8 Phenology and habitat specificity of tropical ferns kl aus mehltreter 8.1 Introduction The focus of this chapter is two aspects of fern sporophyte ecology: phenology and habitat specificity. I define phenology as the study of the periodicity of biological processes caused by intrinsic factors (hormones, circadian clock) or triggered by extrinsic, environmental factors, mainly rainfall, temperature, and photoperiod, or some combination of those elements. Habitat specificity is defined as the biotic and abiotic conditions that favor the development and, consequently, the presence and abundance of fern species on a spatial scale. 8.2 Historical summary Descriptive treatments considering ecological aspects of ferns and lycophytes have been organized geographically (Christ, 1910) and by vegetation types and/or growth forms (Holttum, 1938; Tryon, 1964; Page, 1979a). The latter organization is followed for the two ecological issues treated within this chapter, starting with terrestrial species, followed by rheophytes (fluvial plants), lithophytes (rock plants), epiphytes, and climbers. All other growth forms (e.g., hemiepiphytes, mangrove ferns) are either treated marginally within the nearest group (e.g., tree ferns within terrestrial ferns, mangrove ferns within rheophytes) or omitted because of lack of information. Holttum (1938) observed that ferns and lycophytes are rarely dominant in any plant community. His statement that most vegetation types would not be greatly Biology and Evolution of Ferns and Lycophytes, ed. Tom A. Ranker and Christopher H. Haufler. Published C Cambridge University Press 2008. by Cambridge University Press.  201 202 Klaus Mehltreter modified if all ferns were removed reflects the low importance he accorded ferns in a functional context within tropical forest ecosystems. In fact, we simply do not understand the ecological importance of ferns, because few studies have addressed this issue. Page (1979a) presented an opposite point of view. In his opinion, ferns play an important ecological role in a variety of vegetation types, partly because of their diversity of life forms. Ferns and lycophytes represent about 2–5% of the species diversity of vascular plants. The majority of that diversity is concentrated in the tropics (85%; Tryon, 1964), especially in cloud forests at mid-elevation and on oceanic islands (e.g., Hawaiian Islands, La Réunion Island, Tristan da Cunha; see Chapter 14) where they comprise 16–60% of the flora of vascular plants (Kramer et al., 1995). Holttum (1938) was possibly the first to study the phenology of tropical ferns, because he was aware of the seasonality of several tropical ferns. He stated that Drynaria fortunei is an obligately deciduous epiphyte, which loses its leaves seasonally even under greenhouse conditions. He reported on the coexistence of seasonal (e.g., Platycerium grande) and aseasonal (P. coronarium) fern epiphytes on the Malayan Peninsula. Interestingly, these observations have not been confirmed by more detailed studies. Kornás (1977) observed seasonal phenological patterns of ferns in Zambia and distinguished between species that tolerated the climatic conditions of the dry season and the deciduous species that entered into a dormant stage. Seiler (1981) initiated the first detailed phenological study of a tree fern in El Salvador. He recognized that Alsophila salvinii produced leaves asynchronously during the entire year, but exhibited a strong seasonal emergence of leaves at the start of the rainy season. This somewhat unexpected result was the first to show that seasonal patterns in tropical ferns may occur in spite of the humid conditions at the cloud forest site (2250 mm annual rainfall), apparently because of the drier winter season with less rainfall. However, leaf emergence in spring could be a consequence of rising temperatures or increasing photoperiod, and these hypotheses of correlation between climatic parameters and plant phenology should be tested. Seiler (1981) also used the quotient of mean leaf number (6) and annual leaf production (3) to calculate a mean leaf life span for this species of 2 years. Tanner (1983) identified a correlation between height and age of the tree fern trunk in his study of Alsophila auneae (syn. Cyathea pubescens) in Jamaica. Although the correlation between leaf number and height was significant, leaf production and the number of leaf scars did not correlate well with trunk height and were consequently a poor predictor of trunk age. However, his results confirmed that leaf production was higher after periods of heavy rainfall. These few studies were the starting point for an increasing interest in fern phenology in the 1990s. Phenology and habitat specificity of tropical ferns Holttum (1938) presented some controversial ideas on habitat specificity (also known as habitat preference) based on his observations and the scarce information available in his time. He described dozens of habitat specialists, e.g., Dipteris lobbiana and Tectaria semibipinnata as rheophytes which can tolerate periodic flooding, and Davallia parvula as a trunk epiphyte of mangroves, but also stated that most rock ferns are not specialized to their substrate. Page (1979a) reviewed the apparent habitat specificities of ferns and some of their noteworthy adaptations, but no quantitative data were published until Moran et al. (2003) and Mehltreter et al. (2005). However, tree ferns have been recognized as a specific substrate for epiphytes, especially some species of mosses (Oliver, 1930; Johansson, 1974; Pócs, 1982; Beever, 1984). Based on such observations, it appeared that some epiphytic ferns might have specific host preferences. For example, Oliver (1930) reported that Trichomanes ferrugineum and Crepidomanes venosum from New Zealand grow exclusively on tree ferns, and Copeland (1947) found that Stenochlaena areolaris selectively develops in the leaf axils of Pandanus trees. Rock ferns have been reported to be somewhat habitat specific. For example, Page (1979a) listed Adiantum capillus-veneris, A. philippense, and A. reniforme as limestone ferns and Cheilanthes and Notholaena species as volcanic rock ferns. Today we know that the latter two genera have species with a variety of substrate preferences. 8.3 Review of critical recent advances Although the number of ecological studies of ferns has grown significantly over the last 20 years, few researchers contributed to these advances and consequently the results were restricted to a few sites. Phenological studies were undertaken for dozens of species in Costa Rica (Sharpe and Jernstedt, 1990, 1991; Sharpe, 1993; Bittner and Breckle 1995), Puerto Rico (Sharpe, 1997), Mexico (Mehltreter and Palacios-Rios, 2003; Hernández, 2006; Mehltreter, 2006), Brazil (Schmitt and Windisch, 2005, 2006), Hawaiian Islands (Durand and Goldstein, 2001), Fiji (Ash, 1986, 1987), and Taiwan (Chiou et al., 2001). Most studies focused on tree ferns, with the exception of the mangrove fern Acrostichum danaeifolium (Mehltreter and Palacios-Rios, 2003), the herbaceous forest understory fern Danaea wendlandii (Sharpe and Jernstedt, 1990, 1991; Sharpe, 1993), the climbing fern Lygodium venustum (Mehltreter, 2006), and the rheophyte Thelypteris angustifolia (Sharpe, 1997). The focus of these studies was relating plant age to the correlation between climatic triggers and phenological responses, the measurement of growth rates of leaves and trunks, and the periodicity of leaf production and leaf fertility. 203 204 Klaus Mehltreter 8.3.1 Seasonality in tropical ferns Seasonality or periodicity of growth and reproduction is typical for plants of temperate zones because during the cold winter, soil water freezes and becomes unavailable for plant roots. In tropical environments periodic dry seasons can cause seasonal variation in plant growth, but even without a definite dry season some plants express seasonal phenological patterns because of the periodic appearance of pollinators, animal dispersers, or herbivores. Given that ferns do not interact with pollinators or specialized dispersers (Barrington, 1993), it had been assumed that they would have an aseasonal phenology (Tryon, 1960). Most recent phenological studies of tropical ferns, however, have shown predominantly seasonal patterns (Table 8.1), similar to those of woody angiosperms. In tropical deciduous forests, woody angiosperms are leafless during the dry season and produce a flush of leaves at the end of this period (Rivera et al., 2002) or during the wet season (Lieberman and Lieberman, 1984; Bullock and Solis-Magallanes, 1990). In semideciduous lowland forests, seasonal woody understory plants flush at the beginning of the dry or at the beginning of the wet season (Aide, 1993). In wet tropical climates of montane regions, deciduous trees flush early in the dry season (Williams-Linera, 1997). Although most ferns do not drop their leaves, new leaves are produced mainly during the wet season or rarely earlier at the end of the dry season. Even the evergreen mangrove fern Acrostichum danaeifolium, which stands the entire year with its roots in the water, produces larger leaves and grows faster during the hot rainy summer season, when it produces 1–3 fertile leaves (Mehltreter and Palacios-Rios, 2003). This species has slightly dimorphic leaves, with fertile leaves up to one third larger than sterile leaves and the pinnae of fertile leaves about one third narrower than those of sterile leaves. Leaf dimorphism is generally considered to be a functional adaptation to spore dispersal, with larger fertile leaves favoring wind dispersal of spores (Wagner and Wagner, 1977). If this is true, we might expect fertile leaves to be produced during the dry season, when deciduous canopy species are leafless and wind speeds should be higher. We might also expect that fertile leaves would be shorter lived than sterile leaves because their reduced laminar surface makes them less photosynthetically efficient than sterile leaves. The first hypothesis is probably erroneous, because storms with high winds causing tree falls are frequent during the rainy season (Brokaw, 1996), and may promote spore dispersal. There is some support for the second hypothesis in dimorphic species (Table 8.2), but a larger sample size is needed to test this rigorously. In Cibotium taiwanense, a monomorphic species, fertile leaves have a longer life span than sterile leaves, and shed their spores in the second year after formation (Chiou et al., 2001). The reason for this delay in spore dispersal Phenology and habitat specificity of tropical ferns Table 8.1 Tropical ferns of different vegetation types with seasonal leaf traits; seasonal growth (and leaf production) is more common than seasonal fertility Seasonality of leaf traits Species Life form Growth Fertility Vegetation type Acrostichum danaeifolium7 herbaceous yes yes mangrove Alsophila auneae2 arborescent yes ? cloud forest Alsophila polystichoides4 arborescent yes ? cloud forest Alsophila salvinii1 arborescent yes ? cloud forest Alsophila setosa10 arborescent yes ? lower montane forest Botrychium virginianum8 herbaceous yes yes lower montane forest Cibotium taiwanense6 arborescent no yes subtropical forest Ctenitis melanosticta8 herbaceous yes no lower montane forest Cyathea nigripes4 arborescent yes ? cloud forest Danaea wendlandii3 herbaceous yes yes lowland rain forest Lygodium venustum9 climber yes ? semideciduous forest Pteris orizabae8 herbaceous yes no lower montane forest Pteris quadriaurita8 herbaceous yes no lower montane forest Thelypteris angustifolia5 rheophyte yes no lowland rain forest Woodwardia semicordata8 herbaceous yes no lower montane forest 1 Seiler, 1981; 2 Tanner, 1983; 3 Sharpe, 1993; 4 Bittner and Breckle, 1995; 5 Sharpe, 1997; 6 Chiou et al., 2001; 7 Mehltreter and Palacios-Rios, 2003; 8 Hernández, 2006; 9 Mehltreter, 2006; 10 Schmitt and Windisch, 2006. remains unclear. Production of large fertile leaves may be too costly, causing a decreased rate of sporangial development, or delayed spore release may be considered an adaptation to await better dispersal conditions or improve opportunities for gametophyte development. In monomorphic species, fertile leaves shed their spores earlier but they also have longer life spans than sterile leaves (Table 8.2). This might be a consequence of an ontogenetic effect, when young plants have only sterile leaves and mature plants only fertile leaves, which is typical for Macrothelypteris torresiana (Mehltreter, personal observation). Aseasonal species in the tropics encounter favorable growth conditions throughout the year and are characterized by continuous leaf turnover. Because 205 206 Klaus Mehltreter Table 8.2 Leaf life span in months of monomorphic and dimorphic ferns in ascending order of the life span of fertile leaves Species Danaea Sterile leaves wendlandii1 Acrostichum danaeifolium4 Thelypteris angustifolia2 Macrothelypteris torresiana5 Fertile leaves Dimorphism 39.6 4.0 7.7 4.1 yes yes 11.0 9.6 yes 5.5 14.5 no taiwanense3 16.0 25.0 no Ctenitis melanosticta5 11.5 30.1 no Cibotium 1 Sharpe 2 Sharpe, 3 Chiou and Jernstedt, 1990; Sharpe 1993; 1997; et al., 2001; 4 Mehltreter and Palacios-Rios, 2003; 5 Hernández, 2006. their leaf life span is not restricted by a cold winter or a dry season, it may vary from several months to several years (Westoby et al., 2000). Most terrestrial ferns have mean leaf life spans of 6 months (e.g., Sphaeropteris cooperi; Durand and Goldstein, 2001) to 24 months (e.g., Alsophila salvinii; Seiler, 1981), exceptionally up to 40 months (Table 8.2). Aseasonal epiphytic ferns possess longer leaf life spans between 20 and 30 months (Mehltreter et al., 2006). These longer-lived leaves may invest more in biochemical defenses against herbivores and consequently have a higher specific leaf weight (defined as dry weight per cm2 leaf surface). Terrestrial ferns, especially tree ferns Danaea wendlandii is an herbaceous understory fern growing in the lowland rain forest of Costa Rica. Leaf growth is slow, only 1.6 leaves per year being produced, because of the low light level in the forest understory (Sharpe and Jernstedt, 1990; Sharpe, 1993). However, despite the constantly high humidity within the understory, leaf production and leaf fertility are seasonal, occurring mainly during the wetter summer. Alsophila firma, a Mexican tree fern of the montane forest, is even more seasonal. This species is short-deciduous and surprisingly drops its leaves during the wetter and hotter summer season, replacing them synchronously in one flush after 1–2 months of leaflessness (Mehltreter and Garcia-Franco, in press, Figure 8.1a). Some plants grow up to 50 cm per year (Figure 8.1c, 8.1d). Synchronous leaf production is thought to satiate herbivores during the leaf production peak (Aide, 1993) and may allow for a reduction in the costs of biochemical defense. This explanation seems to apply Phenology and habitat specificity of tropical ferns (a) (b) (c) (d) Figure 8.1 (a, b) Leaf emergence and (c, d) annual trunk growth of Mexican tree ferns. (a) Synchronous emergence of all new crosiers in Alsophila firma. (b) Asynchronous leaf emergence with one new crosier at a time in Cyathea bicrenata. (c, d) Trunk height of a plant of Alsophila firma in (c) May 2005 and (d) June 2006, illustrating an exceptional annual trunk growth of up to 50 cm. 207 208 Klaus Mehltreter to Alsophila firma, because its leaf flush falls in the middle of the wet season when herbivore pressure is very high. At the same site different fern species may follow distinct phenological strategies when these have the same cost benefit. Cyathea bicrenata, another tree fern growing at the same site as A. firma, produces leaves asynchronously throughout the year and considerable herbivore damage has been observed (Mehltreter, personal observation, Figure 8.1b). The cost benefit may be the same for this species, because it saves the costs of storage and recycling of nutrients of seasonal species, perhaps invests in more biochemical defenses, and may compensate for herbivore damage by a stronger continuous growth. Alsophila setosa, another tree fern species of Southern Brazil (Schmitt and Windisch, 2006), seems to be seasonal because of exposure to occasional frost during the winter that damages all older leaves. Plants recover in spring with a strong leaf flush. Rheophytes van Steenis’ (1981, 1987) list of rheophytes includes 40 ferns and two species of Isoëtes. Rheophytes grow on rocks and boulders or along the stream bank, where they are exposed to periodic flooding (van Steenis, 1981). Leaves are often pinnate and possess narrow, long pinnae (e.g., Dipteris lobbiana; Holttum, 1938), which do not resist the water currents when the plant is submersed during periods of flooding. Spores might be expected to be dispersed by both wind and water currents. Only one rheophytic fern has been studied phenologically, Thelypteris angustifolia from a Puerto Rican rain forest (Sharpe, 1997). It has a branching rhizome that can break apart; these pieces can serve as vegetative propagules. Fertility is low, with most plants producing one or no fertile leaves per year. Although it is an evergreen plant primarily found in humid conditions, leaf development occurs mainly in the rainy season. Climbing ferns and epiphytes Phenological patterns vary across different life forms. Climbing ferns must have long-lived leaves to become established in the canopy. In the case of Lygodium venustum, the lamina is replaced after about 1 year, because the same leaf can sprout repeatedly by lateral dormant petiole buds (Mehltreter, 2006). These lateral axes renew the lamina in a way similar to that found for new leaves in woody angiosperms, differing only in that Lygodium venustum has a leaf petiole and rachis that persist rather than the shoot branches. Because there is no secondary stem growth in ferns, all water needs to be transported through the narrow rachis (diameter of 1–2 mm), and consequently collapsed vessels cannot be replaced by new tissues. Ewers et al. (1997) showed that roots of L. venustum hold a positive xylem pressure of up to 66 kPa, which allows refilling Phenology and habitat specificity of tropical ferns of embolized tracheids up to 7 m of plant height. Problems of water conduction within the rhizome may limit the height of most hemi-epiphytic ferns (e.g., Bolbitis and Lomariopsis) to 2–5 m. Epiphytes do not root in the ground, but may have some humus substrate accumulated in tree branches, which allows for nutrient and water storage. However, most epiphytes grow on the bark surface and are exposed directly to daily changes in humidity. During the rainy season they experience strong solar radiation and dryness around midday, but recover quickly with daily rainfall events or the appearance of fog, especially on mountain ridges, and during the night when relative humidity increases. For epiphytes the dry season is more challenging because they cannot rely on water stored within the soil. Species with glabrous, thin textured leaves drop them in response to drying (e.g., Polypodium rhodopleuron). Other epiphytic ferns tolerate the drought, roll their pinnae inwards, exposing the lower scaly leaf surface (e.g., Pleopeltis furfuraceum, Figure 8.2c), or fold their thicker-textured pinnae accordion-like (e.g., Asplenium praemorsum, Figure 8.2d). It is unknown for how long the leaves of these species can remain in this dormant stage and completely recover afterwards. 8.3.2 Habitat specificity Habitat specificities were often reported without any quantitative measurements (Holttum, 1938; Page 1979a, 1979b; Cortez, 2001), with the exception of recent studies on epiphytes (Moran et al., 2003; Mehltreter et al., 2005) and terrestrial species (Poulsen et al., 2006). The role of mycorrhizae in ferns for mediating habitat specificity has been poorly studied. Despite the obligatory mycorrhizae of some fern groups (e.g., Lycopodium, Ophioglossum, Psilotum, Tmesipteris), only facultative mycorrhizae were reported for the sporophytes in a study of Hawaiian ferns (Gemma et al., 1992). Terrestrial species Poulsen et al. (2006) studied the floristic diversity of a plot of 1 ha of lowland Amazonian rain forest in Ecuador with an acidic mean soil pH of 3.33. The distribution and abundance of 29 fern species were correlated with soil calcium and sand content, and to a lesser degree with aluminum content. More studies of this type are needed on ferns at this geographical scale to allow for generalizations; the results of Poulsen et al. (2006) may not be applicable to sites with higher soil pH values, and where the calcium and aluminum contents could be less important to fern distribution. Edaphic niches of Polybotrya spp. in Northwestern Amazonia were best described by differences in soil texture, and cation content (Tuomisto, 2006). 209 210 Klaus Mehltreter (a) (c) (b) (d) Figure 8.2 (a, b) Vegetative reproduction and (c, d) leaf desiccation in some Mexican ferns. (a) Apical leaf buds of Asplenium alatum with young plant rooted in the ground. (b) Asplenium sessilifolium with completely developed plantlet at the leaf tip. (c) Desiccating leaf of Polypodium furfuraceum, bending pinnae inwards, exposing the lower scaly surface. (d) Desiccating leaf of Asplenium praemorsum folding pinnae accordion-like starting at the leaf tip. Mangrove species The three species of mangrove ferns in the genus Acrostichum are exceptionally tolerant to salt stress. They root in the soil and are often flooded, even though never completely submersed. The largest species, A. danaeifolium, is restricted to the Neotropics and is the least salt tolerant (Lloyd and Buckley, 1986; Mehltreter and Palacios-Rios, 2003). The smallest species, A. speciosum, from the Paleotropics seems to be the only obligately halophytic fern species (Kramer et al., 1995). The pantropically distributed A. aureum is ecologically intermediate Phenology and habitat specificity of tropical ferns Table 8.3 Number of species with substrate specificity of four genera of Mexican rock ferns Genus Argyrochosma Limestone Gypsum Igneous rocks No preference 5 0 2 5 Cheilanthes 12 2 11 35 Notholaena 4 2 5 13 Pellaea 2 1 4 7 Data from Mickel and Smith (2004). between the other two species. Other species that may grow in the coastal zones adjacent to the mangroves are Stenochlaena palustris in southeast Asia and Ctenitis maritima on La Réunion Island (Mehltreter, personal observation). Lithophytes Lithophytes (petrophytes) are plants that grow primarily on rocks and boulders. Species that grow on rocks along rivers and stream banks often reproduce vegetatively by apical leaf buds, e.g., Asplenium (Figure 8.2a, 8.2b). Rock ferns are often good indicators for the underlying chemistry of the substrate. For temperate zones, there are dozens of examples of ferns that only grow on igneous rocks (e.g., granite), metamorphic rocks (e.g., serpentine), or sedimentary rocks (e.g., sandstone, gypsum, and limestone). In some genera such as Asplenium these substrate specificities change in newly formed hybrids compared to their parental taxa, e.g. A. adulterinum is restricted to serpentine rocks, although it is the allopolyploid hybrid between calciphilous A. viride and A. trichomanes which grows on silicate rocks (Kramer et al., 1995). Although in tropical humid zones limestone is scarcely found because it erodes quickly, some species are typically restricted to this habitat, especially those in the genera Argyrochosma and Cheilanthes (Table 8.3). Mickel and Smith (2004) report rock substrate specificities for 50 out of 110 species of Argyrochosma, Cheilanthes, Notholaena, and Pellaea with more or less equal proportions occurring on limestone (23 species) or igneous rocks (22 species). Consequently, these species are restricted to mountain ranges with these substrates and may be less common and more frequently endangered than more widespread, substrate-generalist species. Over the last twenty years, some ferns have been reported to hyper-accumulate heavy metals, especially arsenic, cadmium, copper, and zinc (Table 8.4) and, thus, may be good indicators of soil type. Recently, some fern species, especially Athyrium yokoscense (Nishizono et al., 1987) and Pteris vittata (Ma et al., 2001), have been used as phytoremediators to manage heavy-metal contaminated soils. 211 212 Klaus Mehltreter Table 8.4 Heavy metal hyper-accumulating fern species Species Life form Accumulated heavy metals Pityrogramma calomelanos5 terrestrial As Azolla caroliniana6 aquatic Cr, Hg Azolla filiculoides2 aquatic Cd, Cr, Cu, Ni, Zn Marattia spp.3 terrestrial Al Pteris vittata4 terrestrial and lithophytic As Athyrium yokoscense1 terrestrial Cd, Cu, Zn 1 Nishizono 2 Sela 3 Kramer 4 Ma et al., 1987; et al., 1989; et al., 1995; et al., 2001; Barger et al., 2007; 5 Francesconi 6 Bennicelli et al., 2002; et al., 2004. Epiphytes Ferns are the third most species-rich group of epiphytes after orchids and bromeliads in the New World. The three fern families with the greatest number of epiphytic species are Polypodiaceae, Hymenophyllaceae, and Aspleniaceae, all with more than 50% of the family occurring as epiphytes. Vittarioid ferns (Pteridaceae) are entirely epiphytic (Gentry and Dodson, 1987). In comparison to terrestrial ferns, epiphytes must grow in substrates that have a lower nutrient availability and water retention capacity (Benzing, 1990, 1995), and they must cope with large seasonal and daily changes in humidity, as well as an enormous variety of potential hosts (Kramer et al., 1995). Apparent adaptations to prevent water loss include such characteristics as simple or pinnate leaves, thick leaf texture (e.g., Niphidium), an often dense cover of scales (e.g., Polypodium, Elaphoglossum), water storing rhizomes (e.g., Davallia), and leaf succulence together with crassulacean acid metabolism (e.g., Pyrrosia). For humus accumulation and water storage, some ferns have large nest-forming rosettes (e.g., Asplenium) or specific niche-forming leaves (e.g., Drynaria, Platycerium) or leaf bases (e.g., Aglaomorpha). All of the latter group are restricted to the Paleotropics, with the exception of one species of Platycerium (P. andinum) and perhaps Niphidium spp. with large, but morphologically undifferentiated leaves. This nearly complete restriction of humus accumulating fern life forms to the Paleotropics has been interpreted as competitive exclusion by bromeliads, which are absent in the Paleotropics (Kramer et al., 1995). Some other fern species (Solanopteris spp. in the Neotropics, Lecanopteris spp. in the Paleotropics) have ants collecting nutrients for them. These ferns have thick hollow rhizomes that are inhabited Phenology and habitat specificity of tropical ferns by ants. The plants form roots within the interior of the rhizome to take up the nutrients that the ants bring in (Wagner, 1972; Gómez, 1974; Walker, 1986; Gay, 1991). The concentration of gemmae-forming gametophytes in mainly epiphytic groups such as grammitids (Polypodiaceae), Hymenophyllaceae, and vittarioids (Pteridaceae) is often interpreted as an adaptation of epiphytism (Page, 1979b; Farrar, 1990; Dassler and Farrar, 2001). Within the understory of wet tropical forests there is a fairly constant air humidity (i.e., from the base of the trunk to about 3 m above ground). Epiphytic ferns abound as lower trunk epiphytes, especially Hymenophyllaceae, and may be the dominant plant group (Zotz and Büche, 2000; Mehltreter et al., 2005). In the drier and exposed canopy, bromeliads and orchids are apparently better adapted to the extreme changes of temperature and humidity (Johansson, 1974; Kelly, 1985; Benzing, 1990). The first fern epiphytes (e.g., Botryopteris forensis) are known from the Carboniferous, where they grew on marattiaceous tree ferns of the genus Psaronius (Rothwell, 1991). For contemporary epiphytes, three main host groups are available as substrate: tree ferns, gymnosperms (e.g., pines), and woody angiosperms. One species usually found growing on tree ferns is Polyphlebium capillaceum (syn. Trichomanes capillaceum) (Mickel and Beitel, 1988; Moran et al., 2003; Mehltreter et al., 2005; Ebihara et al., 2006; (see Table 8.5, Figure 8.3b). It develops especially on the trunk bases when the tree fern develops its adventitious roots forming a continuous root mantle up to half way to the top. This root mantle has a high water retention capacity and porosity because of its entangled roots, which makes it a favorable substrate for many epiphyte species (Heatwole, 1993; Medeiros et al., 1993; Mehltreter et al., 2005), including recently derived fern clades (e.g., Elaphoglossum, Polypodium) that diversified along with the angiosperms (Schneider et al., 2004). However, most modern epiphytes are not restricted to tree ferns and also grow on a wide range of angiosperm hosts. Nevertheless they may be very abundant on tree fern trunks (Table 8.5), which they can cover entirely, for example Asplenium harpeodes, Blechnum fragile (Figure 8.3c), Elaphoglossum lonchophyllum (Figure 8.3a), and Terpsichore asplenifolia (Figure 8.3a) in Mexican cloud forest (Mehltreter, personal observation). On the other hand, some epiphytic ferns do not occur on tree ferns, perhaps because of the acidic pH and high tannin content of the root mantle (Frei and Dodson, 1972), e.g., Elaphoglossum peltatum (Table 8.5, Figure 8.3d). Another example is Vittaria isoetifolia on La Réunion Island, which is only found on angiosperm trees. Its short rhizome may have problems attaching to the surface of the root mantle or even may be overgrown by the latter. Horizontally extended branches of angiosperm trees allow the large leaves of V. isoetifolia to hang down freely and avoid touching the 213 214 Klaus Mehltreter Table 8.5 Epiphytic ferns with significant host specificities for tree ferns or angiosperm trees in order of their frequency on tree ferns; data are percentages of presence on host trunks Tree ferns Angiosperm trees Elaphoglossum decursivum1 95 30 Blechnum fragile1 90 0 Trichomanes capillaceum2 89 0 Pecluma eurybasis1 65 20 Dryopteris patula1 50 0 Elaphoglossum stenoglossum1 50 10 Blechnum attenuatum3 41 4 Campyloneurum sphenodes1 40 0 elegans1 35 0 Asplenium auriculatum1 35 5 Asplenium serratum1 30 0 Elaphoglossum petiolatum2 29 4 Trichomanes reptans2 18 67 Asplenium nitens3 2 24 Vittaria isoetifolia3 0 16 Elaphoglossum peltatum2 0 19 Hymenophyllum 1 Moran et al., 2003; 2 Mehltreter et al., 2005; 3 Mehltreter, unpublished data from La Réunion Island. vertical trunk surface where they would be exposed to competition with other epiphytes. In conclusion, dozens of epiphytic ferns exhibit host specificity but few are restricted to one host group. Tree ferns are generally a better substrate for trunk epiphytes than angiosperm trees, but there are important exceptions, for which we only have speculative explanations. Specific needs of the gametophyte, the life form of the sporophyte, pH, content of tannins, and structural differences of the root mantle of tree ferns may be involved. Moreover, fern epiphytes specific to angiosperm trees may have been overlooked (Callaway et al., 2002), because these may be restricted to regions where no tree ferns occur. For example, palm trees are especially good substrates when their leaf bases stay attached to the trunk (Zotz and Vollrath, 2003). Their epiphyte communities have been studied mainly in cultivated species. In Costa Rican oil palm fields, Nephrolepis spp. and Phlebodium spp. commonly occur at palm leaf bases (Mehltreter, personal observation). Interestingly, tree fern skirts formed by old leaves that stay attached to the Phenology and habitat specificity of tropical ferns (a) (c) (b) (d) Figure 8.3 Habitat specificities of Mexican trunk epiphytes on tree ferns (a–c) or on angiosperm trees (d). (a) Elaphoglossum lonchophyllum with entire leaves and Terpsichore asplenifolia with pinnate leaves on Alsophila firma. (b) Trichomanes capillaceum on Alsophila firma. (c) Blechnum fragile on the root mantle of Dicksonia sellowiana. (d) Elaphoglossum peltatum on the tree stem of Quercus spp. trunk were found to inhibit the colonization by larger epiphytes and climbers (Page and Brownsey, 1986). 8.4 Synthesis of current perspectives Unexpected phenological patterns suggest that we cannot easily draw general conclusions because of limited observations and little quantitative data. We need more detailed quantitative field data across wider geographical and taxonomic scales to understand the fascinating phenology and habitat requirements of ferns. For horticultural purposes, both issues should be of some 215 216 Klaus Mehltreter concern, when species are known to be difficult to cultivate (for example, grammitids (Polypodiaceae), Hymenophyllaceae, and Gleicheniaceae). For conservation purposes, specific habitat requirements may restrict some fern species geographically, and may be responsible in part for their endangered status. Hyper-accumulators of heavy metals may be more common in ferns than known until recently and can play an important role in the future as bioindicators and for phytoremediation. 8.5 Future goals and directions Within the field of ecological research of ferns and lycophytes, there are at least three areas on which future studies should be focused. (1) (2) (3) Long-term research, especially in the tropics where ferns are most diverse and abundant. Broad-scale studies within a wide range of species at different latitudes, altitudes, and habitats. Multi-disciplinary approaches of ecology, physiology, biochemistry, morphology, systematics, and genetics, which combine molecular methods and field experiments. Whatever approach is selected, quantitative approaches are preferable over observational and merely qualitative studies. Field studies should be comparative or experimental to answer specific questions, for example temperature and soil optima for new species of horticultural interest. 8.6 Importance of long-term studies Most results of phenological studies depend heavily on climatic conditions at the study site during the years of observation. If these have been exceptional, extrapolations and general conclusions cannot be drawn without the risk of committing significant errors. For this reason long-term studies are particularly important. Moreover, for conservation purposes it is critical to document complete life cycles of ferns to improve our understanding of demographic processes (see Chapter 9). Long-term growth measurements allow calculation of the ages of individual plants, and determination of quantified survival rates for better estimations of population turnover, which are fundamental values for conservation management. Our actual understanding of fern phenology is restricted to a few species and even fewer locations. Only studies on a wider geographical scale will allow Phenology and habitat specificity of tropical ferns us to understand, for example, how phenological patterns change within and among species at different latitudes and altitudes. This knowledge is fundamental for addressing future challenges, such as understanding the possible consequences of global warming on ferns. Will tropical fern communities benefit from a warmer climate or will they decline because of a possibly longer dry season? Some species that now produce only one or two fertile leaves per year may discontinue doing so when climatic changes affect their development (Sharpe, 1997; Mehltreter and Palacios-Rios, 2003). Over the long term, this will significantly reduce the reproductive success and increase the chance of extinction of local populations, when these cannot recover from a spore bank. References Aide, T. M. (1993). Patterns of leaf development and herbivory in a tropical understorey community. Ecology, 74, 455–466. Ash, J. (1986). Demography and production of Leptopteris wilkesiana (Osmundaceae), a tropical tree fern from Fiji. Australian Journal of Botany, 34, 207–215. Ash, J. (1987). Demography of Cyathea hornei (Cyatheaceae), a tropical tree-fern from Fiji. Australian Journal of Botany, 35, 331–342. Barger, T. W., Durham, T. J., Andrews, H. T., and Wilson, M. S. (2007). Gametophytic and sporophytic responses of Pteris spp. to arsenic. American Fern Journal, 97, 30–45. Barrington, D. S. (1993). Ecological and historical factors in fern biogeography. Journal of Biogeography, 20, 275–280. Beever, J. E. (1984). Moss epiphytes of tree-ferns in a warm-temperate forest, New Zealand. Journal of the Hattori Botanical Laboratory, 56, 89–95. Bennicelli, R., Stepniewska, Z., Banach, A., Szajnocha, K., and Ostrowski, J. (2004). The ability of Azolla caroliniana to remove heavy metals (Hg(II), Cr(III), Cr(VI)) from municipal waste water. Chemosphere, 55, 141–146. Benzing, D. H. (1990). Vascular Epiphytes. Cambridge: Cambridge University Press. Benzing, D. H. (1995). Vascular epiphytes. In Forest Canopies, ed. M. D. Lowman and N. M. Nadkarni. San Diego, CA: Academic Press, pp. 225–254. Bittner, J. and Breckle, S. W. (1995). The growth rate and age of tree fern trunks in relation to habitats. American Fern Journal, 85, 37–42. Brokaw, N. V. L. (1996). Treefalls: frequency, timing and consequences. In The Ecology of a Tropical Forest: Seasonal Rhythms and Long-term Changes, ed. E. G. Leigh, A. S. Rand, and D. M. Windsor, 2nd edn., Washington, DC: Smithsonian Institution Press, pp. 101–108. Bullock, S. H. and Solis-Magallanes, J. A. (1990). Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica, 22, 22–35. Callaway, R. M., Reinhart, K. O., Moore, G. W., Moore, D. J., and Pennings, S. C. (2002). Epiphyte host preferences and host traits: mechanisms for species-specific interactions. Oecologia, 132, 221–230. 217 218 Klaus Mehltreter Chiou, W.-L., Lin, J. C., and Wang, J. Y. (2001). Phenology of Cibotium taiwanense (Dicksoniaceae). Taiwan Journal of Forestry Science, 16, 209–215. Christ, H. (1910). Die Geographie der Farne. Jena: Fischer. Copeland, E. B. (1947). Genera Filicum. Waltham, MA: Chronica Botanica. Cortez, L. (2001). Pteridofitas epı́fitas encontradas en Cyatheaceae y Dicksoniaceae de los bosques nublados de Venezuela. Gayana Botanica 58, 13–23. Dassler, C. L. and Farrar, D. R. (2001). Significance of gametophyte form in long distance colonization by tropical, epiphytic ferns. Brittonia, 53, 352–369. Durand, L. Z. and Goldstein, G. (2001). Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia, 126, 345–354. Ebihara, A., Dubuisson, J.-Y., Iwatsuki, K., Hennequin, S., and Ito, M. (2006). A taxonomic revision of Hymenophyllaceae. Blumea, 51, 221–280. Ewers, F. W., Cochard, H., and Tyree, M. T. (1997). A survey of root pressures in vines of a tropical lowland forest. Oecologia, 110, 191–196. Farrar, D. R. (1990). Species and evolution in asexually reproducing independent fern gametophytes. Systematic Botany, 15, 98–111. Francesconi, K., Visoottiviseth, P., Sridokchan, W., and Goessler, W. (2002). Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: a potential phytoremediator of arsenic-contaminated soils. Science of the Total Environment, 284, 27–35. Frei, J. K. and Dodson, C. H. (1972). The chemical effect of certain bark substrates on the germination and early growth of epiphytic orchids. Bulletin of the Torrey Botanical Club, 99, 301–307. Gay, H. (1991). Ant-houses in the fern genus Lecanopteris: the rhizome morphology and architecture of L. sarcopus and L. darnaedii. Botanical Journal of the Linnean Society, 106, 199–208. Gemma, J. N., Koske, R. E., and Flynn, T. (1992). Mycorrhizae in Hawaiian Pteridophytes: occurence and evolutionary significance. American Journal of Botany, 79, 843–852. Gentry, A. H. and Dodson, C. H. (1987). Diversity and biogeography of neotropical vascular epiphytes. Annals of the Missouri Botanical Garden, 74, 205–233. Gómez, L. D. (1974). Biology of the potato-fern, Solanopteris brunei. Brenesia, 4, 37–61. Heatwole, H. (1993). Distribution of epiphytes on trunks of the arborescent fern Blechnum palmiforme, at Gough Island, South Atlantic. Selbyana, 14, 46–58. Hernández, A. C. (2006). Fenologı́a foliar de helechos terrestres en un fragmento de bosque mesófilo de montaa en Xalapa, Veracruz, México. Tesis de Licenciatura en Biologı́a, Universidad Veracruzana, Xalapa. Holttum, R. E. (1938). The ecology of tropical pteridophytes. In Manual of Pteridology, ed. F. Verdoorn. The Hague: M. Nijhoff, pp. 420–450. Johansson, D. (1974). Ecology of vascular epiphytes in West African rain forest. Acta Phytogeographica Suecica, 59, 1–130. Kelly, D. L. (1985). Epiphytes and climbers of a Jamaican rain forest: vertical distribution, life forms and life histories. Journal of Biogeography, 12, 223–241. Phenology and habitat specificity of tropical ferns Kornás, J. (1977). Life-forms and seasonal patterns in the pteridophytes of Zambia. Acta Societatis Botanicorum Poloniae, 46, 668–690. Kramer, K. U., Schneller, J. J., and Wollenweber, E. (1995). Farne und Farnverwandte. Stuttgart: Thieme. Lieberman, D. and Lieberman, M. (1984). The causes and consequences of synchronous flushing in a tropical dry forest. Biotropica, 16, 193–201. Lloyd, R. M. and Buckley, D. P. (1986). Effects of salinity on gametophyte growth of Acrostichum aureum and Acrostichum danaeifolium. Fern Gazette, 13, 97–102. Ma, L. Q., Komar, K. M., Tu, C., Zhang, W., Cai, Y., and Kennelley, E. D. (2001). A fern that hyperaccumulates arsenic. Nature, 409, 579. Medeiros, A. C., Loope, L. L., and Anderson, S. J. (1993). Differential colonization by epiphytes on native (Cibotium spp.) and alien (Cyathea cooperi) tree ferns in a Hawaiian rain forest. Selbyana, 14, 71–74. Mehltreter, K. (2006). Leaf phenology of the climbing fern Lygodium venustum in a semi-deciduous lowland forest on the Gulf of Mexico. American Fern Journal, 96, 21–30. Mehltreter, K. and Garcı́a-Franco, J. G. (in press). Leaf phenology and trunk growth of the deciduous tree fern Alsophila firma in a Mexican lower montane forest. American Fern Journal. Mehltreter, K. and Palacios-Rios, M. (2003). Phenological studies of Acrostichum danaeifolium (Pteridaceae, Pteridophyta) at a mangrove site on the Gulf of Mexico. Journal of Tropical Ecology, 19, 155–162. Mehltreter, K., Flores-Palacios, A., and Garcı́a-Franco, J. G. (2005). Host preferences of vascular trunk epiphytes in a cloud forest of Veracruz, México. Journal of Tropical Ecology, 21, 651–660. Mehltreter, K., Hülber, K., and Hietz, P. (2006). Herbivory on epiphytic ferns of a Mexican cloud forest. Fern Gazette, 17, 303–309. Mickel, J. T. and Beitel, J. M. (1988). Pteridophyte Flora of Oaxaca, Mexico. New York: New York Botanical Garden. Mickel, J. T. and Smith, A. R. (2004). The Pteridophytes of Mexico. New York: New York Botanical Garden. Moran, R. C., Klimas, S., and Carlsen, M. (2003). Low-trunk epiphytic ferns on tree ferns versus angiosperms in Costa Rica. Biotropica, 35, 48–56. Nishizono, H., Suzuki, S., and Ishii, F. (1987). Accumulation of heavy metals in the metal-tolerant fern Athyrium yokoscense, growing on various environments. Plant and Soil, 102, 65–70. Oliver, W. R. B. (1930). New Zealand epiphytes. Journal of Ecology, 18, 1–50. Page, C. N. (1979a). The diversity of ferns. An ecological perspective. In The Experimental Biology of Ferns, ed. A. F. Dyer. London: Academic Press, pp. 10–56. Page, C. N. (1979b). Experimental aspects of fern ecology. In The Experimental Biology of Ferns, ed. A. F. Dyer. London: Academic Press, pp. 552–589. Page, C. N. and Brownsey, P. J. (1986). Tree-fern skirts: a defense against climbers and large epiphytes. Journal of Ecology, 74, 787–796. 219 220 Klaus Mehltreter Pócs, T. (1982). Tropical forest bryophytes. In Bryophyte Ecology, ed. A. J. E. Smith. London: Chapman and Hall, pp. 59–104. Poulsen, A. D., Tuomisto, H., and Balslev, H. (2006). Edaphic and floristic variation within a 1-ha plot of lowland Amazonian rain forest. Biotropica, 38, 468–478. Rivera, G., Elliott, S., Caldas, L. S., Nicolossi, G., Coradin, V. T. R., and Borchert, R. (2002). Increasing day-length induces spring flushing of tropical dry forest trees in the absence of rain. Trees, 16, 445–456. Rothwell, G. W. (1991). Botryopteris forensis (Botryopteridaceae), a trunk epiphyte of the tree fern Psaronius. American Journal of Botany, 78, 782–788. Schmitt, J. L. and Windisch, P. G. (2005). Aspectos ecológicos de Alsophila setosa Kaulf. (Cyatheaceae, Pteridophyta) no Rio Grande do Sul, Brasil. Acta Botanica Brasilica, 19, 859–865. Schmitt, J. L. and Windisch, P. G. (2006). Phenological aspects of frond production in Alsophila setosa (Cyatheaceae, Pteridophyta) in Southern Brazil. Fern Gazette, 17, 263–270. Schneider, H., Schuettpelz, E., Pryer, K. M., Cranfill, R., Magallón, S., and Lupia, R. (2004). Ferns diversified in the shadow of angiosperms. Nature, 428, 553–557. Seiler, R. L. (1981). Leaf turnover rates and natural history of the Central American tree fern Alsophila salvinii. American Fern Journal, 71, 75–81. Sela, M., Garty, J., and Tel-Or, E. (1989). The accumulation and the effect of heavy metals on the water fern Azolla filiculoides. New Phytologist, 112, 7–12. Sharpe, J. M. (1993). Plant growth and demography of the neotropical herbaceous fern Danaea wendlandii (Marattiaceae) in a Costa Rican rain forest. Biotropica, 25, 85–94. Sharpe, J. M. (1997). Leaf growth and demography of the rheophytic fern Thelypteris angustifolia (Willdenow) Proctor in a Puerto Rican rainforest. Plant Ecology, 130, 203–212. Sharpe, J. M. and Jernstedt, J. A. (1990). Leaf growth and phenology of the dimorphic herbaceous layer fern Danaea wendlandii (Marattiaceae) in a Costa Rican rain forest. American Journal of Botany, 77, 1040–1049. Sharpe, J. M. and Jernstedt, J. A. (1991). Stipular bud development in Danaea wendlandii (Marattiaceae). American Fern Journal, 81, 119–127. Tanner, E. V. J. (1983). Leaf demography and growth of the tree-fern Cyathea pubescens Mett. ex Kuhn in Jamaica. Botanical Journal of the Linnaean Society, 87, 213–227. Tuomisto, H. (2006). Edaphic niche differentiation among Polybotrya ferns in western Amazonia: implications for coexistence and speciation. Ecography, 29, 273–284. Tryon, R. M. (1960). The ecology of Peruvian ferns. American Fern Journal, 50, 46–55. Tryon, R. M. (1964). Evolution in the leaf of living ferns. Bulletin of the Torrey Botanical Club, 21, 73–85. van Steenis, C. G. G. J. (1981). Rheophytes of the World. Alpen an den Rijn: Sijthoff and Noordhoff. van Steenis, C. G. G. J. (1987). Rheophytes of the world: supplement. Allertonia, 4, 267–330. Phenology and habitat specificity of tropical ferns Wagner, W. H. (1972). Solanopteris brunei, a little known fern epiphyte with dimorphic stems. American Fern Journal, 62, 33–43. Wagner, W. H., Jr. and Wagner, F. S. (1977). Fertile-sterile leaf dimorphy in ferns. Gardens Bulletin Singapore, 30, 251–267. Walker, T. G. (1986). The ant-fern Lecanopteris mirabilis. Kew Bulletin, 41, 533–545. Westoby, M., Warton, D., and Reich, P. B. (2000). The time value of leaf area. American Naturalist, 155, 649–656. Williams-Linera, G. (1997). Phenology of deciduous and broadleaved-evergreen tree species in a Mexican tropical lower montane forest. Global Ecology and Biogeography Letters, 6, 115–127. Zotz, G. and Büche, M. (2000). The epiphytic filmy ferns of a tropical lowland forest – species occurrence and habitat preferences. Ecotropica, 6, 203–206. Zotz, G. and Vollrath, B. (2003). The epiphyte vegetation of the palm Socratea exorrhiza – correlations with tree size, tree age and bryophyte cover. Journal of Tropical Ecology, 19, 81–90. 221