Pot-Pollen in Stingless Bee Melittology (eBook)

Professor Patricia Vit, MSc PhDUniversidad de Los AndesFaculty of Pharmacy and BioanalysisFood Science DepartmentMérida, VenezuelaThe Sydney UniversityCancer Research GroupDiscipline of Biomedical ScienceSydney, AustraliaDr. Silvia R.M. PedroUniversidade de São PauloSchool of Philosophy, Sciences and LiteratureBiology DepartmentBrasilDr. David W. RoubikSmithsonian Tropical Research InstituteTerrestrial Biology DivisionEntomology DepartmentPanama

Dedication 5
Foreword 6
Foreword 7
Acknowledgments 8
Introduction 19
Contents 9
Contributors 13
Part I: Pollen and the Evolution of Mutualism 21
1: Pot-Pollen as a Discipline: What Does It Include? 22
1.1 Pot-Pollen and Palynology from an Ecological Point of View 22
1.2 A Modern Synthesis of Bee Pollen and Pot-Pollen Study 22
1.3 Plant Reproduction 24
1.4 Pollination 24
1.5 Pollen Biology and Palynology 25
1.6 Applied Pollen Taxonomy 27
Appendix 30
References 32
2: Are Stingless Bees a Broadly Polylectic Group? An Empirical Study of the Adjustments Required for an Improved Assessment of Pollen Diet in Bees 35
2.1 Introduction 35
2.2 Pollen Specialization Categories in Bees 36
2.3 Pollen Analysis of Samples 37
2.4 Adjustment Calculations to Assess Pollen Specialization Categories in Stingless Bees 38
2.4.1 Modifying the Number of Foraged Resource Items: Threshold Values and Pollen Type Versus Pollen Species 38
2.4.2 Modifying the Number of Available Resources: Spatial and Temporal Adjustments 38
2.5 The Importance of an Appropriate Assessment of Pollen Specialization in Bees: Factors Causing Low Number of Foraged Items 43
2.5.1 Abundant Versus Minor Pollen Types 43
2.5.2 Recruitment Behavior 43
2.5.3 Intra-nest Pollen Analysis 44
2.6 Factors Causing High Number of Available Items 44
2.7 Polylecty, Broad Polylecty, or Simply Degrees of Polylecty? 44
References 45
3: Pollen Collected by Stingless Bees: A Contribution to Understanding Amazonian Biodiversity 47
3.1 Introduction 47
3.1.1 Origin and Evolution of Plant-­Bee Interactions 47
3.2 The Use of Pollen Analysis in the Study of Bees in the Amazon Rainforest 48
3.3 Diversity of Plants, Stingless Bees, and Their Interactions in Central Amazon 49
3.4 Amazonian Bee Diet, Biology, and Suggested Interactions Potentially Leading to Pollination 56
3.5 How to Improve Meliponiculture for  Sustainable Development in the Amazon 59
3.6 Conclusions 61
References 61
4: The Stingless Honey Bees (Apidae, Apinae: Meliponini) in Panama and Pollination Ecology from Pollen Analysis 65
4.1 An Introduction to the  Stingless Honey bees and  Pot-Pollen, in Panama 65
4.2 Pollen Niche, Relative Specialization, and Pollen Spectrum 67
4.2.1 Qualitative and Quantitative Analyses 67
4.2.2 Field Bee Short-Term Resource Selection 79
4.2.3 Pollen of Popular Meliponines, Africanized Honey bees, and Lesser Known Species 80
4.2.4 Pollination Ecology and Population Biology 80
4.2.5 Conclusions and Ecological Perspective 81
References 82
5: The Value of Plants for the Mayan Stingless Honey Bee Melipona beecheii (Apidae: Meliponini): A Pollen-Based Study in the Yucatán Peninsula, Mexico 85
5.1 Understanding the Ecology of a Mayan Resource and Cultural Icon 85
5.2 Baseline Studies of Invasive Honey bees and Native Neotropical Bees 86
5.3 Fieldwork 86
5.4 Pollen Analysis from  Pot-­Pollen Samples 87
5.5 Understanding Bee Resource Use in Dynamic Natural Environments 88
References 93
6: Melittopalynological Studies of Stingless Bees from the East Coast of Peninsular Malaysia 95
6.1 Introduction 95
6.2 Pollen Collection by Heterotrigona itama in Tropical Island of Taman Tropika Kenyir, Terengganu 96
6.3 Pollen Collection and Abundance Among Colonies of Lepidotrigona terminata from a Meliponary in Besut, Terengganu 100
6.4 Selected Flowers Producing Pollen Preferred by Stingless Bees in Terengganu 102
6.5 Conclusions 102
References 105
7: The Contribution of Palynological Surveys to Stingless Bee Conservation: A Case Study with Melipona subnitida 107
7.1 Introduction 107
7.2 Floral Resources Dynamics: Pot-Pollen Versus Pollen from the Bees’ Body 108
7.3 Melittopalynology as Tool for Restoration Strategies: Suitable Foraging Habitats 113
7.4 Concluding Remarks and Future Steps 114
References 116
8: Pollen Storage by Melipona quadrifasciata anthidioides in a Protected Urban Atlantic Forest Area of Rio de Janeiro, Brazil 120
8.1 Introduction 120
8.2 Getting Pollen Loads and Pollen Grains by  M. quadrifasciata anthidioides 121
8.3 Palynological Characteristics of Pollen Batches Collected from the Baskets of  M. quadrifasciata anthidioides 122
8.3.1 Monofloral Pollen Loads 122
8.3.2 Bifloral Pollen Loads 123
8.3.3 Heterofloral Pollen Loads 123
8.3.4 Additional Pollen Types 124
8.3.5 Additional Structured Elements 124
8.4 Plant Families, Genera, and Species Mostly Visited by M. quadrifasciata anthidioides 124
8.5 Conclusion 125
References 126
9: Angiosperm Resources for Stingless Bees (Apidae, Meliponini): A Pot-Pollen Melittopalynological Study in the Gulf of Mexico 127
9.1 Introduction 127
9.2 Background of Melittopalynological Studies in Mexico 128
9.3 Methods and Study Areas 129
9.4 Floral Resources Recorded in Pot-Pollen Samples of Melipona beecheii from Campeche 130
9.5 Meliponiculture and Melittopalynological Study of Pot-Pollen in Veracruz 131
9.5.1 INANA’s Sustainable Meliponiculture 131
9.5.2 Angiosperm Resources for Plebeia and Scaptotrigona Mexicana in Veracruz 132
9.6 Analysis of the Polliniferous Plant Preferences of Stingless Bees in Campeche and Veracruz, Gulf of Mexico 133
9.7 Angiosperms Recorded in Systematic Mexican Pot-Pollen Melittopalynological Studies of Stingless Bees 136
9.8 General Considerations 137
References 143
10: Annual Foraging Patterns of the Maya Bee Melipona beecheii (Bennett, 1831) in Quintana Roo, Mexico 147
10.1 Introduction 147
10.2 A Case Study 148
10.2.1 Field Observations: Registering Bee Activity 148
10.2.2 Foraging Activity to Collect Pollen and Nectar 149
10.2.3 Stored Pot-Honey and  Pot-­Pollen Reserves 150
10.2.4 Offspring 151
10.3 Correlations Between  the Studied Factors 151
References 152
11: Crop Pollination by Stingless Bees 155
11.1 Introduction 155
11.2 Characteristics of Stingless Bees as Pollinators 156
11.3 Field Crop Pollination by Stingless Bees 157
11.4 Greenhouse Crop Pollination by Stingless Bees 160
11.5 Stingless Bee Management Under Greenhouse Conditions 161
11.6 Perspectives 164
References 165
12: Stingless Bees as Potential Pollinators in Agroecosystems in Argentina: Inferences from  Pot-Pollen Studies in Natural Environments 170
12.1 Introduction 170
12.2 Potential Pollination by Stingless Bees in Argentina: Intrinsic and Extrinsic Factors 171
12.2.1 Advantages and  Disadvantages of a  Reduced to Moderate Flight Range in Stingless Bees 172
12.2.2 Pollination Using Ground-­Nesting Stingless Bees 173
12.3 Pollen Spectra of Pot-Pollen in Colonies of Stingless Bees from Natural Environments 173
12.4 Crops Potentially Pollinated by Stingless Bees in Argentina 173
12.5 Spatial Variation of Crops in Argentina 180
12.6 Temporal Variation of Flower Availability in Agroecosystems 180
12.7 Crop and Non-crop Flowerings Present in Agroecosystems Beneficial for the Maintenance of Permanent Stingless Bee Colonies 182
12.7.1 Pollinating the Target Crop 182
12.7.2 Weeds and Edge Vegetation as Complementary Flowerings for Permanent Stingless Bee Colonies 182
12.7.3 Diversified Agroecosystems as Best Habitat for Stingless Bee Pollination and Colony Management 182
12.8 Case Study: Pollination of Strawberries with Plebeia catamarcensis (Holmberg) in Santa Fe, Central Argentina 183
12.8.1 Strawberry Cultivation in Argentina 183
12.8.2 The Strawberry in Santa Fe 183
12.8.3 Meliponini: Potential Pollinators in Santa Fe Strawberry Crops 184
References 186
Part II: Biodiversity, Behavior and Microorganisms of the Stingless Bees (Meliponini) 191
13: Stingless Bees (Hymenoptera, Apoidea, Meliponini) from Gabon 192
13.1 Introduction 192
13.2 Taxonomy and  Morphological Diversity of  Stingless Bees in Gabon 194
13.3 Distribution of Stingless Bee Fauna in Gabon 195
13.4 Biology, Ecology and Nesting Behaviour of the  Stingless Bees 197
13.5 Knowledge and Traditional Use of Stingless Bees in Gabon 199
13.6 Conclusion 199
References 200
14: 100 Species of Meliponines (Apidae: Meliponini) in a Parcel of Western Amazonian Forest at Yasuní Biosphere Reserve, Ecuador 202
14.1 Introduction 202
14.1.1 Yasuní Forest and Melittological Background 202
14.2 Discovering Meliponine Biodiversity 204
14.3 Species Accounts and Frequency 206
14.4 Insights from Comparative Morphology and Other Rich Amazonian Areas 212
14.5 Bioprospecting for Pollination Knowledge and Sustainable Exploitation 215
References 217
15: Diversity of Stingless Bees in Ecuador, Pot-Pollen Standards, and Meliponiculture Fostering a Living Museum Meliponini of the World 220
15.1 Introduction 220
15.2 Megabiodiversity of Stingless Bees in Ecuador 221
15.3 A Revised Ecuadorian Honey Norm and Approach to Pot-­Pollen Standards 221
15.4 Stingless Bee Keepers are Crucial for the Heritage and Conservation Mission 230
15.5 A Stingless Bee Window to Look at Climate Warming 235
15.6 Why a Living Museum to Embrace Meliponini of the World? 236
15.7 Conclusions 237
References 238
16: Nesting Ecology of Stingless Bees in Africa 241
16.1 Introduction 241
16.2 Meliponine Origin, Dispersal, and Richness 242
16.3 Stingless Bee Species in Africa 244
16.4 Stingless Bee Nest Architecture 247
16.5 African Stingless Bee Nesting Behavior 248
References 250
17: On the Trophic Niche of Bees in Cerrado Areas of Brazil and Yeasts in Their Stored Pollen 253
17.1 Introduction 253
17.2 Pollen Harvested by Native Bees of the Cerrado 255
17.3 Yeast in Stored Pollen: Diversity and Ecological Role 259
References 262
18: A Review of the Artificial Diets Used as Pot-Pollen Substitutes 265
18.1 Introduction 265
18.1.1 Aim of the Chapter 265
18.1.2 How Do Stingless Bees Harvest and Store Their Food? 266
18.2 The Fermentation Process in  Stingless Bee Storage Pots 266
18.2.1 General Characteristics of Pollen Fermentation 266
18.2.2 Microbial Fermentation and Nutritional Enhancement of Pollen 268
18.2.3 Impacts of Exogenous Compounds in Pollen 268
18.3 Microorganisms Present in Pot-Pollen 269
18.3.1 Generalities of Host-­Associated Microorganisms 269
18.3.2 Bacteria 269
18.3.3 Yeasts 270
18.3.4 Filamentous Fungi 270
18.4 Development of Artificial Diets 270
References 272
19: Yeast and Bacterial Composition in Pot-Pollen Recovered from Meliponini in Colombia: Prospects for a Promising Biological Resource 275
19.1 Introduction 275
19.2 General Properties of Corbicular Bee-Derived Pollen 276
19.3 The Key Bacterial Assemblages Known to Be Associated with Bees and Pollen 277
19.4 Yeast Communities Present in Pollen Collected by Colombian Bees 285
19.5 Final Remarks 289
References 289
Part III: Stingless Bees in Culture and Traditions 292
20: Cultural, Psychological, and Organoleptic Factors Related to the Use of Stingless Bees by Rural Residents of Northern Misiones, Argentina 293
20.1 Introduction 293
20.2 Southernmost Atlantic Forest Ecoregion 294
20.3 Ethnobiological Fieldwork 295
20.4 Cultural, Psychological, and Organoleptic Factors 296
20.4.1 Cultural Factors 297
20.4.2 Psychological Factors 297
20.4.3 Organoleptic Factors 298
20.5 Context of Exploitation of Stingless Bees 299
20.6 Cultural and Psychological Factors Related to the Use of Stingless Bees 302
20.7 Relationship Between  Pot-­Honey, Pot-Pollen, and Cultural, Psychological Factors 303
20.8 Conclusions and Future Challenges 304
References 306
21: The Maya Universe in a Pollen Pot: Native Stingless Bees in  Pre-Columbian Maya Art 308
21.1 Introduction 308
21.2 Maya Bee Myths 309
21.3 Small Format Modeled Sculptures 309
21.3.1 Small Clay Bee 310
21.3.2 Ceramic Beehive 310
21.3.3 Censers 311
21.4 Bees and Stingless Beekeeping in a Sacred Maya Book 312
21.4.1 Melipona beecheii in the  Tro-­Cortesianus Codex 313
21.4.2 Hobon 314
21.5 A World View of Humankind Through a Bee Model as Told by a H-men, a Traditional Maya Priest 315
21.6 The Maya Universe in a Pollen Pot 315
21.6.1 Once upon a Time, Long, Long Ago, There Were Bees… 315
21.7 The Flower Dust 316
References 317
Part IV: Chemical Composition, Bioactivity and Biodiversity of Pot-Pollen 319
22: Nutritional Composition of  Pot-Pollen from Four Species of Stingless Bees (Meliponini) in Southeast Asia 320
22.1 Introduction 320
22.2 Shape and Volume of Stingless Bee Pollen Pots 321
22.3 Nutritional Composition 323
22.3.1 Macronutrients of Pot-Pollen 323
22.3.2 Mineral Analysis 325
22.3.3 Fatty Acid Analysis 325
22.3.4 Amino Acid Analysis 326
22.4 Botanical Origin 327
22.5 Conclusions, Suggestion, and Future Research 329
References 330
23: Characterization of Scaptotrigona mexicana Pot-Pollen from Veracruz, Mexico 332
23.1 Introduction 332
23.2 Traditional Values of Scaptotrigona mexicana Meliponiculture in Mexico 335
23.3 Importance of Pot-Pollen in Meliponiculture 336
23.4 Palynological Analyses of Scaptotrigona mexicana Pot-Pollen from Central Veracruz, Mexico 337
23.5 Chemical Parameters of Scaptotrigona mexicana Pot-Pollen from Veracruz, Mexico 339
23.6 Elemental Composition of Scaptotrigona mexicana Pot-Pollen from Central Veracruz, Mexico 341
23.7 Conclusions and Perspectives on Scaptotrigona mexicana Pot-Pollen in Mexico 341
References 342
24: Chemical Characterization and Bioactivity of Tetragonisca angustula Pot-Pollen from Mérida, Venezuela 345
24.1 Introduction 345
24.2 Proximal Analysis of T. angustula Pot-Pollen from Mérida 347
24.3 Methods to Quantify Flavonoids, Polyphenols, Proteins, and Antioxidant Activity in Ethanolic Extracts of T. angustula Pot-Pollen 348
24.3.1 Preparation of Pot-Pollen Ethanolic Extracts 348
24.3.2 Flavonoid Content 348
24.3.3 Polyphenol Content 348
24.3.4 Protein Content 348
24.3.5 Antioxidant Activity by the ABTS+• Method 348
24.3.6 Antioxidant Activity (AOA) by Fenton-Type Reaction 349
24.3.7 Hydroxyl Radical Assay 349
24.4 Biochemical Components and Antioxidant Activity of Ethanolic Extracts from T. angustula Pot-Pollen 349
24.5 Conclusions 351
References 352
25: Chemical, Microbiological, and Palynological Composition of the “Samburá” Melipona scutellaris Pot-Pollen 354
25.1 Introduction 354
25.2 The “Samburá” of the True “Uruçú” Bee 355
25.3 Physicochemical Characteristics of “Samburá” 355
25.3.1 Moisture 356
25.3.2 Ash 357
25.3.3 Lipids 357
25.3.4 Protein 358
25.3.5 Fiber 358
25.3.6 Carbohydrates 358
25.3.7 pH 358
25.3.8 Free Acidity 359
25.3.9 Water Activity (Aw) 359
25.3.10 Total Energy Value 359
25.4 Microbiological Characteristics of “Samburá” 359
25.5 Pollen Analysis 361
References 363
26: Characterization of Pot-Pollen from Southern Venezuela 366
26.1 Introduction 366
26.2 Venezuelan Stingless Bees 367
26.3 Botanical Origin of Venezuelan Pot-Pollen 367
26.4 Proximal Analysis of Venezuelan Pot-Pollen 370
26.5 Bioactive Components and Antioxidant Activity of Pot-Pollen Ethanolic Extracts 372
26.5.1 Preparation of the Ethanolic Extract 372
26.5.2 Bioactive Components 373
26.5.3 Flavonoids by HPLC-UV 374
26.5.4 Antioxidant Activity of Venezuelan Pot-Pollen Ethanolic Extracts 375
26.6 Conclusions 377
References 377
27: Bioactivity and Botanical Origin of Austroplebeia and Tetragonula Australian Pot-Pollen 381
27.1 Introduction 381
27.2 Nutraceutical Properties of Bee Pollen 382
27.3 Botanical Origin of Australian Pot-Pollen 384
27.4 Flavonoids, Polyphenols, and Antioxidant Activity 385
27.5 Antibacterial Activity of Australian Pot-Pollen 388
27.6 Conclusions 391
References 392
28: Antibacterial Activity of Ethanolic Extracts of Pot-Pollen Produced by Eight Meliponine Species from Venezuela 395
28.1 Introduction 395
28.1.1 Biological Potential of Pollen Stored in Bee Nests 395
28.1.2 Aim of the Chapter 396
28.2 Pot-Pollen Samples and Ethanolic Extraction 397
28.3 Well Diffusion Agar and Minimal Inhibitory Concentration Methods 397
28.4 Antibacterial Activity of Venezuelan Pot-Pollen Ethanolic Extracts 398
28.4.1 Inhibition Zone Diameters 398
28.4.2 Minimal Inhibitory Concentrations 398
28.4.3 Antibacterial Activity of Pollen and Polyphenols 399
28.5 Conclusions 401
References 402
29: Metabolomics Analysis of  Pot-Pollen from Three Species of Australian Stingless Bees (Meliponini) 404
29.1 Introduction 404
29.1.1 Historical Accounts of Australian Pot-Pollen 404
29.1.2 Health Benefits of Bee Pollen 405
29.1.3 Botanical Sources within Flight Range 405
29.1.4 Food Security 405
29.1.5 Research in Australian Meliponini Bee Products 406
29.1.6 Aim of the Chapter 406
29.2 Methods of Chromatographic Analysis of Pot-Pollen 407
29.2.1 Sampling Pot-Pollen from Bee Hives of Australian Meliponini 407
29.2.2 Extraction 407
29.2.3 Volatiles by HS-SPME-GC-MS 407
29.2.4 Chemical Constituents by HPLC-DAD-ESI(–)-MS/MS 408
29.2.5 Targeted Analyses of Pyrrolizidine Alkaloids (PA) by ESI(+)-MS/MS 409
29.2.6 Metabolomics of Pot-Pollen VOCs and Phenolics 409
29.3 Chemometrics of Australian Meliponini Pot-Pollen 409
29.3.1 Volatile Organic Compounds (VOCs) 409
29.3.2 Secondary Metabolites by LC-UV-HRMS/MS 412
29.3.3 Chemometrics Using Open Source Data 415
29.4 Future Studies of Australian Pot-Pollen 417
29.4.1 Botanical and Ecological Studies 417
29.4.2 Microbiological Aspects and Metabolomics of Australian Pot-Pollen 417
29.4.3 Recent Trends in Australian Meliponiculture 418
29.5 Conclusions 419
References 419
Part V: Marketing and Standards of Pot-Pollen 421
30: Rural-Urban Meliponiculture and Ecosystems in Neotropical Areas. Scaptotrigona, a Resilient Stingless Bee? 422
30.1 Introduction 422
30.2 Initiatives to Revitalize Stingless Bee Keeping 423
30.3 Traditional Knowledge Involving Scaptotrigona 424
30.4 One Stingless Bee, Scaptotrigona, Preferred over Melipona 426
30.5 Naming Pot-Honey and Pot-Pollen in Labels of Commercial Products 429
30.6 Future of Social Interventions in Meliponiculture 432
References 434
31: Pot-Pollen ‘Samburá’ Marketing in Brazil and Suggested Legislation 436
31.1 Introduction 436
31.2 Pot-Pollen Is Known as ‘Samburá’ in Brazil 437
31.3 Meliponine Species Used for the Production of ‘Samburá’ 437
31.4 Harvesting and Processing 439
31.5 Marketing of Meliponine ‘Samburá’ 440
31.6 Cultural Aspects of Pot-­Pollen Consumption in Brazil 440
31.7 Strategies to Increase the Production of ‘Samburá’ 440
31.8 Seasonality of Pot-Pollen 441
31.9 Pot-Pollen Production Initiatives in Brazilian States 441
31.10 Suggested ‘Samburá’ Standards for Pot-Pollen Legislation 441
References 444
Appendix A: Ethnic Names of Stingless Bees 445
Appendix B: Microorganisms Associated with Stingless Bees or Used to Test Antimicrobial Activity (AM) 448
Index 450