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Title Cross-Pollinating Agriculture, Ecosystems and Food: Human/Bee Relationships in ,

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Author Cely Santos, Marcela

Publication Date 2018

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UNIVERSITY OF CALIFORNIA SANTA CRUZ

CROSS-POLLINATING AGRICULTURE, ECOSYSTEMS AND FOOD: HUMAN/BEE RELATIONSHIPS IN ANOLAIMA, COLOMBIA

A dissertation submitted in partial satisfaction of the requirements for the degree of

DOCTOR OF PHILOSOPHY

in

ENVIRONMENTAL STUDIES

by

Marcela Cely-Santos

March 2018

This dissertation of Marcela Cely-Santos is approved:

______Professor Stacy Philpott, Chair

______Professor Flora Lu

______Professor Andrew Mathews

______Tyrus Miller Vice Provost and Dean of Graduate Studies

Copyright  by Marcela Cely-Santos 2018

ii Table of Contents

List of Figures…………………………………………………..………….. iv

List of Tables…………………………………………………………..…... vi

Abstract…………………………………………………………..………… vii

Acknowledgements………………………………………………………... ix

Introduction……………………………………………………..…………. 1

The little –and big– things that run the world

Chapter 1…………………………………………………………..………. 23

Anolaima: A territory emerging from multi-scale ecologies.

Chapter 2…………………………………………………………..………. 109

Intersections between rural livelihood security and animal pollination

in Anolaima, Colombia.

Chapter 3………………………………………………………………...... 159

Local and landscape habitat influences on bee diversity in agricultural

landscapes in Anolaima, Colombia.

Conclusions……………………………………………………………...... 209

iii List of figures

Figure 1. Representation of the coat of arms of Anolaima made with 28

fruits during the Corpus Christi 2015 festivities.

Figure 2. Modern crop of tomatoes in La Laguna village, Anolaima, 68

March 2016.

Figure 3. Displacement of the local market in Anolaima. 74

Figure 4. Vegetables rejected by food brokers. 77

Figure 5. Little angels nesting next to a power outlet at Doña 81

Blanquita's house.

Figure 6. Timeline describing major socio-political processes, systems 86

of agricultural production, land use change, livelihoods and

agricultural exchange, and major events involving bees in

Anolaima.

Figure 7. Rank-abundance graphs for crops grown for self-subsistence 138

and commercial purposes across farms in Anolaima.

Figure 8. Contribution of animal pollination to foods grown in 139

Anolaiman households.

Figure 9. Socio-economic factors influencing the richness of 140

subsistence crops in Anolaiman households.

Figure 10. Seasonal contribution of animal pollination to foods 141

consumed by households in Anolaima.

iv Figure 11. Factors influencing the richness of foods consumed in 142

Anolaiman households.

Figure 12. Distribution of livelihood activities across Anolaiman 145

households.

Figure 13. Socio-economic drivers of income in Anolaiman households. 146

Figure 14. Map of Anolaima showing the seventeen study sites and land 198

cover types in the study region.

Figure 15. Diagram of the experimental design of the study. 199

Figure 16. Local and landscape drivers of bee abundance in 200

agroecosystems in Anolaima.

Figure 17. Local and landscape drivers of bee richness in 201

agroecosystems in Anolaima.

Figure 18. Local and landscape drivers of bee evenness and dominance. 202

Figure 19. Relative abundance of bee tribes in different land use types, 203

and of land use types sampled across study sites within

25 m x 25m quadrants.

Figure 20. Rank abundance of bee genera registered across 17 farms in 207

Anolaima, Colombia.

Figure 21. Diversity profiles of bees captured across our study sites. 208

v List of Tables

Table 1. Foods grown in Anolaima in the recent past (twenty 91

years ago) and in the present, according to elder women

trading foods in the public market.

Table 2. Socio-economic characteristics and variables regarding 136

crop and dietary diversity across Anolaima.

Table 3. Correlations among socio-economic characteristics of 137

sixteen focus households in Anolaima.

Table 4. General linear models (GLM) predicting the bee 196

abundance, richness and evenness of local bee

assemblages.

Table 5. Bee generic and tribal richness across land use types. 197

Table 6. Variables measured and used in the ecological study. 206

Table 7. Variables selected for data analysis, and results of 208

Pearson’s correlations with correlated variables.

vi Abstract

Cross-Pollinating Agriculture, Ecosystems and Food:

Human/Bee Relationships in Anolaima, Colombia

Marcela Cely-Santos

Behind every cup of coffee, chocolate bar and fruit salad there are hundreds of insects and smallholders in the tropics linking forests, agricultural fields and food. Insects, especially bees, mediate the production of about 75% of crop plants consumed worldwide, and smallholders in the tropics produce about 40% of the world’s food.

Both bees and traditional small-scale production systems are threatened because of the expansion of industrial agriculture. In this dissertation I aim to understand how agrarian change – the transformation from traditional to industrial agriculture– has influenced the relationships between humans and bees through effects on Anolaiman livelihoods and landscapes. In doing so, I re-construct the environmental history of the region and describe socio-economic, cultural and ecological drivers and trajectories of socio-ecological change shaping the current state of Anolaima. To evaluate the interdependence between humans and bees, I evaluate the contribution of animal pollinators to rural livelihood security. I find that local socio-economic asymmetries associated with agrarian change influenced food access in Anolaima in such a way that pollination deficits could disproportionately affect poor households, while nutrient-rich, animal-pollinated crops become luxury foods. To understand the effects of environmental change on bees, I assess the influence of agricultural management and habitat factors at the local and landscape scales on bee diversity, and

vii find that bee communities are undergoing a process of biotic homogenization associated with environmental change. This empirical and interdisciplinary study represents a holistic understanding of bee declines and its emergence from multiple layers of socio-cultural, economic, political and environmental dynamics associated with agrarian change, an urgent issue with important implications for food security throughout the world.

viii Acknowledgements

Ithaka

C.P. Cavafy (Translated by Edmund Keely)

As you set out for Ithaka

hope your road is a long one,

full of adventure, full of discovery.

Laistrygonians, Cyclops,

angry Poseidon—don’t be afraid of them:

you’ll never find things like that on your way

as long as you keep your thoughts raised high,

as long as a rare excitement

stirs your spirit and your body.

Laistrygonians, Cyclops,

wild Poseidon—you won’t encounter them

unless you bring them along inside your soul,

unless your soul sets them up in front of you.

Hope your road is a long one.

May there be many summer mornings when,

with what pleasure, what joy, you enter harbors you’re seeing for the first time;

ix may you stop at Phoenician trading stations

to buy fine things,

mother of pearl and coral, amber and ebony,

sensual perfume of every kind—

as many sensual perfumes as you can;

and may you visit many Egyptian cities

to learn and go on learning from their scholars.

Keep Ithaka always in your mind.

Arriving there is what you’re destined for.

But don’t hurry the journey at all.

Better if it lasts for years,

so you’re old by the time you reach the island,

wealthy with all you’ve gained on the way,

not expecting Ithaka to make you rich.

Ithaka gave you the marvelous journey.

Without her you wouldn't have set out.

She has nothing left to give you now.

And if you find her poor, Ithaka won’t have fooled you.

Wise as you will have become, so full of experience, you’ll have understood by then what these Ithakas mean.

x

When I decided to leave Colombia to study abroad, I did not contemplate the many ways in which my life would change. All the challenges, beautiful people, celebrations, refusals, and achievements have been opportunities to learn. I am grateful that life has given me so many opportunities. I truly hope I can share the privileges of experiencing all what has come to my life with others, especially with those less privileged, many times forgotten.

After I left to conduct fieldwork in Anolaima, I asked myself whether it was a good idea to renounce to the expectations of “my world” for two years. Experiencing a different reality with all its challenges and opportunities was a great gift brought by this dissertation. My fieldwork season was the best–and perhaps the only–way to learn about the infinite generosity, warmth and great sense of humor of peasants; the deep reasons for their supposed irrationality; the wonder and potential of a child holding a camera; and the wisdom and strength of spirit someone develops after a lifetime of apparent failure and indisputable marginalization. I learned about hope, joy, collaboration, and life priorities with farmers; and faced fears, reflected about the limits and consistency of my practices as a scientist, and re-learned how my family is

“my team.” I have uncountable and unforgettable lessons; all of it was worth it.

To all the farmers, beekeepers and people in Anolaima who shared pieces of their lives with me: I have no words to define my immense and absolute gratitude. You helped me grow as a person in ways I could have not imagined, and made me dream –

xi now realistically– about building a reality in which we all can coexist. To Ceineth

Murcia, Angelita, Santi and Simón: thanks so much for your friendship and trust, and for letting me stay with you during the first months of my time in Anolaima. Thanks for not treating me as a princess and for teaching me what it takes to earn a meal in the mountains; my back and hands and all my senses do not forget it. Ceineth, thanks for all the inspiring conversations and for your commitment with “the rural.” Pedro and you are an example of consistency, of how believing is doing. Doña Ligia thanks for sharing your wisdom, knowledge and stamina with me, and thanks for embodying curiosity: it was contagious (you are such a great scientist!). Doña Blanquita and Don

Gustavito: thanks for being such a loving family to me. I still remember your jokes, hugs, juices and gifts. Thanks for walking me through your beautiful farm so many times, for your sincere conversations and collaboration. Yaquie, Maribel and Diana

(and again, Doña Ligia and all the women I met): thanks for exemplifying the power and spirit of women! You are inspiring! Don Antonio, Don LJ, Don Floro, Don

Eduardo and Don Fernando: thank you for trusting in me, for being friends and for your life advice. Doña Yolanda and Don Guillermo: thanks for your smiles and integrity. Don Marco: thanks for all your insights and for sharing “classified” data.

Doña Miriam and Don José: thanks for your support and trust. David: thanks for embodying hope, truly. Javier, Lucho, Natali and your families: thanks so much for sharing your love for bees and for being close colleagues throughout my journey. You taught me so much! I wish I could give this back to you in a meaningful way, and soon. To Manuela and Adrián: Thanks for the beautiful illustrations and for helping design the poster and t-shirts for farmers. To Red de Permacultura de la Región del

xii : you are my inspiration! It was a pleasure to meet you and be part of your performances. You embody a path to build an alternative world, free of the impositions that limit our spirit.

To my parents: it is not possible to express my immense gratitude to you for showing me your love in such diverse ways. You have dealt with this “crazy goat” in the best possible way. Thanks for letting me grow through my mistakes. You never took the obstacles out of my way, but instead gave me protection and tools so that my fall was less painful, and then offered me your hand to recover. I mean this literally as well as figuratively; you supported my idea of motorcycle transport during fieldwork and gave me protection that made me look like a Martian. Thanks for helping me make flower bags, flags, pollinator traps, nets, and other things I used as equipment. Thanks for believing in the bees and in the people of Anolaima! And thanks for always believing in me. I love you.

To my advisors: I do not have enough words to describe my gratitude. You were support, compassion, collaboration and inspiration. Stacy, thanks for sharing your company, for listening, for all your feedback, and for being an example. Also, thanks so much for your patience when my path took deviated from classical ecology, for trusting me and never trying to cut my wings. Also: thanks for sharing your festive and collaborative spirit! Flora, thanks so much for everything! You pushed me to give more since the very beginning and that made me realize that I could do it and also, that I can give in unique ways. Thanks so much for every single conversation; I read

xiii my notes and still find them so fertile! Thanks for encouraging me to break the conventional while asking me to keep rigor in my research, for pushing me to work with and for local people. Also, thanks so much for listening, for airport rides, and also for your economic support. Andrew, thanks so much for all the inspiration and support! The Science and Justice class and that really changed the way I approach my practices. Thanks for encouraging me to include very different skills into my toolbox, and everything you recommended to read, I enjoyed them a lot! Thanks for trusting me and for helping me believe in what I do.

To professors Rodulfo Ospina, Emilio Realpe and Guiomar Nates: thanks for your ideas and support with this project, and for always being open to collaborate. To Juan

Diego Maldonado, Nathalia Florez, Jesús Hernández and Susana Currea: thanks for your support with determining bee identities. Also, it was great to see how you work as a hive. To Cindy Cordoba, Estyben Pirachican and Tomás León: thanks for taking me to Anolaima and for always being open to talk and help. Your friendship means a great deal to me.

To Bronwen Stanford: thanks so much for every application you read, the conversations we had, and all the support along the way. To Alicia and Jorge: thanks for your hospitality and for being a family in Santa Cruz. To the ANTs lab: thanks for your support, for listening and for the lessons you taught me along the way. To the

ENVS 2012 cohort: thanks for your support, especially during coursework. To

Monica Torres: thanks for sharing with me your ideas and for always being there;

xiv your company was of tremendous importance during all the lonely times during this dissertation. To Carole Prouteau: thanks for embodying so much! For your ideas, for listening, for loving the bees! Thanks so much for introducing me to Buddhism, which changed almost every aspect of my life, and nurtured my capacity to pay attention to details during fieldwork and many of my approaches in this dissertation.

To Darío Perez: thanks for being a research buddy! And thanks for your commitment to work with farmers, for teaching me about plants and for inviting me to join your research group. To Nicolás Otero: thanks for showing me that photography is more than looking through a photo camera, and for teaching me how to visually approach the world of bees. To Juan Manuel Rosso: thanks for sharing your bee-worlds, for your support and for spreading love for bees.

Last but not least: thanks to the bees. Partial serendipity took me to them, and I did not imagine they would be such a source of inspiration. It is difficult to describe the many ways in which they are amazing. When I started this path, Juan Manuel mentioned that his life became richer as he run into amazing people who shared his love for bees. I share his view and am grateful all the gifts coming from bees.

xv Introduction:

The little and big things that run the world.

E.O. Wilson (1987) wrote about "the little things that run the world," referring to the need to conserve insects as a way of sustaining other life forms. According to Wilson, small size is key to insect exuberance and diversity, and to the way they regulate processes that enable a vast array of other beings’ living strategies. If we think about the human world, we can add peasants, campesinos, and their diverse agricultures to this image, actors and processes that sustain an important share of food production across the world. Often, the little things running the world are taken for granted, their abundance and seeming ubiquity ironically rendering them invisible and obscuring their fragility. The contributions of insects and peasants to sustaining the integrity of ecosystems upon which our societies depend are massive, and their declines would bring a devastating imbalance.

If bees and campesinos are two of the actors running the world from the bottom up, we can call upon the complementary biological metaphor of top-down regulation too.

John Terborgh (1974) wrote about the big things that run the world to describe how predation regulates the abundance of the little things running the world to sustain a green earth. Small and big things depicting bottom-up and top-down forces, respectively, have acted in concert through the course of history to regulate ecological processes. In the human world, capitalistic projects and power asymmetries act as big top-down forces that control and subdue the "little and abundant". These top-down

1 world making projects, however, resemble invasive species that create major disequilibria, disrupt elements of autonomous socio-ecological systems–, landscapes worldviews and lifescapes–and force them to sustain the interests of few powerful actors at the expense of the alienation and disappearance of a multitude of others.

This dissertation navigates the intersections between two invisibles, bees and campesinos, in the context of the expansion of a top-down world-making project: capitalistic industrial agriculture. These invisibles have a long-term history of companionship, and greatly contribute to sustain worlds through their role in food production. Bee-mediated pollination benefits more than 85% of tropical flowering plant species, which include half of the major crop species grown worldwide and all food resources for innumerable nonhumans (Eilers et al. 2011a). Likewise, more than

50% of the food consumed by humans across the globe is produced by indigenous, black and peasant communities (FAO 2014), who dwell and take care of heterogeneous territories considered to be biological and biocultural refuges. Both bees and campesinos have been fading during the last decades and are threatened by the expansion of industrial agriculture.

Industrialization and the making of a modern "one-world world” (Law 2015) have subdued heterogeneity and undermined many of the little things running the world and the links among them. After the great acceleration in the second half of the 20th century humans improved our abilities to expand standardized production, and to

2 order and control processes to maximize their productivity, efficiency and profitability. Agricultural systems –including the humans managing them– came to be subjected to the principles ruling modern factories to facilitate exploitation. As diversity imposes challenges for ordering beings and processes, what could not be controlled was not trusted and should be eliminated: herbs became weeds and herbivores turned into pests. Diversity was no longer abundance and opportunity but a problem, something to be persecuted. Agroecosystems were simplified and peasants supporting diversity were seen as backwards and obsolete, needing to be modernized

(Nazarea 2005). The modern state promoted the reorganization and legibility of agricultural territories, and through this process disregarded values and uses of the land, which facilitated the appropriation of rural land and exploitation of peasant labor (Dove 1983).

Bee and peasant practices have also been controlled to comply with ideals of modernity. While the European honeybee Apis mellifera has been managed by humans since antiquity, the modernization of beekeeping in the 19th century imposed uniformity on honeybees by placing nests into fixed structures designed to facilitate the extraction of honey for beekeepers, and the legibility of the productivity of the hive (Ransome 1937, Scott 1998). This facilitated the massive reproduction of honeybees, later exploited to pollinate commodity crops in agroindustrial systems.

Thriving in chemically disturbed and simplified agroindustrial landscapes, Apis mellifera populations have declined dramatically in the last decades greatly impacting the market of commercial pollination (Meixner 2010). Meanwhile, several regions in

3 the Americas fought with the Africanized hybrid of this bee after its accidental release in Brazil in the mid 20th century.

Behind Apis mellifera, hundreds of unmanaged native bee species suffered the damages of invisibility: their optimal habitats disappeared, food sources were homogenized and poisoned after the expansion of agroindustrial monocultures, landscapes have been simplified limiting bee dispersal, and chances to recover are considered to be low for many bee species (Goulson et al. 2015). This collapse of animal pollinators, affecting food production and resilience to environmental change, has mobilized ecologists and practitioners to protect these little things running the world. Now it is recognized that high bee diversity contributes to the stability of pollination function over time, which is complemented by managed Apis bees

(Garibaldi et al. 2013). This knowledge has supported policies to increase bee presence in agricultural lands in industrialized countries, yet action is urgently needed in the tropics

On the human side, smallholders are still unseen and persecuted. Despite their immense contribution to human food production, dietary diversity and natural resource management, peasant ways of living are not considered to be compatible with the modern world. All traditional small-scale agricultural systems are unique and supported by intrinsic rationalities where local knowledge about natural cycles and ecologies is the primary driver of adaptation (Conklin 1957, Toledo 1989, Netting

1993). Smallholders do not typically behave as Homo economicus: agricultural costs

4 are seldom calculated, and relationships are not defined by financial transactions.

When small-scale agriculture is under the spotlight, it is perceived as messy, unproductive, and necessitating "improvement." In other words, when farms are reduced to rural enterprises, life needs to be technified and capitalized; agroecosystem designs need to be scalable; and numbers profitability dominates equations to determine the viability of agricultural systems (Chaparro 2013). Promoting a discourse to revitalize traditional family agriculture, the Food and Agricultural

Organization FAO (2014) acknowledged the role of smallholders for global food production and in the sustainable use of natural resources. The counter narrative of smallholders as stewards producing healthy food has been insufficient, however, to significantly ameliorate the marginalization they continue to endure.

Declines in bees and campesinos are one of the many symptoms of the current crisis in food systems derived from the expansion of industrial agriculture, and influence both the material and immaterial engagements linking these actors. Typically, the different components of human-bee relationships are approached independently.

Natural sciences assess the structure of bee communities, their interactions with other organisms and their biophysical context, and assessments of the effects of human activities on bees is done by conducting research in disturbed areas (Kremen et al.

2002, Brosi et al. 2007, Hoehn et al. 2008, Rader et al. 2014, Winfree et al. 2014,

Aguirre-Gutierrez et al. 2016), and by evaluating the economic role of bees in food and fiber production (Klein et al. 2007, Olschewski et al. 2007, Eilers et al. 2011b).

Social sciences focus on human dynamics, and, for example, have assessed the

5 viability of small-scale agriculture by examining farmers’ economic rationalities

(Ellis 1998, Scoones 1998, Brons 2005, Ellis 2008). These sciences discount that social relationships are not restricted to humans (Tsing 2014), and that we are pluralities making worlds by interacting with more-than-humans (Whatmore 2006).

Approaches that describe how humans and bees have co-produced socio-ecological worlds over time, as well as the forces influencing transformations in our relationships with bees (Becker et al. 1999), would offer a better understanding of the deep roots of bee declines, and of potential strategies to promote coexistence and synergies between humans and bees in agricultural lands.

In this dissertation I share stories about humans and bees in Anolaima, a small town in the mountains whose identity as the fruit capital of Colombia was forged through the interactions between wild, native pollinators and peasants. Anolaima is close to the country's capital, , and because of its agricultural diversity and productivity, was an important part of Bogota's food pantry. Likewise other rural regions serving the direct interests of urban cores, this municipality has received continuous interventions from the state and parastatal institutions, shaping landscapes, livelihoods and relationships with different organisms. Currently, people in Anolaima do not think this is the fruit capital of Colombia anymore. Agricultural profitability has declined as have sustainability of traditional livelihoods and landscapes. I provide a more holistic understanding of bee declines in this region, for which I evaluate whether and how agrarian change –the transformation from

6 traditional to industrial agriculture – has influenced the relationships between humans and bees through its effects on Anolaiman livelihoods and landscapes.

Understanding contemporary bee declines requires a look to the past for a description of the emergence, persistence, and unraveling of human-bee relationships in agricultural lands. For this, I reconstructed an environmental history of Anolaima to understand the agency of plants and bees on the making of agricultural systems, and how agrarian transitions have affected landscapes, livelihoods and human-bee relationships across time. In addition, I evaluated the contribution of animal pollination to current food production and consumption, and how that contribution is mediated by socio-economic factors influencing agrarian change. Also, I assessed how the configuration of habitats at the local and landscape scales influence bee diversity in Anolaima. This empirical study is based on social and ecological surveys,

GIS analyses, interviews, focus groups, and participant observation. I describe how these approaches comprise different chapters of the dissertation below.

Anolaima: A territory emerging from multi-scale ecologies

Rural landscapes are dialectical and historically contingent systems resulting from the multiple interactions among humans and more-than-humans. The first chapter delves into environmental history, a field that incorporates environmental responses and sensitivity to historical trajectories of social change, to reconstruct the making of human/bee relationships, landscapes and livelihoods in Anolaima during the 20th century. Customary historical views recreate the past by centering on (some) humans

7 and largely overlooking the plurality of actors co-constituting social worlds. By acknowledging the agency of nonhumans in the co-production of socio-ecological systems through time, and the influence of human worldviews and practices on the composition and interactions of the biophysical world, environmental history helps to dismantle the nature/culture binary in favor of a hybrid condition of the environment

(Cronon 1996, Haraway 2003, Laura A Ogden and Tanita 2013, Smart 2014,

Mathews 2017, Tsing et al. 2017).

In my reconstruction, I explore the relationships between plants and bees, and how their features defined terms of their relationships with humans, nurtured and enabled livelihoods, and shaped landscapes in Anolaima. I portray changes in flora, fauna and landscapes and how they have influenced social relationships across time. Also, I describe the arrival of the exotic European honeybee, Apis mellifera, and of its

Africanized hybrid, and describe how these events greatly influenced bee-human relationships over time.

Interactions framing socio-ecological systems and the construction of naturecultures, as coined by Haraway (2003), are subject to power dynamics exerted across multiple scales. For example, several authors have assessed the remote linkages between global trade and local economies and their influence on the relationships between people and more-than-humans (Zimmerer 2006, Dove 2011). Environmental history traces these linkages to disclose how socio-environmental inequality emerges from power dynamics that constrain segments of the population from accessing natural

8 resources, or by making them vulnerable to the negative effects of environmental degradation (Leal Leòn and Restrepo Uribe 2003). In the case of Anolaima, I describe how the insertion in global world-making projects and economies influenced the emergence of social inequalities and conflicts over the land. These projects have directly impacted land uses through agroindustrial technologies and management practices, and have also influenced the transformation of local, regional and global food circuits. These transformations of food systems have had important repercussions for livelihoods, landscapes and bee-human relationships through time, inducing the abandonment of the countryside and the erosion of agri-food cultures in

Anolaima.

Intersections between rural livelihood security and animal pollination

After addressing the making of agrarian change, in Chapter Two I evaluate how livelihood strategies and class relationships intersect with animal-mediated pollination in Anolaima. Animal pollination contributes to approximately 35% of the global food production by benefiting about 75% of the crop species grown worldwide. Most of the assessments of the contribution of animal pollination for humans are situated in the ecosystem services framework (Kremen et al. 2007, Zhang et al. 2007, Power 2010, Kareiva et al. 2011), which highlights the goods and functions performed by nonhumans that benefit human societies.1 These accounts

1 This framework aims to make visible the relevance of biodiversity to humans, especially to market economies where actors and processes only exist when their financial value are higher than zero. ⁠ This approach has been useful for ecological economics, a

9 seldom explore the distributional asymmetries in the access to the benefits derived from nonhumans and their ecological functions (but see Adekola et al. 2015), a significant oversight given the intersections between biodiversity and human societies with cultural, socio-economic and political factors altering the role of nonhumans in livelihoods. Through a political ecology lens, which evaluate the influence of power dynamics in the use and management of the environment, I analyze whether and in what ways the contribution of animal pollination to Anolaiman households depended on socio-economic characteristics influencing the vulnerability of farming families to agrarian change

Power and class differentiation can influence rural livelihoods through different paths. For example, particular combinations of socio-economic factors can drive variation in the foods grown and consumed by people. In this chapter, I also discuss how animal pollination can make visible tensions between food production and access resulting from agrarian change. I also contextualize the case of Anolaima within the global panorama of the political economy of animal pollination and the agrobiodiversity-food-health nexus to speculate about the implications of bee declines for the sustainability of rural livelihoods. By addressing pathways through which

discipline that aims to internalize both the negative and positive economic implications of human activities in market economies.

In this dissertation I avoid referring to ecological processes as services, as an attempt to decenter the human. However, I find that estimating the contribution of ecological functions for securing livelihoods is useful to acknowledge our dependency on other organisms, while keeping in mind that this is one of the many roles of bees in the persistence of socio- ecological complexity.

10 agrarian change increases the vulnerability of traditional farming to social and environmental change, it is possible to understand the connections between political economy, food production and social marginalization; and the influence of social structures in landscape simplification and bees in agricultural lands.

Local and landscape habitat factors influence bee diversity

Bees and humans are connected through their footprints on the environment, and also through direct encounters emerging from everyday practices. Two of the most important ways through which humans influence bees involve the transformation of plant communities and habitats at local and landscape scales, and the use of toxic pesticides that unintentionally affect bees. These practices influence the biophysical context in which bees dwell and the opportunities they find to adjust to environmental change.

After beekeepers reported bee declines in the 2000s, ecologists have engaged in efforts to understand the effects of land use change and agricultural practices on bee diversity. Initially, research assessed the effects of either local or landscape factors on the diversity of bee communities in agricultural lands, mainly in the northern hemisphere and in coffee-producing systems (Steffan-Dewenter et al. 2001,

Olschewski et al. 2006, James and Pitts-Singer 2008, Ricketts et al. 2008, Carvalheiro et al. 2010). These assessments involved relatively homogeneous and simplified agricultural-dominated areas, although agricultural landscapes are not quite homogeneous and should be seen as mosaics comprising patches representing

11 different opportunities or challenges for the bees. Thus, to better understand responses of biodiversity to agricultural change, new approaches address habitat factors at local and landscape scales simultaneously (Forrest et al. 2015, Quistberg et al. 2016, Sydenham et al. 2016). These efforts resonate with ecological theory on spatial (meta) population and community ecology, and how habitat connectivity and disturbance influence reconfigurations (assembling and disassembling) of biotic communities.

Systems involving diverse land uses in the mountainous tropics have been relatively understudied, and examining them may reveal differences in how bee diversity responds to changing habitat configuration. Anolaima is traversed by the biogeographic particularities of the Andes Mountains, where elevational gradients meet the high productivity of the tropics and render high levels of biodiversity in small scales. Thus, in these areas, the quality of land-uses and the intensity of agricultural disturbance could also influence biological communities at small scales.

In this chapter I assess how local habitat factors and landscape configuration influence bee diversity in Anolaima and shed light on the effect of industrialized agricultural practices on heterogeneous tropical landscapes.

This dissertation contributes to understand multi-layered processes driving bee declines in systems with major importance for food production and ecological functioning in biodiversity hotspots. Steward et al. (2014) pointed out that much research approaching key ecological functions for agriculture, animal pollination and

12 predation of herbivores, is conducted in large-scale systems in the northern hemisphere, which only represents 34% of the global crop land. Only 12% of studies took place in systems involving farms smaller than 3 ha, and 72.3% of the studies conducted in the tropics involved coffee agroecosystems. However, there are more than two billion smallholders sustaining food production through an equal number of unique agricultural strategies.

This study takes place in Colombia, the second most biodiverse country on earth.

Most areas in the country (94.4%) are rural. Multidimensional poverty extends over the 34.7% of the country’s population, mainly affecting rural inhabitants. The majority of campesinos have access to less than three hectares of land per household, are socially marginalized and increasingly food insecure (PNUD 2011). Livelihood security relies on the continuous availability of subsistence crops (Alvarez 2001) and on cash crop yields, many of which are benefited by native wild bees. Current state policies promote the entrepreneurial development of rural populations through crop specialization (Colombian Ministry of Agriculture 2013), which potentially threatens traditional diversified systems and bee populations. In addition, little of the national budget is allocated to conservation programs (Waldrona et al. 2013), thus efforts to protect native bees are highly dependent on farmers. This scenario repeats across several tropical developing countries. As such, this study has relevance beyond the

Colombian context to think about the impacts of simplification in agricultural lands, and to approach broader political and ecological questions associated with agrarian

13 change and bee declines, shedding light on processes happening in similar systems worldwide.

An additional remark

Given my Colombian identity, my previous work as a biologist working in rural areas, and my academic training and interest in interdisciplinary studies, dissertation fieldwork was envisioned and implemented as a collaborative endeavor. The stories I tell emerge from conversations and experiences shared with many interlocutors, especially seventeen focal families. Through an aperture created by the planting of guatila (Sechium edule) and conducting of ecological measurements and experiments on their farms, they shared their worldviews and perceptions about life, agriculture, and bees. I visited each household at least once a month for 22 months. We took care of guatila plants during a drought and commiserated about experiencing agricultural failure. I accompanied them in walks around their farms, and most of them joined me in my obsessive curiosity about bees. They taught me about plants during vegetation surveys, allowed me to sample bees on their farms, and participated in my many forms of data collection, which was impossible to capture fully in this dissertation.

Details noticed by either, farmers or me, gave raise to new questions and ways to answer them, such as modifying insect nets to sample tree crowns people were interested in. Besides in-depth research with these households, I interviewed other actors including local authorities, food vendors, elders, young leaders and municipal planners. I worked closely with local women, who learned and nurtured my methods, and from whom I learned about plants, bees, and life. My work with beekeepers was

14 inspiring. Thus, data presented in this project was influenced by my worldview and the visions of the myriad of people who nurtured this fieldwork.

This work also results from deep concerns about my country and from a commitment to addressing existing problems. Colombia is very under-studied due to decades of armed conflict and other barriers rendering it unattractive to researchers. Such volatility also makes conducting medium and long-term investigations intractable. A lack of scientific endeavors and information runs counter to Colombian society being scientifically informed, taking science seriously and engaging in situated decision making. In terms of biodiversity, little of the national budget is allocated to conservation programs (Waldrona et al. 2013), as people are less likely to seek to protect that which they do not know or understand. As a result, efforts to protect nonhuman lifeforms are highly dependent on peasants, people on the ground whose actions have direct impacts on biodiversity, and who are themselves often marginalized. Engaging in efforts to closely understand the challenges of smallholders and other groups, may revitalize and establish new alliances between them and biodiversity, ultimately promoting coexistence (with bees and other lifeforms) and catalyzing social transformation.

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22 Chapter 1:

Anolaima: A territory emerging from multi-scale ecologies

Don Luis Jairo used to accompany his father to drink chicha2 with his

friends in , the neighboring town. Going up and down imposing hills, the

trip took a day a paso de mula3. Quipile, a land full of sugar cane and corn, was

violent. When don Luis was eight, he witnessed a drunken man killing another

with a machete. Despite the brutality of the act, few noticed and no one cared. The

natural abundance of Quipile was undeniable, yet the violence between godos and

cachiporros4 was intimidating. Don Luis always preferred Anolaima, a quiet town

with relative good connections with the capital. Tranquility attracted many

families to Anolaima during the 1940s. Many came from Boyacá, a northern

region in which the violence was devastating lives and landscapes. Anolaima, a

land of relative peace and abundance, seemed to have plenty for everyone.

Indeed, things were going well in town. When doña Blanquita and don Gustavito

got married they already were adept coffee producers, and while things were not

perfect, this crop provided for a good life. Besides growing coffee they took care

of a home garden, kept honey bees, and tended livestock: a cow, and some poultry,

2 Alcoholic beverage made with fermented corn. 3 On top of a mule. 4 Conservatives and liberals.

23 and a horse that helped transport produce to the public market. Back in the 1950s,

the land provided for all of their needs. There was no electricity, gas or aqueducts,

so they needed money to pay for salt and oil, but not for utilities. They were

healthy, thus obviating the need to buy medicines. Doña Blanquita cooked over an

open fire, the mule carried cans with water from the creek, and carne de monte5

was always available. Their children attended a modest elementary school and

studied with the light of higuerilla6 lamps. They did not even think about university

education; it seemed so far away and perhaps unnecessary. Studying gave prestige

but was not crucial: the land provided for everything. Doña Blanquita and don

Gustavito bought the first TV in their village, San Juanito, and invited neighbors

to watch soap operas on Saturdays. The National Coffee Federation helped them

build their house, buy their TV and increase their coffee production. Like this

couple did, hundreds of growers engaged in the National Coffee Federation and

followed their instructions, including the replacement of their beloved trees.

Times changed and so did their needs. During the 1990s, coffee prices collapsed,

which turned that decade into a time for experimentation out of necessity. Doña

Blanquita and don Gustavito sowed three hectares with tomatoes that were

completely lost to frost. They went back to coffee. What were luxuries are now

necessities. The big, old TV sits in one of the rooms, alongside a smaller one: The

former has sound but no image, and the latter has a picture but no sound, so they

5 Edible animals. 6 Castor oil, Ricinus communis.

24 must work in concert. Doña Blanquita and don Gustavito cannot afford a new TV

now. They procured a loan to buy a refrigerator so that they could store milk for

sale. "In those times coffee had value, crops had value, money had value. Now

100,000 Colombian pesos are nothing. It takes a life to earn them and the blink of

an eye to spend them. We wish to go back to the past." In their 60s, doña

Blanquita and don Gustavito use their imagination to reinvent the good old times.

The coat of arms of Anolaima conveys its history as a fruit-producing territory.

Bordered by a music key and flags of the municipality, there is a chalice holding twenty-three types of fruits, many native to Colombia, others adopted after the

Spaniard conquest, and most benefited by animal pollination. The coat of arms also gives the Spanish meaning of the indigenous Panche word7 Anolayma: "Vuestra alegría" (“your happiness”), also the name of the Panche sub-group that once inhabited this land.

As a town located in the eastern flank of the Colombian Andes, Anolaima faces both the challenges and benefits of the mountains. The municipality extends between 900 and 2800 meters above sea level, a zone of transition between cloud-submontane forest and tropical dry forest that enables the cultivation of crops suited to different climatic conditions. Rugged hills have limited the entrance of tractors and mechanized operations and have kept the municipality in relative isolation despite its

7 Panche language was spoken by this indigenous group in the regions bordering the . It was nested in the Caribe linguistic family (Bernal 1946).

25 proximity to populated centers. Anolaima is 75 km away from Bogotá, Colombia’s capital, 42 km from the neighbor city Facatativa, and 90 km from Cambao, a fluvial port in the Magdalena river. This proximity to trade centers made the municipality a food pantry for different regions of Colombia (Rodriguez 2010), rapidly –yet imperfectly–facilitated market integration, and led to greater receptivity to urban cultural influence.

Every June, the fruit capital of Colombia celebrates its agricultural legacy, when farmers from all villages build arcos (figures) made with fruits and vegetables as a tribute to God (Figure 1). The Corpus Christi festivities are used to express gratitude, ask for abundant harvests, and to display creativity and joy with tourists. In the past, tributes in this celebration used only local produce. Anolaima was the main producer of oranges consumed in Bogotá, the capital city, and the municipality with the third and fifth highest coffee and honey production in Cundinamarca, the pertinent administrative unit. Yet during the last few years, the fruits used in arcos are no longer locally grown. Harvests have declined, and cheaper fruits can be found in the central wholesale food market. Farmers assert that Anolaima is not the fruit capital of

Colombia anymore. The profitability of agriculture has decreased considerably during the last 20 years and the expansion of green houses and recreational farms reflects how rural livelihoods have progressively shifted from family agriculture to waged jobs. The land has been deforested and people mention that water shortages are more frequent than ever. This transformation of Anolaima necessitates a diachronic examination of the underlying forces propelling such change.

26

Environmental History of Anolaima: Agriculture, People, and Bees

In this chapter, I reconstruct the environmental history of Anolaima to underscore how environmental dynamics both shape and are influenced by social history, constraining or enabling mechanisms through which humans and nonhumans relate and co-produce socio-ecological worlds (Berkes and Folke 1998, Brown and

Westaway 2011). Landscapes are not anachronisms; instead, as Crumley (1994) suggests, they reflect multiple interactions among humans and nonhumans at various temporal and spatial scales, shaped by particular world-making projects and their socio-political and economic forces. I aim to disclose dynamics –social, economic, institutional, environmental– associated with changes in power dynamics to understand how local and global forces influenced access and use of resources in

Anolaima (Leal Leòn and Restrepo Uribe 2003), and to covey how the links among these forces “cross scales and strengthen each project's ability to remake the world"

(Tsing 2000).

27 Figure 1. Representation of the coat of arms of Anolaima made with fruits during the Corpus Christi 2015 festivities. Most of the fruits used including papaya, avocado, tangerines and mango are benefited by animal pollination. Photo by the author.

Because "social structures are embedded in complex biotic formations, and ecological structures are embedded in complex social formations" (Rocheleau et al. 2001), I also provide descriptions that integrate nonhuman agency in narratives of environmental change. Since people from Anolaima built their agricultural identity with the help of pollinators, I focus on the interactions among plants, bees and humans through time.

Plants and bees have been managed without being forced to change their ecologies, and have domesticated, being greatly modified by –and modifying –the domesticator for their mutual benefit (Zeder 2015). Plants and bees have also been forced to ideas of scalability, or the ability of a system to change scales without transforming its relations or project frames to facilitate human exploitation (Tsing 2012).

28 Management, domestication and scalability have had different impacts on social relationships, landscapes, and multispecies ecologies. Hence, I approach plants, bees and their interactions with humans to trace the impacts of socio-cultural change and scalable projects in the transformation of Anolaiman lands.

In this history I introduce the Spanish conquest and colonial times influencing rural dynamics in Colombia in general, and Anolaima in particular, and I describe major processes during the XX century. These processes include the life of , changes in coffee landscapes, the establishment of industrial capitalistic agriculture, and the transformation of local food circuits in Anolaima. I base my descriptions on secondary sources (i.e.historical accounts, mainly inspired by interest in political economy and social conflict), oral histories, unstructured interviews, a timeline constructed through focus groups with Anolaiman farmers, and herbarium plant records. Secondary sources correspond to historical economic and political analyses of different agricultural activities such as coffee production and cattle ranching in

Cundinamarca, and to accounts on the political economy of commodity production.

These sources are useful to understand broad social processes and their impacts on land cover during the XX century, and by extension, how bees might have been affected by changes in land use change. However, these sources lack geographic specificity and detail to describe how such processes operated within Anolaima. In addition, I use data obtained through focus groups in which twenty-five local inhabitants built a timeline, which depicts a mainstream and collective narrative about major changes in the landscapes and agricultural practices during the last century. I

29 also use oral histories and interviews with key informants about changes in people's lifeways and on the flora and fauna of the region. These sources offer more detail about the everyday processes happening in this municipality in the recent past. I use a botanical description made by a commission of priests during the 1950s (Daniel

1956) and digital herbarium records8 particular to this municipality to characterize the vegetation of this town. Finally, I rely on bee surveys conducted in this municipality and on literature on bee ecology to imagine how bee communities in Anolaima have interacted with plants and people over time.

The problem of the land: life in Anolaima before the coffee boom

"A landless farmer is a soulless farmer"

Anolaiman Farmer. June 2015.

The land can be considered as a portion of the earth's surface, or as the dialectical convergence of ecological, symbolic, social, economic and political processes over time. Multi-layered territories are co-produced by humans and more-than-humans through everyday practices and dwellings, and are recorded in local knowledge and in the different temporalities of the landscape (Ingold 1993, Haraway 2003, Ingold

2011, Kohn 2013). Meanings attached to land depend on individual and collective

8 Records accessed through the digital UNAL herbarium website and the National Biodiversity System data portal. Instituto de Ciencias Naturales, Facultad de Ciencias, Universidad Nacional de Colombia (2004 -continuously updated). On-line collections. Accessed from http://www.biovirtual.unal.edu.co on June 13 2017.

30 perceptions about territorial construction (Haesbaert 2013). In Colombia, traditional communities find in the land the means for subsistence and reproduction of their social systems, while elites use it as a tool to control population and accumulate wealth–thus, an asset representing political power (Fajardo 2002). These differences, reflected in unequal land distribution and social disparities, have been the root of major conflicts in Colombia. Some authors assert social inequalities were facilitated by the convoluted topography of the Colombian mountains, which exacerbated the weakness of the state to regulate land appropriation in many remote areas (Marquez

2004). Others mention that the partial disruption of the state enabled the abuse of power by land owners over landless peasants, and the emergence of many conflicts over the land and its people (Machado and Vivas 2009, Garay et al. 2011). In the next section I depict some changes in the relationships between people and the land in

Anolaima before the second half of the XX century, and I focus on dynamics of land ownership and appropriation, land use change, and the making of rural livelihoods. I start with a brief description of processes happening after the Spanish conquest as a way to contextualize the historical trajectories of this town.

Before the XIX century

The , a region nested between the eastern flank of the Andes and the Magdalena river, was inhabited by Panche indigenous groups obeying their leader Anolayma, and by a myriad of nonhumans (Velandia 1979). While it is difficult to describe the vegetation, fauna and plant-animal-human relationships, landscapes might have included dense sub-andean and cloud forests (Etter and van

31 Wyngaarden 2000), with diverse assemblages of bees. Panche economic activities allows for some speculation about livelihoods and how people used resources in this territory. Panches were known as untamed warriors who hunted game and grew corn and manioc in terraces or labranzas for subsistence (Perdomo 1975). They also made pottery, suggesting Panches had a close relationship with the soil, and produced fibers and cotton textiles. This group also traded salt and honey with , their indigenous neighbors, and were goldsmiths, presumably using stingless-bee wax to model figures as did other indigenous groups (Perdomo 1975, Falchetti 1999).

Thus, Panches likely formed close relationships with social stingless bees native to this province.

The Spanish conquest and colonization dismantled prior forms of social organization and territorial construction, introducing new dynamics in which colonizers took control over the land and their inhabitants. Spaniards arrived in Santa Fe de Bogotá in

1536, and by 1538 they had exterminated Panches and subjugated the few that survived, geographically segregating them for further indoctrination in resguardos9

(Bernal 1946). Indigenous territorial forms of governance were replaced with , forms of domination in which colonizers received large extensions of land and the right to subdue and demand tributes from Indians (Díaz Hernández

1982). Anolaima was officially named an indigenous curato in 1604, and being close

9 Resguardos were areas restricted for the controlled occupation of indigenous groups. In Anolaima they included Mátima and Tocarema, areas named after local indigenous leaders. Curatos were jurisdictions for the indoctrination of indigenous peoples, containing one or several resguardos.

32 to the core colonial settlement in Santa Fe de Bogotá, land in this region was rapidly privatized to Spanish colonizers10 (Velandia 1979). In this way, the land reflected a geography of power in which the worldviews of native peoples would be only visible to reinforce the colonial/indigenous binary that would shape the contemporary history of the Colombia (Serje 2005). A town for white criollos, or descendants of Spaniards born in the Americas, was only established in 1822 (Velandia 1979), and with time, campesinos or peasants emerged from the fusion between indigenous peoples and criollos (Uribe 1964)11, and embodied a marginalized class.

Besides their social impact, encomiendas introduced major land use changes between the XVI and XIX centuries. Some authors assert pressures over the land relaxed with the decline of indigenous population to introduced diseases such as smallpox and influenza (Etter 2000). However, if natural regeneration replaced forests managed by indigenous people in some areas, deforestation advanced in other portions of the territory. Spaniards established plantations of exotic crops that drastically modified landscapes and human livelihoods. Conquerors brought horses and cattle, and with them, established large areas on pastures (Bernal 1946, Márquez 2001, Etter et al.

2008). Spanish colonists also brought sugarcane from Asia, introducing Anolaima to the global dynamics of a crop with great importance for trade and human trafficking during the XVI-XVII centuries (Mintz 1986). Sugarcane plantations were common in

10 This region was occupied by the archbishop and viceroy Caballero y Góngora, 11 See Uribe (1964) for further information on indigenous declines, the introduction of slavery, and mestizaje in Colombia.

33 Anolaiman lowlands, grown as unshaded monocrops that required permanent clearing of the forest around the current San Jeronimo and Peña Negra villages (Bernal, 1946), where forest cutting and sugar cane harvesting and processing12 were performed by black slaves to supplement labor after the declines of indigenous populations, as in other parts of the Americas (Velandia 1979, Mintz 1986).

The sacredness of bees and reverence given to their products connected Europeans and Indigenous peoples in the Americas. During medieval ages, the old-world honeybee Apis mellifera was a close companion to the European clergy and royalty, and bee wax was used in religious rituals. Upon their arrival to the Americas, colonists found stingless and smaller social bees, and in some areas these bees were kept by local peoples (Ransome 1937, De Jong 1999b). Honey and wax were products used and traded both in Europe and the Americas, and bees themselves were sacred in both regions (Ransome 1937, de Jong 1999a, Falcetti and Nates-Parra

2002). These apparent similarities in the approaches to bees could have served as a bridge between European and American worlds and, possibly, a vehicle for introducing Catholic beliefs and regulation into Indigenous worlds. However, interactions with bees were also subject to the dominion of Spaniards over life forms.

Catholic missions asked Indians for tributes of bee wax for indoctrination rituals, but as tributes were insufficient, the clergy introduced European Apis bees to meet wax

12 Sugar cane was processed into cane honey and panela (solidified raw sugar), in sugar rustic processing factories or trapiches. The process is intensive and involves the extraction and cooking of cane juice in large pots, and even today accidents affecting workers (cuts and skin burnt) are common.

34 domestic requirements (Ransome 1937). Thus, besides bringing African slaves, plants and livestock treated as tradable creatures, Spaniards also brought to the Americas their sacred bee, Apis mellifera, with their associated beekeeping practices.

The introduction and naturalization of the old-world honeybee in the Andes must have altered both bee communities and their relationships with humans. Apis mellifera is a highly competitive species that disrupts interactions between other bees and plants, inducing dietary shifts in native bees and modifying patterns of plant pollination (Giannini et al. 2015, Montero-Castaño et al. 2016). Apis also came to fill social roles important for people such as honey production. Besides being competitive, Apis is more conspicuous than stingless bees, which could have influenced how farmers noticed and interacted with other bees. Thus, the arrival of

Apis mellifera and its relationships plants, native bees and humans may have participated in the definition of trajectories of change in agricultural systems.13

After independence

Colombian independence in 1819 altered the dynamics of territorial appropriation.

The newly formed State expropriated land owned by colonists and used it as an asset to pay debts to former commanders and supporters of independence wars, and to attract private investors to build infrastructure. New large estates for agrarian

13 Besides the introduction of Apis, other human-driven events such as deforestation and the establishment of large crop and pasture areas must have influenced dispersal and nesting habits of many bees species, depending on their resource use and experience of the landscape (Kremen et al. 2007)

35 exploitation, haciendas, were rapidly established in Cundinamarca14 (Palacios 2011).

Uncultivated lands were occupied by both large-holders unofficially extending their properties, and by colonos looking for sites to make an independent life. Purchase and occupation of baldíos, or lands owned by the state, officially empty of people, were legalized with the passage of laws and fiscal policies from the late XIX century (Law

48 1882; 1873 and 1874 and 1902 fiscal codes), allowing landlords and landless peasants to legally occupy tierras incultas, or uncultured lands. Land ownership was legitimized through mejoras or interventions demonstrating human intervention, which usually consisted of deforestation and the establishment of pastures for cattle ranching or perennial crops such as coffee (Deas 1976, Márquez 2001), thus, nonhumans such as cows and shrubs helped demonstrate cultivation to the state.

These processes were similar to the agrarian reforms happening in Mexico (Esparza

1988) and Peru (Mayer 2009) during the XIX century.

The new institutional approach to the land introduced novel ways to experience, value and manage the national territory. As “improved” environments needed to be profitable and legible, diversified systems—viewed as unorganized and unproductive—should be disciplined regardless of the ecological ramifications. Mintz

(1986) described the appropriation of territories and the establishment of sugarcane plantations as simplified, ordered and controlled systems, sustained by regimented slave labor. The modern agricultural landscape also enforces socio-economic

14 By 1870 most lands surrounding the Country's capital were private. For a detailed description of Haciendas, see Deas (1976) and Forero Polo (2014).

36 priorities over both the land and the relationships between humans and more-than- humans, who should be known, organized, and managed to serve the human enterprise. Anolaima, as many other regions in the world, experienced these transforming territorial relationships aimed to maximize profits from the exploitation of the land and marginalized humans.

During the time of haciendas, economic activities to sustain the properties, extract natural resources and produce commodity crops were reflected in land uses extended across large areas. In the XX century, Anolaima comprised its current territory and the one of a neighbor municipality, Cachipay. The region was divided into several haciendas, whose sizes –and for many, names– correspond to present-day veredas15 or villages, including Santa Bárbara, Mátima, San Agustin, San Isidro, Calandayma,

Castañeda and Luchim[b]a, among others (Don A. Bermúdez, Doña L. Pulido, elder farmers. 2015. Oral history interviews). Economic activities included the massive exploitation of naturally grown quinine trees (Chinchona pubescens) for the treatment of fever and malaria, and the expansion of cattle ranching in the highlands, along with the introduction of exotic grasses such as the African pará (Brachiaria mutica) and

Indian pastures (Panicum maximum) (Estrada Herrera 2010). Within haciendas there were large-scale plantations of commodity crops16 such as tobacco (Nicotiana

15 Colombian municipalities are divided into veredas or villages. According to the Real Academy of Spanish Language, veredas refer to trails established for the passage of animals and people, which might have delimited former Haciendas. 16 For example, Castañeda was a large estate with several land uses including higuerilla ⁠ (Ricinus communis) one of the many plants with African origin brought to the Americas after the Spanish conquest, whose oil from the plant seeds was used as fuel for lamps. Other land uses included pastures for cattle ranching and horse keeping, and

37 tabacum) and indigo (Indigoffera suffriticosa), and also areas to produce staple crops17. During the XIX century, plantain (Musa sp.) and coffee (Coffea arabica) were brought from the north of the country (Palacios 2002b, Guhl 2008). Farmers remember hacienda Santa Librada was planted with wheat, barley, coffee and anise, and that Hacienda Santa Bárbara was well-known for its coffee exports.

The different social meanings of plants shaped agroecological designs and cycles of human activities, and also participated in the making of class relationships and of

“different forms of human politics” (Mathews 2017: 146). Reproducing the memories of their parents, farmers mentioned that cores of haciendas corresponded to cash-crop plantations exploited for landlords, where plant ecologies enabled the persistence of complex habitats, or their simplification. People mentioned that cereals were planted in unshaded areas, and coffee and anise were grown in the forest understory.

Convergent ecologies between crops growing in complex environments, and their economic meanings to people, attenuated deforestation and allowed Anolaima to maintain a dense forest cover, as described by Rivas (1972 [1899]) from his trip between Bogotá and the Magdalena Valley at the end of the XX century.

stockyards to temporary keep cattle transported from the eastern areas of the country (Casanare) to fluvial ports in the Magdalena River (Bernal, 1946). Haciendas Luchim[b]a and San Jerónimo, in the lowlands, were well-known for their large plantations of sugarcane and for their trapiches (Bernal, 1946; Velandia, 1979). 17 For a description of the Hacienda dynamics during times of Tobacco see Bejarano (1986), and for a description on quinine and indigo exploitation see Alarcon Alarcon & Arias Buitrago, (1987), Sastoque & Carolina (2011), Vargas Reyes (1850).

38 Plants participated in the definition of peasant workspaces and cycles. Farmers were asked to plant perennial crops such as coffee when they were cleaned more land in haciendas. While perennial crops developed, peasants shared that land to grow staples for self-consumption including manioc or corn. Once the perennial crop was mature, the family had to move to a different area to start the process again. Therefore, campesinos cleared and occupied the land following the planting cycles of commercial crops. Meanwhile, staple crops followed the campesinos as long as they did not interfere with crops representing source of wealth and prestige for landowners. Thus, fields comprising diverse and unmanaged staples would secure food for the landless, while commercially valuable fields, clean from the traces of laborers and their subsistence crops, reproduced the organized wealth of the landlord.

Social hierarchies in Anolaima were reflected in the different affiliations of peasants to the hacienda, in an extension of a colonial regime that conceived landowners at the top of the social hierarchy and peasants as humans embodying wild natures.

Landlords were typically absent and delegated command on foreman or capataces

(Segura 2015), who distributed tasks and had control over laborers. Peasants were jornaleros or paid laborers, renters, or aparceros/patijeros/patigüeros (sharecroppers) in haciendas (Palacios 2002a). Jornaleros depended completely on their wages.

Through aparcerías peasant families were granted a temporary place to clear the forest, live and cultivate staple crops, yet they also worked to grow cash crops for their landlord. However, when working in cash crops all workers experienced subjugation and labor exploitation. Rivas (1972 [1899]) described Anolaima as a land

39 of large agricultural fields full of corn, sugar and honey; and peasants as dirty and almost naked men working the land with their nails. Sons and daughters of Anolaima remembered their fathers never worked with their head crouched after being told that

"an eye and a whip were always on their necks", and that it was common that landlords’ maids and daughters of peasants were raped by foremen or landlords (Don

L. Silva, Doña L. Pulido, elder farmers. 2016. Oral history interviews). Hence, land ownership supported social hierarchies translated in landscapes of exploitation and abuse.

For many peasants, the only way out of the regime of haciendas was to set apart new land. When farmers tried to permanently settle in an area, they engaged into a different form of occupation where they moved to partially clear marginal lands.

Thus, in their oral histories, farmers remember they bought an estancia to live, and many purchased the corresponding land years later.

[T]hose were dreadful lands! We bought an estancia, as they called it in that time, which were mejoras (improvements). The terrain was not owned by my dad, only the improvements. Owners have sold to renters just the estancia, which consisted on the house and trees. Landlords charged each patijero family a tax or rent for the land. They also had to pay with one or two days of work [for free]. Owners had their land, and that is where they took all patijeros to work. Don Luis Segura, elder farmer. November 1 2016. Oral history interview.

Patijero livelihoods were highly dependent on the resource base. Their household possessions were modest and included rustic beds made with corn leaves, fogones or triangular arrangements of three stones and wood on which people put big pots to

40 make soups, and plain stones and lime to clean and prepare corn. Farmers cut moho, iguá and cedro trees and sold lumps of firewood to supplement their livelihoods.

Across oral stories, farmers remember how they grew manioc, plantain, arracacha de cepa o tarro (Arracacia xanthorrhiza), corn (Zea mais), squash (Cucurbita moschata), guatila (Sechium edule), vicente and garrapato beans (Phaseolus vulgaris), batata (sweet ) and batatilla (Convolvulus batata / Ipomoea batatas) in their estancias. They also harvested fruits, leaves and tubers growing in random areas including balú (Erythrina edulis), tomate de monte (wild tomato - Lycopersicum sp.), cidra (Citrus medica), poleo (Mentha arvensis), and maravilla or flor de un día

(Tigridia pavonia) bulbs (Don A. Bermúdez, Doña L. Pulido, elder farmers. 2016.

Oral history interviews).

While patijeros grew staple crops, they accessed animal protein by hunting carne de monte (game)18 and by growing hens and chickens, and engaged in different relationships with animals. Fishing was also part of people's livelihoods, especially during times of high river flow that coincided with fish oviposition, or subiendas, times when people changed the direction of the river towards temporary ponds. As mentioned by Doña Blanquita Martinez, an elder smallholder, “we disrupted the direction of the river to fish during subienda. After that, we returned the river to its

18 People mentioned they use to hunt big birds, and mammals such as faras (Didelphys marsupialis), rabbits, boruga (Agouti sp.), guatín, mortejos and carmos (Pecari tacuja). They mention many of these animals are not common anymore (Bohórquez 2015, Martinez 2015, Pulido 2015b, Vergel 2015). Regional Autonomous Corporations CAR, National Coffee Federation and other institutions have conducted campaigns with people to reduce game consumption in the region.

41 former state and we left it alone. Now we cannot do it. There are no fishes anymore".

While people fished, collected water, or foraged michu (Sapindus saponaria) fruits to use as soap to wash clothes, they ran into tigrillos (Leopardus tigrinus), babillas

(Caiman crocodilus fuscus), turtles and other animals in the forest. Many farmers also had close relationships with stingless bees, keeping them in pots and cocos (totumo and Lagenaria gourds) and using bee honey as eye-medicine (Doña L. Pulido, Doña

B. Moreno, elder farmers. 2016. Oral history interviews). Thus, peasants greatly relied on subsistence production and on their floral and faunal ecological knowledge.

Accounts of the economic transformations in the hacienda system and their impact of agricultural production and landscape configuration help us understand the influence of land use change on nonhumans. For bees, some land uses in haciendas brought both food abundance and challenges, as large- scale plantations had crops that underwent mass-flowering, but also represented deforestation. Indigo plants, which flower although the year, must have been attractive to leaf-cutter bees.19 Flowers and extra-floral nectar of higuerilla20 and of other plants grown by aparceros including guatila (Sechium edule), squash and basil represented important resources for other bees. However, bees restricted to forest areas must have been impacted by the high

19 Leaf-cutter bees use Fabaceae plants in the region (pers. Obs.). This botanic family includes indigo, and bee visits to this plant are reflected in the specific epithet of the bee Megachile indigoferae found in the Madgalena Valley and described by Mitchell during the 1930s (Camargo et al. 2007). 20 This plant is visited by stingless bees and Apis honeybees in Brazil. Besides nectar, the plant produces pollen that is toxic for bees. Stingless bees do not consume it but Apis bees do (Freitas 2009, Junior et al. 2011).

42 rates of local deforestation,21 and the establishment of pastures could have reduced ground cover of bare soils, used as nesting substrate by many bee species.

Despite the abundance of Anolaiman lands, the intersection between population growth and unequal access to the land resulted in a sense of poverty and marginality for peasants. People remember families used to be large (>10 people) and small estancias were insufficient to provide enough –and diverse–food for everyone.

Peasants secured foods by bartering among villages, and food gifts were common

(Doña B. Martinez, elder farmer. 2016. Oral history interview), consolidating a local moral economy in which, as Scott would argue (Scott 1977: 26-27, 162), social ties were as important as money. Cash, when obtained, did not necessarily represent well- being for peasant families, as this interview quote highlights:

Today, youth lives in glory. [In the past] people worked for food and annual clothing, and it was frequently not enough. The issue is that most of [the money that] arrived home turned into chicha22 for the male. Doña Elvirita Molina, elder Anolaiman. May 1 2016. Oral history interview.

The experience of the land and the economic life of haciendas changed with the opening of new roads that connected people with modern commerce. During the second half of the XIX century, farmers and merchants traversed regions in horses or

21 Many bee species nest in wood, and obtain food –nectar, pollen, oils and sap– from flowering trees, or use honeydew from herbivores associated to trees (Oda et al. 2014). However, bees differ considerably in resource requirement and use of space. Thus, while many bee species are restricted to forested areas (Brosi et al. 2007), others use open spaces. Thus, some bees could have learned to use large spaces open by humans and spread across the region, as happens today, while other could have faced negative effects on population size. 22 Fermented beverage made with corn

43 mules through horse trails. Around 1850 many roads were established to connect the capital city with ports along the Magdalena river (Velandia 1979).23 Labor requirements for building infrastructure attracted peasants and other migrants who were offered state lands in exchange for labor (Estrada Herrera 2010). This brought deforestation and further expansion of the agricultural frontier, a demographic increase in the region, and opportunities for peasants to create different livelihoods.

These processes met an economic deadlock of coffee haciendas during the 1930s that resulted from reduced demand for hacienda export products associated with the global economic crisis of the great depression. Bankrupted latinfundistas, or large estate owners, did not meet their obligations with farmers, who engaged in major revolts during the following decades that resulted in two attempts at agrarian reforms

(Bonelo 2016).

23 Roads connecting Bogotá with La Mesa and Cambao, the closest markets where people exchanged products de tierra caliente and fría (from warm and temperate regions), passed by Anolaima. The town was also connected to the city through a train station in , included in the train line connecting Facatativa and La Mesa-Girardot after 1910 (Bernal 1946).

44 Violence and the problem of the land in Colombia

Rebellions demanding rights for the people and access to land have been common in the . Peasant insurrections between the 1930s and 1940s merged with a cruel period of bipartisan violence known as La Violencia (1948 -

1957) and later, the guerrilla violence (1960-2017) (Fajardo 2002, 2014). Each conflict emerged from agrarian struggles and was traversed by the promise of agrarian reforms to redistribute baldíos (Law 200 1936 and Law 135 1961)

(Fajardo 2010).

The 1930s economic crisis was strongly felt in Cundinamarca and catalyzed the organization of ligas campesinas or peasant leagues, whose revolts led to agrarian reform in 1936. This forced large holders to sell part of their haciendas at low prices to peasants in a process known as parcelización. After the assassination of the liberal and populist leader Jorge Eliécer Gaitán, the period La Violencia started and appeared in Cundinamarca with bipartisan persecutions. Farmers in Anolaima remember this period as a conflict related to their landlords, as peasants’ political affiliation depended on that of their patron. Liberals and conservatives disputed over control of different villages through force: while La Florida was a region of

Conservatives, the rest of the municipality was a Liberal area. This bipartisan violence resulted in the abandonment of some haciendas during the 1940s, and in the immigration of many people escaping from political persecution in Tolima,

45 Santander and Boyacá (Doña L. Pulido, Doña E. Molina, Don P. Muñoz, elder farmers. 2015. Oral history interviews) .

La Violencia declined with the formation of a regime of shared power between

Liberals and Conservatives between 1958 and 1974 called Frente Nacional.24

Revolts were tamed with a 1961 agrarian reform, partially executed and supported by the US war against communism. By 1972 the reform had benefited 7% of the

800,000 landless peasants asking for legalization land tittles. During that year, large landowners feeling at risk made an agreement with the Colombian government, El

Pacto de Chicoral (Chicoral agreement) (Bushnell 1993). This agrarian counter- reform established the 4th 1973 and 6th 1975 laws, which protected former large- estate occupants from expropriation of land ownership and re-distribution, and gave major incentives to mechanized agriculture (Fajardo 2002). To compensate for the failure of the 1961 agrarian reform, the government engaged in a series of rural development programs, mostly unsuccessful (Kalmanovitz 2011).

The need for land redistribution has nominally influenced official governmental discourses on land distribution, despite failed attempts to execute agrarian reforms.

The Colombian government defined a unit to define land redistribution in an agrarian reform program.⁠ Family agricultural units (Unidad Agrícola Familiar

24 In 1953 there was a power strike by Gustavo Rojas Pinilla, who declared a military dictatorship after a period in which conservatives were in power. Rojas Pinilla was forced to renounce in 1957, opening a 12 years amnesty between liberals and conservatives, after which democracy returned to the country (Bushnell 1993).

46 UAF) have been defined as "a basic agripecuarian enterprise designed according to local agroecological conditions and appropriate technologies, whose extension should allow families to earn fair incomes for on-farm job and surpluses that add to the accumulation of their belongings" (Gutiérrez et al. 2014). UAF sizes vary across the national territory, depending on the primary productivity of the lands.

For the Tequendama bioregion containing Anolaima, viable UAF ranges between five and ten hectares. Current average farm size in Anolaima is 1.5 hectares.

Currently, traditional family farming is still the predominant production system in

Colombia and includes more than 2,804,714 rural households. However, 70.4% of them have access to less than 5 hectares and occupy 2.0% of rural area, while 0.2% of agricultural units are larger than 1000 hectares and occupy 73.8% of rural area

(DANE 2016). Most large farms are devoted to cattle ranching, representing simplified and hostile landscapes for many organisms.

Peasants in Anolaima benefited from the 1930s and 1960s waves of parcelization, resulting from the breakup of haciendas. During the 1930s many landowners declared bankruptcy and sold their properties in pieces to former aparceros, who became wage laborers of the now smaller haciendas. Further land titling during the 1960s favored people native to Anolaima but also migrants escaping from the 1940s violence in other Colombian regions (Don P. Muñoz, elder farmer. 2015. Oral history interview).

Land distribution problems were partially solved after these two waves of agrarian reform. While land access gave peasants the opportunity to secure food consumption

47 and freedom to create meaningful livelihoods, public services, roads, hospitals and schools were facilitated by an alternative institution: the National Coffee Federation.

Coffee and land use change in Anolaima

Colombia has had a long tradition as a major coffee exporter. This crop entered the country through the north-east region (Santander), arrived in Cundinamarca by 1870s, and spread to other municipalities during the XX century (Palacios 2002a). Coffee plants are woody shrubs resistant to diverse environmental conditions that root deep into the soil and do well in steep slopes, being ideal for the colonization of marginal lands. Coffee represented wealth and progress, and was also a symbol of capitalization: beans can be traded wet or dried anytime, serving as a store of value.

The importance of the crop peaked during the 1970s, accounting for more than 50% of the total Colombian exports; this dominance greatly decreased after the 1990s

(Banco de la República 2002, Palacios 2002). Currently, coffee represents only 7.2% of the total Colombian exports, but still supports more than 500.000 rural livelihoods.

Coffee initially represented a business for urban entrepreneurs, yet it rapidly became a symbol of freedom for smallholders. Coffee arrived in large Haciendas in

Cundinamarca as a crop with high labor requirements met by peasants, and was later commercialized in the cities with the intermediacy of foreign merchants. Landlords and peasants shared-crop staple foods, yet peasants were restricted from coffee yields

48 and profits25 (Palacios 2002). While large landholders retained labor to harvest coffee, workers sought a piece of land of their own and the freedom it would provide.

When the State adopted evidence of productive use and investment as a means of acquiring legal title to lands, coffee represented an ideal crop to attain both land ownership and social freedom. If smallholders had rights over coffee plants, they would be free from the social contract shared with their landlords. This could reverse power relationships, as large estate owners still depended on peasant labor to amass wealth. Thus, as peasants escaped haciendas and took advantage of agrarian reforms that enabled them to own land, they incorporated coffee into livelihoods and became connected to international markets by the mid XX century (Palacios 1980, Guhl

2008).

Coffee exports brought stability to the overall Colombian economy during the XX century, facilitated by the efforts of the National Coffee Federation (NCF), a private initiative supported by the Colombian government. NCF was created in 1927 to uphold coffee producers (Palacios 1980). It aimed to modernize the coffee sector in

Colombia by improving commercialization and increasing the productivity, quality and efficiency of coffee production (Hough 2010). The NCF developed strategies to internally compete with prices offered by foreign merchants, who were the main traders of Colombian coffee at the time, and focused on the social stability of coffee

25 Improvements related to the maintenance of perennial crops or pastures. Proving maintenance of mejoras over at least 25 years would confer legal titling of the land. Thus, coffee could grant smallholders property rights over the land. That was one of the main reasons to forbid peasants to grow perennial crops.

49 producers. NCF strategies included organizing growers around a National Coffee

Fund to stabilize local coffee markets, offering price floors on purchase prices that secured minimum wages for smallholders, and providing social services such as education, health, roads and infrastructure for local communities. Many of these interventions improved conditions for coffee growers, who were better off than peasants working in other sub-sectors of the agricultural economy such as sugar, fruits or flowers (Palacios 1980).

Coffee prices are closely associated with global market dynamics and prone to volatility, thus one of the main NCF goals was to promote price stability and profitability through commercial agreements. In 1940, Colombia and Brazil signed an

Inter-American agreement to partition coffee supply to the US. When countries entered an economic bonanza after World War II and demand for coffee increased, the first world coffee exporters were Brazil and Colombia26. At the end of the 1950s these two countries promoted the negotiation of an International Coffee Agreement

(ICA) to stabilize prices. During that decade, the NCF featured a niche market for

Colombian coffee based on its high quality (as opposed to high volumes), to increase demand for this coffee and protect it from market instability. In 1962, the Kennedy administration agreed to sign the ICA, involving a quota system to regulate coffee

26 The dynamics of Brazilian coffee economies greatly favored other coffee producer countries such as Colombia and Mexico. For a detailed description of the Colombian case, see Palacios 2002.

50 prices and help stabilize rural livelihoods, which would reduce chances of revolts in

Latin America27 (Bates 1997).

Coffee shrubs and their ecologies greatly influenced landscapes and rural livelihoods in Anolaima. Coffee crops were grown under the forest canopy and consisted of typica and borbon varieties of Coffea arabica, a plant species yielding beans with soft and aromatic flavor28. Coffee shrubs started to be productive after five years, reaching a peak of production ten years later and drastically declining after 20 years. Bushes were also tall and required children seated on their parents' shoulders to pick beans and dense shade for sun protection. To regulate shade, people cut trees –without completely clearing the forest– in some areas, while planting trees in former pastures

(Don A. Bermúdez, elder farmer. 2016. Oral history interview). As was the case also in the Dominican Republic (Rocheleau et al. 2001) and Mexico (Vallejo et al. 2015) in Mexico, the cultural modification of landscapes did not necessarily degrade the environment but promoted higher biological diversity and presumably robust biocultural memories.

27 Initially, the idea of an international agreement was not supported by the United States, the main coffee importer (Palacios, 2002). When the Cuban revolution exploded in 1959, it represented the spread of communism into Nations serving the modernist project of the US. In light of the cold war, the US engaged into several agreements to counteract the spread of communism ideologies in Latin America, which included the ICA, the Alliance for Progress, and the facilitation of a Colombian agrarian reform in 1961 (Hough, 2010). 28 Other coffee producer countries grow Coffea canephora syn. robusta, which yields beans with low acidity and high bitterness sold at lower prices than C. arabica. C. canephora beans are used as filler in ground coffee blends.

51 Shaded coffee as a refuge for tropical biodiversity

The ecological benefits of the resemblance between coffee agroforests with complex vegetational structure and undisturbed forests have been frequently highlighted (Perfecto 1996, Pineda et al. 2005, Komar 2006, Bhagwat et al. 2008,

Philpott et al. 2008a, Philpott et al. 2008b, Philpott et al. 2009). Diverse composition and complex vegetational structure allow organisms to freely disperse across sites offering diverse resources, and to engage into complex ecological interactions that translate in the self-regulation of the agricultural-forest coupled system. These self-regulatory properties reflected in the control of coffee berry borer by ants, birds and bats (Vandermeer et al. 2009, Vandermeer et al. 2010,

Karp et al. 2013); the regulation of coffee diseases including the rust by other fungi species (Vandermeer et al. 2009, Jackson et al. 2012); and the cross-pollination of coffee plants, translated into higher yields (Klein et al. 2003, Ricketts 2004).

Coffee shade is also associated to lower vulnerability to biophysical catastrophes such as hurricanes (Philpott et al. 2008b), and higher resilience to climatic shocks

(Lin 2007). The self-regulatory functions of these systems also depend on the landscape context. The structural complexity of surrounding areas limits the probabilities of pest and disease outbreaks (Avelino et al. 2006, Avelino et al.

2012), and differentially influence ecological functions in coffee plantations

(Ricketts et al. 2004, Saturni et al. 2016).

52 Before the 1950s, coffee was managed as what is considered today a rustic plantation

(Toledo and Moguel 2012). Coffee bushes were not pruned and shaded with trees such as cucharos (Clusia sp.), cauchos (Ficus sp.), dinde (Chlorophora tinctoria), matarratón (Gliricidia sepium), guásimo (Guazuma umfolia), caracolí (Anacardium excelsum), totumo (Crescentia cujente), chiraco (Toxicodendron striatum), gualanday

(Jacaranda mimosifolia), amarillo (Aiouea dubia), arrayán (Myrcianthers leucoxyla), iguá (Albizia guachapele), comulá (Aspidosperma polyneuron) and cedro (Cedrela montana).29 Besides trees, other crops accompanied the productive cycle of coffee to secure livelihoods. Staple crops included squash, beans, yuca, guatila and corn; and wild herbs used as human medicine and for local preparations included chipaca

(Bidens pillosa), tabaquillo (Polymnia riparia), Emilia (Emilia sp.), escobo

(Buettneria mollis and Sida rhambifalia), carretón (Triumfetta bogotens and T. mollissima), and verbena (Starchytarpheta sp.). Besides providing for their utility for humans, these plants also represented food and nests for bees, such as the petals of pate' chulo (Anoda hastata) and leaves of ortiga (Urtica sp), plants used as human medicine and as materials used by megachilid bees to build cocoons in which they live (Observation. July 23, 2016).

Local management of coffee crops has been closely associated with the macro dynamics of the coffee economy. In the 1960s, a coffee rust outbreak affected thousands of coffee plants and peasant livelihoods in Brazil and Central America; this

29 For a beautiful description of trees growing in Anolaima during the 1950s, see Daniel (1956).

53 reduced coffee global supply and benefited Colombian markets30. The rust, however, was an incoming threat for Colombian coffee. To avert a production crisis, Cenicafé, the NCF research institute, developed a new production system that included improved coffee strains resistant to the rust, Caturra; an increase in planting density of coffee shrubs; regulation and progressive reduction of shade trees; systematic use of synthetic inputs; contour farming; and scheduled crop renovation (Machado 1977).

The new system was capital- and labor-intensive. Despite NCF offers for subsidies, only middle sized and large coffee producers could afford it (Palacios 2002a). The coffee rust finally arrived in Colombia and devastated crops in Anolaima between

1965 and 1978 (Don O. Sissa, elder merchant. 2016. Oral history interview).

After the 1970s crisis, coffee farmers in Anolaima transformed their land to take advantage of an incoming bonanza. Because of its success, the area in planted in coffee across Colombia increased considerably (Guhl 2004), and was accompanied by a re-making of coffee landscapes with the new system of coffee production. The system involved the replacement of old Arabica coffee shrubs with Caturra, followed by Colombia and Castilla strains, which according to farmers have higher fertilization requirements and lower bean size. While in other areas of Colombia coffee shade was completely eliminated, unshaded coffee plantations do not work well in Anolaima, as told by a farmer who found coffee shrubs and soils "got burnt" after eliminating tree shade in his field. Thus, the NCF suggested that farmers replace native trees of dense

30 Landscape simplification could have facilitated the fast dispersal of the coffee rust in several regions such as Brazil.

54 crowns with species of thinner and higher crowns such as guamo rosalio or copero

(Inga spectabilis), cola 'e mico (I. edulis parvidolia) and rosario (I. laurina), mulche

(Albizia carbonaria) and moho or nogal cafetero (Cordia aliodora) native to

Colombia or northern Latin America, and also urapán (Fraxinus chinensis), a prolific species native to Asia (Doña L. Pulido, Doña B. Martinez, Don A. Bermúdez, elder farmers. 2015. Oral history interviews). Thus, a new wave of land use change, this time driven by smallholders, transformed Anolaima after the 1970s.

Changes in coffee landscapes reflected, once again, how the dream of economic prosperity overshadowed the socio-ecological stability of complex agricultural systems. The simplification of coffee agroforests brought a progressive transformation from subsistence towards commercial crop production and thus, important changes in local economies –and hence, ecologies. In Anolaima, collective stories recall that many smallholders eliminated homegardens and dedicated all of their energy, time, and knowledge to coffee production. Food could be purchased with coffee income, which generated a progressive transformation of diets. Farmers were no longer depending on their diverse subsistence crops–and their knowledge to grow them– to fulfill food needs; they now relied on a single crop. During those times coffee provided for a good life, apparently paying the cost of the negative impacts on wildlife and the constant concern about over-specialization. By the 1990s livelihoods were closely dependent on the global dynamics of coffee markets.

Bees and coffee

55 Besides major changes in plant communities, the NCF also promoted changes in the communities of other organisms such as bees. When Spaniards brought honeybees

(Apis mellifera), the clergy took care of them in the Americas31. In Colombia, Apis beekeeping became popularized in the XX century through governmental programs that imported bee queens from different European strains and fostered the modernization of beekeeping during the 1960s (Santamaría 2009).32 The National

Coffee Federation engaged in this initiative and incorporated beekeeping to support livelihood diversification during the 1970s, bringing honeybees to different coffee- growing regions including the Tequendama province and hence, Anolaima. The NFC developed several beekeeping workshops, to which men and some "rebel women" attended, and distributed equipment among farmers.33 Most caficultores (coffee growers) kept honeybee hives near their houses and some farmers specialized their livelihoods to trade bee-related products. During that time, Anolaima was the third producer of both coffee and honey in Cundinamarca.

31 By the end of the XIX century honeybee keeping was established as a practice in Colombia with the work of the Salesian priest Remigio Rizzardi, whose contributions were published as first manual on rational honeybee keeping in 1910. 32 The National government supported the spread of this activity through the Ministry of Economy by the 1940s, and then through a beekeeping division nested in the Animal Industrial Office of the Ministry of Agriculture (Santamaría 2009). 33 Workshops were conducted in Chinchina, headquarters of Cenicafé. Doña Irené de Vega, wife of a beekeepers couple, said only rebels like her went to such training. Farmers mentioned that, during the workshops, producers where taught about the exploitation of bee products, including the production of industrial "flavorized" honey. This meant, feeding bees with juice extracts of different fruit pulps and harvesting the resulting honey, a practice that today is considered honey falsification (Angarita 2016).

56 Bees communities in Anolaiman landscapes must have changed with the introduction of Apis mellifera, and with the transformations of coffee production systems. Diverse flowering plant communities with long histories of interaction typically have asynchronous flowering seasons in the tropics (Borchert 1983). Changes in flowering tree species suggested by the NCF could have influenced bee diversity in different ways. For example, the narrower pool of tree species grown in modern coffee agroforests appears to have staggered floral episodes, meaning less food diversity and aggregated food availability in time for bees and other pollinators (Fisher et al. 2017).

This would force bees to look for novel foods during times of lean –flowering– months. Also, the reduction of tree shade must have diminished the availability of nesting sites for many social and solitary bees.

An Africanized honeybee strain spread in Latin America after its accidental release in

Brazil in 1957. Farmers remember Africanized bees arrived in Anolaima by the end of the 1980s (Doña B. Moreno, Doña B. Martinez, Don V. Gamba, elder farmers.

2016. Oral history interviews). These honeybees are thought to defy domestication: they abscond more frequently than European strains, their defensive behavior is more unpredictable, and their alarm system usually includes human actions as triggers for aggressiveness. Africanized bees were involved in many fatal incidents involving humans, cattle and poultry, and in reprisal people burnt many swarms. Most people abandoned beekeeping and faced both the loss of their colonies to Africanized hybridization and damages caused by bees. Most of the governmental and NCF

57 support for the activity ended and beekeeping become stigmatized and after this, coffee growing divorced beekeeping in the region.

Belonging to the same exotic species, European and Africanized honeybees represent two different historical paths of relationships with farmers in Anolaima. European honeybee strains occupied Anolaima for several human generations and came to dominate the Figure of "beeness." These honeybees brought modernization and sense of domestication, control and companionship to beekeepers, yet their Africanized counterparts meant rebelliousness and threat. Most people reject Africanized bees and talk about European honeybees with nostalgia, while non-beekeepers consider this aggressive bee as a hazard to be controlled and avoided. Current inhabitants consider the European bee to be native, frequently calling it the Royal, native or true bee, while Africanized bees are extranjeras, foreigner bees. These names account for how colonization involved changes in fauna, and also show that names and meanings emerged from the way bees are recognized and acknowledged as companions after their different encounters with farmers in this region.

Apis beekeeping as an economic activity lost importance with time. After the

Africanization of this bee, keepers adjusted practices including the use of equipment.

However, they could not manage or retain the high number of hives they did when keeping European Apis strains. According to his son, Don Julio Luna used to keep up to 350 beehives in his farm about fifty years ago and based his livelihood on honey production; he was left with 15 hives (J. Luna, 2015. Beekeeper. Interview).

58 Likewise, another prominent beekeeper kept 26 hives twenty years ago, but in 2010 only six of those beehives remained occupied (F. and V. Gamba, 2016. Beekeepers.

Interview) . The Africanization, along with other environmental pressures including the globalization of parasites, affected Apis bees. In the late 1990s beekeepers imported European honeybee queens to reverse the hybridization pattern of the

Africanized bee. The attempt to re-engineer the biological makeup of the species did not work. Beekeepers asserted that the varroa mite (Varroa destructor), a parasite feeding from the hemolymph of larvae and adult bees, arrived with queen imports impairing many of the hives kept in Anolaima. New threats for bees and their keeping involve the increased use of synthetic biocides and landscape simplification, especially of coffee agroforests (L. Casallas, A. Hernández, J. Luna, 2015.

Beekeepers. Interviews).

Coffee decay

Concurrent to the declines of beekeeping, the coffee boom ended by the 1990s and with it, the stability for coffee producers in Anolaima. In 1989 the ICA quota system was eliminated and since then, coffee prices have been completely defined by supply- demand dynamics, cascading in a coffee crisis that affected several coffee producing countries across the world (Bacon et al. 2008, Watson and Achinelli 2008).34

Colombia did not perceive the crisis immediately, as one major producer, Brazil,

34 Changes in the International Coffee Agreement started with a switch in the US political strategies towards Latin America and the world market in the presidency of Ronald Reagan (1981). The entrance on the neo-liberal regime also affected international agreements involving other commodities, including copper.

59 suffered severe frosts in 1994 that increased global demand from other coffee producer countries. However, once Brazilian coffee production recovered and new producers including Vietnam entered the coffee market, a wave of coffee oversupply brought coffee prices down during the 2000s. This coincided with a coffee berry borer outbreak in Anolaima, severely affecting local coffee economies. Global coffee prices increased in the 2010s, yet this trend coincided with an extreme rainy season in

Anolaima and the loss of the coffee harvest (Doña L. Pulido, elder farmer. 2015. Oral history interview). After these upheavals, many farmers abandoned coffee to establish pastures and alternative crops, or, conversely, sold their land (Don O. Sissa, elder merchant. 2016. Oral history interview).

The story of coffee growers resembles what happened with the establishment of commodities in other regions of the world. Before the specialization in one single commodity, smallholders secured livelihood stability by consuming and trading surpluses of staple crops in local and regional markets. The dependence on one single commodity –and the political economy of its trade–transformed local agricultural risk, spread into diverse crops, into risk to market and financial instability, difficult to spread or negotiate (Dove 1983, Dove 2011).

After promoting increases in productivity through technological packages involving the simplification of plant diversity, the NCF has publicly recognized the value of biodiversity and is recreating elements from the past to design new strategies for the sustainability of coffee production in the country. The institution has promoted bio-

60 diversity friendly or specialty production schemes during the last fifteen years, coinciding with the last coffee berry borer outbreak and the prolonged coffee crisis

(Botero et al. 2014). However, official programs offering a price advantage for these systems do not pay enough. In Anolaima, the local NCF committee supported

Rainforest Alliance and 4C certification schemes, granting a 8000 COP premium price per carga (~1.2% of the total value of a 125 kg of coffee, paid at about 200

USD or 600000 COP during the main harvest season of the region in 2015) (Doña B.

Martinez, C. Murcia, 2015. Coffee growers. Oral history interview). The NCF is recognizing the robustness of traditional systems and now recommends diversifying coffee agroecosystems with productive shade trees, planting home gardens as a strategy to reduce household vulnerability to market fluctuations, and using cover crops to increase resilience to climate change.

Farmers, closely attached to the coffee culture, still grow this crop despite its high labor needs and low profitability. While this loyalty involves the relative stability of a crop that can be stored and purchased at any time (Cristancho 2015, Piñeres 2015,

Vargas 2015), the persistence of coffee in Anolaima has to do with the NCF. Coffee exemplifies how institutional power can influence ecological dynamics, relationships between humans and more-than-humans, trade, livelihoods and landscapes. In this case, coffee power was not only exerted through an organization working remotely but through continuous practices that reinforced social relationships with both local and global spheres. The NCF displayed their presence through the continuous offering of technical assistance, courses including rural finances and human nursery;

61 and promoted political participation among coffee growers to select regional and national representatives to NFC committees. The institution also promotes participatory initiatives such as grupos de amistad (friendship groups) in which farmers share experiences and discuss guidelines offered by the local NCF committee. These interventions have sown a sense of belonging among farmers, which translate in their loyalty to both the NCF and the crop. While the institution guidelines have negatively impacted people's livelihoods and food autonomy, the social meanings of coffee combined with the particular shade requirements of coffee shrubs in Anolaima have supported the local persistence of coffee agroforests, considered to be important refugees of tropical biodiversity.

Transforming agri-food territories and the project of modernization

"When I grew food, what worked at the moment were tomatoes and green beans.

They used to give good yields, but then pesticides arrived. After all the drugs one

puts on plants, flowers get weak. They fell easily. Plants no longer produced the

same. [ ] I tell you the truth. When my dad grew food, when I was a little child, we

did not even use wood or strings. We threw peas on the land. We had to barbechar35

and then put water on plants, just that. We did not buy fertilizer, pesticides or

fungicides. Nothing. My dad only asked us to scare birds away. That was our task:

to scare birds away and forbid them to eat everything, because they were bad! I

remember that, when we had cows, we had to pick all the manure up and we used

35 Land fallowing

62 that on plants. We did not purchase anything. The farm produced all fertilizer. When

trees were rotten, we took them and used them on crops. That is why old people had

money, because they did not spend a penny. My dad bought his land plot by plot.

Plots had small bahareque36 houses, all made of mud. Every year, my dad bought a

plot.

When he started using agrochemicals, my dad stopped buying land. He could no

longer afford it. So, most people bought what they could when it was possible to

make money. Now people need to use drugs (on plants) because otherwise they

would get nothing. That is how science goes against itself. After all studies people

do, the world is going to end up on fire, or who knows on what".

Don José López, May 11 2015. Farmer. Oral history interview.

Many parts of the Global North went through a major reconstruction after the Second

World War and started walking the path of economic growth (Rostow 1960).

Modernity and the emergence of development discourses met the creation of a Third

World, regions that did not have anything to offer but raw materials and cheap labor, and that needed to be to be saved from backwardness and tradition to be compatible with the discursive ladder of progress (Escobar 2009). The Alliance for Progress

(AFP) was a US-sponsored reconstruction program for Latin America, which brought donations, loans and rules to create an environment for accelerated economic growth

36 Infrastructure built with woven sticks and canes, covered by mud.

63 and political stability, and to counteract the spread of communist movements after the

Cuban revolution (Rojas 2010). In rural Colombia the AFP agenda included an agrarian reform and interventions to encourage technified agriculture compatible with neoliberal market dynamics. Modernization plans required both changes in land use and the social engineering of farmers.

External interventions and the Green Revolution

Socio-cultural, ecologic and economic conditions in Colombian agriculture are heterogeneous and required tailored interventions to establish the idea of modernization. During the 1960s, the majority of the Colombian population was rural. Many households engaged in both subsistence and commercial activities based in ecological rationalities in which on-farm diversity and traditional, situated ecological knowledge were essential for the self-regulation and problem solving in agroecosystems and households (Toledo 1989, Alvarez 2001). For a modern agriculture to take hold, these ecological rationalities needed to be replaced by a scalable system–made of elements that do not relate with others and that can be extended without transformation–compatible with capitalistic rationalities. The US

Agricultural International Development Agency USAID targeted programs for peasants, prioritized because of their tendency to engage in social protest, but who represented a challenge for the establishment of large-scale systems because of their limited access to capital and land (Rojas 2010)37. USAID worked through projects

37 Different external agencies focused in particular segments of Colombian agriculture. Interventions for large estate owners were conveyed by the Colombia Program, leaded by the

64 linking central and regional institutions to promote modern agriculture, supporting the creation of the Colombian Agropecuarian Institute (ICA) in 1963 to accompany the

1961 agrarian reform.38

The Green Revolution arrived in Anolaima during the 1970s with extension agents advertising agricultural designs, management strategies and agrochemical formulas to rapidly increase yields and exert total control over crops. The goal of the strategy was to technify and increase the production of cheap staples including , tomato, peas and potato for the commercialization in domestic markets (Fajardo 2014). Having access to enough capital, large holders were the first to engage in this new system.

Seeing high increases in yields, the use of synthetic agrochemicals snowballed after many people found in short-cycle crops such as tomato and peas a way to amass capital. During those times land was traded at low prices in Anolaima, and many people used revenues from agroindustrial production to buy and enlarge their properties (López 2015, Díaz 2016).

Green revolution technologies brought important disequilibria in Anolaima and in other parts of the world (Yapa 1993, Gan 2017).The popularity of technified short- cycle crops decreased after several producers lost crops to frost and uncontrollable

World Bank for rural development in Latin America, and by the Inter-American Development Bank. Both institutions focused on bringing cutting edge agricultural technologies that could be implemented in large operations. 38 US missions Rockefeller, Nebraska, Michigan and Kellogg promoted Green Revolution technologies and knowledge in Colombia during the 1950s. Such missions were part of an agreement with the Ministry of Agriculture and included modifications in the curriculum for agronomy university programs. For details, see Arango Marín (2005).

65 pests, or started having health issues (Martinez 2015, Segura 2015). Farmers called synthetic agrochemicals "drogas" or remedies and said that "with every new agronomist it came a new remedy, and with each remedy a new pest" (Don J. López,

2015. Farmer. Oral history interview). Farmers complained that extension agents and resellers did not have knowledge about the land, and were concerned about the ecological disruption triggered by agrochemicals. Typically, one biocide targets a restricted group of organisms. During the 1970s, few products existed to control herbivores and fungi, and the rate with which new biocides appeared on the market targeting specific pests or diseases was low. According to the owner of Agropuntico, an agrochemical retail store in Anolaima, farmers started experimenting with mixtures of products for crop protection, and as the use of biocides was not regulated, they engaged in the vicious cycle of agrochemical use, unraveling the ecological functionality of traditional agroecosystems and falling in the perpetual dependence on external inputs.

The uniformity and simplification of the monocultural agroindustrial project overlooks how agricultural fields are complex socio-ecological systems that, following Tsing (2012), are non-scalable but unique, responsive and transformative.

In the search for scalability, agroindustries create non-relational environments that need to be ordered and controlled to only depend on human action, not on self- regulatory processes and relationships. In these environments, biological diversity is undermined, and peasant knowledge, skills and labor are replaced with modern technological fixes that cannot respond to the indeterminacy of living systems. The

66 search for scalability does not only involve the reduction of biodiversity, it also enforces a change of identity in the actors managing agroecosystems. While peasants are expected to embody narratives of sustained resource use and productive compatibility with the environment in what Tsing calls "the allegory of the peasant"

(Tsing 2003), agroindustrial technologies make smallholders into extractivist entrepreneurs that are predators of the environment. The paradigm shift entails control of land to maximize profits and recover investment costs, lowering tolerance thresholds associated to risk of crop failure and converting encounters with unmanaged nonhumans into a threat. Meanwhile, by hiding the costs of uniformity, simplification and intensification, modernization undermines the persistence of peasants.

At the end of the XX century, the world economy, including Colombia, turned into neoliberalism and globalization. In 1991 the country developed a program to liberalize and modernize the national economy (CONPES 2465). Agriculture was focused on large-scale agroexport operations involving a deepening of liberalization, invigoration of land markets and major fiscal incentives to large-scale agricultural operations. Along with these measures, the country engaged into several free trade agreements –many of them asymmetric–with Canada, European countries and the US

(Garay 2011). With free trade agreements, food imports increased considerably.

While in 1989 Colombia was self-sufficient in the production of fruits and vegetables, and the production of cereals for local consumption was over 80%, by the 2000s

Colombia imported about 50% of food for domestic consumption (Fajardo 2014).

67 Most programs for rural development and promotion of small-scale family agriculture were drastically reduced, and under unequal conditions, smallholders were forced to compete with the disproportionate availability of imported cheap foods (Machado

2003). The sufficiency in food production was dramatically altered and worsened, and neglect for traditional small-scale family agriculture aggravated old conflicts in rural areas, encouraging activities of insurgent groups and their battles across the country (Fajardo 2014).

Figure 2. Modern crop of tomatoes in La Laguna village, Anolaima, March 2016. This 3-ha field is sprayed twice a week with a mixture of pesticides. Photo by the author.

68 External interventions to fulfill the promises of economic growth and materialize development –and underdevelopment– discourses changed focus to convert peasants into rural entrepreneurs. New policies promoted certification schemes and productive projects to prompt the conversion of agrifood territories into ordered, business- oriented and highly efficient farms through technological packages, accounting books and acumen to deal with transaction costs (Chaparro 2013). Contemporary discourses on efficiency, however, involve a perfect balance between the sustainability of antiguos (elder farmers) and the dynamism of entrepreneurs (Tsing 2003). This denotes a schizophrenic and frustrated desire for farmers to be magically tuned with modernity while conserving the competences and wellness of the past. Aiming to achieve this goal, the Ministry of Agriculture has supported projects in Anolaima to technify guava and citrus plantations, or to introduce new crops –and their ecologies– including dominico-hartón plantain.

State projects are still rooted in the idea of scalability, and for some farmers "look more like projectiles" with high potential to undermine communities (Doña L. Pulido, elder farmer. 2015. Oral history interview). These projects require smallholders and the uniqueness of their farms to organize as cooperatives for the production and commercialization of large volumes of one single product. The land must be managed consistently through practices defined by one single agronomist to obtain high and homogenous yields. Quality produce is sold to large companies, usually at lower

69 prices, as in the case of productive alliances models39 (Gutiérrez 2014). While these projects involve smallholders, they reproduce forms of dependency on foreign knowledge and on external inputs that negatively influence ecological dynamics.

According to farmers, negative effects extended to the social fabric of the municipality, as experiences of joint work have failed and discouraged them from joining new cooperatives (Doña L. Pulido, Don L. Segura, elder farmers. 2015. Oral history interview). The weakness of the social fabric is one major challenge of the

Anolaiman community, which learned about mistrust through the extended armed conflict in Colombia.

Armed conflict in Anolaima

Rural Colombia has been the scenario of an extended armed conflict since the 1940s that resulted in the creation of a strong guerrilla group in the 1960s, the FARC40, and greatly worsened after the rise of narcotrafficking during the 1980s. While Anolaima did not experience major material and human losses, rural violence brought mistrust and the erosion of the social fabric through continuous waves of in and out migration, and the contested presence of armed actors. Campesinos in Anolaima avoid talking about the topic. During the 1990s, Anolaima was under control of the 48 FARC front commanded by "El negro Acacio" (C. Murcia, 2015. Coffee grower. Oral history

39 Productive alliances are horizontal business models bridging an operator, commercializing companies, financial entities and small-scale entrepreneurs. Peasants are shareholders providing land and labor. Prices for produce are non-negotiated and fixed by the purchaser. Private investors give a purchase guaranty and support credit access provided by a financial entity for smallholders, yet do not assume social security costs or agricultural risk of any operation (DNP 2007 cited in Salinas, 2008: 11). 40 Revolutionary Armed Forces of Colombia.

70 interview). Farmers briefly invoke memories of guerrillas stopping the commercialization of some goods produced by wealthy Colombian companies,41 or of guerrilla chiefs asking farmers to make regular payments known as vacunas. To conserve their tranquility and avoid displacement of their lands, farmers gave the equivalent of two labor days per week in either kind or cash, reminiscent of taxes paid to landlords in the times of haciendas.

The 48 FARC front made other interventions in Anolaima. According to farmers,

FARC members ordered curfews after 6pm, raped young women, and assaulted young male peasants to incorporate them into the guerrilla army. Many families took their young siblings and migrated to Bogota and small cities (Doña B. Moreno, Don

A. Bermúdez, M. Arévalo, 2015. Farmers. Oral history interviews), and other families abandoned their farms after being threatened (J. Vargas, 2015. Farmer. Interview).

Farmers also mentioned that, because of the high in and out migration, there were always new neighbors who in many cases were guerrillas or paramilitaries disguised among regular people; hence local farmers learned to distrust each other (Doña L.

Pulido, Don A. Bermúdez, elder farmers. 2015. Oral history interviews). Therefore, the conflict took at least one generation of farmers away from Anolaiman lands, and created mistrust among those who remained.

41 Trucks of local beer, Bavaria, were stopped before arriving to any town. To replace beer availability, Polar beer, a Venezuelan brand, was brought as smuggled and distributed in all regions under the control of guerrillas.

71 This undermining of social structures resulted in the difficulty of maintaining social organizations based on trust, structures that represented safety nets for farmers. With a ruptured social fabric, Anolaima fell into what Cordoba (2016) highlights as a generalized lack of capacity to generate grassroots organizational structures. This was further undermined by the disruption of food circuits and local economies taking place in decades to follow.

Transformation of local food circuits

Trade is ancient, and in Anolaima it has included barter, gift exchange and commercial trade of small and big food volumes. As in most Colombian towns, commercial food circuits were centered on farmers’ markets where peasants brought goods transported in their mules and horses. This public food market operated three times a week on the central park (Figure 3, a. and b.). Most produce was traded during Sunday, the day of the Catholic mass; on Mondays peasants finished trading what they had brought; and on Thursdays the market received merchants of clothing, furniture and appliances (Doña A. Arias, Don O. Sissa, 2015. Merchants. Interviews).

With the establishment of a train line that passed by La Florida, a urban core in

Anolaima, the market was highly visited by merchants and tourists from Bogotá

(Molina 2016). Being a middle point between tierra caliente and tierra fría (low warm lands and high cold lands), food commercialization was very dynamic in this town.

72 Negotiation of prices was a practice involving all food trade. Transactions of big volumes were bargained and sealed with spoken contracts "when words had value"

(Don A. Bermúdez, elder farmer. 2015. Oral history interviews). Farmers mentioned they joined food merchants in a bakery at the corner of the main park, played domino and drank aguardiente while defining exchange prices (Doña A. Arias, 2015.

Merchant. Interviews). Small volumes of food were directly sold to tourists. Men traded surpluses of staple crops and women sold cheese, curds and eggs. Smallholders sold goods by puchos (unweighted amounts of goods with a consistent volume), and offered ñapa or vendaje, an additional amount of goods given as gift, to loyal purchasers (Doña B. Moreno, elder farmer. 2015. Oral history interview). Thus, economic transactions were embedded in social dynamics that promoted fairness and repeated exchange, as described by Meyer (2002) for food trade in local Peruvian economies. These dynamics sustained the life of hybrid economies in Anolaima, and the financial viability of traditional diversified systems.

One major event changed the trajectory of the public food market in Anolaima.

During the late 1990s and the 2000s farmers were adjusting to the coffee crisis, economic liberalization and the intensification of the armed conflict. The farmers' market kept operating, yet with fewer visitors. In March 31st of 2000 a car-bomb with

50 kg of dynamite exploded in the police station of Cachipay, Anolaima’s neighbor municipality. This resulted in a local decree to protect civilians from attacks in public areas, stating that farmers markets should not be developed in central squares, neither near churches nor police stations. The traditional market was displaced to a less

73 accessible marketplace located ten blocks away from the central park (Figure 3, c. and d.); the slope to get to the new location is steep and access to cars is limited. In that same time, supermarket Murillo opened at the corner of the central park, supplying food demands. Farmers considered the translocation of the market was fatal for food exchange dynamics in the municipality (Don A. Bermúdez, Don L.

Bohórquez, Don J. López, Don P. Muñoz, Don G. Vergel, Don L. Segura, 2015.

Farmers, and Don O. Sissa, merchant. 2015. Oral history interviews).

Figure 3. Displacement of the local market in Anolaima. The market functioned in the central park of the municipality before the 1960s (a) and until the 1990s (b). During the 2000s, the market was displaced (c- from darker to lighter arrow), and currently is not so active (d). (Figures a and b were facilitated by owners of the grocery store Yarakúa in Anolaima. Pictures c and d were taken by the author).

74 Intermediaries appropriated food commercialization in the new marketplace. While farmers gathered to commercialize their produce in the new site, most customers did not follow. The few remaining purchasers were brokers bringing food to the major wholesale market in Bogota, Abastos, who controlled prices and generated perverse temporal dynamics for product exchange. They paid higher prices to farmers arriving early to sell their produce, and gave lower prices once trucks were half-full. Farmers engaged into a time race to arrive as early as possible to the market. Typically, food exchange started at 5am and peaked at 8am; by the mid 2000s farmers arrived by 2am to sell their produce (Don G. Vergel, elder farmer, and Don O. Sissa, merchant. 2015.

Oral history interviews). With time, food merchants sent trucks to directly purchase foods on farms, offering transport but also nonnegotiable prices. Four men who took charge of the market agreed to divide Anolaima and take control of specific villages

(Doña L. Pulido, elder farmer. 2015. Oral history interview). People told stories about how additional food traders were robbed or threatened, which discouraged them from returning to Anolaima. With free trade agreements and the popularization of supermarkets, food brokers assigned prices according to sold volumes and quality standards in which food could be of first, second or third class. This forced farmers to engage in technified agroindustrial practices to obtain higher and more uniform yields, and took away any power of negotiation peasants had over their produce. This change in food commercialization greatly promoted agricultural intensification and social unrest in the region.

75 Traditional agricultural livelihoods in Anolaima, as in many other parts of the world, were characterized by risk-averse strategies, growing different types of food to secure a minimum income, meet basic needs and avoid over-exploiting their land (Barlett

1980, Flora 1990). When farmers commercialized diverse crop surpluses directly, heterogeneity in yields was not a problem to sell foods and meet subsistence needs.

After food commercialization was imbued in quality standards and intermediacy, post-harvest losses increased automatically because brokers rejected non-uniform produce and only purchased large volumes (Figure 4). Farmers engaged in agroindustrial practices to comply with brokers’ market requests, to either achieve some minimum income or "hit the jackpot" with high prices once in a while. This new system was defined by an "amoral economy" only based in supply-demand dynamics and not in reciprocal negotiation (Scott 1977: 26-27), forcing Anolaiman farmers to surrender to food brokers, losing their dignity and the integrity of the environment that once fed them.

The effects of a displaced farmers' market in Anolaima exemplify linkages between global and local processes, and how random events can unexpectedly and dramatically change the functioning of a socio-ecological system. Surpluses from subsidized large-scale agroindustrial systems in industrialized countries are exported through international trade agreements, resulting in the high availability of cheap food imports in countries with emergent economies. In Colombia, these dynamics interacted with national policies reducing support to small-scale food production, which forced peasants to produce cheap food by overexploiting their labor and land.

76 Peasants managed to thrive, yet the geographical movement of a market, a random shift that could have been triggered by any factor, greatly disrupted the apparent high resilience of Anolaiman economies to long-term socio-political upheavals like the armed conflict. This apparent minor shift brought major changes in local food circuits, and had disproportionate consequences for rural economies, livelihoods and landscapes in the municipality42.

Figure 4. Vegetables rejected by food brokers. Color must be homogeneous and size not larger than a threshold. Because of this, zucchini growers reject cross-pollination and are not affected by how this pollination may increase size and weight of the fruits. The glossy aspect reveals fruits were sprayed before being sold. Photo by the author.

Nostalgia for the past

42 In Cachipay, the town in which exploded the car-bomb, the marketplace is still located at the side of the municipality’s main street, where it is an active trade center for peasants opened all days of the week.

77 Many farmers had fond memories of the way "the land used to provide" and claimed they do not have enough land and have lost the knowledge and energy to re-create their old production systems. Before technification, agricultural practices involved diversified plantations, also staged over time with long fallow periods. In oral stories, farmers recalled they grew home gardens; and squash, corn and beans or habas43

(Vicia faba) in systems similar to Mexican milpas. Some mentioned that tomato chonto was intercropped with peas in large areas (~2ha) after both were planted by throwing seeds on the soil (Don L. Bohórquez, elder farmer. 2015. Oral history interview), and others remembered with pride that a single avocado tree only fertilized with its own leaf litter used to produce five canastillas (about 100 kg) of fruits on each harvest season. Plants were not forced to synthetic fertlizers, tutored or trained on vertical poles, but received nutrients from the slow decomposition of leaves and manure, and climbed chamizos (sticks remaining from forest cleaning)

(Don J. López, 2015. Farmer. Oral history interview). About thirty years ago there were also diversified fields planted with wheat and corn, raspberry and blackberry were common, and passion fruits adapted to different elevations–maracuyá, granadilla, gulupa and curuba – were typically found climbing fruit trees. Once the monte (uncultured land) was gone, farmers "disciplined" plants with industrial knowledge and technologies, and former diversified crops were turned into monocrops.

43 This exemplifies the syncretism between native and American diets. Habas, native to Spain, were inserted in the ancient system of squash/corn/beans. Habas were introduced into traditional soups but also were used as snacks. With time, they were displaced by bubble gum and packed snacks (Bernal, 1946).

78

Time, social and ecological forces have taken many crop species to oblivion.

According to farmers, many crops including passion fruits and berries are not grown anymore because of the impossibility of fighting their pests, and few people maintain these plants for self-consumption. Biocultural memory is practical, enacted (Toledo and Barrera-Bassols 2008), and because of that it is closely influenced by dynamics of supply and demand across food systems. Before the major change in the farmers' market, people consumed maiz cacao, a maize breed with brown grains, and frijol cargamanto and vicente or todo el año; and batatas (sweet potato and other varieties), arracacia and yuca de monte (wild manioc) were grown and sold. As people stopped buying them, farmers stopped producing them, and the practices and knowledge about those crops disappeared as well. For example, now many people do not know batata tubers are edible and have a high nutritional content; they do not know either that batatas are expensive in the capital city. Doña Ligia, a curious traditional farmer in Anolaima, mentioned that people used to learned about plant edibility by seeing what birds and other animals consumed. Now seeing cows eating batata tubers is not a cue to explore this plant, abundant along roadsides, that represents a nutritious food for humans. This reflects the progressive loss of knowledge obtained from close encounters between farmers and plants, and how that eroded relationality can have diverse implications for humans, including our health.

Women selling produce in the public market have witnessed some of the changes in

Anolaiman agriculture through the foods they trade. After making a list of common

79 crops grown and exchanged in the past, and comparing them with the availability of crops currently grown, we found that several local varieties –along with their names– of plantain, corn, guatila and beans have disappeared from both trade and the memories of local people (Table 1). Many of the names describing crops and varieties reflected close interactions between traditional edible plants and humans sharing a territory. For example, guatila varieties were named across gradients of roughness, presence of spines, size and color, but as varieties disappear, textures, shapes and the names acknowledging them also eroded. This loss of names reflects how encounters between people and plants have been disrupted and no longer produce linguistic forms (Mathews 2017: 152) and human sensory experiences, leaving Anolaima with ghosts that once represented abundance –material and immaterial– for their people.

Along with changes in human-plant interactions, relationships between humans and bees have transformed. Mild and unaggressive social stingless bees, Angelitas or little angels (Tetragonisca angustula, Nannotrigona sp., Paratrigona sp.) have been permanent companions to people in Colombia. They belong to several species, but all of these bees share one vernacular name, angels, carrying the legacy of a close relationship between the clergy and bees in Europe. These little angels have settled in human-made constructions, becoming visible for people and fostering new relationships with them (Fig. 5). Many farmers share their houses with angelitas that have colonized walls, pots, chocos, or totumos44, and extract honey from time to time.

44 Empty shells of totumo (Crescentia cujete) of gourd (Lagenaria siceraria) fruits.

80 Other stingless bees have occupied unexpected places, including the building of the

Anolaiman mayoralty45. Some farmers remember candelitas or fire bees (Oxytrigona sp.), as well as bumblebees and carpenter bees, known as abejorros or abejones

(Tribe Bombini, Xylocopa sp.) 46, and mentioned that many have gone with time.

Figure 5. Angelitas nesting next to a power outlet at Doña Blanquita’s house. 2016. Photo by the author.

45 The relationship with stingless bees is similar to the relationship with the European bee Apis mellifera before its Africanization. Farmers used to harvest honey by smashing both honey chambers of Apis bees and stingless bee nests. Some people assert this is the reason why stingless bees became less common with time. 46 These memories about these bees are related to stinging accidents when people found nests on the ground and aimed to harvest honey, or when fighting those bees digging the wood of their homes. There is evidence of the presence of these bees in several parts of the municipality (Chapter 3 of this dissertation).

81 In contrast to the good relationships between most stingless bees and people in

Anolaima, Apis bees entail conflictive relationships with and among humans. These bees are entangled in love-and-hate relationships with farmers, who respect bees because of their honey production but are not aware about the contribution of bees to agricultural production, yet are afraid of bee stings47. Also, Apis bees entail the major cause of friction between beekeepers and farmers, as agroindustrial practices undermine bee health. However, Apis bees and their produce, meanings and performances, silently promote bridges of collaboration across human actors, as they have done since ancient times.

Currently, trends in landscape simplification and agrochemical use may be driving bee populations to ecological traps, whereby fields with abundant food sources, yet hostile for bee survival, are attractive for pollinators but drive their collapse. Current reductions of bee diversity suggest that with the spread of short-cycle crops managed with pesticides, bee communities homogenize (Chapter 3), possibly loosing functional diversity that favors food production and resilience to environmental change.

A brief glimpse into the future

47 In a recent survey with 320 households in Anolaima, 29.6% of households stated they admire bees, while 27.8% reject them and 29.3% mentioned their fields would be the same without pollination.

82 The trajectory of Anolaima depicts the displacement of agrifood territories and of the peasantry, where social asymmetries and conflicts are reflected into demographic changes. In 2015, 55% of the population in Anolaima was rural (6584 people), and

59.3% of Anolaima inhabitants experienced multidimensional poverty, compared with

33.3% reported for Colombia. Between 1985 and 2005 there was a strong drop in peopled aged 19 to 35, as youth has migrated to nearby cities. Most inhabitants are older than 50 years and represent the current working force in the region. Under such a demographic scenario, social change has been accompanied and reinforced by the violent neglect of the peasantry in most spheres of society. Now outmigration and hence, labor scarcity, depicts one major problem for traditional and low-intensity production systems, and it also represents the rejection of peasant identity, the land and of traditional agriculture.

Current social conditions in Anolaima conform with the idea of scarcity that sustains the discursive project of Development. This world-making project is thought to fight unstable economies, greater poverty, malnutrition, and limited public health and education systems, yet its interventions and practices have not resulted in freedom and prosperity for traditional farmers in Anolaima. On the contrary, external interventions have enhanced socio-economic inequality and induced major environmental degradation, undermining the local capacities of farmers and nonhumans to make meaningful livelihoods. Traditional farmers in Anolaima prefer a quiet life with dignity and the necessary social resources to make a livelihood.

83 Paradoxically, they feel trapped by some requirements of modernity48 and witness the deterioration of their livelihoods and practices, which used to support sustainable agricultural systems.

The abandonment of the countryside is currently inducing a new wave of land use conversions. After the armed conflict ceased in the mid 2000s, land prices have increased considerably and many farmers opted to sell their properties. Frequent purchasers come from the city to establish recreational farms or greenhouses for the flower industry. Both have been welcomed by the local government and inhabitants, as they represent employment opportunities. However, these land uses enact the displacement of agrifood territories, and of the people and knowledge formerly associated to traditional agricultural systems. Currently, peasant family farming is jeopardized in Anolaima, along with the rural livelihoods and spaces of coexistence with other beings that support food production in this region of the Andean mountains.

"Life has accelerated. Everything accelerates you, everything. There is no longer tranquility, as we had back in the days. Everything is acceleration, and it is horrible. All that technology… that kills us. One has a TV and listens all those bad news. That is acceleration. Appliances, all that technology is bad for us. Now we

48 In the above-mentioned survey, ___% people stated the thing they value the most in Anolaima is tranquility and freedom.

84 live as slaves. If the cellphone is not active, we get desperate. All is acceleration because of "improvements".

"We would like to go back to the old times. To have the same climates, the life we had which was so beautiful. To go back to our youth (…) Things had value. It was beautiful how we harvested things and we could sell them, or that we interchanged things. Now that does not happen. We are going through bad times because our money does not have worth. Money is worthless. Now 50000 COP are useless. In the past we bought enough groceries with 20000 COP. We took a carga and we sold it, and with that money we bought food and we had spared cash. Now we take one bill and it is gone."

"Three wishes… only two. To go and travel, and have some rest. In the countryside you never rest. Work never forgives, not even on Sunday. How nice it would be that someone said: 'come and have some rest!' Someone giving us that… perhaps our siblings. God. We do not expect anything from the government of from a neighbor.

What they do is to try and hit you on the head".

Doña B. Martinez, elder farmer. January 5, 2016. Interview.

Conclusions

Anolaima is the product of layered social processes and encounters connecting humans and more-than-humans. These processes include the Spanish conquest that

85 promoted a biological and cultural interchange and mixing, the establishment and expansion of simplified land uses, and indigenous expropriation from the land.

Further processes involved the establishment of large scale plantations of commodity crops; the expansion of coffee agroforests and the emancipation of peasant laborers; the introduction of green revolution technologies; and the transformation of local food circuits. All these dynamics have created and perpetuated social inequality and the invisibility of the peasantry, which have both been influenced by and shaped plants-bee and people ecologies (Fig. 6). These multilayered dynamics are deeply rooted in the past, yet still enacted in the present to influence the stability of rural livelihoods, the functionality of agroecosystems, and biodiversity.

86 Figure 6. Timeline describing major socio-political processes, systems of agricultural production, land use change, livelihoods and agricultural exchange, and major events involving bees in Anolaima. (WWII stands for World War II: ICA for International Coffee Agreement; and FTA for Free Trade Agreements).

The making of social dynamics and the relationships between humans, plants and bees in Anolaima has been markedly influenced by the Spanish conquest. The arrival of Europeans led to important changes in the composition of biological communities and in their relationships with humans (Crosby 2015). The big interchange brought diverse types of animals and plants, new forms of agriculture including monocultures, and through that, new livelihoods and landscapes. The Spanish conquest also brought religious ideas and rituals, and with them, the honeybee Apis mellifera, whose arrival has shaped the relationships between humans and bees to the present time.

Colonialism represented a major disruption in the Americas, bringing about processes of original accumulation (Frank 1967) and with it, conflicts over the meaning of the land and the material elements provided by it, or natural resources. This regime generated a subdued and marginalized class, peasants, who secured their livelihoods based on their knowledge about the resource base, yet within limited opportunities defined by their landlords.

Modernity brought to Anolaima market integration, new agricultural practices, enhanced inequality, landscape simplification and biodiversity declines. After the

19th century, livelihoods and landscapes were defined by the hacienda regime and coffee markets. These times brought important land-use changes with the establishment of large-scale commodity crops, especially coffee. An external

87 economic crisis in the US, together with policies for land redistribution, determined the end of the hacienda regime and the possibility for landless peasants to access land.

Changes in global demand, diseases, and pest outbreaks of coffee promoted establishment of a new production system, which involved simplification of both human livelihoods and landscapes. In the second half of the 20th century, green revolution technologies transformed agricultural rationalities, knowledge and practices, inducing a reduction in crop biodiversity and the simplification of habitats in Anolaima. These dynamics have strongly impacted bee diversity, and potentially food crops and the plant communities interacting with these bees.

The history of Anolaima has been mediated by the different ways through which other beings influenced the creation of worldviews, practices, landscapes, and livelihoods in the region. Stonich (1991) suggested that the making and maintenance of class relations in agricultural lands was based on the establishment of commodities, but irrespective of the product being grown. A more inclusive approach highlighting the idiosyncrasy of plants and animals –their characteristics, needs and relationships with other life forms–, and how they intersect with class relationships, exposes their socio-cultural roles to humans and brings different conclusions. Plants like pastures, cultivated especially in the highlands of Anolaima, and sugarcane in the lowlands, were managed as large-scale monocultures, greatly influencing landscapes and promoting social relationships of regimented labor; staple crops and fruits materialized livelihoods for peasants; while other plants mobilized major social transformations. In contrast, coffee represented a source of wealth and connection to

88 the global market, and because of its compatibility with marginal lands, this plant embodied the opportunity to own land and emancipate from a regime of subjugation for many peasants. Also, coffee has influenced the configuration of Anolaiman landscapes to maintain tree cover, despite the reduction of tree diversity in these agroforests.

Bees also took part in the transformation of landscapes and human livelihoods through their ecological responses to human disturbance, and their direct relationships with people. Human-bee relationships in Anolaima have been greatly influenced by the arrival and then the Africanization of Apis mellifera in the 1980s. This generated conflictive relationships with these bees, and then between their keepers and farmers growing foods through agroindustrial practices. While Apis dominates the landscape of human-bee relationships, interactions with stingless bees have been sustained by the docile nature of these bees, and solitary bees are not noticed. However, all bees have been affected by land use and environmental change in the region.

The landscape of Anolaima is a palimpsest wearing the histories of colonial times, commodity crops, side effects products of warfare, and abandonment. These processes built on one another, and influence the potential trajectories of peasants, livelihoods and nonhumans in the future. The trajectories show how socio-ecological systems cannot be simplified to either economic, cultural or ecological narratives, but their multiple dimensions need to be approached to better understand potential

89 alternatives to sustainability. In addition, these historical accounts also serve as a precautionary measure: "those who ignore their history are destined to repeat it".

"Life has accelerated. Everything accelerates you, everything. There is no longer tranquility, as we had back in the days. Everything is acceleration, and it is horrible. All that technology… that kills us. One has a TV and listens all those bad news. That is acceleration. Appliances, all that technology is bad for us. Now we live as slaves. If the cellphone is not active, we get desperate. All is acceleration because of "improvements".

"We would like to go back to the old times. To have the same climates, the life we had which was so beautiful. To go back to our youth (…) Things had value. It was beautiful how we harvested things and we could sell them, or that we interchanged things. Now that does not happen. We are going through bad times because our money does not have worth. Money is worthless. Now 50000 COP are useless. In the past we bought enough groceries with 20000 COP. We took a carga and we sold it, and with that money we bought food and we had spared cash. Now we take one bill and it is gone."

"Three wishes… only two. To go and travel, and have some rest. In the countryside you never rest. Work never forgives, not even on Sunday. How nice it would be that someone said: 'come and have some rest!' Someone giving us that… perhaps our

90 siblings. God. We do not expect anything from the government of from a neighbor.

What they do is to try and hit you on the head".

Doña B. Martinez, elder farmer. January 5, 2016. Interview.

Table 1. Foods grown in Anolaima in the recent past (twenty years ago) and in the present, according to elder women trading foods in the public market. Produced and Common Scientific Botanic Currently Currently sold in the name name family produced sold past Cebolla Allium cepa Amaryllidaceae Yes Uncommon No cabezona Cebolla larga Allium cepa Amaryllidaceae Yes Uncommon No Mango de rila Mangifera indica Anacardiaceae Yes No Yes Mango tommy Mangifera indica Anacardiaceae Less common Yes Yes and others Anón Annona squamosa Annonaceae Yes Yes No Chirimoya Annona cherimola Anonaceae Yes Yes Uncommon Guanábanas Annona muricata Anonaceae Yes Yes Yes Anis Pimpinella anisum Apiaceae Yes Uncommon Uncommon Arracacha de Arracacia Apiaceae Yes No No cepa xanthorrhiza-Banc. Cilantro Coriandrum Apiaceae Yes Yes Yes (European) sativum Cilantro de Eryngium foetidum Apiaceae Yes Uncommon No tierra (local) Petroselinum Perejil Apiaceae Yes Yes No crispum Daucus carota- Zanahoria Apiaceae Yes Uncommon No sativus Xanthosoma Chonque Araceae Yes Uncommon No sagittifolium Lechuga Lactuca sativa Asteraceae Yes Uncommon Uncommon Achiote Bixa orellana Bixaceae Yes Uncommon Uncommon Zapote Matisia cordata Bombacaceae Yes No No Piña Ananas comosus Bromeliaceae Yes Yes Uncommon Selenicereus Pitahaya Cactaceae Yes Uncommon No megalanthus Papaya Carica papaya Caricaceae Yes Yes Yes

91 Vasconcellea Papayuela Caricaceae Yes Yes Yes pubescens Cacao de Clusia sp. Clusiaceae Yes Uncommon No monte Madroño Garcinia madruno Clusiaceae Yes No No Batata dulce y Ipomoea batatas Convolvulaceae Yes No No salada Cucurbita Ahuyama Cucurbitaceae Yes Yes Yes moschata Calabaza Cucurbita sp. Cucurbitaceae Yes Yes No Choco Lagenaria siceraria Cucurbitaceae Yes Uncommon No Guatila negra Sechium edule Cucurbitaceae Yes Yes Yes lisa Guatila blanca Sechium edule Cucurbitaceae Yes Uncommon No Guatila Sechium edule Cucurbitaceae Yes Uncommon No espinosa Melón de Cucumis melo Cucurbitaceae Yes Uncommon No monte Pepino Cucumis sativus Cucurbitaceae Yes Uncommon No cohombro Pepino de Cyclanthera pedata Cucurbitaceae Yes Yes Yes guiso Zucchini Cucurbita pepo Cucurbitaceae Yes Yes No Higuerilla Ricinus communis Euphorbiaceae Yes Uncommon No Yuca Manihot esculenta Euphorbiaceae Yes Yes Yes Arveja Pisum sativum Fabaceae New varieties Yes Yes Fríjol Phaseolus vulgaris Fabaceae Yes Yes Yes Fríjol vicente Phaseolus vulgaris Fabaceae Yes Yes No Fríjol vaquita Phaseolus vulgaris Fabaceae Yes Uncommon No Fríjol blanco Phaseolus vulgaris Fabaceae Yes Uncommon No (d. Antonio) Fríjol Phaseolus vulgaris Fabaceae Yes Yes Yes cargamanto Guama Inga edulis Fabaceae Yes Yes No Guama común Inga edulis Fabaceae Yes Yes No Guama copera Inga spectabilis Fabaceae Yes Yes No Guamo rabo’e Inga edulis Fabaceae Yes Yes No mico Haba Vicium fava Fabaceae Yes Uncommon No Habichuela Phaseolus vulgaris Fabaceae Yes Yes Yes Fríjol Canavalia Fabaceae Yes Uncommon No carnavalia ensiformis Balú Erythrina edulis Fabaceae Yes Yes No Aguacate Persea americana Lauraceae Yes Yes No criollo/común

92 Aguacatillo Persea caerulea Lauraceae Yes Uncommon No Cacao Theobroma cacao Malvaceae Yes Yes No Árbol del pan Artocarpus altilis Moraceae Yes Uncommon No Breva Ficus carica Moraceae Yes Uncommon No Higo Ficus sp. Moraceae Yes Uncommon No Banano Musa sapientum Musaceae Yes Yes Yes Plátano criollo Musa paradisiaca Musaceae Yes Yes Yes Plátano pocho Musa paradisiaca Musaceae Yes Uncommon No Plátano guineo Musa paradisiaca Musaceae Yes Uncommon No Plátano coliero Musa paradisiaca Musaceae Yes Uncommon Uncommon Feijoa Acca sellowiana Myrtaceae Yes Yes No Guayaba Psidium guajava Myrtaceae Yes Yes Yes Granadilla Passiflora ligularis Passifloraceae Yes Uncommon Uncommon Passiflora Gulupa Passifloraceae Yes Uncommon No pinnatistipula Maracuyá Passiflora edulis Passifloraceae Yes Yes Yes Passiflora Curuba Passifloraceae Yes Uncommon No tarminiana Saccharum Caña Poaceae Yes Yes Yes officinarum Cebada Hordeum vulgare Poaceae Yes No No Zea mays - Chócolo Poaceae Yes Uncommon No saccharata Maiz blanco Zea mays Poaceae Yes Yes Yes (white) Maiz porva Zea mays Poaceae Yes Uncommon Yes (yellow) Maiz cacao Zea mays Poaceae Yes Uncommon No (dark) Trigo Triticum sp. Poaceae Yes No No Acedera Rumex acetosa Polygonaceae Yes Yes No Mora castilla Rubus glaucus Rosaceae Yes Uncommon Yes Mora silvestre Rubus floribundus Rosaceae Yes Yes No Frambuesa Rubus ideaus Rosaseae Yes Yes No Café Coffea arabica Rubiaceae Yes Yes yes Lima Citrus latifolia Rutaceae Yes No No Citrus latifolia Limón Rutaceae Yes Yes No (& others) Limón agrio/ Citrus latifolia Rutaceae Yes Yes No mandarino Limón dulce Citrus latifolia Rutaceae Yes Yes Yes Limón Tahití Citrus x latifolia Rutaceae No Yes Yes

93 C. x aurantifolia Limón pajarito Rutaceae Yes Yes No (Christm.) Mandarina Citrus reticulata Rutaceae Yes Yes Yes Citrus sinensis/ Naranja común Rutaceae Yes Yes Irregularly maxima Naranja ombligona Citrus sinensis/ Rutaceae No Yes Yes (improved maxima variety) Naranja Valencia Citrus sinensis/ Rutaceae No Yes Yes (improved maxima variety) Toronja Citrus sp. Rutaceae Yes Yes No Melicoccus Mamoncillo Sapindaceae Yes No No bijugatus Mamey Pouteria sapota Sapotaceae Yes Yes No Capsicum annuum Ají chirca Solanaceae Yes Yes No var. glabriusculum Berenjena (in Solanum Solanaceae Yes No No the lowlands) melongena Lulo Solanum quitoense Solanaceae Yes Yes No Papa sabanera Solanum tuberosum Solanaceae Yes Uncommon No Papa pepina Solanum tuberosum Solanaceae Yes Uncommon No Pimentón Capsicum annuum Solanaceae Yes Yes Yes Lycopersicon Tomate Solanaceae Yes Yes Yes esculentum Solanum Tomate de lycopersicon- Solanaceae Yes Uncommon No monte cerasiforme (cherry) Tomate de Solanum betaceum Solanaceae Yes Yes Yes árbol Uchuva Physalis peruviana Solanaceae Yes Uncommon No

94

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108 Chapter 2:

Intersections between rural livelihood security and animal pollination in

Anolaima, Colombia

Abstract

In the tropics, animal pollinators and smallholders sustain the livelihoods of hundreds of families, yet both are threatened by expansion of industrial agriculture. We discuss some of the intersections between animal pollination and agrarian change through an empirical case study in the Colombian Andes. We conducted surveys, interviews and participant observation to evaluate how animal pollination contributes to food production and consumption, and whether this contribution is influenced by socio- economic factors sensitive to agrarian transformations. We highlight some pathways through which agrarian change increases the vulnerability of traditional farmers to social and environmental change: biodiversity losses of animal pollinators that contribute to the production of a high proportion of foods with high nutritional value; the saturation of food systems with cheap but non-nutritious staples; and the undermining of traditional family agriculture, that contributes a large fraction of food consumed worldwide.

Introduction

Yaquie took some seeds from a vigorous squash fruit harvested within the coffee agroforest and sowed them next to the passion-fruit. She was disappointed: the

109 daughter plant was yielding really small squashes. Don Eugenio, Yaquie's partner, sprayed the passion-fruit vine with pesticides twice a week to deter flies that could deposit its eggs on the floral bud. Don Eugenio felt he needed to protect the fruits to have some for sale, but this time the fruits were light in weight. Yaquie was worried.

With five people in the family to support, the margin between survival and shortfall is small. She had high expectations of the coffee harvest, but the drought and high temperatures precipitated a coffee berry borer infestation. Despite her reservations, she decided to respond to the infestation with chemicals, following the lead of Don

Eugenio, who grows crops through "the modern way". Yaquie mentioned with frustration that in times of need, "economy comes before ecology". Would the remedy be worse than the disease?

Increasing threats to the sustainability and security of food production require a close examination of the intersections between biodiversity, food, and social dynamics at multiple scales and connecting humans and nonhumans. While plants are the basis of food systems, productivity could be drastically impacted by declines in animal- mediated pollination, a process that benefits more than 75% of crop species and contributes about 35% of global food production (Free 1993, Williams 1994, Aizen et al. 2009) and contributes at least 14 billion dollars per year to the global agricultural economy (Winfree et al. 2011). Animal pollination benefits fruit production (quantity, quality and stability) to different degrees and is essential for some, yet unnecessary for others (Klein et al. 2007, Klatt et al. 2014). The intricacies of plant-pollinator- human relationships require investigative approaches that span field-to-fork

110 dynamics. Diets that include fruits reliant upon animal pollination (hereafter AP) contain higher contents of micronutrients essential for human development, including

Vitamin A, iron, folate and calcium (Eilers et al. 2011). Such nutrients are limited across the world, and are especially important in regions with increasing food insecurity, such as the tropics (Chaplin-Kramer et al. 2014, Smith et al. 2015).

Despite their vital role as one of the main animal pollinators, bee populations have declined drastically during the last decades due to habitat simplification, disease, and pesticide use, all factors associated to the expansion of industrial agriculture (Grass et al. 2013, Kennedy et al. 2013b, Goulson et al. 2015).

While pollinator declines happen locally, their socio-economic impacts highlight the interconnections within the global food system. Recent studies show that the area planted on pollinator-dependent crops is increasing in both developed and developing countries in response to dietary diversification and demand for healthy foods in affluent countries (Aizen et al. 2008). Concurrently, the burgeoning prices for pollinator-dependent crops in response to the massive reductions of honeybees in the

US (Lautenbach et al. 2012) suggests that cultivating pollinator-dependent crops currently represents a good economic alternative for producers. Such a scenario could be particularly true for the tropics, a region with a high density of pollinator- dependent crops (Aizen et al. 2008, 2009). Despite nutritional need and economic potential, industrial agriculture—and associated negative environmental and social implications—are rapidly expanding in this region (Gibbs et al. 2010, Lambin et al.

2013, Laurance et al. 2014), paradoxically acting as a force against the animal

111 pollinators upon whose services it relies. Thus, there is a need to better understand the contribution of animal pollination to rural, agricultural livelihoods in the tropics, especially the socio-economic and cultural factors mediating animal pollination in regions undergoing agrarian change.

Traditional smallholder agriculture in the tropics

The tropics, where coffee, cacao and diverse fruit plants are pollinated by wild insects moving between natural habitats and farms (Martins 2013), are home to agriculturalists whose nutritional and economic well-being could be greatly impacted by further animal pollination declines. In Latin America, smallholders account for

60% of the population, manage 15% of agricultural land, and produce 50% of the food humans consume worldwide (Altieri and Toledo 2011, FAO 2014). Most of these growers engage in traditional family agriculture, which is synonymous with robust systems of ecological knowledge that result in diversified cropping systems and high agrobiodiversity without requirements for external inputs (Toledo 2002,

Toledo and Barrera-Bassols 2008). Traditional agroecosystems provide smallholders with access to diverse foods and nutrients, exhibit increased productivity and stability of food production (Mendez et al. 2010, Sampson 2015), and demonstrate the ability to cope with external perturbations such as climatic fluctuations and variability in food prices (Thrupp 2000, Lenne and Wood 2011, Sampson 2015). However, persistence of traditional small-scale farming, and the human and nonhuman interconnections upon which it depends, are threatened by the expansion of industrial agriculture.

112

Agriculture in the tropics is undergoing major transitions with unevenly distributed social and environmental impacts. Neoliberal policies to modernize agricultural production and promote the mass-production of food have become pervasive throughout the region, controlling and homogenizing techniques, knowledge, landscapes, and ecologies (Painter and Durham 1995, Weis 2010). Those policies exacerbate historical asymmetries of land distribution, privileging large estates for the production of exports, and have also encouraged imports of cheap food to former agricultural regions, catalyzing profound dietary and cultural changes (Fajardo 2014).

Smallholders, formerly the most important providers of food for local consumption, are now forced to compete in agroindustrial food markets. Traditional cultivation based on agroecological knowledge and practices becomes more extensive through extending cropping areas and/or more intensive through the use of synthetic inputs, both of which increase environmental degradation, discount traditional knowledge, and jeopardize food security and autonomy (Pretty et al. 2003, Chappell et al. 2013,

Grau et al. 2013). Alongside effects on food production, smallholders transitioning from diversified to simplified agroindustrial systems increase consumption of purchased produce (Reardon et al. 2000, Sandoval 2010, Barthel et al. 2013,

Pellegrini and Tasciotti 2014), reliance on financial income, and vulnerability to food shortages. These processes produce the paradoxical situation of hungry farmers in mega-diverse bioregions and former centers of crop diversification (Zimmerer 2006,

Bacon et al. 2014).

113 In light of the global declines of pollinators and the complexity of agrarian transitions, the current challenge is to produce nutritious food for a continuously growing human population in an environmentally and socially sustainable manner.

This necessitates a deeper understanding of the role of animal pollination for rural livelihoods. Current research to understand pollination declines has addressed the economic contribution of animal pollination to production of commodity crops

(Kremen et al. 2002, Klein et al. 2003, Ricketts et al. 2004, Greenleaf and Kremen

2006, Winfree et al. 2011); the biophysical contexts that enhance animal pollination

(Kremen et al. 2002, Lonsdorf et al. 2009); and its relevance for global food security

(Klein et al. 2007, Chaplin-Kramer et al. 2014). However, most previous studies are based in the northern hemisphere (77% of studies) and in farms larger than 3 ha

(88%) (Steward et al. 2014), thereby overlooking both tropical smallholders and the structural context that mediates access to and distribution of the benefits derived from

AP. Understanding and heightening awareness about the intersections between animal pollination, crop production and consumption, and the social forces influencing how people access foods benefited by animal pollination can be used to inform policies and community-based conservation strategies that protect pollinators in agricultural lands.

We present evidence on the links between plants, animal pollinators and livelihood security in Anolaima, the former fruit capital of Colombia located 70 km away from the capital city, Bogotá. About twenty years ago, coffee and fruit production were the main economic activities in this municipality, but more recently, activities have been

114 supplanted by cattle ranching, tourism, and the agroindustrial production of short cycle crops and foliage for the flower industry. We aim to assess the contribution of animal pollination for rural livelihoods and to examine how socio-economic differentiation associated with agrarian change can enhance the vulnerability to food insecurity under potential pollinator declines in Anolaima. Specifically, we asked: 1)

What is the contribution of animal pollination to crop diversity and food consumption in Anolaima? and 2) Is this contribution contingent on socio-economic factors associated with agrarian change? We also reflected on how future pollinator declines could exacerbate the vulnerability of rural households to food insecurity. We found that, while animal pollination was of great importance for crop production in

Anolaima, access to the benefits of this pollination was strongly mediated by an acute socio-economic differentiation. This differentiation is aggravated by agrarian change, which further marginalizes traditional family agriculture and agribiodiversity in the region.

Methods

Study site

Anolaima is located in the eastern slope of the Colombian Andes, extending between

900 and 2800 meters above sea level, where most lands have steep slopes (50% or higher) and undisturbed areas transition between cloud-submontane forest and tropical dry forest. Anolaima's dominant economic activity is still agriculture, and cattle ranching covers 41.3% of the land in the municipality. Most households engage in a mixed economy that combines subsistence and commercial agriculture, animal

115 husbandry, and off-farm income from agricultural and non-agricultural wage labor, remittances, retirement incomes and state subsidies (Figure S1).

The history of land appropriation in the Colombian Andes rendered Anolaima with an acute class differentiation reflected in a severe inequality in income and access to land. While only 2.6% of the properties are larger than 10 hectares, 92.6% of private properties are smaller than three hectares and represent 53% of the total area of the municipality; according to the government, the size required by a family to sustain a livelihood in this region is 5 hectares (Anolaima 2016). Trends in farm size resemble variability in income (Table 2). Median net income of focus households was $3,844

USD per year and per capita net income was $2,456 USD, which can be compared with $2,757 USD, the 2016 minimum legal wage for Colombia over a 12-month basis

(Decree 2552 3015) (Table 2). Most surveyed households (74.1%) received off-farm income from wage labor, yet only 6% of households received continuous off-farm income throughout the year.

Research design

This study combines survey data, interviews, and participant observation to obtain information about crop diversity, food consumption and livelihood security in

Anolaima. Between February 2015 and December 2016, we surveyed households to explore general relationships between crop diversity and socio-demographic factors, and conducted interviews with a smaller set of households to evaluate patterns of

116 food consumption and to better understand the relationships characterized through survey data.

We surveyed 320 household members across the municipality, asking about different crops grown on farm (herein crop richness), and whether they were produced for commercialization or subsistence consumption. We also asked about farm size and ownership, agri-pecuarian and off-farm livelihood activities, use of synthetic agrochemicals and demographics, and the number of months in economic difficulty as a proxy for perceived livelihood insecurity. Surveys were administered by three members of the community and included equal numbers of male and female respondents.

We conducted semi-structured interviews with sixteen focus households to obtain additional information about food consumption, demographics, land access, and income. Households represented a socio-economic spectrum and were selected through snowball sampling. To obtain data on dietary diversity, we asked households the amount and source of foods (i.e., on-farm or purchased) consumed during the preceding week, based on a list of 100 staples that included starches, legumes, dairy and meat, fruits, vegetables, fat (butter, oil), sweeteners and salt, and traditional foods. Because of the marked agricultural seasonality in the region, we evaluated whether the contribution of animal pollination changed across seasons: dry (February and March); major harvest season of coffee and fruits (June and July); and wet

(October and November). We asked households which foods they consumed for each

117 of the three major meals for three days per each season, and the food source. To understand underlying relationships between people, livelihood activities and crop plants, we also conducted participant observation and informal interviews with each focus household. To obtain data on annual income, we asked about revenues received from on-farm and off-farm activities following the methodology of Forero and

Corrales (1992) for Colombia. We present net monetary balances (herein income) that do not include domestic costs (primarily family labor). Many households do not register in- and out-flows of cash, barter, or subsistence foods, therefore our estimates are limited to farmers' perception on cash flow.

Data analysis

To estimate the contribution of animal pollination, we combined data on foods produced and consumed per household with published records on the requirements of animal pollination for each of those foods. We grouped foods according to whether animal pollination is reported as being essential, great, modest, or of low importance or has no influence on fruit production (Free 1993, Roubik 1995, Klein et al. 2007).

For the quantitative analyses, we used crop richness grown by each surveyed household, and the frequency of foods consumed by each focus household as response variables. We fitted a generalized linear mixed model (GLMM) to test whether the contribution of animal pollination to crops grown by surveyed households changed depending on whether the crop was produced for commercialization or subsistence consumption. We also used a GLMM to test

118 whether the contribution of animal pollination to the frequency of foods consumed across focus households significantly changed across seasons and depending on whether the food was grown or purchased. For illustration purposes, we present foods produced and consumed across households according to different levels of reliance on animal pollination (Klein et al. 2007). To evaluate the influence of socio-demographic factors on crop diversity, we ran bivariate Pearson correlations between all pairs of factors using survey data. We also run Pearson correlations to evaluate factors, including income, influencing weekly dietary richness across focus households. We also tested which and how socio-economic factors influenced the diversity of subsistence crops, household income and dietary diversity of focus households through generalized linear models (GLM), better detailed in the supplementary material (S1). All quantitative analyses were conducted in R (R Development Core

Team 2014).

To analyze qualitative data, we coded answers to open-ended questions in the software Dedoose (Lieber et al. 2011). We use grounded theory to illustrate the perception of rural households regarding food and livelihood security in the region.

Results and Discussion

We present evidence to better understand the contribution of animal pollination to rural livelihoods in Anolaima, and the socio-ecological factors that can increase farmers’ vulnerability during agrarian transformations. In the next sections we present data regarding (1) crop diversity, its reliance on animal pollination and socio-

119 economic factors influencing agriculture in Anolaima; and (2) dietary diversity, how it is benefited by animal pollination, and social aspects influencing food access and security in this municipality.

Crop diversity and animal pollination in Anolaima

We found that, households recognized 52 crop morphospecies grown for subsistence; of those, 42 were also commercialized (Fig. 7). The most common subsistence crops were plantain, guatila (Sechium edule), manioc (Manihot sculenta), squash

(Cucurbita maxima) and balú (Erithryna edulis); different varieties of guatila and squash were also found across farms. Many elder farmers described how they were raised with diets based on these plants, which farmers are able to produce securely across the year. Despite the fact that traditional foods are still common, home gardens—key spaces for the diversified food production of traditional staples—are disappearing. While 89.6% of households maintained at least one crop for self- consumption, only 30% of households maintained a home garden, and households maintained on average only 4.13 crops (Table 2), suggesting how growing foods for subsistence consumption is losing relevance in the region. Commercial crops were as common as subsistence ones: 87.8% of households grew at least one cash crop. The most common cash crop was coffee, typically intercropped with other commercial fruits (e.g., citrus, plantain and guava) in shaded agroforests; 63.52% of coffee growers did not use synthetic biocides. The other common cash crops were green beans, peas, and tomatoes, which have the highest profitability in Anolaima and the highest use of agrochemicals (EOT 2016).

120

Animal pollination contributed to 63.8% of the different crops grown across farms, with similar benefits for commercial and subsistence crops (AIC= 960; df= 485; Z= -

0.782; P= 0.434) (Fig. 8). The most common crops benefited by animal pollination included squash, cherimoya and sour sop for which pollination is essential for fruit production; guatila (Sechium edule), mango (Mangifera indica) and chilies (ají chirca

- Capsicum annuum var. glabriusculum, ajíes de monte - Capsicum sp.), which greatly benefit from animal pollination; and coffee, moderately benefiting from animal pollination (Free 1993, Roubik 1995, Klein et al. 2007). Prevalent crops that do not significantly benefit from animal pollination include plantain, manioc, green beans and peas. We reviewed official reports (Agronet and Ministerio de Agricultura

2017) to estimate the contribution of animal pollination for agricultural productivity in Anolaima. In 2014, crops benefited by animal pollination represented 86.3% of the total agricultural area and 71.2% of produced weight (71.23 tons/year). However, in official records Anolaima only produces coffee, mango, tangerine, guava, bananas, tomato, and green beans, rendering invisible the existence of many subsistence crops grown across the region. Our empirical data, while based only on richness and not on productivity, indicate that crops for which animal pollination is essential or greatly benefits fruit production are important for subsistence, and as a result, that some households could be greatly impacted by pollinator declines.

Socio-economic factors and agricultural production

121 Crop diversity and the significance of animal pollination for agriculture in Anolaima were influenced by the interrelationships between on-farm agrobiodiversity, farm size, livelihood strategies, and agricultural management, with varying consequences for sustainability of the resource base and the procurement of financial revenues.

Higher subsistence crop richness was associated with households that were larger (P=

0.013), engaged in more off-farm activities (P= 0.01), and grew more commercial crop species (P<0.001) (AICc= 665.19; df= 331; R2= 0.26) (Fig. 9). Larger households were, on average, younger; the number of off-farm activities decreased with farm size; and the number of months in need increased with household size

(P<0.001), yet decreased with subsistence crop richness (P= 0.017) (AICc= 912.95, df= 233, R2= 0.08).

Our results suggest that growing a high diversity of subsistence crops, as well as diversifying livelihoods with off-farm income sources, were strategies that large families on smaller farms—comprising the most vulnerable households in the region—utilized to secure food access. Maintaining a high crop diversity has been a strategy to buffer external risks to food insecurity in Mexico (Sampson 2015),

Nicaragua and El Salvador (Mendez et al. 2010, Morris et al. 2013), and in Ecuador

(Perreault 2005). However, our data indicate this strategy is eroding considerably in

Anolaima, increasing household food vulnerability and livelihood insecurity. For instance, farmers in Anolaima experienced a pronounced drought during 2015, which partially overlapped with a transportation strike. The availability of foods grown on- farm decreased and food prices increased considerably. Many households asserted

122 that “the homegarden would have been useful” (Doña B. Martinez, elder farmer.

January 5, 2016. Interview) to secure food intake, suggesting that crop diversity, accompanied by the presence of pollinators to secure crop production, is important for the livelihood security of vulnerable traditional households, especially amidst financial scarcity.

The challenges faced by households engaging in traditional practices contrasts with the panorama of modern agriculture, where households fulfill needs through the simplification and over-exploitation of the land. Painter and Durham (1995) described how the interplay between capital, class differentiation and agrarian change perpetuate processes of agricultural exploitation and impoverishment. Low-income households with insufficient access to land and capital typically rely on agribiodiversity and maintain low-input diversified systems to cope with external perturbations and secure food access and profits (Flora 1990, Eakin and Luers 2006).

In contrast, wealthier households with larger landholdings and more capital engage in input-intensive specialized agriculture. Agroindustrial practices initially bring high returns and allow for capital accumulation, re-investment, and expansion of operations, often resulting in ecological simplification, reductions on crop diversity and environmental degradation (Painter and Durham 1995). When agricultural profitability drops because of productivity or market forces, low-income households increase exploitation of their lands or switch towards off-farm and non-agricultural livelihood activities, whilst wealthier households expand operations. Hence, the expansion of capitalistic agriculture can broaden socio-economic inequality

123 (Bernstein 2004, Van Dusen and Taylor 2005, Zimmerer 2006). We found these dynamics in Anolaima, where focus households obtaining higher income engaged in the use of synthetic agrochemicals (P= 0.028) and grew a lower richness of subsistence crops (P= 0.024) (AICc= 39.204, df= 15, R2= 0.29) (Fig. S1-12). This trend reflects some farmers’ financial motivations to engage into agro-industrial practices, despite the potential depletion of their resource base.

Despite their negative effects, agroindustrial systems that undermine pollinator diversity and the productive potential of the region have become more common in

Anolaima in the past few decades. The contrasting rationales to engage in either agroindustrial or traditional practices are found between new generations and elders.

Young males claimed that “the land doesn't provide anymore” (Don J. López, farmer.

May 5 2015. Interview), and asserted that "it is the same [effort] to maintain a home garden for one than for five, but you lose a lot when you grow food for only one person" (Don F. Cristancho, farmer. January 11, 2016 Interview), holding optimization rationalities disregarding the benefits of diversification and the cultural value of growing plants for self-procurement. Conversely, elder farmers stated that

“the land provides for everything. The problem is that we do not sow anymore or those [foods] have no [good] price anymore” (Don L. Segura, elder farmer.

November 11, 2015. Interview). In fact, many elders in our focus households enjoyed collecting different varieties of crops and trees, and talked with conviction about agroecological management, echoing peasants in other tropical regions (Nazarea

1995, Rhoades and Nazarea 1999, Rocheleau et al. 2001, Sampson 2015). Elders

124 opposed the production and consumption of foods with biocides and considered that industrial agriculture “burns the land”, and that while it could bring in more money, using synthetic agrochemicals would entail spending more of their income on health care. These generational tensions convey ideas about the connections between agricultural productivity and profitability. Younger farmers have surrendered to the perpetual dependency on agrochemicals to sustain themselves in the broken linkage between productivity and commercialization, while elder farmers resist engaging in a system that disrupts the foundation that makes food production possible.

Past generations experienced the plenitude of Anolaima as the “fruit capital of

Colombia.” Farmers asserted they grew more abundant and diverse crops before the simplification of coffee agroecosystems and the expansion of technified monocrops, as has happened in other Andean and Central American regions (Rhoades and

Nazarea 1999, Camacho 2006, Zimmerer 2006). Smallholders said that pest and disease outbreaks increased with use of synthetic agrochemicals, and the high costs of fighting pests were a reason to stop growing several crops, including blackberry and passion fruit, both dependent on animal pollination (Lopez 2015, Silva 2016, Segura

2015). Thus, the transition towards agroindustrial systems has undermined the productive potential of the region. Currently, pastures and agroindustrial monocultures of crops not benefited by animal pollination are expanding and represent 46% of the total land in Anolaima (Anolaima 2016). These land uses negatively impact bee diversity (chapter 3) through use of synthetic agrochemicals, reductions in plant diversity, and landscape simplification. The impacts in pollinator

125 diversity may not influence the productivity of agroindustrial fields, but their regional effects on pollinator communities will likely affect coffee and other crops, and further hinder the potential of this municipality to grow high-value animal-pollinated crops.

The expansion of agroindustrial fields spatially segregates traditional small farms, negatively affecting their sustainability. As animals that disperse large distances across the landscape, pollinators experience both the effects of local management and habitat types and practices in surrounding areas (Kremen et al. 2007). Therefore, even the ecological functionality of traditional fields as refuges for pollinators is impaired when surrendered by inhospitable areas like agroindustrial fields (Winfree et al. 2009,

Kennedy et al. 2013a). The negative effects of large-scale and simplified habitats on pollinators has brought major imbalances, including massive honeybee declines

(Goulson et al. 2015) and drastic changes in Chinese agricultural activities (Partap and Ya 2012). For traditional diversified systems this means that, despite growers’ efforts, pollinators may decline on their farms due to the regional expansion of agroindustries, undermining subsistence crops and livelihoods depending on such pollination.

Dietary diversity, animal pollination and food access

Dietary diversity in Anolaima reflected the broken linkages between food production and consumption. Average weekly dietary diversity across focus households comprised 46 (SE = 2.9) foods, yet only 20.4 (SE = 1.92) of the goods consumed were grown on-farm (Fig. 10). The most frequently consumed foods included

126 plantain and manioc; and purchased cheap foods such as potato, rice, bread and pasta.

Many rural households struggled to secure a livelihood and can only access low- diversity diets rich in carbohydrates to feel satiated. These diets have been correlated with conditions such as obesity, diabetes, and circulatory problems (Fonseca-Centeno et al. 2011, Khoury et al. 2014). Besides, such foods lack micronutrients essential for proper human development such as vitamin A and C, foliate and iron, increasing the risk of fetal malformations, blindness and anemia (Black et al. 2008). This mirrors the global increase of malnourishment in low-income households, associated with high consumption of cheap, caloric but non-nutritious starches (Khoury et al. 2014).

The contribution of animal pollination to foods consumed in Anolaima was lower than the expected. While in industrialized countries animal mediated pollination contributes to 33% of the foods people consume (Eilers et al. 2011), animal pollination contributes to only 18.35% of foods consumed in Anolaima (Fig. 10). The most consumed foods across households included tubers, cereals and wheat derived from plants not benefited by AP. As diets diversified, they included more foods benefited by animal pollination (r= 0.68; P= 0.016).

Diets in Anolaima changed with the pronounced seasonality of the region. Our quantitative assessments suggested that the contribution of animal pollination to diets did not significantly change across seasons (F= 0.164, df= 2, P= 0.849), but this is likely because our data combined information for farmers growing both coffee and other commercial crops that may experience seasonality in different ways. For

127 instance, coffee growers said that in the season between March and August is abundance of harvests and concurrently of jobs. However, many households lived off of their savings after August, and the first months of the year were times of scarcity

(Arévalo 2015, Bermúdez 2015, Muñoz 2015, Pulido 2015, Segura 2015). Farmers growing short-cycle crops experienced seasons differently, as they harvest produce during January and February, and August and September. Thus, farmers mentioned that seasonality strongly defines the rhythms of both on-farm agricultural activities and the availability of wage labor found off-farm. Thus, our results reflect a situation where wealthier families sustained diverse diets throughout the year, while low- income households had less diverse diets across seasons and lower ability to manage external perturbations. During the last food shortage season, 70% of farmers stated they reduced consumption of vegetables and fruits, potato with guatila, and engaged in strategies such as preparing soups because they allow diluting smaller amounts of raw foods to achieve the same level of satiation.

Despite the high consumption of purchased foods, some foods grown on-farm were important for people both because of their cultural significance and role in mitigating subsistence risk. People still relied on two crops that are manly pollinated by native bees, guatila and squash. Squash mainly grows after a rainy season and represents an important source of vitamin A and Iron for low-income families (Fonseca-Centeno et al. 2011). Guatila, an orphan crop in Colombia also known as "potato for the poor," is an important source of antioxidants (Ordonez et al. 2006) and frequently consumed across households, used as a gift among neighbors, and given as food for cattle, cows

128 and pigs. Guatila it is also considered a safety staple as it fruits throughout the year, except for seasons with extremely high temperatures (Aung et al. 1990, Bermúdez

2015). Farmers asserted they maintain several guatila varieties that respond differently to changing temperature and water availability to secure access to this fruit

(Doña B. Martinez, Don A. Bermúdez , Don L. Segura, elder farmers. 2015,

Interviews). Also, guatila and squash are main ingredients in traditional local preparations including tamales, sudados and piquetes (stews), and soups (Doña L.

Pulido, Doña B. Martinez, elder farmers. 2015. Interviews). Thus, in scenarios of bee declines, productivity of these two plants may be negatively impacted, cascading to affect food and nutritional security of rural livelihoods and eroding the gastronomic identity of the region.

Class differentiation, food access and household vulnerability

Food security, associated with production, access and use of nutritious goods, reflected gender relations and socio-economic class in Anolaima. Dietary richness was better explained by and increased with the presence of women (P= 0.022) and the number of purchased foods (P= 0.006) (AICc= 107.78; df= 15; R2= 0.65) (Fig. 11).

Thus, our data featured the role of women as care takers who promote food and nutritional security, emphasized by different organizations during the last decades

(Quisumbing et al. 1995, Arroyo et al. 2001, Segura 2004, Camacho 2006). In all of our focus households, women were in charge of growing and selecting food for consumption, which included maintaining the few home gardens that were in place.

The role of women is acknowledged locally, as local men were aware of how absence

129 of "the female boss" translated into less nutritious fast-made meals (Piñeres 2015,

Vergel 2015). Farmers also mentioned that diets are more varied and nutritious when children are present, and that over time adults are less concerned about what they eat

(Segura 2015). This helps explain relationships between the stage in the household cycle and the maintenance of subsistence crops across surveyed households.

Besides the presence of women, dietary diversity in Anolaima depended on household income. All families relied on purchased foods to meet at least half of their dietary needs, and dietary diversity increased with the number of purchased foods, which in turn increased with off-farm income (AICc= 126.96; df= 15, R2= 0.22; P= 0.05) (Fig.

S2-13). This trend also modulated the contribution of animal pollination to food consumption, as most foods benefited by animal pollination were purchased (Z=

3.272; P= 0.001); which did not significantly change across seasons (Z= 871; P=

0.384) (AIC= 675.0; df= 9; R2= 0.25). These data convey how the transition towards market economies is progressively converting animal pollinated foods into luxury goods. Farmers bought many of the foods greatly benefited by animal pollination that were grown locally in the past, including passion fruits (common passion fruit or

Passiflora edulis; curuba or P. tarminiana; granadilla or P. ligularis, and gulupa or P. pinnatistipula), blackberry and tree tomato, off-farm income allowed wealthier farmers to consume imported foods benefited by animal pollination like kiwi, apple, and almonds. This suggests the maintenance of close cultural ties with former local fruits, despite changes in customs associated with the self-provision of foods for

130 consumption, and also shows how socio-economic differentiation entails changes in class identity reflected in dietary change.

Factors mediating income inequality and access to purchased foods have deep roots in

Anolaima. We found that off-farm income increased with farm size and the level of formal education (Table 3). Thus, our data provides evidence linking land access, social mobility represented in the level of education, and income, suggesting that social structures have strong impacts on food access. Traditional farmers are highly vulnerable to and trapped in food insecurity, as they have limited possibilities to access more stable livelihoods, and their resource base is progressively undermined.

Income inequalities can have magnifying effects when it comes to purchasing food.

Households across socioeconomic segments spend a higher proportion of income as their salaries are smaller (Regmi et al. 2001), thus households with lower income have low elasticity to adequate food consumption by purchasing foods, which makes them even more vulnerable to cases of external perturbations affecting food access.

Being dependent on subsistence crops for food and nutritional security, financially- poor households would be greatly affected by pollinator declines. Smith et al. (2015) and Chaplin-Kramer et al. (2014) warned about these impacts and suggested that malnourished rural communities should grow more pollinator independent crops with high contents of micronutrients such as sweet potato. Ironically, this crop was grown in Anolaima decades ago, but its low commercialization and progressive simplification of agroecosystems eroded both the crop and its associated ecological knowledge (Pulido 2015).

131

Conclusions

This study describes the intersections between rural livelihoods and animal pollination in Anolaima, a tropical region undergoing agrarian transitions where socio-economic factors associated to agrarian change have altered the relationships between pollinators, food production and human diets. In this town, agrarian change has influenced the richness of foods grown and consumed, and the contribution of animal pollination to such foods. Animal pollination benefited households mainly through crop production, as compared to food consumption, and socio-economic and cultural factors including household size, farm size, income, agricultural management, education and gender relationships differentially influenced food production and access in the region. The local production of crops that benefit from animal pollination was of great importance for larger households with small farms and for elder farmers, who currently rely on subsistence crops. This suggests that, given the deepening of socio-economic inequalities and current trends in agricultural simplification, pollinator declines may impact diets and also access to limiting micronutrients of marginalized households. Meanwhile, animal-pollinated foods become purchased luxury foods increasingly inaccessible for low-income farmers.

Decades ago, agricultural industrialization aimed to produce massive volumes of

"cheap" food to reduce hunger and poverty of landless people and smallholders, at the cost of a crisis in biodiversity and in the sustainability of food systems. Currently, the

132 world is concerned by the fact that poverty and hunger still affect more than two billion people, and malnourishment is increasing in developing countries (Pelletier et al. 1995, Krawinkel 2012, McGuire 2013). Those concerns add to the challenge of producing food for a growing human population without further hindering biodiversity. Most popular answers to reduce malnourishment involve "business as usual", or the bio-fortification of cheap staples (e.g. golden rice) grown in industrialized fields (Bouis 2007). Other approaches propose propagating clones of nutritious fruit plants that do not benefit from animal pollination such as pollinator- independent hermaphrodite papaya breeds derived from old varieties that required animal pollination (Free 1993). An alternative paradigm aiming to reconcile agrobiodiversity and human food and nutritional security involves the protection and promotion of diversified traditional farming systems (Toledo and Burlingame 2006,

Frison et al. 2011, Kahane et al. 2013).

Tropical diversified systems materialize ecological rationalities kept by elder farmers or antiguos engaging in practices that maintain and enhance crop diversity, encourage diverse pollinator communities, promote stability in food access, and praise the long- term relationships between humans, animals and plants. Because of their multifunctionality and low impact, these systems represent a viable economic and ecological alternative for food production and social welfare. However, and despite being seen as an alternative to the current food and biodiversity crisis, traditional agriculture in the tropics –along with its ecological and social value–is fading.

133 In Anolaima, traditional small farms are more and more segregated as agroindustrial fields expand in the landscape, which threatens many ecological functions, including animal pollination. Besides spatial segregation, the viability of traditional diversified farming is strongly mediated by socio-political factors shaping current food systems, where agricultural productivity does not equal profitability, sustainability or autonomous access to continuous, nutritional and preferred food sources. Stone

(2002) mentioned that a lack of attention to issues of equity and social justice can mean that increases in productivity have no or even negative impacts on food security. In Anolaima equity and social justice are closely related –yet not limited– to asymmetries in land access restricting households' autonomy to grow enough food to secure a livelihood, and to capital through credits demanding a minimum area to grow crops.

Besides pressures on productivity, failures in commercialization, biased policies and cultural change are weakening the value of traditional agriculture as an activity that supports the creation of meaningful livelihoods. These processes, happening in

Anolaima and most likely in other developing regions, are promoting the disappearance of traditional agri-food territories. Unless more attention is paid to reduce social equality and its multiple implications on ecological functioning in rural lands, agri-food territories will further erode, which would entail losing at least 50% of the current global food production, including a high proportion of nutritious foods benefited by animal pollination.

134 Acknowledgements

We thank Y. Pulido, N. Palacios, A. Pulido for their assistance with data collection.

We thank B. Martinez, Y. Pulido, A. Bermudez, M. Tolosa, M. Arévalo, V. Estevez,

L. García, J. Silva, D. Camelo, F. Cristancho, G. Piñeres, F. López, D. Diaz, N.

Osorio, A. Cediel, L. Pulido and C. Murcia for providing access to study sites and information about agricultural management. Support for this research was provided by a Fulbright-Colciencias Scholarship, a Rufford Small Conservation grant, a UCSC

Heller Agroecology Grant, two UCSC Environmental Studies Departmental research grants, a Social Sciences Research Council - International Dissertation Research

Fellowship, and field supplies from Idea Wild.

135 Table 2. Socio-economic characteristics and variables regarding crop and dietary diversity across Anolaima. The first section of the table presents information regarding the community survey (n= 320). The second section of the table presents information obtained from 16 focus households.

Livelihood characteristics Average CV (%) Max Min Community survey (n= 320) Number of household members 2.43 0.54 7 1 Average age of household members 47.49 0.36 81 12.8 Level of formal education Secondary - College None Percent of women in household (%) 46.5 0.66 0 100 Farm size (ha) 2.52 1.07 17.92 0.25 Percent people born in Anolaima (%) 58.18 0.75 100 0 No. subsistence crops 4.13 0.78 17 0.5 No. subsistence animals 1.69 0.61 5 0.5 No. of cash crops 2.35 0.72 0 6 No. off-farm activities 1.22 0.55 0 3 No. livelihood activities 6.38 0.36 1 14 No. months in need 1.84 1.15 12 0 Focus households (n= 16) Use of synthetic agrochemicals 8 households Presence of women in the household 10 households Number of household members 2.56 0.67 6 1 Average age of household members 50.2 0.28 63 21.5 Number of children 0.63 1.46 3 0 Number of livelihood activities 3.31 0.39 6 1 Farm size (ha) 2.97 1.06 14.08 0.8 Average Net income (USD) 10214.86 0.16 54587.50 1267.17 Average Per capita income (USD) 3641.36 0.93 12105.50 633.59 Average On-farm income (USD) 6970.75 2.05 56007.50 0.00 Average Off-farm income (USD) 3182.74 1.90 24475.33 -1420.00 No. Foods consumed per year 78.00 0.23 100 42 No. Foods consumed per week 46.06 0.25 74 30 No. Foods grown on farm 20.44 0.38 31 7 No. Plants grown on farm 16.5 0.40 27 6 No. Foods purchased 50.8 0.15 90.82 56.67 No. Plants purchased 70.86 0.14 88.89 54.39 Percentage foods grown on farm (%) 29.31 0.36 43.33 9.18 Percentage plants grown on farm (%) 29.14 0.35 45.61 11.11

136 Table 3. Correlations among socio-economic characteristics of sixteen focus households in Anolaima. Values correspond to Pearson correlation coefficients between pairs of variables. Correlation Selected variable Correlated variables coefficient Household size -0.83*** Number of children -0.93*** Average age of Number of livelihood activities -0.67** household members Income (including domestic costs) -0.53* Presence of women Household size 0.64** in the household Number of livelihood activities 0.59** Household size 0.88*** Number of livelihood activities 0.71*** Number of children On-farm income 0.52* Level of education Off-farm income 0.68** Total number of Household size 0.71** agricultural and non- Presence of women in the household 0.55* agricultural Number of children 0.63* activities Number of livelihood activities 0.76** On-farm income 0.60* Household size 0.78*** Average age of household members -0.67** Number of Presence of women in the household 0.59* livelihood activities Number of children 0.71** Total number of agricultural and non- 0.76*** agricultural activities Income 0.55* On-farm income 0.52* Household size 0.58* Number of children 0.23* Income Total number of agricultural and non- 0.56* agricultural activities Number of livelihood activities 0.55* Per capita income 0.72** Household size 0.58* Number of children 0.57* Total number of agricultural and non- On farm income 0.6* agricultural activities Number of livelihood activities 0.52* Income 0.99*** Per capita income 0.7** ***P<0.001; ** 0.001

137

Figure 7. Rank-abundance graphs for crops grown for self-subsistence (a) and commercial (b) purposes across farms in Anolaima (n= 320 households).

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l P 0 Essential Great Moderate Low None Unknown Pollination contribution Figure 8. Contribution of animal pollination to foods grown in Anolaiman households (n= 320). Foods produced across farms were classified according to their production goal (for self-subsistence of commercial agriculture). Panels represent different degrees of contribution by animal pollination to foods eaten by humans as described in Klein et al. (2007) (Essential = 95% of animal contribution to fruit production, Great= 65%, Moderate= 25%, Low= 0.05%, None = 0%).

139

Figure 9. Socio-economic factors influencing the richness of subsistence crops in Anolaiman households (n= 320). Panels represent the drivers of the richness of subsistence crops across the community (a-c) including household size (a), the number of off-farm income sources (b), and the number of cash crops (c).

140

Figure 10. Seasonal contribution of animal pollination to foods consumed by households in Anolaima (n= 16). Foods consumed across households were classified according to their source: off farm (purchased) or on-farm; and to season: dry season (February-March), Harvest season (June-July), and wet season (October-November). Panels represent different degrees of contribution by animal pollination to foods eaten by humans as described in Klein et al. (2013) (Essential = 95% of animal contribution to fruit production, Great= 65%, Moderate= 25%, Low= 0.05%, None = 0%).

141

Figure 11. Factors influencing the richness of foods consumed in Anolaiman households (n= 16). Panels represent socio-economic variables influencing dietary richness across focus households including the presence of women in the household (a) and the number of purchased foods (b).

142 Supplemental material

Data analysis - Methods S1

We tested whether the contribution of animal pollination (yes, no) to crops grown across households changed depending on the production goal of each crop

(subsistence or commercial). For this, we fitted a generalized linear mixed model

(GLMM) with production goal as fixed factors, and household as a random factor. In addition, we tested whether the contribution of animal pollination (yes, no) to the frequency of foods consumed across households significantly changed across seasons

(dry, harvest, wet) and food source (grown or purchased). For this, we used also fitted a GLMM with season and source as fixed factors, and household as a random factor.

We run both GLMMs in the glmer function in R (Warton and Hui 2011) using a binomial error.

We ran bi-variate Pearson correlations between pairs of socio-demographic factors to evaluate their influence on crop diversity, and conducted a separate analysis for focus households including income to evaluate factors influencing weekly dietary diversity.

We also tested what and how socio-economic factors influenced the diversity of subsistence crops, household income and dietary diversity through generalized linear models (GLM) in R (R Development Core Team 2014) using the glmulti package

(Calcagno and de Mazancourt 2010). For these analyses, we only used variables with the highest correlation coefficients or that were uncorrelated with other factors (Table

4). We report conditional averages for significant model factors, AICc values, p- 143

values and multiple linear R2 values for the best predicting models. When more models were within 2 AIC points of the next best model, we averaged models using the R MuMIn package and used conditional averages to account for significant model factors (Bartoń 2013).

144

Figure S1-12. Distribution of livelihood activities across Anolaiman households (n= 320).

145

Figure S2-13. Socio-economic drivers of income in Anolaiman households. Panels represent the drivers of total monetary balance including the use of synthetic agrochemicals (a) and the number of subsistence crops (b).

146

Figure S3. Factors influencing farmers’ perceptions about livelihood insecurity across Anolaiman households (n= 320). Panels represent socio-economic variables influencing the number of months in need, used as a proxy of household insecurity, including the level of formal education (a), the use of synthetic agrochemicals (b), and household size (c).

147

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158

Chapter 3:

Local and landscape habitat influences on bee diversity in agricultural

landscapes in Anolaima, Colombia

Abstract

Agricultural intensification is a main driver of biodiversity loss and is associated with bee declines. Bees are highly sensitive to environmental change, and while their diversity declines in simplified habitats far from undisturbed areas, bees respond to agricultural practices and habitat configuration at different scales. In mountainous tropical agroecosystems the influence of local and landscape habitat factors on the composition of bee communities is still underexplored. We conducted a study in

Anolaima, Colombia, and examined the local and landscape habitat factors influencing bee abundance and diversity, and changes in bee generic and tribe composition. We surveyed bees, measured local habitat features such as flower abundance, tree diversity, ground cover and the vertical structure of the vegetation, and evaluated land cover types and landscape features in seventeen farms. We found that elevation, the vertical structure of the vegetation and landscape structure influenced the structure of the overall bee community. While local factors predicted the response of most individual bee groups, landscape factors influenced the abundance of Apis and Trigona, two genera with disproportionate high abundances compared to other bees across study sites. We also found that human constructions serve as refugees for several bee genera. Our paper suggests a process of biotic homogenization with the loss of bee diversity and concurrent spread of Apis and 159

Trigona in managed landscapes. We also highlight the high sensitivity of native bees to habitat configuration and disturbance and the importance of traditional management systems for the conservation of bee communities in mountainous tropical agroecosystems.

Introduction

Land use change is a main driver of biodiversity declines. Most land conversions are associated with the expansion of croplands, habitat loss and fragmentation, and biodiversity loss (Green et al. 2005, Tilman et al. 2011, Grau et al. 2013, Lambin et al. 2013). Currently, agricultural land conversion is concentrated in the tropics, where most new agricultural lands - especially between 1980 and 2000 - came at the expense of undisturbed and disturbed forests (Gibbs et al. 2010, Meyfroidt et al.

2010) raising important global concerns about biodiversity conservation (Laurance et al. 2014). Furthermore, agricultural intensification, or changes in the actual management within farms may exacerbate the impacts of land use conversion for biodiversity (Tscharntke et al. 2005, Flynn et al. 2009, Williams-Guillén and Perfecto

2010, Mogren et al. 2016). Thus, factors acting at multiple spatial scales (within farm vs. across landscapes) may have strong impacts on diversity and alter processes structuring biotic communities (Tscharntke et al. 2005, Tscharntke et al. 2012).

Yet, the effects of environmental change on community composition are not random

(McKinney and Lockwood 1999, Tylianakis et al. 2008, Gámez-Virués et al. 2015).

Different traits make species susceptible or tolerant to disturbances (Verheyen et al. 160

2003, Hopfenmuller et al. 2014, Rader et al. 2014). Hence, changes in biotic communities depend on the abundance of different taxonomic groups and on particular traits that mediate species’ responses to the magnitude, frequency and spatial patterns of disturbance (Olden et al. 2004, Neal M. Williams 2010). In light of environmental change, communities can undergo biological homogenization whereby sensitive species are lost from a regional pool of species or experience range contraction and tolerant species increase their ranges and abundance (McKinney and

Lockwood 1999, Gámez-Virués et al. 2015). These non-random changes can cascade to affect the functional traits within a community, and thereby affect ecosystem functioning, with important implications for ecosystem services (Suding et al. 2008,

Zavaleta et al. 2009).

Bees provide ecosystem services, but bee communities and populations are affected by environmental change. Most tropical crop plant species (>85%) require or benefit from visits by native and non-managed bees for successful reproduction (Roubik

1995, Klein et al. 2003, Hoehn et al. 2008, Rosso-Londoño 2008, Martins 2013,

Motzke et al. 2016). Thus, conservation of diverse bee communities is important for both food production and tropical plant communities (Freitas et al. 2009). Bee communities and populations are affected by land use modifications at both local and landscape scales (Kremen et al. 2002, Kremen et al. 2004, Brosi et al. 2007a, Ricketts et al. 2008, Carré et al. 2009, Mandelik et al. 2012, Kennedy et al. 2013, Forrest et al.

2015, Sydenham et al. 2016). Bee diversity increases with flowering plant diversity and the availability of nesting sites (i.e. bare soils, mature wood) (Kennedy et al. 161

2013, Torné-Noguera et al. 2014, Quistberg et al. 2016). Agricultural practices such as tillage and sowing that reduce available resources, along with pesticide use, negatively affect bees and drive population declines (Potts et al. 2010, Kohler and

Triebskorn 2013, van der Sluijs et al. 2013). At the landscape scale, land use diversity, connectivity and proximity to undisturbed forest fragments benefits bees (Brosi et al.

2007b, Ricketts et al. 2008, Carré et al. 2009, Jauker et al. 2009, Klein 2009, Jha and

Vandermeer 2010, Marini et al. 2012, Basu et al. 2016, Quistberg et al. 2016). In simplified landscapes, local factors are more important predictors for bee community composition, whereas these same factors are less important in highly diverse landscapes (Kremen et al. 2002, Steffan-Dewenter et al. 2002, Tscharntke et al. 2005).

Furthermore, local and landscape factors differentially influence bee species with specialist and low-dispersal ability species being more strongly affected by intensification and fragmentation compared with generalist, social, and high-dispersal ability species such as Apis mellifera (Brosi et al. 2007a, Jha and Vandermeer 2009).

Most research evaluating how local and landscape factors influence patterns of bee diversity in agricultural landscapes focuses on temperate latitudes, where farms tend to be large (>10 ha) and homogeneous (Steffan-Dewenter et al. 2002, Kremen et al.

2004, Holzschuh et al. 2008) but see (Klein et al. 2002, Garibaldi et al. 2016, Motzke et al. 2016). However, the effects of local and landscape factors on tropical mountainous bee communities is still underexplored (but see Klein et al. 2002, Brosi et al. 2007a, Badano and Vergara 2011). Understanding how local and landscape disturbance affects bees in heterogeneous agricultural landscapes is important for 162

designing conservation strategies in areas with high dependence on non-managed bees. In this study, we ask how differences in local habitat structure and landscape configuration affect bee communities across a heterogeneous, mountainous agricultural landscape in Anolaima, Colombia. We asked (1) Which local and landscape factors influence bee abundance and diversity (species richness, evenness and dominance)?; (2) Which local and landscape factors drive changes in generic and tribe abundance and composition across farms in Anolaima?, and (3) Is the availability of different land use types associated with generic richness and abundance of different bee tribes? We predicted that (1) farms with a higher percent of undisturbed habitat, more complex vegetational structure, lower agricultural disturbance, and surrounded by a higher percent of complex habitat at the landscape scale will host higher abundance and richness of bees; (2) local factors will have greater influence on bee community composition compared with landscape factors; and (3) bee generic richness and abundance of specific tribes will vary depending on availability of land use types.

Methods

Study site

We conducted this study in Anolaima, in the eastern slope of Andes mountains in

Colombia (Fig. 14). This municipality extends between 900 and 2800 m.a.s.l., with an average elevation of 1650 m.a.s.l.. Most lands in the municipality have steep slopes

(50% or higher). The traditional precipitation regime is bimodal, with marked dry seasons between Dec - Mar and Jul - Sept, mean annual precipitation of 1232 mm, and 163

average relative humidity between 70% (dry seasons) and 80% (rainy seasons). Life zones in the municipality transition between cloud-submontane forest and tropical dry forest, but most land cover in the area is comprised of cattle ranching (41.6 % of total area) and cropland (19.3%). Coffee is the most extensive crop covering 10% of the total area. Small farms (<5 ha) represent 92.6% of private landholdings in the area, and cover 53% of the total land area in the municipality (Anolaima 2016).

We worked in seventeen farms chosen to represent a gradient of management intensification. Farms were separated by a minimum of 2 km and represented the full range of agricultural management types present in Anolaima. Land uses included secondary forests; permanent crops arranged as agroforests (e.g. shaded coffee intercropped with native trees, mango, guava, and citrus); shaded crops with simplified shade (coffee intercropped with plantain); unshaded staple crops (e.g. sugar cane, and diversified plots with tomato, guatila, squash, corn grown for self-consumption); unshaded commercial short-cycle crops (e.g. conventional squash, peas, beans, and tomato crops); fallow lands or unmanaged areas undergoing natural regeneration; and pastures. Permanent shaded crops (e.g. coffee, cacao) and traditionally managed staple crops (e.g. guatila, squash, plantain, corn) are managed in diversified systems seldom treated with synthetic biocides. In contrast, conventional short-cycle crops are monocultures or polycultures intensively managed with synthetic biocides and with short fallow periods. Because of the average farm size (1.5 ha), monocropping seldom extends over large areas in this region (Alcaldía Municipal de Anolaima 2016).

164

Experimental design

We measured local and landscape habitat features for each study farm. To survey vegetation, we established a 1-ha plot centered on a random point within each farm and divided it into sixteen 25 m x 25 m quadrants (Fig. 15). We classified land use types and measured canopy cover in each 25 m x 25 m quadrant. Within each quadrant, we established 4 random 2 m x 2 m sub-plots, 64 in total per farm, in which we measured ground cover and flower abundance. In addition, we established a 200 m-radius circle around the center of the 1-ha plot and divided it into six pie pieces. In each pie piece we randomly established a 15 m x15 m plot in which we measured arboreal vegetation. We conducted landscape analyses within circles of 200 m, 500 m and 1 km radii around the 1-ha plot.

Local and landscape vegetation sampling

We measured local vegetation features within each farm. Within each 2 m x 2 m sub- plot we estimated ground cover (percent of pasture, herbs, rocks, leaf-litter, mulch, and bare soil), measured height of the tallest herbaceous vegetation, and counted the number of flowers on herbs and shrubs. Within 25 m x 25 m quadrants we counted the number of flowering trees, and measured canopy cover with a concave spherical densitometer by averaging measurements at the center, and 10 m to the east, west, north and south of the quadrant center. We also observed and registered the land use of each 25 m x 25 m quadrant and then grouped them in one of seven categories: (1) forest/agroforest; (2) crops with simplified shade; (3) unshaded crops with traditional management; (4) fallowed lands; (5) pastures; (6) unshaded crops with conventional 165

management; (7) constructions (e.g. buildings, sheds); and (8) border of roads. We collected this data on the same days that bees were collected in each site. Within each

15 m x 15 m plot, we estimated the vertical structure of the vegetation (percent of the vegetation reaching 1 m, 1-3 m, 3-5 m, >5 m height), counted the number of trees (>5 cm DBH), and registered tree morpho-species, tree height, and tree diameter at breast height (DBH). We measured tree diversity, tree size, and the vertical structure of the canopy between Jun - Aug 2015.

We analyzed the configuration and composition of the landscape surrounding each farm with SPOT satellite images and digitalized aerial photographs from Instituto

Geográfico Agustín Codazzi. To estimate landscape composition and determine the landscape context of each site, we classified images and created four land cover categories: (1) complex habitat (agroforest, secondary and primary forest); (2) unshaded crops; (3) pastures; and (4) eroded soils. We estimated the percent area of each land cover category within 200 m, 500 m and 1000 m of the center of each farm.

We also calculated the nearest distance from the center of the bee survey plot to complex habitat, unshaded crops, and to water. We conducted these analyses in

ArcGis 10.3.

Bee sampling

We used aerial nets and observations to survey bees. We netted and observed bees between 0-3 m above ground in each 25 m x 25 m quadrant during 10 min. and walked all quadrants four times during the same day, for a total of 40 mins. per quadrant. Over 166

the four visits to each 1-ha plot, we varied the time of day each quadrant was visited to capture bees under different temperature, humidity, and sunlight conditions. We netted all bees except for Apis, Trigona (cf. amalthea and fulviventris), Tetragonisca and

Eulaema bees that we identified and counted in the field. We killed bees with ethyl acetate, placed them in dry containers, and pinned them. We determined bees to the genus level using identification keys for bees in Colombia, Panama and Brazil (Nates-

Parra 1990, Michener 2000, Nates-Parra 2001b, a, Camargo et al. 2007, Nates-Parra

2007, Moure 2008) at Laboratorio de Abejas in Universidad Nacional de Colombia.

We sampled bees in the dry (Feb-March) and wet seasons (Jul-Aug) of 2016. We registered the type of land use in which we captured each bee. All bee netting and observations took place between 7 AM and 2 PM on sunny days with low wind speed and with no rain. We took data on relative humidity, temperature, and wind speed at

8:00am and 12:00m as covariates.

Data analysis

We selected five bee abundance variables, two community similarity variables, and three bee diversity variables for inclusion in model analysis. We sampled bees in the

25 m x 25 m quadrants but aggregated bee data at the farm (e.g. 1-ha plot) scale for all analysis. For abundance, we used total bee abundance, partial abundance after excluding the two most common genera, and abundance of the three most common tribes. For community similarity, we used axis 1 of a non-metric multidimensional scaling (NMDS) analysis based on Bray-Curtis similarity for bee genera and for bee tribes. For bee diversity we used estimators of bee richness, evenness and dominance 167

using rarefied Hill numbers. Hill numbers convert basic diversity measures to

“effective number of species” numbers that obey a duplication principle. We calculated Hill numbers at three different orders (q) of diversity. Order q=0 (0D) is equal to species richness, giving more weight to rare species; when q=1 (1D) the weight of each species is based on its relative abundance; and when q=2 (2D) abundant species have a higher weight in the community (Chao and Jost 2012). We used 0D numbers as estimators of richness, the Hill estimator of evenness

(q1:0=0D/1D), and the Hill inequality factor (q2:0=0D/2D) as estimator of dominance

(hereafter dominance) across study sites (Jost 2010). Because sample size differed across farms, we rarefied Hill numbers at q=0, q=1 and q=2 to assemblages of 72 individuals with all genera, and to 31 individuals for analysis without the two most common genera. We calculated rarefied Hill numbers with the iNEXT package

(Hsieh et al. 2016) and plotted diversity profiles with the Entropart package (Marcon and Hérault 2015).

To select explanatory variables for analyses, we grouped local (all variables factors measured within 25x25 m quadrants, 15x15 m plots, and 2x2 sub-plots) and landscape (factors measured within 200 m, 500m and 1000m around farms) features as separate groups and then ran Pearson’s correlations to identify non-correlated variables within each group. Some variables (e.g. management and elevation) did not fit within any group and were included. Other variables (e.g. mulch cover or percentage of eroded soils at 1 km landscape buffer) had high numbers of zeros and were excluded. We used 12 explanatory variables in our models (Table S1). 168

To test whether local and landscape factors influence bee variables, we ran generalized linear models (GLM) in R (R Development Core Team 2014) using the glmulti package (Calcagno and de Mazancourt 2010). We tested all combinations of explanatory factors and compared Akaike Information Criterion (AIC) values to select for the best models. We report conditional averages for significant model factors, AICc values, p-values and multiple linear R2 values for the best predicting models. When more models were within 2 AIC points of the next best model, we averaged models using the R MuMIn package and used conditional averages to account for significant model factors (Bartoń 2013). To test whether factors influenced community similarity, we ran a permutational multivariate analysis of variance on bee genera and tribe similarity matrices using the R vegan package

(Dixon 2003).

To evaluate whether the availability of land use types influenced bee abundance and diversity, we ran Pearson’s chi-square tests of independence. We tested whether the frequency of occurrence of each land use type (number of 25 m x 25 m quadrants) across study sites was associated with the number of 1) captured bees, 2) abundance of the three most common bee tribes, 3) bee genera, and 4) bee tribes. All analyses were conducted in R.

Results

We surveyed 3290 bees from 57 genera, 23 tribes, 8 subfamilies, and all of the five 169

families reported for Colombia. We captured 1512 bees, and visually sampled 1778 bees. The most abundant genus was Apis (38.26 % of individuals) followed by

Trigona (cf. amalthea and cf. fulviventris) (24.79%); of other genera surveyed, 50 represented fewer than 5% of individuals surveyed (Fig. S1-20). The most abundant tribes were Meliponini (n= 1515), Apini (n= 1573) and Augochlorini (n= 99).

Diversity profiles showed large drops in the effective number of genera as the order of diversity (q) increased indicating high levels of dominance in local bee assemblages (Fig. S2-21).

Bee abundance varied with both local and landscape factors, and the factors influencing total bee abundance, abundance without Apis and Trigona, and abundance of the three most common bee tribes were different. Total bee abundance was best predicted by flower abundance, unshaded crop cover within 1 km, and elevation

(AICc= 16.24, df= 13, R2= 0.69, Fig. 16). Bee abundance increased with flower abundance (t= 3.652, P= 0.002), unshaded crop cover within 1 km (t= 3.082, P=

0.009), and with elevation (t= 2.670, P= 0.019). When we excluded the two most abundant genera, Apis and Trigona, the averaged model that best predicted partial bee abundance included flower abundance, pasture cover within 1 km, tree cover, maximum height of non-arboreal vegetation, and distance to a complex habitat fragment. Partial bee abundance increased with flower abundance and marginally decreased with pasture cover within 1 km (Table 4). Number of Apini (i.e. Apis) bees increased with elevation, flower abundance, tree cover and intensive agricultural management. While the total number of Meliponini individuals marginally increased 170

with the maximum height of herbs, abundance of Trigona increased with elevation and with vegetation between 1-3 m according to the best averaged glm model. elevation, tree cover, and agricultural management. Number of Augochlorini bees significantly increased with flower abundance, decreased with vegetation between 1-3 m, and marginally decreased with pasture cover within 1 km; but did not significantly increased with elevation, tree cover, and agricultural management (Table 4).

Bee diversity (richness, evenness, and dominance) varied with both local and landscape factors. The model that best predicted bee richness (0D) included elevation, vegetation between 1-3 m, and unshaded crop cover within 1 km (AICc= 84.84, df=

13, R2= 0.76, Fig. 17). Bee richness decreased with elevation (t= -6.406, P<0.001) and vegetation between 1-3 m (t= -18.063, P< 0.001), but did not significantly vary with unshaded crop cover within 1 km (t= 1.384, P= 0.189). When we excluded the two most abundant genera, Apis and Trigona, bee richness was influenced by different factors. Partial bee richness decreased with elevation, tree cover, and vegetation between 1-3 m (Table 4). Evenness (1D/0D) decreased with elevation (t= -

2.860, P= 0.012) and with increased unshaded crop cover within 1 km (t= -2.258, p=

0.040) (AICc= -39.86, df=14, R2= 0.55, Fig. 18). Dominance (2D/0D) was best predicted by the height of non-arboreal vegetation and unshaded crop cover within 1 km (AICc= 27.427, df= 14, R2= 0.62). Dominance decreased with the height of non- arboreal vegetation (t= -3.593, P= 0.002) and increased with unshaded crop cover within 1 km (t= 3.713, P= 0.002). Generic similarity was explained by elevation

(F=3.34, R2= 0.17, P= 0.02) and flower abundance (F= 2.49, R2 = 0.12, P= 0.05). 171

Tribe similarity was also explained by elevation (F=5.67, R2= 0.21, P= 0.007) and, marginally, by flower abundance (F= 2.82, R2 = 0.10, P= 0.07).

The number of available units of each land use across farms was not independent from the number of bees (휒2= 122.53, df=7, P<0.001), and from the richness of genera (휒2= 59.66, df=7, P<0.001), and tribes (휒2= 35.277, df=7, P<0.001) captured on different land uses. Generic and tribal richness were higher in fallow lands, constructions and borders of roads, and lower in forest-agroforests and in unshaded crops under conventional management (Table 5). Bee abundance of the three most common tribes changed across land use types (휒2= 5874, df = 7, P<0.001).

Representation of Meliponini was the highest across land uses, followed by that of

Apini (17% of individuals ± 32%) and Augochlorini (2% ± 3%). Apini was the tribe with the highest relative abundance in conventionally managed crops (73%) and in crops with simplified shade (37%). Augochlorini abundance was highest in areas surrounding human constructions (7%) and in traditionally managed crops (6%).

Abundance of other bee tribes was also highest in constructions and traditionally managed crops (Fig. 19).

Discussion

We present evidence for the effects of different local and landscape factors on bee abundance and diversity in the Colombian Andes, a region for which this type of studies are scarce. Bee abundance and diversity were influenced by several habitat factors including flower availability, elevation, and unshaded crop cover within 1 km. 172

Contrary to our hypotheses, bee abundance decreased, although diversity increased in farms with higher habitat complexity, and both local and landscape factors greatly influenced bee community composition.

Our first research question examined which local and landscape factors influenced bee abundance and diversity. In general, bee abundance was predicted by flower abundance and elevation. Our results coincide with other studies documenting a positive response of bee density to floral resources (Torné-Noguera et al. 2014), and the unresponsiveness of some groups such as Meliponini to flower availability (Brosi et al. 2007). We found overall bee abundance was greatly influenced by the abundance of Apis and Trigona bees in areas with high flower abundance. Other studies have documented the positive responses of Apis to the spatial aggregation of floral resources (Plascencia & Philpott 2017) and mass-flowering crops (Rader et al.

2009, Holzschuh et al. 2011 but see Boreux et al. 2013), and have suggested Apis can exclude other bees from accessing flowers through interference or exploitative competition (Wilms et al. 1996, Montero-Castaño et al. 2016). Like Apis, Meliponini are social and generalist bees. While there is niche overlap among Meliponini species, and between Meliponini and Apis bees, there is resource partitioning among

Meliponini but not between Meliponini and Apis (Wilms et al. 1996). Thus, a possible explanation for the differential influence of flower abundance on different bee groups may be mediated by their competitive interactions with Apis.

Other factors influencing bee abundance may be related to traits specific to bee 173

groups. For example, Augochlorini abundance decreased with pasture cover within 1 km and increased with % vegetation between 1-3 m. In our study, percent of vegetation cover between 1-3 m was negatively correlated with the percent of vegetation between 0-1 m, which is the strata at which we found more flowering herbs in unshaded land uses. Further, pasture cover within 1 km was negatively correlated with forest or agroforest cover within 1 km. In general, Augochlorini are associated to forest areas (Zillikens et al. 2001, Wcislo et al. 2003, Brosi et al. 2007a), are soil or wood nesters, and use more flowering herbs and vines as feeding resources in comparison with eusocial bees (Wilms et al. 1996). Thus, use of nesting and food resources by this tribe may explain their abundance patterns.

Elevation had a strong influence on the abundance of Apis and Trigona bees.

Elevation may act as a filter structuring biological communities because of its inverse relationship to temperature, which may influence species distributions based on their tolerance to cold environments (McCoy 1990, Rahbek 2004) and to climatic fluctuations, among other biophysical variables (Hodkinson 2005). Apis and native

Trigona cf. amalthea and T. cf. fulviventris have broad altitudinal and geographic ranges (Gonzalez and Engel 2004, González et al. 2005, Nates-Parra 2016) as well as high reproductive capacities with colonies of ~10000 and >2500 individuals respectively (Roubik 2006). The combination of these two factors may explain the high abundance of these genera in our study region, yet it still does not totally explain their positive response to high elevations. It is interesting to consider that, when we excluded these hyperabundant genera, bee abundance was not responsive to elevation. 174

This suggests other mechanisms that favor some groups and undermine others may be at play in the highlands of this region.

Bee richness and evenness were also predicted by elevation. We found a strong gradient of bee richness within a relatively narrow altitudinal range (1230 m.a.s.l. –

1900 m.a.s.l.), which is considered a hump in general altitudinal-diversity gradients

(Rahbek 2004). Potts et al. (2012) found richness of bee taxa decreased with elevation in the Alps due to thermal tolerance of bees found along the elevation gradient. This is consistent with the richness gradient we found, which may also be influenced by the response of different groups to other conditions changing with elevation such as agricultural disturbance. In our study region elevation was positively correlated with the percent of eroded soils at the landscape scale (500 m and 1 km radii buffers), and the number of land use units on pasture and conventionally managed crops increased with elevation. This suggests rates of disturbance increase with elevation, possibly acting as a strong environmental filter excluding species associated with forests and complex habitats (Hopfenmuller et al. 2014, Gámez-Virués et al. 2015) and favoring species with high tolerance to disturbance. This may explain the reduction of rare species and the high presence of Apis and Trigona bees in high elevations, which is reflected in an inverse relationship between evenness and elevation.

Bee richness and evenness decreased and dominance increased with unshaded crop cover at the landscape scale. The percentage of complex habitat within 1 km across study sites was negatively correlated with crop cover. Thus, our results suggest that 175

changes in dominance within communities are associated with the availability of complex habitat at the landscape scale, also found in other studies (Brosi et al. 2007a,

Jha and Vandermeer 2009, Boreux et al. 2013). Changes in dominance may be associated with the negative responses of rare solitary species to landscape simplification (Brosi et al. 2007a, Zurbuchen 2010, Le Féon et al. 2013, Carman and

Jenkins 2016), and with the ability of some groups to equally use complex or simplified habitats. Apis and T. spinipes, closely related to T. cf. amalthea, have been considered hyper-generalist species that do not show negative responses to environmental disturbance and occupy simplified lands (Giannini et al. 2015,

Magrach et al. 2017), thereby increasing their abundance within the community in areas unfavorable for other bees (Veddeler et al. 2006, Giannini et al. 2015). Thus, although we cannot differentiate effects of elevation, agricultural disturbance and landscape simplification, these factors and their interaction may sort bee groups in and out of local bee assemblages in this region.

Vertical structure of the vegetation and flower abundance influenced bee richness as well. The stratum at which we found bees was 0-3 m, thus bees at higher strata were not sampled and these results may reflect our sampling bias. However, a study conducted along an ecological succession gradient using different sampling methods reported bee richness and abundance increased in low vegetational strata, and decreased in areas with dense canopy cover (Smith-Pardo and Gonzalez 2007). In general, dense canopy reduces sunlight reaching the understory, which in turn influences flowering of herbs (Holt 1995). Bee activity may follow the distribution of 176

flowers in the vertical strata (Smith 1972), which may explain our results.

Our second research question addressed changes in bee community composition.

Changes in the composition of bee communities were influenced by elevation and flower abundance. This is consistent with the elevation-richness gradient we found, and may be explained by the degree of specialization and distribution of different bees in our study region. Specialization of plant-pollinator interactions declines with increasing elevation (Rasmann et al. 2014), and biological groups in mountainous regions have narrower ecological niches and altitudinal distributions as elevation decreases (Janzen 1967, McCoy 1990, Hodkinson 2005). The degree of specialization along elevation gradients may also interact with negative effects of disturbance, thus the changes in community composition in our results may indicate either genera turnover or differential loss of species along the altitudinal range. This has additional implications in light of climate change. Studies have shown increasing temperatures and their influence on thermal tolerance have driven range shifts of different organisms towards higher latitudes and elevation (Sheldon et al. 2011). However, shifts do not only depend on physiological responses but are conditioned on species interactions such as competition and mutualism, and on variation in dispersal abilities

(Gilman et al. 2010). Further studies could target range shifts of bee communities in

Anolaima, where environmental change and dominance of highly competitive species are concentrated in areas with higher elevation, possibly influencing range shifts.

Our third research question evaluated whether the availability of different land uses 177

was associated with differences in the diversity and abundance of bee genera and tribes. The influence of local and landscape habitat factors on bee abundance and diversity can be linked to current land uses in the region. In general, abundance and richness was higher in low-impact land uses, and in areas associated with human constructions. Unshaded traditional crops and fallow lands can have high floral abundance and diversity (Motzke et al. (2016). Thus, plant richness may beget bee richness in these land uses. Also, we found nests of different groups (Paratrigona sp.,

Nannotrigona sp., Partamona sp., Megachile sp., Anthidium sp., Melitoma sp.,

Euglossa sp., Centris geminata, Centris adani) in human constructions, and foraging on flower and medicinal gardens and on forbs surrounding houses. Constructions offer areas with favorable features for nest thermoregulation and unmanaged flowering plants may represent continuous floral resources. Thus, human resources may have inadvertent yet important positive impacts on bee populations.

We did not find high bee abundance or richness in habitats with high structural complexity i.e. forest or agroforests. Most areas in this land use correspond to shaded coffee crops. In this region, farmers manually exclude forbs that grow despite the low incidence of light into the understory, and rain-fed coffee shrubs typically bloom synchronously only during two or three days a year. This means the understory of this land use does not offer a continuous availability of floral resources for bees. When flowering, trees may offer feeding resources at the canopy level. Tree availability positively influences bee diversity (Jha & Vandermeer 2010) and the long-term availability of flowering trees positively influences abundance of solitary bees in 178

shaded coffee agroforests in Mexico (Fisher et al. 2017). Some solitary bees are associated with high forest strata, even at the end of the flowering season, perhaps due to supplemental floral resources provided by honeydew and sap from the canopy

(Ulyshen et al. 2010). Besides food sources, trees also offer nesting resources. Nates et al. (2007) found living trees were the most frequent nesting substrate for stingless bees in eastern Colombia. We frequently found Meliponini nests in Inga trees or in abandoned bird nests in citrus trees found in shaded coffee areas. Other studies have found Augochlorini nest in wood and even in bromeliads growing on trees (Zillikens et al. 2001, Wcislo et al. 2003). Therefore, despite the understory of agroforests is not greatly used by bees, the canopy may offer important resources for bees in Anolaima.

However, a dense canopy or the presence of high flowering resources distributed across the landscape may influence negatively the local provision of pollination services to coffee shrubs (Boreux et al. 2013).

We also found evidence for the negative effect of conventional crops for bee richness, despite their smaller scales (<1 ha) when compared to other agricultural landscapes.

Conventional crops in this region are both monocrops and polycrops managed with high agrochemical use (e.g. carbofurans, organophosphates, chlorpyrifos and neonicotinoids, depending on the crop composition). For example, chlorpyrifos and neonicotinoids are systematically used twice a week on tomato for protection from white flies. In extreme cases, application mixtures also include antibiotics to treat cattle from Dermatobia flies. Apis and Trigona were using floral resources in these crops. This suggests bees have different degrees of tolerance to chemical disturbance. 179

For example, while Apis bees and the stingless bee Partamona helleri have different resistance to certain pesticides, both are negatively impacted by mixes of biocides

(Tomé et al. 2017). Thus, species less sensitive to pesticides can thrive in areas with high-impact management, subsidizing the pollination of plants where other bees cannot tolerate agrochemical disturbance. However, areas with high agrochemical disturbance represent a sink for rare bee species yet also a potential threat for bees with relative high resistance to agrochemicals in Anolaima.

Conclusions

Different local and landscape factors influence bee abundance and diversity in

Anolaima. Some factors were associated with the increase in abundance of two hyper- generalist groups, Apis and Trigona, and with reductions in the representation of rare species, reflected in changes in evenness and dominance within local bee assemblages. This suggests a process of biotic homogenization with the loss of some species and the spread of others, especially in high-elevation areas. In addition, we found that factors that may directly affect bee physiology, such as elevation, interact with resource availability and space to influence the composition of bee communities.

We found that land use types such as unshaded conventional crops have negative impacts on bee abundance and diversity, despite the high heterogeneity of agroecosystems in the study region, and that other land uses such as pastures may not benefit some bee groups but are not adverse for others. This suggests bee communities are highly responsive to agricultural management in small-scale farming systems. Our study calls for attention to assess the effect of environmental change on 180

bee communities in mountainous regions where climate change may influence elevational range shifts, such as in the Colombian Andes. This study also highlights the importance of traditional management systems and of smallholder agriculture for the conservation of bee communities in transitioning tropical agroecosystems.

Acknowledgements

We thank N. Palacios, Y. Pulido, L. Casallas, R. Pinto and S. Currea for their assistance with data collection; J. Maldonado, N. Florez, J. Gomez, H. Triana for assistance in bee identification, and R. Ospina for his collaboration at LABUN. We thank A. Martinez for his assistance with GIS analyses, and C. Cordoba for her insights on the study region. We thank B. Martinez, Y. Pulido, A. Bermudez, M.

Tolosa, M. Arévalo, V. Estevez, L. García, J. Silva, D. Camelo, F. Cristancho, G.

Piñeres, F. López, D. Diaz, N. Osorio, A. Cediel, L. Pulido and C. Murcia for providing access to study sites and information about agricultural management.

Funding for the research was provided by a Fulbright-Colciencias Scholarship, a

Rufford Conservation grant, a U. of California - Santa Cruz Heller Agroecology

Grant, a U. of California - Santa Cruz Environmental Studies Departmental research grant, a Social Sciences Research Council International Dissertation Research

Fellowship, and equipment donation by Idea Wild to M. Cely.

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Table 4. General linear models (GLM) predicting the bee abundance, richness and evenness of local bee assemblages after excluding the two most abundant genera, Apis and Trigona; and GLMs predicting the abundance of the three most common bee tribes, and the abundance of the genus Trigona. Dependent Predictors AICc df R2 variable Flower abundance***, % pasture cover within 1 kmns, Abundance Tree coverns, Height of non- 167.1 15 0.43 (no Apis - Trigona) arboreal vegetationns, Distance to complex habitat ns, Elevationns Richness (no Elevation*, Tree cover **, 66.705 13 0.63 Apis - Trigona) % vegetation 1-3m** Tree cover*, % vegetation 1- Evenness 3m *, Elevation*, Flower 70.206 13 0.60 (no Apis - Trigona) abundance *, % pasture cover within 1 kmns Elevation***, Flower Apini abundance abundance **, Tree cover **, 197.16 12 0.77 Agricultural management** Meliponini Height of non-arboreal 176.47 12 0.23 abundance vegetation* Elevation**, % vegetation 1- Trigona abundance 157.08 14 0.57 3m** % vegetation 1-3m **, Flower Augochlorini abundancens, % pastures 1kmns, 100.93 10 0.74 abundance Elevationns, Tree coverns AICc Conditional Akaike Information Criterion values; df Degrees of freedom, R2 Pseudo coefficient of determination *** P<0.001; ** 0.0010.05

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Table 5. Bee generic and tribal richness across land use types. Values correspond to the number of different genera or tribes (richness) captured on the different land uses found across study sites. Number of land units corresponds to the total number of quadrants (25 m x 25 m) on each land use type sampled across study sites.

Number of Generic Tribal Genera/ Tribes/ Land use type land units richness richness land units land units Unshaded crops - 129 17 8 0.13 0.06 conventional Border of roads 69 30 15 0.43 0.22 Pastures 261 38 19 0.15 0.07 Constructions 79 34 15 0.43 0.19 Fallow lands 53 13 6 0.25 0.11 Unshaded crops – 235 44 16 0.19 0.07 traditional Simplified shade 88 20 9 0.23 0.10 Forest /agroforest 211 30 15 0.14 0.07

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1

2 3 4 Figure 14. Map of Anolaima showing the seventeen study sites and land cover types 5 in the study region. Panels show farms surrounded primarily by pastures (a), 6 unshaded crops (b) and forest or agroforests (c). 7 8 9 10 11

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12 13 14 Figure 15. Diagram of the experimental design of the study. Land cover types at the 15 landscape scale were sampled at 200 m, 500 m, and 1000 m scales surrounding the 16 center of the 1-ha plot (a), arboreal vegetation was sampled within 15 m x 15 m plots 17 in 200 m circles centered on the 1-ha plot (b), bees and ground cover were sampled 18 within 25 m x 25 m quadrants in the 1-ha plot (c), and herbaceous vegetation was 19 sampled within four 2 m x 2m mini-plots on each 25 m x 25 m quadrant (d). 20

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c) and excluding the two most abundant most two excluding abundant and the c)

-

) (d), as a function of elevation (m.a.s.l) (a), flower abundance in 2 m x2 x2 m 2 m (m.a.s.l) (a), abundance in flower elevation of function a as (d), )

Trigona

and and

Local and landscape drivers of bee abundance in agroecosystems in Anolaima. Panels Panels Anolaima. bee in abundance agroecosystems drivers in Local of and landscape

. .

Apis

genera ( genera represent the drivers of bee abundance including all all (a bee the bees abundance drivers including of represent % unshaded 1km (c). buffers crops landscape the of and (b,d), in plots 21 16 Figure 22 23 24 25 26 27 28 29 200

30

and and

Apis

low strata) strata) low

-

3m(middle

-

Anolaima. Panels represent Panels the represent Anolaima.

b) and excluding the two most abundant genera ( genera abundant the most two excluding and b)

-

e), as a function of elevation (m.a.s.l) (a), the % of vegetation between 1 between % (a), (m.a.s.l) vegetation of the elevation a of as function e),

-

Local and landscape drivers of bee richness in agroecosystems in bee richness agroecosystems drivers Local in of and in landscape

) (c )

), and canopy cover quadrants 25x25 cover (e). in canopy and ),

Trigona drivers of bee generic richness including all bees (a bees all richness bee generic of including drivers (b,d 31 17. Figure

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32 33 34 Figure 18. Local and landscape drivers of bee evenness and dominance. Evenness 35 corresponds to the ratio 1D/0D (relative abundance of species/richness) (a-b), and the 36 inequity factor, an estimate of dominance within communities, corresponds the ratio 37 2D/0D (Simpsons’ concentration index/richness) (c-d). The panels represent drivers of 38 evenness or dominance as influenced by elevation (m.a.s.l) (a), the % of unshaded 39 crops in 1 km landscape buffers (b,d), and the maximum height of non-arboreal 40 vegetation in 2 m x 2 m subplots (c). 41 42 43 44 45

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46 47 48 Figure 19. Relative abundance of bee tribes in different land use types, and of land 49 use types sampled across study sites within 25 m x 25m quadrants. 50

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SUPPLEMENTAL MATERIAL Table S1. Variables measured and used (*) in the study Explanatory variables Scale Min Max Mean Value value Management* 1-ha plot 2 9 6.05 Elevation* 1-ha plot 1216 1937 1586.79 Temperature (mean) 1-ha plot 18.17 27.48 24.09 Temperature (max) 1-ha plot 18.17 30.80 26.26 Relative humidity (%) 1-ha plot 39.24 70.81 58.11 Flower abundance (No. of flowers) * 2m x 2m 533 8951 3205.88 Bare soil cover (%) * 2m x 2m 2.8 27.0 10.8 Herbaceous plant cover (%) 2m x 2m 12.6 83.3 40.8 Leaf litter cover (%) 2m x 2m 0.2 19.4 6.5 Mulch/Straw cover (%) 2m x 2m 0.0 8.1 1.6 Max. height of non-arboreal vegetation* 2m x 2m 55.52 306.20 134.92 % Pasture/grass cover (%) 2m x 2m 0.5 53.0 19.7 % Rock soil cover (%) 2m x 2m 0.0 6.3 1.2 % Canopy cover (%)* 25 m x 25 m 1.92 78.39 31.66 Number of trees/shrubs in flower 25 m x 25 m 0 6 2.5 Number of trees/shrubs 15 m x 15 m 7.00 89.00 52.48 Number of tree species 15 m x 15 m 6.00 25.00 14.48 Tree height* 15 m x 15 m 3.25 11.32 6.93 Tree DBH 15 m x 15 m 8.54 47.28 18.39 Vegetation >5m (%) 15 m x 15 m 0.63 16.67 8.08 Vegetation <1m (%) 15 m x 15 m 24.58 78.13 50.03 Vegetation 3-5m (%) 15 m x 15 m 2.29 25.63 12.70 Vegetation 1-3m (%)* 15 m x 15 m 12.71 50.58 26.46 Canopy cover (%) 15 m x 15 m 2.02 88.14 41.03 Area with forest and/or agroforest (%) 200-m radius 18.20 77.58 43.52 Unshaded crop cover (%) 200-m radius 10.39 51.33 27.27 Pasture cover (%) 200-m radius 5.94 59.45 26.02 Eroded soils cover (%) 200-m radius 0.00 18.59 1.88 Forest or agroforest cover (%) 500-m radius 23.52 74.94 43.86 Unshaded crop cover (%) 500-m radius 13.90 49.84 28.50 Pasture cover (%) 500-m radius 4.86 46.59 24.75 Eroded soils cover (%) 500-m radius 0.00 20.09 2.09 Forest or agroforest cover (%) 1-km radius 26.04 70.90 45.07 Unshaded crop cover (%)* 1-km radius 16.95 50.64 28.42 Pasture cover (%)* 1-km radius 10.19 42.38 24.67

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Eroded soils cover (%) 1-km radius 0.00 20.30 1.93 Distance to nearest unshaded crops(m)* 1-km radius 0.00 400.00 143.94 Distance to nearest complex habitat (m)* 1-km radius 0.00 300.00 50.91 Distance to nearest water source (m)* 1-km radius 3.00 1000.0 407.76 0 Dependent variables Scale Min-all Max-all Average Abundance of bees 1-ha plot 26 436 98.76 D=0 bee genera (richness) 1-ha plot 4 23 13.36 D=1 bee genera 1-ha plot 1.86 16.65 7.13 D=2 bee genera 1-ha plot 1.48 12.52 5.10 D=0 bee genera excluding Apis and Trigona 1-ha plot 2 12 7.48 D=1 bee genera excluding 1-ha plot 1.54 5.97 3.34 D=2 bee genera excluding 1-ha plot 1.27 4.47 2.43 Abundance of Trigona 1-ha plot 1 5 3.21 Abundance of Apini/Apis 1-ha plot 1 3.07 1.46 Abundance of Meliponini 1-ha plot 1 2.44 1.24 Abundance of Augochlorini 1-ha plot 1 6 3.09

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Table S2. Variables selected for data analysis, and results of Pearson’s correlations with correlated variables. The sign of the correlation coefficient denotes the direction of the correlation. Correlation Selected variable Scale Correlated variables coefficient Flower abundance 2 m x 2 m Number of tree species -0.58 Tree DBH 0.51 % bare soil 2 m x 2 m % Leaf litter 0.5 Max. height non- 2 m x 2 m % herbs 0.51 arboreal vegetation Tree DBH 0.59 Tree height 15 m x 15 m % Leaf litter 0.53 % vegetation 1-3 m 15 m x 15 m % Vegetation 0-1 m -0.66 Canopy cover 25 m x 25 m % Herbs 0.57 % Leaf litter 0.63 % Pasture -0.58 Number of trees 0.61 % Vegetation >5 m 0.87 % Vegetation 3-5 m 0.68 Management 1 Ha Leaf litter 0.71 Number of trees 0.73 Number of tree species 0.5 % Vegetation >5 m 0.78 % Vegetation 3-5 m 0.62 % Vegetation 0-1 m -0.53 Elevation 1 Ha % Vegetation 3-5 m -0.60 % Vegetation 0-1 m 0.49 % Eroded soils 1 km 0.47 % Unshaded crops 1 km 1 km % Complex habitat 1 km -0.67 % Complex habitat 500 m -0.63 % Unshaded crops 500 m 0.93 % Complex habitat 200 m -0.61 % Unshaded crops 200 m 0.94 % Pastures 1 km 1 km % Complex habitat 1 km -0.55 % Complex habitat 500 m -0.5 % Pastures 500 m 0.89 % Pastures 200 m 0.75 Distance to nearest 1 km NA NA complex habitat Distance to nearest 1 km NA NA water source

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. Rank abundance of bee genera registered across 17 farms in Anolaima,Colombia. bee of registered genera abundance in Rank . farms 17 across

20

- Figure S1 Figure

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Figure S2-21. Diversity profiles of bees captured across our study sites. Order q=0 (0D) is equal to species richness, giving more weight to rare species; q=1 (1D) is the equivalent of the exponential of Shannon index and the weight of each species is based on its relative abundance. When q=2 (2D) abundant species have a higher weight in the community and the value accounts for the inverse of Simpson index.

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Conclusions

In Anolaima, the former fruit capital of Colombia, diverse assemblages of bee and peasant lifeways contributed to the creation of an agri-food territory that has eroded after different waves of social and environmental change. One major process unraveling bee-human ecologies has been the transition from traditional to industrial agriculture, which has enhanced the loss of local ecological knowledge and practices, undermined traditional livelihoods, and prompted agrobiodiversity declines and landscape simplification. In this dissertation I show that bee declines result from land use change and intensive agricultural disturbance as proximate causes, but that underlying causes involve the transforming relationships with bees, plants and other nonhumans. In particular, social inequality influenced plant-bee-human relationships in the past, and has shaped the reciprocal influence between bees and humans in the present.

In chapter one, I reconstructed the environmental history of Anolaima, the fruit capital of Colombia, and described the intersections between plant-bee-human relationships and global and local processes affecting social and agricultural dynamics. In this region the Spanish conquest greatly transformed human and more- than-human ecologies through a biotic interchange that included the introduction of the old-world honeybee Apis mellifera; the establishment of simplified land uses including pastures and commodity crops such as sugar cane; and a primitive accumulation of the land. These transformations created major asymmetries in land 209

access and use of resources and resulted in social inequalities perpetuated over time.

The colonial regime was replaced by hacienda systems producing commodity crops, including coffee, with the regimented labor of peasants. In those times, farmers occupied and worked land owned by their lords, and developed diversified systems of food production that sustained local economies. With time, protests and attempts of agrarian reforms gave peasants land access and social freedom, secured through the presence of coffee plantations.

Agriculture in Anolaima experienced a major change after the introduction of Green

Revolution technologies during the second half of the XX century. Large-scale capitalistic industrial agriculture established to produce massive volumes of financially cheap staples at the cost of chemical disturbance, major reductions in plant and animal agribiodiversity, and landscape simplification. In Anolaima, this modern system of agricultural production has enhanced socio-economic inequalities, obliterated local ecological knowledge and traditional practices, strained ecological functioning that affected the productive potential of the region, and contributed to increase farmers’ vulnerability and marginalization. Besides effects on productivity, this industrial agriculture also induced a change from diversified to specialized economies, which interacted with the erosion of local food circuits to make livelihoods highly dependent on market dynamics. This has created a paradoxical sense of scarcity in a region well known for its abundance, but that is progressively losing its socio-ecological capacity to stand as a productive agri-food territory.

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The making of social worlds in Anolaima has been shaped by the different responses of plants, bees and other organisms to human activities. Bee communities were altered by the introduction –and posterior Africanization– of the old world honeybee

Apis mellifera. This highly competitive bee species must have induced changes in the relationships between native plants and bees in the region, and it also shaped human- bee relationships. European Apis honeybees became close companions to farmers, yet

Africanized honeybees created conflictive relationships with humans that increased disconnection from and carelessness towards bees. In addition, bee communities have been influenced by land use change and agricultural practices negatively affecting habitats and the availability of food and nesting resources. While shaded plantations buffered transformations of forest communities, the introduction of monocultures managed with synthetic agrochemicals represented ecological traps greatly influencing bee communities and promoting their homogenization. This decline in diversity affects the resilience of bee communities and limits their responses to further environmental change (Winfree and Kremen 2009, Gill et al. 2016).

The undermining of multispecies ecologies, traditional agricultural systems and landscapes is eroding the productive capacity and stability of food production in

Anolaima. In chapter two, I described how agrarian change can magnify social and environmental inequalities through its intersections with animal pollination. In

Anolaima, animal pollination facilitates the production of coffee, some fruits, and subsistence crops. Coffee is a crop with decreasing profitability in the region, and subsistence crops are underemphasized in official records of agricultural production, 211

yet they are vital for food autonomy and security, especially of large families managing small farms. Currently, fruits benefited by animal pollination are highly valued in global markets and despite they were produced and traded in Anolaima in the past, their production for commercialization was interrupted. Green Revolution technologies brought ecological disequilibria including pest outbreaks that emerged after simplifying and managing crops, and costs to control these pests became too high. Portrayed as efficient and productive, agroindustrial practices aimed to increase market competitiveness, but paradoxically, have negatively influenced the advantage and capacity of Anolaima to produce high-valued tropical fruits, being a liability for farmers seeking to take advantage of the global increases in demand and prices for pollinator-dependent crops.

Evaluating the contribution of animal-pollinated crops to food consumption revealed the effects of socio-economic inequality on food access in Anolaima. Families earning higher incomes did not rely on agricultural production to secure a livelihood or maintain agroindustrial cropfields not benefited by animal pollination. These families consumed more diverse diets, which included high proportions of purchased animal-pollinated crops. In contrast, financially poor traditional farmers keep diverse crops, yet not enough to fulfill household needs, and ate less diverse diets with high proportions of non-nutritious cheap foods. Some of the foods they consumed, important to secure food consumption during lean seasons, were benefited by animal pollinators. Despite traditional smallholders conduct practices that promote bee presence, their farms are more and more segregated by agroindustrial fields, which 212

threatens local and regional communities of animal pollinators. Given the deepening of socio-economic inequalities and current trends in agricultural simplification, pollinator declines may impact diets and also access to limiting micronutrients of marginalized households. In the meantime, farmers inducing environmental degradation would not notice pollinator declines.

The changing interdependencies with animal pollination allow for a closer examination of the biodiversity-food-health nexus. In this dissertation I approach the first part of the connection through data on the richness of foods grown and consumed, which could be complemented by data on the abundance of foods consumed to assess the nutritional contribution of animal pollination to rural livelihoods. This assessment may reflect even larger disparities in food and nutritional access and would be key to highlight the relevance of biodiversity and ecological functioning as drivers of societal stability through its influence on human health.

Acknowledging whether and how the benefits derived from "subsidies of nature" are unevenly distributed, and their broader effects to society, helps understand environmental conflicts leading to land use change and biodiversity declines, and the required approaches to mitigate or revert these declines.

As suggested in chapters one and two, agricultural modes of production operate through local decision makers, yet their effects aggregate at the regional level to influence the productive capacity and identity of a territory, and the well-being of its people and of more-than-humans. In chapter three, I evaluate the effects of habitat 213

configuration at different scales on the diversity of bees in Anolaima, and showed that bee communities are homogenizing with environmental change. The abundance of most bee groups is highly sensitive to local factors such as the structure of the vegetation, the abundance of flowers and the use of agrochemicals. This trend, like the distribution of human activities, intersects with the mountainous nature of the municipality. Bee richness is higher in the lowlands, yet decreases considerably in simplified agroecosystems. In the highlands and in simplified landscapes where other bee groups are declining, two bee genera thrive: Apis mellifera, the bee species that has triggered concerns for the fate of bees around the world; and Trigona amalthea, a highly aggressive bee with broad geographical and elevational distributions. Both bee species, paradoxically the ones most rejected by farmers, seem to be among the few equipped with strategies to thrive and expand in a disturbed world.

The effects of agrarian change at both the local and landscape scales impacted bee communities in Anolaima and revealed an interaction between changes in community composition and elevation. These results are important in a context of climate change and increase of average temperatures, where ecological interactions among bee groups may influence elevational range shifts. More detailed assessments on the functional sensitivity of bees to climatic conditions in Anolaima, on the role of dominant bee species on the access of solitary bees to feeding and nesting resources, and on the specific contribution of different bees to the pollination of crops and other flowering plants would help predict further changes in community composition, and

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their effects on rural livelihoods and ecological functioning, in response to environmental degradation and climate change.

In sum, this dissertation showed that bee declines represent a major disruption in ecological dynamics influenced by economic and social processes associated with agrarian change, and the unravelling of relationships between humans and more-than- humans, undermining the sustainability of Anolaima as an autonomous agri-food territory. Understanding the complexity of human-bee relationships, and of the socio- ecological context shaping such interactions would have been impossible without interdisciplinary approaches. Thus, this dissertation shows that to understand biodiversity declines in agricultural lands it is important to:

• approach the past to understand key factors and events shaping contemporary

socio-ecological systems, and that narrow their potential trajectories in the

future;

• address whether biodiversity declines emerge from and exacerbate inequalities in

the access and use of resources that help secure human livelihoods;

• conduct ecological studies to understand the responses of different organisms –

and their ecological functioning– to environmental change;

• approach the interdependence between humans and bees to make visible factors

driving conflicts or potential collaborations between people and biodiversity.

In the case of bee declines in Anolaima, this approach could be complemented by assessments of the feedback loops between agrobiodiversity and food and nutritional 215

security; explorations about the cultural and affective context influencing the relationships between humans and bees; and evaluations of the intersections between spatio-temporal dynamics of food production and the political economy of subsistence and commodity crops at different scales. This could offer essential insights to design conservation initiatives promoting bee presence in agricultural land.

However, it is important to highlight that many factors influencing conflicts with biodiversity are structural and difficult to approach in conventional conservation programs, yet they determine the potential success of any intervention. For example, this dissertation shows that inherited social inequality and its combined effects with industrial capitalistic agriculture have major impacts on bee diversity, environmental stability, human livelihood security and health. Unless social injustice in tropical rural areas is not realistically and responsibly addressed, strategies to promote biodiversity conservation in these regions will be constrained, unstable and of short temporal scope.

A plight for bees and traditional diversified systems

The modern world is undergoing a crisis in which systems that support biodiversity, food production, and human wellbeing are unravelling. This crisis is closely associated with socio-economic disparities in the access and use of resources that enhance poverty, hunger and malnourishment, affecting more than two billion people in the world and threatening the construction of socially and environmentally fair societies. To overcome these challenges, the UN defined an agenda to "end poverty, protect the planet and ensure prosperity for all,” or Sustainable Development Goals 216

(SDG). As its name suggests, SDG are nested in the discursive project of

Development. Bees participate in the achievement of SDG through their role in food production, but their declines would also threaten the perpetuation of plant communities making possible life on earth. The many ecological processes in which bees take part suggest that, to overcome our planetary crisis, we require approaches de-centered from human exceptionalism and from the discursive idea of Development to organize social relationships.

Anthropocentric approaches that measure the importance of bees in terms of their utility to humans (i.e. ecosystem services frameworks) have dominated research on bee declines. These approaches help us remember our dependency with bees but are narrow in scope. Kleij et al. (2015) claim that promoting ecosystem services is an argument that covers only a small percentage of bee species dominating the provision of crop pollination to intensively managed crop fields, and overlook uncommon species that may stabilize pollination function of plant communities over time49.

Ecosystem services focus on the delivery of ecological functions but not on the means to fulfill this provision, therefore services could be realized through the controlled reproduction of life forms such as the old-world honeybee, and some bumble and solitary bee species. Because they do not prioritize ecological self-regulation, these approaches only offer partial solutions to problems derived from bee declines50. In

49 The propositions of Kleij etal. (2015) also disclose the critiques about biases in research addressing ecological dynamics in large-scale and homogeneous crop fields. 50 Reliance on managed bees had cused socio-ecological imbalances. Examples include the problems caused by the Africanization and release of Apis mellifera in Latin America (Moritz 217

addition, these frameworks are closely linked to markets and the economic valuation of ecological functions, which presupposes financial transactions to protect, produce and access pollinators. This suggests that people managing bees would be main beneficiaries, given that local practices do not guarantee bee presence when the regional configuration of agricultural landscapes discourages bee communities. In a context of pollinator declines, people lacking capital to access pollination services will be limited to produce animal-pollinated foods. Thus, these approaches can perpetuate the same social problems causing bee declines.

Strategies to promote biodiversity conservation may have limited scope when designed with the discursive precepts of Development. This world-making process operates through the construction of a controlled “one-world world” that obliterates diversity to increase profitability for some at the expense of others. The development world-making project operates through binaries, including the nature/culture view of the environment, and neglects worldviews with higher awareness of the interdependencies between humans and more-than-humans. Many of these alternative worldviews embrace ideas of freedom and coexistence, where biodiversity is valued and praised for its capacity to self-regulate and adapt. Such worlds have been enacted by thousands of traditional and peasant communities by co-producing agri-food territories in collaboration with thousands of bees and other organisms.

et al. 2005), or the displacement of several species of bumble bees after the release of the exotic Bombus auratus in Chile (Aizen et al. 2018). 218

Traditional diversified farming systems represent viable ecological, economic and socially fair alternatives to produce food, conserve biodiversity, and sustain meaningful livelihoods. For peasant families in Anolaima, especially those with elders and the most marginalized, working the land was a knowledge-intensive activity of physical, mental and spiritual endurance, and it was also a source of hope and joy. These families managed their territories where plant and bee communities were diverse, and people were either more knowledgeable or more respectful about ecological functioning. Farmers knew how ignorance about something does not equal its absence. Many did not know about pollination, but knew that bees and flowers have a strong relationship that, at some point, benefits birds, forests, and humans.

Many elders did not need "to know" to care; they only needed to trust when they could not see.

The materialization of these ethics of care and trust are eroding rapidly, at least in

Anolaima. Within traditional systems, such ethics could be explained by what Yaquie, one of my friends and assistants, called "the environmentalism of the poor." She explained that traditional farmers are aware of their reliance on the resource base, hence they would not engage into practices that would risk their sustained access to water or food crops, and that this awareness has to do with dignity and the value antiguos, elders, give to autonomy and problem solving. However, Yaquie also clarified that ecological awareness ends in times of pressing needs, sometimes associated with pressing hopes. When opportunities to increase wellbeing through the

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overexploitation of the land are feasible, they engage in practices perceived to allow them to participate in other worlds where they would be treated with more dignity.

During a public dialogue on the future of food in Bogota on June 2016, attendees pointed out how an important driver of the crises of our food system involves the violent disregard of peasants. While most Colombian population is agri-descendant,

"as we urbanized, we have denied ourselves, and have become a product of what others tell us to be.” The neglect for peasant lifeways has encouraged the expansion of industrial capitalistic food systems, which obliterate the sustainability of both urban and rural worlds.

John Vandermeer and Ivette Perfecto (201) proposed that "the movement to divest from the industrial agricultural system is located not in the centers of political and economic power, but rather in the intersection of traditional knowledge, popular social movements, and the natural world." This proposition invites for an active approach to research and practice to confront one of the practices of modernity: the erosion of memory –biological and cultural– that brings freedom and autonomy and sustains the capacity to learn and adapt to crises. Western science can extend its power to make visible interdependencies with more than humans by making alliances with other systems of knowledge. As scientists, we can conduct more engaged and powerful research by incorporating the concerns and practices of world-making of local communities in the questions we purse, our methods, and on reflections about the social role of our scientific practice. Linkages across generations and systems of 220

knowledge can highlight the invisibles and create situated and pertinent knowledges that foster biodiversity conservation and sustainability.

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