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Anatomical features of species of Cyperaceae from northeastern Brazil

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DOI: 10.1007/s12228-009-9073-0

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Anatomical features of species of Cyperaceae
from northeastern Brazil
SHIRLEY MARTINS1,2 AND MARCCUS ALVES1
1
Laboratório de Morfo-taxonomia Vegetal, Departamento de Botânica, Universidade Federal de
Pernambuco, Av. Prof. Moraes Rego s/n, Cidade Universitária, 50560-901, Recife, PE, Brazil;
2
Present address: Departamento de Botânica, IB, Universidade Estadual Paulista, Av. 24-A, 1515,
Bela Vista, 13506-900, Rio Claro, SP, Brazil e-mail: shirley_botany@yahoo.com.br

Abstract. Seventy-three species from 17 genera of Cyperaceae were studied with the
aim of identifying and confirming those species with Kranz anatomy. Among the
species studied, 36 exhibited Kranz anatomy; 37 did not. Of the four types of Kranz
anatomy recognized in Cyperaceae, three were encountered: the chlorocyperoid type
in the genera Cyperus, Kyllinga, Lipocarpha, Pycreus, and Remirea; the fimbristyloid
type in Abildgaardia, Bulbostylis, and Fimbristylis; and the rhynchosporoid type in
Rhynchospora. Non-Kranz anatomy was confirmed in species of the following gen-
era: Becquerelia, Calyptrocarya, Cyperus, Diplacrum, Eleocharis, Fuirena, Hypoly-
trum, Pleurostachys, Rhynchospora, and Scleria. The anatomical data obtained
corroborate earlier studies of species of Cyperaceae as to the presence of Kranz an-
atomy and the anatomical types in several species and the “Kranzkette” pattern in
Cyperus ligularis and Cyperus pohlli.
Key Words: Anatomy, chloroplast, Cyperaceae, Kranz, C4 photosynthesis.
Resumo. Setenta e três espécies pertencentes a 17 gêneros de Cyperaceae foram
estudadas com o objetivo de identificar e confirmar espécies com anatomia Kranz.
Entre as espécies estudadas, 36 exibem anatomia Kranz e 37 não. Dos quatro tipos de
anatomia Kranz reconhecidos em Cyperaceae, três foram encontrados: o tipo cloroc-
iperóide nos gêneros Cyperus, Kyllinga, Lipocarpha, Pycreus e Remirea; o fimbrist-
ilóide em Abildgaardia, Bulbostylis e Fimbristylis; e o tipo rincosporóide em
Rhynchospora. Anatomia não Kranz foi confirmada em espécies dos seguintes gên-
eros: Becquerelia, Calyptrocarya, Cyperus, Diplacrum, Eleocharis, Fuirena, Hypo-
lytrum, Pleurostachys, Rhynchospora e Scleria. Os dados anatômicos obtidos
corroboram recentes estudos para espécies de Cyperaceae, como a presença da anat-
omia Kranz e do tipo anatômico em várias espécies e o padrão “Kranzkette” em
Cyperus ligularis e Cyperus pohlli.

The angiosperms are divided by means of structural characteristics, as well as physio-

the photosynthetic mechanism of carbon logical and ecological differences.
assimilation into three large groups: C3, C4, The term “Kranz” was first used by
and CAM species (Sage, 2001, 2004). Sever- Haberlandt (1882, 1914). It is related to the
al authors (Takeda et al., 1980; Soros & radial, wreath-like, disposition of mesophyll
Bruhl, 2000; Hibberd & Quick, 2002; Bruhl cells around the vascular bundles and the
& Wilson, 2007) affirm that existing varia- presence of a sheath with conspicuous chlor-
tions in the photosynthetic pathway are oplasts (Kranz sheath). The anatomical mod-
strictly associated with anatomical and ultra- ifications existing among C4 species are

Brittonia, 61(2), 2009, pp. 189–200 ISSUED: 1 June 2009

© 2009, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.
190 BRITTONIA [VOL 61

considered relevant to phylogenetic and evo- such as in Chenopodiaceae (Voznesenskaya

lutionary studies (Takeda et al., 1985; Bruhl, et al., 2001, 2002; Sage, 2004; Akhani et al.,
1995; Muasya et al., 2000; Soros & Bruhl, 2005). Except in some species of Eleocharis
2000; Soros & Dengler, 2001; Kadereit et al., R. Br. (Ueno, 2004; Murphy et al., 2007), all
2003; Murphy et al., 2007). studied species of Cyperaceae with Kranz
Species with the C4 photosynthetic path- anatomy also have the C4 photosynthetic
way are characterized by the presence of two pathway (Takeda et al., 1985; Kalapos et al.,
types of specialized photosynthetic tissues. 1997; Soros & Dengler, 1998; Soros & Bruhl,
The radiate parenchyma is responsible for the 2000; Murphy et al., 2007).
primary carbon assimilation (PCA). Photo- Among the four accepted subfamilies of
synthetic carbon reduction (PCR) occurs in Cyperaceae (Goetghebeur, 1998), the occur-
the vascular bundle sheath (Soros & Dengler, rence of Kranz anatomy is recorded only for
1998; Soros & Bruhl, 2000). Primary carbon Cyperoideae. This subfamily has both C3 and
assimilation tissue occurs in contact with C4 photosynthetic pathways and presents a
atmospheric air, across intercellular spaces broad global distribution (Takeda et al., 1985;
and substomatic cavities, while PCR is Goetghebeur, 1998). Cladistic analyses sug-
isolated and is found close to vascular tissues gest that the Kranz syndrome evolved at least
(Soros & Dengler, 1998). four times in Cyperaceae (Muasya et al.,
In C4 species there are also a larger number 1998; Soros & Bruhl, 2000) and four distinct
of vascular bundles compared to C3 species, anatomical types have been identified: chlor-
due to the short distance between PCA and ocyperoid, eleocharoid, fimbristyloid, and
PCR tissues (Soros & Dengler, 1998). The rhynchosporoid (Brown, 1975; Takeda et al.,
short distance or “one cell distance criterion” 1980; Bruhl et al., 1987; Soros & Dengler,
purpose by Hatterley and Watson (1975) is 1998).
one of the principal means of anatomical About 41 genera and 700 species of
identification of species with C4 photosynthe- Cyperaceae occur in Brazil in all vegetation
sis (Soros & Dengler, 1998; Soros & Bruhl, types, and 27 genera and 280 species are
2000). found in the northeastern region (Alves et al.,
About 90 genera and 18 families of 2008). Studies aimed at identification and
angiosperms have C4 photosynthesis (Sage, interpretation of Kranz anatomy, in species
2004). Cyperaceae, Poaceae, and Hydrochar- found in Brazil, are scarce (Estelita-Teixeira
itaceae are the only families with C4 species & Handro, 1987; Estelita, 1992, 1993;
among the monocotyledons (Laetsch, 1974; Rodrigues & Estelita, 2003). Thus, we sought
Soros & Dengler, 1998; Sage, 2004). Cyper- to identify and confirm the occurrence of
aceae is the second largest family in number Kranz anatomy in species of Cyperaceae
of C4 species (Sage, 2004). According to from northeastern Brazil due to the impor-
Bruhl and Wilson (2007) about 15% of tance of these data to the taxonomy and
genera and 34% of the species sampled in phylogeny of the family.
Cyperaceae are C4. In some regions, the
geographical distribution of photosynthetic
pathway of Cyperaceae species is already Materials and methods
known (Terri & Livinstone, 1980; Takeda et The 73 species belonging to 17 genera were
al., 1985; Ueno & Takeda, 1992; Li, 1993; Li collected in different ecosystems in northeast-
et al., 1999; Stock et al., 2004). The major ern Brazil (Table I). The vouchers specimens
contribution to C3/C4 assessments in Cyper- are at the UFP herbarium (Appendix).
aceae has been made by Bruhl and Wilson Transverse sections (TS) were made by
(2007) with information on 107 genera and hand of the median region of fully developed
1406 species. Nevertheless, there is very aerial photosynthetic organs (leaves, bracts,
little information for species occurring in and scapes) of all species studied, except in
Brazil. those species where all of these organs do not
Studies revealed that some species with C4 fully expand. This is the case in species of the
photosynthesis do not have Kranz anatomy, genus Eleocharis R. Br. and in Cyperus
2009] MARTINS & ALVES: CYPERACEAE ANATOMY 191

TABLE I
PRESENCE OF KRANZ ANATOMY AND KRANZ TYPOLOGY IN STUDIED SPECIES OF CYPERACEAE AND THEIR HABITATS FROM
NORTHEASTERN BRAZIL. KA (KRANZ ANATOMY); KT [KRANZ TYPOLOGY: C (CHLOROCYPEROID), F (FIMBRISTYLOID), AND R
(RHYNCHOSPOROID)].

KT
Taxon KA C F R Habitat References
CYPEROIDEAE Suess.
Abildgaardieae Lye
Abildgaardia baeothryon St. Hil. + X Dry forest
A. ovata (Burm f.) Kral + X Restinga Carolin et al. (1977)
Bulbostylis junciformis (Kunth) C. B. Clarke + X Campo rupestre Prata et al. (2007)
B. paradoxa (Spreng.) Lindm. + X Dry forest Prata et al. (2007)
B. scabra (J. Presl. & C. Presl.) C. B. Clarke + X Inselberg Prata et al. (2007)
Fimbristylis cymosa R. Br. + X Coastal dunes Takeda et al. (1985)
F. dichotoma (L.) Vahl + X Inselberg Takeda et al. (1985)
F. vahlii (Lam.) Link. + X Ruderal area
Cypereae Dumort.
Cyperus aggregatus (Willd.) Endl. + X Ruderal area Bruhl and Wilson (2007)
C. articulatus L. + X Ruderal area Bruhl and Wilson (2007)
C. compressus L. + X Ruderal area Takeda et al. (1985)
C. cuspidatus Kunth + X Inselberg Takeda et al. (1985)
C. distans L. + X Ruderal area Ueno and Takeda (1992)
C. entrerianus Boeck. − Moist forest Bruhl and Wilson (2007)
C. eragrostis Lam. − Ruderal area Bruhl and Wilson (2007)
C. haspan L. − Ruderal area Bruhl and Wilson (2007)
C. involucratus Rottb. − Moist forest Bruhl and Wilson (2007)
C. iria L. + X Ruderal area Carolin et al. (1977)
C. laxus Lam. − Moist forest Bruhl and Wilson (2007)
C. ligularis L. + X Ruderal area Bruhl and Wilson (2007)
C. luzulae (L.) Retz. − Moist forest Bruhl and Wilson (2007)
C. maritimus Poir. + X Coastal dunes Martins et al. (2008)
C. meyenianus Kunth + X Dry forest Bruhl and Wilson (2007)
C. odoratus L. + X Dry forest Bruhl and Wilson (2007)
C. pohlli (Nees) Steud. + X Ruderal area
C. rotundus L. + X Ruderal area
C. schomburgkianus Nees − Dry forest Bruhl and Wilson (2007)
C. simplex Kunth − Moist forest
C. sphacelatus Rottb. + X Ruderal area Bruhl and Wilson (2007)
C. subcasteneus D. A. Simpson − Dry forest
C. surinamensis Rottb. − Ruderal area Bruhl and Wilson (2007)
C. uncinulatus Schrad. ex Nees − Inselberg Bruhl and Wilson (2007)
Kyllinga brevifolia Rottb. + X Ruderal area Carolin et al. (1977)
K. odorata Vahl + X Inselberg Metcalfe (1971)
K. pumila Michx. + X Ruderal area Li et al. (1999)
K. squamulata Thonn. ex Vahl + X Inselberg Govindarajalu (1968)
K. vaginata Lam. + X Ruderal area
Lipocarpha micrantha (Vahl) G. Tucker + X Inselberg Bruhl and Wilson (2007)
L. salzmanniana Steud. + X Inselberg
Pycreus capillifolius (A. Rich.) C.B. Clarke + X Inselberg
P. flavescens (L.) Rchb. + X Inselberg Li et al. (1999)
P. lanceolatus (Poir.) C. B. Clarke + X Campo rupestre Bruhl and Wilson (2007)
P. macrostachyos (Lam.) Raynal + X Inselberg Takeda et al. (1985)
P. piceus Liebm. + X Inselberg
P. polystachyos (Rottb.) P. Beauv. + X Ruderal area Soros and Dengler (2001)
Remirea maritima Aubl. + X Coastal dunes Estelita (1993)
Eleocharideae Goetgh.
Eleocharis acuntangula (Roxb.) Schult. − Moist forest Govindaralaju (1975)
E. confervoides (Poir.) Miq. − Moist forest Bruhl and Wilson (2007)
E. filiculmis Kunth − Moist forest Bruhl and Wilson (2007)
E. flavescens (Poir.) Urb. − Inselberg Bruhl and Wilson (2007)
E. geniculata (L.) Roem. & Schult. − Ruderal area Takeda et al. (1985)
E. interstincta (Vahl) Roem. & Schult. − Moist forest Bruhl and Wilson (2007)
192 BRITTONIA [VOL 61

TABLE I
(CONTINUED)

KT
Taxon KA C F R Habitat References

Fuireneae Rchb. ex Fenzl

Fuirena umbellata Rottb. − Moist forest Takeda et al. (1985)
Schoeneae Dumort.
Pleurostachys puberula Brongn. − Moist forest
Rhynchospora caracasana (Kunth) Boeck. − Moist forest Ueno and Koyama (1987)
R. cephalotes (L.) Vahl − Moist forest Bruhl and Wilson (2007)
R. comata (Link) Roem. & Schult. − Moist forest Bruhl and Wilson (2007)
R. contracta (Nees) Raynal − Inselberg
R. globosa (Kunth) Roem. & Schult. + X Campo rupestre Ueno and Koyama (1987)
R. holoschoenoides (L.C. Rich.) Herter − Inselberg Takeda et al. (1980)
R. nervosa (Vahl) Boeck. − Moist forest Ueno and Koyama (1987)
R. pubera (Vahl) Boeck. − Moist forest Ueno and Koyama (1987)
R. ridleyi C. B. Clarke − Dry forest Ueno and Koyama (1987)
R. riparia (Nees) Boeck. − Inselberg
MAPANIOIDEAE C. B. Clarke
Hypolytreae Presl ex Fenzl
Hypolytrum bullatum C. B. Clarke − Moist forest Alves et al. (2002)
SCLERIOIDEAE C. B. Clarke
Bisboeckelereae Pax ex L. T. Eiten
Becquerelia cymosa Brongn. − Moist forest Bruhl and Wilson (2007)
Calyptrocarya glomerulata (Brongn.) Urb. − Moist forest Bruhl and Wilson (2007)
Diplacrum capitatum (Willd.) Boeck. − Moist forest
Sclerieae Kunth ex Fenzl
Scleria bracteata Cav. − Moist forest
S. hirtella Sw. − Moist forest Holm (1899)
S. latifolia Sw. − Moist forest
S. reticularis Michx. ex Willd. − Moist forest Holm (1899)
S. secans (L.) Urb. − Inselberg Bruhl and Wilson (2007)

articulatus L. where leaves are reduced to and located between the parenchymatic
scales. sheath and/or the mesophyll cells and the
Fresh material and previously dried materi- bundles, and “Kranz sheath” for the large
als (rehydrated in glycerol) were used for the cells with thin walls located next to the
studies. Some TS’s were observed without vascular tissues (Brown, 1975; Bruhl, 1995;
treatment. For the anatomical description, Soros & Dengler, 1998; Rodrigues & Estelita,
the TS’s were bleached with 30% sodium 2003).
hypochloride, double stained with safranin
and Astra blue (Kraus & Arduin, 1997) and
mounted on semi permanent slides in 50% Results and discussion
glycerine (Purvis et al., 1964). In order to Of the species studied, 36 present Kranz
see the starch grains present in the Kranz features and 37 non-Kranz (Table I). Vascular
sheath, Lugol histochemical tests (Berlyn bundles were separated by more than four
& Miksche, 1976) were performed on chlorophyllous parenchyma cells in the non-
some TS’s. Observations were recorded by Kranz species (Fig. 1A, B). In this case, the
means of microphotographs using a Zeiss vascular bundles are surrounded by two
photomicroscope. sheaths: an external one with thin-walled
The anatomical terminology used here cells, the parenchymatous sheath; and the
follows previous papers in Cyperaceae. The other internal with thick-walled cells, the
terms used include “radiate parenchyma” for mestome sheath (Fig. 1C, E).
the PCA tissue; “mestome sheath” for the In the species with Kranz features the
sheath formed by cells with very thick walls vascular bundles are close together (Fig. 2A,
2009] MARTINS & ALVES: CYPERACEAE ANATOMY 193

FIG. 1. Transverse sections of leaves and scapes of species of Cyperaceae with non-Kranz anatomy. A. Leaf of
Cyperus laxus, note the presence of widely spaced bundles. B. Scape of Rhynchospora nervosa showing the vascular
bundles with mestome sheaths, parenchymatous cells and absence of radiate parenchyma. C-E. Vascular bundles with
two sheaths and no radiate parenchyma. C. Leaf of Scleria bracteata. D. Leaf of Calyptrocarya glomerulata. E. Scape
of Eleocharis confervoides. Chlorophyllous parenchyma (Cp); Mestome sheath (Ms); parenchymatous cell (Pc);
parenchymatic sheath (Ps); vascular bundles (Vb); vessel element (Ve).

B) with two to four mesophyll cells between complete only in the fimbristyloid type; in the
them. The chlorophyllous parenchyma is other types when the sheath occurs, it has few
radially arranged around the vascular bundles cells (Fig. 2A, D, E).
(Fig. 2A-D). Depending on the Kranz type, According to Soros and Dengler (1998),
the bundles can be surrounded by two or the proximity of photosynthetic tissues in C4
three sheaths. Metaxylem elements interrupt plants results in a greater efficiency in
the Kranz sheath in the major bundles of diffusion of photosynthetic metabolites, facil-
chlorocyperoid and fimbristyloid types itating the transport of photosynthates from
(Fig. 2A, C, E). The mestome sheath is the assimilating tissue (PCA) to the vascular
always present (Fig. 2A, C, D, E), but, the system.
Kranz sheath is absent in the rhynchosporoid In the scape, the species with Kranz
type (Fig. 2D). The parenchymatous sheath is anatomy have peripheral vascular bundles
194 BRITTONIA [VOL 61

FIG. 2. Transverse sections of leaves and scapes of species of Cyperaceae with Kranz anatomy. A. Cyperus
aggregatus showing Kranz anatomy of the chlorocyperoid type with two sheaths, incomplete Kranz sheath, and some
parenchymatous cells. B. Scape of Cyperus articulatus with closely spaced peripheral vascular bundles differing from
those of medullar vascular bundles, which are widely spaced, and intermediate vascular bundles with radiate
parenchyma adjacent to phloem. C. Fimbristylis cymosa, showing the fimbristyloid type, with three sheaths and
incomplete Kranz sheath. D. Rhynchospora globosa showing the rhynchosporoid type with a complete mestome
sheath (PCR tissues) and some parenchymatous cells. E. Cyperus maritimus with the chlorocyperoid type having an
incomplete third sheath with parenchymatous cells and fibers. F. Cyperus ligularis, note the Kranzkette pattern with
air cavities surrounded by chlorocyperoid bundles. Air cavity (Ac); fiber (Fb); intermediate vascular bundles (Ivb);
Kranz sheath (Ks); mestome sheath (Ms); medullar vascular bundles (Mvb); parenchymatous cell (Pc); parenchymatic
sheath (Ps); peripheral vascular bundles (Pvb); radiate parenchyma (Rp); vessel element (Ve).
2009] MARTINS & ALVES: CYPERACEAE ANATOMY 195

that are closer to each other and generally and Abildgaardia the majority of species
completely surrounded by radiate parenchy- have Kranz anatomy, and in Bulbostylis all
ma and the Kranz sheath (Fig. 2B). The do. In Bulbostylis either the fimbristyloid type
medullar vascular bundles are larger and or the eleocharoid type can occur (Soros &
more distant from each other compared to Bruhl, 2000), though this was not observed
the peripheral ones (Fig. 2B). In the vascular here.
bundles located in the intermediate region, The rhynchosporoid type was observed
immediately below the peripheral bundles, only in Rhynchospora globosa (Kunth)
the radiate parenchyma occurs only in the Roem. & Schult. (Table I; Fig. 2D) which
adjacent phloem (Fig. 2B). The same ana- belongs to R. sect. Pluriflorae Kük. (Ueno &
tomical pattern was observed by Metcalfe Koyama, 1987). The Rhynchospora species
(1971) and Estelita-Teixeira and Handro with Kranz anatomy have been observed
(1987) in scapes of different species of exclusively in R. sect. Pauciflorae Kük. and
Cyperaceae with Kranz anatomy. R. sect. Pluriflorae of the subgenus Haplo-
The tests used to observe starch grains in stylis (Nees) Benth. & Hooker (Takeda et al.,
PCR tissue (the Kranz sheath, except in the 1980; Ueno & Koyama, 1987).
rhynchosporoid type, when the PCR tissue is Most of the Kranz species studied (26) has
the mestome sheath) reacted more strongly the chlorocyperoid type (Table I), and are
than in PCA or in chlorophyllous parenchy- represented by the genera Cyperus (Fig. 2A,
ma of non-Kranz species. Several studies E), Kyllinga, Lipocarpha, Pycreus (Fig. 2B),
have shown that the combination of large and Remirea (tribe Cypereae). The tribe
chloroplasts and starch grains in the PCR, as Cypereae represents the major species group
seen in the present study, are one of the with Kranz anatomy in Cyperaceae (Bruhl &
indicators of C4 photosynthesis (Laetsch, Wilson, 2007), and all species studied thus far
1974; Takeda et al., 1980; Estelita-Teixeira present the chlorocyperoid type (Soros &
& Handro, 1987; Kalapos et al., 1997). Bruhl, 2000; Rodrigues & Estelita, 2003;
Eleven of the species studied belong to Martins et al., 2008). According to Takeda
genera with previous indications of non- et al. (1985) and Soros and Dengler (2001)
Kranz anatomy (Table I), such as Becquer- the chlorocyperoid type can have larger
elia, Calyptrocarya, Diplacrum, Hypolytrum, bundles with more than two sheaths external
Fuirena, Pleurostachys, and Scleria to the mestome, and occasionally one or a
(Metcalfe, 1971; Takeda et al., 1985; Bruhl, few parenchyma cells adjacent to the meta-
1995; Alves et al., 2002; Bruhl and Wilson xylem elements. A few parenchyma cells can
2007). The remaining 26 species of non- be seen in some species, such as Cyperus
Kranz plants are in genera where the two aggregatus (Willd.) Engl. (Fig. 2A). Martins
types have been observed (Takeda et al., et al. (2008) pointed out that in Cyperus
1980; Takeda et al., 1985; Li, 1993; Soros maritimus Poir. these cells are thin or thick-
& Bruhl, 2000; Bruhl & Wilson, 2007). walled and form an incomplete third sheath in
Among these are Cyperus (Fig. 1A and 2A, the largest vascular bundles (Fig. 2E). The
E, F), Eleocharis, and Rhynchospora occurrence of more than three cells external
(Fig. 1B; Fig. 2D). Of these genera, only to the mestome sheath is considered uncom-
Eleocharis has no representatives with Kranz mon among species with the chlorocyperoid
anatomy among the studied species. The same type (Brown, 1975; Soros & Bruhl, 2000).
species from other localities were examined by Cyperus ligularis L. and Cyperus pohlli
Bruhl and Wilson (2007), who concluded that (Nees) Steud. have the same pattern of Kranz
this indicated C3 photosynthesis. anatomy described by Li and Jones (1994) for
Of the 36 species studied with Kranz Cyperus japonicus Makino (which was indi-
anatomy, eight have the fimbristyloid type cated by Bruhl and Wilson (2007) as being
(Table I) in the genera Abildgaardia, Bulbos- probably C. orthostachys Franch. & Sav.). Li
tylis and Fimbristylis (Fig. 2C). All of them and Jones (1994) called this pattern “Kranzk-
are of the Abildgaardieae tribe (Goetghebeur, ette” (Kranz in chain), because of the distri-
1998). According to Soros and Bruhl (2000) bution of air cavities. The air cavities are
and Bruhl and Wilson (2007), in Fimbristylis isolated from each other by the largest
196 BRITTONIA [VOL 61

bundles and further surrounded by the small- The restriction of Cyperaceae species with
est ones, all of them of the chlorocyperoid Kranz anatomy to specific habitats is corrob-
type (Fig. 2F). Bruhl and Wilson (2007) orated by several authors (Terri & Livinstone,
pointed out that a similar organization was 1980; Takeda et al., 1985; Ueno & Takeda,
described in other species of Cyperus 1992; Li, 1993; Kalapos et al., 1997; Li et al.,
(Metcalfe, 1971; Govindarajalu, 1974; 1999; Sage, 2001; Kadereit et al., 2003;
Wilson, 1991; Bruhl et al., 1992; Bruhl, Stock et al., 2004).
1995), being referred to as vascular bundles This analysis reinforces the value of ana-
forming “rings” or a “horseshoe pattern”. tomical features that indicate photosynthetic
According to Li and Jones (1994), the pathway. These data further support that
presence of well developed air cavities in Kranz anatomy is restricted to the subfamily
these plants studied reflects an adaptation to Cyperoideae, that most non-Kranz species
flooded areas, aiding the accumulation of O2 occur in shady habitats, and that Kranz
and CO2. This could also be the case in C. species are found in habitats with high light
ligularis and C. pohlli, which occur in a intensity and hydric stress.
similar habitat. The presence of intercellular
air channels, or aerenchyma, which facilitates
aeration is cited by several authors for plants Acknowledgments
that grow in aquatic or highly moist environ- This work was supported by a grant to S.
ments (Beck, 2005; Evert, 2006). Martins from the National Research Council,
In Cyperus, the Kranz syndrome is a useful CNPq (20.1231). The authors thank members
character in infrageneric classification. The of the Plant Morpho-Taxonomy Laboratory
species of C. subg. Anosporum have non- of the Federal University of Pernambuco for
Kranz anatomy and C. subg. Cyperus, have their suggestions, Scott Heald for correcting
Kranz-anatomy (Araújo & Longh-Wagner, the English and anonymous referees for
1997; Goetghebeur, 1998; Muasya et al., providing constructive comments.
2001). The data presented support the tradi-
tional infrageneric classification of the genus.
The studied species of Pycreus, Kyllinga,
and Lipocarpha (Table I) are indicated as Literature Cited
always presenting Kranz anatomy (Takeda et Alves, M., M. E. M. Estelita, M. G. Wanderley & W.
al., 1985; Ueno & Takeda, 1992; Bruhl, 1995; W. Thomas. 2002. Aplicações taxonômicas da
anatomia foliar das espécies brasileiras de Hypoly-
Bruhl & Wilson, 2007). Stock et al. (2004) trum Rich. (Cyperaceae). Revista Brasileira de
considered Lipocarpha rehmannii (Ridl.) Botânica 25: 1–9.
Goetgh. as being C3, but Bruhl and Wilson Alves, M., A. C. Araújo, A. P. Prata, F. A. Vitta, S. M.
(2007) disagreed, reinforcing that all species Hefler, R. Trevisan, A. B. Gil, S. Martins & W. W.
of Lipocarpha are C4. Remirea is monotypic Thomas. 2008. Avanços e desafios no conhecimento
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APPENDIX

VOUCHER INFORMATION FOR THE SPECIES OF CYPERACEAE FROM NORTHEASTERN BRAZIL EMPLOYED IN THIS STUDY. ALL
SPECIMENS ARE DEPOSITED AT UFP.

Taxon Voucher
Abildgaardia baeothryon St. Hil. Pernambuco: Mirandiba, Serra do Tigre, J. Maciel et al. 429
A. ovata (Burm f.) Kral Pernambuco: Mirandiba, Serra do Tigre, D. Amorim et al. 108
Becquerelia cymosa Brongn. Pernambuco: Lagoa dos Gatos RPPN Frei Caneca, A. Santiago 727
Bulbostylis junciformis (Kunth) C. B. Clarke Pernambuco: Buíque, Parque Nacional do Catimbau, E. Rocha et al.
1532
B. paradoxa (Spreng.) Lindm. Bahia: Rio de Contas, M. Alves et al. 1838
B. scabra (J. Presl. & C. Presl.) C. B. Clarke Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 66
Calyptrocarya glomerulata (Brongn.) Urb. Paraíba: Mamanguape, Reserva Biológica Guaribas, A. Santiago 841
Cyperus aggregatus (Willd.) Endl. Piauí: São Espedito Lopez, S. Martins et al. 99
C. articulatus L. Rio Grande do Norte: Tibau do Sul, S. Martins et al. 231
C. compressus L. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
117
C. cuspidatus Kunth Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 68
C. distans L. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
150
C. entrerianus Boeck. Pernambuco: Lagoa dos Gatos RPPN Frei Caneca, A. Santiago 725
C. eragrostis Lam. Pernambuco: Caruaru, Distrito de Terra Vermelha, S. Martins et al.
107
C. haspan L. Bahia: Juazeiro, Ilha do Rodeadouro, S. Martins et al. 61
C. involucratus Rottb. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
149
C. iria L. Pernambuco: Serinhaém, Usina Trapiche, S. Martins et al. 113
C. laxus Lam. Pernambuco: Igarassu, Refúgio Ecológico Charles Darwin, S.
Martins et al. 24
C. ligularis L. Pernambuco: Jaboatão dos Guararapes, Candeias, S. Martins et al.
18
C. luzulae (L.) Retz. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
146
C. maritimus Poir. Rio Grande do Norte: Tibau do Sul, Praia de Pipa, S. Martins et al.
49
C. meyenianus Kunth Pernambuco: Buíque, Parque Nacional do Catimbau, S. Martins et
al. 50
C. odoratus L. Pernambuco: Pombos, Ponte da RFFSA, S. Martins et al. 48
C. pohlli (Nees) Steud. Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 163
C. rotundus L. Pernambuco: Recife, Campus da UFPE, S. Martins et al. 81
C schomburgkianus Nees Pernambuco: Buíque, Parque Nacional do Catimbau, S. Martins et
al. 79
C. simplex Kunth Alagoas: São José da Laje, M. Oliveira 756
C. sphacelatus Rottb. Pernambuco: Igarassu, Refúgio Ecológico Charles Darwin, S.
Martins et al. 23
C. subcasteneus D.A. Simpson Pernambuco: Buíque, Parque Nacional do Catimbau, S. Martins et
al. 72
C. surinamensis Rottb. Bahia: Juazeiro, Ilha do Rodeadouro, S. Martins et al. 60
C. uncinulatus Schrad. ex Nees Pernambuco: Venturosa, Parque Municipal da Pedra Furada, S.
Martins et al. 80
Diplacrum capitatum (Willd.) Boeck. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
39
Eleocharis acuntangula (Roxb.) Schult. Pernambuco: Moreno, Mata do Balãozinho, M. Luceño et al. 95
E. confervoides (Poir.) Miq. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
43
E. filiculmis Kunth Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
10
E. flavescens (Poir.) Urb. Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 67
E. geniculata (L.) Roem. & Schult. Bahia: Juazeiro, Ilha do Rodeadouro, S. Martins et al. 56
E. interstincta (Vahl) Roem. & Schult. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al. 12
200 BRITTONIA [VOL 61

(CONTINUED)

Taxon Voucher

Fimbristylis cymosa R. Br. Pernambuco: Cabo de Santo Agostinho, Praia do Paiva, S. Martins
et al. 42
F. dichotoma (L.) Vahl Pernambuco: Bezerros, Pedra Antônio Bezerra S. Martins et al. 92
F. vahlii (Lam.) Link. Pernambuco: São Lourenço da Mata, Estação Ecológica Tapacurá, S.
Martins 90
Fuirena umbellata Rottb. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
11
Hypolytrum bullatum C. B. Clarke Pernambuco: Serinhaém, Usina Trapiche, S. Martins et al. 186
Kyllinga brevifolia Rottb. Pernambuco: Recife, Campus da UFPE, S. Martins et al. 82
K. odorata Vahl Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 142
K. pumila Michx. Pernambuco: São Lourenço da Mata, Estação Ecológica Tapacurá, S.
Martins 169
K. squamulata Thonn. ex Vahl Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 135
K. vaginata Lam. Pernambuco: Cabo de Santo Agostinho, Praia do Paiva, S. Martins
et al. 53
Lipocarpha micrantha (Vahl) G. Tucker Pernambuco: Venturosa, Parque Municipal da Pedra Furada, S.
Martins et al. 75
L. salzmanniana Steud. Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 134
Pleurostachys puberula Brongn. Pernambuco: Caruaru, Reserva Ecológica Brejo dos Cavalos, M.
Alves 23595
Pycreus capillifolius (A. Rich.) C.B. Clarke Pernambuco: Venturosa, Parque Municipal da Pedra Furada, S.
Martins et al. 100
P. flavescens (L.) Rchb. Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 138
P. lanceolatus (Poir.) C.B. Clarke Bahia: Angüera, F. França et al. 2225
P. macrostachyos (Lam.) Raynal Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 40
P. piceus Liebm. Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 139
P. polystachyos (Rottb.) P. Beauv. Bahia: Juazeiro, Ilha do Rodeadouro, S. Martins et al. 58
Remirea maritima Aubl. Pernambuco: Cabo de Santo Agostinho, Praia do Paiva, S. Martins
et al. 54
Rhynchospora caracasana (Kunth) Boeck. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
15
R. cephalotes (L.) Vahl Pernambuco: Igarassu, Refúgio Ecológico Charles Darwin, S.
Martins et al. 20
R. comata (Link) Roem. & Schult. Pernambuco: Cabo de Santo Agostinho, Reserva Ecológica Gurjaú,
L. Felix 9798
R. contracta (Nees) Raynal Pernambuco: Venturosa, Parque Municipal da Pedra Furada, S.
Martins et al. 77
R. globosa (Kunth) Roem. & Schult. Bahia: Rio das Contas, Pico das Almas, M. Luceño et al. 371
R. holoschoenoides (L.C. Rich.) Herter Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 65
R. nervosa (Vahl) Boeck. Pernambuco: Igarassu, Refúgio Ecológico Charles Darwin, S.
Martins et al. 22
R. pubera (Vahl) Boeck. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
16
R. ridleyi C. B. Clarke Pernambuco: Buíque, Parque Nacional do Catimbau, S. Martins et
al. 78
R. riparia (Nees) Boeck. Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 70
Scleria bracteata Cav. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
13
S. hirtella Sw. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
14
S. latifolia Sw. Pernambuco: Recife, Parque Estadual Dois Irmãos, S. Martins et al.
17
S. reticularis Michx. ex Willd. Pernambuco: Caruaru, Reserva Ecológica Brejo dos Cavalos, J. A.
Siqueira-Filho 861
S. secans (L.) Urb. Pernambuco: Bezerros, Pedra Antônio Bezerra, S. Martins et al. 69

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