Agroforestry Systems 40: 97–104, 1998.

 1998 Kluwer Academic Publishers. Printed in the Netherlands.

Trema micrantha (L.) Blume (Ulmaceae):

A promising neotropical tree for site amelioration of
deforested land

C. VÁZQUEZ-YANES
Instituto de Ecología, UNAM, Apartado Postal 70-275, Ciudad Universitaria, 04510 Mexico
D. F. Mexico; E-mail: cvazquez@miranda.ecologia.unam.mx

Key words: avian wildlife, pioneer trees, secondary succession, tropical rainforest

Abstract. The genus Trema includes many species that are fast growing, short living pioneer
trees common in early successional vegetation and large recent gaps of many tropical moist
forests. They establish themselves and grow in open sites with microclimatic and soil conditions
which are contrasting to those prevailing in dense forests. With time they change the environ-
mental conditions by attenuating the wide alternations of soil temperature and lower midday
air relative humidity characteristic of open places. At the same time, soil moisture and organic
matter content as well as nutrient levels increase due to the reestablishment of an organic cycle
in the soil. Consequently they help generating an environment that permits the establishment of
mature forest species that often do not survive under the environmental conditions of open places.
The propagules of mature forest trees can be reintroduced from conserved areas nearby. The
biological and ecological traits related to the potential use of T. micrantha for site amelioration
previous to the reintroduction of mature forest trees are presented in this paper. Furthermore,
some preliminary experiences in the field are cited. The same use may apply to other fast
growing, short living pioneers.

Introduction

The pantropical genus Trema (Ulmaceae) contains between 14 and 55 species,

according to taxonomic reviews from different authors (Sweitzer, 1971). Some
of the species are fast growing, short living pioneer trees, common in early
successional fallows and large recent gaps of many tropical moist forest of
the world. Plants of T. orientalis have been described in secondary vegeta-
tion since the earliest studies of tropical forest succession in Asia (Symington,
1933; Wyatt-Smith, 1949). The same can be said about T. guineensis of Africa
(Aubreville, 1947) and T. micrantha of tropical America (Kenoyer, 1929;
Shulz, 1960). These species belong to the group of plants called pioneers
that evolved to occupy occasional canopy openings resulting from the occur-
rence of natural disturbances in the tropical moist forest ecosystems
(Whitmore, 1989). Consequently they show adaptations to some of the envi-
ronmental conditions created by human induced forest perturbations like the
capacity to become established and grow in open sites with microclimatic and
soil conditions contrasting with those prevalent in dense forest (Vázquez-
Yanes and Orozco-Segovia, 1993). These plants are often the first colonizers
98

of places that have been heavily perturbed by natural causes like earthquake
originated landslides that destroy the natural vegetation. A very good example
of this phenomenon has been described for Panama (Garwood et al., 1979).
Trema trees are also frequent along the edge of roads built through forests in
the tropics (Corner, 1940).
During their growth these plants may gradually restore the conditions of
the forest: the wide alternations of soil temperature and air relative humidity
characteristic of open places are attenuated by the development of a canopy.
At the same time, soil moisture and soil organic matter content as well as
nutrient content may increase due to the enhancement of the organic cycle.
Consequently an environment is generated that allows the establishment of
mature forest species when their propagules are still available.
In this paper we review the biological and ecological traits related to the
potential use of an early successional pioneer T. micrantha for site ameliora-
tion previous to the reintroduction of mature forest trees and for some
agroforestry practices. The same possibilities may apply to other pioneer
neotropical genera like Cecropia, Heliocarpus, Didimopanax, Robinsonella
and others.

The species

T. micrantha plants are fast growing heliophile, small to medium sized trees
that can be found in tropical moist forest in Southern Florida (there are
differing versions about the classification of the species in Florida) and from
Mexico to Northern Argentina. A number of detailed botanical descriptions
have been published elsewhere (e.g. Nevling, 1960; Nee, 1993). In Mexico
the species can be found in several vegetation types ranging from tropical
lowland evergreen rainforest and moist semideciduous forest to mountainous
mesophilous forest. In the latter case, they can be found close to the altitu-
dinal level where occasional freezing temperatures may occur. It is particu-
larly abundant along the southeastern coastal plains of the Gulf of Mexico
(Nee, 1993).
In secondary vegetation and regenerating forest gaps the life span of this
and other pioneer trees is short. After about 30 years they are usually com-
pletely replaced by longer living mature forest trees (Gómez-Pompa and
Vázquez-Yanes, 1981)

Reproductive biology

T. micrantha trees produce once a year very abundant inflorescences with

small monoecious, staminate and pistillate flowers. Mostly, the trees are
monoecious but sometimes dioecious trees can be found. Pollination is
achieved by a diversity of small insects (Bawa et al., 1985). Most trees develop
 99

massive amounts of small reddish spherical drupes of about 3 mm diameter.

The drupes have a succulent juicy exocarp and a hard endocarp with one seed.
The reproductive season in the northern hemisphere commonly starts in May
and frequently lasts until December. Fruits are most abundant during summer
(Vilamajo, 1985) and are eaten by a wide diversity of birds. A study showed
that in the tropical humidity of Mexico about 25 local and migrant birds
carry these seeds in their feces (Trejo, 1976). Most seeds collected from the
feces are viable so we infer that seed dispersal by birds is effective in most
cases.
The seeds are small and show the distinctive orthodox storage behavior,
therefore they can be kept alive in seed banks at low temperature. The seeds
are for sale by some seed providers in Latin America (Ettori et al., 1988).
The seeds T. guineensis and T. orientalis are often found in the soil seed
bank of old world forests (Alexandre, 1978; Cheke et al., 1979). The seeds
of T. micrantha have also been found in significant numbers in the soil seed
bank of a tropical American forest (Dalling et al., 1997). Seedlings are also
frequent in the tropical forest gaps of Mexico and Central America (Brokaw,
1985; Popma et al., 1988), therefore a combination of efficient seed dispersal
and temporary dormancy in the soil should be responsible for the abundance
of these species in secondary forests.
Freshly collected seeds germinate easily after 20 days of seeding, thus
reaching a relatively high seed germination percentage (70%) either at constant
or fluctuating temperatures between 20° C and 35 °C. They require white light
for germination (Vázquez-Yanes, 1976). On the contrary, T. guineensis show
endogenous dormancy lasting for a few months (Vázquez-Yanes, 1977).
Woody segments of the trees root easily in laboratory conditions by means
of commercial rooting hormones. This makes vegetative propagation an easy
task (personal observation).

Growth

T. micrantha trees are very fast growing. In Costa Rica growth rates after
establishment in forest gaps may reach 6 m during the first year of growth
and the adult size of 20 m after seven years (Brokaw, 1985). The fast growth
of this evergreen species is the result of a combination of factors: the buds
develop continuously forming new heliophyle foliage, and shadowed leaves
are soon replaced. Consequently they produce an abundant and continuously
leave deposition in the soil (Ewel, 1976). The predominance of fresh leaves
in the canopy which are fully exposed to direct sunlight allows an optimal
capture of energy. As in T. guineensis (Coombe, 1960), there is low invest-
ment in wood tissue which is porous and moist. It has a specific gravity (WSG)
of 0.45, which is lower than that of many mature forest trees and similar to
other pioneers from a Mexican forest (Barajas-Morales, 1987). Finally, the
architectural pattern of growth and branching allows the continuous forma-
100

tion of new buds which produce new branches that keep growing toward the
sunlight (Castro e Santos, 1980).
The rate of photosynthesis expressed as Net Assimilation Rate of T.
guineensis is 14 g/m2/week. This rate, however, if similar to that of T.
micrantha, could not explain by itself the fast growth without the combined
effect of the architectural and phenological components (Coombe, 1960).
This also applies to most pioneer trees (Gómez-Pompa and Vázquez-Yanes,
1981).

Root symbiosis

Trema is the closest relative of the only genus outside the legumes that present
nodules infected with nitrogen fixing bacteria of the genus Rhyzobium. This
is the genus Parasponia from tropical Asia. Some species of Trema have some
of the genes of the hemoglobin involved in nitrogen fixation but until today
the capability of nitrogen fixation has not been proved for Trema (Andersson
et al., 1997). However, most of the pioneer fast growing species of Trema,
which are probably the best candidates for nitrogen fixation, have not yet been
studied. Also, the philogenetic closeness between Parasponia (previously
classified as Trema) and Trema itself suggest that transplantation techniques
or possibly genetic engineering by using genes of Paraspomia may conduce
to the development of nitrogen fixing capabilities in some Trema species. This
genetic transformation, if performed, will undoubtedly increase the impor-
tance of the species for agroforestry practices.
T. michranta roots present abundant vesicular arbuscular mycorhiza (St.
John, 1980).

Multipurpose uses

The soft wood of T. micrantha is not of much use other than combustion for
cooking and construction of rudimentary, short lasting rural structures
(personal observations). Other uses in Mexico include the utilization of its
fibrous bark to tie up objects and, in some places, the bark is smashed to
produce a substitute of a traditional bark paper (originally made from Ficus
spp) used in indigenous handicrafts. Finally, leaf infusions are sometimes used
for measles treatment in ethnic medicine (Nee, 1993). Furthermore, its cream
colored wood composed mainly of cellulose shows greater wood specific
gravity (0.45) than other common pioneers like Heliocarpus appendiculatus
(0.19) or even trees commonly used for paper pulp production like Ceiba
pentandra (0.38) (Barajas-Morales, 1987). Consequently, because of their
extremely fast growth, more research is needed on the potential value of
T. micrantha for the production of cellulose.
Some experiments for the use of fodder of T. micrantha in animal nutri-
 101

tion have been performed in Brazil. Studies of nutrient content indicate the
presence of a reasonably high protein content for cattle nutrition (Andrade et
al., 1976a).
An experiment with monogastric animals, in this case chicken, which
included the mixing of up to 5% fodder with regular chicken food showed
satisfactory results. Pigments present in the leaves help to intensify the
yellowish color of the epidermis which most customers relate to qualify when
buying chicken in Brazil (Ariki et al., 1980).
Finally, T. micrantha can be a valuable source of food for numerous species
of birds when the restoration of the vegetation of an area should include the
amelioration of the habitat for the native and migratory aviary fauna. The
attraction of birds from nearby forests to feed on T. Micrantha drupes can
accelerate forest succession and the growth rate of a site’s species diversity
due to the arrival by avian seed dispersal of new plant species (McClanahan
and Wolfe, 1993).

Site amelioration

Several local Brazilian publications suggest the potential value of T. micrantha

for site amelioration in deforested areas (Carpanezzi et al., 1990; Rocha-
Ferretti et al., 1995). Forest tree seedlings have been growing in the shade of
developing pioneer trees including T. micrantha because they provide partial
shade and protection from heavy rain and wind (Kageyama, 1989).
One of the most enlightening trials is being performed in the State of Minas
Gerais in Brazil in order to restore a protective vegetation on deforested land
around a new dam reservoir (Botelho et al., 1996). Six native forest species
were planted in a denuded field: 3 pioneers including T. micrantha and 3
mature forest trees. Fertilizer (N-P-K, 100 g/plant) was applied at the
beginning of the experiment. After 5 month the fastest growing tree was T.
micrantha which provided shade and the formation of a litter layer that
benefited the other plants. The most limiting soil for the growth of T.
micrantha was compact latosoil, but this problem can be reduced by deep
plowing before tree planting (Botelho et al., 1995).
Seeds of T. micrantha mixed with seeds of Malastomataceae species and
some other pioneers have been used to produce pellets, which also contain
mineral nutriments and a hydrophilic substance that helps absorption and
maintenance of moisture from the soil. These pellets have been transported
on airplanes for dissemination from the air over deforested hills in coastal
areas of the State of São Paulo, with the purpose of speeding up the regen-
eration of a vegetation cover and reducing erosion. The results obtained were
successful in some places (Kageyama, 1989).
Unfortunately the Brazilian experiments relating to these subjects remain
to be thoughtfully described in formal international publications.
Agroforestry development in abandoned deforested tropical land can also
102

benefit from site amelioration by pioneer trees in the same way as described
before.

Discussion

After analyzing the available information on the biology, ecology and actual
and potential uses of T. micrantha, there is little doubt that it represents a
valuable resource to be more profusely used for site amelioration in forestry
and possibly in some agroforestry practices. The advantages of the plant for
these purposes are:
1. Propagation by seed or vegetative segments is easy. Seeds can be certified,
stored and traded in large numbers;
2. Seedlings and saplings survive in open places under full sunlight, toler-
ating relatively impoverished soils sometimes with the help of one single
fertilization event;
3. The very fast growth and acquisition of a crown shape generates a shade
that soon changes the microclimate beneath to a more stable temperature
and to moisture conditions that are adequate for the growth of shade
tolerant seedlings and saplings;
4. Due to the particular crown growth and leaf dynamics of this species, the
shade produced is still relatively rich in PAR radiation which allows the
growth of shaded plants. The plant produces abundant litter that soon
improves soil quality;
5. The short life span of Trema allows the growing shade tolerant trees to
occupy the space and reach the canopy after a reasonable period of time;
6. Due to the lack of specificity of the pollination and seed dispersal of the
plants, T. micrantha finds almost anywhere adequate pollinators and seed
disseminators;
7. Edible fruits for birds can attract birds from nearby forests which may
bring seeds of new plant species into cleared land.
Tropical fast growing pioneer species represent a valuable resource to
develop site amelioration techniques that may help transforming areas for
forestry and agroforestry purposes.

Acknowledgements

This work was partially supported by the Mexican Council of Science and
Technology (CONACYT) Grant G0011-N for ‘Basic Research on Ecological
Restoration’. MC Mariana Rojas gave helpful support in the search for ref-
erences.
 103

References

Alexandre DY (1978) Observations sur l’écologie de Trema guineensis en basse Côte d’Ivoire.
Cah. O.R.S.T.O.M. 13: 261–266
Anderson CR, Llewellyn DJ, Peacock WJ and Dennis ES (1997) Cell-Specific expression of
the promoters of two nonlegume hemoglobin in a transgenic legume, Lotus corniculatus.
Plant Physiol 113: 45–57
Andrade P, Vieira PF, Rosa ICA and Andrade AT (1976) Trema micrantha Blume na
alimentação animal. I. Estudos preliminates e composição bromatológica. Acta Amazonica
6: 91–94
Ariki J, Donola E, Macedo EM, Rodrigues ME and Rodrigues AM (1980) Trema micrantha
Blume na alimentção de poadeiras comerciais. Acta Amazonica 10: 697–699
Aubreville A (1947) Les brouses secondaires en Afrique Equatoriale, Côte d’Ivoire, Cameroun,
A.E.F. Bois et Forèts tropiq 2: 24–49
Barajas-Morales J (1987) Wood specific gravity in species from two tropical forest in Mexico.
IAWA Bull 8: 143–148
Bawa KS, Bullock SH, Perry DR, Coville RE and Grayum MH (1985) Reproductive biology
of tropical lowland rain forest trees. II. Pollination systems. Am J Bot 72: 346–356
Botelho SA, Davide AC, Schmidit-Prado N and Fonseca EM (1995) Implantsaô de mata ciliar,
Belo Horizonte. Companhia Energetica de Minas Gerais and Universidade Federal de Lavras,
28 pp
Botelho SA, Davide AC and Rocha-Faria JM (1996) Desenvolvimento inicial de seis espécies
nativas em dois sítios, na regiâo sul de Minas Gerais. CERNE (Universidade Federal de
Lavras) 2: 43–52
Brokaw, NVL (1985) Gap-phase regeneration of three pioneer species in a neotropical forest.
Ecology 66: 682–687
Carpanezzi AA, Da Silva-Costa LG, Kageyama PY and Ferreira C (1990) Funcôes multiplas
das forestas: Conservacâo e recuperacâo do meio ambiente. Congreso Florestal Brasileiro,
Campos de Jordâo, SP. Comissâo Tecnica 5: 200–205
Castro e Santos, A de (1980) Essai de classification des arbres tropicaux selon leur capacité de
réitération. Biotropica 12: 187–194
Coombe DE (1960) An analysis of the growth of Trema guineensis. J Ecol 48: 219–231
Corner DE (1940) Wayside trees of Malaya. Government Printing Office, Singapore Vol. 1,
770 pp
Dalling JW, Dwaine MD and Garwood NC (1997) Soil seed bank community dynamics in
seasonally moist lowland tropical forest, Panama. Journal of Tropical Ecology 13: 659–680
Cheke AS, Nanakorn W and Yankoses C (1979) Dormancy and dispersal of secondary forest
species under the canopy of a primary tropical rain forest in Northern Thailand. Biotropica
11: 89–95
Ettori LC, Baitello JB and Figliolia MB (1988) Index Seminum. Instituto Florestal São Paulo,
Brazil, 17 pp
Ewel, JJ (1976) Litter fall and leaf decomposition in a tropical forest succession in Eastern
Guatemala. J Ecol 64: 293–308
Ferretti AR, Kageyama PY, Arboez GF, Dos Santos JD, Barros MI, Lorza RF and Oliveira C
(1995) Classificacâo das espécies arbôreas em grupos ecológicos para revegetacâo com
nativas no Estado de São Paulo. Florestar Estatístico 3: 73–77
Garwood NC, Janos DP and Brokaw N (1979) Earthquake-caused landslides: a major distur-
bance to tropical forest. Science 205: 997–999
Gómez-Pompa A and Vázquez-Yanes C (1981) Successional studies of a rainforest of Mexico.
In: West DC, Shugart HH and Botking DH (eds) Forest Succession, Concepts and
Applications, pp 246–266. Springer Verlag, New York
Kageyama PY (1989) Sucessâo secundária, estructura genética e plantaçoes de espécies arbóreas
nativas. IPEF, Piracicaba 41/42: 83–93
104

Kenoyer LA (1929) General and successional ecology of the lower tropical rain forest at Barro
Colorado Island, Panama. Ecology 10: 201–222
McClanahan TR and Wolfe RW (1993) Accelerating forest succession in a fragmented land-
scape: The role of birds and perches. Conservation Biology 7: 279–288
Nee M (1993) Ulmaceae. Flora de Veracruz, pp 28–33. Instituto de Ecología A. C. Xalapa,
Veracruz, México
Nevling LI (1960) Ulmaceae. Ann Mo Bot Gdn 47(2): 108–110
Popma J, Bongers F, Martínez-Ramos M and Veneklaas E (1988) Pioneer species distribution
in treefall gaps in Neotropical rain forest: a gap definition and its consequences. J Trop
Ecol 4: 77–88
Schulz JP (1960) Ecological studies on rain forest in northern Suriname. Mededelingen van het
Botanish Museum en Herbarium de Rijsuniversiteit te Utrecht 163, 267 pp
St. John T (1980) Uma lista de espécies de plantas tropicais brasileiras naturalmente infectadas
con micorriza vesicular-arbuscular. Acta Amazonica 10: 229–234
Sweitzer EM (1971) Comparative anatomy of Ulmaceae. J Arnold Arbor 52: 523–585
Symington CF (1933) The study of secondary growth on rain forest sites. Malay Forester 2:
107–117
Trejo L (1976) Diseminación de semillas por aves en ‘Los Tuxtlas’, Veracruz. In: Gómez-Pompa
A, Vázquez-Yanes C, Del Amo S and Butanda A (eds) Regeneración de selvas, pp 447–470.
Compañía Editorial Continental, México D. F.
Vázquez-Yanes C (1976) Estudios sobre ecología de la germinación en una selva cálido-húmeda
de México. In: Gómez-Pompa A, Vázquez-Yanes C, Del Amo S and Butanda A (eds)
Regeneración de Selvas, pp 289–387. Compañía Editorial Continental, México D. F.
Vázquez-Yanes C (1977) Germination of a pioneer tree (Trema guineensis Ficahlo) from
equatorial Africa Turrialba 27: 301–302
Vázquez-Yanes C and Orozco-Segovia A (1994) Signals for seeds to sense and respond to
gaps. In: Caldwell M and Pearcy R (eds) Exploitation of Environmental Heterogeneity by
Plants, pp 209–236. Academic Press, San Diego CA
Vilamajó D (1985) Comportamiento fenológico de especies de vegetación secundaria en Sierra
del Rosario, Cuba. Ciencias Biológicas 13: 51–58
Whitmore, TC (1989) Canopy gaps and the two major groups of forest trees. Ecology 70:
536–538
Wyatt-Smith J (1949) Natural plant succession. Malay Forester 12: 148–152