What Did the First Look like? An Attempt to Reconcile the Morphological and Molecular Evidence Author(s): M. Patrick Griffith Source: Taxon, Vol. 53, No. 2 (May, 2004), pp. 493-499 Published by: International Association for (IAPT) Stable URL: http://www.jstor.org/stable/4135628 . Accessed: 03/12/2014 10:33

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This content downloaded from 192.135.179.249 on Wed, 3 Dec 2014 10:33:44 AM All use subject to JSTOR Terms and Conditions TAXON 53 (2) ' May 2004: 493-499 Griffith * The first cactus

What did the first cactus look like? An attempt to reconcile the morpholog- ical and molecular evidence

M. Patrick Griffith

Rancho Santa Ana Botanic Garden, 1500 N. College Avenue, Claremont, California 91711, U.S.A. michael.patrick. [email protected]

THE EXTANT DIVERSITYOF CAC- EARLYHYPOTHESES ON CACTUS TUS FORM EVOLUTION Cacti have fascinated students of naturalhistory for To estimate evolutionaryrelationships many authors many millennia. Evidence exists for use of cacti as food, determinewhich morphological features are primitive or medicine, and ornamentalplants by peoples of the New ancestral versus advanced or derived. One assumption World for at least 9,000 years (Anderson, 2001), and often made (Bessey, 1915; Cronquist, 1981) is that a cacti have captivated the attention of Old World plant common morphologicalstate (one sharedby many mem- scholars, agriculturists,and hobbyists since their intro- bers of a group) should be considered a primitive condi- duction in the late 15thcentury. The strikingvisual aspect tion. Among cacti, many traits are common, such as of the succulent, spiny, often leafless has received spininess and polytepaly, and we might safely assume much attention, and botanists have been pondering their that these represent ancestral conditions for the extant evolutionaryrelationships for over a century. cacti. But, as cacti are highly specialized plants, it is dif- Three subfamilial groups have been traditionally ficult to determinewhich characterstates are ancestralor recognized within Cactaceae. The easiest group to cir- derived relative to other angiosperms. cumscribe morphologically is , with min- The question of the Cactaceae's relationshipto other ute, barbed, deciduous spines (termed glochids), and plants has long been addressed morphologically. In an small, often ephemeral . Additionally, Opuntioi- extremely influential early work, N. L. Britton and J. N. deae have a bony seed aril (Vaupel, 1925; Anderson, Rose (1919) hypothesized that the leafy 2001). This subfamily includes the familiarprickly pears (Fig. 1C) was the closest relative to other angiosperms, of the genus Mill. (Fig. lA), plus many other and the leafy opuntioid genus Britton & morphotypes.Another large group of cacti are subfamily Rose (Fig. ID) was the closest relative of Pereskia , which include leafless, spiny stem succu- among the other cacti; in other words, Pereskia repre- lents such as the genus TrichocereusRiccob. (Fig. 1B). sented a primitive morphology, Opuntioideae a some- Cactoideae are very diverse in habit and morphology, what more advanced morphology, and Cactoideae and the vast majorityof describedcactus fall into (Cereae sensu Britton & Rose) a very derived morpholo- this group. The remaining subfamily Pereskioideae gy (Fig. 2). This early phylogenetic hypothesis includes leafy, spiny, often non-succulent trees and (Pereskia-as-primitive)has had a great impact upon fur- of the genus Pereskia Mill. (Fig. 1C). ther work. Most subsequent treatments advance this In addition to these three long- and widely-recog- hypothesis without taking a strong stand on the other nized subfamilies, recent molecular evidence supports subfamilial relationships (e.g., Cronquist, 1981; also the recognition of a fourth subfamily of cacti, the mono- Gibson & Nobel, 1986; Barthlott & Hunt, 1993), while generic Maihuenioideae (Wallace, 1995a, b; Nyffeler, some recent phylogenetic papers even state this hypoth- 2002). Phil. contains two little-studied esis as well-supported (Hershkovitz & Zimmer, 1997; species of smaller, succulent, cushion-formingcacti that Martin & Wallace, 2000), even when the data cited or are restricted to western and southern South America presented therein may not support this conclusion (see (Leuenberger,1992a, b; 1997; Mauseth, 1999), and were below). Morphological and anatomical studies of variously included in Opuntioideae and Pereskioideae Pereskia also supportthat these plants possess characters [and at times in a broadly circumscribed Cactoideae: found in other dicot families (Leuenberger, 1986; Vaupel, 1925 (as Malacospermae); Hunt & Taylor, Mauseth & Landrum, 1997; Landrum,2002) including 1986]. ordinary dicot wood and broad leaves. Most notably however, some Pereskia species possess superiorovaries ((A. Berg.) Knuth), a characterstate that is

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Fig. 1. Examples of the diversity of extant cactus form that may illuminate early cactus evolution. All plants pictured here are growing at the Huntington Botanical Gardens, San Marino, California, U.S.A. A, an example from subfamily Opuntioideae: Opuntia robusta Wendl. The jointed stems are typical for this subfamily, although the stem segments may be of various shapes. Glochids and bony seed arils also hold this group together morphologically. B, a represen- tative of Cactoideae: Trichocereus pasacana Britton & Rose. Members of this subfamily lack leaves and glochids. Other architectural diversity of this subfamily can be seen in the background and foreground. C, Pereskia grandifolia, in Pereskioideae. The non-succulent woody shoots and abundant foliage of these plants may have led Britton and Rose (1919) to declare them the most primitive cacti. D, Pereskiopsis aquosa (F. A. C. Weber) Britton & Rose. The glochids and seed structure led Britton & Rose (1919) to place this taxon in Opuntioideae, and this has been confirmed by molecular analyses (Griffith, 2002; Wallace & Dickie, 2002). E, Anacampseros lanigera Burch. (Portulacaceae). Diminutive, succulent plants like this are the closest extant relatives of Cactaceae (Hershkovitz & Zimmer, 1997; Applequist & Wallace, 2001). F, glomerata (Haw.) R. Kiesling (Opuntioideae). Such a taxon is probably plesiomorphic within Opuntioideae, and may possibly represent many character states of the earliest cacti.

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Cactoideae

All other z Opuntioideae 0 'Iv E

Pereskiopsis

Pereskia

Other Dicots

Fig. 2. Phylogram depicting traditional (and widely accepted) morphological phylogeny of Cactaceae, adapted from Britton & Rose (1919), with a primitive Pereskia and highly derived Cactoideae (Cereae sensu Britton & Rose). Character evolution depicted here: i, a woody, broad-leaved common ancestor of Cactaceae, reduction of short shoots into areoles and bud scales into spines; ii, development of succulent stems; iii, development of glochids and bony seed arils (Opuntioideae); iv, reduction of leaves to terete-succulent and mostly ephemeral; v, complete loss of leaves (Cactoideae). often relictual (Cronquist, 1981; Takhtajan, 1991). whether it representsthe early morphology of Cactaceae Shared morphological characters, however, may occa- is not clear. It is difficult to drawphylogenetic inferences sionally reflect convergent adaptationvia natural selec- and determineplesiomorphies without referenceto a spe- tion instead of, or in addition to, reflecting close evolu- cific outgroup.The work of Britton and Rose remains an tionaryrelationship. invaluable contributionto our knowledge of cacti, but it The Pereskia-as-primitive hypothesis is supported is possible that the morphologicalevolutionary hypothe- by other evolutionary considerations. One often-pro- ses presentedtherein may be influenced by possible bias posed mechanism for evolution in Cactaceae that is a toward the temperate, mesic, broad-leaved regions that naturalcorollary of the Pereskia-as-primitiveidea is pae- they (and many 19thand 20thcentury botanists) inhabited domorphicreduction or neotony (Boke, 1944; Buxbaum, and knew so thoroughly; even if a broadleaf can 1956; Anderson, 1986). If the first cacti were leafy trees (perhaps)be thought of as a typical dicot, the closest rel- or shrubs, many extant cacti would be considered atives to cacti still might not fit this concept. reduced forms. Recent theoretical work, however, pro- Morphologies of organisms are subject to and influ- poses that increased size (of plants with a conserved enced by environmental pressures; natural selection shape) may be adaptive in cacti (Mauseth, 2000, 2004), operates on the forms of plants, resulting in the diverse and might then represent a derived character state in adaptations we now see. Perhaps the non-cactus-like some Cactoideae and Opuntioideae. This would not shoots and leaves of Pereskia represent an example of apply to Pereskia, however, as this genus probably has convergentevolution via naturalselection. Recent phylo- the highest surface area/volumeratio of any cacti. genetic researchmay provide insight into this question. Pereskia certainly does resemble other non-cacta- ceous plants morphologically and anatomically, but 495

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lent shrubs and trees similar to Pereskia). Also men- WHAT IS THE MOLECULAREVI- tioned (briefly) was the possibility that cacti in non-arid DENCE? environmentsmight be descended from cacti that were An extremely useful feature of molecular phyloge- arid-adapted,although this was not discussed in context netics is its ability to informus about characterevolution. of the Pereskia-as-primitivehypothesis. Molecular phylogenetic research of Cactaceae has been Martin & Wallace, 2000. - This important slower to develop than in other groups, but a growing paper investigated the photosynthetic modes of cactus body of evidence is now available to begin to test leaves in a phylogenetic context. The authorsadvanced hypotheses about cactus evolution. Recently published the phylogenetic hypothesis that Pereskia representsan work presents independent molecular phylogenies that ancestral character suite and lineage among are not entirely consistent with the Pereskia-as-primitive Cactaceae, and that persistent leafiness is a primitive hypothesis. Although some do advance this hypothesis, character state within Opuntioideae and Cactaceae. often uninformativedata, or data that are in conflict with However, the patternof relationshipsdisplayed (derived that conclusion, are presented. This work is briefly from restriction site and rp116 cpDNA sequence data) reviewed and summarizedbelow: actually supports three equivocally deep clades Wallace, 1995a. - This importantearly paper on (Opuntioideae, Maihuenioideae, and Pereskia + the molecular of Cactaceae presented a Cactoideae), again suggesting that opuntioids or phylogeny of the genus Pereskia in which five lineages Maihuenia may be relatively older than Pereskia. were shown forming a basal polytomy for the group. In Phylogenetic relationships were not the main focus of other words, the relationshipsamong these five lineages this paper,however. were unclear. A landmark paper in cactus evolution Applequist & Wallace, 2001. - Furtherinsight (Hershkovitz & Zimmer, 1997; discussed below) cited into the closest outgroups of Cactaceae is found in this Wallace (1995a) as providing molecular evidence that paper,which demonstratesa close phylogenetic relation- Pereskioideae are basalmost within Cactaceae, but this ship between Cactaceae and diminutive, stem-succulent conclusion was not stated or supported.Wallace present- geophytic or caudiciform members of Portulacaceae, ed either three (Maihuenia, Pereskia + Cactoideae, and such as Anacampseros (Fig. 1E), Grahamia Gill., Opuntioideae), or four (each subfamily) distinct early- Portulaca L., Talinum,and Talinopsis A. Gray. As in diverging lineages, not fully resolved by the data. Hershkovitz& Zimmer (1997), the relationshipsamong Interestingly,in one analysis Pereskia and one represen- subfamilies of cacti were not well resolved (although in tative cactoid (Leptocereus quadricostatus Britton & one analysis Opuntioideaeappear sister to Pereskioideae Rose) formed an unresolved clade distinct from and Maihuenioideae).Again, the morphologicalrelation- Maihuenia and Opuntioideae;this relationship actually ships of these diminutivesucculents to Pereskia were not suggested that Maihuenia and/or Opuntioideae may be addressed. relatively older than Pereskia. Nyffeler, 2002. - Recent, thoroughwork demon- Wallace 1995b. - This importantwork began a strated that the deepest lineage within subfamily recent movement to recognize a fourth subfamily of Cactoideae is the diminutive, succulent genus Cactaceae, Maihuenioideae(Wallace, 1995b; Anderson, Blossfeldia Werderm.This finding generatescontroversy 2001), as it representsa deep lineage within the family. (Gorelick, 2002) because although it challenges morpho- This monogeneric subfamily contains two species of logical phylogenies based on the Britton and Rose con- diminutive, mat- or cushion-forming cacti with terete- cept, it parallelswhat the earlierpapers (above) have pre- succulent leaves; i.e., one of the earliest-divergingcactus dicted, and what current work (below) supports--that groups would be comprised of diminutive succulents. diminutive, stem-succulent(often geophytic) plants rep- Maihuenia was found to be as different from the other resent deep lineages in Cactaceae. Also supportedhere subfamilies as they are from each other. (but less robustly) is the traditional hypothesis that Hershkovitz & Zimmer, 1997. - This paper Pereskia species are early-diverging lineages in sampled three genera of cacti believed to be relictual Cactaceae, yet they appear paraphyleticwith respect to (Maihuenia,Pereskia, and Pereskiopsis), but the resolu- other cacti. tion among these genera (in different subfamilies) was Wallace & Dickie, 2002. - A recent paper pro- unclear.The very importantconclusion (and focus of this posed that the (often leafy) genus paper) however, was that Cactaceae are nested within Backeb. is deepest ("basal"sensu Wallace) within sub- Portulacaceae.Some nearest relatives of Cactaceae pre- family Opuntioideae,although their data actually do not dicted by this work are Anacampseros L. (Fig. iE), support this conclusion (five equivocally deep lineages TalinumAdans., and Talinella Baill., which are diminu- are shown, not one). However, the authorsnote contra- tive and often succulent (and not broadleaf, semisuccu- diction with the Britton & Rose (1919) hypothesis that

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Pereskiopsisis the mostprimitive opuntioid. Blossfeldia, Maihuenia, and Maihueniopsis in many Griffith, 2002, 2003. - This work focusing on cases share the following characters: morphological relationships among subfamily Opuntioideae provided reduction, terete or globular stem shape, and absence of preliminaryevidence that Opuntioideae may be sisterto broad, persistent,nonsucculent leaves. Additionally, all othercacti, i.e., that opuntioidsmight represent the Maihueniopsis and Maihuenia include geophytic deepestlineage. This researchsupports a deep lineage species. Also, all three genera are restricted to western (and possibly an ancestral character suite) for and southern South America, where Cactaceae are pre- Opuntioideaethat is representedby extant members of sumed to have arisen (Griffith, 2002; Nyffeler, 2002; the genus Maihueniopsis Speg., a diminutive, stem-suc- Wallace & Dickie, 2002). culent, often geophytic taxon (Fig. IF). Additonally,this 4. - The nearest outgroupspredicted for Cactaceae work demonstrates that persistent leafiness (as in the by recent phylogenetic studies are diminutiveportulaca- genera Austrocylindropuntia, Pereskiopsis, and ceous succulents, including the genera Anacampseros, Britton & Rose) represents a derived mor- Talinum, Talinella, and Portulaca (Hershkovitz & phological characterstate in Opuntioideae. Zimmer,1997; Applequist & Wallace,2001). None of these could rightly be considered a woody, broad-leaved treeor shrubsimilar to Pereskia;in fact,Pereskia wood may be considered uniquely ordinary in all of (J. Mauseth, pers. comm.). PROBLEMSWITH THE MOLECU- The consensus. - The the LARMODEL relationships among subfamilies are not clearly understood,and Opuntioideae A consensus of evolutionaryinferences gleaned may represent the deepest lineage of Cactaceae. The from moleculardata suggests that an alternativeto the deep lineagesof all subfamiliesinclude geophytic stor- Pereskia-as-primitivehypothesis might be considered. age tissues, and all deep lineagesexcept Pereskioideae Some of the reasonsfor reopeningthis discussionare arearchitecturally simpler plants. The nearest relatives to summarizedbelow. cacti are not woody, broadleafshrubs and trees like I. - The relationshipsamong the subfamiliesof Pereskia, but succulent Portulacaceae,often with Cactaceaeare not clear.There is conflictamong the deep reduced leaves and geophytic tissues. All deep lineages lineages recovered by recent phylogenetic studies of Cactaceae are found in west-central and southern (Griffith,2002; Nyffeler, 2002), althoughneither analy- South America (Anderson,2001). A conceptualmodel of sis is incorrect;both presentstatistically rigorous infer- cactus evolution based on a consensus of the new data is ences of the historyof the genes sampled.Other work presentedin Fig. 3. Looking only at the available molec- does not fully resolve these lineages,yet often places ular evidence, it seems possible that the first cactus may Pereskiain a relativelyderived position (Wallace, 1995a; have been a diminutive, portulacaceous succulent (and Martin& Wallace,2000; Applequist& Wallace,2001). possible geophyte) that evolved spines, and diversified Onepaper that does restatethe traditionalview does not into the extant cactus flora we now observe. Pereskia present or cite molecular phylogenetic support for it may representan early (but not necessarily the earliest) (Hershkovitz & Zimmer, 1997). Pereskia may represent lineage of cacti, which evolved broad leaves and woody a derivedlineage, or perhapsthere occurred a rapidradi- stems as it adaptedto a non-aridenvironment, gaining an ationof cacti at theirorigin, and the currentlyavailable overall appearance more convergent with ordinary molecularphylogenetic data may not be enoughto fully dicots. resolve this pattern of relationship (R. Nyffeler, pers. We have evidence that essentially leafless lineages comm.). of cacti have the potential to derive persistent, often 2. - The species of Pereskia proposed as relictual broad leaves (Wallace & Dickie, 2002; Griffith, 2002): (P aculeata Mill. and P grandifolia Haw.) are equivo- Pereskiopsis, Quiabentia, and Austrocylindropuntia(all cally deep within a lineage that includes P diaz- derived members of Opuntioideae) possess persistent romeroanaCfardenas, P humboldtiiBritton & Rose, and leaves of various degrees of succulence. If we note that a P weberiana K. Schum. (Wallace, 1995a), species pos- more recently evolved genus, Pereskiopsis, has leaves sessingtuberous roots, a featurefound in the deep line- that are less broad, less vascularized, and more succulent ages of Opuntioideae (Griffith, 2002), Maihuenia than Pereskia, we can conceive of what the ancestors of (Anderson, 2001), and among the outgroups of Pereskia might have looked like as they began to adapt Cactaceae(Applequist & Wallace,2001). to more humid regimes. This model contradictsthe phy- 3. - There are interesting similarities among the logenetic hypotheses of Britton & Rose, as we imagine deep lineages recovered for Cactoideae(Nyffeler, 2002), ancient, smaller cacti (like Blossfeldia, Maihuenia, and Opuntioideae(Griffith, 2002), andthe genusMaihuenia. Maihueniopsis), gaining a more erect, open habit, with

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statesare reviewed below. I. - Pereskiaspecies with superiorovaries. Some Other speciesof Pereskia[Rhodocactus (A. Berg)Knuth] pos- Cactoideae sess superiorovaries, a traitconsidered plesiomorphic (Takhtajan,1991). Superior ovaries are also a character of some Portulacaceae,which is consideredthe nearest Blossfeldia outgroupto Cactaceae.The possession of superior ovariesby thesePereskia species supports the ideathat Pereskiaare relictualmembers of Cactaceae.However, Pereskia at least one genus of Portulacaceae(Portulaca L.) has partiallyinferior ovaries (Cronquist,1981), and this genusis supportedas a close relativeof cacti.The molec- Maihueniopsis ularand morphological evidence, then, are both unclear iv with referenceto the polarityof thistrait in this group. 2. - Pereskialeaves. The leaves of Pereskiahave a strongmidrib and pinnate venation (Leuenberger, 1986), whereasthe leaves of Pereskiopsisand Quiabentiado Other not (pers. observ.).It may be difficultto conceiveof Opuntioideae broad,semi- to non-succulentPereskia leaves evolving froma small,succulent-leaved ancestral cactus to super- ficially resemblethose of other dicots. However,the leavesof the relatedPortulacaceae (e.g., Anacampseros, Talinum)are fleshy to succulentand lack strong venation & Evenif Pereskiais relict- Maihuenia (Guralnick Jackson,2001). ual amongstcacti, the evolutionof its formis still puzzling. Associated 3. - Apparentrelictual corollas in Pereskia. Portulacaceae Pereskiadiaz-roemeriana has a corollathat consistsof five in contrastto the corollasof Fig. 3. Conceptual model of the phylogeny of Cactaceae, , polytepalate based on consensus of recent molecular work (see text). most cacti.This pentapetaly could be considereda prim- Numerated points are as follows: i, a diminutive, succu- itive traitamong cacti. It is possibleto conceiveof the lent, portulacaceous common ancestor of Cactaceae; five-petaledcorolla being a derivedtrait in P diaz-roe- reduction of short shoots into areoles and bud scales meriana.A similarcorolla be found in into the the subfamilies may Rhipsalis spines; ii, relationships among a as derived are not resolved; iii, a deep lineage of Cactaceae main- Gaertn.,however, genuswell-supported in tains a smaller, cushion-like, succulent habit (Maihuen- the Cactoideae(Nyffeler, 2002). Futhermore,oligomer- ioideae); iv, evolution of glochids and bony arils izationof the perianthmay also be considereda derived (Opuntioideae); v,. one lineage of cacti evolves broad lea- traitamong angiosperms (Takhtajan, 1991). ves and loses much succulence (Pereskioideae); vi, com- 4. - Woodcharacters of Pereskia.Pereskia loss of leaves This model is for pos- plete (Cactoideae). open sesses dicotwood to othermembers testing with further research. ordinary compared of Cactaceae(Anderson, 2001; J. D. Mauseth,pers. comm.);non-pereskioid cacti have massive parenchyma- persistentleaves (as someAustrocylindropuntia), devel- tous rays (TerrazasSalgado & Mauseth, 2002). A oping broad leaves (such as Pereskiopsis and Pereskialineage, independently deriving ordinary dicot Quiabentia),and losing succulence(e.g., Pereskia)as wood charactersfrom a succulent,geophytic ancestor, they adapta highersurface area to volume ratio over would involve numerous,synchronous character state time. changes,and no heterobathmouscharacter states have yet been documented.It is widelyheld thatsecondarily derivedwoody lineageswould show anatomicaldiffer- ences fromprimary woody lineages (e.g., in Asteraceae, PROBLEMSWITH THE MOLECU- Cucurbitaceae;Takhtajan, 1991). However,Pereskia is LARMODEL exceptional in its ordinary wood anatomy among Thismodel for cactusevolution is difficultto recon- Caryophyllales,as most membersof this order are cile withthe relictualmorphological and anatomical fea- markedby anomalousstem structureof some kind tures found in Pereskia.Several conflictingcharacter (Cronquist,1981), and we have good supportthat the

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towards a new consensus. 4: 65-78. cacti are nested within a derived of the Bradleya lineage Landrum, J. V. 2002. Four succulent families and 40 million Portulacaceae & (Hershkovitz Zimmer, 1997; Applequist years of evolution and adaptationto xeric environments: & Wallace, 2001). What can stem and leaf anatomicalcharacters tell us about their phylogeny? Taxon51: 463-474. Leuenberger, B. E. 1986. Pereskia (Cactaceae). Mem. New YorkBot. Gard. 41: 1-141. ACKNOWLEDGEMENTS Leuenberger, B. E. 1992a. Observations on Maihuenia (Cactaceae) in Argentinaand Chile: Part2. Notes on flow- I thankJim Mauseth and one anonymousreader for especially ers, temperatureand climate. Cact. Succ. J. (U.S.A.) 64: thoroughreviews of this manuscript.I also thankStefanie Brown, 125-130. RichardFelger, Naomi Fraga,Dylan Hannon,Mark Hershkovitz, Leuenberger, B. E. 1992b. Observations on Maihuenia Lee Lenz, GaryLyons, Mark Porter, Karen Walker, Leah Walker, (Cactaceae) in Argentina and Chile. Part 1. Introduction and Ming Zhou for informativeand engagingdiscussions on this and notes on root systems. Cact. Succ. J. (Los Angeles) 64: 71-79. topic. The gorgeous plants depicted here were all meticulously B. E. 1997. of a maintained John andthe rest of the staff at Leuenberger, Maihuenia-monograph by GaryLyons, Trager, of Cactaceae. Bot. Jahrb. 119: thanksto Naomi for Patagonian genus Syst. HuntingtonBotanical Gardens. Special Fraga 1-92. a crucialloan of photographicequipment! Martin, C. E. & Wallace, R. S. 2000. Photosyntheticpathway variation in leafy members of two subfamilies of the Cactaceae.Int. J. Pl. Sci. 161: 639-650. Mauseth, J. D. 1999. Anatomical adaptationsto xeric condi- LITERATURECITED tions in Maihuenia (Cactaceae), a relictual, leaf-bearing cactus. J. Pl. Res. 112: 307-315. Anderson, E. F. 1986. A revision of the genus Neolloydia B. & J. D. 2000. Theoretical of surface-to-volume R. (Cactaceae).Bradleya 4: 1-28. Mauseth, aspects ratios and of succulent shoots. 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