Best management practices in Agriculture for sustainable use and conservation of

pollinators

Agreement FAO- S. Paulo University

Vera Lucia Imperatriz-Fonseca Ecology Department, Biosciences Institute, S. Paulo University

Rua do Matão, travessa 14, n.321. CEP 05508-900 São Paulo, Brasil

2

How to get stingless bees nests in

Nature? Considerations on nesting

behavior and concerns on resources

availability

3

Contents Abstract Foreword Best management practices in Agriculture for sustainable use and conservation of pollinators Introduction 1. How to get stingless bees nests in Nature? Considerations on nesting behaviour and concerns on resources availability

2. Forestry and pollinators conservation

Trees for bees- Annex 1

Table 1. Plant families and their species used for stingless bees for nesting

Table 2. Plant species in alphabetic order used by stingless bees for nesting

Table 3. Stingless bees, in alphabetic order, and the trees used by them for nesting

Table 4. Brazilian biomes with respective stingless bees species and the plants species used as their nest sites

Table 5. World data on stingless bees and the trees used as their nest sites

Table 6. Plants recommended for environmental restoration and used as nest sites by Meliponine bees.

Bees and their floral resources- Annex 2 Table 1. Plants species used by stingless bees as floral resources

Table 2. Plants recommended for environmental restoration in Brazil and used as floral resources for social bees (bumblebees, stingless bees and honeybees).

Tetragonisca angustula: Bee plant calendar in an urban garden; trees for nesting and databank of flowers visited Annex 3

General remarks on the importance of Tetragonisca angustula as a flag species

Table 1. Floral calendar for social bees in an urban garden

Table 2. Floral calendar for Tetragonisca angustula in an urban garden

Table 3. Trees used as resources for Tetragonisca angustula

Table 4. Floral resources for Tetragonisca angustula in Latin America

4

Abstract Stingless bees biodiversity, abundance and nest densities were discussed based on

available literature in tropical areas of the world. In this report we focus on resources

needed by stingless bees survivorship, mainly shelter and food availability. Their

biodiversity is influenced by the quality of their environment. Human activities as

logging and habitat disturbance by agricultural areas were also shown to modify their

communities.

Nests sites for stingless bees are told to be a limit for nests density. Besides, the

new rules for stingless bees keeping and meliponaries settlement in Brazil (resolution

from CONAMA 343), allow the use of trap nests as a source of nests in nature.

Nevertheless, research on the use of trap nests was not done in Brazil concerning

stingless bees. The ecological problems related to nesting were discussed, as well the

literature on trap nests in stingless bees. Annex 1 show data from trees that are used for

stingless bees to nidify in Brazil, in South and Central America and in Asia.

The quality of environment has an influence on stingless bees species composition

in the community, as well as bees as pollinators influence the natural areas botanical

composition through the ecosystem services provided by them. In wet lowland forest at

La Selva, more than 50% of canopy species and 36% of subcanopy trees were pollinated

by bees (Bawa et al. 1985). A change in the pollinator’s community will impact tree

composition and the whole food chain. This is very important for activities related to

forest use, as logging, and the recommendations for best practices with stingless bees and

other bees’ nests management. The general introduction concerns nesting behavior,

resources availability and considerations in logging activity, pollinators and forest

composition. Forestry is an important subject in Brazil nowadays.

Only a few species of stingless bees are used as pollinators in cultivars, mainly

because this is still new approach, a service that was taken for grant until recently.

Although they are generalists in their habits, there is a variation in size and preference for

different floral sources (Biesmeijer et al., submitted). In Annex 2 are data related to floral

resources visited by social bees, including stingless bees, in Brazil. They came for

published and unpublished papers, thesis and data of sparse observations mentioned in

literature and constitutes a data bank.

5

Annex 3 concerns the most common stingless bee in Brazil and in other Latin

American countries, Tetragonisca angustula. For this species a list of important floral

resources is presented, as well as a floral calendar for them in an urban area. Plant species

used as nests sites are also listed. T. angustula is used for crop pollination, and is one of

the species for which trap nests are attractive. Its honey is very appreciated and

considered as medicinal.

Key words: stingless bees, biodiversity, nest sites, trap nests, logging, resources, foraging.

6

Best management practices in Agriculture for sustainable use and conservation of pollinators. Foreword

Best management practices in Agriculture for sustainable use and conservation of

pollinators are focused in recent literature, and mainly by several authors that study

pollinators’ conservation. This means to carry on pesticides (a detailed study is in

preparation by Claire Kremen, p. com.) and their use in the crops; transgenic crops and

gene flow studies; environmental friendly agricultural practices, including land

preparation, in order to keep nests of solitary bees that occur in the soil; agricultural area

and maintenance of their borders with native vegetation, or hedges that can keep

pollinators; to decrease herbicides use in Agricultural crops, that helps the foraging

supply for pollinators and crop attractiveness for them, in larger areas.

Agricultural intensification includes a decline in the proportion of natural habitat, an

increase in pesticide usage, a decrease of floral resource on farm sites, as well as larger

field sizes, crop monocultures, intensive soil and water usages and the use of synthetic

fertilizers. Of course, the sustainability of Agriculture following these patterns of land use

is under concern by 21 Agenda for Agriculture.

All these issues are focused for some crops, mainly those of global commercial

importance. The recent International Pollinators Initiative’s plan of action really is

putting pollinators in the mainstream. Interesting papers focusing the ecosystem services

provided by pollinators were recently published, considering also their economic value,

and trying to measure this. A good example is related to coffee crops. Although this crop

does not depend obligatory on pollinators, Roubik (2002) showed that the feral

Africanized bees increased the coffee production in Central America. Also in coffee

plantation, de Marco & Coelho (2004), in Brazil, found that the farms near forest

fragments had an increase of 14,6% in production, that could be related to pollinating

services; Ricketts (2004) and Ricketts et al (2004) pointed out the importance of tropical

forest fragments to enhance pollinator’s activity in nearby coffee crops. These last studies

7

demonstrated the importance of stingless bees (10 species) as well as Africanized

honeybees Apis as pollinators. The distance between the crop and the fragment showed

that the use of the pollinators in transects along the agricultural areas should increase on

20% the crop production, as well as diminished the peaberries, resulting of unsuccessful

pollination. Based on this, and their analyses in three plots, the authors suggested an

economic value of the forest providing this ecosystem service and that this pollination

service could be paid, by the coffee producers, to the owner of the fragment; they also

present an estimate of the economic value of these natural fragments, based on this

evaluation. But economics of the pollination services is still rare in literature. Kevan and

Phillips (2001) did an estimative for apples, and also present a model to be applied in

economic value of crops. Drucker (2004) discussed the economic value of the bee

pollination services, and their implications for farm management and policy. Is this paper

he presents a selection of studies on economic value of pollination services by bees.

Kremen (2004) also considered the importance of bee community as crop

pollinators, pointing out that if we keep several bee species from natural environments

visiting flowers, the shortage of one species in one year could be compensated by the

other visitor’s species, diminishing the impact of pollinators shortage on crops. Ricketts

(2004) used the same approach considering plots with different percentage of bee species

visiting coffee flowers.

Although the importance of pollinators in Agriculture (see also weevils for oil

palm; bumblebees for tomatoes, among others; solitary bees for apple, pears and alfalfa,

for instance; stingless bees for strawberry, guaraná, açaí, coffee, among several other

crops; honeybees for several crops) is well known, until now their use is not remarkable

in undeveloped countries. But this situation will change very soon, because of new

initiatives concerning pollinators’ use in crops (for instance, the Brazilian Pollinators

Initiative) as well as from successful crops competing in world market, resulting from the

pollinators use in greenhouses, for instance. Developed countries are working with

pollinators’ shortage, although only a small number of them (a dozen, Kremen 2004) are

successful bred for agricultural use. If they are not available nearby due to the intensive

agricultural patterns using large areas, they are bought from biotech companies that breed

them successfully. These companies are multinational and have the technology of large

8

scale breeding. The best example is that of Bombus terrestris use in agriculture (their

breeding in laboratory conditions was successful only in 1985; nowadays, companies

worldwide sell 1 million of nests per year (Velthuis and Van Doorn, 2004). The

introduction of alien pollinators with defined breeding techniques is also undesirable, and

studies of ecological impact are asked in importation process. This will stimulate the

breading of native pollinators for the same service in countries with capacity building in

pollination area.

In many tropical and subtropical areas of the world, a new scenario opens

focusing stingless bees use as crop pollinators (Maeta et al.,1992; Slaa, 2001; Macias et

al., 2001; Cunningham et al., 2002; Malagodi- Braga & Kleinert, 2004; Cruz et al., 2004;

other related investigations were recently improved by Brazilian government). Best

management practices of pollinators in crops means best economic value, and in this

aspect both issues are together. Generally, producers are not interest in resistance (ability

to retain community properties under disturbance) or resilience (ability to recover from

disturbance) of crops when intensifying Agriculture, but in their economic value in this

season. Short time actions and market simulations are important in the producer’s

decisions on what crop to use in next season. They are linked to unpredictable weather

conditions, as well to the market fluctuation on crop values (Kevan and Viana, 2003), as

well as to the economic advantage in having better fruits. Long-term activities concerning

natural resources are almost not considered.

For this document the focus on best practices will be stingless bees (Meliponini).

They are the new possibility to face the pollinators’ shortage in the world. With a high

biodiversity, social, having local well-distributed species living in perennial colonies,

they are suitable for this new approach. Information around the world on Meliponini was

considered related to resources use (as nest sites and bee plants for food). A review was

prepared considering nests sites, in order to provide the list of plants that are used as nest

sites that could be included in official program of environmental compensation and

disturbed area restoration in Brazil. Also the food sources could be included in that list.

This program is a government request for those activities that damage the environment,

they have to restore additional areas. An infant industry arises with stingless bees

breeding in Australia (Heard & Dollin, 2000) and Brazil (Rosso et al., 2001). Their

9

potential use in large scale is in crop pollination (Heard, 1999). How to get nests in nature

and to breed them successfully is a challenge. Resources availability for them, as food

sources, will be discussed. Stingless bees’ breeding was recently ruled in Brazil. To get

nests in Nature, trap nests are allowed. Nevertheless, this is not a conventional practice

for us. A complete survey in literature was done in order to discuss this subject and to

make recommendation for next steps.

References

Eltz,T; Brühl, C.A ;Imiyabir, Z & Linsenmair, K. E. –2003- Nesting and nest trees of stingless bees (Apidae: Meliponini) in lowland dipterocarp forests in Sabah, Malysia, with implications for forest management. Forest Ecology and Management, v. 172, p. 301-313.

Cruz D de O, Freitas BM, Silva LA da, Silva SEM da, Bomfim IGA 2004 Use of the stingless bee Melipona subnitida to pollinate sweet pepper (Capsicum annuum L.) flowers in greenhouse. Proceedings of the 8th IBRA International Conference on Tropical Bees and VI Encontro sobre Abelhas, p.661.

Cunningham, S; FitzGibbon, F & Heard, T.A.-2002-The future of pollinators for Australian agriculture. Aust.J. Agric.Res.53: 893-900.

De Marco Jr, P & Coelho, F.M.-2004-Services performed by the ecosystem: Forest remnants influence agricultural cultures’ pollination and production. Biodiversity and Conservation, v.13, p. 1245-1255.

Drucker, A.G. 2004- Economic valuation of the bee pollination services: implications for farm management and policy. In: Freitas & Pereira ed., Solitary bees: conservation, rearing and management for pollination. Fortaleza, p.125-134.

Heard T.A. 1999 The role of stingless bees in crop pollination. Ann. Rev. Entomol. 44: 183-206.

Heard, T.A. & Dollin, A 2000- Stingless bees beekeeping in Australia, snapshot of an infant industry. Bee World, 82: 116-125.

Kevan. P.G. & Phillips,T.P.-2001- The economics impacts of pollinator declines:an approach to assessing the consequences. Conservation Ecology, v.5, n.1

Kremen, C- 2004. Pollination services and community composition: does it depend on diversity, abundance, biomass or species traits? In: Freitas & Pereira ed., Solitary bees: conservation, rearing and management for pollination. Fortaleza, p.115-124.

Macias MJO, Quezada-Euan JJG, Parra-Tabla V & Reyes OV 2001 Comportamiento y eficiencia de polinizacion de las abejas sin aguijon (Nannotrigona perilampoides) en el cultivo del tomate (Lycopersicum esculentum M) bajo condiciones de invernadero

10

en Yucatan, Mexico. II Seminario Mexicano sobre abejas sin aguijón. Memorias. Mérida, Yucatán, México, pp 119-124.

Maeta Y, Tezuka T, Nadano H, Suzuki K 1992 - Utilization of the Brazilian stingless bee, Nannotrigona testaceicornis, as a pollinator of strawberries. Honeybee Sci. 13: 71-78.

Malagodi-Braga KS & Kleinert AMP 2004 Could Tetragonisca angustula Latreille (Apinae, Meliponini) be used as strawberry pollinator in greenhouses? Aust. J. of Agric. Res. 55 (7): 771-773.

Ricketts, H. T. 2004- Tropical forest fragments enhance pollinators activity in nearby coffee crops. Conservation Biology, v. 18, n. 5, p. 1262-71.

Ricketts, H. T.; Daily, G.C.; Ehrlich. P. R. and Michener, C.D.-2004- Economic value of tropical forest to coffee production. Proc. of National Academy of Sciences, v. 101, n.34, p.12579-12582.

Rosso, J.M.L; Imperatriz-Fonseca, V.L & Cortopassi-Laurino, M. 2001. Meliponicultura en Brasil I: situation en 2001 y perspectivas. II Seminario mexicano sobre abejas sin aguijón-Memorias.Yucatan, Merida, p.28-35.

Roubik, D.W. (2002)- The value of bees in coffee harvest. Nature 417: 708.

Slaa EJ, Sanchez LA, Sandi M & Salazar W -2000 -A scientific note on the use of stingless bees for commercial pollination in enclosures. Apidologie 31: 141-142.

Velthuis, H.H.W. & van Doorn, A. -2004- The breeding, commercialization and economic value of bumblebees. In: Freitas & Pereira ed., Solitary bees: conservation, rearing and management for pollination. Fortaleza,135-149.

11

How to get stingless bees nests in Nature? Considerations on nesting

behavior and concerns on resources availability

Vera Lucia Imperatriz Fonseca- Depto. Ecologia, Instituto de Biociências, Universidade de S. Paulo. Rua do Matão, trav. 14, 321. CEP 05508-900.S. Paulo, Brazil

INTRODUCTION

Stingless bees biodiversity in fragmented Brazilian landscapes

A bee review in Boracéia Biological Station, Atlantic Rainforest in S. Paulo, showed that

it was the richest bee area sampled until now in Brazil, comprising 255 bee species with

38 stingless bees species. This analyzes was done 3 years round collecting bees on

flowers (Wilms et. al., 1996). Bee nests were not recorded.

Oliveira (2001) evaluated stingless bees in different seized fragments in

Amazonian forest. The used method was collections in forest fragments of 1, 10 and

100ha, as well as continuous forest sites and deforested areas. The bees were colleted in

six ways: by honey baits; by collecting clay; by collecting sweat; in flight; in their nests;

in flowers. Stingless bees belonging to 37 species were collected 37 in continuous forests,

11 in 100ha fragments, 22 in 10ha fragments, 21 in 1ha fragments and 25 in deforested

areas! He mentioned that in four fragments of 10ha and in five fragments of 1ha the

number of species found surpassed the number found in 100ha fragment. He also was

surprised with the number of species in the deforested area.

Another important study concerning different landscapes and stingless bees

richness was done in Rondônia (Brown & Albrecht, 2001). These authors analyzed the

landscape and used a method of collecting stingless bees species in Vernonia polyanthes,

an attractive food source for them, planted near the plots of different landscape quality

for samples. They were interested in determining whether deforestation has affected the

incidence of Melipona species. They found that M. seminigra abunensis and M. grandis

12

were common species, followed by M. rufiventris brachychaeta and M. melanoventer.

The rare species were M. schwarzi, M. fuliginosa and M. crinita.

Forests are difficult to be sampled (Ramalho, 2004). In Brazil several bee surveys

with standard methodology were done until now, mainly in open areas (Pinheiro-

Machado et. al., 2002). Data on bee-plant relationship are also available (for a

metanalysis, see Biesmejer et. al., submitted). The use of baits (sugar baits, salt baits,

chemical baits) as a standard method for biodiversity availability is not common yet in

our country, and a methodology must be assessed and tested (see Roubik, 1996 for a

standard methodology for stingless bees biodiversity estimates with baits, in Southeast

Asia).

Stingless bees nests

Stingless bees are a diverse and rich group of tropical and Neotropical bees. They

live in nests that can be aerial and constructed by themselves (as Trigona spinipes in

Brazil and Dactylurina stundigeri in Africa), but generally use natural hollows or man

made cavities for establishing their nests. The trees can be also used as a support for

aerial nests, including here nests from other social insects, as ants and termites. Scaura

latitarsis (Kerr et al., 1967) and Paratrigona impunctata (Camargo & Moure, 1994) in

Brazil, are examples of nesting inside termite nests; in Africa, the same occurs for

Apotrigona nebulata (Darchen, 1972). Cavities constructed by Atta ants and later

abandoned are used as nest sites for Paratrigona subnuda in disturbed habitats (including

agro ecosystems) (Imperatriz-Fonseca et al. 1970), and Schwarziana quadripunctata

(Camargo, 1974), among many others.

Roubik (1983) mentions the variation in nest sites preferences when analyzing

bees from Panama and comparing literature, appointing this plasticity in T. mirandula, T.

pallens, T. cilipes and T. hypogea. T. cilipes can be found in trunks (Roubik, 1983),

inside Azteca ant nests or termite nests (Kerr et al., 1967), showing a broader niche for

nests. A plasticity related to nests requirements is also verified towards these species that

make their nests in disturbed areas, as Tetragonisca angustula, for instance (see Annex

3).

13

Data on trees that hosts colonies of stingless bees are sparse in literature and are

listed in Annex 1. The majority of stingless bees species nest in preformed cavities in live

trees (Roubik, 1983; Sakagami et al., 1983; Salmah et al., 1990). Other can live in dead

trees (as Ptilotrigona lurida mocsaryi and Trigona fulviventris in Brazilian Amazon,

Oliveira et al. 1995; T. melanocephala and T. rufibasalis in Sarawak, Malaysia,

Samejima et al., 2004), including here those that have already felt (for instance, Duckeola

ghiliani, Kerr et al. op. cit.).

Stingless bees as Partamona batesi, P. gregaria, P. pearsoni, P. cupira among

several others nest inside active termite nests, whether epigeous or arboreous (Camargo

& Pedro, 2003). The Partamona genus and nests were recently reviewed and related

information show the large variety of nests sites used by this bee genus. According to

Camargo & Pedro (op. cit),

“All species endemic to western Ecuador to Mexico with known nesting

habits (P. orizabaensis, P. peckolti, P. xanthogastra, P. bilineata, P.

aequatoriana and P. musarum) build their nests in several substrates,

nonassociated with termitaria, such as cavities and crevices in walls, among

roots of epiphytes and in bases of palm leaves, in abandoned bird nests,

under bridges, and in other protected places, except P. peckolti that

occasionally occupies termite nests. In South America, on the eastern side of

the Andes, only P. epiphytophila and P. helleri nest among roots of

epiphytes and other substrates, non-associated with termitaria”.

In Africa, Darchen showed in his films (Stingless bees in African forests and

Apotrigona nebulata, SRFS) how vertebrate as birds and mammals make holes in

suitable nest sites, including termite nests, offering possibilities for stingless bees to make

their nests in them.

Nests can be also found in aggregates [Hypotrigona in Africa (Darchen, 1972);

Starr & Sakagami (1987) found 84 colonies of Trigona (Tetragonula) fuscobalteata and

T. (Tetragonula) sapiens in a bamboo house with an area of 68m2; Partamona cupira

(=orizabaensis, Camargo e Pedro 2003), in Roubik 1983].

14

Hollow trees as shelter and den sites

Hollow trees are ultimately found when decayed invertebrates remove heartwood

material, usually, water or fire are formed (Gibbons and Lindenmayer, 2002; Martin &

Eddie, 1999) and then generally are in older and larger trees, which can be suitable for

logging activities. Hollow trees are special environments for many species of mammals

in Australia (Lindenmayer et al., 1997;) and birds (Newton, 1994 for a review) both for

nesting and hosting. A paucity of tree hollows may limit the abundance and distribution

of species.

Considered as an unavailable resource, because of logging and forest

management, conservation activities supply artificial wood boxes to be offered as nest

sites, in order to keep these animals alive in the environment. A good example, in

Brazilian wetlands, the Pantanal region, is the work done with an endangered population

of the hyacinth macaw, intimately dependent on one species of palm tree the macauba

palm, Acrocomia sclerocarpa (“bocaiúva”), where it is also nests. The cutting-down of

this palm endangered the survival of the macaw. Dr. Neiva Guedes, who conducted this

research, used trap nests constructed with wood, and offered them as nest sites in several

places of her study area. The results were excellent, with an increase in the hyacinth

macaw population (now with 6.500 individuals in Pantanal), who is not endangered any

more. It is interesting that environmental education was very effective: 42 farms added

the conservation program, as well as government centers in other regions. Her method is

also being used in Bolivia and other Pantanal areas. Trapnests for macaws were

distributed; it was found that 90% of them were occupied by other animals instead of

macaws, including local stingless bees (Guedes, p. inf.). She monitors, yearly, 170

artificial nests with hyacinth macaws (see www.wwf.org.br ).

The increased probability of a hollow being present in large diameter trees is in

part a function of the loss of decay resistance as trees ages. Hollows can be found in

trunks (mainly in their base) and in branches.

15

How big must be a cavity to keep a stingless bees nest?

Stingless bees size and populations varies a lot (see Roubik, 1983), as well as their

needs for nest sites. So, they have specific nests requirements, according to their size,

population and habitat quality. Very slender cavities (1-5cm wide) were used by smaller

bees (Roubik, 1983): Melipona marginata micheneri, T. mirandula, T. jatifornis, etc.. On

the other hand, Kerr et al (1967) mention that Melipona semimigra merrilae need more

space, because it produced 20 L of honey/year, twice the quantity observed by the rare

honeybees found in that region in 1967. This situation changed now, with the arrival of

Africanized honeybee, and a competition for nest sites was described between

Africanized honeybee and Melipona bees in several parts of the country, from dry

Caatinga to forests, as described by stingless bee keepers. Some of these descriptions

include parrots, Africanized honeybees and stingless bees nests (Bruening, 1990).

Roubik (1983) listed the cavities sizes form de Panamanian nests. Camargo, in his

several papers on stingless bees nests, also mentions cavities sizes. There is a huge

variation here, and each species must be considered in different environments. Cavity

size constraints nest development. Inoue et al (1993) mention the cavity volume for three

stingless bees species from Sumatra (Trigona canifrons, >30.0 L; Trigona minangkabau,

0.5 L and Trigona fuscobalteata, 0.3 L). Matins et al. (2004) studied the internal diameter

and length of 5 Melipona subnitida nests, representing volumes from 2,4 to 8,6L (mean=

5,6L).

Cavities sizes for the several stingless bees species varies a lot. Small cavities

sometimes constraints nest development. Large cavities are delimited by walls of resin or

batumen (a mixture of resin, mud, wax and sometimes pieces of plants) constructed by

the bees.

16

Competition among stingless bees for nest spacing

Stingless bees colonies can be long lived (some Tetragonisca angustula nests are

40 years old at the University campus in S. Paulo; the same for some Melipona bees kept

by beekeepers). These colonies, fixed by their nests, can swarm if nest sites are available.

Colony density and dispersion modes are important ecological aspects, that will be

deeper considered here.

Hubbell & Johnson (1977) studied the dispersion patterns of five stingless bees

species in Costa Rica, four of them territorial and with uniformly distributed nests. They

stated that suitable nest sites availability do not limit colony dispersion. Rather, food

limitation is suggested as a limitation. The authors considered that “ if there are

shortages of suitable nest sites, this shortage should be more acute for bee species with

nest requirements for larger trees: Trigona fulviventris and T.

silvestriana.…Nevertheless, these species have nests very uniformly spaced through the

forest, an strong limitation against the theory of nesting limitation because they believed

that suitable nest sites are themselves not uniformly spaced”. They also found that bees

occupied only 25 of the 74 potentially available tree species. Another point: some tree

species without nests in the study area were known to have nests of these bee species

elsewhere in the Guanacaste Province. A second source of evidence against the nest-site

limitation was the apparent indiscriminant choice of tree species for nesting.

For this study, the marked nests were in low number; they also considered: “there

is no reason for expecting that every tree species of appropriate diameter is equally likely

to have cavities suitable for nest sites, since undoubtedly some species are more prone to

cavity formation than others”. However, they did not found evidences for trees

selectivity as nest sites.

Eltz et al. (2002) evaluated the nest density of stingless bees in undisturbed and

logged–over dipterocarp forests in Sabah, Borneo. They also focused the population

control mediated by 1) nest predation; 2) limitation of nest trees; 3) food limitation.

Observations, as in the previous study mentioned above, were also 4 years round. They

concluded that the abundance of stingless bees in forests in Sabah is chiefly dependent on

17

the local availability of food resources. Bee populations strongly benefit from edge

effects and increased foraging habitat diversity. The authors found 16,2 nests/ha, far

exceeding 2,8 nests/ha in Belalong Forest from Brunei and 2-4 nests/ha in Costa Rica, by

Hubbell and Johnson. Roubik, in a 5ha area, found 5,88 nest/ha; Michener (1964) in

Panama studied a 64ha area and found 2,17 nests/ha.

Eltz et al. (op. cit.) worked in the boundaries of mangroves, and studied the

pollen collected by the bees. They concluded that Rizophora, an important mangrove

species, was a relevant source of pollen for stingless bees. Mangroves have few plant

species, but present in high quantities. In North Brazil, Venturieri et al. (2003) studied the

Melipona nests in the mangrove area in Pará, who also produces a lot of honey. There are

no available data on nest densities in this area, comparing to those that do not face the

mangrove. But Avicennia, one of the 3 plant species of the local mangrove, was one of

the main plant sources for these bees.

Eltz et al. (2003) also considered the negative impact of logging on stingless bees,

in the same area. They analyzed the commercial potential of 142 nest trees of stingless

bees in dipterocarp forests in Sabah and concluded that one-third would qualify for

harvesting in case of logging operation.

Batista et al. (2003) focused on nesting sites in a fragment of Atlantic Rainforest,

in Bahia. In an area of 11,3ha containing three habitat types 16 species of stingless bees

were found. Tetragonisca angustula was the most abundant species, occurring in all

habitats, with 30,7% of found nests. These authors also consider that its ecological

plasticity is allied with aggressive patrolling of potential nests cavities, and also to the

high swarming rate observe by this bee. Nests were abundant in altered landscape.

Artificial offering of nests sites

Another possibility of deal with nest sites as a limited resource is to establish

artificial trap nests, offering nests sites for stingless bees. Inoue et al. (1993) did these

18

experiments in order to know more about the population dynamics of stingless bees. They

studied an area of the Horticultural Experimental Station in Lubuk Mintrum, in Sumatra,

where the main vegetation was a plantation of tropical fruits (rambutan, N. lappaceum,

and durian, D. zibethinus (ca 480x200m, 8-6ha) where 24 species of stingless bees were

found. The species Trigona (Tetragonula) minangkabau was the most common, and

suitable for their study. They censused tree cavities and possible artificial nesting sites to

estimate the number of natural colonies. At these censuses, 2 persons searched 4 days.

They also set 362 trap nests in the field, of which 248 were perforated bamboo stems and

114 wood boxes with glass tops. Trap nests were set in January 1981 (100); December

1981/January 1982 (138) December 1982 (75) and October 1983 (49). Nests were

observed during 56 months. The results were:

1. Trap nests were used by many animals, as social insects (mainly ants) and

vertebrates (geckos, for instance);

2. Only T. (Tetragonula) minangkabau occupied the trap nests;

3. Ants occupied 20% of empty nets;

4. Bees occupied 6% of empty nests;

5. Colonies were found monthly during all experiment;

6. Successful in nest establishment was also recorded

This experiment shows that additional nest sites offer can improve the bee density

in the area, and that trap nests are suitable only for some species.

Antonini & Martins (2002) used trapnests in Cerrado (Brazilian Savanna) without

any result, in an area where they found 46 nests of Melipona quadrifasciata. This bee

species nested mainly in Caryocar brasiliense, a protected tree from cerrado, abundant in

the studied area. Several trees had hollows available for M. quadrifasciata.

Sometimes M. quadrifasciata swarms to empty Apis colonies that have wax or

food inside. This is common also for other stingless bees: as wax is a costly product, they

19

often swarm to empty hives with residues of construction materials, even if they belong

to other bee species or in laboratories conditions. This is an indication that trap nests

should contain some wax or cerumen inside, in order to be more attractive to the bees.

In Brazil, recently stingless bees keepers are using pet bottles as traps nests. In a

beekeeping meeting this year in Rio Grande do Sul (Encontro dos meliponicultores) some

of them reported that Tetragonisca angustula, a very common stingless bee species and

that could be used as crop pollinators for strawberry (Malagodi-Braga and Kleinert,

2004), nested in pet bottles offer as traps.

A deeper research on this subject is urgent, and will be suggested in our

recommendations.

How many stingless bees nests are there in a tree?

Hubbell & Johnson (1977) verified in Guanacaste Provincia, Costa Rica, the

frequency of nest occupation by tree: 10 sp had 1 nest; 7 species had 2 nests; 4 species, 3

nests; 1 tree species contained 4 nests; 2 species, 5 nests; 1 species was found with 6

nests and 11 nests respectively,

Martins et al. (2004) studied the nesting opportunities that trees offer to stingless

bees (Meliponini), in the semi-arid Caatinga of Northeast Brazil. Samples consisted

mostly of tree trunks, which were kept by Meliponini beekeepers. Nearly 13% of

observed nests were in living trees in the field. Seven species of stingless bees, totaling

227 nests, were found in 12 tress species. More than 75% of stingless bees were found in

Caesalpinea pyramidalis (49%) and Commiphora leptophloeos (Burseraceae, 33,9%).

Furthermore, all bee species nidified in C. pyramidalis. A great part of the nests in trunks

were of Melipona subnitida (n=130), of which 50% were found in C. leptophloeos and

22,3% in C. pyramidalis. M. asilvae was predominantly found in C. pyramidalis (92,3%,

n=39). One of those C. pyramidalis trees had nine nests: seven of Frieseomelitta varia

dispar and two nests of Scaptotrigona aff. depilis. One Schinopsis brasiliensis tree had

20

ten nests of Frieseomelitta varia dispar. Those tree species were indicated for nursery in

Caatinga, important for environmental restoration. Currently, Caatinga suffers from two

main human impacts: the cutting of trees for firewood and its use as cattle land. Some

Caatinga regions already have turned into desert.

Camargo & Pedro (2004) found in Salvertia convallariodora five nests:

Ptilotrigona lurida, Scaptotrigona sp., Tetragona clavipes, Trigona pallens and Melipona

compressipes fasciculata. Remarkable is also Campsiandra angustifolia, a tree from

Amazon igapós where 23 and 30 nests of Schwarzula sp. were found, in tunnels

burrowed by moth larvae. This is a specialized bee species, that live in association with

soft scale insects, Cryptostigma sp., that they house and attend (Camargo, 2002).

Antonini & Martins (2002) in Brazilian Cerrado found 20% of Caryocar

brasiliense trees with two nests of Melipona quadrifasciata, and nests of Frieseomelitta

varia, F. silvestri, Partamona cupira, Scaptotrigona postica and Tetragonisca angustula

(maximum number in a tree, 13 nests).

Stingless bees nests in Asia

In Asia, stingless bees nests have been recently studied with different approach by

several authors. Sakagami et al. 1983 described the nests of some Southeast Asian

stingless bees. Starr & Sakagami (1987) described nest aggregations of stingless bees in

Philippines. Salmah et al. (1990) worked on the influence of human disturbance on

stingless bees in Central Sumatra; they found that species diversity and abundance of

stingless bees decreased along the disturbed gradient. Roubik (1996) also evaluated

diversity of stingless bees in Brunei Darussalan, with salt and sugar baits. Eltz studied the

21

stingless bees in dipterocarp forest from Sabah (Eltz et al. 2002; Eltz et al., 2003, already

mentioned above). Finally, Samejima et al. (2004) studied the effect of human

disturbance on a stingless bee community in a tropical rainforest, in Sarawak, Malaysia.

Eltz et al. (2003, op.cit) studied nesting and nest trees of stingless bees in Sabah,

Borneo. The nests were associated to live (91,5%) or dead (8,5%) trees. The majority of

nests species were cavity nests, 81% of them base nests. 275 nests were studied, and were

often aggregated (mean 1,94 nests/ nest tree, with up to eight colonies and 3 species in a

single tree). The authors took in consideration the tree species, timber quality and size

and concluded that 34,0 or 42,6 % of nest trees were potential harvest trees, depending on

harvesting regulations. This paper suggests that “we should apply harvesting guidelines

that retain high proportions of large and hollow trees should be promoted to preserve

meliponine pollination in sustainable forest management”.

Sarawak, in Malaysia, has been recently studied and is one of the most important

tropical areas with a modern ecological research nowadays. Stingless bees were observed

to pollinate 22,6% of a lowland mixed dipterocarp forest (Mamose et al., 1998). The

human activities have increased in this area, with palm oil plantations and selective

logging. Samejima et al. (2004) studied the effects of human disturbance (logging and

shifting cultivations) on stingless bee community in a tropical rainforest, in Sarawak,

Malaysia. In this area, stingless bees nests are in trees with >50cm DBH. They evaluated

the richness of stingless bees in each sampled area, using baits, as well as did a nest

census and floral resources. Nest density was related with density of large trees. The bait

results indicated that some species were abundant in the primary forests, whereas other in

disturbed forests. They still focus on nest site availability as a limit for nest density. In

Borneo, the distribution of stingless bees nests is often cumpled (Roubik, 1996;

Nagamitsu & Inoue, 1997; Eltz and Brühl, 2001).

Samejima et al (2004) censused bee nests at the base of tree trunks; but arboreal

species were present in the baits. 19 species of stingless bees were observed by nests

censuses and bait traps; 8 of them were collected by both methods, 2 of them only by nest

censuses and 9 species observed only in bait traps. Species richness was not affected by

human disturbance, but relative abundance of these bee species may be affected both by

22

nest site and food resource limitations. But their most important conclusion was that the

effects of the human disturbance observed in this study might influence the reproductive

success of plants pollinated by these bees. They also mentioned “changes in the

composition of pollinator community may also affect the regeneration of particular

species, and thus tree composition in the long-term”.

In disturbed areas by logging the establishing of artificial nests increased the nest

density and they survived to low resources periods due to colony food reserves (Inoue et

al., 1993). There are also inter-specific differences in response to human disturbance.

Conclusions

• Diversity of stingless bees in size, nest sites and environmental resources

vary among species. To increase their number in forest fragments is

desirable as best practices management for improving crops nearby, at

this point considering their role as pollinators (see Roubik, 2002; de

Marco & Coelho 2004; Ricketts et al, 2004a and b for coffee plantations).

• Nest sites research included nest description for several species, some

cases of nests distributions and consideration on the impact of human

activity on their abundances and success. For maintenance of their nests,

food resources are required. Research showed that the nest number

increases with constant floral resources availability (as, for instance, near

large mangroves areas, mentioned above);

• Nests distribution can be clumped, at random or uniformed, according to

the considered species. Foraging methods and floral resources used

influences the nests density in an area. Both aspects are poorly known and

deserves further attention;

• Trap nests are accepted by a few species and this method is poorly

known;

23

• Some trees are used by several bee species, and sometimes many species

can nest in their hollows simultaneously;

• At least, food resources and nest sites availability are for sure important

for bee survivorship and abundance in environment. Because of this, we

present in the annexes of this report lists of bee plants for the stingless

bees already recorded on flowers, in Brazil and elsewhere information

were available. The same for nest sites.

• These information can be used for activities related to sustainable

development, among them nursery for restoring and to support

meliponiculture.

Recommendations:

• Climatic conditions are unpredictable in tropical-changing environments,

and this might affect colonies survivorship. This subject must be

considered and monitored as a long term activity, as well as how different

species of stingless bees answer to them;

• The study of trap nests in several biomes, as an indication of which

species should be available for meliponiculture through this method;

• To test several trap nests and to observe which should be adequate for

different uses;

• The training on standard methods using artificial baits to evaluate the

presence of local species in environment. Salt and sugar baits have been

successfully used (Roubik, 1996) in Asia. We must adapt these methods

for long term monitoring in Brazil;

• The preparation of educational material based on the several data

presented in this report.

24

References

Batista, M. A; Ramalho, M. & Soares, A E E- 2003. Nesting sites and abundance of Meliponini (Hymenoptera: Apidae) in heterogeneous habitats of the Atlantic Rain Forest, Bahia, Brazil. Lundiana, 4(1): 19-23.

Bawa,K.S.; Bullock, S.H.; Perry, D.R.; Coville, RE & Grayum, MH- 1985- Reproductive biology of tropical lowland rain forest trees. II Pollination System. Am. J. Bot. 72: 346-356.

Camargo, J.M.F & Pedro, S.M.R. 2003- Meliponini neotropicais: o gênero Partamona Schwarz, 1939 (Hymenoptera, Apidae, Apinae) - bionomia e biogeografia. Revista Brasileira de Entomologia 47(3): 311-372

Darchen, R. –1972- Écologie de quelques Trigones (Trigona sp.) de la savanne de Lamto (Cote d’Ivoire). Apidologie, 3 (4): 341-367.

Eltz, T.; Brühl, C.A.; van de Kaars, S; Linsenmair, K. E.- 2002- Determinants of stingless bee nest density in lowland dipterocarp forests of Sabah, Malysia . Oecologia, 131: 27-34.

Eltz,T.; Brühl, C.A; Imiyabir, Z & Linsenmair, K.E- 2003. Nesting and nest tress of stingless bees (Apidae: Meliponini) in lowland dipterocarp forests in Sabah, Malaysia, with implications for forest management. Forest Ecology and Management, 172:301-313.

Gibbons, P & Lindenmayer, D.B. 2002- Tree hollows and wildlife conservation in Australia. CSIRO Publ.,Sydney, p 211.

Harper, MJ; McCarthy, MA; van der Ree, R- 2005- The abundance of hollow-bearing tres in urban dry sclerophyll forest and the effect of wind on hollow development. Biological Conservation, 122: 181-192.

Inoue, T.; Nakamura, K.; Salmah, S.; Abbas, I. 1993- Population dynamics of animal unpredictable-changing tropical environments. Journal of Biosciences 18: 425-455.

Lindenmayer, D.B.; Cunningham, R.B.; Donnelly, C.F. 1997-decay and collapse of trees with hollows in eastern Australian forests: impacts on arboreal marsupials. Ecol. Appl. 7: 625-641.

De Marco Jr, P & Coelho, F.M.-2004-Services performed by the ecosystem: Forest remnants influence agricultural cultures’ pollination and production. Biodiversity and Conservation, v.13, p. 1245-1255.

Martin, K & Eadie, J.M.-1999- Nest webs: a community wide approach to the management and conservation of cavity-nesting forest birds. Forest Ecology and Management 115: 243-257.

Martins, C.F.; Cortopassi-Laurino, M.; Koedam, D & Imperatriz-Fonseca, V.L.-2004. Espécies arbóreas utilizadas para nidificação por abelhas sem ferrão na caatinga (Seridó, Pb; João Câmara, RN). Biota Neotropica, v. 4, n.2.

Newton, I,. 1994. The role of nest sites in limiting the numbers of hole-nesting birds: a review. Biol. Cons.70 :265-276

25

Oliveira, M.L. 2001- Stingless bees (Meliponini) and Orchid Bees (Euglossini) in Terra Firme Tropical Forests and Forest Fragments. In: Bierregaard,jr R.O.; Gascon, C; Lovejoy, T.E and Mesquita, R.C.G.eds- Lessons from Amazonia- The ecology and conservation of a fragmented forest, Yale University Press, p. 208-218.

Oliveira, M.; Morato, E. F. & Garcia, M.V.B.-1995- Diversidade de espécies e densidade de ninhos de abelhas sociais sem ferrão (Hymenoptera, Apidae, Meliponinae) em floresta de terra firme da Amazônia central. Rev. Bras. Zool., v.12 (1): 13-24.

Ramalho, M. 2004- Stingless bees and mass flowering trees in the canopy of the Atlantic Rainforest: a tight relationship. Acta Bot. Bras., v.18(1): 37-47.

Ricketts, H. T. 2004- Tropical forest fragments enhance pollinators activity in nearby coffee crops. Conservation Biology, v.18, n.5,doi 10.1111/j.1523-1739.2004.00227.x

Ricketts, H. T.; Daily, G.C.; Ehrlich. P. R. and Michener, C.D.-2004- Economic value of tropical forest to coffee production. Proc. of National Academy of Sciences, v. 101, n.34, p.12579-12582.

Roubik, D.W. 2002- The value of bees in coffee harvest. Nature 417: 708. Roubik, D.W. 1983- Nest and colony characteristics of stingless bees from Panama

(Hym. Apidae; J. of Kansas Ent. Soc., 56(3):.

Roubik, D.W. 1989- Ecology and natural history of tropical bees. Cambridge University Press, Cambridge, 514pp.

Roubik, D. W.-1996. Wild bees of Brunei Darussalam. In: Edwards, D.S., Booth, W.E., Choy, S.C. eds, Tropical Rainforest Research – Current Issues. Kluwer Academic Publishers, Dordrecht, pp. 59-66.

Sakagami, S.F.; Yamane, S., Hambali, G.G. 1983- Nests of some Southeast Asian Stingless bees. Bull. of the Fac. of Education, Ibaraki University 32, :1-21.

Salmah, S.; Inoue, T.; Sakagami, S.F. 1990- An analysis of apid bee richness (Apidae) in central Sumatra. In: Sakagami, S.F., Ohgushi, R, ; Roubik, D.W.-Eds- Natural History of social wasps and bees in Equatorial Sumatra. Hokkaido University Press, Sapporo, pp 139-174.

Samejima, H.; Marzuki, M.; Nagamitsu, T. & Nakasizuka, T. 2004- The effects of human disturbance on a stingless bee community in a tropical rainforest. Biological Conservation, 120 : 577-587.

Starr, C.K. and Sakagami, S.F. 1987- An extraordinary concentration of stingless bees colonies in the Philippines, with notes on the nest structure (Hymenoptera, Apidae: Trigona spp.). Ins. Soc. 34: 96-107.

Wilms, W; Imperatriz-Fonseca. V.L. & Engels, W. 1996- Resource partitioning between highly eusocial bees and possible impact of the introduced honeybee on native stingless bees in the Brazilian Atlantic rainforest. Stud. Neotrop. Fauna and Environm., v. 31, p. 137-151.

26

Exploração florestal e impacto sobre abelhas indígenas sem ferrão

Giorgio Cristino Venturieri giorgio@cpatu.embrapa.br

Após o esgotamento das reservas florestais tropicais da Ásia, as atenções se voltaram para a Amazônia, tanto por parte da comunidade científica e conservacionista, como pelas empresas que sobrevivem do comércio internacional de madeira tropical. A expansão das exportações de madeira sem prejudicar a base do recurso é um desafio considerável. Existem argumentos persuasivos quanto à exposição da indústria de madeira brasileira às preocupações existentes nos mercados internacionais, especialmente se esta demanda combina aumento de eficiência com redução de impactos sociais e ambientais. Existem argumentos poderosos contra um caminho mal planejado na ampliação da produção e cortes de custos, ignorando os impactos ambientais e sociais. O caos social, econômico e ambiental vivido pelo setor florestal no Sudeste Asiático, merece reflexão (Macqueen 2004).

Depois da Rússia, o Brasil tem a maior área de floresta do planeta (mais do que o dobro da próxima maior área, no Canadá) e as florestas brasileiras contêm maior biomassa do que qualquer outro país (FAO 2001). Em termos de florestas tropicais, o Brasil ostenta três vezes mais áreas de floresta do que o segundo país na lista, a República Democrática do Congo, e a maioria destes tipos de floresta ocorrem dentro da Amazônia Legal (Macqueen 2004). Atualmente, a opção tecnológica disponível de exploração destes recursos naturais é o chamado “manejo sustentado de floresta”. Este se baseia principalmente na aplicação de técnicas de silvicultura, aliadas ao monitoramento das espécies de interesse econômico, conforme a sua distribuição e diâmetro. Neste sistema, geralmente, há pouca ou nenhuma preocupação com os aspectos biológicos, como por exemplo sobre a influência do método empregado nas populações de polinizadores naturais existentes na floresta. O corte de lianas (ou cipós), tratamento silvicultural que objetiva aliviar a competição das espécies selecionadas para o manejo e a redução de danos por arraste na ocasião da derrubada (Vidal et al. 1997), é um dos exemplos que certamente influencia o pastoreio de importantes polinizadores, pois muitos cipós são excelentes fornecedores de néctar, florescendo no dossel da floresta. Muitas espécies de abelhas, especialmente de grande porte, robustas o suficiente para conseguirem voar sobre a copa das árvores e cobrir longas distâncias, são especialmente importantes na polinização cruzada e no fluxo gênico, fundamentais na manutenção da diversidade genética da floresta tropical. Segundo Bawa (1974 e 1990), em estudos realizados em florestas tropicais úmidas da América Central, aproximadamente 98% de todas as plantas encontradas são dependentes

27

de animais para a realização de suas polinizações. A anemofilia, diferentemente do que ocorre em florestas temperadas, é relativamente rara.

Dentre os vertebrados, aves, morcegos e outros mamíferos não voadores, são conhecidos como vetores de pólen (Fægri e Pijl 1979, Pesson & Louveaux 1984, Proctor et. al. 1996), mas a grande maioria das espécies é polinizada por invertebrados (Kress & Beach 1994). Dentre os invertebrados, as abelhas constituem o principal grupo de polinizadores destas plantas (Bawa et al. 1985, Bawa 1990, Endress 1994, Frankie 1975, Frankie et al. 1976, 1983, 1990, Janzen 1966, Momose et al. 1998). Em se tratando de árvores de dossel, e do estrato médio das florestas, nas quais se enquadra quase a totalidade das espécies utilizadas na indústria madeireira, a importância dos Apoidea ainda é maior, pois baseando-se nas informações geradas por Bawa et al 1985, Bawa 1990, Kress & Beach 1994 e Renner & Feil 1993, a maioria destas árvores são auto-incompatíveis, necessitando de vetores bióticos para a sua polinização que possam voar entre as árvores isoladas entre si. Estudos fundamentados em técnicas de captura, marcação e recaptura, indicam que os meliponíneos podem cobrir distâncias consideráveis, até 1200m (Roubik & Aluja 1983, Nieuwstadt & Ruano 1996, Venturieri 2000), demonstrando que estes animais podem ser importantes para muitas espécies arbóreas tropicais. Como exemplo podemos tomar o caso descrito por Lepsch-Cunha & Mori (1999), onde as abelhas despenham papel fundamental na reprodução de Couratari multiflora (Lecythidaceae). Esta espécie alógama é encontrada em baixa densidade (um indivíduo a cada 10ha) e mesmo assim, consegue se reproduzir facilmente, mesmo entre indivíduos separados por mais de 1000m.

Meliponina é um grupo muito diversificado de abelhas em toda a região tropical do globo, mas é na Amazônia que ocorre a maior diversidade. A importância destas abelhas na polinização é conhecida e descrita para diversas espécies de importância agrícola e florestal (Heard 1999, Venturieri 2000, 2003, Maués 2001). Estas abelhas nidificam em diferentes tipos de substrato, algumas constroem seus ninhos escavando o solo, como exemplo as espécies do gênero Geotrigona spp., Melipona quinquefasciata, Partamona testacea, entre outras. Outras espécies desenvolvem suas colônias em ninhos vivos de cupinzeiros, como é o caso de Scaura latitarsi, Partamona vicina, entre outras. Muitas espécies ocupam diferentes tipos de cavidades oriundas de ninhos abandonados por formigas, cupins, besouros, etc. Algumas poucas espécies da Amazônia confeccionam seus próprios ninhos externos utilizando fibras vegetais de raspagens da superfície de folhas (Trigona sp.) e celulose de árvores em decomposição caídas na floresta (Trigona dallatorreana), mas é em ocos de árvores vivas que a grande maioria dos meliponíneos costumam abrigar as suas colônias. Melipona constitui o gênero de Meliponina com o maior número de espécies (Silveira et al. 2002). É exclusivo da região Neotropical e é na Amazônia que se encontra a maioria das espécies. Este gênero abriga os meliponíneos de maior porte, são mais pesadas e conseqüentemente mais robustas e capazes de voar maiores distâncias sobre o dossel da floresta. Excetuando Melipona quinquefasciata, que nidifica no solo, o restante das espécies deste gênero nidifica em oco de árvores vivas na floresta de terra firme, a maioria na base, onde a cavidade possui maior diâmetro. Em regiões da Amazônia onde

28

as florestas foram removidas algumas espécies de Melipona, que demandam largas cavidades, raramente são encontradas, como é o caso de M. fuliginosa (a maior espécie da subtribo), M. melanoventer e duas subespécies de M. seminigra. Espécies como M. flavolineata se adaptam bem a árvores de menor diâmetro e podem nidificar na base de árvores de áreas alagáveis em matas ciliares e M. fasciculata, que nidifica em árvores de regiões costeiras, como a siriuba (Avicennia nitida - Avicenniaceae), ainda resistem à intensa ocupação do homem ocorrida no nordeste da Amazônia. Os meliponíneos estão entre os mais freqüentes visitantes das flores de árvores tropicais asiáticas, tanto do dossel quanto do sub-bosque, provavelmente prestando importantes serviços de polinização (Momose et al. 1998). Venturieri (2000) também reporta a importância de meliponíneos dos gêneros Melipona e Scaptotrigona em duas importantes espécies pioneiras e auto-incompatíveis da floresta amazônica, Schizolobium amazônicum e Sclerolobium paniculatum var. paniculatum (Leg: Caesalpinioidea). Maués (2001) destaca a importância de seis espécies de meliponíneos em Vouacapoa americana (Leg: Caesalpinioidea), uma árvore auto-incompatível intensamente explorada na Amazônia Oriental. Eltz (2003) e Samejima et al. (2004) em estudos realizados em florestas de Borneo, na Malásia, observaram que a grande maioria dos ninhos encontrados, ocorria em árvores do último estágio sucessional da floresta, com DAP (diâmetro a altura do peito) maior do que 50 cm, ou seja, em árvores grandes, velhas e grossas, justamente aquelas intensamente exploradas pela indústria madeireira. Os mesmos autores também comprovaram a preferência por determinadas espécies de árvores. Apesar da inexistência de estudos sistemáticos desta natureza, as florestas Amazônicas apresentam características muito semelhantes. Os meliponíneos são abelhas eusociais e vivem em colônias que variam de algumas centenas a milhares de indivíduos (Sakagami 1982). Após a fecundação e início da postura, as rainhas dos meliponíneos desenvolvem seus abdomens (fisogastria) e não mais conseguem voar, permanecendo na colônia durante toda a sua vida. Devido a este fenômeno as colônias tornam-se perenes, altamente dependentes da persistência das árvores que elas habitam, remanescendo na mesma cavidade por seguidas gerações. A eliminação contínua de árvores de diâmetro maior do que 50 cm certamente afetará, a médio e longo prazo, a biologia reprodutiva de muitas espécies da floresta, através do impedimento da polinização, de muitas árvores que dependem da ação de meliponíneos para o sucesso na formação de suas sementes. No modelo de manejo sustentado de florestas naturais empregado no Brasil, adotado e acompanhado tanto pelo IBAMA, como por certificadoras independentes que atuam no Brasil, é recomendado que árvores contendo ocos sejam poupadas na ocasião da exploração. No modelo proposto, essas árvores serviriam de matrizes fornecedoras de sementes, já que as mesmas possuem menor rendimento no aproveitamento de sua madeira (figura 1). O grande problema é que a maioria da madeira oriunda de florestas naturais da Amazônia é consumida no mercado interno (Smeraldi e Veríssimo 1999,

29

tabela 1). Este, por sua vez, é menos sujeito às exigências de controle ambiental, não obedecendo, necessariamente, as regras do chamado “bom manejo”. Tabela 1. Consumo de madeira proveniente da Amazônia Brasileira no ano de 1997.

Destino Mercado estrangeiro

Amazônia Brasileira

Estado de São Paulo

Outros estados brasileiros

Milhões de m3 4.0 2.7 5.6 14.0 % do total 14% 10% 20% 56% Fonte: Smeraldi e Verissimo (1999).

Figura 1. Transporte de madeira bruta em um rio da Amazônia: observar o grande número de árvores contendo ocos. Observar também que a totalidade das árvores com oco são justamente as de maior diâmetro. Essas árvores, segundo as recomendações para o manejo sustentado de florestas naturais para a região, deveriam ser poupadas do corte, servindo de matrizes para o fornecimento de sementes. A exploração continuada de madeira, mesmo obedecendo as atuais regras de manejo florestal, ao longo prazo poderá comprometer a sobrevivência da floresta pela escassez de locais para nidificação de importantes polinizadores, que são as abelhas indígenas sem ferrão. Com a exploração continuada de árvores com diâmetro superior a 50 cm de DAP, paulatinamente seriam reduzidas, reduzindo também a oferta de sítios para a nidificação de meliponíneos, já que estas árvores são fundamentais para muitas espécies do grupo (Eltz 2003, Samejima et al. 2004). Recomendações

30

• Necessidade da realização de inventários sobre de ninhos de meliponíneos entre as árvores da floresta amazônica.

• Necessidade de estabelecimento de protocolos para levantamentos padronizados de meliponíneos na floresta amazônica.

• Necessidade de inventários utilizando protocolos padronizados sobre a população de meliponíneos na Amazônia.

• A introdução de cavidades artificiais para a nidificação de meliponíneos em áreas de manejo florestal, poderia amenizar as conseqüências da retirada de árvores com cavidades utilizadas por meliponíneos para a nidificação.

• Maior controle da derrubada de árvores contendo ocos naturais. • Com vistas a dar apoio aos planos de manejo, investigação e divulgação de

métodos para verificação de árvores com ocos no campo deverão ser implementadas.

• Maior divulgação, entre os exploradores de madeira e técnicos, sobre o impacto da derrubada de árvores contendo ninhos de meliponíneos, na biologia reprodutiva das espécies de árvores manejadas.

• Maior divulgação, entre os exploradores de madeira e técnicos, sobre a importância de outras plantas, não importantes para o comércio madeireiro, na manutenção da população natural de meliponíneos e de polinizadores em geral.

SIGLAS IBAMA - Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis Referências

BAWA, K. S. Breeding systems of tree species of a lowland tropical community. Evolution. v. 28, p. 82-92, 1974.

BAWA, K. S. Plant-pollinator interaction in tropical rain forests. Annual Review of Ecology and Systematic. v. 21, p. 399-422, 1990.

BAWA, K. S., BULLOCK, S. H., PERRY, D. R., COVILLE, R. E., GRAYUM, M. H. Reproductive biology of tropical low land rain forest trees. II. Pollination system. American Journal of Botany, v. 72, n. 3, p. 346-356, 1985.

ENDRESS, P. K. Diversity and evolutionary biology of tropical flowers. Cambridge: Cambridge University Press, 1994. 511p.

FÆGRI, K., van der PIJL, L. The principles of Pollination Ecology. 3 ed. Oxford: Pergamom, 1979. 250p.

FAO. State of the world’s forests. Roma (Itália): FAO, 2001. 181p.

31

FRANKIE, G. W. Tropical forest phenology and pollinator plant coevolution. In: GILBERT, L. E. and RAVEN, P. H. (Eds.). Coevolution of animal and plants, Austin: Univ. of Texas Press. p.192-209, 1975.

FRANKIE, G. W., HABER, W. H., OPLER. P. A. BAWA, K. S. Characteristics and organization of the large bee pollination system in the Costa Rican dry forest. In: JONES, C. E. e LITTLE, R. J. (Ed.). Handbook of experimental pollination biology, New York. S & AE. p. 411-447, 1983.

FRANKIE, G. W., OPLER. P.A., BAWA, K.S. Foraging behaviour of solitaire bees: Implications for outcrossing of a Neotropical forest trees species. Journal of Ecology, v.64, p.1049-57, 1976.

FRANKIE, G.W. VINSON, S.B. NEWSTROM,L.E., BARTHELL, J.F., HABER, W.A., FRANKIE, J.K. Plant phenology, pollination ecology, pollination behaviour and conservation of pollinators in Neotropical dry forest. In: BAWA, K.S., HADLEY, M. (eds.) Reproductive ecology of tropical forest plants. UNESCO, Paris, and Parthenon Publishing Group, Carnsforth, UK, 1990.

HEARD, T. A. The role of stingless bees in crop plantation. Annual Review of Entomology, v. 44, n. 183-206, 1999.

JANZEN, D. H. Syncronization of sexual reproduction of trees within the dry season in Central America. Evolution, v. 21, p. 620-637, 1966.

KRESS, W. J., BEACH, J. H. Flowering Plant Reproductive Systems. In: McDade, L. A., Bawa, K. S., Hespenheide, H. A. and Hartshorn, G. S. (eds.). La Selva: Ecology and Natural History of a Neotropical Rain Forest. p.142-182, 1994.

LEPSCH-CUNHA, N. & MORI, S. A. Reproductive phenology and mating potential in a low density tree population of Couratari multiflora (Lecythidaceae) in central Amazonia. Journal of Tropical Ecology, v. 15, p. 97-121, 1999.

MACQUEEN, D. (Ed). Exportando Sem Crises: A indústria de madeira tropical brasileira e os mercados internacionais. Londres, Reino Unido: IIED. 2004

MAUÉS, M. M. Síndromes de polinização e biologia floral de espécies madeireiras da Amazônia e implicações para o manejo florestal. In SILVA, N. M.; CARVALHO, J. O. P. de; YARED, J. A. G, editores. Silvicultura na Amazônia Oriental, Belém: Embrapa Amazônia Oriental/DFID, 2001, 457p.

MOMOSE, K., YUMOTO, T., NAGAMITSU, T., KATO, M., NAGAMASU, H., SAKAI, S., HARRISON, R. D., ITIOKA, T., HAMID, A. A., INOUE, T. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. American Journal of Botany, n. 85, vol. 10, p. 1477-1501, 1998.

32

van NIEUWSTADT, M. G. L. & RUANO Iraheta, C. E. Relation between size and foraging range in stingless bees (Apidade, Meliponinae). Apidologie, v. 27, p. 219-228, 1996.

PESSON, P. & LOUVEAUX, J. Pollinisation et Productions Végétales. Paris, INRA, 1984, 663p.

PROCTOR, M.; YEO, P. & LACK, A. The Natural History of Pollination. Portland: Timber Press, 1996. 479p.

RENNER, S. S. & FEIL, J. P. Pollinators of tropical dioecious angiosperms. American Journal of Botany, v. 80, n. 9, p. 1100-1107, 1993.

ROUBIK, D. W. & ALUJA, M. Flight ranges of Melipona and Trigona in tropical forest. Journal of the Kansas Entomological Society, v. 56, n. 2, p. 217-222, 1983.

SMERALDI, R. e VERÍSSIMO, A. Hitting the target: timber consumption in the Brasilian domestic market and promotion of forest certification. Belém (Brasil): IMAZON, 1999, 41p.

SAKAGAMI, S. F. Stingless bees. In: Hermann, H. R. (Eds.), Social Insects, vol. 3. Academic Press, New York, 361-423.

SILVEIRA, F. A.; MELO, G. A. R.; ALMEIDA; E. A. B. Abelhas brasileiras: sistemática e identificação. Belo Horizonte. Min. Meio Ambiente/Fund. Araucária. 2002, 253p.

VIDAL, E.; JOHNS, J.; GERWING, J.; BARRETO, P.; Uhl, C. Vine management for reduced-impact logging in the eastern Amazon. Forest Ecology and Management 98: 105-114. 1997.

VENTURIERI, G. C. A ecologia reprodutiva do taxi-branco (Sclerolobium paniculatum var. paniculatum vogel) e do paricá (Schizolobium amazonicum Huber ex Ducke) leg: Caesalpinioideae e a influência da melitofilia na polinização dessas árvores amazônicas. Universidade de São Paulo, Instituto de Biociências. São Paulo, SP. 2000 (Tese de Doutorado).

VENTURIERI, G. C. Plantas visitadas por Meliponina no Estado do Pará. In. Anais do 54º Congresso Nacional de Botânica. Belém, PA. 2003, 261-263p.