Functional trait diversity of Cyclanthaceae and its convergent evolution with Araceae in Neotropical forests

Growth form diversity of cyclanthaceae

The 49 Costa Rican species of Cyclanthaceae were divided into three functional growth form—understory herbs (terrestrial, epilithic, and rheophytic), epiphytes, and root-climbing hemiepiphytes.

Understory herbs

Using data for all of Costa Rica, understory and other terrestrial herb species comprise 35% (17 species) of the Cyclanthaceae (Fig. 2). A key species is Asplundia uncinata (Fig. 3A) which forms a greater area of ground cover and biomass than any other broadleaf herb species in the shaded understory of the primary forest at La Selva (Rundel et al., 2020). This species of understory herb grows to 1–2 m in height with an extensive system of thick underground rhizomes that produce clonal stands that may extend for 10 m or more (Figs. 3B and 3C).

Although typically terrestrial in growth habit, A. uncinata can occasionally be observed using adventitious anchor roots to climb a short distance up a host tree. Individuals with attachments for root-climbing generally extend upward no more than 1–2 m above the ground and commonly lose their primary stem connection to the soil (Table 2). With development, the primary stem is severed, and small secondary roots slowly develop new connections to the soil. This type of flexibility in rooting behavior may be a transitional root-climbing life history, as discussed below.

A second understory species of this genus, Asplundia sleeperae (Fig. 3D), displays very different traits. It is a robust terrestrial herb 1–2 m in height and relatively rare. It favors shaded understory habitats of primary forest on alluvial soils and is absent from swampy areas and secondary forests. Unlike A. uncinata, we have not observed any case of vegetative reproduction from underground rhizomes in A. sleeperae, and it has never been observed to climb.

Dicranopygium umbrophilum (Fig. 4A) is a relatively small understory herb, usually no more than 0.5–1 m in height. Although present in low frequencies on well-drained residual soil, it becomes a dominant understory herb on humid swampy and lowland alluvial soils with a high soil moisture content and humid air in the understory at La Selva. Under these swampy conditions, individual plants typically attach themselves to stems or trunks of trees, changing their growth form to that of root-climbing hemiepiphytes. However, they limit their climb to no more than 1–2 m above the soil level. At this stage all primary stem connection to the soil is lost and the plants begin to develop secondary soil linkage with aerial roots (Table 2). As with occasional root-climbing seen in Asplundia uncinata, the common alteration of growth form to root-climbing in D. umbrophilum suggests an intermediate stage of adaptive change in moving from well drained terrestrial soils to water saturated swamp soils.

Cyclanthus bipartitus (Fig. 1A) is a tall acaulescent understory herb reaching up to 3 m in height. Its mature leaf blades are deeply divided almost to the base. A large underground rhizome allows for vegetative reproduction. Although highly variable in morphology the genus is considered to be monotypic. This species is widely distributed in wet lowland Neotropical forests and is common in large gaps, disturbed habitats, and older secondary forest. Carludovica sulcata (Fig. 1B) is a tall understory herb reaching 2.5 m in height. It is usually acaulescent and palm-like in form. The plants possess large underground rhizomes and readily reproduce vegetatively. This species is locally common in large gaps, disturbed habitats, and older secondary forest. A second species, C. rotundifolia, favors similar habitats but is more locally distributed at La Selva.

The Araceae is well represented in the understory flora of terrestrial herbs in Costa Rica with respect to both diversity of species present and the relative abundance of the species. Understory herbs comprise 25% of the 242 native species of Araceae in Costa Rica (Fig. 2). This group is represented by multiple species each of Spathiphyllum, Dieffenbachia and Xanthosma. Two genera which are more typically epiphytes or hemiepiphytes, Philodendron and Athrurium contribute terrestrial species as well. Spathiphyllum fulvovirens is the understory herb species with the highest frequency of occurrence in the primary forest understory at La Selva (Rundel et al., 2020). Understory aroids are less common in large gaps and along forest edges where solar irradiance is higher.

Many understory herbs in the Cyclanthaceae demonstrate important traits of efficient vegetative reproduction parallel to that well known to be present in herbaceous aroids. Most understory aroids have vegetative means of reproduction using rhizomes or stems with short internodes that creep over the soil and have shallow rhizomes although a few species with deep roots are notable. Examples of deeply rooted understory aroids at La Selva include Philodendron grandipes and Anthurium ochranthum (Croat, 1988), both relatively common and ecologically successful.

Mean values of functional leaf traits for understory herbs are similar between species of Cyclanthaceae and Araceae at La Selva. The values for leaf specific area, nitrogen specific leaf area, δ¹³C, and leaf water content do not differ significantly (Fig. 5). One notable exception is in the significantly higher concentration of nitrogen in herbaceous aroids. This level of leaf nitrogen is also significantly higher than that present in tropical Costaceae, Marantaceae, Heliconiaceae, and Zingiberaceae at La Selva (Rundel et al., 2020).

Emergent aquatics, epilithic growth forms, and rheophytes

There are three small groups of unusual habitats that require specialized functional traits for survival and are present in a small number of species in the Cyclanthaceae and Araceae. These are emergent aquatics, epilithic growth forms, and rheophytes. The Costa Rican flora of Cyclanthaceae include rheophytes but no example of emergent aquatic aroids comparable to a small but significant group of aquatic species within the global Araceae. Some Costa Rican genera are exclusive to wetland habitats, as with Montrichardia and Urospatha, while some large genera have at least one species of rooted terrestrial whose natural habitat is standing water. An example of this can be seen with Spathyphyllum friedrichthalii, the only marsh species in its genus at La Selva. Overall, however, this aquatic habitat is relatively uncommon among Neotropical aroids.

Many species of the relatively large cyclanths genus Dicranopygium display an epilithic growth form that presents a special case of functional root traits that enable secure attachment to rocks. The root structure and development in these epilithic species allows the plants to firmly attach themselves to rocks by penetrating into the fine interstitial spaces within the rock (Mayo et al., 1997). These root traits are successful in establishing themselves on rock types that are sufficiently porous, with limestone being a prime example. Other species grow as appressed plants on tree trunks or on boulders. Porous limestone is particularly suitable for epilithic aroids because of its ability to catch debris and to provide many interfaces for adequate rooting sites but species restricted to limestone are rare. The presence of this trait in multiple species of the same genus suggests the possibility of highly evolved traits of the root rhizosphere. There are no identified epilithic species among the Araceae of Costa Rica although this growth specialization is present within Paleotropical members of the family (Croat, 1988).

The traits of epilithic growth are often associated with rheophytes that are restricted to growth on rocks in moving stream water. Rheophytes rooted in moving water present a specialized niche that combines characteristics of aquatic and epilithic habitats. These species cling to rocks on streambanks or within the stream itself (van Steenis, 1981, 1987). The presence of specialized rheophytes growing on rocks along the margins of fast-flowing streams can be found in in several species of Dichranopygium in Costa Rica, including D. wedelii at La Selva (Figs. 4C and 4D). This growth habit requires functional traits that allow the successful colonization of this highly specialized niche. Aroid rheophytes are widely present in the Paleotropics (Boyce & Wong, 2019). In contrast, rheophytic growth forms are uncommon in Neotropical aroids but do occur in a small number of species within the large genera Anthurium and Spathiphyllum (Croat, 1988).

Epiphytes

Epiphytes make up 28% (18 species) of the Cyclanthaceae in Costa Rica (Fig. 2). These epiphytes all fall into three genera which are represented in the flora of La Selva. Corigyne pendula at La Selva is one of seven species that occur only in Costa Rica and Panama (Fig. 6A). This acaulescent species colonizes large branches and is easy to recognize with its elongate gray-green leaves that hang vertically. It is a relatively common epiphyte in the La Selva forest. Although a true epiphyte, individual plants on larger fallen branches may survive for some time at ground level.

Sphaeradenia forms a relatively large genus of 53 described species characterized by short stems with long and narrow bifid leaves. The range of this genus extends from Nicaragua to northern South America. Some of these species can survive for some period of time on fallen branches but only rarely directly colonize terrestrial environments. Sphaeradenia acutitepala at La Selva is a shade-adapted epiphyte that typically grows more than 10 m above the ground, often as high as 20 m (Fig. 6B).

Ludovia integrifolia is an unusual epiphyte with a wide biogeographic distribution that extend from southern Mexico through Panama, where it is present on Barro Colorado Island (Croat, 1978), to northern South America. This species has smooth cylindrical stems up to 2–3 cm in diameter that display monopodial growth with short internodes between branches (Figs. 6C and 6D) These stems can extend for up to 10 m or more, leading some researchers to describe the species as a liana. In areas of treefalls the elongate stems may be seen dangling down into the lower canopy, giving them an appearance that can be mistaken for an aroid. The leaves are distinct from any other cyclanth at La Selva with the presence of simple blades with entire margins. Ludovia lancifolia from French Guiana is an epiphyte growing 20–25 m high in the canopy (Freiberg & Gottsberger, 2001).

Epiphytes form 28% (65 species) of the Costa Rican species of Araceae (Fig. 2). Much of the Neotropical richness in epiphytic Araceae lies within the genus Anthurium, and secondarily in a few species of Philodendron. There are several epiphytic lineages within Anthurium that develop short stems with associated a dense root mass, adapted to retain rainfall and stem flow of moisture and nutrients. Other species have evolved rosulate morphologies to catch and hold fallen debris in “baskets” formed by the leaves (Gerst et al., 2021). With this structure younger roots are able to grow into this debris, providing nutrients and an added capacity to hold water much as in many tank-forming bromeliads. Assessing the global Araceae, true epiphytes are abundant and diverse in wet Neotropical forests but notably uncommon in the Paleotropics. This difference in diversity of this growth form between the two floristic regions is largely the result of the presence of Anthurium and Philodendron in the Neotropics (Croat, 1988).

Several species of Araceae fit within a special category of species which begin their life as true epiphytes but develop extensive aerial roots which hang pendulously downward and eventually reach the ground and develop into full terrestrial root systems. There are a few examples of these so-called primary hemiepiphytes in Philodendron and Anthurium (Meyer & Zotz, 2004). The characteristics of a primary hemiepiphyte are better known in groups like strangler figs and Clusia (Putz & Holbrook, 1986; Holbrook & Putz, 1996; Williams-Linera & Lawton, 1995).

Root-climbing hemiepiphytes

The third functional group high in species richness in the Cyclanthaceae are the root-climbing hemiepiphytes, often referred to as secondary hemiepiphytes, which make up 21% (12 species) of the Costa Rican species (Fig. 2). A broad morphological diversity of root-climbing hemiepiphytes have evolved within Asplundia where this growth form is the most common functional trait of morphology with six of the eight species of Asplundia at La Selva. Five of these typically climb to intermediate trunk heights of 3–5 m, including Asplundia longitepala (Fig. 7A) and Asplundia ferruginea, both with a coarse unbranched stem. Asplundia multistaminata differs in having slender stems that branch repeatedly, forming tangled masses extending outward for 4 m or more in length laterally to produce a scandent form of growth (Fig. 7B; E. Riordan, 2022, unpublished data).

A few species extend higher into the canopy equal to many of the hemiepiphytic aroids. Asplundia utilis is one of the most common hemiepiphytes at La Selva in moist primary forest throughout the station up to 10 m (Fig. 7C). The root-climbing hemiepiphyte life history is also present in the monotypic Evodianthus funifer, characterized by long and slender stems which extend up to10 m into the canopy and branch freely (Fig. 7D). This species is frequent and widespread in moist primary forest at La Selva, especially on ridges and slopes (E. Riordan, 2022, unpublished data).

An impressive 45% (112 species) of the Araceae in Costa Rica are root-climbing hemiepiphytes (Fig. 2), a group with spectacular ecological success as indicated by their frequency of occurrence and large biomass (E. Riordan, 2022, unpublished data). The Neotropical aroid flora is particularly well known for a diversity of hemiepiphytes in the genera Philodendron, Monstera, Syngonium, Rhodospatha and Heteropsis. All of these genera are widespread and abundant in seasonally moist to very wet tropical forest in Costa Rica (Mayo et al., 1997).

The significance of the atrophy of the main stem early in the development in hemiepiphytesis a key trait that has not been well described. Experimental studies with hemiepiphytic Monstera acuminata showed that upper stem segments with more leaf area have wider vessels and that the production of new adventitious is necessary to prevent a lethal hydraulic constriction (López-Portillo et al., 2000).

One clue in the evolution of the root-climbing hemiepiphyte life history can be seen in our field observations of stem morphology in young developing hemiepiphytes. We found that four of the five cyclanths species we studies had 100% of their primary stem atrophied at an early stage of development (Table 2). All of these sampled species had well developed secondary roots that reestablish some degree of hydrologic connection to the soil. A slightly lower level of 85% loss of stem connection was observed in Asplundia uncinata, a species more typically terrestrial in growth with a full stem to soil connection. This life history was also found in Dicranopygium umbrophilum, an understory herb that may facultatively become a low climber and lose its direct hydraulic stem connection to the soil. For young hemiepiphytic Araceae we found a similar set of field observations that the main stem in was severed in as high a level as 85% in Anthurium subsignatum of our large sample size. The lowest level of severance was found in Anthurium pentaphyllum at 55%, with intermediate frequencies in Philodendron alliodorum (75%) and Philodendron inaequilaterum (67%).

The evolution of root-climbing hemiepiphytes

There has been relatively little conjecture on the evolutionary development of root-climbing hemiepiphytes as a functional growth form with appropriate adaptive traits of morphology, ecophysiology and ecology. Root-climbing vines outside of the Araceae and Cyclanthaceae that might be classified as hemiepiphytes typically do not lose their stem connection to the soil with development.,The Marcgraviaceae is often cited as an example of hemiepiphytes outside of the Araceae and Cyclanthaceae. All Marcgravia species that we have observed at La Selva are rooted lianas or vines and not hemiepiphytes as we define this term.

The most puzzling aspect of the characterization of functional traits for root-climbing hemiepiphytes lies with the loss of the hydraulic connection of the main stem to the soil at a relatively early stage of growth. This condition seems at first thought to be counterintuitive as it would reduce hydraulic flow. With expanded growth of upper stem and upperleaves, however, the basal stem would provide a diminishing share of the water uptake by the plant. Our observations demonstrate that this severance of connection of the main stem commonly occurs at a young age before the plants are mature. We found that four of the five cyclanths species had 100% of their primary stem severed at this stage of development (Table 2). We also found in parallel observations that the main stem in young hemiepiphytic Araceae was severed in the majority of young plants but not at as high a frequency (55–97%) found in hemiepiphytic cyclanths (Table 2).

Other researchers have reported the common loss of main stem connection to the soil in diverse species of hemiepiphytic Araceae but at lower levels than we observed (Zotz et al., 2020; Bautista-Bello et al., 2021). These authors suggest that this loss of soil connection to the main stem is a hydraulic strategy related to the fact that almost all reported hemiepiphytes are monocotyledons that lack secondary growth. They suggest that the development of water uptake by adventitious roots may be the only option to allow sufficient flow to an increasingly larger shoot, making the lower portion of the stem expendable (López-Portillo et al., 2000). The dynamics of hydraulic structure of main stem roots and adventitious aerial roots in the Cyclanthaceae and Araceae remain poorly studied (but see Mantovani, Brito & Mantuano, 2018).

Do hemiepiphytes exist as a distinct functional growth form?

A group of ecologists has recently questioned whether secondary hemiepiphytes should be categorized as a distinct growth form with adaptive traits distinct from other vine species (Zotz et al., 2021). The name nomadic vine has been proposed to replace the term secondary hemiepiphyte (Moffett, 2000) although this terminology has had mixed acceptance in the literature (see Zotz, 2013, 2020; Croat & Ortiz, 2020). The name nomadic vine seems a poor choice to us for several reasons. First, the proposed name adds the descriptor nomadic, which seems entirely inappropriate for characterizing the life history of these species. Nomads in human terms are classically wandering populations that lack a permanent home. The root-climbing hemiepiphytes are far from nomadic and utilize skototropism for directed growth toward dark areas which may represent large-tree diameters (Strong & Ray, 1975; Balcázar-Vargas et al., 2015). In this way they actively seek out permanent host trees.

There are functional traits that collectively distinguish hemiepiphytes from tropical vine that may utilize root-climbing adventitious roots. The trait of early loss of hydraulic connection of the main stem with the soil is typically present in climbing Araceae and Cyclanthaceae. Hydraulic connectivity to the soil is eventually replaced by adventitious roots that reestablish the soil connection (Mantovani, Brito & Mantuano, 2018). We found that this trait of dieback in the main stem was present in the great majority of the young stems of hemiepiphytic Cyclanthaceae and Araceae as they develop (Table 2).

Marcgravia species and other tropical forest vines with adventitious roots for climbing rarely survive after the main stem being severed above the soil line. In tropical root-climbing vines typically only the uppermost nodes typically bear leaves, and the main stem is intact and utilized for physical support as well hydraulic connections to the soil for water and nutrient uptake (Zona, 2020). The most active roots are associated with the leafy sections of the stem. In contrast, root-climbing hemiepiphytes often have leaves along their full length and roots are restricted to the nodes and scattered in occurrence. The stems lack a clear means of accumulating organic debris and associated nutrients compared to vines (Croat, 1988).

Additional evidence for the adaptive traits of the hemiepiphyte life form can be seen in examples of morphological traits that limit water loss and promote nutrient uptake after the primary stem rhizome is severed as the plants climb. These include compact root hairs, the development of more roots per node, or the presence of roots with velamen capable of extracting water directly from the air (Croat, 1981, 1988). In this manner, these are functionally similar to basins formed by leaf rosettes or clusters of stiff roots at the upper internodes that collect water and nutrients (Dressler, 1985; Zona & Christenhusz, 2015; Gerst et al., 2021).