Embed Size (px)
Citation preview
Bees as pollinators in Brazilassessing the status and suggesting best practices
Edited byVera Lucia Imperatriz-Fonseca, Antonio Mauro Saraiva, David De Jong
Bees as p
ollin
ators in
Brazil
assessing
the statu
s and
sug
gestin
g b
est practices
The São Paulo Declaration on Pollinators, was endorsed in May 2000 bythe 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 onagrobiodiversity). COP5 established an International Initiative for theConservation and Sustainable Use of Pollinators, hereafter referred to asthe International Pollinator Initiative (IPI).
A Plan of Action was then prepared by Food and AgriculturalOrganization 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
• Assess the economic value of pollination and the economic impact ofthe decline of pollination services
• Promote the conservation, the restoration and sustainable use of polli-nator diversity in agriculture as well as in related ecosystems
To follow this agenda, the Brazilian Pollinators Initiative, under the sup-port of FAO, Ministry of Environment, Ministry of Science and Technologyand Sao Paulo University, promoted the workshop São Paulo Declarationon Pollinators Plus 5, in October 2003 . We joined the regional Initiatives,discussed common routes and some essential points: standardizedmethodologies, pollinators declining and management practices. Thisbook concerns the results of group discussions in the workshop São PauloDeclaration on Pollinators Plus 5, and was printed with a support fromConservation International-Brasil
HOLOS EDITORA ISBN 85-86699-51-9
Bees as pollinators in Brazil:assessing the status and suggesting best practices
2006
CONSERVATION INTERNATIONAL - BRAZIL
HOLOS EDITORA
Bees as pollinators in Brazil:assessing the status and suggesting best practices
Proceedings of the Workshop on São Paulo Declaration on Pollinatorsplus 5 Forum, held in São Paulo, Brazil, 27th-31st October 2003
Edited by:Vera Lucia Imperatriz-Fonseca, Antonio Mauro Saraiva, David De Jong
With Assistance from Associate EditorsCynthia Pinheiro-Machado; Fernando A. Silveira; Claudia Maria Jacobi;Breno Magalhães Freitas; Marina Siqueira de Castro
Ribeirão Preto2006
Workshop SponsorsFood and Agriculture Organization (FAO)
Ministry of Environment (MMA)
Ministry of Science and Technology (MCT)
São Paulo University (USP)
Printer SponsorsConservation International – Brazil
Brazilian Pollinator Initiative
Editorial assistanceTarcila Lucena
Book designRenata Carpinetti
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, EditoraRua Bertha Lutz, 39014.057-280 Ribeirão Preto , SPTeleFax: (0++16) 3639-9609Email: [email protected]
Dedication
Warwick Estevam Kerr
Pioneer in the study of bee genetics in Brazil, focusing especially on theMeliponini. During all of his life, he has encouraged and supported therearing of these bees, creating regional research groups across the countryand disseminating the importance of the environmental services providedby pollinators.
Both have inspired us with their principles, stimulation and dedication toscience.
Paulo Nogueira-Neto
Pioneer in Brazil in studies of the role of bees as pollinators, in classicresearch on pollination of the Bourbon variety of coffee. He is known world-wide for his innovative techniques for rearing indigenous stingless bees andhis involvement with environmental conservation.
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, BrenoMagalhães Freitas, David de Jong, Lionel Segui Gonçalves, Marina Siqueirade Castro. Also, we thank the cooperation of Bee Laboratory fromInstituto de Biociências, University of São Paulo, mainly to MarianaImperatriz 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 outstandinghelp; 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, forher 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: PolytechnicSchool of the University of São Paulo that has sponsored the workshop onInformation Technology and Pollinators Initiative, and the team from theAgricultural Automation Laboratory and WebBee project, especially TerezaCristina Giannini, Etienne Americo Cartolano Júnior and Renato Sousa daCunha 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 fieldtrip to Mata Atlântica that was very much appreciated.
Finally, for the printing of this book we have received the support fromConservation International Brazil.
The Editors.
Acknowledgements
Acronyms
Presentation
Worshop preparation
International Pollinators Initiatives
Methodological discussions
Protocols and discussions
Information Technology and Pollinators Initiatives
References
Worshop I: Survey methods for bees as pollinators in Brazil: assessing thestatus and suggesting best practices
Group 1: Surveying and monitoring of pollinators in natural landscapes and in cultivated fields
Group 2: Assessment of pollinator – mediated gene flow
Group 3: Bee management for pollination purposes
A) Bumble bees and solitary bees
B) Honey bee
C) Stingless bees
Worshop II: Pollinator Initiatives and the role of Information Technology (IT)
Illustrations and photographs
9
Summary
16
17
17
18
19
19
20
21
23
25
39
53
55
63
75
89
97
10
Adriana De Oliveira Fidalgo, Instituto deBotânica, Divisão do Jardim Botânico de SãoPaulo, Seção de Ecologia. Avenida MiguelEstefano 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 [[email protected]].
Anthony Raw, Laboratório de Entomologia, Departamento de CiênciasBiológicas, Universidade Estadual de SantaCruz (UESC), Rodovia Ilhéus-Itabuna, Km 16, CEP 45650-000, Bahia, BRAZIL, Tel: +55 73 680-5261[[email protected]].
Antonio Mauro Saraiva, Laboratório deAutomação Agrícola, Departamento deEngenharia de Computação e SistemasDigitais, Escola Politécnica, Universidade deSão Paulo, Av. Prof. Luciano Gualberto,Travessa 3, número 158, sala C2-54, CEP05424-970, Cidade Universitária, São Paulo,São Paulo, BRAZIL, Tel: +55 11 3091-5366[[email protected]].
Astrid de Matos Peixoto Kleinert,Departamento de Ecologia Instituto deBiociências, Universidade de São Paulo (USP),Rua do Matão, travessa 14, nº 321 CidadeUniversitária, CEP 05508-900, São Paulo, São Paulo, BRAZIL, Tel: +55 11 30917604[[email protected]].
Barbara Gemmill (Herren) Global PollinationProject Coordinator, Food and AgricultureOrganization of the United Nations, vialedelle Terme di Caracalla Rome, 00100, Italy,[[email protected]]
Braulio Ferreira de Souza Dias, Secretariade Biodiversidade e Florestas do Ministério doMeio Ambiente. SAIN Av. L4 Norte, CampusSede do IBAMA, Bloco H, CEP 70.800-200Brasília, DF, Brasil Tel. +5561 325-41-85 ou317-1120, Fax +5561 325-5755;[[email protected] &[email protected] ]
Breno Magalhães Freitas, Departamento deZootecnia, Universidade Federal do Ceará,Campus Universitário do PICI, Caixa Postal12168, CEP 60355-970, Fortaleza, Ceará,BRAZIL [[email protected]].
Carmen Silvia Soares Pires, Laboratório deBioecologia e Semioquímicos, CentroNacional de Pesquisa de Recursos Genéticos eBiotecnologia, Empresa Brasileira de PesquisaAgropecuária (EMBRAPA), Sain Parque Rural -W5 Final, Asa Norte, CEP 70849-970, Brasília,DF, BRAZIL, Tel: +55 61 448-4682[[email protected]].
Celso Feitosa Martins, Departamento deSistemática e Ecologia (CCEN), UniversidadeFederal da Paraíba, CEP 58059-900, JoãoPessoa, Paraíba, BRAZIL[[email protected]].
Claudia Maria Jacobi, Departamento deBiologia Geral, Universidade Federal de MinasGerais, Avenida Antônio Carlos 6627, CaixaPostal 486, CEP 30161-970, Belo Horizonte,Minas Gerais, BRAZIL[[email protected]].
Clemens Peter Schlindwein, Departamentode Botânica, Centro de Ciências Biológicas,Universidade Federal de Pernambuco (UFPE),Av. Prof. Moraes Rêgo s/n, CidadeUniversitária, CEP 50670-901, Recife,Pernambuco, BRAZIL, Tel: +55 81 3271-8352[[email protected]]
The participants on both workshops were
Participants I 11
Connal Eardley, Bee Systematists &SAFRINET Co-ordinatos, Plant ProtectionResearch Institute Agricultural ResearchCouncil, Plant Protection Research Institute,Private Bag X134, Queenswood, 0121, SouthAfrica, 590 Vermeulen Street, Pretoria,SOUTH AFRICA, Tel +27 (0)12 - 304 9578,Fax +27 (0)12 325 6998[[email protected]].
Cynthia Almeida Pinheiro Machado,Fundação Integrada Municipal de EnsinoSuperior, Rua 22 esq. c/ Av. 01, SetorAeroporto, CEP 75830-000 - Mineiros, GO -BRAZIL, Tel.: (64) 36611970 Fax: (64) 38134151, [[email protected]],www.fimes.edu.br
David De Jong, Departamento de Genética,Faculdade de Medicina, Universidade de São Paulo (FMRP-USP), CEP 14049-900, Ribeirão Preto, São Paulo, BRAZIL, Tel: +55 16 602-4401, fax +55 16 633-6482[[email protected]].
David W. Roubik, Smithsonian TropicalResearch Institute, Unit 0948, APO AA34002-0948or APDO 2072 Balboa, REPUBLICOF PANAMÁ [[email protected] /[email protected]].
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 [[email protected]].
Denise Monique Dubet da Silva Mouga,Departamento de Ciências Biológicas, PróReitoria de Ensino, Universidade da Região deJoinville (UNIVILLE), Campus Universitário, s/n,Bom Retiro, CEP 89201-972, Joinville, SantaCatarina, BRAZIL, Tel: +55 47 461-9000 r. 9072 [[email protected]].
Dieter Wittmann, Institut fürLandwirtschaftliche Zoologie undBienenkunde, Melbweg, 42, University ofBonn, Bonn, 53127, GERMANY[[email protected]].
Dirk Koedam, Departamento de Ecologia,Instituto de Biociências, Universidade de SãoPaulo (USP), Rua do Matão, Travessa 14, nº 321, CEP 05508-900, Cidade Universitária,São Paulo, São Paulo, BRAZIL, Tel: +55 113091-7533 [[email protected]].
Eda Flávia Lotufo Rodrigues AlvesPatrício, Laboratório de Abelhas,Departamento de Ecologia, Instituto deBiociências, Universidade de São Paulo (USP),Rua do Matão, travessa 14, nº 321, CEP05508-900, Cidade Universitária, São Paulo,São Paulo, BRAZIL, Tel: +55 11 3091-7533.
Edivani Vilaron Franceschinelli,Universidade Federal de Goiás, Instituto deCiências Biológicas, Departamento de BiologiaGeral, Campus II - Samambaia - ICB1 -2 andar, Campus Samambaia, CEP 74001970,GOIANIA, GO, BRAZIL, Caixa-Postal: 131, Tel.: (62) 5211112, Fax: (62) 5211109,[[email protected]], www.icb.ufg.br
Farooq Ahmad, Indigenous Honey BeeProject, International Centre for IntegratedMountain Development (ICIMOD), P.O Box3226, Kathmandu, NEPAL, Tel: 09977-1-5525313, Fax 00977-1-5524509[[email protected]].
Favízia Freitas de Oliveira, UniversidadeEstadual de Feira de Santana, Departamentode Ciências Biológicas, Laboratório deSistemática de Insetos Lasis, Av. UniversitáriaS/N, Km 03 - BR 116 (Rodovia Feira deSantana - Serrinha) - Cidade Universitária,CEP 44031460, Feira de Santana, BA,BRAZIL, Tel: (75) 32248194, Fax: (75)32248019, [[email protected]]http://www.uefs.br/dcbio/lent_sis/index.html
12
Felipe Andrés Leon Contrera, University ofCalifornia - Berkeley, University Of California,San Diego - USA, [[email protected]]
Fernando Amaral da Silveira, Laboratóriode Sistemática e Ecologia de Abelhas,Departamento de Zoologia, Instituto deCiências Biológicas, Universidade Federal deMinas Gerais (UFMG), Avenida AntônioCarlos 6627, Caixa Postal 486, CEP 31270-901, Belo Horizonte, Minas Gerais, BRAZIL[[email protected]].
Fernando César Vieira Zanella,Departamento de Engenharia Florestal, Centrode Saúde e Tecnologia Rural, UniversidadeFederal de Campina Grande (UFCG), Bairro do Jatobá, CEP 58700-970, Jatobá – Patos,Paraíba, BRAZIL, Tel: +55 83 421-3397[[email protected]].
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[[email protected]], http://www.ufv.br
Francisco de Sousa Ramalho, CentroNacional 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[[email protected]].
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[[email protected]].
Gisele Garcia Azevedo, Departamento deBiologia 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 [[email protected]].
Guiomar Nates Parra, Laboratorio deInvestigación en Abejas (LABUN),Departamento de Biología, UniversidadNacional de Colombia, A.A. 144590, Bogotá,COLOMBIA, S.A, Tel: +3165000 ext.11335/11337, Fax 3165310[[email protected]].
Isabel Alves dos Santos, Instituto deBiociências da USP, Rua do Matão 321 trav14, Cidade Universitária, 05508-900, SãoPaulo, SP, BRAZIL,Tel: (11) 30917527 Fax: (11) 30917600, [[email protected]]
Jacobus Christiaan Biesmeijer School ofBiology.University of Leeds.Leeds LS2 9JT,UNITED KINGDOM.[[email protected]].
James H. Cane, Bee Biology and SystematicsLaboratory, Utah State University, 5310 OldMain Hill, Logan, Utah 84322-5310, USA,Tel: +01 435 797-3879, Fax 435-797-0461[[email protected]].
Jesus Santiago Moure, Departamento deZoologia, Setor de Ciências Biológicas,Universidade Federal do Paraná (UFPR),Centro Politécnico, Caixa Postal 19020, CEP81531-980, Jardim das Américas, Curitiba,Paraná, BRAZIL, Tel: +55 41 361-1671, Fax:+55 41 266-2042 [[email protected] /[email protected]].
João Israel Bernardo, Centro Federal deEducação Tecnológica do Paraná, ConselhoDiretor, Unidade do Sudoeste, Rodovia PR-469 (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, [[email protected]], URLda Homepage: http://www.pb.cefetpr.br
João 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[[email protected]].
Kátia Peres Gramacho, Faculdade deTecnologia 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, [[email protected]],URL da Homepage: http:\\www.ftc.br
Kátia Sampaio Malagodi Braga,Laboratório de Abelhas, Departamento deEcologia, 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[[email protected]].
Lílian Santos Barreto, Empresa Baiana deDesenvolvimento Agrícola, Estatal, Central deLaboratórios da Agropecuária, Av. Adhemarde Barros, 967, Ondina, CEP 40170-110,Salvador, BA, BRAZIL, Tel: +55 71 2370871 r.37, [[email protected]], URL daHomepage: http://www.ebda.ba.gov.br
Linda Collette, United Nations Food andAgriculture Organization (FAO), Viale delleTerme di Caracalla, 00100 Rome, ITALY[[email protected]].
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
Lucio Antonio de Oliveira Campos,Departamento de Biologia Geral, Centro de
Ciências 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
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, [[email protected]], 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 [[email protected]].
Maria Cristina Arias, Departamento de
Biologia, Instituto de Biociências,
Universidade de São Paulo (USP), Rua do
Matão, no 277, CEP 05508-900, Cidade
Universitária, São Paulo, São Paulo, BRAZIL,
Tel: +55 11 3091-7587 [[email protected]].
Maria Cristina Gaglianone, Laboratório de
Ciências 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
14
Maria José de Oliveira Campos,Departamento de Ecologia, Instituto deBiociências, Universidade Estadual PaulistaJúlio de Mesquita Filho (UNESP), Av. 24A, N.1515, CEP 13506-900, Bela Vista, Rio Claro,São Paulo, BRAZIL, Tel: +55 19 526-4145[[email protected]].
Maria Rodrigues Vianna, UniversidadeFederal de Ouro Preto, Instituto de CiênciasExatas e Biológicas, Departamento deCiências Biológicas, Campus Morro doCruzeiro, Ouro Preto, MG, BRAZIL, Bauxita,CEP 35400000, Tel: +55 31 35591699,[[email protected]]
Mariana de Araújo Melo, Departamento deBiologia Animal, Centro de CiênciasBiológicas e da Saúde, PPG-Entomologia,Universidade Federal de Viçosa (UFV), Av. P.H. Rolfs, s/n, Campus Universitário, CEP36571-000, Viçosa, Minas Gerais, BRAZIL, Tel:+55 31 3899-2531 [[email protected]].
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[[email protected]].
Marina Siqueira de Castro, Empresa Baianade 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: +5571 32351453, Universidade Estadual de Feirade Santana, Avenida Universitária s/n, Feirade Santana, BA, BRAZIL,[[email protected]], URL daHomepage: http://www.uefs.br/
Mauro Ramalho, Departamento de
Botânica, Instituto de Biologia, Universidade
Federal da Bahia (UFBA), Rua Barão de
Geremoabo s/n, Ondina, CEP 40170-290,
Salvador, Bahia, BRAZIL, Tel: +55 71 247-
3810 [[email protected]].
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
Olga Inés Cepeda Aponte, Laboratório de
Abelhas, 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 11 3091-
7533 [[email protected]].
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
Paulo De Marco Junior, Laboratório de
Ecologia Quantitativa, Centro de Ciências
Biológicas e da Saúde, Departamento de
Biologia Geral, Universidade Federal de
Viçosa (UFV), Centro, CEP 36571-000,
Viçosa, Minas Gerais, BRAZIL, Tel: +55 31
3899-1669 [[email protected]].
Paulo Nogueira Neto, Laboratório de
Abelhas, Departamento de Ecologia, Instituto
de 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
Participants I 15
Paulo Yoshio Kageyama, Diretor doPrograma Nacional de Conservação daBiodiversidade, Ministério do Meio Ambiente,Tel: +55 61 40099551,[[email protected]].
Peter G. Kevan, Department ofEnvironmental Biology, University of Guelph,Guelph, Ontario N1G 2W1, CANADA[[email protected]].
Peter K. Kwapong, Department ofBiological Science, University of Cape Coast,Cape Coast, GHANA[[email protected]].
Ricardo Costa Rodrigues de Camargo,Empresa Brasileira de Pesquisa Agropecuária(EMBRAPA Meio-Norte), Av. Duque de Caxias5650, Buenos Aires, Teresina, Piauí BRAZIL,Tel: +55 86 32251141 ramal 270 e fax 55 8632251142 [[email protected]]
Rogério Gribel, Departamento de Botânica,Instituto Nacional de Pesquisas da Amazônia(INPA-CPBO), Caixa Postal 478, Aleixo, CEP69011-970, Manaus, Amazonas, BRAZIL, Tel:+55 92 643-3112 [[email protected]].
Rui Carlos Peruquetti, Departamento deBiologia Geral, Universidade Federal deViçosa (UFV), Av. P.H. Rolfs, s/nº, CEP 36571-000, Viçosa, Minas Gerais, BRAZIL[[email protected]].
Simon G. Potts, Centre for Agri-Environmental Research (CAER), School ofAgriculture, Reading University, PO Box 237,Reading, RG6 6AR, UK, Tel: +44-118-378-6154 , Fax: +44-118-378-6067[[email protected]].
Tereza Cristina Giannini, Departamento deEcologia, 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 [[email protected]].
Terry Griswold, United States Department ofAgriculture (USDA), Bee Biology &Systematics Lab., Utah State University,Logan, Utah 84322-5310, USA, Tel: +01 435 797-2526[[email protected] / [email protected]].
Uma Partap, Pollination International Centrefor Integrated Mountain Development(ICIMOD), P.O Box 3226, Kathmandu, NEPAL,Tel: 09977-1-5525313, Fax 00977-1-5524509[[email protected]].
Valdemar Belchior Filho, Centro Brasileirode Apoio à Pequena e Média Empresa(CEBRAE), Rua Rui Barbosa nº 1, Centro, CEP59600-230, Mossoró, Rio Grande do Norte,BRAZIL, Tel: +55 84 315-4346[[email protected]].
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 - RibeirãoPreto, SP, BRAZIL, Tel: +55 16 36023815,[[email protected]], Laboratório deAbelhas, Departamento de Ecologia, Institutode Biociências da USP, Rua do Matão 321trav 14, Cidade Universitária, CEP 05508900,São Paulo, SP, BRAZIL, Tel: +55 11 30917533,[[email protected]].
Acronyms
API African Pollinators Initiative
ARS Agricultural Research Service
BPI Brazilian Pollinators Initiative
CBD Convention on Biological Diversity
CI Conservation International
COP Conference of the Parties
CRIA Reference Center on EnvironmentalInformation
EMBRAPA Brazilian Agricultural ResearchCorporation
EPI European Pollinators Initiative
EPUSP Polytechnic School, University of SãoPaulo
FAO Food and Agriculture Organization ofthe United Nations
FUSP São Paulo University Foundation
GBIF Global Biodiversity Information Facility
GEF Global Environmental Facility
ICIMOD International Centre for IntegratedMountain Development
INESP Internacional Network for Expertise inSustainable Pollination
INPA National Institute for AmazonianResearch
IPI International Pollinator Initiative
ITIS International Taxonomy InformationService
MMA Ministry of Environment
NAPI North American Pollinators Initiative
OREADES Brasilian NGO
PDF B Project Development Facility phase BSBSTTA Subsidiary Body on Scientific,Technical and Technological Advice
TDWG Taxonomic Database Working Group
UFC Federal University of Ceará
USDA United States Department ofAgriculture
USP University of São Paulo
16
Workshop preparation
In October 1998, São Paulo Workshop onSustainable Use of Pollinators for AgriculturalUse was held, and as a result from this meet-ing the São Paulo Declaration on Pollinatorswas constructed. It was submitted to theConvention of Biological Diversity (CBD), inits 5th Conference of Parties (COP), inNairobi, 2000, where the InternationalPollinators Initiative (IPI) was approved as anew program related to sustainable agricul-ture. Food and Agriculture Organization ofthe United Nations (FAO) was invited to be afacilitator of this process. In COP6 fromCBD, 2002, a plan of action for IPI wasapproved for guiding the actions of regionalpollinator initiatives, proposing goals to beattained in 10 years.
Meanwhile, regional efforts related to IPIdeveloped. In Brazil, several activities wereperformed, coordinated by a committee infor-mally established by the focal point in Ministryof Agriculture, in 2002, during the mainBrazilian meeting on bees (V Encontro sobreAbelhas, Ribeirão Preto). Among these activi-ties was the FAO proposal of a workshoprelated to discuss standardized methodologiesand assessment of best practices in agricul-ture to promote biodiversity in agro ecosys-tems. The title SP Declaration on Pollinators+5, for meeting to be realized in 2003, wassuggested by M. Ruggiero during a workshopin Mabula, Africa, and promptly accepted.
The preparation of this workshopfocused the awareness in the issue to the
potential participants of the BrazilianPollinator Initiative (BPI) program, in this ini-tial phase: scientific community in consoli-date and emergent groups, including herethe agricultural staff from EMBRAPA andother agronomic schools that could beengaged in this initiative. For discussing com-mon routes for the International PollinatorInitiative, we also invited the leaders of otheralready established Pollinator Initiatives, likethat of the International Centre for IntegratedMountain Development (ICIMOD): NorthAmerican, European, African, and Asian. InBrazil, EMBRAPA and bee researchers from allcountry (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 inSustainable Pollination (INESP) and FAO werealso organizations that were present. Federalgovernment ministries from Science andTechnology and Environment also gave theirsupport for this workshop, a counterpart toFAO support.
Taking advantage of the audience at theSP +5 Forum, a second workshop, PollinatorsInitiatives and The Role of IT: BuildingSynergism and Cooperation, was proposed todiscuss and disseminate the importance ofInformation Technology for the PollinatorInitiatives, to help to promote partnership andexchange experiences on the developmentand use of these technologies, and to discussfunding opportunities.
Presentation 17
Presentation
International PollinatorsInitiatives
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 public-private partnership of pollinators’ conserva-tion programs. Among the milestones of pol-linators programs are The ForgottenPollinators Campaign (1996), the São PauloDeclaration on Pollinators Conservation andSustainable Use (1998), the North AmericanPollinator Protection Campaign (NAPPC) in1999, the International Pollinator Initiative (IPI)in CBD (2000; 2002). This is a science-basedprogram, “a portfolio of programs, projectsand activities from the public and private sec-tor, connected by a spirit of cooperation”(Ruggiero, et al., 2004)
The European Pollinator Initiative (EPI) hasadopted the same framework of the IPI, thefour key components being: assessment, adap-tive management, capacity building and main-streaming. To assess pollinator loss, the ALARM(Assessing of LArge-scale Environmental Riskswith tested Methods) project was developed,combining the expertise of 54 partners from26 countries. This program started on February1st., 2004, and it is planned for 5 years initial-ly. In particular, risks arising from pollinators’loss in the context of current and future landuse in Europe will be assessed. SUPER (Sus -tainable Use of Pollinators as an EuropeanResource) will be built directly upon ALARM toaddress identified declines in European pollina-tors resources in a socially and economicallyviable manner (Potts, 2004).
The African Pollinator Initiative (API) wasestablished in 1999, as the African network ofthe IPI. “It strives to improve communicationchannels between all people and organizations
interested in pollinators and pollination biology,including biodiversity conservation, agricultureand general awareness, and to facilitate collec-tive achievements” (Eardley, et al., 2004). In2002, its first Secretariat was formed, and thePlan of Action of African Pollinator Initiativewas published. At this time, API comprisesGhana, Kenya and South Africa, but it is openfor other participants. A major need that existsin Africa is to identify the pollinators. Rapidassessments, taxonomic efforts and capacitybuilding are among the main needs.
ICIMOD initiated its pollinator/pollinationprogram in 1991, to address applied research,development and related issues of pollinatorsand pollination. The overall goal of ICIMOD isto improve the livelihood of mountain peopleby enhancing agricultural productivity andbiodiversity conservation through conserva-tion of indigenous pollinator species in orderto ensure sustainable pollination of crops andother indigenous plant species of the HinduKush-Himalayan region. Several activities arebeing undertaken concerning pollinators(Partap, 2004).
The Brazilian Pollinators Initiative (BPI) wasconstructed based on the São PauloDeclaration on Pollinators, which stimulatedinternational interest and provided strategicdirection for pollinator conservation planning(Dias, et al., 1998; Kevan and Imperatriz-Fonseca, 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 Pollinatorsfor Sustainable Agriculture Through anEcosystem Approach, with FAO as the facilita-tor. In this global scenario, with pollinators inmainstreaming in developed countries andalmost unknown in undeveloped countries, apartnership among scientists and stakeholderswill improve capacity building and sustainable
18
use of pollinators. As the general frameworkof IPI is adopted by all initiatives, including herestandardized methodologies for assessments,it was considered essential to join leadershipsto discuss goals, needs and opportunities. Forglobal comparisons, assessment methodsmust be standardized.
Methodological discussions
The talks were organized in order to give sup-port for the discussion on which standardmethodologies should be used in the develop-ment of the Brazilian Pollinator Initiative. Inoral presentations, several aspects of themethodologies applied until now in pollinationresearch and pollinators assessment were pre-sented by the specialists, showing how someimportant issues should be considered infuture actions. Subjects, such as the influenceof individual collector performance in assess-ment, methods to be applied in assessmentresearch, long-term and short-term evalua-tions, introduction and restoration of pollina-tors, performance evaluation in solitary polli-nators, meta analysis of data on plant-pollina-tor relationships, and priorities for pollinatorsprograms, 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 proto-col to be discussed during the workshop. Thegroups were directed to discuss the methods tobe standardized, and to suggest themes for thePDF B (Project Development Facility phase B ) ofthe GEF project. We needed to consider the
enormous task for some themes, which obvi-ously could not be concluded within a 5-dayworkshop. Some general comments follow.
The first group discussed assessmentmethods for pollinators’ status. Although theyadvanced in the analysis of different methods,the task was not concluded. The main meth-ods to be applied were pointed out, but onlyindications for the manual of standard meth-ods were made. Coordinators answered theproposed questions, gave orientation for casestudies and suggested the next steps in thePDF B of the GEF project.
The gene flow group presented a conclu-sive report. They also indicated the chosenmethods to be used for different purposes,without describing them. Gene flow studiesmust 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, divid-ed 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 pollinatorsbecause they are abundant, easy to breed andto manage in crops. Honey bees were focusedon for crop pollination in the importantMcGregor’s book, Insect pollination of cultivat-ed crop plants, still very useful and updated online. However, Brazil has the Africanized honeybee, which requires special management prac-tices, and knowledge related to their perform-ance as pollinators. In fact, they are quiteeffective in pollination, as Roubik (2002) point-ed out for coffee production in Panama, andas Couto (2002) discussed for several crops.The honey bees study group presented a verycomprehensive report, with valuable sugges-tions and guidelines for further applications ofbees as pollinators. Pollination by honey beescould be much improved by technology
Presentation 19
advances in management, nutrition, patholo-gy and mechanization, especially for transportto pollination sites. Farmers need to be madeaware of the benefits of incorporating pollina-tion into their management practices
Brazil has only seven species of bumble-bees (Bombus); nevertheless they are abun-dant all over the country. They are generallyvery aggressive, and are not reared for pollina-tion purposes in Brazil. The carpenter bee,Xylocopa, can be reared and is a good pollina-tor of passion fruit, among other crops. Thereare 49 species of carpenter bees in Brazil(Silveira, et al., 2002) that are potentiallyimportant in agriculture. The solitary beesmanagement group did a very comprehensivereport, presented the main plants that shouldbenefit 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 iseffective for some species (see Heard, 1999;Malagodi-Braga, et al., 2000), but they are notbred on a large scale to be available for agri-cultural purposes. They have a high potentialfor the use as pollinators: they are diverse,have perennial nests, are generalists, but alsoshow floral preferences (Ramalho, et al., 1990;Biesmeijer, et al., 2005), they communicate flo-ral resources to nestmates, they do not sting,and they store food inside the nests. The useand conservation of stingless bees was dis-cussed by this group, and next steps for relat-ed activities suggested.
It is important to point out that if fundingis not available to develop bee biology projectsand to improve the local knowledge and for
capacity building concerning the other beespecies, Africanized honey bees will soon bethe only available pollinators in sufficientquantity for agricultural use in our country.Loss of habitat and increasingly intense agri-cultural practices are clearly reducing thenative bee populations. Introduced into theAmericas, honey bees are generalists and inmost cases less effective for biodiversity con-servancy. The result will be a drastic loss inplant biodiversity and in agricultural produc-tion, especially in the more tropical regions.
Information Technology andthe Pollinators Initiatives
For this one-day workshop, held during thelast day of the SP+5 Forum, speakers repre-senting the various Pollinators Initiatives pres-ent were invited. Other presentations focusedon local initiatives: the Brazilian PollinatorsInitiative and local projects that make a stronguse of Information Technology (IT) and arerelated to pollinators. The speakers were askedto give a short presentation focusing on howIT is used presently and how, in their ownpoint of view, it might contribute for theadvancement of the national, regional andinternational Pollinators Initiatives. Some timewas allowed for discussions on issues such astechnology and data sharing, systems integra-tion and also funding needs and strategies.
Workshop results, as well as the oral presenta-tions, are on line at http://www.webbee.org.br.
20
References
BIESMEIJER, J.C.; SLAA, J.; CASTRO, M.S.; VIANA, B. F.; KLEINERT, A. M. P. & IMPERATRIZ-FONSECA, 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 abe -lhas, 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 Workshopon 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 August29th 2004.
IMPERATRIZ-FONSECA, V.L; FREITAS, B.M.; SARAIVA, A.M. & DIAS, B.F.S. 2004. The BrazilianPollinator Initiative: Challenges and opportunities. In: Annals of the 8th IBRA InternationalConference 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 linkbetween agriculture and nature. Brasília, Ministério do Meio Ambiente, 313pp. Available athttp://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 Kush-Himalayan Region. In: FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearingand 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 pol-lination. Fortaleza, Imprensa Universitária, p. 43-55.
RAMALHO, M.; KLEINERT-GIOVANNINI, A. & IMPERATRIZ-FONSECA, V. L. 1990. Important beeplants for stingless bees (Melipona and Trigonini) and Africanized honey bees (Apis mellifera) inneotropical habitats: a review. Apidologie, 21:. 469-488
Presentation 21
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 Agricultureand 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 pol-lination. 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 InternationalConference on Tropical Beekeeping and VI Encontro sobre Abelhas, Ribeirão Preto, inCDROM.
SILVEIRA, F. A.; MELO, G.A.R. & ALMEIDA, E.A.B. 2002. Abelhas brasileiras, sistemática e iden-tificação. Belo Horizonte, 253pp.
22
WORKSHOP I
Survey methods for bees as pollinators in Brazil:assessing the status and suggesting best practices
Participants: Cynthia Pinheiro Machado (Coordinator), Fernando A.Silveira (Coordinator), Patricia Albuquerque, Jacobus Biesmeijer, MariaJosé de Oliveira Campos, Connal Eardley, Barbara Gemmill, TerryGriswold, 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 prac-tically no information about pollinator fauna,three strategies for pollinator investigationwere addressed: 1) rapid assessments; 2) sur-veys and 3) monitoring programs. Theexpected product was a manual for standardmethodologies for bee surveys and monitor-ing in natural landscapes and cultivatedfields. Some basic principles were observed:data must be reliable and adequate for statis-tical analyses, and all suggested strategieswere to be realistic, considering time, person-nel and costs constraints, and flexible enoughto be applied in different environments.Surveys should be question oriented. Itbecame obvious that no rigid protocol couldbe built for all situations across the world,then only general guidelines, not protocols,were suggested in order to meet the basicprinciples listed above. Since no comparative
data exist in those methodologies, no con-sensus was reached on which methods torecommend for given situations, but compar-ative data should be sought for before anydefinitive recommendations can be built inthe context of the Brazilian PollinatorInitiative. Three case studies, in a cotton field,in the Atlantic Forest and in open savanna,illustrate how recommendations could beused in the development of survey and mon-itoring protocols.
Aim
Establishment of standard methodologies forbee surveys and monitoring of natural land-scapes and crops.
Expected Product
Production of a manual of standard method-ologies for bee surveys and monitoring of nat-ural landscapes and cultivated fields.
Workshop I 25
Group 1Surveying and monitoring of pollinators innatural landscapes and in cultivated fields
The pollination crisis and the need for surveys and monitoring programs
The impact of deforestation, habitat fragmenta-tion, introduction of exotic species andunfriendly agricultural practices is believed to becausing a decrease in wild pollinator popula-tions. This, in turn, is suspected to be the causeof low fruit and seed productivity in many cropplants, with economic consequences in manyparts of the world. Also the productivity of wildplants may be affected, and this can lead tolocal extinction of populations of those plants,as well as of the animals depending on them.
Since this “pollination crisis” was recog-nized, much effort has been put into initiativesto conserve and sustainably use wild pollina-tors. However, it is widely recognized that welack much of the knowledge we need to pro-pose 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 dif-ferent factors affect wild populations of flowervisiting organisms.
Two basic questions stand out as being ofsurmount importance for any conservation orsustainable management initiative to succeed:1) which pollinator species exist in any givenplace? 2) how are their populations fluctuatingalong time?
For these questions to be answered, weneed to invest in pollinator faunistic surveysand in monitoring programs.
Results
The group discussed the general structure ofstandard procedures to survey and monitorbees 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 beuseful for other initiatives around the world.
• As there are countries and regions with prac-tically no information about pollinator fauna,three strategies for pollinator investigationwere addressed: 1) rapid assessments; 2) sur-veys and 3) monitoring programs.
Recommendations
Basic principlesThe 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 and
costs constraints.• Be flexible enough to be applied in different
environments.• Be question oriented.
DifficultiesMembers of the group suggested and discussedvarious methods in use across the world.Different people had different experiences withdifferent methods. For example, some had verygood results in using pan traps for collectingbees, while others obtained meager data fromtheir use. Such differences could be due to dif-ferent designs, different environmental condi-tions, etc. It became obvious that no rigid pro-tocol could be built that could be recommend-ed for all situations across the world; even with-in Brazil; the group was not able to decide onspecific methods to be employed, due to thevarying opinions on their efficiency.
Thus, it was decided that only generalguidelines would be built, so that dataobtained from surveys and monitoring pro-grams, using any combination of the suggest-
26
ed methods, would meet the basic principleslisted above. It was hoped that further com-parison of the different methodologies wouldenable sound choice of methods in the future.
Considering the difficulties exposedabove, the following recommendations shouldbe accepted as guidelines, not protocols, inorder to assure their applicability.
Workshop I 27
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, in order 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: trapnesting; 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 taxo-nomic keys and reference collections. Those responsible for identifications should be contactedin advance. Manuals should include information on national collections and taxonomy services.
Aims
To obtain the best estimate of local fauna and bee plant relationships, in order to allow for compari-son 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 post collection analysis based on numbers per plant, per hour, per species, and any 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 condi-tions 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 designshould 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: trapnesting; 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 taxonom-ic keys and reference collections. Those responsible for identifications should be contacted inadvance. Manuals should include information on national collection and taxonomy services.
28
Monitoring
Aims
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 for further studies.
Type of data
Species records Species can be counted or collected, depending on the facility of identification and objective of the program.
Species Abundance Number of individuals must be recorded in a manner that allows post collection analysis based on numbers per plant, per hour, per species, and any 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 condi-tions 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 designshould 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: trapnesting; 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.
Workshop I 29
Final Remarks
It was obvious that no fixed protocol could beprovided for all situations. Moreover, differentpeople had different experiences with differ-ent sampling methods. Since no comparativedata exist on those methodologies, no consen-sus was reached on which methods to recom-mend for given situations. Thus, such compar-ative data should be sought for before anydefinitive recommendations can be built in thecontext of the Brazilian Pollinator Initiative.
Case Studies – an exercise
AimTo provide examples of how the above recom-mendations could be used in the developmentof survey and monitoring protocols.
The group was divided into three sub-groups, each of which worked on one casestudy. The resulting protocols presented belowwere constructed based upon literature infor-mation and the expertise of group members,with surveys and monitoring of bees on specif-ic crops and in different kinds of environmentstaken as examples.
1) MONITORING FLOWER-VISITING BEESIN COTTON FIELDS
BackgroundAccording to Barroso & Freire (2003), threespecies 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. hir-sutum are currently cultivated on a commercialscale in Brazil. However, cultivation systems arenot homogeneous across the large cotton-pro-ducing regions of Brazil. An evident contrastexists, for example, between the small-scaleproduction found in the small family-heldfarms in the northeastern region of Brazil,which employ a low technology crop system,and the large scale production systememployed in the huge commercial farms incentral Brazil.
The cotton plant can produce nectar infive different kinds of nectaries distributedinside and outside the flower. However, not allof these nectaries occur in every cultivar (Free,1970; McGregor, 1976). Many differentorganisms are attracted to the cotton flowerby the nectar and pollen it produces. Amongthese, insects and especially bees are the mostabundant. These flower-visiting species maycontribute to increases in fiber productionand/or quality (Free, 1970; McGregor, 1976).
The suggestions below were constructedconsidering a small-scale system. Considerationson how to expand this protocol to a large-scale, high-technology system are presented atthe end of this exercise.
SurveyThe survey of cotton-flower visiting species isproposed for 1 ha fields, considered here assampling units. This is an average size field forcotton in Northeastern Brazil. In each suchsampling unit, two sampling procedureswould be executed in parallel:
A) Arbitrary sampling. This protocolaims to maximize the number of flower visit-
30
Observations: Species identification should be made by trained people, with the aid of taxonom-ic keys and reference collections. Those responsible for identifications should be contacted inadvance. Manuals should include information on national collection and taxonomy services.
ing species recorded on cotton plants. Thefield is slowly inspected and all bees found onthe cotton flowers or flying above them arecollected. It is important to call attention tothe fact that the deep corolla of the cotton-flower makes the use of hand nets relativelyinefficient, as the flower protects the visitinginsects. For this reason, complementary cap-ture methods are suggested: forceps, insectaspirators and hand nets, depending on thesize and position of the bees.
B) Systematic sampling. This protocolaims to quantify the relative density and abun-dance of flower-visiting species. Sampling is tobe done weekly in 10 plots, each including 80cotton plants, 20 in each of four neighboringrows. Those plots should be homogeneouslydistributed across the field, including areasclose to its border and center. Areas close topatches of natural vegetation and other spe-cial environments around the field also shouldbe considered. Each plot is sampled for 10 minby slowly walking between the rows. Any beesfound inside the flowers and on extra floralnectaries will be collected.
Both sampling procedures should be exe-cuted weekly, between 8:00 and 12:00, alongthe flowering season. Sampling should bedone preferably during sunny days, when beesare most active at flowers. Any cultivationpractice proceeded between and on samplingdays should be recorded.
Monitoring Monitoring can be done by repeating yearlythe systematic sampling procedure describedabove. In this way, average abundance of thewhole flower-visiting assemblage and of tar-get species can be compared between yearsand along longer periods. These numbers canalso be associated with factors such as cli-matic parameters and the amount of pesti-cide 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 explainedabove. Such sampling units should be homo-geneously distributed inside the cotton fields,the number of such units being proportionalto the size of the fields, with some of themclose to the borders and others within the inte-rior of the fields.
2) BEE SURVEYS AND MONITORING OF A FRAGMENTED LANDSCAPE IN THEATLANTIC RAIN FOREST BIOME
BackgroundThe Atlantic Tropical Rain Forest is a recognizedbiodiversity hot spot. Its original vegetationcover has been reduced to 8%, and what is leftis threatened by human presence. Populationgrowth has led to destruction of the forestthrough uncontrolled urban expansion, indus-trialization and migration of people from otherareas (Galindo –Leal & Câmara 2003). About100 million people live in the mega cities locat-ed in the Atlantic Forest Region, along with thelargest industrial and silvicultural centers. Onthe other hand, the biodiversity harbored by theAtlantic Forest is one of the greatest in theworld. We believe that 60% of the terrestrialspecies of the planet live within the remainingareas of this forest. This is probably a result ofthe 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 highlystratified, with a canopy as high as 35 meters.
SurveyPollinator surveys should be made along tran-sects. The determination of size, placement andnumber of transects will depend on the hetero-
Workshop I 31
geneity of the forest community, which shouldbe understood beforehand. The size of the tran-sects should be such that they can be coveredin one day. They should be 100 m long.
The sampling units will be floweringplants, with all bees found being collected atall the flowering plants that they visit. Handnets will be the principal collection methodand will be complemented by euglossine baits.Additional methods such as pan, malaise andlight traps and also new baits such assalt/ammonia and antifreeze should be tried.
Sampling should be repeated 3 to 5 timesa month for 8 to 12 months per year, depend-ing on flowering phenology and flower density.
Monitoring The goal of the suggested monitoring pro-gram is to detect differences in bee diversity indisturbed and undisturbed forests over time. Itcould also be used to compare differentdegrees of disturbance.
Sampling units are similar to those used inthe survey. Monitoring subjects may be select-ed, 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 beidentified. Still other subjects could be consid-ered, such as Apis mellifera, trap-nestingCentris 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 AMONITORING PROGRAM TO EVALUATETHE IMPACT OF GRAZING ON FLOWERVISITORS´ RICHNESS
Background The biome of the Cerrado is a gradient of veg-etation physiognomies, including open fields,savannas and open-canopy forests. It coversabout 25% of the Brazilian territory and wasincluded among the world’s hotspots (Myers,et al. 2000), for combining high biodiversityand high rates of disturbance. Until 40 yearsago the Cerrado was primarily used for exten-sive cattle raising. By 1988 Klink & Moreira(2002) estimated that 35% of the naturalcover had already been removed. In a recentstudy, using MODIS satellite images of 2002,(Machado, et al.,2004) concluded that the na -tural 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 cottonare the major threats for the biome, causingsoil loss, water pollution, habitat loss, habitatfragmentation, introduction and spread ofvery agressive invasive species, like Africangrasses, among others (Buschbacher, 2000;Fearnside, 2001; Klink & Machado, 2005).Forecast is not optimistic, according to Ma -chado, et al. (2004), based on present vegeta-tion removal rates by 2030 the whole biomemay have given place to agricultural and cattleraising activities.
Major impacts on pollinators are appar-ently caused by intense use of chemicals, aeri-al spraying, and habitat removal; the latterprovokes reduced nesting opportunities andfood availability.
According to Silberbauer-Gottesbergerand Eiten (1987), the plant species richness ofthe Cerrado open areas is among the highestknown for non-forest vegetation. Seasons arevery well defined. The dry season lasts from 3to 5 months, during winter, and the wet sea-son peaks in December-January. Flowerresource availability varies through the seasons
32
(Oliveira & Gibbs, 2002), but flowers are foundthroughout the year (Batalha, 1997). Bee sur-veys in the Cerrado area have been carried outin Central Brazil, around Brasília, in MinasGerais State, in the Northeast and in someperipheral areas in São Paulo state (Pinheiro-Machado et al., 2002), allowing for a baselinedata set for native fauna.
SurveyThe Cerrado vegetation is a natural mosaic,with many vegetation types, varying from opengrass fields to dry forests. Therefore a previousanalysis of the sampling area has to be donebefore designing the survey. The following stepscan 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 satelliteimages 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 diversityand sampling effort necessary to bestdescribe the focal fauna. Some calculationsinvolving sampling curves in a standardizedway with previous data may be necessary;the studies should indicate period of activity,both seasonally and daily.
4.Visits to collections will produce a betterspecies list and expected richness numbers,because collections are believed to includemany unpublished data.
5.Local evaluations prior to the surveys pro-vides familiarization with flora and allowsidentification of potential plant species for atarget survey. This may be crucial, especiallyin the case of very short budgets. Simplethings 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 speciesintensively visited by bees.
6.Although Brazilian researchers use hand net-ting as the main technique for sampling bees,examination of previously published studiesthat have used other methods can indicatewhat part of the community is not beingsampled if hand netting is the only technique.
7.Plan the type of analyses that will be carriedout and assure that the experimental designwill provide proper data.
8.Sampling area should be marked at the field.
Site selection must be guided by the ques-tion proposed for the survey. The chosen sitemust be representative of the environmental sit-uation to be investigated. If a unique type ofvegetation or physiognomy is targeted, an eval-uation will need to be made to determine if thechosen site adequately represents the situationto be surveyed. This also applies when gradientsor mosaics are the case. Replication and controlareas are important parts of some surveys andhave to be considered during site selection.
Another very important point is the acces-sibility of the site and all the permits thatshould be obtained, both from privatelandowners and governmental agencies.
Sampling design and sampling techniques Sampling design involves choices of samplingunit format, size, number and spatial distribu-tion. For instance, if an overview of diversity inthe area is the aim, sampling units will be needto be randomly distributed; if diversity infor-mation is to be linked to habitat, samplingunits should be selected in a way that theyrepresent all desired situations (Alonso &Agosti, 2000). The sampling design has toconsider areas greater than 2 ha because ofthe typical spatial distribution of plants in theCerrado. At least 10 transects 2 m wide by 1km long, or 5 quadrats of 40x100m, should be
Workshop I 33
established. The method should be calibratedagainst known areas by follow-up proceduresusing species accumulation curves (Soberón &Llorente, 1993) to inform about the efficiencyof the chosen design and techniques. Speciesaccumulation curves are produced fromspecies-by-sample matrices in a spreadsheet,and they can be carried out by the EstimateSprogram (Colwell, 1997).
Sampling techniques that minimize thecollectors’ interference are preferred, but thebest results in Brazil have so far been achievedusing hand nets. To minimize differencesamong collectors, previous training is manda-tory. Different species have different behavioursat flowers; some of them can be very fast andsensitive to movement. Collectors must beadvised 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 net-tingand sweep netting in transects. Althoughpan traps have not had good acceptanceamong Brazilian researchers, good results andnew fluorescent colors reported from othercountries speak for its use. Pan traps tend tobe selective for certain groups, so they shouldnot be used as the only technique for invento-ries. The best method may vary according tosite and logistics, but best results in speciesnumbers are usually achieved when multiplemethods are applied.
The length of the transect needs to bestandardized, but it will depend on the aim ofthe survey, as discussed above. If the transectis divided into sub samples, these should bekept separated for posterior analyses. Thestarting point of the transect should be pickedat random, in order to avoid always collectingduring the peak activity period at the samepart of the transect. One needs to be sure thatthe peak activity period is always covered by
sampling effort. Collectors should also be ran-domized along sites to minimize bias from col-lecting ability.
Complementary data is very important fordata analysis, so a protocol should be appliedto every survey. Recommended data to begathered are the following: • site location with coordinates; use a GPS; if
this is not available, report local geographicreferences 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 character-istics of the landscape in which is it situated;
• the size of the total area from which sam-ples are taken must be indicated, becauseresults are expected to vary if collecting sitesare a part of a 1 ha, a 100 ha or a larger areaof Cerrado;
• general climate description and classificationare very useful and must be complementedwith local weather conditions during the col-lection days and information about averagetemperature and rainfall whenever possible.
Floral associations are important comple-mentary 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 vari-ous insects into each vial. All material is to belabeled in advance allowing quick field infor-mation to be made promptly.
After fieldwork some procedures are rec-ommended that will make data easy to ana-lyze for anyone interested: • standardize the format of data presentation
and codes to facilitate understanding at allinstances of the study;
34
• present results by simple summary descrip-tors, like species richness, and common andpopular diversity indices;
• feed data bases that provide access to thegeneral pubic; indicate the collection wherevoucher material was deposited.
MonitoringThe proposed exercise for this group was togive directions for monitoring the impact ofcattle raising activities on the biodiversity ofpollinators. The group started with the state-ment of the leading question: What is theimpact of introducing cattle “on pollinators”?
To address this question, previous dataabout bees and their relationship with flowersof open areas will be gathered. This informa-tion will be used to choose focal groups formonitoring activities. Preference will be givento bees sensitive to gradients that are in thiscase understood to range from original non-grazed areas to heavily grazed areas. If prelim-inary 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 correla-tion with desired variables, like bee diversity.Once a strong and significant statistical rela-tionship is found, collections will be repeatedthrough time. The sampling design is the sameone proposed for the survey, but will berepeated through time.
HOW DATA FROM MONITORING WILL BEUSED IN THE CONTEXT OF BPI?
Monitoring depends on the choice of soundand easy to measure variables. Variable selec-tion can be made based upon previous data. Itis recommended that a selected taxa or a guildis used for monitoring, but the relationshipbetween the measured variable and the object
of monitoring should be understood and sup-ported by a strong significant positive correla-tion. Direct relationships are preferred. If therelation between the measured variable andthe object of monitoring is not already known,assumptions must be stated clearly at thebeginning of the monitoring program. Theselection of a specific taxa or guild must takeinto consideration the characteristic that thefocal organisms are abundant and easy to iden-tify. A previous survey is mandatory for areaswhere data is lacking, to improve the chance ofchoosing good taxa to be monitored.
Some general recommendations couldbe made for all situations involving polli-nator surveys and monitoring: Training. One problem raised about the useof “manual” collection methods, such ashand-netting is the effect of different abilitiesof different people to find and capture bees.This problem can be reduced by properly train-ing collectors before actual sampling is begun.
Replication. An appropriate number ofreplicates should be set, according to environ-ment heterogeneity and/or other importantfactors. Pseudo-replication should be avoided.For instance, 12 monthly samples collected atone site cannot be considered as replicationsof different disturbance grades or environmenttypes. 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 identifica-tion should preferably be done by experiencedpersonnel. Moreover, voucher specimens of alltaxa involved should be deposited in publiccollections that should be indicated in reportsand publications, so that their identificationcan be checked at any time.
Workshop I 35
Final remark
The group was composed of a number ofresearchers with experience in bee surveysand monitoring. However, the members haddifferent thoughts about the different meth-ods. In part, this may be a consequence of theeffect of different environments (includingcomposition of regional bee fauna) on sam-
pling methods. Consequently, methods thatwere reported by some as very efficient, didnot produce good results in other places,when used by other people. It was suggestedthat experiments (like those going on underthe auspices of the European PollinatorInitiative) should be made on a regional scale,so that a final choice of methods can be madefor each region.
36
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 doPassa 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: origenshistóricas 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 speciesfrom 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. EnvironmentalConservation, 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: biodiversitystatus, 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.
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. Biodiversityhotspots for conservation priorities. Nature, 402: 853:858.
OLIVEIRA, P.E. & GIBBS, P. 2002. Pollination and reproductive biology in Cerrado plant communi-ties In: Oliveira, P.S. & Marquis, R. J. The Cerrado of Brazil. Ecology and natural history of aNeotropical 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: AnIntroduction. In: Galindo-Leal, C. & Câmara, G. I. The Atlantic Forest of South America: biodi-versity 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 37
Abstract
This group discussed the interaction betweenplant and pollinator, emphasizing the impor-tance not only of pollination, but also of goodagricultural, forest management, and conser-vation practices for sustainable development.The group was comprised of researcherswhose areas of expertise encompass floralbiology, plant breeding systems, plant popula-tion genetics, and pollination of tropicalplants. The recommendations made below areintended to contribute to future discussionsregarding the Brazilian Pollinator Initiative(BPI), although some of them are generalenough to be considered more broadly.Emphasis was given to recommendationsother than methods, since there is a vast liter-ature available (including FAO publications) onthe above-mentioned subjects.
Pollen-mediated gene flow in plants isaffected by abiotic agents, such as wind, and anumber of biotic agents, of which the singlemost important pollinator group worldwide isthe 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 speciesdepends directly on these agents in the major-ity of plants, and very often in commercially-important ones. Exceptions are self-fertilizingplants, but even these frequently benefit fromcross-pollination provided by these agents.Traditional selective breeding of plants, habitatfragmentation and overexploitation of naturalstands are currently narrowing the geneticbase, and are leading to genetic erosion of eco-nomically important plants. In addition, genet-ically modified varieties resistant to herbicidesor pesticides could create potential "super-weeds" through pollen-mediated gene flow.
Among the methods proposed to helpperform the recommendations, rapid assess-ment protocols (RAP) are suggested, for thecollection of data on bee behaviour, pollinationsyndromes and landscape diagnosis. Theseprotocols allow data collection in the field bypeople with little or no formal biological train-ing. Other methods, including statistical andgenetic analyses, require both expertise andspecific facilities, and will usually be performedby researchers and trained personnel.
Workshop I 39
Group 2Assessment of Pollinator – Mediated Gene Flow
Participants: Claudia Maria Jacobi (coordinator), Edivani VillaronFranceschinelli, Rogério Gribel, Peter G. Kevan, Alfred Ochieng, Eda FláviaLotufo Rodrigues Alves Patrício, David W. Roubik.
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 asrapid assessment protocols, experimentaldesing for testing breeding systems and mon-itoring methods, making use of case studiesas exemples.
To produce a list of recommendations forthe gene flow assessment and managementof plant species regarding containment meas-ures or enhanced productivity.
This working group focused on the assess-ment of pollinator-mediated gene flow of eco-nomically important plant species.
Discussion
The discussions occured in two sessions; oneon monitoring of flower visitor behaviour,morning October 29th; other on pollinationrequirements and on apllied issues in pollina-tor gene flow, afternoon October 29th.
The goals were to discuss ways of pro-ducing a database containg comparativebehaviour of visitors in different plant specieswithin an area; how to produce a list ofimportant plant species and their pollinatorrequerements, including their breeding sys-tem, pollination syndrome, and resourceoffer; and how to increase awareness/knowl-edge of mechanisms for containment meas-ure or enhanced productivity for selectedplant species.
The questions guiding those discussonswere:
• How to adapt the observational methodsproposed to different plant habits and mor-phologies, 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 applica-tion of the RAP with a minimum of mistakes?
• Will it be feasible to recommend pollencontainment measures based on this infor-mation?
• How to determine the need to assess geneescape (ex. in the case of unwantedhybridization between crop varieties andwild relatives, or related contaminationproblems concerning GMOs)?
• Should recommendations be made on acase-by-case basis, or could we generalizepart of them?
In order to orientate the discussions a listof general guideline of method were drew:• Observations of bee behaviour on the
flower/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 fol-low nearest neighbour pollination rules(optimal foraging)? Is there along-rowbehaviour? Is there flower constancy? Howto estimate carryover?
• Energy economics of foraging: measuretemperature, wind, RH.
• Creation of user-friendly protocols for beebehaviour assessment and comparison.
• Application of simple statistics to determinepollen shadow.
• Standard methodology to test for breedingsystem (includes bagging, hand pollination
and emasculation, followed by fruit/seedset), adapted to each case.
• Creation of user-friendly protocols for breed-ing system assessment.
• Application of simple statistics to analyseresults.
• Estimates of gene flow through geneticmarkers compared with estimates of pollentransport (see above).
• Estimates of pollen shadow with dyes.• Comparison of crop productivity under dif-
ferent pollinator regimes.• Selection and discussion of case studies (e.g.
cotton).
Results
Pollinator mediated gene flowPollen-mediated gene flow in plants isaffected 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 polli-nator populations are probably sufferingnowadays from stress resulting from habitatloss, parasites, insecticides, and misunder-standing by the general public. Meanwhile,the need for their services in natural, agri-cultural and agroforestry systems is growingday by day. In the tropics, pollination isaffected not only by bees (natives and intro-duced Apis), but also by less known ani-mals, whose service is poorly understood bythe general public. Among these, bats areparticularly important because they polli-nate several species of fruit trees, while bee-tles and flies are responsible for high yields inpalms. With such a variety of pollinatorspecies and of plants that need animal polli-nation, it is important that the characteristicsthat affect gene flow are well understood for
each pollinator and likewise the plants thatthey pollinate.
The pollinator requirements of a plantspecies depend on its breeding system.Standard methods to test for self-fertility andself-pollination are among the first featuresassessed when evaluating the need for polli-nators. Other usual procedures allow us toevaluate if a flower visitor is an effective polli-nator. When focusing on gene flow, severaltechniques have been tested to assess how farcan pollen go from a focal plant of group ofplants. This latter parameter involves knowl-edge of the amount of pollen harvested froma flower, flight range, and resource distribu-tion, 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 pol-linator's fidelity to a given plant species, andof the type of resource it is being visited for.Finally, commercial parameters that increasecrop value are usually taken into account tocompare differences in yield among differentpollination regimes.
The understanding of pollinator behaviourwith respect to each plant species is vital notonly to establish adequate agricultural actionsthat increase yield, but also to adopt measuresthat lead to sustainability. Among these areactions to reduce genetic loss in forest speciesdue to isolation, to determine levels of isolationor contamination of crops, to prevent invasive-ness 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 tropi-cal plant species (Roubik, 1995), only a smallpercentage of plants, be they wild or cultivat-ed, have undergone comprehensive studies,and most of the gene flow data which are
Workshop I 41
needed to support conservation and manage-ment initiatives are still lacking.
Importance of pollinator-mediated geneflow in crop management and silviculture Pollinator services have been traditionally con-sidered expendable in many crops. However,case studies have shown that yield is significant-ly improved when pollinators are introduced.Such is the case for coffee (Roubik, 2002), andvarious crops in Brazil (cited in a recent survey byCouto, 2002): passion fruit, red pepper, straw-berry and orange. Possibly, many others, such assunflower and soybean, will also showincreased 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 usu-ally enhances crop performance, when evaluat-ed by commercial parameters. For example,cashew (Anacardium occidentale), which is par-tially self-fertile, requires a high rate of visitationto obtain good nut yields, since most of thefruits derive from cross-pollination (Holanda-Neto, et al., 2002). The introduction of beema na gement to increase yield in crops shouldbe carefully evaluated case by case, since addi-tional costs are involved.
On the other hand, alleged low productiv-ity of some cultivated plants may simply be theresult of incorrect agricultural practices thathave led to low genetic diversity of crop or for-est stands. Poor fruit and seed production canbe the result of inbreeding, not a lack of polli-nators. The common practice of plantationsbased on seeds from very few trees or evenclonal orchards should be analyzed carefullysince this may lead to genetic erosion, low pro-ductivity and inbreeding depression. It is possi-ble that premature fruit drop in cashew is alsorelated to genetic causes.
Current practices of natural standexploitation for timber, pharmaceuticals, rub-
ber, fruit, seeds, and dyes may be reducinggenetic variability and gene flow to levelsthat permanently affect the viability of popu-lations. Some studies from Brazilian econom-ically important species are available. Recentdata (Peres, et al., 2003) from 23 populationsthroughout the Brazilian, Bolivian andPeruvian Amazon have shown that the his-torical levels of exploitation of Brazil nuts(Bertholletia excelsa, Lecythidaceae) have amajor impact on recruitment into naturalpopulations. Populations subjected to moder-ate and high levels of harvest over manydecades lack juvenile trees; in contrast, onlypopulations with a history of light, recent orno exploitation contain large numbers ofjuvenile trees.
At present, there are still few laboratoriesin Brazil (governmental or private) that areinvolved in genetic studies of native plant pop-ulations. We are hopeful that this situation willbe resolved in future years, since many labora-tories are nowadays well equipped and theirpersonnel already prepared for this task.
Habitat fragmentation and reduction ofgenetic diversity Some Brazilian biomes have undergone exten-sive clearing in the past decades, notably foragricultural purposes. This has resulted in theinclusion of the Cerrado (savanna) in the latestlist of "hotspots" (threatened world regionsthat should be given priority in biodiversityprograms). This biome is home to several com-mercially important plant species that areintensively used by local populations.
A typical case of plant populationsalready suffering from habitat fragmentationis that of Caryocar (Caryocaraceae) species.The piqui (C. brasiliense) from the CentralBrazil Cerrado vegetation, and the piquiá (C.villosum) from the Amazonian forest, yield
42
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 thepopulations of these sensitive pollinators.Genetic data for C. brasiliense from 10microsatellite loci indicated a high level ofbiparental inbreeding, which could be attrib-uted to the limited flight range of its pollina-tors and restricted seed dispersal. Habitatfragmentation would isolate populations andtheir pollinators, aggravating the scenario offruit overexploitation (Collevatti, et al., 2001).In the case of mahogany (Swietenia macro-phylla, Meliaceae), the most valuable neotrop-ical timber species, habitat degradationcaused by selective logging and, most impor-tantly, by conversion of forest into soybeanplantations and cattle ranch pastures withrecurrent use of fire, have clearly reduced localpopulation sizes and have led many popula-tions to local extinction (Grogan, 2001).Recent studies using polymorphic microsatel-lite markers (Lemes, et al., 2003) suggest thatthe small, isolated, remnant populations maynot constitute viable units in the long term,owing to the loss of genetic variation causedby genetic drift and inbreeding.
Brazilian legislation has contemplated thehabitat loss problem by establishing, amongother protection measures, that a percentageof uncultivated land be maintained in privateproperties (known as reserva legal) in Brazilianbiomes such as the Amazon forest and Cer -rado. These areas are important both to sus-tain ecological services such as pollination, andto maintain gene flow and diversity of nativeplant species by behaving as corridorsbetween fragments. There is, however, intensedebate nowadays concerning the reduction ofthose percentages. Attempts to change the
law decreasing the proportion of thesereserves should be contested with scientificand economic arguments. In addition to habi-tat preservation, habitat rehabilitation pro-grams might benefit from the introductionand management of pollen and seed dis-persers. This action is a cheap alternative thatcould increase gene flow among fragmentsand accelerate rehabilitation.
Pollinator-mediated genetic contamination It is known that crops easily hybridize with wildrelatives (Ellstrand, et al., 1999). The visitingpatterns of pollinator forage can create crop-to-wild and crop-to-crop pollen exchange. Ifgenetically modified varieties (GMO) areinvolved, there is the risk that non-targetplants (wild relatives or conventional crop vari-eties) acquire the characteristics of resistanceto herbicides or pesticides through pollen-mediated gene flow and turn into unmanage-able weeds (the so-called "superweeds"). Theoccurrence of agricultural weeds from GMOcrop releases has already been reported. InCanada, the presence of unwanted herbicide-resistant canola (Brassica napus, which is beepollinated) is becoming an agricultural nui-sance (Simard, et al., 2002).
Other genetically engineered varieties(modified to resist attack by insects), such assunflower (Helianthus anuus, which is bee pol-linated), and papaya (Carica papaya, pollinatedby bees, birds and moths) have also shownenhanced fitness. They are less attacked byinsects (moths) and in turn produce more seedsthat are themselves more resistant to insectattack. This suggests that non-managed popu-lations may in turn accelerate development ofresistant insect pests. It is evident that to main-tain the utility of herbicides and pesticides inagriculture (i.e., to reduce the risk of hasteningthe development of superweeds), modifications
Workshop I 43
in agricultural practices, which include herbicidemanagement (such as rotation and combina-tion with other actions), are mandatory.
Existing containment measures are mostlydesigned to assure seed purity levels, and maynot be adequate for preventing or, more real-istically, reducing gene escape from GMOcrops (Kareiva, et al., 1994). Physical barriers,such as bare land or non-GMO crops aroundthe target variety, have been used to preventpollen contamination, but they have beeninefficient in many cases, partly because of alack of knowledge on the dynamics of pollenflow in each case.
If reducing the risk of contamination is amain concern, then the choice of managedpollinators of a given crop (most notably if it isa GMO) should weigh not only commercialaspects but environmental safety as well. Therisk of gene escape to non-target species is
related to the behaviour of the pollinator, suchas flight range and its effectiveness as pollina-tor, which varies according to aspects associat-ed involving both pollinator and crop charac-teristics. Purity standards should be stricter incases of gene escape risk than in cases of seedpurity, more so in centers of diversity, such asthe tropics, where traditional varieties, includ-ing progenitors, may disappear.
In addition, environmental monitoringactions focusing on gene escape should givepriority to high-risk crops. These are those withlittle domestication (that is, that are still ecolog-ically and reproductively similar to wild rela-tives), that grow sympatrically with wild rela-tives 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.
44
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 hadtraditionally 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 hand cross-pollination experiments.
2.Traditional genetic improvement methods, such as by phenotype selection of tree crops, should bere-evaluated.
Alleged low productivity of some plantations may be due to inbreeding depression, not a lack ofpollinators.
Proposed methods:
• Molecular techniques (microsatellites, allozymes) to evaluate genetic diversity and dynamics; inbreeding depression, levels of outcrossing, pollen flow, cross-compatibility between varieties of 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 impactassessment 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 "reservalegal") 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.
Workshop I 45
46
Proposed methods:
• Molecular techniques (microsatellites, allozymes) to evaluate geneticdiversity and gene flow.
• Statistical comparison of reproductive parameters of native plants inisolated versus connected forestfragments.
• Legal actions.
2. Exotic plants or pollinators should be priority in long-term, in-depth monitoring programs, to detectoverall 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 ofnative 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 urbangreen 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 pollinationstudies 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 cur-rently 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 areinvolved 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 to practice by final users.
There are currently many comprehensive studies of economically important plants and pollinatorswhose results are unknown to the final user because of restricted (academic, technical) circulation. Itis important that the initiative of producing this material be officially sponsored and supervised by sci-entists so as to gain credibility.
Proposed methods:
• Books could be transformed into PDF with the authors’ consent and be made available at officialsites 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
MethodsExplanations of some recommended tech-niques follow, with emphasis on Brazilianstudy case examples. Among the methodsproposed to help perform the recommenda-tions, several rapid assessment protocols(RAP) could be developed, grouped broadlyinto two: botanical (phenology, flower densi-ty, 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 tobe considered within each of these two, andon how to measure them. These protocols willallow data collection in the field by peoplewith little or no formal biological training.Other methods, including statistical analyses,require both expertise and specific facilities,and will usually be performed by researchersand trained personnel.
48
Genetic diversity Isozyme electrophoresis is a technique formeasuring the rate and direction of move-ment of organic molecules (in this case,enzymes) in response to an electric field(Alfenas, et al., 1998; Pinto, et al., 2001). Therate and direction of enzyme movement in astarch or and agar gel will depend on theenzyme’s net surface charge, size and shape.Enzymes can then be stained, resulting in aseries of bands in the gel. Those enzymes thatmigrate to the same place in a slab of agar orstarch gel and yield similar banding patternswhen stained are considered to representhomologous enzymes (isozymes). When theisozymes are controlled by alleles of one gene,they are called allozymes. The banding pat-terns of specific types of enzymes in the gelmay vary from plant to plant. Allozyme elec-trophoresis is most useful to analyze geneticdiversity and outcrossing rate (the proportionof the progeny generated from cross-pollina-tion) of populations within species. As acodominant marker, allozymes may directlyidentify heterozygous genotypes. Heterozy go -sity indices may be easily calculated for popu-lations or samples of plants.
The visualization of electrophoretical pat-terns of isozymes requires simple procedures,since isozyme bands are obtained through thereaction that identifies the enzyme. The tech-nique of isozyme electrophoresis is simple tolearn, and it is cheaper and involves faster pro-cedures than DNA markers.
This method has been used in a numberof studies on the genetic diversity and popula-tion structure of Brazilian species, such as thecommercially important palmheart (Euterpeedulis, Conte, et al., 2003), rubber (Heveabrasiliensis, Yeang & Chevallier, 1999), and"cagaita" (Eugenia dysenterica, Telles, et al.,2001). However, some native and most culti-vated plants have shown either very low or no
isozyme variability. In this case, molecular tech-niques can provide a larger number of markersthan isozymes.
DNA markers, on the other hand, show ahigher number of alleles per locus and can bemore useful and accurate than isozymes.Higher numbers of markers can give moreaccurate genetic diversity indices and paternityanalysis. However, most markers, such as ran-dom amplified polymorphic DNA (RADP) andamplified fragment length polymorphisms(AFLP), are dominant and cannot show het-erozygous genotypes. In some cases, however,the high sensitivity of these techniques maylimit the detection of the same markersamong genetically divergent individuals.Molecular markers require specialized trainingand more sophisticated and expensive equip-ment, since their protocols are more elaborat-ed. These techniques are also more expensivethan for isozymes, but their prices are drop-ping (Ferreira & Grattapaglia, 1996).
Microsatellites are stretches of DNA thatconsist of tandem repeats of a simplesequence of nucleotides. These repeats caneasily be amplified using PCR (polymerasechain reaction). The number of repeat unitsthat an individual has at a given locus can beeasily determined using polyacrlyamide gelelectrophoresis. Using these gels, we can seetwo genetic marks for most individuals; eachindividual inherits one length of nucleotiderepeats from its mother and one from itsfather (individuals with one band received thesame band from both their mother and theirfather). Primers to the microsatellite flankingregions can be labelled with fluorescent dyes,allowing the amplified products to be separat-ed in a polyacrylamide gel electrophoresis onan automated DNA Sequencer.
In the last decade, microsatellites or simplesequence repeats (SSR) markers have becomean 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 SSRloci allows the accurate discrimination of indi-viduals in natural populations and the estima-tion of genetic parameters, such as levels ofinbreeding, heterozygosity, gene flow and mat-ing system, which are relevant for the geneticconservation and management of tropical treesunder intensive human pressure. Microsatellitemarkers have recently been developed for anumber of tropical tree species, such as the edi-ble piqui (Collevatti, et al., 1999) and palmheart(Gaiotto, et al., 2001), and the timber speciesmahogany (Swietenia macrophylla, Lemes, etal., 2002, 2003), "anani" (Symphonia globulif-era, Aldrich, et al., 1998), "andiroba" (Carapaguianensis, 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 plantspecies depends on its breeding system. Twoaspects are usually evaluated through experi-mental manipulation: self-compatibility andself-pollination. The first evaluates if a flowerreceiving pollen from the same plant is capa-ble of producing viable seeds, and to whatdegree. If the species is self-incompatible,then it will need to be visited by pollinatorsthat carry pollen from another plant in orderto effect cross-pollination. Dioecious plantsare obligate outcrossers. To test for self-com-patibility, manual self-and cross-pollinationexperiments are performed on flowers, andthe results (usually fruit and seed set) are thencompared to those from control (unmanipu-lated) flowers. The difference in fruit or seedset also indicates if natural pollination is defi-cient in a population. If this is the case, furtherobservations should follow to see if low fruit
or seed set is caused by a reduced number ofvisits or by their quality. Poor quality visits area result of visitors who do not perform polli-nation (thieves, for example), or who depositthe 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-compat-ible, then it might not need the help of polli-nators to set seeds. This is usually checked bybagging buds to exclude visitors and then ver-ifying fruit and seed set. These procedures arestandard 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 nutrientcontents of the fruits.
Different pollinators respond to resourcelandscapes and this in turn has consequenceson the extent of pollen dispersal (Bronstein1995). Foraging flights may vary according tothe 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 mathe-matical methods have been used to compareflight behaviour of pollinators, particularlyinsects. They rely on field data that involvetracking techniques, such as telemetry for ver-tebrates, the use of dyes and the direct obser-vation 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 popu-lation isolation.
50
References
ALDRICH, P.R., HAMRICK, J.L., CHAVARRIAGA, P. & KOCHERT, G. 1998. Microsatellite analysis ofdemographic genetic structure in fragmented populations of the tropical tree Symphonia globulif-era. Molecular Ecology, 7: 933-944.
ALFENAS, A.C., PETERS, I., BRUNE, W. & PASSADOR, G.C. 1991. Eletroforese de proteínas eisoenzimas 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 characteriza-tion of microsatellite markers for genetic analysis of a Brazilian endangered tree species Caryocarbrasiliense. Heredity, 83: 748-756.
COLLEVATTI, R.G., GRATTAPAGLIA, D. & HAY, J.D. 2001. High resolution microsatellite basedanalysis of the mating system allows the detection of significant biparental inbreeding in Caryocarbrasiliense, an endangered tropical tree species. Heredity, 86: 60-67.
CONTE, R., NODARI, R.O, VENCOVSKY, R. & DOS REIS, M.S. 2003. Genetic diversity and recruit-ment of the tropical palm, Euterpe edulis Mart., in a natural population from the Brazilian AtlanticForest. Heredity, 91: 401-406.
COUTO, R.H.N. 2002. Plantas e abelhas, uma parceria em crise? Anais do V Encontro sobreAbelhas, 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 molecularesem 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 CentralBrazil 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, NewHaven, CT, USA.
HOLANDA-NETO, J.P., FREITAS, B.M., BUENO, D.M. & ARAUJO, Z.B. 2002. Low seed/nut produc-tivity in cashew (Anacardium occidentale): effects of self-incompatibility and honey bee (Apis mel-lifera) 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-fer-tilization between transgenic crops and wild relatives. Molecular Ecology, 3: 15-21.
KEARNS C.A. & INOUYE D.W. 1993. Techniques for pollination biologists. Colorado UniversityPress, Niewot, Colorado, USA.
LEMES, M.R., BRONDANI, R.P.V. & GRATTAPAGLIA, D. 2002. Multiplexed systems of microsatellitemarkers for genetic analysis in mahogany, Swietenia macrophylla King (Meliaceae), a threatenedNetropical timber species. Journal of Heredity, 93: 287-290.
LEMES, M.R., GRIBEL, R., PROCTOR, J. & GRATTAPAGLIA, D. 2003. Population genetic structure ofmahogany (Swietenia macrophylla King, Meliaceae) across the Brazilian Amazon, based on varia-tion 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 villo-sum (Aubl.) Pers. (Caryocaraceae), uma Árvore Emergente da Floresta Amazônica. Mastersthesis. INPA-UA, Brazil, 63 p.
MORRIS, W.F. 1993. Predicting the consequences of plant spacing and biased movement for pollendispersal 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 microssatélitesem plantas. Biotecnologia, Ciência & Desenvolvimento, 20: 16-19.
PROCTOR, M.; YEO, P.; LACK, A. 1996. The natural history of pollination. Harper CollinsPublishers, London, UK.
52
ROUBIK, D.W. 1995. Pollination of cultivated plants in the tropics. FAO Agricultural ServicesBulletin 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 distri-bution. 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.
Abstract
Pollinating agents, especially insects, are clear-ly essential for agricultural production. Thecentral point of discussions here are the impor-tance, the possibilities, and the managementof native bees, both solitary and stingless bees,as well as honey bees, as pollinators. The par-ticipants were divided in subgroups and so theresults here presented.
Aim
The establishment of standard methodologiesfor managing native bees (solitary and social)as well as Africanized honey bees as pollina-tors of economically and locally importantagricultural crops. To assess the biodiversity oflocal bees important for pollination and toevaluate their status; to define the basic pro-cedures to be developed for rearing bees on ascale to allow their use as pollinators in agri-culture; and to improve capacity building andtraining, at all levels.
Expected Product
• Updated report on knowledge aboutnative and Africanized bees and their useas pollinators.
• A list of recommendations for study casesduring 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 activi-ties (transportation of bees from one area toanother) for pollination purposes.
Discussions
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 rear-ing and management to be used as pollinators
The whole group discussed together atthe end of each session, for one hour. Eachsubgroup was composed by, at least one per-son familiar with the crop, one person familiarwith pollination biology, and one person famil-iar with bee surveys. These discussions sectionswere divided according to the followingaspects: state of art, perspective of the use ofnative and Africanized bees for pollination
Workshop I 53
Group 3Bee Management for Pollination Purposes
purpose; rearing and managing bees on alarge scale for pollination purpose, colony pro-duction on a large scale and best practice inmigratory apiculture and meliponiculture forpollination; and case studies.
Some questions orientated those discus-sions, such as:• Which are the native bee species that polli-
nate Brazilian crops? • Are there species normally being used as
crop pollinators? • What are the main constraints for the use of
native and Africanized bees as pollinators?How to overcome these problems?
• How to measure the efficiency of eachmethod for multiplying colonies on a largescale?
• Which species are included in this methodol-ogy?
• 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 manag-ing native bees and Africanized bees forpollination?
• Is it possible to standardize breeding and man-aging methods for solitary and stingless bees?
• Is it possible to overcome parasitism prob-lems 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 agri-cultural use?
• Is it necessary to change established crop-ping practices for the sustainable use ofbees as pollinators?
• What are the conservation measures neces-sary to maintain a stable population ofnative bees in crop areas?
• What and how detailed should these proto-cols 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 growersabout 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 representedon the table below.
Study Cases
The results will be presented here bygroups: solitary bees and bumbles bees; honeybees; and stingless bees.
54
StinglessBees
Strawberry
Tomato(Melipona)
Melon
Umbu-Spondias
BumbleBees
Tomato(Bombus)
SolitaryBees
Passionfruit
Cashew
Cotton
Acerola
AfricanizedBees
Cucurbitaceae
Eucalyptus
Melon
Coffee
Abstract
Solitary bees have potential for use as pollina-tors of various crops cultivated in Brazil, butno solitary bees are yet commercially availableto growers, and rearing techniques are onlyavailable for a few species, such as Xylocopaspp. Ground-nesting bees of the generaExomalopsis, Epicharis and Centris are goodpollinators of various crops, such as tomato(Lycopersicum esculentum) and acerola or westIndian cherry (Malpighia emarginata), but theyare difficult to manage. In most cases, there isno practical way to colonize areas with newnests, and merely providing suitable nestingsubstrates (e.g. sand) rarely yields productivenesting for many years. For ground-nestingbees that are effective and abundant pollina-tors of a crop (or desired tree species) or itsclose 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 "creat-ed" nesting sites are unlikely to be reliably andquickly colonized. Promising taxa of cavity-nesting species of solitary bees are Xylocopa,Centris, Megachile, Anthidiini and Tetrapedia,but there is lack of knowledge on thesespecies' natural histories, floral hosts, parasites,diseases, etc. Cost-effective technologicalimprovements are needed to reliably providelarge numbers of manageable bees for com-mercial pollination. However, methods/tech-
niques will need to be tailored to each beespecies. The use of solitary bees as pollinatorscould be initiated with small growers, whoprobably will own their own bees. They shouldbe stimulated to show the results that growerscan have when they use pollinators (in num-bers, value, amount of profit). Other growerswill be very rapidly convinced once they see theprofits of their neighbors. As it is not commonin Brazil to value pollination services of bees ingeneral, especially solitary bees, it is importantto disseminate pertinent information (aboutsimple concepts, such as pollination, pollina-tors, their services, etc.), distributed by exten-sion programs (for example in small plantingsof Passiflora, since techniques to rear and useXylocopa 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 ornot of using Bombus as pollinators. If necessary,native species such as B. atratus and B. brevivil-lus (not so aggressive when in small colonies)and meliponinine bees, such as Meliponaquadrifasciata (at least for tomatoes), should beconsidered. There should be national regula-tions forbidding the importation of exoticBombus species and a monitoring program ofinvasive B. terrestris from Uruguay, where it wasfirst introduced in 1995 and is now free-living innature. Finally, research on Bombus and solitarybee natural histories, floral hosts, parasites, dis-eases, foraging behaviour, rearing techniques,management and pollination effectiveness in
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.
various crop species are necessary in order forthese bees to be used as large-scale reliable pol-linators in Brazilian agriculture.
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 Indian
cherry or acerola pollination);• Centris (There are reports of West Indian
cherry or acerola pollination).
Gr ounding nesting bees are difficult tomanage; in most cases there is no practical wayto colonize areas with new nests, and merelyproviding suitable nesting substrates (e.g. sand)rarely yields productive nesting for many years.
There is little knowledge about groundnesting bees as pollinators and about theirmanagement for this purpose. Three mainapproaches are suggested to help identifypotential pollinating bee species: 1.selection of areas with less intensive agricul-
ture for visitation to crop species (e.g. homeplantings of Cucurbita) where insecticide useis unlikely, so that bee populations canincrease without extermination by pesticides;
2.search for promising species of non-socialpollinators (or social Halictidae) on wildcrops and their wild relatives (co generics).ex. Rhambutan, which is visited and pollinat-ed by Euglossa;
3. investigate pollen use by any large aggrega-tions where solitary bee species are found anddiscovered (e.g. Oxaea) to judge if they might
be using flowering species of agriculturalinterest (e.g. aggregations of Peponapis).
Recommendations
In order to promote ground-nesting bees thatare effective and abundant pollinators of acrop (or desired tree species) or of a close rela-tive to this crop species, the farmer must man-age the crop (care with spraying, for instance)and the surrounding land (size of monocultureacreage, proximity to fallow nesting sites), asthese bees' nests cannot be moved, and artifi-cial or "created" nesting sites are unlikely tobe reliably and quickly colonized.
There is considerably more informationon and well-succeeded examples of the useof cavity nesting species of solitary bees.Species such as Osmia lignaria pronpiqua andMegachile rotundata are widely used andmanaged for apple (Malus domestica) andalfalfa (Medicago sativa) pollination, respec-tively, 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 popula-tions for use in pollination. Among these taxa,Xylocopa can be considered special in Brazilbecause there is a demand for these bees andthere is some knowledge on its biology and rear-ing techniques for use especially in Passifloraplantings. Serious constrains have been identi-fied and must be overcome in order to achievelarge scale production and economic viability forexploiting these bees as crop pollinators: • ants are serious predators of bee nests and
must be controlled; • there is a need to eliminate parasites and
diseases (clean management) before estab-lishing populations for increase;
56
• there is a need for improved pest manage-ment 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 cropsbenefit 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 nestsneed to be developed and made available,based on knowledge of which bees aregoing to be used;
• there is a lack of taxonomic pollen analysis orfloral visitation analysis to establish floral use.
Other main recommendations are to com-pile Brazilian studies of past trap-nesting expe-rience in Brazil and produce a starting point forthose species that are present in the countryand can be reared in trap-nests. It is also impor-tant to develop an insecticide managementprogram, in which pest control practices shouldminimize bee mortality (label requirements oninsecticides, for instance, should emphasizescouting and economic thresholds). This pro-gram could be developed by the honey beemanagement group due to their greater expe-rience in using bees for pollination purposes.
Workshop I 57
Some cultivated plants that probably benefit from pollination by solitary bees.
Botanic Family
Apocynaceae
Anacardiaceae
Bixaceae
Cucurbitaceae
Fabaceae
Lecythidaceae
Common names - English
cashew
pumpkin
squash
melon
cucumber
soybean
field bean
kidney bean
lentils
pea
cowpea
Brazil nut
Common names - Portuguese
Mangaba
Caju
Umbu
Caja, Cajarana, Umbu-caja
Urucum, Coloral, Açafrão
Moranga
Abóbora
Melão
Pepino
Soja
Feijão
Lentilha
Ervilha
Feijão de corda
Castanha do Pará
Scientific name
Hancornia speciosa
Anacardium occidentale
Spondias tuberosa
Spondias spp
Bixa orellana
Cucurbita pepo
Cucurbita moschata
Cucumis melo
Cucumis sativus
Glycine max
Vicia faba
Phaseolus vulgaris
Lens esculenta
Pisum sativum
Vigna sinensis
Bertholletia excelsa
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 crassifoliafor 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.
58
Malpighiaceae
Malvaceae
Passifloraceae
Solanaceae
West Indian cherry
wild cherry /nance
cotton
passionfruit
giant granadilla
tomato
egg-plant
sweet pepper
Pepperony
Acerola
Murici
Algodão
Maracujá
Maracujá-açu
Maracujá
Maracujá-doce
Tomate
Beringela
Pimentão
peperoni
Malpighia emarginata
Byrsonima crassifolia
Hibiscus esculentus
Gossypium hirsutum
Passiflora edulis
Passiflora quadrangularis
Passiflora mucronata
Passiflora alata
Lycopersicum esculentum
Solanum melongena
Capsicum annuum
Capsicum spp.
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) onsmall 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).
Workshop I 59
Recommendations
Bee biologists should participate in crop sym-posia 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 general recommendations to use solitary bees as crops pollinators1.Complementary floral resources should be
provided. 2.Plants for nidification (trunks) initially, later pro-
vide nesting substrates (although these alsomay be made from natural materials, such as
stick nests, rather than drilled nesting blocks).3.Conservation of natural areas (in order to
maintain natural populations); need not beproximate to crop of interest (sustainabilityextractive reserves for initiation of trap-nest-ing programs).
4.Spray management - toxic sprays must beavoided during bloom.
5.Different Xylocopa nest substrate structuresshould be compared (Freitas & Oliveira Filhovs. Camillo models).
6.Cultivation of other crops simultaneously foryear-round forage (no extensive monocul-tures at a scale greater than flight range).
7.Adequacy of local/regional conditions. 8.Management of ruderal plants where nec-
essary.
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 moveable-frame hive for honey bees.
2) Use of X-ray units
Reason: needed for evaluating nest contents, progress of development and metamorphosis, loca-tion 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 from overseas if not available within country. Applications detailed in published studies with Osmia lignaria and Megachile rotundata. Alternatively, can use stick nests of soft, easilysplit wood or possibly reeds (Japanese Osmia system). Choice will be guided by practicality, 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 ofacceptable nesting materials for cavity-nesting bees? Are manufacturers of hive equipment interestedin producing interchangeable, easily assembled components of Xylocopa nest boxes? Are there manu-facturers interested in producing drilled wooden nesting blocks in large numbers, or clever methodsfor 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 withMegachile and Osmia in the US, Japan and Europe. Aspects of those programs will clearly need adap-tation 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.
60
Final considerations regarding solitary bees
1. Measuring effectiveness of methods
for population increase
a. The only practical species to manage are
those whose populations can be increased
(more daughters than mothers).
b. Methods that produce populations with
limited parasites and disease.
c. Affordable nesting materials that are practi-
cal to make and endure for Xylocopa and
Megachile; there is a possibility of adaptation
of existing methods.
2. Greenhouse pollination
The main difficulty in using solitary bees as
pollinators in greenhouses is that glass and
plastic 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 the
growers can have when they use the pollina-
tors (in numbers, value, amount of profit).
We only have to convince about 1% of
them; the rest will be very rapidly convinced
once they see the profits of the neighbours.
As it is not common in Brazil to value polli-
nation services, and bees in general, espe-
cially solitary bees, it is important to dissem-
inate information (about simple concepts
such as pollination, pollinators, their services,
etc.), distributed by extension programs (for
example in small scale plantings of
Passiflora).
Final considerations regarding Bombus
1. No importation of non-native species
There should be regulation on importation of
bees:
• brazilian laws must be made controlling
Bombus importation;
• seek an agreement among South American
countries or in the Mercosul related to bum-
blebees importation;
• establish a monitoring program of invasive
Bombus terrestris from Uruguay. This
species was introduced into Uruguay in
1995 and now is free-living in nature, colo-
nizing new areas and spreading towards
the Brazilian border.
2. Need for importation of non-native
Bombus species
There is no need for importation, because:
• these bee species are used only for pollina-
tion of greenhouse crops;
• they are used mainly for tomato pollination,
but recent studies have shown that native
stingless bees Melipona quadrifasciata and
Nannotrigona pirilampoides are good toma-
to pollinator in greenhouses;
• exotic Bombus species may bring parasites
and diseases to native species.
3. Using native Bombus species for crop
pollination
We do not currently have knowledge to han-
dle 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 small
colonies;
• B. brevivillus - in Northeast Brazil, not
aggressive; has potential as a pollinator of
crops of glasshouses and in open areas.
Workshop I 61
Final Remarks
Bombus are used commercially only to polli-nate greenhouse crops. This agricultural seg-ment is still small in the country, compared tothe size of the Brazilian agricultural system,and does not justify the risk and unknownconsequences of importing or allowing theentry of exotic Bombus species. Also, mostgreenhouse cultivation is done with tomatoes
and the stingless bee Melipona quadrifascia-ta has been shown to be a good alternativeto pollinate this crop in enclosures, and thereare promising native Bombus species thatcould also be studied for this purpose. Finally,Brazil should create laws prohibiting andpunishing Bombus importation, follow thespread of B. terrestris in Uruguay, and author-ities should monitor its arrival in the southernpart of the country.
62
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 itsnative 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.; IMPER-ATRIZ-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 WestIndian 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 productiv-ity in cashew (Anacardium occidentale): effects of self-incompatibility and honey bee (Apis melli -fera) behaviour. Journal of Horticultural Science & Biotechnology, 77 n.2: 226 - 231.
Abstract
Pollinating agents, especially insects, are clear-ly essential for agricultural production. Honeybees have become increasingly important, asfield sizes have increased and native bees havedecreased, due to intensive land use and pes-ticides. 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 pollinatorsinto pest management programs. A singletruckload can carry 20 million potential polli-nators. Honey bees contribute to more than80% of the agricultural produce pollinated byinsects. Unfortunately, Brazil does not have astrong tradition of using bees for pollination,different from the USA, where more than 2million colonies are rented annually. Bee -keeping in Brazil has grown considerably dur-ing the last few years, especially due to honeymarket conditions. Brazil now has about 2,5million colonies available for bee products pro-duction (honey, wax, propolis, pollen, royaljelly and bee venom) and for pollination pur-poses. There are beekeepers specialized in pol-lination, especially for apples, melons andcashews. All of these products are both con-sumed in country and exported. To obtainexport quality fruit, insect pollination isabsolutely necessary.
Unfortunately, many of the crops thatcould 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, resultingin production losses due to inefficient pollina-tion. Africanized honey bees are seen muchmore as honey producers than as pollinators.
For many crops that do not traditionallyuse honey bees for pollination, such asoranges, peaches, strawberries, sunflowersand forage soybeans, we have data indicatingsignificant increases in fruit and seed produc-tion and improved fruit quality with pollinationby Africanized honey bees in Brazil (Nogueira-Couto, 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 croplonger 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, flyfaster and are quicker to recruit other hivemates, than are European bees, making themmore active and efficient pollinators. Africa -nized bees forage at lower light levels than doEuropean bees, so that they work longer days.They also do not reduce brood productionduring winter, so the colonies remain strong,with abundant foragers for pollination activi-ties. 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 num-bers of colonies needed for pollination ofcrops. There are well-established migratory
Workshop I 63
B) Honey Bee
Participants: David De Jong, Lionel Segui Gonçalves, Farooq Ahmad, Kátia PeresGramacho, Ricardo Costa Rodrigues de Camargo, Uma Partap, Valdemar Belchior Filho.
beekeeping techniques, and truckloads ofbees can be quickly and timely moved to flow-ering crops (De Jong, 1996).
Discussion
Africanized honey bees have been used for pol-lination in greenhouses in Brazil. However manybees are lost from the colonies and it is difficultto maintain the colonies alive under greenhouseconditions. Some researchers and beekeepershave been able to overcome these problems,but the techniques that they use are not pub-lished, nor is there an established system thatworks uniformly under all circumstances. Mostattempts to use honey bees in greenhouses areinitially unsuccessful, however after numeroustrials some researchers have been able to main-tain colonies for long periods, efficiently polli-nating the crop. In order to make efficient useof this resource, it will be necessary to makecontrolled studies, and develop standard, prac-tical techniques that should be made widelyavailable 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 antici-pated by adequate pollination), and by calcu-lating the percentage fruits that are consideredof high quality. Another important quantitativeaspect is the cost and benefit of the pollinationactivities. Using honey bees has a cost, and thisshould be compared with the gain in crop pro-duction attained with pollination. Photos offruit that are produced by plants exposed tobees, versus those that are produced withoutbees, are often quite useful for illustrating thevalue of bee pollination. Appearance is impor-tant, as the color and shape of the fruit is
often affected by pollination. Photos of crosssections of the fruit can show the number anddistribution of the seeds, which are clear indi-cators of pollination efficiency. The fruit quali-ty can also be evaluated by measuring sugarand protein and other substances, and by eval-uating organoleptic (taste) factors.
We already know how to manageAfricanized honey bees as polinator for somecrops, such as apples and melons, howeverthis is not always done in the most efficientway. Many crops that would clearly benefitfrom the introduction of bee colonies are notroutinely pollinated. Generally speaking, polli-nation is little valued or understood by farm-ers, nor are beekeepers aware of the truevalue of the services that their bees provide.We have data indicating significant increasesin fruit, seed and vegetable production due topollination by Africanized honey bees, howev-er little of this information is available to thegrowers. Often objective studies on commer-cial varieties are lacking. This is true both forfield crops and for greenhouse crops. The lat-ter are unviable commercially unless adequatepollination is provided. Many crops are in factpollinated 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 managingAfricanized bees for pollination can be listed as:1.there are no established techniques for
using Africanized bees under Brazilian con-ditions on most crops;
2.often the hives are not made with standardmeasures, or with inferior materials, makingtransport and management difficult;
3.the bees are quite defensive and growers areoften reluctant to place them in or near thecrops that need pollinating;
64
4.there is not sufficient care in the transporta-tion of colonies, so that accidents are com-mon and this discourages their use for polli-nation;
5.beekeepers are not aware of disease prob-lems, and often incorrectly try to treat theircolonies, and some have introduced con-taminated bee products and equipmentfrom abroad, threatening beekeeping throu -ghout the country;
6.there is a lack of central laboratories that canprovide timely and accurate diagnoses ofbee diseases, and also there are no field per-sonnel 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 insecti-cides indiscriminately and incorrectly with-out any concern for the effects on the beesand the beekeepers;
8.there is no tradition for making pollinationcontracts that include a provision for com-pensation for the beekeeper in the case oflosses due to pesticides or the stealing ofhives on the grower's property. There shouldalso 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 intoagricultural land, without concern about main-taining habitat for pollinators. Loss of naturalpollinators due to the loss of habitat increasesthe need for honey bees. More intensive farm-ing and larger fields of crops overcomes thecapacity of local native bees to pollinate. Weneed to develop techniques and policies that
will 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 appro-priate information about pollination. Unfor -tunately, even in the case of crops for which wehave clear evidence that honey bees signifi-cantly increase production, growers frequentlydo not include pollination in their managementprograms, and often even prohibit the intro-duction of bee colonies onto their property, orthey may charge the beekeepers, while in othercountries the beekeepers are paid for theirservices. This lack of tradition to include beesgreatly diminishes the potential gain of thegrowers. We need to have more good qualitydata and then convince the growers by usingdemonstration plots.
Bee diseases Some new diseases from other countriesthreaten beekeeping and hence can affect theavailability and quality of honey bee coloniesfor pollination. Unfortunately, these incidentsof new diseases have not been sufficientlycontrolled and studied by competent resear -chers and authorities. Beekeepers are alsounaware of the need for good practices thatwill avoid the introduction of these new dis-eases. For instance, honey and pollen that hasbeen imported (both legally and informally) isoften 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 theintroduction of American Foulbrood Disease(Paenibacillus larvae) spores from importedhoney into honey bee colonies. This situationneeds to be more closely investigated, and thebeekeepers should be made aware of the dan-
Workshop I 65
ger of such practices (De Jong, 1996). A simi-lar problem has occurred with a fungus dis-ease, Chalkbrood, caused by Ascosphaeraapis, 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 prac-tices; we need to have more informationabout the impact of this exotic disease onAfricanized honey bees.
There are no central laboratories to iden-tify diseases.Beekeepers need to have a place to send sam-ples in order to learn what diseases they have,and to determine whether their problems arereally caused by parasites or disease organ-isms. This service exists in nearly all major bee-keeping countries and now should be imple-mented in Brazil.
Beekeepers do not know diseases Diseases are normally not a big problem inBrazil, but beekeepers sometimes incorrectlytry to treat colonies with antibiotics and aca-ricides whenever they suspect a disease. Theirlack of knowledge and the lack of govern-ment infrastructure to help them cope withdisease problems often makes them takeinappropriate actions. Besides the unneces-sary costs and damage to the bees due tosuch home-brew treatments, there is a dan-ger of contaminating the bee products. Weneed to study the actual disease problemsand determine nutritional needs. A lack ofinformation about nutrition, especially pro-tein needs, actually causes many problemsthat are mistaken for disease. Techniqueshave been developed to more objectivelyevaluate honey bee diets (Cremonez, et al.,1998), but these new methods need to be
used systematically in order to develop eco-nomically viable pollen substitutes.
There is no sanitary control of the move-ment of colonies. Though Chalkbrood, a fungus disease, hasrecently been diagnosed in Brazil, andAmerican Foulbrood is suspected, there is nosanitary control of the movement of colonies.Consequently these new bee diseases couldbe spread to new regions, causing damage toapiculture, which could affect the availabilityof bees for pollination. It is recommendedintensive studies of those new diseases, todetermine their occurrence and their impacton the colonies. Government agencies shouldbe prepared to diagnose diseases in the labo-ratory and to train bee colony inspectors whocan make field diagnoses and develop andimplement appropriate control policies.
Problems with quality and standardization of the beekeeping equipment In some parts of the country, non-standardhives are used. Many times, among those whouse standard Langstroth equipment, there areproblems with non-standard measurements.Beekeepers are often not aware of the correctstandards and they make their hives based onequipment that they have purchased. As thepurchased hives are frequently not exactlybuilt, badly dimensioned hives are perpetuat-ed. Many times new beekeepers have pur-chased bad equipment with funds that theyhave received on credit. These can be badlybuilt hives, with uncured "green" wood, ormade with wood that is inappropriate for api-culture. Such hives start to bend and openwithin a few months. Unfortunately, the fund-ing agencies that set up programs to fomentapiculture often provoke these kinds of pur-chases of substandard materials due to cost-
66
competitive purchasing policies. Later, the bee-keepers have a difficult time repaying the costof the equipment, as it is commonly discardedwithin a short time.
The handling and transport of beehives inBrazil is not mechanizedNow all hives and honey supers are transport-ed from trucks to the apiary, and back, byhand. Hives are heavy, especially when theyare full of honey. This hand carrying oftencauses back problems for small-scale beekeep-ers, which depend on family labor. Beekeeperswith larger numbers of colonies must hirehelp, and this makes their managementexpensive. A beekeeper in the USA or Canadacan handle more than a thousand colonies byhimself, or with only a single helper. A similarnumber of colonies in Brazil would need atleast five or six laborers, and the movingprocess takes much longer than in other coun-tries. Transporting colonies for pollinationrequires specialized labor, at specific times. Ifbeekeeping had mechanized alternatives thenthis transport would be cheaper and more effi-cient. However, the fork lifter tractors (bob-cats) currently used in other countries are tooexpensive for Brazilian conditions. It would bemore cost efficient to pursue intermediate, lesscostly, alternatives for mechanization. Weneed to identify appropriate techniques forhive lifting and transportation, and test andadapt them to local conditions.
There are problems with transporting beecolonies Beekeepers are not aware of their responsibil-ities and correct procedures when they havean accident during transportation of hivesfrom one region to another. They are unawareof the best ways to transport bees, and there-fore accidents are more common than theyshould be. Frequently they lose bees that
escape from the hives, and many colonies diedue to overheating. The local authorities areunaware of the importance of the need fortimely movement of colonies, and may inter-fere with transport.
Problems with a deterioration of natural areas The lack of natural areas means that bees haveno wild flowers for supporting and maintainingcolony growth. This means that the coloniesare weak or can even die and therefore are notavailable for pollination services. In variousparts of the country there is so little natural for-age that beekeeping is uneconomical, especial-ly in regions where there is intensive agricultureand therefore with a great need for bees forpollination. We need to find ways to promotethe maintenance of natural areas on farms(possibly through tax incentives) and to havestates and municipalities plant trees that pro-vide 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 artifi-cial feeding of sugar and protein diets.However, sugar is often too expensive, so itwould be useful to have a means to providesugar or sugar syrups at a low price for thebeekeepers to properly prepare their coloniesfor pollination. The most important nutritionalproblem is a lack of appropriate protein whenpollen from flowers is not available. At themoment, no adequate artificial diet is avail-able. Such diets need to be developed andtested. A relatively simple laboratory techniquedeveloped in Brazil is available for the initialscreening of food by-products that could beused as protein sources for bees. Large scaletesting should be done, with field testing anddemonstration of the most promising alterna-tives (Cremonez, et al., 1998).
Workshop I 67
There are misconceptions about howbees could impact on crops In some crops, such as oranges, there aremisconceptions about the danger of beestransmitting plant diseases. Generally, deci-sions are made without any real evidence ofsuch a problem.
There are problems with beekeepersobtaining permission to place bees on farm-land - due to fear of the bees interfering withcultural 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 under-stand the real effects of bees on crops. Someof this information is available from othercountries, and can be adapted and appropri-ately communicated. However local experi-mental work should also be done to test theimpact of bees under local conditions.
Beekeepers have problems with hives being stolen Apiaries often have to be placed in remoteplaces where the colonies are easily stolen, dueto 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 proofthat colonies or colony products have beenstolen. Policies should be developed to providelegal and police support to reduce this colonythievery 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 moreprotected areas. Insuring colonies against rob-bery is also unknown, making financial securityfor the beekeeper nearly impossible.
Problems with pesticides Presently many honey bee colonies are killed
by pesticides. Beekeepers avoid crops whereinsecticides are used; this reduces honey pro-duction and agricultural production. Cropssuch as cotton would be more productive ifthe bees could pollinate them. Native bees andwild honey bee colonies are killed by excessiveand inappropriate use of pesticides, making itnecessary to bring in commercial honey beecolonies for pollination purposes. Labeling ofthese pesticides should include informationabout toxicity to bees.
Case studies to assess main pesticide prob-lems that affect beesDevelop a manual about the use, value andcare of honey bees. Take advantage of casestudies about improvement of production andquality of farm products to educate farmersabout how to best incorporate pollination intotheir management practices. The impact ofthe most commonly used pesticides on flower-ing crops should be investigated.
Farmers and policy makers are oftenunaware of the need for pollinationGrowers are often unaware of need for polli-nators and of pollinizer varieties. Internationalpollination techniques need to be adapted tolocal conditions. The agricultural policies nor-mally ignore the need for pollinators. EMBRA-PA, SEBRAE and other appropriate institutions,such as universities, should develop projects totest the value of pollination on crops and vari-eties. They should also develop crop manage-ment schemes that minimize the impact ofinsecticides on honey bees. This informationshould then be made available to the farmers.There should be demonstration fields andcourses to make the farmers aware of howmuch they can gain by including pollination intheir management scheme.
We need clear recommendations aboutnumber and size of colonies needed, and how
68
to place them. Agricultural extension does notcurrently train farmers about ways to managetheir crops for maximum pollination.Extension services need to develop coursesand educational material. They should devel-op case studies in cooperation with localgrowers (on-farm experiments).
Consumers are not aware of how toselect good quality (well pollinated)fruits and vegetablesDemonstration materials should be developedto help the consumer recognize and choosegood quality products. Fruits and vegetables,such as melons, watermelons, apples andcucumbers, often have fewer than normalseeds, which results in inferior products with abad taste. Such an awareness and educationalprograms will create a more sophisticated con-sumer and will encourage growers to use beesto produce high quality fruit.
Other problems:• beekeepers generally are not concerned
about determining the pollinating efficiencyof their colonies, but are only trying to pro-duce the largest possible amount of honey;
• beekeepers do not know how to stimulatethe bees to collect pollen, which increasepollination efficiency, instead of nectar;
• beekeepers do not know how to direct beesto a crop that needs pollination;
• beekeepers distribute their beehives in a man-ner that is convenient for management, with-out concern or knowledge about the mostefficient arrangement to facilitate pollination;
• beekeepers manage their bees only forhoney production because the farmers nor-mally do not pay for pollination services;
• we do not know the support capacity ofagricultural areas for honey bee colonies orhow many honey bee colonies can beplaced in a specific area.
Rearing and management of Africanized honey bees in greenhouses
Current problems: • lack of knowledge of the minimum require-
ments necessary to use Africanized bees ingreenhouses (size of the colony, best time tointroduce the bees to the crop, culturespecifics and management techniques);
• misconceptions about Africanized bees aseffective pollinators;
• aggressiveness of the bees; • lack of technical and practical experience.
Proposals: • make producers aware of the usefulness of
honey bees for pollinating in green houses; • inform public and private agencies involved
in 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 successfulexperiences in Brazil and from other partsof the world, and by examining econom-ic criteria;
• develop incentives for using honey bees aspollinators in greenhouses and reducing theuse of pesticides (tax deductions, low inter-est loans, etc.);
• publicity campaigns informing about thebetter quality of well-pollinated fruits andvegetables, uncontaminated by pesticides;
• encourage and make available techniquesfor producing food in greenhouses;
• capacitate technicians involved in extensionand who assist farmers so that they canhelp them use honey bees as pollinators ingreenhouses.
Workshop I 69
70
State of the art of the use of Africanizedhoney bees for pollinationCurrently, honey bee colonies are rented forpollinating apples, melons, cashews andsome vegetable crops in Brazil. There areefficient techniques for transporting thebees, but data on other cultures are lacking.Isolated experiments have demonstratedthe value of bees for many crops in Brazil,but these have not influenced the growers,and more objective and thorough experi-ments are needed, preferably with demon-
stration plots to show the value of pollina-tion to the farmers.
Rental prices for bee colonies Beekeepers and growers are generallyunaware of how much they can or shouldcharge for their services. There is little traditionfor 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 cropsUse of Africanized bees for pollination Recommendations for case studies
Cotton
Princip al 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 and quality, 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 of including honey bees in cotton production.
Melons
Principal producers: CE, RN.
Export product Initiated and expanded continuously during the last six years, always with honey 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, howeverthe 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 honey bees 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
Citrus
Export 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 and quality for all the various varieties of oranges;
• we need to demonstrate these benefits to the farmers and work with them to reduce the impact of pesticides used in the groves on the bees.
Coffee
One of the principal Brazilian export products.
Problems: • lack of financial incentive for beekeepers to introduce their colonies into the coffee 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 fieldsto 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, takinginto 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 onstandard methodologies for rearing Africa -nized 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 of
São Paulo campus in Ribeirão Preto, SP, butit needs to be improved and made morewidely available. There is a book with a col-lection of 300 thesis abstracts (in Portugueseand English) and a list of over 2000 publica-tions on bees made in Brazil until 1992(Soares & De Jong 1992). This material isupdated periodically and is kept in a data-base, 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 widelyavailable, and will not be lost.
72
4. Initiate a scientific journal on pollinatorbiology in Brazil. Brazil has many beeresearchers, however much of the informa-tion is not readily available. A scientificjournal will help remedy this problem andwill help direct students and professors tostudy pollination problems. This journalcould be produced online at relatively lowcost, and could help consolidate beeresearch in Brazil.
5.Develop a manual on research techniques forpollinator studies, especially to determine thevalue of pollinators for crop production.
Rational Program of Pollination1.Determine how well crops are pollinat-
ed currently and investigate the produc-tion potential if there were full, ade-quate pollination. Some crops are alreadywell pollinated, and additional pollinatorsdo not increase production. In other cropsand regions, there are so few natural polli-nators that supplemental pollination canmake the difference between uneconomi-cal production and profit.
2.Estimate economic viability of pollina-tion program. The producer needs to havean idea about whether it will be economical-ly viable to use pollination for his crop, con-sidering the costs involved with personnel,transport, and renting bee colonies, com-pared to the increases in production.
3.Identification of the requirements of thecrop and determination of the pollina-tion needs. Each vegetal species has itsown specific pollination needs and appropri-ate pollination techniques are needed to ful-fill these needs.
4.Determine the pollination strategy thatshould be used. There is a need to deter-mine the number of colonies per hectare,the arrangement and temporal placement
of the colonies and integration with othercultural practices.
5.Design and install apiaries and infra-structure necessary for pollination.Determine the number of apiaries andcolonies that will be needed at appropriatetimes to give support to the pollinationactivities.
6.Training of personnel responsible formain taining the colonies in conditionsade quate for pollination. Preparing colo -nies for pollination requires specific man-agement so that they will be at an ade-quate stage of development and with suf-ficiently large populations to adequatelypollinate the crop.
7.Training of personnel to collect pollina-tion data in the field or hire such help. Theresults of pollination should be constantlymonitored.
Final recommendations
Considering what are the conservation meas-ures necessary to keep a stable population ofAfricanized bees in the cropping areas:1. incentives, such as tax exemptions for bee-
keepers and for growers for pollination ofcrops in Brazil;
2.PDF-B should make a policy of recogniz-ing the need for Africanized bees for pol-lination;
3.conduct case studies to show the importanceof wild pollinators in respective habitats;
4.stop indiscriminate logging and commercialfelling of trees by enacting laws;
5.promote and encourage re-conversion of acertain percentage of intensively cultivatedareas to provide rescue space for the mul-tiplication of wild honey bee colonies byproviding incentives (tax exemptions, sub-sidies etc.);
Workshop I 73
References
BASUALDO, M.; BEDASCARRASBURE, E.; DE JONG, D. 2000. Africanized honey bees(Hymenoptera: Apidae) have a greater fidelity to sunflowers than European bees. Journal ofEconomic Entomology, 93: 302-307.
COUTO, R.H.N. 2002. Plantas e abelhas, uma parceria em crise? Anais do V Encontro sobreAbelhas. Ribeirão Preto - SP, Brazil, p. 87-94.
CREMONEZ, T.M., DE JONG, D., BITONDI, M.M.G. 1998. Quantification of hemolymph proteins asa fast method for testing protein diets for honey bees. (Hymenoptera: Apidae). Journal ofEconomic Entomology, 91: 1284-1289.
DE JONG, D. 1996. Africanized honey bees in Brazil, forty years of adaptation and success. BeeWorld, 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, cau-sadora 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.
6.train farmers in making judicious and safeuse of carefully selected, less toxic, pesti-cides 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 providefood for wild bees;
9.encourage agro-biodiversity by plantingsome areas with native plants.
Workshop I 75
Abstract
Stingless bees are social bees that live in tropi-cal regions of the world. They are poorly stud-ied 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 onthe role of stingless bees as pollinators, identi-fied some crops that could be pollinated bythem, as well as the constraints for their use aspollinators in large scale for agriculturaldemand in Brazil.Data for this report were updated until 2006.
Introduction
Stingless bees are diverse in tropics and canpotentially be used as pollinators for severalnative and exotic crops cultivated in Brazil(Nogueira-Neto, et al., 1959; Bego, et al., 1989a 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 nativeBrazilian stingless bees richness is estimated in500 species (Camargo, p.c.). Due to the highstingless bee diversity, basic research is still
needed, although many studies had beendone in the last years. Among the 13Australian epiphytic orchids whose pollinatorsare confirmed, 9 are pollinated by stinglessbees (Adam & Lawson, 1993, apud Heard1999). Males of some stingless bees areimportant pollinators of native Brazilianorchids 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 num-ber 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 com-mercially available to growers for pollinationpurposes. The unique example where proto-cols for greenhouse pollination are well estab-lished is the use of Tetragonisca angustula andother small stingless bees for strawberries(Fragaria x ananassa Duchesne, Rosaceae) pol-lination (Malagodi-Braga, 2002; Malagodi-Braga & Kleinert, 2004). Some species ofMelipona could be good pollinators of someSolanaceae crops that need “buzz pollina-tion”, as Melipona quadrifasciata for tomatoes(Lycopersicum esculentum) growing in green-house (Del Sarto, et al., 2005). For native trop-ical fruits, as umbu (Spondias tuberosa), açaí(Euterpe oleraceae) and cupuaçu (Theobroma
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.
76
grandiflorum), the pollination requirementsare being studied (see table 1).
Coevolution between local flora and stin-gless bees should occur in high diverse habi-tats. Despite of their generalist use of floralresources, stingless bees show floral prefer-ences (Ramalho, et al., 1990; Biesmeijer, et al.,2005; Biesmeijer & Slaa, 2006). It is necessaryto improve this knowledge in order to deter-mine preferences and the main plants indi-cated as food source for their successfulbreeding, as well as for using in habitatrestoration programs.
A huge problem for Brazilian stinglessbees breeders and for capacity building activi-ties 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 ofthe present knowledge, written for differentstakeholders, and to provide basic knowledgeneeded for rear them. The WebBee (Saraiva, etal., 2004) was constructed in order to be ourinfoway in this task.
Considering the high biodiversity of sting-less bees, and the new meliponiculture regula-tion for research and for beekeeping (CONA-MA_346, 2004), it is necessary to improve thedevelopment of breeding techniques, in orderto provide bees for research and for meliponi-culture. Nests can be obtained by using trapnests in nature; a nest census and a bait-trapsurvey in natural and agricultural areas for stin-gless bees is also a priority for investigation. Arecent 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 reproductivesuccess of plants and ultimately forest compo-sition. Nests sites are considered as essential
resources, and have some requirements, asspecialization in use of logs of some plantspecies or diameters at breast height biggerthan 50cm. This has implications for reforesta-tion 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 pollinationpurposes should consider the settlement ofcorridors between patches of native vegeta-tion for keeping native populations of polli-nators as well as trees for nesting and flow-ers for food (nectar and pollen). As agricul-ture is increasing in Brazil, the land manage-ment of surrounding agricultural areas is alsovery important. Finally, stingless bees couldbe excellent pollinators to be used by smallfarmers (family growers) because they do notsting, are easy to manage, and are appropri-ate to small lands and cheap to rearing.Besides that, some small farmers have thetraditional knowledge to rearing them, usingtheir honey as medicine. They need to learnhow to manage them for pollination andconservation purposes.
State of art
Stingless bees as greenhouses pollinatorsIn 1988, Luci Rolandi Bego, from São PauloUniversity, went to Japan with a grant ofBrazilian Academy of Sciences to work with Y.Maeta on the use of stingless bees as pollina-tors in strawberry greenhouses. She carriedwith her a colony of Nannotrigona testace-icornis, a colony of Plebeia droryana and oneof Tetragonisca angustula, in rational hives,chosen by chance among the other speciesavailable at São Paulo University BeeLaboratory, 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’ behav-iour under greenhouse condition (Bego, et al.,1989a). Later on, Trigona minangkabau fromSumatra was also tested in strawberry green-houses, and the result compared with the effi-ciency of Apis in the same greenhouses(Katutani, et al., 1993).
In Brazil, stingless bees as pollinators forstrawberries in greenhouses were tested byMalagodi-Braga (1992); Malagodi-Braga andKleinert (2004). Protocols for greenhouse pol-lination are well established related to the useof Tetragonisca angustula and other smallstingless bees. Malagodi-Braga & Kleinert(2004) showed the efficiency of Tetragoniscaangustula as a pollinator in “Oso Grande”cultivar: in a greenhouse with 1350 plantsalmost 100% of flowers developed into well-shaped fruits compared to 88% with openpollination in the field.
Sweet pepper (Capsicum annuum, Sola -na ceae) is another crop cultivated around theworld, in open fields and in greenhouses(where its cycle is extended for production allyear round). Although sweet pepper is a self-pollinating plant, it benefits from bee pollina-tion (Rasmussen, 1985). In Brazil, Cruz, et al.,(2005) tested the efficiency of Melipona sub-nitida as a greenhouse pollinator of sweetpepper, variety All Big. They used four treat-ments in their research: hand cross-pollina-tion, hand self-pollination, pollination by beesand restrict pollination. The fruit set was notimproved by the use of M. subnitida as polli-nators, but the number of seeds per fruit, theaverage fruit diameter and fruit weightincreased; a lower percentage of malformedfruits were also found, comparing with self-pollinated sweet pepper.
Another important crop also often kept ingreenhouses in Brazil and worldwide is the
tomato, Lycopersicum esculentum. Velthuis(2002) tells the successful story of the bumble-bee Bombus terrestris used as tomatoes polli-nators in greenhouses in the Netherlands andBelgium that resulted in a big industry of bum-ble bee rearing in various pary of the world.Nowadays 1 million colonies of Bombus ter-restris are yearly sold for using in agriculture(Velthuis & Van Doorn, 2004). However, exot-ic pollinators are to be avoided in many coun-tries including Brazil. In search of local solu-tions, Brazil found that the use of some speciesof Melipona could be good pollinators ofsome Solanaceae crops that need “buzz polli-nation”, such as the relatively large Meliponaquadrifasciata for tomatoes (Lycopersicumesculentum) growing in greenhouse (Del Sarto,et al., 2005). Nevertheless, Macias & Ma cias(2001) and Cauich, et al., (2004) verified thatNanno trigona pirilampoides is a very success-ful pollinator for tomatoes in greenhouses,opening new possibilities for small stinglessbees use in those.
Open field pollination and stingless beesHeard & Exley (1994) already considered theimportance of agricultural landscape and nat-ural vegetation for providing pollination servic-es (the abundance of Trigona carbonaria inorchards of macadamia was correlated withthe extent of natural surrounding Eucalyptusvegetation). Venturieri (1993) also remarkedthe importance of natural vegetation aroundthe cupuassu crop in order to provide theneeded pollinators. Kremen (2004) consideredthe importance of bee community as crop pol-linators, pointing out that if we maintain sev-eral bee species from natural environments vis-iting flowers, the shortage of one species inone year could be compensated by the othervisitor’s species, diminishing the impact of pol-linators’ shortage on crops.
78
Coffee, a special commodityMost of the world coffee production is origi-nated from C. arabica shrubs, which are nativeto southwestern Ethiopia, as well as from C.canephora var. robusta (also known as C.robusta), native to equatorial Africa. Coffeaarabica plants are typically grown in cold butfrost-free areas at elevations of 500-200m, andC. canephora typically from sea level to 1000m(Klein, et al., 2003a, Donald, 2004). Coffeacanephora 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 selectivelythinned canopy of existing rainforest trees. Thiscombination of shading trees and coffeeshrubs form an integrated agroforestry system(Donald, 2004). There are many benefits origi-nated from this way of production; first, shadecover up to 50% increases yields, and the pres-ence of shade trees can control pest problems;furthermore, the quality and size of coffeebeans, as well as the taste of the final productare better under shade systems than under sys-tems without trees. However, this method wasreplaced for a full-sun production in manyplaces. Where good soils and favorable cli-mates are present, this method produces high-er yields per unit area, although not necessari-ly per plant. Nevertheless, this method also pro-duces some collateral effects, as an increasedrate of pest problems and secondary pesticideproblems. Nowadays, shading is only usedwhere it is necessary to reduce yields to keepproduction sustainable in poor-nutrient soils,where shade-loving varieties are grown, andwhere shade trees form part of economic agro-forestry systems (Donald, 2004).
Another important issue related with cof-fee 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 per-formed by Nogueira-Neto, et al., (1959), whichinvestigated the effect of the exclusion of pol-linating insects on the yield of the varietyBourbon (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 controlgroup, which plants were not allowed to bevisited. They also observed several species ofnative and introduced bees visiting coffeeflowers, as the introduced Apis mellifera andthe stingless bee Melipona quadrifasciata,both relatively big sized bees, the most effec-tive pollinators of coffee flowers in their obser-vations (a total period of observations of sixyears). According to the authors, the smallerbees (Nannotrigona testaceicornis, Plebeia sp.,Tetragonisca angustula, Trigona hyalinata andT. spinipes) observed in the flowers, collectingpollen and/or nectar were not so effective pol-linators as these big sized bees. They conclud-ed that for this variety of coffee (Bourbon),insect visits are not so important as for thediploid 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. arabicaplants in the New World, as well as in the OldWorld. He found a positive correlationbetween 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 CentralAmerica in 1985, he compared the coffeeyields of the period before and after its intro-duction. After the arrival of Africanized bee inCentral America, coffee yields in most coun-tries 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 beeswere always present, coffee production didnot varied in the same rate than the NewWorld. Countries that experienced an inten-sive land usage and loss of habitats for pollina-tors 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 ofnative and introduced pollinators for coffeeyields, although he did not analyze the pollina-tion behaviour itself.
Ricketts (2004), in experiments per-formed at Costa Rica during 2001-2002,showed that eleven eusocial bees (10 nativeplus A. mellifera) were the most common vis-itors of coffee (C. arabica) shrubs, and thatthe distance of the forest fragments to thecultivated areas significantly influenced cof-fee visiting by these bees. Bee richness, over-all visitation rate, and pollen deposition ratewere all significantly higher in sites withinapproximately 100m of forest fragments thanin sites far away (up to 1.6km). Apis melliferaforagers accounted for more than 90% of allvisits in distant sites, and where Apis were notpresent, native species as meliponine beesaccounted for most of the visits at near sites.This is due to the smaller flight range ofmeliponine bees which have a typical flightrange of 100-400m (van Niewestadt &Iraheta, 1996, Heard, 1999), although maxi-mum observed flights ranged from 1 to 2 km
(Roubik & Aluja, 1983). When Apis abun-dance declined substantially, from 2001 to2002, visitation rates dropped about 50% indistant 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 fragmentsprovided nearby coffee with a diversity ofbees that increased both the amount and sta-bility of pollination services by reducingdependence 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 morefruits in farms where there were forest frag-ments nearby. Coffee production increased14.6% when the services of pollinators wereavailable (De Marco & Coelho, 2004). Similarly,C. canephora and C.arabica fruit set increasedwith the increase of diversity and abundanceof flower-visiting bees (C. arabica: 90% when20 bee species were present and 60% whenonly three species were present, Klein, et al.,2003b; C. canephora: 95% when 20 or morebee species were present and 70% when onlysix species were present, Klein, et al., 2003c),and the number of social bees speciesdecreased with distance to forest fragmentsand the number of solitary bees increased withlight intensity (less shade) and greater quanti-ties of blossoms. Additionally, Klein, et al.,(2003b,c) found that solitary bees had animportant participation in the pollination of C.canephora shrubs, leading to higher levels offruit set that originated by members of socialbee assemblages.
These services can be translated into eco-nomic 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. Thisincrease represents an extra income ofUS$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 oneCosta Rica farm.
All these results stressed the importanceof conserving forest fragments and nestingplaces for social and solitary bee species (Klein,et al., 2003c, Ricketts, et al., 2004), which canact as service-providing units (Luck, et al.,2003) for coffee pollination. The costs ofmaintaining conservation areas are far exceed-ed by the economic benefits that the service ofpollinators brings for agriculture. In this way,conserving natural areas nearby coffee farmscan be translated into advantages for biodiver-sity and agriculture (Allen-Wardell, et al., 1998,Ricketts, et al., 2004).
Stingless bees management practicesfor use in agricultureAgricultural intensification worldwide includesa decline in the proportion of natural habitat,an increase in pesticide usage, a decrease offloral resource on farm sites, as well as largerfield sizes, crop monocultures, intensive soiland water usages and the use of synthetic fer-tilizers. Of course, the sustainability of agricul-ture following these patterns of land use isunder concern by 21 Agenda for Agriculture.
Best management practices in agriculturefor sustainable use and conservation of polli-nators are focused in recent literature, andmainly by several authors that study pollina-tors’ conservation. This means to carry on pes-ticides and their use in the crops; gene flowstudies; environmental friendly agriculturalpractices, 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 that
can keep pollinators; to decrease herbicidesuse in agricultural crops, that helps the forag-ing supply for pollinators and crop attractive-ness for them, in larger areas.
Although the already identified impor-tance of pollinators in agriculture (see alsoweevils for oil palm; bumble bees for toma-toes, among others; solitary bees for apple,pears and alfalfa, for instance; stingless beesfor strawberry, guarana, assai, coffee, amongseveral other crops; honey bees for severalcrops) is well known, until now their use is notremarkable in undeveloped countries.However, this situation will change very soon,because of new initiatives concerning pollina-tors use in crops (for instance, the BrazilianPollinators Initiative) as well as from successfulcrops competing in world market, resultingfrom the pollinators use in greenhouses, forinstance. Developed countries are workingwith pollinators’ shortage, although only asmall number of them (a dozen, according toKremen, 2004) are successful bred for agricul-tural use. If they are not available nearby dueto the intensive agricultural patterns usinglarge areas, they are bought from biotechcompanies that breed them successfully. Thesecompanies are multinational and have thetechnology of large scale breeding. The intro-duction of alien pollinators with definedbreeding techniques is also undesirable, andstudies of ecological impact are asked inimportation process. This stimulates the bread-ing of native pollinators for the same service incountries with capacity building in pollinationarea. In many tropical and subtropical areas ofthe world, a new scenario opens focusing stin-gless 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: eco-nomic value of pollinators and economicvalue of crops. Generally, producers are notinterest in resistance (ability to retain commu-nity properties under disturbance) or resilience(ability to recover from disturbance) of cropswhen intensifying agriculture, but in theireconomic value in this season. Short timeactions and market simulations are importantin the producer’s decisions on what crop touse in next season. They are linked to unpre-dictable weather conditions, as well to themarket fluctuation on crop values (Kevan &Viana, 2003), as well as to the economicadvantage in having better fruits. Long-termactivities concerning natural resources arealmost not considered.
The potential use of stingless bees’nests in large scale is for using in crop polli-nation. How to get nests in nature and tobreed them successfully is a challenge.Another point of consideration in relation tothe social bees of Brazil is the new law no.02000.006608.2000-81. This law pretendsto protect these insects and has only recentlybecame effective. To protect these socialbees, it mainly prohibits the exploration ofnatural nests. Unintentionally, this law makesit harder to access biological material of thesebees for who needs to do the necessary, legalstudies. Above all, the restriction put on bythis law makes that the artificial multiplica-tion 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 trapnests, offering nests sites for stingless bees.Inoue, et al., (1993) did these experiments inorder to know more about the populationdynamics of stingless bees. They studied anarea of the Horticultural ExperimentalStation in Lubuk Mintrum, in Sumatra,where the main vegetation was a plantationof tropical fruits, rambutan, N. lappaceum,and durian, D. zibethinus (ca 480x200m, 8-6ha), where 24 species of stingless bees werefound. 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. Atthese censuses, 2 persons searched 4days/month. They also set 362 trap nests inthe field, of which 248 were perforatedbamboo stems and 114 wood boxes withglass tops. Trap nests were set in January1981 (100), December 1981/January 1982(138), December 1982 (75) and October1983 (49). Nests were observed during 56months. The results were:• trap nests were used by many animals, as
social insects (mainly ants) and vertebrates(geckos, for instance);
• only T. (Tetragonula) minangkabau occupiedthe 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 additionalnest sites offer could improve the bee densityin the area, and that trap nests are suitableonly for some bee species.
82
Antonini & Martins (2002) used nest trapsin Cerrado without any result, in an areawhere they found 46 nests of Meliponaquadrifasciata. Beekeepers sometimes men-tion that this bee species nests in abandonednests of Apis mellifera.
In Brazil, recently stingless bee’s keepersare using pet bottles as traps nests. In a bee-keeping meeting this year in Rio Grande doSul (III Encontro dos Meliponicultores) some ofthem reported that Tetragonisca angustulause these pet bottles. A deeper research onthis subject is urgent, and is suggested as arecommendation.
Recommendations
Key stingless bees species for large scalebreeding in Brazil The selection of some stingless bees’ speciesfor large scale breeding is needed. Theyshould be effective as pollinators, easy tomaintain in strong rational hives that couldbe transported, easy to multiply, with a highrange of temperature and humidity for flightactivity. Species should be selected for green-houses 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. Intable 1 there are indications of stingless beespecies already known as good pollinators.Our first selection should include:1.Tetragonisca angustula. This species has a
wide geographical range in Latin America.Very common in several habitats, includingcities, it frequently swarms, accepting artifi-cial traps for establishing new nests. Moredata on queen and males rearing in naturalnests, on queen rearing in vitro under labo-ratory conditions, and controlled reproduc-
tion of the queens under laboratory condi-tions are needed. The minimum populationof bees necessary to begin a new nest, aswell as their age composition must be eval-uated. This bee also produces a honey thatis considered as medicine, and how to con-serve it should be investigated. At thismoment, splitting colonies in two is possi-ble, but this is not enough to allow theirlarge use as pollinators.
2.Melipona quadrifasciata. The queen fer-tilization 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 imme-diately copulate. This result opens condi-tions for genetic manipulations of colo -nies. Besides, this bee can provide buzz pol-lination. Nevertheless the same result wasnot obtained with other Melipona speciesuntil now.
3.Melipona subnitida. In Northeast Brazil(dry regions, Caatinga) this bee species isbred for its honey, very appreciated by localpeople. Until now, their role as pollinatorwas studied in sweet pepper under green-house, with good results (Cruz, et al., 2005)
4.Melipona scutellaris. This species isalready used as a very good honey produc-er in Northeast Brazil, and bred by success-fully by beekeepers. Domesticated and welladapted in hives, this is one of the promis-ing species to be used as pollinators wherethey occur.
5.Nannotrigona spp. The use of Nan no -trigona in greenhouses was shown to beeffective in pollination. Very common inurban areas, and with a wide geographicalrange, must be studied concerning biologyand reproduction. The important resultsfrom Cauich, et al., 2004, in Mexico, show-ing that they are as effective in tomato pol-lination as other pollination treatments gives
Workshop I 83
to this genus a high importance for addi-tional investigation.
6. At least 9 species of stingless bees fromAmazon (Melipona spp., Aparatrigona spp.,Plebeia spp. and Scaptotrigona spp.) couldbe kept massively to be used on pollinationprograms. Tropical crops as cupuassu (Theo -broma grandiflorum), urucum (Bixa orel-lana), assai (Euterpe oleracea), hogplum(Spondias mombim), guaraná (Paulliniacupana) are some examples of Amazonplants witch demands pollination servicesfrom stingless bees.
Improving knowledge base1. Improve regional stingless bees collections
and the use of molecular techniques need-ed 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; nestssizes and densities.
5. Improve nests availability through theestablishment of ecological corridors.
6. Establish techniques for ecological restora-tion and pollinators.
7. Identify pollinators assemblages in eco-tones and fragments.
8. Promote stingless bees conservation inagricultural landscapes, also promotingheterogeneity in landscapes.
9. Study exotic and native pollinators’ ecolog-ical relationships.
10. Study species acceptation in trap nests ofdifferent materials.
11. Use molecular tools to evaluate: density ofcolonies; males provenience; population-characteristics; relatedness among nests;number of nearby nests (through the analy-sis of male clouds near the nest entrance, orby analyzing workers collected in a transect).
12.Develop metanalysis, data analysis andscientific publication diffusion of pollina-tors issues.
14. Improve techniques for nests developmentin hives.
15.Evaluate queen survivorship in the colony.16.Compare the characteristics of initial and
mature nests.17. Study sex-ratio and queen production in
selected species.18. Improve honey production, quality and
conservation.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 forimproving the local knowledge basis. Regionalgroups should be trained in standard method-ologies to apply in their region.
Improve capacity building and training inall levels, as well as concentrate studies innests requirements in order to implement thenew law 02000.006608.2000-81 concerningto stingless bees beekeeping.
Conservation of stingless bees in loggingareas is an important issue, due to the largeBrazilian area that will be used for logging inAmazon region.
Develop life history studies for a selectednumber of stingless bees species that arepotential generalist pollinators.
Provide literature in Portuguese and avail-able on line.
84
Table 1: Stingless bees used as crop pollinators
Crop
Averrhoa carambola(Oxalidaceae)carambola
Bixa orellana(Bixaceae)annatto
Capsicum annuum(Solanaceae)suit pepper
Cocos nucifera(Arecaceae)Coconut
Coffea arabica var.Bourbon (Rubiaceae)
Coffea arabica(Rubiaceae)
Coffea canephora(Rubiaceae)
Coffea canephora
Cucumis sativus(Cucurbitaceae)
Cucumis sativus(Cucurbitaceae)
Euterpe oleraceae –(Arecaceae) “assaí”
Fragaria x ananassa(Rosaceae)strawberry
Stingless BeePollinator (s)
In Malaysia, Trigonathoracica;
Melipona melanoventerand Melipona fuliginosa; Meliponaseminigra merrilae
Trigona carbonaria inAustralia; Meliponasubnitida
Apis mellifera and stinglessbees contribute to thepollination of this crop
Melipona spp.
Bee pollination
Bee biodiversity
Trigona (Lepidotrigona)terminate
Partamona bilineata
Scaptotrigona aff. depilis
Melipona melanoventer,Melipona flavolineata andMelipona fasciculata(Meliponinae, Apidae)
Tetragonisca angustula(Meliponini, Apidae)
Results
Efficient pollinator afterone visit
Buzz pollinated bystingless bees
M. subnitida increasedfruit weight (by 29%) andthe number of seed perfruit (86%); 65% decreaseof deformed fruit
Stingless bees are thedominant visitors in Costa Rica
Higher fruit set andheavier mature fruits
Coffee fruit set washigher in areas with highbee biodiversity (from 70to 95%)
84% fruit set
Frequent visitor
Higher fruit production,higher fruit weight andhigher % of perfect fruits
In development
"Oso Grande" cultivar100% primary flowersdeveloped; higher fruitfresh weight
Author
Phoon et al,1984
Maués & Venturieri,1995; Wille,1976;Absy & Kerr,1997
Cruz et al, 2005; Silvaet al, 2005
Hedström, 1988;Engel and Dingemans-Bakels, 1980
Nogueira-Neto et al1959
Roubik 2002
Klein et al, 2003a
Klein et al, 2003b
Meléndez et al., 2002
Santos et al, 2004
G. C. Venturieri et al,2005
Malagodi-Braga &Kleinert, 2004
Workshop I 85
Fragaria x ananassa(Rosaceae)strawberry
Lycopersicumesculentum(Solanaceae) tomato
Lycopersicumesculentum(Solanaceae)
Macadamia integrifolia(Proteaceae)Macadamia nut
Mangifera indica(Anacardiaceae)mango
Myrciaria dubia(Myrtaceae)camu-camu
Nephelium lappaceum(Sapindaceae)rambutam
Persea americana(Lauraceae) avocado
Persea americana(Lauraceae)
Psidium guajava(Myrtaceae) guava
Psidium guajava(Myrtaceae) guava
Salvia farinaceae(Labiatae)
Salvia splendens
Tetragonisca angustula(Meliponini, Apidae)
Nannotrigonapirilampoides
Melipona quadrifasciata
Trigona carbonaria(in Australia)
Stingless bees are themore common visitors;Tetragonisca angustula inChiapas
Melipona sp andScaptotrigona postica
Scaptotrigona mexicanaand Tetragoniscaangustula
8 species of stingless bees
Trigona nigra; N.pirilampoides
Pollen found in Meliponamarginata,T. spinipes andM. quadrifasciata potsFrieseomelitta spp.
M. subnitida
T. angustula and N.pirilampoides
Geotrigona spp. andPartamona
Sweet Charlie CultivarMisshapen fruit reducedby 86%
As effective as mechanicalvibration in terms of fruitset, fruit weight andnumber of seeds per fruit
Tomato flowers inabsence of vibration donot produce fruits
Yields and fruit qualitybenefit from beepollination
Important for crosspollination, Trigona beesmove from tree to tree.
Caged and openpollination treatmentsyielded a mean of 9.1times the mature fruit offlowers from which beeswere excluded
Efficient as pollinators
Potential efficientpollinators
Studies underdevelopment
together with solitarybees, are efficientpollinators
Produce good qualityseeds in greenhouses
Malagodi-Braga &Kleinert, 2004
Macias & Macias,2001; Cauich et al,2004
Del Sarto et al, 2005
Heard, TA; 1987
Simão & Maranhão,1959
Peters & Vasquez,1986
Rabanales et al, inpress
Ish-am et al., 1999
Can-Alonso et al,2005
Kleinert –Giovannini &I-Fonseca, 1987Castro, p.c.
Alves & Freitas, 2005
Slaa et al, 2000
Bustamante 1998
86
Sechium edule(Cucurbitaceae)chayote, choko
Spondias tuberosa(Anacardiaceae)“umbu” or “imbu”
Theobromagrandiflorum(Sterculiaceae)cupuassu
Theobromagrandiflorum(Sterculiaceae)“cupuassu”
Paullinia cupana(Sapindaceae) guarana
28 stingless bees speciesare important visitors; T.corvina and Partamonacupira are important
Frieseomelitta languidaand T. angustula
Plebeia minima and smallweevils. Most plantas areself incompatible;Ptilotrigona lurida may bea pollinator
Plebeia spp., Paratrigonaspp. & Frieseomelitta spp.(Meliponini, Apidae)
Melipona spp
Stingless bees enhancefruit production
In development
In development (Probio)
together with Apismellifera
Wille et al. 1983
M. S. Castro
Venturieri, GA et al,1993
R. Gribel
Aguilera, FJP, 1983
References
BATISTA, M.A, RAMALHO, M. & SOARES, A.E.E. 2003. Nesting sites and abundance of Meliponini(Hymenoptera: Apidae) in heterogeneous habitats of the Atlantic Rain Forest, Bahia, Brazil.Lundiana, 4 n.1: 19-23.
BIESMEIJER, J.C., SLAA, J., CASTRO, M.S., VIANA, B. F., KLEINERT, A. M. P. & IMPERATRIZ-FONSE-CA, V.L. 2005. Connectance of Brazilian social bee-food plant networks is influenced by habitat,but not latitude, altitude or network size. Biota Neotropica, 5, n.1: 1-10.
BRITO, A. S. 2002. Toxicidade de praguicidas usados no controle da mosca branca Bemisiaargentifolii (Hemiptera, Aleyrodidae), para as abelhas sem ferrão do gêneroScaptotrigona (Hymenoptera, Apoidea). Monografia de conclusão de curso. UniversidadeEstadual de Feira de Santana, Bahia.
CASTRO, M. S. 2001. http://www.webbee.org.br/bpi/pdfs/livro04castro.pdf
CAUICH O., J.J.G. QUEZADA-EUÁN, J. O., MACIAS-MACIAS, V. REYES-OREGEL, S. MEDINA-PER-ALTA, AND V. PARRA-TABLA. 2004. Behavior and pollination efficiency of Nannotrigona perilam-poides (Hymenoptera: Meliponini) on greenhouse tomatoes (Lycopersicum esculentum) inSubtropical México. Horticultural Entomology, 97 n.2: 475-481.
CONAMA_346. 2004. http://www.mma.gov.br/port/conama/index.cfm).
Workshop I 87
DE MARCO J.R., P & COELHO, F.M. 2004. Services performed by the ecosystem: forest remnantsinfluence agricultural cultures’ pollination and production. Biodiversity and Conservation, 13:1245-1255.
DEL SARTO, M.C.L., PERUQUETTI, R.C. & CAMPOS, L.O. 2005. Evaluation of Neotropical stinglessbee Melipona quadrifasciata (Hymenoptera, Apidae) as pollinator of greenhouse tomatoes.Journal of Economic Entomology, 98 n.2: 260-266.
ELTZ, T., BRUHL,C.; VAN DER KAAS, S.;LINSENMAIR, K.E. 2002. Determinants of stingless bees nestdensity in lowland dipterocarp forest of Sabah, Malaysia. Oecologia, 131: 27-31.
ELTZ,T., BRÜHL, C, ZANRIE, I & LINSENMAIR, K.E. 2003. Nesting and nest trees of stingless bees(Apidae, Meliponinae) in lowland dipterocarp forests in Sabah, Malaysia, with implications for for-est management. Forest Ecology and Management, 172: 301-313.
MALAGODI-BRAGA, K.S. (2002) Estudo de agentes polinizadores em cultura de morango(Fragaria x ananassa Duchesne – Rosaceae). Thesis (PhD). Universidade de São Paulo, SãoPaulo - SP, Brazil. 102p.
MALAGODI-BRAGA, KS & KLEINERT, AMP 2004 Could Tetragonisca angustula Latreille (Apinae,Meliponini) be used as strawberry pollinator in greenhouses? Australian Journal of AgriculturalResearch, 55 n.7: 771-773.
MORAES, S. S., BAUTISTA, AR.L. & VIANA, B. F. 2000. Avaliação da toxicidade aguda (DL50 eCL50) de inseticidas para Scaptotrigona tubiba (Smith) (Hymenoptera: Apidae): via de contato.Soc. Entomol. Brasil, 29 n.1: 31 - 37
NOGUEIRA-NETO, P. 1997. Vida e criação de abelhas indígenas sem ferrão. Editora Noguei -rapis, São Paulo – SP, Brazil, 446p.
PORTUGAL–ARAÚJO, V. de. 1955. Colméias para abelhas sem ferrão-Meliponini. Bol. Instituo deAngola, 9 n. 7: 9-31.
RAMALHO, M., KLEINERT-GIOVANNINI, A. & IMPERATRIZ-FONSECA, V.L. 1990. Important beeplants for stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) inneotropical habitats: a review. Apidologie, 21: 469-488.
RICKETTS, H.T. 2004. Tropical forest fragments enhance pollinators activity in nearby coffee crops.Conservation Biology, 18 n.5: 1262-71.
RICKETTS, H. T., DAILY, G.C., EHRLICH. P. R. & MICHENER, C.D. 2004. Economic value of tropicalforest to coffee production. Proc. of National Academy of Sciences, 101 n.34: 12579-12582.
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 InternationalConference on Tropical Beekeeping and VI Encontro sobre Abelhas, Ribeirão Preto, SãoPaulo – SP, Brazil, in CDROM.
SAMEJIMA, H., MARZUKI, M., NAGAMITSU, T. & NAKASIZUKA, T. 2004. The effects of human dis-turbance on a stingless bee community in a tropical rainforest. Biological Conservation, 120:577-587/j.biolcon.2004.03.30.
88
SILVA, G.F., VENTURIERI, G.C. & SILVA, E.S.A. 2004. Meliponiculture as a sustainable developmentalternative: financial management within family groups in northeast Amazon, Brazil. In: FAOreport, 12p.
VENTURIERI, G.C. 2003. Meliponicultura I: Criação de Abelhas Indígenas Sem Ferrão, CaixaRacional para Criação. Rec. Téc, Embrapa Amazônia Oriental, Belém – PA, Brazil.
VENTURIERI, G.C. 2004. Forest exploitation and its impact on the Amazonian stingless bees. InFAO report, Best management practices in Agriculture for sustainable use and conservationof pollinators.
VENTURIERI, G.C., RAIOL, V.F.O. & PEREIRA, C.A.B. 2003. Avaliação da introdução da criaçãoracional de Melipona fasciculata (Apidae, Meliponina) entre os apicultores de Bragança, PA, Brasil.Biota Neotropica, 3 n.2. On line http://www.biotaneotropica.org.br/v3n2
WORKSHOP II
Pollinator Initiatives and the role of InformationTechnology (IT): building synergism and cooperation
Workshop II 91
Abstract
The São Paulo Declaration on Pollinators plus5 Forum was organized by the BrazilianPollinators Initiative, BPI, and held in SãoPaulo with the support of FAO to discuss stan-dardized methodologies for assessing pollina-tor’ status and management practices to stoptheir decline.
The main objectives of the IPI (Inter -national Pollinators Initiatives, in which BPItake 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 and
the economic impact of the decline of polli-nation services;
• promote the conservation, the restora-tion and sustainable use of pollinatordiversity in agriculture as well as in relat-ed ecosystems;
Those tasks demand a huge effort,including a lot of data acquisition (in thefield and in laboratory), and data analysisfor 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 policymaker, 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 thePollinator Initiatives, to help promote partner-ships and exchange experiences on the devel-opment and use of those technologies, andto discuss funding opportunities.
This event was designed as an extensionof the Forum, open to all of its participants.
Workshop objectives
The purpose of this workshop was to discussthe role of Information Technologies (IT) forthe development and for the effectiveness ofthe Pollinators Initiatives in a broad sense,from building a species catalog to providingknowledge for policy making.
The program included reviews of relevantactivities and broader trends in biodiversity infor-matics, and their impact for Pollinators Initiatives.
Efforts, from local to global, were present-ed and their relationships and contributions tothe larger goals were discussed, as well as thepossibilities of networking and of sharingtools, systems and data. Funding opportunitieswas another important topic discussed.
Organization and content
Organizing CommitteeAntonio Mauro Saraiva, Escola Politécnica,Universidade de São Paulo.Vanderlei Perez Canhos, Centro de Refe rên -cia 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 Pau -lo. It was organized as a series of presentationsof local, regional and global initiatives and proj-ects followed by discussion on broader issues.
The local (Brazilian) initiatives presented:• WebBee – The WebBee project, an infor-
mation network on bee diversity was pre-sented by prof. Antonio Mauro Saraiva,from Escola Politécnica - USP, AgriculturalAutomation 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 an
electronic journal on pollinator biology waspresented by prof. David de Jong, fromGenetics Department, Faculdade de Me dicina,Universidade de São Paulo – FMRP-USP, Brazil.
• speciesLink - The speciesLink project, thatintegrates many biological collections waspresented by prof. Vanderlei Peres Canhos,from Reference Center of EnvironmentalInformation - CRIA, Brazil
.The regional initiatives presented:• the International Centre for Integrated
Mountain Development (ICIMOD), waspresented by Dr. Uma Partap and Dr. FarooqAhmad, from ICIMOD, Nepal .
• the North American Pollinators Initiative(NAPI), was presented by Dr. Mike Ruggiero,from the International Taxonomy Infor ma tionService (ITIS) and the National Museum ofNatural 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, fromUniversity of Guelph, Canada.
• the African Pollinators Initiative (API), waspresented by Dr. Barbara Gemmil, fromEnvironment Liaison Center International(ELCI) (Kenya) and Dr. Connal Eardley, fromAgricultural Research Council, Plant Protec -tion Research Institute, South Africa.
• the IABIN Pollinators Network and the NewWorld 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 AgricultureOrganization (FAO).
Discussion
The topics suggested for discussion were:• towards a common agenda - building the
shared infrastructure;• how to integrate actions; • standards, protocols and systems interop-
erability;• on-line directory of institutions, experts, pro-
grams and projects;• on-line databases: taxonomic authority files,
specimen DB, species DB, phenologicaldatasets for meta-analysis;
• computational tools for data mining, analy-sis, synthesis and visualization;
• funding opportunities and co-financing re -quirements - 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 the
development and sharing of the IT infrastruc-ture required for the Pollinator Initiatives: toolsand systems developers and data providers;
• the identification of funding opportunitiesfor the development of the IT infrastructureon a local, regional and global scale.
Introduction
As was pointed out by Saraiva & Imperatriz-Fonseca (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 and
the economic impact of the decline of polli-nation 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 oranother those objectives involve issues relatedto data, information and knowledge: theiracquisition and analysis, their transformationfrom raw data to useful knowledge, their usefor sound decision and policy making, theirdissemination for wider audiences to increaseawareness and education.
Those are typical tasks for InformationTechnology in a broad sense and, more specif-ically speaking, those are simply the goals ofBiodiversity Informatics, a new discipline ordenomination created to deal with the appli-cation of IT to Biodiversity.
The complexity of biodiversity and itsprocesses, the huge figures involved, theamount of variables and data that are to bedealt 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 resultsand 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 experi-ments, on data analysis, i.e., on turning datainto information and knowledge.
As for the taxonomic information, on onehand the information gathered after decadesand maybe centuries of research is not readilyavailable even for the scientific communitybecause it is spread around the world in muse-um collections or the like. Digitizing the collec-tions and publishing them on the Internet willincrease the accessibility while still providingcontrol 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 embed-ded in computer programs.
Once data is acquired, different types ofanalysis need to be made taking into accountthe species distribution, the effect of changeson the environment, the economic value andimpact, and different strategies for conserva-tion, restoration and use. These analyseswould benefit from the use of simulation toolsthat can be used to develop different scenariosupon 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 polli-nators and the risk of their decline. The internetcan play a very important role on that. However,the web can also have a strategic function forthe integration of the research community,which can share data, communicate and coop-erate 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 advantagesand importance of the use of IT tools and tech-niques to help achieve the goals of theInternational Pollinators Initiative and of thenational/regional PIs. The project Conservationand Management of Pollinators for SustainableAgriculture Through an Ecosystem Approach,under the auspices of FAO and GEF, will requirean intensive use of IT on the development of itsfour components. The preliminary phase of theproject, the PDF-B phase, will provide anopportunity to review, identify and analyzegaps on the technology regarding its applica-tion to the PIs. The full-size project that willsubsequently be developed may accommodatepart of that development.
According to what was presented, soft-ware tools seem to be the most widely usedcomponents. Websites for various purposeswere reported for all PIs though their contentand complexity differed significantly. In somecases, simple webpages are used to conveyproject information, educational information,etc. Despite that simplicity, their effectivenessis acknowledged and they fulfill some basicneeds of the developers and users.
At a higher level, there are the databasesthat can be accessed via Internet. Specimeninformation from biological collections atmuseums, for instance, is being digitized and isincreasingly available on-line. Though the per-centage of the specimens of the known world’scollections that is already available on-line issmall, that number is increasing consistentlyand some international and global efforts inthat direction were mentioned. It was stressedthe need to join and to strengthen that digiti-zation effort, which faces many difficultiesrelated to funding and data ownership.
This brings up the problem of the integra-tion of all that data. Such integration is impor-tant for many different purposes, such as forbuilding a global catalogue of life on Earth (such
as the Catalogue of Life, from Species 2000 andITIS ), and for creating checklists of species andresolving naming problems. Further use of inte-grated data is made by analysis software, suchas that for modeling species distribution, extinc-tion risk, and protection strategies. Analysestools are of utmost importance as they can beused to guide the development of environmen-tal public policies on a more solid foundation.
This integration requires the use of stan-dards 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 essentialto allow more seamless access to and share ofbiological data. It was suggested that FAO andGEF should participate of that effort. An exam-ple of the use of those standards to integratedifferent sources via internet was presented atthe SpeciesLink project .
As the use of such information increasesin 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 peer-reviewed journal on pollinators and pollinationis being designed within the BPI, and it wassuggested that this journal should be support-ed within the FAO/GEF project. Such a journalwould both facilitate information exchangeand encourage research and publications onpollinators, especially in the developing coun-tries. Much research on pollinators and pollina-tion in developing has been traditionally donein a haphazard manner, and often the resultsare not readily accessible. A specific journal onpollinators would both provide means to guideand improve such research, through examplesand through peer review, and would also facil-itate publication of such information.
Workshop II 95
It is important that other media, such asimages and videos, be used to convey infor-mation via internet. They must be comple-mented by texts but they have a strong impactand should be incorporated especially for spe-cific audiences and for some purposes. Anexample of an information system that isbased on species information (rather than onspecimen information) and which makesintensive use of visual information was pre-sented on the project WebBee.
Another set of IT tools not very muchmentioned was instrumentation, though itbecame 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 ofthe standard methodologies discussed at theother workshops of the Forum. Part of theWebBee project involves the development anduse of a set of instruments applied to pollina-tors monitoring. Those experiments can beaccessed via internet and can be sharedamong many users collaboratively.
Difficulties and recommendations
Along with the discussions that arose duringthe workshop sessions one important point thatstood out was the need for IT support person-nel. Most institutions that were present at theworkshop do not have IT support personnel orat least not at level required nowadays, consid-ering systems development and infrastructure.
Another issue related to support is themaintenance of such systems. Many of themare developed with funds from research proj-ects but it is often hard obtain funding for sus-taining them on the long term. The sameapplies to the issue of updating the systemwith new information and data: that task
requires people and this is sometimes forgot-ten, and often hard to obtain funding.
Considering the end-users that are expect-ed 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 atthe 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 del-icate, both at the personal level and at thecountry level, since national legislation differand sometimes restrict the access to biologicaldata fearing biopiracy.
Final remarks
The workshop provided a very good opportu-nity to show to the audience a wide range ofcases, tools, systems and initiatives regardingthe application of IT to pollinators and pollina-tion and related areas. For a significant part ofthe audience some of the topics covered pre-sented novelties. The presence of a public withmany end-users was important to help collecttheir feelings and experiences with respect tothe technology. It also allowed a discussionabout some critical issues, technical and politi-cal, that must be dealt with so that IT can beeffective for the Pollinators Initiatives; and pro-moted opportunities for strengthening con-tacts and relationships, for showing areas ofinterest and competencies that may evolve tofuture cooperation, which is a central part ofthe IPI and of the GEF/FAO project.
The workshop achieved its expectedresults and, being the first of its kind, showedthe 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 Beesand VI Encontro sobre Abelhas, 2004, Ribeirão Preto, Brazil. Proceedings. International BeeResearch Association – IBRA; FFCLRP-USP, 2004. CDROM.
ILLUSTRATIONS AND PHOTOGRAPHS
Xylocopa bee pollinating aLecythis pisonis flower.
Copyright Michael
Rothman 1999. Courtesyof the New York Botanical
Garden, Institute ofSystematic Botany
Solitary bees are specialized pollinators. Centris is important for cashew pollination. Above left, nests of EpicharisDejeanii; above right, nest of Ptilothrix plumata; below left, nest of Centris tarsata. Solitary bees can be attracted to trapnests (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 inwww.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.
