Plant community patterns in Moroccan temporary ponds along latitudinal and anthropogenic disturbance gradients

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Plant Ecology & Diversity

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Plant community patterns in Moroccan temporary ponds along latitudinal and anthropogenic

disturbance gradients

Mohammed El Madihi, Laila Rhazi, Maarten Van den Broeck, Mouhssine Rhazi, Aline Waterkeyn, Saber Er-riyahi, Bouahim Siham, Moustapha Arahou, Abdelmajid Zouahri, Anis Guelmami, Serge D. Muller, Luc Brendonck & Patrick Grillas

To cite this article: Mohammed El Madihi, Laila Rhazi, Maarten Van den Broeck, Mouhssine Rhazi, Aline Waterkeyn, Saber Er-riyahi, Bouahim Siham, Moustapha Arahou, Abdelmajid Zouahri, Anis Guelmami, Serge D. Muller, Luc Brendonck & Patrick Grillas (2017): Plant community patterns in Moroccan temporary ponds along latitudinal and anthropogenic disturbance gradients, Plant Ecology & Diversity, DOI: 10.1080/17550874.2017.1346716

To link to this article: http://dx.doi.org/10.1080/17550874.2017.1346716

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Publisher: Taylor & Francis & Botanical Society of Scotland and Taylor & Francis Journal: Plant Ecology & Diversity

DOI: 10.1080/17550874.2017.1346716

Plant community patterns in Moroccan temporary ponds along latitudinal and anthropogenic disturbance gradients

Mohammed El Madihi

, Laila Rhazi

, Maarten Van den Broeck

, Mouhssine Rhazi

, Aline Waterkeyn

, Er-riyahi Saber

, Siham Bouahim

, Moustapha Arahou

, Abdelmajid Zouahri

, Anis Guelmami

, Serge D. Muller

, Luc Brendonck

and Patrick Grillas

a

Laboratory of Botany, Mycology and Environment, Faculty of Sciences, University Mohammed V in Rabat, Morocco;

Laboratory of Aquatic Ecology and Evolutionary Biology, Katholieke Universiteit Leuven, Belgium;

Moulay Ismail University, Faculty of Sciences and Techniques, Department of Biology, Errachidia, Morocco;

Moulay Ismail University, Faculty of Letters and Human Sciences, Department of Geography, Meknes, Morocco;

Agronomic National Research Institute (INRA), CRRA of Rabat, Morocco;

Université de Montpellier2 - CNRS, Institut des Sciences de l’Evolution, Montpellier, France;

Tour du Valat Research Institute for Mediterranean Wetlands, Arles, France.

* Corresponding author: Patrick Grillas

Email: [email protected]

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Abstract

Background: Temporary ponds, an abundant habitat in the Maghreb region and notably in Morocco, have a high conservation value. However, they are mainly known from the North of the country.

Aims: The aim of this work was to characterise the vegetation of Moroccan temporary ponds along a combined gradient of latitude and anthropogenic pressure.

Methods: Eighty-five ponds distributed along a north – south gradient of 750 km were sampled. For each pond, all vegetation was surveyed (flooded and dry parts) and the local abiotic characteristics were measured during two successive hydrological cycles. The prevailing anthropogenic pressures were also identified and were attributed an impact score.

Results: Eighty-one characteristic pond species (including 17 rare species) were recorded, with several new distribution data in the southern part of the latitudinal gradient. Plant communities were related to climatic and anthropogenic factors, but mostly to local factors, such as maximum water depth and soil pH. The northern ponds (wettest macroclimate) were rich in characteristic species and rare species, while the southern (driest macroclimate) ponds were more species poor.

Conclusions: In addition to the direct impact of increasing human activity, a further reduction of the floristic richness of temporary ponds is expected due to climatic changes.

This is particularly the case for characteristic species which have a high conservation value.

Keywords: anthropogenic pressures, climate change, conservation, North Africa, rare

species, wetlands

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Introduction

Temporary ponds provide important ecosystem services, such as flood control, groundwater recharge, toxic pollutant retention and nutrient recycling (Keddy 2000; Williams 2006). In addition to these regulating services, they also have an important societal value because of their provisioning and cultural services (e.g. cattle grazing, water storage, medicinal plant harvesting, recreation). They are also remarkable habitats with a unique flora and fauna, contributing to regional biodiversity (Biggs et al. 2005; Oertli et al. 2008). They are recognised by the Ramsar Convention on Wetlands (Ramsar Resolution VIII.33) and Mediterranean temporary ponds are listed as priority habitats under the Habitats Directive of the European Community (Natura 2000 code: 3170* – Mediterranean temporary ponds) (Ruiz 2008). They harbour a great diversity of flora and fauna including many threatened species (e.g. Grillas et al. 2004).

Temporary ponds are defined as small and shallow wetlands, characterised by an alternation of dry and wet phases (Grillas et al. 2004). Hydroperiod duration and pond depth are the main environmental factors that control the establishment and development of plant species in temporary ponds (e.g. Keeley and Zedler 1996; Spencer and Blaustein 2001; Grillas et al. 2004). Temporary ponds are among the most threatened freshwater habitats, due to anthropogenic activities (Deil 2005; Javornik and Collinge 2016) and climatic changes (Rossetet al. 2010; Ewald et al. 2013). Due to their small size and low depth, these habitats are easily destroyed or degraded by human activities, such as urbanisation, agriculture and pollution (Biggs et al. 2005; Van den Broeck et al. 2015). Furthermore, climate change is expected to strongly impact these small freshwater systems (Pyke 2005; Rosset et al. 2010), since altered precipitation and evapotranspiration patterns (GIEC 2014; TCMCC 2016) will increasing the duration of the dry period (Bauder 2005; Döll and Zhang 2010) and thereby impact their hydrological functioning. However, very few papers address the impact of climate change on temporary and ephemeral freshwater ecosystems (Brooks 2009; Lowe et al. 2015).

The species richness, community composition and distribution of the vegetation of temporary ponds are related to complex interactions between various natural (Holland et al.

1995; Semlitsch and Bodie 1998), and anthropogenic factors (Deil 2005; Bouahim et al.

2014). Understanding the respective effects of these factors is essential, on the one hand for explaining biodiversity patterns, and on the other hand for developing strategies for conservation and sustainable use of these habitats (Declerck et al. 2006; Mikulyuk et al.

2011).

Hydrology and soil variables are usually the most important local factors for plant community composition and richness in temporary ponds (Keeley and Zedler 1998; Grillas et al. 2004; Deil 2005; Rocarpin et al. 2016). Pond characteristic plants are well adapted to the alternation of wet and dry phases and changes in flooding height and hydroperiod (i.e.

duration of flooding) (Zedler 1987; Casanova and Brock 2000; Rocarpin et al. 2016). The

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physicochemical characteristics of the soil (e.g. pH, particle size, nutrient levels) also play an important role in determining temporary-pond species distributions (Keeley and Zedler 1998; Ferchichi-Ben Jamaa et al. 2010).

Anthropogenic factors directly impact pond vegetation through physical soil disturbance (e.g. trampling, ploughing) and indirectly through changes in their functional characteristics (eutrophication, hydrology) (Bouahim et al. 2014). Any long-term change in hydrological parameters will result in significant modification in the species composition and structure of the vegetation. Eutrophication in temporary ponds can affect the species composition by enhancing some functional groups of plants, such as floating vascular plants and algae (Scheffer et al. 1997; Leibold 1999), or by facilitating the development of exotic invasive species (Gerhardt and Collinge 2003).

Climate plays a key role in ecological processes and determines the structure, functioning and biodiversity of temporary wetland ecosystems (Pyke 2005; Brendonck et al. 2014;

Kneitel 2016). Climate impacts are either direct (e.g. temperature, precipitation and drought) or indirect and act through interactions with non-climatic factors (e.g.

anthropogenic or local site variables) (Changhao 2009). Climatic variables (precipitation, temperature...) directly or indirectly affect the hydrological functioning of which the depth of water (Grillas et al. 2004; Kneitel 2016; Stoch et al. 2016) or flooding date (Bliss and Zedler 1997; Grillas and Battedou 1998; Jeffries 2016) have strong influence on plant dynamics.

Therefore, climatic variables influence plant (Lumbreras et al. 2012; Javornik and Collinge 2016) and animal communities (branchiopod crustaceans: Stoch et al. 2016). The diversity of communities varies along latitudinal gradients usually showing a decline of diversity towards higher latitudes (e.g. Rodríguez and Arita 2004; Kraft et al. 2011). However, diverse patterns have been found among ecosystems (Kneitel 2016) and in temporary ponds the reverse pattern found is best explained by climate-related local site factors (hydroperiod stability) (Brendonck et al. 2014; Kneitel 2016).

In the Mediterranean region, Important Pond Areas have been identified (Ewald et al. 2010) and Mediterranean temporary ponds are particularly abundant and preserved in North – Africa (Grillas et al. 2004; de Bélair 2005; Ferchichi-Ben Jamaa et al. 2010) notably in Morocco, throughout the Atlantic plains, the eastern highlands, steppe zones and mountainous areas (Thiéry 1987; Rhazi et al. 2012).These ponds present unique and diverse floral and faunal communities (Grillas et al. 2004)including numerous threatened species listed in the IUCN Red List for North-Africa (Garcia et al. 2010).In Morocco and more generally in North-Africa temporary ponds are increasingly degraded due to population growth and economic development (Rhazi et al. 2012; Van den Broeck et al. 2015). The remaining habitats are often overexploited, which is incompatible with pond conservation (Bouahim et al. 2014).

In Morocco, studies of plant community distribution and composition are mainly

concentrated in the region of Benslimane and Rabat (e.g. Rhazi et al. 2001, 2006, 2012;

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Bouahim et al. 2010; 2014; Lumbreras et al. 2012), with significant gaps in the north and south (where no previous study of pond vegetation could be found).

The objective of this study was to understand the change in the species composition and conservation value of the ponds with latitude in North-Africa (Morocco) hypothesising that the present latitudinal gradient can be used as a proxy of future climate change. In this perspective the following hypotheses were tested: (1) The species richness of the pond decrease with latitude (in the range tested) because of increasing drought stress; (2) Hydrology is the main environmental factor that explain the species richness and species composition of the vegetation of the ponds and (3) The total species richness and the number and abundance of pond characteristic species increases with latitude, (4) conversely, the number of opportunistic terrestrial species declines with latitude.

Material and methods Study areas

In Morocco, most temporary ponds are found in the Atlantic coastal area from Tangier to Agadir, compared to the southern regions and high elevations (Thiéry 1987). A total of 85 temporary ponds were selected from six regions of Morocco (Tangier, Mamora, Benslimane, Chaouia, Jbilets and Essaouira), located between 31° and 35° N (spanning about 750 km) (Figures 1 and 2). Each region corresponds to an Important Pond Area (Ewald et al. 2010) and they were selected in order to cover a wide range of latitude and climate, geological substratum, land-use and anthropogenic pressure. The main characteristics of these regions are shown in Table 1. In each region, ponds were selected to cover the local range of pond size and land-use. The main characteristics of these regions (Table 1) are:

Tangier. In the Atlantic plain located at the northern tip of Morocco five ponds (Table S1) were sampled (Figure 1). Three of them were located in cork oak forest (Quercus suber) on sandstone substratum and two in Aleppo pine (Pinus halepensis) reforestation site on marl substratum. All ponds were grazed and three of them used for recreation and harvesting of medicinal plants (Tables 1 and S1).

Mamora. A total of 18 ponds (Tables 1 and S1) were selected in Quercus suber forest, just north of Rabat. The substratum was homogeneous (Pliocene/Quaternary sand deposit on clay bedding) and anthropogenic pressure varied (Table 1). All ponds were grazed and 10 were used for recreation and three for domestic activities (clothes washing) and submitted to sediment extraction.

Benslimane. This lowland area between the two major cities Rabat and Casablanca is, characterised by a high density of ponds, occupying 2% of the land area (Rhazi et al. 2012).

Forty ponds (Table 1 and Table S1) were sampled on homogeneous geological substratum (quartzitic sandstone): 10 in a hunting reserve without other significant anthropogenic uses;

12 in public Q. suber forest were the anthropogenic uses are moderate (grazing, recreation,

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harvesting of medicinal plants); 18 in agricultural areas with high anthropogenic pressure (crop cultivation, draining through various methods, landfilling and urbanisation).

Chaouia. This vast plain south of Casablanca where predominate fertile agricultural lands on vertisol includes a high density of ponds. Ten ponds (Tables 1 and S1) were sampled in this region. All ponds were grazed, six of them were used for harvesting medicinal plants, and four were partly drained of filled-in including one partly cultivated and another one partly urbanised.

Jbilets. In this area made of small hills north-west of Marrakech (Figure 1) eight ponds were sampled (Tables 1 and S1), located in a dry grassland with sparse Jujube tree (Ziziphus lotus) on sandstone -shale substratum. All ponds were grazed and two of them were partly cultivated.

Essaouira. This Atlantic plain located at the north of Agadir the most southern region sampled (Figure 1) is, characterised by frequent Atlantic wind. The six sampled ponds (Tables 1 and S1) were located in the Argan (Argania spinosa) forest on sandy soil on limestone and marl substratum. All ponds were grazed and two of them had been excavated for sand extraction.

Vegetation study

Each pond was visited twice during two consecutive years (winter and spring of 2013-2014 and 2014-2015). During each visit, a phytosociological survey (Braun-Blanquet 1932; Kent and Coker 1992) was conducted on homogeneous plots of 81 m² using the Braun-Blanquet scale (six classes: from + to 5). The species composition of the vegetation varies strongly within each pond along the hydrological gradient (Wilson and Keddy 1985) and two or three vegetation belts are usually recognised (Rhazi et al. 2001). Two plots were surveyed per pond, randomly located respectively in the centre and in the marginal belt. Data from the two annual recording were aggregated by taking the maximum abundance of each species during the two visits and in the two quadrats. Plants were identified according to flora of Morocco (Fennane et al. 1999, 2007, 2014).

Contrasting with ponds in temperate regions (e.g. Nicolet et al. 2004; Rosset et al. 2014),

temporary ponds experiencing a short flooded period such as those found in Morocco,

harbour large numbers of opportunistic species from neighbouring habitats (crops, forests)

that colonise during the dry seasons and increase their abundance during dry years (Rhazi et

al. 2001; 2009). These opportunistic species show large inter-annual variations and tend to

decline or disappear during wet years (Rhazi et al. 2009). Instead of separating species by

life-forms as often done in aquatic vegetation study, they were separated by their main

phytosociological classes (Rivas-Martínez et al. 2002; Bagella and Caria 2012). The vegetation

of each pond was thus characterised by the cumulative species richness of two main groups

of species: characteristic pond species and terrestrial species. Pond species were defined as

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Isoëto-Nanojuncetea; Isoeto-Littorelletea including also species from Phragmito- Magnocaricetea; Molinio-Arrhenatheretea; Charetea fragilis; Potametea; Lemnetea which can be present as well during temporal succession (Rivas-Martínez et al. 2002; Bagella et al.

2007; Pinto-Cruz et al. 2009).Terrestrial species are defined as opportunistic plants, commonly found in the forested and agricultural areas surrounding the ponds (Fennane et al. 1999, 2007, 2014) and which penetrate into the ponds during the dry phase. These terrestrial species are associated with phytosociological classes Helianthemetea guttate (often associated with temporary ponds but considered here as belonging to drier habitats);

Stellarietea mediae; Saginetea maritimae; Poetea bulbosae; and Polygono-Poetea annuae (Rivas-Martínez et al. 2002).

Rare species constitute a subgroup of characteristic pond species that are of conservation interest in Morocco (Fennane and Ibn Tattou 1998) (no species of conservation interest was found among the terrestrial species group). Rare species were defined by at least one of the following criteria: present in fewer than five localities or known from only one or two floristic regions of Morocco (Jahandiez and Maire 1931–1934) or a decline in their populations has been demonstrated (Fennane and Ibn Tattou 1998). The annual or perennial character was determined according to Fennane et al. (1999, 2007, 2014).

Hydrological and soil factors

For each of the 85 ponds, maximum water depth (when inundated) was measured during each vegetation survey (winter and spring during two consecutive years). Flooded area was mapped using a handheld GPS (Garmin etrex® 20) in the field. In the context of this study, the maximum depth and the surface area of water provide a rough but representative estimate of the hydrological regime of the ponds over 700 km of latitude (Bauder 2000;

Rhazi et al. 2001; Van den Broeck 2016). More detailed hydrological data were not possible to obtain considering the extent of the study area and the impossibility to fit recording devices in the ponds. For the same reasons water chemistry could not be studied (preservation and transportation of samples). However, soil chemistry brings information on the nutrient status of the ponds allowing useful among-site comparisons (Rhazi et al. 2001).

Soil chemistry is more stable between seasons than water chemistry and thus more relevant for broad scale comparisons. Two sediment samples (top 10 cm) were taken with a corer (diameter: 4cm) at the end of the flooding period respectively at the centre and the periphery of each pond, immediately next to the vegetation survey plots, and pooled to determine several soil parameters. Particle size was assessed using the "Bouyoucos" method (Black et al. 1985). The pH of the sediment was measured using a pH meter in a suspension of fine soil with a soil/distilled water ratio of 1:2.5. The salinity of the sediment was measured as electrical conductivity (conductivity meter Philipps PR 9801) of a soil/double- distilled water solution with a ratio of 1:5, after stirring for 1 h (150 rev/min) (Black et al.

1985). Standard protocols were followed for the measurement of organic carbon, types of

phosphorus (Olsen) and total nitrogen (Kjeldahl) (Page et al. 1984).

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Climatic and geographic factors

Monthly precipitation and mean, minimum, and maximum temperature for the 1950–2000 period in Northern Morocco were extracted from 165 meteorological stations in the WorldClim database at a spatial resolution of 30 arcs (Figure 3A).Global precipitation and temperature maps (Figure 3B) were produced using ANUSPLIN software package as an interpolation method (Hijmans et al. 2005).

Finally, using the geographic coordinates recorded in the field by a handheld GPS, it was possible then to extract all values of these climatic variables from the global models for different points corresponding to each of the selected ponds.

Anthropogenic factors

For each pond, different anthropogenic uses around the habitats were identified during field visits and interviews with local people. Anthropogenic uses were classified into nine categories: grazing (which includes both grazing by domestic herbivores and impact of wild boar (Sus scrofa), burrowing for feeding on bulbs and corms), harvesting of medicinal plants, activities that cause drying (e.g. water pumping, drainage, planting Eucalyptus), recreation, extraction of sediment or rock (quarry), domestic activities (e.g. washing clothes), crop cultivation, landfilling and urbanisation. These categories were combined in an anthropogenic pressure index (API), to quantify the degree to which each pond is likely to be affected by human impact, according to Bouahim et al. 2014 (see Appendix).

Data analysis

Multivariate analyses were carried out using R (2.15.1), univariate analyses with STATISTICA 10 (StatSoft Inc., TulsaOK, USA). The ‘Species’ matrix contained the maximum abundance (six classes; 1: cover < 5%; 2: 5 -25%; 3: 25-50%; 4: 50-75%; 5: >75%) of each species in each pond (85) and the ‘Pond’ matrix contained for each pond the variables for the environmental factors (hydrology, soil, climate, geography and anthropogenic pressure).

The respective influence of hydrological and soil factors, climatic and geographic factors (precipitation, mean temperature, latitude and elevation) and those of anthropogenic activities (anthropogenic pressure index) on the vegetation composition of the 85 ponds was studied using multivariate analysis made on the cover-abundance values of species. These analyses were made separately for the terrestrial and pond species in order to test the unique and common variation of the environmental variables on the two groups of species.

We opted for redundancy analyses (RDA), rather than canonical correspondence analysis (CCA), because of the dominance of linear gradients. Firstly, RDA-based forward-selection procedures were used to determine significant explanatory variables within each of the three categories (local, climatic or anthropogenic) both for pond and terrestrial species.

Subsequently, retaining only the significant explanatory variables, RDA-based variation

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partitioning was used to compare the contribution of each category of variables alone or together with other variables (Borcard et al. 1992). The statistical significance of all analyses was assessed by Monte Carlo permutation tests (n = 999). To visualise the relations between the explanatory variables and community composition, Principal Component Analysis (PCA) was used with the selected (i.e. significant in the RDAs with forward selection) local, climatic and anthropogenic factors plotted as supplementary variables. The ordination diagrams were made in CanoDraw 4.0. Rarely encountered species (79 species that occurred in only one or two ponds) were not taken into account in these analyses as they may have had a disproportional impact on the analyses.

Univariate Spearman correlations were carried out to assess the relationship between surface area of ponds and the species richness (total, pond, rare and terrestrial). Linear regressions were made to assess the relationship between latitude and climatic factors (precipitation, average temperature, maximum and minimum temperature).

The difference between regions in plant species richness (total, pond, rare and terrestrial species) was tested using tow-way ANOVA with random factor (vegetation types around the pond). Also, the relative contribution of annual and perennial pond species and annual and perennial terrestrial species to total richness was compared among regions by using one-way ANOVA in order to assess differences among regions in the dominance of annuals in pond vegetation (Zedler 1987; Bagella and Caria 2012). To identify the significant pair-wise differences between regions, post hoc Tukey HSD tests were used, using STATISTICA 10.

In order to explain the variations among ponds of the richness of total species, pond, rare and terrestrial species Generalized Regression Models (GRM) were calculated. Explanatory variables in the GRM were the climatic variables, the local hydrological and soil variables and the anthropogenic variables. The best model was sought by exhaustive research and selection on the Cp Mallow Cp criterion (STATISTICA

).

Results

In the 85 studied ponds, a total of 200 species were recorded (63% annual and 37%

perennial species), with 118 (59%) being terrestrial and 82 (41%) pond species, 17 of them

being rare species (8.5%). Of the rare species, 10 are listed in the IUCN Red List for North

Africa (Table 2). The most frequent pond species across regions were Isoetes velata,

Corrigiola littoralis, Juncus bufonius and Verbena supina (Table 3). Seventeen species were

restricted to a single region: Tangier region (nine species, Elatine macropoda, Romulea

ramiflora, Solenopsis laurentia, Agrostis stolonifera, Baldellia repens, Fimbristylis dichotoma,

Hypericum humifusum, Juncus conglomeratus, Ranunculus muricatus); Mamora (two,

Oldenlandia capensis, Trifolium micranthum); Benslimane (five, Elatine alsinastrum; Cicendia

filiformis; Damasonium polyspermum; Myosotis sicula; Nitella translucens); and Chaouia

(Cressa cretica) (Table 3). Five characteristic pond species were found for the first time in

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geographical areas where they had not been previously reported (Table 3). The distribution of Pilularia minuta and Isoetes setacea, previously known only to the Benslimane region, were extended northward and southward; Verbena supina and Marsilea strigosa were encountered for the first time in southern areas and Elatine macropoda had not previously been known in northern Morocco (Table 3).

Factors structuring plant communities

Some of the explanatory variables used in the analyses were significantly correlated.

Latitude was positively highly correlated with precipitation (R²= 0.97; P<0.0001), maximum water depth (R²= 0.50; P<0.0001), average temperature (R²= 0.40; P<0.0001) and negatively correlated with maximum temperature (R²= -0.24; P= 0.0247). No significant correlation was found between latitude and minimum temperature (R²= 0.07; P> 0.05) and between latitude and the surface area of ponds (R²= -0.06; P>0.05).

Characteristic wetland communities with pond species. Maximum water depth, soil pH and the sand and silt content of soil were identified as the local factors most closely related to the distribution of wetland communities. The most important climatic and geographical factors were precipitation, average temperature and latitude. The Anthropogenic Pressure Index (API) was also significantly related on species composition. These factors together explained 31.7% of total variance in community structure (F= 4.26; P= 0.001).

Variance partitioning (Figure 4A) showed that local and climate factors explained the largest part of community structure variation (6.1%; F= 3.72; P= 0.001 and 5.91%; F= 3.07 P= 0.001, respectively). API explained a small part of the variation (1.8%; F= 1.73; P= 0.029). Most of the explained common variation was shared between natural local and climatic factors (11.0%) (Figure 4A). On the PCA graph (Figure 4B), a group of species is positively correlated with precipitation, the maximum water depth and latitude and negatively with soil pH and API. (e.g. Ranunculus baudotii, Glyceria fluitans,Ranunculus ophioglossifolius, Isoetes velata, Eleocharis palustris, Exaculum pusillum, Callitriche lusitanica, Mentha pulegium, Juncus heterophyllus, Illecebrum verticillatum, Juncus pygmaeus, Baldellia ranunculoides, Lythrum hyssopifolia).These species are dominant or exclusive to the deepest ponds located at the highest latitudes, which receive the largest amounts of precipitation and are subject to low anthropogenic pressure. A second group was composed of post-inundation species (e.g.

Eryngium atlanticum, Cressa cretica, Verbena supina, Lythrum tribracteatum, Coronopus squamatus, Damasonium bourgaei) which are positively correlated with anthropogenic activities and high soil pH. These species were mainly dominant in the most southerly ponds, which receive less rain and dry out rapidly (short hydroperiod). A third group of species (e.g.

Elatine brochonii, Oldenlandia capensis, Isoetes histrix) was positively correlated with high

sand content in soil. These species were dominant or exclusive to the Mamora cork oak

forest and Essaouira Argan forest ponds that are on a loose sandy substrate (Figure 4B).

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Terrestrial species communities. Natural local variables selected by forward selection were the maximum depth of the water, soil pH, the sand and silt content. Significant climatic and geographical factors were precipitation, average temperature and latitude. API also had a significant effect on the structure of communities. Together, these factors explained 26.3%

of total variation in the structure of terrestrial communities (F= 3.17; P= 0.0010). The variance partitioning (Figure 4C) showed that natural local factors explained the largest part in community structure variation (4.9%; 4 F= 4.22; P= 0.001), followed by climatic and geographical factors (4.3%; F= 3.26; P= 0.001). The effect of the API was not significant (1.3%; F= 1.35; P= 0.07). The largest part of the explained common variation was shared between natural local and climatic factors (7.6%) (Figure 4C). The PCA graph (Figure 4D) contrasts two groups of species on axis 1. A first group consists of species positively correlated with maximum water depth, precipitation and latitude but are negatively correlated with the soil pH, the silt content, API and average temperature (e.g. Logfia gallica, Trifolium resupinatum, Leotodon saxatilis, Narcissus viridiflorus, Prospero autumnalis, Bellis annua, Euphorbia exigua). These species are dominant or exclusive to the deepest ponds in the north, which receive largest amounts of rainfall and are subject to low anthropogenic pressure. A second group consists of a great number of species(e.g. Asphodelus fistulosus, Lobularia maritima, Brachypodium distachyum, Ononis natrix, Medicago laciniata, Moraea sisyrinchium, Raphanus raphanistrum, Polygonum aviculare, Cynara humilis, Paronychia argentea) favoured by high temperatures, anthropogenic pressures and silty soils with high pH values and are negatively related with precipitation. These species are dominant or exclusive to ponds in the south where precipitation amounts are lowest and the average temperatures are highest (resulting in short hydroperiods). A third group consists of species positively correlated with soil sand content (e.g. Malcolmia patula, Tuberaria guttata, Ornithopus pinnatus, Crassula muscosa). These species are dominant or exclusive to forest ponds on sandy substrate (Cork oak forest of Mamora and Essaouira Argan forest) (Figure 4D).

Species richness

Total species richness differed significantly between regions (F= 19.90; df= 5; P<0.001) and increased with latitude (Figure 5) without a significant effect of the vegetation types around the ponds (P> 0.05). In the north (Tangier, Mamora, Benslimane), ponds contain on average 34 to 46 species but only 17 per pond in the south (Figure 5).

The richness of pond characteristic species differed significantly between the six studied

regions (F= 38.37; df= 5; P<0.001) and increased with latitude (Figure 5) without a significant

effect of the vegetation types around the ponds (P> 0.05). It was significantly higher in the

northern regions (Tangier, Benslimane, Mamora) containing 15-26 species per pond but

lower in the southern regions ponds (Jbilets, Essaouira) where it reached only three to six

species per pond (Figure 5). The relative proportion of annual and perennial pond

characteristic species decreased significantly from north to south (F= 21.87; df= 5; P<0.0001;

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F= 30.99; df= 5; P<0.001, respectively) (Figure 6). In each region, the proportion of annual pond characteristic was higher than that of perennial pond characteristic, except the Tangier region.

A significant difference between regions (F = 6.39; df = 5; P<0.001) was also found for the richness of rare species (Figure 5). In the north (Tangier, Mamora, Benslimane) ponds contain on average 2 to 3 rare species but only 0.3 per pond in south (Figure 5). Most rare species (17) are found in ponds with latitudes between 35° and 33° N, where precipitation exceeds 400 mm/year (Figure 7A and 7B). Very few rare species (Isoetes setacea, Lythrum thymifolia, Pilularia minuta and Isoetes velata) are located in low latitudinal ponds between 31° and 32° N, where precipitation is low (200 to 300 mm/year) (Figure 7A and 7B).

Terrestrial species richness was significantly different between regions (F= 2.99; df= 5; p=

0.0157) (Figure 5) without a significant effect of the vegetation types around the ponds (P>

0.05). Mamora ponds (with 19.7 species/pond) differed significantly from those of Jbilets (11 species/pond), but not from the other regions (Figure 5). The contribution of the annual terrestrial species (F= 24.45; df= 5; P< 0.001) and perennial terrestrial species (F= 24.45; P <

0.0001) in the total richness, increased significantly from North to South (Figure 6).

The best model to explain the total species richness (R²

= 0.561; F= 22.48; P <0.001) retained 5 variables, the most important being latitude that explained 18.5% of the total variation. The other variables were soil variables (Clay, N, pH, Sand and Organic matter content) that explained 20.3% of the variation (Table 4A). When latitude was excluded, the best model (R²

= 0.566; F= 16.65; P <0.001) retained 7 variables, including 2 variables related to climate (precipitation and minimum temperature) which explained 18.5% of the total variation. The other variables were soil variables (Clay, N, pH, Sand and Organic matter content) that explained 20.3% of the variation.

The best models to explain the 3 components of the species richness (pond characteristic, rare and terrestrial) did not retain latitude as explanatory variables. The best model to explain the richness of ponds characteristic species (R²

= 0.715; F= 27.36; P <0.001) held eight variables, including two climate related ones (precipitation and minimum temperature) that explained 22.2% of the total variance. The other variables were soil variables that explained 28.1% of the variance, and anthropogenic pressure which explained 15% of the variance (Table 4B).

The best model explaining the richness of rare species (R²

= 0.393; F= 10.07; P< 0.001) retained 6 variables including only one climate related (minimum temperature) which explained only 2.6% of the total variance. Soil variables explained 22.6% of variation and anthropogenic pressure 1.8% (Table 4C).

The best model explaining terrestrial species richness (R²

= 0.235; F= 5.29; P< 0.001)

retained 6 variables including only one climate related (precipitation) which explained 9.2%

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of the variation. The other variables were soil variables (13.4%), anthropogenic pressure (6.9%), the maximum depth (2.8%) and pond surface (2.1%) (Table 4D).

Discussion

Plant community structure

The plant communities of the studied temporary ponds were structured by local (maximum depth of the water, soil pH, sand content, silt content) as well as climatic (precipitation, mean temperature, latitude) and anthropogenic factors (API).

The plant communities showed large variation along the regions and latitudinal gradient (Figure5) with, as hypothesized, a significantly lower proportion of characteristic pond species in southern than in northern ponds (Figure 6). However, the strong correlation between latitude and climatic factors (Figure 4) make it difficult to separate their respective importance (Willig et al. 2003). The total species richness and the richness of characteristic pond and rare species as well as the richness in terrestrial species decreased from north (wettest) to the south (driest) parallel to the decrease in precipitation (Figure 5). Literature show contrasting latitudinal-diversity patterns (reviewed in Kneitel 2016), usually showing a decrease of diversity towards higher latitude (e.g. Rodríguez and Arita 2004 for mammals in North-America, Kraft et al. 2011 for forests) but also no correlation (Clarke and Lidgard 2000 for Bryozoan in the Atlantic, Soininen et al. 2007 across diverse ecosystems and organisms groups) or reverse correlation (Buckley et al. 2003 for food-webs in water-filledleaves of Sarracenia purpurea in North-America, Brendonck et al. 2014 for invertebrate communities in rock-pools in Australia). The relationship between latitude and diversity differs from the general pattern in freshwater ecosystems (Hillebrand 2004; Hof et al. 2008). Although focused on invertebrates, the only two studies on temporary pools showed the same reverse pattern of species richness as in Australia (Brendonck et al. 2014) and in California (Kneitel 2016). This reverse richness pattern along latitudinal gradient has been explained by local factors, i.e. hydrological instability increasing at lower latitude (Brendonck et al. 2014) and habitat size (Kneitel 2016). In our study hydrology is the main factor explaining the diversity pattern as highlighted by the strongest relationships with climatic and latitude variables of the pond species rather than the terrestrial species (Table 4). In contrast to our hypothesis, the number of opportunistic terrestrial species per pond showed a weak declining trend towards lower latitude (lower precipitation). The higher aridity in the south is limiting the species richness of all groups including terrestrial species. However, because the reduction of opportunistic terrestrial species was small compared to that of pond species, the contribution of annual terrestrial species was significantly higher in southern regions.

Local factors appear to be most important for structuring the communities, as has also been

shown in other studies in Mediterranean temporary ponds on plants (Lathrop 1976; Bauder

2000; Bouahim et al. 2014) and macro-invertebrates (Waterkeyn et al. 2008; Brendonck et

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al. 2014; Stoch et al. 2016; Van den Broeck 2016). Local and climatic factors are closely involved in the hydrological functioning of wetlands and are partially correlated with each other (Figure 4). The maximum water depth which is correlated to flood duration in ponds in Morocco (Van den Broeck et al. 2016) is the main local variable structuring plant communities. It acts as an environmental filter (Javornik and Collinge 2016), reducing or eliminating the terrestrial species and favouring the recruitment of characteristic pond species (aquatic/amphibious) (Middleton 1999; Bauder 2000). Indeed, hydrology has been largely identified as the key factor determining plant communities of temporary ponds (Bauder 2000; Casanova and Brock 2000). The germination of species depends of their tolerance to water stress and desiccation (Keeley and Zedler 1998; Collinge et al. 2003).

Amphibious species (e.g. Elatine brochonii, Corrigiola littoralis, Lythrum spp.), tolerant to a narrow range of hydrological conditions, are characteristic of Mediterranean temporary ponds; they establish in flooded conditions during the drawdown and complete their cycle (flowering, production of seeds) during the dry phase (on wet sediment).

The other important local variables are soil pH and the contents of sand and silt. These variables were previously found discriminating for Mediterranean temporary pond vegetation (Rhazi et al. 2001; Ferchichi-Ben Jamaa et al. 2010; Bouahim et al. 2014). These variables, highly correlated with the geological nature of the underlying rock, reflect different trophic states of the environment and thus different potential for agriculture. We used soil chemistry instead of water chemistry variables because the former allowed the identification of trophic and non-trophic variables (e.g. pH, grain size) which play an important role for plant species and which vary much less than water chemistry on a daily and seasonal basis. Furthermore, the soil samples are less sensitive to storage conditions than water samples; it was an important criterion in our project. Soil pH is an important variable for temporary pool vegetation, separating sites with low concentrations of soluble ions (often named oligotrophic although bringing confusion with nutrient status) from those with high concentrations of soluble ions and rich in calcium (e.g. Braun-Blanquet 1936;

Directive habitat 1992; Rhazi et al. 2001). In our study ponds on fine-textured soils are

associated with a high API (Figure 4). These soils are relatively nutrient-rich and thus are

suitable for agriculture. Agricultural practices impact communities through physical (soil

disturbance by agriculture) and chemical disturbance (eutrophication by nutrient supply) of

the habitat. Only disturbance- and eutrophication-tolerant species are able to grow on these

soils (e.g. Damasonium bourgaei, Lythrum tribracteatum, Lemna minor). In contrast, coarse

sandy soils are oligotrophic, i.e. have a low retention capacity for water and nutrients. These

sandy soils, characterising the forest regions of Mamora and Essaouira, are the most

favourable for a group of oligotrophic pond characteristic species (e.g. Elatine brochonii,

Oldenlandia capensis, Isoetes histrix, Corrigiola littoralis) (Figure 4). Contrasting with

European ponds were eutrophication prevails (Menetrey et al. 2005; Rosset et al. 2014),

ponds in Morocco are usually poor in nutrients and organic matter resulting from the short

flood period limit primary production and from less nutrients used by farmers in the ponds

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European ponds, the short flood period and the early drought favour amphibious and terrestrial growth forms, limiting the effects of water eutrophication on water transparency.

The effect of anthropogenic pressure on community composition remains relatively limited compared to other factors and notably climatic factors. However, the high level of correlation between the studied factors probably partly masked the true anthropogenic impact. Furthermore, the aggregation into a single index of the different pressures could also have masked some important anthropogenic pressures. However, the shared variation found between anthropogenic and site factors highlights an indirect effect of anthropogenic pressures on plant communities of ponds through the modification of the physical (e.g.

water depth and hence hydroperiod) and chemical (soil quality) characteristics of the ponds.

This is especially the case for pond characteristic species because of their sensitivity to disturbance (Sahib et al. 2009). The anthropogenic impact may be more pronounced in dry years in the densely populated plains. Few characteristic pond species can withstand higher levels of human pressure (Cressa cretica, Frankenia laevis, Eryngium atlanticum, Damasonium bourgaei, Lythrum tribracteatum), probably because they are tolerant to nutrient rich soils and develop when water recedes, i.e. being less exposed to flood conditions.

Our species inventories resulted for some species in a significant extension of their known distribution to the North (Elatine macropoda, Pilularia minuta, Isoetes setacea) or to the South of Morocco (Verbena supina, Marsilea strigosa, Pilularia minuta, Isoetes setacea).

Indeed, beyond Benslimane and Rabat regions where the ponds have been previously studied (Rhazi et al. 2001, 2006, 2012; Bouahim et al. 2010, 2014; Lumbreras et al. 2012), the vegetation of the ponds in Morocco is poorly known. The extension of the area of occurrence of the species could ultimately result in change in their conservation status at the country and Mediterranean levels according to IUCN Red list criteria. Among the pond characteristic species, 21% were found only in one region. These are usually species at the edge of their distribution (e.g. Baldellia repens a species with a Western European distribution or Mariscus hamulosus, a species with a tropical distribution) (Fennane and Ibn Tattou 1998) or Mediterranean species with a narrow distribution (e.g. Damasonium polyspermum, Elatine macropoda, Trifolium micranthum). Some of the latter species were however also found in ponds in mountains (Rif and Middle-Atlas, unpublished results).

Conclusions

What the future may hold for plant communities in temporary ponds? In the context of

climate change major modifications are expected in the species composition and the

conservation value of plant communities in temporary ponds in the Mediterranean basin

and especially in its driest parts in North-Africa. Key factors determining their diversity and

community structure are maximum water depth and the flooding and drying dates. These

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variables depend mainly on winter and spring rains that are likely to decrease with the expected climatic changes in Morocco (rainfall decrease of 10 to 20% and temperature rise of 1 to 1.5°C by 2100) (TCMCC 2016). Thus, the present situation of temporary ponds in the southern region could illustrate the situation of ponds in the northern regions after significant climate change, notably the decrease of the contribution of pond characteristic species in the communities. Amphibious species with a narrow range of tolerance to hydrological conditions (e.g. Elatine brochonii, Oldenlandia capensis, Isoetes histrix, Corrigiola littoralis) could be used as a sensitive indicator of climate change on a large scale.

The richness of rare species is strongly correlated with the number of characteristic species of ponds. Most rare species concentrate in the ponds of high and middle latitudes (36-33°

N). Only a few species (Pilularia minuta, Isoetes setacea, Isoetes velata, Lythrum thymifolia) are found in regions with latitudes of 31°-32°N where precipitation is low and irregular. This large latitudinal distribution of these species is generally linked to their ability to germinate in temporarily saturated soil and to develop further on a more or less dry soil. Some of them produce resistant forms with a very long viability as an adaptation to irregular flooding (Vitalis et al. 2002). This relatively flexible ecology probably allows them to quickly complete their cycle before drought affects ponds. The reduction of the hydroperiod in Moroccan southern ponds may, however, affect the frequency and abundance of sexual reproduction of annual hydrophytes and the survival of perennials. A thorough analysis of the impact of climate change on the vegetation of Mediterranean temporary ponds is necessary, particularly in the south of their distribution area. At present, anthropogenic impact on the ponds remains limited especially in the southern regions. However, with the human population increase, this impact will probably increase notably on the already water resources which will further decrease with climate change.

Acknowledgements

We thank Hayat Mesbah from the Haut Commissariat aux Eaux et Forêts et à la Lutte Contre

la Désertification (Morocco) for her logistic support (permis scientifique N° 241

HCEFLCD/DLCDPN/DPRN/CFF), Said Ameziane from the Direction Provinciale des Eaux et

Forêts de Benslimane for his technical support. We thank also the local population in the

studied region (Tanger, Mamora, Benslimane, Chaouia, Jbilets, Essaouira) for their help on

the field and all the information given about uses of temporary ponds. We thank two

anonymous reviewers and the Associate Editor (David M Wilkinson) for their remarks that

improved the quality of this manuscript. We thank also Laszlo Nagy

(Editor in Chief, Plant Ecology & Diversity) for constructive suggestions. This publication is

contribution ISE-M no. 2017- 078.

Accepted Manuscript

Funding

The work has been achieved with the financial support of a VLIR-UOS SI project [grant

number ZEIN2011Z092/2011-101] and partially by FP7-PEOPLE-IRSES [grant number 612572

MEDYNA 2014-2017].

Accepted Manuscript

Notes on contributors

Mohammed El Madihi is a Ph.D. student. He made most of the field work and data analyses.

His research is mainly focused on the plant communities in the Mediterranean temporary ponds.

Laila Rhazi is a professor. Her research is focused on plant communities in the Mediterranean temporary wetlands in the context of global change and on the population biology of rare and threatened species in this ecosystem.

Maarten Van den Broeck is a Ph.D. student, with a special interest in the ecology of Mediterranean temporary ponds.

Mouhssine Rhazi is a professor, specialising in plant community ecology in Mediterranean temporary pools. He helped with the field work and analysis of data.

Aline Waterkeyn is a teaching assistant and associated researcher. Her research is focused on macro-invertebrate communities in the Mediterranean temporary wetlands.

Er-riyahi Saber is a professor. His research is focused on spatio-temporal dynamics on temporary wetlands using remote sensing.

Siham Bouahim received her Ph.D. in ecology from the University of Casablanca (Morocco) and University of Montpellier 2 (France). Her research is focused on plant communities in the Mediterranean temporary ponds.

Moustapha Arahou, professor and director of the Laboratory of Botany, Mycology and Environment. He conducts research on diverse aspects of plant physiology especially biotic and abiotic stress for plants.

Abdelmajid Zouahri is a researcher with a special interest in soil ecology. He helped with soil analyses.

Anis Guelmami is remote sensing engineer. His main research interest is in the dynamics of land use and spatial analyses using remote sensing data. He produced the climatic syntheses for the study sites.

Serge D. Muller is a lecturer; his research is mainly focused on the past and present dynamics of vegetation in Mediterranean wetlands.

Luc Brendonck is a professor in aquatic ecology and evolutionary biology with a special interest in temporary pond ecosystems around the world.

Patrick Grillas is Programme Director. His main research interest is on the dynamics,

management and conservation of Mediterranean wetlands. He supervised the research

reported, helped with the analysis of data and writing up the paper.

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References

Bagella S, Caria MC, Farris E, Filigheddu RS. 2007. Issues related to the classification of Mediterranean temporary wet habitats according with the European Union Habitats Directive. Fitosociologia 44:245–249.

Bagella S, Caria MC. 2012. Diversity and ecological characteristics of vascular flora in Mediterranean temporary pools. Comptes Rendus Biologies 335(1):69–76.

Bauder ET. 2000. Inundation effects on small-scale plant distributions in San Diego, California vernal pools. Aquatic Ecology 34:43–61.

Bauder ET. 2005. The effects of an unpredictable precipitation regime on vernal pool hydrology. Freshwater Biology 50:2129–2135.

Biggs J, Williams P, Whitfield P, Nicolet P, Weatherby A. 2005. 15 years of pond assessment in Britain: results and lessons learned from the work of Pond Conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 15:693–714.

Black CA, Evans DD, White JL, Ensminger LE, Clark FE. 1985. Methods of soil analysis. Part 1, Physical and Mineralogical properties, Including Statistics of Measurement and Sampling, American Society of Agronomy, Inc Soil Science Society of America 7 eds N°9.

Bliss SA, Zedler PH. 1998. The germination process in vernal pools: sensitivity to environmental conditions and effects on community structure. Oecologia 113:67–73 Bouahim S, Rhazi L, Amami B, Sahib N, Rhazi M, Waterkeyn A, Zouahri A, Mesleard F, Muller

SD, Grillas P. 2010. Impact of grazing impact on the species richness of plant communities in Mediterranean temporary ponds (western Morocco). Comptes Rendus Biologies 333:

670–679.

Bouahim S, Rhazi L, Amami B, Waterkeyn A, Rhazi M, Saber E, Zouahri A,Van Den Broeck M, Muller SD, Brendonck L, Grillas P. 2014. Unravelling the impact of anthropogenic pressure on plant communities in Mediterranean temporary ponds. Marine Freshwater Research65:918–929.

Borcard D, Legendre P, Drapeau P. 1992. Partialling out the spatial component of ecological variation. Ecology73:1045–1055.

Braun-Blanquet J. 1932. Plant sociology, the study of plant community (translation by H.S.

Conard & G.D. Fuller), McGraw Hill Book, New York.

Brendonck L, Jocqué M, Tuytens K, Timms BV, Vanschoenwinkel B. 2014. Hydrological stability drives both local and regional diversity patterns in rock pool metacommunities.

Oikos 124(6):741–749

Brooks R.T. 2009. Potential impacts of global climate change on the hydrology and ecology of ephemeral freshwater systems of the forests of the northeastern United States.

Climate Change 95:469-483; DOI 10.1007/s10584-008-9531-9.

Accepted Manuscript

Buckley HL, Miller TE, Ellison AM, Gotelli NJ. 2003. Reverse latitudinal trends in species richness of pitcher-plant food webs. Ecology Letters 6:825–829.

Casanova M T, Brock MA. 2000. How do depth, duration and frequency of flooding influence the establishment of wetland plant communities? Plant Ecology 147:237–250.

Changhao J, Belinda C, Charles T. 2009. Climate Change Impacts on Wetlands in Victoria and Implications for Research and Policy. Heidelberg, Vic.: Arthur Rylah Institute for Environmental Research, Department of Sustainability and Environment. p. 25–32.

Chevassut G, Quézel P. 1956. Contribution à l’étude des groupements végétaux des mares transitoires à Isoetes velata et des dépressions humides à Isoetes histrix en Afrique du nord. Bulletin de la Société d'Histoire Naturelle d'Afrique du Nord.47:59–73.

Clarke A, Lidgard S. 2000. Spatial patterns of diversity in the sea: bryozoan species richness in the North Atlantic. Journal of Animal Ecology 69:799–814.

CollingeSK, Wise CA, Weaver B. 2003. Germination, early growth, and flowering of a vernal pool annual in response to soil moisture and salinity. Madroño, 50(2):83–93

de Bélair G. 2005. Dynamique de la végétation de mares temporaires en Afrique du Nord (Numidie orientale. N.E.Algérie). Ecologia Mediterranea 31:83–100.

Declerck S, De Bie T, Ercken D, Hampel H, Schrijvers S, Van Wichelen J, Gillard V, Mandiki R, Losson B, Bauwens D, Keijers S, Vyverman W, Goddeeris B, De Meester L, Brendonck L, Martens K. 2006. Ecological characteristics of small farmland ponds: Associations with land use practices at multiple spatial scales. Biological Conservation 131:523–532.

Deil U. 2005. A review on habitats, plant traits and vegetation of ephemeral wetlands – a global perspective. Phytocoenologia 35:533–706.

Döll P, Zhang J. 2010. Impact of climate change on freshwater ecosystems: a global-scale analysis of ecologically relevant river flow alterations. Hydrology and Earth System Sciences 14:783–799.

Ewald N, Hartley S, Stewart A. 2013. Climate change and trophic interactions in model temporary pond systems: the effects of high temperature on predation rate depend on prey size and density. Freshwater Biology 58:2481–2493.

Ewald N, Nicolet P, Oertli B, Della Bella V, Rhazi L, Reymond A-S, Minissieux E, Saber E, Rhazi M, Biggs J, Bressi N, Cereghino R, Grillas P, Kalettka T, Hull A, Scher O, Serrano L 2010. A preliminary assessment of Important Areas for Ponds (IAPs) in the Mediterranean and Alpine Arc.EPCN Technical Report, 46p. (www.europeanponds.org).

Fennane M, Ibn Tattou M, El Oualidi J. 2014. Flore pratique du Maroc, Travaux de l’Institut Scientifique. Vol. 3, Série Botanique 40, Rabat.

Fennane M, Ibn Tattou M, Ouyahya A, El Oualidi J. 2007. Flore pratique du Maroc, Travaux

de l'Institut Scientifique. Série Botanique N°38, Rabat.

Accepted Manuscript

Fennane M, Ibn Tattou M, Mathez J, Ouyahya A, El Oualidi J. 1999. Flore pratique du Maroc.

Manuel de détermination des plantes vasculaires, Vol. 1. Travaux de l'Institut Scientifique, Série Botanique N°36. Rabat.

Fennane M, Ibn Tattou M. 1998. Catalogue des plantes endémiques, rares ou menacées du Maroc. Bocconea 8: 1–243.

Ferchichi-Ben Jamaa H, Muller SD, Daoud-Bouattour A, Ghrabi-Gammar Z, Rhazi L, Soulié- Märsche I, Ouali M, Ben Saad-Limam S. 2010. Structures de végétation et conservation des zones humides temporaires méditerranéennes : la région des Mogods (Tunisie septentrionale). Comptes Rendus Biologies 333:265–279.

Garcia N, Cuttelod A, Abdul Malak D. 2010. The Status and Distribution of Freshwater Biodiversity in Northern Africa. IUCN, Gland, Switzerland, Cambridge, UK, and Malaga, Spain: 141p.

Gerhardt F, Collinge SK. 2003 Exotic plant invasions of vernal pools in the Central Valley of California, USA. Journal of Biogeography 30:1043–1052

GIEC.2014. Cinquième Rapport du GIEC sur les changements climatiques et leurs évolutions futures. Partie 2 : « Impact, adaptation et vulnérabilité », Nations-Unies, Available online at: http://www.ipcc.ch/home_languages_main_french.shtml.

Grillas P, Gauthier P, Yavercovski N, Perennou C. 2004. Mediterranean Temporary Pools: (1) Issues Relating to Conservation, Functioning and Management. Tour du Valat, Le Sambuc, Arles.

Grillas P, Battedou G. 1998. Effects of the date of flooding on the biomass, species composition and seed production of submerged macrophyte beds in temporary marshes in the Camargue (S. France). Proceedings of the Intecol Conference, Perth, September 1996. In Wetlands for the Future (McComb A.J. & J.A. Davis, eds), INTECOL'S V International Wetland Conference, pp:207–218.

Hillebrand H. 2004. On the generality of the latitudinal diversity gradient. American Naturalist 163:192–211.

Hof C, Brändle M, Brandl R. 2008. Latitudinal variation of diversity in European freshwater animals is not concordant across habitat types. Global Ecology and Biogeography 17:539–

546.

Holland C, Honea J, Gwin S, Kentula M. 1995.Wetland degradation and loss in the rapidly urbanizing area of Portland, Oregon.Wetlands 15:336–345.

Jahandiez L, Maire R. 1931-1934. Catalogue des plantes du Maroc (CPM): volumes I (1931), II (1932) et III (1934). Minerva, Alger.

Javornik CJ, Collinge SK. 2016.Influences of annual weather variability on vernal pool plant

abundance and community composition. Aquatic Botany 134:61-67.

Accepted Manuscript

Jeffries MJ. 2016. Flood, drought and the inter-annual variation to the number and size of ponds and small wetlands in an English lowland landscape over three years of weather extremes. Hydrobiologia 76(1): 255–272.

Keeley JE, Zedler PH.1998. Characterization and global distribution of vernal pools. p. 1-14. In Carol C. Witham (ed.) Vernal Pool Ecosystems. California Native Plant Society, Sacramento, CA, USA.

Keddy, P. A., 2000. Wetland Ecology: Principles and Conservation. Cambridge University Press, Cambridge, UK.

Kent M, Coker P. 1992. Vegetation description and analysis, a practical approach. J. Wiley &

Sons 363 p.

Kneitel JM.2016. Climate-driven habitat size determines the latitudinal diversity gradient in temporary ponds. Ecology 97:961–968.

Kraft NJ, Comita LS, Chase JM, Sanders NJ, Swenson NG, Crist TO, Stegen JC, Vellend M, Boyle B, Anderson MJ, Cornell HV. 2011. Disentangling the drivers of β diversity along latitudinal and elevational gradients. Science 333:1755–1758.

Lathrop EW.1976. Vernal ponds of the Santa Rosa Plateau, Riverside County, California. In

‘Vernal ponds, Their Ecology and Conservation’. (Ed. S. Jain.) pp. 22–27. Institute of Ecology Publication No. 9. (University of California: Davis, CA.)

Leibold MA. 1999. Biodiversity and nutrient enrichment in pond plankton communities.

Evolutionary Ecology Research 1:73–95

Lowe K, Castley JG, Hero J.M. 2015. Resilience to climate change: complex relationships among wetland hydroperiod, larval amphibians and aquatic predators in temporary wetlands. Marine and Freshwater Research. 66:886–899. doi:10.1071/MF14128

Lumbreras A, Tahiri H, Pinto-Cruz C, Pardo C, Molina J. 2012. Habitat Variation in Vernal Pool Ecosystems on Both Sides of the Strait of Gibraltar. Journal of Coastal Research 284:1032–

1039.

Menetrey N, Sager L, Oertli B, Lachavanne J.B. 2005.Looking for metrics to assess the trophic state of ponds: Macroinvertebrates and amphibians. Aquatic Conservation-Marine and Freshwater Ecosystems 15:653–664.

Middleton BA. 1999. Wetland Restoration, Flood Pulsing and Disturbance Dynamics. John Wiley and Sons, New York.

Mikulyuk A, Sharma S, Van Egeren S, Erdmann E, Nault M, Hauxwell J. 2011. The relative role of environmental, spatial, and land-use patterns in explaining aquatic macrophyte community composition.Canadian Journal of Fisheries and Aquatic Sciences 68:1778–

1789.

Accepted Manuscript

Nicolet P, Biggs J, Fox G, Hodson MJ, Reynolds C, Whitfield M, WilliamsP. 2004. The wetland plant and macroinvertebrate assemblages of temporary ponds in England and Wales.

Biological Conservation 120:261–278.

Oertli B, Indermuehle N, Gélibert S, Hinden H, Stoll A. 2008. Macroinvertebrate assemblages in 25 high alpine ponds of the Swiss National Park (Cirque of Macun) and relation to environmental variables. Hydrobiologia 597:29–41.

Page Al, Baker DE, Kenny DD, Miller RH, Ellis R, Rhoades JD. 1984. Methods of soil analysis.

Part. 2, Chemical and Microbiological properties. Second edition, N° 9 American Society of Agronomy, Inc Soil Science Society of America, Inc. Publisher Madison, Winsconsin USA.

Pinto-Cruz C, Molina JA, Barbour M, Silva V, Espérito-Santo MD. 2009. Plant communities as a tool in temporary ponds conservation in SW Portugal. Hydrobiologia 634:11–24.

Pyke CP. 2005. Assessing climate change impacts on vernal pool ecosystems and endemicbranchiopods.Ecosystems 8:95–105.

Rhazi L, Grillas P, Saber E, Rhazi M, Brendonck L, Waterkeyn A. 2012 Vegetation of Mediterranean temporary pools: a fading jewel? Hydrobiologia 689:23–36.

Rhazi L, Grillas P, Rhazi M, Aznar JC 2009. Ten-year dynamics of vegetation in a Mediterranean temporary pool in Western Morocco. Hydrobiologia634:185–194.

Rhazi L, Rhazi M, Grillas P, Khyari D. 2006.Richness and structure of plant communities in temporary pools from western Morocco: influence of human activities. Hydrobiologia 570:197–203.

Rhazi L, Grillas P, Mounirou Toure A, Tan Ham L. 2001. Impact of land use and activities on water, sediment and vegetation of temporary ponds in Morocco. Comptes Rendus de l’Académie des Sciences, Paris, Série III, Life Sciences 324:165–177.

Rivas-Martínez S, Diaz TE, Fernàndo-Gonzàlez F, Izco J, Loidi J, Lousã M, Penas A. 2002.

Vascular plant communities of Spain and Portugal. Itinera Geobotanica 15(1-2): 1–922.

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very High Resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25:1965–1978 Rocarpin P, Gachet S, Metzner K, Saatkamp A. 2016. Moisture and soil parameters drive plant community assembly in Mediterranean temporary pools. Hydrobiologia 781(1):55–66 Rodríguez P, Arita H. 2004. Beta diversity and latitude in North American mammals: testing

the hypothesis of covariation. Ecography 27:547–556.

Rosset V, Angélibert S, Arthaud F, Bornette G, Robin J, Wezel A, Vallod D, Oertli B. 2014. Is

eutrophication really a major impairment for small water body biodiversity? Journal of

Applied Ecology 51:415–425.

Accepted Manuscript

Rosset V, Lehmann A, Oertli B. 2010. Warmer and richer? Predicting the impact of climate warming on species richness in small temperate water bodies.Global Change Biology 16:2376–2387.

Ruiz, E., 2008. Management of Natura 2000 habitats, 3170*Mediterranean temporary ponds. European Commission, Technical Report 23.

Sahib N, Rhazi L, Rhazi M, Grillas P. 2009.Experimental study of the effect of hydrology and mechanical soil disturbance on plant communities in Mediterranean temporary pools in Western Morocco. Hydrobiologia 634:77–86.

Scheffer M, Rinaldi S, Gragnani A, Mur LR, Van Nes EH. 1997. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78:272–282

Semlitsch R, Bodie J. 1998. Are Small, Isolated Wetlands Expendable? Conservation Biology 12:1129–1133.

Soininen J, Lennon JJ, Hillebrand H. 2007. A multivariate analysis of beta diversity across organisms and environments. Ecology 88:2830–2838.

Spencer M, Blaustein L. 2001. Risk of Predation and Hatching of Resting Eggs in the Ostracod Heterocypris Incongruens. Journal of Crustacean Biology. 21:575-581.

Stoch F, Korn M, Turki S, Naselli-Flores L, Marrone F. 2016. The role of spatial environmental factors as determinants of large branchiopod distribution in Tunisian temporary ponds.

Hydrobiologia. DOI 10.1007/s10750-015-2637-y

TCMCC. 2016. Troisième Communication Nationale du Maroc à la Convention Cadre des Nations Unies sur les Changements Climatiques. Rapport du Ministère Délégué auprès du Ministre de l’Energie, des Mines, de l’Eau et de l’Environnement Chargé de l’Environnement. 285.

Thiéry A. 1987. Les crustacés branchiopodes des milieux limniques temporaires (dayas) au Maroc. Taxonomie, biogéographie, écologie. Thèse Doctorat de l’Université d'Aix Marseille, [France.

Van den Broeck M, Waterkeyn A, Rhazi L, Grillas P, Brendonck L. 2015. Assessing the ecological integrity of endorheic wetlands, with focus on Mediterranean temporary ponds. Ecological Indicators 54:1–11.

Van den Broeck M. 2016. Monitoring and conservation of Mediterranean temporary ponds.

PhD thesis, Catholic University of Leuven, Belgium, 181p.

Vitalis R, Riba M, Colas B, Grillas P, Olivieri I. 2002. Multilocus genetic structure at contrasted spatial scales of the endangered water fern Marsilea strigosa Willd. (Marsileaceae, Pteridophyta). American Journal of Botany 89:1142–1155.

Waterkeyn A, Grillas P, Vanschoenwinkel B, Brendonck L. 2008. Invertebrate community patterns in Mediterranean temporary wetlands along hydroperiod and salinity gradients.

Freshwater Biology 53:1808–1822.

Accepted Manuscript

Willig MR, Kaufman DM, Stevens RD. 2003. Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual Review of Ecology, Evolution, and Systematics 34:273–309.

Williams DD. 2006. The biology of temporary waters. Oxford University Press, Oxford.

Wilson SD, Keddy PA. 1985. Plant zonation on a lakeshore gradient: physiological response curves of component species. Journal of Ecology 73:851–860.

Zedler PH. 1987. The ecology of Southern California vernal ponds: a community profile. US

Fish and Wildlife Service Biological Report 85:7–11.