Interxylary phloem: Diversity and functions Sherwin Carlquist

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Brittonia ISSN 0007-196X BrittoniaDOI 10.1007/s12228-012-9298-1

Interxylary phloem: Diversity and functions

Sherwin Carlquist

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Interxylary phloem: Diversity and functions

SHERWIN CARLQUIST

Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA;e-mail: [email protected]

Abstract. Interxylary phloem is here defined as strands or bands of phloem embeddedwithin the secondary xylem of a stem or root of a plant that has a single vascularcambium. In this definition, interxylary phloem differs from intraxylary phloem, bi-collateral bundles, pith bundles, and successive cambia. The inclusive but variouslyapplied terms included phloem and internal phloem must be rejected. Histologicalaspects of interxylary phloem are reviewed and original data are presented. Topicscovered include duration of interxylary phloem; relationship in abundance betweensieve tubes in external phloem and interxylary phloem; distinctions between interx-ylary and intraxylary phloem; presence of parenchyma, fibers, and crystals in theinterxylary phloem strands; development of cambia within interxylary phloem stran-ds; three-dimensionalization and longevity of phloem, systematic distribution of int-erxylary phloem; physiological significance; and habital correlations. No singlephysiological phenomenon seems to explain all instances of interxylary phloem oc-currence, but rapidity and volume of photosynthate transport seem implicated in mostinstances.

Key Words: Bicollateral bundles, included phloem, intraxylary phloem, photosyn-thate conduction, successive cambia.

Interxylary phloem consists of strands ofsieve tubes, companion cells, and adjacentparenchyma or other cells embedded withinthe secondary xylem of a stem or root that hasa single vascular cambium. This definition ispresented to distinguish interxylary phloemfrom a series of other histological phenomenathat may have similar functions but arehistologically and ontogenetically different. Forexample, the term successive cambia denotes aseries of vascular increments, each with second-ary phloem, secondary xylem, and a vascularcambium, each of which ultimately originatesfrom the master cambium at the periphery of astem or root (Carlquist, 2007). The mastercambium produces secondary cortex (0 paren-chyma) to the outside, and to the inside,conjunctive tissue and vascular cambia to theinside of an axis. Each vascular cambium thenproduces secondary phloem to the outside andsecondary xylem to the inside. The termincluded phloem was misapplied to successivecambia in some (but not all) Nyctaginaceae by

Chalk and Chattaway (1937), but used also forinstances of interxylary phloem. Misapplica-tions of this sort render the term includedphloem imprecise, and, in any case, are basedon topographic phloem distribution withoutregard to ontogenetic factors. The ontogeny ofphloem and xylem within various cambiavariants can be easily determined from themature histology, and thus can readily beincluded in definitions of cambial variants. Theterm "included" suggests that the phloem ininstances of successive cambia is embeddedwithin secondary xylem (as it is in the case ofinterxylary phloem). In fact, the phloem inexamples of successive cambia lies betweensecondary xylem (internal to it) and conjunctivetissue (external to it) in each vascular increment.The term internal phloem has likewise been

contaminated by conflicting usages and shouldbe rejected. "Internal phloem" has been used torefer to intraxylary phloem, but has beenapplied to other histological conditions. Signif-icantly, like "included" phloem, the term

Brittonia, DOI 10.1007/s12228-012-9298-1ISSN: 0007-196X (print) ISSN: 1938-436X (electronic)© 2013, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

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internal phloem is vague with respect toontogeny as well as location of phloem.Intraxylary phloem, although readily dis-

tinguishable from interxylary phloem, mayhave a similar physiological significance andis covered in a later section of this paper. Thepresent usages are consistent with thoseadopted in earlier accounts of cambial var-iants (Carlquist, 1988, 2001, 2007). For thepresent, workers would be well advised todefine the terms they use for cambial variants.Interpretation of functions of interxylary

phloem is further complicated by the fact thatin woody angiosperms as a whole, interxylaryphloem occurs in only a relatively smallnumber of families and species. Even withina genus such as Combretum or Strychnos,some species have interxylary phloem, otherslack it, with no clear differences in habit orsize of plant (van Vliet, 1979; Mennega,1980). However, there is some correlationwith systematic units within genera such asthese (van Vliet, 1979; Mennega, 1980).There is no unique function for interxylary

phloem; other phloem distributions seem to beadequate alternates. That does not mean,however, that interxylary phloem is not aphysiologically significant way of meeting aplant's photosynthate conduction requirements.Wood anatomy contains many examples ofalternative ways of serving particular functions(e.g., vestured pits, helical sculpture of vesselsurfaces, and vasicentric tracheids are probablyall methods of minimizing embolism formation—or reversing that). Interxylary phloem, likevestured pits, is a device that is homoplastic inwoody angiosperms. In both instances, geneticinformation for the formation of these struc-tures has not been frequently achieved phylo-genetically, perhaps because a complex seriesof genetic changes is required. The datapresented here may offer interesting examplesthat lend themselves to physiological studies.Plant physiological studies have traditionallybeen done on economically important plants,and none of the species with interxylary phloemhas any major economic value.

Materials and methods

Some of the examples cited here are derivedfrom earlier wood anatomical surveys. The

materials and methods used in those studies aregiven in the papers listed below. In all cases,however, the photographs and observations arenew. Re-studied materials include the following:Figure 1: Turbina stenosiphon (Hallier f.)

A. Meeuse (Convolvulaceae): Carlquist andHanson, 1991.Figure 2A–C: Thunbergia laurifolia Lindl.

(Acanthaceae): Carlquist and Zona, 1988Figure 2D: Stylidium glandulosum Salisb.

(Stylidiaceae): Carlquist, 1981Figure 4: Pseudolopezia longiflora Rose

and Oenothera linifolia Nutt. (Onagraceae):Carlquist, 1975.Figure 6: Salvadora persica L.(Salvador-

aceae): Carlquist, 2002.Sources for material not previously studied

are as follows:Figure 3: Orphium frutescens E. Mey.

(Gentianaceae): Carlquist 8212, June 28,2011 (SBBG).Figure 5: Craterosiphon scandens Eng. &

Gilg (Thymeleaceae): Breteler 1227 (WAG).Figure 7A–B. Strychnos madagascariensis

Poir. (Loganiaceae): David Lorence 10285(PTBG), National Tropical Botanical Gardenliving collections accession number 801348.Figure 7C–D. Combretum erythrophyllum

Sond. (Combretaceae): cultivated in theVavra Garden (formerly owned by Universityof California, Los Angeles).The sections in Figs. 3 and 7C–D were

derived from living material that was pre-served in 50 % aqueous ethanol, sectioned ona sliding microtome, and stained with aSafranin-Fast Green combination. The sectionin Fig. 7A–B was derived from livingmaterial that was preserved in aqueous 50 %ethanol. The sections were prepared by drivinga single-edged razor blade into a stem with theaid of a hammer. The sections derived weresubjected to changes of distilled water, anddried between glass slides under pressure (toprevent curling), then sputter-coated with goldand examined with a Hitachi S2600N scanningelectron microscope (SEM).

Aspects of Interxylary Phloem

1. Ontogenetic and Histological Criteria;Allied Phenomena.Because secondary xylem consists mostly

of cells with rigid walls, it is a clear and

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easily read record of the action of the vascularcambium. The products of cambial action areunambiguous, so that there is no need todevelop definitions that exclude ontogeneticaspects and are merely topographic in theirframe of reference (e.g., included phloem). Tobe sure, xylarium specimens have poor preser-vation of meristematic cells and of phloem, but

the location and sequences of cell types withsecondary walls (which are readily seen insections of xylarium specimens) are quitesufficient to permit any appearance to bereferred to one of the categories accepted here.The difference between interxylary phloem

and successive cambia can be seen in Turbinastenosiphon (Fig. 1A–C) of the Convolvula-

FIG. 1. Transections of stem of Turbina stenosiphon (Convolvulaceae), to show diverse types of vascularhistology. A–B. Successive cambia. A. Three vascular increments, each with secondary xylem (sx) and secondaryphloem (sp); the middle vascular increment has an inverted orientation (ivi), atypical for successive cambia. B. Higherpower, area corresponding to center of A. The inverted increment (ivi) above has produced secondary phloemadaxially and secondary xylem abaxially; the crushed secondary phloem (csp) was produced by the invertedincrement. The normal increment below has produced secondary phloem abaxially and secondary xylem adaxially. C.Strand of interxylary phloem, surrounded by fibrous secondary xylem. D. Intraxylary phloem strand (itp) adaxial toprotoxylem (upper left). A cambium (arrows) has developed in the strand and has produced secondary phloem (sp)adaxially. Pith parenchyma, some of which has been converted to pith sclereids (ps) below.

CARLQUIST: INTERXYLARY PHLOEM2013]


ceae. This species is the first, to my knowledge,in which both successive cambia (Fig. 1A–B)and interxylary phloem (Fig. 1C) have beenshown to coexist in a single stem. Interestingly,a third phenomenon, intraxylary phloem, is alsorepresented in Turbina stenosiphon (Fig. 1D).

Successive cambia are increments of secondaryxylem and phloem, each produced by avascular cambium. The cambia, as well asconjunctive tissue and secondary cortex (0parenchyma) are produced by a master cambi-um (Carlquist, 2007). Conjunctive tissue is not

FIG. 2. Sections of rayless stems containing interxylary phloem. A–C. Thunbergia laurifolia (Acanthaceae). A–B.Transections. A. Low power to show secondary phloem (sp) above), and secondary xylem below, with the vascularcambium (vc) between them. The secondary xylem is composed of an axial parenchyma (pax: gray) background inwhich bands or strands of fibrous vessel-bearing xylem (fx: darker) are embedded. B. Higher power photograph toshow the strands of sieve tubes (st) in the axial parenchyma backgrounds. Fibrous xylem may deiverge from eachother (di) by means of parenchyma or may actually break apart (br) due to tensions during growth. C. Radial section toshow sieve plates (sp) in sieve tubes (darker gray), sheathed by parenchyma of the interxylary strand (pix, lightergray); the fibrous xylem cells (fx) are narrower and stain more darkly. Stylidium glandulosum (Stylidiaceae),transection of stem portion with secondary growth. The vascular cambium (vc) is essentially unifacial, producingsecondary xylem externally but nothing more than perhaps a single layer of secondary cortex externally; a phellogen(pg) has developed in the innermost cortical cells. Seven arrows indicate strands of interxylary phloem, which are verynarrow and consist of only two to four cells each.

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a form of axial parenchyma; axial parenchymais produced only by a vascular cambium. Theexample illustrated here, Turbina stenosiphon,is unusual in having one vascular incrementinverted in orientation, with that vascularcambium producing phloem internally andxylem externally. This is the only instance Iknow in which a vascular increment has this

inverted orientation. This occurrence doesunderline the fact that occasionally one doessee a cambial variant with atypical ontog-eny. At the same time, the rarity of suchoccurrences reinforces the regularity ofphenomena described by the definitionsgiven: cambial variants are orderly, andnot "anomalous."

FIG. 3. Transections of stem of Orphium frutescens (Gentianaceae). A. Low power photograph to illustrate thatsecondary phloem (sp) contains only a few strands of sieve tubes (st); the remainder is parenchyma. Vascular cambium(vc) at the juncture with secondary xylem. The secondary xylem consists of fibrous xylem (fx) in which strands orbands of interxylary phloem (ip) are located. B. Intermediate power photograph to illustrate that the interxylaryphloem may take the form of strands (ip) or bands (ipb) located in a background of vessel-bearing fibrous xylem (fx).C–E. Higher power photographs to illustrate intersections between rays (r) and interxylary phloem (ip) in relation tothe fibrous xylem (fx) background. C. Two strands of interxylary phloem are separated by a ray. D–E. Instances inwhich sieve-tube elements and companion cells are derived from ray initials, and in which phloem ray tissue thereforecontains phloem.



The interxylary phloem strand illustrated inTurbina stenosiphon (Fig. 1C) exemplifies allof the features claimed by the definition. It isa strand of sieve tube elements and compan-ion cells surrounded by a sheath of paren-chyma. Because the parenchyma is formed bya vascular cambium, it can be termed axialparenchyma.

Intraxylary phloem is also present inTurbina stenosiphon (Fig. 1D). Intraxylaryphloem occurs at the adaxial tips of vascularbundles of a number of woody angiosperms(for a list, see Metcalfe and Chalk, 1983,appendix). Cambial activity is found in aminority of instances of intraxylary phloem,and there is no list of genera in which it is

FIG. 4. Transections of stems of Onagraceae. A–B. Pseudolopezia longiflora. A. Tangentially wide interxylaryphloem band (ipb) embedded in a background of starch-rich fibers (srf). B. Section showing secondary phloem (sp) inupper half, divided from the secondary xylem, below, by the vascular cambium (vc). Strands of sieve tubes (st) arescarce in the secondary phloem. Fibers of the secondary xylem are rich in starch (srf). C–D. Stem transections ofOenothera linifolia. C. First-year xylem: strands of interxylary phloem (ip) are relatively numerous, but short-lived;gaps appear in them due to collapse of sieve tubes; phloem parenchyma cells surround the gaps. D. Second-yearxylem: strands of interxylary phloem (ip) are few but functional.

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present or absent. It is present in the strandillustrated in Fig. 1D. Where present, cambi-um in intraxylary phloem acts unidirectional-ly, producing secondary phloem adaxiallyrather than (as with an ordinary vascularcambium) abaxially. Secondary xylem isproduced by this cambium only rarely, but

has been figured in Operculina (Carlquist &Hanson 1991; Carlquist, 2012,).Bicollateral bundle is a term that denotes

phloem at both the abaxial and adaxialsurfaces of a bundle (as opposed to acollateral bundle, which has phloem onlyabaxially). Although the term does not spe-

FIG. 5. Stem sections of Craterisiphon scandens (Thymeleaceae). A. Low power photograph of wood transectionto illustrate that earlier-formed secondary xylem is devoid of interxylary phloem, whereas more recently-formed woodcontains bands of interxylary phloem (ipb). B. Intermediate power photograph of transection to illustrate the extent oftwo interxylary phloem bands (ixb). C. High-power wood transection photograph of an interxylary phloem strand anda ray (r); ap 0 axial parenchyma (related to vessel); cs 0 crystal sand; f 0 intrusive fiber in interxylary phloem; sp 0sieve plate as seen in transection. D. Longisection of interxylary phloem strand: f 0 intrusive fibers; pix 0 parenchymaof interxylary phloem; sp 0 sieve plates (seen obliquely).



cifically exclude the presence of secondaryxylem in such a bundle, it is more commonlyapplied when there is little or no secondary

growth in the bundle, as in Cucurbita orSolanum (Lycopersicon). Thus, there is anoverlap with the term "intraxylary phloem."

FIG. 6. Transections of stem of Salvadora persica (Salvadoraceae). A. Low power photograph to illustratesecondary phloem (top 2/5 of picture) and secondary xylem (sx), bottom 3/5 of photograph, indicating variousquantities of parenchyma (pa) within the secondary xylem. B. High power photograph of a portion of the transectionshown in A; secondary phloem (sp, above) contains a single strand of sieve tube elements (to right of the letters sp);below the vascular cambium (arrows) is a strand of fibrous xylem containing two vessels; the remainder of thesecondary xylem consists of parenchyma (pa). C–E. High power photographs to show interxylary phloem. C. Juncturebetween secondary phloem (sp) and secondary xylem, with vascular cambium (arrow) between them. In the secondaryphloem, a strand of sieve tubes is seen (left); in the secondary xylem, a ray (r) and a young strand of interxylaryphloem (left of the letters ip) are embedded in axial secondary xylem that consists of parenchyma (pa), with no fiberspresent. D. A strand of interxylary phloem of intermediate age, farther from the vascular cambium; some of thephloem is crushed (cip); below that, phloem is function, and the formation of a cambium in the interxylary phloemstrand is denoted by arrows. E. An older strand of interxylary phloem; all of the phloem is crushed (cip).

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2. Parenchyma Associated with Strands ofInterxylary Phloem.

Strands of interxylary phloem are mostcommonly strands of axial parenchyma in

FIG. 7. Stem transections to show interxylary phloem. A–B. Strychnos madagascariensis (Loganiaceae). Stemtransections seen with SEM. A. Low power micrograph, to show a typical large interxylary phloem strand (ip) in afibrous xylem (fx) background; bark (b) at top of photograph. B. High power photograph corresponding to lower leftportion of the strand shown in A; a cambium (c, plus arrows) has formed within the interxylary phloem strand; cpa 0crushed parenchyma, fx 0 fibrous xylem; np 0 newer phloem; op 0 older phloem. C–D. Light photomicrographs ofstem transections of Combretum erythrophyllum (Combretaceae). C. An interxylary phloem strand near the vascularcambium (which is not shown, but is just above the top of the photograph); a cambium (c, plus arrow) has recentlyformed within the interxylary phloem strand, but there is no crushed phloem; cpa 0 crystal-bearing parenchyma; fp 0functional phloem; fx 0 fibrous secondary xylem. D. An older strand of interxylary phloem, in which a cambium (c,plus arrow) has been active; crushed phloem (cp) forms a conspicuous band; cpa 0 crystal-bearing parenchyma; fp 0functional phloem; fx 0 fibrous xylem.



which there is a central core of sieve tubeelements and companion cells. This is mosteasily seen in Thunbergia (Fig. 2A–C). Thun-bergia is a vine and the diameter of the sievetubes is larger than in the average nonviningeudicot. In longisections, one can see sieveplates in the strands of interxylary phloem(Fig. 2C). The fibrous xylem consists of non-septate libriform fibers (Fig. 2C, fx). Thunber-gia is rayless, so all of the thin-walled paren-chyma seen in Fig. 2A–C is axial parenchyma.Parenchyma associated with interxylary phloemis transversely subdivided into strands, muchlike axial parenchyma in typically woodyeudicots. Axial parenchyma in Thunbergiaseparates bands and strands of vessel-containingfibers (Fig. 2A, B), which occasionally break(Fig. 2C, br) in response to stem growth andtorsion. Axial parenchyma in Thunbergia thusserves a mechanical function that can often beserved by wide rays in scandent woody plants.Stylidium glandulosum (Fig. 2D), a sub-

shrub, also has rayless wood. The strands ofinterxylary phloem (arrows) consist of littlemore than a sieve tube element plus a compan-ion cell each, and are quite inconspicuous. Anoccasional axial parenchyma cell is present inthese strands. Stylidium and Thunbergia formextremes with respect to quantity of parenchy-ma associated with phloem.Intermediate quantities of parenchyma char-

acterize the strands of most species that haveinterxylary phloem (Figs. 3A–E, 4A and 6C–E).The varied quantities of parenchyma observedin strands of interxylary phloem may be keyedto diverse physiological functions, but there hasbeen no experimental work on this topic.

3. Rays and Interxylary Phloem.By implication, interxylary phloem occurs

as vertical strands in axial xylem. This isclearly demonstrated by most species (e.g.,Thunbergia, Fig. 2A–C). In most species thathave interxylary phloem, rays either do notcross strands of interxylary phloem (Fig. 6A–E) or if they do (Fig. 5A–B), The ray cellsretain their typical histological characteristics.Orphium (Fig. 3) provides some examples ofthis latter condition, but it also, in a fewplaces, forms sieve tube elements and com-panion cells in rays. In Fig. 3C, instances oftypical interxylary phloem strands that do notintersect rays are shown.

In Fig. 3D and E, instances in whichportions of rays have been converted to sievetube elements and companion cells are shown(r 0 rays). One should note that ray cells inOrphium are predominantly upright, as onewould expect from a secondarily woody plant(Carlquist, 1962, 2009), so conversion of raycells to sieve tube elements and companioncells is really not contrary to the expecteddirection of conduction. If one scans largerareas of Orphium wood transections, one seesthat interxylary phloem occurs as eitherstrands or bands (Fig. 3A, B). The ratio ofbands that contain sieve tube elements andcompanion cells in ray areas to those that donot is perhaps only one band out of twenty.

4. Diversity in Patterns: Strands, Bands,Relative Abundance.Interxylary phloem is usually seen as cylin-

drical strands (Figs. 1C and 2B). These strandscan range from inconspicuous and few celled,as in Stylidium, to large and obvious, evenperceptible without microscopy, as in Strychnos(Fig. 7A) and Combretum (Fig. 7C, D).Interxylary phloem is often present in the formof tangential bands (Figs. 4A and 5A. Bandsand strands may occur together.Salvadora (Fig. 6) appears to have bands

rather than cylindrical strands of interxylaryphloem (e.g., Fig. 6C) because the parenchymasurrounding the strands occurs as tangentialbands (Fig. 6A, B). Salvadora exemplifies thepoint that parenchyma may be much moreabundant in transectional area than the strandsof phloem in embedded in the parenchyma.

5. Cell Contents: Crystals, Starch, etc.Crystals occur in parenchyma that sheathes

phloem in a large number of the species thathave interxylary phloem. Exceptions can becited in the case of Stylidium (Fig. 2D)Orphium (Fig. 3) and Salvadora (Fig. 6).Although not shown here, prismatic crys-

tals occur in the axial parenchyma bands thatcontain phloem in stems of Thunbergia alataBojer ex Sims (Carlquist and Zona, 1988;Carlquist, 2001). Raphides are present in suchparenchyma in Onagraceae (Carlquist, 1975).Crystal sand is present in axial parenchyma ofinterxylary phloem strands in Craterosiphon(Fig. 5C; SEM photos in Carlquist, 2001).Druses occur in the phloem-ensheathing paren-

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chyma of Combretum (Fig. 7C–D, cpa). Thepositioning of druses in interxylary phloem-adjacent parenchyma in Combretum as well asin cases of crystal occurrence in other generalisted in the present study suggests thatcrystal-bearing sheaths may deter predationof interxylary phloem by chewing beetles.Such positioning of crystals is often seenin relation to phloem in bark of manywoody species.In woods of Onagraceae, starch is common

in libriform fibers adjacent to strands ofinterxylary phloem (Fig. 4A–B, srf; Carlquist,1975). However, starch is notably absent inthe parenchyma sheathing the phloem strandsin that family (Fig. 4A–B). This circumstancesuggests that starch storage and active trans-port of soluble photosynthates are distinctfunctions performed by these two respectivetissues.

6. Libriform Cells in Interxylary Phloem.Because the root word "liber" refers to

phloem, sieve tube elements (and their asso-ciated companion cells) could be included as"libriform elements" but that is not usuallydone. "Libriform" implies an elongated form,and usually refers to fibers. Certainly sieve-tube elements in Craterisiphon are elongate,their length easily determined from presenceof sieve plates (Fig. 5D). Curiously, however,extraxylary fibers mature in the interxylaryphloem bands of Craterisiphon (Fig. 5B, C).These fibers are gelatinous, and in permanentslides, the secondary walls shrink away fromthe primary walls (Fig. 5C). The fibers areinstrusive, and their tips (Fig. 5D, f) do notalign with the sieve plates of the sieve tubeelements, which are shorter than the fibers.

7. Timing of Interxylary Phloem Onset.Presence of interxylary phloem may change

in abundance with age of stem. This is evidentin Fig. 5A for Craterisiphon. In this stem,interxylary phloem is absent in earlier-formedsecondary xylem. This has been reported inother species, such as Azima tetracantha Lam.of the Salvadoraceae. Den Outer and vanVeenendaal (1995) describe interxylary phloemstrands throughout the stem of this species.Their stem was larger in diameter than the one Istudied (Carlquist, 2002); at the periphery of thestem I studied, interxylary phloem production

had just begun. In other Salvadoraceae, such asDobera (Carlquist, 2002) and Salvadora(Fig. 6), interxylary phloem production beginsearly and remains constant in abundance.Mennega (1980) in her study of wood of

Strychnos and other Loganiaceae mentionsthat interxylary phloem has not been reportedin some species (cf. Pfeiffer, 1926) in whichonly small diameter stems were available,whereas larger-diameter stems prove to haveinterxylary phloem.An apparent exception to this trend

occurs in Oenothera linifolia, in whichinterxylary phloem strands are fewer andsmaller in second-year wood of stems(Fig. 4D) as compared to first-year wood(Fig. 4C). The occurrence of this trend issomewhat masked by the fact that in first-year wood, parenchyma cells of the strandsenlarge and develop secondary walls afterthe collapse of sieve tube elements andcompanion cells.Pfeiffer (1926), following Schenck (1895)

reports sieve tube elements in secondaryxylem of Mucuna altissima DC. as a late orsubsequent (nachträglich) developmentcompared with maturation of other celltypes nearby.

8. Comparison between Interxylary Phloemand Secondary Phloem in a Single Stem.Comparisons of this sort are lacking, pre-

sumably because dried material rather thanliquid-preserved material has been studied,and because soft tissues do not survive slidingmicrotome sectioning as well as harder (fi-brous) tissues. The question that arises inconnection with comparison of these twophloem regions within a given stem is whetherin stems that have interxylary phloem, sievetube elements are less abundant in secondaryphloem (outside the vascular cambium) than instems that lack interxylary phloem. The answerto this question, based on a small sample, is yes,although variability is evident. Whether barkthickness relates to distribution of sieve tubeelements in interxylary phloem vs. secondary(0 external, or bark) secondary phloem is notknown, and needs investigation.The most notable example is found in

Stylidium species that have secondary growth(most species of the genus lack secondarygrowth). Stylidium glandulosum (Fig. 2D)



produces at most one layer of cells external tothe vascular cambium, and the cells of thatlayer are best described as parenchyma.These cells are not radially aligned with theinnermost cortical parenchyma layer, inwhich phellogen develops (Fig. 2D, pg).Thus, there is no true secondary phloem,and no sieve tubes external to the cambium.This was reported, although not thoroughlyillustrated, earlier (Carlquist, 1981).Orphium (Fig. 3A) and Pseudolopezia

(Fig. 4B) show a relative paucity of sieve tubesand companion cells in secondary phloem.Relatively extensive areas of secondary phloemconsist exclusively of phloem parenchyma,with only a few, isolated strands of sieve tubeelements and companion cells present.Some degree of variability occurs in Salva-

dora (Fig. 6). In some areas of secondaryphloem, sieve tube elements and companioncells are relatively sparse (Fig. 6A–B), whereasin others, they are rather more common(Fig. 6C). As a generalization, however, Salva-dora—as well as the other interxylary-phloem-bearing eudicots for which data are reviewedhere—have fewer sieve tube elements andcompanion cells in secondary phloem (bark)than is typically observed in eudicots that lackinterxylary phloem.

9. Organographic Distribution.Work in wood anatomy remains biased

toward stems, for understandable reasons. Infact, so few xylarium specimens are of rootmaterial that no indication of site of origin onthe plant is given on most specimens; thedefault assumption is that stem material isinvolved. (Whether the material comes frommain stem or branches is likewise neverindicated on xylarium labels).Some workers have mentioned interxylary

phloem in roots or rhizomes. For example,Pfeiffer (1926) reports interxylary phloem"islands" (interxylären Inseln) in transectionsof roots and rhizomes of Cochlearia armor-acia L., Brassica napus L., B. rapa L., andRaphanus sativus L. Metcalfe and Chalk(1950), citing Pfeiffer's (1926) reports, men-tioned "secondary interxylary bundles" in theunlignified xylem of the rhizomes of Armor-acia lapathifolia Gileb. and in the root ofBrassica napus, B. rapa, and Raphanussativus. The overlapping nature of these reports

and the impreciseness of the term "secondaryinterxylary bundles" underlines the need formore extensive studies not merely to confirmthe histological nature of these instances, but todetermine the ontogenetic origin of these"bundles" or "islands." The lack of reports ofsuch appearances in the stems of Brassicaceaeis, however, notable in this regard.Pfeiffer (1926) assigned histological

appearances in the roots of Scolopia atro-poides Bercht. & Presl (Solanaceae) to theconcept of interxylary phloem. He likewisereferred similar vascular tissue in roots ofBrowallia viscosa HBK. (Solanaceae) to thiscategory. Pfeiffer (1926) also reproduces abelievable drawing of interxylary phloem inthin-walled root secondary xylem of Atropabelladonna L. (Solanaceae) by Leisering(1899), so there is reason to credit his conceptof interxylary phloem in that species as thesame as mine. Stem interxylary phloem hasnot been reported in Atropa. Pfeiffer (1926)reports interxylary phloem for roots of Ipo-moea versicolor Meissn. (Convolvulaceae),but does not note it in stems of this species.There are obviously many residual oppor-

tunities for confirmation or reassignment intoother catergories of interxylary phloemreports. New discoveries remain to be made,as in Turbina stenosiphon (Fig. 1C). Thematerial available to earlier workers was limited,and often was biased in favor of plants whichwere naturally-occurring or grown in Europe,and in favor of stems rather than roots of those.

10. Cambial Activity within InterxylaryPhloem.Scott and Brebner (1889) described devel-

opment of cambial activity in the interxylaryphloem strands of Strychnos, based uponliving material cultivated in greenhouses.Scott and Brebner figured large strands ofinterxylary phloem much like the one figuredhere (Fig. 7A, B). They reported crushedphloem on the abaxial side of the strands withcambial activity, so that the cambia in thesestrands produces secondary phloem external-ly, thereby in the same direction as thevascular cambium. This activity agrees withthe findings reported here (Fig. 7A, B).Despite the disadvantage of working with

herbarium material, Mennega (1980) reportedthe above facts accurately in a survey of

BRITTONIA [VOL


woods of Strychnos (and other Loganiaceae).As Mennega (1980) stated, not all species ofStrychnos have interxylary phloem in thestems, even when large-diameter stems areexamined. A study devoted to one species, S.millepunctata Leeuwenberg (van Veenendaal& den Outer, 1993) includes some excellentSEM images that reinforce the findings ofScott and Brebner (1889).Note should be taken that cambial activity

in the interxylary phloem strand begins soonafter a strand is produced by the vascularcambium. Cambial action is evident from theradial seriation of the cells produced by theinterxylary phloem cambium (Fig. 7B, np).The earlier-formed interxylary phloem cellsmay not show radial seriation (Fig. 7B, op).The amount of secondary phloem produced bycambial activity within a strand is evident fromthe quantity of radially seriate phloem cells inthe phloem as well as the amount of crushedphloem on the abaxial side of the strand. Barkof Strychnos (Fig. 7A, top) is relatively poor insieve tube element production.Large interxylary phloem strands occur in

the African species of Combretum of theCombretaceae (van Vliet, 1979), but not all ofthem. Histological and ontogenetic detailsgiven to date are relatively few because mostspecimens studied are from herbarium mate-rial or xylarium blocks. Somewhat thicksliding microtome sections of liquid-pre-served material presented here (Fig. 7C, D)illustrate that Combretum interxylary phloemstrands are histologically similar to those inStrychnos and like them in the timing ofcambial initiation within the strand. Strandsclose to the vascular cambium (Fig. 7C)already show the beginning of cambialactivity on the adaxial side of the strand.Older strands (Fig. 7D) show crushed phloem(cp) conspicuously, and a continuation ofcambial activity within the strands. Interxy-lary phloem strands in Combretum are com-posed of fibriform (Fig. 7C, fp) cells (whenseen in longisection) and crystalliferous pa-renchyma cells (cpa) that contain druses.Cambial activity is reported here in the

interxylary phloem strands of one other family,Salvadoraceae, although attention has not hith-erto been called to this phenomenon (Carlquist,2002), presumably because it is so inconspicu-ous. In young strands of interxylary phloem of

Salvadora persica (Fig. 6C, bottom, ip) thereare only sieve tube elements and companioncells that have been derived from the vascularcambium. Crushed phloem and cambial activitywithin younger strands is not observed, contraryto the conditions in Combretum and Strychnos.In moderately old interxylary phloem

strands of Salvadora, no radial seriation ofcells is evident (Fig. 6D). Cambial activity(arrows) is minimal. Some collapsed phloem(Fig. 6D, cip) is evident, but the accumulationis not prominent. Earlier formed (older)interxylary phloem strands show a greateramount of crushed phloem (Fig. 6E).There is a correlation between size of

interxylary phloem strands and presence ofcambial action within these strands, when onecompares the interxylary phloem of Combreta-ceae, Loganiaceae, and Salvadoraceae to that ofother families. These families are woody,ranging from shrubs to trees, and preservationof phloic pathways by means of active replace-ment of sieve tube elements and companioncells by cambial activity within the strandsseems a strategy that is correlated with habit.

11. Relationship between Intraxylary Phloemand Interxylary Phloem.The present study endorses the term intra-

xylary phloem to refer to phloem strands thatoccur adjacent to protoxylem, at margins ofthe pith. This term does not equate entirely tothe term "bicollateral bundle" (see “Aspectsof Interxylary Phloem”, section 1), in whichminimal accumulation of secondary xylem isimplied. Approximately equal amounts ofphloem are seen external and internal to thexylem in species with bicollateral bundles,whereas in instances referred to the conceptof intraxylary phloem, the amount of phloemformed externally from the vascular cambiumcan be relatively large, whereas the intra-xylary phloem strands are relatively finite insize. Because of the uneasy coexistence ofthese terms, listings of families that exemplifyone or the other concept have not always beenassembled based on critical review of material.In addition, misapplication of these termscreates problems. Pfeiffer (1926) cited instan-ces of phloic strands in the pith, for example.One can, however, cite particular families

and genera in which intraxylary phloem ischaracteristically present. Metcalfe and Chalk



(appendices, 1950, 1983) presented such lists.In their listings, Metcalfe and Chalk distin-guished between families that characteristi-cally have intraxylary phloem (bold face) andthose in which intraxylary phloem is occa-sionally reported (ordinary font) or infrequentor perhaps dubious (italics). The families ofMyrtales figure prominently in the list(Combretaceae, Crypteroniaceae, Lythraceae,Melastomataceae, Myrtaceae, Oliniaceae,Onagraceae, Penaeaceae, and Punicaceae).Interestingly, interxylary phloem also occursin an appreciable number of species in threeof these families (Combretaceae, Melastoma-taceae, and Onagraceae). A similar linkbetween intraxylary phloem presence andinterxylary phloem occurrence can be citedfor other families in the Metcalfe and Chalk(1950) list (Gentianaceae, Loganiaceae, Styl-idiaceae, and Thymeleaceae) as well asLeptadenia, an asclepioid genus of Apocyna-ceae (Singh, 1943; Patil & Rajput, 2008).Thus, intraxylary phloem may be a kind of"precursor" for interxylary phloem formationin a given species. In developmental terms,the genetic information for the formation ofstrands of phloem within the xylem (interxy-lary) as well as internal to (adaxial to) the xylem(intraxylary) may be similar. Exceptions to thisconcept can certainly be listed (e.g., Salvador-aceae lack intraxylary phloem), and this theorymay apply only in particular clades.The physiological implications of this

connection between the two sites of phloemformation are, however, even more interest-ing. In, say, Myrtales, why do only some ofthe species that have intraxylary phloem goon to produce interxylary phloem?One of the most interesting aspects of

interxylary phloem is the development of acambium in intraxylary phloem in someinstances. This is illustrated for Turbinastenosiphon (Fig. 1D), but occurs in othereudicots, such as Cucurbitaceae (Carlquist,1992; Patil et al., 2011).When cambium develops within a strand of

intraxylary phloem, the secondary phloem ityields is always produced toward the centerof the stem, rather than toward the outside(the latter, of course, is what happens in theformation of bark by the vascular cambium).The inverted nature of the secondary phloemproduction by cambia at intraxylary phloem

sites is also indicated by the fact that in a fewspecies, the intraxylary phloem cambium alsoproduces some secondary xylem (in anexternal, or abaxial, direction). This has beenillustrated for Operculina palmeri (Wats.)Howe of the Convolvulaceae (Carlquist &Hanson 1991; Carlquist 2012,).

12. Systematic Occurrence of InterxylaryPhloem.As noted above, understanding the system-

atic occurrence of interxylary phloem is awork in progress. Several reports must beregarded as tentative, while others are likelyincorrect. The latter are difficult to provedefinitively, because interxylary phloem mayoccur infrequently in a few species. The lateonset of interxylary phloem production, men-tioned for Azima and Strychnos, is anotherreason to be cautious where lists areconcerned. The multiplicity of individualswho report instances of interxylary phloemresults in variable criteria and thus lack ofprecision in application of the concept.The following list contains instances that

appear well substantiated on the basis ofsupporting drawings or photographs. Earlierworkers occasionally conflated interxylaryphloem (formed from a single vascularcambium) with instances of successive cam-bia under the inclusive rubric "includedphloem." That vague umbrella usage wasfollowed by IAWA Committee (1989).Instances of successive cambia are not in-cluded in this list. The listing is similar to thatpresented earlier (Carlquist, 2001), but withsome emendations. Following this list, acompilation of dubious, incorrect, or unusualinstances that do not conform to the workingdefinition of interxylary phloem.Apocynaceae (including Aslepiadaceae):

Asclepias, Ceropegia, Leptadenia (Singh,1943; Patil & Rajput, 2008).Brassicaceae: roots and rhizomes of Bras-

sica spp., Cochlearia, and Raphanus(Pfeiffer, 1926).Combretaceae: Calycopteris, Combretum,

Guiera, Thiloa (van Vliet, 1979; den Outer &van Veenendaal, 1995; Rajput et al., 2009).Convolvulaceae: Ipomoea versicolor

Meissn. roots and hypocotyl (Scott, 1891);Turbina stenosiphon (infrequent; new report,above).

BRITTONIA [VOL


Fabaceae: Mucuna altissima DC. (Schenck1893).Gentianaceae: Crawfordia, Chiroma, etc.

(Pfeiffer, 1926); Ixanthus (Carlquist, 1984);roots of some other genera (Pfeiffer, 1926).Icacinaceae: Chlamydocarya, Sarcostigma,

etc. (Lens et al., 2008).Lythraceae: roots of Lythrum salicaria L.

(Gin, 1909).Malpighiaceae: Dicella, Stigmaphyllon,

Tetrapteris (Pfeiffer, 1926).Melastomataceae: six genera (Chalk &

Chattaway, 1937; Metcalfe & Chalk, 1950).Onagraceae: at least seven genera (Carlquist,

1975, 1977, 1983, 1987).Salvadoraceae: all genera (den Outer & van

Veenendaal, 1981; Carlquist, 2002).Solanaceae: roots and rhizomes of Atropa

belladonna L.; roots of Datura stramoniumL. and Scolopia sp. (Pfeiffer, 1926).Stylidiaceae: Stylidium (Carlquist, 1981).Thymeleaceae: Aquilaria and eight other

genera (Pfeiffer, 1926; Solereder, 1908; Metcalfe& Chalk, 1950); Craterosiphon (above).Special cases:Coccinia (Cucurbitaceae) develops cambia

adjacent to rays (Carlquist, 1992) or within axialparenchyma of secondary xylem (Patil et al.,2011). In both of these instances, these unusualcambia produce secondary phloem, but nosecondary xylem. Because the secondary phlo-em in both instances lies within the confines ofsecondary xylem, the phloem produced by thesecambia can be called interxylary phloem. Theterminological choice by Patil et al. (2011) istherefore acceptable, but one should note thatCoccinia represents an unusual instance.Excluded instances or dubious cases in

need of re-examination:Acanthaceae: Barleria (Pfeiffer, 1926)Apocynaceae: Lyonsia, Mandevilla, and

Parsonsia were cited by Pfeiffer (1926), buthis definition of interxylary phloem waswider than mine and is not followed here.Asteraceae: Stoebe (Adamson, 1934).Bignoniaceae: Distictis, Haplolophium,

and Pithococtenium (Pfeiffer, 1926).Convolvulaceae: Cuscuta (Pfeiffer, 1926)Clusiaceae:Endodesmia roots (Pfeiffer, 1926).Euphorbiaceae:Dalechampia (Pfeiffer, 1926)Loranthaceae:Nuytsia (original data; reported

as a case of interxylary phloem by Pfeiffer,1926; Nuytsia has successive cambia).

Sapindaceae: Serjania (Pfeiffer, 1926).Urticaceae: Myriocarpa is cited by Chalk

and Chattaway (1937) on the basis of largeparenchyma strands within the secondaryxylem. In fact, these strands, as they conced-ed, do not contain phloem. Rather, theparenchyma strands exemplify the phenome-non of fiber dimorphism (Carlquist, 1958,1961). The occurrence of this kind ofparenchyma in Urticaceae has been confirmedby Bonsen and ter Welle (1984).Study of liquid-preserved material is need-

ed to resolve cases considered dubious here,because sieve tube elements do not survivedrying very well. The erroneous report ofMyriocarpa exemplifies this. Likewise, rootsprovide logistical problems for investigation.The few reports of interxylary phloem inroots (Weiss, 1880; Gin 1909; Solereder,1908; Pfeiffer, 1926) are tantalizing becausethey suggest more instances might be found.

13. Physiological Significance.The study of interxylary phloem (as well as

allied phenomena: intraxylary phloem, bicol-lateral bundles) is obviously still incompletewith respect to descriptive anatomy. Theunderstanding of the physiological significanceof these structural modes of phloem occurrenceis a promising topic for exploration. Neverthe-less, we can ask questions about function basedon our present understanding of anatomy.Physiological studies, like anatomical studies,are most actively pursued in species of eco-nomic interest. In fact, none of the speciesknown to have interxylary phloem is of anymajor economic importance. Living material ofmany of the species is not easy to access. Thus,progress in investigation of how interxylaryphloem works has been slow. The topics listedbelow may be regarded as points for departureof physiological studies.(a) Conduction rather than storage. Ona-

graceae show that parenchyma associatedwith sieve tube elements and companion cellsin interxylary phloem strands is deficient instarch, but tissues distal to the strands (mostlylibriform fibers) are rich in starch (Carlquist,1975). This clearly suggests a marked divi-sion of labor, in which interxylary phloemstrands represent a conductive tissue, whereasthe ground tissue of the secondary xylem isconverted into a significant starch reservoir.



Lack of starch in the parenchyma thatsheathes sieve tube elements is evident inexamples other than Onagraceae reviewedhere: Acanthaceae (Fig. 2A–C), Stylidiaceae(Fig. 2D), Gentianaceae (Fig. 3), Thymelea-ceae (Fig. 5) Salvadoraceae (Fig. 6), Loga-niaceae (Fig. 7A–B) and Combretaceae(Fig. 7C–D) can be cited in this regard.(b) Conduction to large photosynthate sinks.

A number of species with interxylary phloemstrands have large fruit size (Strychnos: Leeu-wenberg, 1980)) simultaneous production oflarge numbers of flowers and fruits (Oenothera)or other organographic features (sudden flushesof growth, Strychnos) that suggest a relation-ship between interxylary phloem and intensephotosynthate utilization. Large inflorescencesin which numerous flowers open at about thesame time (Combretum) are pertinent in thisregard.Instances of bicollateral bundles can be

cited here. Large fruits in Cucurbitaceae andSolanaceae require rapid input of photosyn-thates that may be related to supernumeraryphloem formations.(c) Enhanced rate of photosynthate conduc-

tion: the case of Orphium.This topic is allied to the above, but

differs in stressing the rapid, simultaneousflowering of an entire plant. Orphiumfrutescens (Gentianaceae) has interxylaryphloem. Orphium is a small shrub orsubshrub that flowers during its first year ofgrowth. During some subsequent year, flower-ing is so extensive and simultaneous that theplant devotes its entire reserves of photosyn-thates to the flowering/fruiting process and dies.At this point, it is a monocarpic plant, althoughone would not have designated it as such inprior years.I have cultivated Orphium frutescens in my

garden and attempted to prolong the vegeta-tive growth of a plant by removing all flowersduring its summer flowering season. In thesixth year of growth, it produced onlybranches that terminated in flowers, with noside branches with vegetative buds. At thatpoint, there was no longer any possibility ofdeterring flowering, and the plant flowered,fruited, and rapidly died after fruiting. Anevent of this sort seems correlated with thepresence of interxylary phloem throughoutthe stem of Orphium.

To be sure, there are many monocarpicplants that lack interxylary phloem. We donot know about their phloem abundance orphloem conductive patterns, because phloemof monocarpic plants has not been the subjectof a study. One can, however, cite such plantsas species of Oenothera (Onagraceae) that arebiennials—in a sense, short-lived monocarpicplants. There is interxylary phloem in these.With relationship to Onagraceae as a whole, Isuggested (Carlquist, 1975) that "Production oflarge flowers or large quantities of flowersduring a short period might be related tomassive starch reserves and interxylary phloemfor rapid transport of sugars." In this regard, wemay note that Fuchsia (Onagraceae), whichdoes not have interxylary phloem, producesflowers slowly over a long period of time(sometimes throughout the entire year).(d) Phloem pathway multiplication and

longevity. If interxylary phloem is producedcontinuously over a period of time, theaggregate quantity of sieve tube elementsand companion cells in a stem (or root) soonexceeds the potential amount of phloem inbark. This is a feature relevant to conductiononly if older interxylary phloem stays active.The occurrence of cambial activity producingnew sieve tube elements and companion cellsin interxylary phloem strands, as in Combre-tum, Salvadora, and Strychnos, attests tointerxylary phloem longevity. We do not know,however, about the longevity of interxylaryphloem strands in other species, such as theeight genera of Thymeleaceae (some trees:Aquilaria) that have interxylary phloem.We do know that secondary phloem is

active in earlier increments of species withsuccessive cambia (Carlquist, 2007). Ana-tomical studies show that each vascularcambium continues indefinitely to producesecondary phloem—eventually ceasing activ-ity in older parts of larger stems.Reports of sustained longevity of second-

ary xylem, related to capability to reverseembolisms (e.g., Sperry, 1985), is indirectevidence of prolonged phloem function.Functioning of phloem without simultaneousfunctioning of adjacent vessels (or tracheids)is unlikely: The two are probably correlated(although studies of this are lacking).(e) Phloem pathway three-dimensionaliza-

tion. Strands of interxylary phloem are an

BRITTONIA [VOL


ideal way of dispersing phloem throughout astem or root as a means of aiding storage andretrieval of photosynthates. Validation of thisspeculation can be found in the examples,cited above for Brassicaceae and Solanaceae,in which interxylary phloem occurs in rootsbut is apparently absent in stems of particularspecies. Similar hypotheses were entertainedwith respect to successive cambia, which arealso an ideal mechanism for distributingxylem and phloem throughout a stem or root,as in the beet, Beta (Carlquist, 2007).(f) Phloem pathway protection. Interxylary

phloem strands are often ideally protected bytheir location within a fibrous background. Thatsuch fibrous backgrounds function in maintain-ing or prolonging safety of the strands has notbeen tested, although simple experiments incis-ing bark to see whether interxylary phloemsuffices for conductive needs would be easy todo. The evidence of placement and multiplicitysuggests possible isolation from phytophagousinsects and possibly other influences. Theabundance of crystals in parenchyma sheathsof interxylary phloem strands in Acanthaceae(Thunbergia), Combretaceae (Combretum),Onagraceae (all genera with interxylary phlo-em), and Thymeleaceae (Craterosiphon) seemslike an indirect evidence of predation deterrence.(g) Lianoid correlations and other habit

considerations. The proportion of genera andspecies with interxylary phloem that has alianoid habit is much higher than one wouldexpect on the basis of the frequency of lianasand vines in eudicots as a whole. Families(and pertinent genera) in this regard includeAcanthaceae (Thunbergia), asclepioid Apoc-ynaceae (Asclepias, Ceropegia, Leptadenia),Combretaceae (several genera), Convolvula-ceae (Ipomoea, Turbina), Cucurbitaceae(Cucurbita, Lagenaria), Icacinaceae (severalgenera), Malpighiaceae (several genera), andThymeleaceae (Craterosiphon).Histologically similar phenomena (e.g.,

successive cambia) are also represented in alarger than expected number of lianoid genera(Carlquist, 1988, 2001, 2007). These con-structions include intraxylary phloem, bicol-lateral bundles, successive cambia, andsecondary xylem dispersed by parenchymaproliferation (e.g., Bauhinia, Mendoncia), asshown by the listings in appendices ofMetcalfe and Chalk (1950, 1983).

The parenchyma sheathing of phloemstrands is conspicuous in many instancesof interxylary phloem, such as Thunbergia(Acanthaceae) and Craterosiphon (Thyme-leaceae) in the present study. These sug-gest enhanced flexibility, a feature ascribedto parenchyma of lianas by Schenck(1895). In these examples, interxylaryphloem and parenchyma presence is lessin earlier-formed wood, then increases withage, suggesting parenchyma becomes moreimportant as self-support decreases andresponse to torsion and displacement of stemsincreases.A relatively small number of tree species

have interxylary phloem, but there are somenotable instances of interxylary phloem oc-currence in tree Loganiaceae (Mennega,1980) and Thymeleaceae (Pfeiffer, 1926).Examples should be examined on the basisof individual species, rather than strictlygrouped according to habit.(h) Longevity and other physiological phe-

nomena. Many fascinating questions regard-ing interxylary phloem occurrence remain tobe asked and answered. Among these is thelongevity of interxylary phloem. Circumstan-tial evidence may be obtainable from whetheror not secondary xylem of a range of ages ina given stem is functional or not, but phloemitself tends to be good evidence, because itcollapses so readily if it no longer functions(e.g., Salvadora, Fig. 6). Correlations be-tween longevity of functioning in phloemand that in xylem vessels are to be expected.Phloem longevity is generally thought to beonly a year or two, but greater longevity hasbeen demonstrated in some angiosperms(Parthasarathy 1980).

Acknowledgments

For providing material, thanks are due Dr.David Lorence for stems of Strychnos mada-gascariensis (National Tropical Botanical Gar-den), Dr. Peter H. Raven of the MissouriBotanic Garden for stems of various Onagra-ceae, and the University of California ofCalifornia at Santa Barbara living greenhousecollections for material of Salvadora. JohnBleck provided seeds of Orphium frutescensfrom which my specimens were cultivated.Mark Olson and Edward L. Schneider provided



helpful suggestions. Use of laboratory facilities,including the SEM, at Santa Barbara BotanicGarden, is gratefully acknowledged.

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Interxylary phloem: Diversity and functions Sherwin Carlquist

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