Richness and structure of plant communities in temporary pools from western

Morocco: influence of human activities

Laıla Rhazi1,*, Mouhssine Rhazi2,3, Patrick Grillas2 & Driss El Khyari11Universite Hassan II Faculte des Sciences Aın Chock Laboratoire de Biologie et de Physiologie Vegetale, BP, 5366,

Maarif Casablanca, Maroc2Station Biologique de la Tour du Valat, Le Sambuc, Arles, 13200, France3Universite Aix Marseille III, Faculte des Sciences et Techniques Saint Jerome, 13397, Marseille Cedex 20, France(*Author for correspondence: E-mail: lrhazi@hotmail.com)

Key words: temporary pool, Morocco, human activities, species richness, flora, plant communities

Abstract

Temporary pools are numerous in coastal plains of Atlantic Morocco and have a rich and diverse flora.These habitats are increasingly under pressure by man impact through grazing by domestic livestock andthe development of annual crops in their catchments. The objectives of this work were to evaluate thespecies richness and the species composition of the vegetation of a sample of 30 pools in this region, in orderto assess the structure of the vegetation within pools and to evaluate the role of environmental andanthropogenic factors in their richness and species composition. The results highlighted the species richnessof the pools with 300 species found among which annual species were heavily dominant. The structure ofthe vegetation varied within pools according to a topographical/flooding gradient and between pools inrelation with the land use in the surrounding areas. Three vegetation belts were recognized from the centreto the periphery of the pool. The total species richness per pool was not found significantly related toenvironmental or anthropogenic factors. The species characteristics of the pools were found mostly in thecentre and their number affected by hydrological factors and land use in the pool and in the surroundingareas. The species characteristics of woodland habitats and of agriculture crops were found mostly in theperipheral zone. Temporary pools maintain specific communities of both aquatic and amphibious species,probably because of the selection induced by water level variations. The peripheral zone, although oftendominated by terrestrial species, is clearly interpreted as part of the pool. It contains amphibious specieshighly characteristic of the pool for which the irregular flooding is a key environmental factor whichdecreases competition.

Introduction

Temporary pools (locally called ‘‘dayas’’ in Mor-occo), are depressions that fill with water duringthe rainy season and dry out most frequently alongspring or early summer. There pools are numerousin the Northwest of Morocco (Thiery, 1987) andthey are unique habitats, especially in terms of thenumber of rare or endangered plant and animalspecies they harbour (Metge, 1986; Rhazi et al.,2001a). The diversity of the vegetation of these

temporary pools has been long recognized inEurope and in North-Africa (e.g. Braun-Blanquet,1936; Chevassut & Quezel, 1956; Metge, 1986).The biological diversity of the temporary pools hasbeen maintained over the centuries although sub-jected to extensive human activities. More recentlythese pools have been facing increasing humanpressure by urban, industrial and agriculturaldevelopment (Quezel, 1998). In addition to thethreat of destruction by infrastructural develop-ment, temporary pools are subject to increasing

Hydrobiologia (2006) 570:197–203 � Springer 2006J.M.Caffrey,A.Dutartre, J.Haury,K.J.Murphy&P.M.Wade (eds),Macrophytes inAquaticEcosystems:FromBiology toManagementDOI 10.1007/s10750-006-0180-6

human pressure mainly due to agriculture anddiverse disturbances ranging from the drainage ofthe pools to the extraction of fine sediments orgraveling. These changes could lead to changes inthe species richness of the vegetation of the tem-porary pools (Hill & Keddy, 1992; Rhazi et al.,2001a; Crossle & Brock, 2002) through diversemechanisms (e.g. trampling, erosion, filling-in,selective grazing, nutrient enrichment andpesticide intrusion).

The objectives of this study were (1) to identifythe organisation of the pool vegetation (2) to eval-uate the species richness and the effects of environ-mental variables and human activities on thisfloristic richness of the pools (3) to quantify thecontribution of neighbouring ecosystems to thevegetation.

Description of the study sites

The pools that were studied are located in theprovince of Benslimane (33� 38¢ N, 7� 07¢ W,268, 000 ha), which is situated between Rabat andCasablanca. This region has a Mediterraneanclimate, sub-humid in the coastal part and semi-arid in the continental part. Annual rainfall is462 mm, concentrated mainly in winter (Zidane,1990).

Temporary pools, which are numerous in thisregion, make up 2% of the total area of theprovince (Rhazi, 1990). They are found in twomain types of habitat: cork oak woodland andagricultural land. They vary in size, depth, natureof substrate and length of submersion period.These pools are endoreic and fed by water onlythrough direct rainfall and runoff.

Materials and methods

In the Benslimane Province 30 pools were selectedby means of a stratified sampling system based onthe bio-climate (sub-humid/semi-arid), the geology(quartzite, sandstone, schist, limestone, alternatingsandstone and pelite, alternating sandstoneand quartzite) and location (in woodland or anagro-pastoral environment). Seven pools were sit-uated in woodland and 23 in agricultural envi-ronment. These pools were visited in spring and

summer 1997–1998. During these visits 330 phyto-ecological surveys were carried out along transectsthrough homogenous vegetation units. Thesesurveys consisted in a vegetation releve, (notingthe cover and the growth form for each species),the measure of environmental variables (texture ofthe soil, the parent rock, the bio-climate, themaximum depth of water, the diameter of thewater body and the duration of flooding) and ofman-use variables, (the presence of drains, theoccurrence or not of domestic grazing, the land useby grazing or annual crops of the area surroundingthe pool). The percentage of each type of growthform for all 30 pools and the total species richnessper pool were then calculated. The species found inthe pools were split in 4 groups on the basis of theliterature (Jahandiez & Maire, 1931–1934; Maire,1952–1987; Fennich, 1990; Zidane, 1990; Rhazi etal., 2001a): Pool-species, Forest-species, Agricul-ture-species and Ubiquitous-species. Each groupwas made of species recognized as characteristicsof one type of habitat except the last one (Ubiq-uitous) gathering opportunistic species found in alltypes of habitats. The contribution of the speciesfrom each group to the total richness of the poolswas quantified. The effect of the environmentalvariables on the total species richness per pool wastested by linear regression and the number ofspecies per group (Pool-, Forest- and Agriculture-species) was tested by linear regression and vari-ance analysis (ANOVA) followed by comparisonof means using the Tukey–Kramer test. The rich-ness per vegetation belt in typical species of pools,woodland, agricultural land and the ubiquitousgroup was tested by v2. A correspondence analysiswas conducted using the vegetation data from allthe 330 vegetation releves made at the 2 samplingdates. The CA was conducted with only 200species retaining only species that were present inmore than 6 releves.

Results

Growth form

A total of 300 species was found during the 2 fieldvisits in the 30 pools studied. Among the variousgrowth form (Fig. 1) a very clear predominance of

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therophytes (70%) appeared whereas other growthforms were found uncommon.

Organisation of the vegetation

The first 2 axes of the CA (Fig. 2) explainedrespectively 25.8% and 19% of the total vari-ance. Axis 1 separated the aquatic species(Ranunculus peltatus, Callitriche brutia, Glyceriafluitans, etc.) from the terrestrial (e.g., Leontodontaraxacoides, Plantago coronopus, Trifoliumcampestre). Axis 2 separated the Forest-species(e.g., Cistus spp, Cynara humilis, Asphodelus mi-crocarpus) from the Agriculture-species (e.g., Si-lene gallica, Ormenis mixta, Raphanusraphanistrum). The coordinates of the orthogonalprojection of the vegetation releves on axis 1were significantly correlated to the maximumdepth of the water recorded in these surveys(r2 = 0.53 ; p < 0.05 ; n = 330). Axis 1 wastherefore interpreted as an hydrological gradient.This gradient along axis 1 (Fig. 2) correspondsto a topographical gradient from the externalmargin of the pools (terrestrial), an amphibiouszone and the inner (aquatic) part of the pool.These three zones were designated as ‘‘vegetationbelts’’.

Species richness

The total species richness per pool (Table 2a, b) wasnot significantly correlated (p > 0.05) with the size

of the pool (diameter of the water body), maximumwater depth, nor soil characteristics, nor anthrop-ozoogenic factors nor type of bio-climate(p > 0.05).

Within pools the number of species from thePool-, Forest- Agriculture- and Ubiquitous-groups were significantly different between the 3vegetation belts (Table 1, v2 = 218.94 ;p < 0.0001). The inner and intermediate beltscontained more Pool-species than the peripheralbelt which was richer in species from the Wood-land-, Agriculture and Ubiquitous-groups (Table 1).

The number of species from the Pool-groupwas significantly different according to the type ofenvironment surrounding the pools. The numberof Pool-species was higher within forested envi-ronment (28.00±1.57) than for pools withinagricultural environment (23.26±1.13). Thenumber of Pool-species was also significantlyhigher for pools in a grazed environment (forestand pastures) (26.38±1.12) than for pools in anenvironment made of fields of annual crops(19.66±0.95) (Table 2a,). The number of Pool-species was significantly correlated with thehydrological factors (depth, diameter of the waterbody, Duration of flooding, Table 2b) but notwith other environmental factors. Similarly thenumber of Forest-species was significantly differ-ent according to the land use surrounding thepool. It was higher for pools within a forestedenvironment (15.14±2.38) than for pools withinan agricultural environment (7.78±0.76). Thenumber of Forest-species was not correlated withany other environmental and human factors(Table 2a, b).

The number of Agriculture-species (Table 2)was significantly higher in pools within an agri-cultural environment (21.91±1.61) than forpools established in forests (13.42±1.81). Therewas a significant negative correlation between thenumber of Agriculture-species and the diameterof the water. The number of Agriculture-specieswas higher in drained (25.91±2.11) than non-drained pools (17.44±1.53). The richness inspecies characteristic of agricultural lands wasnot significantly correlated with other environ-mental factors (p > 0.05) (Table 2a, b).

The richness in Ubiquitous species was notsignificantly correlated to the type of land usesurrounding the pools (p > 0.05) (Fig. 3).

g , p g p

0

20

40

60

80

100

Cr PhTh ChHGrowth form

Per

cent

age

Th : therophytes, Cr : cryptophytes H : hemicryptophytesCh : chamaephytes Ph : phanerophytes

Figure 1. Relative frequency of the various growth forms of the

plant species found on the 30 pools (bars = SD).

199

Discussion and conclusions

The predominance of annuals (70%) in the flora ofthe pools is a result of adaptation to harsh envi-ronmental conditions (Medail et al., 1998). Theunpredictability of the filling and drying-up peri-ods of the pools, which is linked to the Mediter-ranean climate, the occurrence of severe droughtsthat alternate with floods, and the intra- and inter-annual variations in water depth, leads to theselection of short-cycle species which invest insexual reproduction to the detriment of theirvegetative development. The predominance of

therophytes has also been observed byMedail et al.(1998) for pools in France and by Zedler (1987) forvernal pools in California. The survival of speciesfrom one year to another depends mainly ongermination from the seed bank (e.g. Bonis et al.,1995; Rhazi et al., 2001b, Brock & Crossle, 2002).

The vegetation of the pools investigated (CA) isarranged in 3 belts that follow the hydrologicalgradient (axis F1) : inner, intermediate andperipheral belts dominated by aquatic, amphibiousand terrestrial species respectively. A similarorganisation of vegetation has been observed inthe vernal pools of California (Bauder, 2000). In

p ( )

F2

F1

Ranunculus peltatus •

Callitriche brutia •

Glyceria fluitans •

• Carlina racemosa

Illecebrum verticillatum •

Lotus hispidus •

• Trifolium campestre

Lythrum borysthenicum •

Isoetes velata •

• Leontodon taraxacoides

Silene gallica •

Ormenis mixta •

Raphanus raphanistrum • • Medicago polymorpha

• Bromus intermedius

Papaver rhoeas

Cistus salviifolius •

Cistus monspeliensis •

Cynara humilis •

Asphodelus microcarpus •

Ornithopus compressus •

Juncus bufonius •

• Euphorbia exigua

• Tolpis barbata

• Trifolium tomentosum

• Trifolium isthmocarpum

• Rumex bucephalophorus

• Plantago coronopus

AQUATIC

TERRESTRIAL

AMPHIBIOUS

AGRICULTURAL

FOREST

• Agrostis salmantica

Figure 2. Plot ½ of the correspondence analysis (CA) on the floristic survey of the 30 pools. Species oflimited contribution, located in

the centre of the diagram, are not shown to facilitate interpretation of the graph.

Table 1. Richness in typical species of pools, forests, agricultural land and the ubiquitous group in the three vegetation belts

Species Pool Forest Agricultural Ubiquitous

Inner Belt 15 0 2 1

Intermediate Belt 59 2 3 1

Peripheral Belt 9 55 95 58

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wetlands this zonation has been attributed to thedistribution of species according to their floodingtolerance (Brewer et al., 1997; Lenssen et al.,1999). However in temporary pools in dry regionsthe intensity of summer drought could also play animportant additional role in this zonation (Rhaziet al., 2001b). This structuring of the vegetation inbelts has been found also in the seed stock in thesetemporary pools (Rhazi et al., 2001b).

The inner and intermediate belts contain typi-cal pool species (Table 1) whose richness is linkedto hydrological factors but independent of pedo-

logical and geological factors. These typical poolspecies are more abundant in pools located inwoodland than in those located in agriculturalenvironments. This result suggests a negative effectof the agricultural practices in the neighbouringareas, possibly through the accumulation viarunoff of pesticides or nutrients (nitrates and sul-phates) from fertilizers (Anderson & Vondracek,1999; Rhazi et al., 2001a). These typical poolspecies do not appear to be affected to the sameextent by grazing and even by the drainage of thepools.

Table 2. (a) Results of variance analyses (ANOVA) of the total species richness, the richness in species characteristic of Pools, Forests

and Agricultural land according to the land use (woodland or agriculture) outside the pool, the type of utilisation of the pool

(agriculture or pasture), the drainage, the bio-climate, the nature of the rock and the texture of the surface soil horizon. (b) Results of

linear regressions between the total species richness, the number of species characteristic of Pools, Forests and Agricultural land and

the maximum depth of water, the diameter of the water surface recorded in spring, the length of the submersion period (n = 30, result

significant when p < 0.05)

Total Richness Pool species Forests species Agriculture species

(a) ddl F p ddl F p ddl F p ddl F p

Land use (outside) 1 3.29 0.080 1 4.43 0.044 1 15.22 0.001 1 18.70 0,018

Utilisation (inside) 1 1.29 0.264 1 13.3 0.001 1 2.73 0.109 1 2.12 0.150

Drainage 1 2.85 0.102 1 1.58 0.210 1 0.01 0.940 1 11.03 0.003

Bio-climate 1 0.12 0.720 1 0.81 0.370 1 0.46 0.500 1 0.09 0.756

Nature of the Rock 5 1.44 0.240 5 1.35 0.270 5 0.24 0.940 5 2.17 0.090

Texture 5 1.93 0.120 5 1.31 0.290 5 3.70 0.120 5 1.06 0.400

(b) R2 p R2 p R2 p R2 p

Maximum Depth of Water 0.03 0.370 0.31 0.001 0.01 0.490 0.08 0.140

Diameter of Water 0.01 0.790 0.22 0.009 0.02 0.440 0.16 0.030

Length of Submersion 0.02 0.480 0.17 0.023 0.01 0.530 0.03 0.320

0%

20%

40%

60%

80%

100%

APools

ubiquitous

agricultural

forest

pool

W

Figure 3. Percentage of species typical of pools, forests, agricultural land and ubiquitous in pools with agricultural catchments (A) and

in pools with woodland catchments (w).

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The ecotonal peripheral belt is the richest(Table 1) which is attributed to lower hydromor-phy (e.g. Gough &Grace, 1998). The species of thisbelt can be found mostly in to the Ubiquitous-,Forest- and Agriculture-species but contain alsoamphibious Pool species. The external belt thusbears the marks of neighbouring woodland andagricultural ecosystems, which contribute 14% and20% respectively to the total richness of the pools.The invasion of the pool margins by species fromsurrounding terrestrial environments is facilitatedby the wind and the frequent movements of live-stock (Metge, 1986) capable of transporting seedsfrom one place to another. The terrestrial speciesfind suitable habitats in the peripheral belt takingadvantage of the low frequency of flooding. How-ever irregular flooding seems to be an importantenvironmental factor selecting annual species. Thefirst year following a high water level is character-ised by a high proportion of annuals in the vege-tation which decreases gradually during thefollowing years (Rhazi et al., 2001b and unpub-lished data). In the centre of the pool, the longsubmersion period and the diameter of the watersurface prevents successful establishment by ter-restrial species from the margins, thus enabling thepool to maintain its typical and original aquaticand amphibious flora. According to Metge (1986),this raises a problem concerning the limits of theseecosystems: should the peripheral belt be includedin the pool ecosystem, or is it an interface betweenthe aquatic environment and surrounding terres-trial environments? The results of this study, to-gether with previous studies (Rhazi et al., 2001a),indicate that the peripheral belt should be includedin the pool ecosystem. Although the species com-position of the peripheral belt can exhibit highsimilarity with adjacent terrestrial habitats, thespecies composition is strongly affected and aqua-tic and amphibious species dominate. Furthermorethis belt is the most favoured habitat for rare andunstable species which are characteristics of theMediterranean temporary pools (e.g. Damasoniumstellatum, Pilularia minuta or Elatine brochoni).These species although abundant in the seed stocks(Rhazi et al., 2001b) appears only during the mostwet years when they beneficiate from the suitablewater regime and the displacement by flood ofcompetitive species.

Acknowledgements

We would like to thank D. Titolet, M. Ibn Tattouand J. Mathez for their help in plant determina-tion, and L. Zidane, J. Chninigue, S. Hassoun, andM.F. Fennich for their assistance in the field andA. Charpentier for help at various stage of dataanalysis and writing up.

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