Morphology and Homology of the Peristome Teeth in Hymenodon and Hymenodontopsis (Rhizogoniaceae: Musci) Author(S): Jonathan Shaw and Lewis E

Morphology and Homology of the Peristome Teeth in Hymenodon and Hymenodontopsis (Rhizogoniaceae: Musci) Author(s): Jonathan Shaw and Lewis E. Anderson Source: Systematic Botany, Vol. 11, No. 3 (Jul. - Sep., 1986), pp. 446-454 Published by: American Society of Plant Taxonomists Stable URL: http://www.jstor.org/stable/2419081 Accessed: 17/11/2010 11:05

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Morphology and Homology of the Peristome Teeth in Hymenodon and Hymenodontopsis (Rhizogoniaceae: Musci)

JONATHAN SHAW and LEWIS E. ANDERSON Departmentof Botany,Duke University,Durham, North Carolina 27706

ABSTRACT. Hymenodonand Hymenodontopsisare two small genera in the Rhizogoniaceae with single peristomestraditionally thought to be endostomes. Based on cellular patternson the inner and outer surfaces,the peristome of Hymenodontopsisis confirmedas an endostome. The single peristomes of Hymenodonsericeus and H. angustifoliusare, however, exostomes, with peristomial formulaeof 4:2. The formerspecies has a preperistomeformed from the OPL-2. Hymenodonparvulus has a double peristome and this, combined with distinctivegametophytic morphology, indicates that the species is misplaced in Hymenodon.A placement in Powellia(Racopilaceae) is accepted with hesitation.

The Rhizogoniaceae are a medium-sized ratherthan reticulations.Reticulate ornamen- familyof mosses consistingof seven genera and tationoccurs on the teeth in several other mor- about 45 species. Morphological featuresthat phologically similar rhizogoniaceous genera define the familyinclude lateral inflorescences (e.g., RhizogoniumBrid., Mesochaete Lindb., and on rather highly branched plants, sharply GoniobryumLindb.) (Shaw 1985b). In Hymeno- toothed leaves that are often bistratose along don Hook.f. & Wils., with about seven species, the margins,and rounded-hexagonal leaf cells and HymenodontopsisHerz., with two species, generallyhaving thickenedwalls. Most species the peristomeconsists of a single ring of teeth are distributedin the Southern Hemisphere in which have been interpreted as endostomes moist tropical or subtropical forests. (Brotherus1924). Details of peristomestructure constitute the It is not always a simple matterto distinguish mostimportant characters defining the families exostomes and endostomes when one of the and orders of mosses (Dixon 1932). Peristomes two is absent. Shaw and Rohrer (1984) inves- of species classifiedin the Bryales,to which the tigated the problem by studying cellular pat- Rhizogoniaceae traditionallybelong (Brother- terns characterizingthe outer and inner sur- us 1924; Vitt 1982, 1984), are diplolepideous faces of exostomes and endostomes in mosses with a reticulate ornamentationon the outer where the homology of the layers is clear, i.e., surfaces of the exostome teeth (Shaw 1985b). when both rings of teeth are present. Their The peristome is generally double, consisting study was built upon the foundation laid by of well-developed exostome and endostome, Edwards (1979, 1984), who showed that the although in some species and genera one or the number of cells in each of the three concentric other ring of teeth may be reduced or absent. layers giving rise to peristome teeth in a de- The Rhizogoniaceae are rather heterogeneous veloping capsule can be inferredfrom the pat- in peristomestructure compared to other bry- terns of lines on mature peristomes. For ex- alian families in that two of the genera (Pyr- ample, Edwards showed that the single ring of rhobryumMitt. and CryptopodiumBrid.) have haplolepideous peristome teeth are derived cross-striationson the outer exostomial surface fromtwo cells on the outside for every three

FIGS. 1-6 SEM photographsof peristomestructure. 1-2. Hymenodontopsisstresemannii, endostome. 1. Out- er surfacewith the capsule rim visible at the bottom.2. Inner surface. 3-5. Hymenodonsericeus, exostome. 3. Outer surfacewith the capsule rim visible at the bottom.The basal membrane consists of the fused bases of the teeth and a pre-peristome.4. Outer surfaceabout midway up a tooth. 5. Inner surfaceabout midway up a tooth. 6. Hymenodonangustifolius, exostome outer surface; a pre-peristomeis absent. Scale on 1, 2 = 100 ,um;scale on 3, 6 = 40 ,um;scale in 4, 5 = 20 ,um.

446 1986] SHAW & ANDERSON: PERISTOME TEETH 447

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FiGs. 7-8. SEM photographsof the exostomein Hymenodonangustifolius. Outer (7) and inner(8) surfaces aboutmidway up a tooth.Scale = 10 ,um.

cells on the inside. Shaw and Rohrer(1984) are thoughtto have single,endostomial peri- foundthat exostome teeth consist of remnants stomes,the teethare rathermassive and have of fourcells on the outsidefor every two on the superficialappearance of exostomes.In theinside. Endostomes, however, consist of two addition,a preliminarysurvey of peristome cells on the outsidefor every two, four,six, structurein severalspecies reveals significant eight,or 10 cells on theinside. The numberof inter-specificmorphological heterogeneity. cellscontributing wall materialto endostomes Therefore,this study was undertakento clarify on theirinner surfaces varies from two to 10 themorphology of the peristome teeth in three (or veryrarely up to 14-Shaw 1985a) but is speciesof Hymenodonwhich appear to encom- alwaysan even number.Thus, exostomes and pass the variationfound in the genus.In par- endostomescan be distinguishedby theirdif- ticular,our goal was to determinewhether the feringcell patternson theouter and innersur- teethin these species are homologousto the faces.When examiningexostome teeth, they exostomes,or endostomes,of diplolepideous consistof fourcolumns of cell wall remnants peristomes.In addition,one speciesof Hymeno- on theouter surface for every pair of teeth, and dontopsiswas examinedto determinethe ho- thereis thus a median verticalline on each mologyof its singleperistome, which is more toothas well as a verticalline betweeneach delicatethan those of species in Hymenodon.We tooth(visible where the teeth join at thebase). use theterm homology in thesense of the teeth Since thereare only two columnsof cell wall developingfrom the same cell layersas either remnantsfor each pairof endostome segments, an exostomeor endostome. thereis also a medianvertical line on each segment,but there are no linesbetween segments MATERIALS AND METHODS on the outersurface. (In accordancewith ac- The peristomes of three species of Hymeno- ceptedterminology in bryology,processes of donwere investigated:H. angustifoliusLac., H. an exostomeare called teeth,and thoseof an sericeus(Dozy & Molk.) C. M., and H. parvulus endostomeare called segments.)Study of cel- Bartr.Hymenodontopsis stresemannii Herz. was lularpatterns allows one in mostcases to dis- examined as a representativeof that genus. All tinguishexostomes from endostomes when available specimens of these four species in onlyone ringis presentand developmentalin- DUKE, NY, and US were examined by light formationis notavailable. microscopy and representatives were then Althoughtraditionally species of Hymenodon studied with SEM. Only one fruitingspecimen 1986] SHAW & ANDERSON: PERISTOME TEETH 449

each of Hymenodonparvulus (Brass 30348-NY) and Hymenodontopsisstresemannii (Weber & McVean B-31974-US) were available. The fol- lowing additional specimens were studied with SEM: H. sericeus(Fleischer, Musci Frond. Ar- chip. Indici 35-US; Kurz 873-NY) and H. angustifolius(Carr 15604-NY; JacobsB-962-NY). There appeared to be relativelylittle infra-spe- cific variation in peristome morphology in H. sericeusand H. angustifolius. For SEM study, capsules were thoroughly moistened, cut longitudinally, and the distal portions of the capsules placed on glass slides in water with the outer surface of one half up and the inner surface of the other up. After examinationwith a light microscope,the slides were allowed to dry with a weight placed on the cover slip to avoid curling of the peristome teeth. The specimens were then transferredto an aluminumstub, coated with carbonand gold, and examined at 15 kV.

RESULTS The single peristomeof Hymenodontopsisstre- semanniiis hyaline,thin, and very delicate (figs. 1, 2). A basal membraneextends 35-50 ,umhigh fromthe capsule rim and 16 slender teeth extend upward as much as 175-220 ,umfrom the rim. The teeth are 20 ,umor less wide at the base and taper toward theirapices (fig. 1). They are irregular in outline and in length, often with laterallyprojecting appendages (figs.1, 2). These appendages are related in position to the horizontal lines visible on the outer peristomial surface (fig. 1) but are unrelated to lines on the inner surface(fig. 2). On the outersurface, the peristomeis smooth and there is a vertical line running the length of each tooth.Although there are tightlyspaced horizontal lines on the basal membrane(fig. 1), no vertical lines occur between teeth. On the FIGS. 9. Longitudinal section of the peristome in inner surface,there are no verticallines on the Hymenodonsericeus. PPL and OPL = primaryand out- teeth but two lines occur between each pair of er peristomial layers, respectively.The exostome is teeth (fig. 2). This cellular patternis typical of derived fromadjacent walls in the PPL and OPL; the an endostome: there are two columns of cell pre-peristomevisible in figure3 is derived fromthe wall remnants on the outer surface for each OPL-2. Extremelythickened walls of the OPL and PPL below the region where the exostome is formed pair of teeth and four columns on the inside. and shaded. Such thickeningshave not been report- The peristomial formula (Edwards 1979, 1984) ed in the literature.The capsule wall is shaded on is 2:4. the right.Scale = 50 ,um. The peristome of Hymenodonsericeus is less delicate than that of Hymenodontopsis,and the teeth are 240-300 Am high from the capsule rim.The teeth are fused at the base as a contin- 450 SYSTEMATICBOTANY [Volume 11

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43l,, 1986] SHAW & ANDERSON: PERISTOME TEETH 451 uous membrane45-60 gm high (fig. 3). On the The peristomeof H. angustifoliusconsists, like outer surface,the teeth bear coarse, somewhat that of H. sericeus,of a basal membrane and 16 wavy vertical striations(fig. 4). On the inner teeth (fig. 6). The basal membrane extends 25- surface,the striaeare more irregularin pattern 35 ,umfrom the capsule rim and the teeth are although they are as conspicuous and coarse as 190-250 ,umhigh. The teeth are ca. 18-25,um on the outer surface (fig. 5). The basal mem- broad and rather irregularin outline. On the brane bears no ornamentationon the outer sur- outer surface,the basal membraneis smooth or face but gives the appearance of being multi- sparsely papillose (fig. 6) but the teeth bear layered as viewed with SEM (fig. 3). coarse papillae (fig. 7). On the inner surface, There is a vertical zig-zag line on the outer the basal membrane is smooth and the teeth surface of each peristome tooth in H. sericeus are roughened by coarse papillae (fig. 8). (figs.3, 4). In addition, two vertical lines occur The cellular pattern on the peristome of H. between each toothon the basal membrane.On angustifoliusis typically exostomial with verti- the inner surface,there are no verticallines on cal lines on each tooth and between each pair the teeth, and one line occurs between each on the outer surface (fig. 6) and a vertical line pair of teeth (not illustrated). This pattern of between each tooth on the inner surface (not lines on the inner and outer peristomialsurface illustrated).Unlike H. sericeus,there is no pre- is not typical of an endostome or an exostome; peristomeexternal to the teeth in H. angustifo- on the formerthere are no vertical lines be- lius. tween teeth on the outer surface, and in the The peristome of H. parvulusis significantly latterthere is only one. As the basal membrane differentfrom those of the previous species. of the peristomeappears to consistof more than There is a continuous outer ring of wall mate- one layer (fig. 3), a longitudinal section was rial that is only sometimes divided into sepa- made to determine the number of cell layers rate teeth and is extremelyirregular in outline contributingwall material to the basal mem- (fig. 10). The ring extends 50-75 ,umabove the brane. It is evident (fig. 9) that in addition to capsule rim and bears coarse horizontal or the outer and primaryperistomial layers (OPL sometimesvertical or oblique striationson the and PPL, respectively),the OPL-2 extendsabove outer surface (figs. 10, 11). There are vertical the capsule rim and formsa pre-peristomeex- lines on the irregularteeth as well as a vertical ternalto the actual peristometeeth. Because the line between each tooth on the outer surface. OPL-2 consistsof more cells than the OPL, more (The lines between teethare not readily visible than one vertical line is visible between teeth in fig. 10, but when the membrane is split into on the outer peristomialsurface. separateteeth the splitsoccur along these lines.) The patternof lines on the inner and outer On the inner surface,there are 16 verticallines peristomial surface of H. sericeusis consistent which occur between teeth when the mem- with an exostome ratherthan an endostome as brane is divided into separate teeth.On the ba- it is traditionallyinterpreted. Our longitudinal sis of cellular pattern,the outer ring of peristo- sections indicate thatthe teethare formedfrom mial materialappears to be an exostome. cell walls between the PPL and OPL, charac- The inner peristome in H. parvulusis typi- teristicof exostome teeth. The inner peristo- cally endostomial. Vertical lines occur on the mial layer (IPL), which is continuous with the outer surface of each segment, but only hori- outer spore sac of the capsule urn, does not zontal lines occur on the basal membrane be- extend up to the peristomial region and pre- tween segments (fig. 12). The basal membrane sumably breaks down at an earlier develop- is smooth and extends 90-130 ,um above the mental stage. capsule rim.The segmentsare papillose on both

FIGS. 10-15. SEM photographs of peristomestructure in Hymenodonparvulus. 10. Outer surfaceshowing the irregularring of exostome tissue in frontof two long endostome segments. 11. Exostome tooth. 12. Outer surfaceof the endostome. 13. Outer surface of an endostome segment about midway up. 14. Inner surfaceof the endostome. Note the keeled shape of the segments. 15. Inner surfaceof an endostome segment about midway up. Scale on 10, 12, 14 = 50 Am; scale on 11, 13, 15 = 10 Am. 452 SYSTEMATIC BOTANY [Volume 11

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surfacesalthough the papillae are more dense DISCUSSION on the outersurface (fig. 13) than the inner (fig. Each of the four species of Hymenodonand 15). The cellular patternon the inner surfaceis Hymenodontopsishas a distinctive peristome like that of Hymenodontopsisstresemannii, hav- morphology.Hymenodontopsis has a single en- ing no verticallines on the segmentswith two dostomial peristomewhereas in Hymenodonse- vertical lines between the segments (fig. 14). riceusand H. angustifoliusthe single peristome The keeled shape of the segments, typical of is an exostome. A pre-peristomeoccurs in H. endostomes,is visible in figure14. sericeusbut is absent in H. angustifolius.The 1986] SHAW & ANDERSON: PERISTOME TEETH 453 peristome of H. parvulusis actually double al- has a long-excurrentcosta (fig. 18). Species of though the species has been placed in Hymen- Powellia have thick-walled, isodiametric or odon because of a presumed single peristome shortlyoblong leaf cells like those of H. par- (Brotherus 1924). This diversity in peristome vulus (fig. 19). At least one species of Powellia, morphology, added to the diversity already P. involutifoliaMitt., has a border of thinner- recognized in the Rhizogoniaceae, makes the walled, more rectangular cells along the leaf family notably heterogeneous in spite of a margins. Although a border is not present on number of gametophyticcharacters that unite the leaves of the type specimen of H. parvulus, the included genera. Although Brotherus a second specimen (Brass30348) has such a bor- (1924), Crosby (1980), and Vitt (1982, 1984), der, albeit weakly developed. Bartram(1953) among others, include the Rhizogoniaceae in reportedthe presence of flagellateappendages the Bryales, cross-striationson the outer exo- bearing minute brood bodies on the type of H. stomial surface in Pyrrhobryumand Cryptopo- parvulus.However, the type specimen is rather diumare like those found in the Hypnobryales. scrappy and slender and the "flagellate ap- The reticulate ornamentationon the teeth of pendages" may be etiolated stems. The second other rhizogoniaceous genera is, however, in- specimen of H. parvuluslacks these append- distinguishable from the ornamentationtypi- ages. The absence of a leaf border in the type cal of bryalian families.The ornamentationof specimen of H. parvulusmay also be a result of exostome teeth in Hymenodonsericeus and H. the poor condition of the plants. angustifoliusis not like thatof eitherthe Bryales We accept the placement of H. parvulusin the or Hypnobryales. One approach to the enig- Racopilaceae as suggested by Koponen and matic taxonomic position of the Rhizogoni- Norris (pers. comm.), but their argument for aceae was taken by Buck and Vitt (in press), including the species in Powellia seems less who described the Rhizogoniales to accom- convincing. The peristome of H. parvulusis so modate this and several other families. unlike those of otherPowellia species thatit may Unlike other species of Hymenodon,the peri- be necessary,pending a thoroughexamination stome of H. parvulusconsists of both exostome of the Racopilaceae, to describe a new genus and endostome (fig. 16). In addition, the ga- forit. metophytesof H. parvulusare unusual for Hy- WithH. parvulusremoved fromthe Rhizogo- menodonin being highly branched, prostrate, niaceae, the familystill includes considerable and more clearly pleurocarpous (fig. 17). The diversityin peristomestructure: single and en- gametophyticfeatures, combined with a dou- dostomial in Hymenodontopsis,single and ex- ble peristome,indicate that H. parvulusis mis- ostomial in Hymenodon,and double in the re- placed in Hymenodon.Koponen and Norris maining genera. The type of Hymenodon,H. (pers. comm.) recentlycame to the same con- piliferHook.f. & Wils., has a single exostomial clusion and transferredH. parvulusfrom Hy- peristome like those of H. sericeusand H. an- menodonto Powellia (Racopilaceae). They dis- gustifolius.These species should thereforere- cussed several gametophytic characters that main in Hymenodon.The presence of genera relate H. parvulusto the Racopilaceae and sug- with cross-striateexostome teeth and others gested thatof the two genera in thatfamily, H. with reticulate teeth suggest that a thorough parvulusis more similar to Powelliathan to Ra- understandingof the Rhizogoniaceae is impor- copilum.The peristome of H. parvulusis quite tant for the interpretationof phylogenetic re- unlike those found in species of Powellia,how- lationships of diplolepideous mosses. ever, which have long, triangularor lanceolate ACKNOWLEDGMENTS. Support forthis researchwas exostome teeth. there is variation Although provided, in part, by the National Museum of Nat- among the species of Powelliain the degree of uralHistory, Smithsonian Institution. development of the endostome, the presence of long exostome teeth is a uniform feature LITERATURE CITED readily distinguishingH. parvulusfrom Powel- BARTRAM,E. B. 1953. Additional mosses fromnorth- lia. The capsules of H. parvulusare furrowed east New Guinea. Svensk Bot. Tidskr.47:397-401. when dry, also unlike the smooth capsules of BROTHERUS,V. F. 1924. Musci. Pp. 1-478 in Die na- Powellia. In addition, Powellia typically has a turlichenPflanzenfamilien, ed. 2, vol. 10, eds. A. non-excurrentcosta (sometimes shortlyexcur- Engler and K. Prantl. Leipzig: Wilhelm Engel- rentin P. subelimbataZant.) whereas H. parvulus mann. 454 SYSTEMATIC BOTANY [Volume 11

BUCK, W. R. and D. H. VITT. A reclassificationof the ofbryology, ed. R. M. Schuster.Nichinan: Hattori pleurocarpous mosses. Taxon (in press). Botanical Laboratory. CROSBY, M. R. 1980. The diversityand relationships SHAW, J. 1985a. The correlationbetween taxonomy of mosses. Pp. 115-129 in The mossesof North and peristomestructure in the Bryaceae. J. Hat- America,eds. R. J.Taylor and A. E. Leviton. San tori Bot. Lab. 59:79-100. Francisco: PacificDivision AAAS. . 1985b. Exostomial ornamentation in the DIXON, H. N. 1932. Classificationof mosses. Pp. 397- Bryales.J. Hattori Bot. Lab. 59:303-324. 412 in Manual of bryology,ed. F. Verdoorn. The and J. R. ROHRER. 1984. Endostomial archi- Hague: Martinus Nijhoff. tecturein diplolepideous mosses. J. Hattori Bot. EDWARDS, S. R. 1979. Taxonomic implicationsof cell Lab. 57:41-61. wall patterns in haplolepideous moss peri- VITT, D. H. 1982. Bryopsida.Pp. 307-336 in Synopsis stomes. Pp. 317-346 in Bryophytesystematics, eds. and classificationof livingorganisms, vol. 1, ed. S. G. C. S. Clarke and J. G. Duckett. London, New P. Parker. New York: McGraw-Hill. York, Toronto, Sydney, and San Francisco: Aca- . 1984. Classification of the Bryopsida. Pp. demic Press. 696-759 in New manual of bryology,ed. R. M. . 1984. Homologies and inter-relationships Schuster. Nichinan: Hattori Botanical Labora- of moss peristomes.Pp. 658-695 in New manual tory.

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