Structure, Delimitation, Nomenclature and Classification

Received 10 Oct. 2002 Accepted 7 Jul. 2003

http://www.chineseplantscience.com

Structure, Delimitation, Nomenclature and Classification of Stomata

Malvey PRABHAKAR

(Plant Anatomy and Taxonomy Laboratory, Department of Botany, Osmania University, Hyderabad-500 007, India)

Abstract: The paper reviews stomatal types observed in 500 species of angiosperms besides thosedescribed in the literature and deals with the problems of their structure, delimitation, nomenclature andclassification. In view of the varied definitions available in the literature for subsidiaries, stomatal types and,the definition and delimitations being variously interpreted by different workers, a modified definition forthe subsidiaries and stomata is presented. In accordance with the international code of nomenclature forplants, the names of the stomata widely in use are retained (rule of priority). They have been presentlyclassified as pericytic, desmocytic, paracytic, diacytic, anisocytic, anisotricytic, isotricytic, tetracytic,staurocytic, anomocytic, cyclocytic and a good number of varieties under each type are presented. Thesestomatal types are recognised on the basis of their structure rather than its ontogenetic pathways.Key words: classification; definition; plant stomata

The early history of stomatal nomenclature dates backto Prantle (1872; 1881). Subsequently several classificatorysystems have come into existence, which are mostly basedon ontogeny ( Florine, 1931; 1933; Pant, 1965; Payne, 1970;1979), or combination of structure and ontogeny (Paliwal,1969b; Fryns-Claessens and van Cotthem, 1973; Stevensand Martin, 1978). Though several classificatory systemsand review works (Vesque, 1889; Francey, 1936; Metcalfeand Chalk, 1950; Metcalfe, 1961; Stace, 1965; van Cotthem,1970b; Dilcher, 1974; Patel, 1979; Rasmussen, 1981; Kidwai,1981; Inamdar et al., 1986; Baranova, 1987; 1992) have beenpublished, we lack precise definition for subsidiaries andstomatal types.

Francey (1936) recognised eight categories and 34 struc-tural stomatal types based on the number, position andsize of the subsidiaries. Though his classificatory systemwas fairly good but it was not used by subsequent workers.Survey of the literature reveals that the most widely ac-cepted and used stomatal classificatory system based onthe mature stomatal structure is that of Metcalfe and Chalk’s(1950), Metcalfe (1961) and Stace (1965). While using theirclassificatory systems some strictly followed the definitionof the subsidiaries and delimit the stomata, while others donot (Prabhakar and Leelavathi, 1992 ). For example, thoughthe stomata of Lathyrus (Simola, 1968), which may nor-mally be considered as paracytic on the basis of orienta-tion of the two surrounding cells in relation to the guardcells, following strictly the definition of Metcalfe and Chalk(1950), they have been classified under anomocytic bySimola (1968), because of the indistinct nature of the abut-ting cells. However, Stace (1965) has named such stomata

as paracytic. Metcalfe and Chalk (1950) also did not seemconsistent in applying their definition of subsidiariesthroughout their book. For example the stoma representedin Figs.1788, 2220, 3098 (Metcalfe and Chalk, 1950) aresurrounded by two parallel indistinct cells and hence shouldbe assigned to anomocytic stomata sen. str. Metcalfe andChalk (1950). The authors however described them asparacytic stomata. While others classified such stomatahaving four or more abutting cells into paracytic stomata(Paliwal, 1961; Inamdar, 1968; 1970; Fryns-Claessens andvan Cotthem, 1973; Wilkinson, 1979; Kidwai, 1981) and astoma having only two abutting cells/subsidiaries parallelto the guard cells have been designated as hemiparacytic,parallelocytic Eupara-twi-monocyclic, obliparatwi-monocyclic, duplo-para-tetra-bicyclic, para-polycyclic,para-spirocyclic, etc. (Patel, 1979; Wilkinson, 1979). Theclassificatory systems provided subsequent to Metcalfeand Chalk (1950), Metcalfe (1961) and Stace (1965), I do notfeel at all an improvement over the concept of Metcalfe andChalk (1950). In these new classifications several new termswhich the authors themselves were not able to use them instrict sense in their subsequent publication for describingthe stomata have been introduced.

The draw back of all these classificatory systems in-cluding that of Metcalfe and Chalk (1950 ) mainly lies in thedefinitions of subsidiaries and partly the definitions of sto-matal types. Further several researcher have provided dif-ferent definitions for a single type of stomata. Some of thesedefinitions for paracytic stomata are listed below:

Vesque (1889): “Stomata with two subsidiary cells par-allel to the long axis of the pore-Rubiaceous” (*Figs.1-10).

Acta Botanica Sinica植 物 学 报 2004, 46 (2): 242-252

Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata 243

Solereder (1908): “The pair of the guard cells are accom-panied on either sides (i.e. to the right and left) by one ormore subsidiary cells, which are placed parallel to the pore-Rubiaceous type” (*Figs.1-5, 7, 9, 10, 13 -16).

Francey (1936): Stoma surrounded by two parallely ori-ented cells which may be equal or unequal, designated astypes 3 and 4 respectively (*Figs.1-3, 11, 12 ).

Metcalfe and Chalk (1950): “Stoma accompanied on ei-ther sides by one or more subsidiary cells (cells distinctfrom other epidermal cells) parallel to the long axis of thepore and guard cells-Paracytic type” (*Figs.1-5, 7, 9, 10,13-16).

Stace (1965): “Stoma with two subsidiary cells lying par-allel to the guard cells-Paracytic” (Figs.1-10).

*, figures cited here fit into the definition given by the respective authors.

Figs. 1-62. 1-24. Diagrammatic representation of the so called paracytic stomata. 25-36. Stomata surrounded by distinct or indistinctsubsidiaries. 25, 26. Stomata with distinct subsidiaries. 27, 28. Stomata with indistinct subsidiaries. 29-33. Subsidiaries dicyclic. 34, 35.Stomata with distinct crystalliferous subsidiaries. 36. Stomata with one distinct and the other indistinct subsidiary. 37-62. Pericyticstomata. 37, 38. Stomata with distinct or indistinct subsidiary. 39, 40. Subsidiary transversly oriented to guard cells. 41, 42. Subsidiaryparallel to guard cells. 43, 44. Subsidiary oblique to guard cells. 45-51. Subsidiaries 1 1/2 cyclic. 52-59. Subsidiaries dicyclic. 60-62.Subsidiaries tricyclic.

Acta Botanica Sinica 植物学报 Vol.46 No.2 2004244

Cronquist (1968): “Stoma with two equal subsidiary cellsflanking the guard cells-Paracytic stomata” (*Fig.1).

Fahn (1969): “Each guard cell is accompanied by one ormore subsidiary cells, the longitudinal axis of which areparallel to that of the guard cells and aperture-Rubiaceousor Paracytic type” (*Figs.1-5, 7, 9, 10, 13-16).

Paliwal (1969a): “Two or more subsidiary cells flank thestomata parallel with long axis of the guard cells-Paracyticstomata” (*Figs.1-5, 13, 14, 16 ).

Rajagopal (1973): “Abutting subsidiaries two, parallelto the guard cells, distinct or indistinct, with or withoutconjoint walls towards one or both poles-a Diacytic type”(*Figs.1-5, 7, 9-12, 15, 18-21 ).

Note: When the two subsidiaries are without conjointwalls towards one or both poles of the guard cells, it isbound to leave a space which will be abutted by one ormore cells as also illustrated by the same author (Figs.18-21).

Dilcher (1974): “One or two cells adjacent to the guardcells with their long axis parallel to the long axis of theguard cells-Paracytic type” (*Figs.1-4, 7, 9-12, 15, 17-22).

Cutter (1978): “One or more (often two) subsidiary cellsare present, with their long axis parallel to the guard cells-Paracytic” (*Figs.1-10, 13-17).

Esau (1979): “One or more subsidiary cells border thestoma parallel with the long axis of the guard cells- Paracytictype” (*Figs.1-10, 13-17 ).

Wilkinson (1979): “Stoma accompanied on either sideby one or more subsidiary cells parallel to the long axis ofthe pore and guard cells. The subsidiaries may or may notmeet over the poles and may or may not laterally elongate-Paracytic type” (*Figs.1-5, 7, 9, 10, 13-16, 19, 20, 23, 24).

Following strictly the above definitions the stomata rep-resented in Figs.1-24 can be accommodated under the socalled paracytic ones.

A New Classification and Modified DefinitionsIt is clear from the above introduction that the defini-

tions provided by various workers for different stomataltypes, are ambiguous. In order to remove the ambiguity theauthor felt the necessity to redefine the subsidiaries andstomatal types which is presented below based on his ob-servations on more than 500 species of angiosperms (fordetails of the species c.f. Anna Mani & Prabhakar, 1991a;1991b; 1993; 1994a; 1994b; 1995; Anna Mani et al., 1993;Bhatia et al., 1986; 1988; Ferzana et al., 1991; 1994a; 1994b;Jelani and Prabhakar, 1991; 1992; 1993; Jelani et al., 1990;1991; 1993; Koteswar Rao et al., 1988; Leelavathi andRamayya, 1975; Leelavathi et al., 1980; 1981; 1984a; 1984b;

1985; 1988a; 1988b; Padma Rao et al., 1988; Prabhakar andAnna Mani, 1995; 1996; Prabhakar and Leelavathi, 1989;1991;1992; Prabhakar and Ramayya, 1975; 1979; Prabhakaret al., 1984; 1985;1986; 1988a; 1988b; 1988c; 1990; Ramayyaand Prabhakar, 1973; 1975; Ramayya et al., 1983; Rao et al.,1991; 1992a; 1992b; 1992c, 1993a; 1995; Verma et al., 1989;1991; 1992; Vijay Kumar et al., 1986) and also the informa-tion available in the literature.

Stomatal pore: An opening in the epidermis surroundedby a pair or more guard cells.

Stoma: Stomatal pore and a pair of guard cells.Stomatal complex: Stoma surrounded by subsidiaries

(stomatal types).Subsidiary cells*: Cells surrounding a pair of guard cells

in one (Fig. 25) or more cycles (Fig.26); subsidiaries of thecycle abutting on stoma may (Figs.25, 26, 34-36) or maynot be distinct from the adjacent epidermal cells ( Figs. 27,28 ), but of the other cycle(s) when present are morphologi-cally distinct (Fig. 26). The subsidiaries of the outer cyclemay (Fig. 26) or may not coincide with those of the abuttingcycle in number, arrangement and orientation, etc. (Figs.29-33). The term subsidiary is restricted to mature stomataonly. The subsidiaries of the abutting as well as other cycle(s) may be perigynous or mesogenous in origin and can bereferred as perigene and mesogen cells (while describingthe ontogeny) depending upon their origin. A subsidiaryderived from stomatal meristemoid need not be distinct atmaturity from other epidermal cells. Similarly a subsidiarynot derived from stomatal meristemoid ( i.e. perigene ) maybe distinct from other epidermal cells or other subsidiarycells.

Pericytic stomata: Stoma (pair of guard cells) surrounded

*, cells abutting the stoma has been designated as subsidiaries/auxillarycells when they are distinct from other epidermal cells and as an-nexes/surrounding cells/accessory cells/contact cells/ordinary cellswhen they are indistinct (Francey, 1936; Eames and Mc Daniels,1947; Metcalfe and Chalk, 1950; Mc Lean and Cook, 1951; Fryns-Claessens and van Cotthem, 1973; Tomlinson, 1974; Patel, 1978;Cutter, 1978; Rasmussen, 1981). However the criteria to judge thedistinctness has been mostly left to the subjective judgement. Inretrospect the criteria used for distinctness by various workers aremorphological (shape, size, anticlinal walls and surface), cytological(density of cytoplasm, size of the nucleus, presence or absence ofplastids and ergastic substances) (Figs.34-36), number, position,orientation, physiological and ontogenetical (Patel, 1978; Stevensand Martin, 1978). Tracing cytological, physiological andontogenetical characters in the herbarium and fossil materials isimpracticable. All the cells abutting the guard cells are distinct fromthe other epidermal cells by virtue of their position (i.e. abuttingnature to the guard cells) hence prefer to call them subsidiaries.

Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata 245

Figs. 63-122. 63-90. Desmocytic stomata. 63. Stomata with distinct subsidiary. 64. Stomata with indistinct subsidiary. 65, 66.Subsidiary transversely oriented to guard cells. 67, 68. Subsidiary parallelly oriented to guard cells. 69, 70. Subsidiary obliquely orientedto guard cells. 71-78. Subsidiaries 1 1/2 cyclic. 79-89. Subsidiaries dicyclic. 90. Subsidiaries tricyclic. 91-122. Paracytic stomata. 91.Stomata with distinct subsidiaries. 92. Stomata with indistinct subsidiaries. 93-96. Subsidiaries parallel to the guard cells. 97-101.Subsidiaries transverse to guard cells. 102-103. Subsidiaries oblique to guard cells. 104-112. Subsidiaries 1 1/2 cyclic. 113-120.Subsidiaries dicyclic. 121. Subsidiaries hemitricyclic. 122. Subsidiaries tricyclic.

by a single distinct or indistinct subsidiary cell (Figs. 37-44). The subsidiary cell may be variously oriented to theguard cell and may be monocyclic ( Figs.37-44 ), 11/2 cy-clic ( Figs.45-51 ), di-, tri- to polycyclic ( Figs. 52-62 ).

Synonyms: Adetostomy, amphipericytic, co-pericytic,

coperi-desmo-twi-bicyclic, coperi-polohemibicyclic, copolo-peri-hemibicyclic, duplopericytic, double floating,duploperi-twi-bicyclic, floting, pericytic, pyrosia type, peri-haplo-monocyclic, Ringzellen-type, stomata libera,unizyklisch (Prantle, 1881; Maroti, 1961; Mickel, 1962;

Acta Botanica Sinica 植物学报 Vol.46 No.2 2004246

Mickel and Lersten, 1967; van Cotthem, 1970a, 1970b;Probst, 1971; Dilcher, 1974; Patel, 1979).

Desmocytic: A stoma completely surrounded by a singledistinct or indistinct cell with a conjoint wall. The subsid-iary cell may be variously oriented to the guard cells andthe conjoint wall may be variable in position. The subsid-iaries may be monocyclic ( Figs.63-70 ), 1 1/2 cyclic, di-, tri-to polycyclic (Figs.71-90).

Synonyms: Codesmoperi-twi-bicyclic, codesmo-polo-hemibicyclic, copolo-desmo-hemibicyclic, desmocytic,desmo-haplo-monocyclic, duplodesmo-twi-bicyclic, hang-ing or suspended stomates, stomata suspensa (Mickel andLersten, 1967; van Cotthem, 1970a; 1970b; Dilcher, 1974;Patel, 1979; Prantle, 1881) or indistinct (Figs. 91-96 ), equalor unequal (Figs. 91-96 ), parallel (Figs. 91-96 ), transverse(Figs. 97-101 ) or obliquely oriented (Figs. 102,103 ) to theguard cells, but their conjoint walls are towards the polesof the guard cells. The subsidiaries may be mono- to poly-cyclic (Figs. 91-122 ).

Note: Francey (1936) recognised two types of stomataunder this category based on the size of subsidiaries. Type1 is represented by more or less equal sized subsidiaries(Figs.91, 92). Type 2 by unequal sized subsidiaries (Figs.91,92). These can be now recognised as varieties under thetype paracytic only. Similarly the stoma having distinct orindistinct subsidiaries, parallel oblique or transversely ori-ented subsidiaries can be recognized into different varieties.

Synonyms: Allelocytic, amphiparacytic, bicycticparacytic, duplo-para-tetra-bicyclic, eupara-twimonocyclic,laterocytic oblipara-twimonocyclic, paracytic, parallelocytic,para-polycyclic, paraspirocyclic, rubiaceous (Vesque, 1889;Metcalfe and Chalk, 1950; Payne, 1970; Guyot, 1971; Dilcher,1974; Hortog and Bass, 1978; Patel, 1979).

Diacytic stomata: A stoma completely surrounding byonly two distinct or indistinct subsidiaries (Figs.123, 124),equal or unequal (Figs.123-126), parallel (Figs. 127, 128),transverse (Figs. 129, 130) or obliquely oriented (Figs. 131,132 ) to the guard cells, but the conjoint wall of the abuttingsubsidiaries are lateral to the guard cells. The subsidiariesmay be monocyclic to polycyclic ( Figs. 123-147 ).

Note: Francey (1936) recognised two types of stomataunder this category also, based on equal ( Figs. 123, 124 ) orunequal sized subsidiaries (Figs.125, 126). These can berecognised as varieties under the diacytic stomata only.Similarly a stoma having distinct or indistinct subsidiaries,transversely, obliquely or parallelly oriented subsidiariescan be recognised into different varieties.

Synonyms: Amphidiacytic, axillocytic, bicyclic diacytic,caryophyllaceous, coaxilocytic, coparirtocytic, copolocytic,

diacytic, diallelocytic, diapolocyclic, diapolycyclic, dia-spirocyclic, diatwi-monocyclic, duplodia-tetra-bicyclic,labiateous, oblidia-monocyclic, perietocytic, polocytic,polohaplo-acyclic, polycytic, pteris type, stomata applicata,stomata adnata (Prantle, 1881; Vesque, 1889; Giesenhagen,1901; Metcalfe and Chalk, 1950; Payne, 1970; van Cotthem,1970a; 1970b; Guyot, 1971; Probst, 1971; Dilcher, 1974; Patel,1979).

Anisocytic stomata: A stoma completely is surroundedby only three subsidiaries, variable in position and shape,but one of the subsidiary is distinctly small (Figs.148-156).The subsidiaries may be mono- to polycyclic (Figs.148-164).

Synonyms: Amphianisocytic, anisocytic, aniso-tri-monocyclic, axillocytic, coaxillocytic, cruciferous,helicocytic, helico-spirocyclic obli-haplo-acyclic (Vesque,1889; Metcalfe and Chalk, 1950; Payne, 1970; Dilcher, 1974;Patel, 1979).

Anisotricytic stomata: A stoma completely surroundedby only three subsidiaries, variable in position and shape,but one of the subsidiary is distinctly large. The subsidiar-ies may be mono- to polycyclic (Figs.165-170).

Synonyms: Anisocytic, anomocytic, helicocytic,diacytic ( Metcalfe and Chalk, 1950; Stace, 1965; Wilkinson,1979 ).

Isotricytic stomata: A stoma completely surrounded byonly three subsideries, variable in position and shape,butthe three subsidiaries are more or less of equal size. Thesubsidiaries may be mono- to polycyclic ( Figs.171-174 ).

Synonyms: Anomocytic (Metclafe and Chalk, 1950;Stace, 1965).

Note: Francey (1936) recognised seven types under theabove three categories (i.e. stoma surrounded by threecells), based on the size and position of the subsidiarycells. The definitions of some of these types and figuresrepresented are overlapping. Hence presently they are di-vided into three categories of stomata which are structur-ally distinct from one another, i.e. anisocytic, isotricyticand anisotricytic. Under each of these categories a goodnumber of varieties can be recognised based on the shape,size, structure of inner and outer cycles of the subsidiaries.

Tetracytic stomata: Stomata completely surrounded byonly four subsidiaries, of variable size and shape, of whichtwo are polar and two lateral in position. The subsidiariesmay be mono- to polycyclic (Figs.175-186).

Synonyms: Anphibrachiparatetracytic, amphiparatetra-cytic, angiopteris type, bicytic paracytic, brachyparahexacy-tic, brachyparatetracytic, cyclocytic, duplo-para-tetra-acyclic, grass type, hemidiahaplo-acyclic, hemiparacytic,

Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata 247

hemipara-haplo-acyclic, hexacytic, hexa-a-hemibicyclic,hexa-bhemibicyclic, obli-tri-acyclic, obli-twi-acyclic-tetracytic, palm type, paracytic, parahexacytic,paratetracytic, para-twi-acyclic, quadricytic, rubaceous,staurocytic, stomata quadricellulaires, tetra cyclocytic,tetracytic, tetramonocyclic, tricyclic (Vesque, 1889; Metcalfeand Chalk, 1950; Maroti, 1958; Prat, 1960; Metcalfe, 1961;

Stace, 1965; van Cotthem, 1970b; Guyot, 1971; Dilcher, 1974;Tomlinson, 1974; Patel, 1979; Wilkinson, 1979).

Staurocytic stomata: Stoma completely surrounded byonly four subsidiaries, variable in shape and size but two oftheir conjoint walls polar, while the other two are lateral toguard cells. The subsidiaries may be mono to polycyclic(Figs.187-194 ).

Figs. 123-174. 123-147. Diacytic stomata. 123, 124. Stomata with distinct and indistinct subsidiaries respectively. 125, 126. Stomatawith unequal subsidiaries. 127, 128. Subsidiaries parallel to guard cells. 129, 130. Subsidiaries transverse to guard cells. 131, 132.Subsidiaries oblique to guard cells. 133, 134, 140-142, 145, 146. Subsidiaries 1 1/2 cyclic. 135-139, 143, 144, 147. Subsidiaries dicyclic.148-164. Anisocytic stomata. 148. Stomata with indistinct subsidiaries. 149, 150. Stomata with distinct subsidiaries. 151-156. Stomatawith one or two distinct subsidiaries. 157. Subsidiaries 1 1/2 cyclic. 158-164. Subsidiaries dicyclic. 165-170. Anisotricytic stomata.165. Stomata with indistinct subsidiaries. 166, 167. Stomata with distinct subsidiaries. 168, 169. Stomata with one or two distinctsubsidiaries. 170. Subsidiaries 1 1/2 cyclic. 171-174. Isotricytic stomata. 171, 172. Stomata with indistinct and distinct subsidiariesrespectively. 173, 174. Stomata with one or two distinct subsidiaries.

Acta Botanica Sinica 植物学报 Vol.46 No.2 2004248

Synonyms: Type 15, stauro-cyclocytic, staurocytic,stauro-tetra-monocylic (Francey, 1936; van Cotthem, 1970a;1970b; Dilcher, 1974; Patel, 1979; Wilkinson, 1979 ).

Anomocytic stomata: Stoma surrounded by four or moresubsidiaries, variable in position, shape and size ( otherthan tetracytic and staurocytic types; Figs.195-206 ).

Synonyms: Actinocytic, amphibrachyparacytic,anomocytic-polycytic, brachyparacytic, hemiparacytic,latero-twi-acyclic, oblitwi-acyclic, paracytic, stephanocytic,termino-twi-acyclic (Dilcher, 1974; Patel, 1979; Wilkinson,1979; Baranova, 1987).

Cyclocytic stomata: Stoma is surrounded by four or moresubsidiaries, variable in position, shape and size but ar-ranged in a narrow ring ( Figs.207-212 ).

Note: A desmocytic (Fig. 37), pericytic (Fig. 63), paracytic(Fig. 91), diacytic (Fig.123 ), anisocytic (Fig. 149 ), isotricytic(Fig.172 ), anisotricytic ( Fig.167 ), staurocytic ( Fig.187)and tetracytic stoma (Fig.175), having one to four subsid-iaries arranged in a narrow ring are not included undercyclocytic stomata.

Synonyms: Amphicyclocytic, angiopteris type,cyclocytic, cyclo-multi-monocyclic, encyclocytic, hexa-monocytic, multi-bicyclic, multi-polycyclic, polycytic(Shtromberg, 1956; Stace, 1965; Probst, 1971; Dilcher, 1974;Patel, 1979).

Actinocytic, stephanocytic, actino-multi-monocyclic: Ifeel that identification of actinocytic stomata ( so also withother types like stephanocytic ) is a difficult problem

Figs. 175-212. 175-186. Tetracytic stomata. 175, 176. Stomata with distinct or indistinct subsidiaries respectively. 177-181.Stomata with one to three distinct subsidiaries. 182, 183. Subsidiaries 1 1/2 cyclic. 184-186. Subsidiaries dicyclic, hemitricyclic andtricyclic respectively. 187-194. Staurocytic stomata. 187, 188. Stomata with distinct and indistinct subsidiaries respectively. 189-191.Stomata with one to three small subsidiary cells. 192-194. Stomata with one to three large subsidiary cells. 195-206. Anomocyticstomata. 195, 196, 202, 203. Stomata with one, three or more radiating subsidiaries. 197, 199. Stomata with one distinct parallelsubsidiary. 200. Stomata with two distinct parallel subsidiaries. 201. Subsidiaries hemidicyclic. 204. Subsidiaries parallel to guard cells.205. Subsidiaries transverse to guard cells. 206. Some subsidiaries parallel to guard cells while other radiating. 207-212. Cyclocyticstomata. 207-211. Subsidiaries monocyclic. 212. Subsidiaries dicyclic.

Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata 249

because in a number of angiosperms taxa I have come acrossstomata in which some of the subsidiaries are arranged in aradiating fashion while others are otherwise (Figs.195,196,202-206). Further in a number of publications the stomatawith radiating subsidiaries are also described as anomocyticstomata. For example, Fig. 10.3a represented by Wilkinson(1979) is more like an actinocytic stomata by definition buthas designated as anomocytic stomata, and Fig.6a byBaranova (1987) is an anomocytic type but has been de-scribed as stephanocytic one. In order to avoid these con-fusions the present author prefer to categorise them asanomocytic stomata only and do not recognise actinocytic,stephanocytic stomata, etc.

Cycles: Depending upon the cycles of subsidiaries thestoma may be described as monocyclic (Figs.53, 54, 63, 64),1 1/2 cyclic ( hemidicyclic; Fig.77), dicyclic (Figs.55, 78 -83), hemitricyclic (Figs.185), tricyclic and so on. However,the above definitions of stomata are not applicable to theabnormal stomata viz., stoma having more (Fig.87) or lessthan a pair of guard cells (Fig.88), abutting stoma (Figs.89,90), etc.

References:

Anna M B, Prabhakar M. 1991a. Foliar architecture of some

medicinal plants (Celastrales). Asian J Pl Sci, 3:17-21.

Anna M B, Prabhakar M. 1991b. Foliar architecture in flora of

Visakhapatnam. 1. Magnoliales. Indian J For, 14:131-137.

Anna M B, Prabhakar M. 1993. Foliar architecture of some me-

dicinal plants of Visakhapatnam (Rubiales). Biome, 6(2):65-

72.

Anna M B, Prabhakar M. 1994a. Foliar architecture of some

medicinal plants (Myrtales). Biol Sci Res Bull, 10:9-16.

Anna M B, Prabhakar M. 1994b. Foliar architecture of some

medicinal plants in Ficoidales. Chin J Bot, 6:19-22.

Anna M B, Prabhakar M. 1995. Foliar architecture of passiflorales

occurring at Visakhapatnam. Geophytology, 24:147-154.

Anna M B, Prabhakar M. 1996. Foliar architecture of Asterales.

Khan I A. Frontiers in Plant Science. Hyderabad, India:

Anwarul Uloom Education Society Publ. 1037-1043.

Anna M B, Prabhakar M, Ferzana J. 1993. Foliar architecture of

some medicinal plants (Verbenaceae). J Sci Res Pl Med, 13:8-

16.

Baranova M. 1987. Historical development of the present classi-

fication of morphological types of stomata. Bot Rev, 53:53-

79.

Baranova M. 1992. Principles of comparative stomatographic

studies of flowering plants. Bot Rev, 58:49-99.

Bhatia R Y P, Prabhakar M, Verma H K. 1986. Forensic studies

of poisonous and medicinal plants-Ⅱ Calatropis gigantia R.

Br. (Asclepiadaceae). J Indian Acad For Sci, 25:15-22.

Bhatia R Y P, Prabhakar M, Rao T S. 1988. Dermotype studies

on different cultivars of Beedi tobacco in relation to forensic

science. J Indian Acad For Sci, 26:1-11.

Cronquist A. 1968. The evolution and classification of flowering

plants. Steere W C, Glass H B. London: Thomos Nelson and

Sons Ltd.

Cutter G. 1978. Plant Anatomy Part Ⅰ. London: Edward Arnold.

Dilcher D L. 1974. Approaches to the identification of angiosperm

leaf remains. Bot Rev, 40:1-157.

Eames A J, Mc Daniels L H. 1947. An Introduction to Plant

Anatomy. London: McGraw-Hill Book Co.

Esau K. 1979. Anatomy of Seed Plants. New Dehli, India: Wiley

Eastern Ltd.

Fahn A. 1969. Plant Anatomy. New York: Pergamon Press.

Ferzana J, Prabhaka M, Leelavathi P. 1991. Foliar architecture in

relation to taxonomy of Malvales. Asian J Pl Sci, 3(2):17-53.

Ferzana J, Prabhakar M, Leelavathi P. 1994a. Structure, distribu-

tion and taxonomic significance of crystalliferous cells in

Malvales. J Indian Bot Soc, 73:89-94.

Ferzana J, Prabhakar M, Leelavathi P. 1994b. Pharmacognostic

studies on foliar drugs (Malvaceae). J Sci Res Pl Med, 14,15:

31-52.

Florine R. 1931. Untersuchungen Zur stammesgeschichte der

coniferales and corditates. Svensk K Veternskaps Handl Ⅲ,

10(1):1-588.

Florine R. 1933. Studien Uber die cyacadales des mesozoikums.

Svenska K Vetensk Akad Handl, 12:134.

Francey P. 1936. Etude de L’appareil stomatique chez les,

dictoyledones dans Un but taxinomique. Bull Soc Vaud Sci

Nat, 59:1-12.

Fryns-Claessens E, van Cotthem W. 1973. A new classification

of the ontogenetic types of stomata. Bot Rev, 39:71-138.

Giesenhagen K. 1901. Die Farngattung Niphobolus. Jena.

Guyot. 1971. Phylogenetic and systematic value of stomata in

the umbillifereae. Heywood V H. The Biology and Chemistry

of Umbelliferae. London: Academic Press. 199-214.

Hortog R M, Bass P. 1978. Epidermal characters of the

Celastraceae sensu lato. Acta Bot Neerl, 27:355-388.

Inamdar J A. 1968. Epidermal structure and ontogeny of stomata

in some Nyctaginaceae. Flora, 158:159-166.

Inamdar J A. 1970. Epidermal structure and development of sto-

mata in some Polygonaceae. Proc Indian Acad Sci, LXXⅡ:

Acta Botanica Sinica 植物学报 Vol.46 No.2 2004250

91-98.

Inamdar J A, Mohan J S S, Subramanian R B. 1986. Stomatal

classification — a review. Feddes Report, 97(3, 4):147-160.

Jelani S, Leelavathi P, Prabhakar M. 1990. Foliar epidermis in

relation to taxonomy of Cleome (Capparaceae). Asian J Pl Sci,

2(2):13-24.

Jelani S, Leelavathi P, Prabhakar M. 1991. The morphological,

anatomical, histochemical study of leaf Ocimum sanctum Linn

(Lamiaceae). J Sci Res Pl Med, 12:24-30.

Jelani S, Leelavathi P, Prabhakar M, Ferzana J. 1993. Pharmacog-

nostic studies on Centella asiatica (L.). Urban Ans Sci Life,

12:439-450.

Jelani S, Prabhakar M. 1991. Pharmacognostic studies of leaf of

Hyptis suaveolens L. Ans Sci Life, 11(1, 2):31-37.

Jelani S, Prabhakar M. 1992. Pharmacognostic studies on leaf of

Ocimum basilicum Benth (Lamiaceae). Biol Sci Res Bull, 8(1,

2):65-72.

Jelani S, Prabhakar M. 1993. Pharmacognostic study on leaf of

Salvia officindalis L. J Sci Res Plants Med, 13:31-38.

Kidwai P. 1981. An illustrated glossary of technical terms used in

stomatal studies. Dehra Dun, India: Bishen Singh Mahendra

Pal Singh Publication.

Koteshwar R K, Prabhakar M, Vijay kumar B K, Ramayya N.

1988. Lithocysts and their taxonomic significance in Ficus L.

subgenus Urostigma. Indian J Bot, 11:139-144.

Leelavathi P, Prabhakar M, Ramayya N. 1984a. Structure,

distribution, ontogeny and taxonomic significance of

crystalliferous cells in Leguminosae. Indian J Bot, 7:125-131.

Leelavathi P, Prabhakar M, Ramayya N. 1984b. Structure and

ontogeny of Capitate hairs in Mimosa L. Geobios New Rep, 3

(2):183-185.

Leelavathi P, Prabhakar M, Ramayya N. 1985. Cavitated tri-

chomes in Caesalpinioideae (Leguminosae). Iselya, 2:113-119.

Leelavathi P, Prabhakar M, Ramayya N. 1988a. Pharmacognos-

tic studies on the leaf of Acalypha indica L. Indian J Bot, 11:

129-138.

Leelavathi P, Ramayya N. 1975. Rapid isolation of leaf epidermis

by double-treatment method. Geobios, 2:117-119.

Leelavathi P, Ramayya N, Prabhakar M. 1980. Foliar stomatal

distribution patterns in the Leguminosae and their taxonomic

significance. Phytomorphology, 30 (2, 3):195-204.

Leelavathi P, Ramayya N, Prabhakar M. 1981. Study of the leaf

costal cell distribution patterns and their taxonomic signifi-

cance in Legumionosae. Geophytology, 11:125-132.

Leelavathi P, Veerabhadra Rao A, Prabhakar M, Vijay Kumar B

K. 1988b. Structure, distribution and ontogeny of cylindrical

hair in Leguminsoae. J Swamy Bot Cl, 5(1):23-33.

Maroti I. 1958. Untersuchung der Epidermis von Pteropsida-

Blatt mit besonderer Rucksicht auf die einheimischen Arten.

Acta Biol (Szeged), Ⅳ (3, 4):175-163.

Maroti I. 1961. Untersuching der Entwicklung der Epidermis des

Psilotinae und des Filicinae-Blattes und der Entwicklung der

Stomas. Acta Biol (Szeged), Ⅶ (3, 4):43-67.

McLean R C, Cook W R I. 1951. Text Book of Theoritical Botany

Vol. 1. N. York, London: University of Toronto Press.

Metcalfe C R. 1961. The anatomical approach to systematics:

general introduction with special reference to recent work on

monocatyledons. Rec Adv Bot, 1:146-150.

Metcalfe C R, Chalk L. 1950. Anatomy of Dicotyledons, Vols. Ⅰ

and Ⅱ. Oxford: Clarendon Press.

Mickel J T. 1962. A monographic study of the fern genus Anemia,

subgenus Captophyllum. Iow State J Sci, 36:349-482.

Mickel J T, Lersten N R. 1967. Floating stomates (adetostomy)

in ferns: distribution and ontogeny. Am J Bot, 54:1181-1185.

Padma R P, Prabhakar M, Ramayya N. 1988. Trichome distribu-

tional patterns and their taxonomic significance in

Clerodendrum L. J Swamy Bot Cl, 5(2):59-63.

Paliwal G S. 1961. The development of stomata in Linum

usitatissium L. Curr Sci, 30:269-271.

Paliwal G S. 1969a. Stomata in Certain Angiosperms: their

Structure, Ontogeny and Systematic Value, in Recent Advances

in Anatomy of Tropical Seed Plants. Delhi: Hindustan

Publication.

Paliwal G S. 1969b. Stomatal ontogeny and phylogeny. Ⅰ.

Monocotyledons. Acta Bot Neerl, 18:654-668.

Pant D D. 1965. On the ontogeny of stomata and their homolo-

gous structure. Plant Sci Series,Ⅰ:1-24.

Patel J D. 1978. How should we interpret and distinguish subsid-

iary cells? Bot J Linn Soc, 77:65-72.

Patel J D. 1979. New morphological classification of stomatal

complexes. Phytomorphology, 29:218-229.

Payne W W. 1970. Helicocytic and allelocytic stomata: unrecog-

nized patterns in the dicotyledonae. Am J Bot, 57:140-147.

Payne W W. 1979. Stomatal patterns in embryophytes: their

evolution ontogeny and interpretation. Taxon, 28:117-132.

Prabhakar M, Anna M B. 1995. Foliar architecture of sapindales

occurring at Visakhapatnam. J India Bot Soc, 74:9-14.

Prabhakar M, Anna M B. 1996. Foliar architecture in identifica-

tion of the flora. Khan I A. Frontiers in Plant Science.

Hyderabad, India: Anwarul Uloom Education Society Publ.

Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata 251

1005-1026.

Prabhakar M, Bhatia R Y P, Verma H K. 1988a. Forensic studies

of poisonous and medicinal plants Casacabela thevetia (L.).

Lippold (Apocynaceae). Indian J For Sci, 2:21-32.

Prabhakar M, Leelavathi P. 1989. Structure, delimitation, nomen-

clature and classification of plant trichomes. Asian J Pl Sci, 1

(1):49-66.

Prabhakar M, Leelavathi P. 1991. Structure and ontogeny of uni-

cellular conical hairs in Leguminosae. J Swamy Bot Cl, 8(1, 2):

23-29.

Prabhakar M, Leelavathi P. 1992. Structure, delimitation and dis-

tribution of paracytic stomata in Leguminasae and

Portulacaceae. J Swamy Bot Cl, 9 (3, 4):93-102.

Prabhakar M, Leelavathi P, Ramayya N. 1986. Structure, distri-

bution and ontogeny of multiseriate conical hairs in

Leguminosae. Proc Nat Acad Sci, 56:39-42.

Prabhakar M, Leelavathi P, Jelani S, Shoba Rani G, Narayan R.

1990. Pharmacognostic studies of Adatoda zeylanica medicus.

J Swamy Bot Club, 7(1, 2):1-7.

Prabhakar M, Ramayya N. 1975. Structure and development of

trichomes in the family Portulacaceae. Mohan Ram H Y, Shah

J J, Shah C K. Form Structure and Function in Plants. Johri B

M. Commemoration Volume. Sarita Prakashan, Nauchandi,

Meerut, India. 356-368.

Prabhakar M, Ramayya N. 1979. Anatomical studies in the In-

dian Portulacaceae. Ⅱ. Leaf Lamina, “Histochemistry, De-

velopmental and Structural Anatomy of Angiosperms”.

Pereasamy K. Symposium Volume. Tiruchirapally, India: P

and B Publications. 159-169.

Prabhakar M, Ramayya N, Leelavathi P. 1984. Structure and

distribution of epidermal elements in the angiosperms. Ⅰ.

Epidermal cell complex. Geophytology, 14:55-68.

Prabhakar M, Rao T S, Bhatia R Y P. 1988a. Micromorphological

studies on tobacco and its significance in forensic science.

Indian J For Sci, 2:67-78.

Prabhakar M, Shoba R G, Narayan R, Leelavathi P. 1988b. Struc-

ture distribution and taxonomic significance of lithocysts and

cystoliths in Acanthaceae. J Swamy Bot Cl, 5:13-18.

Prabhakar M, Vijay K B K, Ramayya N, Leelavathi P. 1985.

Structure, distribution and taxonomic significance of trichomes

in some Indigofera L. (Fabaceae). Proc Indian Acad Sci (Plant

Sci), 95:309-314.

Prantle K. 1872. Die Ergebnisse der neueren untersuchugen Uber-

die spaltoffnungen. Flora, 55:305-312, 321-328, 337-346,

369-382.

Prantle K. 1881. Untersuchungen zur Morphologie der

Gefasskryptogamen.Ⅱ. Die Schizaeaceen. Leipzig W.

Engelman.

Prat H. 1960. Vers une classification naturelle des Graminees.

Bull Soc Bot France, 107(1, 2):51.

Probst W. 1971. Vergleichende morphologie und Entwicklungs

geschiete der spltaffnungen bei Farnen. Dissertation Univer-

sity Tubingen.

Rajagopal T. 1973. Flora of Hyderabad including a study of the

foliar epidermal characters of the species as an aid to taxonomy.

PhD Thesis, Hyderabad: Osmania University.

Ramayya N, Leelavathi P, Prabhakar M. 1983. Pharmacognostic

studies in the leaf of Tylophora indica (Burm.f.). Merr Hahne,

Glean, 50:124-133.

Ramayya N, Prabhakar M. 1973. Growth dynamics and devel-

opmental patterns in the unicellular trichomes of angiosperms.

Curr Sci, 42:376-381.

Ramayya N, Prabhakar M. 1975. Morphology of the shaggy

appendages Ⅱ. Elatinaceace. J Indian Bot Soc, 54:110-115.

Rao T S, Prabhakar M, Bhatia R Y P, Verma H K. 1991.

Dermotype studies of beedi wrappers of different brands and

its significance to forensic science. Indian J For Sci, 5:188-

197.

Rao T S, Bhatia R Y P, Prabhakar M. 1992a. Morphochemical

analysis of beedies in relation to forensic science. J Indian

Acad For Sci, 31:38-41.

Rao T S, Prabhakar M, Bhatia R Y P. 1992b. Epidermal studies

on different brands of beedies as an aid to criminal investigation.

Indian J For Sci, 6:157-164.

Rao T S, Prabhakar M, Bhatia R Y P. 1992c. Epidermal studies

on cigarette tobacco cultivars in relation to forensic science

Indan. J Criminol Criminoastics, 13(3, 4):55-64.

Rao T S, Bhatia R Y P, Prabhakar M, Verma H K. 1993a. Micro-

morphological studies on different brands of beedi wrappers

and its significance to forensic science. Adva Pl Sci, 6:265-

272.

Rao T S, Jelani S, Bhatiya R Y P, Prabhakar M. 1993b. Foliar

surface characters of Nicotiana tabacum L. cultivars in rela-

tion to forensic science. J Indian Bot Soc, 74:24-33.

Rao T S, Prabhakar M, Bhatia R Y. 1993c. Dermotype studies on

different brands of cigarettes as an aid to criminal investiga-

tion Adl. Tip Derg, 9:15-19.

Rasmussen H. 1981. Terminology and classification of stomata

and stomatal development. Bot J Linn Soc, 83:199-212.

Shtromberg A Y A. 1956. On the question of classification of

stomatal types of dicotyledonous plants. Sci Publ Chem

Pharmoc Inst, 8:51-66.

Acta Botanica Sinica 植物学报 Vol.46 No.2 2004252

Simola L K. 1968. Comparative studies on number of leaflets,

venation and epidermal structure in the genus Lathyrus. Can J

Bot, 46:71-84.

Solereder H. 1908. Systematic Anatomy of the Dicotyledons.

Vol. 2. Oxford: Clarendon Press.

Stace C A. 1965. Cuticular studies as an aid to plant taxonomy.

Bull Brit Muss Bot, 4:1-78.

Stevens R A, Martin E S. 1978. A new ontogenetic classification

of stomatal types. Bot J Linn Soc, 77:53-64.

Tomlinson P B. 1974. Development of stomatal complex as a

taxonomic character in the Monocotyledons. Taxon, 23:109-

128.

van Cotthem W. 1970a. Comparative morphological study of the

stomata in the Filicopsida. Bull Jard Bot Nat Belg, 40:81-

239.

van Cotthem W. 1970b. A classification of stomatal types. Bot J

Linn Soc, 63:235-246.

Verma H K, Bhatia R Y P, Prabhakar M, Rao T S. 1989. Forensic

studies of poisonous and medicinal plants- Ⅱ Abrus

precatorius L. (Fabaceae). Front For, 1:363-371.

Verma H K, Bhatia R Y P, Prabhakar M. 1991. Forensic studies

of poisonous and medicinal plants IV. Nerium indicum Miller

(Apocynaceae). J Indian Acad For Sci, 30:41-49.

Verma H K, Bhatia R Y P, Prabhakar M, Rao T S. 1992. Forensic

studies of poisonous and medicinal plants Ⅲ. Argemone

mexicana L. (papavaraceae). Indian J For Sci, 6:165-172.

Vesque J. 1889. De l’emploi des caracteres anatomiques dans la

classification des vegetaux. Bull Soc Bot Fr, 36:41-77.

Vijay Kumar B K, Prabhakar M, Ramayya N, Leelavathi P. 1986.

Structure, distribution and development of cavitated trichomes

in Indigofera L. (Fabaceae). Geophytology, 16:227-231.

Wilkinson H P. 1979. The plant surface (Mainly leaf) part 1:

stomata in the anatomy of the dicotyledons. Vol. 1. Metcalfe

C R, Chalk L. 2nd ed. Oxford: Clarendon Press. 97-117.

(Managing editor: HE Ping)