The anatomy and occurrence of foliar nectaries in Cyathea (Cyatheaceae).

ABSTRACT.--This study reports the widespread occurrence of foliar nectaries in most New World species of the genus Cyathea. The anatomy of these glands and the variation in structure among the species is described. Some Cyathea species primitively lack glands, and the presence or absence of these glands and their structure correlate with recent molecular phylogenies.

KEY WORDS.--anatomy, Cyathea, glands, nectaries, phylogeny

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In contrast to the widespread prominence of both floral and extrafloral nectaries in the flowering plants, nectaries have been reported in relatively few pteridophytes. Here we report the widespread occurrence of nectary-like foliar glands among many New World species of the tree fern genus Cyathea, and describe the anatomical structure of these glands for the first time.

Classifications of Cyatheaceae are still variable at the generic level. Some researchers include all species in Cyathea, while many others recognize three or more genera. DNA phylogenies have now greatly clarified the main subgroups of the scaly tree ferns (e.g., Korall et al., 2007, Janssen et al., 2008, and Bystriakova et al., 2011). The described differences in morphological features among these major groups have chiefly involved the details of scales and spores. Here, we report on a distinctive characteristic of a large group of species within the genus Cyathea: the occurrence of foliar nectaries or nectary-like glands on the fronds. These nectaries are often conspicuously present on Cyathea pinna and pinnule bases, but previously have been little noted in the literature.

There is a long history of studies of the structure and function of nectaries, both floral and extrafloral (Zimmerman, 1932; Fahn, 1979). The major focus in studies of floral nectaries in angiosperms is primarily on their role in the pollination biology of the species; studies of extrafloral nectaries tend to consider the nectaries in relationship to insect-plant mutualism and defense strategies of plants (e.g., Agrawal, 2011; Bentley, 1977; Fahn, 1979; Bentley and Elias, 1983; Elias, 1983; Elias and Sun An-ci, 1985; Freitas et al., 2001; Koptur, 1985, 1992; Rosumek et al., 2009).

Detailed anatomical descriptions of nectar glands are available for numerous flowering plants (e.g., Elias, 1983; Marginson et al., 1985; Durkee, 1987; McDade and Turner, 1997; Machado et al., 2008; Thadeo et al., 2008)). In contrast, detailed studies of nectaries in the ferns are relatively rare. Early studies include a pioneer description of glands in Pteridium (Darwin, 1877). Another early study reported the presence of nectaries in Angiopteris and in two species of the Cyathea group of tree ferns (Bonnier, 1879), but provided little detail of anatomical structure. Over the many years of subsequent research additional examples of ferns with foliar nectaries have been added to the list: Platycerium (Dummer, 1911); the Aglaomorpha and Drynaria group (Luttge, 1971; Zamora and Vargas, 1974; Potes, 2010); Polybotrya and Pleopeltis (as Polypodium) (Koptur, 1982; Koptur et al., 1998).

As in many studies of angiosperm extrafloral nectaries, research on fern nectaries has focused on the composition of the exudate (e.g., Koptur et al., 1982) and the interaction between the plants and nectar-feeding ants (Tempel, 1983; Rashbrook et al., 1992; Koptur et al., 1998). Few of these fern nectaries have been described anatomically, with the notable exception of those of Pteridium, which have been described in ultrastructural detail (Power and Skog, 1987; Rumpf et al., 1994). Most recently the anatomy of nectaries of Aglaomorpha and Drynaria was described (Potes, 2010).

After the initial early report of nectaries in Cyathea species (e.g., Bonnier, 1879), more than a century elapsed before the next significant notice of their existence. However, some careful descriptions of new Cyathea species described recently do refer to aerophores, and to "dark circular or oblong patches", as well as to nodules present at the bases of pinnae (Moran, 1991). Additionally, there are examples of structures at the pinna bases that are illustrated for the new species, but not described in the text (Moran, 1991; 1995). More recently, in the description of a new species of Cyathea, C. planadae, the presence of distinctive pads of tissue on the fronds and an association of these areas with feeding activity by ants was described (Arens and Smith, 1998). The discussion here, as with Cnemidaria (Mickel and Beitel, 1988), focused on these areas as being associated with aerophores and on their possibly being glandular.

In the recent description of a new species of Cyathea in Bolivia, Cyathea dintelmannii, reference is made to "...a conspicuous black spot..." at the termination of the pinna with the rachis of the leaves and to "... one black (when dried) glutinous spot..." at that location (Lehnert, 2006). This ... "black spot can be regarded as homologue [sic] with the nectaries found in Cyathea planadae ... where an interaction between the fern and ants has been documented." (Arens and Smith, 1998; Lehnert, 2006).

Our examination of numerous species of Cyathea in the field, as liquid-preserved material and as dried herbarium specimens, confirms that these pinna-base glands in fact characterize a large group of species within the genus. We describe the anatomy of the glands, which differs from previously described nectaries in other ferns. Comparisons of the anatomical results with recent analyses of tree fern phylogeny may help elucidate the evolutionary origin of nectaries in the tree ferns.

MATERIALS AND METHODS

The anatomy of the glands was examined in the Cyathea species listed in Table 1. In addition, the following non-Cyathea species were examined: Sphaeropteris cooperi (W.J. Hooker ex F. von Mueller) Tryon, S. medullaris (G. Forster) Bernhardi, Alsophila firma (Baker) Conant, and A. polystichoides Christ.

All vouchers are deposited in the Duke University Herbarium [DUKE] unless otherwise noted, e.g., Museo National de Costa Rica [CR], University of California [UC] and Lyndon State College Herbarium [LSC].

In addition to the anatomical study of preserved materials, a survey was made of herbarium collections (UC, DUKE and CR), based on which the presence or absence of glands was described for 161 species of Cyathea. This represents a large proportion of the total number of Cyathea species, which has been estimated to be between ca. 200 (Lehnert, 2011b) and 270 species (based on Tryon, 1970). The latter number includes Tryon's estimated totals for Cyathea, Trichipteris, and Cnemidaria, and those Cyathea species he had assigned to Sphaeropteris and Alsophila. It also includes the species formerly classified as Hymenophyllopsis. Recent phylogenetic studies indicate that these groups are nested within Cyathea (Smith et al., 2006; Smith et al., 2008).

In order to study the anatomy of the glands, expanding crosiers and frond axes were preserved in formalin-acetic-acid-alcohol (FAA). Samples were processed through a tertiary butyl alcohol dehydration series, embedded and sectioned in paraffin, and stained with safranin, fast green and iron hematoxylin (Johansen, 1940). In addition, fragments of dried herbarium specimens were rehydrated, embedded and sectioned.

Limited field observations were made of Cyathea mutica, C. choricarpa, C. multiflora, C. delgadii, C. trichiata and C. poeppigii. Fronds of these species were examined for the presence of glands, liquid drops and ants.

RESULTS

Foliar glands in Cyathea spp. occur on the abaxial surface of the frond axes at the bases of the pinnae near their points of attachment to the rachis (Figs. 1 and 2). In most species with pinna-base glands, anatomically similar but much smaller glands occur on the bases of the pinnule stalks (Fig. 3).

The characteristic anatomy of the pinna axis immediately distal to the gland is histologically similar in the main stipe and rachis: there is an epidermis which bears trichomes and small scales, a few-seriate parenchymatous outer hypodermis and an inner hypodermis of elongate fiber-like sclerified cells. The anatomy of the leaf glands described below is distinctly different: no scales or hairs occur on the gland, and the cells of the gland are organized in characteristically distinct zones, which are absent in the non glandular regions.

No vascular bundles extend to or into the glands, and adjacent vascular strands of the nearest parts of the rachis and pinna lack any obvious modifications.

This review of the anatomical diversity of the glands among the tree ferns that were studied suggests three broad categories of glands, which have been designated the Cyathea delgadii (Type I), Cyathea multiflora (Type II) and Cyathea trichiata (Type III) types as exemplified by these species (Table 2). In addition, there are Cyathea species that lack glands.

Cyathea delgadii (Type I)

The most commonly occurring anatomical "type" of gland among the species of Cyathea we studied is represented by Cyathea delgadii.

Organography.--The pinna bases in croziers and young fronds bear a prominent rounded green waxy-appearing gland (Figs. 2 and 4). The gland in mature leaves is less prominent (Fig. 5). An aerophore is adjacent to the gland, is oval in shape and proximal to the gland on the pinna base.

[FIGURES 1-6 OMITTED]

An unusual feature seen only in Cyathea delgadii among the species we surveyed is an asymmetric distribution of unusually prominent glands on the pinnule bases along the pinnae. These are restricted to the distal region of each pinna and occur only on the pinnules of the acroscopic side of the pinna.

Anatomy.--Glands are prominently raised above the surrounding leaf surface (Figs. 2 and 4), and histological sections reveal that four main zones of cells compose the gland (Fig. 6). The epidermis of the gland is composed of a single layer of densely-staining anticlinally elongate cells. A thick cuticle covers the surface of the gland; no stomates are present, and scales and trichomes are absent. Subjacent to this layer is a discrete subepidermal zone of parenchyma which is 3-6 cells seriate. These cells are more or less isodiametric in shape and highly vacuolated. They are larger than the epidermal cells but smaller than the parenchyma cells which characterize the parenchyma tissue of the leaf axis. Subjacent to this zone of parenchyma is a zone of transversely- elongate cells which are usually densely stained, with granular cytoplasm. This tanniniferous layer is laterally continuous with the hypodermal fibrous layer of the pinna axis and rachis. Finally, subjacent to this tanniniferous zone is a zone of ground tissue parenchyma similar to the subjacent cortical ground tissue of the leaf axis.

Adjacent aerophores have numerous stomates and prominent intercellular spaces.

Numerous Cyathea species, including those formerly named Cnemidaria (see below), which were seen to have glands histologically similar to those of Cyathea delgadii include Cyathea borinquena (Fig. 7), C.caracasana, (Fig. 8), C. decomposita (Fig. 9), C. divergens (Fig. 10), C. furfuracea (Fig. 11), C. senilis (Fig. 12), C. squamata (Fig. 13), C. tenera (Figs 14 and 15). Other species included in the anatomical survey with Type I glands include C. barringtonia, C. fulva, C. gibbosa, C. horrida, C. planadeae, C. pungens, C. schiedeana, C. squamulosa and C. suprastrigosa.

Cyathea choricarpa (formerly Cnemidaria) (Type I)

Material was examined originally as Cnemidaria species. These have now been incorporated into Cyathea (Korall et al., 2007; Lehnert, 2011a). The anatomy of the glands, which is similar to that which characterizes most Cyathea species, is consistent with this.

Organography.--Glands in this species are recognized as bulbous waxy regions on the abaxial side of the leaflet base (Figs. 1 and 16). A bulge is present in young leaf material, but it is not as prominent in mature leaves. The gland tends to be somewhat elongate along the pinna base. A small aerophore is located immediately proximal to each gland.

Anatomy.--The epidermis of the gland is a single layer of anticlinally-elongate cells which are slightly larger than the cells which characterize the epidermis adjacent to the gland (Fig. 17). Subjacent to the secretory epidermis is a zone of isodiametric parenchyma cells 6-10 cell layers deep. There is a gradation of cell size in this zone. The cells of the 3-4 layers immediately subjacent to the epidermis are smaller and more compact than the cells of the more internal layers. Immediately subjacent to this subepidermal parenchymatous zone is a zone composed of 10-12 layers of thick-walled cells. This zone is laterally continuous with the fibrous hypodermal layer of the pinna and rachis.

[FIGURES 7-12 OMITTED]

[FIGURES 13-18 OMITTED]

The aerophore immediately adjacent to each gland (Fig. 16) has numerous stomata and prominent airspaces.

Three other species of Cyathea (formerly Cnemidaria) with gland anatomy similar to that of Cyathea choricarpa included in this survey are C. cocleana, C. horrida, and C. mutica.

Cyathea multiflora (Type II)

This species is characterized by the most structurally elaborate foliar glands seen in this study.

Organography.--A prominent bright green gland occurs on each pinna base on fresh croziers and expanding fronds. The glands appear as rounded or bulging, shiny, glabrous patches on the abaxial surface of the pinna base immediately distal on the pinna to its junction with the rachis (Fig. 3). Pinnule bases of this species have much smaller glands (Fig. 3), which have anatomy similar to that of the larger glands on the pinna. This is also true, for example for Cyathea tenera (Fig. 14). As in the other species of Cyathea, the glands on more mature and expanded fronds appear less prominent (Fig. 18).

In addition to the gland, there is a distinctive aerophore which tends to be a relatively small oval patch adjacent to the gland at its border with the rachis (Fig. 3; Fig. 18).

Anatomy.--The epidermal layer of the gland consists of a region of narrow anticlinally-elongate cells with densely staining cytoplasm and a thick cuticle. These cells are characterized by having prominent large nuclei and dense granular cytoplasm with small vacuoles (Fig. 20). Many of the cells in this epidermal layer are subdivided by periclinal cross walls, so that the palisade-like glandular epidermis varies locally from 1-seriate to 2-seriate. Stomata, trichomes and scales are absent. Immediately subjacent to this characteristic epidermis, is a 1- to 2seriate zone of rounded isodiametric cells that are distinctly larger and lighter-staining than cells of surrounding layers (Figs. 19 and 20). Subjacent to this subepidermal zone, the fiber layer characteristic of the non-glandular area is interrupted. In place of hypodermal fibers, multiple layers of parenchyma cells compose a zone of cells which are smaller and more densely staining than those of the parenchymatous zone subjacent to the secretory epidermis (Fig. 19). This inner parenchymatous zone forms most of the characteristic bulge of the gland. Finally this latter zone is subtended by several layers of tanniniferous-staining cells which are similar to, and continuous with, the ground tissue of the pinna axis (Fig. 19).

Characteristic aerophores adjacent to each gland (Figs. 3 and 18) have numerous stomata and prominent air spaces.

Species in this survey characterized by gland anatomy similar to Cyathea multiflora include Cyathea acutidens (Fig. 21) and Cyathea andina (Fig. 22).

Cyathea trichiata (Type III)

Organography.--There is no prominently elevated glandular bulge in this species, but the glandular area is recognizable as an irregularly-shaped area of the epidermis at the pinna base which lacks trichomes and scales (Fig. 23). An aerophore is associated with the pinna base, and is clearly separate from the gland. Small amounts of a liquid secretion were observed on glands in field observations of this species.

[FIGURES 19-24 OMITTED]

Anatomy.--The epidermis of the gland is composed of one or two rows of cells which are anticlinally elongate and larger than the cells of the single layered epidermis of the pinna adjacent to the gland (Figs. 24 and 25). The secretory epidermis has a thick cuticle, and the area has no stomata, hairs or scales. Subjacent to the epidermis is a one- to three-layered zone of isodiametric, highly vacuolated parenchyma cells. Finally, subjacent to this subepidermal zone is a multi-layered zone of densely-staining fiber cells. These cells are longitudinally elongate with respect to the pinna axis and are continuous with, though somewhat less elongate than, the fibrous layer which is characteristic of the main axis and rachis (Fig. 25). Unlike the other gland types, there is no interruption of the fibrous layer below the gland. Also, there is no extensive inner parenchymatous zone and consequently the glands are not elevated or bulging.

The characteristic aerophore has numerous stomata and prominent airspaces.

Cyathea armata (Fig. 26) has glands similar to those of Cyathea trichiata.

Cyathea Species Lacking Glands

The anatomical survey revealed that the following Cyathea species lack glands: Cyathea alata, C. arborea, C. costaricensis, C. parvula, and C. poeppigii. The survey of herbarium specimens confirmed the lack of glands in these species, and in addition noted the lack of glands in several other species (Table 3).

No glands were observed on the species which were examined of Alsophila (e.g., Alsophila firma and A. polystichoides) and Gymnosphaera. The species of Sphaeropteris that were examined anatomically (Sphaeropteris cooperi, and S. medullaris) also lacked glands. However, observations of herbarium specimens suggest that glands similar to those of Cyathea spp. may be present in Sphaeropteris robinsonii (Copel.) R. M. Tryon of the Philippines, and possibly in a few other Sphaeropteris species. Except for S. robinsonii, observations of herbarium specimens of numerous species of the other Cyatheaceous genera indicate a general lack of glands throughout Cyatheaceae other than in Cyathea.

Field observations have so far provided few data in regard to the function of the putative pinna-base nectaries in Cyathea species. In the Cyathea multiflora and C. delgadii types, the glands are large and bright green in young expanding leaves (Fig. 3; Fig. 2), but much less conspicuous in mature leaves (Fig. 18; Fig. 5). Despite their prominence, the glands on young fronds of both these species were never observed to be wet with secretions when closely examined in the field. However, small droplets of liquid were observed on the pinna-base glands of young expanded fronds of Cyathea choricarpa, and small amounts of secreted liquid were consistently present on glands of Cyathea trichiata, both in the field and in the greenhouse. A small number of ants was observed on fronds of some plants of Cyathea choricarpa, but ants were not observed visiting the glands. Gland surfaces in some species (e.g. C. acutidens, Fig. 27; C. multiflora, Fig. 28) were frequently observed to be damaged and scarred, possibly due to feeding by ants or other insects. The glands of Cyathea acutidens were heavily damaged in this way, including the small pinnule-base glands.

[FIGURES 25-30 OMITTED]

The review of selected herbarium sheets indicates that indeed glands can be identified on the dried leaves of Cyathea species. These structures appear as dark, often shiny and shriveled spots, and are located where glands are seen to occur in live plants (Cyathea delgadii, Fig. 29; C. multiflora, Fig. 30; Cyathea horrida, Fig. 31). Some of these spots appear to have visible surface deposits of dried secretion, and others appear to be sticky, with spores and sporangia attached to the gland areas (e.g., Cyathea cocleana (Fig. 32).

Table 3 summarizes our herbarium survey of Cyathea foliar glands. For each species cited, a single representative specimen is listed. The four species we examined of Old World Cyatheas (the Cyathea decurrens group) lack glands. Among the New World species surveyed, there were five species which were observed to lack glands, in addition to six glandless species formerly members of the genus Hymenophyllopsis. Glands were observed to be present in specimens of the remaining 146 Cyathea species surveyed.

Where species were included in both the anatomical survey and the herbarium survey, the observations are consistent. Of the 15 Cyathea species in the herbarium survey that lack nectaries, the absence of glands was confirmed anatomically for five of them. Similarly, of the 146 gland-bearing species in the herbarium survey, the glands were studied anatomically for 25 species.

DISCUSSION

The anatomy of the foliar glands in the species of Cyathea which were examined is distinctly different from the foliar nectaries that have been previously described for a few other species of ferns (e.g., Bonnier, 1879; Power and Skog, 1967; Potes, 2010). We have identified three distinctive anatomical features which characterize Cyathea glands: (1) the cells of the epidermis of the gland can be distinguished from the epidermal cells adjacent to the glands. The secretory epidermal cells of the gland are densely staining, anticlinally elongate, have a thick cuticle, and scales, scurf and trichomes are absent; (2) subjacent to the epidermis there is a subepidermal zone of a few to several layers of larger more highly vacuolated parenchyma cells; and (3) subjacent to this latter zone is an inner zone of parenchyma and an interruption of the fibrous hypodermal zone (except for Type III) characteristic of adjacent areas of the pinna axis and rachis. We have observed no modification or specialization of vascular tissue associated with nectaries in any Cyathea species.

[FIGURES 31-32 OMITTED]

The glands of the Cyathea species we reviewed can be organized into three general groups. This characterization of gland "types" is not intended to be rigid, however. The detailed anatomical structure of the glands in Cyathea varies from the more standard and general form which is widely distributed among the species we examined (Type I) to a more elaborate and distinctive type found in only a few species (Type II), to a form which is far less elaborate in anatomy compared to the other types, with less modified epidermal cells and fewer cells composing the subjacent parenchyma zones. These most simple glands are not associated with an interruption of the fibrous layer, and do not form an elevated bulge on the leaf surface (Type III).

The presence of nectaries varies among the species in Cyathea. As noted, in addition to species with nectaries, there are Cyathea species which lack them. The presence and absence of glands among species of a given genus has been reported in other genera (e.g., Pleopeltis as Polypodium: P. plesiosorus Kunze and P. furfuraceum Schltdl. & Cham. lack glands (Koptur et at., 1998). In this survey, as noted earlier, Alsophila and Gymnosphaera consistently lack glands. Although nearly all species of Sphaeropteris we examined lacked glands, a very few species appear to have them (e.g., S. robinsonii).

Based on these results compared with recent phylogenetic analyses, the presence and structure of the foliar glands appear to have potential value as markers of major clades within Cyathea. The members of the earliest diverging branch of the genus, the Old World Cyathea decurrens group (e.g., Conant et al., 1995, 1996; Korall et al., 2007; Janssen et al., 2008; Bystriakova et al., 2011), lack these glands, as do the other genera of Cyatheaceae (viz. Alsophila, Gymnosphaera and some species of Sphaeropteris). Within another early branch of the Cyathea clade, which includes the C. armata group of Korall et al. (2007), several species were observed to lack glands, including C. arborea, C. parvula and C. poeppigii. However, within this group there is a distinctive sub-group, the Trichipteris armata group of Barrington (1978) and Gastony (1979), including C. armata, C. trichiata, C. stipularis and C. nesiotica, which do have glands. It is noteworthy that the glands of C. armata and C. trichiata are of the simplest anatomical type we have seen (Type III).

A large clade of New World Cyathea species comprising the Cnemidaria group, the Cyathea gibbosa group, and the Cyathea divergens group (sensu Conant et al., 1995, 1996; Korall et al., 2007) includes most species of this genus. The members of this large group that we have examined all possess well-developed foliar glands of Type I or Type II. Although we made only a modest anatomical survey of species, the review of herbarium specimens has identified the presence of foliar glands in numerous other species of Cyathea throughout these groups. Thus, these more elaborate, more prominent foliar glands appear to be a shared derived characteristic which marks the largest clade within New World Cyathea.

The presence of the group of Cyathea species with Type III glands (e.g., C. armata, C. trichiata, and C. stipularis) within a clade that otherwise lacks glands (e.g., C. arborea, C. parvula and C. poeppigii) is problematic. Possible explanations include: (1) the common ancestor of this clade with the Cnemidaria-C. gibbosa-C. divergens group had glands, and the glandless C. armata group members have lost glands; (2) the C. armata/ C. trichiata gland-bearing subgroup represents an independent, parallel or convergent origin of glands; or (3) it is possible that an ancient hybridization between an ancestor of the C. armata/ C. trichiata species group and an early member of the gland-bearing Cnemidaria-C. gibbosa-C. divergens group would explain the presence of glands in this group. The glandless Cyathea arborea is known to form hybrids with different gland-bearing Cyathea species today (Conant, 1975; Caluff, 2002). Early members of the two groups might similarly have been able to hybridize.

The group of Cyathea species that was formerly considered the genus Hymenophyllopsis has recently been reclassified as subgenus Hymenophyllopsis of Cyathea (Christenhusz, 2009). This group has been weakly supported as the sister group to all other New World Cyathea species (Korall et al., 2007), or sister to a large group corresponding to the Cnemidaria-C. gibbosa-C. divergens group (Janssen et al., 2008; Bystriakova et al., 2011). The observed lack of pinna-base glands in Cyathea (Hymenophyllopsis) dejecta may be consistent with either position. On the other hand, the absence of glands might be expected from its great reduction in size and complexity, even if Hymenophyllopsis was derived from gland-bearing Cyathea ancestors.

The presence of nectaries marks a large group of Cyathea species and the shared presence of nectaries helps unify the group which contains most New World Cyathea species. This includes the species formerly included in the genus Cnemidaria (Korall et al., 2007; Lehnert, 2011a), Trichipteris (Lellinger, 1987) and a group of Cyathea species formerly included in Sphaeropteris (Tryon, 1970; Windisch, 1977, 1978).

The comparatively simple morphology and anatomy of the glands in the C.armata/C. trichiata group may well represent the most primitive state of the gland seen in extant gland-bearing Cyathea.

As mentioned earlier, although all the Sphaeropteris species we examined anatomically lack glands, herbarium specimens of S. robinsonii of the Phillipines (e.g., Ramos & Edano, Bureau of Sci. 47350 [UC]) do have dark areas similar in appearance and position to the pinna-base glands of Cyathea species. An anatomical examination of this and related Sphaeropteris species is needed. If pinna-base nectaries are indeed present in this one or a few Sphaeropteris species, most likely they will have evolved independently from the Cyathea nectaries reported here.

In previous tree fern literature, reference is made to observations of glands and aerophores at the base of fern pinnae. Ants have been observed on "glabrous pads at the base of primary pinnae" (Arens and Smith, 1998), "swollen dark glossy aerophores" have been described (Holttum and Edwards, 1983), dark spots have been observed on herbarium specimens (Arens and Smith, 1998) and reference has been made to the need to clarify "the dark spots at the base of each pinna ... regarding its fundamental origin as a possible nectary or aerophore" (Mickel and Beitel, 1988; Mickel and Smith, 2004; Lehnert, 2006).

It is clear that there has been some confusion in the literature in distinguishing between pinna-base glands and aerophores. Our observations confirm that these glands have a distinctive anatomy and that they exist as structures independent of the adjacent aerophores. Functionally, they have been shown to have exudate of interest to ants (Arens and Smith, 1998), and to have fungi associated with them, reflecting the likely presence of sugary exudate. The dark spots on herbarium specimens have been useful in identifying the presence and location of nectaries. All of this is to say that careful observations are necessary in order to describe the presence of nectaries and to distinguish these from aerophores.

Field observations have so far provided few data in regard to the function of the pinna-base glands in Cyathea species. In Cyathea multiflora, and C. delgadii, the glands are large and bright green in young expanding leaves, but much less conspicuous in mature leaves. Despite their prominence, the glands on young fronds of both these species were never observed to be wet with secretions when examined closely in the field. Cyathea leaf glands are not vascularized, and this may explain the very low secretion rates that we observed. However, droplets of liquid were observed on the pinna-base glands of young expanded fronds of Cyathea choricarpa, and small amounts of secreted liquid were consistently present on glands of Cyathea trichiata, both in the field and in the greenhouse. A small number of ants was observed on the fronds of some plants of Cyathea choricarpa, but were not observed in association with the glands. The surfaces of glands in some species, for example in Cyathea acutidens, were frequently observed to be damaged and scarred, possibly due to feeding by ants or other insects.

On the basis of these anatomical studies, their location on the leaves, and the modest observations of droplets, and insect activity, we have concluded that these glands are indeed nectaries. In support of this conclusion there is an obvious need for more extensive field observations and greenhouse studies as well as chemical analyses of the exudate. The presence or absence of glands and the variation in gland anatomy may well be useful as markers in analyses of species relationships within a genus and among fern families. A broader survey of the presence or absence of fern glands, their distribution and their anatomical structure is fully warranted.

ACKNOWLEDGMENTS

We thank the following people for their advice, materials and technical assistance: David Conant, Marcus Lehnert, Robin Moran, Kathleen Pryer, Amber Ratchford, and Alan Smith. We also acknowledge the support of the herbarium curators of CR, DUKE, LSC and UC.

LITERATURE CITED

AGRAWAL, A. A. 2011. Current trends in evolutionary ecology of plant defences. Functional Ecology 25:420-432.

ARENS, N. C. and A. R. SMITH. 1998. Cyathea planadae, a remarkable new creeping tree fern from Colombia, South America. Amer. Fern J. 88:49-59.

BARRINGTON, D. S. 1978. A Revision of the Genus Trichipteris. Contrib. Gray Herbarium. Harvard Univ. 208:3-93.

BENTLEY, B. L. 1977. Extrafloral nectaries and protection by pugnacious bodyguards. Ann. Rev. Ecol. Syst. 8:407-427.

BENTLEY, B. L. and T. ELIAS. (eds). 1983. The Biology of Nectaries. Columbia Univ. Press, N.Y.

BONNIER, G. 1879. Les nectaries: etude critique, anatomique et physiologique. Ann. Sci. Nat. [Ser. VI] 8:5-212.

BYSTRIAKOVA, N., H. SCHNEIDER and D. COOMES. 2011. Evolution of the climatic niche in scaly tree ferns (Cyatheaceae, Polypodopsida). Bot. J. Linn. Soc. 165:1-19.

CALUFF, M. G. 2002. xCyathidaria, a new nothogenus in the Cyatheaceae (Pteridophyta). Willdenowia 32:281-283.

CHRISTENHUSZ, M. J. M. 2009. New combinations and an overview of Cyathea subg. Hymenophyllopsis (Cyatheaceae). Phytotaxa 1:37-42.

CONANT, D. S. 1975. Hybrids in American Cyatheaceae. Rhodora 77:441-455.

CONANT, D. S., L. A. RAUBESON, D. K. ATTWOOD and D. B. STEIN. 1995. The relationships of Papuasian Cyatheaceae to New World tree ferns. Amer. Fern J. 85:328-340.

CONANT, D. S., L. A. RAUBESON, D. K. ATTWOOD, S. PERERA, E. A. ZIMMER, J. A. SWEERE and D. B. STEIN. 1996. Phylogenetic and evolutionary implications of combined analysis of DNA and morphology in the Cyatheaceae. Pp. 231-248, in Pteridology in Perspective, J. M. Camus, M. Gibby and R. J. Johns, eds, Royal Botanic Gardens, Kew.

DARWIN, F. 1877. On the nectar-glands of the common brakefern. J. Linn. Soc. Bot. 15:407-409.

DUMMER, R. 1911. Grape sugar as an excretion in Platycerium. Ann. Bot. 25:1205-1206.

DURKEE, L. T. 1987. Ultrastructure of extrafloral nectaries in Aphelandra spp. (Acanthaceae). Proc. Iowa. Acad. Sci. 94:78-83.

ELIAS, T. S. 1983. Extrafloral nectaries: their structure and distribution, Pp. 175-203, in The Biology of Nectaries, B. L. Bentley and T. S. Elias, eds, Columbia University Press, NewYork.

ELIAS, T. S. and SUN AN-CI. 1985. Morphology and anatomy of foliar nectaries and associated leaves in Mallotus (Euphorbiaceae). Aliso 11:17-25.

FAHN, A. 1979. Secretory Tissues in Plants. Academic Press, London; New York.

FREITUS, L., G. BERNARDILLO, L. GALETTO and A. A. S. PAOLI. 2001. Nectaries and reproductive biology in Croton sarcopetalus (Euphorbiaceae). Bot. J. Linn. Soc. 136:267-277.

GASTONY, G. J. 1979. Spore morphology in the Cyatheaceae III. The Genus Trichipteris. Amer. J. Bot. 66:1238-1260.

HOLTTUM, R. E. and P. J. EDWARDS. 1983. The tree ferns of Mount Roraima and neighboring areas of the Guayana Highlands with comments on the family Cyatheaceae. Kew Bull. 38:155-188.

JANSSEN, T., N. BYSTRIAKOVA, F. RAKOTONDRAINIBE, D. COOMES, J. N. LABAT and H. SCHNEIDER. 2008. Neoendemism in Madagascan scaly tree ferns results from recent coincident diversification bursts. Evolution 62:1876-1889.

JOHANSEN, D. A. 1940. Plant Microtechnique. McGraw-Hill Book Co., New York.

KOPTUR, S., A. R. SMITH and I. BAKER. 1982. Nectaries in some neotropical species of Polypodium (Polypodiaceae): Preliminary observations and analyses. Biotropica 14:108-113.

KOPTUR S, 1985. Alternative defenses against herbivores in Inga (Fabaceae,Mimosoideae) over an elevational gradient. Ecology 66:1639-1659.

KOPTUR S, 1992. Extrafloral nectary-mediated interactions between insects and plants. Pp. 81-129, in Insect-Plant Interactions vol. IV, E. A. Bernays, ed, CRC Press, Boca Raton, Fl, USA.

KOPTUR S, V. RICO-GRAY and M. PALACIOS-RIOS. 1998. Ant protection of the nectaried fern Polypodium plebium in central Mexico. Amer. J. Bet. 85:736-739.

KORALL, P., D. S. CONANT, J. S. METZGAR, H. A. SCHNEIDER and K. M. PRYER. 2007. A molecular phylogeny of scaly tree ferns. Amer. J. Bot. 94:873-886.

LEHNERT, M. 2006. The Cyatheaceae and Dicksoniaceae (Pteridophyta) of Bolivia. Brittonia 58:229-244.

LEHNERT, M. 2011a. The Cyatheaceae (Polypodopsida) of Peru. Brittonia 63:11-45.

LEHNERT, M. 2011b. Species of Cyathea in America related to the western Pacific species C. decurrens. Phytotaxa 26:39-59.

LELLINGER, D. B. 1987. The disposition of Trichopteris (Cyatheaceae). Amer.Fern J. 77:90-94.

LUTTGE, V. 1971. Structure and function of plant glands. Ann. Rev.Pl. Physiol. 22:23-44.

MACHADO, S. R., L. P. C. MORELLATO, M. G. SAJO and P. S. OLIVEIRA. 2008. Morphological patterns of extrafloral nectaries in woody plant species of the Brazilian cerrado. Plant Biology 10:660-673.

MARGINSON, R., M. SEDGLEY and R. B. KNOX. 1985. Structure and histochemistry of the extrafloral nectary of Acacia terminalis (Salisb). McBride (Leguminosae, Mimosoideae). Protoplasma. 127:21-30.

MCDADE, L. A. and M. D. TURNER. 1997. Structure and development of bracteal nectary glands in Aphelandra (Acanthaceae). Amer. J. Bot. 84:1-15.

MICKEL, J. T. and J. BEITEL. 1988. Pteridophyte Flora of Oaxaca Mexico. New York Botanical Gardens, New York.

MICKEL, J. T. and A. R. SMITH. 2004. The Pteridophytes of Mexico. Mem. N.Y. Bot Garden 88:216. MORAN, R. C. 1991. Eight new species of tree ferns (Cyathea, Cyatheaceae) from the American tropics and three new combinations. Novon 1:88-104.

MORAN, R. C. 1995. Five new species and two new combinations of ferns (Polypodiopsida) from Ecuador. Nordic Jour. Bot. 15:49-58.

POTES, A. 2010. Comparative anatomy of the nectaries of Agloamorpha and Drynaria (Polypodiaceae). Amer. Fern J. 100:80-92.

POWER, M. S. and J. E. SKOC. 1987. Ultrastructure of the extrafloral nectaries of Pteridium aquilinum. Amer. Fern J. 77:1-15.

RASHBROOK, V. K., S. G. COMPTON and J. H. LAWTON. 1992. Ant-herbivore interactions: reasons for the absence of benefits to a fern with foliar nectaries. Ecology 73:2167-2174.

ROSUMEK, F. B., F. A. O. SILVEIRA, F. D. NEVES, N. P. D. BARBOSA, L. DINIZ, Y. OKI, F. PEZZINI, G. W. FERNANDES and T. CORNELISSEN. 2009. Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537-549.

RUMPF, S. M., M. CROMEY and C. J. WEBB. 1994. Ultrastructure and function of the nectaries of New Zealand bracken (Pteridium esculentum (Forst. f.) Cockayne). New Zealand J. Bot. 32:487-496.

SMITH, A. R., K. M. PRYER, E. SCHUETTPELZ, P. KORALL, H. SCHNEIDER and P. G. WOLF. 2006. A classification for extant ferns, Taxon 55:705-731.

SMITH, A. R., K. M. PRYER, E. SCHUETTPELZ, P. KORALL, H. SCHNEIDER and P. WOLF. 2008. Fern Classification. Pp. 417-467, in Biological Evolution of Ferns and Lycophytes, T. A. Ranker and C. H. Haufler, eds, Cambridge Univ. Press, New York.

TEMPEL, A. S. 1983. Bracken fern (Pteridium aquilinum) and nectar-feeding ants: a non-mutualistic interaction. Ecology 64:1411-1422.

THADEO, M., M. F. CASSINO, N. H. VITARELLI, A. A. AZEVEDO, J. M. ARAUJO, V. M. M. VALENTE and R. M. S. A. MEIRA. 2008. Anatomical and histochemical characterization of extrafloral nectaries of Prockia crucis (Salicaceae). Amer. J. Bot. 95:1515-1522.

TRYON, R. M. 1970. The classification of the Cyatheaceae. Contrib. from the Gray Herb. 200:3-50.

WINDISCH, P. G. 1977. Synopsis of the genus Sphaeropteris with a revision of the neotropical exindusiate species. Bot. Jahr. fur Systematic Pflanzengeschicte und Pflanzengeographie 92:176-198.

WINDISCH, P. G. 1978. The systematics of the group of Sphaeropteris hirsuta (Cyatheaceae). In The Botany of the Guayana Highland, B. Maguire, ed. Mem. N.Y. Bot. Gard. 29:2-22.

ZAMORA, P. M. and N. S. VARGA. 1974. Nectary-costule association in Philippine drynarioid ferns. The Philipp. Agric. 57:72-88.

ZIMMERMAN, J. 1932. Uber die extrafloralen Nektarien der Angiospermen. Beih. Bot. Zentralbl. 49:99-196.

RICHARD A. WHITE * and MELVIN D. TURNER Department of Biology, Duke University, P.O. Box 90338, Durham NC 27708

* Corresponding author

TABLE 1. Cyathea species included in the anatomical survey.

Species                             Vouchers

Cyathea acutidens (Christ) Domin    White 200205 [DUKE]
Cyathea alata Copel.                P414; P419 [LSC]
Cyathea andina (H. Karst.) Domin    Conant 4888 [LSC]
Cyathea arborea (L.) Sm.            Conant 4893; Conant 4894 [LSC]
Cyathea armata (Sw.) Domin          Conant 4881 [LSC]
Cyathea barringtonii A.R. Sm. ex    White & Lucansky 1970127 [DUKE]
  Lellinger
Cyathea borinqueno (Maxon) Domin    Conant 4872 [LSC]
Cyathea caracasana (Klotzsch)       Conant 4884 [LSC
  Domin
Cyathea choricarpa (Maxon) Domin    White 200201 [DUKE
Cyathea cocleona (Stolze) Lehnert   Wilbur 11111 [DUKE]
Cyathea costaricensis Domin         McAlpin 1089 [DUKE]
Cyathea decomposita (Karsten)       White 1969238 [DUKE]
  Domin
Cyathea dejecta (Baker) Christenh.  Beitel 8517 [UC]
Cyathea delgadii Sternb.            White 199906 [DUKE]
Cyathea divergens Kunze             Seeder 90-3 [DUKE]
Cyathea fulva (M. Martens &         White 1969226 [DUKE]
  Galeotti) Fee
Cyathea furfuracea Baker            Conant 4880 [LSC]
Cyathea horrido (L.) Sw.            Conant 4873 [LSC]
Cyathea multiflora Sm.              White 199907; White 200207 [DUKE]
Cyathea mutica (H. Christ) Domin    White 200204 [DUKE]
Cyathea parvula (Jenman) Domin.     Conant 4885 [LSC]
Cyathea planadae N.C.Arens &        Arens, s.n. [UC]
  A.R.Sm.
Cyathea poeppigii (Hook.) Domin     White 200202 [DUKE]
Cyathea pungens (Willd.) Domin      White 1969224 [DUKE]
Cyathea schiedeana (C. Presl)       White 2002C5 [DUKE]
  Domin
Cyathea senilis (Klotzsch) Domin    White & Lucansky 1969222 [DUKE]
Cyathea squamata (Klotzsch) Domin   White 1970159 [DUKE]
Cyathea squamulosa [I. Losch] R.    White 200203 [DUKE]
  C. Moran
Cyathea suprastrigosa (Christ)      White & Lucansky 1971035 [DUKE]
  Maxon
Cyathea tenera (J. Sm. ex Hook.)    Conant 4869 [LSC]
  T. Moore
Cyathea trichiata (Maxon)           White 199904 [DUKE]

TABLE 2. Summary of anatomical observations, and distribution of gland
types.

Type 1. Cyathea     Gland bulging;            Cyathea barringtonii
  delgadii type       secretory epidermis       A.R. Sm. ex
                      usually a single          Lellinger; Cyathea
                      layer of anticlinally     caracasana (Klotzsch)
                      elongate cells;           Domin; Cyathea
                      modest subepidermal       choricarpa (Maxon)
                      zone; innermost           Domin; Cyathea
                      parenchymatous zone       cocleana (Stolze)
                      prominent; fiber          Lehnert; Cyathea
                      layer interrupted.        decomposita (Karsten)
                                                Domin; Cyathea
                                                delgadii Sternb.;
                                                Cyathea divergens
                                                Kunze; Cyathea fulva
                                                (M. Martens &
                                                Galeotti) Fee;
                                                Cyathea horrida (L.)
                                                Sw.; Cyathea mutica
                                                (H. Christ) Domin;
                                                Cyathea pungens
                                                (Willd.) Domin;
                                                Cyathea schiedeana
                                                (C. Presl) Domin;
                                                Cyathea senilis
                                                (Klotzsch) Domin;
                                                Cyathea squamata
                                                (Klotzsch) Domin;
                                                Cyathea squamulosa
                                                [I. Losch] R. C.
                                                Moran; Cyathea
                                                suprostrigosa
                                                (Christ) Maxon;
                                                Cyathea tenero (J.
                                                Sm. ex Hook.) T.
                                                Moore

Type II. Cyathea    Gland bulging; one or     Cyathea acutidens
  multiflora type     two layered secretory     (Christ) Domin;
                      epidermis of              Cyathea andina (H.
                      anticlinally elongate     Karst.) Domin;
                      cells; distinctive        Cyathea multiflora
                      subepidermal layer;       Sm.
                      inner zone of
                      numerous vacuolated
                      more or less
                      isodiametric
                      parenchyma cells;
                      fiber layer
                      interrupted

Type III. Cyathea   Gland flat (no            Cyathea ormata (Sw.)
  trichiata type      bulge); secretory         Domin; Cyathea
                      epidermis a single        trichiata (Maxon)
                      layer of cells less       Domin
                      anticlinally elongate
                      than the previous two
                      types; subepidermal
                      layer not
                      distinctive; inner
                      parenchymatous zone
                      lacking; fiber layer
                      not interrupted.

Glands lacking        No parenchymatous         Cyathea olata Copel.;
                      bulge; nonsecretory       Cyathea arborea (L.)
                      epidermis with hairs      Sm.; Cyathea
                      and scales present;       costaricensis Domin;
                      hypodermal fibrous        Cyathea parvulo
                      layer not                 (Jenman) Domin;
                      interrupted.              Cyathea poeppigii
                                                (Hook.) Domin;
                                                Alsophila firma
                                                (Baker) D.S.Conant;
                                                Alsophila
                                                polystichoides H.
                                                Christ; Sphaeropteris
                                                cooperi (Hook. ex F.
                                                Muell.) R. Tryon;
                                                Sphaeropteris
                                                medullaris (G.
                                                Forster) Bernhardi.

TABLE 3. Cyathea glands presence/absence based on herbarium survey.

Old World Cyathea species

NO GLANDS:

  Species                            Representative Specimen

    Cyathea alata Copel.             White 1969561 [DUKE]

    Cyathea decurrens Copel.         Muzik 19006 [DUKE]

    Cyathea epaleata (Holttum)       M. L. Grant 4233 [UC]
    Holttum

    Cyathea robertsiana (F.Muell.)   van der Werff & Gray 17037 [UC]
    Domin

New World Cyathea species

NO GLANDS:

  Species                            Representative Specimen

    Cyathea arborea (L.) Sm.         Crosby & Anderson 1044 [DUKE]

    Cyathea costaricensis Domin      Hellwig & Whitaker 1437 [DUKE]

    Cyathea myosuroides (Liebm.)     Mexia 9244 [UC]
    Domin

    Cyathea parvula (Jenman) Domin   Hespenheide 957 [DUKE]

    Cyathea poeppigii (Hook.)        White & Lucansky 1968212 [DUKE]
    Domin

  Formerly Hymenophyllopsis:

    Cyathea asplenioides (A. C.      Maguire & Politti 27764 [UC]
    Sm.) Christenh.

    Cyathea ctenitoides              Wurdack 34175 [UC]
    (Lellinger) Christenh.

    Cyathea dejecta (Baker)          Beitel 8517 [UC]
    Christenh.

    Cyathea hymenophylloides (L.     Maguire 32895 [DUKE]
    D. Gomez) Christenh.

    Cyathea tepuiana Christenh.      Liesner 25302 [UC]

    Cyathea trichomanoides           Beitel 85314 [UC]
    Christenh.

GLANDS PRESENT:

    Cyathea acutidens (Christ)       Stone 2104 [DUKE]
    Domin

    Cyathea alatissima (Stolze)      van der Werff et al. 19540 [UC]
    Lehnert

    Cyathea alfonsiana L. D. Gomez   Trusty 528 [DUKE]

    Cyathea amabilis (C. V.          Meier & Molina 9217 [UC]
    Morton) Lehnert

    Cyathea amazonica R. C. Moran    Ollgard 99065 [UC]

    Cyathea anocampta Alston         White & White 197073 [DUKE]

    Cyathea andicola Domin           Forero et al. 6803 [UC]

    Cyathea andina (H. Karst.)       White & Lucansky 1970150 [DUKE]
    Domin

    Cyathea aristata Domin           Mickel 5935 [UC]

    Cyathea armata (Sw.) Domin       Watt 194 [UC]

    Cyathea aspera (L.) Sw.          Nicolson 1934 [DUKE]

    Cyathea atahuallpa (R.M.         Hutchinson & Wright 6922 [UC]
    Tryon) Lellinger

    Cyathea aterrima (Hook.) Domin   van der Werff et al. 16327 [UC]

    Cyathea atrovirens (Langsd. &    Hatschbach 27670 [UC]
    Fisch.) Domin

    Cyathea austropollescens         Smith, Leon & Young 13134 [DUKE]
    Lehnert

    Cyathea barringtonii A.R. Sm.    White & Lucansky 1970126 [DUKE]
    ex Lellinger

    Cyathea bicrenata Liebm.         Hellwig 302 [DUKE]

    Cyathea bipinnata (R.M.Tryon)    van der Werff, Gray, & Tipas
    R.C.Moran                        12002 [UC]

    Cyathea bipinnatifida (Baker)    Beitel 85102 [UC]
    Domin

    Cyathea boliviana R. M. Tryon    Smith, Quintana & Garcia 13415
                                     [DUKE]

    Cyathea borinquena (Maxon)       Blomquist 11740 [UC]
    Domin

    Cyathea bradei (Windisch)        van der Werff, Vasquez &
    Lellinger                        Jaramillo 10179

    Cyathea brevistipes R. C.        van der Werff & Palacios 9185
    Moran                            [UC]

    Cyathea brunnescens              Moran & Rohrbach 5297 [UC]
    (Barrington) R. C. Moran

    Cyathea caracasana (Klotzsch)    Lehnert 998 [DUKE]
    Domin

    Cnemidaria chocoense Stolze      Lellinger & de la Sota 853 [CR]

    Cyathea choricarpa (Maxon)       Wilbur 27576 [DUKE]
    Domin

    Cyathea cnemidaria Lehnert       Metcalf & Cuatrecasas 30122 [UC]

    Cyathea cocleana (Stolze)        Wilbur 11111 [DUKE]
    Lehnert

    Cyathea columbiana Domin         Rubio, Tipaz & Taicuz 2114 [UC]

    Cyatheo conjugata (Hook.)        White & White 197027 [DUKE]
    Domin

    Cyathea corcovadensis (Raddi)    Mexia 4634 [UC]
    Domin

    Cyathea cyatheoides (Desv.)      Cremers 9834 [DUKE]
    Kramer

    Cyathea decomposita (Karsten)    White & White 1970104 [DUKE]
    Domin

    Cyathea decorota (Maxon) R.M.    Croat & Watt 70293 [UC]
    Tryon

    Cyathea decurrentiloba Domin     Hodel 1466 [UC]

    Cyathea delgadii Sternb.         Stone 2700 [DUKE]

    Cyathea dicromatolepis (Fee)     Brade 8594 [UC]
    Domin

    Cyathea dintelinannii Lehnert    van der Werff et al. 20269 [UC]

    Cyathea dissimilis (C.V.         Liesner & Holst 20435 [UC]
    Morton) Stolze

    Cyathea divergens Kunze          Hellwig 1433 [DUKE]

    Cyathea dudleyi R. M. Tryon      Palacios & van der Werff 3748
                                     [UC]

    Cyathea ebenina H. Karst         van der Werff, et al. 15823 [UC]

    Cyathea ewanii Alston            Schuettpelz 208 [DUKE]

    Cyathea frigida (H. Karst.)      van der Werff & Palacios 9425
    Domin                            [UC]

    Cyathea fulva (M. Martens &      White & Lucansky 1969237 [DUKE]
    Galeotti) Fee

    Cyatheo furfurocea Baker         Hellwig & Whitaker 1472 [DUKE]

    Cyathea gibbosa (Klotzsch)       White & White 197017 [DUKE]
    Domin

    Cyathea gracilis Griseb.         Crosby et al. 316 [DUKE]

    Cyathea grandifolia Willd.       Wilbur 7781 [DUKE]

    Cyathea grayumii A. Rojas        Hodel 1486 [UC]

    Cyathea guentheriana Lehnert     Vargas, et al. 2179 [UC]

    Cyathea hendepiphytica R. C.     van der Werff, Gray & Tipas 11951
    Moran                            [UC]

    Cyathea herzogii Rosenst.        van der Werff et al. 18570 [UC]

    Cyathea hirsuta C. Presl         Mexia 4956 [UC]

    Cyathea horrida (L.) Sw.         White & Lucansky 1970130 [DUKE]

    Cyathea iheringii (Rosenst.)     Brade 9842 [UC]
    Domin

    Cyathea impar R. M. Tryon        Neves, Hammel & Herrera 8529 [UC]

    Cyathea karsteniana (Klotzsch)   Meier et al. 3962 [UC]
    Domin

    Cyathea lasiosora (Kuhn) Domin   van der Werff & Palacios 10320
                                     [DUKE]

    Cyathea lechleri Mett.           Neill et al. 15286 [DUKE]

    Cyathea leucolepismata Alston    Olgaard 99065 [UC]

    Cyathea lindenia C. Presl        van der Werff & Rivero 8761 [UC]

    Cyathea lindigii (Baker) Domin   van der Werff & Ortiz 5681 [UC]

    Cyathea lockwoodiana (P.G.       White & White 197047 [DUKE]
    Windisch) Lellinger

    Cyathea macrocarpa (C. Presl)    Boudrie MB-3024 [UC]
    Domin

    Cyathea mocrosora (Baker)        van der Werff et al. 18171 [UC]
    Domin

    Cyathea marginalis (Klotzsch)    Liesner 19544 [UC]
    Domin

    Cyathea maxonii Underw. ex       Wilbur & Luteyn 18370 [DUKE]
    Maxon

    Cyathea meridensis H. Karst.     Duna & Riina 1469 [UC]

    Cyathea mexiae Copel.            Mexia 5175 [UC]

    Cyathea microdonta (Desv.)       Grayum 3069 [DUKE]
    Domin

    Cyathea moranii Lehnert          Lehnert 1076 [UC]

    Cyathea mucilagina R. C. Moran   van der Werff et al. 13295 [UC]

    Cyathea multiflora Sm.           Wilbur & Luteyn 18252 [DUKE]

    Cyathea mutica (H. Christ)       Lellinger 1281 [DUKE]
    Domin

    Cyathea neblinae A. R. Sm.       Stergios 11892 [UC]

    Cyathea nephele Lehnert          van der Werff, et al. 8562 [UC]

    Cyathea nervosa (Maxon)          Mexia 6291 [UC]
    Lehnert

    Cyathea nesiotica (Maxon)        Trusty 527 [DUKE]
    Domin

    Cyathea nigripes (C. Chr.)       Forero & Jaramillo 5315 [DUKE]
    Domin

    Cyathea nodulifera R. C. Moran   Grayum, Herrera & Santana 7800
                                     [CR]

    Cyathea notabilis Domin          Trusty 533 [DUKE]

    Cyathea obnoxia Lehnert          Lehnert 802 [UC]

    Cyathea onusta Christ            Wilson & Wilson 69-26 [UC]

    Cyatheo oxapampana Lehnert       Mellado & Monteagudo 0464 [UC]

    Cyathea palaciosii R.C. Moran    Neill, et al. 14437 [UC]

    Cyathea ponamensis Domin         Lellinger & de la Sota 374 [CR]

    Cyathea parianensis (P. G.       Meier & Elsner 6647 [UC]
    Windisch) Lellinger

    Cyathea parvifolia Sodiro        van der Werff & Palacios 9185
                                     [UC]

    Cyathea patens H. Karst.         Lehnort 950 [DUKE]

    Cyathea pauciflora (Kuhn)        White & Lucansky 1970125 [DUKE]
    Lellinger

    Cyathea petiolata (Hook.) R.     Croat 4299 [DUKE]
    M. Tryon

    Cyathea phalerata Mart.          White & White 197046 [DUKE]

    Cyathea pilozona Morillo &       Betancur et al. 3213 [UC]
    Murillo

    Cyathea pinnula (H. Christ)      Croat 66590 [DUKE]
    Domin

    Cyathea planadae N.C.Arens &     Palacios & Freine 4988 [UC]
    A.R.Sm.

    Cyathea platylepis (Hook.)       Liesner, Steyermark & Hoist 20873
    Domin                            [UC]

    Cyathea plicata Lehnert          Lehnert 844 [UC]

    Cyathea pseudonanna (L.D.        Moran 4013 [UC]
    Gomez) Lellinger

    Cyathea punctata R.C.Moran &     Lehnert 1581 [UC]
    B. Ollg.

    Cyathea pungens (Willd.) Domin   White & Lucansky 1969224 [DUKE]

    Cyathea purpurea C.V. Morton     Huher 11879 [UC]

    Cyathea roraimensis Domin        Liesner & Stannard 16919 [UC]

    Cyathea rufa (Fee) Lellinger     Rodin 8856 [UC]

    Cyathea ruiziana Klotzsch        van der Werff et al. 21185 [UC]

    Cyathea sagittifolia (Hook.)     Hekking 1438 [DUKE]
    Domin.

    Cyathea schiedeana (C. Presl)    Morton 7588 [DUKE]
    Domin

    Cyathea schlimii (Melt. ex       MacDougal et al. 4023 [UC]
    Kuhn) Domin

    Cyathea senilis (Klotzsch)       White & Lucansky 1969222 [DUKE]
    Domin

    Cyathea serpens (R. M. Tryon)    Mellado & Monteagudo 464 [UC]
    Lehnert

    Cyathea sipapoensis (R.M.        Maguire & Politi 28765 [UC]
    Tryon) Lellinger

    Cyathea speciosa Willd.          White & Lucansky 1969223 [DUKE]

    Cyathea spectabilis (Kunze)      Fendler 25 [UC]
    Domin

    Cyathea squamota (Klotzsch)      White & White 197016 [DUKE]
    Domin

    Cyathea squamipes H. Karst.      Gentry et al. 55093 [UC]

    Cyathea squamulosa [I. Losch]    Wilbur & Stone 8914 [DUKE]
    R. C. Moran

    Cyothea squarrosa (Rosenst)      Brade 405 [UC]
    Domin

    Cyathea stipularis (H. Christ)   Wilbur & Luteyn 18299 [DUKE]
    Domin

    Cyathea stolzei A.R. Sm. ex      Kennedy 2750 [DUKE]
    Lellinger

    Cyathea stromineo H. Karst.      Palacios & Tirado 12952 [UC]

    Cyathea subincisa (Kunze)        Wood 14938 [UC]
    Domin.

    Cyathea suprapilosa Lehnert      Croat 79065 [UC]

    Cyathea suprastrigosa (Christ)   Stone 2023 [DUKE]
    Maxon

    Cyathea surinamensis (Miq.)      McDowell 4225 [DUKE]
    Domin

    Cyathea tenera (J. Sm. ex        Morton 5492 [DUKE]
    Hook.) T. Moore

    Cyathea thelypteroides A. R.     van der Werff, et al. 16323 [UC]
    Smith

    Cyathea thysanolepis             Boom & Weitzman 5825 [UC]
    (Barrington) A. R. Sm.

    Cyathea tortuosa R. C. Moran     van der Werff, et al. 16542 [UC]

    Cyathea trailii (Desv.) K. U.    van der Werff, et al. 19965 [UC]
    Kramer

    Cyathea trichiata (Maxon)        Wilbur & Luteyn 18225 [DUKE]
    Domin

    Cyathea tryonorum (Riba)         White & White 197049 [DUKE]
    Lellinger

    Cyathea tuerckheimii Maxon       Hallberg 1531 [UC]

    Cyathea tungurahuae Sodiro       Wilson et a]. 2770 [UC]

    Cyathea uleana (A. Samp.)        Kessler et al. 7289 [UC]
    Lehnert

    Cyathea ulei (H. Christ) Domin   Anderson 13415 [DUKE]

    Cyathea ursina (Maxon)           Hammel 8710 [DUKE]
    Lellinger

    Cnemidaria varians R. C. Moran   Valdespino & Aranda 139 [UC]

    Cyathea venezuelensis A. R.      Steyermark et al. 21547 [UC]
    Smith

    Cyathea villosa Humb.& Bonpl.    Hatschbach 29880 [UC]
    ex Willd.

    Cyathea weatherbyana (C.V.       Mears & Adsersen 5390 [UC]
    Morton) C.V. Morton

    Cyathea wendlandii (Mett. ex.    White & Lucansky 1968185 [DUKE]
    Kuhn) Domin

    Cyathea weiffii R.C. Moran       van der Werff & Gudino 11386

    Cyathea williamsii (Maxon)       Foster & Kennedy 1878 [DUKE]
    Domin

    Cyathea windischiana A. R.       van der Werff, et al. 16207
    Smith

    Cyathea xenoxyla Lehnert         Kessler et al. 7220 [UC]