom remains in the sediments of saline lakes can provide estimates of past salinity that can be used to infer past water level and climate. In an attempt to obtain more accurate reconstructions of past salinities we are merging saline lake diatom and water chemistry datasets from the Northern Great Plains (N. America) and Africa; ensuring taxonomic consistency is a vital prerequisite.

We

examined material from two localities cited by Ehrenberg and compared populations from the Baltic and from inland saline lakes, both Recent and Holocene Sub-fossil material. We present new data on the frustule morphology of this taxon and show that the populations cannot be clearly separated, either morphologically or ecologically by salinity optima or ion type, and therefore, should be regarded as the same taxon.

1

Introduction

Campylodiscus clypeus is well known to Quaternary geologists interested in the Baltic Sea as it gives its name to a diatom assemblage, the clypeus flora, that frequently signals the stage in sediment sequences immediately preceding lake basin isolation in Litorina times (Florin, 1946). The potential of this species as an indicator for lake isolation, and thus for reconstructing the position of former shorelines, has been discussed already by Lundquist & Thomasson (1923) and Cleve-Euler (1923). Our paper is concerned with Campylodiscus clypeus in recognition of Urve Miller's contribution to the study of shoreline displacement in Sweden (e.g. Miller & Robertson, 1979, Miller, 1986) and her own interest in this taxon (Miller, 1969). C. clypeus has been recorded world-wide in coastal and lagoonal habitats (e.g. van der Werff & Huls, 1961; Archibald, 1983; Rivera, 1983; Foged, 1984; Witkowski, 1990), and Flower (pers. comm.) found it in a lagoon in Morocco where it formed a monospecific population. It is a large benthic diatom that clearly favours shallow, brackish water environments. However, as with many taxa of the brackish coastal zone it is not restricted to thalassic waters. Hustedt (1930) described its occurrence in inland saline lakes such as the Neusiedler See.

It is also commonly found in shallow

mesohaline inland saline lakes in Africa (Gasse, 1986; Gasse et al., in press) and the Northern Great Plains (NGP) of North America (Fritz et al., 1993), where the dominant anions are often carbonate and sulphate rather than chloride. Whereas diatom changes in the sediments of lakes around the Baltic can be used to reconstruct the position of past shorelines (Florin, 1948; Eronen, 1974; Miller, 1982), diatom remains in the sediments of saline lakes are able to provide estimates of past salinity that can be used to infer past water level and climate (Fritz, 1990; Fritz et al., 1991). In an attempt to obtain more accurate reconstructions of past salinities we are merging saline lake diatom and water chemistry datasets from the NGP and Africa. Ensuring taxonomic consistency is a necessary prerequisite. Because of its abundance in the NGP dataset and its presence in African saline lakes (Gasse, 1986), the identity of C. clypeus is important. Furthermore, there is some confusion over its relationship to C. bicostatus Wm Smith. The latter was not recorded by Fritz et al. (1993) in the NGP but is present, although never common, in Africa (Gasse, 1986).

Re-examination of

samples from the NGP, however, has revealed that in one sample material recorded as

2

C. clypeus was in fact C. bicostatus, while in another sample an intermediate form was present. It is not just recently that there has been uncertainty over the identity of these two taxa. In 1930, Hustedt considered C. bicostatus a variety of C. clypeus as he had observed populations in which a range of forms between the two were present. However, Krammer & Lange-Bertalot (1988) kept the two taxa apart after examining Hustedt’s collection and finding no intermediates. In this paper we only discuss samples in which a taxon is clearly identifiable with C. clypeus. We examined material in the Kützing collection from Eger, one of the localities cited by Ehrenberg (1838b) and from Franzensbad, the type locality. We compared these specimens with populations from the Baltic and inland saline lakes, both Recent and Holocene Sub-fossil material. We present new information on frustule morphology and show that the populations cannot be clearly separated, morphologically or ecologically by salinity optima or brine type, and should be regarded as the same taxon.

Taxonomic background

Ehrenberg (1838a) first described the taxon, as Cocconeis? clypeus, from fossil deposits at Franzensbad (Františkovy Lázne), Czech Republic (50° 07´ N, 12° 22´ E). That same year he recorded it in abundance from fossil deposits nearby, at Eger, and transferred it to his new genus Campylodiscus (Ehrenberg, 1838b). There have, however, been few taxonomic treatments of members of this genus since Deby’s monograph (1891). Miller (1969) published several SEM images of C. clypeus from Baltic post-glacial deposits, Paddock & Sims (1977) surveyed the raphe structure of several advanced groups of diatoms, including Campylodiscus, and Paddock (1985) discussed the morphological parallels between Surirella fastuosa and Campylodiscus fastuosus and the evolution of the crossed axes of this genus.

Material and Methods

3

Recent material taken from surface sediments in North American (Shinbone Lake, School Lake, Horseshoe Lake, and Lake Isabel) and African (Lake Kindai, Tanzania) saline lakes were examined together with Holocene sub-fossil material from deposits in West Africa (Adrar Bous, N. Niger). These were compared with fossil material from Franzensbad and Kützing material from Eger, held in the diatom herbarium at the Natural History Museum, London. Both appear to have assemblages identical to those Ehrenberg illustrated in Mikrogeologie (1854). The Eger material is rich in specimens of C. clypeus and was therefore chosen for SEM studies. Recent material from lagoons in Sweden (Forsmarch) and Finland (Lammaslampi) and Eemian fossil material from Norinkylä, Finland were also examined. Details of the North American sites are given in Fritz et al. (1993), and in Gasse (1986) and Dubar (1988) for the African sites. Grönlund (1991) provides details of the Norinkylä core. The material was prepared for light microscopy (LM) and scanning electron microscopy (SEM) using standard methods, and photographed on a Zeiss Universal photomicroscope and a Hitachi S800 field emission scanning electron microscope. Terminology follows Anonymous (1975) and Ross et al. (1979). The terms for the raphe canal follow Paddock & Sims (1977).

Results

Frustules from all localities showed the same general structural features with the characteristic saddle-shaped valves.

Valves are circular in outline, with a shallow

mantle. The central area is delimited by a 4-cornered, approximately oval, hyaline area, bisected by an axial area. These hyaline areas are raised internally, and depressed externally (Figs 3-4). Two short, transapically-directed rows of puncta are situated either side of the axial area. The outer part of the valve face consists of radiating rows of puncta, separated at intervals by costate fibulae (Figs 1-2). Both the fibulae and the rows of puncta are interrupted by two sickle-shaped hyaline areas, one on each side of the apically-orientated central hyaline area. The sickle-shaped hyaline areas are more obvious on some specimens than others (Figs 10 & 14). The canal raphe system is raised on a keel and runs around the entire perimeter of the valve, terminating at the poles, although these features are not frequently observed under the light microscope.

4

Because of focussing difficulties with conventional light microscopy, SEMs provide a more effective means of depicting the valve structure. Measurements of valve diameter and costa density of all the material examined are detailed in Table 1. In some samples very few intact valves are present and girdle elements are very rarely seen.

Description of material from Eger & Franzensbad, Bohemia (Figs 1-9) Valves are 92-132 µm in diameter with a costa density of 14-17/100 µm and a narrow axial area (Figs 1-4). Despite few intact valves viewed from Franzensbad, it was clear that it was the same species in both deposits. The SEM pictures show further details of the external and internal features of the valve. The raphe is subtended internally by costate fibulae, forming fenestrae. Within each fenestra there is a perforate fibulate plate, with 1, or occasionally 2, non-costate fibulae linking the plate across the raphe canal (Fig. 5, arrowed). The areolae are particularly visible in partially dissolved valves (Fig. 6) and are found in the central area (Fig. 7) and between the costae of the marginal rays (Figs 5 & 8). However, there is a band, approximately 2 µm wide, around the margin of the valve face that is devoid of areolae (Fig. 8). Rows of poroid areolae can also be seen on the valve mantle (Fig. 9). The raphe endings, situated on the keel at either end of the axial axis, are slightly expanded when viewed externally (Fig. 9). The valve face and mantle are corrugated: they are slightly raised along the outer rows of puncta but form slight depressions along the lines of the costate fibulae (Figs 3 & 8).

Baltic lagoon material (Figs 10-12) Valves are 103-198 µm in diameter (mean: 135 µm) with 12-17 costae/100 µm (Table 1). The general areola distribution (Figs 10-11) is similar to that in the Eger material, although, due to dissolution, details of the areolae and fibulae could not be resolved (Fig. 12).

Saline lake material (Figs 13-30) Valves are 77-223 µm in diameter (mean: 116 µm) with 12-21 costae/100 µm (Figs 1317). Internally 1, occasionally 2, non-costate fibulae were observed per fenestra (Figs 18-19). As in the material from Eger, the raphe endings are slightly expanded when viewed externally (Fig. 20). The areola distribution of the saline lake material (Figs 2126) is similar to that found in the type material, although internal views (Figs 23-26)

5

reveal that there is considerable variation in the shape and distribution of the central rows of areolae within and between samples. Valves from Holocene deposits at Adrar Bous (Figs 25-26) diverge most from the type valves as the areolae are more irregularly scattered and the central area more rounded, particularly in the larger valves from the former site. The internal view of a valvocopula and first copula were obtained for a valve from School Lake. The open copula has 2 rows of lineate pores. At the ligule, the row proximal to the valve bends towards the valve and 2 puncta are found between the 2 rows at this point (Figs 27-28). Another valve from this sample showed that, in external view, 1 of the rows of pores is usually hidden (Fig. 29). Six open girdle elements were also found with a valve from Adrar Bous (Fig. 30), 4 copulae and what appear to be both valvocopulae. Only a single row of lineate pores was visible externally on each copula.

Distribution and ecology

Table 2 gives details of the saline lake sites in the NGP and in Africa where C. clypeus has been recorded at a frequency greater than 1% (Fritz et al., 1993; Gasse et al., in press). It is clear that this taxon is characteristic of shallow, low salinity lakes, having an abundance-weighted salinity optimum for the combined NGP and African dataset of 4.4 g l-1 (Fig. 31). From Table 2 and Fig. 32, it is evident that C. clypeus is not restricted by brine type, nor is there a clear brine type preference. Previous analyses of distribution patterns of C. clypeus in the NGP dataset (Fritz et al., 1993) and saline lakes in western North America (Blinn, 1993) suggested that this species is more characteristic of sodium carbonate lakes, than sulphate-dominated lakes. However, from our enlarged dataset, it is apparent that this species does not show a clear ion type preference.

Discussion

The main sources of variation were the diameter of the valve, costa density, and central area areolae distribution. No clear distinctions can be made between samples on the

6

basis of valve diameter or costa density; all samples having overlapping ranges. One valve in the Adrar Bous sample (Fig. 25) has a characteristic areola distribution pattern in its central area, but there is variation in central area shape and areola distribution between all samples; without further distinguishable morphological differences the significance of this variation is unclear. No morphotypes appear to be associated with particular brine types and the response curve to salinity was unimodal. Further evidence that we are dealing with a single species is provided by the regular associated presence of Anomoeoneis costata (Kütz.) Hustedt (formerly A. sphaerophora v. costata) and Surirella peisonis Pant. The former has been recorded in many East African sites and over 75% of the saline lakes in the NGP that contained C. clypeus. A. sphaerophora v. sculpta (Kütz.) Pfitzer, a closely related taxon, was recorded in the Clypeus flora described by Florin (1944) and in the Kützing material from Eger. The salinity optima for A. costata and S. peisonis in the NGP dataset were 3.8 g l-1 and 3.3 g l-1 respectively. Therefore, on present knowledge it appears that the populations examined from North America, Africa, and Europe should be regarded as the same taxon and the refined salinity optimum calculated for the North American dataset can be used in palaeosalinity studies elsewhere, particularly in regions where C. clypeus is presently absent, or rare, such as East Africa. Its occurrence in carbonate-, sulphate- and chloride-dominated waters suggests that it cannot be used as a clear indicator of a particular brine type. Further studies into populations of C. clypeus, C. bicostatus, and intermediate forms are required to elucidate their relationships. More detailed taxonomic treatment may further improve environmental reconstructions, whether in relation to sea level change or climate change.

Acknowledgements This paper is dedicated to Urve Miller, for whose help and support over the last 25 years Rick Battarbee expresses his thanks. The work was supported by an NERC research grant (GR3/8854) to Rick Battarbee, Steve Juggins, Pat Sims, and Eileen Cox and by British Council, UK/Ministère des Affaires Etrangères, France Alliance project 93.093. Thanks are due to Peter York for the light photomicrographs. Material was kindly provided by Sheri Fritz (Horseshoe Lake, Lake Isobel), David Ryves (Shinbone Lake), Platt Bradbury (School Lake), Francoise Gasse (Adrar Bous, L. Kindai), Tuulikki Grönlund (Norinkylä), Atte Korhola (Lammaslampi), and Pauli Snoejis (Forsmarch).

7

References

Anonymous, 1975. Proposals for a standardization of diatom terminology and diagnoses. Nova Hedwigia, Beiheft, 53, 323-354. Archibald, R.E.M., 1983. The diatoms of the Sundays and Great Fish Rivers in the Eastern Cape Province of South Africa. Bibliotheca Diatomologica Band 1 Blinn, D. W., 1993. Diatom community structure along physicochemical gradients in saline lakes. Ecology, 74, 1246-1263. Cleve-Euler, A., 1923. Försök till analys av Nordens senkvartära nivåförändringar jämte några konsekvenser. Geologiska Föreningens i Stockholm Förhandlingar, 45, 19-107. Deby, J., 1891. Analysis of the diatomaceous genus Campylodiscus: being the prelude to a monograph of the same. London: J. Deby. Dubar, C., 1988. Eléments de paléohydrologie de L'Afrique Saharienne: les dépôts quaternaires d'origine aquatique du Nord-Est de l'Air (Niger). Ph.D. Thesis, Université de Paris-Sud. Ehrenberg, C. G.,1838a. Die infusionsthierchen als vollkommende organismen. Ein Blick in das tiefere organische Leben der Natur. Leipzig: Leopold Voss. Ehrenberg, C. G., 1838b. Bericht über die zur Bekanntmachung geeigneten Verhandlungen der königl. preuss. Akademie der Wissenschaften zu Berlin, S, 10-11. Ehrenberg, C. G., 1854. Mikrogeologie. Das Erden und Felsen schaffende Wirken des unsichtbar kleinen selbständigen Lebens auf der Erde. Leopold Voss, Leipzig. Eronen, M., 1974. The history of the Litorina Sea and associated Holocene events. Comment. Physico-Math., 44, 79-195. Florin, M.B., 1946. Clypeusfloran i postglaciala fornsjölagerföljder i östra Mellansverige. Geologiska Föreningens i Stockholm Förhandlingar, 68, 429458. Florin, S., 1948. Kustförskjutningen och bebyggelseutvecklingen i östra Mellansverige under senkvartär tid. II De baltiska strandbildningarna och stenåldersboplatsen

8

vid Dammstugan nära Katrineholm. Geologiska Föreningens i Stockholm Förhandlingar, 70, 17-196. Florin, M.B., 1973. Ekologiska salthaltsfrågor med tyngdpunkt på diatomeer inom Östersjöområdet, en historisk översikt. Report from Diatom Symposium, Lund. pp 12-34. Foged, N., 1984. Freshwater and littoral diatoms from Cuba. Bibliotheca Diatomologica, Band 5 Fritz, S. C., 1990. Twentieth century salinity and water level fluctuations in Devil's Lake, North Dakota: a test of a diatom-based transfer function. Limnology & Oceanography, 35, 1771-1781. Fritz, S. C., Juggins, S., & Battarbee, R. W., 1993. Diatom assemblages and ionic characterization of lakes of the Northern Great Plains, North America: a tool for reconstructing past salinity and climate fluctuations. Canadian Journal of Fisheries and Aquatic Sciences, 50, 1844-1856. Fritz, S. C., Juggins, S., Battarbee, R. W., & Engstrom, D. R. 1991. Reconstruction of past changes in salinity and climate using a diatom-based transfer function. Nature, 352, 702-704. Gasse, F., 1986. East African diatoms. Berlin: J. Cramer. Gasse, F., Juggins, S. & Ben Khelifa, L., (In press). Diatom-based transfer functions for inferring

hydrochemical

characteristics

of

African

palaeolakes.

Palaeogeography, Palaeoclimatology, Palaeoecology. Grönlund, T., 1991. New cores from Eemian interglacial deposits in Ostrobothnia, Finland. Geological Survey of Finland, Bulletin 352. Halden, B. E., 1929. Kvartärgeologiska diatomacéstudier belysande den postglaciala transgressionen å svenska Västkusten. Geol Fören Förhandl, 51, 311-66. Hustedt, F., 1930. Bacillariophyta (Diatomaceae). In A. Pascher. Die Süßwasser-flora Mitteleuropas, Heft 10, 466pp. Jena: Gustav Fischer Verlag. Krammer, K., & Lange-Bertalot, H., 1988. Süßwasserflora von Mitteleuropa. Bacillariophyceae. Teil 2. Lundquist, G. & Thomasson, H., 1923. Diatomacéekologien och kvartärgeologien. Geologiska Föreningens i Stockholm Förhandlingar, 45, 379-385. Miller, U., 1969. Fossil diatoms under the scanning electron microscope. Sveriges Geologiska Undersökning, C, 642, 5-65. 9

Miller, U., 1982. Shore displacement and coastal dwelling in the Stockholm region during the past 5000 years. Annales Academie Scientiarum Fennicae, A134, 185-211. Miller, U., 1986. Ecology and palaeoecology of brackish water diatoms with special reference to the Baltic basin. In Ricard, M. (Ed.), Proceedings of the Eigth International Diatom Symposium, Paris 1984., Koeltz Scientific Books. Miller, U. & Robertson, A.-M., 1979. Biostratigraphical investigations in the Anundsjö region, Ångermanland, N. Sweden. Early Norrland, 12, 1-76. Paddock, T. B. B., 1985. Observations and comments on the diatoms Surirella fastuosa and Campylodiscus fastuosus and on other species of similar appearance. Nova Hedwigia, 41, 417-444. Paddock, T. B. B., & Sims, P. A., 1977. A preliminary survey of the raphe structure of some advanced groups of diatoms (Epithemiaceae - Surirellaceae). Beiheft zur Nova Hedwigia, 54, 291-322. Rivera, R., 1983. A guide for references and distribution for the class Bacillariophyceae in Chile between 18° 28´ S and 58° S. Roper, F. C. S., 1854. Some observations on the Diatomaceae of the Thames. Transactions of the Microscopical Society of London, 2, 67-80. Ross, R., Cox, E. J., Karayeva, N. I., Mann, D. G., Paddock, T. B. B., Simonsen, R., & Sims, P. A., 1979. An amended terminology for the siliceous components of the diatom cell. Nova Hedwigia Beiheft, 64, 513-533. Van der Werff, A. & Huls, H., 1961. Daitomeeënflora van Nederland. Aflevering 6, December 1961. Privately published. Witkowski, A., 1990. Fossilization processes of the microbial mat developing in clastic sediments of Puck Bay (southern Baltic Sea, Poland). Acta Geologica Polonica, 40, 1-27.

10

Table 1. Measurements of valve diameter and costa density. Site Eger (n=15)

Diameter (µm) Mean Range 114 92-132

Costae/100 µm Mean Range 15 14-17

Horseshoe (n=25) Isabel (n=50) School (n=25) Shinbone (n=15)

145

114-186

16

14-18

101

77-143

19

17-21

109

92-134

16

15-17

116

104-141

17

16-19

Kindai (n=1) Adrar Bous (n=15)

99

-

14

-

149

100-223

15

12-17

Lammaslampi (n=10) Forsmarch (n=15) Norinkylä (n=6)

142

127-158

13

12-14

170

136-198

14

13-16

114

103-123

16

15-17

11

Table 2. Saline lake site details. Site Alkali, N. Dakota Free People, N. Dakota Hazelden, S. Dakota Horseshoe, N. Dakota Isabel, N. Dakota Moon, N. Dakota Piyas, S. Dakota Roslyn Pond, S. Dakota School Lake, Nebraska Shinbone, N. Dakota Spring, N. Dakota Tramping, Saskatchewan Sidi Mahdi, Algeria Lake Kindai, Tanzania Ain el Atrous, Tunisia Oued ben Ali, Tunisia

% Abundance 3 4 1 16 5 1 7 1 Abundant 29 4 8

Salinity (g l-1) 6.1 8.9 36.0 6.3 2.5 5.8 3.0 3.8 3.5 2.7 4.8 11.1

Conductivity (mS cm-1) 7.4 12.0 30.2 8.0 2.8 6.9 3.2 4.9 4.5 3.2 5.7 13.7

7 4 1 1

5.1 2.6

26.1 4.8 6.8 3.5

pH

Ion dominance

9.1 9.2 8.9 9.2 9.3 9.2 9.0 9.1 8.7 9.0

NaSO4(Cl) NaSO4(CO3) Mg(Na)SO4 NaSO4(CO3)(Cl) Na(Mg)CO3(SO4) Na(Mg)SO4(CO3) Na(Mg)SO4(Cl) K(Na)CO3(SO4) NaCO3(Cl) Na(Mg)SO4 NaSO4

8.3 -

NaCl(SO4) NaCl Na(Mg)SO4(Cl) Na(Mg)Cl(SO4)

12

Depth (m) 2.6 3.1 0.1 2.9 1.9 11.5 1.6 2.0 1.5 2.2 4.3 0.1