A Plan of Action was then prepared by Food and Agricultural
Organization of the United Nations (FAO) and the CBD Secretariat,
endorsed by SBSTTA7, and recommended for adoption by CBD COP6.
The Plan of Action of the IPI was accepted by member countries andadopted at COP 6 (decision VI/5).
Since then, most regions of the world have established or are in processof establishing wide-ranging pollinators initiatives. The core objectivesof IPI are also kept by the regional Initiatives. They are:
• Monitor pollinator decline, its causes and its impact on pollinator services• Address the lack of taxonomic information on pollinators• Promote the conservation, the restoration and sustainable use of pollinator diversity in agriculture as well as in related ecosystems
To follow this agenda, the Brazilian Pollinators Initiative, under the support of FAO, Ministry of Environment, Ministry of Science and Technology
and Sao Paulo University, promoted the workshop São Paulo Declaration
on Pollinators Plus 5, in October 2003 . We joined the regional Initiatives,
discussed common routes and some essential points: standardized
methodologies, pollinators declining and management practices. This
book concerns the results of group discussions in the workshop São Paulo
Declaration on Pollinators Plus 5, and was printed with a support from
Conservation International-Brasil

HOLOS EDITORA

ISBN 85-86699-51-9

assessing the status and suggesting best practices• Assess the economic value of pollination and the economic impact ofthe decline of pollination services

Bees as pollinators in Brazil

The São Paulo Declaration on Pollinators, was endorsed in May 2000 by
the fifth Conference of Parties of Convention of Biological Diversity(COP5), held in Nairobi (section II of the decision v/5, that reviewed theimplementation of decisions III/11 and IV/6 on the program of work on
agrobiodiversity). COP5 established an International Initiative for theConservation and Sustainable Use of Pollinators, hereafter referred to as
the International Pollinator Initiative (IPI).

Bees as pollinators in Brazil
assessing the status and suggesting best practices

Edited by
Vera Lucia Imperatriz-Fonseca, Antonio Mauro Saraiva, David De Jong

Bees as pollinators in Brazil:
assessing the status and suggesting best practices

2006

CONSERVATION INTERNATIONAL - BRAZILHOLOS EDITORA

Bees as pollinators in Brazil:
assessing the status and suggesting best practices
Proceedings of the Workshop on São Paulo Declaration on Pollinators
plus 5 Forum, held in São Paulo, Brazil, 27th-31st October 2003

Edited by:
Vera Lucia Imperatriz-Fonseca, Antonio Mauro Saraiva, David De JongWith Assistance from Associate Editors
Cynthia Pinheiro-Machado; Fernando A. Silveira; Claudia Maria Jacobi;
Breno Magalhães Freitas; Marina Siqueira de Castro

Ribeirão Preto
2006

Workshop Sponsors
Food and Agriculture Organization (FAO)
Ministry of Environment (MMA)
Ministry of Science and Technology (MCT)São Paulo University (USP)
Printer Sponsors
Conservation International – Brazil
Brazilian Pollinator Initiative
Editorial assistance
Tarcila LucenaBook design
Renata Carpinetti(renatacarpinetti@gmail.com)
Cover
Melipona compressipes fasciculata (Apidae, Meliponini)pollinating assai flowers (Euterpe oleracea - Arecaceae)
Photo by Giorgio C. Venturieri

Catalog for International Publication
Bees as pollinators in Brazil: assessing the status and suggesting best practices /Vera Lucia Imperatriz Fonseca, ed.; Antonio Mauro Saraiva, ed.; David de Jong, ed.
Ribeirão Preto: Holos, Editora, 2006, 112 pp.
Workshop on São Paulo Declaration on Pollinators Plus 5 Forum, São Paulo, 2003.
1. Pollinators – agriculture. 2. Bees – use and conservation.
I. Imperatriz-Fonseca, V.L.II. Saraiva, A.M. III. De Jong, D. IV Holos Editora.
Environment. V. Title

ISBN 85-86699-51-9

Holos, Editora
Rua Bertha Lutz, 390
14.057-280 Ribeirão Preto , SP
TeleFax: (0++16) 3639-9609
Email: holos@holoseditora.com.br
www.holoseditora.com.br

Dedication

Paulo Nogueira-Neto
Pioneer in Brazil in studies of the role of bees as pollinators, in classic
research on pollination of the Bourbon variety of coffee. He is known worldwide for his innovative techniques for rearing indigenous stingless bees andhis involvement with environmental conservation.

Warwick Estevam Kerr
Pioneer in the study of bee genetics in Brazil, focusing especially on the
Meliponini. During all of his life, he has encouraged and supported therearing of these bees, creating regional research groups across the country
and disseminating the importance of the environmental services provided
by pollinators.
Both have inspired us with their principles, stimulation and dedication toscience.

Acknowledgements

The Workshop São Paulo Declaration on Pollinators plus five involved ateam with different profiles, and several institutions. Concerning theorganization, we thank especially the dedication of Fernando A. Silveira,
Cynthia Pinheiro Machado, Claudia Maria Jacobi, Rogério Gribel, Breno
Magalhães Freitas, David de Jong, Lionel Segui Gonçalves, Marina Siqueirade Castro. Also, we thank the cooperation of Bee Laboratory from
Instituto de Biociências, University of São Paulo, mainly to Mariana
Imperatriz Fonseca, Denise de Araújo Alves, Favízia Freitas de Oliveira,
Marilda Cortopassi-Laurino and Patrícia Nunes Silva, in all steps of thisprocess that ends with this publication.
Financial support was obtained from several sources, and we thank theirrepresentatives: FAO – Linda Collette, for her collaboration and outstanding
help; Brazilian Ministry of Environment – Paulo Y. Kageyama, Braulio Ferreirade Souza Dias e Marina Landeiro who have participated in all steps of thiswork; Brazilian Ministry of Science and Technology - Regina P. Markus, for
her advice and collaboration in the workshop; University of São Paulo (USP)and Fundação de Apoio à USP (FUSP) – Mr. Kem Yoshida.
We would also like to thank some institutions and specialists: Polytechnic
School of the University of São Paulo that has sponsored the workshop on
Information Technology and Pollinators Initiative, and the team from theAgricultural Automation Laboratory and WebBee project, especially Tereza
Cristina Giannini, Etienne Americo Cartolano Júnior and Renato Sousa da
Cunha for the workshop’s website and Vanderlei Canhos from ReferenceCenter of Environmental Information (CRIA), for his collaboration in theorganization. The Ecofuturo welcomed the participating group in their field
trip to Mata Atlântica that was very much appreciated.
Finally, for the printing of this book we have received the support from
Conservation International Brazil.
The Editors.

9

Summary
Acronyms

16

Presentation17

Worshop preparation

17

International Pollinators Initiatives

18

Methodological discussions

19

Protocols and discussions

19

Information Technology and Pollinators Initiatives

20

References

21

Worshop I: Survey methods for bees as pollinators in Brazil: assessing thestatus and suggesting best practices

23

Group 1: Surveying and monitoring of pollinators in natural landscapesand in cultivated fields

25Group 2: Assessment of pollinator – mediated gene flow

39

Group 3: Bee management for pollination purposes

53A) Bumble bees and solitary bees

55B) Honey bee

63C) Stingless bees

75

Worshop II: Pollinator Initiatives and the role of Information Technology (IT)89

Illustrations and photographs

97

10

The participants on both workshops wereAdriana De Oliveira Fidalgo, Instituto deBotânica, Divisão do Jardim Botânico de São
Paulo, Seção de Ecologia. Avenida Miguel
Estefano 3687, Água Funda 01061-970,
São Paulo, SP, BRAZIL, Caixa-Postal: 4005,
Telefone: (11) 50736300, Ramal: 298, Fax:
(11) 50733678
Alfred Ochieng, ICIPE, P.O.Box 30772,
Nairobi, KENYA, Tel: +254 2 861680-4,
Fax: +254 2 860110 [aochieng@icipe.org].
Anthony Raw, Laboratório deEntomologia, Departamento de Ciências
Biológicas, Universidade Estadual de Santa
Cruz (UESC), Rodovia Ilhéus-Itabuna,
Km 16, CEP 45650-000, Bahia, BRAZIL,
Tel: +55 73 680-5261[antony_raw@yahoo.com.br].
Antonio Mauro Saraiva, Laboratório deAutomação Agrícola, Departamento de
Engenharia de Computação e Sistemas
Digitais, Escola Politécnica, Universidade deSão Paulo, Av. Prof. Luciano Gualberto,
Travessa 3, número 158, sala C2-54, CEP
05424-970, Cidade Universitária, São Paulo,São Paulo, BRAZIL, Tel: +55 11 3091-5366[amsaraiv@usp.br].
Astrid de Matos Peixoto Kleinert,
Departamento de Ecologia Instituto deBiociências, Universidade de São Paulo (USP),
Rua do Matão, travessa 14, nº 321 Cidade
Universitária, CEP 05508-900, São Paulo,São Paulo, BRAZIL, Tel: +55 11 30917604[astridkl@ib.usp.br].
Barbara Gemmill (Herren) Global Pollination
Project Coordinator, Food and Agriculture
Organization of the United Nations, vialedelle Terme di Caracalla Rome, 00100, Italy,[Barbara.Herren@fao.org]

Braulio Ferreira de Souza Dias, Secretaria
de Biodiversidade e Florestas do Ministério do
Meio Ambiente. SAIN Av. L4 Norte, Campus
Sede do IBAMA, Bloco H, CEP 70.800-200
Brasília, DF, Brasil Tel. +5561 325-41-85 ou
317-1120, Fax +5561 325-5755;[braulio.dias@mma.gov.br &bfsdias@terra.com.br ]Breno Magalhães Freitas, Departamento deZootecnia, Universidade Federal do Ceará,Campus Universitário do PICI, Caixa Postal
12168, CEP 60355-970, Fortaleza, Ceará,
BRAZIL [freitas@ufc.br].
Carmen Silvia Soares Pires, Laboratório de
Bioecologia e Semioquímicos, Centro
Nacional de Pesquisa de Recursos Genéticos e
Biotecnologia, Empresa Brasileira de Pesquisa
Agropecuária (EMBRAPA), Sain Parque Rural W5 Final, Asa Norte, CEP 70849-970, Brasília,DF, BRAZIL, Tel: +55 61 448-4682[cpires@cenargen.embrapa.br].
Celso Feitosa Martins, Departamento deSistemática e Ecologia (CCEN), Universidade
Federal da Paraíba, CEP 58059-900, JoãoPessoa, Paraíba, BRAZIL[cmartins@dse.ufpb.br].
Claudia Maria Jacobi, Departamento de
Biologia Geral, Universidade Federal de Minas
Gerais, Avenida Antônio Carlos 6627, Caixa
Postal 486, CEP 30161-970, Belo Horizonte,
Minas Gerais, BRAZIL[jacobi@mono.icb.ufg.br].
Clemens Peter Schlindwein, Departamento
de Botânica, Centro de Ciências Biológicas,
Universidade Federal de Pernambuco (UFPE),
Av. Prof. Moraes Rêgo s/n, Cidade
Universitária, CEP 50670-901, Recife,
Pernambuco, BRAZIL, Tel: +55 81 3271-8352[schlindw@ufpe.br]Participants I 11

Connal Eardley, Bee Systematists &SAFRINET Co-ordinatos, Plant Protection
Research Institute Agricultural ResearchCouncil, Plant Protection Research Institute,Private Bag X134, Queenswood, 0121, South
Africa, 590 Vermeulen Street, Pretoria,
SOUTH AFRICA, Tel +27 (0)12 - 304 9578,
Fax +27 (0)12 325 6998
[EardleyC@arc.agric.za].
Cynthia Almeida Pinheiro Machado,
Fundação Integrada Municipal de Ensino
Superior, Rua 22 esq. c/ Av. 01, Setor
Aeroporto, CEP 75830-000 - Mineiros, GO BRAZIL, Tel.: (64) 36611970
Fax: (64) 38134151, [cpm@fimes.edu.br],
www.fimes.edu.br
David De Jong, Departamento de Genética,
Faculdade de Medicina, Universidade deSão Paulo (FMRP-USP), CEP 14049-900,
Ribeirão Preto, São Paulo, BRAZIL,
Tel: +55 16 602-4401, fax +55 16 633-6482[ddjong@rgm.fmrp.usp.br].
David W. Roubik, Smithsonian TropicalResearch Institute, Unit 0948, APO AA
34002-0948or APDO 2072 Balboa, REPUBLICOF PANAMÁ [roubik@ctfs.stri.si.edu /roubik@tivoli.si.edu].
Denise de Araújo Alves, Laboratório deAbelhas, Departamento de Ecologia, Institutode Biociências, Universidade de São Paulo(USP), Rua do Matão, travessa 14, nº 321,
CEP 05508-900, Cidade Universitária,São Paulo, São Paulo, BRAZIL,
Tel: +55 11 3091-7533 [daalves@ib.usp.br].
Denise Monique Dubet da Silva Mouga,
Departamento de Ciências Biológicas, Pró
Reitoria de Ensino, Universidade da Região deJoinville (UNIVILLE), Campus Universitário, s/n,
Bom Retiro, CEP 89201-972, Joinville, Santa
Catarina, BRAZIL, Tel: +55 47 461-9000
r. 9072 [biologia@univille.edu.br].

Dieter Wittmann, Institut für
Landwirtschaftliche Zoologie undBienenkunde, Melbweg, 42, University ofBonn, Bonn, 53127, GERMANY[wittmann.bonn@gmx.de].
Dirk Koedam, Departamento de Ecologia,
Instituto de Biociências, Universidade de São
Paulo (USP), Rua do Matão, Travessa 14,
nº 321, CEP 05508-900, Cidade Universitária,São Paulo, São Paulo, BRAZIL, Tel: +55 113091-7533 [dkoedam@usp.br].
Eda Flávia Lotufo Rodrigues Alves
Patrício, Laboratório de Abelhas,
Departamento de Ecologia, Instituto deBiociências, Universidade de São Paulo (USP),
Rua do Matão, travessa 14, nº 321, CEP
05508-900, Cidade Universitária, São Paulo,São Paulo, BRAZIL, Tel: +55 11 3091-7533.
Edivani Vilaron Franceschinelli,
Universidade Federal de Goiás, Instituto deCiências Biológicas, Departamento de Biologia
Geral, Campus II - Samambaia - ICB1 2 andar, Campus Samambaia, CEP 74001970,
GOIANIA, GO, BRAZIL, Caixa-Postal: 131,
Tel.: (62) 5211112, Fax: (62) 5211109,[edivanif@yahoo.com.br], www.icb.ufg.br
Farooq Ahmad, Indigenous Honey Bee
Project, International Centre for Integrated
Mountain Development (ICIMOD), P.O Box
3226, Kathmandu, NEPAL, Tel: 09977-15525313, Fax 00977-1-5524509[fahmad@icimod.org.np].
Favízia Freitas de Oliveira, Universidade
Estadual de Feira de Santana, Departamento
de Ciências Biológicas, Laboratório deSistemática de Insetos Lasis, Av. Universitária
S/N, Km 03 - BR 116 (Rodovia Feira deSantana - Serrinha) - Cidade Universitária,CEP 44031460, Feira de Santana, BA,
BRAZIL, Tel: (75) 32248194, Fax: (75)32248019, [favos@uefs.br]
http://www.uefs.br/dcbio/lent_sis/index.html

12

Felipe Andrés Leon Contrera, University ofCalifornia - Berkeley, University Of California,
San Diego - USA, [fcontrera@ucsd.edu]
Fernando Amaral da Silveira, Laboratóriode Sistemática e Ecologia de Abelhas,
Departamento de Zoologia, Instituto deCiências Biológicas, Universidade Federal de
Minas Gerais (UFMG), Avenida Antônio
Carlos 6627, Caixa Postal 486, CEP 31270901, Belo Horizonte, Minas Gerais, BRAZIL[fernando@mono.icb.ufmg.br].
Fernando César Vieira Zanella,
Departamento de Engenharia Florestal, Centro
de Saúde e Tecnologia Rural, Universidade
Federal de Campina Grande (UFCG), Bairro
do Jatobá, CEP 58700-970, Jatobá – Patos,Paraíba, BRAZIL, Tel: +55 83 421-3397[fzanella@cstr.ufcg.edu.br].
Flavia Monteiro Coelho Ferreira,
Universidade Federal de Viçosa, Centro deCiências Biológicas e da Saúde,
Departamento de Biologia Geral, Avenida P.
H. Holfs, s/ número, CEP36570-001 - Vicosa,
MG - BRAZIL, Tel.: (31) 38991178[monteiro@vicosa.ufv.br], http://www.ufv.br
Francisco de Sousa Ramalho, Centro
Nacional de Pesquisa de Algodão, Unidadede Controle Biológico, Empresa Brasileira dePesquisa Agropecuária (EMBRAPA),
Rua Osvaldo Cruz 1143, Centenário,CEP 58107-720, Campina Grande, Paraíba,
BRAZIL, Tel: +55 83 341-3608[framalho@cnpa.embrapa.br].
Giorgio Cristino Venturieri, Centro dePesquisa Agroflorestal da Amazônia Oriental,
Empresa Brasileira de Pesquisa Agropecuária(EMBRAPA - Amazônia Oriental),
Tv. Dr. Enéas Pinheiro, s/nº, CEP 66095100,
Marco – Belém, Belém, Pará, BRAZIL,
Tel: +55 91 2994500 r. 4697
[giorgio@cpatu.embrapa.br].

Gisele Garcia Azevedo, Departamento de
Biologia Centro de Ciências da Saúde,
Universidade Federal do Maranhão (UFMA),
Av. dos Portugueses s/n, CEP 65040-080,
Bacanga, São Luis, Maranhão, BRAZIL, Tel:
+55 98 32178542 [giselegarcia@ufma.br].
Guiomar Nates Parra, Laboratorio deInvestigación en Abejas (LABUN),
Departamento de Biología, Universidad
Nacional de Colombia, A.A. 144590, Bogotá,
COLOMBIA, S.A, Tel: +3165000 ext.
11335/11337, Fax 3165310[gnates@ciencias.unal.edu.co].
Isabel Alves dos Santos, Instituto deBiociências da USP, Rua do Matão 321 trav
14, Cidade Universitária, 05508-900, SãoPaulo, SP, BRAZIL,Tel: (11) 30917527
Fax: (11) 30917600, [isabelha@usp.br]
Jacobus Christiaan Biesmeijer School of
Biology.University of Leeds.Leeds LS2 9JT,
UNITED KINGDOM.
[J.C.Biesmeijer@leeds.ac.uk].
James H. Cane, Bee Biology and Systematics
Laboratory, Utah State University, 5310 Old
Main Hill, Logan, Utah 84322-5310, USA,
Tel: +01 435 797-3879, Fax 435-797-0461[jcane@biology.usu.edu].
Jesus Santiago Moure, Departamento de
Zoologia, Setor de Ciências Biológicas,
Universidade Federal do Paraná (UFPR),
Centro Politécnico, Caixa Postal 19020, CEP
81531-980, Jardim das Américas, Curitiba,
Paraná, BRAZIL, Tel: +55 41 361-1671, Fax:
+55 41 266-2042 [jsmoure@bol.com.br /urban@bio.ufpr.br].
João Israel Bernardo, Centro Federal de
Educação Tecnológica do Paraná, Conselho
Diretor, Unidade do Sudoeste, Rodovia PR469 (via do Conhecimento) km01 Fraron,
CEP 85501-970 , Pato Branco, PR , BRAZIL,Participants I 13

Caixa Postal 571, Tel: +55 46 2202511, Fax:
+55 46 2202500, [israel@pb.cfetpr.br], URL
da Homepage: http://www.pb.cefetpr.brJoão Rodrigues de Paiva, Centro Nacionalde Pesquisa de Agroindústria Tropical,
Empresa Brasileira de Pesquisa Agropecuária(EMBRAPA), Rua Dra. Sara Mesquita, 2270,
Planalto do PICI, CEP 60511-110, Fortaleza,
Ceará, BRAZIL, Tel: +55 85 3299 1864
[paiva@cnpat.embrapa.br].
Kátia Peres Gramacho, Faculdade de
Tecnologia e Ciências, Somesb, Salvador, Av.
Luis Viana Filho s/n, CEP 41730006, Salvador,BA, BRAZIL, Tel: +55 71 2818000 r. 8102 Fax:
+55 71 2818019, [gramacho.ssa@ftc.br],
URL da Homepage: http:\\www.ftc.br
Kátia Sampaio Malagodi Braga,
Laboratório de Abelhas, Departamento de
Ecologia, Instituto de Biociências,
Universidade de São Paulo (USP), Rua doMatão, travessa 14, nº 321, CEP 05508-900,
Cidade Universitária, São Paulo, São Paulo,
BRAZIL, Tel: +55 11 3091-7533[ckbraga@terra.com.br].
Lílian Santos Barreto, Empresa Baiana de
Desenvolvimento Agrícola, Estatal, Central deLaboratórios da Agropecuária, Av. Adhemar
de Barros, 967, Ondina, CEP 40170-110,
Salvador, BA, BRAZIL, Tel: +55 71 2370871 r.
37, [lilian_bio@yahoo.com.br], URL da
Homepage: http://www.ebda.ba.gov.br
Linda Collette, United Nations Food andAgriculture Organization (FAO), Viale delle
Terme di Caracalla, 00100 Rome, ITALY[linda.collette@fao.org].
Lionel Segui Gonçalves, Departamento de
Biologia, Faculdade de Filosofica Ciências e
Letras de Ribeirão Preto, Universidade de São
Paulo (FFCLRP-USP), CEP 14.040-901,
Ribeirão Preto, São Paulo, BRAZIL,

Tel: +55 16 602-3054, Fax +55 16 633-6482[lsgoncal@usp.br].
Lucio Antonio de Oliveira Campos,
Departamento de Biologia Geral, Centro deCiências Biológicas e da Saúde, Universidade
Federal de Viçosa (UFV), Av. P. H. Rolfs, s/n,
CEP 36571-000, Centro, Viçosa, Minas
Gerais, BRAZIL, Tel: +55 31 3899-1299[lcampos@ufv.br].
Márcia de Fátima Ribeiro, Universidade
Federal do Ceará, Depto. de Zootecnia, Bloco
948, campus do Pici, Grupo de Pesquisas
com Abelhas
Antonio Bezerra, CEP 60021-970,
Fortaleza, CE, BRAZIL, Caixa Postal: 12168,
Tel: +55 85 40089697 Fax: +55 85
40089701, [marib@ufc.br], URL da
Homepage: http://www.abelhas.ufc.br
Márcia Maria Corrêa Rêgo, Departamento
de Biologia, Centro de Ciências da Saúde,
Universidade Federal do Maranhão (UFMA),
Av. dos Portugueses, s/n Campus
Universitário do Bacanga, Bacanga, CEP
65080-040, Sao Luis, Maranhão, BRAZIL, Tel:
+55 98 217-8544 [regommc@uol.com.br].
Maria Cristina Arias, Departamento de
Biologia, Instituto de Biociências,
Universidade de São Paulo (USP), Rua doMatão, no 277, CEP 05508-900, Cidade
Universitária, São Paulo, São Paulo, BRAZIL,
Tel: +55 11 3091-7587 [mcarias@ib.usp.br].
Maria Cristina Gaglianone, Laboratório deCiências Ambientais, Centro de Biociências e
Biotecnologia , Universidade Estadual do
Norte Fluminense Darcy Ribeiro (UENF), Av.
Alberto Lamego 2000, CEP 28013-600,
Campos dos Goytacazes, Rio de Janeiro,
BRAZIL, Tel: +55 22 2726-1602[mcrisgag@uenf.br].

14

Maria José de Oliveira Campos,
Departamento de Ecologia, Instituto deBiociências, Universidade Estadual Paulista
Júlio de Mesquita Filho (UNESP), Av. 24A, N.
1515, CEP 13506-900, Bela Vista, Rio Claro,São Paulo, BRAZIL, Tel: +55 19 526-4145[mjoc@rc.unesp.br].
Maria Rodrigues Vianna, Universidade
Federal de Ouro Preto, Instituto de Ciências
Exatas e Biológicas, Departamento deCiências Biológicas, Campus Morro do
Cruzeiro, Ouro Preto, MG, BRAZIL, Bauxita,
CEP 35400000, Tel: +55 31 35591699,[mia_vianna@yahoo.com.br]
Mariana de Araújo Melo, Departamento de
Biologia Animal, Centro de Ciências
Biológicas e da Saúde, PPG-Entomologia,
Universidade Federal de Viçosa (UFV), Av. P.
H. Rolfs, s/n, Campus Universitário, CEP
36571-000, Viçosa, Minas Gerais, BRAZIL, Tel:
+55 31 3899-2531 [mariana@insecta.ufv.br].
Marilda Cortopassi Laurino, Laboratório deAbelhas, Departamento de Ecologia, Institutode Biociências, Universidade de São Paulo(USP), Rua do Matão, travessa 14, nº 321,
CEP 05508-900, São Paulo, São Paulo,
BRAZIL, Tel: +55 11 3091-7533[mclaurin@usp.br].
Marina Siqueira de Castro, Empresa Baiana
de Desenvolvimento Agrícola, Central deLaboratórios da Agropecuária, Laboratório deAbelhas Labe. Av. Ademar de Barros, 967,
Ondina, CEP 40170110, Salvador, BA ,BRAZIL, Tel: +55 71 32352517 R. 33 Fax: +55
71 32351453, Universidade Estadual de Feirade Santana, Avenida Universitária s/n, Feirade Santana, BA, BRAZIL,[marinascastro@uol.com.br], URL da
Homepage: http://www.uefs.br/
Mauro Ramalho, Departamento deBotânica, Instituto de Biologia, Universidade

Federal da Bahia (UFBA), Rua Barão de
Geremoabo s/n, Ondina, CEP 40170-290,
Salvador, Bahia, BRAZIL, Tel: +55 71 2473810 [ramauro@ufba.br].
Michael A. Ruggiero, Integrated Taxonomy
Information System, U.S. Geological Survey,
Smithsonian Institution, P.O.Box 37012
NMNH, Room CE-120, MCR 0180,
Washington DC, 20013-7012, USA[RuggieroM@si.edu
Ruggiero.Michael@NMNH.SI.EDU].
Olga Inés Cepeda Aponte, Laboratório deAbelhas, Departamento de Ecologia, Institutode Biociências, Universidade de São Paulo(USP), Rua do Matão, travessa 14, nº 321,
CEP 05508-900, Cidade Universitária, SãoPaulo, São Paulo, BRAZIL, Tel: +55 11 30917533 [ocpeda@usp.br].
Patricia Maia Correia de Albuquerque,
Laboratório de Entomologia, Departamento
de Biologia, Centro de Ciências da Saúde,
Universidade Federal do Maranhão (UFMA),
Av. dos Portugueses, Campus Univ. do
Bacanga, CEP 65080-040, São Luis,
Maranhão, BRAZIL, Tel: +55 98 217-8544[palbuq@elo.com.br].
Paulo De Marco Junior, Laboratório deEcologia Quantitativa, Centro de Ciências
Biológicas e da Saúde, Departamento de
Biologia Geral, Universidade Federal deViçosa (UFV), Centro, CEP 36571-000,
Viçosa, Minas Gerais, BRAZIL, Tel: +55 31
3899-1669 [pdemarco@ufv.br].
Paulo Nogueira Neto, Laboratório deAbelhas, Departamento de Ecologia, Institutode Biociências, Universidade de São Paulo(USP), Rua do Matão, trav.14, nº321, CEP
05508-900, Cidade Universitária, São Paulo,São Paulo, BRAZIL, Tel: +55 11 3091-7533[paulonogueiraneto@superig.com.br].

Participants I 15

Paulo Yoshio Kageyama, Diretor do
Programa Nacional de Conservação da
Biodiversidade, Ministério do Meio Ambiente,
Tel: +55 61 40099551,[paulo.kageyama@mma.gov.br].
Peter G. Kevan, Department ofEnvironmental Biology, University of Guelph,
Guelph, Ontario N1G 2W1, CANADA[pkevan@uoguelph.ca].
Peter K. Kwapong, Department of
Biological Science, University of Cape Coast,
Cape Coast, GHANA[pkwapong@yahoo.com].
Ricardo Costa Rodrigues de Camargo,
Empresa Brasileira de Pesquisa Agropecuária(EMBRAPA Meio-Norte), Av. Duque de Caxias
5650, Buenos Aires, Teresina, Piauí BRAZIL,
Tel: +55 86 32251141 ramal 270 e fax 55 86
32251142 [ricardo@cpamn.embrapa.br]
Rogério Gribel, Departamento de Botânica,
Instituto Nacional de Pesquisas da Amazônia(INPA-CPBO), Caixa Postal 478, Aleixo, CEP
69011-970, Manaus, Amazonas, BRAZIL, Tel:
+55 92 643-3112 [rgribel@inpa.gov.br].
Rui Carlos Peruquetti, Departamento de
Biologia Geral, Universidade Federal deViçosa (UFV), Av. P.H. Rolfs, s/nº, CEP 36571000, Viçosa, Minas Gerais, BRAZIL[peruquetti@ufv.br].
Simon G. Potts, Centre for AgriEnvironmental Research (CAER), School of
Agriculture, Reading University, PO Box 237,
Reading, RG6 6AR, UK, Tel: +44-118-3786154 , Fax: +44-118-378-6067[s.g.potts@reading.ac.uk].
Tereza Cristina Giannini, Departamento de
Ecologia, Instituto de Biociências,
Universidade de São Paulo (USP), Rua doMatão, travessa 14, nº 321, CEP 05508-900,

São Paulo, São Paulo, BRAZIL, Tel: +55 113091-7527 [giannini@usp.br].
Terry Griswold, United States Department ofAgriculture (USDA), Bee Biology &Systematics Lab., Utah State University,
Logan, Utah 84322-5310, USA,
Tel: +01 435 797-2526[tgris@biology.usu.edu / tgris@cc.usu.edu].
Uma Partap, Pollination International Centre
for Integrated Mountain Development(ICIMOD), P.O Box 3226, Kathmandu, NEPAL,
Tel: 09977-1-5525313,
Fax 00977-1-5524509[upartap@icimod.org.np].
Valdemar Belchior Filho, Centro Brasileirode Apoio à Pequena e Média Empresa(CEBRAE), Rua Rui Barbosa nº 1, Centro, CEP
59600-230, Mossoró, Rio Grande do Norte,
BRAZIL, Tel: +55 84 315-4346[valdemar@sebraern.com.br].
Vera Lúcia Imperatriz Fonseca,
Universidade de São Paulo, Faculdade deFilosofia Ciências e Letras de Ribeirão Preto,
Departamento de Biologia, Av Bandeirantes,
3.900, Monte Alegre, 14040-901 - Ribeirão
Preto, SP, BRAZIL, Tel: +55 16 36023815,[veralif@ffclrp.usp.br], Laboratório deAbelhas, Departamento de Ecologia, Institutode Biociências da USP, Rua do Matão 321
trav 14, Cidade Universitária, CEP 05508900,
São Paulo, SP, BRAZIL, Tel: +55 11 30917533,[vlifonse@ib.usp.br].

16

Acronyms

API African Pollinators Initiative
ARS Agricultural Research Service
BPI Brazilian Pollinators Initiative
CBD Convention on Biological Diversity
CI Conservation International

PDF B Project Development Facility phase B
SBSTTA Subsidiary Body on Scientific,
Technical and Technological Advice
TDWG Taxonomic Database Working GroupUFC Federal University of Ceará

COP Conference of the Parties

USDA United States Department ofAgriculture

CRIA Reference Center on Environmental
Information

USP University of São PauloEMBRAPA Brazilian Agricultural Research
Corporation
EPI European Pollinators Initiative
EPUSP Polytechnic School, University of SãoPaulo
FAO Food and Agriculture Organization of
the United Nations
FUSP São Paulo University Foundation
GBIF Global Biodiversity Information Facility
GEF Global Environmental Facility
ICIMOD International Centre for Integrated
Mountain Development
INESP Internacional Network for Expertise in
Sustainable Pollination
INPA National Institute for Amazonian
Research
IPI International Pollinator Initiative
ITIS International Taxonomy Information
Service
MMA Ministry of Environment
NAPI North American Pollinators Initiative
OREADES Brasilian NGO

Presentation 17

Presentation

Workshop preparation
In October 1998, São Paulo Workshop on
Sustainable Use of Pollinators for Agricultural
Use was held, and as a result from this meeting the São Paulo Declaration on Pollinators
was constructed. It was submitted to theConvention of Biological Diversity (CBD), in
its 5th Conference of Parties (COP), in
Nairobi, 2000, where the International
Pollinators Initiative (IPI) was approved as a
new program related to sustainable agriculture. Food and Agriculture Organization of
the United Nations (FAO) was invited to be afacilitator of this process. In COP6 from
CBD, 2002, a plan of action for IPI wasapproved for guiding the actions of regional
pollinator initiatives, proposing goals to beattained in 10 years.
Meanwhile, regional efforts related to IPI
developed. In Brazil, several activities were
performed, coordinated by a committee informally established by the focal point in Ministryof Agriculture, in 2002, during the main
Brazilian meeting on bees (V Encontro sobre
Abelhas, Ribeirão Preto). Among these activities was the FAO proposal of a workshop
related to discuss standardized methodologies
and assessment of best practices in agriculture to promote biodiversity in agro ecosystems. The title SP Declaration on Pollinators+5, for meeting to be realized in 2003, wassuggested by M. Ruggiero during a workshop
in Mabula, Africa, and promptly accepted.
The preparation of this workshop
focused the awareness in the issue to thepotential participants of the Brazilian
Pollinator Initiative (BPI) program, in this initial phase: scientific community in consolidate and emergent groups, including here
the agricultural staff from EMBRAPA andother agronomic schools that could beengaged in this initiative. For discussing common routes for the International Pollinator
Initiative, we also invited the leaders of otheralready established Pollinator Initiatives, likethat of the International Centre for Integrated
Mountain Development (ICIMOD): North
American, European, African, and Asian. In
Brazil, EMBRAPA and bee researchers from all
country (15 research centers, from 15 states)
were invited. We had 77 attendants to thisworkshop. Eleven countries participated inthis SP Declaration on Pollinators plus 5.
International Taxonomy Information Service(ITIS), Internacional Network for Expertise in
Sustainable Pollination (INESP) and FAO werealso organizations that were present. Federal
government ministries from Science andTechnology and Environment also gave theirsupport for this workshop, a counterpart to
FAO support.
Taking advantage of the audience at theSP +5 Forum, a second workshop, Pollinators
Initiatives and The Role of IT: Building
Synergism and Cooperation, was proposed to
discuss and disseminate the importance ofInformation Technology for the Pollinator
Initiatives, to help to promote partnership andexchange experiences on the development
and use of these technologies, and to discuss
funding opportunities.

18

International Pollinators
Initiatives
The North American Pollinator Initiative (NAPI)
comprises an established net of institutions,associations and researchers involved in thepollinators’ issue, as well as in the ecologicalservices provided by pollinators. It is a publicprivate partnership of pollinators’ conservation programs. Among the milestones of pollinators programs are The Forgotten
Pollinators Campaign (1996), the São Paulo
Declaration on Pollinators Conservation andSustainable Use (1998), the North American
Pollinator Protection Campaign (NAPPC) in
1999, the International Pollinator Initiative (IPI)in CBD (2000; 2002). This is a science-based
program, “a portfolio of programs, projects
and activities from the public and private sector, connected by a spirit of cooperation”(Ruggiero, et al., 2004)
The European Pollinator Initiative (EPI) has
adopted the same framework of the IPI, thefour key components being: assessment, adaptive management, capacity building and mainstreaming. To assess pollinator loss, the ALARM(Assessing of LArge-scale Environmental Risks
with tested Methods) project was developed,
combining the expertise of 54 partners from26 countries. This program started on February
1st., 2004, and it is planned for 5 years initially. In particular, risks arising from pollinators’
loss in the context of current and future land
use in Europe will be assessed. SUPER (Sustainable Use of Pollinators as an European
Resource) will be built directly upon ALARM to
address identified declines in European pollinators resources in a socially and economically
viable manner (Potts, 2004).
The African Pollinator Initiative (API) wasestablished in 1999, as the African network of
the IPI. “It strives to improve communication
channels between all people and organizations

interested in pollinators and pollination biology,
including biodiversity conservation, agriculture
and general awareness, and to facilitate collective achievements” (Eardley, et al., 2004). In
2002, its first Secretariat was formed, and thePlan of Action of African Pollinator Initiative
was published. At this time, API comprises
Ghana, Kenya and South Africa, but it is open
for other participants. A major need that exists
in Africa is to identify the pollinators. Rapid
assessments, taxonomic efforts and capacity
building are among the main needs.
ICIMOD initiated its pollinator/pollination
program in 1991, to address applied research,development and related issues of pollinatorsand pollination. The overall goal of ICIMOD is
to improve the livelihood of mountain people
by enhancing agricultural productivity andbiodiversity conservation through conservation of indigenous pollinator species in orderto ensure sustainable pollination of crops andother indigenous plant species of the Hindu
Kush-Himalayan region. Several activities arebeing undertaken concerning pollinators(Partap, 2004).
The Brazilian Pollinators Initiative (BPI) wasconstructed based on the São Paulo
Declaration on Pollinators, which stimulated
international interest and provided strategic
direction for pollinator conservation planning(Dias, et al., 1998; Kevan and ImperatrizFonseca, 2002; Imperatriz-Fonseca & Dias,
2004; Imperatriz-Fonseca, et al., 2004).
API, BPI and ICIMOD are together in a GEF(Global Environmental Facility) project entitledConservation and Management of Pollinators
for Sustainable Agriculture Through an
Ecosystem Approach, with FAO as the facilitator. In this global scenario, with pollinators inmainstreaming in developed countries andalmost unknown in undeveloped countries, apartnership among scientists and stakeholders
will improve capacity building and sustainable

Presentation 19

use of pollinators. As the general frameworkof IPI is adopted by all initiatives, including here
standardized methodologies for assessments,
it was considered essential to join leaderships
to discuss goals, needs and opportunities. For
global comparisons, assessment methods
must be standardized.

Methodological discussions
The talks were organized in order to give support for the discussion on which standard
methodologies should be used in the development of the Brazilian Pollinator Initiative. Inoral presentations, several aspects of themethodologies applied until now in pollination
research and pollinators assessment were presented by the specialists, showing how some
important issues should be considered infuture actions. Subjects, such as the influenceof individual collector performance in assessment, methods to be applied in assessment
research, long-term and short-term evaluations, introduction and restoration of pollinators, performance evaluation in solitary pollinators, meta analysis of data on plant-pollinator relationships, and priorities for pollinators
programs, were presented. Gene flow, beespecies visiting flowers of important crops andpollinator breeding possibilities in Brazil werealso part of oral presentations and specificgroup discussions.

Protocols and discussions
The sessions’ coordinators established a protocol to be discussed during the workshop. The
groups were directed to discuss the methods tobe standardized, and to suggest themes for the
PDF B (Project Development Facility phase B ) of
the GEF project. We needed to consider theenormous task for some themes, which obviously could not be concluded within a 5-day
workshop. Some general comments follow.
The first group discussed assessment
methods for pollinators’ status. Although they
advanced in the analysis of different methods,
the task was not concluded. The main methods to be applied were pointed out, but only
indications for the manual of standard methods were made. Coordinators answered the
proposed questions, gave orientation for casestudies and suggested the next steps in the
PDF B of the GEF project.
The gene flow group presented a conclusive report. They also indicated the chosen
methods to be used for different purposes,
without describing them. Gene flow studies
must be included in the full project, and aselection of subjects was suggested by thegroup for next steps.
Management of bees that could be usedas crop pollinators was the next subject, divided into 3 parts: honey bees; stingless bees;
and bumblebees and solitary bees.
In Brazil, as well as in other countries,
honey bees are used as generalist pollinators
because they are abundant, easy to breed andto manage in crops. Honey bees were focusedon for crop pollination in the important
McGregor’s book, Insect pollination of cultivated crop plants, still very useful and updated online. However, Brazil has the Africanized honeybee, which requires special management practices, and knowledge related to their performance as pollinators. In fact, they are quite
effective in pollination, as Roubik (2002) pointed out for coffee production in Panama, andas Couto (2002) discussed for several crops.
The honey bees study group presented a very
comprehensive report, with valuable suggestions and guidelines for further applications ofbees as pollinators. Pollination by honey bees
could be much improved by technology

20

advances in management, nutrition, pathology and mechanization, especially for transport
to pollination sites. Farmers need to be madeaware of the benefits of incorporating pollination into their management practices
Brazil has only seven species of bumblebees (Bombus); nevertheless they are abundant all over the country. They are generally
very aggressive, and are not reared for pollination purposes in Brazil. The carpenter bee,
Xylocopa, can be reared and is a good pollinator of passion fruit, among other crops. There
are 49 species of carpenter bees in Brazil(Silveira, et al., 2002) that are potentially
important in agriculture. The solitary bees
management group did a very comprehensive
report, presented the main plants that should
benefit from their use as pollinators and theneeds for breeding them in large quantities.
An effort for a workshop focusing only onthese bees as pollinators was indicated as aneed, and was held in April 2004.
Stingless bees are native in Brazil, withmore than 500 species in the country.
Breeding techniques are known for somespecies. Most stingless bees species have notbeen studied yet. Their use as pollinators is
effective for some species (see Heard, 1999;
Malagodi-Braga, et al., 2000), but they are notbred on a large scale to be available for agricultural purposes. They have a high potential
for the use as pollinators: they are diverse,
have perennial nests, are generalists, but also
show floral preferences (Ramalho, et al., 1990;
Biesmeijer, et al., 2005), they communicate floral resources to nestmates, they do not sting,and they store food inside the nests. The use
and conservation of stingless bees was discussed by this group, and next steps for related activities suggested.
It is important to point out that if funding
is not available to develop bee biology projects
and to improve the local knowledge and forcapacity building concerning the other bee
species, Africanized honey bees will soon be
the only available pollinators in sufficientquantity for agricultural use in our country.
Loss of habitat and increasingly intense agricultural practices are clearly reducing thenative bee populations. Introduced into theAmericas, honey bees are generalists and in
most cases less effective for biodiversity conservancy. The result will be a drastic loss inplant biodiversity and in agricultural production, especially in the more tropical regions.

Information Technology and
the Pollinators Initiatives
For this one-day workshop, held during thelast day of the SP+5 Forum, speakers representing the various Pollinators Initiatives present were invited. Other presentations focusedon local initiatives: the Brazilian Pollinators
Initiative and local projects that make a strong
use of Information Technology (IT) and are
related to pollinators. The speakers were asked
to give a short presentation focusing on how
IT is used presently and how, in their own
point of view, it might contribute for theadvancement of the national, regional andinternational Pollinators Initiatives. Some time
was allowed for discussions on issues such astechnology and data sharing, systems integration and also funding needs and strategies.

Workshop results, as well as the oral presentations, are on line at http://www.webbee.org.br.

Presentation 21

References
BIESMEIJER, J.C.; SLAA, J.; CASTRO, M.S.; VIANA, B. F.; KLEINERT, A. M. P. & IMPERATRIZFONSECA, V.L. 2005. Connectance of Brazilian social bee-food plant networks is influenced byhabitat, but not latitude, altitude or network size. Biota Neotropica, 5(1):1-10.
COUTO, R.H.N. 2002. Plantas e abelhas, uma parceria em crise? Anais do V Encontro sobre abelhas, Ribeirão Preto, p. 87-94.
DIAS, B.F.S.; RAW, A. & IMPERATRIZ-FONSECA, V.L.1998. International Pollinators Initiative:
The São Paulo Declaration on Pollinators. Report on the Recommendations of the Workshop
on the Conservation and Sustainable Use of Pollinators in Agriculture with Emphasis on Bees.
(http://www.fao.org/biodiversity/docs/pdf/Pollinators.PDF), accessed on August 29th 2004.
EARDLEY, C.; GEMMIL, B.; KWAPONG, P. & KINUTHIA, W. 2004. The African Pollinator Initiative.
In: FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearing and management inpollination. Fortaleza, Imprensa Universitária, p. 67-69.
HEARD, T. 1999. The role of stingless bees in crop pollination. Annu.Rev.Entomol., 44: 183-206
IMPERATRIZ-FONSECA, V.L. & DIAS, B. F. S. 2004. The Brazilian Pollinator Initiative. In: FREITAS &PEREIRA (eds.). Solitary bees: conservation, rearing and management for pollination. Fortaleza,
Imprensa Universitária. p. 27-33. Available at http://www.webbee.org.br , accessed on August
29th 2004.
IMPERATRIZ-FONSECA, V.L; FREITAS, B.M.; SARAIVA, A.M. & DIAS, B.F.S. 2004. The Brazilian
Pollinator Initiative: Challenges and opportunities. In: Annals of the 8th IBRA International
Conference on Tropical Beekeeping and VI Encontro sobre abelhas, Ribeirão Preto, in CDROM.
KEVAN, P. G.; IMPERATRIZ-FONSECA, V. L. (eds.). 2002. Pollinating bees: the conservation link
between agriculture and nature. Brasília, Ministério do Meio Ambiente, 313pp. Available at
http://www.webbee.org.br , accessed on August 29th 2004.
MCGREGOR, S.E. 1976. Insect Pollination of cultivated crop plants. USDA-ARS, Washington,
DC. Available at http://gears.tucson.ars.ag.gov/book/index.html , accessed on August 29th 2004.
PARTAP, U. 2004. An overview of pollinators’ research and development in the indu KushHimalayan Region. In: FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearing
and management in pollination. Fortaleza, Imprensa Universitária, p.57-66.
POTTS, S. (ed.). 2004. European Pollinators Initiative (EPI): Assessing the risks of Pollinators loss. In:
FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearing and management in pollination. Fortaleza, Imprensa Universitária, p. 43-55.
RAMALHO, M.; KLEINERT-GIOVANNINI, A. & IMPERATRIZ-FONSECA, V. L. 1990. Important bee
plants for stingless bees (Melipona and Trigonini) and Africanized honey bees (Apis mellifera) in
neotropical habitats: a review. Apidologie, 21:. 469-488

22

ROUBIK, D.W. 2002. Feral African Bees augment Neotropical coffee yield. In: KEVAN, P &IMPERATRIZ-FONSECA, V.L. (eds.). Pollinating bees: the conservation link between Agriculture
and Nature. Brasilia, p. 255-266. Available on line in http://www.webbee.org.br.
RUGGIERO, M.; BUCHMANN, S. & ADAMS, L. 2004. The North American Pollinators Initiative. In:
FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearing and management in pollination. Fortaleza, Imprensa Universitária. p. 35-41.
SARAIVA, A.M. & IMPERATRIZ-FONSECA, V.L. 2004. A proposal for an information network for theBrazilian Pollinator Initiative – BPI – based on WebBee. In: Annals of the 8th IBRA International
Conference on Tropical Beekeeping and VI Encontro sobre Abelhas, Ribeirão Preto, in
CDROM.
SILVEIRA, F. A.; MELO, G.A.R. & ALMEIDA, E.A.B. 2002. Abelhas brasileiras, sistemática e identificação. Belo Horizonte, 253pp.

WORKSHOP I
Survey methods for bees as pollinators in Brazil:
assessing the status and suggesting best practices

Workshop I 25

Group 1
Surveying and monitoring of pollinators innatural landscapes and in cultivated fields
Participants: Cynthia Pinheiro Machado (Coordinator), Fernando A.
Silveira (Coordinator), Patricia Albuquerque, Jacobus Biesmeijer, Maria
José de Oliveira Campos, Connal Eardley, Barbara Gemmill, Terry
Griswold, Peter Kwapong, Paulo de Marco, Favízia Freitas de Oliveira,João Rodrigues Paiva, Carmen Pires, Simon Potts, Francisco Ramalho,
Mauro Ramalho, Anthony Raw, Márcia Rego, Michael Ruggiero,
Fernando Zanella.

Abstract
This workshop aimed the establishment ofstandard methodologies for bee surveys andmonitoring of natural landscapes and crops.
As there are countries and regions with practically no information about pollinator fauna,
three strategies for pollinator investigation
were addressed: 1) rapid assessments; 2) surveys and 3) monitoring programs. The
expected product was a manual for standard
methodologies for bee surveys and monitoring in natural landscapes and cultivatedfields. Some basic principles were observed:
data must be reliable and adequate for statistical analyses, and all suggested strategies
were to be realistic, considering time, personnel and costs constraints, and flexible enoughto be applied in different environments.
Surveys should be question oriented. It
became obvious that no rigid protocol could
be built for all situations across the world,
then only general guidelines, not protocols,
were suggested in order to meet the basic
principles listed above. Since no comparative

data exist in those methodologies, no consensus was reached on which methods torecommend for given situations, but comparative data should be sought for before any
definitive recommendations can be built in
the context of the Brazilian Pollinator
Initiative. Three case studies, in a cotton field,in the Atlantic Forest and in open savanna,
illustrate how recommendations could be
used in the development of survey and monitoring protocols.

Aim
Establishment of standard methodologies forbee surveys and monitoring of natural landscapes and crops.

Expected ProductProduction of a manual of standard methodologies for bee surveys and monitoring of natural landscapes and cultivated fields.

26

The pollination crisis andthe need for surveys
and monitoring programs
The impact of deforestation, habitat fragmentation, introduction of exotic species andunfriendly agricultural practices is believed to becausing a decrease in wild pollinator populations. This, in turn, is suspected to be the causeof low fruit and seed productivity in many crop
plants, with economic consequences in many
parts of the world. Also the productivity of wild
plants may be affected, and this can lead to
local extinction of populations of those plants,
as well as of the animals depending on them.
Since this “pollination crisis” was recognized, much effort has been put into initiatives
to conserve and sustainably use wild pollinators. However, it is widely recognized that welack much of the knowledge we need to propose effective actions to achieve conservationand management practices. We are not evencertain about the geographic extension andintensity of pollinator population decreases.
We also lack basic information on how the different factors affect wild populations of flower
visiting organisms.
Two basic questions stand out as being of
surmount importance for any conservation orsustainable management initiative to succeed:1) which pollinator species exist in any given
place? 2) how are their populations fluctuating
along time?
For these questions to be answered, weneed to invest in pollinator faunistic surveys
and in monitoring programs.

Results
The group discussed the general structure ofstandard procedures to survey and monitor
bees in cultivated fields and natural areas.

Rationale• Data to be obtained by the suggested
guidelines will be used in the context of theBrazilian Pollinator Initiative and should be
useful for other initiatives around the world.
• As there are countries and regions with practically no information about pollinator fauna,
three strategies for pollinator investigation
were addressed: 1) rapid assessments; 2) surveys and 3) monitoring programs.

Recommendations
Basic principles
The group agreed that suggested actions should:• Assure data quality, i.e., data must be reliable
and adequate for statistical analyses.
• Be realistic, considering time, personnel andcosts constraints.
• Be flexible enough to be applied in different
environments.
• Be question oriented.
Difficulties
Members of the group suggested and discussed
various methods in use across the world.
Different people had different experiences withdifferent methods. For example, some had very
good results in using pan traps for collecting
bees, while others obtained meager data fromtheir use. Such differences could be due to different designs, different environmental conditions, etc. It became obvious that no rigid protocol could be built that could be recommended for all situations across the world; even within Brazil; the group was not able to decide on
specific methods to be employed, due to thevarying opinions on their efficiency.
Thus, it was decided that only general
guidelines would be built, so that dataobtained from surveys and monitoring programs, using any combination of the suggest-

Workshop I 27

ed methods, would meet the basic principles
listed above. It was hoped that further comparison of the different methodologies would
enable sound choice of methods in the future.

Considering the difficulties exposed
above, the following recommendations shouldbe accepted as guidelines, not protocols, inorder to assure their applicability.

Rapid Assessments and Surveys
Aims
To best describe given local faunas. To maximize number of species recorded.

Type of data
Species records

Through collection and deposit as vouchers in public collections.

Species Abundance

Not necessary. Priority should be given to increase the number of new
species detected.

Habitat description

Follow a basic protocol** that describes the collection site on many scales.
Geographical coordinates must be taken for species distribution analysis.
When GPS is not available, geographical clues should be used*.

Association with plants

Whenever possible, plants visited by pollinators should be recorded, inorder to give clues on possible target plants for future surveys.

Sampling design
Plan a pilot study to verify the adequacy of techniques.
Plan data collection to be useful in the future as meta data.
Sampling efforts must be measurable and recorded.

Sampling techniques
A combination of methods may be used, but sampling effort for each method should always berecorded. Whenever possible, hand netting should be applied. Other recommended methods are: trap
nesting; aspirators, malaise traps, and pan traps.

Statistical analysis
Use recommended statistical analysis. Statistical techniques should be known in advance. A guide ofstatistical procedures or references should be part of the manual.

Observations Species identification should be made by trained people, with the aid of taxonomic keys and reference collections. Those responsible for identifications should be contacted
in advance. Manuals should include information on national collections and taxonomy services.

28

Aims
To obtain the best estimate of local fauna and bee plant relationships, in order to allow for comparison among areas.

Type of data
Species records

Through collection and deposit as vouchers in public collections.

Species Abundance.

Number of individuals must be recorded in a manner that allows postcollection analysis based on numbers per plant, per hour, per species, andany other relevant unit.

Habitat description

Follow a basic protocol** that describes the collection site in many scales.
Geographical coordinates must be taken for species distribution analysis.
When GPS is not available, geographical clues should be used*.

Association with plants

Plants should be collected and deposited as vouchers in public collections
for identification. Record the resource used by plant visitor. Weather conditions and time of the day must be recorded for resource availability analysis.

Sampling design
Use previous data to plan collection and build a list of expected species.
Plan a pilot study to check the adequacy of techniques.
Plan data to be useful in the future as meta data.
Sampling effort must be measurable and recorded.
Adequate number of replications should be employed. Environment patchiness and plot design
should be taken into account to define the number of replicates.
The sampling area should be visited before sampling, and plant collection and individual plant labelingshould be done whenever possible to facilitate plant identification.
Consider time to be spent in obtaining information on habitat and surroundings that may be useful inthe future.
Identify data that should be collected and only collect data that will be useful for future analyses.

Sampling techniques
A combination of methods may be used, but sampling effort for each method should always berecorded. Whenever possible, hand netting should be used. Other recommended methods are: trap
nesting; aspirators, malaise traps, and pan traps.

Statistical analysis
Use recommended statistical analysis. Statistical techniques should be known in advance. A guide ofstatistical procedures or references should be part of the manual.

Observation: Species identification should be made by trained people, with the aid of taxonomic keys and reference collections. Those responsible for identifications should be contacted inadvance. Manuals should include information on national collection and taxonomy services.

Workshop I 29

MonitoringAims
To identify and describe patterns and variations through time and changing conditions of selectedvariables. To evaluate population fluctuations To guide decisions in conservation actions; To guidedecisions in management actions; To generate basic data for selecting potential pollinators forfurther studies.

Type of data
Species records

Species can be counted or collected, depending on the facility ofidentification and objective of the program.

Species Abundance

Number of individuals must be recorded in a manner that allows postcollection analysis based on numbers per plant, per hour, per species, andany other relevant unit.

Habitat description

Follow a basic protocol** that describes the collection site on many scales.
Geographical coordinates must be taken for species distribution analysis.
When GPS is not available, geographical clues should be used*.

Association with plants

Plants should be collected and deposited as vouchers in public collections
for identification. Record the resource used by plant visitor. Weather conditions and time of the day must be recorded for resource availability analysis.

Sampling design
Use previous data to plan collection and build a list of expected species.
Plan a pilot study to check the adequacy of techniques.
Plan data to be useful in the future as meta data.
Sampling effort must be measurable and recorded.
Adequate number of replications should be employed. Environment patchiness and plot design
should be used to define the number of replicates.
The sampling area should be visited before sampling, and plant collection and individual plant labelingshould be done whenever possible to facilitate plant identification.
Consider time to be spent in obtaining information on habitat and surroundings that may be useful inthe future.
Identify data that should be collected and only collect data that will be useful for future analyses.

Sampling techniques
A combination of methods may be used, but sampling effort for each method should always berecorded. Whenever possible hand netting should be used. Other recommended methods are: trap
nesting; aspirators, malaise traps, and pan traps.

Statistical analysis
Use recommended statistical analysis. Statistical techniques should be known in advance. A guide ofstatistical procedures or references should be part of the manual.

30

Observations: Species identification should be made by trained people, with the aid of taxonomic keys and reference collections. Those responsible for identifications should be contacted inadvance. Manuals should include information on national collection and taxonomy services.

Final Remarks
It was obvious that no fixed protocol could be
provided for all situations. Moreover, different
people had different experiences with different sampling methods. Since no comparative
data exist on those methodologies, no consensus was reached on which methods to recommend for given situations. Thus, such comparative data should be sought for before any
definitive recommendations can be built in thecontext of the Brazilian Pollinator Initiative.

Case Studies – an exercise
Aim
To provide examples of how the above recommendations could be used in the developmentof survey and monitoring protocols.
The group was divided into three subgroups, each of which worked on one casestudy. The resulting protocols presented below
were constructed based upon literature information and the expertise of group members,
with surveys and monitoring of bees on specific crops and in different kinds of environments
taken as examples.

1) MONITORING FLOWER-VISITING BEES
IN COTTON FIELDS
Background
According to Barroso & Freire (2003), three
species of cotton are found in Brazil,
Gossypium hirsutum (L.), G. barbadense (L.)
and G. mustelinum (Mier). Of these, only

herbaceous cultivars of the introduced G. hirsutum are currently cultivated on a commercial
scale in Brazil. However, cultivation systems are
not homogeneous across the large cotton-producing regions of Brazil. An evident contrast
exists, for example, between the small-scale
production found in the small family-heldfarms in the northeastern region of Brazil,
which employ a low technology crop system,and the large scale production system
employed in the huge commercial farms incentral Brazil.
The cotton plant can produce nectar infive different kinds of nectaries distributed
inside and outside the flower. However, not allof these nectaries occur in every cultivar (Free,
1970; McGregor, 1976). Many different
organisms are attracted to the cotton flower
by the nectar and pollen it produces. Amongthese, insects and especially bees are the mostabundant. These flower-visiting species may
contribute to increases in fiber production
and/or quality (Free, 1970; McGregor, 1976).
The suggestions below were constructedconsidering a small-scale system. Considerations
on how to expand this protocol to a largescale, high-technology system are presented at
the end of this exercise.
SurveyThe survey of cotton-flower visiting species is
proposed for 1 ha fields, considered here as
sampling units. This is an average size field forcotton in Northeastern Brazil. In each such
sampling unit, two sampling procedures
would be executed in parallel:A) Arbitrary sampling. This protocol
aims to maximize the number of flower visit-

Workshop I 31

ing species recorded on cotton plants. The
field is slowly inspected and all bees found on
the cotton flowers or flying above them arecollected. It is important to call attention to
the fact that the deep corolla of the cottonflower makes the use of hand nets relatively
inefficient, as the flower protects the visiting
insects. For this reason, complementary capture methods are suggested: forceps, insect
aspirators and hand nets, depending on thesize and position of the bees.
B) Systematic sampling. This protocol
aims to quantify the relative density and abundance of flower-visiting species. Sampling is tobe done weekly in 10 plots, each including 80
cotton plants, 20 in each of four neighboringrows. Those plots should be homogeneously
distributed across the field, including areas
close to its border and center. Areas close topatches of natural vegetation and other special environments around the field also should
be considered. Each plot is sampled for 10 min
by slowly walking between the rows. Any bees
found inside the flowers and on extra floral
nectaries will be collected.
Both sampling procedures should be executed weekly, between 8:00 and 12:00, along
the flowering season. Sampling should bedone preferably during sunny days, when bees
are most active at flowers. Any cultivation
practice proceeded between and on samplingdays should be recorded.
Monitoring
Monitoring can be done by repeating yearly
the systematic sampling procedure describedabove. In this way, average abundance of thewhole flower-visiting assemblage and of target species can be compared between years
and along longer periods. These numbers canalso be associated with factors such as climatic parameters and the amount of pesticide application.

Adapting the protocols for large-scale,
high-technology systems
The same 1 ha sampling units could be used,each with 10 sampling plots, as explained
above. Such sampling units should be homogeneously distributed inside the cotton fields,
the number of such units being proportional
to the size of the fields, with some of themclose to the borders and others within the interior of the fields.

2) BEE SURVEYS AND MONITORING OFA FRAGMENTED LANDSCAPE IN THE
ATLANTIC RAIN FOREST BIOME
Background
The Atlantic Tropical Rain Forest is a recognizedbiodiversity hot spot. Its original vegetation
cover has been reduced to 8%, and what is left
is threatened by human presence. Population
growth has led to destruction of the forest
through uncontrolled urban expansion, industrialization and migration of people from otherareas (Galindo –Leal & Câmara 2003). About
100 million people live in the mega cities located in the Atlantic Forest Region, along with thelargest industrial and silvicultural centers. On
the other hand, the biodiversity harbored by the
Atlantic Forest is one of the greatest in theworld. We believe that 60% of the terrestrial
species of the planet live within the remaining
areas of this forest. This is probably a result of
the large range of latitude it covers, its variationin altitude, the diverse climatic regimes, and theavailability of water and energy to the system(Pinto & Brito 2003). These forests are highly
stratified, with a canopy as high as 35 meters.
SurveyPollinator surveys should be made along transects. The determination of size, placement andnumber of transects will depend on the hetero-

32

geneity of the forest community, which should
be understood beforehand. The size of the transects should be such that they can be coveredin one day. They should be 100 m long.
The sampling units will be flowering
plants, with all bees found being collected at
all the flowering plants that they visit. Hand
nets will be the principal collection method
and will be complemented by euglossine baits.
Additional methods such as pan, malaise andlight traps and also new baits such as
salt/ammonia and antifreeze should be tried.
Sampling should be repeated 3 to 5 times
a month for 8 to 12 months per year, depending on flowering phenology and flower density.
Monitoring
The goal of the suggested monitoring program is to detect differences in bee diversity in
disturbed and undisturbed forests over time. It
could also be used to compare different
degrees of disturbance.
Sampling units are similar to those used in
the survey. Monitoring subjects may be selected, based on survey results. For example,
euglossines or Melipona. Such subjects a)
include species sensitive to deforestation; b)occur in large numbers and c) can easily be
identified. Still other subjects could be considered, such as Apis mellifera, trap-nesting
Centris or specialist taxa.
The monitoring design should include sitein or adjacent to undisturbed area (control),disturbed area (treatment 1) and intermediatearea (treatment 2).
A minimum of five years of sampling isneeded for conclusions to be drawn.
3) SURVEY OF POTENTIAL POLLINATORSIN THE BRAZILIAN SAVANNA, AND A
MONITORING PROGRAM TO EVALUATE
THE IMPACT OF GRAZING ON FLOWER
VISITORS´ RICHNESSBackgroundThe biome of the Cerrado is a gradient of vegetation physiognomies, including open fields,savannas and open-canopy forests. It covers
about 25% of the Brazilian territory and wasincluded among the world’s hotspots (Myers,
et al. 2000), for combining high biodiversity
and high rates of disturbance. Until 40 years
ago the Cerrado was primarily used for extensive cattle raising. By 1988 Klink & Moreira(2002) estimated that 35% of the natural
cover had already been removed. In a recent
study, using MODIS satellite images of 2002,(Machado, et al.,2004) concluded that the natural cover loss has changed to 55% .
Agriculture occupies 6% of the total area,
but this figure is increasingly stimulated bypresent national agricultural policy. Pasturesand large plantations of soybean and cotton
are the major threats for the biome, causing
soil loss, water pollution, habitat loss, habitat
fragmentation, introduction and spread ofvery agressive invasive species, like African
grasses, among others (Buschbacher, 2000;
Fearnside, 2001; Klink & Machado, 2005).
Forecast is not optimistic, according to Machado, et al. (2004), based on present vegetation removal rates by 2030 the whole biome
may have given place to agricultural and cattle
raising activities.
Major impacts on pollinators are apparently caused by intense use of chemicals, aerial spraying, and habitat removal; the latterprovokes reduced nesting opportunities andfood availability.
According to Silberbauer-Gottesberger
and Eiten (1987), the plant species richness of
the Cerrado open areas is among the highest
known for non-forest vegetation. Seasons arevery well defined. The dry season lasts from 3
to 5 months, during winter, and the wet season peaks in December-January. Flower
resource availability varies through the seasons

Workshop I 33

(Oliveira & Gibbs, 2002), but flowers are foundthroughout the year (Batalha, 1997). Bee surveys in the Cerrado area have been carried out
in Central Brazil, around Brasília, in Minas
Gerais State, in the Northeast and in someperipheral areas in São Paulo state (PinheiroMachado et al., 2002), allowing for a baseline
data set for native fauna.
SurveyThe Cerrado vegetation is a natural mosaic,with many vegetation types, varying from open
grass fields to dry forests. Therefore a previous
analysis of the sampling area has to be done
before designing the survey. The following steps
can be used to guide the sampling procedures.
1.The very first task must be the definition of
the question that the survey is aiming to ask;
all of the succeeding steps depend on a veryclear and objective question.
2.A good view of the large area, using satellite
images or local driving around to picture theheterogeneity of the area to be sampled.
3.Accessing previous studies in the area, orsimilar areas, to create estimates of diversity
and sampling effort necessary to best
describe the focal fauna. Some calculations
involving sampling curves in a standardized
way with previous data may be necessary;
the studies should indicate period of activity,
both seasonally and daily.
4.Visits to collections will produce a better
species list and expected richness numbers,
because collections are believed to include
many unpublished data.
5.Local evaluations prior to the surveys provides familiarization with flora and allows
identification of potential plant species for atarget survey. This may be crucial, especiallyin the case of very short budgets. Simple
things that might turn into difficulties in thefield can be observed, like the height oftrees to be sampled. Previous studies may

also provide information about plant species
intensively visited by bees.
6.Although Brazilian researchers use hand netting as the main technique for sampling bees,
examination of previously published studies
that have used other methods can indicate
what part of the community is not being
sampled if hand netting is the only technique.
7.Plan the type of analyses that will be carriedout and assure that the experimental design
will provide proper data.
8.Sampling area should be marked at the field.
Site selection must be guided by the question proposed for the survey. The chosen sitemust be representative of the environmental situation to be investigated. If a unique type ofvegetation or physiognomy is targeted, an evaluation will need to be made to determine if thechosen site adequately represents the situation
to be surveyed. This also applies when gradientsor mosaics are the case. Replication and control
areas are important parts of some surveys andhave to be considered during site selection.
Another very important point is the accessibility of the site and all the permits thatshould be obtained, both from private
landowners and governmental agencies.
Sampling design and sampling techniques
Sampling design involves choices of sampling
unit format, size, number and spatial distribution. For instance, if an overview of diversity inthe area is the aim, sampling units will be need
to be randomly distributed; if diversity information is to be linked to habitat, sampling
units should be selected in a way that they
represent all desired situations (Alonso &Agosti, 2000). The sampling design has toconsider areas greater than 2 ha because of
the typical spatial distribution of plants in the
Cerrado. At least 10 transects 2 m wide by 1
km long, or 5 quadrats of 40x100m, should be34established. The method should be calibrated
against known areas by follow-up procedures
using species accumulation curves (Soberón &Llorente, 1993) to inform about the efficiencyof the chosen design and techniques. Species
accumulation curves are produced from
species-by-sample matrices in a spreadsheet,and they can be carried out by the EstimateS
program (Colwell, 1997).
Sampling techniques that minimize thecollectors’ interference are preferred, but thebest results in Brazil have so far been achieved
using hand nets. To minimize differencesamong collectors, previous training is mandatory. Different species have different behavioursat flowers; some of them can be very fast andsensitive to movement. Collectors must be
advised to collect any bees and all wasps andsmall flies, because some bee species looks likewasps or are too small to be differentiatedfrom another insect when observed in the field.
Recommended techniques are hand nettingand sweep netting in transects. Although
pan traps have not had good acceptanceamong Brazilian researchers, good results andnew fluorescent colors reported from othercountries speak for its use. Pan traps tend to
be selective for certain groups, so they should
not be used as the only technique for inventories. The best method may vary according tosite and logistics, but best results in species
numbers are usually achieved when multiple
methods are applied.
The length of the transect needs to be
standardized, but it will depend on the aim of
the survey, as discussed above. If the transect
is divided into sub samples, these should be
kept separated for posterior analyses. The
starting point of the transect should be picked
at random, in order to avoid always collecting
during the peak activity period at the same
part of the transect. One needs to be sure thatthe peak activity period is always covered bysampling effort. Collectors should also be randomized along sites to minimize bias from collecting ability.
Complementary data is very important fordata analysis, so a protocol should be applied
to every survey. Recommended data to begathered are the following:• site location with coordinates; use a GPS; if
this is not available, report local geographic
references like roads, bridges, or equivalents;• date, including month/day/year ;• time of the day, indicating sampling hours;• a clear vegetation classification, informing
not only details about the vegetation foundin the sampling areas, but also the characteristics of the landscape in which is it situated;• the size of the total area from which samples are taken must be indicated, because
results are expected to vary if collecting sites
are a part of a 1 ha, a 100 ha or a larger areaof Cerrado;• general climate description and classification
are very useful and must be complemented
with local weather conditions during the collection days and information about averagetemperature and rainfall whenever possible.
Floral associations are important complementary information, but time can be saved ifcollectors add flowers to a bag, identify it, andleave a numbered tag on the plant to proceedwith plant identification later on.
Field equipment must include spare handnets, and enough vials to avoid jamming various insects into each vial. All material is to belabeled in advance allowing quick field information to be made promptly.
After fieldwork some procedures are recommended that will make data easy to analyze for anyone interested:• standardize the format of data presentationand codes to facilitate understanding at all
instances of the study;

Workshop I 35

present results by simple summary descriptors, like species richness, and common andpopular diversity indices;• feed data bases that provide access to thegeneral pubic; indicate the collection wherevoucher material was deposited.
•

Monitoring
The proposed exercise for this group was togive directions for monitoring the impact of
cattle raising activities on the biodiversity ofpollinators. The group started with the statement of the leading question: What is theimpact of introducing cattle “on pollinators”?
To address this question, previous data
about bees and their relationship with flowersof open areas will be gathered. This information will be used to choose focal groups formonitoring activities. Preference will be given
to bees sensitive to gradients that are in thiscase understood to range from original nongrazed areas to heavily grazed areas. If preliminary data fails to point out the taxa to bemonitored, the initial monitoring is used toestablish a baseline for further comparisons.
The preliminary data will be tested for correlation with desired variables, like bee diversity.
Once a strong and significant statistical relationship is found, collections will be repeatedthrough time. The sampling design is the sameone proposed for the survey, but will be
repeated through time.

HOW DATA FROM MONITORING WILL BE
USED IN THE CONTEXT OF BPI?
Monitoring depends on the choice of soundand easy to measure variables. Variable selection can be made based upon previous data. It
is recommended that a selected taxa or a guild
is used for monitoring, but the relationshipbetween the measured variable and the objectof monitoring should be understood and supported by a strong significant positive correlation. Direct relationships are preferred. If therelation between the measured variable andthe object of monitoring is not already known,
assumptions must be stated clearly at the
beginning of the monitoring program. The
selection of a specific taxa or guild must take
into consideration the characteristic that the
focal organisms are abundant and easy to identify. A previous survey is mandatory for areas
where data is lacking, to improve the chance ofchoosing good taxa to be monitored.
Some general recommendations could
be made for all situations involving pollinator surveys and monitoring:
Training. One problem raised about the useof “manual” collection methods, such as
hand-netting is the effect of different abilities
of different people to find and capture bees.
This problem can be reduced by properly training collectors before actual sampling is begun.
Replication. An appropriate number of
replicates should be set, according to environment heterogeneity and/or other importantfactors. Pseudo-replication should be avoided.
For instance, 12 monthly samples collected at
one site cannot be considered as replicationsof different disturbance grades or environment
types. In these cases, different areas should besampled as replications of each treatment.
Identification and voucher specimens.
Specimens both of target (pollinators) andassociate (e.g. food sources) taxa should beproperly collected, preserved and labeled tofacilitate proper identification. Such identification should preferably be done by experienced
personnel. Moreover, voucher specimens of all
taxa involved should be deposited in public
collections that should be indicated in reports
and publications, so that their identification
can be checked at any time.

36

Final remark
The group was composed of a number of
researchers with experience in bee surveys
and monitoring. However, the members had
different thoughts about the different methods. In part, this may be a consequence of theeffect of different environments (including
composition of regional bee fauna) on sam-pling methods. Consequently, methods thatwere reported by some as very efficient, did
not produce good results in other places,
when used by other people. It was suggested
that experiments (like those going on under
the auspices of the European Pollinator
Initiative) should be made on a regional scale,so that a final choice of methods can be madefor each region.

References
AGOSTI, D., MAJER, J.D., ALONSO, L.E. & SCHULTZ, R. 2000 Biodiversity studies, monitoring andants: an overview. In: Ants. Standard methods for measuring and monitoring biodiversity.
Smithsonian Institution Press. Washington DC, USA, p. 1-8.
BARROSO, P. A. V. & FREIRE, E. C. 2003. Fluxo gênico em algodão no Brasil. In: PIRES, C.S.S.,
FONTES, E.M.G. & SUJII, E. R. Impacto Ecológico de Plantas Geneticamente Modificadas.
EMBRAPA, Brasília-DF, Brazil, p. 163-193.
BATALHA, M. A. 1997. Análise da vegetação da ARIE Cerrado Pé-de-Gigante (Santa Rita do
Passa Quatro, SP). Masters thesis. Universidade de São Paulo, São Paulo-SP, Brazil, 185 p.
BUSCHBACHER, R. 2000. Expansão agrícola e perda da biodiversidade no Cerrado: origens
históricas e o papel do comércio internacional. Série Técnica Volume VII .WWF Brasil, 104p.
COWELL, R, K. 1997. EstimateS: statistical estimation of species richness and shared species
from samples. Version 5. User’s guide and application. published at http://viceroy.eeb.uconn.edu/
estimates.
FEARNSIDE, P. 2001. Soybean cultivation as a threat to the environment in Brazil. Environmental
Conservation, 28 n.1: 23-38.
FREE, J. B. 1970. Insect pollination of crops. Academic Press, London, UK, 544 p.
GALINDO-LEAL, C. & CÂMARA, G. I. 2003 The Atlantic Forest of South America: biodiversity
status, threats and outloook. Conservation International Island Press, USA,488p.
KLINK, C. A.. & MOREIRA, A. 2002. Past and current human occupation and land-use In:OLIVEIRA,
P.S. & MARQUIS, R. J. The Cerrado of Brazil. Ecology and natural history of a neotropicalsavanna. Columbia University Press, New York, USA, p.69-88.
KLINK, C. A. & MACHADO, R.B. 2005. A conservação do Cerrado Brasileiro. Megadiversidade,
1 n.1: 147-155.

Workshop I 37

MACHADO, R.B.; RAMOS-NETO, M.B.; PEREIRA, P.; CALDAS, E.; GONÇALVES,D.; SANTOS,
N.;TABOR, K & STEININGER, M. 2004. Estimativas de perda da área do Cerrado brasileiro.
Technical Report. Conservation International Brazil, Brasília-DF, Brazil. 26pp.
MCGREGOR, S. E. 1976. Insect pollination of cultivated crop plants. Agriculture Handbook n.
496. United States Department of Agriculture, Washington, D.C. 411 pp.
MYERS, N., MITTERMEIR, R.A., MITTERMEIER, C.G., FONSECA, G.A.B., KENT, J. 2000. Biodiversity
hotspots for conservation priorities. Nature, 402: 853:858.
OLIVEIRA, P.E. & GIBBS, P. 2002. Pollination and reproductive biology in Cerrado plant communities In: Oliveira, P.S. & Marquis, R. J. The Cerrado of Brazil. Ecology and natural history of a
Neotropical savanna. Columbia University Press, New York, USA, 329:347.
PINTO, L.P. & BRITO, M.C.W. 2003. Dynamics of Biodiversity Loss in the Atlantic Forest: An
Introduction. In: Galindo-Leal, C. & Câmara, G. I. The Atlantic Forest of South America: biodiversity status, threats and outloook. Conservation International Island Press. USA. 27:59.
SOBERRON, M.L. & LORENTE, B.J. 1993. The use of species accumulation curves functions for theprediction of species richness. Conservation Biology, 7: 480-488.

Workshop I 39

Group 2
Assessment of Pollinator –Mediated Gene Flow
Participants: Claudia Maria Jacobi (coordinator), Edivani VillaronFranceschinelli, Rogério Gribel, Peter G. Kevan, Alfred Ochieng, Eda Flávia
Lotufo Rodrigues Alves Patrício, David W. Roubik.

Abstract
This group discussed the interaction between
plant and pollinator, emphasizing the importance not only of pollination, but also of good
agricultural, forest management, and conservation practices for sustainable development.
The group was comprised of researchers
whose areas of expertise encompass floral
biology, plant breeding systems, plant population genetics, and pollination of tropicalplants. The recommendations made below areintended to contribute to future discussions
regarding the Brazilian Pollinator Initiative(BPI), although some of them are generalenough to be considered more broadly.
Emphasis was given to recommendations
other than methods, since there is a vast literature available (including FAO publications) on
the above-mentioned subjects.
Pollen-mediated gene flow in plants is
affected by abiotic agents, such as wind, and anumber of biotic agents, of which the single
most important pollinator group worldwide is
the bees. Also of great importance for manynative fruit trees in the tropics are bats, beetles

and flies. The production of fruits, seeds, andof more individuals of the pollinated species
depends directly on these agents in the majority of plants, and very often in commerciallyimportant ones. Exceptions are self-fertilizing
plants, but even these frequently benefit fromcross-pollination provided by these agents.
Traditional selective breeding of plants, habitat
fragmentation and overexploitation of natural
stands are currently narrowing the genetic
base, and are leading to genetic erosion of economically important plants. In addition, genetically modified varieties resistant to herbicides
or pesticides could create potential "superweeds" through pollen-mediated gene flow.
Among the methods proposed to help
perform the recommendations, rapid assessment protocols (RAP) are suggested, for thecollection of data on bee behaviour, pollination
syndromes and landscape diagnosis. These
protocols allow data collection in the field bypeople with little or no formal biological training. Other methods, including statistical andgenetic analyses, require both expertise andspecific facilities, and will usually be performedby researchers and trained personnel.

40

Aim
To propose standard methodologies for theassessment of pollen transfer in crops and innatural areas.

Expected products
To produce a list of methodologies, such as
rapid assessment protocols, experimental
desing for testing breeding systems and monitoring methods, making use of case studies
as exemples.
To produce a list of recommendations forthe gene flow assessment and managementof plant species regarding containment measures or enhanced productivity.
This working group focused on the assessment of pollinator-mediated gene flow of economically important plant species.

Discussion
The discussions occured in two sessions; oneon monitoring of flower visitor behaviour,
morning October 29th; other on pollination
requirements and on apllied issues in pollinator gene flow, afternoon October 29th.
The goals were to discuss ways of producing a database containg comparative
behaviour of visitors in different plant species
within an area; how to produce a list ofimportant plant species and their pollinator
requerements, including their breeding system, pollination syndrome, and resource
offer; and how to increase awareness/knowledge of mechanisms for containment measure or enhanced productivity for selected
plant species.
The questions guiding those discussons
were:

How to adapt the observational methods
proposed to different plant habits and morphologies, and landscapes (ex: trees vs.
shrubs; natural vs. agricultural systems)?
• Should these methods be made widespreadand user-friendly?
• Should we encourage their use by laymen inorder to increase the number of areas andsituations?
• If so, how to standardize the use and application of the RAP with a minimum of mistakes?
• Will it be feasible to recommend pollen
containment measures based on this information?
• How to determine the need to assess geneescape (ex. in the case of unwanted
hybridization between crop varieties andwild relatives, or related contamination
problems concerning GMOs)?
• Should recommendations be made on acase-by-case basis, or could we generalize
part of them?
•

In order to orientate the discussions a listof general guideline of method were drew:• Observations of bee behaviour on theflower/inflorescence: pollinator or visitor?
(frequency and kind of stigmatic contact)• Amount and availability of pollen carried:
where in the body, how tightly packed?
• Bee flight among plants: do individuals follow nearest neighbour pollination rules(optimal foraging)? Is there along-row
behaviour? Is there flower constancy? Howto estimate carryover?
• Energy economics of foraging: measuretemperature, wind, RH.
• Creation of user-friendly protocols for bee
behaviour assessment and comparison.
• Application of simple statistics to determine
pollen shadow.
• Standard methodology to test for breeding
system (includes bagging, hand pollination

Workshop I 41

and emasculation, followed by fruit/seedset), adapted to each case.
• Creation of user-friendly protocols for breeding system assessment.
• Application of simple statistics to analyse
results.
• Estimates of gene flow through genetic
markers compared with estimates of pollentransport (see above).
• Estimates of pollen shadow with dyes.
• Comparison of crop productivity under different pollinator regimes.
• Selection and discussion of case studies (e.g.
cotton).

Results
Pollinator mediated gene flow
Pollen-mediated gene flow in plants is
affected by abiotic agents, such as wind, andbiotic agents, such as bees, butterflies andmoths, beetles, flies, bats, birds, and otherless frequent agents like rodents, marsupials,
and thrips (Proctor, et al., 1996). Many pollinator populations are probably suffering
nowadays from stress resulting from habitat
loss, parasites, insecticides, and misunderstanding by the general public. Meanwhile,the need for their services in natural, agricultural and agroforestry systems is growing
day by day. In the tropics, pollination isaffected not only by bees (natives and introduced Apis), but also by less known animals, whose service is poorly understood by
the general public. Among these, bats are
particularly important because they pollinate several species of fruit trees, while beetles and flies are responsible for high yields inpalms. With such a variety of pollinatorspecies and of plants that need animal pollination, it is important that the characteristics
that affect gene flow are well understood foreach pollinator and likewise the plants thatthey pollinate.
The pollinator requirements of a plant
species depend on its breeding system.
Standard methods to test for self-fertility andself-pollination are among the first featuresassessed when evaluating the need for pollinators. Other usual procedures allow us toevaluate if a flower visitor is an effective pollinator. When focusing on gene flow, several
techniques have been tested to assess how far
can pollen go from a focal plant of group ofplants. This latter parameter involves knowledge of the amount of pollen harvested froma flower, flight range, and resource distribution, and it is directly related to the pollinatormorphology, the flower morphology, andwhether the resource is a crop or grows wild.
Evaluating the extent of pollinator-mediatedgene flow also requires knowledge of the pollinator's fidelity to a given plant species, andof the type of resource it is being visited for.
Finally, commercial parameters that increase
crop value are usually taken into account tocompare differences in yield among different
pollination regimes.
The understanding of pollinator behaviour
with respect to each plant species is vital not
only to establish adequate agricultural actions
that increase yield, but also to adopt measuresthat lead to sustainability. Among these areactions to reduce genetic loss in forest species
due to isolation, to determine levels of isolationor contamination of crops, to prevent invasiveness of exotic plants and improve conservationof native genetic diversity, and to enhanceawareness of pollinators' services to humanity.
At present, given the enormous variety ofpollinators and commercially important tropical plant species (Roubik, 1995), only a small
percentage of plants, be they wild or cultivated, have undergone comprehensive studies,and most of the gene flow data which are42needed to support conservation and management initiatives are still lacking.
Importance of pollinator-mediated geneflow in crop management and silviculture
Pollinator services have been traditionally considered expendable in many crops. However,case studies have shown that yield is significantly improved when pollinators are introduced.
Such is the case for coffee (Roubik, 2002), andvarious crops in Brazil (cited in a recent survey by
Couto, 2002): passion fruit, red pepper, strawberry and orange. Possibly, many others, such as
sunflower and soybean, will also show
increased yield with insect-mediated pollination.
Although pollinators are not essential for fruit orseed set in many species, on account of theirself-fertility, it is clear that cross-pollination usually enhances crop performance, when evaluated by commercial parameters. For example,
cashew (Anacardium occidentale), which is partially self-fertile, requires a high rate of visitation
to obtain good nut yields, since most of the
fruits derive from cross-pollination (HolandaNeto, et al., 2002). The introduction of bee
management to increase yield in crops should
be carefully evaluated case by case, since additional costs are involved.
On the other hand, alleged low productivity of some cultivated plants may simply be theresult of incorrect agricultural practices thathave led to low genetic diversity of crop or forest stands. Poor fruit and seed production canbe the result of inbreeding, not a lack of pollinators. The common practice of plantations
based on seeds from very few trees or evenclonal orchards should be analyzed carefully
since this may lead to genetic erosion, low productivity and inbreeding depression. It is possible that premature fruit drop in cashew is also
related to genetic causes.
Current practices of natural standexploitation for timber, pharmaceuticals, rub-ber, fruit, seeds, and dyes may be reducing
genetic variability and gene flow to levels
that permanently affect the viability of populations. Some studies from Brazilian economically important species are available. Recent
data (Peres, et al., 2003) from 23 populations
throughout the Brazilian, Bolivian andPeruvian Amazon have shown that the historical levels of exploitation of Brazil nuts
(Bertholletia excelsa, Lecythidaceae) have amajor impact on recruitment into natural
populations. Populations subjected to moderate and high levels of harvest over many
decades lack juvenile trees; in contrast, only
populations with a history of light, recent or
no exploitation contain large numbers ofjuvenile trees.
At present, there are still few laboratories
in Brazil (governmental or private) that are
involved in genetic studies of native plant populations. We are hopeful that this situation will
be resolved in future years, since many laboratories are nowadays well equipped and theirpersonnel already prepared for this task.

Habitat fragmentation and reduction ofgenetic diversity
Some Brazilian biomes have undergone extensive clearing in the past decades, notably for
agricultural purposes. This has resulted in the
inclusion of the Cerrado (savanna) in the latest
list of "hotspots" (threatened world regionsthat should be given priority in biodiversity
programs). This biome is home to several commercially important plant species that are
intensively used by local populations.
A typical case of plant populations
already suffering from habitat fragmentationis that of Caryocar (Caryocaraceae) species.
The piqui (C. brasiliense) from the Central
Brazil Cerrado vegetation, and the piquiá (C.
villosum) from the Amazonian forest, yield

Workshop I 43

fruits and seeds that are an excellent source ofedible oil. Pollination studies in both species(Gribel & Hay, 1993; Martins, 2002) haveshown a moderate degree of self-compatibility,and pollination by bats and sphingid moths.
Habitat and roost disturbance may affect the
populations of these sensitive pollinators.
Genetic data for C. brasiliense from 10
microsatellite loci indicated a high level ofbiparental inbreeding, which could be attributed to the limited flight range of its pollinators and restricted seed dispersal. Habitat
fragmentation would isolate populations andtheir pollinators, aggravating the scenario offruit overexploitation (Collevatti, et al., 2001).
In the case of mahogany (Swietenia macrophylla, Meliaceae), the most valuable neotropical timber species, habitat degradation
caused by selective logging and, most importantly, by conversion of forest into soybean
plantations and cattle ranch pastures withrecurrent use of fire, have clearly reduced local
population sizes and have led many populations to local extinction (Grogan, 2001).
Recent studies using polymorphic microsatellite markers (Lemes, et al., 2003) suggest thatthe small, isolated, remnant populations may
not constitute viable units in the long term,owing to the loss of genetic variation caused
by genetic drift and inbreeding.
Brazilian legislation has contemplated thehabitat loss problem by establishing, among
other protection measures, that a percentage
of uncultivated land be maintained in private
properties (known as reserva legal) in Brazilian
biomes such as the Amazon forest and Cerrado. These areas are important both to sustain ecological services such as pollination, andto maintain gene flow and diversity of nativeplant species by behaving as corridors
between fragments. There is, however, intense
debate nowadays concerning the reduction of
those percentages. Attempts to change thelaw decreasing the proportion of thesereserves should be contested with scientificand economic arguments. In addition to habitat preservation, habitat rehabilitation programs might benefit from the introduction
and management of pollen and seed dispersers. This action is a cheap alternative that
could increase gene flow among fragments
and accelerate rehabilitation.

Pollinator-mediated genetic contamination
It is known that crops easily hybridize with wild
relatives (Ellstrand, et al., 1999). The visiting
patterns of pollinator forage can create cropto-wild and crop-to-crop pollen exchange. If
genetically modified varieties (GMO) are
involved, there is the risk that non-target
plants (wild relatives or conventional crop varieties) acquire the characteristics of resistanceto herbicides or pesticides through pollenmediated gene flow and turn into unmanageable weeds (the so-called "superweeds"). The
occurrence of agricultural weeds from GMO
crop releases has already been reported. In
Canada, the presence of unwanted herbicideresistant canola (Brassica napus, which is bee
pollinated) is becoming an agricultural nuisance (Simard, et al., 2002).
Other genetically engineered varieties(modified to resist attack by insects), such as
sunflower (Helianthus anuus, which is bee pollinated), and papaya (Carica papaya, pollinatedby bees, birds and moths) have also shown
enhanced fitness. They are less attacked by
insects (moths) and in turn produce more seeds
that are themselves more resistant to insect
attack. This suggests that non-managed populations may in turn accelerate development ofresistant insect pests. It is evident that to maintain the utility of herbicides and pesticides inagriculture (i.e., to reduce the risk of hastening
the development of superweeds), modifications

44

in agricultural practices, which include herbicide
management (such as rotation and combination with other actions), are mandatory.
Existing containment measures are mostly
designed to assure seed purity levels, and may
not be adequate for preventing or, more realistically, reducing gene escape from GMO
crops (Kareiva, et al., 1994). Physical barriers,
such as bare land or non-GMO crops aroundthe target variety, have been used to prevent
pollen contamination, but they have beeninefficient in many cases, partly because of alack of knowledge on the dynamics of pollen
flow in each case.
If reducing the risk of contamination is amain concern, then the choice of managed
pollinators of a given crop (most notably if it isa GMO) should weigh not only commercial
aspects but environmental safety as well. The
risk of gene escape to non-target species isrelated to the behaviour of the pollinator, suchas flight range and its effectiveness as pollinator, which varies according to aspects associated involving both pollinator and crop characteristics. Purity standards should be stricter incases of gene escape risk than in cases of seedpurity, more so in centers of diversity, such as
the tropics, where traditional varieties, including progenitors, may disappear.
In addition, environmental monitoring
actions focusing on gene escape should givepriority to high-risk crops. These are those withlittle domestication (that is, that are still ecologically and reproductively similar to wild relatives), that grow sympatrically with wild relatives or cross-compatible domesticated species,
which can turn into weeds themselves, andthose whose commercialization requires thatthe crop blooms or sets fruits/seeds. In Brazil,
cotton would be one of the best candidates.

Recommendations
Crop and silviculture management
1. Commonly accepted ("common wisdom") practices of crop pollination should be re-evaluated toextend the knowledge of the mechanisms of pollination, and of pollinator role and benefits. Casestudies have shown that fruit yield is improved with pollinator service in crops where pollinators had
traditionally been considered expendable.
Proposed methods:• Standard breeding system tests and exclusion experiments.
• Pollination syndrome.
• Pollinator behaviour in flower and among plants.
• Statistical comparison of productivity parameters between traditional methods and handcross-pollination experiments.

2.Traditional genetic improvement methods, such as by phenotype selection of tree crops, should be
re-evaluated.
Alleged low productivity of some plantations may be due to inbreeding depression, not a lack ofpollinators.

Workshop I 45

Proposed methods:• Molecular techniques (microsatellites, allozymes) to evaluate genetic diversity and dynamics;

inbreeding depression, levels of outcrossing, pollen flow, cross-compatibility between varietiesof cultivars and clones.
• Pollinator behaviour in flowers and among plants.
• Statistical comparison of productivity parameters between cultivars.

3.Traditional methods of exploitation of timber and NTFP (non-timber forest products) should be
re-evaluated.
Natural stand exploitation practices may be reducing genetic variability and gene flow.
Proposed methods:• Molecular techniques (microsatellites) to evaluate genetic diversity, mating systems, and gene flow.
• Observation of flight patterns of each pollinator species.

4. GMO crops with geographically close wild relatives should receive priority in environmental impact
assessment actions.
Crops such as cotton and corn may hybridize with wild relatives and these may become "superweeds".
Proposed methods:• Paternity analysis (microsatellites).
• Investigate time (phenology) or biological barriers (common pollinators).
• Observation of flight patterns of each pollinator species.

5. Containment measures should be tested and proposed in the case of any crop that has a risk ofgene escape or has to maintain its purity.
Existing containment measures are still under development and have shown to be inefficient inmany cases.
Proposed methods:• Test and adoption of physical barriers that discourage pollinator flight.
• Observation of flight patterns of each pollinator species.
• Paternity analysis (microsatellites).
• Production of gene flow curves.

Pollinator conservation
1. The percentage of legally determined uncultivated land in private properties (known as "reserva
legal") in Brazilian biomes such as the Amazon forest and Cerrado (savanna) should be maintainedand enforced by law.
These areas are important both to sustain ecological services, such as pollination, and to maintaingene flow and diversity of native plant species.

46

Proposed methods:• Molecular techniques (microsatellites, allozymes) to evaluate geneticdiversity and gene flow.
• Statistical comparison of reproductive parameters of native plants inisolated versus connected forest

fragments.
• Legal actions.

2. Exotic plants or pollinators should be priority in long-term, in-depth monitoring programs, to detect
overall impact in the ecosystem.
The invasiveness of an exotic plant may be benefited by a native pollinator, or the exotic pollinatormay outcompete native species for resources and reduce productivity and regeneration patterns of
native plants.
Proposed methods:• Observation of pollinator behaviour in flower and among plants.
• Survey of pollinators in the area.
• Monitoring of the invasive plant spread.

3. Pollen and seed dispersal by animals should be encouraged in habitat rehabilitation programs. Theiraction enhances seed set and accelerates the rehabilitation process, besides being a cheap alternative.
Proposed methods:• Introduction of meliponiculture in rehabilitation areas.
• Introduction of nesting and roosting places.

4. Native species cultivation in urban areas, instead of exotics, should be preferred and encouraged,
as well as urban ecological interactions among native plants and their pollen and seed dispersers.
Their use in public parks will preserve native plant-pollinator interactions, aid in the conservation ofgenetic diversity, and promote awareness of native species by the public.
Proposed methods:• Promote urban ecology awareness programs.
• Distribute material (specimens, seeds) and know-how among theauthorities responsible for urban

green areas.
• Introduce nesting and roosting places, and artificial trapnests for bees.

Other recommendations
1. National programs should be promoted to increase public awareness on the need for pollination
studies and conservation.
Efforts should be made to create awareness of the services to humanity performed by pollinators, tochange the perception concerning a variety of animals whose important service as pollinators is currently unknown to the public, so as to reduce the pressure on these animals caused by pesticides,
deforestation and others.

Workshop I 47

Proposed methods:• List flagship plant species and explain their need for pollinators.
• Stress the beneficial role of non-charismatic animals, such as bats.
• Invent popular, appealing names for pollinators.
• Promote courses on the use of urban green areas.
• Produce and distribute user-friendly, informative material.

2. Leading laboratories should be encouraged to participate in the mapping of genetic diversity andstructure of native plant populations of economic importance.
Currently many laboratories throughout Brazil are well equipped for the task, but few of them are
involved in studying these organisms.
Proposed methods:• Cooperative training courses.
• Government funding through public calls.
• Propose charismatic national or local species to obtain private or public funds.

3. Government agencies should produce, support and make widely available user-friendly
material (printed, electronic, training courses), so that the above recommendations are put topractice by final users.
There are currently many comprehensive studies of economically important plants and pollinators
whose results are unknown to the final user because of restricted (academic, technical) circulation. It
is important that the initiative of producing this material be officially sponsored and supervised by scientists so as to gain credibility.
Proposed methods:• Books could be transformed into PDF with the authors’ consent and be made available at official

sites linked to agriculture, such as FAO, EMBRAPA, and WebBee (Brazil).
• Production and distribution of user-friendly, informative material, such as leaflets and booklets.
• Training courses.

Final remarks
Methods
Explanations of some recommended techniques follow, with emphasis on Brazilian
study case examples. Among the methods
proposed to help perform the recommendations, several rapid assessment protocols(RAP) could be developed, grouped broadly
into two: botanical (phenology, flower density, pollination syndromes, plant breeding sys-tems) and pollinator (bee behaviour in theflower and among plants, flight range) RAPs.
There is a vast literature on the parameters to
be considered within each of these two, andon how to measure them. These protocols willallow data collection in the field by people
with little or no formal biological training.
Other methods, including statistical analyses,
require both expertise and specific facilities,
and will usually be performed by researchers
and trained personnel.

48

Genetic diversity
Isozyme electrophoresis is a technique formeasuring the rate and direction of movement of organic molecules (in this case,enzymes) in response to an electric field(Alfenas, et al., 1998; Pinto, et al., 2001). The
rate and direction of enzyme movement in a
starch or and agar gel will depend on the
enzyme’s net surface charge, size and shape.
Enzymes can then be stained, resulting in aseries of bands in the gel. Those enzymes that
migrate to the same place in a slab of agar or
starch gel and yield similar banding patterns
when stained are considered to represent
homologous enzymes (isozymes). When the
isozymes are controlled by alleles of one gene,they are called allozymes. The banding patterns of specific types of enzymes in the gel
may vary from plant to plant. Allozyme electrophoresis is most useful to analyze genetic
diversity and outcrossing rate (the proportionof the progeny generated from cross-pollination) of populations within species. As acodominant marker, allozymes may directly
identify heterozygous genotypes. Heterozygosity indices may be easily calculated for populations or samples of plants.
The visualization of electrophoretical patterns of isozymes requires simple procedures,
since isozyme bands are obtained through thereaction that identifies the enzyme. The technique of isozyme electrophoresis is simple tolearn, and it is cheaper and involves faster procedures than DNA markers.
This method has been used in a numberof studies on the genetic diversity and population structure of Brazilian species, such as thecommercially important palmheart (Euterpe
edulis, Conte, et al., 2003), rubber (Hevea
brasiliensis, Yeang & Chevallier, 1999), and"cagaita" (Eugenia dysenterica, Telles, et al.,2001). However, some native and most cultivated plants have shown either very low or no

isozyme variability. In this case, molecular techniques can provide a larger number of markers
than isozymes.
DNA markers, on the other hand, show ahigher number of alleles per locus and can be
more useful and accurate than isozymes.
Higher numbers of markers can give moreaccurate genetic diversity indices and paternity
analysis. However, most markers, such as random amplified polymorphic DNA (RADP) andamplified fragment length polymorphisms(AFLP), are dominant and cannot show heterozygous genotypes. In some cases, however,
the high sensitivity of these techniques may
limit the detection of the same markers
among genetically divergent individuals.
Molecular markers require specialized training
and more sophisticated and expensive equipment, since their protocols are more elaborated. These techniques are also more expensive
than for isozymes, but their prices are dropping (Ferreira & Grattapaglia, 1996).
Microsatellites are stretches of DNA thatconsist of tandem repeats of a simple
sequence of nucleotides. These repeats caneasily be amplified using PCR (polymerase
chain reaction). The number of repeat units
that an individual has at a given locus can beeasily determined using polyacrlyamide gelelectrophoresis. Using these gels, we can see
two genetic marks for most individuals; eachindividual inherits one length of nucleotide
repeats from its mother and one from its
father (individuals with one band received thesame band from both their mother and theirfather). Primers to the microsatellite flanking
regions can be labelled with fluorescent dyes,
allowing the amplified products to be separated in a polyacrylamide gel electrophoresis on
an automated DNA Sequencer.
In the last decade, microsatellites or simple
sequence repeats (SSR) markers have become
an attractive tool for population genetic studies

Workshop I 49

in plants due to their co-dominant inheritance,high allelic diversity and their abundance inplant genomes. The variability observed at SSR
loci allows the accurate discrimination of individuals in natural populations and the estimation of genetic parameters, such as levels of
inbreeding, heterozygosity, gene flow and mating system, which are relevant for the genetic
conservation and management of tropical trees
under intensive human pressure. Microsatellite
markers have recently been developed for anumber of tropical tree species, such as the edible piqui (Collevatti, et al., 1999) and palmheart(Gaiotto, et al., 2001), and the timber species
mahogany (Swietenia macrophylla, Lemes, etal., 2002, 2003), "anani" (Symphonia globulifera, Aldrich, et al., 1998), "andiroba" (Carapa
guianensis, Dayanandan, et al., 1999), and"angelim-vermelho" (Dinizia excelsa, Dick &Hamilton 1999).
Plant reproductive biology
and pollinator behavior
The importance of pollinator visits to a plant
species depends on its breeding system. Two
aspects are usually evaluated through experimental manipulation: self-compatibility andself-pollination. The first evaluates if a flower
receiving pollen from the same plant is capable of producing viable seeds, and to what
degree. If the species is self-incompatible,
then it will need to be visited by pollinatorsthat carry pollen from another plant in order
to effect cross-pollination. Dioecious plants
are obligate outcrossers. To test for self-compatibility, manual self-and cross-pollination
experiments are performed on flowers, andthe results (usually fruit and seed set) are thencompared to those from control (unmanipulated) flowers. The difference in fruit or seed
set also indicates if natural pollination is deficient in a population. If this is the case, further
observations should follow to see if low fruitor seed set is caused by a reduced number ofvisits or by their quality. Poor quality visits area result of visitors who do not perform pollination (thieves, for example), or who deposit
the wrong kind of pollen (self-pollen if theplant is self-incompatible, or pollen from otherspecies if the pollinator carries pollen fromother plant species). If the plant is self-compatible, then it might not need the help of pollinators to set seeds. This is usually checked bybagging buds to exclude visitors and then verifying fruit and seed set. These procedures are
standard and well explained in a number ofbooks (Dafni,1992; Kearns & Inouye, 1993;
Proctor, et al., 1996). In addition, data oncommercially important parameters may bemeasured and compared among treatments,
such as color, weight, shape, size and nutrient
contents of the fruits.
Different pollinators respond to resource
landscapes and this in turn has consequenceson the extent of pollen dispersal (Bronstein1995). Foraging flights may vary according to
the homogeneity of resources (crop vs. naturalenvironments), plant spacing (Manasse, 1992;
Morris, et al., 1994; Morris 1993), and theirflight range (Jacobi, 2000; Turchin 1998),
among others. Several statistical and mathematical methods have been used to compare
flight behaviour of pollinators, particularly
insects. They rely on field data that involve
tracking techniques, such as telemetry for vertebrates, the use of dyes and the direct observation and mapping of flight trajectories insome cases (Turchin, 1998). These flight pathanalyses are sometimes compared with geneflow curves using marked pollen or, if available,
genetically marked seeds (Kareiva, et al., 1994).
All the above procedures are the basis forpollen flow estimation, and they are usefulfor establishing actions concerning geneescape, contamination risk, and plant population isolation.

50

References
ALDRICH, P.R., HAMRICK, J.L., CHAVARRIAGA, P. & KOCHERT, G. 1998. Microsatellite analysis of
demographic genetic structure in fragmented populations of the tropical tree Symphonia globulifera. Molecular Ecology, 7: 933-944.
ALFENAS, A.C., PETERS, I., BRUNE, W. & PASSADOR, G.C. 1991. Eletroforese de proteínas e
isoenzimas de fungos e essências florestais. Universidade Federal de Viçosa, Viçosa – MG, Brazil.
BRONSTEIN, J.L. 1995. The plant-pollinator landscape. In: Hansson, L., Fahrig L. & Merriam, G.
Mosaic landscapes and ecological processes. Chapman and Hall, London, UK, p.256-288.
COLLEVATTI, R.G., BRONDANI, R.V. & GRATTAPAGLIA, D. 1999. Development and characterization of microsatellite markers for genetic analysis of a Brazilian endangered tree species Caryocar
brasiliense. Heredity, 83: 748-756.
COLLEVATTI, R.G., GRATTAPAGLIA, D. & HAY, J.D. 2001. High resolution microsatellite based
analysis of the mating system allows the detection of significant biparental inbreeding in Caryocar
brasiliense, an endangered tropical tree species. Heredity, 86: 60-67.
CONTE, R., NODARI, R.O, VENCOVSKY, R. & DOS REIS, M.S. 2003. Genetic diversity and recruitment of the tropical palm, Euterpe edulis Mart., in a natural population from the Brazilian Atlantic
Forest. Heredity, 91: 401-406.
COUTO, R.H.N. 2002. Plantas e abelhas, uma parceria em crise? Anais do V Encontro sobre
Abelhas, Ribeirão Preto - SP, Brazil, p.87-94.
DAFNI, A. 1992. Pollination ecology. A practical approach. Oxford University Press, New York,USA.
DAYANANDAN S., DOLE J., BAWA K. & KESSELI, R. 1999. Population structure delineated withmicrosatellite markers in fragmented populations of a tropical tree, Carapa guianensis (Meliaceae).
Molecular Ecology, 10: 1585-1592.
DICK, C.W. & HAMILTON, M.B. 1999. Microsatellites from the Amazonian tree Dinizia excelsa(Fabaceae). Molecular Ecology, 8: 1753-1768.
ELLSTRAND, N.C.; PRENTICE, H.C. & HANCOCK, J.F. 1999. Gene flow and introgression fromdomesticated plants into their wild relatives. Annual Review of Ecology and Systematics, 30:
539-563.
FERREIRA, M. E. & GRATTAPAGLIA, D. 1996. Introdução ao uso de marcadores moleculares
em análise genética. EMBRAPA, CENARGEN, Brasília – DF, Brazil.
GAIOTTO, F.A.; BRONDANI, R.P.V. & GRATTAPAGLIA, D. 2001. Microsatellite markers for Heart ofPalm - Euterpe edulis and E. oleracea Mart. (Arecaceae). Molecular Ecology, Notes: 86-88.
GRIBEL, R. & HAY, J. D. 1993. Pollination ecology of Caryocar brasiliense (Caryocaraceae) in Central
Brazil cerrado vegetation. Journal of Tropical Ecology, 9: 199-211.

Workshop I 51

GROGAN, J.E. 2001. Bigleaf mahogany (Swietenia macrophylla King) in southeast Pará,
Brazil: a life history study with management guidelines for sustained production fromnatural forests. Ph.D. thesis. Yale University School of Forestry & Environmental Studies, New
Haven, CT, USA.
HOLANDA-NETO, J.P., FREITAS, B.M., BUENO, D.M. & ARAUJO, Z.B. 2002. Low seed/nut productivity in cashew (Anacardium occidentale): effects of self-incompatibility and honey bee (Apis mellifera) foraging behaviour. Journal of Horticultural Science and Biotechnology, 77: 226-231.
JACOBI, C.M. 2000. Modelamento de rotas de visitação. In:, Martins, R.P., Lewinsohn T.M. &Barbeitos, M.S.. Ecologia e Comportamento de Insetos Oecologia Brasiliensis, VII: 39-58,
PPGE-UFRJ, Rio de Janeiro – RJ, Brazil.
KAREIVA, P.M., MORRIS, W.F. & JACOBI, C.M. 1994. Studying and managing the risk of cross-fertilization between transgenic crops and wild relatives. Molecular Ecology, 3: 15-21.
KEARNS C.A. & INOUYE D.W. 1993. Techniques for pollination biologists. Colorado University
Press, Niewot, Colorado, USA.
LEMES, M.R., BRONDANI, R.P.V. & GRATTAPAGLIA, D. 2002. Multiplexed systems of microsatellite
markers for genetic analysis in mahogany, Swietenia macrophylla King (Meliaceae), a threatened
Netropical timber species. Journal of Heredity, 93: 287-290.
LEMES, M.R., GRIBEL, R., PROCTOR, J. & GRATTAPAGLIA, D. 2003. Population genetic structure of
mahogany (Swietenia macrophylla King, Meliaceae) across the Brazilian Amazon, based on variation at microsatellite loci: implications for conservation. Molecular Ecology, 12: 2875-2883.
MANASSE, R. 1992. Ecological risks of transgenic plants: effects of spatial dispersion on gene flow.
Ecological Applications, 2: 431-438.
MARTINS, R. L. 2002. Polinização, Sistema de Cruzamento e Fluxo Gênico em Caryocar villosum (Aubl.) Pers. (Caryocaraceae), uma Árvore Emergente da Floresta Amazônica. Masters
thesis. INPA-UA, Brazil, 63 p.
MORRIS, W.F. 1993. Predicting the consequences of plant spacing and biased movement for pollen
dispersal by honey bees. Ecology, 74: 493-500.
MORRIS, W.; KAREIVA, P. & RAYMER, P. 1994. Do barren zones and pollen traps reduce geneescape from transgenic crops? Ecological Applications, 4: 157-165.
PERES, C.A., BAIDER, C., ZUIDEMA, P.A., WADT, L.H.O., KAINER, K.A., GOMES-SILVA, D.A. P.,
SALOMÃO, R., SIMÕES, L.L., FRANCIOSI, E.R.N., VALVERDE, F.C., GRIBEL, R., SHEPARD JR, G.,
KANASHIRO, M., CONVENTRY, P., YU, D.W., WATKINSON, A. R. & FRECKLETON, R. P. 2003.
Demographic threats to the sustainability of Brazil nut exploitation. Science, 302: 2112 – 2114.
PINTO, L. R.; VIEIRA, M. L. C.; SOUZA, A. P.; JUNIOR, C. L. S. 2001. Isoenzimas e microssatélites
em plantas. Biotecnologia, Ciência & Desenvolvimento, 20: 16-19.
PROCTOR, M.; YEO, P.; LACK, A. 1996. The natural history of pollination. Harper Collins
Publishers, London, UK.

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ROUBIK, D.W. 1995. Pollination of cultivated plants in the tropics. FAO Agricultural Services
Bulletin n.118, Rome, Italy.
ROUBIK, D.W. 2002. The value of bees to the coffee harvest. Nature, 417: 708.
SIMARD, M.J.; LEGERE, A.; PAGEAU, D.; LAJEUNESSE, J.; WARWICK, S. 2002. The frequency andpersistence of volunteer canola (Brassica napus) in Quebec cropping systems. Weed Technology,
16: 433-439.
TELLES, M.P.D., SILVA, R.S.M., CHAVES, L.J.; COELHO, A.S.G. & DINIZ, J.A.F. 2001. Divergenceamong local populations of Eugenia dysenterica in response to edaphic patterns and spatial distribution. Pesquisa Agropecuária Brasileira, 36: 1387-1394.
TURCHIN, P. 1998. Quantitative analysis of insect movement. Sinauer, Massachusetts.
YEANG, H. Y.; CHEVALLIER, H. M. 1999. Range of Hevea brasiliensis pollen dispersal estimated byesterase isoenzyme markers. Annals of Botany, 84: 681-68.

Workshop I 53

Group 3
Bee Management for Pollination Purposes

Abstract
Pollinating agents, especially insects, are clearly essential for agricultural production. The
central point of discussions here are the importance, the possibilities, and the managementof native bees, both solitary and stingless bees,
as well as honey bees, as pollinators. The participants were divided in subgroups and so theresults here presented.

A list of recommendations for study cases
during the PDF B project in Brazil.
• Manual of protocols, according to thespecies, for rearing and managing nativeand Africanized bees for greenhouse andfield pollination.
• Protocols for using native and Africanizedbees to pollinate crops defined for study cases.
• A guide for sanitary care of migratory activities (transportation of bees from one area toanother) for pollination purposes.
•

Aim
Discussions
The establishment of standard methodologies
for managing native bees (solitary and social)
as well as Africanized honey bees as pollinators of economically and locally important
agricultural crops. To assess the biodiversity of
local bees important for pollination and toevaluate their status; to define the basic procedures to be developed for rearing bees on ascale to allow their use as pollinators in agriculture; and to improve capacity building andtraining, at all levels.

Expected Product•Updated report on knowledge about
native and Africanized bees and their use
as pollinators.

The group was divided into three subgroups,
according to the number of participants.
Subgroup 1: Africanized bees rearing andmanagement to be used as pollinators.
Subgroup 2: stingless bees rearing andmanagement to be used as pollinators.
Subgroup 3: solitary and bumble bees rearing and management to be used as pollinators
The whole group discussed together atthe end of each session, for one hour. Each
subgroup was composed by, at least one person familiar with the crop, one person familiar
with pollination biology, and one person familiar with bee surveys. These discussions sections
were divided according to the following
aspects: state of art, perspective of the use ofnative and Africanized bees for pollination

54

purpose; rearing and managing bees on alarge scale for pollination purpose, colony production on a large scale and best practice inmigratory apiculture and meliponiculture forpollination; and case studies.
Some questions orientated those discussions, such as:• Which are the native bee species that pollinate Brazilian crops?
• Are there species normally being used as
crop pollinators?
• What are the main constraints for the use ofnative and Africanized bees as pollinators?
How to overcome these problems?
• How to measure the efficiency of eachmethod for multiplying colonies on a large
scale?
• Which species are included in this methodology?
• What are the solutions for the problems ofrearing bees in greenhouses?
• How to measure the result of using bees ingreenhouses?
• Do we know how to manage native andAfricanized honey bees for pollination?
• What are the main difficulties with managing native bees and Africanized bees forpollination?
• Is it possible to standardize breeding and managing methods for solitary and stingless bees?
• Is it possible to overcome parasitism problems for rearing bees in the tropics?
• Can we already provide plant growers withnative bees for pollination?
• How should people become involved inbreeding solitary and stingless bees for agricultural use?
• Is it necessary to change established cropping practices for the sustainable use ofbees as pollinators?
• What are the conservation measures necessary to maintain a stable population ofnative bees in crop areas?

What and how detailed should these protocols be?
• Is it possible to expand these protocols toother crops/bees?
• Are there other interesting plants species tobe included in the study cases?
• How to build awareness in crop growers
about the role of native and Africanizedbees as pollinators?
• How to involve government institutions withbees as pollinators?
• Is it possible to develop government policyon the use of native and Africanized bees aspollinators?
• What is necessary to make native andAfricanized bee pollination feasible in Brazil?
•

The case studies discussed are represented
on the table below.
Study Cases
Stingless
Bees

BumbleBees

Strawberry
Tomato(Melipona)

Tomato(Bombus)

Solitary
Bees

Africanized
Bees

Passionfruit

Cucurbitaceae

Cashew

Melon

CottonUmbuSpondias

AcerolaEucalyptus
Melon
CoffeeThe results will be presented here bygroups: solitary bees and bumbles bees; honeybees; and stingless bees.

Workshop I 55

A) Bumble Bees and Solitary Bees
Participants: Breno Magalhães Freitas (Coordinator), Celso Feitosa Martins, ClemensPeter Schlindwein, Dieter Wittman, Isabel Aves dos Santos, James H. Cane, Márcia deFátima Ribeiro, Maria Cristina Gaglianone.

Abstract
Solitary bees have potential for use as pollinators of various crops cultivated in Brazil, but
no solitary bees are yet commercially available
to growers, and rearing techniques are only
available for a few species, such as Xylocopa
spp. Ground-nesting bees of the genera
Exomalopsis, Epicharis and Centris are goodpollinators of various crops, such as tomato(Lycopersicum esculentum) and acerola or west
Indian cherry (Malpighia emarginata), but they
are difficult to manage. In most cases, there is
no practical way to colonize areas with newnests, and merely providing suitable nesting
substrates (e.g. sand) rarely yields productive
nesting for many years. For ground-nesting
bees that are effective and abundant pollinators of a crop (or desired tree species) or its
close relatives, the farmer must manage thecrop (care with spraying, for instance) and thesurrounding land (size of monoculture acreage,
proximity to fallow nesting sites), as these bees’
nests cannot be moved, and artificial or "created" nesting sites are unlikely to be reliably andquickly colonized. Promising taxa of cavitynesting species of solitary bees are Xylocopa,
Centris, Megachile, Anthidiini and Tetrapedia,
but there is lack of knowledge on these
species' natural histories, floral hosts, parasites,
diseases, etc. Cost-effective technologicalimprovements are needed to reliably provide
large numbers of manageable bees for commercial pollination. However, methods/tech-niques will need to be tailored to each bee
species. The use of solitary bees as pollinators
could be initiated with small growers, whoprobably will own their own bees. They should
be stimulated to show the results that growers
can have when they use pollinators (in numbers, value, amount of profit). Other growers
will be very rapidly convinced once they see theprofits of their neighbors. As it is not common
in Brazil to value pollination services of bees ingeneral, especially solitary bees, it is important
to disseminate pertinent information (about
simple concepts, such as pollination, pollinators, their services, etc.), distributed by extension programs (for example in small plantingsof Passiflora, since techniques to rear and use
Xylocopa as pollinators are already available inthe country). In the case of Bombus species, it isnecessary to investigate the economic value ofgreenhouse crops in Brazil to assess the need or
not of using Bombus as pollinators. If necessary,native species such as B. atratus and B. brevivillus (not so aggressive when in small colonies)
and meliponinine bees, such as Melipona
quadrifasciata (at least for tomatoes), should beconsidered. There should be national regulations forbidding the importation of exotic
Bombus species and a monitoring program ofinvasive B. terrestris from Uruguay, where it was
first introduced in 1995 and is now free-living in
nature. Finally, research on Bombus and solitary
bee natural histories, floral hosts, parasites, diseases, foraging behaviour, rearing techniques,
management and pollination effectiveness in56various crop species are necessary in order forthese bees to be used as large-scale reliable pollinators in Brazilian agriculture.

be using flowering species of agriculturalinterest (e.g. aggregations of Peponapis).

Recommendations
Solitary bee species
Considering nesting habits, solitary bees canbe split into two distinct groups:
1. grounding nesting bees;
2. cavity nesting bees.
Currently promising taxa to be worked on are:
• Exomalopsis (there are reports of tomato
pollination);• Epicharis (There are reports of West Indiancherry or acerola pollination);• Centris (There are reports of West Indiancherry or acerola pollination).
Grounding nesting bees are difficult tomanage; in most cases there is no practical way
to colonize areas with new nests, and merely
providing suitable nesting substrates (e.g. sand)rarely yields productive nesting for many years.
There is little knowledge about groundnesting bees as pollinators and about their
management for this purpose. Three main
approaches are suggested to help identify
potential pollinating bee species:
1.selection of areas with less intensive agriculture for visitation to crop species (e.g. home
plantings of Cucurbita) where insecticide use
is unlikely, so that bee populations canincrease without extermination by pesticides;
2.search for promising species of non-social
pollinators (or social Halictidae) on wild
crops and their wild relatives (co generics).
ex. Rhambutan, which is visited and pollinated by Euglossa;
3.investigate pollen use by any large aggregations where solitary bee species are found anddiscovered (e.g. Oxaea) to judge if they might

In order to promote ground-nesting bees thatare effective and abundant pollinators of acrop (or desired tree species) or of a close relative to this crop species, the farmer must manage the crop (care with spraying, for instance)
and the surrounding land (size of monoculture
acreage, proximity to fallow nesting sites), as
these bees' nests cannot be moved, and artificial or "created" nesting sites are unlikely tobe reliably and quickly colonized.
There is considerably more information
on and well-succeeded examples of the useof cavity nesting species of solitary bees.
Species such as Osmia lignaria pronpiqua and
Megachile rotundata are widely used andmanaged for apple (Malus domestica) andalfalfa (Medicago sativa) pollination, respectively, and their commerce amounts to millionsof American dollars per year.
Other promising taxa, such as Xylocopa,
Centris, Megachile, Anthidiini, Tetrapedia,
already nest in artificial nesting-sites and canpotentially be managed to attain large populations for use in pollination. Among these taxa,
Xylocopa can be considered special in Brazil
because there is a demand for these bees andthere is some knowledge on its biology and rearing techniques for use especially in Passiflora
plantings. Serious constrains have been identified and must be overcome in order to achieve
large scale production and economic viability for
exploiting these bees as crop pollinators:• ants are serious predators of bee nests andmust be controlled;• there is a need to eliminate parasites anddiseases (clean management) before establishing populations for increase;

Workshop I 57

there is a need for improved pest management so that insecticide sprays are notapplied during blooming periods;• there is a lack of knowledge of techniquesand species' potential to produce bees inlarge numbers;• there is a lack of knowledge of what crops
benefit most from pollination by solitary bees;• agricultural lands lack margins/fallow/
hedgerow areas for grounding nesting bees;• we need good methods for field assessmentof pollination value;• affordable nesting materials/trap nests
need to be developed and made available,
based on knowledge of which bees aregoing to be used;••

there is a lack of taxonomic pollen analysis or
floral visitation analysis to establish floral use.

Other main recommendations are to compile Brazilian studies of past trap-nesting experience in Brazil and produce a starting point for
those species that are present in the country
and can be reared in trap-nests. It is also important to develop an insecticide management
program, in which pest control practices should
minimize bee mortality (label requirements on
insecticides, for instance, should emphasize
scouting and economic thresholds). This program could be developed by the honey bee
management group due to their greater experience in using bees for pollination purposes.

Some cultivated plants that probably benefit from pollination by solitary bees.
Botanic Family

Scientific name

Apocynaceae

Hancornia speciosa

Anacardiaceae

Anacardium occidentale

Common names English

Common names Portuguese
Mangabacashew

Caju

Spondias tuberosa

Umbu

Spondias spp

Caja, Cajarana, Umbu-caja

Bixaceae

Bixa orellana

Urucum, Coloral, Açafrão

Cucurbitaceae

Cucurbita pepo

pumpkinMoranga

Cucurbita moschatasquashAbóboraCucumis melo

melon

Melão

Cucumis sativus

cucumberPepinoGlycine max

soybean

Soja

Vicia faba

field bean

Phaseolus vulgaris

kidney beanFeijãoLens esculenta

lentils

Lentilha

Pisum sativum

pea

ErvilhaVigna sinensis

cowpeaFeijão de corda

Bertholletia excelsa

Brazil nut

Castanha do ParáFabaceae

Lecythidaceae

58

Malpighiaceae

Malvaceae

Passifloraceae

Solanaceae

Malpighia emarginata

West Indian cherry

AcerolaByrsonima crassifolia

wild cherry /nance

Murici

Gossypium hirsutum

cottonAlgodão

Passiflora edulis

passionfruit

Maracujá

Passiflora quadrangularis

giant granadilla

Maracujá-açu

Hibiscus esculentus

Passiflora mucronata

Maracujá

Passiflora alata

Maracujá-doce

Lycopersicum esculentum

tomatoTomateSolanum melongena

egg-plant

Beringela

Capsicum annuum

sweet pepper

Pimentão

Capsicum spp.

Pepperonypeperoni

Study Cases - Recommendations for some individual crops
Passion Fruit (Passiflora edulis)
Bees:

Xylocopa frontalis, X. grisescens, X.augusti, X. ordinaria, X. suspecta,
and other large Xylocopa spp..

Nests:

dead tree trunks, trap nests, Xylocopa nests.

Bee density:

25 females/ha in the case of X. frontalis.

Crop management:

need of complementary floral resources: buzz pollinated species(Melastomataceae, Cassia, Sena, Solanum, etc).

Cashew (Anacardium occidentale)
Bees:

Centris species. Centris tarsata tested, but other species can also be important.
Take into account bee behavior, pollen distribution on the bee body;pollen viability is important: it is only viable for 4 hours.

Nests:

trap nests.

Bee density:

unknown.

Crop management:

There is a need to supply pollen and oil producing plants (Byrsonima crassifolia
for wild cashew), possibly through mixed culture with West Indian cherry(acerola) in commercial plantations.

Cotton (Gossypium spp.)
Bees:

Emphorini spp.; Augochlorini; Bombus; Xylocopa.

Nests:

depends on species used.

Bee density:

very large crops will need hundreds of bees (to be estimated).

Crop management:

depending on variety, there is a possibility of gain in the fruit production period.

Workshop I 59

Cucurbitaceae
Bees:several taxa of ground-nesters (Peponapis, Augochlorines).

Nests:

natural, in the ground (see discussion above).

Bee densitiy:unknown.

Crop management:

local conservation should be promoted through education of growers. Free
pollinators when available, but impossible to re-colonize once exterminated.

West Indian cherry (Malpighia emarginata)
Bees:

Centris (both ground and cavity nesters), Epicharis (ground-nester).

Nests:

both natural, in the ground, and trap-nests, depending on the species.

Bee density:

unknown.

Crop management:

Not visited by bees that do not use oil (ex. honey bee). Will need to understandbee behaviour, pollen distribution on the bee body, optimize trap nesting
techniques; could be beneficial to grow near cashew plantings.

Vegetable or oil seed crops
Production of high-value specialty seed, such as onion and carrot, or hybrid seed crops (sunflower) on
small acreages.

Regional or specialty fruits
Some solitary bee species can be important pollinators of regional or specialty fruits like mangaba(Apocynaceae: Hancornia speciosa) and umbu (Anacardiaceae: Spondias tuberosa).

Recommendations
Bee biologists should participate in crop symposia sponsored by the International Societyfor Horticulture Science (ISHS), in order toexchange expertise with the world's mostknowledgeable producers, breeders andprocessors of specific crops.
Protocol with generalrecommendations to use solitary
bees as crops pollinators
1.Complementary floral resources should be
provided.
2.Plants for nidification (trunks) initially, later provide nesting substrates (although these also
may be made from natural materials, such as

stick nests, rather than drilled nesting blocks).
3.Conservation of natural areas (in order tomaintain natural populations); need not beproximate to crop of interest (sustainability
extractive reserves for initiation of trap-nesting programs).
4.Spray management - toxic sprays must be
avoided during bloom.
5.Different Xylocopa nest substrate structures
should be compared (Freitas & Oliveira Filho
vs. Camillo models).
6.Cultivation of other crops simultaneously for
year-round forage (no extensive monocultures at a scale greater than flight range).
7.Adequacy of local/regional conditions.
8.Management of ruderal plants where necessary.

60

Cost-effective technological improvements needed to reliably provide large numbersof manageable bees for commercial pollination
1) Paper nesting straw inserts
Reason:need these in large numbers for selection of precise sizes for both a
trap-nesting program and for handling large numbers of managed species(ex. for Centris, anthidiines).

Advantages: easy re-use of drilled nesting blocks, better control of disease and parasites (esp. mites)from generation to generation, opportunity to X-ray nest contents to eliminate
diseased or parasitized cells prior to establishing new populations. Plastic straws
unsuitable, as many bees do not like the slick surface, plus lack of air permeability
leads to serious mold problems.
Options:purchase paper straws from manufacturers in North America (list of suppliers at:www.loganbeelab.usu.edu or Europe). Should consider technique of thin-walled paper
straw inserted in hole in nesting block. The benefits are analogous to the moveableframe hive for honey bees.

2) Use of X-ray units
Reason:needed for evaluating nest contents, progress of development and metamorphosis, location of diseased or parasitized cells (for surgical removal from nest) and other applications.

Advantages: quick and reliable.
Options:

could be a central unit at one laboratory to which samples can be sent by researchers
from all over Brazil. Consider purchase of a used unit from a hospital, possibly fromoverseas if not available within country. Applications detailed in published studies with
Osmia lignaria and Megachile rotundata. Alternatively, can use stick nests of soft, easily
split wood or possibly reeds (Japanese Osmia system). Choice will be guided bypracticality, cost, use by bees, and local availability.

3) Mass-production for drilled nesting blocks
For Brazil's economy and labor market, what is the most cost-effective method for mass production of
acceptable nesting materials for cavity-nesting bees? Are manufacturers of hive equipment interested
in producing interchangeable, easily assembled components of Xylocopa nest boxes? Are there manufacturers interested in producing drilled wooden nesting blocks in large numbers, or clever methods
for using paper straws inserted within cardboard tubes within boxes (holes must be straight andapprox. 15 cm deep for larger species, although research with individual species will demonstrate thehole diameters and depths that yield the greatest number of daughters per nest)?
The mass production for drilled nesting blicks can begin by mimicking techniques already in use with
Megachile and Osmia in the US, Japan and Europe. Aspects of those programs will clearly need adaptation to Brazil's tropical environments (for instance, how to handle multivoltine species, irrelevance ofrefrigerated overwintering), although some aspects may be more applicable in the south, such as forapple pollination in Santa Catarina.

4) Control of enemies
Simple techniques needed for excluding ants from nesting blocks, especially blocks managed for croppollination (would be nice for trap-nesting too, but perhaps not practical).
Options: Physical barrier over which ants cannot walk. Must persist and not catch bees.

Workshop I 61

Final considerations
regarding solitary bees

Final considerations
regarding Bombus

1. Measuring effectiveness of methods
for population increasea. The only practical species to manage arethose whose populations can be increased(more daughters than mothers).
b. Methods that produce populations withlimited parasites and disease.
c. Affordable nesting materials that are practical to make and endure for Xylocopa and
Megachile; there is a possibility of adaptationof existing methods.

1. No importation of non-native species
There should be regulation on importation ofbees:• brazilian laws must be made controlling
Bombus importation;• seek an agreement among South Americancountries or in the Mercosul related to bumblebees importation;• establish a monitoring program of invasive
Bombus terrestris from Uruguay. This
species was introduced into Uruguay in1995 and now is free-living in nature, colonizing new areas and spreading towards
the Brazilian border.

2. Greenhouse pollination
The main difficulty in using solitary bees aspollinators in greenhouses is that glass andplastic absorb UV, which interferes with bee
orientation during flight. How to measure
their pollination efficiency in greenhouses is
not relevant; at this stage it is known which
species can be used.
3. Stimulating people to get
involved in rearing and selling
solitary bees.
Stimulate small growers who probably will
own their own bees; to show the results thegrowers can have when they use the pollinators (in numbers, value, amount of profit).
We only have to convince about 1% ofthem; the rest will be very rapidly convinced
once they see the profits of the neighbours.
As it is not common in Brazil to value pollination services, and bees in general, especially solitary bees, it is important to disseminate information (about simple concepts
such as pollination, pollinators, their services,etc.), distributed by extension programs (forexample in small scale plantings ofPassiflora).

2. Need for importation of non-native
Bombus species
There is no need for importation, because:• these bee species are used only for pollination of greenhouse crops;• they are used mainly for tomato pollination,
but recent studies have shown that native
stingless bees Melipona quadrifasciata andNannotrigona pirilampoides are good tomato pollinator in greenhouses;• exotic Bombus species may bring parasites
and diseases to native species.
3. Using native Bombus species for croppollination
We do not currently have knowledge to handle native Bombus. If it is going to be used,
research is needed on biology and rearing
methods. Two species are promising:• B. atratus - not so aggressive when in smallcolonies;• B. brevivillus - in Northeast Brazil, notaggressive; has potential as a pollinator ofcrops of glasshouses and in open areas.

62

Final Remarks
Bombus are used commercially only to pollinate greenhouse crops. This agricultural segment is still small in the country, compared tothe size of the Brazilian agricultural system,and does not justify the risk and unknown
consequences of importing or allowing theentry of exotic Bombus species. Also, mostgreenhouse cultivation is done with tomatoes

and the stingless bee Melipona quadrifasciata has been shown to be a good alternative
to pollinate this crop in enclosures, and there
are promising native Bombus species that
could also be studied for this purpose. Finally,
Brazil should create laws prohibiting andpunishing Bombus importation, follow the
spread of B. terrestris in Uruguay, and authorities should monitor its arrival in the southernpart of the country.

References
FREITAS, B.M. 1997. Changes with time in the germinability of cashew (Anacardium occidentale)pollen grains found on different body areas of its pollinator bees. Brazilian Journal of Biology,
57 n.2: 289 - 294.
FREITAS, B.M., PAXTON, R.J. 1998. A comparison of two pollinators: the introduced honey bee(Apis mellifera) and a indigenous bee (Centris tarsata) on cashew (Anacardium occidentale) in its
native range of NE Brazil. Journal of Applied Ecology, 35 n.1: 109 - 121.
FREITAS, B.M., OLIVEIRA-FILHO, J.H. 2001. Criação Racional de Abelhas Mamangavas: parapolinização em áreas agrícolas. Banco do Nordeste, Fortaleza – CE, Brazil.
FREITAS, B.M., PAXTON, R.J., HOLANDA NETO, J.P. 2002. Identifying pollinators among an arrayof flower visitors, and the case of inadequate cashew pollination in NE Brazil In: KEVAN, P.; IMPERATRIZ-FONSECA, V. Pollinating bees: the conservation link between agriculture and nature.
Ministry of Environment, Brasília – DF, Brazil, p. 229-244.
FREITAS, B.M., ALVES, J.E., BRANDÃO, G.F., ARAÚJO, Z.B. 1999. Pollination requirements of West
Indian cherry (Malpighia emarginata) and its putative pollinators, Centris bees in NE Brazil. Journalof Agriculture Science, 133: 303 - 311.
HOLANDA NETO, J.P., FREITAS, B.M., BUENO, D.M., ARAÚJO, Z.B. 2002. Low seed/nut productivity in cashew (Anacardium occidentale): effects of self-incompatibility and honey bee (Apis mellifera) behaviour. Journal of Horticultural Science & Biotechnology, 77 n.2: 226 - 231.

Workshop I 63

B) Honey Bee
Participants: David De Jong, Lionel Segui Gonçalves, Farooq Ahmad, Kátia Peres
Gramacho, Ricardo Costa Rodrigues de Camargo, Uma Partap, Valdemar Belchior Filho.

Abstract
Pollinating agents, especially insects, are clearly essential for agricultural production. Honeybees have become increasingly important, as
field sizes have increased and native bees havedecreased, due to intensive land use and pesticides. An important advantage of honey beesis that they can be quickly taken to andremoved from the fields in large numbers,
facilitating the integration of these pollinators
into pest management programs. A single
truckload can carry 20 million potential pollinators. Honey bees contribute to more than
80% of the agricultural produce pollinated by
insects. Unfortunately, Brazil does not have astrong tradition of using bees for pollination,different from the USA, where more than 2
million colonies are rented annually. Beekeeping in Brazil has grown considerably during the last few years, especially due to honeymarket conditions. Brazil now has about 2,5million colonies available for bee products production (honey, wax, propolis, pollen, royaljelly and bee venom) and for pollination purposes. There are beekeepers specialized in pollination, especially for apples, melons andcashews. All of these products are both consumed in country and exported. To obtain
export quality fruit, insect pollination isabsolutely necessary.
Unfortunately, many of the crops that
could benefit from pollination, are either notpollinated at all, or are incidentally and haphaz-ardly pollinated by wild honey bee colonies orby apiaries that happen to be nearby, resulting
in production losses due to inefficient pollination. Africanized honey bees are seen much
more as honey producers than as pollinators.
For many crops that do not traditionallyuse honey bees for pollination, such asoranges, peaches, strawberries, sunflowers
and forage soybeans, we have data indicating
significant increases in fruit and seed production and improved fruit quality with pollination
by Africanized honey bees in Brazil (NogueiraCouto, et al., 1998, Couto 2002). Africanizedhoney bees are very active pollen collectors,
making them good pollinators, and they havebeen found to remain on the target crop
longer than do the European honey bees thatare traditionally used for pollination in othercountries (Basualdo, et al,. 2000). Africanizedbees also are more active on the flowers, fly
faster and are quicker to recruit other hive
mates, than are European bees, making themmore active and efficient pollinators. Africanized bees forage at lower light levels than do
European bees, so that they work longer days.
They also do not reduce brood production
during winter, so the colonies remain strong,with abundant foragers for pollination activities. It is relatively easy to establish newcolonies by collecting swarms with bait hives,
and Africanized colonies grow quickly, so thatbeekeepers can easily produce the large numbers of colonies needed for pollination ofcrops. There are well-established migratory

64

beekeeping techniques, and truckloads ofbees can be quickly and timely moved to flowering crops (De Jong, 1996).

Discussion
Africanized honey bees have been used for pollination in greenhouses in Brazil. However many
bees are lost from the colonies and it is difficult
to maintain the colonies alive under greenhouseconditions. Some researchers and beekeepers
have been able to overcome these problems,
but the techniques that they use are not published, nor is there an established system thatworks uniformly under all circumstances. Most
attempts to use honey bees in greenhouses are
initially unsuccessful, however after numerous
trials some researchers have been able to maintain colonies for long periods, efficiently pollinating the crop. In order to make efficient useof this resource, it will be necessary to makecontrolled studies, and develop standard, practical techniques that should be made widely
available to beekeepers and growers.
We can measure the result of using honeybees in greenhouses by examining the cropquantitatively and qualitatively. Normally, thisis done by measuring the weight, size andnumber of fruits, by determining the time tillproduction of the fruits (which may be anticipated by adequate pollination), and by calculating the percentage fruits that are consideredof high quality. Another important quantitative
aspect is the cost and benefit of the pollination
activities. Using honey bees has a cost, and thisshould be compared with the gain in crop production attained with pollination. Photos offruit that are produced by plants exposed tobees, versus those that are produced without
bees, are often quite useful for illustrating thevalue of bee pollination. Appearance is important, as the color and shape of the fruit isoften affected by pollination. Photos of crosssections of the fruit can show the number anddistribution of the seeds, which are clear indicators of pollination efficiency. The fruit quality can also be evaluated by measuring sugar
and protein and other substances, and by evaluating organoleptic (taste) factors.
We already know how to manage
Africanized honey bees as polinator for somecrops, such as apples and melons, however
this is not always done in the most efficientway. Many crops that would clearly benefit
from the introduction of bee colonies are notroutinely pollinated. Generally speaking, pollination is little valued or understood by farmers, nor are beekeepers aware of the true
value of the services that their bees provide.
We have data indicating significant increases
in fruit, seed and vegetable production due topollination by Africanized honey bees, however little of this information is available to thegrowers. Often objective studies on commercial varieties are lacking. This is true both forfield crops and for greenhouse crops. The latter are unviable commercially unless adequate
pollination is provided. Many crops are in fact
pollinated incidentally by honey bees fromnearby apiaries, or by wild honey bee colonies,
however the grower is not aware of theimportance of these services. Frequently hehas low production, without realizing that thereason is a lack of pollinators.
The main difficulties with managing
Africanized bees for pollination can be listed as:
1.there are no established techniques forusing Africanized bees under Brazilian conditions on most crops;
2.often the hives are not made with standard
measures, or with inferior materials, making
transport and management difficult;3.the bees are quite defensive and growers areoften reluctant to place them in or near thecrops that need pollinating;Workshop I 65

4.there is not sufficient care in the transportation of colonies, so that accidents are common and this discourages their use for pollination;
5.beekeepers are not aware of disease problems, and often incorrectly try to treat theircolonies, and some have introduced contaminated bee products and equipmentfrom abroad, threatening beekeeping throughout the country;
6.there is a lack of central laboratories that can
provide timely and accurate diagnoses ofbee diseases, and also there are no field personnel to advise beekeepers about this kindof problem;
7.growers are frequently unaware of theimportance of bees and pollination, and infact they often prohibit the introduction ofbees into their properties; they use insecticides indiscriminately and incorrectly without any concern for the effects on the bees
and the beekeepers;
8.there is no tradition for making pollination
contracts that include a provision for compensation for the beekeeper in the case oflosses due to pesticides or the stealing of
hives on the grower's property. There should
also be a provision for responsibilities in thecase of an accident with the bees.

Problems to be overcome
Changes in agriculture have created anincreased need for honey bees.
There is pressure to convert natural areas into
agricultural land, without concern about maintaining habitat for pollinators. Loss of naturalpollinators due to the loss of habitat increases
the need for honey bees. More intensive farming and larger fields of crops overcomes thecapacity of local native bees to pollinate. We
need to develop techniques and policies thatwill increase the availability of honey bees tosatisfy these increasing needs for pollination.
Landowners need to be made aware of thevalue of having bees placed near the crops.
The extension service (Agriculture House Casa de Agricultura) does not provide appropriate information about pollination. Unfortunately, even in the case of crops for which wehave clear evidence that honey bees significantly increase production, growers frequently
do not include pollination in their management
programs, and often even prohibit the introduction of bee colonies onto their property, or
they may charge the beekeepers, while in othercountries the beekeepers are paid for theirservices. This lack of tradition to include bees
greatly diminishes the potential gain of thegrowers. We need to have more good quality
data and then convince the growers by using
demonstration plots.
Bee diseases
Some new diseases from other countries
threaten beekeeping and hence can affect theavailability and quality of honey bee colonies
for pollination. Unfortunately, these incidentsof new diseases have not been sufficiently
controlled and studied by competent researchers and authorities. Beekeepers are also
unaware of the need for good practices thatwill avoid the introduction of these new diseases. For instance, honey and pollen that has
been imported (both legally and informally) is
often exposed to the bees. Honey is handled inprocessing plants, and often some of it isinadequate for commerce; beekeepers feedsuch discarded honey to their bees (Message& De Jong, 1998). This has resulted in the
introduction of American Foulbrood Disease(Paenibacillus larvae) spores from imported
honey into honey bee colonies. This situationneeds to be more closely investigated, and thebeekeepers should be made aware of the dan-66

ger of such practices (De Jong, 1996). A similar problem has occurred with a fungus disease, Chalkbrood, caused by Ascosphaera
apis, which entered Brazil in imported pollen.
The beekeeper normally separates the pollenpellets in the bags of imported pollen and thepowdered pollen that is left is fed to the bees.
Chalkbrood has now become established inseveral parts of Brazil as a result of these practices; we need to have more information
about the impact of this exotic disease on
Africanized honey bees.
There are no central laboratories to identify diseases.
Beekeepers need to have a place to send samples in order to learn what diseases they have,and to determine whether their problems arereally caused by parasites or disease organisms. This service exists in nearly all major beekeeping countries and now should be implemented in Brazil.
Beekeepers do not know diseases
Diseases are normally not a big problem inBrazil, but beekeepers sometimes incorrectly
try to treat colonies with antibiotics and acaricides whenever they suspect a disease. Theirlack of knowledge and the lack of government infrastructure to help them cope withdisease problems often makes them takeinappropriate actions. Besides the unnecessary costs and damage to the bees due tosuch home-brew treatments, there is a danger of contaminating the bee products. We
need to study the actual disease problems
and determine nutritional needs. A lack of
information about nutrition, especially protein needs, actually causes many problems
that are mistaken for disease. Techniques
have been developed to more objectively
evaluate honey bee diets (Cremonez, et al.,1998), but these new methods need to be

used systematically in order to develop economically viable pollen substitutes.
There is no sanitary control of the movement of colonies.
Though Chalkbrood, a fungus disease, hasrecently been diagnosed in Brazil, andAmerican Foulbrood is suspected, there is no
sanitary control of the movement of colonies.
Consequently these new bee diseases could
be spread to new regions, causing damage to
apiculture, which could affect the availabilityof bees for pollination. It is recommended
intensive studies of those new diseases, todetermine their occurrence and their impact
on the colonies. Government agencies should
be prepared to diagnose diseases in the laboratory and to train bee colony inspectors who
can make field diagnoses and develop andimplement appropriate control policies.
Problems with quality andstandardization of thebeekeeping equipment
In some parts of the country, non-standard
hives are used. Many times, among those who
use standard Langstroth equipment, there areproblems with non-standard measurements.
Beekeepers are often not aware of the correct
standards and they make their hives based on
equipment that they have purchased. As thepurchased hives are frequently not exactly
built, badly dimensioned hives are perpetuated. Many times new beekeepers have purchased bad equipment with funds that they
have received on credit. These can be badly
built hives, with uncured "green" wood, ormade with wood that is inappropriate for apiculture. Such hives start to bend and open
within a few months. Unfortunately, the funding agencies that set up programs to foment
apiculture often provoke these kinds of purchases of substandard materials due to cost-

Workshop I 67

competitive purchasing policies. Later, the beekeepers have a difficult time repaying the costof the equipment, as it is commonly discarded
within a short time.
The handling and transport of beehives in
Brazil is not mechanized
Now all hives and honey supers are transported from trucks to the apiary, and back, byhand. Hives are heavy, especially when they
are full of honey. This hand carrying oftencauses back problems for small-scale beekeepers, which depend on family labor. Beekeepers
with larger numbers of colonies must hire
help, and this makes their management
expensive. A beekeeper in the USA or Canada
can handle more than a thousand colonies byhimself, or with only a single helper. A similar
number of colonies in Brazil would need atleast five or six laborers, and the moving
process takes much longer than in other countries. Transporting colonies for pollination
requires specialized labor, at specific times. If
beekeeping had mechanized alternatives thenthis transport would be cheaper and more efficient. However, the fork lifter tractors (bobcats) currently used in other countries are too
expensive for Brazilian conditions. It would be
more cost efficient to pursue intermediate, lesscostly, alternatives for mechanization. We
need to identify appropriate techniques forhive lifting and transportation, and test andadapt them to local conditions.
There are problems with transporting bee
colonies
Beekeepers are not aware of their responsibilities and correct procedures when they havean accident during transportation of hives
from one region to another. They are unawareof the best ways to transport bees, and therefore accidents are more common than theyshould be. Frequently they lose bees thatescape from the hives, and many colonies die
due to overheating. The local authorities areunaware of the importance of the need fortimely movement of colonies, and may interfere with transport.
Problems with a deteriorationof natural areas
The lack of natural areas means that bees haveno wild flowers for supporting and maintainingcolony growth. This means that the colonies
are weak or can even die and therefore are notavailable for pollination services. In various
parts of the country there is so little natural forage that beekeeping is uneconomical, especially in regions where there is intensive agriculture
and therefore with a great need for bees forpollination. We need to find ways to promote
the maintenance of natural areas on farms(possibly through tax incentives) and to havestates and municipalities plant trees that provide forage (nectar and pollen) for pollinators.
There is lack of natural forage for the bees
The lack of natural forage during various timesof the year can be partially overcome by artificial feeding of sugar and protein diets.
However, sugar is often too expensive, so it
would be useful to have a means to provide
sugar or sugar syrups at a low price for the
beekeepers to properly prepare their colonies
for pollination. The most important nutritional
problem is a lack of appropriate protein whenpollen from flowers is not available. At the
moment, no adequate artificial diet is available. Such diets need to be developed andtested. A relatively simple laboratory techniquedeveloped in Brazil is available for the initial
screening of food by-products that could be
used as protein sources for bees. Large scaletesting should be done, with field testing anddemonstration of the most promising alternatives (Cremonez, et al., 1998).

68

There are misconceptions about how
bees could impact on crops
In some crops, such as oranges, there are
misconceptions about the danger of beestransmitting plant diseases. Generally, decisions are made without any real evidence ofsuch a problem.
There are problems with beekeepers
obtaining permission to place bees on farmland - due to fear of the bees interfering with
cultural practices, while growers are unawareof the value of pollination. We need to havecase studies about how bees interact withcrops and to have documented informationthat will help growers and beekeepers understand the real effects of bees on crops. Someof this information is available from othercountries, and can be adapted and appropriately communicated. However local experimental work should also be done to test the
impact of bees under local conditions.
Beekeepers have problems withhives being stolen
Apiaries often have to be placed in remoteplaces where the colonies are easily stolen, due
to inappropriate management and fear of thebees. The government and the police normallygives little support to the colony owners, andoften take no action, even when there is proof
that colonies or colony products have beenstolen. Policies should be developed to provide
legal and police support to reduce this colony
thievery problem. Case studies need to bemade to find ways to maintain apiaries in waysthat there is less impact on farm workers andanimals, so that apiaries can be kept in more
protected areas. Insuring colonies against robbery is also unknown, making financial security
for the beekeeper nearly impossible.
Problems with pesticides
Presently many honey bee colonies are killedby pesticides. Beekeepers avoid crops where
insecticides are used; this reduces honey production and agricultural production. Crops
such as cotton would be more productive if
the bees could pollinate them. Native bees andwild honey bee colonies are killed by excessive
and inappropriate use of pesticides, making it
necessary to bring in commercial honey beecolonies for pollination purposes. Labeling ofthese pesticides should include information
about toxicity to bees.
Case studies to assess main pesticide problems that affect bees
Develop a manual about the use, value andcare of honey bees. Take advantage of casestudies about improvement of production andquality of farm products to educate farmers
about how to best incorporate pollination into
their management practices. The impact ofthe most commonly used pesticides on flowering crops should be investigated.
Farmers and policy makers are often
unaware of the need for pollination
Growers are often unaware of need for pollinators and of pollinizer varieties. International
pollination techniques need to be adapted to
local conditions. The agricultural policies normally ignore the need for pollinators. EMBRAPA, SEBRAE and other appropriate institutions,such as universities, should develop projects totest the value of pollination on crops and varieties. They should also develop crop management schemes that minimize the impact ofinsecticides on honey bees. This information
should then be made available to the farmers.
There should be demonstration fields andcourses to make the farmers aware of how
much they can gain by including pollination in
their management scheme.
We need clear recommendations about
number and size of colonies needed, and how

Workshop I 69

to place them. Agricultural extension does not
currently train farmers about ways to manage
their crops for maximum pollination.
Extension services need to develop courses
and educational material. They should develop case studies in cooperation with local
growers (on-farm experiments).
Consumers are not aware of how to
select good quality (well pollinated)fruits and vegetables
Demonstration materials should be developed
to help the consumer recognize and choose
good quality products. Fruits and vegetables,such as melons, watermelons, apples andcucumbers, often have fewer than normal
seeds, which results in inferior products with abad taste. Such an awareness and educational
programs will create a more sophisticated consumer and will encourage growers to use bees
to produce high quality fruit.
Other problems:• beekeepers generally are not concerned
about determining the pollinating efficiencyof their colonies, but are only trying to produce the largest possible amount of honey;• beekeepers do not know how to stimulate
the bees to collect pollen, which increase
pollination efficiency, instead of nectar;• beekeepers do not know how to direct bees
to a crop that needs pollination;• beekeepers distribute their beehives in a manner that is convenient for management, without concern or knowledge about the mostefficient arrangement to facilitate pollination;• beekeepers manage their bees only forhoney production because the farmers normally do not pay for pollination services;• we do not know the support capacity ofagricultural areas for honey bee colonies or
how many honey bee colonies can beplaced in a specific area.

Rearing and managementof Africanized honey beesin greenhouses
Current problems:• lack of knowledge of the minimum requirements necessary to use Africanized bees ingreenhouses (size of the colony, best time tointroduce the bees to the crop, culture
specifics and management techniques);• misconceptions about Africanized bees as
effective pollinators;• aggressiveness of the bees;• lack of technical and practical experience.
Proposals:• make producers aware of the usefulness ofhoney bees for pollinating in green houses;• inform public and private agencies involvedin rural extension, technical assistance andpromotion;• encourage research institutions to makestudies on this subject, through specificguidelines and financing;• develop informative material, as a tool toencourage increased use of honey bees ingreenhouses, informing about successful
experiences in Brazil and from other partsof the world, and by examining economic criteria;• develop incentives for using honey bees aspollinators in greenhouses and reducing theuse of pesticides (tax deductions, low interest loans, etc.);• publicity campaigns informing about thebetter quality of well-pollinated fruits andvegetables, uncontaminated by pesticides;• encourage and make available techniques
for producing food in greenhouses;• capacitate technicians involved in extension
and who assist farmers so that they canhelp them use honey bees as pollinators ingreenhouses.

70

State of the art of the use of Africanizedhoney bees for pollination
Currently, honey bee colonies are rented forpollinating apples, melons, cashews andsome vegetable crops in Brazil. There are
efficient techniques for transporting thebees, but data on other cultures are lacking.
Isolated experiments have demonstrated
the value of bees for many crops in Brazil,
but these have not influenced the growers,
and more objective and thorough experiments are needed, preferably with demon-

stration plots to show the value of pollination to the farmers.
Rental prices for bee colonies
Beekeepers and growers are generally
unaware of how much they can or should
charge for their services. There is little tradition
for this activity, and beekeepers often have adifficult time to determine their real costs andthe monetary benefits for the farmers. Thisrequires economic studies, which should thenbe made available to both parties.

Case studies to determine the need for pollination of major crops
Use of Africanized bees for pollination Recommendations for case studies
CottonPrincipal Producer: Mid Eastern states, high tech production in the NE: MA, CE, PA, PE, AL, BA.
Problems:• incorrect use of pesticides;• lack of knowledge about natural pollinators;• though this plant produces abundant nectar, the intensive use of insecticides
results in extremely reduced pollinator populations in and around the fields;• we have some data that cotton is benefited by honey bee pollination;• we need to determine the real effect of honey bees on cotton yield andquality, and determine the integrated pest management techniques that will
permit co-existence of the bees with the crop;• economic studies should be made to determine the costs and benefits ofincluding honey bees in cotton production.

MelonsPrincipal producers: CE, RN.
Export productInitiated and expanded continuously during the last six years, always withhoney bee pollination.

Problems:• incomplete information about the benefits of using pollination to improve thequality and the quantity of the fruits produced;• fear of the strong defensive behavior of the africanized bees;• productivity can be increased more than 40% with adequate pollination, however

the responsibilities of the farmer and the beekeeper are often not well defined;• we need to have good data on the real economic advantages of using honeybees for melon pollination, and how to maximize this contribution, taking into
account the negative effects of cultural practices on the honey bee colonies;• we also need to determine the most efficient means to improve pollination efficiency.

Workshop I 71

CitrusExport crop (juice concentrate).
Problems:• intensive use of insecticides;• spraying during flowering;• the increased quality and quantity of fruits that come with pollination is

generally unknown;• the growers unjustly fear that the bees will spread diseases;• fear of the strong defensive behavior of the bees; the farmers may reject

having them near their orchards;• we need good data on the benefits of pollination for fruit production andquality for all the various varieties of oranges;• we need to demonstrate these benefits to the farmers and work with them toreduce the impact of pesticides used in the groves on the bees.

CoffeeOne of the principal Brazilian export products.
Problems:• lack of financial incentive for beekeepers to introduce their colonies into thecoffee fields;• flowering is very fast, less than a week;• flowering occurs at a time when the bees are in orange orchards;• coffee honey is not highly valued;• use of pesticides;• though we have some good data on the value of honey bees for improving

coffee production, we need more thorough testing in modern cultivars and fields
to determine the best recommendations for pollination;• as beekeepers would not normally take their hives to coffee plantations,

economic studies should be made to determine adequate pollination fees, taking
into consideration the benefits for the growers.

Recomendations
1.A document should be developed about thestate of art of the use of Africanized honeybees for pollination.
2.Preparation and distribution of a manual on
standard methodologies for rearing Africanized bees for pollination purposes.
3.Development of a central library with all theavailable Brazilian literature on pollination,
including theses and congress proceedings,
and that those be made available via Internet.
This has been initiated at the University ofSão Paulo campus in Ribeirão Preto, SP, but
it needs to be improved and made more
widely available. There is a book with a collection of 300 thesis abstracts (in Portuguese
and English) and a list of over 2000 publications on bees made in Brazil until 1992
(Soares & De Jong 1992). This material is
updated periodically and is kept in a database, which is available to some researchers.
We need to create means to archive anddigitalize all of those articles and theses, sothat this information will be more widely
available, and will not be lost.

72

4.Initiate a scientific journal on pollinator
biology in Brazil. Brazil has many bee
researchers, however much of the information is not readily available. A scientificjournal will help remedy this problem andwill help direct students and professors to
study pollination problems. This journal
could be produced online at relatively low
cost, and could help consolidate bee
research in Brazil.
5.Develop a manual on research techniques forpollinator studies, especially to determine thevalue of pollinators for crop production.

Rational Program of Pollination
1.Determine how well crops are pollinated currently and investigate the production potential if there were full, adequate pollination. Some crops are alreadywell pollinated, and additional pollinators
do not increase production. In other crops
and regions, there are so few natural pollinators that supplemental pollination canmake the difference between uneconomical production and profit.
2.Estimate economic viability of pollination program. The producer needs to havean idea about whether it will be economically viable to use pollination for his crop, considering the costs involved with personnel,transport, and renting bee colonies, compared to the increases in production.
3.Identification of the requirements of thecrop and determination of the pollination needs. Each vegetal species has its
own specific pollination needs and appropriate pollination techniques are needed to fulfill these needs.
4.Determine the pollination strategy thatshould be used. There is a need to determine the number of colonies per hectare,
the arrangement and temporal placementof the colonies and integration with othercultural practices.
5.Design and install apiaries and infrastructure necessary for pollination.
Determine the number of apiaries andcolonies that will be needed at appropriate
times to give support to the pollination
activities.
6.Training of personnel responsible formaintaining the colonies in conditions
adequate for pollination. Preparing colonies for pollination requires specific management so that they will be at an adequate stage of development and with sufficiently large populations to adequately
pollinate the crop.
7.Training of personnel to collect pollination data in the field or hire such help. The
results of pollination should be constantly
monitored.

Final recommendations
Considering what are the conservation measures necessary to keep a stable population of
Africanized bees in the cropping areas:
1.incentives, such as tax exemptions for beekeepers and for growers for pollination ofcrops in Brazil;
2.PDF-B should make a policy of recognizing the need for Africanized bees for pollination;
3.conduct case studies to show the importanceof wild pollinators in respective habitats;4.stop indiscriminate logging and commercial
felling of trees by enacting laws;
5.promote and encourage re-conversion of acertain percentage of intensively cultivatedareas to provide rescue space for the multiplication of wild honey bee colonies by
providing incentives (tax exemptions, subsidies etc.);

Workshop I 73

6.train farmers in making judicious and safeuse of carefully selected, less toxic, pesticides in safer formulations;7.promote IPM (Integrate Pest Management);
8.provide nesting strips/spaces near the culti-

vated areas and encourage multiplicationand growth of native plants that can provide
food for wild bees;
9.encourage agro-biodiversity by planting
some areas with native plants.

References
BASUALDO, M.; BEDASCARRASBURE, E.; DE JONG, D. 2000. Africanized honey bees
(Hymenoptera: Apidae) have a greater fidelity to sunflowers than European bees. Journal of
Economic Entomology, 93: 302-307.
COUTO, R.H.N. 2002. Plantas e abelhas, uma parceria em crise? Anais do V Encontro sobre
Abelhas. Ribeirão Preto - SP, Brazil, p. 87-94.
CREMONEZ, T.M., DE JONG, D., BITONDI, M.M.G. 1998. Quantification of hemolymph proteins as
a fast method for testing protein diets for honey bees. (Hymenoptera: Apidae). Journal of
Economic Entomology, 91: 1284-1289.
DE JONG, D. 1996. Africanized honey bees in Brazil, forty years of adaptation and success. Bee
World, 77: 67-70.
DE JONG, D. 1996. Loque americana, o grande perigo para o futuro da apicultura brasileira.
Mensagem Doce, 39: 11 -12.
MESSAGE, D., DE JONG, D. 1998. Dispersão Internacional da bactéria Paenibacillus larvae, causadora da doença de abelhas, Cria Pútrida Americana, através da comercialização de mel.
Mensagem Doce, 50: 8 -12.
NOGUEIRA-COUTO, R.H, PEREIRA, J.M.S., DE JONG, D. 1998. Pollination of Glycine wightii, aperennial soybean, by Africanized honey bees. Journal of Apicultural Research, 37: 289-291.
SOARES, A.E.E., DE JONG, D. 1992. Brazilian Bee Research. Sociedade Brasileira de Genética.

Workshop I 75

C) Stingless bees
Participants: Marina Siqueira de Castro, Dirk Koedam, Felipe Andrés León Contrera,
Giorgio C. Venturieri, Guiomar Nates Parra, Kátia Sampaio Malagodi-Braga, Lucio de O.
Campos, Maria Viana, Marilda Cortopassi-Laurino, Paulo Nogueira Neto, Rui C.
Peruquetti, Vera Lúcia Imperatriz-Fonseca.

Abstract
Stingless bees are social bees that live in tropical regions of the world. They are poorly studied and known, even though they are themain visitors of numerous flowering plants inthe tropics and likely the principal pollinatorsof many of them (for a review, see Heard,1999). Only recently attention on their role aspollinators has been paid. Here we evaluatedthe knowledge obtain worldwide until now on
the role of stingless bees as pollinators, identified some crops that could be pollinated bythem, as well as the constraints for their use aspollinators in large scale for agricultural
demand in Brazil.
Data for this report were updated until 2006.

Introduction
Stingless bees are diverse in tropics and canpotentially be used as pollinators for several
native and exotic crops cultivated in Brazil(Nogueira-Neto, et al., 1959; Bego, et al., 1989
a and b; Heard, 1987, 1993, 1994, 1999;
Heard & Exley, 1994; Ish-Am, et al., 1999;
Malagodi-Braga, et al., 2000; Slaa, 2000;
Castro, 2002; Malagodi-Braga, 2002; Cauich,
et al., 2004; Cruz, et al., 2004). The native
Brazilian stingless bees richness is estimated in
500 species (Camargo, p.c.). Due to the highstingless bee diversity, basic research is stillneeded, although many studies had been
done in the last years. Among the 13
Australian epiphytic orchids whose pollinators
are confirmed, 9 are pollinated by stinglessbees (Adam & Lawson, 1993, apud Heard
1999). Males of some stingless bees areimportant pollinators of native Brazilian
orchids of Maxillaria genus (Singer, 2002;
Singer & Koehler, 2004) who offer fragrancesand colors that attract workers of Trigona.
Recently, Slaa, et al. (2006) reviewed the roleof stingless bees as pollinators and the cropsthat they effective pollinate doubled in number since the excellent review of Heard (1999)
Although their breeding techniques areavailable to beekeepers, at least for sometaxa such as Melipona, Scaptotrigona andTetragonisca, no stingless bees are yet commercially available to growers for pollination
purposes. The unique example where protocols for greenhouse pollination are well established is the use of Tetragonisca angustula andother small stingless bees for strawberries(Fragaria x ananassa Duchesne, Rosaceae) pollination (Malagodi-Braga, 2002; MalagodiBraga & Kleinert, 2004). Some species ofMelipona could be good pollinators of someSolanaceae crops that need “buzz pollination”, as Melipona quadrifasciata for tomatoes(Lycopersicum esculentum) growing in greenhouse (Del Sarto, et al., 2005). For native tropical fruits, as umbu (Spondias tuberosa), açaí
(Euterpe oleraceae) and cupuaçu (Theobroma

76

grandiflorum), the pollination requirements
are being studied (see table 1).
Coevolution between local flora and stingless bees should occur in high diverse habitats. Despite of their generalist use of floral
resources, stingless bees show floral preferences (Ramalho, et al., 1990; Biesmeijer, et al.,2005; Biesmeijer & Slaa, 2006). It is necessary
to improve this knowledge in order to determine preferences and the main plants indicated as food source for their successful
breeding, as well as for using in habitat
restoration programs.
A huge problem for Brazilian stinglessbees breeders and for capacity building activities is that relevant literature is in English or noteasily available; most bee species have notbeen studied yet. A recommendation is tomake available, in Portuguese, a synthesis of
the present knowledge, written for different
stakeholders, and to provide basic knowledge
needed for rear them. The WebBee (Saraiva, etal., 2004) was constructed in order to be ourinfoway in this task.
Considering the high biodiversity of stingless bees, and the new meliponiculture regulation for research and for beekeeping (CONAMA_346, 2004), it is necessary to improve thedevelopment of breeding techniques, in orderto provide bees for research and for meliponiculture. Nests can be obtained by using trap
nests in nature; a nest census and a bait-trap
survey in natural and agricultural areas for stingless bees is also a priority for investigation. A
recent research developed in Sarawak, Asia,
showed the effects of human disturbance on astingless bee community in a tropical rainforest,
as a result of changes in resources availability(Eltz, et al., 2002 and Eltz, et al., 2003;
Samejima, et al., 2004). Such changes in thebee community may affect the reproductive
success of plants and ultimately forest composition. Nests sites are considered as essential

resources, and have some requirements, as
specialization in use of logs of some plant
species or diameters at breast height bigger
than 50cm. This has implications for reforestation programs as well for the sustainable use offorest and the conservation of stingless bees,
important native pollinators (Venturieri, 2004).
The use of stingless bees for pollination
purposes should consider the settlement ofcorridors between patches of native vegetation for keeping native populations of pollinators as well as trees for nesting and flowers for food (nectar and pollen). As agriculture is increasing in Brazil, the land management of surrounding agricultural areas is also
very important. Finally, stingless bees could
be excellent pollinators to be used by small
farmers (family growers) because they do notsting, are easy to manage, and are appropriate to small lands and cheap to rearing.
Besides that, some small farmers have thetraditional knowledge to rearing them, using
their honey as medicine. They need to learn
how to manage them for pollination andconservation purposes.

State of art
Stingless bees as greenhouses
pollinators
In 1988, Luci Rolandi Bego, from São Paulo
University, went to Japan with a grant ofBrazilian Academy of Sciences to work with Y.
Maeta on the use of stingless bees as pollinators in strawberry greenhouses. She carried
with her a colony of Nannotrigona testaceicornis, a colony of Plebeia droryana and oneof Tetragonisca angustula, in rational hives,chosen by chance among the other species
available at São Paulo University Bee
Laboratory, where they were know to be verystrong. Nannotrigona testaceicornis was test-

Workshop I 77

ed in strawberry greenhouse, and the resultsof its efficiency is in Bego, et al., The othercolonies were used to study foragers’ behaviour under greenhouse condition (Bego, et al.,1989a). Later on, Trigona minangkabau from
Sumatra was also tested in strawberry greenhouses, and the result compared with the efficiency of Apis in the same greenhouses(Katutani, et al., 1993).
In Brazil, stingless bees as pollinators forstrawberries in greenhouses were tested by
Malagodi-Braga (1992); Malagodi-Braga andKleinert (2004). Protocols for greenhouse pollination are well established related to the useof Tetragonisca angustula and other small
stingless bees. Malagodi-Braga & Kleinert(2004) showed the efficiency of Tetragonisca
angustula as a pollinator in “Oso Grande”
cultivar: in a greenhouse with 1350 plants
almost 100% of flowers developed into wellshaped fruits compared to 88% with open
pollination in the field.
Sweet pepper (Capsicum annuum, Solanaceae) is another crop cultivated around theworld, in open fields and in greenhouses(where its cycle is extended for production all
year round). Although sweet pepper is a selfpollinating plant, it benefits from bee pollination (Rasmussen, 1985). In Brazil, Cruz, et al.,(2005) tested the efficiency of Melipona subnitida as a greenhouse pollinator of sweet
pepper, variety All Big. They used four treatments in their research: hand cross-pollination, hand self-pollination, pollination by bees
and restrict pollination. The fruit set was not
improved by the use of M. subnitida as pollinators, but the number of seeds per fruit, theaverage fruit diameter and fruit weightincreased; a lower percentage of malformed
fruits were also found, comparing with selfpollinated sweet pepper.
Another important crop also often kept ingreenhouses in Brazil and worldwide is thetomato, Lycopersicum esculentum. Velthuis(2002) tells the successful story of the bumblebee Bombus terrestris used as tomatoes pollinators in greenhouses in the Netherlands andBelgium that resulted in a big industry of bumble bee rearing in various pary of the world.
Nowadays 1 million colonies of Bombus terrestris are yearly sold for using in agriculture(Velthuis & Van Doorn, 2004). However, exotic pollinators are to be avoided in many countries including Brazil. In search of local solutions, Brazil found that the use of some speciesof Melipona could be good pollinators ofsome Solanaceae crops that need “buzz pollination”, such as the relatively large Melipona
quadrifasciata for tomatoes (Lycopersicum
esculentum) growing in greenhouse (Del Sarto,
et al., 2005). Nevertheless, Macias & Macias(2001) and Cauich, et al., (2004) verified that
Nannotrigona pirilampoides is a very successful pollinator for tomatoes in greenhouses,
opening new possibilities for small stinglessbees use in those.
Open field pollinationand stingless bees
Heard & Exley (1994) already considered theimportance of agricultural landscape and natural vegetation for providing pollination services (the abundance of Trigona carbonaria inorchards of macadamia was correlated withthe extent of natural surrounding Eucalyptus
vegetation). Venturieri (1993) also remarked
the importance of natural vegetation aroundthe cupuassu crop in order to provide theneeded pollinators. Kremen (2004) considered
the importance of bee community as crop pollinators, pointing out that if we maintain several bee species from natural environments visiting flowers, the shortage of one species in
one year could be compensated by the othervisitor’s species, diminishing the impact of pollinators’ shortage on crops.

78

Coffee, a special commodity
Most of the world coffee production is originated from C. arabica shrubs, which are native
to southwestern Ethiopia, as well as from C.
canephora var. robusta (also known as C.
robusta), native to equatorial Africa. Coffea
arabica plants are typically grown in cold but
frost-free areas at elevations of 500-200m, andC. canephora typically from sea level to 1000m(Klein, et al., 2003a, Donald, 2004). Coffea
canephora is a self-sterile, diploid species, andC. arabica is a self-sterile tetrapoid species(Klein, et al., 2003a).
Traditionally, coffee farming involves theplanting of coffee bush under a selectively
thinned canopy of existing rainforest trees. This
combination of shading trees and coffee
shrubs form an integrated agroforestry system(Donald, 2004). There are many benefits originated from this way of production; first, shadecover up to 50% increases yields, and the presence of shade trees can control pest problems;
furthermore, the quality and size of coffee
beans, as well as the taste of the final productare better under shade systems than under systems without trees. However, this method was
replaced for a full-sun production in many
places. Where good soils and favorable climates are present, this method produces higher yields per unit area, although not necessarily per plant. Nevertheless, this method also produces some collateral effects, as an increased
rate of pest problems and secondary pesticide
problems. Nowadays, shading is only used
where it is necessary to reduce yields to keep
production sustainable in poor-nutrient soils,
where shade-loving varieties are grown, andwhere shade trees form part of economic agroforestry systems (Donald, 2004).
Another important issue related with coffee production is the presence or absence ofpollinating insects. Formerly, the importanceof pollinators for coffee shrubs was neglect-ed (Free, 1993), but in recent years theirimportance is being evidenced after a seriesof experiments made in several countries.
Here we describe these results in order toshow the importance of pollinators for thecoffee harvest.
A pioneer work in this area was performed by Nogueira-Neto, et al., (1959), whichinvestigated the effect of the exclusion of pollinating insects on the yield of the variety
Bourbon (C. arabica var. Bourbon) in a farm inSão Paulo State, Brazil. They found a tendency(although the differences were not significant)towards a higher production of fruits on theplants that were allowed to receive the visit ofpollinating insects, in contrast to a control
group, which plants were not allowed to bevisited. They also observed several species ofnative and introduced bees visiting coffee
flowers, as the introduced Apis mellifera andthe stingless bee Melipona quadrifasciata,
both relatively big sized bees, the most effective pollinators of coffee flowers in their observations (a total period of observations of six
years). According to the authors, the smaller
bees (Nannotrigona testaceicornis, Plebeia sp.,
Tetragonisca angustula, Trigona hyalinata andT. spinipes) observed in the flowers, collecting
pollen and/or nectar were not so effective pollinators as these big sized bees. They concluded that for this variety of coffee (Bourbon),insect visits are not so important as for the
diploid self-sterile species of Coffea arabica,
which needs the visiting of insects, especiallybees, as well as the wind, for their pollination(Nogueira-Neto, et al., 1959).
Roubik (2002) strongly suggested theimportance of honey bees and native bees forthe increasing of pollination of C. arabica
plants in the New World, as well as in the Old
World. He found a positive correlation
between the coffee yields and the presence ofhoney bees in the New World. As AfricanizedWorkshop I 79

honey bees were introduced in the New Worldin the middle 1960´s, and they reached Central
America in 1985, he compared the coffee
yields of the period before and after its introduction. After the arrival of Africanized bee inCentral America, coffee yields in most countries of this region increased substantially,
except for the Caribbean countries (e.g. Haiti),
where native and introduced pollinators wereabsent. In the Old World, where honey bees
were always present, coffee production did
not varied in the same rate than the New
World. Countries that experienced an intensive land usage and loss of habitats for pollinators had reduced yields (loss of 20-50%),although they had increased cultivated areas(Ivory Coast, Ghana, Kenya, Cameroon,
Indonesia, El Salvador and Haiti) (Roubik,
2002). This work stressed the importance of
native and introduced pollinators for coffee
yields, although he did not analyze the pollination behaviour itself.
Ricketts (2004), in experiments performed at Costa Rica during 2001-2002,
showed that eleven eusocial bees (10 native
plus A. mellifera) were the most common visitors of coffee (C. arabica) shrubs, and thatthe distance of the forest fragments to thecultivated areas significantly influenced coffee visiting by these bees. Bee richness, overall visitation rate, and pollen deposition rate
were all significantly higher in sites withinapproximately 100m of forest fragments thanin sites far away (up to 1.6km). Apis mellifera
foragers accounted for more than 90% of all
visits in distant sites, and where Apis were notpresent, native species as meliponine bees
accounted for most of the visits at near sites.
This is due to the smaller flight range ofmeliponine bees which have a typical flight
range of 100-400m (van Niewestadt &Iraheta, 1996, Heard, 1999), although maximum observed flights ranged from 1 to 2 km

(Roubik & Aluja, 1983). When Apis abundance declined substantially, from 2001 to
2002, visitation rates dropped about 50% in
distant sites, but only 9% in near sites. Thiscan be explained by the compensating effectof native bees, which replaced Apis as themost important visitor in nearby sites. So,
according to the author, forest fragments
provided nearby coffee with a diversity ofbees that increased both the amount and stability of pollination services by reducing
dependence on a single introduced pollinator(Ricketts, 2004).
Similar results were found in Brazil (DeMarco & Coelho, 2004) and Indonesia (Klein,
et al., 2003b,c). Coffee (C. arabica) brancheswith free access to pollinators produced more
fruits in farms where there were forest fragments nearby. Coffee production increased
14.6% when the services of pollinators wereavailable (De Marco & Coelho, 2004). Similarly,
C. canephora and C.arabica fruit set increased
with the increase of diversity and abundanceof flower-visiting bees (C. arabica: 90% when
20 bee species were present and 60% when
only three species were present, Klein, et al.,2003b; C. canephora: 95% when 20 or more
bee species were present and 70% when only
six species were present, Klein, et al., 2003c),
and the number of social bees species
decreased with distance to forest fragments
and the number of solitary bees increased withlight intensity (less shade) and greater quantities of blossoms. Additionally, Klein, et al.,(2003b,c) found that solitary bees had an
important participation in the pollination of C.
canephora shrubs, leading to higher levels offruit set that originated by members of social
bee assemblages.
These services can be translated into economic advantages. For example, De Marco &Coelho (op.cit.) found, as previously stated,that coffee production increased 14.6% when

80

the services of pollinators were available. This
increase represents an extra income of
US$1860.55 per ha per year. Ricketts, et al.,(2004), showed that pollinating services fromtwo small fragments (46 and 111 ha) could betranslated into ~US$60,000 per year for one
Costa Rica farm.
All these results stressed the importanceof conserving forest fragments and nesting
places for social and solitary bee species (Klein,
et al., 2003c, Ricketts, et al., 2004), which can
act as service-providing units (Luck, et al.,2003) for coffee pollination. The costs ofmaintaining conservation areas are far exceeded by the economic benefits that the service ofpollinators brings for agriculture. In this way,conserving natural areas nearby coffee farms
can be translated into advantages for biodiversity and agriculture (Allen-Wardell, et al., 1998,
Ricketts, et al., 2004).
Stingless bees management practices
for use in agriculture
Agricultural intensification worldwide includes
a decline in the proportion of natural habitat,
an increase in pesticide usage, a decrease offloral 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 isunder concern by 21 Agenda for Agriculture.
Best management practices in agriculture
for sustainable use and conservation of pollinators are focused in recent literature, andmainly by several authors that study pollinators’ conservation. This means to carry on pesticides and their use in the crops; gene flow
studies; environmental friendly agricultural
practices, including land preparation, in orderto keep nests of solitary bees that occur in thesoil; agricultural area and maintenance of theirborders with native vegetation, or hedges thatcan keep pollinators; to decrease herbicides
use in agricultural crops, that helps the foraging supply for pollinators and crop attractiveness for them, in larger areas.
Although the already identified importance of pollinators in agriculture (see also
weevils for oil palm; bumble bees for tomatoes, among others; solitary bees for apple,
pears and alfalfa, for instance; stingless beesfor strawberry, guarana, assai, coffee, among
several other crops; honey bees for several
crops) is well known, until now their use is not
remarkable in undeveloped countries.
However, 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, forinstance. Developed countries are working
with pollinators’ shortage, although only asmall number of them (a dozen, according to
Kremen, 2004) are successful bred for agricultural use. If they are not available nearby due
to the intensive agricultural patterns usinglarge areas, they are bought from biotech
companies that breed them successfully. These
companies are multinational and have thetechnology of large scale breeding. The introduction of alien pollinators with defined
breeding techniques is also undesirable, andstudies of ecological impact are asked inimportation process. This stimulates the breading of native pollinators for the same service incountries 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 (Macias, etal., 2001; Cunningham, et al., 2002). An infantindustry arises with stingless bees breeding inAustralia (Heard & Dollin, 2000) and Brazil(Rosso, et al., 2001), growing in the world(Cortopassi-Laurino, et al., 2006).

Workshop I 81

Best management practices of pollinatorsin crops mean best crop economic value, andin this aspect both issues are together: economic value of pollinators and economic
value of crops. Generally, producers are notinterest in resistance (ability to retain community properties under disturbance) or resilience(ability to recover from disturbance) of crops
when intensifying agriculture, but in theireconomic value in this season. Short time
actions and market simulations are importantin the producer’s decisions on what crop touse in next season. They are linked to unpredictable weather conditions, as well to themarket fluctuation on crop values (Kevan &Viana, 2003), as well as to the economic
advantage in having better fruits. Long-term
activities concerning natural resources arealmost not considered.
The potential use of stingless bees’
nests in large scale is for using in crop pollination. How to get nests in nature and to
breed them successfully is a challenge.
Another point of consideration in relation to
the social bees of Brazil is the new law no.
02000.006608.2000-81. This law pretends
to protect these insects and has only recently
became effective. To protect these social
bees, it mainly prohibits the exploration ofnatural nests. Unintentionally, this law makes
it harder to access biological material of thesebees for who needs to do the necessary, legal
studies. Above all, the restriction put on by
this law makes that the artificial multiplication of colonies is the only option to obtainenough colonies to study these bees and,
thereafter, to use them in large scale projects.
This fact once more demonstrates thatknowledge about the reproductive biology ofthese bees is indispensable. We need morebiological information on nest sites, foodsources for improving colony development,colony multiplication, diseases.

Artificial offering of nests sites
Another possibility of deal with nest sites asa limited resource is to establish artificial trap
nests, offering nests sites for stingless bees.
Inoue, et al., (1993) did these experiments inorder to know more about the population
dynamics of stingless bees. They studied anarea of the Horticultural Experimental
Station in Lubuk Mintrum, in Sumatra,
where the main vegetation was a plantationof tropical fruits, rambutan, N. lappaceum,and durian, D. zibethinus (ca 480x200m, 86ha), where 24 species of stingless bees were
found. The species Trigona (Tetragonula)minangkabau was the most common, andsuitable for their study. They censused treecavities and possible artificial nesting sites toestimate the number of natural colonies. At
these censuses, 2 persons searched 4days/month. They also set 362 trap nests inthe field, of which 248 were perforated
bamboo stems and 114 wood boxes withglass 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:• trap nests were used by many animals, associal insects (mainly ants) and vertebrates(geckos, for instance);• only T. (Tetragonula) minangkabau occupied
the trap nests;• ants occupied 20% of empty nets;• bees occupied 6% of empty nests;• colonies were found monthly during all
experiment;• successful in nest establishment was also
recorded.
This experiment showed that additional
nest sites offer could improve the bee density
in the area, and that trap nests are suitable
only for some bee species.

82

Antonini & Martins (2002) used nest traps
in Cerrado without any result, in an area
where they found 46 nests of Melipona
quadrifasciata. Beekeepers sometimes mention that this bee species nests in abandoned
nests of Apis mellifera.
In Brazil, recently stingless bee’s keepers
are using pet bottles as traps nests. In a beekeeping meeting this year in Rio Grande doSul (III Encontro dos Meliponicultores) some ofthem reported that Tetragonisca angustula
use these pet bottles. A deeper research on
this subject is urgent, and is suggested as arecommendation.

Recommendations
Key stingless bees species for large scale
breeding in Brazil
The selection of some stingless bees’ species
for large scale breeding is needed. They
should be effective as pollinators, easy tomaintain in strong rational hives that could
be transported, easy to multiply, with a highrange of temperature and humidity for flightactivity. Species should be selected for greenhouses pollination as well as for pollinationin open field.
Due to the large size of Brazilian territory,
the selection should be regionally determined,
to facilitate breeding and colony trading. In
table 1 there are indications of stingless bee
species already known as good pollinators.
Our first selection should include:
1.Tetragonisca angustula. This species has awide geographical range in Latin America.
Very common in several habitats, including
cities, it frequently swarms, accepting artificial traps for establishing new nests. Moredata on queen and males rearing in natural
nests, on queen rearing in vitro under laboratory conditions, and controlled reproduc-tion of the queens under laboratory conditions are needed. The minimum populationof bees necessary to begin a new nest, as
well as their age composition must be evaluated. This bee also produces a honey thatis considered as medicine, and how to conserve it should be investigated. At thismoment, splitting colonies in two is possible, but this is not enough to allow theirlarge use as pollinators.
2.Melipona quadrifasciata. The queen fertilization under controlled conditions wasdone in M. quadrifasciata by Camargo(1972), that verified to be possible to put agyne and a male in a box and they immediately copulate. This result opens conditions for genetic manipulations of colonies. Besides, this bee can provide buzz pollination. Nevertheless the same result was
not obtained with other Melipona species
until now.
3.Melipona subnitida. In Northeast Brazil(dry regions, Caatinga) this bee species isbred for its honey, very appreciated by local
people. Until now, their role as pollinator
was studied in sweet pepper under greenhouse, with good results (Cruz, et al., 2005)
4.Melipona scutellaris. This species isalready used as a very good honey producer in Northeast Brazil, and bred by successfully by beekeepers. Domesticated and well
adapted in hives, this is one of the promising species to be used as pollinators where
they occur.
5.Nannotrigona spp. The use of Nannotrigona in greenhouses was shown to beeffective in pollination. Very common in
urban areas, and with a wide geographicalrange, must be studied concerning biology
and reproduction. The important resultsfrom Cauich, et al., 2004, in Mexico, showing that they are as effective in tomato pollination as other pollination treatments gives

Workshop I 83

to this genus a high importance for additional investigation.
6. At least 9 species of stingless bees from
Amazon (Melipona spp., Aparatrigona spp.,
Plebeia spp. and Scaptotrigona spp.) could
be kept massively to be used on pollination
programs. Tropical crops as cupuassu (Theobroma grandiflorum), urucum (Bixa orellana), assai (Euterpe oleracea), hogplum(Spondias mombim), guaraná (Paullinia
cupana) are some examples of Amazon
plants witch demands pollination services
from stingless bees.
Improving knowledge base
1. Improve regional stingless bees collections
and the use of molecular techniques needed to help identification.
2. Automatic monitoring of flight activity formodeling in climate change issues.
3. Promote stingless bees’ conservation inareas where logging is allowed.
4. Study nest sites; nests populations; nests
sizes and densities.
5. Improve nests availability through theestablishment of ecological corridors.
6. Establish techniques for ecological restoration and pollinators.
7. Identify pollinators assemblages in ecotones and fragments.
8. Promote stingless bees conservation inagricultural landscapes, also promoting
heterogeneity in landscapes.
9. Study exotic and native pollinators’ ecological relationships.
10. Study species acceptation in trap nests ofdifferent materials.
11. Use molecular tools to evaluate: density ofcolonies; males provenience; populationcharacteristics; relatedness among nests;
number of nearby nests (through the analysis of male clouds near the nest entrance, orby analyzing workers collected in a transect).

12. Develop metanalysis, data analysis andscientific publication diffusion of pollinators issues.
14. Improve techniques for nests development
in hives.
15. Evaluate queen survivorship in the colony.
16. Compare the characteristics of initial andmature nests.
17. Study sex-ratio and queen production in
selected species.
18. Improve honey production, quality andconservation.
19. Evaluate pollen availability and quality.
20. Study foragers’ lifetable in different seasons.
21. Study seasonal aspects of life cycle, mainly
in subtropical environment.

Final remarks
Concerning stingless bees’ biology, there is anurgent need for implement the researchgroups in the different Brazilian regions for
improving the local knowledge basis. Regionalgroups should be trained in standard methodologies to apply in their region.
Improve capacity building and training in
all levels, as well as concentrate studies innests requirements in order to implement the
new law 02000.006608.2000-81 concerning
to stingless bees beekeeping.
Conservation of stingless bees in logging
areas is an important issue, due to the large
Brazilian area that will be used for logging inAmazon region.
Develop life history studies for a selected
number of stingless bees species that arepotential generalist pollinators.
Provide literature in Portuguese and available on line.

84

Table 1: Stingless bees used as crop pollinators
Crop

Stingless Bee
Pollinator (s)Results

AuthorAverrhoa carambola(Oxalidaceae)
carambola

In Malaysia, Trigona
thoracica;

Efficient pollinator after
one visit

Phoon et al,1984

Bixa orellana(Bixaceae)
annattoMelipona melanoventerand Meliponafuliginosa; Melipona
seminigra merrilae

Buzz pollinated bystingless bees

Maués & Venturieri,
1995; Wille,
1976;Absy & Kerr,
1997

Capsicum annuum(Solanaceae)
suit pepper

Trigona carbonaria inAustralia; Melipona
subnitida

M. subnitida increased
fruit weight (by 29%) and Cruz et al, 2005; Silva
the number of seed per
et al, 2005
fruit (86%); 65% decreaseof deformed fruit

Cocos nucifera(Arecaceae)
Coconut

Apis mellifera and stingless Stingless bees are thebees contribute to thedominant visitors inpollination of this crop
Costa Rica

Hedström, 1988;
Engel and DingemansBakels, 1980

Coffea arabica var.
Bourbon (Rubiaceae)

Melipona spp.

Nogueira-Neto et al
1959

Coffea arabica(Rubiaceae)

Bee pollination

Higher fruit set andheavier mature fruits

Roubik 2002

Coffea canephora(Rubiaceae)

Bee biodiversity

Coffee fruit set was
higher in areas with highbee biodiversity (from 70
to 95%)

Klein et al, 2003aCoffea canephora

Trigona (Lepidotrigona)
terminate

84% fruit set

Klein et al, 2003b

Cucumis sativus(Cucurbitaceae)

Partamona bilineata

Frequent visitor

Meléndez et al., 2002

Cucumis sativus(Cucurbitaceae)

Scaptotrigona aff. depilis

Higher fruit production,
Santos et al, 2004
higher fruit weight andhigher % of perfect fruits

Euterpe oleraceae –(Arecaceae)“assaí”

Melipona melanoventer,
Melipona flavolineata andMelipona fasciculata(Meliponinae, Apidae)

In development

G. C. Venturieri et al,
2005

Fragaria x ananassa(Rosaceae)
strawberry

Tetragonisca angustula(Meliponini, Apidae)"Oso Grande" cultivar
100% primary flowers
developed; higher fruit
fresh weight

Malagodi-Braga &Kleinert, 2004

Workshop I 85

Fragaria x ananassa(Rosaceae)
strawberry

Tetragonisca angustula(Meliponini, Apidae)

Sweet Charlie Cultivar
Misshapen fruit reduced
by 86%

Lycopersicum
esculentum(Solanaceae)
tomatoNannotrigona
pirilampoides

As effective as mechanical Macias & Macias,
vibration in terms of fruit 2001; Cauich et al,set, fruit weight and2004
number of seeds per fruit

Lycopersicum
esculentum(Solanaceae)

Melipona quadrifasciata

Tomato flowers in
absence of vibration do
not produce fruits

Del Sarto et al, 2005

Macadamia integrifolia Trigona carbonaria(Proteaceae)(in Australia)
Macadamia nut

Yields and fruit quality
benefit from bee
pollination

Heard, TA; 1987

Mangifera indica(Anacardiaceae)
mango

Stingless bees are themore common visitors;
Tetragonisca angustula in
ChiapasImportant for crosspollination, Trigona bees
move from tree to tree.

Simão & Maranhão,1959

Myrciaria dubia(Myrtaceae)
camu-camu

Melipona sp andScaptotrigona postica

Nephelium lappaceum Scaptotrigona mexicana(Sapindaceae)
and Tetragonisca
rambutamangustula

Malagodi-Braga &Kleinert, 2004

Peters & Vasquez,
1986
Caged and open
pollination treatments
yielded a mean of 9.1
times the mature fruit offlowers from which bees
were excluded

Rabanales et al, in
press

Persea americana(Lauraceae) avocado

8 species of stingless bees Efficient as pollinators

Ish-am et al., 1999

Persea americana(Lauraceae)

Trigona nigra; N.
pirilampoides

Potential efficientpollinators

Can-Alonso et al,2005

Psidium guajava(Myrtaceae)
guava

Pollen found in Meliponamarginata,T. spinipes andM. quadrifasciata pots
Frieseomelitta spp.

Studies underdevelopment

Kleinert –Giovannini &I-Fonseca, 1987
Castro, p.c.

Psidium guajava(Myrtaceae)guava

M. subnitida

together with solitarybees, are efficientpollinators

Alves & Freitas, 2005

Salvia farinaceae(Labiatae)

T. angustula and N.
pirilampoides

Produce good quality
seeds in greenhouses

Slaa et al, 2000

Salvia splendens

Geotrigona spp. andPartamona

Bustamante 1998

86

Sechium edule(Cucurbitaceae)chayote, choko

28 stingless bees species
are important visitors; T.
corvina and Partamona
cupira are important

Stingless bees enhance
fruit production

Wille et al. 1983

Spondias tuberosa(Anacardiaceae)“umbu” or “imbu”

Frieseomelitta languida
and T. angustula

In development

M. S. Castro

Theobroma
grandiflorum(Sterculiaceae)
cupuassu

Plebeia minima and small
weevils. Most plantas areself incompatible;
Ptilotrigona lurida may be
a pollinator

Theobroma
grandiflorum(Sterculiaceae)“cupuassu”

Plebeia spp., Paratrigona
spp. & Frieseomelitta spp.
(Meliponini, Apidae)

Paullinia cupana
Melipona spp(Sapindaceae) guarana

Venturieri, GA et al,
1993

In development (Probio)

R. Gribel

together with Apis
mellifera

Aguilera, FJP, 1983

References
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Biota Neotropica, 3 n.2. On line http://www.biotaneotropica.org.br/v3n2

WORKSHOP II
Pollinator Initiatives and the role of Information
Technology (IT): building synergism and cooperation

Workshop II 91

Abstract

Workshop objectives

The São Paulo Declaration on Pollinators plus
5 Forum was organized by the Brazilian
Pollinators Initiative, BPI, and held in São
Paulo with the support of FAO to discuss standardized methodologies for assessing pollinator’ status and management practices to stop
their decline.
The main objectives of the IPI (International Pollinators Initiatives, in which BPI
take part) are:• monitor pollinator decline, its causes and its
impact on pollinator services;• address the lack of taxonomic information
on pollinators;• assess the economic value of pollination andthe economic impact of the decline of pollination services;• promote the conservation, the restoration and sustainable use of pollinator
diversity in agriculture as well as in related ecosystems;

The purpose of this workshop was to discuss
the role of Information Technologies (IT) for
the development and for the effectiveness of
the Pollinators Initiatives in a broad sense,from building a species catalog to providing
knowledge for policy making.
The program included reviews of relevant
activities and broader trends in biodiversity informatics, and their impact for Pollinators Initiatives.
Efforts, from local to global, were presented and their relationships and contributions to
the larger goals were discussed, as well as thepossibilities of networking and of sharing
tools, systems and data. Funding opportunities
was another important topic discussed.

Those tasks demand a huge effort,
including a lot of data acquisition (in thefield and in laboratory), and data analysis
for building knowledge on pollinators andpollination.
Many of those tasks can benefit from theuse of a variety of Information Technology (IT)tools that can help the scientist, the policy
maker, the extensionist, the student.
Taking advantage of the presence of avery distinguished audience at the Forum,
this workshop was proposed to discuss anddisseminate the importance of IT for the
Pollinator Initiatives, to help promote partnerships and exchange experiences on the development and use of those technologies, andto discuss funding opportunities.
This event was designed as an extensionof the Forum, open to all of its participants.

Organization and content
Organizing Committee
Antonio Mauro Saraiva, Escola Politécnica,
Universidade de São Paulo.
Vanderlei Perez Canhos, Centro de Referência em Informação Ambiental - CRIA.
Vera Lucia Imperatriz Fonseca, Instituto deBiociências, Universidade de São Paulo.
The workshop was held in 31st. October 2003,
at Escola Politécnica da Universidade de São Paulo. It was organized as a series of presentationsof local, regional and global initiatives and projects followed by discussion on broader issues.
The local (Brazilian) initiatives presented:• WebBee – The WebBee project, an information network on bee diversity was presented by prof. Antonio Mauro Saraiva,
from Escola Politécnica - USP, Agricultural
Automation Laboratory, Brazil.
• Brazilian Pollinators Initiative - BPI – waspresented by Bráulio Dias, from the Brazilian

92

Ministry of the Environment (MMA), Brazil.
Pollinators e-Journal – The proposal of anelectronic journal on pollinator biology waspresented by prof. David de Jong, from
Genetics Department, Faculdade de Medicina,
Universidade de São Paulo – FMRP-USP, Brazil.
• speciesLink - The speciesLink project, that
integrates many biological collections waspresented by prof. Vanderlei Peres Canhos,from Reference Center of Environmental
Information - CRIA, Brazil.
The regional initiatives presented:• the International Centre for Integrated
Mountain Development (ICIMOD), waspresented by Dr. Uma Partap and Dr. Farooq
Ahmad, from ICIMOD, Nepal .
• the North American Pollinators Initiative(NAPI), was presented by Dr. Mike Ruggiero,from the International Taxonomy Information
Service (ITIS) and the National Museum of
Natural History, Smithsonian Institution, USA.
• the European Pollinators Initiative (EPI),
was presented by Dr. Simon Potts, from theCentre for Agri-Environmental Research,
Reading University, UK.
• the International Network for Expertisein Sustainable Pollination (INESP), waspresented by prof. Peter Kevan, from
University of Guelph, Canada.
• the African Pollinators Initiative (API), waspresented by Dr. Barbara Gemmil, from
Environment Liaison Center International(ELCI) (Kenya) and Dr. Connal Eardley, from
Agricultural Research Council, Plant Protection Research Institute, South Africa.
• the IABIN Pollinators Network and the New
World Bee Catalog were presented by prof.
Vanderlei Peres Canhos, from CRIA, Brazil.
•

The Global Initiative presented:
the International Pollinators Initiative(IPI), was presented by Linda Collette from•the United Nations Food and Agriculture
Organization (FAO).

Discussion
The topics suggested for discussion were:• towards a common agenda - building theshared infrastructure;• how to integrate actions;• standards, protocols and systems interoperability;• on-line directory of institutions, experts, programs and projects;• on-line databases: taxonomic authority files,
specimen DB, species DB, phenologicaldatasets for meta-analysis;• computational tools for data mining, analysis, synthesis and visualization;• funding opportunities and co-financing requirements - GEF projects and local Funding;• recommendations.

Expected Results
Expected results of the workshop included:• a clearer understanding of the role of IT in
the Pollinator Initiatives;• the establishment of partnerships for thedevelopment and sharing of the IT infrastructure required for the Pollinator Initiatives: tools
and systems developers and data providers;• the identification of funding opportunities
for the development of the IT infrastructure
on a local, regional and global scale.

Introduction
As was pointed out by Saraiva & ImperatrizFonseca (2004), Information Technology (IT)
has a decisive role to play on the development

Workshop II 93

of the Pollinators Initiatives (PIs), and that canbe analyzed based on the core objectives ofboth the International Pollinators Initiative (IPI).
These core objectives are:• monitor pollinator decline, its causes and its
impact on pollinator services;• address the lack of taxonomic information
on pollinators;• assess the economic value of pollination andthe economic impact of the decline of pollination services;• promote the conservation, the restorationand sustainable use of pollinator diversity inagriculture as well as in related ecosystems.
It is not difficult to see that one way or
another those objectives involve issues related
to data, information and knowledge: theiracquisition and analysis, their transformationfrom raw data to useful knowledge, their use
for sound decision and policy making, theirdissemination for wider audiences to increaseawareness and education.
Those are typical tasks for Information
Technology in a broad sense and, more specifically speaking, those are simply the goals of
Biodiversity Informatics, a new discipline ordenomination created to deal with the application of IT to Biodiversity.
The complexity of biodiversity and its
processes, the huge figures involved, theamount of variables and data that are to be
dealt with, the regional and global coveragethat is usually necessary, all demands IT tools toacquire data, to store and manipulate them, tohelp analyze them, and to convey the results
and findings in different formats and media todifferent target audiences.
It is not different in the case of the PIs.
Monitoring pollinator decline demands moreaccurate and automated methods and toolsthat will help researchers collect more and bet-

ter data with less effort, while allowing themto concentrate on the design of field experiments, on data analysis, i.e., on turning data
into information and knowledge.
As for the taxonomic information, on one
hand the information gathered after decades
and maybe centuries of research is not readily
available even for the scientific community
because it is spread around the world in museum collections or the like. Digitizing the collections and publishing them on the Internet will
increase the accessibility while still providing
control over the data whenever this isrequired. On the other hand, IT tools can beused to help automate species identification,
be it with instrumentation systems or withidentification keys whose rules can be embedded in computer programs.
Once data is acquired, different types ofanalysis need to be made taking into accountthe species distribution, the effect of changes
on the environment, the economic value andimpact, and different strategies for conservation, restoration and use. These analyses
would benefit from the use of simulation toolsthat can be used to develop different scenarios
upon which decisions can be made.
One of the most important points stressedin the PIs is increasing awareness raising: it isurgent to demonstrate the importance of pollinators and the risk of their decline. The internet
can play a very important role on that. However,
the web can also have a strategic function for
the integration of the research community,
which can share data, communicate and cooperate more efficiently, even though remotely.

Results
The presentations made at the workshop(which are available at WebBee portal)
showed a wide range of uses, systems andfuture possibilities for IT applied to the PIs.

94

They unanimously stressed the advantages
and importance of the use of IT tools and techniques to help achieve the goals of theInternational Pollinators Initiative and of thenational/regional PIs. The project Conservationand Management of Pollinators for Sustainable
Agriculture Through an Ecosystem Approach,under the auspices of FAO and GEF, will require
an intensive use of IT on the development of its
four components. The preliminary phase of the
project, the PDF-B phase, will provide an
opportunity to review, identify and analyze
gaps on the technology regarding its application to the PIs. The full-size project that willsubsequently be developed may accommodatepart of that development.
According to what was presented, software tools seem to be the most widely usedcomponents. Websites for various purposes
were reported for all PIs though their content
and complexity differed significantly. In somecases, simple webpages are used to convey
project information, educational information,etc. Despite that simplicity, their effectivenessis acknowledged and they fulfill some basic
needs of the developers and users.
At a higher level, there are the databasesthat can be accessed via Internet. Specimen
information from biological collections atmuseums, for instance, is being digitized and isincreasingly available on-line. Though the percentage of the specimens of the known world’s
collections that is already available on-line issmall, that number is increasing consistently
and some international and global efforts inthat direction were mentioned. It was stressed
the need to join and to strengthen that digitization effort, which faces many difficulties
related to funding and data ownership.
This brings up the problem of the integration of all that data. Such integration is important for many different purposes, such as forbuilding a global catalogue of life on Earth (suchas the Catalogue of Life, from Species 2000 and
ITIS ), and for creating checklists of species andresolving naming problems. Further use of integrated data is made by analysis software, suchas that for modeling species distribution, extinction risk, and protection strategies. Analyses
tools are of utmost importance as they can beused to guide the development of environmental public policies on a more solid foundation.
This integration requires the use of standards and protocols for data exchange. Thesestandards are under development with thesupport of institutions such as GBIF, TDWG,
among others, with the participation ofgroups from many countries. This is anotherarea that needs more support, as it is essential
to allow more seamless access to and share of
biological data. It was suggested that FAO and
GEF should participate of that effort. An example of the use of those standards to integratedifferent sources via internet was presented at
the SpeciesLink project .
As the use of such information increases
in its complexity, more tools are necessary toallow automation of many of the boring andrepetitive tasks.
An important part of the remote access todata is related to bibliography. An on–line peerreviewed journal on pollinators and pollination
is being designed within the BPI, and it wassuggested that this journal should be supported within the FAO/GEF project. Such a journal
would both facilitate information exchange
and encourage research and publications onpollinators, especially in the developing countries. Much research on pollinators and pollination in developing has been traditionally donein a haphazard manner, and often the results
are not readily accessible. A specific journal on
pollinators would both provide means to guideand improve such research, through examples
and through peer review, and would also facilitate publication of such information.

Workshop II 95

It is important that other media, such asimages and videos, be used to convey information via internet. They must be complemented by texts but they have a strong impact
and should be incorporated especially for specific audiences and for some purposes. An
example of an information system that isbased on species information (rather than on
specimen information) and which makes
intensive use of visual information was presented on the project WebBee.
Another set of IT tools not very muchmentioned was instrumentation, though it
became clear that it is fundamental forincreasing the capacity of data acquisition andthe quality of this data. It is also important forallowing the application and the replication of
the standard methodologies discussed at theother workshops of the Forum. Part of the
WebBee project involves the development anduse of a set of instruments applied to pollinators monitoring. Those experiments can beaccessed via internet and can be shared
among many users collaboratively.

Difficulties andrecommendations
Along with the discussions that arose during
the workshop sessions one important point thatstood out was the need for IT support personnel. Most institutions that were present at theworkshop do not have IT support personnel orat least not at level required nowadays, considering systems development and infrastructure.
Another issue related to support is themaintenance of such systems. Many of them
are developed with funds from research projects but it is often hard obtain funding for sustaining them on the long term. The same
applies to the issue of updating the systemwith new information and data: that task

requires people and this is sometimes forgotten, and often hard to obtain funding.
Considering the end-users that are expected to benefit from those systems another pointthat was discussed was the access to internet inrural areas, especially in developing countries.
That should be considered in the technicaldesign of the systems and on other actions at
the level of public policies for digital inclusion.
Another topic is related to the question ofdata ownership and sharing by researchersand countries. That question is sometimes delicate, both at the personal level and at thecountry level, since national legislation differ
and sometimes restrict the access to biological
data fearing biopiracy.

Final remarks
The workshop provided a very good opportunity to show to the audience a wide range ofcases, tools, systems and initiatives regarding
the application of IT to pollinators and pollination and related areas. For a significant part of
the audience some of the topics covered presented novelties. The presence of a public withmany end-users was important to help collect
their feelings and experiences with respect tothe technology. It also allowed a discussion
about some critical issues, technical and political, that must be dealt with so that IT can beeffective for the Pollinators Initiatives; and promoted opportunities for strengthening contacts and relationships, for showing areas ofinterest and competencies that may evolve tofuture cooperation, which is a central part of
the IPI and of the GEF/FAO project.
The workshop achieved its expected
results and, being the first of its kind, showed
the importance of further discussion andmeetings to increase the use of IT for theadvancement of the Pollinators Initiative.

96

Notes
1. http://www.webbee.org.br/bpi/english/workshop_ 2003.htm
2. http://www.species2000.org/2005/search.php
3. http://splink.cria.org.br/

Reference
Saraiva, A.M & Imperatriz-Fonseca, V.L. 2004. A proposal for an information network for theBrazilian Pollinators Initiative – BPI. In: 8th.IBRA International Conference on Tropical Bees
and VI Encontro sobre Abelhas, 2004, Ribeirão Preto, Brazil. Proceedings. International Bee
Research Association – IBRA; FFCLRP-USP, 2004. CDROM.

ILLUSTRATIONS AND PHOTOGRAPHSXylocopa bee pollinating a
Lecythis pisonis flower.
Copyright Michael
Rothman 1999. Courtesyof the New York Botanical
Garden, Institute of
Systematic Botany

Solitary bees are specialized pollinators. Centris is important for cashew pollination. Above left, nests of Epicharis
Dejeanii; above right, nest of Ptilothrix plumata; below left, nest of Centris tarsata. Solitary bees can be attracted to trap
nests (below right), and moved to crops for pollination purposes.
From Schlindwein, et al., 2003, A quantitative approach to assess specialized bee plant pollinator systems, in http://
www.webbee.org acessed in March 10th 2006.

Biotic pollination dependence in melon farming: malformed (left) and export quality (right).
Photos by Raimundo Maciel de Souza.

Africanized honey bees are important pollinators. Above, orange flower. Photo by Tom Wenseleers.

Africanized honey bee visiting assai flower. Photo by Giorgio Venturieri.

Above left, assai is the second most important crop for Amazonian. Below, male and female flowers of assai need bees aspollinators.

Above, assai flower visited by Melipona fasciculata. Below, assai flower visited by Trigona spp. Photos by Giorgio Venturieri.

Melipona fasciculata hives in assai crop.

Melipona fasciculata nest entrance (above). Below, honey tray from a Melipona fasciculata hive; right, brood cells tray.
Photos by Giorgio Venturieri.

Malformed strawberry’s fruits (above left) and pollinated wellformed fruits (above right). Below, Tetragonisca angustulavisiting strawberry flower. Photo by Katia Malagodi-Braga.

Tetragonisca angustula nest entrance. Photo by Tom Wenseleers.

Vertical hive with special ventilation system for stingless bees of tropical areas (from Giorgio C. Venturieri in
www.cpatu.embrapa.br/paginas/meliponicultura.htm)

Embrapa provides field training is stingless bees breeding for Kumenê indians from Indigenous land Uacá, Oiapoque,Amapá state. Giorgio C. Venturieri teaches how to transfer a natural nest to a hive. Photo by Marcos Sztutman.