Demography, Wild Harvest Patterns and Trade of Culturally Important Species: Priorities for Management and Conservation

DEMOGRAPHY, WILD HARVEST PATTERNS AND TRADE OF CULTURALLY IMPORTANT SPECIES: PRIORITIES FOR MANAGEMENT AND CONSERVATION

A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF

THE UNIVERSITY OF HAWAI‘I AT MĀNOA IN PARTIAL FULFILLMENT

OF THE REQUIREMENTS FOR THE DEGREE OF

DOCTOR OF PHILOSOPHY

BOTANY

December 2014

Daniela Dutra Elliott

DISSERTATION COMMITTEE:

Tamara Ticktin, Chairperson

David Duffy

Thomas Ranker

Lyndon Wester

Demetria Mondragon

Daniela Dutra Elliott

ABSTRACT

We know very little about the impacts of harvest on populations of epiphytic plants, the species that depend on them on the canopy, and their ecosystems. The impacts of orchid collecting depend on the life history of the species, the type of collecting being conducted, and socioeconomic factors surrounding communities.

In this dissertation, I detail the population biology, structure, and dynamics of populations for orchid species. In addition, I assess the cultural and socioeconomic patterns that influence harvest in order to fill knowledge gaps on tropical orchid species as well as to provide accurate metrics for the development of sustainable management plans in areas where overharvest is likely to occur. I documented the cultural and socioeconomic patterns of epiphyte use and trade in a market setting. Market studies can provide information of what is happening over a wide range of environments across long distances offering valuable information for conservation. I documented 19 species being sold in the market and a high volume of orchids being traded. There was a clear seasonal trend for orchid sales with two seasons identified. There was a strong cultural component to harvest with plants being part of major cultural and religious celebrations. I also documented that different orchid species are harvested using different methods. The type of harvest that was documented here offers valuable information on what is happening in the natural populations. In the demographic study, the projected population growth rate (λ) for P. karwinskii differed among the three study populations and this is likely due to differences in harvest pressure. Populations of P. karwinskii that experience high-medium harvest

pressures are declining and are expected to continue to decline if circumstances do not change. By contrast, the population that has the lowest harvest pressure is projected to continue to grow slowly over the long term (λ is significantly greater than 1). My results suggest that sustainable harvest can be possible if less than

30% of flowering pseudobulbs are harvested per year from large adult plants in a population. However, this assumes harvest from only the adult plants (the largest pseudobulb > 19 cm) and not from any of the smaller sizes, even if they flower.

A ban on orchid harvest on the national level has clearly not stopped the harvest of wild orchid species. The high volume of orchids traded combined with the available literature on orchid demography related to harvest suggests that harvest at those levels documented here is not likely sustainable. However, results suggest that lower levels may be sustainable, and that this could be achieved if communities had rights to harvest and therefore an investment in the future. Wild orchid harvest could be complemented with propagation as seen in bromeliads. In addition, a change of climate, land-use, or other factors should also be taken into consideration when applying these results to management in the future.

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TABLE OF CONTENTS

ABSTRACT ...... ii CHAPTER 1: INTRODUCTION ...... 7 CHAPTER 2: PLANTS AS NTFPS FROM THE FOREST CANOPIES ...... 11 Abstract ...... 12 Introduction ...... 13 CHAPTER 3: WILD HARVEST PATTERNS AND TRADE ...... 23 Abstract ...... 24 Introduction ...... 25 Materials and Methods ...... 28 Results ...... 30 Discussion ...... 37 CHAPTER 4: DEMOGRAPHY AND HARVEST EFFECTS ...... 42 Abstract ...... 43 Introduction ...... 44 Materials and Methods ...... 45 Results ...... 51 Discussion ...... 60 CHAPTER 5: CONSERVATION RECOMENDATIONS ...... 63 REFERENCES ...... 68

LIST OF TABLES

Table 1: Data Collected using semi-structured interviews with wild orchid vendors...... 30

Table 2: Wild orchid species information, price and total plant volume found in the Abastos Market ..... 33

Table 3: Origin information of orchid species sold in the market...... 34

Table 4: Sample sizes and harvest pressure in P. karwinskii populations ...... 47

Table 5: Size class categories used to create matrix models...... 49

Table 6: Transient analysis results for P. karwinskii populations...... 55

LIST OF FIGURES

Figure 1: Study site in the State of Oaxaca...... 29

Figure 2: Orchid vendors at the Abastos market in Oaxaca City...... 32

Figure 3: Orchids specimens found at Abastos market...... 35

Figure 4: Volume of orchid species sold in Abastos market, Oaxaca...... 36

Figure 5: Temporal variation in sales of five most traded orchid species ...... 37

Figure 6: Life history stages of Prosthechea karwinskii...... 49

Figure 7: Structure of the epiphytic orchid, P. karwinskii in three populations...... 52

Figure 8: Lambda values for populations of Prosthechea karwinskii...... 53

Figure 9: Stochastic lambda values for populations of Prosthechea karwinskii...... 54

Figure 10: Elasticity values for Prosthechea karwinskii...... 56

Figure 11: Life Table Response Experiment analyses for populations of Prosthechea karwinskii...... 58

Figure 12: Simulated effects of a) flower harvest and b) flower and pseudobulb harvest...... 59

CHAPTER 1

INTRODUCTION

Daniela Dutra Elliott

Department of Botany

University of Hawai‘i at Manoa

3190 Maile Way

Honolulu, HI 96822

In order to develop effective conservation plans for species and ecosystems, one must look at the complete picture and also understand the different components that will influence outcomes.

Worldwide, a wide range of plants are harvested for their economic and cultural value

(Cunningham, 2001; FAO, 1995), yet little is known about the impacts of harvest on populations of vascular and non-vascular epiphytic plants, the canopy species that depend on them, and their ecosystems. The potential for over-harvesting has generated concerns as a threat to species conservation and conservationists worldwide have sounded the alarm bells on plant trade for the past decades blaming in certain instances the disappearance of species on collectors (Koopowitz

2001; Flores-Palacios & Valencia-Díaz 2007; Mondragón 2009). The Convention on

International of Endangered Flora and Fauna (CITES) has imposed international regulations in the trade of many species. For example, the entire orchid family is under CITES regulation.

However, very few peer-review studies have documented the harvest or orchid species and looked at the different parts of the issue (Flores-Palacios & Valencia-Díaz 2007; Wolf &

Konings 2001; Mondragón 2008; Mondragón 2009; Mondragón & Ticktin 2011; Peck & Christy

2006; Peck & Frelich 2008; Peck & Muir 2007; Molleman et al. 2011). Some of these components are:

1. Market trends: Who is buying, who is selling, how much, how many species?

2. Traditional Ecological Knowledge and cultural practices related to orchid species: Who uses these plants? For what purposes? Do they have knowledge related to those species? Do they manage these populations?

3. Demographic effects: How does harvest impact populations? Can we set effective harvest limits?

In order to look at these issues in more detail, I chose to study some of the social and ecological issues related to orchid harvest and conservation in Oaxaca, Mexico. The state of

Oaxaca encompasses the most biologically (Peterson et al. 1993) and culturally (Muñoz 2005) diverse region in Mexico and provides an ideal context for the study of the human and ecological dimensions of wild harvested plants. The state has been relatively isolated because of its two large mountain ranges. One of these ranges, the Sierra Norte, is home of many Zapotec and

Chinantec communities that are autonomous and have their own internal governance mechanisms. The communities in this region harvest various species of orchids for market sale

(Mondragón & Villa-Guzmán 2008.). In Mexico, in addition to CITES, national legal restrictions on wild orchid harvest have been introduced as a conservation measure for endangered species; however, little is known regarding this policy's interlocution with existing trade, cultural practices and traditional ecological knowledge.

In Chapter 2, I review the literature and what we know to date about the harvest and trade in the forest canopy, focusing on four categories of epiphytic plants: orchids, bromeliads, ferns, and nonvascular plants. I conclude by identifying research priorities that address the key knowledge gaps identified in the review.

Understanding epiphyte harvest and its effects necessitates the study of cultural and socioeconomic patterns of use and trade, in addition to biological data, yet very few studies address that. Existing research on the epiphyte market indicate that a high diversity and volume of species are traded (Flores-Palacios & Valencia-Díaz 2007; Mondragón 2009). This is especially important because it can strengthen conservation efforts. In Chapter 3, I assess the wild harvest and trade of epiphytic orchids in Oaxaca, Mexico. This chapter looks at the cultural and some of the economic aspects of harvest. Specifically, I assesses the harvest and sale of

orchid species in the state of Oaxaca by addressing the following questions: 1) Who are the orchid vendors and harvesters and how do they fit in the market chain? 2) What are the species being sold and the volume of these species? 3) Are there seasonal trends over the course of one year?

To gain a better understanding of conservation status and potential, markets studies can be complemented by demographic analyses of wild populations. Matrix population projection models (Caswell 2001), are useful tools for projecting long-term population growth rates and determining the importance of each life stage for the destiny of a population, and are widely to inform the management and conservation of wild plant species (Crone et al. 2011). Even though more than 100 species of epiphytic orchids are on the IUCN Red List, the population dynamics have been studied for only nine of these species (Zotz & Schmidt 2006; Mondragón et al. 2007;

Tremblay 1997; Schödelbauerová et al. 2010; Tremblay & Hutchings 2003; Winkler et al. 2009).

However, only one study took anthropogenic effects into consideration. Mondragón et al. (2009) simulated the effects of harvest on the demography of the epiphytic orchid Guarianthe aurantiaca (Mondragón 2009). No studies have assessed populations that have been subjected to different levels of harvest. In Chapter 4, I address the following questions: 1) What are the population dynamics and 2) What are the impacts of harvest on populations of Prosthechea karwinskii, an epiphytic orchid species commonly sold in the markets of Oaxaca, Mexico.

Chapter 5 includes recommendations for local conservation and management based on my research findings.

CHAPTER 2

PLANTS AS NTFPS FROM THE FOREST CANOPIES: PRIOORITIES FOR MANAGEMENT AND CONSERVATION

Daniela Dutra Elliott

Department of Botany

University of Hawai‘i at Manoa

3190 Maile Way

Honolulu, HI 96822

Abstract

A wide range of canopy plants are harvested for their economic and cultural value, yet little is known about the impacts of harvest on populations of vascular and non-vascular epiphytic plants, the canopy species that depend on them, and their ecosystems. In addition, understanding epiphyte harvest and its effects necessitates the study of cultural and socioeconomic patterns of use and trade, in addition to biological data, yet very few studies address that. Existing research on the epiphyte market indicate that a high diversity and volume of species are traded. This is specifically important because it can strengthen conservation efforts since most of these species are listed under CITES including the Orchidaceae. We review what we know to date about the harvest and trade in the forest canopy, focusing on four categories of epiphytic plants: orchids, bromeliads, ferns, and nonvascular plants. We conclude by identifying research priorities that address the key knowledge gaps identified in the review.

Introduction

The harvest of wild plants for cultural and economic reasons is highly important in the lives of hundreds of millions of people worldwide (Cunningham, 2001; FAO, 1995). Non-timber forest products (NTFPs) are used for food, shelter, medicine, and as a source of income (FAO 1995;

Cunningham 2001). NTFPs may also play an important part in other cultural and religious practices (FAO 1991; Ticktin, Whitehead, et al. 2006; Ticktin, Fraiola, et al. 2006). Some of the most important but understudied NTFPs include canopy species of cultural and economic value that have been used extensively by people (Bennett 1992; Nadkarni 1992). Indeed, a wide diversity of canopy species has been documented to be used across the globe (Alcorn 1984;

Bennett et al. 1995; Bulpitt et al. 2007; Haeckel 2008; Hornung Leoni 2011; Lawler 1984;

Ossenbach 2009; Upreti et al. 2005).

Epiphytic plants are characteristic and distinctive components of forests, contributing significantly to total biomass, species diversity, and nutrient cycling in these ecosystems(Gentry

& Dodson 1987; Nadkarni & Matelson 1992). The potential for over-harvesting has generated concerns over the conservation of epiphytic species in many parts of the world (Koopowitz 2001;

Flores-Palacios & Valencia-Díaz 2007; Mondragón 2009). In this chapter, I define canopy as

“the above ground plant organs within a community” (Moffett 2000) and consider NTFPs from the canopy to be epiphytic plants. Although fruits, bark, and resin can be considered canopy

NTFPs under this definition, they are not the focus of this chapter.

We know very little about how harvest impacts populations of epiphytic plants, the species that depend on them on the canopy, and their ecosystems. Wolf and Konings (2001) were the first to develop theoretical recommendations for epiphytic species harvest (Wolf & Konings

2001). Since then, there have been only a few published studies to evaluate the ecological effects of harvesting vascular (Mondragón 2009; Mondragón & Ticktin 2011) and nonvascular (Peck &

Christy 2006; Peck & Frelich 2008; Peck & Muir 2007; Molleman et al. 2011) epiphytes.

Moreover, understanding the effects of epiphyte harvest goes beyond biological data and requires information on cultural and socioeconomic patterns of epiphyte use and trade. However, very few studies have focused on epiphyte or moss markets (Flores-Palacios & Valencia-Díaz

2007; Peck & Muir 2007; Mondragón 2008). Below I review what we know to date about harvesting from the forest canopy, focusing on the four main categories of epiphytic plants harvested from the canopy: orchids, bromeliads, ferns, and nonvascular plants. Based on this review, I then present some research priorities.

Orchids

A very high percentage of harvested epiphytes belong to the Orchidaceae. Epiphytic orchids are especially threatened with extinction caused by the high demand generated by their horticultural and cultural uses, habitat destruction, and their vulnerability to harvest (Soto Arenas et al. 2007). The latter is due to their life history characteristics, including their requirements for mycorrhizal associations, breeding systems, and nutrient limitations (Ackerman et al. 1996;

Tremblay 1997; Otero et al. 2005). Orchids are one of the few plant groups that receive blanket protection internationally (CITES) due to conservation concerns generated by the high-volume trade (Koopowitz 2003; Koopowitz 2001).

Epiphytic orchid use has been recorded historically in different parts of the globe. In

Australia the pseudobulbs of epiphytic orchid species have been used as binder for paintings

(Boustead 1966) and medicinally to treat pediatric cases (Pearn 2005). In pre-Columbian times,

the Mayans of Central America used many species of orchids (Ossenbach 2009), and Aztec

Mexico orchid pseudobulbs were used as a source of gums (Berdan et al. 2009). Today, the demand for orchids is diverse and is generated by specialized international collectors, traditional cultural uses at the local level, and widespread commercialization as ornamentals.

The impact of orchid collecting, which usually involves harvest of the whole plant, depends on the life history of the species and the type of collecting being conducted (Cribb et al.

2003). A detailed understanding of population biology, structure, and dynamics of populations is therefore needed to fill knowledge gaps on tropical orchid species as well as to provide accurate metrics for the development of sustainable management plans in areas where overharvest is likely to occur. Unfortunately, such information for tropical orchid taxa is rare (Koopowitz

2001). For example, we know that many epiphytic orchid species are harvested in China for medicinal use (Zheng & Xing 2009; Ghorbani et al. 2011; Bulpitt et al. 2007), but there is little information on the impacts of harvest on populations. In certain areas of Nepal, orchid species are disappearing due to over collection (Rajbhandari et al. 2000; Koirala et al. 2011). Among 92 species of orchids used medicinally in Nepal, 43 are epiphytes (Acharya & Rokaya 2011).

However, very little is known (or is currently published as peer review publications) about the harvest of these species. Koirala et al. (2010) assessed of the current stock of traded orchid species in the Rolpa district of Western Nepal and documented the species being harvested and traded. This is an important step towards the understanding of trade in the area; however, further research is needed to understand the impacts of harvesting these epiphytic orchid species.

We are aware of only one published study to date on the ecological impacts of harvesting epiphytic orchids, which was carried out on a commonly harvested species, Guarianthe aurantiaca, in Mexico (Mondragón 2009). This study shows that populations of this species can

withstand only very low rates (<5 %) of harvest. Information on the intensity and frequency of harvest of epiphytic orchid species is also lacking, but all evidence indicates that harvest is extensive and unsustainable for orchid populations worldwide. The severity of harvest impacts at the population level varies according to the decisions local harvesters make, specifically on harvest practices such as plant selection, intensity, and frequency. The impacts of harvest can be mitigated by practices informed by local or traditional ecological knowledge (Ticktin 2004).

Finally, very little is known about the trade of orchids. Only one study has been published on the market sales of orchid species. Conducted in Veracruz, Mexico, this study illustrated that 81 % of epiphytic plant species being traded in markets were orchids (Flores-

Palacios & Valencia-Díaz 2007). This illustrates how strong harvest pressure can be for orchid species and how little is known about this issue. Unless we understand how and why people make decisions to harvest, we cannot design locally appropriate plans for management or conservation. Clearly research is urgently needed on the decision making and environmental behavior driving orchid collecting and trade.

As a response to heavy harvest and trade, propagation protocols for native epiphytic orchid species have been developed in recent years (Ávila-Díaz et al. 2009; Dutra et al. 2009;

Santos-Hernández et al. 2005). Although many orchid conservation efforts in the tropics have involved ex situ micro-propagation labs to relieve the pressure on rare species, these techniques are expensive and require expertise in vitro propagation. They therefore limit the power of local communities to be involved in conservation efforts. In areas where epiphytic orchids are used as decorations and then discarded (e.g., Mexico), programs that foster the reestablishment of these home gardens where they can be reused in following years are extremely valuable. Damon et al.

(2005) investigated ways to develop rustic cultivation techniques for seven epiphytic orchid

species using plants that had been propagated in an ex situ lab. Community members established orchid galleries in their home gardens and coffee plantations (Damon et al. 2005). However, propagating orchids from seeds can be time consuming, since most species take many years to bloom depending on the species and cultivation conditions. Reusing mature plants or harvesting only parts to be used for propagation from the forest can speed up the process of flowering and give incentive to people to propagate plants instead of only relying on harvesting new plants from the forest.

Bromeliads

The Bromeliaceae family is comprised of over 3,000 species spread across the

Neotropics, with one species found outside the Americas. Epiphytic bromeliads play important roles in nutrient cycling (Nadkarni & Matelson 1992) and in supporting animal communities in the canopy. Among some of the animals that epiphytic bromeliads house are crabs (Diesel 1989), ants (Blüthgen et al. 2000), endemic ciliates (Foissner 2003), and even earthworms (Fragoso &

Rojas-Fernández 1996).

The harvest of bromeliads is common in the Neotropics (Bennett 1990; Acebey et al.

2010; Haeckel 2008; Negrelle et al. 2012) and especially for use as ornamental plants and for religious decorations (Mondragón & Villa-Guzmán 2008). Throughout the year and especially during the Christmas and Holy week holidays, thousands of plants are collected to sell in urban markets (J.D. 1976; Mondragón 2008) and to decorate churches (Haeckel 2008) and nativity scenes in Southern Mexico. Flores-Palacios and Valencia-Diaz’s 2007 market study in Veracruz demonstrated the high diversity and volume of bromeliad species that are sold. However, very little is known about the effects harvest has on epiphytic bromeliad populations and the

surrounding ecosystems. Mondragon and Ticktin (2011) used matrix population models to study the demography of two species of bromeliads (Tillandsia macdougallii and T. violacea) in

Oaxaca, Mexico, and the potential to sustainably harvest their populations. They found that the populations for these two bromeliads are unlikely to support even low levels of harvest. This is because these species, like the other (non-harvested) epiphytic bromeliads studied to date

(Mondragn et al. 2004; Zotz et al. 2005; Winkler et al. 2007; Valverde & Bernal 2010) are most sensitive to changes in survival of large or reproductive individuals, and these are precisely the stages that are harvested.

However, throughout the year high volumes of bromeliads fall naturally to the forest floor, where they are unable to survive. Mondragon and Ticktin (2011) illustrated that harvest of these fallen bromeliads from the forest floor can be a both ecological and economically sustainable alternative to harvest from the canopy. This has recently been shown to be true also for other bromeliad species in Veracruz, Mexico (Toledo & Hernandez, unpublished results).

The harvest of fallen bromeliads may offer a promising alternative for epiphytic bromeliads elsewhere and needs further investigation.

Ferns

Ferns and their allies have been used all over the world for thousands of years: their rhizomes, leaves, and spores have been used as medicine, their fibers to construct baskets and other artifacts (May 1978; Thomas 1999), and their fronds for cultural traditions such as adornment in hula in Hawaii (Ticktin, Whitehead, et al. 2006; Ticktin, Fraiola, et al. 2006).

Although there is literature on the effects of harvest on terrestrial ferns, very little has been published on epiphytic fern harvest. In the Ivory Coast the commercial harvest of Platycerium

stemaria (Polypodiaceae) caused a large local decline in the population size of this epiphytic fern

(Porembski & Biedinger 2001).

The harvest of epiphytic ferns is likely misrepresented in the literature since most studies in the ethnobotanical literature do not mention the life form, and it is difficult to know if species are being harvested from the canopy or not. However, much can be learned from the literature pertaining to terrestrial fern harvest. For example, many tree fern species (Cyatheales) are critically endangered due to harvest of their trunks to be used as orchid medium in the ornamental trade. This type of harvest affects many different epiphytic fern species (and other vascular and nonvascular epiphytes) that are growing on tree fern trunks. Therefore, the harvest of terrestrial ferns can have an indirect impact on the demography of other species. Roberts et al.

(2005) assessed the diversity of epiphytic fern species found on Tasmanian tree ferns and found

97 fern and bryophyte species on one species of tree fern (Dicksonia antarctica) and 64 species on the trunks of a second, Cyathea cunninghamii (Roberts et al. 2005). Similar studies on the diversity of epiphytic ferns on the trunks of tree ferns have been conducted in other places including Brazil and Argentina (Schmitt & Windisch 2010; Marquez 2012), and they show a high diversity of epiphytic ferns growing on tree fern trunks.

Nonvascular Plants

Moss harvest has been defined as the collection of either moss or a mixture of mosses, liverworts, and lichen and some vascular plants (Peck & Muir 2007). Epiphytic moss harvest has been studied mainly in North America. Commercial moss harvest of epiphytic species takes place in the Pacific Northwest (Peck & Christy 2006) and Appalachians (Muir et al. 2006) and has been going on for decades. Three million kilograms of mosses are harvested per year (Peck

& Muir 2007). Large mats are peeled off from tree trunks and branches and sold in the national and international markets (Peck 2006b). Harvested moss is mainly used in the floriculture and horticulture industry as decorations, packing material, and as a medium for growing epiphytes such as orchids.

Moss harvest mainly takes place in National forests (Peck 2006a) and permits are required. We know more about moss harvest in North America than we know about harvest of any other epiphyte. Species involved in the commercial trade have been identified (Muir 2004;

Peck & Muir 2007), the epiphyte communities removed by harvest have been described (Peck

1997), and harvest impacts such as biomass accumulation and changes in relative species composition over time have been assessed (J. Peck & Frelich 2008). The effects of different harvest practices on species abundance, richness, and composition have also been quantified

(Peck & Christy 2006). Based on this research, several harvest guidelines have been established and implemented for the sustainable management of moss. For example, the method of harvest

(partial vs. total stripping) can have enormous impacts on how epiphytic communities recover after harvest in terms of species diversity, abundance, and composition and how long recovery takes (J. Peck & Frelich 2008). However, there are still many gaps of knowledge on moss harvest research (Peck 2006b). Moss is harvested from areas other than the United States, for example, in Mexico; moss is heavily harvested for nativity decorations during the Christmas season.

In India, epiphytic lichens are very important NTFPs. They are harvested by indigenous communities as a form of income (Molleman et al. 2011) and are sold as spices, in the perfumery and medical industries, and as a raw material for paint (Kaushal & Upreti 2001; Upreti et al.

2005). Harvesters scrape the branches to remove the lichens and large volumes of lichens are

harvested. In 1997 alone, 1,000 metric tons was harvested nationally (Shah 1998). To date, only one quantitative lichen harvest study has been published: Molleman et al. (2011) showed that 7 years after harvesting, the lichen community showed significant regeneration capacity. They also demonstrated that the harvest method makes a difference: shallow harvesting resulted in a quicker recovery of species abundance and richness compared with deep harvesting. This highlights the importance of studies that investigate how people make decisions to harvest and their effects on species composition and population structure.

Research Priorities

To gain a better understanding of epiphyte harvest and its ecological consequences, the following research is needed:

1. More research, and especially integrated research, on the population dynamics, market dynamics, local management, and ecosystem impacts of epiphyte harvest is needed. The information is essential for designing sustainable management plans.

2. Traditional ecological knowledge should be taken into account in harvest studies. There is little information available on how local people make decisions on the harvest or management of wild epiphyte populations, which are often common pool resources. This knowledge is critical for understanding patterns and intensity of use and their ecological implications. Imposing management policies and regulations that ignore preexisting management practices, and related social institutions, may deteriorate existing land and resource management capacities (Alcorn &

Toledo 1998; Agrawal, Arun and Ostrom 2001).

3. National and international studies on the trade of epiphytes are especially important. We know, for example, that orchids are being heavily harvested in many parts of the world; however,

they are greatly underreported in CITES (Phelps et al. 2010). In parts of Brazil, for example, orchids are harvested from natural areas and sold on sides of roads, but there are no publications that we know of the internal trade of orchids in that country.

4. Research on the effects of heavy epiphyte harvest, on the organisms that depend on them, is needed. No studies to date have examined this for epiphytes, but, for example, a study on acai palms showed that heavy harvest of canopy fruit can lead to changes in the abundance and composition of frugivores (Moegenburg & Levey 2003).

5. Community-based propagation of heavily harvested epiphytes may reduce pressure on wild populations and provide income to local communities, and more research is needed in this area.

6. More research on a broader spectrum of epiphytes is needed. Not only do we have little or no information on many of the most commonly harvested species of epiphytes, but there are also entire plant families of epiphytes for which no harvest studies are available. For example, Flores-

Palacios and Valencia-Diaz (2007) report that epiphytic species belonging to the Araceae,

Cactaceae, and Lycopodiaceae are harvested in Veracruz, Mexico; however, nothing is known about their harvest or of its ecological consequences.

CHAPTER 3

WILD HARVEST PATTERNS AND TRADE OF EPIPHYTIC ORCHIDS IN OAXACA, MEXICO

Daniela Dutra Elliott

Department of Botany

University of Hawai‘i at Manoa

3190 Maile Way

Honolulu, HI. 96822

Abstract

The harvest of wild plants is of cultural and economic importance for the lives of hundreds of millions of people worldwide and the potential for over-harvesting has generated concerns as a threat to species conservation. In the state of Oaxaca, various species of epiphytic orchids are harvested for market sale and for use in religious practices. The overall aim of this research were to identify the patterns of trade and wild harvest of orchid species in Oaxaca, and assess the local ecological knowledge associated with these activities in order to provide recommendations for management strategies. We surveyed the largest market in Oaxaca state over a one-year period and interviewed orchid sellers and harvesters. In the market, 22 epiphytic orchid species were found being sold; however, three species constitute the majority of the volume of the orchid trade. Species harvested varied seasonally according to blooming seasons and demand was driven by local holidays such as Christmas and Easter with volume and sells peaking during the months of April and December. A vast majority of sellers (95.2%) were women who harvested the plants themselves in their communities sometimes with family help and brought them to the urban markets to be sold. Despite a legal ban on orchid harvesting, wild harvest was still associated with cultural celebrations. The volume of plants being sold during the holiday seasons was high. Some of the species sold in the market may require the attention of local indigenous groups who design management plans for their lands and local conservation organizations.

Introduction

Non-timber forest products (NTFPs) are collected and sold by individuals as a source of income and are also used for food, shelter, medicine and religious practices (Belcher 2003; FAO 1995;

Cunningham 2001). People who rely on the harvest of NTFPs tend to live in remote rural areas and are more likely to be impoverished (Hulme & Shepherd 2003; Belcher et al. 2005).

Sunderlin et al. (2005) listed three categories for people who are poor and depend on forests:

Traditional/indigenous minorities living in their ancestral lands, people who have been living in forests but are not considered indigenous/traditional, and displaced people who have moved to forested areas.

There are proponents of the use of forest resources as poverty alleviation tools while being able to conserve of natural resources (Sunderlin et al. 2005). Others have shown that poverty alleviation cannot be achieved in this manner due to other constraints (Belcher et al.

2005). The proportion of overall household income generated by the harvest of NTFPs can vary widely from place to place and may serve as a form of security net (Shackleton & Shackleton

2004; Mahapatra et al. 2005; Quang & Anh 2006). Most rural people who are poor may have diversified livelihood strategies because of the risks associated with relying on a single form of income (Sunderlin et al. 2005). The case for forest resource extraction for poverty alleviation while conserving forests has been shown to be possible in some areas of the globe such as in certain areas in Mexico that have community organized timber extraction (Bray et al. 2008; Bray et al. 2003)

In Mexico, communities govern 80% of forested lands and some of these community- managed forests are viewed as models for sustainability (Bray et al. 2003). These communities

had a long struggle to gain land tenure (communal land grants) and later on to gain control over the management of forest resources. Followed by the Mexican revolution, the agrarian reform in the early 20th century gave many communities land tenure. However, it was not until 1992 that these communities were finally able to gain rights over their resources such as timber (Chapela

2005; Hajjar et al. 2012). Although communities control such forest resources, the Mexican government still has control over what and how things get extracted from community lands. La

Procuraduría Federal de Protección al Ambiente (PROFEPA) is the governmental entity responsible for regulating natural resources, as the U.S. Fish and Wildlife Service is in the

United States. Communities must obtain permits to enact a timber extraction plan. Although

NTFPs such as orchids and bromeliads are heavily harvested and sold by local communities in some regions (Flores-Palacios & Valencia-Díaz 2007), harvest and sale is considered illegal by the federal government. There is a process to obtain permission to harvest but permits can be very difficult to obtain since communities need to provide detailed ecological studies on the plant populations (Mondragon per. comm.) and that normally requires outside help of scientists.

The state of Oaxaca encompasses the most biologically (Peterson et al. 1993) and culturally (Muñoz 2005) diverse region in Mexico and provides an ideal context for the study of the human and ecological dimensions of wild harvested plants. The state has been relatively isolated because of its two large mountain ranges. One of these ranges, the Sierra Norte, is home of many Zapotec and Chinantec communities that are autonomous and have their own internal governance mechanisms. The communities in this region harvest various species of orchids for market sale and for use in religious practices. These plants are taken to large cities where they can be sold in markets responding to the demands of a growing urban population.

Some of the most important but understudied NTFPs species of the Orchidaceae (Flores-

Palacios & Valencia-Díaz 2007; Dutra Elliott & Ticktin 2013). Orchids are one of the few plant groups that receive blanket protection internationally due to conservation concerns generated by the high volume trade through horticultural and cultural uses, habitat destruction (Cribb et al.

2003; Arenas et al. 2007), and their vulnerability to harvest due to life history characteristics including their requirements for mycorrhizal associations and pollinator and nutrient limitations

(Ackerman et al. 1996; Tremblay 1997; Otero et al. 2005).

A market study conducted in the Mexican state of Veracruz showed that 81% of epiphytic plant species being traded were orchids (Flores-Palacios & Valencia-Díaz 2007), therefore the potential for over-harvesting has generated concerns for the conservation of many species. For the past two decades, conservationists have been pointing at the orchid harvest in

Oaxaca as unsustainable (Mondragon Pers. comm.), however no studies exist and, therefore, little is known about the diversity and volume of the orchid trade. Domestic markets are used in the developing world as trade hubs for NTFPs by hundreds of millions of people (Scherr et al.

2004; Shackleton et al. 2007). Many of these regional markets are growing worldwide due to high demand for these products. Urban populations are increasing as well as growth in the demand for low cost and traditional products (Shackleton et al. 2007). Market studies can inform understanding about patterns and scales of harvest and implications for plant populations and for human livelihoods.

This study assessed the harvest and sale of orchid species in the state of Oaxaca by addressing the following questions: 1) Who are the orchid vendors and harvesters and how do they fit in the market chain? 2) What are the species being sold and the volume of these species?

3) Are there seasonal trends (species and volume) over the course of one year?

Materials and Methods

To assess the volume and diversity of wild-collected orchids sold in the state of Oaxaca; I conducted a study in the Abastos market (Central de Abastos), which is located in Oaxaca City (Figure 1) from

March 2010 to April 2011. Abastos is one of the largest and most important market in southern

Mexico and, therefore, the best place to study orchid trade. For the first month of the study, I visited the market everyday from 7am to 4pm. I walked the entire market and interviewed vendors who sold any type of plant including cut flowers, medicinal plants, and potted nursery plants. I mapped the market and identified where orchid vendors were most likely to be and what days of the week they would come to market. After that first month, I selected the most likely day of the week and time of the day vendors would be selling orchids. I then began visiting the market once per week (Tuesdays) from 8 am-10 am. I interviewed orchid vendors using semi-structured interviews and asked their age, community of residence, when they came to market, and if they harvested the plants themselves of bought them from someone else. I also asked about the plant name, price, origin of the plant, and uses (Table 1). I purchased plants, took pictures, and made herbarium vouchers for newly encountered species. A local expert helped identify plant specimens when flowers were not present.

I calculated the volume of plants sold based on my counts from one day of the week. Plants were sold either by the pseudobulb, as a whole plant, or potted. I considered a plant whole if the specimen had more than 3 pseudobulbs attached to the roots. Potted plants were collected from the wild and potted.

Figure 1: Study site in the State of Oaxaca.

Table 1: Data Collected using semi-structured interviews with wild orchid vendors.

Data Collected Plant Vendor Name Gender Number of specimens for sale Age Origin Community of origin Price Market status (permanent, occasional or temporary) Uses Days of the week selling at this market Harvester or buyer

Results

Who are the orchid vendors and harvesters and how do they fit in the market chain?

Most of the vendors were female (95.2%) compared to only 4.8% of male vendors. There were three types of vendors I observed selling orchids: Permanent, periodic, and seasonal. Permanent vendors had permanent structures for booths where they could store merchandize. These vendors were most likely to be open all days of the week and purchased merchandized from producers, harvesters, or other middlemen. They sold a variety of things including vegetables and flowers.

When they sold orchids, they were purchased directly from harvesters who brought them down from their communities of origin.

Periodic vendors came to market once or twice a week (Tuesdays, Fridays, and/or

Saturdays) and set up in temporary stations on the ground, but had their place saved for them by other vendors or the market manager. These vendors traveled to market from the communities where they resided bringing a variety of things they grew themselves such as flowers, potted plants, and seasonal fruits and vegetables (Figure 2). The last type of vendor was the seasonal vendor who normally showed up for major holidays. These vendors focused mainly on orchids and other plants used in holiday celebrations such as bromeliads, ferns, and mosses.

There were a total of 209 observations of vendors selling orchids, but only 74 individual vendors because some of these appeared more than once. Out of those vendors, two were responsible for 28.2% of appearances (59 appearances at the market combined). Both of these vendors sold other plants (wild harvested and nursery plants that they had propagated themselves); one was a permanent vendor while the other a periodic vendor. Permanent and periodic vendors combined comprised only 13.5% of vendors (10 out of 74) while 86.5% were seasonal vendors. All permanent vendors purchased plants from harvesters. On the other hand, periodic and seasonal vendors harvested the plants themselves (or someone in the household did). Permanent and periodic vendors were responsible for 14% of the volume of orchids sold compared to seasonal vendors, which were responsible for 86% of the total orchid volume sold in the market.

There were 19 orchid species recorded, 18 of them were identified to the genus level and

15 of those to species level (Table 2). Ten out of the 18 species were sold by the pseudobulb only. Eight species were sold as whole plants and 1 (Prosthechea karwinskii (Mart.) Soto Arenas

& Salazar) as both (Table 2; Figure 3). Laelia furfuracea Lindl. comprised 33.1% of all plants sold (35,790 pseudobulbs), followed by Artorima erubescens (Lindl.) Dressler & G.E. Pollard

(20.6%, 22,287 pseudobulbs), Rhynchostele maculata (Lex.) Soto Arenas & Salazar (16.7%,

18,130 pseudobulbs), Laelia albida Bateman ex Lindl. (7.6%, 8,210 pseudobulbs), and

Prosthechea karwinskii (17.2%, 18,599 pseudobulbs). The volume of the remaining 14 species added up to 4.8% (Table 2; Figure 4).

Figure 2: Orchid vendors at the Abastos market in Oaxaca City. A) Periodic vendor selling Laelia furfuracea, a popular orchid species during the month of December. The yellow lines delineate their space on the floor where they set up weekly. B) A permanent vendor selling P. karwinskii during month of May for Easter. The roof over their heads is characteristic of a permanent booth that can be locked at night and vendors will stay in the market year around. C) A permanent vendor selling Laelia furfuracea, fruits and vegetables. C) Seasonal vendors selling Prosthechea karwinskii at the entrance of the market. We obtained plant origin information for 78.9 % of species harvested. These species originated from at least 15 different municipalities. Out of these, we could only obtain general location information for 12.1% of the locations. The location in which most plants originated from was NZ (23.4%; Table 3). Out of all harvest locations, 76.4% were at least 50Km from market. Most species were harvested for either horticultural or religious uses (Table 2). Only

Prosthechea michuacana was also harvested for medicinal uses. Plant prices (Table 2) did not significantly vary over time.

Table 2: Wild orchid species information, price and total plant volume found in the Abastos Market from 2010-2011. Potted plants can either be whole plants or plant parts. Price was calculated based on 1 Mexican Peso = 0.08 dollars. Uses: Ornamental (o), religious (r) and medicinal (m). Distribution: Oaxaca endemic (oe), Mexico endemic (me), Mexico and Central America endemic (mce), Mexico and other wider locations (mo). Conservation status (con. status) corresponds to the Mexican Government publication (SEMARNAT, 2010). Pr, subject to special protection; T, threatened. During the study period the mean exchange rate was 9.7+- 0.6 Mx pesos for 1 US dollar.

Table 3: Origin information of orchid species sold in the market.

Location # of occurrences % Distance (Km) Unknown EP 11 5.3 80.5 - I 5 2.4 104.6 - LG 13 6.2 67.6 - M1 5 2.4 125.5 - M2* 1 0.5 - 0.6 M3* 6 2.9 - 3.6 N 6 2.9 82.1 - NZ 49 23.4 91.7 - SMP 16 7.7 109.4 - SCI 13 6.2 85.3 - SPE 11 5.3 30.6 - ST 5 2.4 104.6 - SBJ* 19 9.1 - 11.5 SS* 1 0.5 - 0.6 T 3 1.4 130.4 - Z 1 0.5 14.5 - Data points without locations 44 21.1 - - Total data points 209 100.0 - 16.4 *General locations without municipalities. These were not taken into consideration for distance calculations in this table.

Figure 3: Orchids specimens found at Abastos market. A) Epidendrum propiquum specimen purchased as a whole plant with multiple pseudobulbs attached to the roots. B) Laelia furfuracea being sold in bundles of 4 individual pseudobulbs. C) Prosthechea karwinskii being sold in bundles of individual pseudobulbs. The top bundle is wrapped in Tillandsia usneoides. D) Laelia furfuracea being sold at the market.

Figure 4: Volume of orchid species sold in Abastos market, Oaxaca. (March 2010-February 2011).

Are there seasonal trends (species and volume) over the course of one year?

There was a seasonal trend for orchids in the market (Figure 5) with two major seasons identified. The volume of orchids and number of vendors increased during April-May and

November-December. During the peak time of April-May, Prosthechea karwinskii was the most sold species while in the November-December season there were four other popular species

(Figure 5): Artorima erubescens, Laelia albida, Laelia furfuracea, and Rhynchostele maculata.

Figure 5: Temporal variation in sales of five most traded orchid species

Discussion We found that the orchids sold in the state of Oaxaca’s largest market, the Central de

Abastos, were harvested and most of the time sold by the same people who harvested them. We also found that harvesters may bring the plants to the market and sell them to permanent vendors.

While orchid harvest can be an activity in which anyone from the household may be involved, vendors are mainly women who come down from their communities to sell these plants.

However, the 4.8% of vendors who were men sold orchids as seasonal vendors during the peak of holiday season when orchid volumes are high. On a global scale, women play a large role in

the trade and sale of NTFPs given that these resources provide a source of personal income

(Falconer 1996; Sunderland et al. 2004).

Permanent and periodic vendors relied on the sales of many products other than NTFPs showing that NTFP harvest complements their income during that time of the year, but vendors do not solely depend on these NTFPs for their livelihoods. On the other hand, seasonal vendors only came to market for short periods of time during the year to sell only orchids and sometimes other NTFPs such as bromeliads and mosses. The average pay per day in Oaxaca is approximated $20. Vendors could sell one plant for $2 and the average day sale was approximately $400. In this case, seasonal vendors do rely on orchid harvest especially during the holiday season.

Religious holidays strongly influence orchid appearance in the market. The highest volume of plants was sold the weeks prior to Day of the Dead, Christmas, and Holy Week. There are also a higher number of seasonal vendors during this time of the year. These two times peak seasons also overlap with the blooming period of these species. We observed during this study that seasonal vendors sell whole plants during holidays (Prosthechea karwinskii during the month of April and Rhynchostele maculata during November and December). In the case of

Rhynchostele maculata, the foliage of the plant is valued as decoration for nativity scenes therefore the whole plant is harvested. This type of harvest can be troublesome because it can have a higher impact on wild populations compared to harvesting only parts of the plant and leaving live plants in the wild populations.

Species we found in the market traveled long distances to get there, for example, 76.4% came from communities located more than 50 km away. Of the 19 species found, 15 were

identified to species level. Out of those 15 species, 8 species were also recorded in another market study in Veracruz, Mexico, that took place from 2001 to 2003 for 21 months (Flores-

Palacios & Valencia-Díaz 2007). The state of Veracruz borders the state of Oaxaca and we expected to see some of the same species in this market study. Out of the remaining 7 species that were not seen in the Veracruz market study, 3 are endemic to the state of Oaxaca (Table 2).

Although the orchid diversity in the Veracruz market study was a lot higher (144 species compared to 19), the total number of plants in the current study was a lot higher. I recorded a total of 4,253 whole plants and 87,814 plant parts (pseudobulbs) while Flores-Palacios &

Valencia-Díaz (2007) recorded 6,762 plants and plant parts in a 21-month study in which they visited the market once a week. Most of the plants in the Veracruz study were whole plants, the opposite of the current study. There was no clear seasonal pattern with the Veracruz study, compared to the current study, which showed a clear seasonal pattern based on religious holidays.

Orchid harvest is considered illegal by the Mexican government since orchids have blanket protection on the national and international levels. A ban on orchid harvest on the national level has clearly not stopped the harvest of wild orchid species in the state of Oaxaca as seen in this market study and also in a previous study in Veracruz (Flores-Palacios & Valencia-

Díaz 2007). The harvest ban may have in fact worsened the conditions of wild populations since now there is no benefit for local communities to protect these plants. According to interviews carried out in orchid-harvesting communities before the ban (Chapter 4), harvesters who collected plants from communal lands would return to the same areas year after year to harvest and therefore benefited from not overharvesting these restricted populations. These harvesters had detailed knowledge of where orchids grow and of their ecology. Orchids mature extremely

slowly and take a minimum of 7 years to flower from seed, however, they are long lived

(Dressler 1981). Orchid harvesters frequently mentioned that they only harvest parts of a mature plant (pseudobulb with the flower attached), leaving most of the plant behind. They stated that the mature plant will bloom again the following year and harvesters can come back and gather from the same populations. After the harvest ban was enforced, harvesters were afraid of being caught but continued to harvest plants. They also reported that they did not know if they could come back to the same site to harvest the following year and that traditional limits and territorial rules no longer applied when the resource became illegal. Therefore, the way harvesters interact with wild orchid populations have changed since harvesting based on traditional rules no longer necessarily benefited them. This uncertainty in resource tenure has been shown around the globe to decrease the harvester incentives for forest conservation, therefore, decreasing their own livelihood security (Cunningham 1993; Nygren et al. 2006).

Large plants can survive the removal of flowering pseudobulbs and new pseudobulbs emerge the following year (personal observation). My demographic research on Prosthechea karwinskii (Chapter 4) has shown that a heavily harvested population showed no recruitment and declining long term population growth rates. It is likely that most flowering pseudobulbs were harvested leaving no flowers behind to set fruit. On the other hand, the population under low harvest pressure had increasing long-term population growth rates, which suggests that some harvest can be possible. However, based on the volume of plants observed in the market, harvest of Laelia furfuracea, Artorima erubescens, Rhynchostele maculata, and Laelia albida populations is likely unsustainable.

The high volume of orchids traded combined with the available literature on orchid demography related to harvest (Chapter 4, Mondragón 2009) suggests that harvest at those levels

and patterns (lots of pseudobulbs and mature plants) documented here is not likely sustainable.

However, demographic studies suggest that lower levels may be sustainable, and that this could be achieved if communities had rights to harvest and therefore an investment in the future

(Agrawal et al. 2001; Agrawal & Gupta 2005). Wild orchid harvest could be complemented with propagation as seen in bromeliads (Mondragón & Ticktin 2011).

There are shortcomings to this study. First, we only visited the market for one year and our volume calculations are based on a single weekday. It is possible that the actual numbers are higher than reported here. Second, vendors were reluctant to talk about where plants came from for fear of the governmental authorities. In many cases we acquired an overall locality only.

CHAPTER 4:

DEMOGRAPHY AND HARVEST EFFECTS ON A WILD ORCHID SPECIES

Daniela Dutra Elliott

Department of Botany

University of Hawai‘i at Manoa

3190 Maile Way

Honolulu, HI. 96822

Abstract

The study of population dynamics using matrix population projection models is a widely used tool to inform the management and conservation of wild plant species. Even though more than

100 species of epiphytic orchids are on the IUCN Red List, the population dynamics have been studied for only a few of these species. In this study, I addressed the following questions: 1)

What are the population dynamics and 2) What are the impacts of harvest on populations of

Prosthechea karwinskii, an epiphytic orchid species commonly sold in the markets of Oaxaca,

Mexico. I monitored 3 populations of P. karwinskii for 3 years and used matrix population models to project long-term population growth rates. The projected population growth rate (λ) for P. karwinskii differed among the three study populations and this is likely due to differences in harvest pressure. Stochastic lambda values differed significantly among populations:

Populations with high and medium harvest pressures had lambda values below 1 and the population with the lowest harvest pressure having a lambda value above 1. Life Table Response experiments (LTRE) results suggest that the higher population growth rates in the low-harvested population are due to higher rates of survival and reproduction of adults, and higher growth of all of the other stage classes. Harvest simulations suggest that sustainable harvest can be possible if less than 30% of flowering pseudobulbs are harvested per year from large adult plants.. In addition, a change of climate, land-use, or other factors should also be taken into consideration when applying these results to management in the future. Given that the medium and high harvest populations are declining, harvest has likely been higher than this level over time.

Introduction

Non-timber forest products (NTFPs) are used for food, shelter, medicine, and as a source of income (FAO 1995; Cunningham 2001). NTFPs may also play an important part in other cultural and religious practices (FAO 1991; Ticktin, Fraiola, et al. 2006; Ticktin, Whitehead, et al. 2006).

Some of the most important but understudied NTFPs include canopy species of cultural and economic value that have been used extensively by people (Bennett 1992; Nadkarni & Matelson

1992).

A very high percentage of harvested epiphytes belong to the Orchidaceae, which constitute the largest single group covered by the Convention on International Trade in

Endangered Species (CITES) and the International Union for Conservation of Nature (IUCN)

Red List. Epiphytic orchids are especially threatened with extinction caused by the high demand generated by their horticultural and cultural uses, habitat destruction (Arenas et al. 2007), and vulnerability to harvest. The last is due to their life history characteristics, including their requirements for mycorrhizal associations, breeding systems, and nutrient limitations (Ackerman et al. 1996; Tremblay 1997; Otero et al. 2005).

The study of population dynamics using matrix population projection models (Caswell

2001), which project long-term population growth rates and determine the importance of each life stage for the destiny of a population, is a widely used tool for the management and conservation of wild plant species (Crone et al. 2011). Even though more than 100 species of epiphytic orchids are on the IUCN Red List, the population dynamics have been studied for only nine of these species (Zotz & Schmidt 2006; Mondragón et al. 2007; Tremblay 1997;

Schödelbauerová et al. 2010; Tremblay & Hutchings 2003; Winkler et al. 2009). However, only

one study took anthropogenic effects into consideration. Mondragón et al. (2009) simulated the effects of harvest on the demography of the epiphytic orchid Guarianthe aurantiaca (Mondragón

2009). No studies have assessed populations that have been subjected to different levels of harvest.

A market study conducted in the Mexican state of Veracruz showed that 81% of epiphytic plant species being traded were orchids (Flores-Palacios & Valencia-Díaz 2007). A large volume of wild collected orchids is sold in the state of Oaxaca’s largest market. I recorded

19 species and a total of 4,253 whole plants and 87,814 plant parts (pseudobulbs) offered for sale at the market during one year (Chapter 3). Therefore, the potential for over-harvesting has generated concerns over the conservation of many species. For the past two decades, conservationists have been pointing at the orchid harvest in Oaxaca as unsustainable (Mondragón pers. comm.), however, no studies on orchid demography exist for orchid species in the state.

In this study, I addressed the following questions: 1) What are the population dynamics and 2) What are the impacts of harvest on populations of Prosthechea karwinskii, an epiphytic orchid species commonly sold in the markets of Oaxaca, Mexico (Chapter 3). I expected that populations with high harvest pressure would have a lower projected growth value (λ) than populations with lower harvest pressure because levels of reproduction would likely be affected by harvest.

Materials and Methods Study Site and Species

This study took place in the Sierra Norte (17-15’ N, 96-33 W), located in the southwestern Mexican state of Oaxaca. This area is known as a biological hotspot in Mexico

where the eastern and western Sierra Madre mountain chains meet (Challenger & Caballero

1998). This is the region where both pine and oak reach their highest global diversity

(Mittermeier et al. 2005). Elevation of the field sites ranged from 2,000-22,000 meters. The vegetation is characterized by oak-chaparral (Zacarías-Eslava & Del Castillo n.d.; Del Castillo et al. 2013) dominated by Quercus glaucoides M. Martens & Galeotti and Q. obtusata Bonpl. The annual precipitation and temperature means in the area are 18.3°C and 772.8 mm, respectively

(Nacional 2009). The areas where this research took place are considered community-managed forests where people have tenure over their lands. These communities had a long struggle to gain land tenure and to gain control over the management of forest resources (Chapela 2005).

Although communities managed some of their natural resources (e.g., timber), they still need approval by the governmental authorities. PROFEPA (La Procuraduría Federal de Protección al

Ambiente) was created in 1990s as the governmental entity responsible for regulating natural resources in Mexico. It controls the legal and illegal harvest of natural resources. Orchids have been protected at the national level since the 1990s and at the communal level for the past 10 years. People in this region harvest various species of orchids for market sale and for use in their own religious practices. The use of flowers for religious and cultural purposes has been happening since pre-Spanish contact, however, harvest for market sale in this area has been taking place for at least 50 years (Del Castillo et al. 2013). Those plants harvested for sale are taken to large cities where they can be sold in markets responding to the demands of a growing urban population. Plants can be harvested and sold whole or by pseudobulbs (stems) with the flowers attached.

Three populations of Prosthechea karwinskii (Mart.) J.M.H.Shaw were located. These populations varied based on harvest pressure (Table 4). The populations were chosen based on

triangulated information from interviews, from expert harvesters, and from field observations.

Populations 1 and 2 are located in relatively easy access from the main road (0.4 and 0.8 Km respectively). Population 3 has low anthropogenic harvest pressure; it is located far from roads on a steep part of the mountain across a river.

Table 4: Sample sizes and harvest pressure in P. karwinskii populations Population # of trees # of orchids Harvest pressure 1 33 128 High 2 52 301 Moderate 3 42 281 Low Total 127 710 ---

Study species

Prosthechea karwinskii is an epiphytic orchid, endemic to the state of Oaxaca. The local name is

“limoncillo” because of its yellow flowers with a fragrant citrusy aroma, possibly exuded to attract pollinators. Although this species is self-compatible, it is not autogamous and requires a pollinator to set fruit (pers. obs.). It is only found growing on Quercus glaucoides and Q. obtusata, although it can rarely be seen growing on other tree species such as Acacia spp. This species blooms once per year, from March–May right before the wet season (May–October).

New pseudobulbs emerge from the plants at the time of blooming and continue to mature throughout the year. Inflorescences, if they emerge, can do so only from the newest pseudobulb the year after it emerges. After the inflorescences dry out, the pseudobulb will continue to photosynthesize and may loose its leaves during the dry season (November–April). A pseudobulb will only bloom once.

Measuring Species Demographic Rates

In April 2010, I selected trees containing P. karwinskii in each of the three study sites, marked and identified all individuals growing on those trees (n=127; Table 4). I also searched all trees in the area annually for new seedlings even if these trees did not originally have the target species.

Populations were censused annually for three years (2010-2013), and at each census, all plants were measured and new seedlings tagged. To identify new seedlings, I recorded the number of dead and live pseudobulbs, measured the diameter of the largest live pseudobulb, and measured the height and number of inflorescences. Every year, the number of fruits per plant was counted.

A total of 710 P. karwinskii individuals were tagged.

Parameterization of Matrix Models

I constructed a stage-based matrix model (Lefkovitch projection matrices; Caswell 2001) for each of the three populations of P. karwinskii and years (2010–2011, 2011–2012, 2012–2013).

I classified P. karwinskii individuals into one of four stages based on diameter and number of pseudobulbs (Table 5, Figure 6): seedlings (S; <3 pseudobulbs and 6 mm diameter); small juveniles (J1; >4 pseudobulbs, <12mm diameter); medium juveniles (J2; >13 and <18mm diameter); and adults (A; >19mm diameter). Size classes were chosen based on the probability and quantity of reproductive output, and morphological characteristics of seedlings. I built 4X4

Lefkovitch stage-structure transition matrices directly from the annual census field data. The number of orchid seeds produced per capsule was estimated (5000 per capsule). I calculated fecundity F, (number of seedlings produced per individual) as:

F= (no. seeds produced per individual)/total no. of seeds) * total no. of new recruits

The number of new seedlings recruited was calculated from counting the new seedlings that appeared the following year.

Table 5: Size class categories used to create matrix models. Stage Pseudobulb diameter (mm) # Pseudobulbs Seedling (S) < 6.0 < 3 Juvenile 1(J1) < 12 - Juvenile 2 (J2) 13-18 - Adult (A) >19 -

Figure 6: Life history stages of Prosthechea karwinskii. The following letters represent: F, fecundity; R, reproduction; G, growth; and S, stasis. S= seedling, J= juvenile 1, J2 =juvenile 2, and A=adult.

Calculation of long term and transient population growth rates

For each population and year, I calculated the projected deterministic population growth rate of

P. karwinskii, λ, (the dominant eigenvalue of the matrix, interpreted as the rate at which a population would grow over the long-term under the parameterization conditions) and determined the 95% percent confidence intervals of λ with 2000 bootstrap runs (Caswell 2001).

To take environmental variation into account, for each population, I calculated the stochastic population growth rates (λs) by averaging successive growth rates over a simulation with 50,000 iterations, which involved the random alternation of matrices from the three different years. I considered differences in λ and λs to be significant when the confidence intervals did not overlap.

For each matrix and year, I also calculated transient dynamics. Transient dynamic analysis focuses on short-term demographic responses and depends on the starting density of individuals in different stage classes (e.g., the population structure). When the observed population structure is not similar to the stable stage structure (the structure when the growth rate stabilizes to λ), then the behavior of the population over the short term may differ from its projected behavior over the long-term (e.g., lambda values; (Stott et al. 2010)). For all transient analyses, I used the standardized observed population structure for each year.

Harvest simulations

Orchid flowers can be harvested by cutting only the flower, or by removing the pseudobulb(s) that are flowering. To simulate the effects of cutting flowers in the low harvest population, I decreased fecundity values of the adults (by 10%, 30%, 50%, and 100%) and calculated the stochastic λ values. The removal of pseudobulbs likely leads to retrogression, since it involves removal of the largest bulbs, which also causes the plant to lose stored resources that would have

been shared with smaller pseudobulbs. To simulate harvest of flowers with pseudobulbs, I therefore reduced both fecundity and retrogression values of adults in the low harvest population

(by 10%, 30%, 50%, and 100%) and calculated the stochastic λ values. The observed stochastic λ value was assumed to represent a no-harvest scenario.

Elasticities and Life Table Response Experiments

To identify the life-history transitions to which lambda was most sensitive, I carried out elasticity analyses for each population and year. To identify which life history transitions were most responsible for observed differences in lambda values between the high harvest (population 1) and the low harvest population (population 3), I carried out Life Table Response Experiments

(LTREs, Caswell 2001). All demographic analyses were carried out using Popbio (Stubben &

Milligan 2007) and Popdemo (Stott et al. 2012) packages in “R” (R Development Core Team

2013).

Results

The population with the highest harvest pressure (population 1) had fewer individuals in all stage classes proportionate to the other populations (Figure 7). Lambda values varied across years and populations (Figure 8). For all populations, confidence intervals overlapped. Stochastic lambda values differed significantly among populations (Figure 9): population 1 had the lowest value

0.9673 (C.I.=0.9672-0.9676), and population 2 had the intermediate value of 0.9756 (C.I.=

0.9754- 0.9763) and both were significantly less than 1. Population 3 had the highest lambda value (1.0155, C.I.= 1.0152-1.0154; Figure 7).

Analyses of transient dynamics showed that populations 1 and 2 were expected to decrease in density even faster over the short term than predicted by lambda values (Table 6). In contrast, over the short term, population 3 was expected to increase in density at a rate similar to or slightly lower than that predicted by lambda (Table 6).

Figure 7: Structure of the epiphytic orchid, P. karwinskii in three populations, from 2010-2013. Values represent means ± 1 SD. Harvest pressure was highest in population 1 and lowest in population 3.

Figure 8: Lambda values for populations of Prosthechea karwinskii.

Figure 9: Stochastic lambda values for populations of Prosthechea karwinskii organized from high harvest pressure to low harvest pressure.

Table 6: Transient analysis results for P. karwinskii populations.

Population Year First time step Inertia Max attenuation

1 2010-2011 0.997 0.973 0.973 1 2011-2012 0.996 0.993 0.993 1 2012-2013 0.996 0.992 0.99 2 2010-2011 0.985 0.955 0.955 2 2011-2012 1.047 0.744 1.047 2 2012-2013 0.99 0.970 0.978 3 2010-2011 0.952 0.956 0.941 3 2011-2012 1.00333 1.007 1.007 3 2012-2013 1.00986 1.011 1.011

Elasticities and Life Table Response Experiments

The elasticity of survival was dominant in all populations and stages (Figure 10). Elasticity of growth was the second most dominant value for juveniles in population 1 and for seedlings and juveniles in populations 2 and 3. Life Table Response Experiments showed that the two contributors to the higher lambda observed in population 3 versus population 1 for both the

2010-2011 and 2012-2013 time periods were survival and fecundity of adults and growth for all other stages (Figure 11). The years of 2010–2011 and 2012–1013 had similar patterns with growth values for seedlings and juveniles being the largest contributors to lambda (Figure 11).

Figure 10: Elasticity values for Prosthechea karwinskii. A) Low harvest pressure, B) Medium harvest pressure, C) High harvest pressure.

A. High harvest pressure λ =0.995

Low harvest pressure λ =1.031 Period: 2010-2011

B. High harvest pressure λ =0.964

Low harvest pressure λ =0.992 Period: 2011-2012

C. High harvest pressure λ =0.954

Low harvest pressure λ =1.008 Period: 2012-2013

Figure 11: Life Table Response Experiment analyses for populations of Prosthechea karwinskii. Top: Population with high harvest pressure: λ =0.995. Bottom: Population with low harvest pressure: λ =1.031.

Harvest simulations

The harvest simulation experiments with different harvesting intensities showed that lambda dropped below 1 if more than 30% of flowers or flowers and pseudobulbs were extracted (Figure

12).

! Figure 12: Simulated effects of a) flower harvest and b) flower and pseudobulb harvest on P. karwinskii stochastic long-term population growth rates (λs). Simulations were carried out on population 3, the low/no harvested population. Error bars indicate 95% confidence intervals.

Discussion

The projected population growth rate (λ) for P. karwinskii differed among the three study populations and this is likely due to differences in harvest pressure. Populations of P. karwinskii that experience high-medium harvest pressures are declining and are expected to continue to decline if circumstances do not change. By contrast, the population that has the lowest harvest pressure is projected to continue to grow slowly over the long term (i.e., it is significantly greater than 1).

Studies of epiphytic orchid demography have shown lambda values to be close to equilibrium (Lepanthes caritensis Tremblay & Ackerman, λ = 0.995 and 0.999; Lepanthes eltoroensis Stimson, λ = 1.003 ± 0.056; Guarianthe aurantiaca (Bateman) Dressler & W.E.

Higgins, λ = 0.989 ± 0.103 and 0.990 ± 0.087) (Tremblay 1997; Tremblay & Hutchings 2003;

Mondragón 2009). These values suggest that even species that are not being harvested have populations that are close to equilibrium. However, Zotz & Schmidt (2006) documented decline of populations of the epiphytic orchid Aspasia principissa Rchb.f. (λ = 0.92 ± 0.06) in Panama.

They attributed the projected decline to changes in precipitation and forest dynamics, since decreasing annual rainfall affects recruitment and growth (Zotz & Schmidt 2006). Epiphytes are heavily dependent on precipitation (Otero et al. 2005; Zotz & Schmidt 2006); therefore, global climate change can impact epiphyte populations if rainfall is affected at the local level. Climate change projections predict a warming trend over the twenty-first century and precipitation is also likely to change causing a drier climate in this region (Del Castillo et al. 2013). Populations of P. karwinskii are already growing in an oak-chaparral ecosystem, which is relatively drier than the pine-oak forest that surrounds this region. Its host trees may be able to shift up the mountain to other previously cooler environments in the future if the temperatures increase, as has been

documented for other tree species (Del Castillo et al. 2013). However, the predicted decrease in precipitation will likely be a barrier for epiphytes in general and P. karwinskii may be in peril if this occurs.

My LTRE results suggest that the higher population growth rates in the low-harvested population are due to higher rates of survival and reproduction of adults, and higher growth of all of the other stage classes. The effects of harvest may explain this: harvest can remove pseudobulbs and therefore reduce stored resources for reproduction and for growth of plants. The water and starch stored in pseudobulbs may be important for species living in a climate with a pronounced dry season like P. karwinskii. The stored resources are used throughout the season when water is in short supply. For the year of 2011–2012, the contribution from growth to the difference in lambda values between the two populations was much lower. This may be due to the year of 2011–2012 having lower precipitation relative to the other years.

For most epiphytic species, survival is the highest elasticity value (Tremblay 1997;

Tremblay & Hutchings 2003; Mondragón 2009). In the present study, survival also had the highest elasticity value. This suggests that harvest practices that decrease survival can be expected to have a large negative impact on long-term population growth rates.

The only demographic study to assess the potential effects of harvest on an orchid species showed that simulations of harvest of entire reproductive plants could have a serious impact on the survival of the population (Mondragón 2009). The harvest of the entire reproductive plant was used to calculate the probability of quasi-extinction, however, the type of harvest I observed on the populations in this study was only the removal of individual flowering pseudobulbs.

Harvesters removed only the pseudobulbs with the flowers attached and left the remainder of the

plant behind. Plants that had been harvested, survived and some produced flowers the following year (pers. obs.). I also observed that most orchids were being sold by the pseudobulbs in markets in Oaxaca (Chapter 3). This brings up an important point: harvest strategies make a difference in recovery of wild harvested species (Molleman et al. 2011; Nantel et al. 1996). This highlights the importance of studies that investigate how people make decisions to harvest and their effects on population structure of epiphyte populations.

My results suggest that sustainable harvest can be possible if less than 30% of flowering pseudobulbs are harvested per year from large adult plants in a population. However, this assumes harvest from only the adult plants (the largest pseudobulb > 19 cm) and not from any of the smaller sizes, even if they flower. In addition, a change of climate, land-use, or other factors should also be taken into consideration when applying these results to management in the future.

Given that the medium and high harvest populations are declining, harvest has likely been higher than this level over time. Further research to identify the effects of different kinds of harvest on flowering patterns and on the potential to complement wild harvest with community-based cultivation would provide more insight on strategies that can promote conservation, local livelihoods, and cultural traditions.

CHAPTER 5:

CONSERVATION AND MANAGEMENT RECOMENDATIONS

Daniela Dutra Elliott

Department of Botany

University of Hawai‘i at Manoa

3190 Maile Way

Honolulu, HI. 96822

We documented a high volume of orchids being traded during the holiday seasons in Oaxaca. A ban on orchid harvest on the national level has clearly not stopped the harvest of wild orchid species in the state of Oaxaca as seen in Chapter 3 and also in a previous study in the Mexican state of Veracruz (Flores-Palacios & Valencia-Díaz 2007). The harvest ban may have in fact worsened the conditions of wild populations in certain areas since now there is no benefit for local communities to manage populations of these species. According to interviews carried out in orchid-harvesting communities, before the ban harvesters who collected plants from communal lands would return to the same areas year after year to harvest and therefore benefited from not overharvesting these restricted populations. These harvesters had detailed knowledge of where orchids grow and of their ecology. After the harvest ban was enforced, harvesters were afraid of being caught but continued to harvest plants. This uncertainty in resource tenure has been shown around the globe to decrease the harvester incentives for forest conservation, therefore, decreasing their own livelihood security (Cunningham 1993; Nygren et al. 2006).

Demographic studies can tell us what kind of effects has at the population level. The results from the studies conducted here can be applied to conservation and management in the following ways:

1) The harvest of entire individuals should be avoided in all costs.

My results showed that survival of individual plants had the highest elasticity value. This suggests that harvest practices that decrease survival can be expected to have a large negative impact on long-term population growth rates. Results also suggest that the higher population growth rates in the low-harvested population are due to higher rates of survival and reproduction of adults, and higher growth of all of the other stage classes. The effects of harvest may explain this: harvest can remove pseudobulbs and therefore reduce stored resources for reproduction and

for growth of plants. The water and starch stored in pseudobulbs may be important for species living in a climate with a pronounced dry season like P. karwinskii.

2) Sustainable harvest is possible if only parts of adult plants are removed

Results suggest that sustainable harvest can be possible if less than 30% of flowering pseudobulbs are harvested per year from large adult plants in a population. However, this assumes harvest from only the adult plants (the largest pseudobulb > 19 cm) and not from any of the smaller sizes, even if they flower. In addition, a change of climate, land-use, or other factors should also be taken into consideration when applying these results to management in the future.

Given that the medium and high harvest populations are declining, harvest has likely been higher than this level over time.

3) Climate change should be taken into consideration while developing a conservation plans for these species. Epiphytes are heavily dependent on precipitation (Otero et al. 2005; Zotz &

Schmidt 2006); therefore, global climate change can impact epiphyte populations if rainfall is affected at the local level. Climate change projections predict a warming trend over the twenty- first century and precipitation is also likely to change causing a drier climate in this region (Del

Castillo et al. 2013). Populations of P. karwinskii are already growing in an oak-chaparral ecosystem, which is relatively drier than the pine-oak forest that surrounds this region. Its host trees may be able to shift up the mountain to other previously cooler environments in the future if the temperatures increase, as has been documented for other tree species (Del Castillo et al.

2013). However, the predicted decrease in precipitation will likely be a barrier for epiphytes in general and P. karwinskii may be in peril if this occurs.

There are shortcomings to this study. For the market study, volume calculations were based on a single weekday during the 1-year study period. It is possible that the actual numbers are higher than reported here. It is also possible that trends vary from year to year depending on socioeconomic pressures. Also, vendors were reluctant to talk about where plants came from for fear of the governmental authorities. In many cases we acquired an overall locality only and could not corroborate on the localities. This brings up another shortcoming. I could not observe first hand people harvesting plants and the information provided were obtained through interviews. Being present while people are harvesting plants in natural populations would provide extra information related to harvest impacts. The demographic study was conducted for three years. Ideally these plants would be monitored for a longer period so that management plans can be based on data from multiple years. One could also possibly document the effects of climate change on the demography of these populations if longer studies are conducted and management plans can then be modified if needed.

Further research to identify the effects of different kinds of harvest on flowering patterns and on the potential to complement wild harvest with community-based cultivation would provide more insight on strategies that can promote conservation, local livelihoods, and cultural traditions. A local conservation plan that includes the issuing of harvest permits and the inclusion of communities in the management of harvested species could benefit these orchid populations and strengthen cultural ties. These plants are important part of culture and have been linked to pre-Hispanic ceremonies and are currently used in many local celebrations. There is an opportunity here for those involved in local conservation. When plants are important to people, more likely they will care about the fate of the species.

Further studies on the harvest, trade, and ecology of wild orchid populations could be instrumental in strengthening conservation actions at the local level that can protect species, cultural traditions, and local livelihoods. More research, and especially integrated research, on the population dynamics, market dynamics, local management, and ecosystem impacts of epiphyte harvest is needed. The information is essential for designing sustainable management plans. Traditional ecological knowledge should be taken into account in harvest studies. There is little information available on how local people make decisions on the harvest or management of wild epiphyte populations, which are often common pool resources. This knowledge is critical for understanding patterns and intensity of use and their ecological implications. Imposing management policies and regulations that ignore preexisting management practices, and related social institutions, may deteriorate existing land and resource management capacities (Alcorn &

Toledo 1998; Agrawal, Arun and Ostrom 2001).

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