Outline
Comptes Rendus

Ecology/Écologie
Spatio-temporal variability of faunal and floral assemblages in Mediterranean temporary wetlands
Comptes Rendus. Biologies, Volume 337 (2014) no. 12, pp. 695-708.

Abstracts

Six temporary wetlands in the region of Sejenane (Mogods, NW Tunisia) were studied in order to characterize the aquatic flora and fauna and to quantify their spatio-temporal variability. Samplings of aquatic fauna, phytosociological relevés, and measurements of the physicochemical parameters of water were taken during four different field visits carried out during the four seasons of the year (November 2009–July 2010). Despite the strong anthropic pressures on them, these temporary wetlands are home to rich and diversified biodiversity, including rare and endangered species. Spatial and temporal variations affect fauna and flora differently, as temporal variability influences the fauna rather more than the plants, which are relatively more dependent on spatial factors. These results demonstrate the interest of small water bodies for maintaining biodiversity at the regional level, and thus underscore the conservation issues of Mediterranean temporary wetlands that are declining on an ongoing basis currently.

Supplementary Materials:
Supplementary materials for this article are supplied as separate files:

Six zones humides temporaires de la région de Sejenane (Mogods, Tunisie du Nord-Ouest) ont été étudiées afin de caractériser leur faune et leur flore aquatiques, et de quantifier leur variabilité spatio-temporelle. Des échantillonnages de la faune aquatique, des relevés phytosociologiques, et des mesures de paramètres physicochimiques de l’eau ont été réalisés au cours des quatre saisons (novembre 2009–juillet 2010). Malgré la forte pression anthropique qui les affecte, ces milieux humides temporaires hébergent une biodiversité riche et diversifiée, avec des espèces rares et menacées. Les variations spatio-temporelles peuvent affecter différemment la faune et la flore, la faune étant relativement plus influencée par la variabilité saisonnière, alors que les plantes sont davantage dépendantes des facteurs spatiaux. Ces résultats révèlent l’intérêt des petits plans d’eau pour le maintien de la biodiversité à l’échelle régionale, et soulignent ainsi les enjeux de conservation des zones humides temporaires méditerranéennes, aujourd’hui en déclin continu.

Compléments :
Des compléments sont fournis pour cet article dans les fichiers suivants :

Metadata
Received:
Accepted:
Published online:
DOI: 10.1016/j.crvi.2014.09.006
Keywords: Aquatic fauna, Biodiversity, Hydrophytes, Northern Tunisia, Seasonal dynamics
Mot clés : Faune aquatique, Biodiversité, Hydrophytes, Tunisie septentrionale, Dynamique saisonnière

Maya Rouissi 1, 2, 3; Dani Boix 4; Serge D. Muller 5; Stéphanie Gascón 4; Albert Ruhí 4; Jordi Sala 4; Ali Bouattour 6; Imtinen Ben Haj Jilani 2, 7; Zeineb Ghrabi-Gammar 2, 8; Samia Ben Saad-Limam 1, 2; Amina Daoud-Bouattour 1, 2

1 Département de biologie, faculté des sciences de Tunis, université de Tunis El-Manar, 2092 Tunis, Tunisia
2 UR99/UR/02-04 biogéographie, climatologie appliquée et dynamique érosive, faculté des lettres, des arts et des humanités de Manouba, université de la Manouba, 2010 Manouba, Tunisia
3 Faculté des sciences de Bizerte, université de Carthage, 7021 Bizerte, Tunisia
4 Institut d’Ecologia Aquàtica, Universitat de Girona, campus Montilivi, 17071 Girona, Spain
5 Institut des sciences de l’évolution de Montpellier (ISE-M), université Montpellier-2/CNRS, case 061, 34095 Montpellier cedex 05, France
6 Service d’entomologie médicale, institut Pasteur, laboratoire d’épidémiologie et de microbiologie vétérinaire, université de Tunis El Manar, BP n° 74, 1002 Belvédère, Tunis, Tunisia
7 Institut supérieur des études préparatoires en biologie et géologie de la Soukra (ISEPBG) Choutrana II, université de Carthage, 2036 Soukra, Tunisia
8 Institut national agronomique de Tunisie, université de Carthage, 43, avenue Charles-Nicolle, 1082 Cité Mahrajène, Tunis, Tunisia
@article{CRBIOL_2014__337_12_695_0,
     author = {Maya Rouissi and Dani Boix and Serge D. Muller and St\'ephanie Gasc\'on and Albert Ruh{\'\i} and Jordi Sala and Ali Bouattour and Imtinen Ben Haj Jilani and Zeineb Ghrabi-Gammar and Samia Ben Saad-Limam and Amina Daoud-Bouattour},
     title = {Spatio-temporal variability of faunal and floral assemblages in {Mediterranean} temporary wetlands},
     journal = {Comptes Rendus. Biologies},
     pages = {695--708},
     publisher = {Elsevier},
     volume = {337},
     number = {12},
     year = {2014},
     doi = {10.1016/j.crvi.2014.09.006},
     language = {en},
}
TY  - JOUR
AU  - Maya Rouissi
AU  - Dani Boix
AU  - Serge D. Muller
AU  - Stéphanie Gascón
AU  - Albert Ruhí
AU  - Jordi Sala
AU  - Ali Bouattour
AU  - Imtinen Ben Haj Jilani
AU  - Zeineb Ghrabi-Gammar
AU  - Samia Ben Saad-Limam
AU  - Amina Daoud-Bouattour
TI  - Spatio-temporal variability of faunal and floral assemblages in Mediterranean temporary wetlands
JO  - Comptes Rendus. Biologies
PY  - 2014
SP  - 695
EP  - 708
VL  - 337
IS  - 12
PB  - Elsevier
DO  - 10.1016/j.crvi.2014.09.006
LA  - en
ID  - CRBIOL_2014__337_12_695_0
ER  - 
%0 Journal Article
%A Maya Rouissi
%A Dani Boix
%A Serge D. Muller
%A Stéphanie Gascón
%A Albert Ruhí
%A Jordi Sala
%A Ali Bouattour
%A Imtinen Ben Haj Jilani
%A Zeineb Ghrabi-Gammar
%A Samia Ben Saad-Limam
%A Amina Daoud-Bouattour
%T Spatio-temporal variability of faunal and floral assemblages in Mediterranean temporary wetlands
%J Comptes Rendus. Biologies
%D 2014
%P 695-708
%V 337
%N 12
%I Elsevier
%R 10.1016/j.crvi.2014.09.006
%G en
%F CRBIOL_2014__337_12_695_0
Maya Rouissi; Dani Boix; Serge D. Muller; Stéphanie Gascón; Albert Ruhí; Jordi Sala; Ali Bouattour; Imtinen Ben Haj Jilani; Zeineb Ghrabi-Gammar; Samia Ben Saad-Limam; Amina Daoud-Bouattour. Spatio-temporal variability of faunal and floral assemblages in Mediterranean temporary wetlands. Comptes Rendus. Biologies, Volume 337 (2014) no. 12, pp. 695-708. doi : 10.1016/j.crvi.2014.09.006. https://comptes-rendus.academie-sciences.fr/biologies/articles/10.1016/j.crvi.2014.09.006/

Version originale du texte intégral

1 Introduction

Mediterranean temporary wetlands are characterized by alternating phases of flooding and drying and by a very self-contained hydrology [1]. Their roles are important with respect to the landscape in terms of flood control, renewal of groundwater, retention of toxic products, and the recycling of nutrients [2,3]. They also provide various resources to the human population, including water availability, storage for grazing and agriculture, or harvesting of medicinal plants [4,5]. Last but not least, they host many rare and endangered taxa, even supporting species and communities that are not found in other water bodies [6]. These habitats there benefit from conservation policies in most European Mediterranean countries [7,8]. At the same time, the ecological relevance of these wetlands contrasts with the decline of Mediterranean temporary wetlands during the last decades, particularly in North Africa where the decline has been severe [9–13]. The temporary hydrology and reduced size of these ecosystems make them highly vulnerable to anthropogenic impacts and pressures from both agricultural practices and urban growth [1,3,4,14–16]. It is thus extremely timely to identify those factors controlling biodiversity in Mediterranean temporary wetlands and also the ultimate cross-taxon congruence patterns that could help determine priorities for their preservation.

The tremendous biodiversity found in wetlands has been attributed to their high spatio-temporal variability [17–19]. Changes in such environmental conditions as the duration of flooding, water depth [6,13,20–22] and surface area [8,23,24] are known to affect both faunal and floral assemblages [25–29]. These environmental characteristics may all vary in any given wetland during the hydroperiod and across wetlands, making it difficult to distinguish between the effects of spatial and of temporal variability. Moreover, none of the studies referred to have considered both flora and fauna at the same time. Only recently have some studies on Mediterranean temporary wetlands begun to consider both faunal and floral assemblages by means of cross-taxon congruence approaches (e.g., [27–31]). The scarcity of available information to date suggests that flora is relatively more determined by spatial variables, whereas faunal groups are probably more closely linked to temporal variability [19–30]. Nevertheless, there are overriding factors that determine biodiversity in local assemblages in some cases such as the size of the ecosystem: it is hypothesized that larger wetlands support more species than smaller ones regardless of the taxonomic group. Yet when tested in temporary habitats (e.g., [23,32,33]), this idea (see Theory of Island Biogeography [31]) has yielded contradictory outputs. The climate in which a wetland is located can be another overarching factor, since this large-scale environmental filter can disrupt the cross-taxon congruence relationships in small areas within a regional scale [34,35]. Overall, to improve the management and conservation strategies for these habitats, it is crucial to further identify the variability (spatial vs. temporal) affecting faunal and floral assemblages of Mediterranean temporary wetlands, and to identify the species-area and/or cross-taxon congruence relationships that may hold across larger scales.

Many temporary wetlands are located in Tunisia, essentially in the northern part of the country [36]. Scientific studies have focused to date on the great wetland complexes such as the Ichkeul National Park (e.g., [37–41]) and have more or less ignored the northern temporary Tunisian wetlands, with the exception of some late 19th century studies [42] and others carried out between 1930 and 1960 [43–46]. Since that time, no further research on Tunisian temporary wetlands has been undertaken until the appearance of several studies, which have focused primarily on vegetation (e.g., [36,47–54]), Crustaceans (e.g., [55,56]) and on amphibians (e.g., [57–60]). The present paper presents the first study integrating both aquatic faunal (amphibians and macroinvertebrates) and floral assemblages in North African temporary wetlands.

Our overarching aim was to characterize flora and fauna of six temporary wetlands in the Sejenane region of northern Tunisia and to quantify their spatio-temporal variability. As found in previous cross-taxon congruence studies in other Mediterranean climate areas, we predicted that:

  • • temporal variability would be more relevant for faunal than for floral assemblages;
  • • the converse would be true for spatial variability.

2 Material and methods

2.1 Study sites

The study was carried out on six temporary wetlands near Sejenane (Mogods region, north-western Tunisia; Fig. 1). This region experiences a Mediterranean wet bioclimate of mild winters, and annual rainfalls ranging from 800 to 1000 mm. The Mogods Hills, composed of Oligocene sandstone, are covered by degraded thermo-Mediterranean cork oak forests and scrub. The six temporary wetlands differ mainly in their mesological parameters (Fig. 1; Table 1).

Fig. 1

Location of the six temporary wetlands studied (in Mogods region, Northern Tunisia). EZZ: Ezzoubia; GGT: Garâa Guetma; GS1: Garâa Sejenane1; GS2: Garâa Sejenane2; Gue: Guetma; MCh, Majen Choucha.

Table 1

Mesological parameters for the six temporary wetlands studied. COD, chemical oxygen demand; A, autumn; W, winter; P, spring; S, summer. See Fig. 1 for site codes.

Site GUE GS1 EZZ GS2 GGT MCH
Type Temporary pond Temporary pond Temporary pond Temporary marsh Temporary marsh Semi-permanent lake
Altitude (m) 98 101 117 102 96 445
Latitude N 37°07’37" 37°05’56" 37°04’40" 37°06’12" 37°08’02" 37°00’38"
Longitude E 09°15’59" 09°11’39" 09°08’36" 09°12’06" 09°15’06" 09°12’42"
Area (m2) 400 15 000 1000 30 000 65 000 4500
Flooding duration (seasons) 2 2 3 3 3 4
Maximal water depth (cm) 20 20 50 45 65 120
Organic matter (%) 9.1 2.7 2.2 2.2 2.7 14.2
Carbonates (%) 8.2 18.7 5.7 16.7 14.8 3.9
Particles > 63 μm (%) 47.89 86.67 20.80 40.53 97.92 20.27
Particles < 63 μm (%) 37.10 46.00 79.93 19.99 16.00 79.74
Human activities Close to homes Mowed Cultivated Mowed Pastured
Season A W A W A W P A W P A W P A W P S
Water level (cm) 20 10 20 20 50 50 30 45 30 15 65 20 20 100 120 110 45
Temperature (°C) 9.8 13.4 10.2 17.0 10.5 18.0 23.6 14.4 13.0 18.0 13.0 18.0 19.3 7.4 12.5 16.5 31.0
pH 7.2 7.5 8.2 7.5 7.6 7.0 6.5 7.4 6.7 7.7 7.4 6.7 7.7 7.1 7.0 8.3 7.8
Conductivity (μs) 277 440 119 92 23 38 693 157 177 238 270 257 293 73 77 87
Nitrite (mg/l) 0.000 0.170 0.001 0.001 0.001 0.006 0.001 0.007 0.050 0.050 0.003 0.002 0.004 0.010 0.010 0.030 0.030
Nitrate (mg/l) 1.2 3.0 1.0 0.5 0.5 0.5 0.5 0.5 0.5 0.5 1.2 0.5 0.6 0.5 0.5 0.7 0.7
Ammonium (mg/l) 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5
Azote total (mg/l) 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 35
Total phosphorus (mg/l) 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5
COD (mg/l d’O2) 10 10 130 10 30 30 26 75 10 37 46 40 12 172 10 24 234

MCH is a semi-permanent freshwater acidic lake located atop Jbel Choucha (445 m), surrounded by an overgrazed cork oak forest. The area is used to pasture cattle, sheep and goats, and is also a bountiful source of leeches used by the local population for traditional health treatments. The five other sites (GUE, GS1, GS2, GGT AND EEZ) are located in and around Garâa Sejenane, a vast endorheic plain formed by a mosaic of cultivated-pastured lands and shallow temporary pools formed on hydromorphic soils [49]. GS1 and GS2 are situated at the northeastern border of Garâa Sejenane, and are respectively a large temporary pond and an extended temporary marsh. The two sites were completely mowed in the summer. GGT is also a large temporary marsh, located in Garâa Guetma, 6 km east of Garâa Sejenane. GUE and EZZ are two small temporary ponds located on the roadside. EZZ is an artificial pond with irregular topography that is cultivated in the summer (e.g., peppers, melon). GUE is neither cultivated nor grazed, but is located close to residential developments. MCH and Gue are clearly delineated by three vegetation belts (marginal, intermediate and central), EZZ has only two zones (marginal and central), and GS1, GS2 and GGT show no zonation.

2.2 Data collection

Water, plant cover and aquatic fauna were sampled simultaneously over a period of 10 months (from November 2009 to July 2010) during four field visits carried out during all four seasons. Water variables (temperature, depth, conductivity and pH) were measured in situ. Substrate texture (particle size, carbonates and organic matter) and nutrients (nitrate, nitrite, total nitrogen, total phosphate and chemical oxygen demand) were analyzed in a laboratory (Table 1). Aquatic fauna was sampled using a 250 μm mesh dip-net (20 cm diameter), and the sampling procedure was based on 20 rapid-succession dip-net sweeps covering all different microhabitats visually detected in the littoral zone of the wetlands. Samples were preserved in 4% formalin. Aquatic fauna was identified mainly to family level as per the extant literature (e.g., [61–63]). The abundance of fauna is expressed in the number of specimens per sample. Phytosociological relevés were carried out in all sites in the area of sampling fauna using the Braun-Blanquet [64] method with an abundance/dominance scale from + to 5. Plant nomenclature follows Le Floc’h et al. [65]. Moreover, the ecological requirements of plants were established using Bagella and Caria [66].

2.3 Data analysis

2.3.1 Relationships between assemblage parameters and wetland sites and season

Three assemblage parameters were estimated: taxonomic richness, Shannon–Wiener diversity [67] and Jassby–Goldman succession index [68]. The latter was calculated as per the equation:

Sj=iCiaCibab21/2Cia=biaibia21/2
where Sj is the daily rate of the community change, (a-b) is the time interval in days, Cia and Cib are the contributions of the species i in the abundance of the community on days a and b respectively, bia is the abundance of the species i on day a.

An analysis of variance (ANOVA, one-way) was performed using the function ‘aov’ of the R program [69] on the three assemblage parameters to check the significance effect of the site or the season on each dataset (flora and fauna). For the flora, two datasets, one at species level and the other at family level, were used to check whether, in our study, ANOVA results were related to taxonomic resolution.

2.3.2 Variability in faunal and floral composition

We used an analysis of similarities (ANOSIM; [70]) to test for changes in assemblage composition among sites and seasons (ANOSIM, 999 iterations, significance level = 0.05). Two ANOSIM analyses were performed for each dataset (i.e. fauna and flora), using site and season respectively as factors. In the case of flora, ANOSIM tests were performed using matrices at species and family levels, to determine whether the results depended on taxonomic resolution. For cases with significant differences, similarity percentages (SIMPER analysis; [71]) made it possible to identify the particular species that typified each site relatively to seasons, and each season relatively to sites (site and season as factors). Such ‘typifying’ taxa of one particular site (season) explain the highest proportions of the between-seasons (sites) similarity in this site (season). Finally, we used non-parametric multidimensional scaling (NMDS) to visualize how aquatic faunal or floral assemblages differed among the sites and during the various seasons. Statistical tests (NMDS, ANOSIM, SIMPER) and some assemblage parameters were calculated using PRIMER v6 [72].

3 Results

3.1 Faunal and floral assemblages’ overview

A total of 106,627 faunal specimens (vertebrates and macroinvertebrates) belonging to 68 taxa were identified during the study (see Supplementary Material, Appendix S1). The macroinvertebrates were qualitatively dominated by insects (52 taxa), of which 23 were Coleoptera, 15 Diptera, 8 Hemiptera, 4 Odonata, and 1 Trichoptera. Gastropods (4 taxa), macrocrustaceans (3 taxa), Hydracarina (2 taxa) and Oligochaeta (1 taxon) were also found. Amphibians were represented by one species of newt and two anurans: Bufotes boulengeri (Lataste, 1879) was found only in EZZ, while Discoglossus pictus (Otth, 1837) and the Algero-Tunisian endemic Pleurodeles nebulosus (Guichenot, 1850) were found in all sites except GGT (see Supplementary Material, Appendix S1). Taxa richness was roughly the same in all sites (24 - 36 taxa; Table 2) and seasons (16 - 21 taxa; Table 3). In terms of abundance, gastropods (mainly Planorbidae) dominated in all sites except in EZZ and MCH, where Chironomidae and Baetidae were the dominant groups respectively (Fig. 2). Moreover, fauna showed seasonal variations in relative abundance (Fig. 2): whereas in autumn and winter, Gastropoda was the most abundant group and Ephemeroptera dominated in summer. Lower dominances were observed in spring when Ephemeroptera, Chironomidae, Gastropoda and Notonectidae were the most abundant (Fig. 2).

Table 2

Number of samples, total taxonomic richness (cumulative richness), taxonomic richness, ecological diversity (Shannon–Wiener index) and succession rate (Jassby–Goldman index) for each temporary wetland. For the latter three variables, average (AVE) and standard deviation (STD) are given. The last column (P-value) shows the one-way ANOVA results. See Fig. 1 for site codes.

Site GUE GS1 EZZ GS2 GGT MCH P-value
FAUNA (at family level)
 Number of samples 2 2 3 3 3 4
 Total taxonomic richness 25 24 29 29 36 32
 Taxonomic richness AVE 20.0 17.5 20.0 18.7 19.7 15.8 > 0.05
STD 2.8 0.7 1.0 2.9 3.2 3.9
 Ecological diversity AVE 1.40 1.93 2.50 1.06 2.02 2.00 > 0.05
STD 1.04 0.81 0.99 0.58 0.93 0.43
 Succession rate (month−1) AVE 0.15 0.43 0.42 0.34 0.46 0.46 > 0.05
STD 0.07 0.45 0.20 0.10
FLORA (at species level)
 Number of samples 4 3 4 4 4 4
 Total taxonomic richness 34 29 41 26 38 25
 Taxonomic richness AVE 15.3 17.7 26.0 13.0 19.0 12.8 > 0.05
STD 7.1 6.7 7.2 7.5 9.0 4.9
 Ecological diversity AVE 3.47 3.78 4.49 3.20 3.82 3.37 > 0.05
STD 0.62 0.47 0.36 1.27 0.63 0.57
 Succession rate (month−1) AVE 0.31 0.29 0.23 0.39 0.27 0.21 > 0.05
STD 0.12 0.28 0.10 0.14 0.08 0.13
Table 3

Number of samples, taxonomic richness, ecological diversity (Shannon–Wiener index) and succession rate (Jassby–Goldman index) for each season. For the latter three variables, average (AVE) and standard deviation (STD) are shown. The last column (P-value) shows the one-way ANOVA results. Similar letters noted in superscript indicate significant correlations.

Season Autumn Winter Spring Summer P-value
FAUNA (at Family level)
 Number of samples 6 6 4 1
 Taxonomic richness AVE 16.3 19.0 20.7 18.0 > 0.05
STD 3.3 2.3 1.9
 Ecological diversity AVE 2.05a,b 1.24b 2.57a 1.38a,b 0.04
STD 0.74 0.55 0.68
 Succession rate (month−1) AVE 0.36 0.47 0.35 > 0.05
STD 0.22 0.15
FLORA (at Species level)
 Number of samples 6 6 6 5
 Taxonomic richness AVE 13.3b 16.2a,b 26.0a 12.8b 0.03
STD 3.6 5.3 7.0 8.1
 Ecological diversity AVE 3.44a,b 3.66a,b 4.41a 3.14b < 0.01
STD 0.42 0.50 0.38 1.15
 Succession rate (month−1) AVE 0.15b 0.35a 0.35a < 0.01
STD 0.06 0.13 0.06
Fig. 2

Percentages of taxonomic richness (upper panels) and abundance (lower panels of the faunal groups. Site faunal composition (left panels) and seasonal faunal composition (right panels) are shown. See Fig. 1 for site codes.

A total of 79 plant species belonging to 27 families were recorded in the six temporary wetlands (see Supplementary Material, Appendix S2). Therophytes (annual species) dominated species richness, with 50 species (63%). Thirty-nine species (49%) were hydrophytic or characteristic of temporary wetlands. Eighteen species were rare or infrequent, of which 7 were endangered in North Africa according to the IUCN categories (“critically endangered” or “near threatened” [73]). The remaining species (38% of the total species richness) were opportunists. When comparing wetlands by size, small pond species richness (GUE and EZZ) was higher or similar (34 and 41 species, respectively) than that of the larger habitats such as marshes (GGT and GS2; 38 and 26 species, respectively), the large pond of GS1 (29 species) and the semi-permanent lake of MCH (25 species) (Table 2). Overall, the most abundant families in the wetlands were Poaceae and Cyperaceae, except in MCH where Haloragaceae, with a single species (Myriophyllum alterniflorum) was most abundant (Fig. 3). This could be due to the fact that this has the longest hydroperiod, as this species was present here only. Isoetes velata had also a high abundance at MCH (the third most abundant species after M. alterniflorum and Glyceria spicata), contrasting with its abundance in the other wetlands where it was present (GS1 and EZZ). Relative abundances among families did not differ seasonally, although the abundance of Ranunculaceae decreased from autumn to spring and was quasi absent in summer (Fig. 3).

Fig. 3

Percentages of taxonomic richness (upper panels) and abundance (lower panels of the flora groups. Site floral composition (left panels) and seasonal floral composition (right panels) are shown. See Fig. 1 for site codes.

3.2 Spatio-temporal variability

When assessing the potential effects of taxonomic resolution (ANOVA, ANOSIM and NMDS in species-vs. family-level matrices), we observed coincident outputs. For this reason, we only show the results obtained using species level.

None of the three assemblage parameters (taxonomic richness, ecological diversity, and succession rate) used to measure fauna and flora differed significantly from site to site (ANOVA, Table 2). By contrast, ecological diversity differed from season to season, peaking for both flora and fauna in the spring, at a minimal level in the winter for animals and in the summer for plants (Table 3). The succession rate was significantly low for plants in the winter.

With regard to the spatial component, different results were obtained for fauna and flora: fauna presented homogeneous compositions (ANOSIM, R = 0.034, P = 0.347) while the flora differed significantly among wetlands (ANOSIM, R = 0.466, P = 0.001). In contrast, both fauna and flora showed significant differences for composition across seasons (fauna: R= 0.373, P = 0.006; flora: R = 0.118, P = 0.034). These results were in accordance with the NMDS ordination analysis (Fig. 4), with samples grouped by sites for flora only. Moreover, NMDS plots showed seasonal clustering for both faunal and floral assemblages (Fig. 4).

Fig. 4

Nonmetric multidimensional scaling (NMDS) plots of faunal (upper panels) and floral (lower panels) assemblages among sites (left panels) and seasons (right panels). See Fig. 1 for site codes.

SIMPER analyses identified taxa that contributed highly to the similarity among samples for each season, i.e. ‘typifying’ taxa (Table 4). Some of these typified the three seasons that were analyzed, such as Chironomidae and Planorbidae, while others were characteristic of two seasons (i.e. Lymnaeidae in autumn and winter, or Baetidae in winter and spring), or only one (i.e. Corixidae in autumn, Salamandridae in winter, and Dixidae in spring). Note that from autumn to spring, some taxa showed an increase in their contribution to similarity (i.e. Baetidae), while others showed a decrease (i.e. Planorbidae). When SIMPER tests were run for plant species (Table 5), we identified only one of the five species contributing highly to seasonal similarity that consistently typified the assemblage across all seasons (Eleocharis palustris), whereas some other species characterized just one season (Ranunculus sardous in autumn, Myosotis sicula in winter, Alopecurus bulbosus in spring, and Mentha pulegium in summer). The set of characteristic species in summer was clearly different from the rest, with four of the five taxa characterizing summer alone, and two characteristic species of the other seasons absent from the ‘summer set’ (Glyceria spicata and Alisma lanceolatum). Finally, SIMPER analyses identified the five plant species that contributed highly to the similarity among samples of each site (Table 6). Two sites with a high similarity in percentage (GUE, 72.0%; MCH, 68.4%), a site with a low percentage (i.e., EZZ, 36.3%), and the four remaining sites with intermediate percentages (51.8%–61.3%) (Table 6). Moreover, MCH had the highest number of typifying species that were uncharacteristic of the other wetlands (three of the five species). GUE and GS1, by contrast, each harbored only a single species of this kind (Juncus fontanesii and Ranunculus sardous, respectively).

Table 4

Faunal species typifying each season (SIMPER analysis). The five species that contribute most to between-sites similarity were selected.

Autumn Winter Spring
(64.5% average similarity) (76.2% average similarity) (58.1% average similarity)
Taxa % Taxa % Taxa %
Planorbidae 32.2 Planorbidae 52.2 Baetidae 22.5
Chironomidae 10.1 Chironomidae 7.0 Chironomidae 14.0
Notonectidae 8.7 Lymnaeidae 6.0 Planorbidae 7.5
Corixidae 6.9 Baetidae 6.0 Dixidae 7.4
Lymnaeidae 6.6 Salamandridae 5.0 Dytiscidae 6.7
Table 5

Floral species typifying each season (SIMPER analysis). The five species contributing that contribute most to between-sites similarity were selected.

Autumn Winter
(69.4% average similarity) (61.2% average similarity)
Taxa % Taxa %
Glyceria spicata 27.5 Glyceria spicata 22.0
Ranunculus baudotii 11.9 Ranunculus baudotii 13.2
Eleocharis palustris 10.2 Eleocharis palustris 12.2
Alisma lanceolatum 10.1 Alisma lanceolatum 8.4
Ranunculus sardous 9.7 Myosotis sicula 5.4
Spring Summer
(40.9% average similarity) (81.5% average similarity)
Taxa % Taxa %
Glyceria spicata 9.9 Mentha pulegium 33.8
Alisma lanceolatum 9.2 Bolboschoenus glaucus 15.4
Eleocharis palustris 8.7 Lotus hispidus 13.7
Alopecurus bulbosus 7.9 Cynodon dactylon 10.2
Ranunculus ophioglossifolius 5.2 Eleocharis palustris 8.4
Table 6

Floral species typifying each site (SIMPER analysis). See Fig. 1 for site codes. The five species that contribute most to between-seasons similarity were selected.

GUE GS1 EZZ
(72% average similarity) (51.8% average similarity) (36.3% average similarity)
Species % Species % Species %
Lotus hispidus 18.5 Myosotis sicula 12.9 Paspalum distichum 8.1
Eryngium pusillum 16.1 Glyceria spicata 10.8 Lotus hispidus 8.0
Juncus fontanesii 15.5 Alisma lanceolatum 10.5 Alisma lanceolatum 6.9
Eleocharis palustris 11.3 Ranunculus sardous 9.0 Eleocharis palustris 6.8
Glyceria spicata 10.6 Eleocharis palustris 8.6 Cynodon dactylon 6.5
GS2 GGT MCH
(58.6% average similarity) (61.3% average similarity) (68.4% average similarity)
Species % Species % Species %
Bolboschoenus glaucus 28.3 Bolboschoenus glaucus 18.8 M. alterniflorum 18.6
Glyceria spicata 8.2 Eryngium pusillum 14.6 Isoetes velata 15.4
Rumex tunetanus 8.0 Panicum repens 11.4 Glyceria spicata 14.9
Myosotis sicula 7.6 Schoenoplectus lacustris 8.4 Ranunculus baudotii 9.9
R. ophioglossifolius 6.5 Glyceria spicata 8.1 Eleocharis palustris 9.6

4 Discussion

4.1 Fauna communities

The temporary wetlands that we studied were rich in fauna, most of the taxa were known from the temporary wetlands of Morocco [74–77], Italy [78–80] and Spain [17,81,82]. While certain taxa such as Lepidurus apus subsp. lubbocki are known exclusively in temporary wetlands [83], others are widespread in all types of aquatic habitats. This is true for Pleurodeles nebulosus, Discoglossus pictus [57], some Coleoptera (Dytiscidae, Gyrrinidae, Haliplidae, Hydrochidae, Noteridae) [84,85], Ephemeroptera (Baetidae [86]), Hemiptera (Coriidae, Naucoridae including Naucaurus masculatus, Notonectidae, Gerridae, Pleidae [87]) and Oligochaeta (Enchytraeidae [88]). Within this context, the temporary wetlands that we examined contained two different types of aquatic macroinvertebrates [76]:

  • • on the one hand, resident taxa that have developed adaptive strategies against desiccation (e.g., production of resistant forms), such as Branchiopoda [89,90], gastropods (Physidae, Planorbidae, Lymnaeidae [76]), some coleopterans (Hydrophilidae: Berosus [91]; Helophorus and Laccobius [76]), and some dipterans (Chironomidae: Chironomini [92]);
  • • on the other hand, migrant taxa originating from permanent aquatic habitats, temporarily colonizing the body of water and leaving it before desiccation, such as heteropterans (Corixidae, Notonectidae), some coleopterans (Dytiscidae, Hydrophilidae [76]) and some dipterans (Chironomidae, Culicidae, Ceratopogonidae).

In accordance with previous studies [81,93,94], we observed that insects were the most diverse macroinvertebrate group, dominated by the order of dipterans and family of Chironomidae [81,95]. Our results also confirmed the presence of the three amphibian species that were supposed to occur in the region: the Bufotes boulengeri toad, the Mediterranean Painted Frog Discoglossus pictus, and the Algero-Tunisian Ribbed Newt Pleurodeles nebulosus [57,58,96,82]. However, in contrast with previous studies (e.g., [97–99]) and while the total taxonomic faunal richness is lower in sites with the lowest hydroperiod duration (2 months), no significant changes in faunal assemblages can be attributed to hydroperiod duration (temporary vs. semi-permanent). Such an apparent homogeneity between sites with different hydroperiods could be explained, at least partially, by the low taxonomic resolution achieved in this study.

4.2 Plant communities

The wealth of plants recorded in this study (79 species in six temporary wetlands) fall into a similar range (Pearson correlation: R = 0.970; P < 0.001) to those observed in the Mogods-Kroumirie region: (244 species in 36 wetlands [54]), and from different Mediterranean areas such as Sardinia (113 species in 9 pools [19]), Minorca (360 species in 63 pools [100]), Portugal (168 species in 29 pools [101]), Morocco (253 species in 48 pools [102]), and Algeria (136 species in 26 pools [103]). Annual species predominated, accounting for 66% of the total number of species, including hydrophytes and opportunistic species, a finding that is consistent with previous studies in a variety of Mediterranean-climate regions, namely North Africa [11,13,54,73,104–106], Southwest Europe [1,100,107,108] and California [105]. This dominance reflects a strong adaptation to the fluctuating environmental conditions of temporarily wet habitats [3]. Constraints such as these favor short-cycled species that invest more in sexual reproduction than in vegetative development [13,107,109]. The presence of 11 rare species, including 7 that are endangered in North Africa [73], confirms the importance of Mediterranean temporary wetlands as a key habitat for the conservation of rare and endemic flora [1,107,110,111]. In this sense, it is important to note that we also found Rumex tunetanus, a strict endemic of Garâa Sejenane found only in the two sites of this garâa (GS1 and GS2), and Nitella opaca and Pilularia minuta, two species recently discovered in Tunisia [36,49,54].

4.3 Seasonal dynamics

The temporary wetlands that we studied are affected by the Mediterranean climate, which during a year typically alternates between at least one flooded phase from September to April, and one dry summer phase. It was not surprising, therefore, that seasons have a significant effect on both floral and faunal compositions. In the case of flora, the alternation between wet and dry phases probably favors the establishment of two distinct groups of plants: an assemblage of aquatic and amphibious species during the flooded period, and an assemblage of terrestrial species during the dry period (as described by [1,112,113]). In the case of fauna, compositions appear to depend primarily the length of the hydroperiod and secondarily, on seasonality [3,114,115]. This observation is consistent with other studies that have shown the unique importance of the length of the hydroperiod for both faunal composition [34,116,117] and richness [118,119]. Indeed, in temporary habitats, community structure is well known to change as the hydroperiod advances [28]: In autumn, when temporary wetlands are usually filled, macroinvertebrates begin to recolonize the habitats [1,3,120,121]. Taxa that are resistant to dry phases, such as pioneer crustaceans (Anostraca, Notostraca), oligochaetes, gastropods, water mites and some insects (e.g., the hydrophilid Berosus or the chironomid Chironomus), appear early after inundation [98,122–124]. Additionally, other insects (e.g., dytiscids, baetids, notonectids, libellulids) take advantage of their mobility and great capacity to discover and colonize “new” water bodies [125]. Later, a second wave of insects may cause further increases in species richness during winter [95], although it is not before spring that the richness of some particular insect groups (mostly coleopterans and heteropterans) typically peaks. During this period, tadpoles accelerate their development (as observed in the longer-hydroperiod sites; EZZ, GS2, GGT and MCH). Subsequently, aquatic insects generally migrate to permanent waters until the next filling phase (if their adult stage is aquatic) or alternatively, survive as terrestrial adults [114].

4.4 Spatial patterns

Although the wetlands we studied were situated relatively close to one another (except MCH, higher than the rest), the sites differed greatly in their plant assemblages. This finding confirms the importance of habitat type (pond, marsh, lake) for floral composition, as already described from the same region by Ferchichi-Ben Jamaa et al. [54]. In accordance with their observations, both Garâa Sejenane sites (GS1 and GS2) harbor similar hydrophytic (amphibious and helophytic) communities.

To date, several studies have described significant species richness-area relationships for both fauna and flora in temporary wetlands [8,19,23,24,30,76,126,127]. The Theory of Island Biogeography [128] applied to isolated wetland metacommunities would predict that relatively larger bodies of water bodies allow for more ecological niches and thereby accommodating more taxonomic groups [23]. While some authors have found positive relationships between plant richness and wetland size [19,23,30], our study did not show this relationship. Rather, we observed that small bodies of water were richer than larger ones. This result could be triggered by higher microhabitat heterogeneity in small wetlands when compared to larger ones [54]. It could be also related to the biological type of the present species, as clonal perennial species have a tendency to create more homogeneous communities than do annual species. However, our data do not support this last hypothesis (not significant Pearson correlations). Nevertheless, for fauna, our study shows comparable taxa richness among sites. The lack of richness-area relationship for fauna could be explained by the fact that our study:

  • • was carried at the level of major taxonomic groups that include species with diverse ecological requirements;
  • • has not taken into account overriding filters, such as hydroperiod length [34,118], biotic interactions [129], water chemistry (e.g., [130,131]), or human activities, particularly cultivation [132,133].

Although it is not possible to disentangle the effects of these potential drivers from our study, we think that agriculture practices may have had a significant impact on the observed spatial patterns, as has been described by studies that explicitly address the influence of agriculture in wetland communities [132].

4.5 Congruence between faunistic and floristic patterns, and implications for biodiversity conservation

Many authors have showed positive correlations between plant and fauna diversities [8,23,134–137]. Hydrophytic plants generally play a major role in freshwater ecosystems by structuring the habitat [138], providing refuges [139] and egg-laying sites, and constituting a food source for macroinvertebrates and amphibians. In our study, the effects of the varying lengths of the hydroperiod and agricultural practices seem to obscure the relationship between fauna and flora richness as they seem to affect respectively the faunistic and floristic assemblages. Nevertheless, congruence relationships between faunal and floral assemblages can be useful for helping to define and prioritize areas of conservation interest. Therefore, while our results exemplify that such relationships can be “broken” by overriding factors such as those discussed (or even larger scale factors such as climate [32]), we consider that congruence should continue to be explored.

Overall, the present study demonstrates that temporary wetlands harbor rich and diversified floral and faunal assemblages (including rare and endangered species), even when submitted to strong anthropogenic pressures. This study also supports the idea that spatial and temporal variations affect fauna and flora differently, with fauna being relatively more influenced by seasonal dynamics [19–30], and plants more dependent on spatial factors. Although predicting global patterns based solely on fauna or flora remains difficult, our results show how small bodies of water can help maintain regional biodiversity, which is relevant for the purposes of conservation in light of the ongoing decline of Mediterranean temporary freshwater habitats.

Acknowledgements

Financial support was provided by UR99/UR/02-04 Biogéographie, Climatologie Appliquée et Dynamique Érosive, FLAHM, Université de la Manouba, Tunisia. The authors express their gratitude to the “Direction générale des Forêts” (“Ministère de l’Agriculture et des Ressources hydrauliques” of Tunisia) for fieldwork authorizations and facilities, and to D. Glassman for editorial assistance. This paper constitutes contribution ISE-M No. 2014-144.


References

[1] P. Grillas; P. Gauthier; N. Yavercovski; C. Perennou Mediterranean temporary pools, station biologique de la Tour du Valat, Arles, 2004 (2 vols)

[2] P.A. Keddy Wetland ecology: principles and conservation, Cambridge University Press, Cambridge, UK, 2000

[3] D.D. Williams The biology of temporary waters, Oxford University Press, Oxford, 2006

[4] P. Williams; J. Biggs; G. Fox; P. Nicolet; M. Whitfield History, origins and importance of temporary ponds, Freshw. Forum, Volume 17 (2001), pp. 7-16

[5] J. Biggs; P. Williams; M. Whitfield; P. Nicolet; A. Weatherby 15 years of pond assessment in Britain: results and lessons learned from the work of Pond Conservation, Aquat. Conserv. Mar. Freshwat. Ecosyst., Volume 15 (2005), pp. 693-714

[6] P. Williams; M. Whitfield; J. Biggs; S. Bray; G. Fox; P. Nicolet; D. Sean Comparative biodiversity of rivers, streams, ditches and ponds in an agricultural landscape in Southern England, Biol. Conserv., Volume 115 (2003), pp. 329-341

[7] J. Biggs; D. Bilton; P. Williams; P. Nicolet; L. Briggs; B. Eeles; M. Whitfield Temporary ponds of eastern Poland: an initial assessment of their importance for nature conservation, Arch. Sci., Volume 57 (2004), pp. 73-83

[8] P. Nicolet; J. Biggs; G. Fox; M.J. Hodson; C. Reynolds; M. Whitfield; P. Williams The wetland plant and macroinvertebrate assemblages of temporary ponds in England and Wales, Biol. Conserv., Volume 120 (2004), pp. 261-278

[9] B. Samraoui; G. de Bélair; S. Benyacoub A much-threatened lake: Lac des Oiseaux in North-eastern Algeria, Environ. Conserv., Volume 19 (1992), pp. 264-267

[10] G. de Bélair; B. Samraoui Death of a lake: Lac Noir in the Northeastern Algeria, Environ. Conserv., Volume 21 (1994), pp. 169-172

[11] L. Rhazi Étude de la végétation des mares temporaires et l’impact des activités humaines sur la richesse et la conservation des espèces rares au Maroc,, Université Hassan II, Casablanca, 2001 ([Doctoral thesis])

[12] L. Rhazi; P. Grillas; A. Mounirou Touré; L. Tan Ham Impact of land use in catchment and human activities on water, sediment and vegetation of Mediterranean temporary pools, C. R. Acad. Sci. Paris, Ser. III, Volume 324 (2001), pp. 165-177

[13] L. Rhazi; M. Rhazi; P. Grillas; D. El Khyari Richness and structure of plant communities in temporary pools from western Morocco: influence of human activities, Hydrobiologia, Volume 570 (2006), pp. 197-203

[14] J.H. Bratton Seasonal pools: an overlooked invertebrate habitat, British Wildlife, Volume 2 (1990), pp. 22-29

[15] L. Serrano; L. Serrano Influences of groundwater exploitation for urban water supply on temporary ponds from the Donana National Park (Southwest Spain), J. Environ. Manage., Volume 46 (1995), pp. 229-238

[16] I. Zacharias; A. Parasidoy; E. Bergmeier; G. Kehayias; E. Dimitriou; P. Dimopoulos A “DPSIR” model for Mediterranean temporary ponds: European, national and local scale comparisons, Ann. Limnol-Int. J. Lim., Volume 44 (2008), pp. 253-266

[17] M. Florencio; L. Serrano; C. Gómez-rodríguez; A. Millán; C. Díaz-paniagua Inter- and intra annual variations of macroinvertebrate assemblages are related to the hydroperiod in Mediterranean temporary ponds, Hydrobiologia, Volume 634 (2009), pp. 167-183

[18] L. Rhazi; P. Grillas; M. Rhazi; J.C. Aznar Ten-year dynamics of vegetation in a Mediterranean temporary pool in western Morocco, Hydrobiologia, Volume 634 (2009), pp. 185-194

[19] S. Bagella; S. Gascón; M.C. Caria; J. Sala; M.A. Mariani; D. Boix Identifying key environmental factors related to plant and crustacean assemblages in Mediterranean temporary ponds, Biodivers. Conserv., Volume 19 (2010), pp. 1749-1768

[20] C. Fernández-Aláez; M. Fernández-Aláez; E. Bécares Influence of water level fluctuation on the structure and composition of the macrophyte vegetation in two small temporary lakes in the northwest of Spain, Hydrobiologia, Volume 415 (1999), pp. 155-162

[21] M.G. Barbour; A.I. Solomeshch; R.F. Holland; C.W. Witham; R.L. Macdonald; S.S. Cilliers; J.A. Molina; J.J. Buck; J.M. Hillman Vernal pool vegetation of California: community of long-inundated deep habitats, Phytocoenologia, Volume 35 (2005) no. 2–3, pp. 177-200

[22] L.L. Battaglia; B.S. Collins Linking hydroperiod and vegetation response in Carolina bay wetlands, Plant Ecol., Volume 184 (2006), pp. 173-185

[23] B. Oertli; D.A. Joye; E. Castella; R. Juge; D. Cambin; J.B. Lachavanne Does size matter? The relationship between pond area and biodiversity, Biol. Conserv., Volume 104 (2002) no. 1, pp. 59-70

[24] A. Ruggiero; R. Cereghino; J. Figuerola; P. Marty; S. Angelibert Farm ponds make a contribution to the biodiversity of aquatic insects in a French agricultural landscape, C. R. Biologies, Volume 331 (2008), pp. 298-308

[25] P. Grillas Distribution of submerged macrophyte in the Camargue in relation to environmental factors, J. Veg. Sci., Volume 1 (1990), pp. 393-402

[26] S. Bagella; M.C. Caria; E. Farris; R. Filigheddu Phytosociological analyses in Sardinian Mediterranean temporary wet habitats, Fitosociologia, Volume 46 (2009), pp. 11-26

[27] S. Bagella; M.C. Caria; V. Zuccarello Patterns of emblematic habitat types in Mediterranean temporary wetlands, C. R. Biologies, Volume 333 (2010) no. 9, pp. 694-700

[28] D. Boix; J. Sala; X.D. Quintana; R. Moreno-amich Succession of the animal community in a Mediterranean temporary pond, J. N. Am. Benthol. Soc., Volume 23 (2004), pp. 29-49

[29] M. Seminara; D. Vagaggini; F.G. Margaritora Differential responses of zooplankton assemblages to environmental variation in temporary and permanent ponds, Aquat. Ecol., Volume 42 (2008), pp. 129-140

[30] S. Bagella; S. Gascón; M.C. Caria; J. Sala; D. Boix Cross-taxon congruence in Mediterranean temporary wetlands: vascular plants, crustaceans, and coleopterans, Community Ecol., Volume 12 (2011) no. 1, pp. 40-50

[31] R.H. MacArthur; E.O. Wilson The theory of island biogeography, Princeton University Press, New Jersey, USA, 1967

[32] F. March; D. Bass Application of island biogeography theory to temporary tools, J. Fresh. Ecol., Volume 10 (1995), pp. 83-85

[33] D.W. Schneider; T.M. Frost Habit duration and community structure in temporary ponds, J. N. Am. Benthol. Soc., Volume 15 (1996), pp. 64-86

[34] A. Ruhí; E. Chappuis; D. Escoriza; M. Jover; J. Sala; D. Boix; S. Gascón; E. Gacia Environmental filtering determines community patterns in temporary wetlands–a multi taxon approach, Hydrobiologia, Volume 723 (2014), pp. 25-39

[35] A. Ruhí; D. Boix; S. Gascón; J. Sala; D. Batzer Functional and phylogenetic relatedness in temporary wetland invertebrates: current macroecological patterns and implications for future climatic change scenarios, Plos one, Volume 8 (2013), p. e81739

[36] Z. Ghrabi-Gammar; A. Daoud-Bouattour; H. Ferchichi; A.M. Gammar; S.D. Muller; L. Rhazi; S. Ben Saad-Limam Flore vasculaire, endémique et menacée des zones humides de Tunisie, Rev, Ecol. (Terre Vie), Volume 64 (2009), pp. 19-40

[37] G.E. Hollis; C.T. Agnew; R.W. Battarbee; N. Chisnal; R.C. Fisher; R. Flower; F.B. Phethean; S.J. Goldsmith; J. Skinner; A.C. Stevenson; A. Warren; J.B. Wood; R. Fuller; T.W. Parr; A. Tamisier; D. Bredin; G. Rocamora; M. Smart The modeling and management of the internationally important wetland at Garaet el Ichkeul, Tunisia, IWRB, Special publ. 4, Slimbridge, England, 1986

[38] F. Ayache The conservation and development of Tunisian wetlands: a case study of grazing at Ichkeul, University College London, 1990 ([Doctoral thesis])

[39] Z. Ghrabi-Gammar; Z. Lili-Chabaane; M. Zouaghi Evolution de la couverture végétale du Parc national de l’Ichkeul (Tunisie), Rev. Ecol. (Terre Vie), Volume 61 (2006), pp. 317-326

[40] Z. Ghrabi-Gammar; A. Bouattour; S. Ben Saad; Z. Lili-Chabaane; M. Zouaghi Impact of constructions and dry years for evolution of wetland vegetation distribution of Ichkeul National Park, J. Arid Land Stud., Volume 15 (2006), pp. 343-347

[41] M. Ouali; A. Daoud-Bouattour; S. Ettaieb; A.M. Gammar; S. Ben Saad-Limam; Z. Ghrabi-Gammar Le marais de Joumine, Parc National de l’Ichkeul, Tunisie: diversité floristique, cartographie et dynamique de la végétation (1925-2011), Rev. Ecol. (Terre Vie), Volume 69 (2014), pp. 3-23

[42] E. Cosson Note sur la flore de la Kroumirie centrale, Bull. Soc. Bot. Fr., Volume 32 (1885), pp. 5-33

[43] H. Gauthier Recherches sur la faune des eaux continentales d’Algérie et de la Tunisie, Minerva, Alger, Algérie, 1928 ([Thèse])

[44] L. Gauthier-Lièvre Recherches sur la flore des eaux continentales de l’Afrique du Nord, mémoire hors-série, Soc. Hist. Nat. Afr. Nord, Volume 43 (1931), pp. 1-299

[45] G. Pottier-Alapetite Note préliminaire sur l’Isoetion tunisien, Sessions Extr. Soc. Bot. Fr., Volume 99 (1952), pp. 4-6

[46] G. Pottier-Alapetite Intérêt phytogéographique de la région de Sedjenane en Tunisie, Vegetatio, Volume 8 (1958), pp. 176-180

[47] S.D. Muller; A. Daoud-Bouattour; H. Ferchichi; Z. Gammar-Ghrabi; S. Limam-BenSaad; I. Soulié-Marsche Garaâ Sejenane (northern Tunisia): an unknown and threatened biological richness, Eur. Pond Conserv. Network Newslett., Volume 1 (2008), pp. 7-8

[48] S.D. Muller; A. Daoud-Bouattour; B. Amami; H. Ferchichi-Ben Jamaa; J. Ferrandini; M. Ferrandini; Z. Ghrabi-Gammar; P. Grillas; M.L. Pozzo di Borgo; L. Rhazi; I. Soulié-Märsche; S. Ben Saad-Limam Interest of historical data for conservation of temporary pools (P. Fraga i Arguimbau, ed.), International Conference on Mediterranean Temporary Ponds, Proceedings et Abstracts, Consell Insular de Menorca, Recerca, 14. Maó, Menorca, 2009, pp. 339-351

[49] A. Daoud-Bouattour; S.D. Muller; H. Ferchichi-Ben Jamaa; Z. Ghrabi-Gammar; L. Rhazi; A. Mokhtar Gammar; M. Raouf Karray; I. Soulié - Märsche; H. Zouaïdia; G. de Bélair; P. Grillas; S. Ben Saad-Limam Recent discovery of the small pillwort (Pilularia minuta Durieu, Marsileaceae) in Tunisia: hope for an endangered emblematic species of Mediterranean temporary pools?, C. R. Biologies, Volume 332 (2009), pp. 886-897

[50] A. Daoud-Bouattour; S.D. Muller; H. Ferchichi-Ben Jamaa; S. Ben Saad-Limam; L. Rhazi; I. Soulié-Märsche; M. Rouissi; B. Touati; I. Ben Haj Jilani; A.M. Gammar; Z. Ghrabi-Gammar Conservation of Mediterranean wetlands: interest of historical approach, C. R. Biologies, Volume 334 (2011), pp. 742-756

[51] A. Daoud-Bouattour; M. Bottollier-Curtet; H. Ferchichi-Ben Jamaa; Z. Gammar; Ghrabi Gammar; S. Ben Saad-Limam; L. Rhazi; S.D. Muller Effects of hydrology on recruitment of Pilularia minuta Durieu (Marsileaceae), an endangered plant of Mediterranean temporary pools, Aquat. Bot., Volume 112 (2014), pp. 76-83

[52] H. Ferchichi-Ben Jamaa Fonctionnement, biodiversité, structure et dynamique des communautés végétales des zones humides temporaires de la région des Mogods, Tunisie septentrionale, Université de Tunis el Manar, Tunis and Université Montpellier-2, 2010 ([Doctoral thesis])

[53] H. Ferchichi-Ben Jamaa; S.D. Muller; Z. Ghrabi-Gammar; L. Rhazi; I. Soulié-Märsche; A.M. Gammar; M. Ouali; S. Ben Saad-Limam; A. Daoud-Bouattour Influence du pâturage sur la structure, la composition et la dynamique de la végétation de mares temporaires méditerranéennes (Tunisie septentrionale), Rev. Ecol. (Terre Vie), Volume 69 (2014), pp. 196-213

[54] H. Ferchichi-Ben Jamaa; S.D. Muller; A. Daoud-Bouattour; Z. Ghrabi-Gammar; L. Rhazi; I. Soulié-Märsche; M. Ouali; S. Ben Saad-Limam Structures de végétation et conservation des zones humides temporaires méditerranéennes : la région des Mogods (Tunisie septentrionale), C. R. Biologies, Volume 333 (2010), pp. 265-279

[55] H.J. Dumont; P. Laureys; J. Pensaert Anostraca, Conchostraca, Cladocera and Copepoda from Tunisia, Hydrobiologia, Volume 66 (1979), pp. 259-274

[56] S. Turki; S. Turki Copepoda and Branchiopoda from Tunisian temporary waters, Int. J. Biodiv. Conserv., Volume 2 (2010), pp. 86-97

[57] A. Sicilia; F. Marrone; R. Sindaco; S. Turki; M. Arculeo Contribution to the knowledge of Tunisian amphibians: notes on distribution, habitat features and breeding phenology, Herpetol. Notes, Volume 2 (2009), pp. 107-132

[58] J. Ben Hassine; S. Nouira Répartition géographique et affinités écologiques des Amphibiens de Tunisie, Rev. Ecol. (Terre Vie), Volume 67 (2012), pp. 437-457

[59] J. Ben Hassine; S. Nouira The amphibians of Tunisia: biodiversity, distribution, status and majors threats, FrogLog, Volume 101 (2012), pp. 32-34

[60] J. Ben Hassine; A. Kassabi; S. Nouira Pleurodeles nebulosus (Guichenot, 1850) en Tunisie : répartition, habitat, reproduction et statut, Bull. Soc. Herpetol. Fr., Volume 144 (2013), pp. 51-66

[61] F. Angel Faune de France. 45. Reptiles et amphibiens, Lechevalier, Paris, 1946

[62] H. Tachet; P. Richoux; M. Bournaud; P. Usseglio-Polatera Invertébrés d’eau douce: systématique, biologie, écologie, CNRS Éditions, Paris, 2000

[63] I.M. Smith; D.R. Cook; B.P. Smith Water mites (Hydrachnida) and other arachnids (J.H. Thorp; A.P. Covich, eds.), Ecology and classification of North American freshwater invertebrates, Academic Press, San Diego, CA, USA, 2001, pp. 551-659

[64] J. Braun-Blanquet Plant sociology, the study of plant community, McGraw Hill Book, New York, 1932 ([translation by H.S. Conard, G.D. Fuller])

[65] E. Le Floc’h; L. Boulos; E. Véla Flore de Tunisie. Catalogue synonymique commenté, Banque nationale de gènes, ministère de l’Environnement et du Développement durable, Tunis, 2008

[66] S. Bagella; M.C. Caria Diversity and ecological characteristics of vascular flora in Mediterranean temporary pools, C. R. Biologies, Volume 335 (2012), pp. 69-76

[67] E.C. Pielou An introduction to mathematical ecology, Wiley, New York, 1969

[68] A.D. Jassby; C.R. Goldman A quantitative measure of succession rate and its application to the phytoplankton of lakes, Am. Nat., Volume 108 (1974), pp. 688-693

[69] R Development Core Team R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria, 2008 http://www.R-project.org

[70] K.R. Clarke; R.M. Warwick Change in marine communities: an approach to statistical analysis and interpretation, Plymouth Marine Laboratory, Plymouth, 1994

[71] K.R. Clarke Non-parametric multivariate analyses of changes in community structure, Aust. J. Ecol., Volume 18 (1993), pp. 117-143

[72] K.R. Clarke; R.N. Gorley PRIMER v6: user manual, PRIMER-E, Plymouth UK, 2006

[73] N. García; A. Cuttelod; D. Abdul Malak The status and distribution of freshwater biodiversity in Northern Africa. The IUCN Red List of Threatened Species–Regional Assessment, IUCN, Gland, Switzerland, Cambridge, UK & Malaga, Spain, 2010

[74] C. Boutin; L. Lesne; A. Thiery Écologie et typologie de quelques mares temporaires à Isoetes d’une région aride du Maroc occidental, Ecol. Mediterr., Volume 8 (1982), pp. 31-56

[75] G. Metge Étude des écosystèmes hydromorphes (dayas et merjas) de la meseta occidentale marocaine, Université Aix-Marseille-III, Marseille, France, 1986 ([Doctoral thesis])

[76] J. Giudicelli; A. Thiery La faune des mares temporaires, son originalité et son intérêt pour la biodiversité des eaux continentales méditerranéennes, Ecol. Mediterr., Volume 24 (1998), pp. 135-143

[77] W. Beukema; P. De Pous; D. Donaire-Barroso; S. Bogaerts; J. Garcia-Porta; D. Escoriza; O.J. Arribas; E.H. El Mouden; S. Carranza Review of the systematics, distribution, biogeography and natural history of Moroccan amphibians, Zootaxa, Volume 3661 (2013), pp. 1-60

[78] M. Bazzanti; S. Baldoni; M. Seminara Invertebrate macrofauna of a temporary pond in Central Italy: composition, community parameters and temporal succession, Arch. Hydrobiol., Volume 137 (1996), pp. 77-94

[79] M. Bazzanti; V.F. Della Bella Functional characteristics of macroinvertebrate communities in Mediterranean ponds (Central Italy): influence of water permanence and mesohabitat type, Ann. Limnol-Int. J. Lim., Volume 45 (2009), pp. 29-39

[80] J.L. Culioli; J. Foata; C. Mori; A. Orsini; B. Marchand Temporal succession of the macroinvertebrate fauna in a Corsican temporary pond, Vie Milieu, Volume 56 (2006), pp. 215-221

[81] D. Boix; J. Sala; R. Moreno-Amich The faunal composition of Espolla pond (NE Iberian peninsula): the neglected biodiversity of temporary waters, Wetlands, Volume 21 (2001), pp. 577-592

[82] D. Escoriza; D. Boix Assessing the potential impact of an invasive species on a Mediterranean amphibian assemblage: a morphological and ecological approach, Hydrobiologia, Volume 680 (2012), pp. 233-245

[83] B. Dussart Limnologie. L’étude des eaux continentales, Gauthier-Villars, Paris, 1966

[84] N. Bennas; D. Sanchez-Fernandez; P. Abellan; A. Millan Analyse de la vulnérabilité des coléoptères aquatiques dans la rive sud méditerranéenne : cas du Rif Marocain, Ann. Soc. Entomol. Fr. (n.s.), Volume 45 (2009), pp. 309-320

[85] S. Touaylia; M. Bejaoui; M. Boumaiza; J. Garrido Nouvelles données sur la famille des Hydraenidae Mulsant, 1844, de Tunisie (Coleoptera), Bull. Soc. Entomol. Fr., Volume 114 (2009), pp. 317-326

[86] M. Korbaa; M. Bejaoui; M. Boumaiza Variation spatio-temporelle de la structure de l’éphéméroptérofaune dans l’oued Sejnane (Ichkeul, Tunisie septentrionale), Rev. Sci. Eau, Volume 22 (2009), pp. 373-381

[87] A. Thiery Contribution à la connaissance des Hétéroptères du Maroc : les Hétéroptères aquatiques du Haut-Atlas occidental, Bull. Inst. Scient. Rabat, Volume 5 (1981), pp. 13-34

[88] M. Boumaiza; E. Martinez-Ansemil; N. Giani Les oligochètes et Aphanoneura des eaux courantes de Tunisie. I - données faunistiques, Ann. Limnol., Volume 22 (1986), pp. 231-237

[89] A. Thiery Ponte et ultrastructure de l’oeuf chez Triops granarius Lucas (Crustacea, Notostraca) : adaptations à l’assèchement de l’habitat, Verh. Int. Verein. Limnol., Volume 22 (1985), pp. 3024-3028

[90] A. Thiery; J. Brtek; C. Gasc Cyst morphology of European branchiopods (Crustacea: Anostraca, Notostraca, Spinicaudata, Laevicaudata), Bull. Mus. Natl. Hist. Nat. Paris série, Volume 4 (1995) no. 17, pp. 107-140

[91] A. Thiery Étude des communautés d’invertébrés aquatiques dans différents biotopes des marais du Plan du Bourg (Bouches-du-Rhône, France), Université d’Aix-Marseille-III, France, 1978 ([3rd cycle thesis])

[92] A. Thiery Influence de l’assèchement estival sur le peuplement d’insectes aquatiques d’un marais saumâtre temporaire en Crau (Bouches-du-Rhône), Ann. Limnol., Volume 15 (1979), pp. 181-191

[93] A. Thiery Les crustacés branchiopodes Anostraca, Nodostraca et Concostracha des milieux limniques temporaires (Dayas) au Maroc. Taxonomie, biogéographie, écologie, Université d’Aix Marseille-III, France, 1987 ([Doctoral thesis])

[94] A. Thiery; R. Barthelemy; A. Baud; C. Cuoc Inventaire et expertise portant sur les invertébrés aquatiques, l’analyse de l’eau et les enjeux patrimoniaux des lacs de Bonne Cougne, Redon et Gavoti (Var), DIREN/CEEP, Rapport NATURA 2000, 2002

[95] A. Arab; S. Lek; A. Lounaci; Y.S. Park Spatial and temporal patterns of benthic invertebrate communities in an intermittent river (North Africa), Ann. Limnol-Int. J. Lim., Volume 40 (2004), pp. 317-327

[96] S. Carranza; E. Wade Taxonomic revision of Algero-Tunisian Pleurodeles (Caudata: Salamandridae) using molecular and morphological data. Revalidation of the taxon Pleurodeles nebulosus (Guichenot, 1850), Zootaxa, Volume 488 (2004), pp. 1-24

[97] N.H. Collinson; J. Biggs; A. Corfield; M.J. Hodson; D. Walker; M. Whitfield; P.J. Williams Temporary and permanent ponds: an assessment of the effects of drying out on the conservation value of aquatic macroinvertebrate communities, Biol. Conserv., Volume 74 (1995), pp. 125-133

[98] T.L. Tarr; M.J. Baber; K.J. Babbitt Macroinvertebrate community structure across a wetland hydroperiod gradient in southern New Hampshire, USA, Wetlands Ecol. Manage., Volume 13 (2005), pp. 321-334

[99] D. Boix; J. Sala; S. Gascón; A.M. Martinoy; J. Gifre; S. Brucet; A. Badosa; R. López-Flores; X.D. Quintana Patterns of composition and species richness of crustaceans and aquatic insects along environmental gradients in Mediterranean wetlands, Hydrobiologia, Volume 597 (2008), pp. 53-69

[100] P. Fraga i Argimbau Vascular flora associated to Mediterranean temporary ponds on the islands of Minorca, Anales Jard. Bot. Madrid, Volume 65 (2008), pp. 393-418

[101] C. Pinto-Cruz; J.A. Molina; M. Barbour; V. Silva; M.D. Espírito-Santo Plant communities as a tool in temporary ponds conservation in SW Portugal, Hydrobiologia, Volume 634 (2009), pp. 11-24

[102] L. Rhazi; P. Grillas; E.R. Saber; M. Rhazi; L. Brendonck; A. Waterkeyn Vegetation of Mediterranean temporary pools: a fading jewel?, Hydrobiologia, Volume 689 (2012), pp. 23-36

[103] G. de Bélair Dynamique de la végétation de mares temporaires en Afrique du Nord (Numidie Orientale, NE Algérie), Ecol. Mediterr., Volume 31 (2005), pp. 1-18

[104] R. Nègre Notes sur la végétation de quelques dayas des Jbilets orientaux et occidentaux, Bull. Soc. Sci. Nat. Maroc, Volume 36 (1956), pp. 229-241

[105] B. Amami Dynamiques temporelles à court et long terme d’une mare temporaire méditerranéenne et implications pour la conservation (Maroc occidental), Université Hassan II Aïn Chock, Casablanca and Université de Montpellier, 2010 ([Doctoral thesis])

[106] S. Bouahim; L. Rhazi; B. Amami; N. Sahib; M. Rhazi; A. Waterkeyn; A. Zouahri; F. Mesleard; S.D. Muller; P. Grillas Impact of grazing on the species richness of plant communities in Mediterranean temporary pools (western Morocco), C. R. Biologies, Volume 333 (2010), pp. 670-679

[107] F. Médail; H. Michaud; J. Molina; G. Paradis; R. Loisel Conservation de la flore et de la végétation des mares temporaires dulçaquicoles et oligotrophes de France méditerranéenne, Ecol. Mediterr., Volume 24 (1998) no. 2, pp. 119-134

[108] V. Della Bella; M. Bazzanti; M.G. Dowgiallo; M. Iberite Macrophyte diversity and physico-chemical characteristics of Tyrrhenian coast ponds in central Italy: implications for conservation, Hydrobiologia, Volume 597 (2008), pp. 85-95

[109] P.H. Zedler The ecology of southern California vernal pools: a community profile, U.S. Fish and Wildlife Service, Washington, DC, USA, Biol. Report 85 (7.11), 1987

[110] P. Grillas; J. Roché Végétation des marais temporaires, écologie et gestion, conservation des zones humides méditerranéennes 8, Tour du Valat, Le Sambuc, 1997

[111] P. Quézel La végétation des mares transitoires à Isoetes en région méditerranéenne, intérêt patrimonial et conservation, Ecol. Mediterr., Volume 24 (1998), pp. 111-117

[112] B. Gopal Vegetation dynamics in temporary and shallow freshwater habitats, Aquat. Bot., Volume 23 (1986), pp. 391-396

[113] U. Deil A review on habitats, plant traits and vegetation of ephemeral wetlands - a global perspective, Phytocoenologia, Volume 35 (2005), pp. 533-705

[114] J. Lahr; A.O. Diallo; K.B. Ndour; A. Badji; P. Diouf Phenology of invertebrates living in a sahelian temporary pond, Hydrobiologia, Volume 405 (1999), pp. 189-205

[115] D. Boix; J. Sala; S. Gascón; A. Ruhí; X.D. Quintana Structure of invertebrate assemblages: contribution to the ecological functioning of the Mediterranean temporary ponds (P. Fraga i Arguimbau, ed.), International Conference on Mediterranean Temporary Ponds, Proceedings & Abstracts, Consell Insular de Menorca, Recerca, 14. Maó, Menorca, Spain, 2009, pp. 151-187

[116] M. Jeffries Invertebrate communities and turnover in wetlands ponds affected by drought, Freshw. Biol., Volume 32 (1994), pp. 603-612

[117] G.A. Wellborn; D.K. Skelly; E.E. Werner Mechanisms creating community structure across a fresh water habitat gradient, Annu. Rev. Ecol. Syst., Volume 27 (1996), pp. 337-363

[118] R.T. Brooks Annual and seasonal variation and the effects of hydroperiod on benthic macroinvertebrates of seasonal forest (“vernal”) ponds in Central Massachusetts, USA, Wetlands, Volume 20 (2000), pp. 707-715

[119] G.B. Wiggins; R.J. Mackay; I.M. Smith Evolutionary and ecological strategies of animals in annual temporary pools, Arch. Hydrobiol., Volume 58 (1980), pp. 97-206

[120] B.E. Taylor; D.A. Leeper; M.A. Mc Clure; A.E. De Biase Carolina Bays: ecology of aquatic invertebrates and perspectives on conservation (D. Batzer; R.B. Rader; S.A. Wissinger, eds.), Invertebrates in freshwater wetlands of North America, 1999, pp. 167-196

[121] M. Hansen Coleoptera Hydrophiloidea and Hydraenidae, water scavengers beetles (A. Nilsson, ed.), The aquatic insects of North Europe, Vol. 1, Apollo Books, Denmark, 2005, pp. 146-173

[122] A.N. Nilsson Coleoptera Dytiscidae, diving water beetles (A. Nilsson, ed.), The Aquatic Insects of North Europe, Vol. 1, Apollo Books, Denmark, 2005, pp. 146-173

[123] A.N. Nilsson Coleoptera Gyrinidae, whirligig beetles (A. Nilsson, ed.), The Aquatic Insects of North Europe, Vol. 1, Apollo Books, Denmark, 2005, pp. 146-173

[124] A.N. Nilsson Coleoptera Haliplidae, crawling water beetles (A. Nilsson, ed.), The aquatic insects of North Europe, Vol. 1, Apollo Books, Denmark, 2005, pp. 146-173

[125] A.N. Nilsson Coleoptera, introduction (A. Nilsson, ed.), The aquatic insects of North Europe, Vol. 1, Apollo Books, Denmark, 2005, pp. 146-173

[126] M.S. Spencer; L. Blaustein; S.S. Schwartz; J.E. Cohen Species richness and the proportion of predatory animal species in temporary freshwater pools: relationships with habitat size and permanence, Ecol. Lett., Volume 2 (1999), pp. 157-166

[127] A. Eitam; L. Blaustein; K. Van Damme; H.J. Dumont; K. Martens Crustacean species richness in temporary pools: relationships with habitat traits, Hydrobiologia, Volume 525 (2004), pp. 125-130

[128] R.H. Mcarthur; E.O. Wilson The theory of island biogeography, Princeton University Press, NJ, USA, Princeton, 1967

[129] L.E. Barnes The colonization of ball-clay ponds by macroinvertebrates and macrophytes, Freshw. Biol., Volume 13 (1983), pp. 561-578

[130] L.E. Friday The diversity of macroinvertebrate and macrophyte communities in ponds, Freshw. Biol., Volume 18 (1987), pp. 87-104

[131] E. Jeppesen; J.P. Jensen; M. Søndergaard; T. Lauridsen; F. Landkildehus Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient, Freshw. Biol., Volume 45 (2000), pp. 201-218

[132] N.H. Euliss; D.M. Mushet Influence of agriculture on aquatic invertebrate communities of temporary wetlands in the prairie pothole region of North Dakota, USA, Wetlands, Volume 19 (1999), pp. 578-583

[133] S.M. Borthwick Impacts of agricultural pesticides on aquatic invertebrates inhabiting prairie wetlands, Colorado State University, USA, 1988 ([M.S. Thesis])

[134] J. Dvorack; E.P.G. Best Macroinvertebrates communities associated with the macrophytes of Lake Vechten: structural, functional relationships, Hydrobiologia, Volume 95 (1982), pp. 115-126

[135] D.F. Lodge Macrophyte–gastropod associations: observations and experiments on macrophyte choice by gastropods, Freshw. Biol., Volume 15 (1985), pp. 695-708

[136] J.-L. Dommanget Étude faunistique et bibliographique des Odonates de France, Inventaires de faune et de flore, Museum national d’histoire naturelle/Secrétariat de la faune et de la flore, Paris, 1987

[137] S. Angélibert; P. Marty; R. Céréghino; N. Giani Seasonal variations in physico-chemical characteristics of ponds: implications for biodiversity conservation, Aquat. Conserv. Mar. Freshwat. Ecosyst., Volume 14 (2004), pp. 439-456

[138] K.L. Heck; J.L.B. Crowder Habitat structure and predator-prey interactions in vegetated aquatic systems (E. McCoy; S.S. Bell; H.R. Mushinsky, eds.), Habitat structure: the physical arrangement of objects in space, Chapman and Hall, London, 1991, pp. 281-295

[139] E. Jeppesen; J.P. Jensen; M. Søndergaard; T. Lauridsen; L.J. Pedersen; L. Jensen Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth, Hydrobiologia, Volume 342 (1997), pp. 151-164


Comments - Policy