EVIDENCE FOR A CONDUCTING STRAND IN EARLY SILURIAN (LLANDOVERIAN) PLANTS: IMPLICAnONS FOR THE EVOLUTION OF THE LAND PLANTS
KARL J. NIKlAS AND VASSIUKI SMOCOVITIS
Made in United States ofAmerica Reprinted from PALEOBIOLOGY Vol. 9, No.2, Spring 1983 Copyright © 1983 The Paleontological Society Paleobiology, 9(2), 1983, pp. 126-137
Evidence for a conducting strand in early Silurian (Llandoverian) plants: implications for the evolution of the land plants
Karl J. Niklas and Vassiliki Smocovitis
Abstract.-Macerations of fragmented plant compressions of Silurian (Llandoverian) age yield sheets of organic material bearing ridges and depressions (interpreted as corresponding to surficial dimensions of cells), fragments of smooth walled tubular elements, and fragments of tubular elements with differentially thickened walls ("banded tubes"). A fragment of tissue (1.2 mOl long), consisting of smooth walled tubes (17 ± 6.9 ""'01 in diameter), surrounding 2-3 larger (18.8 ± 2.1 ""'01 in diameter) banded tubes, wasisolated from an irregularly shaped, relatively large (1 x 3 mOl) compression. Comparisons between (I) fragments of tubular cell types, not organized into strands, isolated from 122 compressions, and (2) dispersed tubular cell types previously reported from the Massanutten Formation and other Silurian formations (Tuscarora and Clinton), reveal no significant morphologic differences. Comparisons between the organization of smooth-walled and banded tubular cell types found in the tissue strand and the or~anization of cell types in nematophytic plants (Nematothallus, Nematoplexus, Prototaxites) indicate a similarity in construction (tubular) hut a lack of correspondence in organization. The strand of tissue is interpreted as representing part of the internal anatomy of a nonvascular land plant of unknown taxonomic affinity. On the ba-,is of analogy with present-day embryophytes, the strand of tubular cell types is inferred to have functioned as a conductive tissue. The significance of "banded tubes" in Silurian strata is discussed, and it is concluded that, until more is known about the anatomy, morphology, and biochemistry of the parent plant(s), the habitat and systematic affinity of these organisms are conjectural.
Karl 1. Niklas and Vassiliki Smocovitis Section of Plant Biology, Cornell University, Ithaca, New York 14853
Accepted: May 3 I, 1983
Introduction analogous in function to supportive or conduct Previous studies of Llandoverian and Wen ing plant cell types. lockian compression fossils from North America This paper describes additional plant have recognized three categories of microfossils: compressions collected from the localities pre (1) tubular elements of variable length having viously reported by Pratt et al. (1978) in the smooth and banded (=differentially thickened) lower Massanutten Sandstone, Virginia. Among walls, (2) membranous sheets of organic mate the various cell and tissue fragments recovered rial bearing irregularly shaped depressions, and from 122 plant fragments, a single strand of tis (3) alete and trilete spores, and tetrads (Gray sue was isolated consisting of smooth-walled tu and Boucot 1977; Pratt et aI. 1978; Strother and bular elements surrounding a small number of Traverse 1979). Llandoverian microfossils from banded tubular cell types. This fragment of tis the Massanutten Formation of Virginia are sue, interpreted to be part of the internal anat thought to be the fragmented remains of a non omy of an as yet unspecified macrophyte, is the vascular macrophyte of unknown taxonomic af largest fragment thus far reported for the Mas finity based on an inferred fluvial depositional sanutten localities, and provides evidence for a environment, the presence of spores, and chem discrete organization of smooth and banded ical composition (Pratt et aI. 1978; Niklas and tubes. In addition to the new morphologic in I3 Pratt 1980). Owing to poor preservation, the formation, stable isotope (6C ) analyses of du general morphology and internal organization plicate fossils are presented. In conjunction with of these plants were previously unknown. How previously reported organic chemical profiles,
er I Pratt et aI. (1978) have speculated that the these data provide some insight into the bio th and banded tubes represent fragments chemical composition of the Massanutten plant bular-filamentous tissue (nematophytic), remains. The additional morphologic and bio , e Paleontological Society. All rights reserved. 0094.8373/8310902--o00S/$I.00 EVOLUTION OF LAND PLANTS 127
30 chemical data presented here and elsewhere (d. SKEWNESS" fbt = 0 614* KURTOSIS'" bz = 254 t Niklas 1982) are relevant to the biologic inter 25 KURTOSIS = 0 =0.19* 25 24 n = 122 pretation of the Massanutten fossils and provide "z w i = 1.32 a context for evaluating current concepts on the ! 20 19 v =.!051 u w first occurrence of the land plants and the sub " 16 "" 15 sequent appearance of tracheophytes (Banks o 13 a: 10 1975; Gray and Boucot 1977, 1979). w 10
sheets of irregL bearing an Ope rounding transIt /-tm by 7.9 ::t l These dimensiOi for surficial dep under SEM (Fig: of tubular cells ations: (1) smoot 3 1 /-tm in diam (Figs. 15-19); (;; 11-35 /-tm in di with pronounce 20); and (3) tubt thickened walls 3.6 /-tm, N = 2. "tubes" ranged 6.6),26-110 J.l-rr 7.9), respective) tubular elemen~ ken ends. Stati tubes indicate longer fragment walled tubes. 5. tubular element longitudinally a fragments of tu wall constructic alignment to or were found onL greater in diamE sion). Maceration oj (1 mm wide, 3 r: of tissue (1.2 mr (Fig. 22). Both· transversely, anc length was ocelt monstrable cell
FIGURES 2-12. Re Compressions on su surface, normal to t (Figs. 22-25) was is from which strand v ularities (No. 1204). of matrix (No. 1204 lOA). 280x. Fig. 9, lOA). 280x. Fig. l( ~etate peels of com ,0. 129-130). 22x. EVOLUTION OF LAND PLANTS 129 sheets of irregularly shaped organic material strand was composed of an indeterminate num bearing an opaque reticulum of ridges sur ber of longitudinally aligned, externally smooth rounding translucent areas measuring 6.5 ± 1.3 walled tubes (17 ± 6.9 /Lm in diameter, N = /Lm by 7.9 ± 2.1 /Lm (N = 50) (Figs. 13-14). 28), that surrounded 2-3 banded tubes (18.8 ± These dimensions correspond to those observed 2.1/Lm in diameter) (Figs. 23-25). Examination for surficial depressions on specimens examined of the exposed, internal surface of the banded under SEM (Figs. 8-10). In addition, three types tubes revealed ridges or corrugations 1. 7 /Lm of tubular cells were observed in these macer apart (Fig. 25). ations: (1) smooth-walled, tubular elements, 15 Stable isotope (8CI3) analyses of the compres 31 /Lm in diameter (18 ± 3.6 /Lm, N = 100) sions described here and of the material previ (Figs. 15-19); (2) smooth, thick-walled tubules ously described by Pratt et al. (1978) yield com 11-35 /Lm in diameter (19 ± 4.3 /Lm, N = 56) parable values (-25.6 ± 0, N = 2; -26.2 ± with pronounced fibrillar or frayed ends (Fig. 0.15, N = 2, respectively) (Table 1). 20); and (3) tubular elements with differentially thickened walls, 13-35 /Lm in diameter (23 ± Discussion 3.6 /Lm, N = 20) (Fig. 21). These categories of The most significant finding from the reex "tubes" ranged in length from 26-53 /Lm (34 ± amination of Llandoverian plant remains, pre 6.6),26-110 /Lm (56 ± 10) and 15-50 /Lm (32 ± viously described by Pratt et al. (1978), is a sin 7.9), respectively. However, all three types of gle fragment of tissue consisting of a cylindrical tubular elements were fragmented and had bro strand of smooth-walled tubular cell types sur ken ends. Statistical analyses of "lengths" of rounding 2-3 tubes with differentially thick tubes indicate that banded tubes break into ened cell walls (="banded" tubes). This speci longer fragments than either of the two smooth men is the largest intact tissue fragment (showing walled tubes. Smooth-walled and frayed-ended a discrete biological organization) of a Lower tubular elements were occasionally found to be Silurian macrophyte of presumed terrestrial longitudinally aligned (Figs. 19-20). However, habit. Aside from showing the anatomical re fragments of tubular elements of different cell lationship betweeen smooth-walled and banded wall constructions were not found in parallel tubes in a Silurian plant, the tissue fragment alignment to one another. Tubular cell types has a general morphologic correspondence with were found only in compressions 2.4 mm or the strands of conducting cell types in present greater in diameter (= maximum lateral dimen day embryophytes. The implication that smooth sion). and banded tubes found in some Silurian plants Maceration of a relatively large compression may have functioned as conducting elements in (1 mm wide, 3 mm long) yielded a single strand a terrestrial macrophyte is consistent with the of tissue (1.2 mm long; 88-100 /Lm in diameter) fluvial depositional environment in which these (Fig. 22). Both ends of the strand were broken fossils were buried (d. Pratt et al. 1978), and transversely, and roughly one-fifth of the strand's the isolation from similar fossils of organic length was occluded by a mass lacking any de chemical constituents of a lignin-like nature monstrable cellular structure (Fig. 22). The (Niklas and Pratt 1980; Niklas 1982). Similarly,
FIGURES 2-12. Representative compression fossils from horizon 8-9, Massanutten Formation, Virginia. Figs. 2-3, Compressions on surfaces of bedding plane (specimen No. 1203). 2.5 x. Fig. 4, Compressions as viewed along broken surface, normal to bedding plane (No. 1204). 2.0X. Fig. 5, Compression (between arrows) from which strand of tissue (Figs. 22-25) was isolated (No. 1203). 3.0x. Fig. 6, Enlargement of Fig. 5, showing compression fossils and specimen from which strand was isolated (between arrows) (No. 1203). lOAX. Fig. 7, Surface of compression with surficial irreg ularities (No. 1204). 33 x. Figs. 8-10, Scanning electron micrographs of compression fossils (Fig. 7) cut from larger block of matrix (No. 1204). 280X. Fig. 8, Surficial depressions contiguous over larger lobelike irregularities (SEM stub No. lOA). 280x. Fig. 9, Surficial reticulum of depressions and ridges showing some evidence of a pattern (SEM stub No. lOA). 280x. Fig. 10, Perforations through surfaces of compression (SEM stub No. 14). 578 x. Figs. 11-12, Cellulose etate peels of compression fossils with opaque organic material (arrows) interspersed with less opaque material (slides o.129-130).22X. ----
130 KARL J. NIKLAS & VASSILIKI SMOCOVITIS
the SC l3 values rE compression mat. ~. restrial origin of t (Table 1). :',\ The additiona Llandoverian pia eral issues. The fi around the evol cheid-like" (Gray types among the rian plants, whie interpretation. G erature cited thet tubes represent e terrestrial flora . pearance of vase and Boucot 1977 have argued that groups may have as such these cell uous information affinity or anatorr: Schopf 1978). T: more general qUi pearance of bioct that permitted tt restrial habitat (r- ry et al. 1980; Ni Hill 1980). The p that the early lane ticellular aquatic tures permitting: Niklas 1976; Ra~ bins and Hill (19 evolved into terr· undifferentiated f A.5.5e.55ed on U1f
n t 1 EVOLUTION OF LAND PLANTS 131 the 8Ca values reported for dupliate samples of TABLE I. Stable isotope ratio analyses. compression material are consistent with a ter Sample Description liC l3a restrial origin of the Massanutten plant remains Massanutten A -25.6 (Table 1). Organic matter in shale -25.6 The additional information uncovered for -25.6 0.00" Llandoverian plants has a bearing on two gen Massanutten B Organic matter - 26.4 eral issues. The first is the controversy revolving in shale -26.1 around the evolutionary significance of "tra -26.2 0.15" cheid-like" (Gray and Boucot 1977, p. 164) cell types among the remains of some Lower Silu rian plants, which has resulted in a polarized interpretation. Gray and Boucot (1977 and lit 10 Pairwise comparison between A and B indicates t ,.\£\1 = 2.81 with looo;;2 = 4.30. erature cited therein) have argued that banded tubes represent evidence for the existence of "a vious studies on Llandoverian fossils, the fol terrestrial flora . . . well prior to [sic] the ap lowing sections address the various issues of pearance of vascular plant megafossils" (Gray taxonomic affinity, habitat, function, and evo and Boucot 1977, p. 145). By contrast, others lutionary patterns raised in the literature. have argued that a number of plant and animal Taxonomic affinity.-The fragmented nature groups may have evolved "banded" tubes, and of most Lower Silurian plant remains provides as such these cell types provide at best ambig few morphologic features whereby comparisons uous information on habitat or on taxonomic can be drawn with better-known Paleozoic taxa. affinity or anatomy (Eisenack 1972; Banks 1975; Among the only consistently available features Schopf 1978). The second issue concerns the of Llandoverian and Wenlockian microfossils are more general question of the evolutionary ap the surficial dimensions of cells associated with pearance of biochemical and structural features membranous sheets ("cuticle-like" material of that permitted the survival of plants in a ter Gray and Boucot [1977], p. 161) and the di restrial habitat (Niklas 1976; Raven 1977; Low ameters of tubular cell types (Tables 2-3). Sta ry et al. 1980; Niklas et al. 1980; Stebbins and tistical comparisons among the cellular dimen Hill 1980). The paleobotanical literature argues sions of the Llandoverian material and various that the early land plant flora evolved from mul better-known thallophytes reveal no significant ticellular aquatic green algae that acquired fea differences (Table 4). Thus quantitative com tures permitting survival on land (Bower 1908; parisons among cell fragments for purposes of Niklas 1976; Raven 1977). By contrast, Steb assessing systematic affinities become a futile bins and Hill (1980) have proposed that plants exercise, and emphasis must be placed on qual evolved into terrestrial habitats as unicellular, itative differences. undifferentiated forms living in the soil. Although smooth and banded tubes have been Assessed on the basis of the present and pre- frequently reported as components of Lower Si-
FIGURES 13-25. Fragments of tissue and tubular elements isolated from macerations of Llandoverian plant compressions from the Massanutten Formation in Virginia. Figs. 13-14, Membranous sheets of organic material bearing elliptical to irregular depressions (cf. Figs. 8-10). Fig. 13 (slide No. 210). 344X. Fig. 14 (slide No. 53). 350x. Figs. 15-18, Fragments of smooth-walled tubes isolated from macerations. Fig. IS (slide No. 93). 580x. Fig. 16 (slide No. 55). 580X. Fig. 17 (slide No. 113). 43S x. Fig. 18 (slide No. 110). 435 x. Fig. 19, Two partially aligned (between arrows) smooth-walled tubes (slide No. 207). 580 x. Fig. 20, Scanning electron micrograph of parallel aligned tubes with frayed or "fibrillar" broken ends (arrows) and striationslfractures along external surfaces (SEM stub No. II). 745 x. Fig. 21, Tubular cell type with differentially thickened cell walls (arrows); compare with Fig. 25 (slide No. 103). 832 x. Figs. 22-25, Scanning electron micrographs of a strand of tissue isolated from a single compression (cf. Figs. 5-6) (SEM stub No. II). Fig. 22, Banded tubes (a) surrounded by smooth-walled tubes (b), and amorphous organic material (e) occluding surface of tissue strand. 1l0X. Fig. 23, Enlargement of broken end of strand (cf. Fig. 22a) showing internal banded tubes (a) and external smooth walled tubes (b). 432 x. Fig. 24, Enlargement of region (cf. Fig. 23b) showing rounded ends of smooth-walled tubes (arrows). 1.15kx. Fig. 25, Enlargement of fractured end of strand (Figs. 22-23a) showing large tube with differentially thickened (banded) wall (arrow) and surrounding smaller-diameter banded tubes. I.9kx. r 132 KARL J. NIKLAS & VASSILIKI SMOCOVITIS
lurian microfossil assemblages, information re TABLE 3. Campa] garding the anatomic relationships between these two cell types is lacking (Pratt et al. 1978; Nonvascular pia Strother and Traverse 1979). Smooth-walled Massanutten tubes have been reported to be crudely aligned Tuscaroraa Clinton" ~ but not attached to one another (Pratt et al. 0; Prototaxites: '-< 1978, p. 131), while banded tubes have been OJ 0,_"'.,, found aggregated into compact clusters of four Large, unbranchi Thick, branching ]~ across and at least two deep (Pratt et al. 1978, U N ematothallus p. 127). No previous study has reported the or N ematoplexus
ganic attachment of dispersed, smooth, and a Reported by Strother an 0' ;; 00 banded tubular cell types. The present report +1 +1 ~ confirms the occasional longitudinal alignment ameter). N emat( o ::: C' of smooth-walled tubes and of tubes with frayed, E 00x x "" x 28 !-tm in diam ~ 00 fibrillar ends. In addition, a single strand of tis ~ ~ ",,0 V") grouped into ir o N N sue recovered from macerations of 122 plant +1 +1 +1 +1 +1 +1 +1 +1 +1 +1 +1 fragments shows the parallel alignment of 1962). Similarly, 00 V) .,, o::tr"')o::t 0("")1-- NOO ...... N f"""') N N f"""') N l"") types (19-50 p.r \D 0\ N smooth and banded tubular elements. This an atomical configuration is not the result of con are oriented par solidation during or after deposition. The basic mens, this taxor tubular construction of the strand has an ana walls (Arnold 19 logue with the tissue organization seen in other walled, profusel Silurian and Devonian plant fossils, that have diameter) in Pr, been described as "nematophytes." The nema around the large tophytes are an artificial group of problematic that the strand taxa consisting of N ematothallus, N ematoplexsmaller fragmenl us, and Prototaxites. The organization of these ence of banded t plants may be grouped into two categories: thick-walled tub against an affini (1) thin-walled, banded tubes intertwining with smooth-walled, smaller tubular cell types (Neit might be argu matothallus and N ematoplexu;); and (2) thin ing the juvenil walled, branched, and septate tubes inter Prototaxites. T twined among thicker-walled, large, and a functional per unbranched tubular elements (Prototaxites). more efficacious Owing to the presence of tubular cell types with The organiza differentially thickened walls, previous studies in the strand als of Llandoverian and Wenlockian microfossil as ducting ti~sues 0 semblages have emphasized Nematothallus and and vascular pI N ematoplexus in drawing morphologic ana tral strand or logues (Pratt et al. 1978; Strother and Traverse metophytes, as 1979). sists of nume surrounding hy U> The fragment of tissue isolated from the Mas o ter. According t '"U> sanutten material has a clearly defined arrange .~ droids are elon 0 ment of aligned, smooth-walled tubes (17 :±: 6.9 S o minal walls, wh' u !-tm in diameter) surrounding a much smaller number of banded tubes (18.8 :±: 2.1 p.m in di hydrolysis. Hy ameter). This organization is unlike either of the at maturity and two categories of nematophytic organization. In eral walls, pits, N ematothallus there is no evidence for the dis Pratt et al. (19 crete parallel alignment of banded (10-50 !-tm to be tapered e in diameter) and smooth tubes (2.5 !-tm in di- and even thou EVOLUTION OF LAND PLANTS 133
es, information re TABLE 3. Comparisons among tubular elements of nonvascular fossil plants. ships between these Diameter (J-Lrn) Distance between bands Cum) (Pratt et al. 1978; Nonv4,;cular plants Smooth N Banded N N 9). Smooth-walled Massanutten 18 ± 3.6 20 22 ± 3.6 20 1.6 ± 2.8 40 be crudely aligned Tuscaroraa 8-12 other (Pratt et al. Clinton" 10 30 d tubes have been Prololaxiles: act clusters of four Large, unbranching tubes 32 ± 6.2 10 Thick, branching tubes 7 ± 2.3 10 1978, p (Pratt et al. N emalolhallus 2.5 10(24)50 4 ± 0.9 4 has reported the or Nemaloplexus 7-10 2( 18)28
rsed, smooth, and a Reported by Strother and Traverse (1979). The present report gitudinal alignment ameter). Nematoplexus has thickened tubes (2 mented, they are clearly elongate. Leptoids are of tubes with frayed, 28 p.m in diameter) occurring individually or single strand of tis elongated, possess thickened lateral walls, and grouped into irregular "branch-knots" (Lyon usually have enlarged tibia-like end walls (He ations of 122 plant 1962). Similarly, although the larger tubular cell allel alignment of bant 1977, figs. 142, 283; 286). Although not types (19-50 p.m in diameter) in Prototaxites elements. This an described by Pratt et al. (1978), the smooth are oriented parallel to the main axis of speci walled tubes seen in our material have tapered, ot the result of con mens, this taxon lacks tubes with banded cell hemispherical end walls, quite unlike the tibia eposition. The basic walls (Arnold 1952, 1954). However, the thick like endings of leptoids (Fig. 24). It is evident, strand has an ana walled, profusely branched tubes (5-10 p.m in therefore, that the strand of tissue and isolated ization seen in other diameter) in Prototaxites do form a "sheath" tubes reported here as well as elsewhere (Pratt nt fossils, that have around the larger tubes. It might be speculated et al. 1978; Strother and Traverse 1979) have phytes." The nema that the strand of tissue described here is a morphologic features unlike the conducting cell roup of problematic smaller fragment of a sheath; however, the pres types of extant bryophytes (Table 5). hallus, Nematoplex ence of banded tubes and the lack of branched, Comparisons have been made between the organization of these thick-walled tubes in our specimen would argue structure of banded tubular cell types found in nto two categories: against an affinity with Prototaxites. Similarly, Lower Silurian strata and cell types found in es intertwining with it might be argued that banded tubes occur dur tracheophytes. This comparison represents a bular cell types (Ne ing the juvenile phase in the development of central theme in controversies over the first ap lexus); and (2) thin Prototaxites. This appears unlikely, since from pearance of the land plants and of tracheo eptate tubes inter a functional perspective banded tubes would be phytes (Banks 1975; Gray and Boucot 1977; ailed, large, and more efficacious in plants of larger size. Schopf 1977; Pratt et al. 1978; Strother and Tra ents (Prototaxites). The organization of smooth and banded tubes verse 1979; Niklas and Pratt 1980). Two factors bular cell types with mitigate the usefulness of drawing comparisons lIs, previous studies in the strand also parallels that seen in the con ducting ti"sues of bryophytes (leptoids-hydroids) ckian microfossil as d Nematothallus and and vascular plants (phloem-xylem). The cen tral strand or hydrom seen in some moss ga g morphologic ana TABLE 4. Comparisons (2-sample I-test) among the surfi metophytes, as well as in sporophyte setae con trother and Traverse cial cellular dimensions of various Paleozoic plants (cf. Ta sists of numerous smooth-walled leptoids, ble 2). For all entries 100 cells were sampled (N = 100, 3.291 < 1 . ",,148 < 3.373). Double entries x (x) refer to surrounding hydroids that are larger in diame 0 05 olated from the Mas comparisons between the small and large cellular dimen arly defined arrange ter. According to Hebant (1977, pp. 53-54), hy sions for each pair. droids are elongated and possess inclined ter aIled tubes (17 ± 6.9 A 3" 4' minal walls, which are usually thin due to partial ing a much smaller hydrolysis. Hydroids lack a living protoplasm A 18.8 ± 2.1 p.m in di- 1 17.8 (14.8) is unlike either of the at maturity and lack differentially thickened lat 2 827 (75.6) 89.1 (74.9) eral walls, pits, or any ornamentation (Table 5). 3 a 45.5 (29.5) 48.2 (29.5) 58.9 (67.1) hytic organization. In a Pratt et al. (1978) have described what appear 4 49.1 (40.2) 44.2 (37.4) 14.5 (45.0) 24.8 evidence for the dis sa 56.6(46.9) 52.6(45.7) 7.28(40.5) 33.1 6.15 to be tapered end walls in their banded tubes, f banded (10-50 J-tm 01 Protosalvinia dimensions are for the small~st cells toward the base of the tubes (2.5 p.m in di and even though these microfossils were frag thallus. 134 KARL J. NIKLAS & VASSILIKI SMOCOVITIS
TABLE 5. Comparisons among Silurian banded tubes, moss hydroids, and tracheids. its relationship Hydroids Banded tubes Tracheids algae. The term 'J. Shape Elongated Elongated Elongated cular in reasonin 2. Protoplasm Protoplasm absent Unknown Protoplasm absent on land") and i: at maturity" at maturity" must define an 3. End walls Thin, hydrolyzed, Tapering to oblique Hydrolyzed, oblique grade. It is evid. oblique of habitat and U 4. Lateral wall ornamenta- Completely lacking Spiral, annular spiral, annular, to tions and pits thickenings lack- scalariform, vari flora can be diva ing pits ety of pits ic affinity. 5. Secondary wall Absent Lateral wall thick- Present The similarit:. enings appear to be internal has lead some to 6. Movement of water Preferentially Unknown Preferentially correspondence through end walls through lateral Boucot 1977). S: and end wall pits functional analoE 7. Biochemistry of walls Polyphenols Polyphenols (lignin-like Lignin one to infer the moiety) ("tracheid-like") a Hebant (1973) has demonstrated that, during degeneration of the hydroid protoplasm, acid phosphatase activity reaches a peak. This paralleles the physiology of tracheid protoplasm decomposition. fore, to infer (ne plants containin to clearly define between our Silurian banded tubes and tra who argue that banded tube cell types do not tubular element cheids. The first is the occurrence of banded provide prima facie evidence for vascular plants. ogy of extant 1= tubes in plants that are clearly not vascular (ne H abitat-function. -Although often related, thickened cells matophytes), suggesting that banded or differ habitat and taxonomic affinity are independent functions: (1) to entially thickened cells may have evolved in a issues. A "land plant" must be considered as a duced by the ra number of potentially unrelated plant groups. grade level of structural and biochemical orga cheids); and (2) The second factor is the variability in the mor nization rather than as a clade of organisms. incurred by the phology of tracheids seen in modern-day tra However, some authors (Gray and Boucot 1977, (elators). It shol cheophytes (Bierhorst 1960). Tracheids conduct pp. 145-146; Taylor 1982, p. 156) conclude that conducting cell water and are found in some gametophytes and the land plants are those autotrophs that cus droids); howevE most sporophytes of vascular plants. They are tomarily live on land and that have relations dealing with Sil elongated, nonliving at maturity, have tapering that "are primarily to other plants living on land" banding. The e' imperforate ends, and possess a variety of pits (Gray and Boucot 1977, p. 145; original italics). appropriate to 1 and differentially thickened cell walls that are From the context, it appears that a clade per types, on the ba lignified. Thus three criteria define a tracheid spective is taken, one that delimits "land plant" the fragmented function, structure, and biochemistry (Table 5). at the level of embryophytes, and excludes ter ment by smootb When collectively present these three criteria restrial green algae. Thus, the land plants are tors and indivic provide an unambiguous identification of a tra apparently defined as monophyletic. Such a def tors seen in ant cheid and hence of a vascular plant. However, inition delimits the land plants on the basis of (50-80 f.Lm; d. : Bierhorst (1960) lists exceptions to every com a reproductive cycle (diplobiontic) and the pres son 1971), and: ponent in the definition of a tracheid. Some tra ence of a structural set of characters (e.g., ar reveal end walls cheids may be functional and mature but lack chegonium). This definition is weak since it re reported for frag a secondary wall with thickenings. Similarly, stricts from consideration the significance of However, the E lignification may be an incidental, secondary terrestrially adapted nonembryophyte ances out, since model modification of a tracheid cell wall. Even within tors, and it requires knowledge of life-history tative of past m an anatomic context, a "deviate" tracheid may details that are unlikely to be recovered from the strand of ai fail to be recognized. the fossil record. The definition of land plant types has the g Based on these two mitigating factors (par given by Gray and Boucot is acceptable when ducting tissue. I allel or convergent evolution, and the often am dealing with extant organisms, for which cla phytes, water-c biguous characteristics of tracheids in modern distic relationships may reasonably be deduced. rounded by cell day plants), and despite the similarities between However, the fact that a plant exploited a land central location banded tubes and tracheids, we agree with those habitat in the past provides no information about types in the Ll EVOLUTION OF LAND PLANTS 135
its relationship with modern embryophytes or consistent, therefore, with cells adapted to water Tracheids algae. The term "land plant" is by necessity cir transport, while surrounding smooth-walled Elongated cular in reasoning ("a land plant is one that lives tubes may have served as analogues to phloem Protoplasm absent on land") and if it is to have any meaning it or leptoid cell types. at maturity· must define an ecologic or niche concept-a Even if the conducting function of tissues Hydrolyzed, oblique grade. It is evident, therefore, that the question composed of banded and smooth cell types is of habitat and the establishment of a land plant accepted (but as yet unproven), a terrestrial spiral, annular, to scalariform, vari flora can be divorced from the issue of taxonom habitat is not an a priori conclusion. Indeter ety of pits ic affinity. minate growth resulting in an elongate growth Present The similarity of banded tubes to tracheids habit places demands on metabolite transport has lead some to argue that there is a functional even in aquatic environments. Large marine Preferentially correspondence between the two (Gray and macrophytes such as Macrocystis, N ereocystis, through lateral Boucot 1977). Since tracheids conduct water, a and Laminaria have medullary cells (e.g., and end wall pits functional analogy with banded tubes would lead "trumpet cells"), albeit unbanded, that are mod Lignin one to infer that Silurian plants with banded ified for conducting metabolites (Ziegler and ("tracheid-like") tubes were terrestrial. There Ruck 1967; Parker 1971a,b; Schmitz and Sri eak. This paralleles the physiology fore, to infer (not prove) a terrestrial habitat for vastava 1974, 1975; Nicholson 1976). Similarly, plants containing banded tubes, it is necessary reports of lignin-like moieties in the organic re to clearly define and prove the function of such mains of Llandoverian plant fossils are not pri be cell types do not tubular elements. On the basis of the morphol ma facie evidence of a terrestrial habitat (contra e for vascular plants. ogy of extant plants, elongated, differentially Gray and Boucot 1977), since a number of ma ough often related, thickened cells have evolved for basically two rine algae are known to synthesize and excrete nity are independent functions: (1) to resist the implosive stresses in plant phenolics that could given similar profiles st be considered as a duced by the rapid internal flow of a fluid (tra when fossilized (Yentsch and Reichert 1962; nd biochemical orga cheids); and (2) to resist the explosive stresses Craigie and McLachlan 1964; Sieburth and Jen clade of organisms. incurred by the compression of internal fluids sen 1969). Finally, Gray and Boucot (1977) have ray and Boucot 1977, (elators). It should be noted that not all water argued that tracheid-like tubes, functioning as p. 156) conclude that conducting cell types possess thickenings (hy water-conducting elements, may even be ex autotrophs that cus droids); however, this is a trivial point when pected in an emergent aquatic (p. 164). Since that have relations dealing with Silurian tube cell types that have these authors make a distinction between a "land plants living on land" banding. The elator analogy would appear in plant" and an "emergent aquatic" we can con . 145; original italics), appropriate to the function of the banded cell clude that, even if a conducting function was ars that a clade per types, on the basis of the latter's length (even in proven for "banded" tubes, the question of hab delimits "land plant" the fragmented condition) and their ensheath itat still remains open to these authors. tes, and excludes ter ment by smooth-walled tubular cell types. Ela Pratt et al. (1978) point out that the strongest , the land plants are tors and individual components of pseudoela evidence for the terrestrial origin of the Mas ophyletic. Such a def tors seen in anthoceropsids are relatively short sanutten plant remains comes from their occur lants on the basis of (50-80 JLm; cf. Smith 1955; Parihar 1962; Wat ence in sediments of fluvial origin. Their inter biontic) and the pres son 1971), and if broken into fragments would pretation of the depositional environment f characters (e.g., ar reveal end walls at a higher frequency than those associated with these fossils is consistent with n is weak since it re- reported for fragments of Silurian banded tubes. the stable isotope (8CI3) analyses reported here n the significance of However, the elator analogy cannot be ruled (Table 1, Fig. 26). Nier and Gulbrandsen (1939) embryophyte ances out, since modern examples may be unrepresen first observed that carbon present in biological wledge of life-history tative of past morphologic diversity. However, systems had a lower 13C value than that found to be recovered from the strand of aligned smooth and banded cell in atmospheric CO2or carbonate minerals. Park finition of land plant types has the general configuration of a con and Epstein (1960) found that ribulose diphos t is acceptable when ducting tissue. In both bryophytes and tracheo phatase fixes 12C02 1.017 times faster than isms, for which cla phytes, water-conducting cell types are sur 13C02. Solution of CO2 in water results in a asonably be deduced. rounded by cell-sap-conducting elements. The preferential concentration of 13C, so land plants plant exploited a land central location of differentially thickened cell are expected to contain less 13C relative to ma s no information about types in the Llandoverian tissue fragment is rine plants and more of the isotopically lighter 136 KARL J. NIKLAS & VASSILIKI SMOCOVITIS
BANKS, AVERAGE MARINE all known "cuticles" that are impermeable to jectur CARBONATES water are also highly impermeable to gases (such BIERHO MARIN E ""I'·.."""'.,-,··+t·~·..,....,..,. :[;1 as oxygen and carbon dioxide) and to potentially Phyto BICARBONATESq RANGE BOWER, ¢:J ATMOSPHERIC toxic secondary metabolites. To accommodate Lond, W/II///(4'/////1!! MAR INE ALGA E C02 gas exchange, plants have increased their sur CHALO~ face area-to-volume ratios by means of pores Non-~ W/I/I/IJ4'i$lA MAR IN E tolog) !:.ld COAL INVERTEBRATES opening into internal chambers, thereby per CRAIGH _LAND PLANTS mitting gas exchange and limiting water loss (by ultra. 23-33 1"'=£'=-"'-'=-.'1 MARl NE PETROLEUM means of boundary larger effects or regulating EISENA' tl=,cJFRESH WATER PETROLEUM pore diameter). The evolution of an endohydric der B I I I I I I I Strati -35 -30 -25 -20 -15 -10 -5 0 5 water and mineral transport system (e.g., hy GRAY, J I3 droids-Ieptoids, xylem-phloem) is generally con -DEPLETION -- 8C _-ENRICHMENT proof sidered to have evolved after plants established GRAY, ~ FIGURE 26. Range and average values (see upper left in a tenuous, terrestrial existence. It would be rea Proto sert) of .sC13·values for various organic and inorganic sources. I3 HEBAN1 Analyses of Massanutten plant compressions indicate a .sC • sonable to conclude, therefore, that plants pos cerosJ value of -25.6 ± a and -26.2 ± 0.15 (cf. Table 1). Al sessing cuticles and conducting cell types would ti~ though these values are consistent with a terrestrial in· ing 1 have evolutionarily preceded the first appear HEBAN1 terpretation (land plant .sC 3 = -25; coal .sC" = -24), ophyt methanogenic bacterial decomposition of brackish or even ance of the vascular plants, perhaps even the marine plant material can deplete .sC13-values. LOWRY, first embryophytes. This conjecture would ap plant.< pear to be verified by the isolation of "cuticle LYON, J like" and "tracheid-like" tissue fragments from refera toplex 12CO Z found in the atmosphere. Marine algae Lower Silurian strata. However, the identifi 65:79 typically yield BC 13 values ranging from -19 to cation of "cuticles" and "tracheids" requires a NICHOL -11, whereas land plants yield values ranging morphological and anatomical context in which Bot. I NIER, !' from -27 to -23. (Coal samples derived from to verify function. It is through function that relatil vascular plant tissues have values of - 26 to habitat is inferred. Until we know the mor 61:69 -24.) Within the context of freshwater organ phology, anatomy, and reproductive biology of NIKLAS procit isms, BC 13 values are less clear-cut, since car the parent organism(s) that gave rise to the tis 1239 bonate sources in these waters may be derived sue fragments described here, speculations on NIKLAS in part from formerly marine carbonate-bearing the first appearance of a land plant flora will plant. M.H: sediments typically yielding -5 to +4 BCI3 val remain as ambiguous in result as they are am Univ_ ues. However, the fact that Silurian material is bitious in goal. NIKLAS 13C deficient strongly favors a terrestrial origin, tosalv Acknowledgment J. BOo since sediment sources of carbonates bias in the NIKLAS opposite (less negative) direction. We wish to thank Drs. Harlan P. Banks (Cor stitue. Evolutionary implications.-Various authors nell University), Francis Hueber (Smithsonian 396·3 NIKLA5; have speculated on the sequence of events lead Institution), and Tom L. Phillips (University of paren ing to the appearance of the first land plants Illinois at Urbana-Champaign) for their com (Niklas 1976; Raven 1977; Niklas et al. 1980; ments on an earlier draft of this paper, and Dr. Stebbins and Hill 1980). A common theme to LisaM. Pratt (U.S.G.S., Denver, Colorado) for many of these scenarios has been the physiologic providing field information and assistance in and morphologic constraints attending the tran collecting. We acknowledge funding of NSF sition from an aquatic to terrestrial habitat. In grant DEB-81-18416 to K.J.N. and a fellowship an aquatic environment, surface area to volume from the Natural Science and Engineering Re ratios can be large to facilitate light gathering, search Council of Canada to V. S. gas exchange, and detoxification. Although these same functions are necessary for survival on Literature Cited land, the need to prevent excessive water loss ARNOLD, C. A. 1952. A specimen of Prototaxites from the Kettle restricts the plant body's surface area to volume Point black shale of Ontario. Palaeontographica 93B :45-46. ARNOLD, C. A. 1954. Microscopic structure and nomenclature of ratio. A common solution to many life forms on Prototaxites. 8th Congr. Int. Bot. Paris, 1954, Proc. Ser. 5:137 land was the evolution of a cuticle. However, 138. EVOLUTION OF LAND PLANTS 137
BANKS, H. P. 1975. Early va.5cular land plants: proof and con K. Hecht, W. C. Steere, and B. Wallace, eds. Evolutionary Bi at are impermeable to jecture. BioScience 25: 730-737. ology. Vol. 12. Plenum, New York. ermeable to gases (such BIERHORST, D. W. 1960. Observations on tracheary elements. PARIHAR, N. S. 1962. Bryophyta. 4th ed. Central Book Depot, xide) and to potentially Phytomorphology 10:249-305. Allahabad. BOWER, F. O. 1908. The Origin of a Land Flora. MacMillan, PARK, R. AND S. EpSTEIN. 1960. Carbon isotope fractionation lites. To accommodate London. during photosynthesis. Geochim. Cosmochim. Acta 21:110-126. ve increased their sur CHALONER, W. G., M. K. MENSAH, AND M. D. CRANE. 1974. PARKER, B. C. 1971a. The internal structure of Macrocystis. Pp. 'os by means of pores Non-vascular land plants from the Devonian of Ghana. Palaeon 99-121. In: W. ]. North, ed. The Biology of Giant Kelp Beds. tology 17:925-948. Beihefte z. Nova Hedw. 32. hambers, thereby per- CRAIGIE, ]. S. AND J. McLACHLAN. 1964. Excretion of coloured PARKER, B. C. 1971b. Studies of translocation in Macyocystis. limiting water loss (by ultraviolet absorbing substances in marine algae. Can. J. Bot. 42: Pp. 191-195. In: W. J. North, ed. The Biology of Giant Kelp er effects or regulating 23-33. Beds. Beihefte z. Nova Hedw. 32. EISENACK, A. 1972. Chitinozoen und andere mikrofossi1ien aus PRATT, L. M., T. L. PHILLIPS, AND J. M. DENNISON. 1978. Evi lution of an endohydric der Bohrung Leba Pommern. Palaeontogr. Abt. A. Palaeozool. dence of non-va.5cular land plants from the early Silurian (Llan sport system (e.g., hy Stratigr. 139A: 1-87. doverian) at Virginia. U.S.A. Rev. Palaeobot. Palynol. 25: 121 hioem) is generally con GRAY, ]. AND A. ]. BOUCOT. 1977. Early vascular land plants: 149. proof and conjecture. Lethaia 10:145-174. RAVEN, J. A. 1977. The evolution of va.5cular land plants in re after plants established GRAY, ]. AND A. ]. BOUCOT. 1979. The Devonian land plant lation to supracellular transport processes. Adv. Bot. Res. 5: 153 stence. It would be rea Pyotosalvinia. Lethaia 12:57-63. 219. refore, that plants pos HEBANT. C. 1973. Acid phosphomonoesterase activities (B-gly SCHMITZ, K. AND L. M. SRIVASTAVA. 1974. Fine structure and cerosphosphata.5e and naphtol AS-MX phosphata.5e) in conduct development of sieve tubes in Laminaria groendandica Rosenv. ucting cell types would ing tissues of bryophytes. Protopla.5ma 77:231-241. Cytobiologie 10:66-87. ceded the first appear HEBANT, C. 1977. The Conducting Tissues of Bryophytes. Bry SCHMITZ, K. AND L. M. SRIVASTAVA. 1975. On the fine structure ants, perhaps even the ophytonium Bibliotheca 10. Cramer, Lehre. of sieve tubes and the physiology of a.5similate transport in Alana LOWRY, B., D. LEE, AND C. HEBANT. 1980. The origin of land mayginata. Can. J. Bot. 53:861-876. s conjecture would ap plants: a new look at an old problem. Taxon 29: 183-197. SCHOPF, J. M. 1978. 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Press, Ames. til we know the mor 61 :697. STEBBINS, G. C. AND G. ]. C. HILL. 1980. Did multicellular reproductive biology of NIKLAS, K.]. 1976. The role of morphological biochemical reci plants invade the land? Amer. Nat. 115:342-353. procity in early land plant evolution. Ann. Bot. (London) 40: STROTHER, P. K. AND A. TRAVERSE. 1979. Plant microfossils at gave rise to the tis 1239-1254. from Llandoverian and Wenlockian rocks of Pennsylvania. Pal d here, speculations on NIKLAS, K. J. 1982. Chemical diversification and evolution of ynology 3: 1-21. a land plant flora will plants a.5 inferred from paleobiochemical stUdies. Pp. 29-91. In: TAYLOR, T. N. 1982. The origin of land plants: a paleobotanical M. H. Nitecki, ed. Biochemical Aspects of Evolutionary Biology. perspective. Taxon 31: 155-177. result as they are am Univ. Chicago Press, Chicago. WATSON, E. V. 1971. The Structure and Life of Bryophytes. 3d NIKLAS, K. ]. AND T. L. PHILLIPS. 1976. Morphology of PyO ed. Hutchinson, London. tosalvinia from the Upper Devonian of Ohio and Kentucky. Amer. YENTSCH, C. S. AND C. A. REICHERT. 1962. The interrelation J. Bot. 63:9-29. ship between water-soluble yellow substances and chloroplastic NIKLAS, K. ]. AND L. PRATT. 1980. Evidence for lignin-like con pigments in marine algae. Bot. Mar. 3:65-74. . Harlan P. Banks (Cor stituents in early Silurian (Llandoverian) plant fossils. Science 209: ZIEGLER, H. AND J. RUCK. 1967. Untersuchungen iiber die Fein is Hueber (Smithsonian 396-397. Struktur des Phloems. III. Die "Trumkpetenzellen" von Lami NIKLAS, K. ]., B. H. TIFFNEY, AND A. H. KNOLL. 1980. Ap nana-Arten. Planta 73:62-73. . Phillips (U niversity of parent changes in the diversity of land plants. Pp. 1-89. In: M. mpaign) for their com t of this paper, and Dr. ., Denver, Colorado) for ation and assistance in ledge funding of NSF K.].N. and a fellowship ce and Engineering Re da to V.S.
en of Pyototaxites from the Kettle alaeontographica 938 :45--46. opic structure and nomenclature of Bot. Paris, 1954, Proc. Ser. 5: 137