<<

Impacts of Unsustainable Harvesting of - Producing

By

Krystal Gonzalez

(Valerian 2015)

A Capstone

Submitted to

Oregon State University

In partial fulfillment of the requirements for the degree of

Master of Natural Resources

Fall Quarter 2020 2

Abstract

The use of Boswellia ’s fragrant , known as frankincense has been used in religious rituals and medicines for thousands of years. Those same uses have only increased in popularity throughout the world, and have made their way into western culture, where frankincense is a main ingredient in many skin care, cosmetic and medicinal products. The resin that only Boswellia trees produce make frankincense an important non-timber . Additionally, frankincense producing trees have a limited growing range in high altitudes, with specific growing conditions in the arid regions of the Middle East. These factors make the survival of the frankincense tree, all that more vital. Worldwide increases in demand for frankincense has put strain on the few known Boswellia that produce the highly sought- after resin. The harvesting practices of tapping the tree to let the wound response resin seep out, is proving to also be hindering the tree’s ability to reproduce, and maintain population numbers. Harvesters are pressured to tap the tree beyond its capable limits in order to get the most resin they can to sell. Boswellia trees are on the decline, and possibly face extinction if sustainable management practices are not explored and enforced. Conservation and restoration management practices, along with sustainable harvesting techniques are suggested as a means of protecting frankincense producing Boswellia for the livelihoods of the people who depend on the tree as well as for future generations.

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Table of Contents

Abstract ...... 2

List of Figures ...... 4

List of Abbreviations ...... 5

Introduction ...... 6

Geographic Distribution ...... 10

Uses of Frankincense ...... 13

Statement of Problem ...... 15

Purpose of Study ...... 16

Harvesting Practices ...... 17

Effects of Tapping on Boswellia Trees ...... 20

Ecological Significance ...... 24

Socio-economic Significance ...... 26

Recommendations for Sustainable Management ...... 27

Conclusion ...... 32

Bibliography ...... 36

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List of Figures

Figure 1: Thin, paper-like (Kew Science, 2020)...... 7

Figure 2: Yellowish-white frankincense flower with honeybee (AUYB, n.d.)...... 8

Figure 3: Boswellia (AUYB, n.d.)...... 8

Figure 4: Incision and puncture with hardening frankincense resin (AUYB, n.d.)...... 9

Figure 5: Distribution of historically known major frankincense producing species before B. oculta was discovered. Dots represent known locations of Boswellia from several sources (Bongers et al. 2019)...... 11

Figure 6: Identification of new species, Boswellia oculta. (a) Tree in . (b) Tree showing swollen disk-shaped base on rock. (c) Branches showing foliage. (d) Trunk with incisions, showing resin oozing out. Photograph: Ahmed Mohamed Dhunkaal (Thulin, Decarlo and Johnson, 2019)...... 12

Figure 7: 'Pearls of the desert' ooze out within minutes of cutting, immediately releasing their fragrance (Highet, 2006)...... 18

Figure 8: Various frankincense grades. (b) Royal grade harvested from desert areas with little rain. (c) Superior grade, commonly placed in water. (d) Regular grade, commonly used for . (e) Lowest grade, harvested from old or dying trees (Lin et al. 2013) ...... 19

Figure 9: Endogenous phytohormonal (jasmonic acid, abscisic acid and salicylic acid) analysis of tree in response to incision. Asterisk(s) indicate values that are significantly different from those of the control B. sacra tree samples (Khan et al. 2018)...... 22

Figure 10: Reserve of total non-structural carbohydrate (TNC) concentrations for tapped and untapped B. papyrifera trees (Mengistu et al. 2013)...... 23

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List of Abbreviations

ABA Abscisic Acid

BCE Before Common Era

CITIES Convention of International Trade in Endangered Species of Wildlife Fauna and Flora

DBH Diameter at Breast Height

EABC Ethiopian Agricultural Businesses Corporation

IUCN International Union for Conservation of Nature

JA Jasmonic Acid

NGZ North Gondor Zone

NTFP Non-Timber Forest Product

Mg/ha Mega-grams per hectare

USD United States Dollar

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Introduction

Boswellia is a of moderately-sized, deciduous flowering trees and in the family . Boswellia are native to arid regions of the , east Africa, and India. The trees are hardy, but scraggly looking with a whitish to pale brown peeling, paper- like bark (Figure 1). Boswellia produce cosexual single flowers that are yellowish-white (Figure

2) and start to bloom in the winter but may last until April. Boswellia fruit is a capsule (Figure 3) which usually begins to ripe in March. Boswellia trees are best known for its fragrant oleo-gum- resin. The oleo-gum-resin from Boswellia trees is called frankincense, but is also sometimes referred to as olibanum. Frankincense trees begin resin production around eight to ten years after planting. 7

Figure 1: Thin, paper-like bark (Kew Science, 2020). 8

Figure 2: Yellowish-white frankincense flower with honeybee (AUYB, n.d.).

Figure 3: Boswellia fruit (AUYB, n.d.). 9

The fragrance of the gum-resin is described as having a pleasant spicy, citrus, and even woodsy, earthy scent. Frankincense is obtained from making incisions in the trunk or branches, which removes the bark (Figure 4). This process is called tapping. When the tree is slashed, precious white resin oozes from the opening and immediately releases the pronounced fragrance. The resin is the tree’s response to wounding to protect itself from water loss, invasion or diseases. The gum resin is then allowed to harden into granules before it is harvested from the tree. Various forms of frankincense have been a staple in Middle Eastern cultures for thousands of years.

Figure 4: Incision and puncture with hardening frankincense resin (AUYB, n.d.).

Traditional uses of frankincense are still used today in religious and spiritual meditations through incense burning, and for healing certain medical conditions. Frankincense oil is also used in high end cosmetics, such as skin care products and . Currently, due to the high demand of the resin, frankincense production has been on the rise, prompting harvesters to increase the number and intensity of tapping incisions and tapping rounds on individual tree, as a way to promote more resin production. Studies show that increased tapping has a negative 10 impact on the longevity of the health of the tree. Population numbers are declining, and stands have low germination rates. Unsustainable harvesting of frankincense greatly affects the long- term survivability and threatens extinction of the species. The consequences if frankincense

Boswellia species continue to decline, or disappear altogether, have severe socio-economic and ecological implications.

Geographic Distribution

Frankincense producing Boswellia species are known to survive on steep rocky slopes, with an average gradient of 30-40 percent and shallow (< 20 cm), dry soils (Gebrehiwot et al.

2003). The greatest concentration of historically known Boswellia is in the (Figure

5), where 75 percent of all Boswellia are endemic (Lovett and Friis, 1996 as cited in Ogbazghi,

2006). There has been known of only a few species which produce true frankincense; B. sacra,

B. carterii, B. neglecta, B. frereana, B. serrata, and B. papyrifera are the most notable ones.

However, in October 2018, a frankincense producing Boswellia tree was confirmed, through photographs taken for further study (Figure 6), as being a new species. 11

Figure 5: Distribution of historically known major frankincense producing species before B. oculta was discovered. Dots represent known locations of Boswellia from several sources (Bongers et al. 2019).

The new species, Boswellia occulta was found in a small area in northwestern

() (Thulin, Decarlo, and Johnson, 2019). This recent evidence of other frankincense species demonstrates that even though certain frankincense producing species are known to local harvesters, the remote locations of these stands makes frankincense hard to study, and therefore less known in the scientific community. The tree being studied was photographed growing on limestone hillsides and straight out of a large rock, a typical characteristic for

Boswellia in this area (Figure 6b). 12

Figure 6: Identification of new species, Boswellia oculta. (a) Tree in leaf. (b) Tree showing swollen disk- shaped base on rock. (c) Branches showing foliage. (d) Trunk with incisions, showing resin oozing out. Photograph: Ahmed Mohamed Dhunkaal (Thulin, Decarlo and Johnson, 2019). 13

In addition to the unique substrate in which the trees find stability in, Boswellia trees also have a specific geographical growing distribution which is mostly affected by altitude, rainfall and length of the growing period. A study conducted in , in eastern Africa demonstrates that the greatest number of Boswellia are between an altitude range of 800-1850 m (2624-6069 feet), receiving a mean annual rainfall of 375-700 mm (14-27 inches) and with a growing season between 45-100 days (Ogbazghi et al. 2006).

Sources of frankincense species have shifted geographically throughout history. B. sacra was the principal species of classical times, around 500-336 BCE, and is known to produce the most therapeutic and highly sought-after frankincense, which grows in , , and

Somalia (Highet, 2006). B. papyrifera was the principal species of antiquity, around the Middle

Ages, which grows in northeast and West Africa, but inferior forms of this frankincense have been found in Ethiopia, Sudan and East Africa (Highet, 2006). B. serrata grows in Somalia and

India, where Indian Frankincense (Indian olibanum) is also derived from this species (Highet,

2006). B. neglecta is known as “ frankincense” due to the dark color of the dried tears, and occurs mostly in Ethiopia, Kenya, Somalia, Tanzania and Uganda (Mokria et al. 2017). B. carteri and B. frereana are the main sources of frankincense today native to Somalia, Iran and Iraq

(Highet, 2006).

Uses of Frankincense

Once known to be as valuable as in ancient times and an important symbol in many religious faiths, frankincense has been burned, chewed, traded, and even idolized as being the sweat of the gods. The use of frankincense has a long history, which continues today. One of 14 the first recordings of frankincense being burned was in Sumerian temples, which can be dated as far back as 3500 BCE (Highet, 2006). When burned, it has been reported to enhance spiritual perception, and improve emotional well-being, making it popular in religious rituals and meditations. Frankincense powders and teas have been used in Chinese medicine since at least

500 BC(E) to treat rheumatic disease, menstrual disorders and bruises (Ulbricht et al. 2004). It was believed that frankincense reduces pain and swelling that is typically associated with these conditions. Additionally, olibanum can also be dated back to where the oil was used as an ingredient in embalming liquids for mummification (Ulbricht et al. 2004).

In modern times, frankincense has become a main ingredient in high-end perfumes and skincare products, and is used in medicine to treat mild and severe medical conditions. Still today, local people chew the resin as a way to quench thirst or suppress stomach pains (Worku and Bantihun, 2018). Meanwhile, scientific studies are being conducted to determine the extent of what the anti-inflammatory properties in frankincense can achieve. For example, a

2012 study confirmed frankincense suppressed pancreatic tumor growth and induced pancreatic tumor death in a xenograft nude mouse model (Ni et al. 2012). Another, demonstrated that high-doses of frankincense can accelerate neurological function after a sciatic nerve injury (Jiang et al. 2016).

With growing scientific studies confirming frankincense’s perceived health benefits in modern culture, coupled with the wide variety of cosmetic, and aromatic uses, this multifaceted gum resin continues to gain popularity around the world. With such a high 15 demand for this resin, the ‘pearls of the desert’ have an important place in societies. However, like all valuable natural resources, frankincense is threated by .

Statement of Problem

Frankincense producing Boswellia trees are among only a few woody trees that are capable of surviving in the harsh environments of the Middle East, where other tree species often fail. Boswellia are best known globally for their non-timber forest product (NTFP), frankincense, but it also has socio-economic, and ecological importance to the local people and the region. Commercial harvesting of NTFP’s can be detrimental to a species, especially if there is an already low natural abundance of the said species (Van Valkenburg, 1997; Van Dijk, 1999 as cited in Hernández-Barrios et al. 2015). Increased global pressure for higher frankincense yields has local harvesters tapping more frequently than what the tree can handle, causing physiological effects to the tree. Additionally, wild trees in more populated areas such as near roads and communities, where accessibility is easier, are being exploited for their resin from unskilled locals. Due to unsustainable tapping practices, coupled with a changing climate, frankincense producing Boswellia population numbers are on the decline, and the species faces extinction if misuse and overexploitation continue.

The frankincense producing Boswellia are very well known to local harvesters but there is a lack of scientific study, effective long-term management and protection from overexploitation and degradation of the species’ habitat. Additionally, data needs to be updated on current population numbers and the overall health of the species in these areas.

Currently, only one frankincense producing Boswellia, B. sacra, is listed on the International 16

Union for Conservation of Nature (IUCN) “Red list” of Threatened Species, as ‘near threatened’

(The IUCN Red List of Threatened Species, 2020). Additionally, B. serrata is listed as Critically

Endangered Possible Extinct (CEPE) on the National Red List of Sri Lanka, but not on the IUCN

(MOE, 2012 as cited in Brendler, Brinckmann and Schippmann, 2018). However, other Boswellia also show a decline in total numbers. Model analysis of B. papyrifera in the woodlands of

Ethiopia showed a continuous and alarming decline in population and volume of the species

(Lemenih et al. 2014). This trend is being seen among other Boswellia species which show a similar decline.

The species is not only suffering from adult mortality, but Boswellia forest lack regeneration and juvenile trees as well. One study site reported no trees younger than 55 years and no stem diameters of <10 cm (Tolera et al. 2003b). Another showed that two stands in

Ethiopia had an average age of 71, suggesting that tree regeneration has failed over the last half century (Tolera et al. 2013b). This suggest, with no intervention, populations would collapse. Conservation and restoration efforts are urgently needed to ensure the long-term availability of frankincense resin as a means to provide a certain quality of life for present and future generations who depends on the species for their livelihoods.

Purpose of Study

The objectives of this capstone project are to identify ways in which Boswellia trees are being harvested for frankincense, and determine how harvesting techniques are hindering the long-term survival of the species. Based on a synthesis of existing data, this study will demonstrate how a decline in Boswellia populations in this area are a result of unsustainable 17 harvesting practices, which create interconnected problems from socio-economic hardships, to ecological degradation. Furthermore, this study will then provide recommendations based on these findings that suggest implementation of local and international conservation and restoration management practices, that will include proven harvesting techniques, the likes of which can provide a more long-term sustainable use of the Boswellia’s NTFP, Frankincense.

Additionally, this paper recommends conservation information be updated for frankincense producing Boswellia, and those with rapidly declining number be internationally protected through the Convention of International Trade in Endangered Species of Wildlife

Fauna and Flora (CITES) under Appendix II.

Harvesting Practices

Resin secretion from Boswellia trees is an immediate response as a result of abiotic or biotic stress, including purposeful human made wounds. Resin production is a result of the tree sealing and protecting itself from disease, insect invasion, and/or water loss (Eshete, Sterck, and Bongers, 2012). Tapping for resin production is done along the branches and stem with a traditional tool which resembles a chisel called a mangaf. The mangaf tool has a metal end, about 2 cm wide, with a wooden handle (Tadesse, Feleke, and Eshete, 2004).

Tapping starts in October, the start of the dry season when the trees are without , and goes to the first week of June, when the rainy season begins (Eshete, Sterck and Bongers,

2012). The first tapping wound in the first round is a longitudinal incision about 4-8 cm with a depth of 1 mm (Tadesse, Feleke, and Eshete, 2004; Eshete, Sterck and Bongers, 2012). After an 18 incision is made, the white resin immediately flows out (Figure 7), dries and hardens into granules before it is removed with the blunt end of the mangaf. Hardened granules are called tears. Frankincense tears are hand graded and sorted based on color, purity, aroma, and age.

The wide variety of grades depends on many factors such as, the geographic location, time of harvest, climate, or on the age of the tree. There are four common commercial grades (Figure

8). Each cycle of cut and collection of dried tears are called rounds.

Figure 7: 'Pearls of the desert' ooze out within minutes of cutting, immediately releasing their fragrance (Highet, 2006). 19

Figure 8: Various frankincense grades. (b) Royal grade harvested from desert areas with little rain. (c) Superior grade, commonly placed in water. (d) Regular grade, commonly used for incense. (e) Lowest grade, harvested from old or dying trees (Lin et al. 2013)

Each subsequent tapping round deepens and enlarges the original tapping spot. The number of tapping wounds on a single tree depends on the diameter or the trunk; the larger the tree, the more space for tapping wounds. Typically, trees with a diameter of 30 cm can have

8-12 tapping spots around the stem. However, with the higher demand, trees have been reported to have up to 27 tapping spots in some commercial sites (Kebede, 2010 as cited in

Tolera et al. 2013a). Each tapping spot on a tree can go through 8-12 tapping rounds per year

(Eshete, Sterck and Bongers, 2012). Larger trees produce more frankincense yield as well as with each subsequent tapping round. Trees with 10-15 cm DBH produce between 84-181 grams 20 of resin from 7 tapping rounds, while a tree with at least a 30 cm DBH produces 744-1233 grams from 14 tapping rounds (Eshete, Sterck, and Bonger, 2012). However, it has been shown that increased production levels off beyond the 9th tapping round and gradually levels off from trees that have greater than 20 cm stem diameters (Eshete, Streck and Bongers, 2012).

Effects of Tapping on Boswellia Trees

The effects of harvesting NTFP is typically only assessed over short periods, in which harvesting that may appear sustainable in the short term, is actually not in the long run. Often times with harvesting of NTFP, harvesting techniques that maximize short-term economic gain also tend to have little consideration for the long-term ecological consequences. To assess sustainability, it is necessary to look at the ecological effects over a long-time span (Hernández-

Barrios et al. 2015). Several recent studies are suggesting that tapping Boswellia trees for frankincense are, in fact, having a negative effect on the long-term survival of the species.

These studies are showing that population numbers are declining as a direct result of the physiological impacts tapping has on the tree.

Boswellia trees are already at a disadvantage from the start compared to other that co-dominate the drylands. Boswellia are a slower growing tree compared with other species in the region, averaging between 0.71 and 1.80 mm annually (Tolera et al. 2013b).

Additionally, based on age diameter relationships, most frankincense stands are dominated by large, old trees, suggesting that regeneration failure has occurred during several decades across the Horn of Africa (Bongers et al. 2019). Due to the lack of regeneration among the species, scientists have gathered information regarding the cause of declining populations, and traced it 21 back to the thousands of years of stress that has been put on Boswellia from intense tapping for resin. Tapped Boswellia trees are showing physiological, chemical, and reproductive stresses, all of which are impacting the future growth of the species.

Samples collected from B. sacra in two locations in a wild desert woodland of southern

Oman show that endogenous abscisic acid (ABA) and jasmonic acid (JA) were significantly higher in wounded tree samples (Figure 9) (Khan et al. 2018). ABA is a hormone in plants that regulates growth, development and stress responses (Chen et al. 2020). Similarly, JA plays a role in regulating and modifying the negative effects of wound induced physiological changes in plants (Khan et al. 2018). Wounded trees in these sample stands also showed changes in selected gene transcripts, which is corelated with the JA response to wounding (Khan et al.

2018). 22

Figure 9: Endogenous phytohormonal (jasmonic acid, abscisic acid and salicylic acid) analysis of Boswellia sacra tree in response to incision. Asterisk(s) indicate values that are significantly different from those of the control B. sacra tree samples (Khan et al. 2018).

Wounding also negatively influences the accumulation of essential nutrients, the amino acid content, and the composition of sugars (Khan et al. 2018). Soluble sugars such as sucrose, fructose and glucose, along with amino acids, are activated during plant growth stages beginning from seed germination into later developmental stages (Couee et al. 2006 as cited in

Khan et al. 2018). Sugars play an active role in stress factors and are more readily available and therefore more easily mobilized when needed, this cannot be said for other physiological functions needed by the tree such as starches (Khan et al. 2018) (Mengistu et al. 2013).

Other studies on B. papyrifera stand in the highland and lowlands of Ethiopia demonstrate tapping also reduces the carbohydrate storage (Figure 10) (Mengistu et al. 2013).

When deciduous trees, such as Boswellia, have a full canopy, their leaves acquire carbon 23 through photosynthesis. The tree then stores excess carbon as starch and sugars to be used later, perhaps in a time of stress. Trees accumulate carbon reserves in different tissues such as the leaves, stems, branches or (Mengistu et al. 2013). Stored carbon is used in the dry season when the tree is without leaves and pools are expected to be filled again in the rainy season when the tree is in leaf.

Tapping may cause the tree to allocate photosynthetic products, such as carbohydrates, to healing wounds, where the carbon-rich resin depletes the tree’s carbon storage. This explains results of tapped Boswellia trees producing less flowers, , leaves and seeds than non-tapped trees, where these carbohydrates would normally be allocated to (Rijkers et al.

2006).

Figure 10: Reserve of total non-structural carbohydrate (TNC) concentrations for tapped and untapped B. papyrifera trees (Mengistu et al. 2013).

Tapping also effects seed viability and the susceptibility of the seed to insect attack.

Proportions of seeds attacked by in untapped stand ranged from 7.7% to 19.17% while tapped stands ranged from 13.9% to 17.3% (Eshete et al. 2012). Similarly, seeds from annually 24 tapped stands in Eritrea have significantly lower germination rates, as low as 13.5% to 16% when compared from untapped trees (94% and 80%) (Rijkers et al. 2006). However, free grazing of livestock in most of Ethiopia, Eritrea and Sudan mainly affect the regeneration of the frankincense trees (Teshome, Eshete, and Bongers, 2017). This is caused from removing whole plants or important reproductive plant parts, as well as trampling of the soil, resulting in compaction which limits seedling establishment (Teshome, Eshete, and Bongers, 2017).

Ecological Significance

Trees, no matter their location provides social, economic, and ecological benefits to the land and people around them. Boswellia trees are no exception, and in fact play a crucial role in ecosystem services in the arid areas of the Middle East, India and Africa. As we will see, forest ecosystems have complex interrelationships that affect all aspects of the biosphere.

North Africa and the Arabian Peninsula are characterized as having sandy soils which are weakly structured and susceptible to erosion (ISIRC, 2015). Similarly, a study of the topsoil in

Eritrea, located in the Horn of Africa was also shown to have very low organic matter content

(Ogbazghi et al. 2006). Trees in these arid areas help fight against desertification, and soil erosion from wind and water. The leaf litter from the deciduous Boswellia trees improve soil fertility, enhancing the biodiversity from the ground up. Additionally, the flowers are an important source of and nectar for honeybees (Eshete, Teketay and Hulten, 2012). The long flowering season of Boswellia trees from October to February is helpful for bee colony maintenance (Gebrehiwot et al. 2003). 25

Land cover from trees alone are important features during the world’s climate crisis by lowering air and surface temperatures and providing shade to people. Boswellia, like all trees, release oxygen and remove carbon dioxide from the air, becoming great sources of carbon sequestration. In Ethiopia alone, Boswellia forests account for 45.7% of the total carbon stock in the area (Mogers et al. 2010 as cited in Mokria et al. 2017). Similarly, studies conducted in

India on the belowground and aboveground carbon measured Boswellia forest as having a total carbon stock of 104.7 Mg C/ha (Raha et al. 2010). In this area in the Boswellia forest types,

Boswellia serrata was the highest contributor (73%) of the total biomass and carbon stocks

(Raha et al. 2010). These features are important all over the world, but especially crucial where other carbon sequestering plant species struggle to survive.

Just in Ethiopia, the drylands comprise over 70% of the landmass and dryland forest account for 48% (Lemenih, Feleke, and Tadesse, 2007; WBISPP, 2004 as cited in Mokria, 2017).

B. papyrifera alone covered 510,000 hectares of land in Ethiopia in the late 1970’s, but has already been reduced to an estimated 330,000 hectares (BoPED, 2000 as cited in Tilahun et al.

2007).

The fact that these trees grow in harsh conditions, and sites where other species often fail, proves that, by protecting and promoting increased population numbers, the tree is beneficial for other natural resources from the soil to the sky. 26

Socio-economic Significance

Frankincense producing Boswellia are not only important trees for their oleo-gum-resin locally, regionally and nationally, but they also are used locally for their various other resources.

Boswellia timber is used in fence construction, household furniture, and firewood. Leaves and seeds are used as fodder for goats, camels and other livestock (Gebrehiwot et al. 2003). The bark is used as medicine to cure stomach pains and is also burned as an insecticide against mosquitos (Worku and Bantihun, 2018). In addition to the most common uses of the gum resin that was discussed earlier, it is also used to fix or bind broken material (Worku and Bantihun,

2018).

Frankincense production creates jobs and provides an income for people who harvest, sort, and sell the resin. In Ethiopia, tapping and grading of frankincense generated an estimated employment of 20,000 to 30,000 people a season, nationally (Girma, 1998 as cited in Tilahun et al. 2007). Ethiopia is one the world’s largest producers of frankincense and therefore exploitation of the resin is the top income and employment generating activities, besides the livestock sector, even in the remotest part of the country (Worku and Bantihun, 2018). This makes frankincense production an important source of revenue, not only for the local people, but also for the country. However, local people benefit the most.

In the southeastern lowlands of Ethiopia, nearly one-third of the local people’s household income comes from frankincense gum collection and sale (Lemenih, Feleke, and

Tadesse, 2007). Similarly, in Tigray, the northernmost region in Ethiopia, about 7,000 seasonal laborers are employed annually, of which, 31 percent are women (Worku and Bantihun, 2018). 27

Men are mainly involved in tapping while women normally are in charge of sorting and grading.

A tapper can collect about 1,000-1,500 kg of resin per year and earn an income of $100 to $150

USD, while women accrue an annual average income of $160 USD (Aregawi, 1997 as cited in

Gebrehiwot et al. 2003; Tilahun, 1997 as cited in Gebrehiwot et al. 2003).

Recommendations for Sustainable Management

The fact that Boswellia trees grow in unforgiving substrates, and survive in climates where other species fail, makes the tree an important element in ecosystem services of its native arid regions. Stronger conservation and management actions need to be implemented in order to save the species from complete extinction, so that the trees can continue to provide the socio-economic and ecosystem services that are so desperately needed. Conservation and management of the resource needs to start at the local level first and foremost, where harvesters have an important responsibility to maintain the resource in a sustainable way.

Harvesters are not oblivious to the fact that that management needs to begin at the local level. A survey conducted in the North Gondor Zone (NGZ) of Ethiopia confirmed that native inhabitants agree that the Boswellia forest are declining as a result of the tragedy of the commons (Lemenih et al. 2007). Most farms are family owned, and although there are not official records of boundaries, they are known precisely by the owners themselves (Decarlo, Ali,

Ceroni, 2020). There is no responsible government body at the local level for the proper conservation and sustainable management of the woodlands. However, management is individually determined and traditional law sets certain rules to be followed. For example, the tree is not to be unnecessarily harmed, such as not cutting the branches for livestock fodder 28

(Decarlo, Ali and Ceroni, 2020). Additionally, traditional law is to let the tree rest periodically after harvesting (Decarlo, Ali and Ceroni, 2020). Although landowners and harvesters want to follow these traditional laws, corporations that purchase the resin apply pressure to increase frankincense yield to keep up with the increasing demand, disregarding the indigenous knowledge that has, thus far, sustained frankincense production. Without an overarching governmental body, it leads to exploitation and improper tapping for frankincense.

Synthesis of Sustainable Harvesting Practices

Tapping, which intentionally induces stress to the tree, seems to be one of the main causes of declining population numbers for Boswellia trees. Because there is such an important socio-economic significance attached to the species as well, a complete ban of tapping is not realistic. However, it is necessary to minimize physiological stress to the tree during harvesting, so that normal growth functions and seed germination can occur. Many suggestions have been put forth as viable alternatives to current tapping practices, all taking into account maximum resin yield, while minimizing stress occurrences to the tree. These suggestions also hope to improve seed germination.

Given that Boswellia populations are dominated by mature individuals, improvements in seed germination is an important factor for regrowing Boswellia forest. Experiments with “in vitro” propagation using mature green fruits in different media and sucrose concentrations are showing promise. A study conducted in western India reported that 91 percent of the embryos in the Murashige and skoog (MS) media containing a 3 percent sucrose concentation showed signs of typical germination in 4 weeks (Ghorpade, Chopra, and Nikam, 2010). Although more 29 frankincense is harvested from the wild than from plantations, results from studies such as this can be used in nurseries to successfully germinate Boswellia before being transferred to farms or plantations.

On the other hand, untapped populations also showed no successful regeneration, indicating that impacts of other factors such as fire and grazing must be considered

(Groenendijk et al. 2012 as cited in Tolera et al. 2013b). Therefore, protection against anthropogenic disturbances by fire and grazing may also allow successful development of seedlings to juvenile stages and beyond. This protection can be done by closing wild forest to grazing and browsing by livestock. In addition to benefits received for Boswellia seedlings in closed forest, where access is restricted, there is evidence of economic benefits as well. Studies conducted on an open and closed forest revealed that annual net income from closed forest was substantially higher than that from open forestland (Tilahun et al. 2007). As a result, these forests have a higher tree density and therefore increased frankincense yield. Higher frankincense revenues from closed forests are socially attractive, and therefore it increases the attention for conservation of these forest by the people who depend on them (Tilahun et al.

2007).

In relation to tapping techniques, suggestions to reduce the number of tapping rounds per tree and reduce the number of tapping spots per tree have been considered. These considerations also take into account the size of the tree. The cessation of tapping on small, younger trees is suggested. There is a low yield of frankincense on small trees (10-15 cm), and tapping causes more physiological stress to smaller trees than larger trees (Eshete et al. 2012). 30

A minimum of 20 cm DBH for tapping is suggested for all trees (Eshete et al. 2012). Reducing the damage to smaller trees will increase their ability to grow to a larger, more productive size.

It is important to note that based on the slow growth of Boswellia trees, it is estimated that it would take about 73 years for a tree to reach the 20 cm minimum diameter (Tolera et al.

2013). Therefore, frankincense production may initially decrease, even if improved seedling growth started today.

A resting period after tapping has also been proposed to allow the tree to heal following wound incisions. A period of 4 and 14 years has been suggested in order for the tree to attain full potential for viable seed production (Ogbazghi, 2001, as cited in Gebrehiwot et al. 2003).

However, this scenario seems unlikely to happen, given the high demand for frankincense, and short supply of frankincense bearing trees.

Tree size plays a factor for proper management. Frankincense production was determined by tree size in studies conducted on B. papyrifera in Ethiopia. These studies concluded that on smaller diameter stems with a DBH between 10-20 cm, frankincense production leveled off beyond 3-6 tapping rounds (Eshete, Sterck, and Bongers, 2012).

Conversely, stems with a DBH between 15-20 cm leveled off between 6-9 tapping rounds

(Eshete, Sterck, and Bongers, 2012). Based on these findings, at the least, tapping should be maximized to no more than 3 tapping rounds on smaller trees, if complete production cannot be stopped on stems <20 cm DBH, as discussed earlier, and maximized to no more than 7 tapping rounds on trees with >20 cm DBH. 31

Most important in the production of frankincense is to maximize resin yield while minimizing stress to the tree. This is possible by making one, deep incision in the bark of the tree. An analysis of the resin secretory structures of B. papyrifera found that these structures are predominantly found in the bark, which has an average thickness of 17.2mm with two main layers (Tolera et al. 2013a). The inner bark makes up 17.0 mm while the outer bark is 0.2 mm and the two layers together make up about 15% of the stem radius (Tolera et al. 2013a). Axial and radial resin canals are connected through phloem forming a three-dimensional network, making them functional for short and long-distance resin transport (Tolera et al. 3013a).

Based on this study, with the presence of interconnected canals, coupled with the findings that frankincense is present in the secretory system as a preformed resin, it could be beneficial to drain all the preformed resin with one, deep cut into the intact part of the bark, to the depth that is usually reached during the 7th tapping round that yields the maximum yield

(Tolera et al. 2013a; Ethete et al. 2012). The flow of resin would eventually dry and harden and would need to be re-opened to drain the remaining resin. Regardless, this strategy would be less harmful to the tree by reducing the number of wounds needed to drain the same pool, and require less labor for production (Tolera et al. 2013a).

Improved tapping techniques alone cannot prevent the species from population decline or total extinction and therefore do need further protection at the national level. It is recommended that all frankincense producing Boswellia be further reviewed for international protection from CITES. Those of which meet the criteria for protection under any of the

Appendices, will be protected through international agreements between governments, the 32 likes of which will ensure that international trade of frankincense resin does not threaten the survival of the species. These agreements will hopefully minimize trade of unsustainably harvested frankincense going out of major producing nations as well as prevent frankincense that is unsustainably harvested from entering other nations.

Similarly, local corporations, such as a newly established Federal Government Public

Enterprise, the Ethiopian Agricultural Businesses Corporation (EABC) can ensure that the natural gums they harvest, purchase and value are collected sustainably, before being supplied to domestic and international markets. Additionally, conservation and research projects, such as Save Frankincense, are continuing to work with these governmental agencies as well as with academic, corporate and private partners to protect Boswellia forest and ensure a fair and sustainable frankincense economy.

Conclusion

The production of frankincense resin from Boswellia trees has been a common practice among local harvesters for thousands of years. The multitude of uses that frankincense provides has created a global demand for the natural resource. Like many of earth’s important commodities, high demand threatens overexploitation. Harvesters are pressured to intensify tapping to keep up with demand. Conversely, tapping is causing physiological, chemical, and physical stresses to the tree, which are hindering the species’ ability to reproduce effectively.

If Boswellia forest cease to exists in their native region, it can cause irreversible ecological degradation and socio-economic hardships to the land and people which depend on 33 the trees for their livelihood. The ecosystem services the trees provide are complex and dynamic systems that are inter-related to one another. A change in one can have far reaching impacts on others. Just to name a few, the trees improve soil fertility and prevent soil erosion from wind and rain. The tree’s flowers are a great source nectar for honeybees, which provide ecosystem services in their own right. Leaves take in carbon dioxide, provide oxygen, and reduce surface and air temperatures, an important feature in parts of the world where climate change can greatly impact not only the land, but also the people.

Equally, Boswellia trees provide socio-economic benefits as well. Frankincense production provides jobs and an income for local people. The trees also provide fodder for livestock, camels and goats. Timber from the trees is used in fence construction, furniture, and firewood.

The socio-economic benefits coupled with the important ecological and ecosystem services the trees supply are reasons enough to bring forth natural resource management and protection of the species from decline and possible extinction. Improving tapping techniques that reduce stress to the tree, will also allow the tree to better allocation photosynthetic products for more viable seeds. These recommendations also take into account maximum frankincense yield.

One recommendation for tapping is to minimize the number of tapping rounds to no more than 3, in trees with stems of <10 cm DBH, and no more than 7 rounds in stems greater than 20 cm, the number at which resin production begins to level off. Another option is to ban tapping on younger trees all together, typically this categorizes trees with stems less than 20 34 cm DBH. Lastly, minimizing the total stress from each individual tapping round is ideal. To do this, creating a single, deep incision to drain all resin at once is a viable option. This last recommendation also reducing the amount of labor needed for harvesting.

Tapping techniques will help tree numbers recover but other protection of Boswellia forest is also needed. Closing forests to livestock grazing and browsing will allow seedlings and samplings to develop into juvenile and later developmental stages, creating more tree density in these forests. In concert, more trees mean increased frankincense production. Lastly, it is recommended that frankincense producing Boswellia species be reviewed for international protection from CITES to investigate if the species meet the criteria to be listed under any of the CITES appendices.

The management of Boswellia forest’s natural resources are complex and inter-related with other systems. This paper has only discussed one aspect of the dynamic situation, and therefore additional natural resource management should be considered. Landowners, who manage the harvesting on their own farms should have support from local government so that they are able to enforce any local or international regulations listed above.

While more research needs to be conducted, sustainable harvesting of frankincense through improved tapping techniques, coupled with local forest management and national protection, can significantly prevent frankincense producing Boswellia species from population decline, or worse, extinction.

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Bibliography

AYUB. “Frankincense.” Accessed December 5, 2020. https://ayublab.com/frankincense.

Bongers, Frans, Peter Groenendijk, Tesfaye Bekele, Emiru Birhane, Abebe Damtew, Mathieu

Decuyper, Abeje Eshete, et al. 2019. “Frankincense in Peril.” Nature Sustainability 2 (7):

602–10. https://doi.org/10.1038/s41893-019-0322-2.

Brendler, T., J. A. Brinckmann, and U. Schippmann. 2018. “Sustainable Supply, a Foundation for

Natural Product Development: The Case of Indian Frankincense ( Roxb.

Ex Colebr.).” Journal of Ethnopharmacology 225 (October): 279–86.

https://doi.org/10.1016/j.jep.2018.07.017.

Chen, Kong, Guo-Jun Li, Ray A. Bressan, Chun-Peng Song, Jian-Kang Zhu, and Yang Zhao. 2020.

“Abscisic Acid Dynamics, Signaling, and Functions in Plants.” Journal of Integrative Plant

Biology 62 (1): 25–54. https://doi.org/10.1111/jipb.12899.

DeCarlo, Anjanette, Ali Saleem, and Marta Ceroni. 2020. "Ecological and Economic

Sustainability of Non-Timber Forest Products in Post-Conflict Recovery: A Case Study of

the Frankincense (Boswellia Spp.) Resin Harvesting in Somaliland

(Somalia)." Sustainability 12 (9): 3578.

doi:http://dx.doi.org.ezproxy.proxy.library.oregonstate.edu/10.3390/su12093578.

http://proxy.library.oregonstate.edu.ezproxy.proxy.library.oregonstate.edu/login?url=h

ttps://www-proquest-com.ezproxy.proxy.library.oregonstate.edu/scholarly-

journals/ecological-economic-sustainability-non-timber/docview/2397285770/se-

2?accountid=13013. 37

Eshete, A., D. Teketay, and H. Hulten. 2012. “The Socio-Economic Importance and Status of

Populations of (Del.) Hochst. in Northern Ethiopia: The Case of

North Gonder Zone.” Forests, Trees and Livelihoods 15 (1): 55–74.

https://doi.org/10.1080/14728028.2005.9752507.

Eshete, Abeje, Demel Teketay, Mulugeta Lemenih, and Frans Bongers. 2012. “Effects of Resin

Tapping and Tree Size on the Purity, Germination and Storage Behavior of Boswellia

Papyrifera (Del.) Hochst. Seeds from Metema District, Northwestern Ethiopia.” Forest

Ecology and Management 269 (April): 31–36.

https://doi.org/10.1016/j.foreco.2011.12.049.

Eshete, Abeje, Frank J. Sterck, and Frans Bongers. 2012. “Frankincense Production Is

Determined by Tree Size and Tapping Frequency and Intensity.” Forest Ecology and

Management 274 (June): 136–42. https://doi.org/10.1016/j.foreco.2012.02.024.

Gebrehiwot, K., B. Muys, M. Haile, and R. Mitloehner. 2003. “Introducing Boswellia papyrifera

(Del.) Hochst and its non-timber forest product, frankincense.” International

Review 5 (4): 348–353. https://doi.org/10.1505/IFOR.5.4.348.22661.

Ghorpade, Ravi P., Arvind Chopra, and Tukaram D. Nikam. 2010. “In Vitro Zygotic Embryo

Germination and Propagation of an Endangered Boswellia Serrata Roxb., a Source of

Boswellic Acid.” Physiology and Molecular Biology of Plants 16 (2): 159–65.

https://doi.org/10.1007/s12298-010-0017-7. 38

Hernández-Barrios, Juan C., Niels P. R. Anten, and Miguel Martínez-Ramos. 2015. “Sustainable

Harvesting of Non-Timber Forest Products Based on Ecological and Economic Criteria.”

Journal of Applied Ecology 52 (2): 389–401. https://doi.org/10.1111/1365-2664.12384.

Highet, Juliet. 2006. Frankincense: Oman’s Gift to the World. Munich; New York: Prestel.

ISRIC. 2015. “World Reference Base for Soil Resources (WRB).” ISRIC World Soil Information.

World Data System, 2015. https://www.isric.org/explore/wrb.

Jiang, Xiaowen, Jun Ma, Qingwei Wei, Xinxin Feng, Lu Qiao, Lin Liu, Binqing Zhang, and Wenhui

Yu. 2016. “Effect of Frankincense Extract on Nerve Recovery in the Rat Sciatic Nerve

Damage Model.” Evidence - Based Complementary and Alternative Medicine, January,

NA-NA. https://doi.org/10.1155/2016/3617216.

Kew Science. “Boswellia Sacra Flück.: Plants of the World Online: Kew Science.” Plants of the

World Online, 2020.

http://www.plantsoftheworldonline.org/taxon/urn:lsid:ipni.org:names:127065-1.

Khan, Abdul Latif, Ahmed Al-Harrasi, Raheem Shahzad, Qari Muhammad Imran, Byung-Wook

Yun, Yoon-Ha Kim, Sang-Mo Kang, Ahmed Al-Rawahi, and In-Jung Lee. 2018. “Regulation

of Endogenous Phytohormones and Essential Metabolites in Frankincense-Producing

Boswellia Sacra under Wounding Stress.” Acta Physiologiae Plantarum 40 (6): 113.

https://doi.org/10.1007/s11738-018-2688-6.

Lemenih, M., B. Arts, K. F. Wiersum, and F. Bongers. 2014. “Modelling the Future of Boswellia

Papyrifera Population and Its Frankincense Production.” Journal of Arid Environments

105 (June): 33–40. https://doi.org/10.1016/j.jaridenv.2014.02.006. 39

Lemenih, M., S. Feleke, and W. Tadesse. 2007. “Constraints to Smallholders Production of

Frankincense in Metema District, North-Western Ethiopia.” Journal of Arid Environments

71 (4): 393–403. https://doi.org/10.1016/j.jaridenv.2007.04.006.

Lin, Hk, Mahmoud Suhail, KM Fung, CL Woolley, and DG Young. 2013. “Extraction of Biologically

Active Compounds by Hydrodistillation of Boswellia Species Gum for Anti-Cancer

Therapy.” OA Alternative Medicine 1 (February). https://doi.org/10.13172/2052-7845-1-

1-385.

Mengistu, Tefera, Frank J. Sterck, Masresha Fetene, and Frans Bongers. 2013. “Frankincense

Tapping Reduces the Carbohydrate Storage of Boswellia Trees.” Tree Physiology 33 (6):

601–8. https://doi.org/10.1093/treephys/tpt035.

Mokria, Mulugeta, Motuma Tolera, Frank J. Sterck, Aster Gebrekirstos, Frans Bongers, Mathieu

Decuyper, and Ute Sass-Klaassen. 2017. “The Frankincense Tree Boswellia Neglecta

Reveals High Potential for Restoration of Woodlands in the Horn of Africa.” Forest

Ecology and Management 385 (February): 16–24.

https://doi.org/10.1016/j.foreco.2016.11.020.

Ni, Xiao, Mahmoud M. Suhail, Qing Yang, Amy Cao, Kar-Ming Fung, Russell G. Postier, Cole

Woolley, Gary Young, Jingzhe Zhang, and Hsueh-Kung Lin. 2012. “Frankincense Essential

Oil Prepared from Hydrodistillation of Boswellia Sacra Gum Resins Induces Human

Pancreatic Cancer Cell Death in Cultures and in a Xenograft Murine Model.” BMC

Complementary and Alternative Medicine 12 (1). https://doi.org/10.1186/1472-6882-

12-253. 40

Ogbazghi, Woldeselassie, Toon Rijkers, Marius Wessel, and Frans Bongers. 2006. “Distribution

of the Frankincense Tree Boswellia Papyrifera in Eritrea: The Role of Environment and

Land Use.” Journal of Biogeography 33 (3): 524–35.

Raha, Debojyoti, Javid Ahmad Dar, Praveen Kumar Pandey, Parvaiz Ahmad Lone, Satyam Verma,

Pramod Kumar Khare, and Mohammed Latif Khan. “Variation in Tree Biomass and Carbon

Stocks in Three Tropical Dry Deciduous Forest Types of Madhya Pradesh, India.” Carbon

Management 11, no. 2 (2020): 109–20. https://doi.org/10.1080/17583004.2020.1712181.

Rijkers, Toon, Woldeselassie Ogbazghi, Marius Wessel, and Frans Bongers. 2006. “The Effect of

Tapping for Frankincense on Sexual Reproduction in Boswellia Papyrifera.” Journal of

Applied Ecology 43 (6): 1188–95. https://doi.org/10.1111/j.1365-2664.2006.01215.x.

Tadesse, Wubalem, Sisay Feleke, and Teshome Eshete. 2004. “Comparative Study of Traditional

and New Tapping Method on Frankincense Yield of Boswellia Papyrifera.” Ethiopian

Journal of Natural Resources 6 (January): 287–99.

Teshome, Mindaye, Abeje Eshete, and Frans Bongers. 2017. “Uniquely Regenerating

Frankincense Tree Populations in Western Ethiopia.” Forest Ecology and Management

389 (April): 127–35. https://doi.org/10.1016/j.foreco.2016.12.033.

The IUCN Red List of Threatened Species, 2020. https://www.iucnredlist.org/.

Thulin, Mats, Anjanette Decarlo, and Stephen P. Johnson. 2019. “Boswellia Occulta

(Burseraceae), a New Species of Frankincense Tree from Somalia (Somaliland).”

Phytotaxa 394 (3): 219–224. https://doi.org/10.11646/phytotaxa.394.3.3.

Tilahun, Mesfin, Roland Olschewski, Christoph Kleinn, and Kindeya Gebrehiwot. 2007.

“Economic Analysis of Closing Degraded Boswellia Papyrifera Dry Forest from Human 41

Interventions — A Study from Tigray, Northern Ethiopia.” Forest Policy and Economics 9

(8): 996–1005. https://doi.org/10.1016/j.forpol.2006.09.004.

Tolera, Motuma, David Menger, Ute Sass-Klaassen, Frank J. Sterck, Paul Copini, and Frans

Bongers. 2013a. “Resin Secretory Structures of Boswellia Papyrifera and Implications for

Frankincense Yield.” Annals of 111 (1): 61–68.

https://doi.org/10.1093/aob/mcs236.

Tolera, Motuma, Ute Sass-Klaassen, Abeje Eshete, Frans Bongers, and Frank J. Sterck. 2013b.

“Frankincense Tree Recruitment Failed over the Past Half Century.” Forest Ecology and

Management 304 (September): 65–72. https://doi.org/10.1016/j.foreco.2013.04.036.

Ulbricht, Catherine, Ethan Basch, Heather Boon, Theresa Davies Heerema, Ivo Foppo, Sadaf

Hashmi, Jens Hasskarl, and David Sollars. 2004. “Boswellia: An Evidence-Based

Systematic Review by the Natural Standard Research Collaboration.” Journal of Herbal

Pharmacotherapy 4 (3): 63–83. https://doi.org/10.1080/J157v04n03_06.

Valerian G, Frankincense tree, above Rosh, Socotra, Yemen, 2015. Digital Image, Flickr,

https://www.flickr.com/photos/valerian1985/24265908553/in/photostream/

Worku M, Bantihun A. 2018. “Review the Significant of Non-Timber Forest Product and

Boswellia papyrifera Species in Ethiopia.” Journal of Ecosystem & Ecography 8: 248. doi:

10.4172/2157-7625.248