Pugnaire F.I. Valladares F. Functional Plant Ecology

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2. Polyaxial trees, characterized by repeated development of equivalent orthotropic

modules in the form of basal branches initially restricted to the epicotiledonary region

of the seedling axis and the basal nodes in the subsequent axes (Tomlinson’s model), or

those that grow from meristems producing orthotropic or plagiotropic trunks forking

at regular but distant intervals by equal dichotomy, with lateral inflorescences but

without vegetative lateral branches (Shoute’s model). The former group includes

almost all multistemmed palms, with species such as Bactris gasipaes, Euterpe oleracea,

Hyphaene guineensis, Oncosperma tigilaria, Phoenix dactilifera, and Raphia gigantea.

The second group of this type is less frequent and includes species such as Allagoptera

arenaria, Chamaedorea cataractarum, Hyphaene thebaica, Nannorrhops ritchiana, Nypa

fruticans, and Vonitra utilis.

Light and Water Relations

Palms are a taxonomically uniform group constituting the only monocots that contribute to

the canopy, subcanopy, and forest floor layers of most tropical humid forests. Their ecophy-

siological differentiation is considerable and excluded only from the driest tropical forest

communities. In the Amazon region they occupy the whole range of available habitats to such

an extent that a key for the forest formations in this large expanse of tropical forest

communities has been developed on the basis of the palm species (Kahn and de Granville

1992; Table 10.3). The range of habitats of ecophysiological interest vary from permanently

water-logged forests (Mauritia flexuosa or minor), and seasonally flooded palm savannas with

sandy or clay soils (Sabal mauritiaeformis, Orbignya martiana), to hyperseasonal sites in

savannas with 3–5 month dry periods and water logging during the rainy season (Copernicia

tectorum, Copernicia cerifera, and Cocos schizophylla) (Hueck 1966, Walter 1973, Kahn and

de Granville 1992, Kalliola et al. 1993).

The diffuse distribution of the vascular tissue within the stem renders these plants

resistant to burning, critical for survival of palm species occurring in savannas of Africa

(Borassus) and South America (Copernicia, Acrocomia, Sabal ). Their tolerance to flooding

and comparatively long periods of drought is also related to their anatomy. Holbrook and

Sinclair (1992) showed in Sabal palmetto that the amount of water accumulated in the stem

per unit of living leaf area increases linearly with plant height. In addition, leaf epidermal

conductance was in the range reported for xerophytes. Tolerance to prolonged drought is

reduced by the fact that palms do not have a resting phase during their life cycle.

Tropical palms frequently constitute a dense understory layer in tropical moist forests

(Gentry and Emmons 1987, Kahn and de Granville 1992, Kalliola et al. 1993). In these

environments, light is the main factor influencing plant growth rate and time of reproduction.

Photosynthesis studies on understory palms showed positive carbon balances at the leaf level

when exposed to light intensities as low as 25 mmol m

2

1

. However, their growth under

natural conditions was stimulated significantly when growing in gap edges compared with

plants under full shade in the forest understory (Chazdon 1986). Computer simulations of

carbon gain of full-shade-grown seedlings indicate that 24 h positive carbon balance is

reached whenever daily irradiation is greater than 0.2 mol m

2

The long-lasting leaf scars on the palm stem have been used as a marker to age palm

populations and to detect changes in growth conditions (Pin

ero et al. 1984). A gap formed by

the fall of one or a few trees not only opens the forest canopy, allowing more light to reach the

forest floor, but turns down small undercanopy palms without uprooting them. The tilted

stems of Astrocaryum mexicanum in this study continued to grow vertically, forming a sharp

bend that indicated the occurrence of a disturbance. The number of leaf scars after the

bending of the stems multiplied by the average leaf life span was found to be an accurate

measure of the time elapsed since the disturbance. However, although growth is continuous,

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330 Functional Plant Ecology

TABLE 10.3

Forest Types and Palm Genus Diversity in the Amazon Basin

Forest Type

Arborescent: Single or

Multistemmed Large (Leaf

> 4m)

or Slender (Leaf

4m)

Medium Sized: Large or Slender,

Single or Multistemmed, Erect to

Creeping

Small: Erect, Prostrate, or

Climbing; Single, Multistemmed or

Acaulescent

Subterranean Stemmed:

Large Leaved

Terra firme forests

Astrocaryum, Dyctiocaryum,

Iriartea, Jessenia, Maximiliana,

Oenocarpus, Orbygnia, Socratea

Astrocaryum, Oenocarpus,

Socratea, Syagrus, Wettinia

Aiphanes, Astrocaryum, Bactris,

Chamaedorea, Chelyocarpus,

Desmoncus, Geonoma,

Hyospathe, Iriartella,

Pholidostachys

Astrocaryum, Orbignya Scheelea

Forests on periodically

flooded alluvial soils

Astrocaryum, Attalea, Iriartea,

Euterpe, Socratea, Oenocarpus,

Orbignya, Scheelea

Astrocaryum, Chelyocarpus Itaya,

Phytelephas

Bactris, Geonoma, Desmoncus

Forests periodically

flooded by Blackwater

Astrocaryum

Leopoldinia

Bactris, Leopoldinia

, Desmoncus

Swamp forests on organic,

permanently flooded

soils

Mauritia, Euterpe Socratea

Oenocarpus

Bactris, Desmoncus

Seasonal swamp forest on

water-logged,

irregularly flooded soils

Euterpe, Jessenia, Mauritia,

Mauritiella Socratea

Astrocaryum, Eleaeis, Manicaria,

Oenocarpus, Wettinia

Asterogyne, Bactris Catoblastus,

Desmoncus, Geonoma,

Hyospathe

Forests on dry, white-

sandy soils

Mauritiella

Bactris, Desmoncus

Forests on water-logged,

white-sandy soils

Jessenia, Mauritia, Mauritiella Elaeis, Euterpe

Bactris, Desmoncus Lepidocaryum,

Pholidostachys

Astrocaryum, Orbignya Scheelea

Submontane and montane

forests

Dictyocaryum, Euterpe Iriartea,

Prestoea

Geonoma, Oenocarpus Wettinia Aiphanes, Chamaed

orea Geonoma

Savannahs

Acrocomia, Astrocaryum

Copernicia, Mauritia, Syagrus

Mauritiella, Syagrus

Bactris, Desmoncus

Source

: Kahn, F. and de Granville, J.-J.

Palms in Forest Ecosystems of Amazonia. Ecological Studies

Vol. 95, Springer-Verlag, Berlin, 1992.

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Tropical Forests: Diversity and Function of Dominant Life-Forms 331

the rates of height growth and leaf production may change significantly with ecological condi-

tions. In populations of Prestoea montana in a lower montane forest in Puerto Rico, average leaf

production rate after a 36 year observation period was 4 leaves year

1

, but the production rate

changed with the age of the population sampled and was also lower in the suppressed individuals

compared with those that reached the canopy (Lugo and Rivera-Battle 1987).

CLIMBING PLANTS AND HEMIEPIPHYTES

A characteristic structural feature of tropical forests is the occurrence of woody plants that

use other trees as a support for expanding their photosynthetic area under full sun. These

species either climb from the forest floor to the upper canopy (climbers) or descend with their

roots from the upper canopy to the forest floor (hemiepiphytes) (Richards 1952, 1996, Walter

1973, Whitmore 1990). Climbing plants may be herbaceous (mostly called vines) or woody

(frequently called lianas), although, there may be changes in the structural characteristics of

the stem during the lifetime of certain species. They are conveniently distinguished by the

method of climbing: (1) scandent climbers (with thorns or hooks); (2) tendrillar climbers (with

tendrils); (3) root or bole climbers (with adhesive organs); and (4) twiners (twisting apical

organs around the host) (Hegarty 1989).

Biomass allocation in these types of plants is characterized by a larger investment in

photosynthetic surface at the expense of the production of self-supporting tissues, at least

during a significant portion of their life cycle. The consequences of this pattern of biomass

allocation for the ecophysiology of these plants vary in lianas and hemiepiphytes. The former

are connected to the forest floor throughout their life cycle, no more limited in their water

and nutrient supply than the host trees, whereas the hemiepiphytes have to cope with

water and nutrient stress during the establishment phase, until they are able to establish

contact with the forest floor through adventitious roots.

Lianas

Woody vines (lianas) contribute significantly to the total leaf area of lowland forests (Gentry

1983, Putz 1983), and their number and diversity in certain forest types may be comparable to

those of tree species (Rollet 1969, Pe

rez-Salicrup et al. 2001, Burnham 2002). Lianas species

are capable of rapid growth and thereby affect the development of leaf area and branching of

the host trees and may increase mortality (Putz 1984). In fact, the presence of lianas does not

greatly affect the total leaf area of the forest, the development of liana leaf area is compensated

by a reduction in leaf area production by the host tree (Hegarty 1989). The larger ratio of leaf

litter production to wood production observed in tropical forests compared with temperate

forests may simply be the result of the frequency of lianas in the tropics (Gentry 1983).

The life cycle of a liana begins by germinating in the forest floor, either in a process of

natural regeneration or in explosive growth events after natural or man-made disturbances in

forest gaps. Light requirements of lianas are similar in variety to those reported for rain forest

trees. Rollet (1969) documented the regeneration behavior of 95 liana species in an evergreen

forest in the venezuelan Guayana. The most abundant species (8) were absent from the

regeneration plots and were categorized as shade intolerant. Among the rest there

were shade-tolerant species with weak regeneration but long survival, and intermediate-

illumination species with abundant regeneration but small survivorship. It is therefore

erroneous, to consider all liana species as shade intolerant.

During the initial phases lianas are self-supporting, but after a few years they begin to

climb on neighboring trees in a process that is tightly coupled to the gap dynamics of the

forest. Gaps promote development of lianas, which take advantage of their rapid growth in

length to gain height in the forest using neighboring trees as a support (Putz 1984).

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332 Functional Plant Ecology

Lianas are characterized by a larger leaf biomass=stem biomass ratio than self-supporting

trees (Putz 1983), and their xylem vessels are large, offering little resistance to water transport

(Ewers 1985). In fact, lianas and vines from evergreen and deciduous tropical forests are

characterized by higher specific conductivity of the stem than those of the trees of the same

communities, at least when stems of similar diameter are compared (Ewers 1985, Gartner et al.

1990). Putz and Windsor (1987) hypothesized that the large lumen of the xylem vessels was

more prone to cavitation; therefore, lianas should be quite sensitive to drought, shedding

their leaves at the beginning of the dry season. However, lianas were found to be evergreen,

with a longer leaf-producing period than that of the tree species used for comparison. In

the study site (Barro Colorado, Panama

), water availability during the dry season was not as

severely curtailed as expected, or there were other mechanisms preventing cavitation in

these plants. Despite the anatomical differences, Andrade et al. (2004) found that both lianas

and co-occurring trees follow the same linear relationship between sap flow and DBH.

Besides, measurements of D=H ratios in xylem water indicated that lianas compete

with self-supporting trees tapping water at similar soil depths. Lianas inhibit saplings and

seedling growth of self-supporting tree species, the main cause is the belowground competi-

tion (Pe

rez-Salicrup 2001, Schnitzer et al. 2005). Therefore, the water status of trees should be

affected by the presence of lianas. Experimental removal of lianas during the dry season in

seasonally dry forests in Bolivia produced contradictory results. Senna multijuga trees

increased their water potential by liana removal as soon as 1 day after cutting, and grew

twice as fast compared with controls (Pe

rez-Salicrup and Baker 2000). Similar experiments

with Swietenia macrophylla trees showed that lianas had higher water potential and leaf

conductance than the host tree, but host trees with and without lianas had similar water

status, indicating that lianas do not reduce the water availability.

Hemiepiphytes

Hemiepiphytes are plants that germinate on branches or stems of trees and that grow and

develop leaves and roots using nutrient and water resources that accumulate within the

crevices of the stem bark (Richards 1952, 1996, Walter 1973). Their roots eventually reach

the soil and develop there in a similar fashion as roots of their host trees. In this process, the

plants pass from a truly epiphytic stage, characterized mainly by frequent drought stress, to a

self-supporting stage in which the plant functions as a normal tree. A large group of the

hemiepiphytic species behave as ‘‘stranglers’’ because their roots grow around the stem of

the host tree. As root diameter increases, they compress the stem underneath. This process

eventually continues until the host tree stem cannot transport water and nutrient upward and

therefore dies, leaving the strangler as a self-supporting independent tree. The group of

strangler species is rather limited and is frequently found among the genus Ficus, while

permanent hemiepiphytes remain host-dependent for support despite extensive root systems

in contact with the soil (Todzia 1986).

Epiphytic and tree forms of hemiepiphytes differ in their growth habit and water rela-

tions. Holbrook and Putz (1996) found that the epiphytic form of hemiepiphytic Ficus

strangler species produced thinner leaves with larger specific leaf areas and water contents

(%), but lower stomatal densities than the leaves produced at the tree stage. In correspond-

ence with their higher water content, osmotic potential at full turgor was lower in the

epiphytic forms, but the rate of cuticular water loss was smaller than that measured in excised

tree leaves. In this group of hemiepiphytes, the functional properties of the epiphytic stage is

directed to conservative water use according to the uncertainty of water supply in the

epiphytic habitat, particularly during the dry season. Although nutrient supply is linked to

water availability, it did not appear to be a limiting factor for the development of plants at

this stage.

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Tropical Forests: Diversity and Function of Dominant Life-Forms 333

One outstanding group among the hemiepiphytes in the neotropics is constituted by the

species of the genus Clusia that perform a combination of C3 and crassulacean acid meta-

bolism (CAM) photosynthesis. This process was originally described in Clusia lundelli (Clu-

siaceae) (Tinoco-Oranjuren and Va

squez-Yanes 1983), a true strangler, beginning its life cycle

as an epiphyte and then developing roots that eventually anchor in the soil. The same

photosynthetic metabolism has been thoroughly documented in the large tree strangler Clusia

rosea in the United States. Virgin Islands (Ting et al. 1985, Ball et al. 1991) and confirmed in

several species of this genus (Popp et al. 1987, Sternberg et al. 1987, Ting et al. 1987, Borland

et al. 1992, Winter et al. 1992).

Gas exchange of Clusia CAM species has been shown to be highly flexible, going from

typical CAM to typical C3, including continuous net fixation of CO

during a 24 h cycle,

depending on light intensity during growth, day–night temperature cycles, drought, and even

nutrition (Schmitt et al. 1988, Lee et al. 1989, Zotz and Winter 1993). Drought induces

contrasting effects on Clusia species that fix CO

during the night. In Clusia uvitana, daytime

uptake decreased rapidly without irrigation, whereas nocturnal fixation increased throughout

the treatment (Winter et al. 1992).

VASCULAR EPIPHYTES

Epiphytes are plants that can complete their life cycle living on the stem, branches, or even

leaves of other plants. They acquire water and nutrients from rain water and dust, and from

accumulation of organic debris accumulated on the body of the plant or on the surface of the

host tree. This life-form has been successful from the evolutionary point of view. Within

the higher vascular plants (Magnoliophyta), approximately 6% of the genera and 9% of the

species have been recorded as epiphytes (Madison 1977, Kress 1986, Benzing 1990). Epiphytic

genera and species are more frequent among monocots (Liliopsida) than among dicots

(Magnoliopsida). Benzing (1990) registered 520 genera and 16,608 species of epiphytic mono-

cots compared with 262 genera and 4521 species of epiphytic dicots. The Orchidaceae account

for the predominance of epiphytes within the monocots with 67% of the vascular epiphytes.

Epiphytic habitats restrict plant growth mainly through drought stress. Nutrient supply is

also restricted because accumulation of organic matter and flow of nutrients in rain water and

dust is scarce and erratic. Many epiphytes therefore depend on their capacity to accumulate

organic residues produced by the supporting trees, or by animals associated with them (ants,

termites), and by their capacity to accumulate water internally via a specialized morphology.

Water and nutrient availability vary with the location of the epiphyte within the forest.

Those located in the topmost branches depend on the interception of dust particles and the

absorption of dissolved nutrients in rain water, and are exposed to nearly full sunlight.

Exposed epiphytic habitats are characterized by a high evapotranspiration demand. Drought

spells may be of short duration, but frequent. The duration of the dry spells increases from

wet rain forests to dry seasonal forests.

In the middle to low canopy, evapotranspiration demands are lower, and nutrient avail-

ability increases because of tree leaf litter accumulation and enrichment of rain water through

nutrient leaching. On the other hand, light availability may be limiting for photosynthesis.

Patterns of vascular epiphytes diversity have been documented in many tropical moun-

tains since the original observations of Gentry and Dodson (1987a). Epiphytes reach their

peak in biomass and species diversity at middle elevations in a fashion closely correlated with

rainfall and air humidity (Ku

per et al. 2004). Cardelu

s et al. (2006) showed that larger

diversity at middle elevations results at the overlap of large-ranged species at these elevations.

Nutrient N is a limiting factor for most epiphytes. Stewart et al. (1995) used natural

abundance of

N(d

N) to investigate the source of N for epiphytes compared with their

host trees. Samples from six rain forests in several continents showed that epiphytes were

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334 Functional Plant Ecology

consistently depleted in

N compared with trees at each site. Authors hypothesized that

epiphytes were using

N depleted N from atmospheric deposition and perhaps also from N

fixation. Hietz et al. (1999) showed in an altitudinal transect in Mexico that variations in d

were caused by the N acquisiton from different sources. Atmospheric bromeliads presented

lower d

N values than tank-forming bromeliads. Ground-rooted hemiepiphytes showed the

highest N concentrations and d

N values. Analyses of distribution of d

N values in

different positions within the forests led to the conclusion that differences are not only due

to the sources, but also due to different patterns of

N discrimination during N acquisition

(Wania et al. 2002). Before a definitive statement is made in this direction it is necessary to

analyze the form of available N in each position (proportions of NO

and NH

Main adaptations of vascular plants to the epiphytic habitat are related to their water and

nutrient economy. They may be summarized as follows:

1. Development of foliose structures capable of retaining rain water and accumulating

organic detritus, the so-called tanks and nests. Many bromeliads are tank formers and

develop short roots that penetrate into accumulated organic matter and absorb water and

nutrients (Pittendrigh 1948). Nests are less efficient than tanks at retaining rain water, but

litter accumulation provides a substrate rich in nutrients that are absorbed by the roots of

the nest-forming plants. This structure is found among ferns, orchids, and aroids.

2. Development of water-accumulating tissues (succulence). Many epiphytes possess

succulent roots, stems, and leaves. These organs accumulate amounts of water and

are protected against evaporation by epidermises and highly impermeable cuticles.

Water accumulated in these tissues maintains turgor of photosynthetic tissues during

prolonged dry spells. Succulent leaves are rather frequent in epiphytic species belong-

ing to the families Piperaceae, Gesneriaceae, Orchidaceae (developing also succulents

pseudobulbs), and Bromeliaceae.

3. Sclerophyllous photosynthetic organs resistant to desiccation and with high-nutrient use

efficiency. These characteristics are found within the epiphytic Ericaceae and Rubiaceae

that form fiber-rich leaves with highly impermeable cuticles. These leaves are long-lived,

have low-nutrient concentration per unit dry weight, and are desiccation resistant.

4. Specialized mechanisms for water and nutrient uptake. The bromeliad leaves, particu-

larly within the subfamily Tillandsioideae, possess specialized trichomes for the uptake

of water and nutrients. Orchid roots, on the other hand, are covered by a hygroscopic

tissue operative in the absorption of water and nutrients, the velamen. According to

Benzing et al. (1983) this structure may be important in explaining the predominance

of orchids in epiphytic tropical habitats.

5. Mutualistic symbiosis. Mycorrhizae are a common feature of vascular plants in the

tropics (Janos 1983). Among the richest group of epiphytic plants, the orchids, a highly

specialized mycorrhiza, dominate. Orchid seeds are not nutritionally independent and

associate with fungi to complete their germination process until they reach photosynthetic

independence. Later, they develop permanent mycorrhizal associations.

6. High water use efficiency and nocturnal CO

fixation. A large number of epiphytes

among the Orchidaceae, Bromeliaceae, and Cactaceae, particularly those of strongly

seasonal forests, are capable of nocturnal CO

fixation via CAM. CO

taken up during

the night is accumulated in the vacuoles as malic acid. This acid is remobilized during

the following day, decarboxylated in the cytoplasm, and the evolving CO

is taken up

via the photosynthetic reduction cycle in the chloroplasts. In this process, stomata

open during the night and remain closed during part of the day, depending on

the water status of the photosynthetic tissue and the actual amount of malic acid

accumulated. The consequence of this inverted stomatal rhythm is a high water use

efficiency (amount of water transpired per unit carbon taken up).

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Tropical Forests: Diversity and Function of Dominant Life-Forms 335

Ecophysiology of CAM Epiphytes

CAM plants may be constitutive or facultative (Winter 1985, Medina 1990). The former

show CAM characteristics under a wide range of environmental conditions, whereas the latter

only show CAM under conditions of water or salt stress. Most CAM plants in the tropics are

constitutive, as the number of facultative species described is limited. There are two variations

in the nocturnal organic acid accumulation process that are considered to be related to CAM

and are frequently found in epiphytes of humid forests: CAM-idling and CAM-cyc1ing

(Kluge and Ting 1978, Benzing 1990). In both processes, nocturnal increases of acid concen-

tration are observed without net CO

uptake from the atmosphere. CAM-idling occurs in

water-stressed constitutive CAM plants and results from the refixation of respiratory CO

(Szarek et al. 1973, Ting 1985), whereas CAM-cyc1ing occurs in tissues without water stress

(Ting 1985). CAM-cyc1ing has been hypothesized to be a precursor of full-CAM plants

(Monson 1989, Martin 1994), but it is still not clear why the reduction in internal CO

partial

pressure resulting from fixation of respiratory CO

during the night does not influence

stomatal behavior.

The following ecophysiological features are essential to understand the abundance and

ecological significance of CAM in humid tropical forests:

1. High water use efficiency. Constitutive CAM plants take up CO

mainly during the

night, when the leaf-air water vapor saturation deficit is lower. High water use

efficiency associated with the succulent morphology of photosynthetic organs allows

the maintenance of a positive carbon balance in drought-prone habitats, and is

therefore crucial for the occupation of exposed epiphytic habitats in rainforests.

2. Respiratory CO

recycling. In many constitutive CAM plants, simultaneous measure-

ments of CO

exchange and organic acid accumulation during the night frequently

reveal that the increase in acid concentration is larger than that expected from

the amount of CO

taken up by PEP-carboxylase. Dark CO

fixation should yield

two acid equivalents (malic acid) per CO

molecule taken up. However, this is not the

case with several species of the Bromeliaceae and Orchidaceae, of the genus Clusia,

and in CAM ferns. This difference is apparently due to refixation of respiratory

(Griffiths 1988). Recycling of respiratory CO

may be a significant carbon

conservation mechanism under stressful environmental conditions.

3. Adaptation to shady environments. The numerous taxa with CAM in humid tropical

forests that can grow and compete with C3 plants in shady environments indicate that

CAM by itself does not appear to be a liability in low-light environments. In humid

forest environments, shade-adapted CAM plants have growth rates and net carbon

gains similar to those of C3 plants that are limited by low light (Martin et al. 1986,

Medina 1990). It seems that CO

fixation during the night by CAM plants might be

favored by the high CO

concentrations of the air under the canopy of humid tropical

forests (Martin 1994).

Occurrence of CAM in Specific Groups of Epiphytes

The number of epiphytic genera with reported CAM species is substantial (Table 10.4) and is

clearly dominated by orchids.

Pteridophytes. Only species of the genera Pyrrosia (Hew and Wong 1974, Ong et al. 1986,

Winter et al. 1986, Kluge et al. 1989b) and Microsorium (Earnshaw et al. 1987) have been

reported as CAM plants among ferns. Pyrrosia longifolia can be found growing under fully

exposed or shaded conditions in humid tropical forests, performing CAM in both conditions.

In both populations, the proportion of total carbon gain derived from night CO

fixation is

similar as indicated by their d

C values (Winter et al. 1986).

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336 Functional Plant Ecology

The question of how CAM may have evolved within the Polypodiaceae has been dis-

cussed by Kluge et al. (1989a) and Benzing (1990). All relatives of the genus Pyrrosia grow in

humid, shady environments; therefore, it seems improbable that the CAM species are derived

TABLE 10.4

Families and Genera in Which Epiphytic CAM Species of Humid Tropical Forests

Have Been Reported

Family

Genera with CAM Species

Polypodiaceae Pyrrosia

Microsorium

Bromeliaceae Acantostachys Canistrum Tillandsia

Aechmea Hohenbergia Portea

Araeococcus Neoregelia Quesnelia

Billbergia Nidularium Wittrockia

Bromelia Streptocalyx

Orchidaceae (~500 genera and

more than 20,000 epiphytic species)

Bulbophyllum Luisia Robiquetia

Cadetia Micropera Saccolabiopsis

Campylocentrum Mobilabium Saccolabium

Cattleya Oberonia Sarchochilus

Chilochista Oncidium Schoenorchis

Cymbidium Phalenopsis Taeniophyllum

Dendrobium Pholidota Thrixspermum

Epidendrum Plectorrhiza Trachoma

Eria Pomatocalpa Trichoglottis

Flickingeria Rhinerrhiza Vanda

Asclepiadaceae Hoya

Dischidia

Cactaceae (25 epiphytic genera,

most probably all CAM)

Epiphyllum

Hylocereus

Rhipsalis

Strophocactus

Zygocactus

Clusiaceae Clusia

Oedematopus

Crassulaceae Echeveria

Sedum

Gesneriaceae Codonanthe

Piperaceae Peperomia

Rubiaceae Myrmecodia

Hydnophytum

Sources: Data from Coutinho, L.M., Bol. Fac. Filosofia, 288, 81, 1963, Coutinho, L.M., Novas observac¸oes sobre a

ocorrencia do ‘‘Efeito de DeSaussure’’ e suas relac¸oes com a suculencia, a temperatura folhear e os movimentos

estoma

ticos. Boletin Faculda

de de Filosofia, Ciencias e Letras, Universidade de Sao Paulo, 331, 1969; McWilliams,

E.L., Bot. Gazette, 131, 285, 1970; Medina, E., Evolution, 28, 677, 1974; Medina, E., Delgado, M., Troughton, J.H., and

Medina, J.D., Flora, 166, 137, 1977, Medina, E. and Cuevas, E., Mineral Nutrients in Tropical Forest and Savanna

Ecosystems, J. Proctor, ed., Blackwell Scientific Publications, Oxford, 1989; Griffiths, H. and Smith, J.A.E., Oecologia,60,

176, 1983; Ting, L.P., Bates, L., Sternberg, L.S.L., and DeNiro, M.J., Plant Physiol., 78, 246, 1985; Winter, K., Wallace,

B.J., Stocker, G.C., and Roksandic, Z., Oecologia, 57, 129, 1983, Winter, K., Medina, E., Garcı

a, V., Mayoral, M.L., and

Mun

iz, R., J. Plant Physiol., 111, 73, 1985; Earnshaw, M.J., Winter, K., Ziegler, H., Stichler, W., Cruttwell, N.E.G.,

Kerenga, K., Cribb, P.J., Wood, J., Croft, J.R., Carver, K.A., and Gunn, T.C., Oecologia, 73, 566, 1987; Griffiths, H.,

Ecol. Stud., 76, 42, 1989; Benzing, D.H., Vascular Epiphytes, Cambridge University Press, Cambridge, 1990; Lu

ttge, U.,

ed., Vascular Plants as Epiphytes. Ecological Studies, Vol. 76, Springer-Verlag, Berlin, 1991; Martin, C.E., Bot. Rev.,60,1,

1994; Franco, A.C., Olivares, E., Ball, E., Lu

ttge, U., and Haag-Kerwer, A., New Phytol., 126, 203, 1994.

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Tropical Forests: Diversity and Function of Dominant Life-Forms 337

from xerophytic ancestors. In this particular case, it appears that high light and frequent low

humidity, characteristic of epiphytic environments, may have been the selective factors

leading to the development of CAM in this genus. In addition, ferns are a group of plants

highly dependent on continuous water availability during their gametophytic stage. It seems

more feasible that CAM ferns are derived from shade forms in humid forests, and that CAM

evolved secondarily in the epiphytic environment (Kluge et al. 1989a).

Gesneriaceae and Piperaceae. The Gesneriaceae and Piperaceae have a large number of

epiphytic species, many of which are succulent. In a few species (Codonanthe crassifolia in the

Gesneriaceae and approximately 15 species within the genus Peperomia), CAM activity has

been detected only as acid accumulation during the night period (Ting et al. 1985, Guralnick

et al. 1986). Their isotopic composition indicates that all carbon used for growth derives from

daytime CO

uptake, but their dD values are more similar to those of CAM plants than to

those of C3 or C4 plants (Ting et al. 1985).

Orchidaceae and Bromeliaceae. Orchids and bromeliads contain the largest number

of epiphytic species with constitutive CAM metabolism, and many grow under partial- or

heavy-shade conditions. The orchids occupy pantropical epiphytic habitats, whereas the

bromeliads are restricted to the neotropics. Both families contain epiphytic and terrestrial

species with typical CAM, expressed in gas exchange patterns, nocturnal malic acid accumu-

lation, and reduction of nonstructural carbohydrate content during the night (Coutinho 1969,

McWilliams 1970, Medina 1974, Neales and Hew 1975, Goh et al. 1977, Griffiths and Smith

1983, Lu

ttge et al. 1985, Goh and Kluge 1989). There are several accounts on the morpho-

logy, physiology, and ecology of epiphytes in these two families (Benzing 1990, Martin 1994,

Medina 1990, Lu

ttge 1991).

Distribution of epiphytic species of orchids and bromeliads is correlated with atmospheric

humidity. In montane forests, the proportion of CAM epiphytes decreases with altitude in

direct correlation with air humidity (Earnshaw et al. 1987, Smith 1989).

The larger genera of bromeliads and orchids contain both C3 and CAM species. The genus

Tillandsia in the Bromeliaceae, for instance, has species ranging from dry to humid forests.

CAM species predominate in the former, while C

species predominate in the 1atter. Another

bromeliad genus, Aechmea, contains only CAM species, some of which are restricted to

the floor of humid forests. In the Orchidaceae, similar photosynthetic diversity can be observed

in the genera Bulbophyllum (1000 epiphytic species) and Dendrobium (900 epiphytic species). In

these genera, there is an almost continuous variation in d

C values, from less than 30%

to 12%. CAM activity in these orchid genera is correlated with the development of succu-

lence. This morphologica1 property is associated both with the presence of cells with big

vacuoles, where malic acid is accumulated during the night, and with the development of

water-storage parenchyma, often photosynthetically inactive. For example, the leaf thickness

of high-altitude orchids in upper montane forests of Papua New Guinea, is due to the

development of a chlorophyll-free hypodermis (Earnshaw et al. 1987), very similar to that

described for Peperomia spp. (Ting et al. 1985) and Codonanthe spp. (Guralnick et al. 1986,

Medina et al. 1989).

Roots of many orchid species contain chloroplasts that are photosynthetically active

(Benzing et al. 1983). Chloroplast-bearing cells, specialized in photosynthesis, and mycor-

rhizal cells, specialized in nutrient uptake, coexist in the roots of some leafless species. These

roots are capable of performing CAM (Winter et al. 1985).

The process of shade adaptation of CAM plants in view of the relatively higher energetic

requirement merits more research at the biochemical level. A number of epiphytic CAM

bromeliads grow in a wide range of light conditions, although their abundance tends to

increase under full sun exposure (Pittendrigh 1948, Smith et al. 1986).

Cactaceae. Differentiation between terrestrial and epiphytic species in the Cactaceae is

more pronounced. There is no genus with both terrestrial and epiphytic species; however,

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338 Functional Plant Ecology

several climbing and decumbent species are found within the genera Acanthocereus and

Heliocereus. The epiphytic cacti are confined within the tribes Rhipsalidanae (8 genera),

Epiphyllanae (9 genera), and Hylocereanae (9 genera) within the subfamily Cereoideae

(Britton and Rose 1963). The photosynthetic metabolism of epiphytic cacti has been studied

in only a few genera (Tab1e 10.4), but there is little doubt that all the species are most likely

constitutive CAM plants. Species growing in deep shade, such as Strophocactus witti (Medina

et al. 1989), are damaged when exposed to high-light intensity, yet they show typical CAM

gas exchange and acid accumulation.

FOREST DYNAMICS AND CLIMATE CHANGE

What are the roles tropical forests are playing in the carbon balance of the atmosphere?

Answers to this questions are in the center of a debate to identify where is the

sink for approximately 2 Pg of carbon that are produced by the combustion of fossil

fuels and deforestation in the tropics (Tian et al. 1998, Grace 2004). The answer requires

(1) an accurate assessment of the impact of increasing atmospheric CO

concentrations

and temperature on the forest productive capacity and the accumulation and turnover of

organic matter and (2) a precise estimation of the magnitude of deforestation in the

tropics. The first part may be accomplished using experimental approaches such as meas-

uring the increase in photosynthetic carbon fixation in isolated plants or whole sections of

natural ecosystems, or using forest inventories to estimate biomass. The second aspect is

dealt with successfully using remote sensing techniques (http:== www-gvm.jrc.it=glc2000=;

http:== lpdaac.usgs.gov=modis=).

Grace et al. (1995) published a report showing that a forest site in the Amazon basin was

acting as a carbon sink during the period of measurements (55 days including wet and dry

seasons). The report generated a strong response in the scientific community involved in

global change and biogeochemical research. The study was based on the use of micrometeoro-

logical techniques to measure CO

fluxes into the forest, and has been subjected to severe

scrutiny regarding the accuracy and the capability of this methodological approach to be

expanded to large forests tracts.

In the assessment of forest C balance long-term measurements and climate variations

has to be taken into account before concluding if a certain forest tract is a source or a sink.

The impact of seasonal and episodic events on the forest net primary productivity was

analyzed by Tian et al. (1998) using a transient process-based biogeochemical model of

terrestrial ecosystems. During El Nin

o years the hot, dry weather caused most of the

Amazon basin to act as a source (0.2 Pg in 1987 and 1992). In wet years the same systems

acts as sink (0.7 Pg C in 1981 and 1983). During the same period deforestation accounted

for 0.3 Pg C per year.

Mahli and Grace (2000) argue that the lack of any significant tropical source detected in

the distribution of atmospheric CO

, in spite of the large CO

efflux brought about by

deforestation indicates the presence of a large tropical sink amounting to 1–3 Pg C per

year. The accumulation of micrometeorological data in several undisturbed forests sites

within the Amazon basin shows that carbon balance in generally negative, that is, forest

are acting as carbon sinks (Andreae et al. 2002). A long-term study using eddy covariance

methods in Santarem, Brazil gave unexpected results (Saleska et al. 2003). The forest studied

lost C during the wet season and gained it in the dry season. Calculated losses over the 3 year

period were 1.3  10

Mg ha

1

year

1

. This net loss was attributed to recent disturbances

superimposed on long-term C balances, but the authors indicate that this kind of disturbance

is characteristic of old-growth forests and probably reduce the carbon sequestration values

reported by other studies using similar methodology.

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Tropical Forests: Diversity and Function of Dominant Life-Forms 339