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Summary: Succulence is an adaptive strategythat allows plants to remain active during sea-sonal water shortage. The term was first usedformally by Johann (Jean) Bauhin in 1619 torefer to plants with thick, juicy leaves. Its subse-quent use and selected definitions are criticallydiscussed, including concepts such as utilizablewater, caudiciforms and pachycauls, and rootsucculence. A unified definition of succulenceconsiders aspects of morphology and anatomy,ecology, and physiology. Stem succulence and the“cactus life form” are used to illustrate the paral-lel evolution of functional adaptations in mor-phology, and to contrast the obvious externalsimilarities with the widely variable internalarchitecture, including the participation of dif-ferent stem tissues in water storage.

Zusammenfassung: Sukkulenz ist eine Strategie,welche Pflanzen auch während periodischemjahreszeitlichem Wassermangel erlaubt, aktiv zubleiben. Der Begriff wurde zuerst 1619 vonJohann (Jean) Bauhin zur Bezeichnung vonPflanzen mit dicken, saftigen Blättern benutzt.Die spätere Verwendung des Begriffs sowie aus-gewählte Definitionen von Sukkulenz werdenmit Blick auf nutzbares Wasser, Caudexpflan -zen, pachycaule Pflanzen und Wurzelsukkulenzkritisch diskutiert. Eine vereinheitlichteDefinition des Begriffs Sukkulenz berücksichtigtAspekte der Morphologie und Anatomie, derÖkologie und der Physiologie. Stammsukku -lenten und die “Kaktus-Lebensform” dienen alsBeispiel für die unabhängige Evolution einervergleichbaren äusseren Morphologie als funk-tionale Adaptation. Den offensichtlichen äusse-ren Ähnlichkeiten stehen äusserst unterschiedli-che Verhältnisse im inneren Bau gegenüber, und

an der Wasserspeicherung können ganz unter-schiedliche Achsengewebe beteiligt sein.

IntroductionSucculent plants, or “succulents“ for short, are aprominent component of the vegetation ofregions with semi-arid and arid climatic condi-tions (i.e. with yearly precipitation lower thanpotential annual evapotranspiration [technicalterms like this one are explained in the glossaryin Appendix 2]). Many succulents inhabit whatwe perceive as inhospitable and harsh environ-ments. They often occur in the subtropics, and, toa lesser extent, in the tropics, and comparativelyfew representatives are found in temperate andtemperate-cool climatic zones. The diversity oftheir architecture and appearance has madethem horticultural “collectibles“ from a veryearly time onwards (Rowley, 1997).

Succulents are an ecological and evolutionary“Sonderfall“ in many respects; they are testimo-ny of the power of adaptive evolution under spe-cific environmental conditions and the daily com-petition for limited resources such as water, lightand nutrients. The prominence of adaptation (i.e.the state that evolved because of improved repro-ductive performance; Stearns & Hoeckstra,2005) exemplified by the diversity of these pecu-liar plants is best explained by reference to thetheory of biological evolution through naturalselection (i.e. differential survival and reproduc-tion of individuals that differ in heritable traits)as originally put forward by Charles Darwin andAlfred Wallace in 1858, and later worked out indetail by the former (Darwin, 1859). However,succulence is obviously only one of several possi-ble “answers” to the challenge of surviving aridconditions − other plants with completely differ-

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Living under temporarily arid conditions – succulence as anadaptive strategy

Urs Eggli 1 and Reto Nyffeler 2

1 Sukkulenten-Sammlung Zürich, Grün Stadt Zürich, Mythenquai 88, CH-8002 Zürich, Switzerland (email: urs.eggli@zuerich.ch; author for correspondence).

2 Institut für Systematische Botanik, Universität Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland(email: rnyffeler@systbot.unizh.ch).

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ent adaptive strategies co-occur, and evolution ofplant life in (semi-) arid climates has not result-ed in a single “fittest” surviving adaptation inany given place (Figures 1, 2). It must be kept inmind that adaptations are not necessarily perfectbut must function just well-enough to permit sur-vival and reproduction (Niklas, 1997).

The major stress factor imposed on life in aridclimates is the temporary shortage of availablewater. Reactions to a stress factor (stress = pres-sure, condition causing hardship, disquiet; stress= deviation from optimal life conditions resultingin temporary or permanent decrease of vitality)are diverse, and the terminology used to classifyplant reactions is equally varied. According toLarcher (2001), the possible reactions of a plantto any factor of stress can be classified either asattenuation or as tolerance of the stress factor.“Attenuation” means that the impact of thestress factor is alleviated, while “tolerance“means increased resistance at the cellular level.Levitt (1972, 1980) makes a basic distinction ofescape versus resistance reactions, and subdi-vides “resistance” reactions into avoidance (equalto Larcher’s “attenuation”) and tolerance(Gibson, 1996: 8; Sitte et al., 2002). The term“avoidance” is prone to misinterpretation, and wetherefore prefer “attenuation” for this suite ofreactions.

“Tolerance” of the effects of water shortageresults in increased desiccation tolerance and isexemplified by poikilohydric plants (“resurrec-tion plants”). While homoiohydric plants main-tain their water status at the cellular level with-in a very narrow range, and rapidly develop non-recoverable cell damage followed by subsequentdeath, poikilohydric plants equilibrate theirwater content with that of the environment(Evenari, 1985). They can dry out completely (toenter a state of anabiosis; Evenari, 1985), andcontinue to live and grow when rewetted (e.g.lichens, Selaginella spp., Myrothamnus flabelli-folius). Their metabolism can be repeatedlyswitched on and off in reaction to availability orlack of water. Tolerance is due to modifications atcellular and metabolic levels.

“Attenuation” (“avoidance”) of the effects ofwater shortage can have several forms, of whichthe most common are drought-deciduous peren-nials (shedding leaves to minimize the transpir-ing surface), phreatophytes (perennials withdeep-reaching roots that tap underground waterresources), and succulents (storage of water tosupply sufficient water to allow active metabo-lism to continue). All these adaptations allow a

delay of desiccation under conditions of waterstress (Larcher, 2001: 336). Attenuation is large-ly due to structural modifications.

Fahn & Cutler (1992), taking up terms origi-nally introduced by Kearney & Shantz (1911,cited from Fahn & Cutler, 1992), call drought tol-erating and drought attenuating plants “droughtresistant xerophytes”, as opposed to “droughtescaping xerophytes”, such as therophytes anddrought-deciduous geophytes. This correspondsto three possible reactions of plants to droughtconditions: (1) escaping the stress factor, (2)attenuation of the stress factor, or (3) enduranceof the stress factor. In a strict sense, escaping thestress factor is a special case of stress attenua-tion in the sense of Larcher (2001), since surviv-ing the stress time in the form of seeds, or as dor-mant underground corms, rhizomes or bulbs, isessentially a complete attenuation of the stressfactor. The distinction between stress attenua-tion and stress tolerance is not absolute. Fahn &Cutler (1992) regard succulence as a phenome-non of stress tolerance, rather than stress atten-uation. Here we follow the more rigid applicationof the terms by Larcher (2001: 283) but note thatanother possibility (in line with Sitte et al., 2002:891 for frost tolerance) would be to classify suc-culence as a form of escape reaction, insofar assucculents due to their special morphology storeavailable water to avoid or at least alleviate prob-lems of water shortage at the level of the photo-synthetically active tissue.

Homoiohydric plants growing under condi-tions of temporary water-stress can also be clas-sified in a scheme of arido-passive versus arido-active plants (Evenari, 1985). Note that theseterms are not co-extensive with the terminologyused by Fahn & Cutler (1992). Arido-passiveplants survive the dry season in a largely dor-mant state (aestivation / hibernation, dormancy,quiescence, cryptobiosis), and the metabolicallyactive period (growth, flowering and fruiting) isprimarily controlled by the availability of water.Perennial arido-passive plants are usually geo-phytes or drought deciduous shrubs or trees,while seasonal annuals (pluviotherophytes;Evenari, 1985) survive in the form of seeds.Arido-active plants, on the other hand, continueto be at least in part metabolically active. Notethat Walter (1931) uses this term in a morerestricted sense for plants that maintain func-tional photosynthetic tissue during times ofdrought. Succulence is one of several possibleadaptations shown by arido-active plants.

Even though succulence is not a unique

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reaction of plants to periodical water shortage,succulents are a prime example of a successfuladaptive strategy (in the sense of having passedthe test of selection during evolution) and theconcomitant repeated independent evolution ofcertain characteristics, as we will show below.But before doing so, we have to ask: do we reallyknow what succulents are? Do we have a workingdefinition to decide whether a given plant is suc-culent?

History of the term “succulent“In ancient times and well through the MiddleAges, botany was merely part of what we wouldtoday call pharmacology. Only in the 17th centu-ry, botany started to became a proper and sepa-rate discipline, marked by the beginning of anarea that could be termed “descriptive botany“.Already much earlier, the Swiss botanist Johann(Jean) Bauhin (1541−1613) was the first to usethe term succulence (Rowley, 1997) (rather thanthe English botanist John Ray in 1682, as indi-cated by Wagenitz, 2003, or the Dutch JustusHeurnius in a description of Orbea variegata in1644, indicated by Stafleu, 1966). In a posthu-mously published classification of the plants thenknown to science, Bauhin classified a group ofplants as “herbae crassifolia et succulentae“ (i.e.,“thick-leaved and juicy herbs“) (Bauhin &Cherler, 1619, taken up and elaborated inBauhin & Cherler, 1650−1651), embracing taxaof the modern genera Agave, Aloe, Portulaca,Crassula, Rhodiola, Sedum etc. Bauhin specifi-cally restricted the group to leaf succulents, andthe same is true for the first key to succulentplants, published by Ray 1668 (Rowley, 1997).Ray (1668) was also the first to provide some-thing like a formal definition for his “succulentherbs“: “having thick juicie leaves, covered with aclose membrane, through which the moisturecannot easily transpire, which makes them con-tinue in dry places“ (cited from Rowley, 1997: 65).

“Succulentae“ was in continued use as agroup in plant classification well into the secondhalf of the 18th century, and later also includedthe cacti. With time, the “Succulentae“ becamemore and more a heterogenous assemblage, andthe grouping – still used by Linné as a “naturalorder” in his Philosophia Botanica (Linné, 1750:32) − soon disappeared in favour of “modern“ sys-tems starting with Linné’s famous “SpeciesPlantarum“ in 1753.

Definition of the term “succulent“Ray’s 1668 definition of his “succulent herbs“ isremarkably modern in so far as it includes char-acteristics from three different research fields: itcovers aspects of function and morphology (inmodern words: succulent leaves with a thickeneddermal system), physiology (reduced transpira-tion), and ecology (survival of arid conditions).Interestingly enough, the ecological componentwas already part of Bauhin’s first concept of suc-culence, insofar as Bauhin stated that the “suc-culentae” have the unique ability to remain aliveand grow when cut off at the root without addednutriment (cited from Rowley, 1997, our empha-sis). This part of Bauhin’s definition is an immi-nently practical approach and very close to themodern horticulturist’s approach to defining“succulence”. Not much has been added to Ray’sdefinition of succulents in subsequent years, andthere were no significant discussions of its appli-cation. An interesting addition to Ray’s concept isfound in the first ever book published on succu-lent plants by the Englishman Richard Bradley(?1688−1732, Rowley, 1997). Here, the title “TheHistory of Succulent Plants“ is supplementedwith a list of examples of genera included, plusthe statement “and such others as are not capa-ble of an Hortus-siccus“ (Bradley, 1716−1727). A“hortus siccus“ (literally a “dry garden”) is aherbarium, and Bradley obviously alluded to thedifficulty to press and dry specimens of succu-lents for the herbarium. The thousands ofherbarium specimens of succulents present todayin herbaria world-wide testify that Bradley wasnot quite right, but with the techniques availableat his time, preparing succulents for the herbari-um was certainly a challenge (Figures 3, 4).

The most general modern definition of succu-lence is given by von Willert et al. (1990: 135): “Asucculent is a plant possessing at least one suc-culent tissue. A succulent tissue is a living tissuethat, besides possible other tasks, serves andguarantees an at least temporary storage of uti-lizable water, which makes the plant temporarilyindependent from external water supply, whensoil water conditions have deteriorated such thatthe root is no longer able to provide the necessarywater from the soil“ [important concepts empha-sized by us in italics]. Subsequently (Willert etal., 1992: 6), the definition is clarified by the sup-plementary statement that “succulent tissuesmay develop in different plant organs“, and theterm “succophyte”* (footnote on p.16) is added asa synonym for “succulent plant”.

Aspects of morphology are not directly

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addressed in this definition, but much weight isplaced on aspects of physiology (storage in livingtissue, utilizable water) and functional ecology(temporarily independent from external watersupply).

The von Willert et al. 1990/92-definitionincludes two points of crucial importance:Utilizable water: the absolute amount of storedwater (expressed either as percentage of dry mat-ter, or as percentage of fresh weight) is of noimportance in connection with the ability to sur-vive arid conditions. The important figure israther, which part of the stored water is con-served against loss through transpiration andthat which can be accessed and consumed (“mobi-lized”, Fahn & Cutler, 1992) to maintain physio-logical activity without imposing undue risks onsurvival. With the possible exception of annuals,being “juicy“ is not in itself an adaptation to sur-vive droughts, if the stored water cannot be with-drawn from storage to be used to sustain life andperhaps even some growth until water becomesavailable again, and/or if there are no adapta-tions (thick cuticle, xeromorphic epidermis and,when present, hypodermis) to restrict transpira-tional loss. Gibson (1982: 1; 1996: 117) uses theterm “fleshy” (as opposed to “succulent”) forplants with watery leaves, which might be some-what tolerant to drought but cannot endure anysignificant water loss. Many halophytes andespecially hygrohalophytes fall into this category.These plants quickly wilt beyond recovery whenuprooted or cut off – very unlike the “true” suc-culents that continue to stay alive for months oryears. The amount of utilizable water is difficultand perhaps impossible to measure. It can beassessed indirectly by observing the water con-tent at the “point of no return” (i.e. imminentdeath) and comparing this value to the watercontent of the fully turgescent plant.Temporary independence from external water:although succulents are considered as primeexamples of desert plants, and even though theycontribute both in number and size to the land-scape of arid regions, succulents are not adaptedto survive prolonged droughts (e.g., Miriti et al.,2007, showing a higher survival rate for the non-succulent desert shrub Larrea tridentata than forthe succulent Cylindropuntia ramosissima dur-ing a period of exceptional drought in California).

With the exception of annual species, succulentsare especially adapted to grow in regions withperiodically occurring seasonal droughts, regu-larly and with statistical predictability followedby a rainy season that allows filling water stor-age to prepare the plant for the subsequent dryseason. In areas where precipitation comes atvery irregular intervals, and where the dry peri-ods regularly exceed a duration of 12 months,perennial succulents are notably underrepre-sented or even absent (Ellenberg, 1981; vonWillert et al., 1992).

Apart from being unnecessarily restrictive toapply only to terrestrial succulents (by referenceto the root and to soil water conditions), the vonWillert et al. 1990/92-definition is remarkablyinclusive and specifically covers a number ofgroups that are controversially discussed or thatare excluded in definitions by other authors (seeAppendix 1 for verbatim quotations of theirrespective definitions of succulence):� Succulence can occur in any systematic groupof plants. Restricting the term succulents toflowering plants as in the definition of Rowley(1980: 1) is unnecessary, and succulence cer-tainly occurs also in a small number of ferns(moderate leaf succulence in Pyrrosia (c. 11 outof 51 species) and Dictymia (1 of 2−3 species)(both Polypodiaceae)).

� Succulence is completely independent from lifeform. Restricting the term to perennial plantsas done by Gibson (1982) is unwarranted. Forsucculent annuals, the stored water allows aprolongaton of life time well into the dry sea-son, when especially flowering and fruitingoccurs independently from the availability ofsoil water, and is sustained by the stored water.Annuals are a special case of monocarpy. Deathis pre-programmed, and not being able to sur-vive the dry season is not contradictory to thedefinition of von Willert et al. (1990, 1992).

� Even though von Willert et al. (1992: 6) subse-quent to the definition refer to the necessitythat a succulent plant has in “refilling of itssucculent tissues“, the concept of a re-usablewater storage (also figuring in the definition ofsucculence by Fahn & Cutler, 1992) is not partof the original definition (Willert et al., 1990:134). While the idea of a recycling water storeis attractive at first glance (as also casually

*The linguistically barbarian term “succophyte” failed to get general acceptance; Google just finds 8 links as of 27th

Feb. 2009; and the linguistically more correct “chylophyte” [from Gr. `chylos’, juice, moisture] did not make it beyondan obscure dictionary [Vaczy, 1980; obviously derived from the terms `chylophyllae’ and `chylocaulae’ introduced bySchimper (Jackson, 1916)]; the term “chylophyte” is moreover also used for “plants growing on hard ground” [translated; Forêt, 2006], and its use should be discouraged to avoid confusion.

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mentioned by Ihlenfeldt, 1985), there is no rea-son for such a restriction – it would excludepopular and undisputed succulents such asspecies of Lithops or Bulbine. In Lithops, storedwater is completely transferred from the old tothe next younger leaves. Several species ofBulbine use all the water of the present sea-son’s leaf/leaves, and produce new leaves whenwater is becoming available again. They pro-vide striking examples of plant organs forwhich the total stored water is utilizable water.

� Succulent tissue can develop in any plant part.Any of the plant’s three basic organs (root,stem, leaf) can be modified as a whole or par-tially to engage in water storage (Goebel, 1889:45; Rowley, 1980; Fahn & Cutler, 1992). Apartfrom reasons of practicability regarding caudi-ciform and pachycaul plants, the restrictionput forward by Ihlenfeldt (1985: 410) and alsoaccepted e.g. by Wyka (2008) to call only thoseplants succulent that store water in organswith at least minimal photosynthetic activity,can be justified neither on physiological nor onecological grounds. The place where the wateris stored is unimportant as long as it is utiliz-able water that makes the plant temporarilyindependent from external water resources. Ifwater is stored in non-green plant organs, suchas roots or non-photosynthesizing leaf or stemparts, there is a division of labour betweenwater storage on the one hand and photosyn-thesis on the other hand. This division oflabour is comparable to that involved in the so-called “storage succulents“ (vs. “all-cell succu-lents“, Ihlenfeldt, 1985; Figures 5–8). Storagesucculents in the sense of Ihlenfeldt (1985)store water in photosynthetically active plantorgans, but not in the chlorophyll-containingtissue (e.g. Aloe, Gasteria, Lithops) (Figures 5,6, 8). Ihlenfeldt’s restricted usage of the termsucculent is likely based on Walter (1931: 112),who defines “active drought resistance” asdrought resistance of the photsynthetic organs.Walter (1931) makes no assumptions, however,on the location of the water storage in relationto the photosynthetically active organs.

� Succulent tissues can be derived from any ofthe plant’s basic tissue layers (medulla, vascu-lature/wood, cortex, phelloderm if present, epi-dermis, hypodermis if present, mesophyll), andwater storage is not necessarily the only func-tion of the tissue(s) involved. This latter pointis most notably exemplified by the “all-cell suc-culents“ as defined by Ihlenfeldt (1985), wherethe water-storage tissue is coextensive with the

photosynthetically active tissue (a common fea-ture of leaf-succulent Crassulaceae (Figure 7)and of many leaf-succulent Aizoaceae).

� There is no need to restrict succulence by defi-nition to those plants with a water storage tis-sue consisting of extra large, translucent, thin-walled parenchyma cells (Rowley, 1987), or towater storage tissues consisting of any type ofparenchyma (Newton, 1974b; Sitte, 2002). Thiswould exclude many leaf succulents where theepidermis is the primary water storage tissuesuch as Peperomia (Kaul, 1977) (Figure 8).

� Succulence is not a priori connected with phys-iological traits. While the CAM (CrassulaceanAcid Metabolism) pathway of photosynthesisoccurs amongst many succulents, it is neither aprerequisite of succulence nor a result of it. Therestriction of succulence to plants exhibitingCAM as in the definition of Rowley (1987) isunwarranted.

� Xerohalophytes, i.e. halophytic plants from dryclimates (as opposed to hygrohalophytes, i.e.halophytic plants not experiencing a shortageof water at any time of the year, e.g. Salicorniaspp. from sea shores), are not excluded by thevon Willert et al.-1990/92 definition. For xero-halophytes, aridity is both climatical andedaphical (through the salinity of the soil).

A unified definition of succulenceBased on the above discussion, and without mak-ing any a priori assumptions, succulence can bedefined as follows:Succulence = storage of utilizable water in liv-ing tissues in one or several plant parts in such away to allow the plant to be temporarily indepen-dent from external water supply but to retain atleast some physiological activity.This definition means:� The location of the water storage tissue is inde-pendent from the place of photosynthesis (all-cell succulence = storage in the photosyntheti-cally active cells; tissue succulence = storage ina non-chlorophyllous tissue either in the photo-synthesizing plant parts, or in different plantparts).

� Succulence is not connected with one or anoth-er photosynthetic pathway – in fact, all knownphotosynthetic pathways (C3, C4, CAM) occurin different species of succulents.

� At least a part of the stored water must be uti-lizable water.

� The utilizable water is used to maintain physi-ological processes during at least part of thedry season (“arido-active plants”, Evenari,

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1985; “actively drought resistant“, Walter,1931, Sitte et al., 2002).

� The water storage tissues can perform otherfunctions simultaneously.

� The water storage tissues are composed of liv-ing cells, ensuring that storage and withdraw-al of water is under active physiological con-trol, rather then passively following water con-tent gradients (as e.g. in Sphagnum mosses,Hájek & Beckett, 2008).

� The water storage tissue can be long-lived(“recycled“ over several seasons) or short-lived(“one-time use“ only).

The case o f caudic iform and pachycaulplantsThe question whether caudiciform and pachycaulplants are succulents or not is about as old as therevival of the term caudiciform itself by Rowley(1948). Rowley in his magnum opus on the sub-ject does not give a full answer, and his definitionof succulence falls short of our unified definitionprovided above in all three criteria he used(Rowley, 1987; see Appendix 1).

According to Ihlenfeldt’s (1985) restricted def-inition, neither caudiciform nor pachycaul plantsqualify as succulents because the water storageis (at least for the majority of taxa) not in thephotosynthetically active plant part. Gibson(1996: 15) gives some consideration to the subjectand concludes that the heterogenous assemblageof caudiciform and pachycaul plants, i.e. waterstorage primarily or exclusively in the stem orstem-root axis is “conveniently treated as succu-lents“. This view is implicitly shared by Lüttge(2008), who without hesitation uses the term“woody succulent trees” for pachycaul taxa in thefamilies Anacardiaceae, Malvaceae (incl.Bombacaceae, Sterculiaceae), etc., with non-pho-tosynthetic stems (as opposed to “fleshy stem suc-culents” for stem succulents with photosyntheti-cally active stems, such as cacti etc.). Smith et al.(1997) use the term “cryptic succulence” forpachycaul trees (but not for caudiciforms, whichare treated as a separate category of succulence),and Newton (2006) treats caudiciform and pachy-caul plants as “honorary succulents“, togetherwith bulbs and orchids. Already much earlier, hemade a distinction between caudiciform plantson the one hand, and succulent plants in thestrict sense on the other hand (Newton, 1974a).According to this classification, caudiciforms areengaging primarily in the storage of starch as areserve substance to allow rapid growth of a newshoot system at the start of the vegetation peri-

od, and survive the dry period as dormant geo-phytes. In contrast, succulents in the strict senseengage primarily in the storage of water, andhave no need for a large carbohydrate reservoir.Ihlenfeldt (1985), with his restricted definition ofsucculence, avoids the problematical distinctionbetween the two different storage strategies (car-bohydrates vs. water), and rightly points out thatthe majority of geophytes from arid and semi-arid climates would probably have some claim tosucculence.

The problems of how to distinguish succu-lents from non-succulents are, however, not agood reason to define pachycauls and caudici-forms ex cathedra as “not succulent“.Unfortunately, there are very little good dataavailable as to the nature of the storage organs ofcaudiciform plants. Rowley (1987), on the base ofcasual observations reported in old literature,mentions that the tuber of Ibervillea sonorae(Cucurbitaceae) is simultaneously a food andwater store, while both Cussonia thyrsiflora(Araliaceae) and Dioscorea elephantipes(Dioscoreaceae) have primarily water-storingtubers. Marloth (1908: 314–319) gives a watercontent of 97% for Dioscorea elephantipes, and95% for Cussonia thyrsiflora, and mentionsnumerous other taxa with geophytic storageorgans he considered as succulents. The detailedanalyses of Australian tuberous plants by Pate &Dixon (1981, 1982) show that conditions vary sig-nificantly among the species investigated. Theseauthors found large differences in total watercontent of the tubers at the start of the dry sea-son, varying from 2 – 95% of total fresh weight.Extreme cases were tubers of two species ofPentapeltis (Apiaceae) with water contents of95% (Pate & Dixon, 1981: 201, 213). Anatomicalstudies of the tubers of Pentapeltis deflexarevealed a highly parenchymatous tissue withoutany accumulation of reserve substances, whilereserves were found in the cell walls of P. pelti -gera (l.c., 212−13). These findings certainly mustbe interpreted as true succulence. These andother tubers lost only small proportions(1.2–8.2%) of the total stored water during dor-mancy, and the stored water is used to producenew shoots and/or flowers (hysteranthous flower-ing) towards the end of the dry period, but wellbefore the first rains were registered.

Similar findings are reported for the roottubers of the geophyte Asphodelus aestivus(Asphodelaceae) by Sawidis et al. (2005). Thetubers are the only surviving plant parts duringthe dry season, with a water content remaining

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above 70%. Water is stored in the large-celledparenchymatous cortex, and polysaccharide stor-age is confined to scattered dedicated carbohy-drate storage cells. No data are availablewhether the stored water is used to maintainphysiological activity during the dry season, or topromote growth before the availability of soilwater, and so it is uncertain whether A. aestivusshould be considered to be succulent or not.

In a discussion of pachycaul plants, Newton(1974b) defines succulence as water storage inparenchyma tissues. Since the prime example ofa pachycaul tree, the Baobab (Adansonia digita-ta, Malvaceae/Bombacaceae), stores most of itswater in the wood, it was not qualified as succu-lent by Newton (1974b), while Smith et al. (1997:ii) note that its stems are “fibrous rather thansucculent”. The studies of Chapotin et al. (2006)show, however, that parenchyma tissue makes up69−88% of the wood volume for MadagascanBaobabs. The total water content of the wood canreach 79%, and living cells occur to at least 35 cminto the wood (measured from the cambium; 35cm = maximum depth measurable with theequipment used). Good data for the AfricanBaobab are not available but is likely to be com-parable, and the presence of succulence can thusnot be denied. Moreover, about 10% of the totalstored water is used towards the end of the dryseason but well before the occurrence of firstrains for growing a new flush of leaves (Chapotinet al. 2006). Larcher (2001: 337) considers that“succulent wood plants” have a water content 2−6times that of other sympatrically occurringplants.

The case of succulent bulbsBulbous plants are not usually considered as suc-culents, although a few (e.g. Ornithogalum unifo-liatum, Hyacinthaceae; Rauhia spp.,Amaryllidaceae) certainly qualify by havingdecidedly succulent foliage leaves. Consideringthe bulb proper, an undisputable case of succu-lence is found in the genus Bowiea(Hyacinthaceae, 1 or 2 species, depending onauthority) with above-ground, green, succulentbulbs that qualify for succulence even under therestrictive definition of Ihlenfeldt (1985).

The problems of defining succulence in geo-phytic bulbs are the same as for caudiciformplants, and data are scanty. For the hyster -anthous geophyte Urginea maritima (Hyacinth -aceae), Al-Tardeh et al. (2008) found bulb watercontents of 79% during the vegetation period and67% during dormancy. The living, thickened bulb

scales show a large-celled parenchymatic tissuewith scattered mucilage cells, and have a highwater-storage capacity. The stored water is usedto produce the inflorescence during the dry sea-son, and based on the combination of presence ofwater storage tissue and physiological activityduring the dry season, U. maritima must be con-sidered succulent. Many other hysteranthousbulbs (i.e. bulbs that flower during or towards theend of the dry season) would equally qualify assucculents. Since bulb scales represent modifiedleaf bases, bulbs are merely a special case of leafsucculents characterized by having geophyticnon-photosynthesizing rosettes for water storagecoupled with seasonally deciduous foliage leavesfor photosynthesis. Numerous Tillandsia spp.show another extreme development of a bulb –here the succulent bulb (Horres & Zizka, 1995) isepiphytic and is provided with succulent or non-succulent foliage leaves for photosynthesis.

Succulence – a matter of degreeSucculence is a response to seasonally dry cli-mates, and in parallel to the gradual changesfrom very wet to very dry climatic conditions,succulence is likewise a matter of degree. Almostall authors discussing the definition and natureof succulence are aware of the associated difficul-ty by using statements such as “more than usu-ally fleshy“ (Rowley, 1980: 1), “complete series oflife forms from ... mesophytes ... to highly xero-phytic succulents“ (Rowley, 1980: 2), “store sig-nificant proportions of water“ (Ihlenfeldt, 1985:410), “a quality that can be possessed to a higheror lesser degree” (Willert et al., 1990: 133), or“thicker than expected” (Newton, 2006, forpachycaul plants). Very obviously there is noclear-cut boundary that separates succulentplants from non-succulent plants, and horticul-turists as well as hobbyists have long-standingarguments about “what is a succulent?” (e.g.West (1931) for an early voice; Rowley (1980:2−3); Smith et al. (1997: ii) as “contrieved succu-lence”). A good example of a gradual series frommesophytes to succulent xerophytes is foundamong the species of the genus Peperomia.Members of this genus also exemplify the impor-tance of environmental influences – insofar assome taxa have the capacity to become succulentunder conditions of restricted water availability,but are predominantly mesophytic under moremesic growing conditions. Many other groups ofleaf succulents show similar grades of succu-lence. The expression of succulence can also bedevelopmentally regulated: some species of

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Figure 1. Landscape with cacti (Echinopsis atacamensis) as example of stem succulents, occurring together with amultitude of shrubs and herbs in the Andes of Catamarca, N. Argentina. Figure 2. Landscape dominated by stemsucculent Euphorbia canariensis and E. balsamifera, growing together with many other shrubs and herbs onTenerife, Canary Islands.

1

2

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Figure 3. Example of a modern herbarium specimen (pressed and dried material) of Selenicereus setaceus. Figure 4. Herbarium specimen of Cactus grandiflorus (= Selenicereus grandiflorus) in the Linnean Herbarium(specimen LINN 633.1, by permission of the Linnean Society of London, www.linnean.org). Figure 5. Cross-section of a leaf of an unidentified Aloe species. This is a representative of “storage succulence” where water stor-age and photosynthesis are taking place in different tissues. Figure 6. Longitudinal section of the body (= pair offused leaves) of Lithops lesliei. This is another example of a storage succulent.

3 4

5 6

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Figure 7. Cross-section of a leaf of Cotyledon tomentosa ssp. ladismithiensis, showing all-cell succulence: waterstorage and photosynthesis takes place in the same tissue (= leaf mesophyll). Figure 8. Cross-sections of a leaf ofPeperomia nivalis. This is another example of a storage succulent, but here, a modified multi-layered epidermisserves as storage tissue. Figure 9 (a). Diversity of stem succulents (from left to right): Pelargonium paniculatum(Geraniaceae), Pittocaulon bombycophole (Asteraceae), Dioscorea basiclavicaulis (Dioscoreaceae), Euphorbiaevansii, E. sipolisii, Pedilanthus diazlunanus (all Euphorbiaceae), Dorstenia foetida (Moraceae), Kleinia longiflora (Asteraceae), Euphorbia tubiglans, E. alluaudii (both Euphorbiaceae), Portulaca molokiniensis(Portulacaceae), Adenia ballyi (Passifloraceae).

7 8

9a

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Figure 9 (b). Diversity of stem succulents (from left to right): Kleinia stapeliiformis (Asteraceae), Ceropegiadichotoma, Caralluma arachnoidea (both Apocynaceae), Kleinia obesa (Asteraceae), Cissus quadrangularis(Vitaceae), Selenicereus hamatus (Cactaceae), Echidnopsis sharpei, Stapelia grandiflora (both Apocynaceae),Dendrobium anosmum (Orchidaceae). Figure 9 (c). Diversity of stem succulents (from left to right): Euphorbiamayuranathanii (Euphorbiaceae), Beiselia mexicana (Burseraceae), Monadenium guentheri, Euphorbia gottlebei(both Euphorbiaceae), Alluaudia procera (Didiereaceae), Euphorbia venenata (Euphorbiaceae), Didierea trollii(Didiereaceae), Euphorbia viguieri (Euphorbiaceae).

9b

9c

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Figure 10 (a, b). Dioscorea basiclavicaulis (Dioscoreaceae): water storage in the fibrous-spongy primary parenchymatic tissue. The yellow spots are the primary vascular bundles, which are dispersed in the ground tissueas is typical for monocots. Figure 11 (a, b). Cyphostemma bainesii (Vitaceae): water storage in parenchymatouswood with many easily seen rays and a photosynthetically active outermost cortex.

10a 10b

11a 11b

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Figure 12 (a, b). Didierea trollii (Didiereaceae): water storage both in the medulla and in the cortex. The whitespaces in the cortex are mucilage ducts. Figure 13 (a, b). Euphorbia viguieri (Euphorbiaceae): water storage predominantly in the medulla, to a lesser extent also in the cortex.

12a 12b

13a 13b

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Figure 14 (a, b). Cereus validus (Cactaceae): water storage both in the medulla and the cortex. Figure 15 (a, b).Euphorbia venenata (Euphorbiaceae): water storage both in the medulla and the cortex.

14a 14b

15a 15b

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Figure 16 (a, b). Austrocylindropuntia subulata (Cactaceae): water storage predominantly in the medulla; vascularcylinder highly irregular and little-developed. Figure 17 (a, b). Monadenium guentheri (Euphorbiaceae): waterstorage both in the medulla and the cortex.

16a 16b

17a 17b

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Figure 18 (a, b). Euphorbia mayuranathanii (Euphorbiaceae): water storage predominantly in the medulla, to alesser extent also in the cortex. Figure 19 (a, b). Kleinia obesa (Asteraceae): water storage almost exclusively in themedulla. The round dot-like structures are mucilage ducts.

18a 18b

19a 19b

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Figure 20 (a, b). Desmidorchis speciosa (Apocynaceae): water storage both in medulla and cortex. The vascularsystem is particularly weakly developed and hardly visible. Figure 21 (a, b). Cissus quadrangularis (Vitaceae): waterstorage almost entirely in the medulla, with particularly weakly developed vascular system. The pellucid dots aremucilage ducts.

20a 20b

21a 21b

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Figure 22 (a, b). Hoodia gordonii (Apocynaceae): water storage both in medulla and cortex, with particularlyweakly developed and almost invisible vascular system. Figure 23 (a, b). Calymmanthium substerile (Cactaceae):water storage predominantly in the cortex.

22a 22b

23a 23b

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Figure 24 (a, b). Echinopsis strigosa (Cactaceae): water storage almost exclusively in the cortex, with well visiblevascular strands leading to the areoles. Figure 25 (a, b). Borzicactus fieldianus (Cactaceae): water storage almostexclusively in the cortex, with well visible vascular strands leading to the areoles, and anastomosing cortical bundles.

24a 24b

25a 25b

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Figure 26. Cumulopuntia chichensis (Cactaceae): water storage in the stem (right) is in the medulla and the cortex,while in the root (left), water storage is in secondary xylem and phloem.

26

Peperomia have succulent leaves when growingvegetatively, but produce larger, non-succulentleaves once inflorescence development begins.

In many other plants from water-limitedecosystems, succulence is more subtle and lesseasily seen. Volkens (1887) describes severalexamples where minimal water storage tissuesare clearly present (characterized by the com-plete or almost complete lack of chloroplasts) butlimited to a couple of cell layers, e.g. in the cen-tral part of leaves. Shields (1951) made similarobservations for several species of Haplopappus,Chrysothamnus and Senecio (all Asteraceae)from White Sands National Monument, NewMexico, USA and describes how the cells of thewater storage tissue, however minimal it may be,are the first to lose turgor and contract and even-tually reversibly collapse supported by undula-tions developed in radial cell walls, obviously asa result of the transfer of water from the waterstorage tissue to the chlorenchyma. Species ofFouquieria possess a non-succulent cortex tra-versed by a network of anastomosing strandsthat consist of thin-walled parenchyma, whichfunctions as water storage tissue (Scott, 1932;Humphrey, 1935). While such plants do not showexternal succulent properties, they certainlyfunction like succulents at the cellular level.

They clearly illustrate the impossibility to draw aclear line between succulent and non-succulentplants.

The sheer number of plants regarded as suc-culent (between 12,000 and 13,000, put forwardas a working hypothesis by Eggli (2007)) testifiesthe success of this adaptive strategy to cope withseasonally arid conditions. Succulence occurs in30 out of about 50 orders currently recognized forthe Angiosperms (APG, 2003). As succulence hasnot been identified as ancestral character for anyof the deeper nodes in the phylogeny ofAngiosperm orders, it must have evolved inde-pendently at the very least 30 times, i.e. at leastonce in each order. The total number of indepen-dent occurrences of succulence is, however, with-out doubt significantly higher, since even withinfamilies (e.g. Apocynaceae) succulence hasevolved repeatedly in different phylogenetic lin-eages.

Stem succulents: morpho-anatomical diver-sity exemplifiedStem succulence and the “cactus life form“ isoften regarded as the prime example of an adap-tive strategy, and it is frequently cited as a “text-book case“ of convergent adaptive evolution in anenvironmental context in which concerted

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evolutionary changes are prevalent (Futuyma,1997; Niklas, 1997). The evolution of stem succu-lence is an important functional adaptation asexemplified by its diversity (c. 3,950 species, i.e.about 1/3 of the total number of succulents).

Almost all of the stem tissues (from centre toperiphery: medulla, wood, cortex, phelloderm ifpresent, hypodermis if present, epidermis forDicotyledons; primary parenchyma for Mono -cotyledons) can be involved in the storage ofwater, and the diversity of morphological solu-tions to resolve the challenge of building a waterstore is amazing. The overall external similarityof stem succulents from an array of differentplant families (Figures 9a, b, c) is both striking aswell as grossly misleading, and can make theidentification of sterile material difficult attimes. The parallel development of external mor-phological features (homoplasious evolution,Futuyma, 1997: 220−221) conceals widely differ-ent internal architectures (Figures 10−25). Inaddition, even within a plant, water storage indifferent plant parts can be radically different asto anatomy: while stems of cacti store water pre-dominantly in the enlarged cortex and to a lesserdegree in the medulla, enlarged roots store waterin secondary xylem and phloem, and no cortex ispresent (Mauseth & Stone-Palmquist, 2001;Stone-Palmquist & Mauseth, 2002) (Figure 26).An overview of anatomical features of photosyn-thetic succulent stems, and especially of the rela-tive importance of cortex and medulla for waterstorage, is presented by Mauseth (2004; 28species from 7 families, limited to species withenlarged medulla and/or cortex).

The evolution of stem succulence can simulta-neously be interpreted as the product of conver-gence and parallelism, depending on the focusand the definitions used. In the context of a mor-phology-based view, stem succulence is a case ofparallel evolution: the plant axis (stem) of plantsnot closely related to each other has indepen-dently evolved similarities in appearance andfunction as the result of adaptation to the samestress factor, i.e. temporary water shortage. Thefocus is at the level of plant parts, i.e. the sameorgan (stem) developed similar traits in unrelat-ed taxa, and the case is simultaneously both oneof analogy and of homology (analogy = similarityof structure or function; homology = property ofcommon ancestry). In the context of an anatomy-based view, stem succulence is a case of conver-gent evolution, since different tissues have devel-oped in a similar way to serve as water storage,and the case is one of analogy, since different tis-

sues assumed a similar function by convergentadaptive evolution.

In the context of a phylogeny-based view,stem succulence is also a case of convergent evo-lution: according to phylogenetic terminology,convergence is the independent evolution of sim-ilar forms in unrelated taxonomic groups asadaptation to similar environmental conditions.The “cactus form”, i.e. spiny succulent photosyn-thetic stems such as those of New World cacti(Cactaceae) and Old World euphorbs(Euphorbiaceae), is the commonly cited textbookexample for convergent adaptive evolution (e.g.,Niklas, 1997; Stearns & Hoekstra, 2005).

ConclusionsSucculence has repeatedly evolved independentlyas a conspicuous adaptation to temporarily aridconditions. About 4% of all extant species of high-er plants can be classified as succulents (12,000 –13,000 out of c. 260,000 species). The diversity ofsucculent plants is an illustrative “text bookexample“ for adaptive evolution in the form ofnatural selection under conditions of limitedresources. Succulence is a matter of degree andits expression is environmentally modified inmany taxa. The definition of succulence is a com-bination of morphological/anatomical considera-tions (storage in living tissues of one or severalplant parts), ecological conditions (occurrence intemporarily arid environments), and physiologi-cal aspects (spending utilizable water in physio-logical processes such as photosynthesis orgrowth / flowering during the dry season).

AcknowledgmentsA word of thanks goes to the administration ofthe Sukkulenten-Sammlung Zürich of GrünStadt Zürich for supplying the plant materialused to illustrate this paper. Gordon Rowley’sthoughtful comments on an earlier version of thispaper have been very helpful. Nicolas Ruch haskindly helped with the photography of stem suc-culents.

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Appendix 1. Verbatim citations of recent defi nitions for “succulence” (chronological list)

Newton (1974a: 15): “Succulent plants haveshoots with water-storage tissues in either theleaves or the stems, and these shoots are usuallyperennial”.

Newton (1974b: 57): “Succulent plants are char-acterised by the possession of water-storageparenchyma, sometimes called aqueous tissue. …In water-storage parenchyma the cells are largeand contain a lot of mucilage, and water is stored

by being held in the mucilage. … A biochemicalfeature associated with succulent plants is`Crassulacean Acid Metabolism’…”.

Rowley (1980: 1): “Succulents are defined as flow-ering plants in which the leaves, stems or rootshave become more than usually fleshy by thedevelopment of water-storage tissues”.

Gibson (1982: 1): “The term `succulent’ has beenused to describe perennial plants having greatlythickened vegetative organs that are modified tostore large quantities of water”.

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form cult. Nation. Cact. Succ. J. 29: 14–17.NEWTON, L.E. (1974b). Is the Baobab tree

succulent? Cact. Succ. J. Gr. Brit. 36: 57–58.NEWTON, L.E. (2006). Honorary succulents. Succ.

News 14(3): 11–12.NIKLAS, K.J. (1997). The evolutionary biology of

plants. The University of Chicago Press,Chicago.

PATE, J.S. & DIXON, K.W. (1981). Plants withfleshy underground storage organs – aWestern Australian survey. In PATE, J.S. &MCCOMB, A.J. (eds.) The biology of Australianplants. University of Western Australia Press,Nedlands, pp. 181–215.

PATE, J.S. & DIXON, K.W. (1982). Tuberous, cormous and bulbous plants. Biology of anadaptive strategy in Western Australia.University of Western Australia Press,Nedlands.

ROWLEY, G.D. (1948). Caudiciform succulents.Nation. Cact. Succ. J. 3: 102–103.

ROWLEY, G.D. (1980). Name that succulent. Keysto the families and genera of succulent plantsin cultivation. Stanley Thornes (Publishers)Ltd., Cheltenham.

ROWLEY, G.D. (1987). Caudiciform and pachycaulsucculents. Pachycauls, bottle-, barrel- andelephant-trees and their kin: A collector’s mis-cellany. Strawberry Press, Mill Valley.

ROWLEY, G.D. (1997). A history of succulentplants. Strawberry Press, Mill Valley.

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P., WEILER, E.W., KADEREIT, J.W., BRESINSKY,A. & KÖRNER, C. Lehrbuch der Botanik fürHochschulen. Ed. 35. Spektrum Akade -mischer Verlag, Heidelberg / Berlin.

SMITH, G.F., JAARSVELD, E.J. VAN, ARNOLD, T.H.,STEFFENS, F.E., DIXON, R.D. & RETIEF, J.A.(eds.) (1997). List of Southern African succu-lent plants. Umdaus Press, Pretoria.

STAFLEU, F.A. (1966). Haworth’s complete works.Taxon 15: 274–276.

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STONE-PALMQUIST, M.E. & MAUSETH, J.D. (2002.)The structure of enlarged storage roots incacti. Int. J. Pl. Sci. 163: 89–98.

SWARTZ, D. (1971). Collegiate dictionary ofbotany. Ronald Press Company, New York.

VACZY, C. (1980). Lexicon Botanicum Polyglottum.Editura Siintifica si Enciclopedica, Bucuresti.

VOLKENS, G. (1887). Die Flora der aegyptisch-ara-bischen Wüste auf Grundlage anatomisch-physiologischer Forschungen. GebrüderBorntraeger, Berlin.

WALTER, H. (1931). Die Hydratur der Pflanze undihre physiologisch-ökologische Bedeutung(Untersuchungen über den osmotischen Wert).Verlag von Gustav Fischer, Jena.

WEST, J. (1931). What is a succulent? Cact. Succ.J. (U.S.) 3: 71–72.

WILLERT, D.J. VON, ELLER, B.M., WERGER, M.J.A.& BRINCKMANN, E. (1990). Desert succulentsand their life strategies. Vegetatio 90:133–144.

WILLERT, D.J. VON, ELLER, B.M., WERGER, M.J.A.,BRINCKMANN, E. & IHLENFELDT, H.-D. (1992).Life strategies of succulents in deserts. Withspecial reference to the Namib desert.Cambridge University Press, Cambridge.

WYKA, T. (2008). Water tissues of succulents. Part1. Kaktusy i Inne 5(1): 4–11.

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Rowley (1987: 25): “1. Water storage tissue madeup of extra large, translucent, thin walledparenchyma cells, often polyploid, with mucilageand often air spaces. 2. High water content. 3.CAM respiration”.

Fahn & Cutler (1992: 90): “Succulents aredrought tolerant plants. They store in their bodyconsiderable amounts of water, which duringdrought can be mobilized and used to maintainessential life processes, such as maintenance ofmeristems and for survival of other vegetativecells. When water is available again the water-storage tissues are refilled, i.e. the process ofwater mobilization is reversible.” (l.c. p. 92):“Conventionally, the succulents are divided intoleaf-, stem- and root-succulents”.

Willert et al. (1992: 6): quoted verbatim in thetext above (p. 15).

Smith et al. (1997: ii): “A succulent is … a plantthat stores water in its tissues as a mechanism tosurvive periods of drought in the growing phase”.

Sitte (2002: 123, translated): Succulence: “Plantsof very dry habitats, which remain active evenunder prolonged water shortage, and which storewater in the vacuoles of extremely enlargedparenchyma cells (diameter up to 0.5 mm)(hydrenchyma). The respective plant organsbecome visibly swollen, their volume is enlarged,and the surface diminished”.

Newton (2006: 11): “Succulent plants are usuallydefined as plants with water storage tissues,enabling them to survive long periods ofdrought”.

G. D. Rowley (2009, pers. comm.): “A succulentplant is any plant that looks right and grows wellin a succulent [plant] collection”.

Appendix 2. Glossary of selected technicalterms (cf. Lincoln et al., 1998, and other sources)anabiosis: a state of greatly reduced metabolicactivity assumed during unfavourable environ-mental conditions.

arido-active: used of plants that remain metabol-ically active during times of water stress, employ-ing mechanisms such as improved water uptake,water storage, efficient water conduction orreduction of transpiration.

arido-passive: used of plants that are sensitive todrought, and which survive periods of waterstress by the production of desiccation resistantseeds or structures.

cryptobiosis: a state where all external signs ofmetabolic activity are absent from a dormantorganism.

evapotranspiration: the total potential loss ofwater by evaporation from the ground, and bytranspiration from the vegetation, expressed perunit area and time.

halophyte: a plant that can tolerate high salt con-centrations in the soil. hygrohalophyte: a halo -phyte growing in permanently wet soil / xero-halophyte: a halophyte growing under climatical-ly arid conditions.

homoiohydric : said of plants that regulate theirwater status to maintain it at a given level inde-pendent of ambient humidity.

hygrohalophyte: ➞ halophyte.

hysteranthous: producing foliage leaves after theflowering season.

phreatophyte: a plant with long roots that accessthe permanent water table of the soil.

pluviotherophyte: a therophyte that only germi-nates after heavy rainfall and rapidly completesits life cycle while soil moisture conditionsremain adequate.

poikilohydric : said of plants than cannot regulatetheir water status, which therefore follows ambient humidity levels. Under extremely dryconditions, poikilohydric plants enter a state ofanabiosis or cryptobiosis.

synanthous: producing foliage leaves simultane-ously with the appearance of the inflorescence.

therophyte: an annual plant that completes itslife cycle from germination to seed within a sin-gle season.

xerohalophyte: ➞ halophyte.