LIFE STRATEGIES OF SEMI- : MECHANISMS OF DISPERSAL AND REPRODUCTIONIN THE THERMOMEDITERRANEAN SHRUBLAND COMMUNITY ANABASIO-EUZOMODENDRETUM BOURGAEANI

by ISABELLHENSEN'

Resumen HENSEN, I. (1999). Las estrategias de vida de las plantas semidesérticas: mecanismos de dispersión y reproducción en la comunidad de matorral termomediterráneo Anabasio- Euzomodendretum bourgaeani. Anales Jard. Bot. Madrid 57(1): 63-79 (en inglés). El presente trabajo describe los mecanismos de dispersión y reproducción en la comunidad de matorral termomediterráneo Anabasio hispanicae-Euzomodendretum bourgaeani. El análisis de las estrategias de vida se basa en inventarios fitosociológicos realizados en el desierto de (provincia de Almería). La importancia biológica de las estrategias de vida es expresada por el cociente medio de la cantidad del grupo (GM). La estrategia de vida predo­ minante es el subgrupo de los perennes con dispersión a corta distancia, con reproducción sexual. Las especies se reproducen principalmente por semillas y la reproducción clonal no parece tener importancia para la colonización del habitat semidesértico. La comunidad está caracterizada por una baja capacidad de dispersión que se consigue por mecanismos que impiden la dispersión secundaria de las diásporas. Para asegurar que la germinación de las diásporas coincide con una economía hídrica favorable, un alto porcentaje de las especies que maduran y fructifican un poco antes o dentro del período seco almacena por lo menos una parte de sus diásporas en un banco aéreo. Además, la inmediata germinación de las diásporas es frecuentemente impedida por las altas temperaturas. Palabras clave: Euzomodendron bourgaeanum, banco aéreo de diásporas, dispersión, estrategias de vida, producción de mucosidad, reproducción.

Abstract HENSEN, I. (1999). Life strategies of semi-desert plants: mechanisms of dispersal and reproduction in the thermomediterranean shrubland community Anabasio-Euzomodendretum bourgaeani. Anales Jard. Bot. Madrid SI {Y): 63-79. The present study describes mechanisms of dispersal and reproduction in the thermo­ mediterranean shrubland community Anabasio hispanicae-Euzomodendretum bourgaeani. The life strategy analysis based on sociological releves was carried out in Tabernas Desert (Province Almería). The biological significance of the occurring life strategies is represented by the mean group quantity fraction (GM). The dominant life strategy subdivisión of Anabasio-Euzomodendretum bourgaeani is that of Perennial stayers with short-range dispersal, with sexual reproduction. Reproduction takes place mainly by seeds; clonal reproduction does not appear to have any significance for the colonization of this semi-desert habitat. The community is characterized by a low dispersal capacity, achieved by several mechanisms for avoiding dispersal. A high percentage of the that mature and fructify shortly before or during the hot and rainless summer, stores at least a subset of seeds in an aerial diaspore bank to assure that dispersal and germination coincide with an advantageous soil

1 Institut für Systematische Botanik und Pflanzengeographie, Freie Universitat Berlín. Altensteinstr. 6. D-14195 Berlin (Germany). E-mail: [email protected]. 64 ANALES JARDÍN BOTÁNICO DE MADRID, 57(1) 1999

water supply. Additionally, immediate seed germination is frequently inhibited by high temperature. Key words: Euzomodendron bourgaeanum, aerial diaspore bank, dispersal, Ufe strategies, productum of mucilage, reproductíon.

iNTRODUCnON The present study is mainly aimed to analyze the dominant life strategies within The shrubland community Anabasio Anabasio-Euzomodendretum bourgaeani. hispanicae-Euzomodendretum bourgaeani The term life strategy is defined as a "system Rivas Goday & Esteve 1965 is among the of co-evolved adaptive traits" developed by floristically and ecologically most remarkable parallel differentiation and evolution of associations of the semi-arid habitats in characteristics in different taxa (STEARNS, Southeastern . This association is rich 1976; DURING, 1979). The concept was in endemisms. It colonizes the inclined originally applied to the functional charac- and highly eroded hillsides of the Tabernas terization of bryophyte communities (e.g. DU­ Desert, a semi-desert landscape located in the RING, 1979,1981,1992; FREY & KÜRSCHNER, north of Almería city (Almería Province, 1991a, b, 1995a, b; FREY & al., 1995b; HALF- figs. 1-2). MANN, 1991; GONZÁLEZ-MANCEBO á al.,

Fig. l.-Location of the Tabernas Desert (Almería, Southeastern Spain). I. HENSEN: LIFE STRATEGIES OF SEMI-DESERT PLANTS 65

2o 25' W, 200-700 m above sea level; fig. 1). The climate in the área is semi-arid. The climatic diagram (fig. 3) gives a mean annual temperature of 17.3 °C and a mean annual rainfall of 243 mm. There is a pronounced and constant dry season from May to September, in contrast to a changeable annual rainfall from year to year (range of 41-365 mm between 1960 and 1990). Due to the marly substrates which establish the main geological basis of soil formation, nearly the Fig. 2.-Overview of the Tabernas Desert (Almería, whole Tabernas Desert has the characteristics Southeastern Spain). of badland, with very eroded slopes and sparse vegetation (fig. 2). 1992; KÜRSCHNER, 1994; ZIPPEL, 1998), and funher developed by FREY & HENSEN (1995a) for a synstrategical evaluation of com- MATERIAL AND METHODS munities dominated by phanerogames. FREY Analysis of vegetation & HENSEN'S (1995a) classification focuses mainly on sexual and asexual mechanisms The quantitative analysis of the existing of dispersal and reproduction, and has been life strategies is based on the cover abundance found to be applicable to several plant index for all species composing the plant communities in Central Europe (e.g. FREY & community. Eighteen releves were carried out HENSEN, 1995a, b; FREY & HAUSER, 1996; in May 1996 and June 1997, being classified BÓTTNER & al, 1997; HENSEN, 1997, 1998; in Anabasio-Euzomodendretum bourgaeani HENSEN & KENTRUP, 1998). Life strategy using BRAUN-BLANQUET'S (1964) method analyses provide information about groups of (extended by BARKMAN & al., 1964 and species characterized by the same strategies DIERSCHKE, 1994) and according to PEINADO forcolonization and recolonization, establish- ment, occupation, and maintenance of habitats, facilitating to assess the degree to which a plant community is endangered. The present study is part of a research project analysing the predominant mechanisms of dispersal and reproduction in plant communities along an altitudinal gradient in the semi-arid habitats of South­ eastern Spain, where the life strategies of four mediterranean communities have already been studied (SCHRAMM, 1998; GROENKE, 1999; HENSEN, 1999C; HENSEN «fe ZUTHER, 1999). Fig. 3.-Climatic diagram of Tabernas (Almería, South­ eastern Spain). H = probable frost period; M = mean maximum temperature of the warmest month; M* = absolute maximum temperature of the warmest STUDY ÁREA month; m = mean minimum temperature of the coldest month, m' = absolute minimum temperature of the The study área is the Tabernas Desert, coldest month; P = mean annual rainfall in mm; pr = precipitation; PAV - Period of vegetative activity; situated 25 km north of the city of Almería, T = mean annual temperature; t = temperature (according Andalucía, Southeastern Spain (37° 05' N, to PEINADO & al., 1992, modified). 66 ANALES JARDÍN BOTÁNICO DE MADRID, 57(1) 1999

& al. (1992). Plant ñames were taken from acanthophorous: hooked; myxophorous: mu- TUTIN & al. (1968-1980,1993), CASTROVIEJO cilaginous when wetted; pogonophorous: & al. (1990-1997), and NAVARRO (1995; plumous by a pappus or hairy awn; ptero- Teucrium). Mosses and lichens were not phorous: winged; saccophorous: containing studied. Measurements of soil profundity air; sarcophorous: fleshy; trypanophorous: were carried out in several different áreas to turning around, creeping or drilling by estímate soil water conditions. hygroscopic movement; none: without cha- racteristic furthering or hindering dispersal. It Classification oflife strategies may be noted that the properties of diaspores and evaluation oftheir biological do not necessarily correlate with tfie primary significance dispersal types: ballautochory: spread by mechanisms of turgescence or dessication; Life strategy classification of the species endozoochory: transponed within animal comprising the plant community is based on intestines; epizoochory: transported by FREY & HENSEN (1995a, b), who elaborated a system of co-evolved adaptive traits to attachment to animáis; meteoranemochory: environmental conditions comprising life able to fly; ombrohydrochory s.str.: diaspore history, dispersal and reproductive behaviour released by rain, according to GUTTERMAN (table 1). The biological significance can be (1993); semachory: spread by movement calculated from the mean group quantity (caused by wind or animáis). fraction (GM, comp. DIERSCHKE, 1994; FREY The presence of an aerial diaspore bank & HENSEN, 1995a): ("aestatiphory", ZOHARY, 1937) was as- certained in August 1997. £ of mean coverage percentage of all group members within the association To determine the dispersal potential of GM =4— f —- x 100 meteoranemochorous seeds, flight expe- £ of mean coverage percentage of all riments with morphologically distinct species occurring in the association diaspores of lanifera, Lygeum (= total coverage percentage) spartum, and Stipa capensis were carried out Mean percentages of plant coverage are: using a nozzle-driven blower (method + (0.5 %), 1 (2.5 %), lm (2.5 %), 2a (10.0 %), according to HENSEN & MÜLLER, 1997). At 2b (20.0 %), 3 (37.5 %), 4 (62.5 %), 5 (87.5 %); different wind speeds, 25 diaspores of each r is not considered (DIERSCHKE, 1994; FREY & species were held in front of the opening, with LÓSCH, 1998). Estimation of dispersal behaviour (non-, long-range, short-range the center of gravity lying below, and dispersal, shuttle) includes sexually and released. The trajectory was photographed asexually produced diaspores. Clonal growth against a black background, visible as a bright and clonal reproduction was determined in stripe in the transparency. Horizontal flight the study área. Clonal reproduction is defined distances were calculated using the relation as a fragmentation of a genet in morpho- x = h tan a (x = horizontal flight distance, logically similar ramets which are able to h = height of exposition, a = angle between become independent. This mechanism results the trajectory and the vertical line). in a lateral spread of the individuum (HENSEN, 1997; FREY & LÓSCH, 1998). Germination experiments Germination experiments with freshly Dispersal behaviour of sexually collected and 6 month dry-stored diaspores of produced diaspores Diplotaxis harra subsp. lagascana, Euzo­ Sexually produced dispersal units of all modendron bourgaeanum, Lygeum spartum, appearing species were collected in May 1996 Moricandia foetida, Phagnalon rupestre, and June, August and December 1997. They Serratula flavescens, Stipa capensis, S. parvi­ were classified according to JENNY (1995) flora, and S. tenacissima were carried out in into the following dispersal categories: order to obtain information about dormancy I. HENSEN: LIFE STRATEGIES OF SEMI-DESERT PLANTS 67

TABLEI

LIFE STRATEGY SYSTEM (according to FREY & HENSEN, 1995a, b) 1. Annual shuttle species AnS Short life span (annual), short-range dispersal of sexual diaspores (shuttle), sexual reproduction effort high, no asexual reproduction.

2. Fugitives Fu Short life span (annual, biennial), long-range dispersal of sexual diaspores, sexual reproduction effort high, asexual reproduction infrequent.

3. Cryptophytes (= Geo-, Helo-, Hydrophytes) Cr Perennials, long- and short-range dispersal of sexual diaspores, sexual and asexual reproduction frequent.

4. Short-lived shuttle species PaS Biennials or pauciennials, short-range dispersal of sexual diaspores (shuttle), sexual reproduction frequent, asexual reproduction infrequent.

5. Colonists C Mainly pauciennials, long-range dispersal of sexual diaspores, sexual reproduction effort high, asexual reproduction frequent.

6. Perennial colonists PC Perennials, high mortality rates, long-range dispersal of sexual diaspores, sexual reproduction effort high, asexual reproduction infrequent.

7. Perennial shuttle species PS Perennials, short-range dispersal of sexual diaspores (shuttle), sexual reproduction effort high, asexual reproduction frequent.

8. Perennial stayers P Perennials, non or long- and short-range dispersal of sexual diaspores, sexual and asexual reproduction frequent.

9. Perennial stayers with diaspore years PDi Perennial trees setting fruits only in certain periods ("mast years"), thus building up a deposit of juvenile plants. Long- and short-range dispersal of sexual diaspores, sexual and asexual reproduction frequent.

Subdivisión according to dispersal potential of sexual and/or asexual produced diaspores with long-range dispersal (Telechory) T e.g. PT with short-range dispersal (Engychory) E PTE with long- and short-range dispersal (Telechory and Engychory) TE PTE according to reproduction type

with sexual reproduction s e.g. PTS with asexual reproduction s.str. as with clonal reproduction .el with passive reproduction p with sexual and asexual reproduction s, as or other combination respectively 68 ANALES JARDÍN BOTÁNICO DE MADRID, 57(1) 1999

types. Germination was tested in climate strategies of Anabasio-Euzomodendretum chambers with a warm white light source bourgaeani is compiled in table 3. It indicates (12 h of light / 12 h of darkness) providing that most species of Anabasio-Euzomo­ 20 umol m~2s~' at seed level at four fluctuating dendretum bourgaeani mature and fructify temperaturas: 8/2 °C; 16/10 °C; 24/18 °C; shortly before or during the drought period. 32/24 °C. Each experiment consisted of three Almost 40 % of these keep all or part of their replícate Petri dishes with at least 50 viable seeds within an aerial diaspore bank, so that at seeds. A seed was considered to have least a few diaspores remain attached to the germinated when its radicle had become mother plant until the next rainy season. elongated. A survey of the predominant mechanisms of dispersal and reproduction (table 4) shows that within Anabasio-Euzomodendretum RESULTS bourgaeani, sexual reproduction is far more significant than asexual reproduction. Only Syntaxonomy and habitat conditions 6.9 % GM of the species are capable of clonal of Anabasio-Euzomodendretum reproduction. There is a clear dominance bourgaeani of sexually produced diaspores provided The endemic association Anabasio-Euzo­ with flying structures, such as wing-like modendretum bourgaeani is found on the formations or plumous hairs, and diaspores steep and highly eroded slopes between Rioja with mucilage production. Meteoran- and Tabernas (figs. 1-2). This permanent-type emochory is the predominant dispersal type community grows on poorly developed soils (46.4 % GM; table 4). However, meteor- without upper horizon. The marly subsoils anemochory does not necessarily result in of an almost white to light grey color are long-range dispersal; only diaspores with frequently covered by a saline crust over well-established flight structures could be the soil surface. The soil profundity of the dispersed by wind over longer distances predominant entisols is low. Because they are (figs. 4a-c). Other significant dispersal types heavily compressed and have very poor are ombrohydrochory s.str. (31.5 % GM) and infiltration characteristics, the mean field ballautochory (30.4 % GM; table 4). layer coverage of vegetation is only about 10%(table2). Life strategies Anabasio-Euzomodendretum bourgaeani The following life strategy subdivisions is one of the plant communities on the Iberian are of biological significance within Peninsula richest in endemic species (table 2). Anabasio-Euzomodendretum bourgaeani It is sociologically included within Rosma- (fig. 5): perennial stayers with short-range rinetea officinalis Br.-Bl. 1947 em. Rivas- dispersal and sexual reproduction (PES; GM Martínez et al. 1991 (Anthyllidetalia terni- 43.6 %), perennial stayers with long-range florae Rivas Goday et al. in Rivas Goday dispersal and sexual reproduction (PTS; GM & Borja 1961). Characteristic taxa of 26.3 %), fugitives with long- and short-range association are two locally endemic Bras­ dispersal and sexual reproduction (FuTEs; sicaceae: Euzomodendron bourgaeanum and GM 8.8 %), and annual shuttle species (AnS; Moricandia foetida (PEINADO & al, 1992). GM 6.3 %). It is remarkable that almost all Among the character species of Anthylli­ perennial stayers belong to the chamaephytic detalia terniflorae, Launaea lanifera is highly life form (table 3). constató (table 2). Perennial stayers with short-range dispersal Predominating mechanisms of sexual and sexual reproduction (PES) and asexual reproduction Perennial stayers with short-range The character complex determining the life dispersal and sexual reproduction is the I. HENSEN: LIFE STRATEGIES OF SEMI-DESERT PLANTS 69

TABLE2

ANABASIOHISPAMCAE-EUZOMODENDRETUM BOURGAEANl OFTKE TABERNAS DESERT, SOUTHEASTERN SPAIN (* Iberian endemisms)

Relevé number m above sea level Exposition Slope inclination Soil profundity (cm) Extentionofarea(m!) Degreeofcoverage Species number

Character species Euzomodendron bourgaeanum* Salsola genistoides* Moricandia foetida* Anabasis articulata Launaea lanifera Herniaria fontanesii subsp. almeriana* Serratula flavescens Helianthemum almeriense* Diplotaxis harra subsp. lagascana* Thymus baeticus

Othertaxa Asparagus horridus Lygeum spartum Stipa capensis Stipa tenacissima Stipa parviflora Teucrium capitatum subsp. gracillimum Artemisia herba-alba Phagnalon rupestre Fagonia cretica Plantago albicans Cuscuta planiflora Frankenia corymbosa Launaea resedifolia Limonium insigne* Haloxylon articulatum Reichardia tingitana Reseda lanceolata Suaeda pruinosa Atractylis cancellata Calendula arvensis

Additional taxa: in 1: Lobularia maritima 1; in 2: Asteriscus aquaticus 1, Linum strictum 1, Salsola oppositifolia +, Thesium humile +; in 3: Carlina racemosa +, Limonium tabernense* 1, Thapsia villosa +; in 7: Bromus rubens lm, Helianthemum salicifolium +; in 8: Genista umbellata +; in 10: Launaea arborescens 1; in 12: Reseda phyteuma +; in 16: Lycium intricatum +. Relevé locations: Tabernas Desert. 70 ANALES JARDÍN BOTÁNICO DE MADRID, 57(1) 1999 I. HENSEN: LIFE STRATEGIES OF SEMI-DESERT PLANTS 71 72 ANALES JARDÍN BOTÁNICO DE MADRID, 57(1) 1999 dominant Ufe strategy subdivisión of Anabasio-Euzomodendretum bourgaeani. The most significant representatives are chamaephytes: Euzomodendron bourgaea­ num, Artemisia herba-alba, Helianthemum almeriense, and Herniaria fontanesii subsp. almeriense. The locally endemic character species Euzomodendron bourgaeanum (Brassicaceae), with a GM of 26.1 %, clearly dominates the community. Its population is composed of Fig. 5.-Life strategy spectra of Anabasio-Euzomo­ different age groups. The shrub grows up to a dendretum bourgaeani, and biological significance of height of approximately 50 cm and is charac- myxospermy as the most important mechanism prevent- terized by dehiscent carneous pinnate leaflets. ing dispersal. Analysis based on the mean group quantity fraction (GM). Other life strategy subdivisions: PEs,ci; GM 3.5 %; PTEs,ci; GM 3.4 %; PaS; GM 3.2 %; CrTEs; GM 3.1 %; PTEs; GM 0.9 %. For abbreviations of life strategies see table 1.

Its siliquas contain 16 winged seeds on average, which develop mucilage after being wetted (fig. 6). Diaspores are dispersed pre- dominantly between April and June, but a

TABLE 4

MEAN GROUP QUANTITY FRACTION (GM) OF CLONAL GROWTH, CLONAL REPRODUCTION, AND CHARACTERISTICS OF SEXUALLY PRODUCED DIASPORES AND DISPERSAL WITHIN ANABASIO- EUZOMODENDRETUM BOURGAEANI GM%

Clonal growth / clonal reproduction 23.8/6.9 Diaspore characteristics pterophorous 53.5 myxophorous 42.7 pogonophorous / pogonophorous* 22.5/2.5 acanthophorous 10.5 trypanophorous 9.5 none 3.8 sarcophorous 3.2 saccophorous 3.2

Main primary dispersal type Figs. 4a-c.-Horizontal flight distance (cm) in dependence meteoranemochory 46.4 of wind vclocity (mean valué and span for n = 25) of ombrohydrochory s.str. 31.5 diaspores of Stipa capensis: a, Lygeum spartum; b, and ballautochory 30.4 Launaea arborescens; c (data of Lygeum spartum provided by GROKNKE, 1999). In brackets: exposition epizoochory 20.0 height of diaspores. The quadratic equations describe the semachory 18.8 dispersal behaviour. endozoochory 3.2 I. HENSEN: LIFE STRATEGIES OF SEMI-DESERT PLANTS 73 small fraction remains on the mother plant (see HENSEN, 1999a for Salsola genistoides). during the drought period (partial aestati- Long-range dispersal is equally promoted by phory). The ballautochorous seeds are spread pappus in Launaea lanifera (see fig. 4c for by an explosión mechanism under the the similar stuctured achenes to Launaea influence of a sudden movement. Such arborescens) and Phagnalon rupestre (As­ movement can be caused by gusty wind, rain, teraceae). The latter is characterized by or animáis. Field observations show that the xerochastic capitula which endose their seeds seeds disperse up to 1.5 m through this when wetted, and expose them when primarily dispersal mechanism. Under humid atmospheric humidity is very low. The weather conditions, secondary transpon of aerodynamic diaspores of Phagnalon ru­ seeds is prevented by the production of sticky pestre are very small however (0.02 mg; mucilage. The capacity of the seeds to adhere table 3). After being dispersed at the begin- to soil crust is very strong. The seeds remain ning of summer, they rapidly become covered by dust and other soil particles. Germination attached to the soil even under a wind of experiments reveal that they remain dormant 18 m/s (unpublished data). This mechanism for at least six months. may also prevent major predation by harvester ants. Seeds of Euzomodendron bourgaeanum germinate in a wide range of Fugitives with long- and short-range temperatures (8-32 °C). There is no innate dispersal and sexual reproduction (FuTEs) dormancy, but germination is clearly reduced This subdivisión is represented by Stipa at temperatures over 24 °C (fig. 7a). capensis, one of the most common annual The locally endemic Herniaria fontane­ grasses of southeastern Spain. This thero- sii subsp. almeriana (Caryophyllaceae) phyte completes its life cycle by producing develops its saccophorous diaspores im- and dispersing mature caryopses at the mediately above ground level, where any beginning of the drought period. The spikelets further transport is prevented by the plant's are characterized by a long lemma-awn which own densely arranged small leaves. The serve as a fiight mechanism. However, at chamaephytes Artemisia herba-alba and He­ a wind speed of 5 m/s, diaspores of Stipa lianthemum almeriense are characterized by capensis reach short fiight distances not the development of myxophorous diaspores. longer than approximately 2 m (fig. 4a). These are spread out semachorously, and Additionally, during the process of fruit adhere strongly to the soil surface under the ripening, their awns often keep hooked influence of rain. The diaspores oí Artemisia together in a way that several caryopses are herba-alba mature during the rainy season, blown away as a single, much heavier disper­ when the time of seed maturation is cióse to sal unit (synaptospermy). Long-range the time of seed germination. The seeds of Helianthemum almeriense drop out of their capsules shortly before the drought period.

Perennial stayers with long-range dispersal and sexual reproduction (PTS) Salsola genistoides, Anabasis articulata, Launaea lanifera, and Phagnalon rupestre are the most significant representatives of this group. Seeds of Salsola genistoides and Anabasis articulata (Chenopodiaceae) mature and germinate during the rainy period. Their small nutfruits remain enclosed by the Fig. 6.-Euzomodendron bourgaeanum: seed in moist tepals which enhance their fiight efficiency condition (mucilaginous cells marked by an arrow). 74 ANALES JARDÍN BOTÁNICO DE MADRID, 57(1) 1999 dispersal, on the other hand, is easily under a wide range of temperature conditions promoted by attachment to animáis. The (fig. 7c). It seems likely that timing of importance of such process of epizoochory germination is regulated by the duration and should be investigated in this habitat. degreeof wetting. The diaspores of Stipa capensis are Stipa parviflora and S. tenacissima trypanophorous: the lower part of the awn (Poaceae) are perennial stayers with long- twists when dry and straightens when wet. and short-range dispersal and sexual and They are able to penétrate the soil where at clonal reproduction. They develop an least a part of them remain dormant until the extensively branched rhizome that fragments next rainy season. Then, after several months by withering. In terms of their dispersal of after-ripening, all caryopses are able to behaviour, fruits of both species are similar germinate within a few hours and under a to those of Stipa capensis (fig. 4a). No in­ wide range of temperatures (fig. 7b). nate dormancy is found, but germination is inhibited at higher temperatures in Stipa Annual shuttle species (AnS) tenacissima (fig. 7d). Annual shuttle species are represented by The biennial Serratula flavescens (As­ eight therophytes. It is remarkable that five of teraceae), a short-lived shuttle species, them, including Moricandia foetida and develops xerochastic capitula which endose Diplotaxis harra subsp. lagascana (Bras­ its seeds when wetted, and open them when sicaceae) develop myxophorous seeds. atmospheric humidity is very low. However, Ballautochorous seeds of this two species during the summer, diaspores of Serratula spread out from the narrow siliquas shortly flavescens are held deep in the capitula, where before the drought period. In case of high they are additionally protected by dense and site humidity, they stick firmly to the ground abundant receptacular bristles. Seeds are and become buried. Although similar in characterized by inhibited germination under their ecology, both species display a distinct high temperatures (fig. 7e). germination behaviour. The immediate germination of tiie diaspores of Moricandia DISCUSSION foetida is prevented by an innate dormancy whereas germination of freshly collected In the thermomediterranean landscape of Diplotaxis harra subsp. lagascana diaspores the Tabernas Desert, the locally endemic takes place only when soil temperatures are Anabasio hispanicae-Euzomodendretum low (results not shown). bourgaeani is the dominant association on the highly eroded hillsides of the región. The high Other Ufe strategy types number of endemic species to Southeastem Lygeum spartum (Poaceae), a perennial Spain indicates that these badland áreas have stayer with short-range dispersal and sexual been formed naturally. The denuded slopes and clonal reproduction, is among the few may have already been in existence during the clonally reproducing species existing within more humid glacial periods, because the light- Anabasio-Euzomodendretum bourgaeani. requiring species are not able to compete The fragments of a clone consist of a large within a dense vegetation structure (FREITAG, number of ramets which are lined up like 1971). pearls on a string. The lemmas of the In this semi-desert environment, a system caryopses are covered with long silky hairs of specific co-evolved adaptive traits to the and keep together in pairs, thereby enclosing climatically and edaphically extreme habitat 2 grains that remain connected until germina­ conditions has been developed. A quantitative tion. The flight capacity of these synapto- evaluation of the existing colonization and spermous diaspores is low (fig. 4b). Germi­ reproduction mechanisms, as assessed by nation of non-dormant seeds is carried out converting species amplitude and constancy I. HENSEN: LIFE STRATEGIES OF SEMI-DESERT PLANTS 75

Fig. 7.-Percentages of germination of 6 month dry-stored diaspores at different diurnally fluctuating temperatures: a, Euzomodendron bourgaeanum; b. Stipa capensis; c, Lygeum spartum; d, Stipa tenacissima; e, Serratula flavescens. 76 ANALES JARDÍN BOTÁNICO DE MADRID, 57(1) 1999

into mean group quantity fractions (GM), retain a proportion of seeds sufficient to main- shows that perennial stayers of the tain the population within the habitat chamaephytic life form are best adapted to (GUTTERMAN, 1993). this habitat. The most significant life strategy The species dispersing their diaspores subdivisión is that of perennial stayers with immediately after fruit maturity possess short-range dispersal and sexual reproduction further mechanisms to survive the long un- followed by perennial stayers with long- favourable time between the short growing range dispersal and sexual reproduction. periods. Seeds of several species collected in Reproduction takes place mainly by sexually the Tabernas Desert are protected by inhibited produced diaspores, which represent the germination under extreme temperatures (e.g. most resistent stage of a plant's Ufe history. Euzomodendron bourgaeanum, Serratula It is remarkable that species spreading flavescens, Stipa parviflora, S. tenacissima, laterally are rare due to extreme water figs. 7a, d, e), whereas the existence of innate conditions, and clonal reproduction is nearly dormancy plays a minor role as expected without significance for colonization and (comp. e.g. MOTT, 1972; HARPER, 1977; maintenance of this badland surfaces FENNER, 1991; JURADO & WESTOBY, 1992; (table 4). However, this does not apply to the GUTTERMAN, 1993; SCHÜTZ & MILBERG, semi-desert habitat in general, as shown by 1997). HENSEN (1999c). The results of the present life strategy As previously reported for several analysis reveal that there is a notable tendency or semi-deserts (e. g. GUTTERMAN, 1993), also towards short-range dispersal within most species of the Anabasio-Euzomo- Anabasio-Euzomodendretum bourgaeani. dendretum bourgaeani mature and fructify Biologically, the production of mucilage is shortly before or during the hot and rainless one of the most important mechanisms to summer (see NAVARRO & al, 1993). There- reduce dispersal in species such as Euzomo­ fore, their offspring success is influenced not dendron bourgaeanum, Moricandia foetida, only by the unpredictability of precipitation Artemisia herba-alba, etc. (table 3,4; fig. 5). and by the high summer temperatures, but Myxospermy is an effective mechanism also by strong winds and seed-harvesting ants of adhesión to the soil (GRUBERT, 1974; (see HENSEN, 1999b). The open vegetation GUTTERMAN, 1993; GUTTERMAN & SHEM- structure of Anabasio-Euzomodendretum Tov, 1997a), and appears to decrease a bourgaeani, the strong slope inclination of its secondary dispersal by wind or rain and seed locality, and the formation of a soil crust predation by ants (GUTTERMAN, 1990, 1993; suggest that a high percentage of diaspores is GUTTERMAN & SHEM-TOV, 1997b). Although most likely carried away from its current types and structure of mucilage differ consid- habitat by wind or flowing water. erably among the investigated diaspores, their A high percentage of the observed species adhesiveness under natural conditions is very within Anabasio-Euzomodendretum bour­ strong. The significance of mucilaginous gaeani stores at least a part of their seeds seeds under humid conditions is best describ- in an aerial diaspore bank during the ed by the character species Euzomodendron drought period (aestatiphory; table 3). This bourgaeanum. To be effective, myxospermy mechanism protects the species from heavy requires conditions of variable atmospheric losses of diaspores, and assures that dispersal humidity. Thus, the myxophorous seeds and germination coincide with an of Euzomodendron bourgaeanum mature advantageous soil water supply. In autumn, successively during spring when sporadic seed reléase may be triggered by moisture showers could still occur. The time of (EVENARI & al, 1982; GUTTERMAN, 1990). germination is regulated by the duration and Therefore, for most aestatiphorous plants, the degree of wetting, as well as by the presence time of dispersal is cióse to that of seed germi­ of modérate soil temperatures. Germination nation. This dispersal peculiarity may help to usually does not occur until autumn in this I. HENSEN: LIFE STRATEGffiS OF SEMI-DESERT PLANTS 77

group of plants (see SCHÜTZ & MILBERG, 1997 not feed on. Nevertheless, it has to be kept in for Launaea arborescens). The combination mind that due to the tendency towards short- of perennial life history, avoidance of range dispersal, the habitat colonized by secondary transpon and predation, and the Anabasio-Euzomodendretum bourgaeani delay of germination until the rainy season will never fall below the minimum necessary results in a strong emphasis on permanent for maintaining the complete species variety. habitat colonization and maintenance. Thus, a further size reduction or a further The other significant life strategy sub­ habitat fragmentation will have to be división of Anabasio-Euzomodendretum prevented. Fortunately, a large step in the bourgaeani, perennial stayers with long- right direction has already been made by range dispersal and sexual reproduction, is the establishment of the "Paraje Natural del characterized by telechory as prevailing Desierto de Tabernas". dispersal behaviour. These species have not developed mechanisms for hindering or preventing dispersal. However, it is important ACKNOWLEDGMENTS to note that several of these species mature and disperse their diaspores during the rainy This research was supported by the DAAD season when the time of germination is cióse programme "Acciones Integradas Hispano-Ale- to that of dispersal, and long-range dispersal manas". I gratefully acknowledge the invaluable cooperation and helpfulness of Prof. Dr. J. Guerra, is probably less likely to occur due to the Dr. R. Ros, Dr. P. Sánchez and Dr. M. Cano moist climate conditions (see HENSEN, 1999a, (University of Murcia, Spain). Additionally, for Salsola genistoides). I would like to thank Prof. Dr. W. Frey for The results of the present life strategy constructive comments on this manuscript, analysis demónstrate that under alternating H. Lünser for drawing the figures 1, 3, and 4, site conditions, the maintenance of habitat is S. Iorgova, Stanford University, for help with of great importance for the regeneration translation, and two anonymous reviewers for success of the species. Considering the improvements in this article. tendency towards short-range dispersal, Anabasio-Euzomodendretum bourgaeani is REFERENCES comparable to several already described xerothermous plant communities of Central BARKMAN, J.J., H. DOING & S. SEGAL (1964). Kritische Europe, such as e.g. Drabo-Hieracietum Bemerkungen und Vorschlage zur quantitativen humilis (FREY & ai, 1995a), Stipetum ca- Vegetationsanalyse. Acta Bot. Neerl. 13: 394-419. pillatae, Adonido-Brachypodietum pin- BÓTTNER, I., W. FREY & I. HENSEN (1997). Carex humilis-Gesellschaft im unteren Unstruttal (mittel- nati (HENSEN, 1997), or Carex humilis- deutsches Trockengebiet) - Lebensstrategien in einer community (BÓTTNER & al, 1997). In open xerothermen Vegetationseinheit. Feddes Repert. 108: landscapes, many sites to which a seed might 425-452. be transponed, will never be suitable BRAUN-BLANQUET, J.-J. (1964). Pflanzensoziologie, for germination and establishment. Thus, ed. 3. Berlin, Wien, New York. CASTROVIEJO, S., M. LA(NZ, G. LÓPEZ-GONZÁLEZ, the maintenance of habitat prevails over P. MONTSERRAT, F. MUÑOZ GARMENDIA, J. PAIVA & dispersal, and the new offspring is retained at L. VILLAR (eds.) (1990). Flora iberica 2. Madrid. the parental site which has already been CASTROVIEJO, S., C. AEDO, S. CIRUJANO, M. LAÍNZ, proved to be favourable for the existence of P. MONTSERRAT, R. MORALES, F. MUÑOZ GARMENDIA, C. NAVARRO, J. PAIVA & C SORIANO (eds.) (1993a). the species. Flora iberica 3. Madrid. Several species oí Anabasio-Euzomo­ CASTROVIEJO, S., C. AEDO, C. GÓMEZ CAMPO, M. LAÍNZ, dendretum bourgaeani are restricted to the P. MONTSERRAT, R. MORALES, F. MUÑOZ GARMENDIA, Tabernas Desert. The threat of this semi- G. NETO FELINER, E. RICO, S. TALAVERA & L. VILLAR desert landscape seems to be low, due to its (eds.) (1993b). Flora iberica 4. Madrid. CASTROVIEJO, S., C. AEDO, M. LAINZ, R. MORALES, sparse vegetation coverage which even F. MUÑOZ GARMENDIA, G. NIETO FELINER & J. PAIVA grazing animáis subsisüng on very little can- (eds.) (1997a). Flora iberica 5. Madrid. 78 ANALES JARDÍN BOTÁNICO DE MADRID, 57(1) 1999

CASTROVIEJO, S., C. AEDO, C. BENEDI, M. LAÍNZ, GONZÁLEZ-MANCEBO, J.M., A. LOSADA-LIMA, C.D. F. MUÑOZ GARMENDIA, G. NIETO FELINER & J. PATVA HERNÁNDEZ & H.J. DURING (1992). Bryophyte flora (eds.) (1997b). Flora iberica 8. Madrid. of volcanic caves in the Azores and the Canary DIERSCHKE, H. (1994). Pflanzensoziologie. Stuttgart. Islands. Lindbergia 17: 37-46. DURING, H.J. (1979). Life strategies of bryophytes: a GROENKE, T. (1999). Dactylo hispanicae-Lygeetum preliminary review. Lindbergia 5:2-18. sparti - Lebensstrategien in einer thermo- DURING, H.J. (1981). Bryophyte flora and vegetation of mediterranen Rasengesellschaft (Südostspanisches Lanzarote, . Lindbergia 7: 113-125. Trockengebiet, Almería). Degree diss., Berlin. DURING, H.J. (1992). Ecological classification of GRUBERT, M. (1974). Studies on the distribution of bryophytes and lichens. In: Bates, J.W. & H.M. myxospermy among seeds and fruits of Angio- Farmer (eds.), Bryophytes and lichens in a changing spermae and its ecological importance. Acta Biol. environment: 1-31. New York. Venez. 8: 315-551. EVENARI, M., L. SHANAN & N. TADMOR (1982). The GUTTERMAN, Y. (1990). Seed dispersal by rain (ombro- - the challenge ofa desert, ed. 2. Cambridge. hydrochory) in some of the flowering desert plants in FENNER, M. (1991). The effects of the parent environment the deserts of Israel and the Sinai Península. Mitt. Inst. on seed germinability. Seed Sci. Res. 1:75-84. Allg. Bot. Hamburg 23:841-852. FREITAG, H. (1971). Die natürliche Vegetation des GUTTERMAN, Y. (1993). Seed germination in desert südostspanischen Trockengebietes. Bot. Jahrb. Syst. plants. Berlin. 91: 147-308. GUTTERMAN, Y. & S. SHEM-TOV (1997a). Mucilaginous FREY, W. & A. HAUSER (1996). Onopordetum acanthii seed coat structure of Carrichtera annua and (Eselsdistel-Gesellschaft) im mittleren und unteren Anastatica hierochuntica from the Negev Desert Unstruttal - Lebensstrategien in einer warmelie- highlands of Israel, and its adhesión to the soil crust. benden Ruderalgesellschaft. Haussknechtia Beih. 6: J. Arid Env. 35:695-705. 1-84. GUTTERMAN, Y. & S. SHEM-TOV (1997b). The efficieney FREY, W. & I. HENSEN (1995a). Lebensstrategien bei of the strategy of mucilaginous seeds of some Pflanzen: ein Klassifizierungsvorschlag. Bot. Jahrb. common annuals of the Negev adhering to the soil Syst. 117:187-209. crust to delay collection by ants. Israel J. Plant Sci. FREY, W. & I. HENSEN (1995b). Spergulo morisonii- 45:317-327. Corynephoretum canescentis (Frühlingsspark- HALFMANN, J. (1991). Die Struktur der Vegetation auf Silbergrasflur) - Lebensstrategien von Binnendünen- periglazialen Basaltblockhalden des Hessischen und Lockersandbesiedlern. Feddes Repert. 106: 533- Berglandes. Bryophytenvegetation und Waldgesell- 553. schaften: Morphologisch-anatomische Merkmale, FREY, W. & H. KÜRSCHNER (1991a). Lebensstrategien Fortpflanzungs- und Ausbreitungsbiologie. Diss. Bot. von terrestrischen Bryophyten in der Judaischen 168: 1-212. Wüste. Bot. Acta 104: 172-182. HARPER, J.L. (1977). Population biology of plants. FREY, W. & H. KÜRSCHNER (1991b). Lebensstrategien London. epiphytischer Bryophyten im tropischen Tieflands- HENSEN, I. (1997). Life strategy systems of xerothermic und Bergregenwald am Mt. Kinabalu (Sabah, Nord- grasslands - mechanisms of reproduction and Borneo). Nova Hedwigia 53: 307-330. colonization within Stipetum capillatae s.l. and FREY, W. & H. KÜRSCHNER (1995a). Bryosoziologische Adonido-Brachypodietum pinnati. Feddes Repert. Untersuchungen in Jordanien. 3. Lebensstrategien- 108:425-452. analyse der terrestrischen und epilithischen HENSEN, I. (1998). Life strategies in salt marsh Moosgesellschaften. Fragm. Florist. Geobot. 40: communities of the East Frisian North Sea Coast 491-511. (Northwestern Germany). Fragm. Florist. Geobot. FREY, W. & H. KÜRSCHNER (1995b). Soziologie und 43: 237-256. Lebensstrategien epiphytischer Bryophyten in Israel HENSEN, I. (1999a). Reproductive patterns in five und Jordanien. Nova Hedwigia 61: 211-232. important semi-desert perennials of Southeastern FREY, W., I. HENSEN & H. KÜRSCHNER (1995a). Drabo- Spain. Bot. Jahrb. Syst. 121 (in press). Hieracietum humilis (Habichtskraut-Felsspalten- HENSEN, I. (1999b). A comparative analysis of dispersal gesellschaft) - Lebensstrategien von Felsspal- strategies in semi-desert plant communities of tenbesiedlern. Bot. Jahrb. Syst. 117: 249-272. Southeastern Spain and xerothermic plant FREY, W.. H. KÜRSCHNER & U.H. SEIFERT (1995b). communities of Eastern Germany. Flora (in press). Scientific results of the BRYOTROP expedition to HENSEN, I. (1999c). Life strategies in a widespread Zaire and Rwanda. 7. Life strategies of epiphytic thermomediterranean grassland community - bryophytes from tropical lowland and montane mechanisms of dispersal and reproduction within forests, ericaceous woodlands and the Dendrosenecio Lapiedra martinezü-Stipetum tenacissimae (semi- subpáramo of the eastern Congo basin and the arid Southeastern Spain). Feddes Repert. 110 (in adjacent mountains (Pare National de Kahuzi- press). Biega/Zaire.Forét de Nyungwe/Rwanda). Trop. HENSEN, I. & M. KENTRUP (1998). Teucrio botryos- Bryol. 11:129-149. Melicetum ciliatae (Traubengamander-Wimper- FREY, W. & R. LOSCH (1998). Lehrbuch der Geobotanik. perlgrasflur) - Lebensstrategien in einer xerothermen Stuttgart. Jena, Lübeck, Ulm. Fels-Pioniergesellschaft. Tuexenia 28: 217-236. I. HENSEN: LIFE STRATEGIES OF SEMI-DESERT PLANTS 79

HENSEN, I. & C. MÜLLER (1997). Experimental and (Tabernas, Almería. España). Acta Bot. structural investigations of anemochorous dispersal. Malac. 18:189-198. PtantEcol. 133:169-180. PEINADO, M., F. ALCARAZ & J.M. MARTÍNEZ-PARRAS HENSEN, I. & S. ZUTHER (1999). Die Anthyllis cytisoides- (1992). Vegetation ofSoutheastern Spain. Berlin. Gesellschaft im südostspanischen Trockengebiet - SCHRAMM, G. (1998). Astragalo-Velletum spinosae - Lebensstrategien in einer mesomediterranen Ersatz- Lebensstrategien in einer Dornpolstergesellschaft gesellschaft. Tuexenia 19 (in press). aus den südostspanischen Betischen Kordilleren. JENNY, M. (1995). Dispersal and micro-habitat Degree diss., Berlin. conditions within a desert plant community (Wadi SCHUTZ, W. & P. MILBERG (1997). Seed germination in Araba, Jordán). Bot. Jahrb. Syst. 116:483-504. Launaea arborescens: a continuously flowering semi- JURADO, E. & M. WESTOBY (1992). Germination biology desert shrub. /. Arid Environm. 36: 113-122. of selected central Australian plants. Austr. J. Ecol. STEARNS, S.C. (1976). Life history tactics: a review of the 17: 341-348. ideas. Quart. Rev. Biol. 51: 3-47. KÜRSCHNER, H. (1994). Adaptationen und Lebens­ TUTIN, T.G., V.H. HEYWOOD, N.A. BURGES, D.M. strategien in basiphytischen Gesteinsmoos- MOORE, D.H. VALENTINE, S.M. WALTERS & D.A. gesellschaften am Nordrand der Schwabischen Alb WEBB (eds.) (1968-1980). Flora Europaea 2-5. (Süddeutschland). Phytocoenologia 24:531-558. Cambridge. Morr, J.J. (1972). Germination studies on some annual TUTIN, T.G., N.A. BURGES, A.O. CHATER, J.R. species from an arid región of Western Australia. EDMONDSON, V.H. HEYWOOD, D.M. MOORE, D.H. J. Ecol. 60:293-304. VALENTINE, S.M. WALTERS & D.A. WEBB (1993). NAVARRO, T. (1995). Revisión del género Teucrium L. Flora Europaea 1, ed. 2. Cambridge. sección Polium (Mill.) Schreb. (Lamiaceae) en la ZIPPEL, E. (1998). Die epiphytische Moosvegetation der Península Ibérica y Baleares. Acta Bot. Malac. 20: Kanarischen Inseln. Bryophyt. Biblioth. 52: 1-149. 173-265. ZOHARY, M. (1937). Die verbreitungsókologischen NAVARRO, T., J.M. NIETO CALDERA, A.V. PÉREZ LATO- Verháltnisse der Pflanzen Palástinas. Beih. Bot. RRE & B. CABEZUDO (1993). Estudios fenomor- Centralbl. 56: 1-155. fológicos en la vegetación del sur de España. III. Editado por Pablo Vargas Comportamiento estacional de una comunidad de Aceptado para publicación: 3-V-1999