IAWA Journal, Vol. 16 (2),1995: 133-150

WOOD AND STEM ANATOMY OF SAURURACEAE WITH REFERENCE TO ECOLOGY, PHYLOGENY, AND ORIGIN OF THE MONOCOTYLEDONS by

Sherwin Carlquist I, Karen Dauer2 & Stefanie Y. Nishimura 2 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, U. S. A.

SUMMARY

Stern and rhizome anatomy is reported for Anemopsis californica Hook., Houttuynia cordata Thunb., and Saururus cernuus L. Secondary growth is reported for the first time in Saururaceae. Cambia function indefinitely in Anemopsis in both fascicular and interfascicular areas. Interfascicular cambium is minimal in Saururus and absent in Houttuynia; fascicular cambium is present in both genera and produces a finite quantity of ves­ sels, fiber-tracheids, and axial parenchyma but no rays. Anemopsis has vessels with simple perforation plates plus tracheids in wood, suggestive of adaptation to fluctuating water availability. The scalariform perfora­ tion plates of Houttuynia and Saururus suggest an unbroken history of occupancy of mesic habitats. Ethereal oil cells are reported for rays of Anemopsis, and for pith and cortex of the three genera studied. Stern idioblasts and other histologieal details are ineluded along with wood data in anatomical deseriptions of sterns. DNA data as weIl as maero­ morphologie al data implicate Saururaeeae, along with Aristolochia­ ceae, Lactoridaceae, and Piperaceae as paleoherbs elose to the origin of monoeotyledons. Key wood features that unite these families are cited. Chloranthaeeae, whieh share stern endodermis and sealariform perfora­ tion plates with Saururaeeae, are also considered elose. Features of Sau­ ruraceae that are analyzed with respeet to monoeotyledon origin inelude loss of interfaseieular cambium, minimization of faseieular cambium, lack of imperforate traeheary elements in monocotyledon bundles, tri­ mery, the sympodial habit, and production of adventitious roots. Key words: Angiosperm origins, Anemopsis, Aristolochiaceae, endoder­ mis, ethereal oil ceIls, Houttuynia, Lactoridaeeae, monoeotyledon origins, paleoherbs, Piperaceae, Saururus.

INTRODUCTION

Saururaceae eonsist of four genera eontaining six speeies. A fifth genus (Cheirotheca) has been redueed to synonymy under Zippelia of the Piperaceae (see Tueker et a1.

1) Address far correspondence: 4539 Via Huerto, Santa Barbara, CA 93110, U. S. A. 2) Plant Scholar's Program, Santa Barbara Botanic Garden.

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1993), The genus Gymnotheca (two species) occurs in China and is not included in the present study, Saururus also contains one Chinese species not studied here, but S, cernuus of eastern North America has been included, The remaining genera contain one species each. Houttuynia cordata, native from the Himalayas to Japan, is widely cultivated and has been included. Anemopsis californica, native to the southwestern United States and adjacent Mexico, is also included. Saururaceae are thought close­ ly related to Piperaceae and the two families are often grouped as Piperales (e.g., Dahlgren 1980). No mention of cambial activity in Saururaceae occurs in Solereder (1908) or Met­ calfe & Chalk (1950). One re cent essay on angiosperm origins (Taylor & Hickey 1992) codes Saururaceae as lacking secondary growth. In fact, the stern of Anemopsis (not previously studied anatomically) has several years of secondary growth and even growth rings, and limited amounts of secondary growth can be demonstrated in sterns of Hout­ tuynia and Saururus also. The limited secondary growth of Houttuynia and Saururus is of potential significance as illustrating how secondary growth might have been lost during origin of monocotyledons. Saururaceae are suggested as phylogenetically close to origin of monocotyledons according to the rbcL results of Qiu et al. (1993). These studies feature a clade that groups Aristolochiaceae, Lactoridaceae, Piperaceae, and Saururaceae - a result sup­ porting the paleoherb hypothesis of such authors as Zimmer et al. (1989) and Taylor and Hickey (1992). Wood anatomy has, thus far, tended to support the grouping of three of the four families listed above: the wood anatomy of Aristolochiaceae (Carlquist 1993) is very similar to that of Lactoridaceae, which in turn is very much like that of Piperaceae (Carlquist 1990). These three families share 10 distinctive wood features. Because wood anatomy of Saururaceae has not been hitherto investigated, it is of great interest in assessing the relationships of the family. The paleoherbs are claimed to be close to the origin of monocotyledons. The anatomical features relevant to this con­ cept have been analyzed with respect to Chloranthaceae (Carlquist 1992). Anatomical features can reflect particular habits, so one must take habits and habi­ tats into account when making comparisons of the paleoherbs to monocotyledons. Saururus and Houttuynia are rhizomatous herbs of wet places, with underground sterns (termed rhizomes here) that give rise to aboveground sterns; the rhizomes, although perennial, are relatively short-lived. Anemopsis has thick sterns, often mostly under­ ground or in mud; each stern bears a rosette of leaves; the sterns mayaiso produce slender stolons that can root at internodes. Houttuynia and Saururus typically grow in wet soil and can withstand flooding. Anemopsis occurs in margins of marshes or on streambanks with various degrees of salinity. Some Anemopsis localities experience moderate drying, but some appear to be wet most of the year; floristic works do not detail the nature of Anemopsis ecology and its range clearly. To assess this range, one would have to visit a number of Anemopsis localities, not one or two. The habitats of Saururaceae can be characterized as mesic, transitional to aquatic, whereas the habitats of Aristolochiaceae, Lactoridaceae, and Piperaceae can mostly be termed mesic (some Piperaceae are succulent and withstand drought, particularly epiphytic species).

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MATERIALS AND METHODS

Because sterns of Saururaceae do not contain large amounts of hard woody tissue, they cannot be sectioned satisfactorily on a sliding microtome, Ordinary paraffin methods were successful with Anemopsis californica, although soaking of the exposed stern embedded in paraffin improved sectioning. Presence of sc1erenchyma, along with soft tissue, in sterns and rhizomes of Houttuynia and Saururus made alternative methods desirable for these two genera; the ethylenediamine method (Carlquist 1982) was em­ ployed, but with briefer exposure (two hours) to that chemical than in the schedule as published. Sections were stained with a safranin-fast green combination. Macerations were prepared with Jeffrey's fluid and stained with safranin. Measurement of imperforate tracheary elements in Houttuynia and Saururus was not possible because macerations contained extraxylary fibers not distinguishable from fiber-tracheids. The vessel elements of Houttuynia and Saururus are mostly primary xylem vessel elements, but some are from secondary xylem, so the figures on dimen­ sions of these cells represent a mixture of both; in Anemopsis, secondary xylem is relatively abundant, and vessel elements and tracheids in astern maceration are pre­ dominantly from secondary xylem. Terms are in accordance with the IAWA Committee on N omenc1ature (1964). Shirley C. Tucker kindly provided liquid-preserved material of Saururus cernuus from her garden in Baton Rouge, Louisiana. The plant of Houttuynia cordata was cultivated at the University of California, Santa Barbara, and is represented by the specimen Carlquist 8174 (SBBG). The material of Anemopsis californica was collected in Carpenteria Marsh, Santa Barbara Co., and a voucher specimen, Carlquist 8175 (SBBG), was pre­ pared. Sterns of Anemopsis, Houttuynia and Saururus were preserved in formalin acetic alcohol.

RESULTS AND DISCUSSION

Descriptions of anatomical findings are given below. The sequence of genera is based on putative degrees of specialization in secondary xylem and secondary growth. For Saururus and Houttuynia, anatomy of the rhizome is described, followed by a para­ graph in which features by which aerial sterns differ from rhizomes are listed. Anemop­ sis lacks such dimorphism in stern portions. Details of xylem anatomy are incorpo­ rated into descriptions that inc1ude all aspects of stern anatomy.

Saururus cernuus (Fig. 1-10) Epidermis and cortex with thin primary walls. Cortical parenchyma cells large, isodiametric as seen in transection (Fig. 1-3), square to rectangular as seen in longisections; starch common in cortical parenchyma. Thin-walled idioblasts contain­ ing solid yellowish masses scattered in 1-3 outermost cortex layers and also present in phloem (Fig. 1, 2, dark cells in phloem). A scattering of isodiametric cells with thin but lightly lignified walls present in cortex and pith. Thin-walled cortical cells with variously granular contents, likely ethereal oil cells, scattered in idioblastic fashion in

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Fig. 1-5. Seetions of Saururus cernuus. - 1 & 2: Vascular bundles from rhizome. - 1: Larger bundle; fiber-tracheids in central portion of bundle have been produced by cambium, as has an equivalent amount of the phloem, in all likelihood. - 2: Smaller bundle; fiber-tracheids are not present; radial cell seriation in interfascicular areas, right and left, indicate vestigial cam­ bi al activity. - 3: Vascular bundle from aerial stern; vestigial cambial activity indicated by tangential divisions at left. - 4: Rhizome longisection, showing Casparian strip (left) in endoder­ mis. - 5: Scalariform perforation plate from radial rhizome seetion, showing forking in two bars. - Fig. 1-3, scale above Fig. 1; Fig. 4, 5, sc ale above Fig. 4 (divisions = 10 J.lIll) .

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Fig, 6-10. Saururus cemuus, seetions of tracheary elements from radial section of rhizome. - 6-8: Vessel seetions showing perforation plates. - 6: Perforation plate, upper left, similar to the lateral wall pitting of vessels elsewhere in the photograph. - 7: Perforation plate with inter­ connections among the bars. - 8: Portion of long perforation plate. - 9: Two fiber-tracheids (center) with clearly bordered pits. - 10: Fiber-tracheid with vestigially bordered pits. - Fig. 6-10, scale above Fig. 4.

Downloaded from Brill.com10/07/2021 08:30:43AM via free access 138 IAWA Journal, Vol. 16 (2), 1995 cortex and pith, Idioblasts with relatively thick walls present in cortex and pith: these idioblasts circular in transection, elongate in longisection and often with widened ends (i,e" osteosc1ereids) and mostly in vertical files; in pith, sometimes in groups of three or four, Thin-walled parenchyma cells facing the osteosc1ereids contain numerous small calcium oxalate crystals with rhomboidal shapes (Fig, 11, sc1ereid wall at left) , Endodermis with Casparian strip present (Fig, 4), Most vascular strands with proto­ phloem fibers, tibers lacking only in a few smaller strands (Fig, 1, 2), Extraxylary fibers also present at pith margins of vascular strands (Fig, 2, 3), Secondary growth,is evident in ray areas as files of cells, some subdivided relatively recently (Fig, 2, left and right; Fig, 3, left) , In fascicular areas, sieve tube elements in radial rows (aJ;ld therefore likely derived from cambial activity); a central group of imperforate tracheary elements (Fig. 1, dark cells in center) present in larger vascular strands also shows some radial seriation. Radial seriation is not c1early evident in vessels (perhaps be­ cause of their enlarging during cell maturation), but a portion of the vessels likely derived from the cambium. This situation is discussed later. Earlier phloem devoid of companion cells; some later formed sieve-tube elements storied, but most not. Both thin-walled (primary xylem, chiefly) and thick-walled (secondary xylem, chiefly) axial parenchyma present, the latter often in strands of two cells as seen in longisection. Vessel elements with scalariform perforation plates (Fig. 5 - 8), mean number of bars 14.0 (this condition shown in Fig. 5). Bars occasionally forked (Fig. 5, 6, 8), some­ times with interconnections (Fig. 7). All bars bordered. Lateral wall pitting mostly scalariform (Fig. 6, lower half; Fig. 7, lower half; Fig. 9, upper left), infrequently transitional or alternate. Mean vessel element length 590 !IDl; mean diameter of vessel lumen at widest point 72 !IDl (range 20-104 !IDl). Mean vessel wall thickness 1.8 !IDl. Fiber-tracheids present in larger bundles, surrounded on all sides except the cambial side by vessels (Fig. 1). Most fiber-tracheids septate. Bordered pits prominent on walls of fiber-tracheids facing vessels (Fig. 9), contacts between pairs of imperforate tracheary elements typically vestigially bordered (Fig. 10). Mean fiber-tracheid diameter at wid­ est point 22 !IDl, mean wall thickness 2.5 !IDl. Stern anatomy similar to that of rhizomes except that stern bundles are commonly smaller (Fig. 3) and usually lacking in fiber-tracheids. Divisions indicative of cambial activity in interfascicular areas present in some places (Fig. 3, left), lacking in others. Air spaces in pith and cortex less conspicuous than in the rhizomes.

Houttuynia cordata rhizomes (Fig. 11-19) Epidermis composed of small thin-walled cells (Fig. 12). Stomata raised. One layer of starch-free hypodermis present. Phellogen origin in cortex layer beneath the hypodermis. Cortical parenchyma composed of cells circular in transeetion (Fig. 12), but markedly elongate in longisection. Most cortical cells rich in starch and some with a single druse each; cells without starchy contents probably ethereal oil cells. A few elongate cells with thin lignified walls distributed idioblastically in the cortex. Pith composed of thin-walled parenchyma cells, round and enlarged; most pith cells with stareh, a few lacking in starch and distributed idioblastically are likely ethereal oil cells. Severallayers of thick-walled sc1ereids present as a cylinder around the stern

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Fig. 11-14. Seetions of Houttuynia cordata. - 11. Cells from longisection of rhizome; wall of osteosclereid, left; cells adjacent to the osteosclereid contain crystal sand. - 12-14: Transections of rhizome. - 12: Lower magnification, showing that the fibrous sheaths of bundles are inter­ connected by fibers. - 13: Larger bundle, with about 20 fiber-tracheids produced by secondary growth (radial seriation visible in some pairs of these cells). - 14: Smaller bundle, very few fiber-tracheids present. - Fig. 11, scale above Fig. 4; Fig. 12, scale above Fig. 12 (divisions = 10 ~); Fig. 13 & 14, sca1e above Fig. 1.

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Fig. 15-19. Houttuynia cordata, tracheary elements from radial section ofrhizome. -15: Per­ foration plate and alternate lateral wall pitting on vessel, left. -16: Perforation plate with inter­ connections between bars, right. -17: Scalariform lateral wall pitting of larger vessel. -18: Lateral wall pitting of two vessels: transitional pitting, left; sparse alternate pitting, right. -19: Two fiber-tracheids with circular bordered pits. - Fig. 15-19, scale above Fig. 4.

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Fig. 20-24. Anemopsis californica, seetions of stern. - 21 & 22: Stern transeetions. - 20: Entirety of a fascicular area frorn stern, interfascicular area (ray) at right. - 21: High rnagnification - largest cells are vessels, smaller thick-walled cells are tracheids, smaller thin-walled cells are axial parenchyrna. - 22 & 23: Tangential seetions. - 22: Vessel with simple perforation plate and scalariform lateral wall pitting. - 23: Fascicular area (left) and portion of ray (right). - 24: Radial seetion; upright ray cells, upper right; tyloses in vessels at left, especially in vessel at lower left. - Fig. 20, 23, 24, scale above Fig. 1; Fig. 21, 22, scale above Fig. 4.

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(Fig. 12-14); these sclereids are intercontinuous with the extraxylary fibers that sheathe the vascular strands (Fig. 12-14). Endodermis with Casparian strip present as the cell layer external to the fibers. No cambial activity evident in interfascicular areas. Cambial activity evident in vascular strands by virtue of radial seriation of sieve tube elements (these rows radiating from the indented point of protophloem fibers, Fig. 13) and by virtue of other criteria, discussed below. Radial seriation indicative of cambial activity also evident in fiber-tracheids in those strands in which fiber-tracheids are more abun­ dant (e. g., Fig. 12). Vessels present in a U-shaped arc as seen in transection, ',',rith fiber­ tracheids, if present, external to and adjacent to the vessels (Fig. 12-14). Thin-walled parenchyma present among the vessels (Fig. 13, 14). Perforation plates scalariform (Fig. 15, 16), often with a few interconnections between bars (Fig. 15) or forkings of bars (Fig. 16). Mean number of bars 14.7. Bars all bordered. Lateral wall pitting scalariform (Fig. 17), transitional, or alternate (Fig. 18), the three types about equally common. Mean vessel element length 993 j..Ull; diameter of vessel lumen at widest point 55 j..Ull. Mean vessel wall thickness 2.4 j..Ull. Fiber-tracheids with clearly bordered pits on contacts between fiber-tracheids and vessel elements or parenchyma (Fig. 19), pits with vestigial borders on contacts between fiber-tracheids. Mean diameter of fiber­ tracheids 17 j..Ull; mean wall thickness 2.4 j..Ull. Axial parenchyma among fiber-tracheids with lignified walls and in strands of two cells. Anatomy of stern very similar to that of rhizome, but in the stern, two or three ceU layers beneath the hypodermis contain chloroplasts.

Anemopsis californica (Fig. 20-24) Thick periderm present on stern. Cortical and pith parenchyma cells globose to ovoid in transeetion and longisection, associated with large air spaces (but not as large as those of aerenchyma). Parenchyma ceUs fiUed with starch. Idioblastic ethereal oil cells in cortex and pith, slightly larger than neighboring parenchyma cells and devoid of starch. Endodermis absent. Secondary growth of indefinite extent, although not suf­ ficient to characterize the stern as woody (Fig. 20). Primary and secondary phloem devoid of fibers, and fibers absent elsewhere in stern (Fig. 20). Vessels mostly grouped (Fig. 20). Vessels with simple perforation plates (Fig. 23), a very few with two or three circular perforations seen. Lateral wall pitting of vessels mostly scalariform (Fig. 22), some transitional and alternate pitting present; if alternate, the pits laterally widened. Vertical pit diameter about 4 j..Ull. Tyloses common in vessels (Fig. 24). Mean vessel element length 163 j..Ull; mean vessel lumen diameter at widest point 48 j..Ull (range = 17-72 j..Ull). Mean vessel wall thickness 2.8 j..Ull. Vessel elements at least three times as abundant as tracheids (Fig. 20), some fascicular areas devoid of tracheids. Tracheids, the sole type of imperforate tracheary element present, identifiable with certainty only in macerations because of their resemblance to narrow vessels. Tracheids with densely placed fuUy bordered pits; pits oval, about 4 j..Ull in vertical dimension. Mean tracheid length 230 j..Ull. Mean tracheid waU thickness 2.0 j..Ull (Fig. 21). Axial parenchyma with thin nonlignified walls common among the vessels (Fig. 20, 21); as seen in longitu­ dinal section, the axial parenchyma not subdivided or, less commonly, in strands of two cells. Rays wide (typically about 20 cells wide at widest point, mostly between

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1,000 !ill1 and 2,000 !ill1 tall). Outer 2 or 3 celllayers of rays composed of upright cells (Fig. 23, left; Fig. 24, right), central portions of rays composed of square to procumbent cells. Occasional ethereal oil cells present in rays. Upright cells of rays occasionally storied. The occurrences of ethereal oil cells in sterns of Anemopsis, Houttuynia, and Saururus are all new records for the family. The only previous record of ethereal oil cells in Saururaceae is in leaves of Saururus (see Gregory & Baas 1989). Stern endodermis has been reported for Houttuynia by Metcalfe and Chalk (1950), but the record for Saururus is new. All instances given above for secondary growth in Saururaceae are new reports.

Secondary growth: criteria and problems Secondary growth is quite obvious in Anemopsis, although the section shown in Figure 20 does not show much secondary growth. This section was selected for illus­ tration because of its optimal sectioning. Other stern transeetions of Anemopsis, less well sectioned than the one illustrated, have several years of secondary xylem accu­ mulation and even growth rings with somewhat narrower vessels in latewood. The secondary growth of Anemopsis is much like that of Aristolochia, which shows less active addition to ray areas than in fascicular areas (Carlquist 1993). Radial seriation of phloem and xylem cells is mentioned above as a possible indica­ tion of secondary growth presence, and where extensive, as in Anemopsis and even Saururus, this can be cited as a criterion. However, various authors mention that tan­ gential divisions leading to radial seriation in xylem and phloem cells of a bundle can occur in procambium (Philipson et al. 1971). The fact that cambia are less active in ray areas than in fascicular areas is one reason why secondary growth can be claimed in Saururus, since interfascicular cambium is vestigial in that genus. There are other criteria, however, but a number of criteria that might be advanced are not applicable. For example, Philipson et al. (1971) mention addition of uniseriate rays by fascicular cambial areas. However, Piperales do not have uniseriate rays added by fascicular cambium, regardless of the extent of secondary growth; this is one of the interesting characteristic features of Piperales, in fact. One cannot doubt that extensive secondary growth is present in large woody sterns of Piper, but uniseriate rays are absent in those sterns. Esau (1965), after discarding other criteria for citing secondary growth as present because of exceptions, mentions the drop in tracheary element length just prior to commencement of secondary growth, after which point there is an upswing in tracheary element length, as a reliable criterion. However, Esau was unaware than in many 'woody herbs' with various growth forms other than strongly woody, there is often a continual drop in tracheary element length during secondary growth (Carlquist 1962). In fact, one of the examples cited in that paper is Macropiper, a piperalean genus, although many dicotyledons outside of Piperales show a drop in tracheary element length dur­ ing secondary growth, no matter how extensive. Saururaceae, like Macropiper, follow a paedomorphosis curve rather than the curve characteristic for strongly woody dico­ tyledons.

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One subsidiary indication of secondary growth does see m a feature worthy of con­ sideration: absence of imperforate tracheary elements in primary xylem, In primary xylem of Aristolochiaceae, as in monocotyledons, parenchyma is intermixed with ves­ seI elements, and imperforate tracheary elements are absent. As secondary growth be­ gins, imperforate tracheary elements are produced. In the bundles of Houttuynia and Saururus, vessels are at first formed together with parenchyma (Fig. 1-3, 13, 14). By the time imperforate tracheary elements are formed, secondary growth is present in our opinion. Occurrence ofbundles encased in sc1erenchyma, like those of Houttuynia (Fig. 13, 14) may be thought by some to prove absence of secondary growth. However, in transections of sterns of annual Asteraceae prepared by the first author, some second­ ary growth can be seen within bundles encased in sc1erenchyma (unpublished data). To be sure, only very limited quantities of secondary growth are to be expected when bundles are encased in sc1erenchyma.

Ecological conclusions There is a marked contrast between the scalariform perforation plates of Houttuynia and Saururus on the one hand and the simple ones of Anemopsis on the other (perfora­ tion plates in roots of Anemopsis are also simple). The simplest explanation for this contrast among the genera would be that Houttuynia and Saururus have had an un­ broken his tory of occupancy of mesic sites, whereas Anemopsis has had some seasonal exposure to dry conditions during its evolutionary history - perhaps as much today as in the past. The present-day habitats of Anemopsis show fluctuation in water availability, al­ though descriptions in floristic literature do not illuminate the precise degree of season­ ality in water availability in various Anemopsis habitats. The simple perforation plates are not related to survival through dry periods, but rather rapid conduction when water is available after a dry period, judging from the ecological distribution of this perfora­ tion plate type in dicotyledons at large (Carlquist 1975). Other xeromorphic features of Anemopsis wood, judging from citation of these features in literature on ecological wood anatomy, inc1ude short vessel elements, thick-walled vessel elements, presence of tracheids, and the large amount of stern parenchyma (which likely stores water, not merely starch). Vessel grouping occurs prominently in Anemopsis. Grouped vessels are likely a feature that permits maintenance of conductive pathways when embolisms deactivate some vessels in a group (Carlquist 1984). The presence of tracheids in a wood tends to deter grouping of vessels (Carlquist 1984), but this is not operative in Anemopsis because of the paucity of tracheids in this plant: they are present in such small numbers that they would not consititute an effective subsidiary conductive sys­ tem. The thick periderm (most of which is phellern) likely prevents loss of water dur­ ing dry periods. The presence of tracheids as a subsidiary conductive system has been cited as a xeromorphic feature of woods in Mediterranean-type c1imates where water availability fluctuates markedly (Carlquist 1985). The tracheids of Anemopsis are densely pitted, suggesting that they are effective in conduction but have minimal

Downloaded from Brill.com10/07/2021 08:30:43AM via free access CarIquist, Dauer & Nishirnura - Stern anatorny of Saururaceae 145 mechanical function. The thick periderm on sterns of Anemopsis likely minimizes ex­ cessive water loss, a probable adaptation to c1imates that feature a dry season. The fiber-tracheids of Houttuynia and Saururus are likely not primarily of conduc­ tive significance. Although at least some of the fiber-tracheids have fuHy bordered pits (in others pits are vestigially bordered), the fiber-tracheids of Houttuynia are nuc1eate and those of Saururus are septate, indications that conductive function is absent. The stern structure of Houttuynia and Saururus is not indicative of any xeromorphy. Scalariform perforation plates, which are characteristic of these two genera, are corre­ lated with mesic habitats (Carlquist 1975). There are few herbaceous or minimally woody dicotyledons with scalariform perforation plates in secondary xylem: the ex­ ceptions are Paeoniaceae (Keefe & Moseley 1978) and Pentaphragmataceae (Carlquist 1975). The scalariform perforation plates of Pentaphragma may, in part, be indicative of paedomorphosis, but such plates in Houttuynia and Saururus, as weIl as in Paeonia, are likely indicators of continuous occupancy of mesic sites by those genera.

Phylogenetic and systematic conclusions Anemopsis differs from Houttuynia and Saururus in its indefinite amount of sec­ ondary growth, lack of extraxylary fibers, lack of an endodermis, lack of sc1eren­ chymatous idioblasts in cortex or pith, presence of simple perforation plates on vessel elements, presence of tracheids rather than fiber-tracheids, and presence of thick phel­ lern on sterns. Most of these features are related to ecology, as noted above, but they can be cited in a systematic context regardless of their functional basis. Houttuynia differs from Saururus in aseries of anatomie al features, none of which secm directly related to ecology, because the two genera occupy much the same kind of habitat. Saururus has appreciable secondary growth in vascular bundles, and some in ray areas; in Houttuynia secondary growth in vascular bundles is less, and cambial activity is lacking in interfascicular areas. Saururus has protophloem fibers as weH as fibers at the pith margins of vascular bundles, whereas in Houttuynia, extraxylary fibers form a complete sheath around vascular strands and form a cylinder around the stern as weIl, interconnecting the vascular bundles. Saururus has osteosc1ereid idioblasts en­ sheathed by cells containing erystal sand composed of rhomboidal birefringent crys­ tals, whereas pith and cortex of Houttuynia have equivalent idioblasts that have thin lignified walls and are fusiform to rectangular in shape; in Houttuynia, druses occur diffusely in pith or cortex. Houttuynia has astern hypodermis, Saururus does not. There is little difference between the two genera with respect to perforation plates, but thc reduction in cambial activity in Houttuynia is best interpreted as a specialization. Tucker et al. (1993) present a c1adistic analysis of Saururaceae and Piperaceae, and several of the trees they present appear to show Anemopsis as possessing the greatest number of derived character states, and pair Anemopsis c10sely with Houttuynia. However, some of the trees they present show a lack of resolution of genera within Saururaceae. The relatively abundant secondary growth and the tracheids of Anemopsis would appear more likely ancestral character states, although the simple perforation plates are apomorphic.

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Saururaceae have traditionally been placed close to Piperaceae, and the two fami­ lies have constituted the order Piperales (e. g., Dahlgren 1980). The results of Tucker et al. (1993) confirm this proposed relationship. Dahlgren (1980) placed Aristolochia­ ceae next to Piperales, as did Cronquist (1988). The wood ofLactoridaceae is remark­ ably similar to that of Piperaceae (Carlquist 1990), as is that of Aristolochiaceae (Carlquist 1993). These groupings foreshadow a clade that includes Aristolochiaceae, Lactoridaceae, Piperaceae, and Saururaceae in the scheme of Qiu et al. (1994), which is based upon rbcL evidence. In a monograph on wood anatomy of Aristolochiaceae, Carlquist (1993) listed ten distinctive wood features that unite Aristolochiaceae with Lactoridaceae and Piperaceae. From this listing, the following eight features can also be found in Saururaceae: ves­ sels with simple perforation plates (Anemopsis only); vessels in radial chains or pore multiples; vessel to axial parenchyma pitting scalariform to alternate; imperforate tracheary elements with vestigially bordered pits (Houttuynia, Saururus); axial paren­ chyma not subdivided or in strands of two cells; rays wide and tall with little ontogenetic subdivision (rays wide and not subdivided in Anemopsis, but rays short in that genus perhaps because of shortness of internodes); ray cells mostly upright (Anemopsis); upright ray cells in severallayers adjacent to fascicular areas (Anemopsis). The two features from the 1993 listing that do not characterize the Saururaceae studied are scanty vasicentric axial parenchyma and storying. Axial parenchyma distribution in woods is described on the basis ofaxial parenchyma within a fibrous background; such a background is absent in Anemopsis (and thus, for example, diffuse parenchyma could not be present), but there are axial parenchyma cells between vessels (Fig. 21), so in asense, scanty vasicentric parenchyma could be said to be present in Anemopsis. No extensive storied areas were observed in tangential sections of the three species studied, but some storying in phloem was observed in Houttuynia; occasionally a few upright ray cells in Anemopsis appeared storied. These instances were regarded as insufficient to claim that storying really is present. In fact, appreciable numbers of cambial divisions that increase cambial circumference must occur before storying is exhibited; the relatively small amount of cambial activity in Saururaceae is likely in­ sufficient for storying to be visible to any extent. Thus, the list of features that unite Aristolochiaceae, Lactoridaceae, and Piperaceae is very nearly realized also in Saururaceae, and the relative lack of woodiness in Saururaceae may account for the relatively few incongruities. Wood evidence does support the grouping of the four families as represented in the rbcL cladogram of Qiu et al. (1994). However, one must note that one of the wood features listed above, simple perforation plates, occurs in Anemopsis but not in Houttuynia or Saururus, which have perforation plates with numerous bars (plates with one bar are occasional near the pith in Lactoris wood: Carlquist 1990). Assuming the four families form a natural group, scalariform perforation plates are probably a plesiomorphy for the clade, and simple perforation plates have been evolved not only within Saururaceae in the case of Anemopsis, but also at least one other time in the three families other than Saururaceae. The presence of scalariform perforation plates (and with borders on the bars, a primitive condition) in this clade is interesting, because scalariform perforation

Downloaded from Brill.com10/07/2021 08:30:43AM via free access Carlquist, Dauer & Nishirnura - Stern anatorny of Saururaceae 147 plates tend to occur in so few herbaceous families - only Paeoniaceae and Penta­ phragmataceae, as noted above. The presence of scalariform perforation plates in Pentaphragma may involve paedomorphosis (Carlquist 1975), but the occurrence of scalariform plates in Paeonia does not involve any such ontogenetic process and seems a simple retention of a primitive wood feature, as in Saururaceae. Scalariform perfora­ tion plates also occur in some minimally woody Chloranthaceae - Chloranthus and Sarcandra (Carlquist 1992). The ancestry of Chloranthaceae may be minimally woody, with arborescence, as in Hedyosmum, secondary (Carlquist 1992). Chloranthaceae are not far from Saururaceae in some recent cladograms (e. g., Taylor & Hickey 1992, Qiu et al. 1994). The occurrence of such a signal indicator of primitive wood as scalariform perfo­ ration plates in minimally woody phylads such as those that include Saururaceae and Chloranthaceae lends support to the concept of paleoherbs (Taylor & Hickey 1992). To be sure, the cladogram of Qiu et al. (1993) recognizes two groups of paleoherbs: Chloranthaceae and Nymphaeaceae fall into a clade not direcdy adjacent to the clade that includes Aristolochiaceae, Lactoridaceae, Piperaceae, and Saururaceae (the pres­ ence of stern endodermis is a curious similarity between Chloranthaceae and Saurura­ ceae worthy of mention in this context). One can ask how herbaceous the paleoherbs really were, either as an entire group or in terms of ancestral genera. Nymphaeaceae are thoroughly adapted to the aquatic habit, and lack of secondary xylem in them is congruent with adaptation to that extreme habitat. Secondary xylem does, however, characterize all of the remaining families of paleoherbs-the report in the present paper of secondary xylem in three genera of Saururaceae is notable in this regard. The ju­ venilistic rays of Aristolochiaceae, Chloranthaceae, Lactoridaceae, Piperaceae, and Saururaceae suggest that at least some woodiness in these families may be secondary. The concept of 'paleoherb' need not connote complete absence of cambial activity, and evidence from the wood anatomy of the paleoherb families suggests that paleoherbs did have some cambial activity except for Nymphaeaceae, in which lack of cambial activity seems likely an apomorphy. In fact, the data matrix of Taylor and Hickey (1992) agrees with this interpretation.

Saururaceae and the origin of monocotyledons The cladogram of Qiu et al. (1993) places the four families of the piperalean clade close to the origin of monocotyledons, along with Laurales. All of these families have ethereal oil cells, as do Chloranthaceae and the families of Magnoliales (Gregory & Baas 1989). Origin of monocotyledons may thus be hypothesized to involve loss of ethereal oil cells. Attention has been called to the sympodial habit as likely basic to monocotyledons (Carlquist 1992). The sympodial habit characterizesAristolochiaceae (Apama, Thottea), Chloranthaceae (Chloranthus, Sarcandra), and many Piperaceae. The sympodial habit occurs in Gymnotheca, Houttuynia, and Saururus; the rosulan habit of Anemopsis is likely an apomorphy. There is every reason to consider the sympodial habit as plesiomorphic in the paleoherbs, and this is a link between them and the mono­ cotyledons, which are basically sympodial even though in some groups (e. g., palms) a

Downloaded from Brill.com10/07/2021 08:30:43AM via free access 148 IAWA Journal, Vol. 16 (2), 1995 rosulan habit has been evolved. Related to the sympodial habit is presence of adventi­ tious roots. Adventitious roots are characteristic of all Saururaceae. Seedling data on Saururaceae are not available, but likely the seedling primary root is as ephemeral in Saururaceae as it is in monocotyledons. Origin of monocotyledons must have featured reduction of cambial activity. Tn­ deed, some sources generalize that absence of cambial activity characterizes monocotyledons, but Philipson et al. (1971) note that cambia that produce tracheids and sieve elements may be present in a few monocotyledons, such as Gloriosa and Veratrum; these cambia, however, do not produce any ray tissue. The limited cambial activity of Houttuynia and Saururus is reminiscent of this condition: there is a fascicular cambium in both genera, but it does not produce ray tissue. Interfascicular cambial activity is minimal in Saururus and absent in Houttuynia. Thus, Houttuynia and Saururus perfectly represent the changes that must have occurred in origin of monocotyledons. Others of the piperalean clade are also relevant. Rays are often initiated within fascicular areas of dicotyledons, often as uniseriate rays. However, no rays are initiated within the fasicular areas of Saururaceae, nor are they in most Aristolochiaceae (Carlquist 1993), Lactoridaceae, or Piperaceae (Carlquist 1990). Rays do not originate in fascicular areas of Chloranthus and Sarcandra of the Chloranthaceae (Carlquist 1992). In addition to minimization of fascicular cambium in Houttuynia and Saururus, the vascular strands of these two genera show a stage in the extinction of mechanical tissue (tiber-tracheids) produced by the cambium. This extinction of cambially pro­ duced mechanical tissue coexists with production of extraxylary tibers produced from procambium: tibrous sheaths around vascular strands of Houttuynia and at poles of vascular strands of Saururus. The tibers interconnecting the vascular strands in Houttuynia must, on the basis of their position, originate from ground meristem rather than procambium. A central conceptual point concerns the absence of mechanical tis­ sue within vascular bundles of monocotyledons, in which bundles are typically sur­ rounded by extraxylary tibers. Mechanical tissue within xylem depends on origin of vessels, because without origin of vessels, there is no division of labor into conduc­ tively efticient cells (vessel elements) and mechanically strong cells (tiber-tracheids, libriform tibers). This division of labor is evident in its most minimal form in the roots of Sarcandra (Carlquist 1987). Is this division of labor present without secondary growth? Apparently not, which is a feature rarely discussed: primary xylem, whether the conductive cells are tracheids (ferns, conifers), or vessel elements (specialized dico­ tyledons) or a mixture of vessel elements and tracheids, contains parenchyma sepa­ rating these conductive cells, and mechanical cells are lacking within the xylem itself. Therefore, in origin of monocotyledons, bundles likely had extraxylary tibers, but mechanical cells in the form of imperforate tracheary elements within the secondary xylem were lost as secondary xylem itself was extinguished (see discussion of criteria for secondary growth presence, above). The stern vascular bundles of the mono­ cotyledons Gloriosa and Veratrum contain only tracheids, so no origin of vessels with its attendant division of labor is present in these monocotyledons despite their reten­ tion of some cambial activity. Vessels, as well as cambial activity, were already present in the ancestors of the piperalean clade, so that tiber-tracheids as well as vessels are

Downloaded from Brill.com10/07/2021 08:30:43AM via free access Carlquist, Dauer & Nishimura - Stern anatomy of Saururaceae 149 produced by the cambium in Saururaceae, minimal though the activity of the fascicu­ lar cambium is in Houttuynia and Saururus. Houttuynia and Saururus have vessels more primitive than those of any other paleoherbs, except for Chloranthaceae. Not only are perforation plates scalariform in Houttuynia and Saururus, scalariform lateral wall pitting is common. However, pri­ mary xylem tends to contain xylem more primitive than that of secondary xylem in any particular dicotyledon (Bailey 1944), and the vessels of these two genera are in primary xylem or, if in secondary xylem, likely to have a morphology similar to ves­ sels of the primary xylem because so little secondary xylem is produced. Floral trimery, a notable feature of monocotyledons, occurs in Magnoliales (espe­ cially Annonaceae and Magnoliaceae) and Laurales (especially Hernandiaceae and Lauraceae). Trimery is clear in two families of the piperalean clade, Aristolochiaceae (perianth) and Lactoridaceae (all floral whorls). Trimery occurs in Chloranthaceae (ves­ tigial perianth in some genera). In Saururaceae, six stamens characterize Anemopsis, Gymnotheca, and Saururus, while Houttuynia has three (Liang & Tucker 1990). Three carpels occur in Anemopsis and Houttuynia (Liang & Tucker 1990). However, Liang and Tucker (1. c.) offer this apparently contradictory statement: "The paleoherbs ... are said to have two perianth cycles and trimery. Neither character, however, is found in Saururaceae nor in Piperaceae." This statement is likely not an outright error, but rather based on Tucker's discovery that unusual ontogenetic sequences underlie the stamens and carpels of Saururaceae (see papers cited in Liang & Tucker 1990). The primordium ontogenies seen in flowers of Saururaceae and Piperaceae may be influ­ enced by the spicate condensation of inflorescences. In any case, the trimery of sta­ mens and carpels of Saururaceae as cited above is certainly clear at anthesis. In sum, Saururaceae have anatomical features concordant with the idea that the family is close to other families of the piperalean clade and, in turn, close to the origin of monocotyledons. The primitive vessels and loss of cambial activity in Houttuynia and Saururus are particularly compelling as anatomical conditions that resemble stages in monocotyledon origin, but other features should be considered in this regard (e.g., pollen grains).

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