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
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.
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.
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.
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.
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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]