Charophytes, indicators for low salinity phases in North African sebkhet

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Journal of African Earth Sciences 51 (2008) 69–76 www.elsevier.com/locate/jafrearsci

Charophytes, indicators for low salinity phases in North African sebkhet Ingeborg Soulie´-Ma¨rsche * Institut des Sciences de l’Evolution, UMR 5554 du CNRS, Universite´ Montpellier II, C.c. 062, Place E. Bataillon, 34095 Montpellier-Cedex 5, France Received 25 June 2007; received in revised form 24 October 2007; accepted 10 December 2007 Available online 23 December 2007

Abstract Among water plants of lakes and ponds, the charophytes are useful for palaeolimnology because they provide autochthonous fossils in the form of their calcified fructifications, termed gyrogonites. Particular species of the Characeae are adapted to brackish water and serve as a modern analogue to infer the salinity of salt lake sediments. Here we focus on Lamprothamnium papulosum whose significance in terms of palaeo-salinity is reviewed with particular attention to the ecological requirements for calcification. New data describe the finding of L. papulosum from Holocene sediments at Sebkha Mellala, Algeria. Previous Quaternary records of this species from North Africa (Mauritania, Libya (Fezzan), Sudan, Mali and Morocco) are discussed in terms of their significance for palaeolimnology. The present paper highlights the potential of fossil charophyte gyrogonites as indicators of former low salinity phases in present-day hypersaline environments. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Holocene; Palaeolake; Brackish water; Sahara; Sabkha; Characeae

1. Introduction Charophytes (stoneworts) are a group of non-vascular, benthic macrophytes living entirely submerged in freshwater and brackish water. The general outline of the plants, somewhat resembling an aquatic horsetail due to the whorls of branchlets arising from a ‘‘stem”, makes them easy to recognise. Charophytes never occur in marine habitats neither in water bodies with permanently high salinity (Soulie´-Ma¨rsche, 1991a). Thus, living charophytes are not usually found in sebkha environments. The scarce vegetation when sebkhet are flooded is mostly composed of marine algae and cyanobacteria (Belnap, 2002). Morgan and Boy (1982) proposed a classification of continental saline waters in north-west Africa distinguishing hypersaline chotts and unvegetated sebkhet with salinity up to >300 g NaCl per litre, in contrast to vegetated sebkhet with a salinity range from 2 to 42 g NaCl per litre. This type of envi*

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ronment is generally classified as temporary brackish water lakes. Living Characeae, although noted as infrequent or in small numbers, were reported only from the ‘‘vegetated sebkhet” (Morgan, 1982). However, charophytes occur frequently in Pleistocene and Holocene deposits of unvegetated sebkhet. These fossils deserve attention, as they allow inferring conclusions about palaeo-salinity in what is today a hypersaline habitat. Usually, the fossil remains consist in the calcified female fructifications, termed gyrogonites, which display a typical and unique spiralled structure (Fig. 1). The gyrogonites represent very resistant survival organs able to withstand prolonged periods of dry out. They provide the initial source for the colonisation of watersheds. Dispersal by migrating water birds is very common (Proctor, 1962). Given the small size and highly resistant nature of these ‘‘seeds”, the strong winds in desert areas may also contribute to the dissemination of the gyrogonites. The charophytes establish pioneer vegetation in coastal ponds, interdunal ponds as well as in saline inland lakes.

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Fig. 1. Gyrogonites of L. papulosum (Wallr.) J. Groves. (a–c) Morphological variation in lateral view; (d) basal view; (e and f) apical structure. All from sebkha Mellala, Ouargla, level ALG87/320 at 1.88 m depth. Scale bars = 200 lm.

The present paper concentrates on Lamprothamnium papulosum (Wallr.) J. Groves, the foxtail stonewort, widely distributed in the Mediterranean realm and characteristic for habitats with fluctuating salinity. New material of L. papulosum from Holocene deposits of Sebkha Mellala, Algeria, is described with comments on its significance in terms of palaeo-salinity. Occurrences from other sebkhet in the Sahara, previously described from Mauritania, Libya, Sudan and Mali, are discussed. The aim of the present paper is to show the significance of gyrogonites as indicators of former periods of low salinity in present-day sebkhet. 1.1. Salinity tolerance of extant charophytes (Charales) The charophytes are basically freshwater plants. About a dozen of species can be found in brackish water. The species adapted to withstand salinity can be classified into two groups: (i) halotolerant species, meaning taxa that usually occur in freshwater but are able to support low amounts of salt, so-called ‘‘occasional halophilous” (Corillion, 1957): for instance Chara aspera Detharding ex Willdenow, a species that grows luxuriously in clear freshwater lakes in the Alps as well as in temporary brackish water ponds in the Mediterranean area; (ii) true halophilous species, meaning they need salinity to germinate and to grow: for instance Chara baltica Bruzelius with maximum salinity of 18 g l1 TDS

(total dissolved solutes) recorded in its type-region, the Baltic Sea (Blu¨mel, 2003). The halophilous taxa of the genera Chara and Nitella are usually restricted to oligo-mesohaline water (Corillion, 1957). A list of species including taxa from the Southern Hemisphere confirms this range (Garcia, 1994; Garcia and Chivas, 2006). Their salinity tolerance appears very low compared to the conditions that prevail in sebkhet when they are flooded. The most halo-tolerant taxa and the only ones hitherto recorded from sebkhet, belong to genus Lamprothamnium Groves. The habitat characteristics are similar for any of its species worldwide and make the fossil remains a suitable tool for inferring palaeo-salinity. The important point for the interpretation of fossil charophytes, however, is to know the precise conditions for a given species to produce gyrogonites. As an equivalent of the seeds of higher plants, gyrogonites are the sign of sexual reproduction, a crucial necessity for plants in temporary habitats. According to records from the literature, green, photosynthetic active plants of Lamprothamnium occur in nature from oligohaline to polyhaline water in Europe (Guerlesquin, 1992), and even under hyperhaline conditions up to 80 g l1, in diverse Australian pools (Burne et al., 1980). These data must be critically reviewed insofar the reproductive stage of Lamprothamnium is concerned. Indeed, the salinity limits for the fructification and, moreover, the calcification of the oospores of brackish water charophytes reveal much narrower, thus more significant as environ-

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mental indicators, than the range where the plants are able to stay alive. 1.2. Ecological significance of the gyrogonites Until recently, botanists were unaware of the potential interest of the gyrogonites and did not mention whether the fructifications of their material under study were calcified or not. This lack of information is still a limitation for the palaeoecological use of the Characeae. Because increasing salinity has inhibitory effect on fertilisation, the salinity range known for the plants does not necessarily apply to the conditions of full ripening and calcification. However, the gyrogonites of several characteristic brackish water species are already calibrated with respect to their ecological requirements. Significant results were obtained from culture experiments of two extant Tolypella species from brackish water localities showing that ripe oospores were only formed up to 12 g l1 of salinity whereas the plants were able to grow and regulate turgor up to 23 g l1 (Winter et al., 1996). In the case of L. papulosum, fluctuating salinity appears as a basic requirement for the species to establish population. The regular, often weekly, survey of a monospecific population in a Mediterranean pond over several consecutive years led to depict the life cycle of the species as follows (Soulie´-Ma¨rsche, 1998): (i) germination takes place at earliest 4 weeks after flooding, given that the freshwater input was sufficient to dilute the water to salinity of 20 g l1 or less in the natural habitat studied. Similarly, culture experiments of L. macropogon from Western Australia pointed to first emergence of germinands after 30 days (Sim et al., 2006), whereas Porter (2007) noted very late germination (350 days) for L. macropogon from the seedbank of saline wetlands in New South Wales. (ii) The complete life cycle from germination to full ripening of the gametangia requires a minimum time span of 3 months. Depending on temperature and light conditions, which vary from year to year, this stage may need considerably more time (Soulie´-Ma¨rsche, 1991a,b). (iii) Salinity of 40 g l1 was registered as the uppermost threshold for fecundation to take place. At higher levels of salinity, the oogonia became abortive and decayed without forming gyrogonites (Soulie´-Ma¨rsche, 1998). Even though the plants continued growing and setting both antheridia and oogonia (L. papulosum is a monoecious species), the oogonia at the whorl which had reached the developmental stage necessary for fecundation (c. the 5th whorl from top) became all white, a clear sign of abortion. In case of subsequent dilution to less than 40 g l1, through heavy rainfall for instance, the oogonia of the next whorl which, meanwhile, had reached the right stage

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of maturity became fertilised and then formed the black oospores prior to calcificaton. Thus, in case of rapid salinity fluctuation, the plants could show a whorl bearing well-calcified gyrogonites situated above a lower whorl with abortive oogonia. These basic ecological requirements were recently confirmed through culture experiments of Australian Lamprothamnium-species (Sim et al., 2006), so that they are likely to apply to the overall genus. Indications for the presence of gyrogonites are still scarce in the botanical literature. Collections of fertile specimens of Lamprothamnium, though not necessarily bearing gyrogonites, were mentioned especially in Australia, where much attention is drawn on saline wetlands. At Little Dip lake, South Australia, the developmental stages of L. papulosum as a function of the salinity curve clearly show that fertile specimens occurred only at low salinity of ±20 g l1 (Brock, 1981). Sebkha-like conditions with salinity of 50–100 g l1 and halite crust on the bottom at lake Cockajemmy, Victoria, showed many dead charophytes whereas a healthy fertile population of L. macropogon (A. Braun) Ophel was collected at Lake Glenthompson at 32 g l1 TDS (Garcia and Chivas, 2004). Abundant L. succinctum gyrogonites were also described from lake Wollumboola, New South Wales, at a total salinity of 20 g l1 (Garcia and Chivas, 2004). The salinity at time of collection of fruiting L. haesseliae Donterberg in Laguna La Salada, Argentina was 23 g l1 in a water body ranging annually from 10 to 50 g l1 (Garcia, 1993). In several cases, gyrogonites were mentioned from plants collected at high salinity (Davis and Lipkin, 1986; Garcia and Chivas, 2004). The point is that the salinity in this case corresponds to the values measured on the day of collection. However, it is evident that the gyrogonites on these plants had formed a couple of days or even weeks prior to collecting at a moment when the salinity was undoubtedly different and certainly lower than the day of collection. Salts concentrate very quickly as a function of evaporation in habitats as shallow as 30–40 cm depth. In Mediterranean ponds observed by the author, salinity sometimes increased by 10 g l1 in 1 week. Taking in account this point, the presence of gyrogonites on plants collected at high salinity cannot be considered a proof that they actually did form and calcify at high salinity. Careful survey of the correlation between life cycle and salinity dynamics will be necessary in the future to provide a valuable picture for other brackish water species. Insofar L. papulosum from Europe and North Africa is concerned, despite the fact that the vegetative parts can support concentrated water, the gyrogonites attest to a salinity range between 20 and 40 g l1 (Soulie´-Ma¨rsche, 1998). 2. Study site and material Sebkha Mellala is an endorheic basin located in the vicinity of Ouargla, Algeria, northern Sahara (32°110 N;

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5°120 E). In an early paper, Sebkha Mellala was described as a shallow Miocene subsidence basin occupied by a salt pan (Wurm, 1953). The site was then the subject of intensive investigations within the frame of PALHYDAF, a program devoted to the palaeo-hydrology of Africa (Fontes and Gasse, 1986, 1991; Gibert, 1989; Gasse et al., 1990). The presence of charophyte gyrogonites in the Holocene sediments from Sebkha Mellala was first mentioned by Boye´ et al. (1978) who reported Characeae s. l. (Chara spp.) in sediments collected from a yardang in the western part of Sebkha Mellala. This outcrop was again sampled by the PALHYDAF-team and completed by a core down to 6.2 m. Detailed study, including sedimentology, mineralogy, stable isotope analyses and 14C dating was performed by Gibert (1989). Biological remains (ostracodes, molluscs, charophytes and foraminifera) were also taken in account. Here we focus on the charophytes, previously noted as Lamprothamnium cf. papulosum (Gibert et al., 1990). Location and description of the section are given in that paper. The gyrogonites were recovered from the outcrop part of the section by Gibert and are studied here for the first time from the micropaleontological point of view. Material: sample numbers and radiocarbon dating refer to the levels as indicated in Gibert (1989) (figs. 93 and 102). Gyrogonites were isolated from three levels in the section: ALG 87/320 located at 1.88 m depth 14C dated 8370 ± 800 yr BP; ALG 87/331, 332, 333 from 1 m depth with an 14C age of 7240 ± 250 yr BP and ALG 87/338 at 0.5 m. In the following, 14C ages from earlier references were converted to cal. yr BP according to the terrestrial radiocarbon age calibration by Reimer et al. (2004). 3. Results 3.1. Systematic account     

Class Charophyta Migula 1890. Order Charales Lindley 1836. Family Characeae L.Cl. Richard 1815. Genus Lamprothamnium Groves 1916. L. papulosum (Wallr.) J. Groves (Fig. 1a–f).

3.1.1. Description Gyrogonites medium sized, 625–950 mostly 750– 850 lm in length and 500–600 lm in width, with cylindrical to broadly cylindrical shape; apex and basal pole rounded; 7–9, mostly 8 spiral turns visible in lateral view. Lime spirals concave or flat; apical ends of the spiral cell typically less or even not calcified; however, sutural crests pursuing to top. Basal opening pentagonal with basal plug visible at outer level. Well-preserved specimens display fan-like structure of the calcification, visible on sections only. The biometrical parameters for length, width and length-width-ratio  100 (ISI) of the gyrogonites are added in order to enable comparison with other and further Lamprothamnium finds (Table 1).

Table 1 L. papulosum (Wallr.) J. Groves. Biometrical data for the gyrogonites from three different levels of Sebkha Mellala, Ouargla, Algeria Sample no.

N

Min.a Max.a Meana Confid. int.a s2

V (%)

Length (lm) 338 20 333 30 320 50

700 625 700

900 875 975

781 736 823

771–791 722–749 819–836

2492 4254 4190

6.4 8.9 7.9

Width (lm) 338 333 320

20 30 50

400 425 450

600 575 625

494 484 544

483–505 476–492 537–551

3018 1530 1213

11.1 8.1 6.4

ISI (100 L/w) 338 20 333 30 320 50

120 130 127

200 194 195

160 153 152

156–165 149–156 149–155

0.05 13.7 0.03 10.9 0.02 9.4

Abbreviations: ISI, Isopolarity index = 100  length/width; N, number of measurements; min., lowest value; max., highest value measured in each sample; mean, average value; confidence interval as x ± 2sd; s2, variance; V, variation index. a Measurements are in micrometers (lm).

3.1.2. Remarks The gyrogonites of all Lamprothamnium species share typical morphological features that allow easy recognition in the fossil state. These were defined as follows (Soulie´Ma¨rsche, 1989): general outline tending from prolate to cylindrical with apex truncate in lateral view; calcification of the spiral tips weak or absent at the apical pole; basal plug visible at outer level; section of the spiral cells showing locally a fan-like structure due to the calcification which appears oriented towards the sutures and not in parallel layers like in Chara (Soulie´-Ma¨rsche, 1989, Pl. IX); oospore inside the gyrogonite densely covered with granules and typically undulated intercellular crests (Soulie´-Ma¨rsche, 1989, Pl. V). These features proved constant at generic level and are valid for both living and fossil material. Although subject to important variation, size and shape of the gyrogonites serve to delimit various species (Soulie´-Ma¨rsche, 1982; Garcia, 1993; Garcia and Chivas, 2004). The gyrogonites from the three levels analysed for Sebkha Mellala display a shift of average size from large specimens (in level 320) to relatively smaller ones towards top of the section (Table 1). Compared to the variability in extant populations, this suggests that submersion time tended to become shorter in the more recent levels (Soulie´-Ma¨rsche, 1982, 1989). During the earlier stage, Sebkha Mellala could have been even an intermittent lake with longer lasting periods of salinity fluctuation within the range of 20–40 g l1 NaCl. 3.2. Comparison with geochemical data Sebkha Mellala represents the first example from the Sahara where the Charophytes can be correlated with results from geochemical data. According to previous investigations (Gibert, 1989), the Lamprothamnium occur-

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rences correspond to portions of the section that show relatively low values of o13C and o18O from the inorganic carbonates which were interpreted as phases of dilution (ibid fig. 96). In parallel, the mineralogy showed high calcite content and remarkably low percentage of bassanite and gypsum (less than 25%) compared to most of the mineralogical profile where gypsum was largely dominant (Gibert, 1989). The maximum dilution appeared at 1.88 m depth in sample 320 which was 14C dated to 8370 ± 800 (corresponding to 9320 cal. yr BP). This level contained also the highest amount of charophyte gyrogonites indicating that Sebkha Mellala was a shallow saline lake subjected to seasonal fluctuations of salinity with prolonged phases of dilution. This part of the section (stage IIIB in Gibert et al., 1990) also contained numerous other calcareous microorganisms such as the foraminifera Ammonia beccarii Linne´ var. tepida Cushman, Miliolids and the ostracode Cyprideis gr. torosa Jones. This fossil assemblage is typical for brackish water habitats with fluctuating salinity. Because Ammonia beccarii, in contrast to other benthic foraminifera, cannot survive to a dry up phase (Cann and De Deckker, 1981), it points to a period when Sebkha Mellala was a permanent, however lowsaline, inland lake. Dilution down to 19.5 g l1 was mentioned as the lowest salinity where A. beccarii was found (Menon et al., 2000). The association is a sign of contrasted seasonal alternance of low and high saline phases. In terms of climate, this implies that freshwater input through precipitation or river discharge must have occurred to create the salinity range for optimal development of both L. papulosum and A. beccarii. After that, Sebkha Mellala underwent a period of severe drought attested by positive o18O values and the absence of fossils. Consecutively, a second phase of dilution, corroborated by the presence of gyrogonites, started abruptly around 7240 ± 250 yr BP (Gibert, 1989) corresponding to 8130 cal. yr BP (Gasse, 2002). The upper part of the section, from 1 m depth to surface, contained Cyprideis gr. torosa almost throughout. Charophytes made a short reappearance only at 0.5 m (sample 338). We interpret this as a sign of short-lived, ephemeral floods that allowed the ostracods to hatch but not the plants to fulfil their life cycle. Due to deflation of the younger sediments, the top of the sequence stops at 4950 ± 90 yr BP, corresponding to an age of 5690 cal. yr BP (Gasse, 2002). The close parallel of geochemical and mineralogical results with the occurrence of calcified L. papulosum fructifications, depicted in the studied section, confirms that the ecological requirements known for the living species can be used as a modern analogue to interpret the salinity of ancient sediments. The results from the pluridisciplinary study of the Sebkha Mellala profile led to infer the existence of two main periods of dilution during the Early Holocene. The humid phase was interrupted by a sudden phase with high evaporation rate (at ca. 8300 cal. yr BP) when the lake water had concentrated beyond the tolerance

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of even brackish water organisms (Gibert et al., 1990; Gasse, 2002). This short but abrupt lake-status reduction was evidenced as a general trend for numerous palaeolakes in the Sahara (Damnati, 2000; Hoelzmann et al., 2004). 4. Discussion L. papulosum, the most salt tolerant species among the Characeae, points to ecosystems of ‘‘vegetated sebkha type” characterised by significant periods of at least 3 months of salinity below 40 g l1.The species has been identified in a number of other North African palaeolakes. The context of all these localities corresponds to similar ecological conditions. 4.1. Mauritania The presence of hundreds of gyrogonites in the lacustrine marl collected from Sebkha Idjill (22°750 N; 12°410 W) and Sebkha Touirist (26°820 N; 7°310 W), both located on the tropic of Cancer, indicate actively reproducing populations growing under optimal conditions. The waterbodies were probably brackish lakes of ca. 1–1.5 m depth, which filled these topographic depressions during humid intervals of the Nouakchottian period (ca. 7840–4440 cal yr BP). This led to infer a period of regular seasonal precipitation in northern Mauritania, a region that receives less than 50 mm of rainfall today (Soulie´-Ma¨rsche, 1998). A considerable amount of freshwater input must be assumed so as to compensate for the salinity due to washout of the underlying substrate which had to become diluted to as low as 20 g l1. Subsequently, the salinity had to remain at no more than 40 g l1 during at least 3 months to allow L. papulosum to fulfil its life cycle. 4.2. Wadi Ash Shati, Fezzan, Libya The area of Wadi Shati (23°300 N; 13–15°E) was occupied by a Pleistocene lake characterised by the presence of huge accumulation of Cerastoderma glaucum shells (Petit-Maire et al., 1980; Petit-Maire, 1982). The deposits alternate locally with thin fine-grained layers containing Melania tuberculata Mu¨ller as well as freshwater Gastropods (Rosso and Gaillard, 1982). Microfaunal remains of Cyprideis and Ammonia beccarii were also identified (Carbonel, 1982; Blanc-Vernet, 1982). L. papulosum was described from the outcrop section XIV, located in the north-central part of the 220 km long depression of Wadi Shati (Soulie´-Ma¨rsche, 1982). This section corresponds to the second out of three Pleistocene lacustrine phases evidenced by Th/U dating and was given an age of 90,000 yr BP (Gaven et al., 1981; Gaven, 1982). Recently published OLS datings tend to elder the deposits to 100–110 ka (Armitage et al., 2007). The palaeolake of Wadi Shati was mainly a highly saline lake as inferred from the proliferation and dominance of the marine bivalves (Cerastoderma glaucum Bruguie`re

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being considered a synonym of Cerastoderma (Cardium) edule Linneaus). However, the occurrence of organisms needing low salinity or even freshwater obviously attests to a complex salinity pattern. Section XIV, which contained the gyrogonites, shows topographic relationship to a fluvial system that could have provided freshwater input from the catchment, thus locally diminishing the salinity. The context of Wadi Ash Shati as a huge depression with three successive lacustrine phases suggests that the lake was not always a single, continuous water body but had split into a number of separate saline lakes and ponds. Depending on surface and depth, every individual water body thus would have had different water regimes and different salinity. Such a patchy pattern of habitats gave rise to a great variety of fossil assemblages of different ecological conditions.

the infill phase of the lake. The water was then brackish due to the washout of the salts that had accumulated during the previous arid phases. The development of L. papulosum indicates that dilution occurred rapidly in parallel to abrupt climate change. The immediately following levels contained Chara zeylanica Willdenow, a species restricted to fresh- or oligohaline water (Soulie´-Ma¨rsche, 1991b, 1993b, 2002). The palaeolake El Haijad thus changed rapidly from sebkha-like conditions to a nearly freshwater lake. A considerable amount of freshwater input appears necessary to dilute the initial brine so as to enable C. zeylanica to establish a healthy population. The thickness and topographic distribution of the lacustrine sediments suggest a lake area of 55 km2 with an optimal depth of 9 m in the centre of the lake (Fabre, 1991). 4.5. Global significance of brackish water Charophytes

4.3. North-eastern Sahara Charophytes were published from a great number of Early to Mid Holocene palaeolakes in Sudan (Soulie´-Ma¨rsche, 1993a). A highly significant freshwater species, Nitellopsis obtusa (Desvaux in Lois.-Deslongchamps) Groves, allowed to identify several relatively deep (4–12 m), perennial freshwater lakes (Pachur and Kro¨pelin, 1987; Pachur et al., 1987; Kro¨pelin and Soulie´-Ma¨rsche, 1991; Soulie´Ma¨rsche, 1993a). Saline conditions, inferred from L. papulosum, appeared in the Late Mid-Holocene in playa lakes at Wadi Shaw (Gabriel and Kro¨pelin, 1984; Gabriel, 1986). It was shown that the lakes had progressively changed from an oligohaline habitat with Chara vulgaris L. to brackish water playas (Soulie´-Ma¨rsche, 1993b). L. papulosum pointed to saline conditions also for a short dry interval at Selima (21°19’N; 29°180 E) confirmed by the ostracods and gypsum intercalation (Pachur and Wu¨nnemann, 1996; Pachur and Hoelzmann, 2000). 4.4. Taoudenni basin, Mali During the Holocene, the present-day hyperarid Taoudenni basin was occupied by a mosaic of water bodies of various types ranging from perennial freshwater to brackish water. L. papulosum was found in several short-lived ponds or playa lakes. The species provided highly significant information about the infill phase of palaeolake El Haijad. The lacustrine sequence of El Haijad was analysed over 4.20 m thickness. According to the 14C datation, the sequence covers the time span from 8300 ± 100 BP to 4400 ± 270 yr BP (Petit-Maire et al., 1987; Delibrias et al., 1991; Petit-Maire, 1991). Conversion appears somewhat divergent: 9240 to 5020 cal. yr BP was proposed by Gasse (2002); 8800–4700 in Hoelzmann et al. (2004). L. papulosum was present only in the lowermost level of the El Haijad section (original reference MT6 in PetitMaire, 1991; referenced to as S5 in Gasse, 2002; as S2 in Hoelzmann et al., 2004). This single horizon represents

Charophyte gyrogonites were also mentioned in Mesozoic sebkhet sequences (Look, 2002). Similar to Recent, they are indicative for fresh- to low salinity environments. The palaeoecological conditions for the main groups of Mesozoic charophytes were inferred through comparison with associated ostracod species (Schudack, 1993). Only three taxa appeared to tolerate brackish water within a salinity range estimated to 16–30 g l1. Unless they are very sparse due to transportation, Mesozoic charophytes always point to supra-tidal environment. Lamprothamnium gyrogonites are useful environmental indicators in two different ways. As shown in this paper, Lamprothamnium points to periods of low salinity when found in hypersaline environments. Inversely, it can indicate times of increasing salinity when found in a context of freshwater as for instance at Sidi Bou Rhaba lake, Morocco (34°240 N; 06°670 W) (ElKhiati et al., 2004). Physico-chemical analyses of the lake water during the past 20 years recorded a salinity range of 2–8 g l1 and only a flora of low saline species of genus Chara was known. A core in this coastal lake revealed the presence of L. papulosum at 0.40 m and 1 m depth. In that case, the finds attest to phases of increased salinity that could be correlated with periods of hydrological deficit. 5. Conclusion Charophytes are a group of aquatic macrophytes that produce highly resistant calcified survival organs, the gyrogonites (Fig. 1). The present paper stresses the potential of the gyrogonites of genus Lamprothamnium as indicator taxa for low salinity phases in sebkhet. Sebkha environments require a high potential of reproduction so as to insure the survival of aquatic plants over prolonged hypersaline and/or dry periods. The gyrogonites represent the seed bank of the charophytes. The essential point for accurate interpretation of the fossil gyrogonites is the precise calibration of the ecological conditions that actually allow sexual reproduction and calcification.

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To fulfil its life cycle, the circum-Mediterranean species, L. papulosum needs salinity fluctuation with low salt content of less than 20 g l1 at the time of germination, and a minimum flooding period of 3 months. Salinity of 40 g l1 represents the uppermost threshold for fecundation to take place. At higher salinity, the oogonia fail to calcify and do not produce gyrogonites, thus will not provide fossils (Soulie´-Ma¨rsche, 1998). The presence of fossil gyrogonites of L. papulosum in Holocene palaeolake sediments makes evidence that the growth conditions were suitable for complete ripening and calcification of the fructifications. They indicate habitat characteristics corresponding to brackish water bodies subjected to intermittent water regime with periodically diluted phases at low salinity about or less than 20 g l1. The L. papulosum occurrences from palaeolakes in the Sahara correspond to this type of environment and can be correlated with the Holocene humid periods. The presence of L. papulosum gyrogonites can be a useful tool for palaeolimnology in two different ways: (i) found in sebkha sediments, they indicate obligatory low saline phases; (ii) found in a context of freshwater or low saline deposits, they point to phases with increased salinity. Charophytes have been present in non-marine rocks since the Upper Silurian (420 Ma). They are not infrequent in Mesozoic deposits and can provide palaeo-environmental information for sebkha deposits of any geological period. Acknowledgements The gyrogonite material from Sebkha Mellala was kindly provided by E. Gibert. I wish to thank J. Maley for fruitful discussion and help with literature. This is publication n. 2008-002 of the Institut des Sciences de l’E´volution, UMR 5554/ CNRS. References Armitage, S.J., Drake, N.A., Stokes, S., El-Hawat, A., Salem, M.J., White, K., Turner, P., McLaren, S.J., 2007. Multiple phases of North African humidity recorded in lacustrine sediments from the Fazzan Basin, Libyan Sahara. Quaternary Geochronology 2, 181– 186. Belnap, J., 2002. Macroalgae associated with sabkha. In: Barth, H.-J., Bo¨er, B. (Eds.), Sabkha Ecosystems, vol. 1, The Arabian Peninsula and Adjacent Countries. Tasks for Vegetation Sciences, vol. 36. Kluwer Academic Publishers, Dordrecht, NL, pp. 227–232. Blanc-Vernet, L., 1982. Foraminife`res. In: Petit-Maire, N. (Ed.), Le Shati, lac ple´istoce`ne au Fezzan (Libye). Centre Re´gional de Publication du C.N.R.S, Marseille, pp. 72–77. Blu¨mel, C., 2003. Chara baltica Bruzelius 1824. In: Charophytes of the Baltic Sea. The Baltic marine Biologists Publication No. 19. A.R.G. Gantner Verlag, Ruggell, Finland, pp. 53–63. Boye´, M., Marmier, E., Nesson, C., Trecolle, G., 1978. Les de´poˆts de la sebkha Mellala, environs de Ouargla Sahara alge´rien N-E se´dimentologie, aˆge, enseignement morphologique. Revue de Ge´ologie Dynamique 28 (2–3), 49–52. Brock, M.A., 1981. The ecology of halophytes in the south-east of South Australia. Hydrobiologia 81, 23–32. Burne, R.V., Bauld, J., De Deckker, P., 1980. Saline lake charophytes and their geological significance. Journal of Sedimentary Petrology 50, 281–293.

75

Cann, J.H., De Deckker, P., 1981. Fossil Quaternary and living foraminifera from athalassic (non-marine) saline lakes, Southern Australia. Journal of Palaeontology 55 (3), 660–670. Carbonel, P., 1982. Ostracodes. In: Petit-Maire, N. (Ed.), Le Shati, lac ple´istoce`ne au Fezzan (Libye). Centre Re´gional de Publication du C.N.R.S., Marseille, pp. 69–71. Corillion, R., 1957. Les Charophyce´es de France et d’Europe occidentale (e´tude syste´matique, e´cologique, phytosociologique et phytoge´ographique). The`se-e`s-Sciences, Universite´ Toulouse, Rennes, Imprimerie Bretonne. Damnati, B., 2000. Holocene lake records in the Northern Hemisphere of Africa. Journal of African Earth Sciences 31 (2), 253–262. Davis, J.S., Lipkin, Y., 1986. Lamprothamnium prosperity in permanently hypersaline water. Schweizer Zeitschrift fu¨r Hydrobiologie 48 (2), 240– 246. Delibrias, G., Fontugne, M., Arnold, M., 1991. Datations par le 14C. In: Petit-Maire, N. (Ed.), Pale´oenvironnements du Sahara. Lacs Holoce`nes a` Taoudenni (Mali). Centre Re´gional de Publication du C.N.R.S, Marseille, pp. 177–180. Elkhiati, N., Soulie´-Ma¨rsche, I., Gemayel, P., Flower, R., Ramdani, M., 2004. Recent environmental changes at Sidi Bou Rhaba lake (Morocco) inferred from sub-fossil Charophyte gyrogonites. Cryptogamie-Algologie 25 (2), 185–198. Fabre, J., 1991. Le lac holoce`ne de Haijad: cadre ge´ologique et e´volution. In: Petit-Maire, N. (Ed.), Pale´oenvironnements du Sahara. Lacs Holoce`nes a` Taoudenni (Mali). Centre Re´gional de Publication du C.N.R.S., Marseille, pp. 81–89. Fontes, J.-C., Gasse, F., 1986. Palhydaf: e´tat d’avancement novembre 1985. In: Inqua-Asequa (Ed.), Dakar Symposium, ‘‘Changements globaux en Afrique durant le Quaternaire”. Orstom, Bondy, France, pp. 149–152. Fontes, J.-C., Gasse, F., 1991. PALHYDAF (Palaeohydrology in Africa) program: objectives, methods, major results. Palaeogeography, Palaeoclimatology, Palaeoecology 84, 191–215. Gabriel, B., 1986. Die o¨stliche lybische Wu¨ste im Jungquarta¨r. Berliner Geographische Studien 19, 1–219. Gabriel, B., Kro¨pelin, S., 1984. Holocene lake deposits in Northwest Sudan. In: Coetze, J.A., Van Zinderen Bakker, E.M. Sr. (Eds.), Palaeoecology of Africa and the Surrounding Islands, vol. 16. Balkema, Rotterdam, pp. 295–299. Garcia, A., 1993. Quaternary and recent Lamprothamnium Groves (Charophyta) from Argentina. In: Hurlbert, S.H. (Ed.), Saline Lakes V, Hydrobiologia, vol. 267, pp. 143–154. Garcia, A., 1994. Charophyta: their use in paleolimnology. Journal of Paleolimnology 10, 43–52. Garcia, A., Chivas, A.R., 2004. Quaternary and extant Lamprothamnium Groves (Charales) from Australia: Gyrogonite morphology and paleolimnological significance. Journal of Paleolimnology 31, 321–341. Garcia, A., Chivas, A.R., 2006. Diversity and ecology of extant and quaternary Australian charophytes (Charales). Cryptogamy/Algology 27 (4), 323–340. Gasse, F., 2002. Diatom-inferred salinity and carbonate oxygen isotopes in Holocene waterbodies of the western Sahara and Sahel (Africa). Quaternary Science Reviews 21, 737–767. Gasse, F., Te´het, R., Durand, A., Gibert, E., Fontes, J.C., 1990. The aridhumid transition in the Sahara and the Sahel during the last deglaciation. Nature 346, 141–146. Gaven, C., 1982. Radiochronologie isotopique ionium-uranium. In: Petit-Maire, N. (Ed.), Le Shati, lac ple´istoce`ne au Fezzan (Libye). Centre Re´gional de Publication du C.N.R.S., Marseille, pp. 44–54. Gaven, C., Hillaire-Marcel, C., Petit-Maire, N., 1981. A Pleistocene lacustrine episode in southeastern Libya. Nature 290, 131–133. Gibert, E., 1989. Ge´ochimie et pale´ohydrologie des bassins lacustres du nord-ouest saharien. Programme Palhydaf, site 2. Unpublished Thesis. Universite´ Paris-Sud. Gibert, E., Arnold, M., Conrad, G., De Deckker, P., Fontes, J-Ch., Gasse, F., Kassir, A., 1990. Retour des conditions humides au Tardiglaciaire

76

I. Soulie´-Ma¨rsche / Journal of African Earth Sciences 51 (2008) 69–76

au Sahara septentrional (Sebkha Mellala, Alge´rie). Bulletin de la Socie´te´ ge´ologique de France (8) t. VI no. 3, 497–504. Guerlesquin, M., 1992. Systematique et bioge´ographie du genre Lamprothamnium (Charace´es) caracte´ristique des biotopes aquatiques saumaˆtres. Revue des Sciences de l’Eau 5, 415–430. Hoelzmann, P., Gasse, F., Dupont, L., Salzmann, U., Staubwasser, M., Leuschner, D.C., Sirocko, F., 2004. Palaeoenvironmental changes in the arid and subarid-belt (Sahara-Sahel-Arabian Peninsula) from 150 ka to present. In: Battarbee, W., Gasse, F., Stickley, C.E. (Eds.), ‘‘Past Climate Variability through Europe and Africa” Developments in Paleoenvironmental Research. Springer, pp. 219– 256. Kro¨pelin, S., Soulie´-Ma¨rsche, I., 1991. Charophyte remains from Wadi Howar as evidence for deep mid-Holocene freshwater lakes in Eastern Sahara (NW Sudan). Quaternary Research 36, 210–223. Look, B., 2002. Sabkhas ancient and modern. Gulf Coast Association of Geological Societies Transactions 52, 645–657. Menon, N.N., Balchand, A.N., Menon, N.R., 2000. Hydrobiology of the Cochin brackwater system – a review. Hydrobiologia 430, 149–183. Morgan, N.C., 1982. An ecological survey of standing waters in North West Africa: II Site descriptions for Tunisia and Algeria. Biological Conservation 24, 83–113. Morgan, N.C., Boy, V., 1982. An ecological survey of standing waters in North West Africa: I. Rapid survey and classification. Biological Conservation 24, 5–44. Pachur, H.-J., Hoelzmann, P., 2000. Later Quaternary plaeoecology and palaeoclimates of the eastern Sahara. Journal of African Earth Sciences 30 (4), 929–939. Pachur, H.-J., Kro¨pelin, S., 1987. Wadi Howar: palaeoclimatic evidence from an extinct river system in the southeastern Sahara. Science 237, 298–300. Pachur, H.-J., Ro¨per, H.-P., Kro¨pelin, S., Goschin, M., 1987. Late Quaternary hydrogeography of the eastern Sahara. Berliner geowissenschaftliche Abhandlungen (A) 75 (2), 331–384. Pachur, H.-J., Wu¨nnemann, B., 1996. Reconstruction of the palaeoclimate along 30°E in the eastern Sahara during the Pleistocene/Holocene transition. Palaeoecology of Africa and the surrounding Islands 24, 1– 32. Petit-Maire, N., 1982. Le Shati, lac ple´istoce`ne au Fezzan (Libye). Centre Re´gional de Publication du C.N.R.S., Marseille. Petit-Maire, N., 1991. Pale´oenvironnements du Sahara. Lacs Holoce`nes a` Taoudenni (Mali). Centre Re´gional de Publication du C.N.R.S., Marseille. Petit-Maire, N., Delibrias, G.G., Gaven, C., 1980. Pleistocene lakes in the Shati area, Fezzan. Palaeoecology of Africa and the surrounding Islands 12, 289–295. Petit-Maire, N., Fabre, J., Carbonel, P., Schulz, E., Aucour, A.-M., 1987. La depression de Taoudenni (Sahara malien) a` l’Holoce`ne. Ge´odynamique 2/2, 61–67. Porter, J.L., 2007. Contrasting emergence patterns of Lamprothamnium macropogon (Characeae, Charophyceae) and Ruppia tuberosa (Potamogetonaceae) from arid-zone saline wetlands in Australia. Charophytes 1 (1), 19–27.

Proctor, V.W., 1962. Viability of Chara oospores taken from migratory water birds. Ecology 45, 656–658. Reimer, P.J., Baillie, M.G.L., Bard, E., Bayliss, A., Beck, J.W., Bertrand, C., Blackwell, P.G., Buck, C.E., Burr, G., Cutler, K.B., Damon, P.E., Edwards, R.L., Fairbanks, R.G., Friedrich, M., Guilderson, T.P., Hughen, K.A., Kromer, B., McCormac, F.G., Manning, S., Bronk Ramsey, C., Reimer, R.W., Remmele, S., Southon, J.R., Stuiver, M., Talamo, S., Taylor, F.W., van der Plicht, J., Weyhenmeyer, C.E., 2004. IntCal04 Terrestrial radiocarbon age calibration, O-26 cal kyr BP. Radiocarbon 46, 1029–1058. Rosso, J.-C., Gaillard, J., 1982. Mollusques testace´s (Macrofaune). In: Petit-Maire, N. (Ed.), Le Shati, lac ple´istoce`ne au Fezzan (Libye). Centre Re´gional de Publication du C.N.R.S., Marseille, pp. 55–68. Schudack, M.E., 1993. Die Charophyten in Oberjura und Unterkreide Westeuropas mit einer phylogenetischen Analyse der Gesamtgruppe. Berliner geowissenschaftliche Abhandlungen (Reihe E) 8, 1–209. Sim, L.L., Chambers, J.M., Davis, J.A., 2006. Ecological regime shifts in salinised wetland systems I. Salinity thresholds for the loss of submerged macrophytes. Hydrobiologia 573, 89–107. Soulie´-Ma¨rsche, I., 1982. Charophytes. In: Petit-Maire, N. (Ed.), Le Shati, lac ple´istoce`ne au Fezzan (Libye). Centre Re´gional de Publication du C.N.R.S., Marseille. Soulie´-Ma¨rsche, I., 1989. Etude compare´e de gyrogonites de Charophytes actuelles et fossiles et phyloge´nie des genres actuels. (The`se-e`s-Sciences, Universite´ Montpellier, 1979, revised edition). Millau, France, Imprimerie des Tilleuls. Soulie´-Ma¨rsche, I., 1991a. Charophytes as lacustrine biomarkers during the Quaternary in North Africa. Journal of African Earth Sciences 12 (1/2), 341–351. Soulie´-Ma¨rsche, I., 1991b. Flores de Charophytes des pale´olacs de Taoudenni. In: Petit-Maire, N. (Ed.), Pale´oenvironnements du Sahara. Lacs Holoce`nes a` Taoudenni (Mali). Centre Re´gional de Publication du C.N.R.S., Marseille, pp. 167–172. Soulie´-Ma¨rsche, I., 1993a. Diversity of Quaternary aquatic environments in NE Africa as shown by fossil Charophytes. In: Thorweihe, U., Schandelmeier, H. (Eds.), Geoscientific Research in Northeast Africa. Balkema, Rotterdam, pp. 575–579. Soulie´-Ma¨rsche, I., 1993b. Apport des Charophytes fossiles a` la recherche de phe´nome`nes climatiques abrupts. Bulletin de la Socie´te´ ge´ologique de France 164 (1), 123–130. Soulie´-Ma¨rsche, I., 1998. Fossil Lamprothamnium papulosum (Charophyta), a biomarker for seasonal rainfall in northern Mauritania. Palaeoecology of Africa and the surrounding Islands 25, 65–76. Soulie´-Ma¨rsche, I., 2002. Les Charophytes comme biomarqueurs pour la reconstitution des pale´oenvironnements lacustres. In: Miskovsky, J.Cl. (Ed.), Ge´ologie de la Pre´histoire: Me´thodes Techniques Applications. GEOPRE, Paris, pp. 751–769. Winter, U., Soulie´-Ma¨rsche, I., Kirst, G., 1996. Effects of salinity on turgor and fertility in Tolypella (Characeae). Plant, Cell and Environment 19, 869–879. Wurm, A., 1953. Der Schott von Mellala. Natur und Volk 83 (6), 202–203.