“Cocoa fruit has improved greatly” “In one tree, around three hundred fruits” “A lot of broken branches because of too many fruits” “Pollination is indeed very tiring, but the yields are very satisfying” “I keep pollinating and my family is always good” (Cocoa farmers of Napu Valley) Cocoa pollination as a potential yield driver under changing management and climate Dissertation to obtain the Ph. D. degree in the International Ph. D. Program for Agricultural Sciences in Göttingen (IPAG) at the Faculty of Agricultural Sciences, Georg-August-University Göttingen, Germany presented by Manuel Toledo-Hernández born in Merida, Mexico Göttingen, November 2019 D7 1. Name of supervisor: Prof. Dr. Teja Tscharntke 2. Name of co-supervisor: Dr. Michael Rostás Date of dissertation: 13 February 2020 CONTENTS Contents General Introduction ................................................................................................... 4 Ecological Intensification and Cocoa Production in a Changing World .................. 5 Understanding Cocoa Pollination for Effective Ecological Intensification ............... 6 Research Aims and Questions .................................................................................. 8 Research Approach ................................................................................................. 10 Study Site............................................................................................................ 10 Landscape and Farm Characterization ................................................................ 11 Manipulation of Litter Amounts and Monitoring of Flower Visitors ........................ 13 Hand Pollination Study ........................................................................................ 14 References .............................................................................................................. 18 Chapter I - Neglected Pollinators: Can Enhanced Pollination Services Improve Cocoa Yields? A Review ...................................................................................................................... 22 Abstract ................................................................................................................... 23 Introduction ............................................................................................................. 23 Literature Review .................................................................................................... 25 The Cocoa Cycle from Flower to Harvest ................................................................ 25 Flowering (Phase I) ............................................................................................. 26 Flower Opening and Pollination (Phase II) .......................................................... 29 Flower Fecundation and Fruit Set (Phase III) ...................................................... 30 Fruit Development and Harvest (Phase IV) ......................................................... 31 The Cocoa Pollinators ............................................................................................. 33 The Ceratopogonids ............................................................................................ 33 Non-Ceratopogonid Species as Pollinator Agents ............................................... 36 Ecological Intensification, Yield Deficits, and Pollination Services ........................... 37 Climate Risk on Cocoa Production – Ecological Intensification as a Solution ...... 37 Management Strategies to Enhance Pollination Services .................................... 38 Trade-off between Pollination and other Yield-affecting Factors .......................... 39 Future Research ...................................................................................................... 40 Knowledge Gaps and Research Needs ............................................................... 41 Conclusions ............................................................................................................. 44 Acknowledgments ................................................................................................... 45 References .............................................................................................................. 46 Electronic Supplementary Material .......................................................................... 56 Chapter II - Landscape Complexity and Farm Management Moderate Cocoa Flower Visitors in Indonesian Agroforests ............................................................................................. 66 1 CONTENTS Abstract ................................................................................................................... 67 Introduction ............................................................................................................. 68 Materials and Methods ............................................................................................ 69 Study Site............................................................................................................ 69 Farm Characterization ......................................................................................... 69 Landscape Characterization ................................................................................ 70 Field Study Design .............................................................................................. 70 Flower Visitors Monitoring ................................................................................... 71 Data Analysis ...................................................................................................... 72 Results .................................................................................................................... 73 Overall Flower Visitors ........................................................................................ 73 Flower Visitor Species Richness and Abundance ................................................ 73 Correlative Approach .......................................................................................... 75 Experimental Approach ....................................................................................... 75 Discussion ............................................................................................................... 78 Flower Visitation and Flower Visitors ................................................................... 78 Pollinator Potential of the Main Flower Visitors .................................................... 79 Landscape Effect on Flower Visitors ................................................................... 80 Farm Management Effect on Flower Visitors ....................................................... 80 Conclusion and Outlook .......................................................................................... 81 Acknowledgments ................................................................................................... 82 References .............................................................................................................. 83 Electronic Supplementary Material .......................................................................... 88 Chapter III - Hand Pollination, not Pesticides or Fertilizers, Increases Cocoa Yields and Farmer Income ...................................................................................................................... 94 Abstract ................................................................................................................... 95 Introduction ............................................................................................................. 95 Materials and Methods ............................................................................................ 97 Study Site............................................................................................................ 97 Farm Survey ....................................................................................................... 97 Experimental Design ........................................................................................... 97 Hand Pollination Method ..................................................................................... 99 Fruit Monitoring and Harvesting ........................................................................ 100 Statistical Analysis ............................................................................................ 101 Hand Pollination and Farmer Income ................................................................ 102 The IPollnet scenarios justification ........................................................................ 104 Results and Discussion ......................................................................................... 104 2 CONTENTS Partial Hand Pollination Effects on Yield Related Variables ............................... 104 The Cocoa Fruit Development ........................................................................... 106 The Economic Benefit of Pollination in Napu Valley .......................................... 108 Hand Pollination and Cocoa Sustainability ........................................................ 109 Conclusions and the Way Forward ........................................................................ 110 Acknowledgments ................................................................................................. 112