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Revue d’Ecologie (Terre et Vie), Vol. 73 (4), 2018 : 414-430

PALAEOECOLOGICAL SIGNIFICANCE AND CONSERVATION OF PEAT-FORMING WETLANDS OF ALGERIA

Karima GHIT1*, Serge D. MULLER2, Gérard DE BÉLAIR1, Djamila BELOUAHEM-ABED3, Amina DAOUD-BOUATTOUR4,5 & Mohamed BENSLAMA1

1 Laboratoire de recherche en Sols et Développement Durable, Département de Biologie, Faculté des Sciences, Université Badji-Mokhtar, BP 12, 23000 Annaba, Algérie 2 Université de Montpellier/CNRS, Institut des Sciences de l’Evolution de Montpellier, Place E. Bataillon, case 061, 34095 Montpellier cedex 05, France 3 Institut National de Recherche Forestière, Station de Recherche, El Kala (El Tarf), Algérie 4 Université de la Manouba, Faculté des Lettres, des Arts et des Humanités - UR99/UR/02-04 Biogéographie, Climatologie Appliquée et Dynamique Érosive, 2010 Manouba, Tunisie 5 Université de Tunis El Manar, Faculté des Sciences de Tunis, Département de Biologie, Campus Belvédère, 2092 Tunis, Tunisie * Corresponding author: [email protected]

RÉSUMÉ.— Signification paléoécologique et conservation des zones humides tourbeuses d’Algérie.— Les complexes humides de Numidie (Maghreb nord-oriental) abritent des milieux tourbeux dont l’histoire est très mal connue. Des études palynologiques ont été réalisées dans une aulnaie et une ériçaie tourbicole du complexe de Guerbès-Senhadja, dans le but de préciser leur origine, leur histoire et leur signification paléoécologique. Les séquences étudiées remontent à 8000 et 5300 ans, respectivement pour l’ériçaie et l’aulnaie. L’ériçaie à Erica scoparia, jamais décrite sur le plan phytosociologique, apparaît comme une formation ancienne et bien préservée, à très fort enjeu conservatoire. L’aulnaie a en revanche une origine récente (< 2000 ans), possiblement en lien avec une (ré-)immigration holocène de l’aulne depuis l’Europe méridionale. Les dégradations anthropiques très fortes subies par les milieux étudiés au cours des dernières années rendent urgentes l’implémentation de mesures conservatoires drastiques dans le but de préserver les derniers vestiges régionaux de ces milieux humides patrimoniaux.

SUMMARY.— The wetland complexes of Numidia (northeastern Maghreb) include peat-forming habitats whose history is largely unknown. To explore their origin, history, and palaeoecological significance, palynological studies were undertaken in an alder carr and a wet heathland of the Guerbès-Senhadja wetland complex, which go back 5300 and 8000 years respectively. The Erica scoparia heathland, which has never been described phytosociologically, appears to be an ancient and well-preserved ecosystem with a very high conservation value. The alder carr, which is recent (< 2000 years), may well be related to a Holocene (re-) immigration of alder from southern Europe. Given the significant anthropogenic disturbances of these habitats over the last years, drastic conservation measures are urgently needed to preserve these last regional vestiges of these patrimonial wetlands.

______The Numidia, a hotspot of biodiversity in the Mediterranean basin (Véla & Benhouhou, 2007), constitutes a major biogeographical crossroads of European, Mediterranean, and subtropical floristic elements (Arènes, 1951; de Bélair, 2005). The region is also unusual for its many wetlands, which are unique in the Maghreb by virtue of their size and diversity. Given the diversity of functions fulfilled by these ecosystems (feeding and reproduction habitat for avifauna, rich flora refuge, etc.; Stevenson et al., 1988; Boulekhssaïm et al., 2006), they have major ecological and conservation value (Samraoui & de Bélair, 1998). The Guerbès-Senhadja wetland complex (western Numidia) covers approximately 400 ha, or nearly 20 % of the vast wetland eco- complex of northeastern Algeria (Abdenouri, 1996; Samraoui & de Bélair, 1997). Together with the El Kala complex, it houses exceptional biodiversity that was first described in the pioneering works of Cosson (1885), Maire (1926) and Gauthier-Lièvre (1931). G. de Bélair (1987, 2005) and Samraoui & de Bélair (1997) have also shown that they are home to some of the richest aquatic

414 and amphibious plant communities of the Maghreb. Among these communities, Alnus glutinosa constitutes extensive peat-forming alder carrs with northern affinities, entirely unusual in North Africa (Junqua, 1954; Belouahem-Abed et al., 2011). Such formations are found in northern Morocco (Fennane et al., 1999; Lepais et al., 2013) and northwestern Tunisia (Nègre, 1952; Pottier-Alapetite, 1979-1981), but nowhere are they as extensive as in the El Kala and Guerbès- Senhadja wetland complexes. For this reason, northeastern Algerian wetlands were classified as Ramsar sites in 2001. Their fragile biodiversity remains under threat in the short term from rapidly growing anthropogenic pressures (Aouadi, 1989; Belouahem-Abed et al., 2011; Bouldjedri et al., 2011). In addition to their proximity to cities and extensive agriculture, the sustainability of these areas is threatened by the development of tourism, irrigation for agriculture, uncontrolled water pumping, illegal deforestation and uncontrolled landfill. Implementing long-term conservation measures is thwarted by the lack of knowledge about the past dynamics and resilience of these ecosystems (Willis & Birks, 2006; Daoud-Bouattour et al., 2011). Very few palaeoecological studies have been made in northern Algeria. Of those that have been done, some have addressed the history of vegetation in the Akfadou Massif (western Kabylia), focusing on Cedrus atlantica (Salamani, 1991, 1993), and others have looked at peat accumulation and the history of vegetation in the wetland complexes of northeastern Algeria (Benslama, 2001; Ibncherif, 2012). Other regions in the Maghreb are better known thanks to palynological studies documenting vegetation and climate histories in the principal Tunisian (Ben Tiba, 1982; Stambouli-Essassi et al., 2007) and Moroccan mountains (Reille, 1976; Muller et al., 2014) and southern steppes (Ritchie, 1984; Damblon & Vanden Berghen, 1993). Some studies have addressed the history of societies and their impact on palaeoenvironments (Ballouche, 1986; Ballouche & Damblon, 1988) but very few have examined the local dynamics of wetlands for historical clues to their conservation management (Birks, 1996; Willis & Birks, 2006): We can cite the work of Amami et al. (2013) who reconstructed the origin and developmental history of a temporary pond in the Benslimane region in Morocco and the work of Daoud-Bouattour et al. (2011), who argues for a palaeoecological approach to wetland conservation in Northern Tunisia. The present work aims to: (1) reconstruct the origin and historical dynamics of two peat- forming wetlands located in the Guerbès-Senhadja complex, (2) evaluate the current state compared to the historical state of the wetlands, and (3) specify the previous influence of human activities.

MATERIAL AND METHODS

GEOGRAPHICAL AND GEOLOGICAL SETTING The Guerbès-Senhadja wetland complex (Fig. 1) covers the eastern coastal area of Skikda Province in western Numidia. It is bordered to the northeast by the Edough Massif, to the northwest by the Filfila Massif, to the north by the Mediterranean, to the southeast by the Boumaïza massif, and to the southwest by Jebel Safia. It extends between the latitudes 36°46' N and 37°00' N and longitudes 07°08' E and 07°25' E. Located downstream of the Wadi El-Kebir West basin, the complex is mostly covered by wetlands (c. 230 km²). Its slopes vary between 0-16 % and elevation ranges from sea level to 472 m. The lands surrounding the wetlands are locally used to raise vegetable crops in sand. The area’s geological formations are complex (Hedjal, 2014). The bedrock consists of crystallophyllian metamorphic series (glandular gneiss, schistose gneiss, micaschist granifer with cipolin and laminated gneiss), and Mesozoic-Cenozoic sediments, the facies of which indicate deposits in various marine environments from lagoons to continental-fluvial depending on climatic and eustatic variations. These geological formations are mainly outcropping on reliefs (Edough, Boumaïza and Ain Mokra-Wady El Aneb Mountains) overlooking the valleys of Wadis El Kebir East and West. Although dune formations represent the marine Quaternary locally, continental Quaternary formations dominate the plains and the valleys carved by the wadis.

PRESENT-DAY CLIMATE AND VEGETATION The study area belongs to the subhumid ambiance of the thermomediterranean bioclimate, characterized by wet, cold winters and hot, dry summers. Average annual rainfall ranges from 800 to 1000 mm. The average temperatures in the

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Skikda region are 17.8°C for the year, 12.7°C for the coldest month and 25.7°C for the hottest month (source: Skikda weather station, period 1997-2013). Humidity is high and almost constant around 70 % throughout the year. It peaks in January (71.8 %) and reaches its minimum in August (67.4 %). This is probably due to the numerous wetlands of the area, to the proximity of the sea and to the important forest cover (Bazri, 1999). The average annual potential evapotranspiration of the region varies between 1100 and 1300 mm (Mebarki, 2005), while the actual evapotranspiration of the study area is between 870 and 890 mm (Hadj-Saïd, 2007), which can be attributed to the extensive swamps along Wadi El Kebir. Prevailing northwest and northeastly winds model coastal dunes and trees. These climatic and geomorphological conditions (Morgan, 1982) together with the presence of sandy-clay substrates that favour the formation of hydromorphic soils (Benslama, 1993) have led to a local abundance of alders (Alnus glutinosa). The Guerbes plain is a huge water reservoir of approximately 40 million m3 in volume with many depressions and valleys. Its drainage system consists essentially of Wadis El Kebir and Magroune (DGF, 2002). Degraded formations of cork oak (Quercus suber) on the interior dunes and kermes oak (Q. coccifera) on the coastal dunes are the primary vegetation. Wetlands are represented mainly by alder carrs, freshwater or brackish marshes, wadis, dams, and water reservoirs (Samraoui & de Bélair, 1997).

Figure 1.— Location of studied sites. A. Studied region. Numbers correspond to previous palynological studies: 1, la Châtaigneraie (Salamani, 1991); 2, Messaoussa (Ibncherif, 2012); 3, Lac Noir (Benslama, 2001); 4, Righia (Benslama, 2001); 5, Bourdim (Benslama et al., 2010); 6, Beni M’Tir (Stambouli-Essassi et al., 2007); 7, Dar Fatma (Ben Tiba & Reille, 1982; Stambouli-Essassi et al., 2007); 8, Majen Ben M’Hida (Stambouli-Essassi et al., 2007). B. Wetland complex of Guerbès-Senhadja, with both studied sites (triangles) and the Messaoussa alder carr (2). C. Location of cores taken respectively in the alder carr of Bouchagora (Bou) and in the heathland of Sidi Freitis (SF3).

STUDY SITES Our study focused on two contrasted peaty habitats located near the town of Ben Azzouz (Skikda Province): the Bouchagora alder carr and the Sidi Freitis wet heathland (Fig. 1). They were selected for their important surface areas, their relatively preserved vegetation covers, and because they belong to the same wetland unit, making them putatively two different stages of the local hydroseral dynamic. The Bouchagora alder carr (36°54'34"N, 07°17'35"E, 7 m a.s.l.) is a 54 ha peat-forming habitat located approximately 1 km from Sidi Freitis Lake and a few kilometres upstream of the Messaoussa alder carr, the largest of the Guerbès- Senhadja complex (280 ha) (Ibncherif, 2012). These carrs have a dense canopy dominated by Alnus glutinosa, associated with Ficus carica, Laurus nobilis, Prunus avium, Rubus ulmifolius, Salix pedicellata and Vitis vinifera. The understory varies with the microtopography, and includes Athyrium filix-femina, Carex spp., Iris pseudacorus, Lycopus europaeus, Ludwigia palustris, Lythrum salicaria, Osmunda regalis, Persicaria spp., Sparganium erectum, Tamus communis and Thelypteris palustris (Appendix).

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The peat-forming heathland of Sidi Freitis (36°54'11''N, 07°17'05''E, 32 m a.s.l.) sits on a slight slope in an interdunal depression oriented NW to SE above Sidi Freitis Lake. It is fed by subterranean dune waters in the northwest and by several dune springs in the west and east. The peat is not deeper than 70 cm. The area is now severely degraded: drainage ditches have been dug, the peripheries of the heathland have been cleared for several years, and the center of the heathland was almost entirely burned in 2013 (Fig. 1). As a result, the former shrub formation has gradually been replaced by wet meadows. In 2010, those areas of the heathland that were still preserved were dominated by Erica scoparia, locally associated with Cladium mariscus, Eleocharis multicaulis, Hypericum afrum, Potamogeton polygonifolius, Rhynchospora modesti-lucennoi, Rubus ulmifolius, Salix pedicellata and Succisa pratensis (Fig. 1). Secondary wet meadows were heavily grazed by livestock, but impressive populations of rare and/or endemic hydrophytes (Bellis prostrata, Carex hispida, C. punctata, Dactylorhiza munbyana, Fuirena pubescens, Ranunculus flammula and Schoenus nigricans) continued to exist.

FIELDWORK AND LABORATORY ANALYSES In February and March 2014, two cores were taken using a Russian corer (Jowsey, 1966) in the Sidi Freitis heathland (SF3) and the Bouchagora alder carr (Bou). They were described superficially in the field and refrigerated until sampling. Botanical surveys (following Braun-Blanquet, 1932) were carried out in both environments (20-30 m radius around the coring site). Initial identifications were made using the Flora of Algeria (Quézel & Santa, 1962-1963) and the botanical nomenclature was revised with synonymic indexes of plants of North Africa (Dobignard & Chatelain, 2010-2013) and Tunisia (Le Floc’h et al., 2010). The cores were accurately described in the laboratory. Sediment colours were codified using Munsell Colour charts (Munsell Colour, 1975). 2 cm3 samples were then taken every 5 cm for physico-chemical analysis, and 1 cm3 samples were taken for pollen analysis every 5 cm (24 samples) on the SF3 core, and every 2 cm (48 samples) on the Bou core. A physico-chemical analysis was carried out on wet peat to measure water pH, electrical conductivity, and the respective proportions of organic carbon, humidity and organic matter. Water pH (standard AFNOR X 31-103) was determined by electrometric measurement using a pH-meter equipped with a glass electrode (AFES, 1995) in a supernatant solution of a soil mixture liquid in a 1:2.5 proportion. Electrical conductivity (EC, in μS/cm) was determined by an electrometric measurement in the same solution using a conductivity meter (model WTW Multiline P3 PH/LF-SET, CellOx 325, modified from Aubert, 1978). Organic carbon content (OC, in %) was measured by wet oxidation in a sulphochromic environment that was heated (Anne method; ISO-14235, 1998). Water content (WC, in %) was measured by drying at 105°C for 24 hours (Baize, 1988), and organic matter content (OM, in %) was measured by burning at 450°C for 4 hours (loss-on-ignition method; Dean, 1974). Pollen was extracted using the conventional method of a hydrofluoric acid (HF) attack followed by acetolysis (Erdtman, 1960; Berglund & Ralska-Jasiewiczowa, 1986). Under an optical microscope, pollen grains were identified using the reference collection of the Institut des Sciences de l’Evolution (Université de Montpellier) and pollen atlas (Reille, 1992-1999). Pollen sums, which exclude Pteridophyta spores (Berglund & Ralska-Jasiewiczowa, 1986), exceeded 500 grains. Because our study deals with the past dynamics of local hydrophytic vegetation, aquatic taxa were integrated within pollen sums. Pollen concentrations (PC, in grains.cm-3) were measured using the volumetric method (Davis, 1965). Pollen richness was standardized according to the pollen count (individual rarefaction analysis) using the PAST program (Hammer et al., 2001). Diagrams were made with Polpal software program (Nalepka & Walanus, 2003), and zoning was done with the CONISS program (Grimm, 1987).

RADIOCARBON DATING AMS radiocarbon dating was carried out on five sediment samples at the Poznań (Poland) laboratory and calibrated using CALIB software program version 7.04 (Stuiver & Reimer, 1993), based on the IntCal13 standard (Reimer et al., 2013). Because the studied sediments are strongly decomposed and contain neither macroremains nor rootlets, the radiocarbon measurements were made on bulk sediments.

RESULTS

CHRONOLOGY Age-depth models (Fig. 2) were made by linear interpolation using 4 radiocarbon ages (Tab. I). Linear interpolation gives erroneous models, with artificial sharp changes in estimated accumulation rates at dated horizons, but the limited dating evidence does not allow calculating reliable smoothed age-depth models. For this reason, the presented linear models should be used cautiously. They nevertheless allow calculating mean sediment accumulation rate between dated levels and estimating approximate dating of past events. The three ages of the Bou sequence are consistent, but the modern age obtained for the 30- 31 cm level, which may result from bioturbation or root penetration, was rejected. The alder carr

417 sequence (Bou) covers the last 5300 years; the heathland sequence, although less thick, covers the last 8000 years. Sediment accumulation rates are very low in the sandy-silty deep deposits (0.03 to 0.08 mm/yr), and higher in the upper peat layers, where they have accumulated over the last centuries (0.44 to 0.83 mm/yr). While neither pollen nor stratigraphy evidences sedimentation hiatuses, their possible occurrence in the studied sequences should modify both the proposed chronology and the estimated accumulation rates.

Figure 2.— Stratigraphy and age-depth models of cores Bou and SF3. The white dot on the Bou diagram represents the rejected modern age.

TABLE I Radiocarbon dating of Bouchagora (Bou) and Sidi Freitis (SF3)

Site Depth (cm) Labo code Dated material Age BP Age cal. BP Bou 30-31 Poz-79616 Peat - 900 ± 23 Modern 52-53 Poz-79617 Silty sand 710 ± 30 690-570 89-90 Poz-79618 Silty sand 4610 ± 35 5460-5090 SF3 30-32 Poz-74081 Silty sand 775 ± 30 1280-1210 55-57 Poz-74082 Silty sand 7120 ± 50 6070-5900

SEDIMENTOLOGY AND PHYSICO-CHEMICAL PARAMETERS Alder carr of Bouchagora. The core Bou (Fig. 3) presents 4 sediment facies: - Zone BS1 (90-42 cm) is composed of sandy sediment that is poor in organic matter (OM). The deposit is uniform and grey in colour (code 5/1 5YR). - Zone BS2 (42-15 cm) presents a fibrous texture more or less rich in OM. This zone contains organic residues and radicels, and is dark brown in colour (code 2.5/2 5YR).

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- Zone BS3 (15-10 cm) shows a marked change of sediment (sand), with less organic residues and is grey-brown (code 3/1 5YR). - Zone BS4 (10-0 cm) corresponds to a dark brown to black peat (code 2.5/1 5YR) that is rich in organic residues and roots. Its OM content is the highest of the core.

Figure 3.— Physico-chemical data of sediment sequences of Bouchagora alder carr (Bou) and Sidi Freitis heathland (SF3). OC, Organic carbon; OM, Organic matter; PC, Pollen concentration.

pH is slightly acidic in the entire sequence and acidity tends to increase from the base to the surface. Similarly, the electric conductivity (EC) reaches a peak of 168 µS at a depth of 15-20 cm. The OM content increases progressively to reach a maximum of 75% in the surface peat layer. The organic carbon (OC) content is very low and surprisingly constant. Finally, the humidity curve is similar to the one of OM. Peat-forming heathland of Sidi Freitis. The core SF3 (Fig. 3) presents 3 sediment facies: - Zone FS1 (60-30 cm) is constituted by sandy sediment without organic residues and is dark grey brown (code 3/2 10YR). - Zone FS2 (30-10 cm) has a clayey-peaty texture with inclusions of organic residues and is black (code 2/1 10YR). - Zone FS3 (10-0 cm) corresponds to a black peat (code 2.5/1 5YR), and is rich in residues and OM. The pH is almost neutral and stable along the whole profile. The EC records weak fluctuations and tends to increase from the base to the surface. Similarly, the humidity and OM content increase towards the top, whereas the OC content remains constant.

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POLLEN DIAGRAM Alder carr of Bouchagora. The alder carr pollen diagram (Fig. 4) presents high pollen richness, with a total of 63 taxa for a standardized average of 39.7 taxa per level. Many taxa present continuous curves along the profile, but two major changes in pollen spectra composition make it possible to identify 3 pollen zones:

Figure 4.— Simplified pollen diagram of Bouchagora alder carr (Bou). Grey curves correspond to hydrophytic taxa.

- Zone BP1 (90-54 cm; c. 5280-880 cal. BP) is dominated by Erica-type, which represents 40-50% of the pollen assemblages in the lower part of the sequence. Calystegia, Pinus and Poaceae present optimums in this zone. Osmunda is well recorded. - Zone BP2 (54-32 cm; c. 880-390 cal. BP) appears as a transition between Erica-type that strongly declines and Alnus that increases. Frangula and Osmunda are particularly well recorded, and Persicaria appears in the pollen spectra. The percentages of some anthropogenic indicators (Amaranthaceae, Asteroideae, Olea, Plantago) increase roughly synchronously around 50 cm. - Zone BP3 (32-0 cm; c. 390-0 cal. BP) is dominated by Alnus that reaches 62% towards the surface. Pollen concentrations (Fig. 3) are relatively high (average of 277 000 grains.cm-3) and vary enormously. More specifically, two phases present extreme variations (90-76 and 26-12 cm), without any obvious relationship with the nature of sediments. Peat-forming heathland of Sidi Freitis (SF3). The pollen diagram (Fig. 5) presents a total richness of 43 taxa with a standardized average of 42.0 taxa per level. The very stable curves make it difficult to interpret the diagram, which does however show the constant abundance of Erica- type, which fluctuates around 30 % along the whole profile. Two pollen zones have been defined (Fig. 5): - Zone FP1 (60-44 cm; c. 7940-4460 cal. BP) is characterized by the dominance of herbs, and by a slight decrease in Pinus percentages and a peak of Myrtus at a depth of 50 cm. The Myrtus peak, corresponding to one level only, could result from the local occurrence of the species and/or a falling stamen. Surrounding mesophilous vegetation is characterized by Olea and Quercus suber. - Zone FP2 (44-0 cm; c. 4460-0 cal. BP) shows a peak of Arbutus that reaches 15 % at a depth of 25 cm, associated with some trees such as Olea and Quercus suber. Anthropogenic

420 indicators are weakly recorded, but the Carduus-type presents a continuous curve and the percentage of Fabaceae increases from 27.5 cm and higher. Pollen concentrations (Fig. 3) are also relatively high (average of 233 000 grains.cm-3) and variable.

Figure 5.— Simplified pollen diagram of Sidi Freitis heathland (SF3). Grey curves correspond to hydrophytic taxa.

DISCUSSION

ECOLOGICAL SIGNIFICANCE OF PEAT-FORMING HEATHLAND OF ERICA SCOPARIA Pollen diagrams (Figs. 4 & 5) reveal that both coring sites were occupied by a formation of Erica-type. The heathland persisted for the last c. 8000 years at Sidi Freitis and from c. 5300 to 900 cal. BP at Bouchagora. Similar records occurred in the northeastern Maghreb: Righia, Lac Noir and Bourdim in El Kala National Park (Benslama, 2001; Benslama et al., 2010), Messaoussa in the wetland complex of Guerbès-Senhadja (Ibncherif, 2012), Beni M’Tir and Dar Fatma in Kroumiria (Ben Tiba & Reille, 1982; Stambouli-Essassi et al., 2007) and Majen Ben M’Hida in Mogods (Stambouli-Essassi et al., 2007). In all of these diagrams, Erica-type curves (that can reach 70 % of pollen sum) have been interpreted as a regional development of Erica arborea. Indeed, the Erica-type pollen record may exceed 50 % in E. arborea stands (Ben Tiba, 1982). However, its regional signal trapped in lake sediments is always weak (Peglar et al., 2001; Benslama et al., 2010; Touati, 2013), whereas, by contrast, it often becomes dominant in peaty habitats (Ben Tiba & Reille, 1982; Benslama, 2001; Stambouli-Essassi et al., 2007; Benslama et al., 2010). This indicates that the pollen record of Erica-type in Maghreb is mainly of local – rather than regional – origin. The taxon Erica-type includes two species growing in the region and around the studied sites. Erica arborea is generally abundant in dry open cork oak forests. Locally, it occurs in the cork oak belt bordering the Bouchagora alder carr and is lacking at Sidi Freitis. In contrast, the ecological significance of Erica scoparia in the Maghreb is poorly understood. This species, absent from Bouchagora, constitutes an almost pure peat-forming heathland at Sidi Freitis. Curiously, botanists and palynologists have never investigated its current or past role in the regional vegetation. For instance, the phyto-ecological map of Northern Tunisia (Gounot & Schoenenberger, 1967) mentions it only as constituting a facies of the endemic Pinus pinaster subsp. renoui forests. However, in the region encompassing Numidia, Kroumiria and Mogods (Fig. 1), the species dominates peat-forming heathlands that are home, in particular, to Carex spp., Eleocharis

421 multicaulis, Lythrum salicaria, Osmunda regalis, Pteridium aquilinum and Salix pedicellata (Ferchichi-Ben Jamaa et al., 2010; unpublished data). Floristic data from southern Spain and Corsica reveal that E. scoparia becomes water-demanding in the southern part of its distribution area where it is confined in valley bottoms and wet depressions (Merino et al., 1976; Jeanmonod & Gamisans, 2007). All these elements suggest that the Erica-type pollen found in the peats of northeastern Maghreb corresponds primarily to E. scoparia that is the only regional Erica species to constitute peat-forming swamps. Moreover, available floristic data attest to the local occurrence of E. scoparia in 4 of the studied sites: Bourdim (de Bélair, 1990-1995), Dar Fatma (unpublished data), Lac Noir (de Bélair & Samraoui, 1994) and Righia (Belouahem-Abed et al., 2011). In Bourdim, it has become rare, and has disappeared from the dense alder carr of Messaoussa (Appendix) (de Bélair, 1990-1995; Belouahem-Abed et al., 2011). A comparison of pollen and phytosociological data from Sidi Freitis (Fig. 5; Appendix) confirms the existence of numerous taxa for the last 8000 years that were still present locally today: Asteroideae (Bellis annua, B. prostrata, Dittrichia viscosa), Callitriche (C. brutia, C. obtusangula, C. stagnalis), Caryophyllaceae (Malcolmia ramosissima, Spergula arvensis), Cyperaceae (Carex hispida, C. punctata, Cladium mariscus, Eleocharis multicaulis, Fuirena pubescens, Rhynchospora modesti-lucennoi, Schoenus nigricans), Fabaceae (Dorycnium rectum, Genista ferox), Juncus-type (J. articulatus, J. bulbosus, J. effusus, J. tenageia), Lythrum borysthenicum-type (L. hyssopifolia, L. junceum, L. portula), Poaceae (Phragmites australis), Potamogeton (P. nodosus, P. polygonifolius), Myrtus communis, Rubiaceae (Galium palustre, Rubia peregrina), Ranunculus-type (R. flammula, R. macrophyllus), Salix (pedicellata) and Sparganium-Typha (T. domingensis). The peat-forming heathland probably occupied the entire interdunal depression overhanging Sidi Freitis Lake until it was cleared in the late 20th century. Prior to 900 cal. BP, Bouchagora vegetation was very similar to that in Sidi Freitis, but also included Calystegia sepium and Osmunda regalis. The persistence of the composition and diversity of the peat-forming heathland for at least 8000 years at Sidi Freitis and for more than 4000 years at Bouchagora, as well as its numerous palaeoecological records thoughout the northeastern Maghreb (Ben Tiba & Reille, 1982; Benslama, 2001; Stambouli-Essassi et al., 2007; Benslama et al., 2010), suggest that this habitat should be considered ancient (maybe even pristine) and to predate the alder carr onset.

ORIGIN AND DYNAMICS OF ALDER CARR In northeastern Maghreb, Alnus glutinosa dominates vast peat-forming swamps located on riverbanks or in interdunal depressions (Schoenenberger et al., 1970; Géhu et al., 1993) where as much as 10 m of peat have accumulated (Benslama, 2001; Ibncherif, 2012). The mean accumulation rates calculated for the alder phases of Bouchagora and Messaoussa (Ibncherif, 2012) are 0.83 and 1.21 mm/yr respectively, more than 10 times that of the Erica phases at Bouchagora (0.08 mm/yr) and Sidi Freitis (0.07 mm/yr on average). This difference could reflect the amount of biomass produced, which is supposed to be higher in the alder carr (higher and larger trees and shrubs) than in the heathland. While the regional presence of Alnus in Kroumiria from 50,000 to 30,000 cal. BP (Ben Tiba & Reille, 1982; Stambouli-Essassi et al., 2007) and in western Kabylia from 12,000 to 6000 cal. BP (Salamani, 1991) are confirmed, the rare chronologies available for the NE Maghreb suggest that its carrs developed between 1900 (Bourdim; Benslama et al., 2010) and 900 cal. BP (Bouchagora; this study). Alder never extended to Mogods (Stambouli-Essassi et al., 2007; Rouissi, 2016) in Tunisia, and was recorded sporadically during the Holocene in Kroumiria (Stambouli-Essassi et al., 2007). Erica scoparia is a heliophilous species that doubtless disappeared from Bouchagora and Messaoussa as it lost the competition for light with alder. The recent onset of alder carrs implies either that local environmental conditions were unfavourable for

422 the development of Alnus glutinosa or that it was not present in the region during most of the Holocene. The first hypothesis necessarily involves an environmental change during the last two millennia and presents two problems. First, the available climate reconstructions for the central Mediterranean (Magny et al., 2007) show that precipitation tended to decrease during the last millennia. This seems unlikely to support the late development of a water-demanding species such as alder. Second, the early record of peat-forming habitats could indicate that local favourable conditions may have existed prior to 2000 cal. BP, i.e. before the onset of alder carrs. It however should be noted that all peats are not necessarily suitable for alder growth (a local example is given by the heathland of Sidi Freitis where no alder occurs). The second hypothesis implies that Alnus glutinosa became rare or extinct in the region during the Holocene. The current extension of the species makes this difficult to imagine, but there are two supporting arguments. The first is the weak, discontinuous pollen record of Alnus in all Holocene diagrams of northeastern Maghreb. Given that the hydrochore dispersion of the species (McVean, 1955) should promote its spread along rivers, this suggests that it was absent from regional watersheds. A comparable situation could have existed during the early Holocene in NW Europe, where alder was widely distributed but persisted in low abundance until conditions became suitable (e.g. Bennett & Birks, 1990). It however differs from the Algerian history by the determinism of the alder limitation that was climatic in Europe and probably not in Maghreb. The second argument is provided by a coalescent-based simulation approach applied on a microsatellite genotyping (Lepais et al., 2013). This study suggests that Alnus glutinosa arrived late in Tunisia and Algeria from southern European populations, by contrast with the northern Moroccan populations, which have ancient origins. However, the available palaeoclimate and pollen data are too scarce and fragmentary to validate this hypothesis definitively, especially for explaining why Alnus declined during the Holocene in the northeastern Maghreb.

PAST INFLUENCE OF ANTHROPIZATION Although the pollen records of Bouchagora and Sidi Freitis that show a very local signal provide little information about the dynamics of regional vegetation, some features can be highlighted. Wetland surroundings comprised wooded dunes and hills that were probably covered for millennia by Quercus coccifera, Q. suber and Juniperus oxycedrus subsp. macrocarpa, as reflected in 19th century descriptions (Cosson, 1861; Vars, 1896). Pollen data suggest that these formations, which included Arbutus unedo and Olea europaea, remained stable for most of the Holocene. Local populations were probably limited by the malaria that was endemic in the wetland complexes of northeastern Algeria until the early 20th century (and led to the death in 1861 of the French botanist La Perraudière; Cosson, 1861; Bensaid & Gasmi, 2008). Both studied sequences show a surprising non-synchronous decrease in pine pollen percentages, dated around c. 6000 cal. BP at Sidi Freitis, and between c. 3000 and 1600 cal. BP at Bouchagora. It is unlikely that these features, which do not figure in other regional pollen studies, reflect modifications of the endemic maritime pine (Pinus pinaster subsp. renoui) populations growing on the hinterland mountains. Rather, they could result from the closure of local canopies filtering long-distance pollen input (Tauber, 1965; Muller et al., 2006), and obviously should not be attributed to anthropogenic activities. Consequently, our data reveal that the initial inhabitants of Numidia (Berber populations called Lybians in ancient texts; Kitouni Daho & El Mostepha Filah, 2003), like those in the Moroccan Rif (Muller et al., 2014), had no impact on the surrounding vegetation cover. Nor did the Phoenicians who traded with indigenous populations along the Kabylian-Numidian coast as of the 5th century BC, or the Punics who controlled the main ports as of the end of the 3rd century BC (Bertrandy, 1976; Laporte, 2004). A maritime Punic settlement, called Stora, was established in the most sheltered part of Skikda bay (Vars, 1896).

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Greek and Latin historians (e.g. Polybius, Caesar, Sallustus, Titus-Livius, Diodorus, Plutarch, Appian, etc.), and archaeological remains suggest that the primary function of romanized North Africa was to supply Rome with necessary agricultural products such as cereals and oil (Albertini, 1931). Their cultivation during the Roman-Byzantine expansion has been recorded in many parts of the Mediterranean (Brun, 1992), but was not detectable in our diagrams. The apparent stability of vegetation during Roman times, as recorded by palynological studies (Muller et al., 2014), could be attributed to the fact that the vegetation impacted, especially in the large alluvial valleys, was primarily composed of weak pollen producers such as Olea, Pistacia and Tamarix spp. The Romans occupied Skikda, known as Rusicade, as of 44 BC; it was elevated to the rank of colony in 26 BC. In the 2nd century AD during the reign of Hadrian, an ingenious irrigation system was built using the water supplying the city and its port (Bouchareb, 2006). While our study sites are only 30 km from Skikda, our pollen diagrams show no contemporary regional changes provoked by humans. Because of the local origin of the recorded pollen, this indicates that anthropogenic activities did not extend to the vicinity of Bouchagora and Sidi Freitis. After the Vandals settled in North Africa in 429 AD (Kitouni Daho & El Mostepha Filah, 2003) following the fall of the Roman empire, Rusicade was plundered and eventually razed in 533 AD (Bouchareb, 2006). The town was not rebuilt until 1838, when it became known as Philippeville (Gsell, 1898). Neither the 6th century Byzantine invasion nor the 7th century Muslim conquest left any trace in pollen diagrams or in historical or archaeological sources (Laporte, 2004). Despite the chronological uncertainties and the local pollen record of the studied sequences, the unchanging landscape surrounding the investigated sites over successive invasions resembles the situation observed in the Moroccan Rif (Muller et al., 2014). It suggests that the waves of invaders remained in coastal cities primarily to promote local trade and/or export agricultural products from the large alluvial valleys rather than settling in the rural hinterlands. Anthropization indicators were almost absent from most of the studied sedimentary sequences. The continuous pollen record of Olea and Poaceae could reflect the local development of wild olive and aquatic Poaceae such as Glyceria, which has a cereal-type pollen (mean diameter: 42.7 ± 1.8 µ) and is still present in Sidi Freitis Lake. However, anthropization indicators point to a late, slight but obvious sign of human activities, mainly grazing (Amaranthaceae, Asteroideae, Carduus-type, Fabaceae, Plantago; Behre, 1981). Notwithstanding the low chronological resolution of the study, the onset of anthropization is dated synchronously to about 600 cal. BP in both diagrams. This date coincides with the beginning of the reign of the Hafsid Sultan Abû Faris, who unified Numidia and Tunisia in the early 15th century. It just predates the first signs of anthropization detected in the Moroccan Rif, contemporaneous with the beginning of the Sharifian Arab dynasties (Muller et al., 2014).

CONCLUSION

Scientists have long decried the ongoing dramatic decline of wetlands provoked by humans in the studied zone and more specifically in northeastern Algeria (Bougazelli et al., 1976; de Bélair & Samraoui, 1994; Bouazouni, 2004; Belouahem-Abed et al., 2011; Bouldjedri et al., 2011). Their warnings have had no effect on the illegal burning, draining, pumping and the uncontrolled expansion of seasonal production of watermelon, melon, tomato, and pepper which are destroying the last vestiges of the Guerbès-Senhadja wetlands. Palynological data have confirmed the historical significance of both great types of swamps of the large Algero-Tunisian region encompassing Numidia, Kroumiria and Mogods. They show (1) the ancient origin of the peat-forming heathland, a rare plant formation that has not been described phytosociologically, and (2) the relatively recent origin of alder carrs that have developed for less than 2 millennia at the expense of heathlands in the wetter zones of the watersheds.

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These natural habitats have existed for millennia thanks to very weak anthropogenic impacts. Highly natural and virtually undisturbed, they are home to exceptional biodiversity (Samraoui & de Bélair, 1997; Muller et al., 2010). All of this points to the gravity of the threats and makes it extremely urgent that local authorities address the situation. Without protection, these habitats will surely disappear in the coming years. Nevertheless, the current species diversity is a legacy of past, species-rich communities, which are at risk of extinction debt, i.e. slow but inevitable extinction triggered by habitat destruction (Tilman et al., 1994), so current diversity is no guarantee of continued survival, even if anthropogenic pressures were removed.

ACKNOWLEDGEMENTS

The authors express their gratitude to M. Robles for the measurements of Poaceae pollen grains from slides of the ISEM reference pollen collection (Université de Montpellier), to the three anonymous reviewers whose comments were greatly appreciated and helped to improve the manuscript, and to D. Glassman for her editorial assistance. This paper is the contribution ISE-M no 2018-048.

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APPENDIX

Phytosociological relevés realised in the alder carrs of Bouchagora (BOU) and Messaoussa (MES), located downstream from Bouchagora, and in the heathland of Sidi Freitis (SFE)

Species Family BOU1 BOU2 BOU3 MES SFE1 SFE2 SFE3 Relevé date 05.05.12 25.11.17 25.11.17 13.05.11 07.04.10 25.11.17 25.11.17 Vegetation cover (%) 80 60 60 70 100 100 100 Naked soil (%) 20 40 40 30 10 10 10 Species richness 38 30 39 22 31 28 24 Surface (ha) 54 54 54 280 2 2 2 Agrostis semiverticillata (Forssk.) Christ. Poaceae 1 Agrostis stolonifera L. Poaceae 1 1 Alnus glutinosa (L.) Gaertn. Betulaceae 5 4 1 5 2 Alternanthera sessilis (L.) DC. Amaranthaceae 2 Amaranthus lividus L. Amaranthaceae 2 Anagallis crassifolia Thore Primulaceae 1 Arisarum vulgare Targ.Tozz. Araceae 2 2 1 Arum italicum Mill. Araceae + 2 Asphodelus ramosus L. Xanthorrhoeceae 1 Asplenium obovatum Viv. Aspleniaceae + + Athyrium filix-femina (L.) Roth. Woodsiaceae 5 2 3 Bellis annua L. Asteraceae 1 1 1 Bellis prostrata Pomel Asteraceae 2 2 Brachypodium sylvaticum (Huds.) P.Beauv. Poaceae 2 1 Bryonia dioica Jacq. Cucurbitaceae 1 Callitriche brutia Petagna Plantaginaceae 1 Callitriche obtusangula Le Gall Plantaginaceae 1 1 Callitriche stagnalis (L.) Scop. Plantaginaceae 1 1 Calystegia sepium (L.) R.Br. Convolvulaceae 1 1 1 1 Carex elata All. Cyperaceae 3 1 Carex hispida Willd. Cyperaceae 2 1 Carex paniculata L. Cyperaceae 1 + Carex pendula Huds. Cyperaceae 1 1 Carex pseudocyperus L. Cyperaceae 4 1 Carex punctata Gaudin Cyperaceae 2 Carex remota L. Cyperaceae 4 2 2 4 Chenopodium sp. Amaranthaceae 2 Circaea lutetiana L. Oenotheraceae + 1 Cladium mariscus (L.) Pohl. Cyperaceae 2 3 2 Coleostephus myconis (L.) Cass. ex Rchb. f. Asteraceae 1 Cynodon dactylon (L.) Pers. Poaceae 2 Cynoglossum cheirifolium L. Boraginaceae 1 Cynosurus polybracteatus Poir. Poaceae + 1 Dactylorhiza munbyana (Boiss. & Reut.) Aver. Orchidaceae 1 Daphne gnidium L. Thymelaeaceae 1 Datura stramonium L. Solanaceae 1 Daucus carota L. subsp. maximus (Desf.) Ball Apiaceae 2 Digitaria sanguinalis (L.) Scop. Poaceae 1 Dittrichia viscosa (L.) Greuter Asteraceae 2 Dorycnium rectum (L.) Ser. Fabaceae + 1 Eleocharis multicaulis (Sm.) Desv. Cyperaceae 3 3 Erica scoparia L. Ericaceae 5 3 4 Ficus carica L. Moraceae 2 2 2 Fuirena pubescens (Poir.) Kunth Cyperaceae 1 Galium palustre L. subsp. elongatum (C.Presl) Lange Rubiaceae 1 1 + Genista ferox Poir. Fabaceae 1 Geranium dissectum L. Geraniaceae 1 Hedera helix L. Araliaceae 2 2 2 Hypericum afrum Lam. Hypericaceae 3 3 2 Hypochaeris radicata L. Asteraceae 1 2 1 Iris pseudacorus L. Iridaceae 2 2 Jacobae eratica (Bertol.) Fourr. Asteraceae 1 Juncus articulatus L. Juncaceae 1 1 1

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Species Family BOU1 BOU2 BOU3 MES SFE1 SFE2 SFE3 Juncus bulbosus L. Juncaceae 1 Juncus effusus L. Juncaceae 1 + Juncus tenageia L.fil. Juncaceae 1 Laurus nobilis L. Lauraceae 2 2 Ludwigia palustris (L.) Elliot Oenotheraceae 1 2 1 Lycopus europaeus L. Lamiaceae 1 1 1 1 Lysimachia tenella Primulaceae 1 Lythrum hyssopifolia L. Lythraceae 1 Lythrum junceum Banks & Sol. Lythraceae 2 1 Lythrum portula (L.) D.A. Webb Lythraceae + Lythrum salicaria L. Lythraceae 1 1 + Malcolmia ramosissima (Desf.) Thell. Caryophyllaceae 1 Mentha suaveolens Ehrh. Lamiaceae 4 Myrtus communis L. Myrtaceae 1 3 3 Nasturtium officinale R.Br. Brassicaceae 1 1 Olea europaea L. var. sylvestris (Mill.) Lehr. Oleaceae 2 Osmunda regalis L. Osmundaceae 2 + Panicum repens L. Poaceae 2 Paspalum distichum L. Poaceae 2 Persicaria hydropiper (L.) Spach Polygonaceae 3 Persicaria lapathifolia (L.) Gray Polygonaceae 2 2 Phragmites australis (Cav.) Trin. ex Steud. Poaceae 2 Pistacia lentiscus L. Anacardiaceae 2 2 Polypodium cambricum L. Polypodiaceae 1 Potamogeton nodosus Poir. Potamogetonaceae 1 1 Potamogeton polygonifolius Pourr. Potamogetonaceae 1 Potentilla reptans L. Rosaceae 1-2 1 Prunus avium L. Rosaceae 2 + 1 Pteridium aquilinum (L.) Kuhn Dennstaedtiaceae 1 1 2 2 2 1 2 Ranunculus flammula L. Ranunculaceae 1-2 Ranunculus macrophyllus Desf. Ranunculaceae 2 2 Ranunculus sardous Crantz. Ranunculaceae 1 Ranunculus sceleratus L. Ranunculaceae + Rosa sempervirens L. Rosaceae 2 Rorippa amphibia (L .) Besser Brassicaceae 1-2 Rhynchospora modesti-lucennoi Castrov. Cyperaceae 2 Rubia peregrina L. Rubiaceae 1-2 + 1 Rubus ulmifolius Schott. Rosaceae 4 4 3 1 2 2 2 Rumex conglomeratus Murray Polygonaceae 1 1 Salix pedicellata Desf. Salicaceae 2 2 2 2 3 2 Sambucus ebulus L. Adoxaceae + 3 1 Schoenus nigricans L. Cyperaceae 2 Scrophularia sambucifolia L. Scrophulariaceae 1 Smilax aspera L. Smilacaceae 1 2 1 Solanum dulcamara L. Solanaceae 1 1 + Solanum nigrum L. Solanaceae 2 Sonchus asper (L.) Hill. Asteraceae 1 Sparganium erectum L. Typhaceae 3 2 Spergula arvensis L. Caryophyllaceae 1 Succisa pratensis Moench. Caprifoliaceae 3 Tamus communis L. Dioscoreaceae 1-2 1 Thelypteris palustris Schott. Thelypteridaceae 2 Torilis arvensis (Huds.) Link Apiaceae 1 Trifolium repens L. Fabaceae 1 Typha domingensis (Pers.) Poir. ex Steud. Typhaceae 2 Urtica urens L. Urticaceae 1 1 Veronica agrestis L. Plantaginaceae + Vitis vinifera L. subsp. sylvestris (C.C.Gmel.) Berger & Hegi Vitaceae 1 1 Wolffia arrhiza (L.) Horkel ex Wimm. Araceae 3

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