Bees As Pollinators in Brazil Conservation and Sustainable Use of Pollinators, Hereafter Referred to As the International Pollinator Initiative (IPI)

Home , Melipona, Melipona quadrifasciata, Ptilothrix, Scaptotrigona postica, Warwick Estevam Kerr

The São Paulo Declaration on Pollinators, was endorsed in May 2000 by the fifth Conference of Parties of Convention of Biological Diversity (COP5), held in Nairobi (section II of the decision v/5, that reviewed the implementation of decisions III/11 and IV/6 on the program of work on agrobiodiversity). COP5 established an International Initiative for the Bees as pollinators in Brazil Conservation and Sustainable Use of Pollinators, hereafter referred to as the International Pollinator Initiative (IPI). Bees as pollinators in Brazil assessing the status and suggesting best practices A Plan of Action was then prepared by Food and Agricultural Organization of the United Nations (FAO) and the CBD Secretariat, endorsed by SBSTTA7, and recommended for adoption by CBD COP6. The Plan of Action of the IPI was accepted by member countries and adopted at COP 6 (decision VI/5).

Since then, most regions of the world have established or are in process of establishing wide-ranging pollinators initiatives. The core objectives of 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 of assessing the status and suggesting best practices the decline of pollination services • Promote the conservation, the restoration and sustainable use of pollinator diversity in agriculture as well as in related ecosystems Edited by Vera Lucia Imperatriz-Fonseca, Antonio Mauro Saraiva, David De Jong To follow this agenda, the Brazilian Pollinators Initiative, under the support of FAO, Ministry of Environment, Ministry of Science and Technology and Sao Paulo University, promoted the workshop São Paulo Declaration on Pollinators Plus 5, in October 2003 . We joined the regional Initiatives, discussed common routes and some essential points: standardized methodologies, pollinators declining and management practices. This book concerns the results of group discussions in the workshop São Paulo Declaration on Pollinators Plus 5, and was printed with a support from Conservation International-Brasil

HOLOS EDITORA ISBN 85-86699-51-9 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 Pollinators plus 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 Editors Cynthia Pinheiro-Machado; Fernando A. Silveira; Claudia Maria Jacobi; Breno Magalhães Freitas; Marina Siqueira de Castro

Ribeirão Preto 2006 Workshop Sponsors Food and Agriculture Organization (FAO) Ministry of Environment (MMA) Ministry of Science and Technology (MCT) São Paulo University (USP)

Printer Sponsors Conservation International – Brazil Brazilian Pollinator Initiative

Editorial assistance Tarcila Lucena

Book design Renata Carpinetti ([email protected])

Cover Melipona compressipes fasciculata (Apidae, Meliponini) pollinating assai flowers (Euterpe oleracea - Arecaceae) Photo by Giorgio C. Venturieri

Catalog for International Publication

Bees as pollinators in Brazil: assessing the status and suggesting best practices / Vera Lucia Imperatriz Fonseca, ed.; Antonio Mauro Saraiva, ed.; David de Jong, ed. Ribeirão Preto: Holos, Editora, 2006, 112 pp.

Workshop on São Paulo Declaration on Pollinators Plus 5 Forum, São Paulo, 2003.

1. Pollinators – agriculture. 2. Bees – use and conservation. I. Imperatriz-Fonseca, V.L.II. Saraiva, A.M. III. De Jong, D. IV Holos Editora. Environment. V. Title

ISBN 85-86699-51-9

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

Paulo Nogueira-Neto

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

Warwick Estevam Kerr

Pioneer in the study of bee genetics in Brazil, focusing especially on the Meliponini. During all of his life, he has encouraged and supported the rearing of these bees, creating regional research groups across the country and disseminating the importance of the environmental services provided by pollinators.

Both have inspired us with their principles, stimulation and dedication to science. Acknowledgements

The Workshop São Paulo Declaration on Pollinators plus five involved a team with different profiles, and several institutions. Concerning the organization, we thank especially the dedication of Fernando A. Silveira, Cynthia Pinheiro Machado, Claudia Maria Jacobi, Rogério Gribel, Breno Magalhães Freitas, David de Jong, Lionel Segui Gonçalves, Marina Siqueira de Castro. Also, we thank the cooperation of Bee Laboratory from Instituto de Biociências, University of São Paulo, mainly to Mariana Imperatriz Fonseca, Denise de Araújo Alves, Favízia Freitas de Oliveira, Marilda Cortopassi-Laurino and Patrícia Nunes Silva, in all steps of this process that ends with this publication.

Financial support was obtained from several sources, and we thank their representatives: FAO – Linda Collette, for her collaboration and outstanding help; Brazilian Ministry of Environment – Paulo Y. Kageyama, Braulio Ferreira de Souza Dias e Marina Landeiro who have participated in all steps of this work; Brazilian Ministry of Science and Technology - Regina P. Markus, for her advice and collaboration in the workshop; University of São Paulo (USP) and Fundação de Apoio à USP (FUSP) – Mr. Kem Yoshida.

We would also like to thank some institutions and specialists: Polytechnic School of the University of São Paulo that has sponsored the workshop on Information Technology and Pollinators Initiative, and the team from the Agricultural Automation Laboratory and WebBee project, especially Tereza Cristina Giannini, Etienne Americo Cartolano Júnior and Renato Sousa da Cunha for the workshop’s website and Vanderlei Canhos from Reference Center of Environmental Information (CRIA), for his collaboration in the organization. The Ecofuturo welcomed the participating group in their field trip to Mata Atlântica that was very much appreciated.

Finally, for the printing of this book we have received the support from Conservation International Brazil.

The Editors. 9

Summary

Acronyms 16 Presentation 17 Worshop preparation 17 International Pollinators Initiatives 18 Methodological discussions 19 Protocols and discussions 19 Information Technology and Pollinators Initiatives 20 References 21 Worshop I: Survey methods for bees as pollinators in Brazil: assessing the status and suggesting best practices 23 Group 1: Surveying and monitoring of pollinators in natural landscapes and in cultivated fields 25 Group 2: Assessment of pollinator – mediated gene flow 39 Group 3: Bee management for pollination purposes 53 A) Bumble bees and solitary bees 55 B) Honey bee 63 C) Stingless bees 75 Worshop II: Pollinator Initiatives and the role of Information Technology (IT) 89 Illustrations and photographs 97 10

The participants on both workshops were

Adriana De Oliveira Fidalgo, Instituto de Braulio Ferreira de Souza Dias, Secretaria Botânica, Divisão do Jardim Botânico de São de Biodiversidade e Florestas do Ministério do Paulo, Seção de Ecologia. Avenida Miguel Meio Ambiente. SAIN Av. L4 Norte, Campus Estefano 3687, Água Funda 01061-970, Sede do IBAMA, Bloco H, CEP 70.800-200 São Paulo, SP, BRAZIL, Caixa-Postal: 4005, Brasília, DF, Brasil Tel. +5561 325-41-85 ou Telefone: (11) 50736300, Ramal: 298, Fax: 317-1120, Fax +5561 325-5755; (11) 50733678 [[email protected] & [email protected] ] Alfred Ochieng, ICIPE, P.O.Box 30772, Nairobi, KENYA, Tel: +254 2 861680-4, Breno Magalhães Freitas, Departamento de Fax: +254 2 860110 [[email protected]]. Zootecnia, Universidade Federal do Ceará, Campus Universitário do PICI, Caixa Postal Anthony Raw, Laboratório de 12168, CEP 60355-970, Fortaleza, Ceará, Entomologia, Departamento de Ciências BRAZIL [[email protected]]. Biológicas, Universidade Estadual de Santa Carmen Silvia Soares Pires, Laboratório de Cruz (UESC), Rodovia Ilhéus-Itabuna, Bioecologia e Semioquímicos, Centro Km 16, CEP 45650-000, Bahia, BRAZIL, Nacional de Pesquisa de Recursos Genéticos e Tel: +55 73 680-5261 Biotecnologia, Empresa Brasileira de Pesquisa [[email protected]]. Agropecuária (EMBRAPA), Sain Parque Rural - Antonio Mauro Saraiva, Laboratório de W5 Final, Asa Norte, CEP 70849-970, Brasília, Automação Agrícola, Departamento de DF, BRAZIL, Tel: +55 61 448-4682 Engenharia de Computação e Sistemas [[email protected]]. Digitais, Escola Politécnica, Universidade de Celso Feitosa Martins, Departamento de São Paulo, Av. Prof. Luciano Gualberto, Sistemática e Ecologia (CCEN), Universidade Travessa 3, número 158, sala C2-54, CEP Federal da Paraíba, CEP 58059-900, João 05424-970, Cidade Universitária, São Paulo, Pessoa, Paraíba, BRAZIL São Paulo, BRAZIL, Tel: +55 11 3091-5366 [[email protected]]. [[email protected]]. Claudia Maria Jacobi, Departamento de Astrid de Matos Peixoto Kleinert, Biologia Geral, Universidade Federal de Minas Departamento de Ecologia Instituto de Gerais, Avenida Antônio Carlos 6627, Caixa Biociências, Universidade de São Paulo (USP), Postal 486, CEP 30161-970, Belo Horizonte, Rua do Matão, travessa 14, nº 321 Cidade Minas Gerais, BRAZIL Universitária, CEP 05508-900, São Paulo, [[email protected]]. São Paulo, BRAZIL, Tel: +55 11 30917604 Clemens Peter Schlindwein, Departamento [[email protected]]. de Botânica, Centro de Ciências Biológicas, Barbara Gemmill (Herren) Global Pollination Universidade Federal de Pernambuco (UFPE), Project Coordinator, Food and Agriculture Av. Prof. Moraes Rêgo s/n, Cidade Organization of the United Nations, viale Universitária, CEP 50670-901, Recife, delle Terme di Caracalla Rome, 00100, Italy, Pernambuco, BRAZIL, Tel: +55 81 3271-8352 [[email protected]] [[email protected]] Participants I 11

Connal Eardley, Bee Systematists & Dieter Wittmann, Institut für SAFRINET Co-ordinatos, Plant Protection Landwirtschaftliche Zoologie und Research Institute Agricultural Research Bienenkunde, Melbweg, 42, University of Council, Plant Protection Research Institute, Bonn, Bonn, 53127, GERMANY Private Bag X134, Queenswood, 0121, South [[email protected]]. Africa, 590 Vermeulen Street, Pretoria, Dirk Koedam, Departamento de Ecologia, SOUTH AFRICA, Tel +27 (0)12 - 304 9578, Instituto de Biociências, Universidade de São Fax +27 (0)12 325 6998 Paulo (USP), Rua do Matão, Travessa 14, [[email protected]]. nº 321, CEP 05508-900, Cidade Universitária, Cynthia Almeida Pinheiro Machado, São Paulo, São Paulo, BRAZIL, Tel: +55 11 Fundação Integrada Municipal de Ensino 3091-7533 [[email protected]]. Superior, Rua 22 esq. c/ Av. 01, Setor Eda Flávia Lotufo Rodrigues Alves Aeroporto, CEP 75830-000 - Mineiros, GO - Patrício, Laboratório de Abelhas, BRAZIL, Tel.: (64) 36611970 Departamento de Ecologia, Instituto de Fax: (64) 38134151, [[email protected]], Biociências, Universidade de São Paulo (USP), www.fimes.edu.br Rua do Matão, travessa 14, nº 321, CEP 05508-900, Cidade Universitária, São Paulo, David De Jong, Departamento de Genética, São Paulo, BRAZIL, Tel: +55 11 3091-7533. Faculdade de Medicina, Universidade de São Paulo (FMRP-USP), CEP 14049-900, Edivani Vilaron Franceschinelli, Ribeirão Preto, São Paulo, BRAZIL, Universidade Federal de Goiás, Instituto de Tel: +55 16 602-4401, fax +55 16 633-6482 Ciências Biológicas, Departamento de Biologia [[email protected]]. Geral, Campus II - Samambaia - ICB1 - 2 andar, Campus Samambaia, CEP 74001970, David W. Roubik, Smithsonian Tropical GOIANIA, GO, BRAZIL, Caixa-Postal: 131, Research Institute, Unit 0948, APO AA Tel.: (62) 5211112, Fax: (62) 5211109, 34002-0948or APDO 2072 Balboa, REPUBLIC [[email protected]], www.icb.ufg.br OF PANAMÁ [[email protected] / [email protected]]. Farooq Ahmad, Indigenous Honey Bee Project, International Centre for Integrated Denise de Araújo Alves, Laboratório de Mountain Development (ICIMOD), P.O Box Abelhas, Departamento de Ecologia, Instituto 3226, Kathmandu, NEPAL, Tel: 09977-1- de Biociências, Universidade de São Paulo 5525313, Fax 00977-1-5524509 (USP), Rua do Matão, travessa 14, nº 321, [[email protected]]. CEP 05508-900, Cidade Universitária, Favízia Freitas de Oliveira, Universidade São Paulo, São Paulo, BRAZIL, Estadual de Feira de Santana, Departamento Tel: +55 11 3091-7533 [[email protected]]. de Ciências Biológicas, Laboratório de Denise Monique Dubet da Silva Mouga, Sistemática de Insetos Lasis, Av. Universitária Departamento de Ciências Biológicas, Pró S/N, Km 03 - BR 116 (Rodovia Feira de Reitoria de Ensino, Universidade da Região de Santana - Serrinha) - Cidade Universitária, Joinville (UNIVILLE), Campus Universitário, s/n, CEP 44031460, Feira de Santana, BA, Bom Retiro, CEP 89201-972, Joinville, Santa BRAZIL, Tel: (75) 32248194, Fax: (75) Catarina, BRAZIL, Tel: +55 47 461-9000 32248019, [[email protected]] r. 9072 [[email protected]]. http://www.uefs.br/dcbio/lent_sis/index.html 12

Felipe Andrés Leon Contrera, University of Gisele Garcia Azevedo, Departamento de California - Berkeley, University Of California, Biologia Centro de Ciências da Saúde, San Diego - USA, [[email protected]] Universidade Federal do Maranhão (UFMA), Av. dos Portugueses s/n, CEP 65040-080, Fernando Amaral da Silveira, Laboratório Bacanga, São Luis, Maranhão, BRAZIL, Tel: de Sistemática e Ecologia de Abelhas, +55 98 32178542 [[email protected]]. Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Guiomar Nates Parra, Laboratorio de Minas Gerais (UFMG), Avenida Antônio Investigación en Abejas (LABUN), Carlos 6627, Caixa Postal 486, CEP 31270- Departamento de Biología, Universidad 901, Belo Horizonte, Minas Gerais, BRAZIL Nacional de Colombia, A.A. 144590, Bogotá, [[email protected]]. COLOMBIA, S.A, Tel: +3165000 ext. 11335/11337, Fax 3165310 Fernando César Vieira Zanella, [[email protected]]. Departamento de Engenharia Florestal, Centro de Saúde e Tecnologia Rural, Universidade Isabel Alves dos Santos, Instituto de Federal de Campina Grande (UFCG), Bairro Biociências da USP, Rua do Matão 321 trav do Jatobá, CEP 58700-970, Jatobá – Patos, 14, Cidade Universitária, 05508-900, São Paraíba, BRAZIL, Tel: +55 83 421-3397 Paulo, SP, BRAZIL,Tel: (11) 30917527 [[email protected]]. Fax: (11) 30917600, [[email protected]]

Flavia Monteiro Coelho Ferreira, Jacobus Christiaan Biesmeijer School of Universidade Federal de Viçosa, Centro de Biology.University of Leeds.Leeds LS2 9JT, Ciências Biológicas e da Saúde, UNITED KINGDOM. Departamento de Biologia Geral, Avenida P. [[email protected]]. H. Holfs, s/ número, CEP36570-001 - Vicosa, MG - BRAZIL, Tel.: (31) 38991178 James H. Cane, Bee Biology and Systematics [[email protected]], http://www.ufv.br Laboratory, Utah State University, 5310 Old Main Hill, Logan, Utah 84322-5310, USA, Francisco de Sousa Ramalho, Centro Tel: +01 435 797-3879, Fax 435-797-0461 Nacional de Pesquisa de Algodão, Unidade [[email protected]]. de Controle Biológico, Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA), Jesus Santiago Moure, Departamento de Rua Osvaldo Cruz 1143, Centenário, Zoologia, Setor de Ciências Biológicas, CEP 58107-720, Campina Grande, Paraíba, Universidade Federal do Paraná (UFPR), BRAZIL, Tel: +55 83 341-3608 Centro Politécnico, Caixa Postal 19020, CEP [[email protected]]. 81531-980, Jardim das Américas, Curitiba, Paraná, BRAZIL, Tel: +55 41 361-1671, Fax: Giorgio Cristino Venturieri, Centro de +55 41 266-2042 [[email protected] / Pesquisa Agroflorestal da Amazônia Oriental, [email protected]]. Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA - Amazônia Oriental), João Israel Bernardo, Centro Federal de Tv. Dr. Enéas Pinheiro, s/nº, CEP 66095100, Educação Tecnológica do Paraná, Conselho Marco – Belém, Belém, Pará, BRAZIL, Diretor, Unidade do Sudoeste, Rodovia PR- Tel: +55 91 2994500 r. 4697 469 (via do Conhecimento) km01 Fraron, [[email protected]]. CEP 85501-970 , Pato Branco, PR , BRAZIL, Participants I 13

Caixa Postal 571, Tel: +55 46 2202511, Fax: Tel: +55 16 602-3054, Fax +55 16 633-6482 +55 46 2202500, [[email protected]], URL [[email protected]]. da Homepage: http://www.pb.cefetpr.br Lucio Antonio de Oliveira Campos, João Rodrigues de Paiva, Centro Nacional Departamento de Biologia Geral, Centro de de Pesquisa de Agroindústria Tropical, Ciências Biológicas e da Saúde, Universidade Empresa Brasileira de Pesquisa Agropecuária Federal de Viçosa (UFV), Av. P. H. Rolfs, s/n, (EMBRAPA), Rua Dra. Sara Mesquita, 2270, CEP 36571-000, Centro, Viçosa, Minas Planalto do PICI, CEP 60511-110, Fortaleza, Gerais, BRAZIL, Tel: +55 31 3899-1299 Ceará, BRAZIL, Tel: +55 85 3299 1864 [[email protected]]. [[email protected]]. Márcia de Fátima Ribeiro, Universidade Kátia Peres Gramacho, Faculdade de Federal do Ceará, Depto. de Zootecnia, Bloco Tecnologia e Ciências, Somesb, Salvador, Av. 948, campus do Pici, Grupo de Pesquisas Luis Viana Filho s/n, CEP 41730006, Salvador, com Abelhas BA, BRAZIL, Tel: +55 71 2818000 r. 8102 Fax: +55 71 2818019, [[email protected]], Antonio Bezerra, CEP 60021-970, URL da Homepage: http:\\www.ftc.br Fortaleza, CE, BRAZIL, Caixa Postal: 12168, Tel: +55 85 40089697 Fax: +55 85 Kátia Sampaio Malagodi Braga, 40089701, [[email protected]], URL da Laboratório de Abelhas, Departamento de Homepage: http://www.abelhas.ufc.br Ecologia, Instituto de Biociências, Universidade de São Paulo (USP), Rua do Márcia Maria Corrêa Rêgo, Departamento Matão, travessa 14, nº 321, CEP 05508-900, de Biologia, Centro de Ciências da Saúde, Cidade Universitária, São Paulo, São Paulo, Universidade Federal do Maranhão (UFMA), BRAZIL, Tel: +55 11 3091-7533 Av. dos Portugueses, s/n Campus [[email protected]]. Universitário do Bacanga, Bacanga, CEP 65080-040, Sao Luis, Maranhão, BRAZIL, Tel: Lílian Santos Barreto, Empresa Baiana de +55 98 217-8544 [[email protected]]. Desenvolvimento Agrícola, Estatal, Central de Laboratórios da Agropecuária, Av. Adhemar Maria Cristina Arias, Departamento de de Barros, 967, Ondina, CEP 40170-110, Biologia, Instituto de Biociências, Salvador, BA, BRAZIL, Tel: +55 71 2370871 r. Universidade de São Paulo (USP), Rua do 37, [[email protected]], URL da Matão, no 277, CEP 05508-900, Cidade Homepage: http://www.ebda.ba.gov.br Universitária, São Paulo, São Paulo, BRAZIL, Linda Collette, United Nations Food and Tel: +55 11 3091-7587 [[email protected]]. Agriculture Organization (FAO), Viale delle Maria Cristina Gaglianone, Laboratório de Terme di Caracalla, 00100 Rome, ITALY Ciências Ambientais, Centro de Biociências e [[email protected]]. Biotecnologia , Universidade Estadual do Lionel Segui Gonçalves, Departamento de Norte Fluminense Darcy Ribeiro (UENF), Av. Biologia, Faculdade de Filosofica Ciências e Alberto Lamego 2000, CEP 28013-600, Letras de Ribeirão Preto, Universidade de São Campos dos Goytacazes, Rio de Janeiro, Paulo (FFCLRP-USP), CEP 14.040-901, BRAZIL, Tel: +55 22 2726-1602 Ribeirão Preto, São Paulo, BRAZIL, [[email protected]]. 14

Maria José de Oliveira Campos, Federal da Bahia (UFBA), Rua Barão de Departamento de Ecologia, Instituto de Geremoabo s/n, Ondina, CEP 40170-290, Biociências, Universidade Estadual Paulista Salvador, Bahia, BRAZIL, Tel: +55 71 247- Júlio de Mesquita Filho (UNESP), Av. 24A, N. 3810 [[email protected]]. 1515, CEP 13506-900, Bela Vista, Rio Claro, São Paulo, BRAZIL, Tel: +55 19 526-4145 Michael A. Ruggiero, Integrated Taxonomy [[email protected]]. Information System, U.S. Geological Survey, Smithsonian Institution, P.O.Box 37012 Maria Rodrigues Vianna, Universidade NMNH, Room CE-120, MCR 0180, Federal de Ouro Preto, Instituto de Ciências Washington DC, 20013-7012, USA Exatas e Biológicas, Departamento de [[email protected] Ciências Biológicas, Campus Morro do [email protected]]. Cruzeiro, Ouro Preto, MG, BRAZIL, Bauxita, CEP 35400000, Tel: +55 31 35591699, Olga Inés Cepeda Aponte, Laboratório de [[email protected]] Abelhas, Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo Mariana de Araújo Melo, Departamento de (USP), Rua do Matão, travessa 14, nº 321, Biologia Animal, Centro de Ciências CEP 05508-900, Cidade Universitária, São Biológicas e da Saúde, PPG-Entomologia, Paulo, São Paulo, BRAZIL, Tel: +55 11 3091- Universidade Federal de Viçosa (UFV), Av. P. 7533 [[email protected]]. H. Rolfs, s/n, Campus Universitário, CEP 36571-000, Viçosa, Minas Gerais, BRAZIL, Tel: Patricia Maia Correia de Albuquerque, +55 31 3899-2531 [[email protected]]. Laboratório de Entomologia, Departamento de Biologia, Centro de Ciências da Saúde, Marilda Cortopassi Laurino, Laboratório de Universidade Federal do Maranhão (UFMA), Abelhas, Departamento de Ecologia, Instituto Av. dos Portugueses, Campus Univ. do de Biociências, Universidade de São Paulo Bacanga, CEP 65080-040, São Luis, (USP), Rua do Matão, travessa 14, nº 321, CEP 05508-900, São Paulo, São Paulo, Maranhão, BRAZIL, Tel: +55 98 217-8544 BRAZIL, Tel: +55 11 3091-7533 [[email protected]]. [[email protected]]. Paulo De Marco Junior, Laboratório de Marina Siqueira de Castro, Empresa Baiana Ecologia Quantitativa, Centro de Ciências de Desenvolvimento Agrícola, Central de Biológicas e da Saúde, Departamento de Laboratórios da Agropecuária, Laboratório de Biologia Geral, Universidade Federal de Abelhas Labe. Av. Ademar de Barros, 967, Viçosa (UFV), Centro, CEP 36571-000, Ondina, CEP 40170110, Salvador, BA , Viçosa, Minas Gerais, BRAZIL, Tel: +55 31 BRAZIL, Tel: +55 71 32352517 R. 33 Fax: +55 3899-1669 [[email protected]]. 71 32351453, Universidade Estadual de Feira Paulo Nogueira Neto, Laboratório de de Santana, Avenida Universitária s/n, Feira Abelhas, Departamento de Ecologia, Instituto de Santana, BA, BRAZIL, de Biociências, Universidade de São Paulo [[email protected]], URL da (USP), Rua do Matão, trav.14, nº321, CEP Homepage: http://www.uefs.br/ 05508-900, Cidade Universitária, São Paulo, Mauro Ramalho, Departamento de São Paulo, BRAZIL, Tel: +55 11 3091-7533 Botânica, Instituto de Biologia, Universidade [[email protected]]. Participants I 15

Paulo Yoshio Kageyama, Diretor do São Paulo, São Paulo, BRAZIL, Tel: +55 11 Programa Nacional de Conservação da 3091-7527 [[email protected]]. Biodiversidade, Ministério do Meio Ambiente, Tel: +55 61 40099551, Terry Griswold, United States Department of [[email protected]]. Agriculture (USDA), Bee Biology & Systematics Lab., Utah State University, Peter G. Kevan, Department of Logan, Utah 84322-5310, USA, Environmental Biology, University of Guelph, Tel: +01 435 797-2526 Guelph, Ontario N1G 2W1, CANADA [[email protected] / [email protected]]. [[email protected]]. Uma Partap, Pollination International Centre Peter K. Kwapong, Department of for Integrated Mountain Development Biological Science, University of Cape Coast, (ICIMOD), P.O Box 3226, Kathmandu, NEPAL, Cape Coast, GHANA Tel: 09977-1-5525313, [[email protected]]. Fax 00977-1-5524509 [[email protected]]. Ricardo Costa Rodrigues de Camargo, Empresa Brasileira de Pesquisa Agropecuária Valdemar Belchior Filho, Centro Brasileiro (EMBRAPA Meio-Norte), Av. Duque de Caxias de Apoio à Pequena e Média Empresa 5650, Buenos Aires, Teresina, Piauí BRAZIL, (CEBRAE), Rua Rui Barbosa nº 1, Centro, CEP Tel: +55 86 32251141 ramal 270 e fax 55 86 59600-230, Mossoró, Rio Grande do Norte, 32251142 [[email protected]] BRAZIL, Tel: +55 84 315-4346 [[email protected]]. Rogério Gribel, Departamento de Botânica, Instituto Nacional de Pesquisas da Amazônia Vera Lúcia Imperatriz Fonseca, (INPA-CPBO), Caixa Postal 478, Aleixo, CEP Universidade de São Paulo, Faculdade de 69011-970, Manaus, Amazonas, BRAZIL, Tel: Filosofia Ciências e Letras de Ribeirão Preto, +55 92 643-3112 [[email protected]]. Departamento de Biologia, Av Bandeirantes, 3.900, Monte Alegre, 14040-901 - Ribeirão Rui Carlos Peruquetti, Departamento de Preto, SP, BRAZIL, Tel: +55 16 36023815, Biologia Geral, Universidade Federal de [[email protected]], Laboratório de Viçosa (UFV), Av. P.H. Rolfs, s/nº, CEP 36571- Abelhas, Departamento de Ecologia, Instituto 000, Viçosa, Minas Gerais, BRAZIL de Biociências da USP, Rua do Matão 321 [[email protected]]. trav 14, Cidade Universitária, CEP 05508900, Simon G. Potts, Centre for Agri- São Paulo, SP, BRAZIL, Tel: +55 11 30917533, Environmental Research (CAER), School of [[email protected]]. Agriculture, 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 de Ecologia, Instituto de Biociências, Universidade de São Paulo (USP), Rua do Matão, travessa 14, nº 321, CEP 05508-900, 16

Acronyms

API African Pollinators Initiative PDF B Project Development Facility phase B ARS Agricultural Research Service SBSTTA Subsidiary Body on Scientific, Technical and Technological Advice BPI Brazilian Pollinators Initiative TDWG Taxonomic Database Working Group CBD Convention on Biological Diversity UFC Federal University of Ceará CI Conservation International USDA United States Department of COP Conference of the Parties Agriculture CRIA Reference Center on Environmental USP University of São Paulo Information EMBRAPA Brazilian Agricultural Research Corporation EPI European Pollinators Initiative EPUSP Polytechnic School, University of São Paulo FAO Food and Agriculture Organization of the United Nations FUSP São Paulo University Foundation GBIF Global Biodiversity Information Facility GEF Global Environmental Facility ICIMOD International Centre for Integrated Mountain Development INESP Internacional Network for Expertise in Sustainable Pollination INPA National Institute for Amazonian Research IPI International Pollinator Initiative ITIS International Taxonomy Information Service MMA Ministry of Environment NAPI North American Pollinators Initiative OREADES Brasilian NGO Presentation 17

Presentation

Workshop preparation potential participants of the Brazilian Pollinator Initiative (BPI) program, in this ini- In October 1998, São Paulo Workshop on tial phase: scientific community in consoli- Sustainable Use of Pollinators for Agricultural date and emergent groups, including here Use was held, and as a result from this meet- the agricultural staff from EMBRAPA and ing the São Paulo Declaration on Pollinators other agronomic schools that could be was constructed. It was submitted to the engaged in this initiative. For discussing com- Convention of Biological Diversity (CBD), in mon routes for the International Pollinator its 5th Conference of Parties (COP), in Initiative, we also invited the leaders of other Nairobi, 2000, where the International already established Pollinator Initiatives, like Pollinators Initiative (IPI) was approved as a that of the International Centre for Integrated new program related to sustainable agricul- Mountain Development (ICIMOD): North ture. Food and Agriculture Organization of American, European, African, and Asian. In the United Nations (FAO) was invited to be a Brazil, EMBRAPA and bee researchers from all facilitator of this process. In COP6 from country (15 research centers, from 15 states) CBD, 2002, a plan of action for IPI was were invited. We had 77 attendants to this approved for guiding the actions of regional workshop. Eleven countries participated in pollinator initiatives, proposing goals to be this SP Declaration on Pollinators plus 5. attained in 10 years. International Taxonomy Information Service Meanwhile, regional efforts related to IPI (ITIS), Internacional Network for Expertise in developed. In Brazil, several activities were Sustainable Pollination (INESP) and FAO were performed, coordinated by a committee infor- also organizations that were present. Federal mally established by the focal point in Ministry government ministries from Science and of Agriculture, in 2002, during the main Technology and Environment also gave their Brazilian meeting on bees (V Encontro sobre support for this workshop, a counterpart to Abelhas, Ribeirão Preto). Among these activi- FAO support. ties was the FAO proposal of a workshop Taking advantage of the audience at the related to discuss standardized methodologies SP +5 Forum, a second workshop, Pollinators and assessment of best practices in agricul- Initiatives and The Role of IT: Building ture to promote biodiversity in agro ecosys- Synergism and Cooperation, was proposed to tems. The title SP Declaration on Pollinators discuss and disseminate the importance of +5, for meeting to be realized in 2003, was Information Technology for the Pollinator suggested by M. Ruggiero during a workshop Initiatives, to help to promote partnership and in Mabula, Africa, and promptly accepted. exchange experiences on the development The preparation of this workshop and use of these technologies, and to discuss focused the awareness in the issue to the funding opportunities. 18

International Pollinators interested in pollinators and pollination biology, Initiatives including biodiversity conservation, agriculture and general awareness, and to facilitate collec- The North American Pollinator Initiative (NAPI) tive achievements” (Eardley, et al., 2004). In comprises an established net of institutions, 2002, its first Secretariat was formed, and the associations and researchers involved in the Plan of Action of African Pollinator Initiative pollinators’ issue, as well as in the ecological was published. At this time, API comprises services provided by pollinators. It is a public- Ghana, Kenya and South Africa, but it is open private partnership of pollinators’ conserva- for other participants. A major need that exists tion programs. Among the milestones of pol- in Africa is to identify the pollinators. Rapid linators programs are The Forgotten assessments, taxonomic efforts and capacity Pollinators Campaign (1996), the São Paulo building are among the main needs. Declaration on Pollinators Conservation and ICIMOD initiated its pollinator/pollination Sustainable Use (1998), the North American program in 1991, to address applied research, Pollinator Protection Campaign (NAPPC) in development and related issues of pollinators 1999, the International Pollinator Initiative (IPI) and pollination. The overall goal of ICIMOD is in CBD (2000; 2002). This is a science-based to improve the livelihood of mountain people program, “a portfolio of programs, projects by enhancing agricultural productivity and and activities from the public and private sec- biodiversity conservation through conserva- tor, connected by a spirit of cooperation” tion of indigenous pollinator species in order (Ruggiero, et al., 2004) to ensure sustainable pollination of crops and The European Pollinator Initiative (EPI) has other indigenous plant species of the Hindu adopted the same framework of the IPI, the Kush-Himalayan region. Several activities are four key components being: assessment, adap- being undertaken concerning pollinators tive management, capacity building and main- (Partap, 2004). streaming. To assess pollinator loss, the ALARM The Brazilian Pollinators Initiative (BPI) was (Assessing of LArge-scale Environmental Risks constructed based on the São Paulo with tested Methods) project was developed, Declaration on Pollinators, which stimulated combining the expertise of 54 partners from international interest and provided strategic 26 countries. This program started on February direction for pollinator conservation planning 1st., 2004, and it is planned for 5 years initial- (Dias, et al., 1998; Kevan and Imperatriz- ly. In particular, risks arising from pollinators’ Fonseca, 2002; Imperatriz-Fonseca & Dias, loss in the context of current and future land 2004; Imperatriz-Fonseca, et al., 2004). use in Europe will be assessed. SUPER (Sus - API, BPI and ICIMOD are together in a GEF tainable Use of Pollinators as an European (Global Environmental Facility) project entitled Resource) will be built directly upon ALARM to Conservation and Management of Pollinators address identified declines in European pollina- for Sustainable Agriculture Through an tors resources in a socially and economically Ecosystem Approach, with FAO as the facilita- viable manner (Potts, 2004). tor. In this global scenario, with pollinators in The African Pollinator Initiative (API) was mainstreaming in developed countries and established in 1999, as the African network of almost unknown in undeveloped countries, a the IPI. “It strives to improve communication partnership among scientists and stakeholders channels between all people and organizations will improve capacity building and sustainable Presentation 19

use of pollinators. As the general framework enormous task for some themes, which obvi- of IPI is adopted by all initiatives, including here ously could not be concluded within a 5-day standardized methodologies for assessments, workshop. Some general comments follow. it was considered essential to join leaderships The first group discussed assessment to discuss goals, needs and opportunities. For methods for pollinators’ status. Although they global comparisons, assessment methods advanced in the analysis of different methods, must be standardized. the task was not concluded. The main methods to be applied were pointed out, but only indications for the manual of standard meth- Methodological discussions ods were made. Coordinators answered the proposed questions, gave orientation for case The talks were organized in order to give sup- studies and suggested the next steps in the port for the discussion on which standard PDF B of the GEF project. methodologies should be used in the develop- The gene flow group presented a conclu- ment of the Brazilian Pollinator Initiative. In sive report. They also indicated the chosen oral presentations, several aspects of the methods to be used for different purposes, methodologies applied until now in pollination without describing them. Gene flow studies research and pollinators assessment were pre- must be included in the full project, and a sented by the specialists, showing how some selection of subjects was suggested by the important issues should be considered in group for next steps. future actions. Subjects, such as the influence Management of bees that could be used of individual collector performance in assess- as crop pollinators was the next subject, divid- ment, methods to be applied in assessment ed into 3 parts: honey bees; stingless bees; research, long-term and short-term evalua- and bumblebees and solitary bees. tions, introduction and restoration of pollina- In Brazil, as well as in other countries, tors, performance evaluation in solitary polli- honey bees are used as generalist pollinators nators, meta analysis of data on plant-pollina- because they are abundant, easy to breed and tor relationships, and priorities for pollinators to manage in crops. Honey bees were focused programs, were presented. Gene flow, bee on for crop pollination in the important species visiting flowers of important crops and McGregor’s book, Insect pollination of cultivat- pollinator breeding possibilities in Brazil were ed crop plants, still very useful and updated on also part of oral presentations and specific line. However, Brazil has the Africanized honey group discussions. bee, which requires special management practices, and knowledge related to their performance as pollinators. In fact, they are quite Protocols and discussions effective in pollination, as Roubik (2002) pointed out for coffee production in Panama, and The sessions’ coordinators established a proto- as Couto (2002) discussed for several crops. col to be discussed during the workshop. The The honey bees study group presented a very groups were directed to discuss the methods to comprehensive report, with valuable sugges- be standardized, and to suggest themes for the tions and guidelines for further applications of PDF B (Project Development Facility phase B ) of bees as pollinators. Pollination by honey bees the GEF project. We needed to consider the could be much improved by technology 20

advances in management, nutrition, patholo- capacity building concerning the other bee gy and mechanization, especially for transport species, Africanized honey bees will soon be to pollination sites. Farmers need to be made the only available pollinators in sufficient aware of the benefits of incorporating pollina- quantity for agricultural use in our country. tion into their management practices Loss of habitat and increasingly intense agri- Brazil has only seven species of bumble- cultural practices are clearly reducing the bees (Bombus); nevertheless they are abun- native bee populations. Introduced into the dant all over the country. They are generally Americas, honey bees are generalists and in very aggressive, and are not reared for pollina- most cases less effective for biodiversity con- tion purposes in Brazil. The carpenter bee, servancy. The result will be a drastic loss in Xylocopa, can be reared and is a good pollina- plant biodiversity and in agricultural produc- tor of passion fruit, among other crops. There tion, especially in the more tropical regions. are 49 species of carpenter bees in Brazil (Silveira, et al., 2002) that are potentially important in agriculture. The solitary bees Information Technology and management group did a very comprehensive the Pollinators Initiatives report, presented the main plants that should benefit from their use as pollinators and the For this one-day workshop, held during the needs for breeding them in large quantities. last day of the SP+5 Forum, speakers repre- An effort for a workshop focusing only on senting the various Pollinators Initiatives pres- these bees as pollinators was indicated as a ent were invited. Other presentations focused need, and was held in April 2004. on local initiatives: the Brazilian Pollinators Stingless bees are native in Brazil, with Initiative and local projects that make a strong more than 500 species in the country. use of Information Technology (IT) and are Breeding techniques are known for some related to pollinators. The speakers were asked species. Most stingless bees species have not to give a short presentation focusing on how been studied yet. Their use as pollinators is IT is used presently and how, in their own effective for some species (see Heard, 1999; point of view, it might contribute for the Malagodi-Braga, et al., 2000), but they are not advancement of the national, regional and bred on a large scale to be available for agri- international Pollinators Initiatives. Some time cultural purposes. They have a high potential was allowed for discussions on issues such as for the use as pollinators: they are diverse, technology and data sharing, systems integra- have perennial nests, are generalists, but also tion and also funding needs and strategies. show floral preferences (Ramalho, et al., 1990; Biesmeijer, et al., 2005), they communicate floral resources to nestmates, they do not sting, Workshop results, as well as the oral presenta- and they store food inside the nests. The use tions, are on line at http://www.webbee.org.br. and conservation of stingless bees was discussed by this group, and next steps for related activities suggested. It is important to point out that if funding is not available to develop bee biology projects and to improve the local knowledge and for Presentation 21

References

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COUTO, R.H.N. 2002. Plantas e abelhas, uma parceria em crise? Anais do V Encontro sobre abelhas, Ribeirão Preto, p. 87-94.

DIAS, B.F.S.; RAW, A. & IMPERATRIZ-FONSECA, V.L.1998. International Pollinators Initiative: The São Paulo Declaration on Pollinators. Report on the Recommendations of the Workshop on the Conservation and Sustainable Use of Pollinators in Agriculture with Emphasis on Bees. (http://www.fao.org/biodiversity/docs/pdf/Pollinators.PDF), accessed on August 29th 2004.

EARDLEY, C.; GEMMIL, B.; KWAPONG, P. & KINUTHIA, W. 2004. The African Pollinator Initiative. In: FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearing and management in pollination. Fortaleza, Imprensa Universitária, p. 67-69.

HEARD, T. 1999. The role of stingless bees in crop pollination. Annu.Rev.Entomol., 44: 183-206

IMPERATRIZ-FONSECA, V.L. & DIAS, B. F. S. 2004. The Brazilian Pollinator Initiative. In: FREITAS & PEREIRA (eds.). Solitary bees: conservation, rearing and management for pollination. Fortaleza, Imprensa Universitária. p. 27-33. Available at http://www.webbee.org.br , accessed on August 29th 2004.

IMPERATRIZ-FONSECA, V.L; FREITAS, B.M.; SARAIVA, A.M. & DIAS, B.F.S. 2004. The Brazilian Pollinator Initiative: Challenges and opportunities. In: Annals of the 8th IBRA International Conference on Tropical Beekeeping and VI Encontro sobre abelhas, Ribeirão Preto, in CDROM.

KEVAN, P. G.; IMPERATRIZ-FONSECA, V. L. (eds.). 2002. Pollinating bees: the conservation link between agriculture and nature. Brasília, Ministério do Meio Ambiente, 313pp. Available at http://www.webbee.org.br , accessed on August 29th 2004.

MCGREGOR, S.E. 1976. Insect Pollination of cultivated crop plants. USDA-ARS, Washington, DC. Available at http://gears.tucson.ars.ag.gov/book/index.html , accessed on August 29th 2004.

PARTAP, U. 2004. An overview of pollinators’ research and development in the indu Kush- Himalayan Region. In: FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearing and management in pollination. Fortaleza, Imprensa Universitária, p.57-66.

POTTS, S. (ed.). 2004. European Pollinators Initiative (EPI): Assessing the risks of Pollinators loss. In: FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearing and management in pollination. Fortaleza, Imprensa Universitária, p. 43-55.

RAMALHO, M.; KLEINERT-GIOVANNINI, A. & IMPERATRIZ-FONSECA, V. L. 1990. Important bee plants for stingless bees (Melipona and Trigonini) and Africanized honey bees (Apis mellifera) in neotropical habitats: a review. Apidologie, 21:. 469-488 22

ROUBIK, D.W. 2002. Feral African Bees augment Neotropical coffee yield. In: KEVAN, P & IMPERATRIZ-FONSECA, V.L. (eds.). Pollinating bees: the conservation link between Agriculture and Nature. Brasilia, p. 255-266. Available on line in http://www.webbee.org.br.

RUGGIERO, M.; BUCHMANN, S. & ADAMS, L. 2004. The North American Pollinators Initiative. In: FREITAS, B. F. & PEREIRA, J. O. (eds.). Solitary bees: conservation, rearing and management in pollination. Fortaleza, Imprensa Universitária. p. 35-41.

SARAIVA, A.M. & IMPERATRIZ-FONSECA, V.L. 2004. A proposal for an information network for the Brazilian Pollinator Initiative – BPI – based on WebBee. In: Annals of the 8th IBRA International Conference on Tropical Beekeeping and VI Encontro sobre Abelhas, Ribeirão Preto, in CDROM.

SILVEIRA, F. A.; MELO, G.A.R. & ALMEIDA, E.A.B. 2002. Abelhas brasileiras, sistemática e iden- tificação. Belo Horizonte, 253pp. WORKSHOP I

Survey methods for bees as pollinators in Brazil: assessing the status and suggesting best practices Workshop I 25

Group 1 Surveying and monitoring of pollinators in natural landscapes and in cultivated fields

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

Abstract data exist in those methodologies, no con- sensus was reached on which methods to This workshop aimed the establishment of recommend for given situations, but compar- standard methodologies for bee surveys and ative data should be sought for before any monitoring of natural landscapes and crops. definitive recommendations can be built in As there are countries and regions with prac- the context of the Brazilian Pollinator tically no information about pollinator fauna, Initiative. Three case studies, in a cotton field, three strategies for pollinator investigation in the Atlantic Forest and in open savanna, were addressed: 1) rapid assessments; 2) sur- illustrate how recommendations could be veys and 3) monitoring programs. The used in the development of survey and mon- expected product was a manual for standard itoring protocols. methodologies for bee surveys and monitoring in natural landscapes and cultivated fields. Some basic principles were observed: Aim data must be reliable and adequate for statistical analyses, and all suggested strategies Establishment of standard methodologies for were to be realistic, considering time, person- bee surveys and monitoring of natural land- nel and costs constraints, and flexible enough scapes and crops. to be applied in different environments. Surveys should be question oriented. It became obvious that no rigid protocol could Expected Product be built for all situations across the world, then only general guidelines, not protocols, Production of a manual of standard method- were suggested in order to meet the basic ologies for bee surveys and monitoring of nat- principles listed above. Since no comparative ural landscapes and cultivated fields. 26

The pollination crisis and Rationale the need for surveys • Data to be obtained by the suggested and monitoring programs guidelines will be used in the context of the Brazilian Pollinator Initiative and should be The impact of deforestation, habitat fragmenta- useful for other initiatives around the world. tion, introduction of exotic species and • As there are countries and regions with prac- unfriendly agricultural practices is believed to be tically no information about pollinator fauna, causing a decrease in wild pollinator popula- three strategies for pollinator investigation tions. This, in turn, is suspected to be the cause were addressed: 1) rapid assessments; 2) sur- of low fruit and seed productivity in many crop veys and 3) monitoring programs. plants, with economic consequences in many parts of the world. Also the productivity of wild plants may be affected, and this can lead to Recommendations local extinction of populations of those plants, as well as of the animals depending on them. Basic principles Since this “pollination crisis” was recog- The group agreed that suggested actions should: nized, much effort has been put into initiatives • Assure data quality, i.e., data must be reliable to conserve and sustainably use wild pollina- and adequate for statistical analyses. tors. However, it is widely recognized that we • Be realistic, considering time, personnel and lack much of the knowledge we need to pro- costs constraints. pose effective actions to achieve conservation • Be flexible enough to be applied in different and management practices. We are not even environments. certain about the geographic extension and • Be question oriented. intensity of pollinator population decreases. We also lack basic information on how the dif- Difficulties ferent factors affect wild populations of flower Members of the group suggested and discussed visiting organisms. various methods in use across the world. Two basic questions stand out as being of Different people had different experiences with surmount importance for any conservation or different methods. For example, some had very sustainable management initiative to succeed: good results in using pan traps for collecting 1) which pollinator species exist in any given bees, while others obtained meager data from place? 2) how are their populations fluctuating their use. Such differences could be due to dif- along time? ferent designs, different environmental condi- For these questions to be answered, we tions, etc. It became obvious that no rigid pro- need to invest in pollinator faunistic surveys tocol could be built that could be recommend- and in monitoring programs. ed for all situations across the world; even within Brazil; the group was not able to decide on specific methods to be employed, due to the Results varying opinions on their efficiency. Thus, it was decided that only general The group discussed the general structure of guidelines would be built, so that data standard procedures to survey and monitor obtained from surveys and monitoring pro- bees in cultivated fields and natural areas. grams, using any combination of the suggest- Workshop I 27

ed methods, would meet the basic principles Considering the difficulties exposed listed above. It was hoped that further com- above, the following recommendations should parison of the different methodologies would be accepted as guidelines, not protocols, in enable sound choice of methods in the future. order to assure their applicability.

Rapid Assessments and Surveys

Aims

To best describe given local faunas. To maximize number of species recorded.

Type of data

Species records Through collection and deposit as vouchers in public collections.

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

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

Association with plants Whenever possible, plants visited by pollinators should be recorded, 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 be recorded. Whenever possible, hand netting should be applied. Other recommended methods are: trap nesting; aspirators, malaise traps, and pan traps.

Statistical analysis

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

Observations Species identification should be made by trained people, with the aid of taxonomic keys and reference collections. Those responsible for identifications should be contacted in advance. Manuals should include information on national collections and taxonomy services. 28

Aims

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

Species records Through collection and deposit as vouchers in public collections.

Species Abundance. Number of individuals must be recorded in a manner that allows 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 conditions and time of the day must be recorded for resource availability analysis. Sampling design

Use previous data to plan collection and build a list of expected species.

Plan a pilot study to check the adequacy of techniques.

Plan data to be useful in the future as meta data.

Sampling effort must be measurable and recorded.

Adequate number of replications should be employed. Environment patchiness and plot design should be taken into account to define the number of replicates.

The sampling area should be visited before sampling, and plant collection and individual plant labeling should be done whenever possible to facilitate plant identification.

Consider time to be spent in obtaining information on habitat and surroundings that may be useful in the 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 be recorded. Whenever possible, hand netting should be used. Other recommended methods are: trap nesting; aspirators, malaise traps, and pan traps. Statistical analysis

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

Observation: Species identification should be made by trained people, with the aid of taxonomic keys and reference collections. Those responsible for identifications should be contacted in advance. Manuals should include information on national collection and taxonomy services. Workshop I 29

Monitoring

Aims

To identify and describe patterns and variations through time and changing conditions of selected variables. To evaluate population fluctuations To guide decisions in conservation actions; To guide decisions 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.

Use previous data to plan collection and build a list of expected species.

Plan a pilot study to check the adequacy of techniques.

Plan data to be useful in the future as meta data.

Sampling effort must be measurable and recorded.

Adequate number of replications should be employed. Environment patchiness and plot design should be used to define the number of replicates.

The sampling area should be visited before sampling, and plant collection and individual plant labeling should be done whenever possible to facilitate plant identification.

Consider time to be spent in obtaining information on habitat and surroundings that may be useful in the 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 be recorded. Whenever possible hand netting should be used. Other recommended methods are: trap nesting; aspirators, malaise traps, and pan traps. Statistical analysis

Use recommended statistical analysis. Statistical techniques should be known in advance. A guide of statistical procedures or references should be part of the manual. 30

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

Final Remarks herbaceous cultivars of the introduced G. hirsutum are currently cultivated on a commercial It was obvious that no fixed protocol could be scale in Brazil. However, cultivation systems are provided for all situations. Moreover, different not homogeneous across the large cotton-pro- people had different experiences with differ- ducing regions of Brazil. An evident contrast ent sampling methods. Since no comparative exists, for example, between the small-scale data exist on those methodologies, no consen- production found in the small family-held sus was reached on which methods to recom- farms in the northeastern region of Brazil, mend for given situations. Thus, such compar- which employ a low technology crop system, ative data should be sought for before any and the large scale production system definitive recommendations can be built in the employed in the huge commercial farms in context of the Brazilian Pollinator Initiative. central Brazil. The cotton plant can produce nectar in five different kinds of nectaries distributed Case Studies – an exercise inside and outside the flower. However, not all of these nectaries occur in every cultivar (Free, Aim 1970; McGregor, 1976). Many different To provide examples of how the above recom- organisms are attracted to the cotton flower mendations could be used in the development by the nectar and pollen it produces. Among of survey and monitoring protocols. these, insects and especially bees are the most The group was divided into three sub- abundant. These flower-visiting species may groups, each of which worked on one case contribute to increases in fiber production study. The resulting protocols presented below and/or quality (Free, 1970; McGregor, 1976). were constructed based upon literature infor- The suggestions below were constructed mation and the expertise of group members, considering a small-scale system. Considerations with surveys and monitoring of bees on specif- on how to expand this protocol to a large- ic crops and in different kinds of environments scale, high-technology system are presented at taken as examples. the end of this exercise.

Survey 1) MONITORING FLOWER-VISITING BEES The survey of cotton-flower visiting species is IN COTTON FIELDS proposed for 1 ha fields, considered here as sampling units. This is an average size field for Background cotton in Northeastern Brazil. In each such According to Barroso & Freire (2003), three sampling unit, two sampling procedures species of cotton are found in Brazil, would be executed in parallel: Gossypium hirsutum (L.), G. barbadense (L.) A) Arbitrary sampling. This protocol and G. mustelinum (Mier). Of these, only aims to maximize the number of flower visit- Workshop I 31

ing species recorded on cotton plants. The Adapting the protocols for large-scale, field is slowly inspected and all bees found on high-technology systems the cotton flowers or flying above them are The same 1 ha sampling units could be used, collected. It is important to call attention to each with 10 sampling plots, as explained the fact that the deep corolla of the cotton- above. Such sampling units should be homo- flower makes the use of hand nets relatively geneously distributed inside the cotton fields, inefficient, as the flower protects the visiting the number of such units being proportional insects. For this reason, complementary cap- to the size of the fields, with some of them ture methods are suggested: forceps, insect close to the borders and others within the inte- aspirators and hand nets, depending on the rior of the fields. size and position of the bees. B) Systematic sampling. This protocol aims to quantify the relative density and abun- 2) BEE SURVEYS AND MONITORING OF dance of flower-visiting species. Sampling is to A FRAGMENTED LANDSCAPE IN THE be done weekly in 10 plots, each including 80 ATLANTIC RAIN FOREST BIOME cotton plants, 20 in each of four neighboring rows. Those plots should be homogeneously Background distributed across the field, including areas The Atlantic Tropical Rain Forest is a recognized close to its border and center. Areas close to biodiversity hot spot. Its original vegetation patches of natural vegetation and other spe- cover has been reduced to 8%, and what is left cial environments around the field also should is threatened by human presence. Population be considered. Each plot is sampled for 10 min growth has led to destruction of the forest by slowly walking between the rows. Any bees through uncontrolled urban expansion, indus- found inside the flowers and on extra floral trialization and migration of people from other nectaries will be collected. areas (Galindo –Leal & Câmara 2003). About Both sampling procedures should be exe- 100 million people live in the mega cities locat- cuted weekly, between 8:00 and 12:00, along ed in the Atlantic Forest Region, along with the the flowering season. Sampling should be largest industrial and silvicultural centers. On done preferably during sunny days, when bees the other hand, the biodiversity harbored by the are most active at flowers. Any cultivation Atlantic Forest is one of the greatest in the practice proceeded between and on sampling world. We believe that 60% of the terrestrial days should be recorded. species of the planet live within the remaining areas of this forest. This is probably a result of Monitoring the large range of latitude it covers, its variation Monitoring can be done by repeating yearly in altitude, the diverse climatic regimes, and the the systematic sampling procedure described availability of water and energy to the system above. In this way, average abundance of the (Pinto & Brito 2003). These forests are highly whole flower-visiting assemblage and of tar- stratified, with a canopy as high as 35 meters. get species can be compared between years and along longer periods. These numbers can Survey also be associated with factors such as cli- Pollinator surveys should be made along tran- matic parameters and the amount of pesti- sects. The determination of size, placement and cide application. number of transects will depend on the hetero- 32

geneity of the forest community, which should Background be understood beforehand. The size of the tran- The biome of the Cerrado is a gradient of veg- sects should be such that they can be covered etation physiognomies, including open fields, in one day. They should be 100 m long. savannas and open-canopy forests. It covers The sampling units will be flowering about 25% of the Brazilian territory and was plants, with all bees found being collected at included among the world’s hotspots (Myers, all the flowering plants that they visit. Hand et al. 2000), for combining high biodiversity nets will be the principal collection method and high rates of disturbance. Until 40 years and will be complemented by euglossine baits. ago the Cerrado was primarily used for exten- Additional methods such as pan, malaise and sive cattle raising. By 1988 Klink & Moreira light traps and also new baits such as (2002) estimated that 35% of the natural salt/ammonia and antifreeze should be tried. cover had already been removed. In a recent Sampling should be repeated 3 to 5 times study, using MODIS satellite images of 2002, a month for 8 to 12 months per year, depend- (Machado, et al.,2004) concluded that the na - ing on flowering phenology and flower density. tural cover loss has changed to 55% . Agriculture occupies 6% of the total area, Monitoring but this figure is increasingly stimulated by The goal of the suggested monitoring pro- present national agricultural policy. Pastures gram is to detect differences in bee diversity in and large plantations of soybean and cotton disturbed and undisturbed forests over time. It are the major threats for the biome, causing could also be used to compare different soil loss, water pollution, habitat loss, habitat degrees of disturbance. fragmentation, introduction and spread of Sampling units are similar to those used in very agressive invasive species, like African the survey. Monitoring subjects may be select- grasses, among others (Buschbacher, 2000; ed, based on survey results. For example, Fearnside, 2001; Klink & Machado, 2005). euglossines or Melipona. Such subjects a) Forecast is not optimistic, according to Ma- include species sensitive to deforestation; b) chado, et al. (2004), based on present vegeta- occur in large numbers and c) can easily be tion removal rates by 2030 the whole biome identified. Still other subjects could be consid- may have given place to agricultural and cattle ered, such as Apis mellifera, trap-nesting raising activities. Centris or specialist taxa. Major impacts on pollinators are appar- The monitoring design should include site ently caused by intense use of chemicals, aeri- in or adjacent to undisturbed area (control), al spraying, and habitat removal; the latter disturbed area (treatment 1) and intermediate provokes reduced nesting opportunities and area (treatment 2). food availability. A minimum of five years of sampling is According to Silberbauer-Gottesberger needed for conclusions to be drawn. and Eiten (1987), the plant species richness of the Cerrado open areas is among the highest 3) SURVEY OF POTENTIAL POLLINATORS known for non-forest vegetation. Seasons are IN THE BRAZILIAN SAVANNA, AND A very well defined. The dry season lasts from 3 MONITORING PROGRAM TO EVALUATE to 5 months, during winter, and the wet sea- THE IMPACT OF GRAZING ON FLOWER son peaks in December-January. Flower VISITORS´ RICHNESS resource availability varies through the seasons Workshop I 33

(Oliveira & Gibbs, 2002), but flowers are found also provide information about plant species throughout the year (Batalha, 1997). Bee sur- intensively visited by bees. veys in the Cerrado area have been carried out 6.Although Brazilian researchers use hand net- in Central Brazil, around Brasília, in Minas ting as the main technique for sampling bees, Gerais State, in the Northeast and in some examination of previously published studies peripheral areas in São Paulo state (Pinheiro- that have used other methods can indicate Machado et al., 2002), allowing for a baseline what part of the community is not being data set for native fauna. sampled if hand netting is the only technique. 7.Plan the type of analyses that will be carried Survey out and assure that the experimental design The Cerrado vegetation is a natural mosaic, will provide proper data. with many vegetation types, varying from open 8.Sampling area should be marked at the field. grass fields to dry forests. Therefore a previous analysis of the sampling area has to be done Site selection must be guided by the ques- before designing the survey. The following steps tion proposed for the survey. The chosen site can be used to guide the sampling procedures. must be representative of the environmental sit- 1.The very first task must be the definition of uation to be investigated. If a unique type of the question that the survey is aiming to ask; vegetation or physiognomy is targeted, an eval- all of the succeeding steps depend on a very uation will need to be made to determine if the clear and objective question. chosen site adequately represents the situation 2.A good view of the large area, using satellite to be surveyed. This also applies when gradients images or local driving around to picture the or mosaics are the case. Replication and control heterogeneity of the area to be sampled. areas are important parts of some surveys and 3.Accessing previous studies in the area, or have to be considered during site selection. similar areas, to create estimates of diversity Another very important point is the acces- and sampling effort necessary to best sibility of the site and all the permits that describe the focal fauna. Some calculations should be obtained, both from private involving sampling curves in a standardized landowners and governmental agencies. way with previous data may be necessary; the studies should indicate period of activity, Sampling design and sampling techniques both seasonally and daily. Sampling design involves choices of sampling 4.Visits to collections will produce a better unit format, size, number and spatial distribu- species list and expected richness numbers, tion. For instance, if an overview of diversity in because collections are believed to include the area is the aim, sampling units will be need many unpublished data. to be randomly distributed; if diversity infor- 5.Local evaluations prior to the surveys pro- mation is to be linked to habitat, sampling vides familiarization with flora and allows units should be selected in a way that they identification of potential plant species for a represent all desired situations (Alonso & target survey. This may be crucial, especially Agosti, 2000). The sampling design has to in the case of very short budgets. Simple consider areas greater than 2 ha because of things that might turn into difficulties in the the typical spatial distribution of plants in the field can be observed, like the height of Cerrado. At least 10 transects 2 m wide by 1 trees to be sampled. Previous studies may km long, or 5 quadrats of 40x100m, should be 34

established. The method should be calibrated sampling effort. Collectors should also be ran- against known areas by follow-up procedures domized along sites to minimize bias from col- using species accumulation curves (Soberón & lecting ability. Llorente, 1993) to inform about the efficiency Complementary data is very important for of the chosen design and techniques. Species data analysis, so a protocol should be applied accumulation curves are produced from to every survey. Recommended data to be species-by-sample matrices in a spreadsheet, gathered are the following: and they can be carried out by the EstimateS • site location with coordinates; use a GPS; if program (Colwell, 1997). this is not available, report local geographic Sampling techniques that minimize the references like roads, bridges, or equivalents; collectors’ interference are preferred, but the • date, including month/day/year ; best results in Brazil have so far been achieved • time of the day, indicating sampling hours; using hand nets. To minimize differences • a clear vegetation classification, informing among collectors, previous training is manda- not only details about the vegetation found tory. Different species have different behaviours in the sampling areas, but also the character- at flowers; some of them can be very fast and istics of the landscape in which is it situated; sensitive to movement. Collectors must be • the size of the total area from which sam- advised to collect any bees and all wasps and ples are taken must be indicated, because small flies, because some bee species looks like results are expected to vary if collecting sites wasps or are too small to be differentiated are a part of a 1 ha, a 100 ha or a larger area from another insect when observed in the field. of Cerrado; Recommended techniques are hand net- • general climate description and classification tingand sweep netting in transects. Although are very useful and must be complemented pan traps have not had good acceptance with local weather conditions during the col- among Brazilian researchers, good results and lection days and information about average new fluorescent colors reported from other temperature and rainfall whenever possible. countries speak for its use. Pan traps tend to be selective for certain groups, so they should Floral associations are important comple- not be used as the only technique for invento- mentary information, but time can be saved if ries. The best method may vary according to collectors add flowers to a bag, identify it, and site and logistics, but best results in species leave a numbered tag on the plant to proceed numbers are usually achieved when multiple with plant identification later on. methods are applied. Field equipment must include spare hand The length of the transect needs to be nets, and enough vials to avoid jamming vari- standardized, but it will depend on the aim of ous insects into each vial. All material is to be the survey, as discussed above. If the transect labeled in advance allowing quick field infor- is divided into sub samples, these should be mation to be made promptly. kept separated for posterior analyses. The After fieldwork some procedures are rec- starting point of the transect should be picked ommended that will make data easy to ana- at random, in order to avoid always collecting lyze for anyone interested: during the peak activity period at the same • standardize the format of data presentation part of the transect. One needs to be sure that and codes to facilitate understanding at all the peak activity period is always covered by instances of the study; Workshop I 35

• present results by simple summary descrip- of monitoring should be understood and sup- tors, like species richness, and common and ported by a strong significant positive correla- popular diversity indices; tion. Direct relationships are preferred. If the • feed data bases that provide access to the relation between the measured variable and general pubic; indicate the collection where the object of monitoring is not already known, voucher material was deposited. assumptions must be stated clearly at the beginning of the monitoring program. The Monitoring selection of a specific taxa or guild must take The proposed exercise for this group was to into consideration the characteristic that the give directions for monitoring the impact of focal organisms are abundant and easy to iden- cattle raising activities on the biodiversity of tify. A previous survey is mandatory for areas pollinators. The group started with the state- where data is lacking, to improve the chance of ment of the leading question: What is the choosing good taxa to be monitored. impact of introducing cattle “on pollinators”? To address this question, previous data Some general recommendations could about bees and their relationship with flowers be made for all situations involving polli- of open areas will be gathered. This informa- nator surveys and monitoring: tion will be used to choose focal groups for Training. One problem raised about the use monitoring activities. Preference will be given of “manual” collection methods, such as to bees sensitive to gradients that are in this hand-netting is the effect of different abilities case understood to range from original non- of different people to find and capture bees. grazed areas to heavily grazed areas. If prelim- This problem can be reduced by properly train- inary data fails to point out the taxa to be ing collectors before actual sampling is begun. monitored, the initial monitoring is used to Replication. An appropriate number of establish a baseline for further comparisons. replicates should be set, according to environ- The preliminary data will be tested for correla- ment heterogeneity and/or other important tion with desired variables, like bee diversity. factors. Pseudo-replication should be avoided. Once a strong and significant statistical rela- For instance, 12 monthly samples collected at tionship is found, collections will be repeated one site cannot be considered as replications through time. The sampling design is the same of different disturbance grades or environment one proposed for the survey, but will be types. In these cases, different areas should be repeated through time. sampled as replications of each treatment. Identification and voucher specimens. Specimens both of target (pollinators) and HOW DATA FROM MONITORING WILL BE associate (e.g. food sources) taxa should be USED IN THE CONTEXT OF BPI? properly collected, preserved and labeled to facilitate proper identification. Such identifica- Monitoring depends on the choice of sound tion should preferably be done by experienced and easy to measure variables. Variable selec- personnel. Moreover, voucher specimens of all tion can be made based upon previous data. It taxa involved should be deposited in public is recommended that a selected taxa or a guild collections that should be indicated in reports is used for monitoring, but the relationship and publications, so that their identification between the measured variable and the object can be checked at any time. 36

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

References

AGOSTI, D., MAJER, J.D., ALONSO, L.E. & SCHULTZ, R. 2000 Biodiversity studies, monitoring and ants: an overview. In: Ants. Standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press. Washington DC, USA, p. 1-8.

BARROSO, P. A. V. & FREIRE, E. C. 2003. Fluxo gênico em algodão no Brasil. In: PIRES, C.S.S., FONTES, E.M.G. & SUJII, E. R. Impacto Ecológico de Plantas Geneticamente Modificadas. EMBRAPA, Brasília-DF, Brazil, p. 163-193.

BATALHA, M. A. 1997. Análise da vegetação da ARIE Cerrado Pé-de-Gigante (Santa Rita do Passa Quatro, SP). Masters thesis. Universidade de São Paulo, São Paulo-SP, Brazil, 185 p.

BUSCHBACHER, R. 2000. Expansão agrícola e perda da biodiversidade no Cerrado: origens históricas e o papel do comércio internacional. Série Técnica Volume VII .WWF Brasil, 104p.

COWELL, R, K. 1997. EstimateS: statistical estimation of species richness and shared species from samples. Version 5. User’s guide and application. published at http://viceroy.eeb.uconn.edu/ estimates.

FEARNSIDE, P. 2001. Soybean cultivation as a threat to the environment in Brazil. Environmental Conservation, 28 n.1: 23-38.

FREE, J. B. 1970. Insect pollination of crops. Academic Press, London, UK, 544 p.

GALINDO-LEAL, C. & CÂMARA, G. I. 2003 The Atlantic Forest of South America: biodiversity status, threats and outloook. Conservation International Island Press, USA,488p.

KLINK, C. A.. & MOREIRA, A. 2002. Past and current human occupation and land-use In:OLIVEIRA, P.S. & MARQUIS, R. J. The Cerrado of Brazil. Ecology and natural history of a neotropical savanna. Columbia University Press, New York, USA, p.69-88.

KLINK, C. A. & MACHADO, R.B. 2005. A conservação do Cerrado Brasileiro. Megadiversidade, 1 n.1: 147-155. Workshop I 37

MACHADO, R.B.; RAMOS-NETO, M.B.; PEREIRA, P.; CALDAS, E.; GONÇALVES,D.; SANTOS, N.;TABOR, K & STEININGER, M. 2004. Estimativas de perda da área do Cerrado brasileiro. Technical Report. Conservation International Brazil, Brasília-DF, Brazil. 26pp.

MCGREGOR, S. E. 1976. Insect pollination of cultivated crop plants. Agriculture Handbook n. 496. United States Department of Agriculture, Washington, D.C. 411 pp.

MYERS, N., MITTERMEIR, R.A., MITTERMEIER, C.G., FONSECA, G.A.B., KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature, 402: 853:858.

OLIVEIRA, P.E. & GIBBS, P. 2002. Pollination and reproductive biology in Cerrado plant communi- ties In: Oliveira, P.S. & Marquis, R. J. The Cerrado of Brazil. Ecology and natural history of a Neotropical savanna. Columbia University Press, New York, USA, 329:347.

PINTO, L.P. & BRITO, M.C.W. 2003. Dynamics of Biodiversity Loss in the Atlantic Forest: An Introduction. In: Galindo-Leal, C. & Câmara, G. I. The Atlantic Forest of South America: biodiversity status, threats and outloook. Conservation International Island Press. USA. 27:59.

SOBERRON, M.L. & LORENTE, B.J. 1993. The use of species accumulation curves functions for the prediction of species richness. Conservation Biology, 7: 480-488. Workshop I 39

Group 2 Assessment of Pollinator – Mediated Gene Flow

Participants: Claudia Maria Jacobi (coordinator), Edivani Villaron Franceschinelli, Rogério Gribel, Peter G. Kevan, Alfred Ochieng, Eda Flávia Lotufo Rodrigues Alves Patrício, David W. Roubik.

Abstract and flies. The production of fruits, seeds, and of more individuals of the pollinated species This group discussed the interaction between depends directly on these agents in the major- plant and pollinator, emphasizing the impor- ity of plants, and very often in commercially- tance not only of pollination, but also of good important ones. Exceptions are self-fertilizing agricultural, forest management, and conser- plants, but even these frequently benefit from vation practices for sustainable development. cross-pollination provided by these agents. The group was comprised of researchers Traditional selective breeding of plants, habitat whose areas of expertise encompass floral fragmentation and overexploitation of natural biology, plant breeding systems, plant popula- stands are currently narrowing the genetic tion genetics, and pollination of tropical base, and are leading to genetic erosion of eco- plants. The recommendations made below are nomically important plants. In addition, genet- intended to contribute to future discussions ically modified varieties resistant to herbicides regarding the Brazilian Pollinator Initiative or pesticides could create potential "super- (BPI), although some of them are general weeds" through pollen-mediated gene flow. enough to be considered more broadly. Among the methods proposed to help Emphasis was given to recommendations perform the recommendations, rapid assess- other than methods, since there is a vast liter- ment protocols (RAP) are suggested, for the ature available (including FAO publications) on collection of data on bee behaviour, pollination the above-mentioned subjects. syndromes and landscape diagnosis. These Pollen-mediated gene flow in plants is protocols allow data collection in the field by affected by abiotic agents, such as wind, and a people with little or no formal biological train- number of biotic agents, of which the single ing. Other methods, including statistical and most important pollinator group worldwide is genetic analyses, require both expertise and the bees. Also of great importance for many specific facilities, and will usually be performed native fruit trees in the tropics are bats, beetles by researchers and trained personnel. 40

Aim • How to adapt the observational methods proposed to different plant habits and mor- To propose standard methodologies for the phologies, and landscapes (ex: trees vs. assessment of pollen transfer in crops and in shrubs; natural vs. agricultural systems)? natural areas. • Should these methods be made widespread and user-friendly? • Should we encourage their use by laymen in Expected products order to increase the number of areas and situations? To produce a list of methodologies, such as • If so, how to standardize the use and applica- rapid assessment protocols, experimental tion of the RAP with a minimum of mistakes? desing for testing breeding systems and mon- • Will it be feasible to recommend pollen itoring methods, making use of case studies containment measures based on this infor- as exemples. mation? To produce a list of recommendations for • How to determine the need to assess gene the gene flow assessment and management escape (ex. in the case of unwanted of plant species regarding containment meas- hybridization between crop varieties and ures or enhanced productivity. wild relatives, or related contamination This working group focused on the assess- problems concerning GMOs)? ment of pollinator-mediated gene flow of eco- • Should recommendations be made on a nomically important plant species. case-by-case basis, or could we generalize part of them?

Discussion In order to orientate the discussions a list of general guideline of method were drew: The discussions occured in two sessions; one • Observations of bee behaviour on the on monitoring of flower visitor behaviour, flower/inflorescence: pollinator or visitor? morning October 29th; other on pollination (frequency and kind of stigmatic contact) requirements and on apllied issues in pollina- • Amount and availability of pollen carried: tor gene flow, afternoon October 29th. where in the body, how tightly packed? The goals were to discuss ways of pro- • Bee flight among plants: do individuals fol- ducing a database containg comparative low nearest neighbour pollination rules behaviour of visitors in different plant species (optimal foraging)? Is there along-row within an area; how to produce a list of behaviour? Is there flower constancy? How important plant species and their pollinator to estimate carryover? requerements, including their breeding sys- • Energy economics of foraging: measure tem, pollination syndrome, and resource temperature, wind, RH. offer; and how to increase awareness/knowl- • Creation of user-friendly protocols for bee edge of mechanisms for containment meas- behaviour assessment and comparison. ure or enhanced productivity for selected • Application of simple statistics to determine plant species. pollen shadow. The questions guiding those discussons • Standard methodology to test for breeding were: system (includes bagging, hand pollination Workshop I 41

and emasculation, followed by fruit/seed each pollinator and likewise the plants that set), adapted to each case. they pollinate. • Creation of user-friendly protocols for breed- The pollinator requirements of a plant ing system assessment. species depend on its breeding system. • Application of simple statistics to analyse Standard methods to test for self-fertility and results. self-pollination are among the first features • Estimates of gene flow through genetic assessed when evaluating the need for polli- markers compared with estimates of pollen nators. Other usual procedures allow us to transport (see above). evaluate if a flower visitor is an effective polli- • Estimates of pollen shadow with dyes. nator. When focusing on gene flow, several • Comparison of crop productivity under dif- techniques have been tested to assess how far ferent pollinator regimes. can pollen go from a focal plant of group of • Selection and discussion of case studies (e.g. plants. This latter parameter involves knowl- cotton). edge of the amount of pollen harvested from a flower, flight range, and resource distribution, and it is directly related to the pollinator Results morphology, the flower morphology, and whether the resource is a crop or grows wild. Pollinator mediated gene flow Evaluating the extent of pollinator-mediated Pollen-mediated gene flow in plants is gene flow also requires knowledge of the pol- affected by abiotic agents, such as wind, and linator's fidelity to a given plant species, and biotic agents, such as bees, butterflies and of the type of resource it is being visited for. moths, beetles, flies, bats, birds, and other Finally, commercial parameters that increase less frequent agents like rodents, marsupials, crop value are usually taken into account to and thrips (Proctor, et al., 1996). Many polli- compare differences in yield among different nator populations are probably suffering pollination regimes. nowadays from stress resulting from habitat The understanding of pollinator behaviour loss, parasites, insecticides, and misunder- with respect to each plant species is vital not standing by the general public. Meanwhile, only to establish adequate agricultural actions the need for their services in natural, agri- that increase yield, but also to adopt measures cultural and agroforestry systems is growing that lead to sustainability. Among these are day by day. In the tropics, pollination is actions to reduce genetic loss in forest species affected not only by bees (natives and intro- due to isolation, to determine levels of isolation duced Apis), but also by less known ani- or contamination of crops, to prevent invasive- mals, whose service is poorly understood by ness of exotic plants and improve conservation the general public. Among these, bats are of native genetic diversity, and to enhance particularly important because they polli- awareness of pollinators' services to humanity. nate several species of fruit trees, while bee- At present, given the enormous variety of tles and flies are responsible for high yields in pollinators and commercially important tropi- palms. With such a variety of pollinator cal plant species (Roubik, 1995), only a small species and of plants that need animal polli- percentage of plants, be they wild or cultivat- nation, it is important that the characteristics ed, have undergone comprehensive studies, that affect gene flow are well understood for and most of the gene flow data which are 42

needed to support conservation and manage- ber, fruit, seeds, and dyes may be reducing ment initiatives are still lacking. genetic variability and gene flow to levels that permanently affect the viability of popu- Importance of pollinator-mediated gene lations. Some studies from Brazilian econom- flow in crop management and silviculture ically important species are available. Recent Pollinator services have been traditionally con- data (Peres, et al., 2003) from 23 populations sidered expendable in many crops. However, throughout the Brazilian, Bolivian and case studies have shown that yield is significant- Peruvian Amazon have shown that the his- ly improved when pollinators are introduced. torical levels of exploitation of Brazil nuts Such is the case for coffee (Roubik, 2002), and (Bertholletia excelsa, Lecythidaceae) have a various crops in Brazil (cited in a recent survey by major impact on recruitment into natural Couto, 2002): passion fruit, red pepper, straw- populations. Populations subjected to moder- berry and orange. Possibly, many others, such as ate and high levels of harvest over many sunflower and soybean, will also show decades lack juvenile trees; in contrast, only increased yield with insect-mediated pollination. populations with a history of light, recent or Although pollinators are not essential for fruit or no exploitation contain large numbers of seed set in many species, on account of their juvenile trees. self-fertility, it is clear that cross-pollination usu- At present, there are still few laboratories ally enhances crop performance, when evaluat- in Brazil (governmental or private) that are ed by commercial parameters. For example, involved in genetic studies of native plant pop- cashew (Anacardium occidentale), which is par- ulations. We are hopeful that this situation will tially self-fertile, requires a high rate of visitation be resolved in future years, since many labora- to obtain good nut yields, since most of the tories are nowadays well equipped and their fruits derive from cross-pollination (Holanda- personnel already prepared for this task. Neto, et al., 2002). The introduction of bee mana gement to increase yield in crops should be carefully evaluated case by case, since addi- Habitat fragmentation and reduction of tional costs are involved. genetic diversity On the other hand, alleged low productiv- Some Brazilian biomes have undergone exten- ity of some cultivated plants may simply be the sive clearing in the past decades, notably for result of incorrect agricultural practices that agricultural purposes. This has resulted in the have led to low genetic diversity of crop or for- inclusion of the Cerrado (savanna) in the latest est stands. Poor fruit and seed production can list of "hotspots" (threatened world regions be the result of inbreeding, not a lack of polli- that should be given priority in biodiversity nators. The common practice of plantations programs). This biome is home to several com- based on seeds from very few trees or even mercially important plant species that are clonal orchards should be analyzed carefully intensively used by local populations. since this may lead to genetic erosion, low pro- A typical case of plant populations ductivity and inbreeding depression. It is possi- already suffering from habitat fragmentation ble that premature fruit drop in cashew is also is that of Caryocar (Caryocaraceae) species. related to genetic causes. The piqui (C. brasiliense) from the Central Current practices of natural stand Brazil Cerrado vegetation, and the piquiá (C. exploitation for timber, pharmaceuticals, rub- villosum) from the Amazonian forest, yield Workshop I 43

fruits and seeds that are an excellent source of law decreasing the proportion of these edible oil. Pollination studies in both species reserves should be contested with scientific (Gribel & Hay, 1993; Martins, 2002) have and economic arguments. In addition to habi- shown a moderate degree of self-compatibility, tat preservation, habitat rehabilitation pro- and pollination by bats and sphingid moths. grams might benefit from the introduction Habitat and roost disturbance may affect the and management of pollen and seed dis- populations of these sensitive pollinators. persers. This action is a cheap alternative that Genetic data for C. brasiliense from 10 could increase gene flow among fragments microsatellite loci indicated a high level of and accelerate rehabilitation. biparental inbreeding, which could be attrib- uted to the limited flight range of its pollinators and restricted seed dispersal. Habitat Pollinator-mediated genetic contamination fragmentation would isolate populations and It is known that crops easily hybridize with wild their pollinators, aggravating the scenario of relatives (Ellstrand, et al., 1999). The visiting fruit overexploitation (Collevatti, et al., 2001). patterns of pollinator forage can create crop- In the case of mahogany (Swietenia macro- to-wild and crop-to-crop pollen exchange. If phylla, Meliaceae), the most valuable neotrop- genetically modified varieties (GMO) are ical timber species, habitat degradation involved, there is the risk that non-target caused by selective logging and, most impor- plants (wild relatives or conventional crop vari- tantly, by conversion of forest into soybean eties) acquire the characteristics of resistance plantations and cattle ranch pastures with to herbicides or pesticides through pollen- recurrent use of fire, have clearly reduced local mediated gene flow and turn into unmanage- population sizes and have led many popula- able weeds (the so-called "superweeds"). The tions to local extinction (Grogan, 2001). occurrence of agricultural weeds from GMO Recent studies using polymorphic microsatel- crop releases has already been reported. In lite markers (Lemes, et al., 2003) suggest that Canada, the presence of unwanted herbicide- the small, isolated, remnant populations may resistant canola (Brassica napus, which is bee not constitute viable units in the long term, pollinated) is becoming an agricultural nui- owing to the loss of genetic variation caused sance (Simard, et al., 2002). by genetic drift and inbreeding. Other genetically engineered varieties Brazilian legislation has contemplated the (modified to resist attack by insects), such as habitat loss problem by establishing, among sunflower (Helianthus anuus, which is bee pol- other protection measures, that a percentage linated), and papaya (Carica papaya, pollinated of uncultivated land be maintained in private by bees, birds and moths) have also shown properties (known as reserva legal) in Brazilian enhanced fitness. They are less attacked by biomes such as the Amazon forest and Cer - insects (moths) and in turn produce more seeds rado. These areas are important both to sus- that are themselves more resistant to insect tain ecological services such as pollination, and attack. This suggests that non-managed popu- to maintain gene flow and diversity of native lations may in turn accelerate development of plant species by behaving as corridors resistant insect pests. It is evident that to main- between fragments. There is, however, intense tain the utility of herbicides and pesticides in debate nowadays concerning the reduction of agriculture (i.e., to reduce the risk of hastening those percentages. Attempts to change the the development of superweeds), modifications 44

in agricultural practices, which include herbicide related to the behaviour of the pollinator, such management (such as rotation and combina- as flight range and its effectiveness as pollination with other actions), are mandatory. tor, which varies according to aspects associat- Existing containment measures are mostly ed involving both pollinator and crop charac- designed to assure seed purity levels, and may teristics. Purity standards should be stricter in not be adequate for preventing or, more real- cases of gene escape risk than in cases of seed istically, reducing gene escape from GMO purity, more so in centers of diversity, such as crops (Kareiva, et al., 1994). Physical barriers, the tropics, where traditional varieties, includ- such as bare land or non-GMO crops around ing progenitors, may disappear. the target variety, have been used to prevent In addition, environmental monitoring pollen contamination, but they have been actions focusing on gene escape should give inefficient in many cases, partly because of a priority to high-risk crops. These are those with lack of knowledge on the dynamics of pollen little domestication (that is, that are still ecolog- flow in each case. ically and reproductively similar to wild rela- If reducing the risk of contamination is a tives), that grow sympatrically with wild rela- main concern, then the choice of managed tives or cross-compatible domesticated species, pollinators of a given crop (most notably if it is which can turn into weeds themselves, and a GMO) should weigh not only commercial those whose commercialization requires that aspects but environmental safety as well. The the crop blooms or sets fruits/seeds. In Brazil, risk of gene escape to non-target species is cotton would be one of the best candidates.

Recommendations

Crop and silviculture management

1. Commonly accepted ("common wisdom") practices of crop pollination should be re-evaluated to extend the knowledge of the mechanisms of pollination, and of pollinator role and benefits. Case studies have shown that fruit yield is improved with pollinator service in crops where pollinators had traditionally been considered expendable.

Proposed methods:

• Standard breeding system tests and exclusion experiments.

• Pollination syndrome.

• Pollinator behaviour in flower and among plants.

• Statistical comparison of productivity parameters between traditional methods and hand cross-pollination experiments.

2.Traditional genetic improvement methods, such as by phenotype selection of tree crops, should be re-evaluated.

Alleged low productivity of some plantations may be due to inbreeding depression, not a lack of pollinators. Workshop I 45

Proposed methods:

• Molecular techniques (microsatellites, allozymes) to evaluate genetic diversity and dynamics; inbreeding depression, levels of outcrossing, pollen flow, cross-compatibility between 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 impact assessment actions.

Crops such as cotton and corn may hybridize with wild relatives and these may become "superweeds".

Proposed methods:

• Paternity analysis (microsatellites).

• Investigate time (phenology) or biological barriers (common pollinators).

• Observation of flight patterns of each pollinator species.

5. Containment measures should be tested and proposed in the case of any crop that has a risk of gene escape or has to maintain its purity.

Existing containment measures are still under development and have shown to be inefficient in many cases.

Proposed methods:

• Test and adoption of physical barriers that discourage pollinator flight.

• Observation of flight patterns of each pollinator species.

• Paternity analysis (microsatellites).

• Production of gene flow curves.

Pollinator conservation

1. The percentage of legally determined uncultivated land in private properties (known as "reserva legal") in Brazilian biomes such as the Amazon forest and Cerrado (savanna) should be maintained and enforced by law.

These areas are important both to sustain ecological services, such as pollination, and to maintain gene flow and diversity of native plant species. 46

Proposed methods:

• Molecular techniques (microsatellites, allozymes) to evaluate geneticdiversity and gene flow.

• Statistical comparison of reproductive parameters of native plants inisolated versus connected forest fragments.

• Legal actions.

2. Exotic plants or pollinators should be priority in long-term, in-depth monitoring programs, to detect overall impact in the ecosystem.

The invasiveness of an exotic plant may be benefited by a native pollinator, or the exotic pollinator may outcompete native species for resources and reduce productivity and regeneration patterns of native plants.

Proposed methods:

• Observation of pollinator behaviour in flower and among plants.

• Survey of pollinators in the area.

• Monitoring of the invasive plant spread.

3. Pollen and seed dispersal by animals should be encouraged in habitat rehabilitation programs. Their action 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 of genetic diversity, and promote awareness of native species by the public.

Proposed methods:

• Promote urban ecology awareness programs.

• Distribute material (specimens, seeds) and know-how among theauthorities responsible for urban green areas.

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

Other recommendations

1. National programs should be promoted to increase public awareness on the need for pollination studies and conservation.

Efforts should be made to create awareness of the services to humanity performed by pollinators, to change the perception concerning a variety of animals whose important service as pollinators is currently unknown to the public, so as to reduce the pressure on these animals caused by pesticides, deforestation and others. Workshop I 47

Proposed methods:

• List flagship plant species and explain their need for pollinators.

• Stress the beneficial role of non-charismatic animals, such as bats.

• Invent popular, appealing names for pollinators.

• Promote courses on the use of urban green areas.

• Produce and distribute user-friendly, informative material.

2. Leading laboratories should be encouraged to participate in the mapping of genetic diversity and structure of native plant populations of economic importance.

Currently many laboratories throughout Brazil are well equipped for the task, but few of them are involved in studying these organisms.

Proposed methods:

• Cooperative training courses.

• Government funding through public calls.

• Propose charismatic national or local species to obtain private or public funds.

3. Government agencies should produce, support and make widely available user-friendly material (printed, electronic, training courses), so that the above recommendations are put to practice by final users.

There are currently many comprehensive studies of economically important plants and pollinators whose results are unknown to the final user because of restricted (academic, technical) circulation. It is important that the initiative of producing this material be officially sponsored and supervised by scientists so as to gain credibility.

Proposed methods:

• Books could be transformed into PDF with the authors’ consent and be made available at official sites linked to agriculture, such as FAO, EMBRAPA, and WebBee (Brazil).

• Production and distribution of user-friendly, informative material, such as leaflets and booklets.

• Training courses.

Final remarks tems) and pollinator (bee behaviour in the flower and among plants, flight range) RAPs. Methods There is a vast literature on the parameters to Explanations of some recommended tech- be considered within each of these two, and niques follow, with emphasis on Brazilian on how to measure them. These protocols will study case examples. Among the methods allow data collection in the field by people proposed to help perform the recommenda- with little or no formal biological training. tions, several rapid assessment protocols Other methods, including statistical analyses, (RAP) could be developed, grouped broadly require both expertise and specific facilities, into two: botanical (phenology, flower densi- and will usually be performed by researchers ty, pollination syndromes, plant breeding sys- and trained personnel. 48

Genetic diversity isozyme variability. In this case, molecular tech- Isozyme electrophoresis is a technique for niques can provide a larger number of markers measuring the rate and direction of move- than isozymes. ment of organic molecules (in this case, DNA markers, on the other hand, show a enzymes) in response to an electric field higher number of alleles per locus and can be (Alfenas, et al., 1998; Pinto, et al., 2001). The more useful and accurate than isozymes. rate and direction of enzyme movement in a Higher numbers of markers can give more starch or and agar gel will depend on the accurate genetic diversity indices and paternity enzyme’s net surface charge, size and shape. analysis. However, most markers, such as ran- Enzymes can then be stained, resulting in a dom amplified polymorphic DNA (RADP) and series of bands in the gel. Those enzymes that amplified fragment length polymorphisms migrate to the same place in a slab of agar or (AFLP), are dominant and cannot show het- starch gel and yield similar banding patterns erozygous genotypes. In some cases, however, when stained are considered to represent the high sensitivity of these techniques may homologous enzymes (isozymes). When the limit the detection of the same markers isozymes are controlled by alleles of one gene, among genetically divergent individuals. they are called allozymes. The banding pat- Molecular markers require specialized training terns of specific types of enzymes in the gel and more sophisticated and expensive equip- may vary from plant to plant. Allozyme elec- ment, since their protocols are more elaborat- trophoresis is most useful to analyze genetic ed. These techniques are also more expensive diversity and outcrossing rate (the proportion than for isozymes, but their prices are drop- of the progeny generated from cross-pollina- ping (Ferreira & Grattapaglia, 1996). tion) of populations within species. As a Microsatellites are stretches of DNA that codominant marker, allozymes may directly consist of tandem repeats of a simple identify heterozygous genotypes. Heterozy go - sequence of nucleotides. These repeats can sity indices may be easily calculated for popu- easily be amplified using PCR (polymerase lations or samples of plants. chain reaction). The number of repeat units The visualization of electrophoretical pat- that an individual has at a given locus can be terns of isozymes requires simple procedures, easily determined using polyacrlyamide gel since isozyme bands are obtained through the electrophoresis. Using these gels, we can see reaction that identifies the enzyme. The tech- two genetic marks for most individuals; each nique of isozyme electrophoresis is simple to individual inherits one length of nucleotide learn, and it is cheaper and involves faster pro- repeats from its mother and one from its cedures than DNA markers. father (individuals with one band received the This method has been used in a number same band from both their mother and their of studies on the genetic diversity and popula- father). Primers to the microsatellite flanking tion structure of Brazilian species, such as the regions can be labelled with fluorescent dyes, commercially important palmheart (Euterpe allowing the amplified products to be separat- edulis, Conte, et al., 2003), rubber (Hevea ed in a polyacrylamide gel electrophoresis on brasiliensis, Yeang & Chevallier, 1999), and an automated DNA Sequencer. "cagaita" (Eugenia dysenterica, Telles, et al., In the last decade, microsatellites or simple 2001). However, some native and most culti- sequence repeats (SSR) markers have become vated plants have shown either very low or no an attractive tool for population genetic studies Workshop I 49

in plants due to their co-dominant inheritance, or seed set is caused by a reduced number of high allelic diversity and their abundance in visits or by their quality. Poor quality visits are plant genomes. The variability observed at SSR a result of visitors who do not perform polli- loci allows the accurate discrimination of indi- nation (thieves, for example), or who deposit viduals in natural populations and the estima- the wrong kind of pollen (self-pollen if the tion of genetic parameters, such as levels of plant is self-incompatible, or pollen from other inbreeding, heterozygosity, gene flow and mat- species if the pollinator carries pollen from ing system, which are relevant for the genetic other plant species). If the plant is self-compat- conservation and management of tropical trees ible, then it might not need the help of polli- under intensive human pressure. Microsatellite nators to set seeds. This is usually checked by markers have recently been developed for a bagging buds to exclude visitors and then ver- number of tropical tree species, such as the edi- ifying fruit and seed set. These procedures are ble piqui (Collevatti, et al., 1999) and palmheart standard and well explained in a number of (Gaiotto, et al., 2001), and the timber species books (Dafni,1992; Kearns & Inouye, 1993; mahogany (Swietenia macrophylla, Lemes, et Proctor, et al., 1996). In addition, data on al., 2002, 2003), "anani" (Symphonia globulif- commercially important parameters may be era, Aldrich, et al., 1998), "andiroba" (Carapa measured and compared among treatments, guianensis, Dayanandan, et al., 1999), and such as color, weight, shape, size and nutrient "angelim-vermelho" (Dinizia excelsa, Dick & contents of the fruits. Hamilton 1999). Different pollinators respond to resource landscapes and this in turn has consequences Plant reproductive biology on the extent of pollen dispersal (Bronstein and pollinator behavior 1995). Foraging flights may vary according to The importance of pollinator visits to a plant the homogeneity of resources (crop vs. natural species depends on its breeding system. Two environments), plant spacing (Manasse, 1992; aspects are usually evaluated through experi- Morris, et al., 1994; Morris 1993), and their mental manipulation: self-compatibility and flight range (Jacobi, 2000; Turchin 1998), self-pollination. The first evaluates if a flower among others. Several statistical and mathe- receiving pollen from the same plant is capa- matical methods have been used to compare ble of producing viable seeds, and to what flight behaviour of pollinators, particularly degree. If the species is self-incompatible, insects. They rely on field data that involve then it will need to be visited by pollinators tracking techniques, such as telemetry for ver- that carry pollen from another plant in order tebrates, the use of dyes and the direct obser- to effect cross-pollination. Dioecious plants vation and mapping of flight trajectories in are obligate outcrossers. To test for self-com- some cases (Turchin, 1998). These flight path patibility, manual self-and cross-pollination analyses are sometimes compared with gene experiments are performed on flowers, and flow curves using marked pollen or, if available, the results (usually fruit and seed set) are then genetically marked seeds (Kareiva, et al., 1994). compared to those from control (unmanipu- All the above procedures are the basis for lated) flowers. The difference in fruit or seed pollen flow estimation, and they are useful set also indicates if natural pollination is defi- for establishing actions concerning gene cient in a population. If this is the case, further escape, contamination risk, and plant popu- observations should follow to see if low fruit lation isolation. 50

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YEANG, H. Y.; CHEVALLIER, H. M. 1999. Range of Hevea brasiliensis pollen dispersal estimated by esterase isoenzyme markers. Annals of Botany, 84: 681-68. Workshop I 53

Group 3 Bee Management for Pollination Purposes

Abstract • A list of recommendations for study cases during the PDF B project in Brazil. Pollinating agents, especially insects, are clear- • Manual of protocols, according to the ly essential for agricultural production. The species, for rearing and managing native central point of discussions here are the impor- and Africanized bees for greenhouse and tance, the possibilities, and the management field pollination. of native bees, both solitary and stingless bees, • Protocols for using native and Africanized as well as honey bees, as pollinators. The par- bees to pollinate crops defined for study cases. ticipants were divided in subgroups and so the • A guide for sanitary care of migratory activi- results here presented. ties (transportation of bees from one area to another) for pollination purposes.

Aim Discussions The establishment of standard methodologies for managing native bees (solitary and social) The group was divided into three subgroups, as well as Africanized honey bees as pollina- according to the number of participants. tors of economically and locally important Subgroup 1: Africanized bees rearing and agricultural crops. To assess the biodiversity of management to be used as pollinators. local bees important for pollination and to Subgroup 2: stingless bees rearing and evaluate their status; to define the basic pro- management to be used as pollinators. cedures to be developed for rearing bees on a Subgroup 3: solitary and bumble bees rear- scale to allow their use as pollinators in agri- ing and management to be used as pollinators culture; and to improve capacity building and The whole group discussed together at training, at all levels. the end of each session, for one hour. Each subgroup was composed by, at least one person familiar with the crop, one person familiar Expected Product with pollination biology, and one person familiar with bee surveys. These discussions sections • Updated report on knowledge about were divided according to the following native and Africanized bees and their use aspects: state of art, perspective of the use of as pollinators. native and Africanized bees for pollination 54

purpose; rearing and managing bees on a • What and how detailed should these proto- large scale for pollination purpose, colony pro- cols be? duction on a large scale and best practice in • Is it possible to expand these protocols to migratory apiculture and meliponiculture for other crops/bees? pollination; and case studies. • Are there other interesting plants species to Some questions orientated those discus- be included in the study cases? sions, such as: • How to build awareness in crop growers • Which are the native bee species that polli- about the role of native and Africanized nate Brazilian crops? bees as pollinators? • Are there species normally being used as • How to involve government institutions with crop pollinators? bees as pollinators? • What are the main constraints for the use of • Is it possible to develop government policy native and Africanized bees as pollinators? on the use of native and Africanized bees as How to overcome these problems? pollinators? • How to measure the efficiency of each • What is necessary to make native and method for multiplying colonies on a large Africanized bee pollination feasible in Brazil? scale? • Which species are included in this methodol- The case studies discussed are represented ogy? on the table below. • What are the solutions for the problems of rearing bees in greenhouses? Study Cases • How to measure the result of using bees in Stingless Bumble Solitary Africanized greenhouses? Bees Bees Bees Bees • Do we know how to manage native and Strawberry Passion Cucurbitaceae fruit Africanized honey bees for pollination? Tomato Tomato Eucalyptus (Melipona) (Bombus) Cashew • What are the main difficulties with manag- Melon Melon Cotton ing native bees and Africanized bees for Coffee Umbu- Acerola pollination? Spondias • Is it possible to standardize breeding and managing methods for solitary and stingless bees? The results will be presented here by • Is it possible to overcome parasitism prob- groups: solitary bees and bumbles bees; honey lems for rearing bees in the tropics? bees; and stingless bees. • Can we already provide plant growers with native bees for pollination? • How should people become involved in breeding solitary and stingless bees for agricultural use? • Is it necessary to change established cropping practices for the sustainable use of bees as pollinators? • What are the conservation measures necessary to maintain a stable population of native bees in crop areas? Workshop I 55

A) Bumble Bees and Solitary Bees

Participants: Breno Magalhães Freitas (Coordinator), Celso Feitosa Martins, Clemens Peter Schlindwein, Dieter Wittman, Isabel Aves dos Santos, James H. Cane, Márcia de Fátima Ribeiro, Maria Cristina Gaglianone.

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

various crop species are necessary in order for be using flowering species of agricultural these bees to be used as large-scale reliable pol- interest (e.g. aggregations of Peponapis). linators in Brazilian agriculture.

Recommendations Solitary bee species In order to promote ground-nesting bees that Considering nesting habits, solitary bees can are effective and abundant pollinators of a be split into two distinct groups: crop (or desired tree species) or of a close rela- 1. grounding nesting bees; tive to this crop species, the farmer must man- 2. cavity nesting bees. age the crop (care with spraying, for instance) and the surrounding land (size of monoculture Currently promising taxa to be worked on are: acreage, proximity to fallow nesting sites), as • Exomalopsis (there are reports of tomato these bees' nests cannot be moved, and artifi- pollination); cial or "created" nesting sites are unlikely to • Epicharis (There are reports of West Indian be reliably and quickly colonized. cherry or acerola pollination); There is considerably more information • Centris (There are reports of West Indian on and well-succeeded examples of the use cherry or acerola pollination). of cavity nesting species of solitary bees. Species such as Osmia lignaria pronpiqua and Gr ounding nesting bees are difficult to Megachile rotundata are widely used and manage; in most cases there is no practical way managed for apple (Malus domestica) and to colonize areas with new nests, and merely alfalfa (Medicago sativa) pollination, respec- providing suitable nesting substrates (e.g. sand) tively, and their commerce amounts to millions rarely yields productive nesting for many years. of American dollars per year. There is little knowledge about ground Other promising taxa, such as Xylocopa, nesting bees as pollinators and about their Centris, Megachile, Anthidiini, Tetrapedia, management for this purpose. Three main already nest in artificial nesting-sites and can approaches are suggested to help identify potentially be managed to attain large popula- potential pollinating bee species: tions for use in pollination. Among these taxa, 1.selection of areas with less intensive agricul- Xylocopa can be considered special in Brazil ture for visitation to crop species (e.g. home because there is a demand for these bees and plantings of Cucurbita) where insecticide use there is some knowledge on its biology and rear- is unlikely, so that bee populations can ing techniques for use especially in Passiflora increase without extermination by pesticides; plantings. Serious constrains have been identi- 2.search for promising species of non-social fied and must be overcome in order to achieve pollinators (or social Halictidae) on wild large scale production and economic viability for crops and their wild relatives (co generics). exploiting these bees as crop pollinators: ex. Rhambutan, which is visited and pollinat- • ants are serious predators of bee nests and ed by Euglossa; must be controlled; 3.investigate pollen use by any large aggrega- • there is a need to eliminate parasites and tions where solitary bee species are found and diseases (clean management) before estab- discovered (e.g. Oxaea) to judge if they might lishing populations for increase; Workshop I 57

• there is a need for improved pest manage- • there is a lack of taxonomic pollen analysis or ment so that insecticide sprays are not floral visitation analysis to establish floral use. applied during blooming periods; • there is a lack of knowledge of techniques Other main recommendations are to com- and species' potential to produce bees in pile Brazilian studies of past trap-nesting expe- large numbers; rience in Brazil and produce a starting point for • there is a lack of knowledge of what crops those species that are present in the country benefit most from pollination by solitary bees; and can be reared in trap-nests. It is also impor- • agricultural lands lack margins/fallow/ tant to develop an insecticide management hedgerow areas for grounding nesting bees; program, in which pest control practices should • we need good methods for field assessment minimize bee mortality (label requirements on of pollination value; insecticides, for instance, should emphasize • affordable nesting materials/trap nests scouting and economic thresholds). This pro- need to be developed and made available, gram could be developed by the honey bee based on knowledge of which bees are management group due to their greater expe- going to be used; rience in using bees for pollination purposes.

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

Botanic Family Scientific name Common names - Common names - English Portuguese Apocynaceae Hancornia speciosa Mangaba Anacardiaceae Anacardium occidentale cashew Caju Spondias tuberosa Umbu Spondias spp Caja, Cajarana, Umbu-caja Bixaceae Bixa orellana Urucum, Coloral, Açafrão Cucurbitaceae Cucurbita pepo pumpkin Moranga Cucurbita moschata squash Abóbora Cucumis melo melon Melão Cucumis sativus cucumber Pepino Fabaceae Glycine max soybean Soja Vicia faba field bean Phaseolus vulgaris kidney bean Feijão Lens esculenta lentils Lentilha Pisum sativum pea Ervilha Vigna sinensis cowpea Feijão de corda Lecythidaceae Bertholletia excelsa Brazil nut Castanha do Pará 58

Malpighiaceae Malpighia emarginata West Indian cherry Acerola Byrsonima crassifolia wild cherry /nance Murici Malvaceae Hibiscus esculentus Gossypium hirsutum cotton Algodão Passifloraceae Passiflora edulis passionfruit Maracujá Passiflora quadrangularis giant granadilla Maracujá-açu Passiflora mucronata Maracujá Passiflora alata Maracujá-doce Solanaceae Lycopersicum esculentum tomato Tomate Solanum melongena egg-plant Beringela Capsicum annuum sweet pepper Pimentão Capsicum spp. Pepperony peperoni

Study Cases - Recommendations for some individual crops

Passion Fruit (Passiflora edulis) Bees: Xylocopa frontalis, X. grisescens, X.augusti, X. ordinaria, X. suspecta, and other large Xylocopa spp..

Nests: dead tree trunks, trap nests, Xylocopa nests.

Bee density: 25 females/ha in the case of X. frontalis.

Crop management: need of complementary floral resources: buzz pollinated species (Melastomataceae, Cassia, Sena, Solanum, etc). Cashew (Anacardium occidentale) Bees: Centris species. Centris tarsata tested, but other species can also be important. Take into account bee behavior, pollen distribution on the bee body; pollen viability is important: it is only viable for 4 hours.

Nests: trap nests.

Bee density: unknown.

Crop management: There is a need to supply pollen and oil producing plants (Byrsonima crassifolia for wild cashew), possibly through mixed culture with West Indian cherry (acerola) in commercial plantations. Cotton (Gossypium spp.) Bees: Emphorini spp.; Augochlorini; Bombus; Xylocopa.

Nests: depends on species used.

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

Crop management: depending on variety, there is a possibility of gain in the fruit production period. Workshop I 59

Cucurbitaceae

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

Nests: natural, in the ground (see discussion above).

Bee densitiy: unknown.

Crop management: local conservation should be promoted through education of growers. Free pollinators when available, but impossible to re-colonize once exterminated. West Indian cherry (Malpighia emarginata)

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

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

Bee density: unknown.

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

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

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

Recommendations stick nests, rather than drilled nesting blocks). 3.Conservation of natural areas (in order to Bee biologists should participate in crop sym- maintain natural populations); need not be posia sponsored by the International Society proximate to crop of interest (sustainability for Horticulture Science (ISHS), in order to extractive reserves for initiation of trap-nest- exchange expertise with the world's most ing programs). knowledgeable producers, breeders and 4.Spray management - toxic sprays must be processors of specific crops. avoided during bloom. 5.Different Xylocopa nest substrate structures Protocol with general should be compared (Freitas & Oliveira Filho recommendations to use solitary vs. Camillo models). bees as crops pollinators 6.Cultivation of other crops simultaneously for 1.Complementary floral resources should be year-round forage (no extensive monocul- provided. tures at a scale greater than flight range). 2.Plants for nidification (trunks) initially, later pro- 7.Adequacy of local/regional conditions. vide nesting substrates (although these also 8.Management of ruderal plants where nec- may be made from natural materials, such as essary. 60

Cost-effective technological improvements needed to reliably provide large numbers of 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, location of diseased or parasitized cells (for surgical removal from nest) and other applications. Advantages: quick and reliable. Options: could be a central unit at one laboratory to which samples can be sent by researchers from all over Brazil. Consider purchase of a used unit from a hospital, possibly 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, easily split 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 of acceptable nesting materials for cavity-nesting bees? Are manufacturers of hive equipment interested in producing interchangeable, easily assembled components of Xylocopa nest boxes? Are there manufacturers interested in producing drilled wooden nesting blocks in large numbers, or clever methods for using paper straws inserted within cardboard tubes within boxes (holes must be straight and approx. 15 cm deep for larger species, although research with individual species will demonstrate the hole diameters and depths that yield the greatest number of daughters per nest)? The mass production for drilled nesting blicks can begin by mimicking techniques already in use with Megachile and Osmia in the US, Japan and Europe. Aspects of those programs will clearly need adaptation to Brazil's tropical environments (for instance, how to handle multivoltine species, irrelevance of refrigerated overwintering), although some aspects may be more applicable in the south, such as for apple pollination in Santa Catarina. 4) Control of enemies Simple techniques needed for excluding ants from nesting blocks, especially blocks managed for crop pollination (would be nice for trap-nesting too, but perhaps not practical). Options: Physical barrier over which ants cannot walk. Must persist and not catch bees. Workshop I 61

Final considerations Final considerations regarding solitary bees regarding Bombus

1. Measuring effectiveness of methods 1. No importation of non-native species for population increase There should be regulation on importation of a. The only practical species to manage are bees: those whose populations can be increased • brazilian laws must be made controlling (more daughters than mothers). Bombus importation; b. Methods that produce populations with • seek an agreement among South American limited parasites and disease. countries or in the Mercosul related to bum- c. Affordable nesting materials that are practi- blebees importation; cal to make and endure for Xylocopa and • establish a monitoring program of invasive Megachile; there is a possibility of adaptation Bombus terrestris from Uruguay. This of existing methods. species was introduced into Uruguay in 1995 and now is free-living in nature, colo- 2. Greenhouse pollination nizing new areas and spreading towards The main difficulty in using solitary bees as the Brazilian border. pollinators in greenhouses is that glass and plastic absorb UV, which interferes with bee 2. Need for importation of non-native orientation during flight. How to measure Bombus species their pollination efficiency in greenhouses is There is no need for importation, because: not relevant; at this stage it is known which • these bee species are used only for pollina- species can be used. tion of greenhouse crops; • they are used mainly for tomato pollination, 3. Stimulating people to get but recent studies have shown that native involved in rearing and selling stingless bees Melipona quadrifasciata and solitary bees. Nannotrigona pirilampoides are good toma- Stimulate small growers who probably will to pollinator in greenhouses; own their own bees; to show the results the • exotic Bombus species may bring parasites growers can have when they use the pollina- and diseases to native species. tors (in numbers, value, amount of profit). We only have to convince about 1% of 3. Using native Bombus species for crop them; the rest will be very rapidly convinced pollination once they see the profits of the neighbours. We do not currently have knowledge to han- As it is not common in Brazil to value polli- dle native Bombus. If it is going to be used, nation services, and bees in general, espe- research is needed on biology and rearing cially solitary bees, it is important to dissem- methods. Two species are promising: inate information (about simple concepts • B. atratus - not so aggressive when in small such as pollination, pollinators, their services, colonies; etc.), distributed by extension programs (for • B. brevivillus - in Northeast Brazil, not example in small scale plantings of aggressive; has potential as a pollinator of Passiflora). crops of glasshouses and in open areas. 62

Final Remarks and the stingless bee Melipona quadrifasciata has been shown to be a good alternative Bombus are used commercially only to polli- to pollinate this crop in enclosures, and there nate greenhouse crops. This agricultural seg- are promising native Bombus species that ment is still small in the country, compared to could also be studied for this purpose. Finally, the size of the Brazilian agricultural system, Brazil should create laws prohibiting and and does not justify the risk and unknown punishing Bombus importation, follow the consequences of importing or allowing the spread of B. terrestris in Uruguay, and author- entry of exotic Bombus species. Also, most ities should monitor its arrival in the southern greenhouse cultivation is done with tomatoes part of the country.

References

FREITAS, B.M. 1997. Changes with time in the germinability of cashew (Anacardium occidentale) pollen grains found on different body areas of its pollinator bees. Brazilian Journal of Biology, 57 n.2: 289 - 294.

FREITAS, B.M., PAXTON, R.J. 1998. A comparison of two pollinators: the introduced honey bee (Apis mellifera) and a indigenous bee (Centris tarsata) on cashew (Anacardium occidentale) in its native range of NE Brazil. Journal of Applied Ecology, 35 n.1: 109 - 121.

FREITAS, B.M., OLIVEIRA-FILHO, J.H. 2001. Criação Racional de Abelhas Mamangavas: para polinização em áreas agrícolas. Banco do Nordeste, Fortaleza – CE, Brazil.

FREITAS, B.M., PAXTON, R.J., HOLANDA NETO, J.P. 2002. Identifying pollinators among an array of 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 West Indian cherry (Malpighia emarginata) and its putative pollinators, Centris bees in NE Brazil. Journal of Agriculture Science, 133: 303 - 311.

HOLANDA NETO, J.P., FREITAS, B.M., BUENO, D.M., ARAÚJO, Z.B. 2002. Low seed/nut productivity in cashew (Anacardium occidentale): effects of self-incompatibility and honey bee (Apis melli - fera) behaviour. Journal of Horticultural Science & Biotechnology, 77 n.2: 226 - 231. Workshop I 63

B) Honey Bee

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

Abstract ardly pollinated by wild honey bee colonies or by apiaries that happen to be nearby, resulting Pollinating agents, especially insects, are clear- in production losses due to inefficient pollina- ly essential for agricultural production. Honey tion. Africanized honey bees are seen much bees have become increasingly important, as more as honey producers than as pollinators. field sizes have increased and native bees have For many crops that do not traditionally decreased, due to intensive land use and pes- use honey bees for pollination, such as ticides. An important advantage of honey bees oranges, peaches, strawberries, sunflowers is that they can be quickly taken to and and forage soybeans, we have data indicating removed from the fields in large numbers, significant increases in fruit and seed produc- facilitating the integration of these pollinators tion and improved fruit quality with pollination into pest management programs. A single by Africanized honey bees in Brazil (Nogueira- truckload can carry 20 million potential polli- Couto, et al., 1998, Couto 2002). Africanized nators. Honey bees contribute to more than honey bees are very active pollen collectors, 80% of the agricultural produce pollinated by making them good pollinators, and they have insects. Unfortunately, Brazil does not have a been found to remain on the target crop strong tradition of using bees for pollination, longer than do the European honey bees that different from the USA, where more than 2 are traditionally used for pollination in other million colonies are rented annually. Bee- countries (Basualdo, et al,. 2000). Africanized keeping in Brazil has grown considerably dur- bees also are more active on the flowers, fly ing the last few years, especially due to honey faster and are quicker to recruit other hive market conditions. Brazil now has about 2,5 mates, than are European bees, making them million colonies available for bee products pro- more active and efficient pollinators. Africa- duction (honey, wax, propolis, pollen, royal nized bees forage at lower light levels than do jelly and bee venom) and for pollination pur- European bees, so that they work longer days. poses. There are beekeepers specialized in pol- They also do not reduce brood production lination, especially for apples, melons and during winter, so the colonies remain strong, cashews. All of these products are both con- with abundant foragers for pollination activi- sumed in country and exported. To obtain ties. It is relatively easy to establish new export quality fruit, insect pollination is colonies by collecting swarms with bait hives, absolutely necessary. and Africanized colonies grow quickly, so that Unfortunately, many of the crops that beekeepers can easily produce the large num- could benefit from pollination, are either not bers of colonies needed for pollination of pollinated at all, or are incidentally and haphaz- crops. There are well-established migratory 64

beekeeping techniques, and truckloads of often affected by pollination. Photos of cross bees can be quickly and timely moved to flow- sections of the fruit can show the number and ering crops (De Jong, 1996). distribution of the seeds, which are clear indi- cators of pollination efficiency. The fruit quality can also be evaluated by measuring sugar Discussion and protein and other substances, and by evaluating organoleptic (taste) factors. Africanized honey bees have been used for pol- We already know how to manage lination in greenhouses in Brazil. However many Africanized honey bees as polinator for some bees are lost from the colonies and it is difficult crops, such as apples and melons, however to maintain the colonies alive under greenhouse this is not always done in the most efficient conditions. Some researchers and beekeepers way. Many crops that would clearly benefit have been able to overcome these problems, from the introduction of bee colonies are not but the techniques that they use are not pub- routinely pollinated. Generally speaking, polli- lished, nor is there an established system that nation is little valued or understood by farm- works uniformly under all circumstances. Most ers, nor are beekeepers aware of the true attempts to use honey bees in greenhouses are value of the services that their bees provide. initially unsuccessful, however after numerous We have data indicating significant increases trials some researchers have been able to main- in fruit, seed and vegetable production due to tain colonies for long periods, efficiently polli- pollination by Africanized honey bees, howev- nating the crop. In order to make efficient use er little of this information is available to the of this resource, it will be necessary to make growers. Often objective studies on commer- controlled studies, and develop standard, prac- cial varieties are lacking. This is true both for tical techniques that should be made widely field crops and for greenhouse crops. The lat- available to beekeepers and growers. ter are unviable commercially unless adequate We can measure the result of using honey pollination is provided. Many crops are in fact bees in greenhouses by examining the crop pollinated incidentally by honey bees from quantitatively and qualitatively. Normally, this nearby apiaries, or by wild honey bee colonies, is done by measuring the weight, size and however the grower is not aware of the number of fruits, by determining the time till importance of these services. Frequently he production of the fruits (which may be antici- has low production, without realizing that the pated by adequate pollination), and by calcu- reason is a lack of pollinators. lating the percentage fruits that are considered The main difficulties with managing of high quality. Another important quantitative Africanized bees for pollination can be listed as: aspect is the cost and benefit of the pollination 1.there are no established techniques for activities. Using honey bees has a cost, and this using Africanized bees under Brazilian con- should be compared with the gain in crop pro- ditions on most crops; duction attained with pollination. Photos of 2.often the hives are not made with standard fruit that are produced by plants exposed to measures, or with inferior materials, making bees, versus those that are produced without transport and management difficult; bees, are often quite useful for illustrating the 3.the bees are quite defensive and growers are value of bee pollination. Appearance is impor- often reluctant to place them in or near the tant, as the color and shape of the fruit is crops that need pollinating; Workshop I 65

4.there is not sufficient care in the transporta- will increase the availability of honey bees to tion of colonies, so that accidents are com- satisfy these increasing needs for pollination. mon and this discourages their use for polli- Landowners need to be made aware of the nation; value of having bees placed near the crops. 5.beekeepers are not aware of disease prob- The extension service (Agriculture House - lems, and often incorrectly try to treat their Casa de Agricultura) does not provide appro- colonies, and some have introduced con- priate information about pollination. Unfor - taminated bee products and equipment tunately, even in the case of crops for which we from abroad, threatening beekeeping throu - have clear evidence that honey bees signifi- ghout the country; cantly increase production, growers frequently 6.there is a lack of central laboratories that can do not include pollination in their management provide timely and accurate diagnoses of programs, and often even prohibit the intro- bee diseases, and also there are no field per- duction of bee colonies onto their property, or sonnel to advise beekeepers about this kind they may charge the beekeepers, while in other of problem; countries the beekeepers are paid for their 7.growers are frequently unaware of the services. This lack of tradition to include bees importance of bees and pollination, and in greatly diminishes the potential gain of the fact they often prohibit the introduction of growers. We need to have more good quality bees into their properties; they use insecti- data and then convince the growers by using cides indiscriminately and incorrectly with- demonstration plots. out any concern for the effects on the bees and the beekeepers; Bee diseases 8.there is no tradition for making pollination Some new diseases from other countries contracts that include a provision for com- threaten beekeeping and hence can affect the pensation for the beekeeper in the case of availability and quality of honey bee colonies losses due to pesticides or the stealing of for pollination. Unfortunately, these incidents hives on the grower's property. There should of new diseases have not been sufficiently also be a provision for responsibilities in the controlled and studied by competent resear- case of an accident with the bees. chers and authorities. Beekeepers are also unaware of the need for good practices that will avoid the introduction of these new dis- Problems to be overcome eases. For instance, honey and pollen that has been imported (both legally and informally) is Changes in agriculture have created an often exposed to the bees. Honey is handled in increased need for honey bees. processing plants, and often some of it is There is pressure to convert natural areas into inadequate for commerce; beekeepers feed agricultural land, without concern about main- such discarded honey to their bees (Message taining habitat for pollinators. Loss of natural & De Jong, 1998). This has resulted in the pollinators due to the loss of habitat increases introduction of American Foulbrood Disease the need for honey bees. More intensive farm- (Paenibacillus larvae) spores from imported ing and larger fields of crops overcomes the honey into honey bee colonies. This situation capacity of local native bees to pollinate. We needs to be more closely investigated, and the need to develop techniques and policies that beekeepers should be made aware of the dan- 66

ger of such practices (De Jong, 1996). A simi- used systematically in order to develop eco- lar problem has occurred with a fungus dis- nomically viable pollen substitutes. ease, Chalkbrood, caused by Ascosphaera apis, which entered Brazil in imported pollen. There is no sanitary control of the move- The beekeeper normally separates the pollen ment of colonies. pellets in the bags of imported pollen and the Though Chalkbrood, a fungus disease, has powdered pollen that is left is fed to the bees. recently been diagnosed in Brazil, and Chalkbrood has now become established in American Foulbrood is suspected, there is no several parts of Brazil as a result of these prac- sanitary control of the movement of colonies. tices; we need to have more information Consequently these new bee diseases could about the impact of this exotic disease on be spread to new regions, causing damage to Africanized honey bees. apiculture, which could affect the availability of bees for pollination. It is recommended There are no central laboratories to iden- intensive studies of those new diseases, to tify diseases. determine their occurrence and their impact Beekeepers need to have a place to send sam- on the colonies. Government agencies should ples in order to learn what diseases they have, be prepared to diagnose diseases in the labo- and to determine whether their problems are ratory and to train bee colony inspectors who really caused by parasites or disease organ- can make field diagnoses and develop and isms. This service exists in nearly all major bee- implement appropriate control policies. keeping countries and now should be imple- mented in Brazil. Problems with quality and standardization of the Beekeepers do not know diseases beekeeping equipment Diseases are normally not a big problem in In some parts of the country, non-standard Brazil, but beekeepers sometimes incorrectly hives are used. Many times, among those who try to treat colonies with antibiotics and aca- use standard Langstroth equipment, there are ricides whenever they suspect a disease. Their problems with non-standard measurements. lack of knowledge and the lack of govern- Beekeepers are often not aware of the correct ment infrastructure to help them cope with standards and they make their hives based on disease problems often makes them take equipment that they have purchased. As the inappropriate actions. Besides the unneces- purchased hives are frequently not exactly sary costs and damage to the bees due to built, badly dimensioned hives are perpetuat- such home-brew treatments, there is a dan- ed. Many times new beekeepers have pur- ger of contaminating the bee products. We chased bad equipment with funds that they need to study the actual disease problems have received on credit. These can be badly and determine nutritional needs. A lack of built hives, with uncured "green" wood, or information about nutrition, especially pro- made with wood that is inappropriate for api- tein needs, actually causes many problems culture. Such hives start to bend and open that are mistaken for disease. Techniques within a few months. Unfortunately, the fund- have been developed to more objectively ing agencies that set up programs to foment evaluate honey bee diets (Cremonez, et al., apiculture often provoke these kinds of pur- 1998), but these new methods need to be chases of substandard materials due to cost- Workshop I 67

competitive purchasing policies. Later, the bee- escape from the hives, and many colonies die keepers have a difficult time repaying the cost due to overheating. The local authorities are of the equipment, as it is commonly discarded unaware of the importance of the need for within a short time. timely movement of colonies, and may inter- fere with transport. The handling and transport of beehives in Brazil is not mechanized Problems with a deterioration Now all hives and honey supers are transport- of natural areas ed from trucks to the apiary, and back, by The lack of natural areas means that bees have hand. Hives are heavy, especially when they no wild flowers for supporting and maintaining are full of honey. This hand carrying often colony growth. This means that the colonies causes back problems for small-scale beekeep- are weak or can even die and therefore are not ers, which depend on family labor. Beekeepers available for pollination services. In various with larger numbers of colonies must hire parts of the country there is so little natural for- help, and this makes their management age that beekeeping is uneconomical, especial- expensive. A beekeeper in the USA or Canada ly in regions where there is intensive agriculture can handle more than a thousand colonies by and therefore with a great need for bees for himself, or with only a single helper. A similar pollination. We need to find ways to promote number of colonies in Brazil would need at the maintenance of natural areas on farms least five or six laborers, and the moving (possibly through tax incentives) and to have process takes much longer than in other coun- states and municipalities plant trees that pro- tries. Transporting colonies for pollination vide forage (nectar and pollen) for pollinators. requires specialized labor, at specific times. If beekeeping had mechanized alternatives then There is lack of natural forage for the bees this transport would be cheaper and more effi- The lack of natural forage during various times cient. However, the fork lifter tractors (bob- of the year can be partially overcome by artifi- cats) currently used in other countries are too cial feeding of sugar and protein diets. expensive for Brazilian conditions. It would be However, sugar is often too expensive, so it more cost efficient to pursue intermediate, less would be useful to have a means to provide costly, alternatives for mechanization. We sugar or sugar syrups at a low price for the need to identify appropriate techniques for beekeepers to properly prepare their colonies hive lifting and transportation, and test and for pollination. The most important nutritional adapt them to local conditions. problem is a lack of appropriate protein when pollen from flowers is not available. At the There are problems with transporting bee moment, no adequate artificial diet is avail- colonies able. Such diets need to be developed and Beekeepers are not aware of their responsibil- tested. A relatively simple laboratory technique ities and correct procedures when they have developed in Brazil is available for the initial an accident during transportation of hives screening of food by-products that could be from one region to another. They are unaware used as protein sources for bees. Large scale of the best ways to transport bees, and there- testing should be done, with field testing and fore accidents are more common than they demonstration of the most promising alterna- should be. Frequently they lose bees that tives (Cremonez, et al., 1998). 68

There are misconceptions about how by pesticides. Beekeepers avoid crops where bees could impact on crops insecticides are used; this reduces honey pro- In some crops, such as oranges, there are duction and agricultural production. Crops misconceptions about the danger of bees such as cotton would be more productive if transmitting plant diseases. Generally, deci- the bees could pollinate them. Native bees and sions are made without any real evidence of wild honey bee colonies are killed by excessive such a problem. and inappropriate use of pesticides, making it There are problems with beekeepers necessary to bring in commercial honey bee obtaining permission to place bees on farm- colonies for pollination purposes. Labeling of land - due to fear of the bees interfering with these pesticides should include information cultural practices, while growers are unaware about toxicity to bees. of the value of pollination. We need to have case studies about how bees interact with Case studies to assess main pesticide prob- crops and to have documented information lems that affect bees that will help growers and beekeepers under- Develop a manual about the use, value and stand the real effects of bees on crops. Some care of honey bees. Take advantage of case of this information is available from other studies about improvement of production and countries, and can be adapted and appropri- quality of farm products to educate farmers ately communicated. However local experi- about how to best incorporate pollination into mental work should also be done to test the their management practices. The impact of impact of bees under local conditions. the most commonly used pesticides on flowering crops should be investigated. Beekeepers have problems with hives being stolen Farmers and policy makers are often Apiaries often have to be placed in remote unaware of the need for pollination places where the colonies are easily stolen, due Growers are often unaware of need for polli- to inappropriate management and fear of the nators and of pollinizer varieties. International bees. The government and the police normally pollination techniques need to be adapted to gives little support to the colony owners, and local conditions. The agricultural policies nor- often take no action, even when there is proof mally ignore the need for pollinators. EMBRA- that colonies or colony products have been PA, SEBRAE and other appropriate institutions, stolen. Policies should be developed to provide such as universities, should develop projects to legal and police support to reduce this colony test the value of pollination on crops and vari- thievery problem. Case studies need to be eties. They should also develop crop manage- made to find ways to maintain apiaries in ways ment schemes that minimize the impact of that there is less impact on farm workers and insecticides on honey bees. This information animals, so that apiaries can be kept in more should then be made available to the farmers. protected areas. Insuring colonies against rob- There should be demonstration fields and bery is also unknown, making financial security courses to make the farmers aware of how for the beekeeper nearly impossible. much they can gain by including pollination in their management scheme. Problems with pesticides We need clear recommendations about Presently many honey bee colonies are killed number and size of colonies needed, and how Workshop I 69

to place them. Agricultural extension does not Rearing and management currently train farmers about ways to manage of Africanized honey bees their crops for maximum pollination. in greenhouses Extension services need to develop courses and educational material. They should devel- Current problems: op case studies in cooperation with local • lack of knowledge of the minimum require- growers (on-farm experiments). ments necessary to use Africanized bees in greenhouses (size of the colony, best time to Consumers are not aware of how to introduce the bees to the crop, culture select good quality (well pollinated) specifics and management techniques); fruits and vegetables • misconceptions about Africanized bees as Demonstration materials should be developed effective pollinators; to help the consumer recognize and choose • aggressiveness of the bees; good quality products. Fruits and vegetables, • lack of technical and practical experience. such as melons, watermelons, apples and cucumbers, often have fewer than normal Proposals: seeds, which results in inferior products with a • make producers aware of the usefulness of bad taste. Such an awareness and educational honey bees for pollinating in green houses; programs will create a more sophisticated con- • inform public and private agencies involved sumer and will encourage growers to use bees in rural extension, technical assistance and to produce high quality fruit. promotion; • encourage research institutions to make Other problems: studies on this subject, through specific • beekeepers generally are not concerned guidelines and financing; about determining the pollinating efficiency • develop informative material, as a tool to of their colonies, but are only trying to pro- encourage increased use of honey bees in duce the largest possible amount of honey; greenhouses, informing about successful • beekeepers do not know how to stimulate experiences in Brazil and from other parts the bees to collect pollen, which increase of the world, and by examining econom- pollination efficiency, instead of nectar; ic criteria; • beekeepers do not know how to direct bees • develop incentives for using honey bees as to a crop that needs pollination; pollinators in greenhouses and reducing the • beekeepers distribute their beehives in a man- use of pesticides (tax deductions, low inter- ner that is convenient for management, with- est loans, etc.); out concern or knowledge about the most • publicity campaigns informing about the efficient arrangement to facilitate pollination; better quality of well-pollinated fruits and • beekeepers manage their bees only for vegetables, uncontaminated by pesticides; honey production because the farmers nor- • encourage and make available techniques mally do not pay for pollination services; for producing food in greenhouses; • we do not know the support capacity of • capacitate technicians involved in extension agricultural areas for honey bee colonies or and who assist farmers so that they can how many honey bee colonies can be help them use honey bees as pollinators in placed in a specific area. greenhouses. 70

State of the art of the use of Africanized stration plots to show the value of pollina- honey bees for pollination tion to the farmers. Currently, honey bee colonies are rented for pollinating apples, melons, cashews and Rental prices for bee colonies some vegetable crops in Brazil. There are Beekeepers and growers are generally efficient techniques for transporting the unaware of how much they can or should bees, but data on other cultures are lacking. charge for their services. There is little tradition Isolated experiments have demonstrated for this activity, and beekeepers often have a the value of bees for many crops in Brazil, difficult time to determine their real costs and but these have not influenced the growers, the monetary benefits for the farmers. This and more objective and thorough experi- requires economic studies, which should then ments are needed, preferably with demon- be made available to both parties.

Case studies to determine the need for pollination of major crops Use of Africanized bees for pollination Recommendations for case studies

Cotton

Principal 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 the quality and the quantity of the fruits produced; • fear of the strong defensive behavior of the africanized bees; • productivity can be increased more than 40% with adequate pollination, however the responsibilities of the farmer and the beekeeper are often not well defined; • we need to have good data on the real economic advantages of using 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 fields to determine the best recommendations for pollination; • as beekeepers would not normally take their hives to coffee plantations, economic studies should be made to determine adequate pollination fees, taking into consideration the benefits for the growers.

Recomendations São Paulo campus in Ribeirão Preto, SP, but it needs to be improved and made more 1.A document should be developed about the widely available. There is a book with a col- state of art of the use of Africanized honey lection of 300 thesis abstracts (in Portuguese bees for pollination. and English) and a list of over 2000 publica- 2.Preparation and distribution of a manual on tions on bees made in Brazil until 1992 standard methodologies for rearing Africa - (Soares & De Jong 1992). This material is nized bees for pollination purposes. updated periodically and is kept in a data- 3.Development of a central library with all the base, which is available to some researchers. available Brazilian literature on pollination, We need to create means to archive and including theses and congress proceedings, digitalize all of those articles and theses, so and that those be made available via Internet. that this information will be more widely This has been initiated at the University of available, and will not be lost. 72

4.Initiate a scientific journal on pollinator of the colonies and integration with other biology in Brazil. Brazil has many bee cultural practices. researchers, however much of the informa- 5.Design and install apiaries and infra- tion is not readily available. A scientific structure necessary for pollination. journal will help remedy this problem and Determine the number of apiaries and will help direct students and professors to colonies that will be needed at appropriate study pollination problems. This journal times to give support to the pollination could be produced online at relatively low activities. cost, and could help consolidate bee 6.Training of personnel responsible for research in Brazil. main taining the colonies in conditions 5.Develop a manual on research techniques for adequate for pollination. Preparing colo - pollinator studies, especially to determine the nies for pollination requires specific man- value of pollinators for crop production. agement so that they will be at an adequate stage of development and with sufficiently large populations to adequately Rational Program of Pollination pollinate the crop. 1.Determine how well crops are pollinat- 7.Training of personnel to collect pollina- ed currently and investigate the production data in the field or hire such help. The tion potential if there were full, ade- results of pollination should be constantly quate pollination. Some crops are already monitored. well pollinated, and additional pollinators do not increase production. In other crops and regions, there are so few natural polli- Final recommendations nators that supplemental pollination can make the difference between uneconomi- Considering what are the conservation meas- cal production and profit. ures necessary to keep a stable population of 2.Estimate economic viability of pollina- Africanized bees in the cropping areas: tion program. The producer needs to have 1.incentives, such as tax exemptions for bee- an idea about whether it will be economical- keepers and for growers for pollination of ly viable to use pollination for his crop, con- crops in Brazil; sidering the costs involved with personnel, 2.PDF-B should make a policy of recogniz- transport, and renting bee colonies, com- ing the need for Africanized bees for pol- pared to the increases in production. lination; 3.Identification of the requirements of the 3.conduct case studies to show the importance crop and determination of the pollina- of wild pollinators in respective habitats; tion needs. Each vegetal species has its 4.stop indiscriminate logging and commercial own specific pollination needs and appropri- felling of trees by enacting laws; ate pollination techniques are needed to ful- 5.promote and encourage re-conversion of a fill these needs. certain percentage of intensively cultivated 4.Determine the pollination strategy that areas to provide rescue space for the mul- should be used. There is a need to deter- tiplication of wild honey bee colonies by mine the number of colonies per hectare, providing incentives (tax exemptions, sub- the arrangement and temporal placement sidies etc.); Workshop I 73

6.train farmers in making judicious and safe vated areas and encourage multiplication use of carefully selected, less toxic, pesti- and growth of native plants that can provide cides in safer formulations; food for wild bees; 7.promote IPM (Integrate Pest Management); 9.encourage agro-biodiversity by planting 8.provide nesting strips/spaces near the culti- some areas with native plants.

References

BASUALDO, M.; BEDASCARRASBURE, E.; DE JONG, D. 2000. Africanized honey bees (Hymenoptera: Apidae) have a greater fidelity to sunflowers than European bees. Journal of Economic Entomology, 93: 302-307. COUTO, R.H.N. 2002. Plantas e abelhas, uma parceria em crise? Anais do V Encontro sobre Abelhas. Ribeirão Preto - SP, Brazil, p. 87-94. CREMONEZ, T.M., DE JONG, D., BITONDI, M.M.G. 1998. Quantification of hemolymph proteins as a fast method for testing protein diets for honey bees. (Hymenoptera: Apidae). Journal of Economic Entomology, 91: 1284-1289. DE JONG, D. 1996. Africanized honey bees in Brazil, forty years of adaptation and success. Bee World, 77: 67-70. DE JONG, D. 1996. Loque americana, o grande perigo para o futuro da apicultura brasileira. Mensagem Doce, 39: 11 -12. MESSAGE, D., DE JONG, D. 1998. Dispersão Internacional da bactéria Paenibacillus larvae, 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, a perennial soybean, by Africanized honey bees. Journal of Apicultural Research, 37: 289-291. SOARES, A.E.E., DE JONG, D. 1992. Brazilian Bee Research. Sociedade Brasileira de Genética. Workshop I 75

C) Stingless bees

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

Abstract needed, although many studies had been done in the last years. Among the 13 Stingless bees are social bees that live in tropi- Australian epiphytic orchids whose pollinators cal regions of the world. They are poorly stud- are confirmed, 9 are pollinated by stingless ied and known, even though they are the bees (Adam & Lawson, 1993, apud Heard main visitors of numerous flowering plants in 1999). Males of some stingless bees are the tropics and likely the principal pollinators important pollinators of native Brazilian of many of them (for a review, see Heard, orchids of Maxillaria genus (Singer, 2002; 1999). Only recently attention on their role as Singer & Koehler, 2004) who offer fragrances pollinators has been paid. Here we evaluated and colors that attract workers of Trigona. the knowledge obtain worldwide until now on Recently, Slaa, et al. (2006) reviewed the role the role of stingless bees as pollinators, identi- of stingless bees as pollinators and the crops fied some crops that could be pollinated by that they effective pollinate doubled in num- them, as well as the constraints for their use as ber since the excellent review of Heard (1999) pollinators in large scale for agricultural Although their breeding techniques are demand in Brazil. available to beekeepers, at least for some Data for this report were updated until 2006. taxa such as Melipona, Scaptotrigona and Tetragonisca, no stingless bees are yet commercially available to growers for pollination Introduction purposes. The unique example where protocols for greenhouse pollination are well estab- Stingless bees are diverse in tropics and can lished is the use of Tetragonisca angustula and potentially be used as pollinators for several other small stingless bees for strawberries native and exotic crops cultivated in Brazil (Fragaria x ananassa Duchesne, Rosaceae) pol- (Nogueira-Neto, et al., 1959; Bego, et al., 1989 lination (Malagodi-Braga, 2002; Malagodi- a and b; Heard, 1987, 1993, 1994, 1999; Braga & Kleinert, 2004). Some species of Heard & Exley, 1994; Ish-Am, et al., 1999; Melipona could be good pollinators of some Malagodi-Braga, et al., 2000; Slaa, 2000; Solanaceae crops that need “buzz pollina- Castro, 2002; Malagodi-Braga, 2002; Cauich, tion”, as Melipona quadrifasciata for tomatoes et al., 2004; Cruz, et al., 2004). The native (Lycopersicum esculentum) growing in green- Brazilian stingless bees richness is estimated in house (Del Sarto, et al., 2005). For native trop- 500 species (Camargo, p.c.). Due to the high ical fruits, as umbu (Spondias tuberosa), açaí stingless bee diversity, basic research is still (Euterpe oleraceae) and cupuaçu (Theobroma 76

grandiflorum), the pollination requirements resources, and have some requirements, as are being studied (see table 1). specialization in use of logs of some plant Coevolution between local flora and stin- species or diameters at breast height bigger gless bees should occur in high diverse habi- than 50cm. This has implications for reforesta- tats. Despite of their generalist use of floral tion programs as well for the sustainable use of resources, stingless bees show floral prefer- forest and the conservation of stingless bees, ences (Ramalho, et al., 1990; Biesmeijer, et al., important native pollinators (Venturieri, 2004). 2005; Biesmeijer & Slaa, 2006). It is necessary The use of stingless bees for pollination to improve this knowledge in order to deter- purposes should consider the settlement of mine preferences and the main plants indi- corridors between patches of native vegeta- cated as food source for their successful tion for keeping native populations of polli- breeding, as well as for using in habitat nators as well as trees for nesting and flow- restoration programs. ers for food (nectar and pollen). As agricul- A huge problem for Brazilian stingless ture is increasing in Brazil, the land manage- bees breeders and for capacity building activi- ment of surrounding agricultural areas is also ties is that relevant literature is in English or not very important. Finally, stingless bees could easily available; most bee species have not be excellent pollinators to be used by small been studied yet. A recommendation is to farmers (family growers) because they do not make available, in Portuguese, a synthesis of sting, are easy to manage, and are appropri- the present knowledge, written for different ate to small lands and cheap to rearing. stakeholders, and to provide basic knowledge Besides that, some small farmers have the needed for rear them. The WebBee (Saraiva, et traditional knowledge to rearing them, using al., 2004) was constructed in order to be our their honey as medicine. They need to learn infoway in this task. how to manage them for pollination and Considering the high biodiversity of sting- conservation purposes. less bees, and the new meliponiculture regulation for research and for beekeeping (CONA- MA_346, 2004), it is necessary to improve the State of art development of breeding techniques, in order to provide bees for research and for meliponi- Stingless bees as greenhouses culture. Nests can be obtained by using trap pollinators nests in nature; a nest census and a bait-trap In 1988, Luci Rolandi Bego, from São Paulo survey in natural and agricultural areas for stin- University, went to Japan with a grant of gless bees is also a priority for investigation. A Brazilian Academy of Sciences to work with Y. recent research developed in Sarawak, Asia, Maeta on the use of stingless bees as pollina- showed the effects of human disturbance on a tors in strawberry greenhouses. She carried stingless bee community in a tropical rainforest, with her a colony of Nannotrigona testace- as a result of changes in resources availability icornis, a colony of Plebeia droryana and one (Eltz, et al., 2002 and Eltz, et al., 2003; of Tetragonisca angustula, in rational hives, Samejima, et al., 2004). Such changes in the chosen by chance among the other species bee community may affect the reproductive available at São Paulo University Bee success of plants and ultimately forest compo- Laboratory, where they were know to be very sition. Nests sites are considered as essential strong. Nannotrigona testaceicornis was test- Workshop I 77

ed in strawberry greenhouse, and the results tomato, Lycopersicum esculentum. Velthuis of its efficiency is in Bego, et al., The other (2002) tells the successful story of the bumble- colonies were used to study foragers’ behav- bee Bombus terrestris used as tomatoes polli- iour under greenhouse condition (Bego, et al., nators in greenhouses in the Netherlands and 1989a). Later on, Trigona minangkabau from Belgium that resulted in a big industry of bum- Sumatra was also tested in strawberry green- ble bee rearing in various pary of the world. houses, and the result compared with the effi- Nowadays 1 million colonies of Bombus ter- ciency of Apis in the same greenhouses restris are yearly sold for using in agriculture (Katutani, et al., 1993). (Velthuis & Van Doorn, 2004). However, exot- In Brazil, stingless bees as pollinators for ic pollinators are to be avoided in many coun- strawberries in greenhouses were tested by tries including Brazil. In search of local solu- Malagodi-Braga (1992); Malagodi-Braga and tions, Brazil found that the use of some species Kleinert (2004). Protocols for greenhouse pol- of Melipona could be good pollinators of lination are well established related to the use some Solanaceae crops that need “buzz polli- of Tetragonisca angustula and other small nation”, such as the relatively large Melipona stingless bees. Malagodi-Braga & Kleinert quadrifasciata for tomatoes (Lycopersicum (2004) showed the efficiency of Tetragonisca esculentum) growing in greenhouse (Del Sarto, angustula as a pollinator in “Oso Grande” et al., 2005). Nevertheless, Macias & Ma cias cultivar: in a greenhouse with 1350 plants (2001) and Cauich, et al., (2004) verified that almost 100% of flowers developed into well- Nanno trigona pirilampoides is a very success- shaped fruits compared to 88% with open ful pollinator for tomatoes in greenhouses, pollination in the field. opening new possibilities for small stingless Sweet pepper (Capsicum annuum, Sola- bees use in those. na ceae) is another crop cultivated around the world, in open fields and in greenhouses Open field pollination (where its cycle is extended for production all and stingless bees year round). Although sweet pepper is a self- Heard & Exley (1994) already considered the pollinating plant, it benefits from bee pollina- importance of agricultural landscape and nat- tion (Rasmussen, 1985). In Brazil, Cruz, et al., ural vegetation for providing pollination servic- (2005) tested the efficiency of Melipona sub- es (the abundance of Trigona carbonaria in nitida as a greenhouse pollinator of sweet orchards of macadamia was correlated with pepper, variety All Big. They used four treat- the extent of natural surrounding Eucalyptus ments in their research: hand cross-pollina- vegetation). Venturieri (1993) also remarked tion, hand self-pollination, pollination by bees the importance of natural vegetation around and restrict pollination. The fruit set was not the cupuassu crop in order to provide the improved by the use of M. subnitida as polli- needed pollinators. Kremen (2004) considered nators, but the number of seeds per fruit, the the importance of bee community as crop pol- average fruit diameter and fruit weight linators, pointing out that if we maintain sev- increased; a lower percentage of malformed eral bee species from natural environments vis- fruits were also found, comparing with self- iting flowers, the shortage of one species in pollinated sweet pepper. one year could be compensated by the other Another important crop also often kept in visitor’s species, diminishing the impact of pol- greenhouses in Brazil and worldwide is the linators’ shortage on crops. 78

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

honey bees were introduced in the New World (Roubik & Aluja, 1983). When Apis abun- in the middle 1960´s, and they reached Central dance declined substantially, from 2001 to America in 1985, he compared the coffee 2002, visitation rates dropped about 50% in yields of the period before and after its intro- distant sites, but only 9% in near sites. This duction. After the arrival of Africanized bee in can be explained by the compensating effect Central America, coffee yields in most coun- of native bees, which replaced Apis as the tries of this region increased substantially, most important visitor in nearby sites. So, except for the Caribbean countries (e.g. Haiti), according to the author, forest fragments where native and introduced pollinators were provided nearby coffee with a diversity of absent. In the Old World, where honey bees bees that increased both the amount and sta- were always present, coffee production did bility of pollination services by reducing not varied in the same rate than the New dependence on a single introduced pollinator World. Countries that experienced an inten- (Ricketts, 2004). sive land usage and loss of habitats for pollina- Similar results were found in Brazil (De tors had reduced yields (loss of 20-50%), Marco & Coelho, 2004) and Indonesia (Klein, although they had increased cultivated areas et al., 2003b,c). Coffee (C. arabica) branches (Ivory Coast, Ghana, Kenya, Cameroon, with free access to pollinators produced more Indonesia, El Salvador and Haiti) (Roubik, fruits in farms where there were forest frag- 2002). This work stressed the importance of ments nearby. Coffee production increased native and introduced pollinators for coffee 14.6% when the services of pollinators were yields, although he did not analyze the pollina- available (De Marco & Coelho, 2004). Similarly, tion behaviour itself. C. canephora and C.arabica fruit set increased Ricketts (2004), in experiments per- with the increase of diversity and abundance formed at Costa Rica during 2001-2002, of flower-visiting bees (C. arabica: 90% when showed that eleven eusocial bees (10 native 20 bee species were present and 60% when plus A. mellifera) were the most common vis- only three species were present, Klein, et al., itors of coffee (C. arabica) shrubs, and that 2003b; C. canephora: 95% when 20 or more the distance of the forest fragments to the bee species were present and 70% when only cultivated areas significantly influenced cof- six species were present, Klein, et al., 2003c), fee visiting by these bees. Bee richness, over- and the number of social bees species all visitation rate, and pollen deposition rate decreased with distance to forest fragments were all significantly higher in sites within and the number of solitary bees increased with approximately 100m of forest fragments than light intensity (less shade) and greater quanti- in sites far away (up to 1.6km). Apis mellifera ties of blossoms. Additionally, Klein, et al., foragers accounted for more than 90% of all (2003b,c) found that solitary bees had an visits in distant sites, and where Apis were not important participation in the pollination of C. present, native species as meliponine bees canephora shrubs, leading to higher levels of accounted for most of the visits at near sites. fruit set that originated by members of social This is due to the smaller flight range of bee assemblages. meliponine bees which have a typical flight These services can be translated into eco- range of 100-400m (van Niewestadt & nomic advantages. For example, De Marco & Iraheta, 1996, Heard, 1999), although maxi- Coelho (op.cit.) found, as previously stated, mum observed flights ranged from 1 to 2 km that coffee production increased 14.6% when 80

the services of pollinators were available. This can keep pollinators; to decrease herbicides increase represents an extra income of use in agricultural crops, that helps the forag- US$1860.55 per ha per year. Ricketts, et al., ing supply for pollinators and crop attractive- (2004), showed that pollinating services from ness for them, in larger areas. two small fragments (46 and 111 ha) could be Although the already identified impor- translated into ~US$60,000 per year for one tance of pollinators in agriculture (see also Costa Rica farm. weevils for oil palm; bumble bees for toma- All these results stressed the importance toes, among others; solitary bees for apple, of conserving forest fragments and nesting pears and alfalfa, for instance; stingless bees places for social and solitary bee species (Klein, for strawberry, guarana, assai, coffee, among et al., 2003c, Ricketts, et al., 2004), which can several other crops; honey bees for several act as service-providing units (Luck, et al., crops) is well known, until now their use is not 2003) for coffee pollination. The costs of remarkable in undeveloped countries. maintaining conservation areas are far exceed- However, this situation will change very soon, ed by the economic benefits that the service of because of new initiatives concerning pollina- pollinators brings for agriculture. In this way, tors use in crops (for instance, the Brazilian conserving natural areas nearby coffee farms Pollinators Initiative) as well as from successful can be translated into advantages for biodiver- crops competing in world market, resulting sity and agriculture (Allen-Wardell, et al., 1998, from the pollinators use in greenhouses, for Ricketts, et al., 2004). instance. Developed countries are working with pollinators’ shortage, although only a Stingless bees management practices small number of them (a dozen, according to for use in agriculture Kremen, 2004) are successful bred for agricul- Agricultural intensification worldwide includes tural use. If they are not available nearby due a decline in the proportion of natural habitat, to the intensive agricultural patterns using an increase in pesticide usage, a decrease of large areas, they are bought from biotech floral resource on farm sites, as well as larger companies that breed them successfully. These field sizes, crop monocultures, intensive soil companies are multinational and have the and water usages and the use of synthetic fer- technology of large scale breeding. The intro- tilizers. Of course, the sustainability of agricul- duction of alien pollinators with defined ture following these patterns of land use is breeding techniques is also undesirable, and under concern by 21 Agenda for Agriculture. studies of ecological impact are asked in Best management practices in agriculture importation process. This stimulates the bread- for sustainable use and conservation of polli- ing of native pollinators for the same service in nators are focused in recent literature, and countries with capacity building in pollination mainly by several authors that study pollina- area. In many tropical and subtropical areas of tors’ conservation. This means to carry on pes- the world, a new scenario opens focusing stin- ticides and their use in the crops; gene flow gless bees use as crop pollinators (Macias, et studies; environmental friendly agricultural al., 2001; Cunningham, et al., 2002). An infant practices, including land preparation, in order industry arises with stingless bees breeding in to keep nests of solitary bees that occur in the Australia (Heard & Dollin, 2000) and Brazil soil; agricultural area and maintenance of their (Rosso, et al., 2001), growing in the world borders with native vegetation, or hedges that (Cortopassi-Laurino, et al., 2006). Workshop I 81

Best management practices of pollinators Artificial offering of nests sites in crops mean best crop economic value, and Another possibility of deal with nest sites as in this aspect both issues are together: eco- a limited resource is to establish artificial trap nomic value of pollinators and economic nests, offering nests sites for stingless bees. value of crops. Generally, producers are not Inoue, et al., (1993) did these experiments in interest in resistance (ability to retain commu- order to know more about the population nity properties under disturbance) or resilience dynamics of stingless bees. They studied an (ability to recover from disturbance) of crops area of the Horticultural Experimental when intensifying agriculture, but in their Station in Lubuk Mintrum, in Sumatra, economic value in this season. Short time where the main vegetation was a plantation actions and market simulations are important of tropical fruits, rambutan, N. lappaceum, in the producer’s decisions on what crop to and durian, D. zibethinus (ca 480x200m, 8- use in next season. They are linked to unpre- 6ha), where 24 species of stingless bees were dictable weather conditions, as well to the found. The species Trigona (Tetragonula) market fluctuation on crop values (Kevan & minangkabau was the most common, and Viana, 2003), as well as to the economic suitable for their study. They censused tree advantage in having better fruits. Long-term cavities and possible artificial nesting sites to activities concerning natural resources are estimate the number of natural colonies. At almost not considered. these censuses, 2 persons searched 4 The potential use of stingless bees’ days/month. They also set 362 trap nests in nests in large scale is for using in crop polli- the field, of which 248 were perforated nation. How to get nests in nature and to bamboo stems and 114 wood boxes with breed them successfully is a challenge. glass tops. Trap nests were set in January Another point of consideration in relation to 1981 (100), December 1981/January 1982 the social bees of Brazil is the new law no. (138), December 1982 (75) and October 02000.006608.2000-81. This law pretends 1983 (49). Nests were observed during 56 to protect these insects and has only recently months. The results were: became effective. To protect these social • trap nests were used by many animals, as bees, it mainly prohibits the exploration of social insects (mainly ants) and vertebrates natural nests. Unintentionally, this law makes (geckos, for instance); it harder to access biological material of these • only T. (Tetragonula) minangkabau occupied bees for who needs to do the necessary, legal the trap nests; studies. Above all, the restriction put on by • ants occupied 20% of empty nets; this law makes that the artificial multiplica- • bees occupied 6% of empty nests; tion of colonies is the only option to obtain • colonies were found monthly during all enough colonies to study these bees and, experiment; thereafter, to use them in large scale projects. • successful in nest establishment was also This fact once more demonstrates that recorded. knowledge about the reproductive biology of these bees is indispensable. We need more This experiment showed that additional biological information on nest sites, food nest sites offer could improve the bee density sources for improving colony development, in the area, and that trap nests are suitable colony multiplication, diseases. only for some bee species. 82

Antonini & Martins (2002) used nest traps tion of the queens under laboratory condi- in Cerrado without any result, in an area tions are needed. The minimum population where they found 46 nests of Melipona of bees necessary to begin a new nest, as quadrifasciata. Beekeepers sometimes men- well as their age composition must be eval- tion that this bee species nests in abandoned uated. This bee also produces a honey that nests of Apis mellifera. is considered as medicine, and how to con- In Brazil, recently stingless bee’s keepers serve it should be investigated. At this are using pet bottles as traps nests. In a bee- moment, splitting colonies in two is possi- keeping meeting this year in Rio Grande do ble, but this is not enough to allow their Sul (III Encontro dos Meliponicultores) some of large use as pollinators. them reported that Tetragonisca angustula 2.Melipona quadrifasciata. The queen fer- use these pet bottles. A deeper research on tilization under controlled conditions was this subject is urgent, and is suggested as a done in M. quadrifasciata by Camargo recommendation. (1972), that verified to be possible to put a gyne and a male in a box and they imme- diately copulate. This result opens condi- Recommendations tions for genetic manipulations of colonies. Besides, this bee can provide buzz pol- Key stingless bees species for large scale lination. Nevertheless the same result was breeding in Brazil not obtained with other Melipona species The selection of some stingless bees’ species until now. for large scale breeding is needed. They 3.Melipona subnitida. In Northeast Brazil should be effective as pollinators, easy to (dry regions, Caatinga) this bee species is maintain in strong rational hives that could bred for its honey, very appreciated by local be transported, easy to multiply, with a high people. Until now, their role as pollinator range of temperature and humidity for flight was studied in sweet pepper under green- activity. Species should be selected for greenhouse, with good results (Cruz, et al., 2005) houses pollination as well as for pollination 4.Melipona scutellaris. This species is in open field. already used as a very good honey produc- Due to the large size of Brazilian territory, er in Northeast Brazil, and bred by success- the selection should be regionally determined, fully by beekeepers. Domesticated and well to facilitate breeding and colony trading. In adapted in hives, this is one of the promis- table 1 there are indications of stingless bee ing species to be used as pollinators where species already known as good pollinators. they occur. Our first selection should include: 5.Nannotrigona spp. The use of Nan no- 1.Tetragonisca angustula. This species has a trigona in greenhouses was shown to be wide geographical range in Latin America. effective in pollination. Very common in Very common in several habitats, including urban areas, and with a wide geographical cities, it frequently swarms, accepting artifi- range, must be studied concerning biology cial traps for establishing new nests. More and reproduction. The important results data on queen and males rearing in natural from Cauich, et al., 2004, in Mexico, show- nests, on queen rearing in vitro under labo- ing that they are as effective in tomato pol- ratory conditions, and controlled reproduc- lination as other pollination treatments gives Workshop I 83

to this genus a high importance for addi- 12.Develop metanalysis, data analysis and tional investigation. scientific publication diffusion of pollina- 6. At least 9 species of stingless bees from tors issues. Amazon (Melipona spp., Aparatrigona spp., 14. Improve techniques for nests development Plebeia spp. and Scaptotrigona spp.) could in hives. be kept massively to be used on pollination 15. Evaluate queen survivorship in the colony. programs. Tropical crops as cupuassu (Theo - 16. Compare the characteristics of initial and broma grandiflorum), urucum (Bixa orel- mature nests. lana), assai (Euterpe oleracea), hogplum 17. Study sex-ratio and queen production in (Spondias mombim), guaraná (Paullinia selected species. cupana) are some examples of Amazon 18. Improve honey production, quality and plants witch demands pollination services conservation. from stingless bees. 19. Evaluate pollen availability and quality. 20. Study foragers’ lifetable in different seasons. Improving knowledge base 21. Study seasonal aspects of life cycle, mainly 1. Improve regional stingless bees collections in subtropical environment. and the use of molecular techniques needed to help identification. 2. Automatic monitoring of flight activity for Final remarks modeling in climate change issues. 3. Promote stingless bees’ conservation in Concerning stingless bees’ biology, there is an areas where logging is allowed. urgent need for implement the research 4. Study nest sites; nests populations; nests groups in the different Brazilian regions for sizes and densities. improving the local knowledge basis. Regional 5. Improve nests availability through the groups should be trained in standard method- establishment of ecological corridors. ologies to apply in their region. 6. Establish techniques for ecological restora- Improve capacity building and training in tion and pollinators. all levels, as well as concentrate studies in 7. Identify pollinators assemblages in eco- nests requirements in order to implement the tones and fragments. new law 02000.006608.2000-81 concerning 8. Promote stingless bees conservation in to stingless bees beekeeping. agricultural landscapes, also promoting Conservation of stingless bees in logging heterogeneity in landscapes. areas is an important issue, due to the large 9. Study exotic and native pollinators’ ecolog- Brazilian area that will be used for logging in ical relationships. Amazon region. 10. Study species acceptation in trap nests of Develop life history studies for a selected different materials. number of stingless bees species that are 11. Use molecular tools to evaluate: density of potential generalist pollinators. colonies; males provenience; population- Provide literature in Portuguese and avail- characteristics; relatedness among nests; able on line. number of nearby nests (through the analysis of male clouds near the nest entrance, or by analyzing workers collected in a transect). 84

Table 1: Stingless bees used as crop pollinators

Crop Stingless Bee Results Author Pollinator (s)

Averrhoa carambola In Malaysia, Trigona Efficient pollinator after Phoon et al,1984 (Oxalidaceae) thoracica; one visit carambola

Bixa orellana Melipona melanoventer Buzz pollinated by Maués & Venturieri, (Bixaceae) and Melipona stingless bees 1995; Wille, annatto fuliginosa; Melipona 1976;Absy & Kerr, seminigra merrilae 1997

Capsicum annuum Trigona carbonaria in M. subnitida increased (Solanaceae) Australia; Melipona fruit weight (by 29%) and Cruz et al, 2005; Silva suit pepper subnitida the number of seed per et al, 2005 fruit (86%); 65% decrease of deformed fruit

Cocos nucifera Apis mellifera and stingless Stingless bees are the Hedström, 1988; (Arecaceae) bees contribute to the dominant visitors in Engel and Dingemans- Coconut pollination of this crop Costa Rica Bakels, 1980

Coffea arabica var. Melipona spp. Nogueira-Neto et al Bourbon (Rubiaceae) 1959

Coffea arabica Bee pollination Higher fruit set and Roubik 2002 (Rubiaceae) heavier mature fruits

Coffea canephora Bee biodiversity Coffee fruit set was Klein et al, 2003a (Rubiaceae) higher in areas with high bee biodiversity (from 70 to 95%)

Coffea canephora Trigona (Lepidotrigona) 84% fruit set Klein et al, 2003b terminate

Cucumis sativus Partamona bilineata Frequent visitor Meléndez et al., 2002 (Cucurbitaceae)

Cucumis sativus Scaptotrigona aff. depilis Higher fruit production, Santos et al, 2004 (Cucurbitaceae) higher fruit weight and higher % of perfect fruits

Euterpe oleraceae – Melipona melanoventer, In development G. C. Venturieri et al, (Arecaceae) Melipona flavolineata and 2005 “assaí” Melipona fasciculata (Meliponinae, Apidae)

Fragaria x ananassa Tetragonisca angustula "Oso Grande" cultivar Malagodi-Braga & (Rosaceae) (Meliponini, Apidae) 100% primary flowers Kleinert, 2004 strawberry developed; higher fruit fresh weight Workshop I 85

Fragaria x ananassa Tetragonisca angustula Sweet Charlie Cultivar Malagodi-Braga & (Rosaceae) (Meliponini, Apidae) Misshapen fruit reduced Kleinert, 2004 strawberry by 86%

Lycopersicum Nannotrigona As effective as mechanical Macias & Macias, esculentum pirilampoides vibration in terms of fruit 2001; Cauich et al, (Solanaceae) set, fruit weight and 2004 tomato number of seeds per fruit

Lycopersicum Melipona quadrifasciata Tomato flowers in Del Sarto et al, 2005 esculentum absence of vibration do (Solanaceae) not produce fruits

Macadamia integrifolia Trigona carbonaria Yields and fruit quality Heard, TA; 1987 (Proteaceae) (in Australia) benefit from bee Macadamia nut pollination

Mangifera indica Stingless bees are the Important for cross Simão & Maranhão, (Anacardiaceae) more common visitors; pollination, Trigona bees 1959 mango Tetragonisca angustula in move from tree to tree. Chiapas

Myrciaria dubia Melipona sp and Peters & Vasquez, (Myrtaceae) Scaptotrigona postica 1986 camu-camu

Nephelium lappaceum Scaptotrigona mexicana Caged and open Rabanales et al, in (Sapindaceae) and Tetragonisca pollination treatments press rambutam angustula yielded a mean of 9.1 times the mature fruit of flowers from which bees were excluded

Persea americana 8 species of stingless bees Efficient as pollinators Ish-am et al., 1999 (Lauraceae) avocado

Persea americana Trigona nigra; N. Potential efficient Can-Alonso et al, (Lauraceae) pirilampoides pollinators 2005

Psidium guajava Pollen found in Melipona Studies under Kleinert –Giovannini & (Myrtaceae) marginata,T. spinipes and development I-Fonseca, 1987 guava M. quadrifasciata pots Castro, p.c. Frieseomelitta spp.

Psidium guajava M. subnitida together with solitary Alves & Freitas, 2005 (Myrtaceae) bees, are efficient guava pollinators

Salvia farinaceae T. angustula and N. Produce good quality Slaa et al, 2000 (Labiatae) pirilampoides seeds in greenhouses

Salvia splendens Geotrigona spp. and Bustamante 1998 Partamona 86

Sechium edule 28 stingless bees species Stingless bees enhance Wille et al. 1983 (Cucurbitaceae) are important visitors; T. fruit production chayote, choko corvina and Partamona cupira are important

Spondias tuberosa Frieseomelitta languida In development M. S. Castro (Anacardiaceae) and T. angustula “umbu” or “imbu”

Theobroma Plebeia minima and small Venturieri, GA et al, grandiflorum weevils. Most plantas are 1993 (Sterculiaceae) self incompatible; cupuassu Ptilotrigona lurida may be a pollinator

Theobroma Plebeia spp., Paratrigona In development (Probio) R. Gribel grandiflorum spp. & Frieseomelitta spp. (Sterculiaceae) (Meliponini, Apidae) “cupuassu”

Paullinia cupana Melipona spp together with Apis Aguilera, FJP, 1983 (Sapindaceae) guarana mellifera

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 Bemisia argentifolii (Hemiptera, Aleyrodidae), para as abelhas sem ferrão do gênero Scaptotrigona (Hymenoptera, Apoidea). Monografia de conclusão de curso. Universidade Estadual 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) in Subtropical 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 remnants influence 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 stingless bee 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 nest density 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 forest 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, São Paulo - 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 Agricultural Research, 55 n.7: 771-773.

MORAES, S. S., BAUTISTA, AR.L. & VIANA, B. F. 2000. Avaliação da toxicidade aguda (DL50 e CL50) 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 de Angola, 9 n. 7: 9-31.

RAMALHO, M., KLEINERT-GIOVANNINI, A. & IMPERATRIZ-FONSECA, V.L. 1990. Important bee plants for stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical 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 tropical forest 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 the Brazilian Pollinator Initiative- BPI- based on WebBee. In: Annals of the 8th IBRA International Conference on Tropical Beekeeping and VI Encontro sobre Abelhas, Ribeirão Preto, São Paulo – SP, Brazil, in CDROM.

SAMEJIMA, H., MARZUKI, M., NAGAMITSU, T. & NAKASIZUKA, T. 2004. The effects of human disturbance on a stingless bee community in a tropical rainforest. Biological Conservation, 120: 577-587/j.biolcon.2004.03.30. 88

SILVA, G.F., VENTURIERI, G.C. & SILVA, E.S.A. 2004. Meliponiculture as a sustainable development alternative: financial management within family groups in northeast Amazon, Brazil. In: FAO report, 12p.

VENTURIERI, G.C. 2003. Meliponicultura I: Criação de Abelhas Indígenas Sem Ferrão, Caixa Racional para Criação. Rec. Téc, Embrapa Amazônia Oriental, Belém – PA, Brazil.

VENTURIERI, G.C. 2004. Forest exploitation and its impact on the Amazonian stingless bees. In FAO report, Best management practices in Agriculture for sustainable use and conservation of pollinators.

VENTURIERI, G.C., RAIOL, V.F.O. & PEREIRA, C.A.B. 2003. Avaliação da introdução da criação racional 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 Information Technology (IT): building synergism and cooperation Workshop II 91

Abstract Workshop objectives

The São Paulo Declaration on Pollinators plus The purpose of this workshop was to discuss 5 Forum was organized by the Brazilian the role of Information Technologies (IT) for Pollinators Initiative, BPI, and held in São the development and for the effectiveness of Paulo with the support of FAO to discuss stan- the Pollinators Initiatives in a broad sense, dardized methodologies for assessing pollina- from building a species catalog to providing tor’ status and management practices to stop knowledge for policy making. their decline. The program included reviews of relevant The main objectives of the IPI (Inter- activities and broader trends in biodiversity infor- national Pollinators Initiatives, in which BPI matics, and their impact for Pollinators Initiatives. take part) are: Efforts, from local to global, were present- • monitor pollinator decline, its causes and its ed and their relationships and contributions to impact on pollinator services; the larger goals were discussed, as well as the • address the lack of taxonomic information possibilities of networking and of sharing on pollinators; tools, systems and data. Funding opportunities • assess the economic value of pollination and was another important topic discussed. the economic impact of the decline of pollination services; • promote the conservation, the restora- Organization and content tion and sustainable use of pollinator diversity in agriculture as well as in relat- Organizing Committee ed ecosystems; Antonio Mauro Saraiva, Escola Politécnica, Universidade de São Paulo. Those tasks demand a huge effort, Vanderlei Perez Canhos, Centro de Referên - including a lot of data acquisition (in the cia em Informação Ambiental - CRIA. field and in laboratory), and data analysis Vera Lucia Imperatriz Fonseca, Instituto de for building knowledge on pollinators and Biociências, Universidade de São Paulo. pollination. Many of those tasks can benefit from the The workshop was held in 31st. October 2003, use of a variety of Information Technology (IT) at Escola Politécnica da Universidade de São Pau- tools that can help the scientist, the policy lo. It was organized as a series of presentations maker, the extensionist, the student. of local, regional and global initiatives and proj- Taking advantage of the presence of a ects followed by discussion on broader issues. very distinguished audience at the Forum, this workshop was proposed to discuss and The local (Brazilian) initiatives presented: disseminate the importance of IT for the • WebBee – The WebBee project, an infor- Pollinator Initiatives, to help promote partner- mation network on bee diversity was pre- ships and exchange experiences on the devel- sented by prof. Antonio Mauro Saraiva, opment and use of those technologies, and from Escola Politécnica - USP, Agricultural to discuss funding opportunities. Automation Laboratory, Brazil. This event was designed as an extension • Brazilian Pollinators Initiative - BPI – was of the Forum, open to all of its participants. presented by Bráulio Dias, from the Brazilian 92

Ministry of the Environment (MMA), Brazil. the United Nations Food and Agriculture • Pollinators e-Journal – The proposal of an Organization (FAO). electronic journal on pollinator biology was presented by prof. David de Jong, from Genetics Department, Faculdade de Me dicina, Discussion Universidade de São Paulo – FMRP-USP, Brazil. • speciesLink - The speciesLink project, that The topics suggested for discussion were: integrates many biological collections was • towards a common agenda - building the presented by prof. Vanderlei Peres Canhos, shared infrastructure; from Reference Center of Environmental • how to integrate actions; Information - CRIA, Brazil • standards, protocols and systems interop- . erability; The regional initiatives presented: • on-line directory of institutions, experts, pro- • the International Centre for Integrated grams and projects; Mountain Development (ICIMOD), was • on-line databases: taxonomic authority files, presented by Dr. Uma Partap and Dr. Farooq specimen DB, species DB, phenological Ahmad, from ICIMOD, Nepal . datasets for meta-analysis; • the North American Pollinators Initiative • computational tools for data mining, analy- (NAPI), was presented by Dr. Mike Ruggiero, sis, synthesis and visualization; from the International Taxonomy Informa tion • funding opportunities and co-financing re- Service (ITIS) and the National Museum of quirements - GEF projects and local Funding; Natural History, Smithsonian Institution, USA. • recommendations. • the European Pollinators Initiative (EPI), was presented by Dr. Simon Potts, from the Centre for Agri-Environmental Research, Expected Results Reading University, UK. • the International Network for Expertise Expected results of the workshop included: in Sustainable Pollination (INESP), was • a clearer understanding of the role of IT in presented by prof. Peter Kevan, from the Pollinator Initiatives; University of Guelph, Canada. • the establishment of partnerships for the • the African Pollinators Initiative (API), was development and sharing of the IT infrastruc- presented by Dr. Barbara Gemmil, from ture required for the Pollinator Initiatives: tools Environment Liaison Center International and systems developers and data providers; (ELCI) (Kenya) and Dr. Connal Eardley, from • the identification of funding opportunities Agricultural Research Council, Plant Protec - for the development of the IT infrastructure tion Research Institute, South Africa. on a local, regional and global scale. • the IABIN Pollinators Network and the New World Bee Catalog were presented by prof. Vanderlei Peres Canhos, from CRIA, Brazil. Introduction

The Global Initiative presented: As was pointed out by Saraiva & Imperatriz- • the International Pollinators Initiative Fonseca (2004), Information Technology (IT) (IPI), was presented by Linda Collette from has a decisive role to play on the development Workshop II 93

of the Pollinators Initiatives (PIs), and that can ter data with less effort, while allowing them be analyzed based on the core objectives of to concentrate on the design of field experi- both the International Pollinators Initiative (IPI). ments, on data analysis, i.e., on turning data into information and knowledge. These core objectives are: As for the taxonomic information, on one • monitor pollinator decline, its causes and its hand the information gathered after decades impact on pollinator services; and maybe centuries of research is not readily • address the lack of taxonomic information available even for the scientific community on pollinators; because it is spread around the world in muse- • assess the economic value of pollination and um collections or the like. Digitizing the collec- the economic impact of the decline of polli- tions and publishing them on the Internet will nation services; increase the accessibility while still providing • promote the conservation, the restoration control over the data whenever this is and sustainable use of pollinator diversity in required. On the other hand, IT tools can be agriculture as well as in related ecosystems. used to help automate species identification, be it with instrumentation systems or with It is not difficult to see that one way or identification keys whose rules can be embed- another those objectives involve issues related ded in computer programs. to data, information and knowledge: their Once data is acquired, different types of acquisition and analysis, their transformation analysis need to be made taking into account from raw data to useful knowledge, their use the species distribution, the effect of changes for sound decision and policy making, their on the environment, the economic value and dissemination for wider audiences to increase impact, and different strategies for conserva- awareness and education. tion, restoration and use. These analyses Those are typical tasks for Information would benefit from the use of simulation tools Technology in a broad sense and, more specif- that can be used to develop different scenarios ically speaking, those are simply the goals of upon which decisions can be made. Biodiversity Informatics, a new discipline or One of the most important points stressed denomination created to deal with the appli- in the PIs is increasing awareness raising: it is cation of IT to Biodiversity. urgent to demonstrate the importance of polli- The complexity of biodiversity and its nators and the risk of their decline. The internet processes, the huge figures involved, the can play a very important role on that. However, amount of variables and data that are to be the web can also have a strategic function for dealt with, the regional and global coverage the integration of the research community, that is usually necessary, all demands IT tools to which can share data, communicate and coop- acquire data, to store and manipulate them, to erate more efficiently, even though remotely. help analyze them, and to convey the results and findings in different formats and media to Results different target audiences. It is not different in the case of the PIs. The presentations made at the workshop Monitoring pollinator decline demands more (which are available at WebBee portal) accurate and automated methods and tools showed a wide range of uses, systems and that will help researchers collect more and bet- future possibilities for IT applied to the PIs. 94

They unanimously stressed the advantages as the Catalogue of Life, from Species 2000 and and importance of the use of IT tools and tech- ITIS ), and for creating checklists of species and niques to help achieve the goals of the resolving naming problems. Further use of inte- International Pollinators Initiative and of the grated data is made by analysis software, such national/regional PIs. The project Conservation as that for modeling species distribution, extinc- and Management of Pollinators for Sustainable tion risk, and protection strategies. Analyses Agriculture Through an Ecosystem Approach, tools are of utmost importance as they can be under the auspices of FAO and GEF, will require used to guide the development of environmen- an intensive use of IT on the development of its tal public policies on a more solid foundation. four components. The preliminary phase of the This integration requires the use of stan- project, the PDF-B phase, will provide an dards and protocols for data exchange. These opportunity to review, identify and analyze standards are under development with the gaps on the technology regarding its applica- support of institutions such as GBIF, TDWG, tion to the PIs. The full-size project that will among others, with the participation of subsequently be developed may accommodate groups from many countries. This is another part of that development. area that needs more support, as it is essential According to what was presented, soft- to allow more seamless access to and share of ware tools seem to be the most widely used biological data. It was suggested that FAO and components. Websites for various purposes GEF should participate of that effort. An exam- were reported for all PIs though their content ple of the use of those standards to integrate and complexity differed significantly. In some different sources via internet was presented at cases, simple webpages are used to convey the SpeciesLink project . project information, educational information, As the use of such information increases etc. Despite that simplicity, their effectiveness in its complexity, more tools are necessary to is acknowledged and they fulfill some basic allow automation of many of the boring and needs of the developers and users. repetitive tasks. At a higher level, there are the databases An important part of the remote access to that can be accessed via Internet. Specimen data is related to bibliography. An on–line peer- information from biological collections at reviewed journal on pollinators and pollination museums, for instance, is being digitized and is is being designed within the BPI, and it was increasingly available on-line. Though the per- suggested that this journal should be support- centage of the specimens of the known world’s ed within the FAO/GEF project. Such a journal collections that is already available on-line is would both facilitate information exchange small, that number is increasing consistently and encourage research and publications on and some international and global efforts in pollinators, especially in the developing coun- that direction were mentioned. It was stressed tries. Much research on pollinators and pollina- the need to join and to strengthen that digiti- tion in developing has been traditionally done zation effort, which faces many difficulties in a haphazard manner, and often the results related to funding and data ownership. are not readily accessible. A specific journal on This brings up the problem of the integra- pollinators would both provide means to guide tion of all that data. Such integration is impor- and improve such research, through examples tant for many different purposes, such as for and through peer review, and would also facil- building a global catalogue of life on Earth (such itate publication of such information. Workshop II 95

It is important that other media, such as requires people and this is sometimes forgot- images and videos, be used to convey infor- ten, and often hard to obtain funding. mation via internet. They must be comple- Considering the end-users that are expect- mented by texts but they have a strong impact ed to benefit from those systems another point and should be incorporated especially for spe- that was discussed was the access to internet in cific audiences and for some purposes. An rural areas, especially in developing countries. example of an information system that is That should be considered in the technical based on species information (rather than on design of the systems and on other actions at specimen information) and which makes the level of public policies for digital inclusion. intensive use of visual information was pre- Another topic is related to the question of sented on the project WebBee. data ownership and sharing by researchers Another set of IT tools not very much and countries. That question is sometimes del- mentioned was instrumentation, though it icate, both at the personal level and at the became clear that it is fundamental for country level, since national legislation differ increasing the capacity of data acquisition and and sometimes restrict the access to biological the quality of this data. It is also important for data fearing biopiracy. allowing the application and the replication of the standard methodologies discussed at the other workshops of the Forum. Part of the Final remarks WebBee project involves the development and use of a set of instruments applied to pollina- The workshop provided a very good opportu- tors monitoring. Those experiments can be nity to show to the audience a wide range of accessed via internet and can be shared cases, tools, systems and initiatives regarding among many users collaboratively. the application of IT to pollinators and pollination and related areas. For a significant part of the audience some of the topics covered pre- Difficulties and sented novelties. The presence of a public with recommendations many end-users was important to help collect their feelings and experiences with respect to Along with the discussions that arose during the technology. It also allowed a discussion the workshop sessions one important point that about some critical issues, technical and politi- stood out was the need for IT support person- cal, that must be dealt with so that IT can be nel. Most institutions that were present at the effective for the Pollinators Initiatives; and pro- workshop do not have IT support personnel or moted opportunities for strengthening con- at least not at level required nowadays, consid- tacts and relationships, for showing areas of ering systems development and infrastructure. interest and competencies that may evolve to Another issue related to support is the future cooperation, which is a central part of maintenance of such systems. Many of them the IPI and of the GEF/FAO project. are developed with funds from research proj- The workshop achieved its expected ects but it is often hard obtain funding for sus- results and, being the first of its kind, showed taining them on the long term. The same the importance of further discussion and applies to the issue of updating the system meetings to increase the use of IT for the with new information and data: that task advancement 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 the Brazilian Pollinators Initiative – BPI. In: 8th.IBRA International Conference on Tropical Bees and VI Encontro sobre Abelhas, 2004, Ribeirão Preto, Brazil. Proceedings. International Bee Research Association – IBRA; FFCLRP-USP, 2004. CDROM. ILLUSTRATIONS AND PHOTOGRAPHS Xylocopa bee pollinating a Lecythis pisonis flower. Copyright Michael Rothman 1999. Courtesy of the New York Botanical Garden, Institute of Systematic Botany

Solitary bees are specialized pollinators. Centris is important for cashew pollination. Above left, nests of Epicharis Dejeanii; above right, nest of Ptilothrix plumata; below left, nest of Centris tarsata. Solitary bees can be attracted to trap nests (below right), and moved to crops for pollination purposes. From Schlindwein, et al., 2003, A quantitative approach to assess specialized bee plant pollinator systems, in http:// www.webbee.org acessed in March 10th 2006. Biotic pollination dependence in melon farming: malformed (left) and export quality (right). Photos by Raimundo Maciel de Souza. Africanized honey bees are important pollinators. Above, orange flower. Photo by Tom Wenseleers. Africanized honey bee visiting assai flower. Photo by Giorgio Venturieri. Above left, assai is the second most important crop for Amazonian. Below, male and female flowers of assai need bees as pollinators. 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 angustula visiting strawberry flower. Photo by Katia Malagodi-Braga. Tetragonisca angustula nest entrance. Photo by Tom Wenseleers. Vertical hive with special ventilation system for stingless bees of tropical areas (from Giorgio C. Venturieri in www.cpatu.embrapa.br/paginas/meliponicultura.htm) Embrapa provides field training is stingless bees breeding for Kumenê indians from Indigenous land Uacá, Oiapoque, Amapá state. Giorgio C. Venturieri teaches how to transfer a natural nest to a hive. Photo by Marcos Sztutman.