JOURNAL OF THE DRYLANDS 6(2): 489 - 498, 2016 DEGRADATION OF Boswellia papyrifera DOMINATED DRY LOW LAND DECIDUOUS FORESTS IN TIGRAY, NORTHERN ETHIOPIA Kindeya Gebrehiwot1, Aklilu Negussie2, Emiru Birhane1,* Mekonnen Yohannes3, Nigussie Hagazi2 and Sarah Teweldebirhan1 Kindeya Gebrehiwot, Aklilu Negussie, Emiru Birhane, Mekonnen Yohannes, Nigussie Hagazi and Sarah Teweldebirhan (2016): Degradation of Boswellia papyrifera Dominated Dry Low Land Deciduous Forests in Tigray- Northern Ethiopia. Journal of the Drylands, 6(2): 489 – 498 The frankincense tree, Boswellia papyrifera (Del.) Hochst is one of the tree species in the drylands of Ethiopia with significant economic and ecological importance. However, the species is under threat due to natural and human induced factors. It needs effective conservation strategies, yet, little is known about its ecology and management. The purpose of this systematic review paper is to look at the population structure and investigate the long horn beetle and parasitic plant infestation on B. papyrifera trees in two different land use management systems. Two management systems (open grazed and closed) were chosen in the natural habitat of B. papyrifera. Thirty two randomly selected plots measuring 20 m x 20 m for trees and shrubs and 5 m x 5 m for saplings were used to compare the population structure of the two land use systems. Beetle and parasitic plant infestation was investigated by selecting 40 trees from 3 diameter classes in the two land uses in both sites. The study showed that B. papyrifera dominated forests composed of very few young trees and very few saplings, indicating that the natural regeneration dynamics of the species have been disrupted. The nocturnal long horned beetles Idactus spinipennis Gahan, from the family Cerambycidae (sub family Lamiinae) infestation and the parasitic plants are serious problems causing degradation and death of B. papyrifera trees. The study revealed that, exclosures have a better vegetation density. The infestation rates were significantly different in the two sites and diameter classes rather than on the land use systems investigated. It should, however, be noted that the open grazing sites witnessed a lot of death of these trees, and these have not been accounted for in this study. Overall, urgent intervention is needed if the regeneration and future sustainability of B. papyrifera is to be ensured. Key words: B. papyrifera; horned beetle; parasitic plant; area enclosure; open grazed land 1 Land Resources Management and Environmental Protection Department, Collage of Dryland Agriculture and Natural Resources, Mekelle University, P.O. Box 231, Mekelle, Ethiopia 2 ICRAF, World Agroforestry Centre-Ethiopia, P.O. Box 5689, Addis Ababa, Ethiopia 3 Biomedical Institute, Collage of Health Sciences, P.O. Box 1871, Mekelle, Ethiopia * Corresponding author: email: [email protected] Received: January 19, 2016; Accepted: November 29, 2016 INTRODUCTION Vast areas of land, approximately 620,000 km2, in Ethiopia are arid to semi-arid with erratic rainfall characteristics (NCSS 1994, Lemenih et al 2003). Most parts of the northern Ethiopia are severely degraded and left barren as a result of years of deforestation and indiscriminate removal of vegetation cover. In Tigray, recurring droughts, war and frequent crop and fodder failures have made socio-economic development difficult. Therefore, the need for supplementary options that diversify the economy of the households are imperative (Lemenih et al 2003). In 1996 the forest cover was less than one percent of the land area of the Tigray region (TFAP 1996), while currently, there is a trend of increase which is especially significant for bush-lands (de Mûelenaere et al 2014). In this regard, B. papyrifera is one of the most promising tree species in the drylands of Ethiopia as an alternative income earning source for the livelihood of the people. Its product, frankincense - the white oleo-gum-resin exudate, has a long history in human civilization. The natural oil contents and pleasant smell of frankincense have made it desirable to burn as incense in temple rituals (Groom 1981, Gebrehiwot et al 2003). It is also a desired global ingredient in the fabrications of perfume, medicines and similar products (Lemenih et al 2003). Ecologically, it has a great contribution in the reduction of speedy runoff in the hilly areas where shallow and undeveloped soils dominated. B. papyrifera provides much of the plant cover and biomass in the marginal areas of the lowlands of Northern Ethiopia (Gebremedhin 1997). The species appears to be able to adapt to harsh growing conditions where other tree species often fail; in hilly areas with shallow soils of low fertility within an 489 Copyright © Journal of the Drylands 2016 ISSN 1817-3322 altitudinal range of 950 to 1800 m (Gebrehiwot et al 2003, Ogbazghi et al 2006a,b). The distribution of B. papyrifera in Tigray is categorized in two based on the extent of human interference: these are highly dense in the western zone of Tigray and highly disturbed and severely exploited for a long period of time in the central zone (TFAP 1996, Birhane et al 2010, Birhane et al 2011). Despite its ecological, economic, cultural and religious importance, the species is fast declining and threatened as a result of abiotic and biotic factors such as, improper incense production, over-tapping, moisture inconsistency, insecure land tenure systems, illegal cutting of trees, land clearing for farming practice and settlement, overgrazing, invasion of parasitic plants, wind and undetermined insects and fungi (Gebremedhin 1997, Gebrehiwot 2003, Rijkers et al 2006, Negussie 2008, Birhane et al 2010, Eshete et al 2012, Groenendijk et al 2012, Tolera et al 2013) MATERIALS AND METHODS Study area and data organization Tigray is located between 120 15’ to 140 50’ North and 36027’ to 39059’ East in the Northern most part of Ethiopia. This study was carried out in Tanqu Abergelle wereda, Central Tigray and Kafta-Humera, Western Tigray. The site characteristics as described by Birhane et al (2010) are presented in Table 1. Previous studies carried out by Negussie (2008), Hagazi (2008) and Birhane (2010) were used to support the paper. Table 1. Location, elevation, soil types and characteristics of the study sites (Birhane et al 2010) Locality Specific area Area of specific site (ha) Location Altitude (m) Geology Soil types Slope position Disturbance Erosion type Abergelle Jijike/Serabite and Siye 51 13°14’ to 13°42’N, 38°38’ to 39°02’E 1500 -1640 Limestone; mixture of schist & limestone with quartz Cambic Arenosols, Chromic Cambisols and Leptosols Middle High Sheet & rill Population structure survey The current population structure of B. papyrifera was surveyed in both sites (Abergelle and Humera). The survey was made on two land use systems: open grazed and exclosures. Tree diameter and total number of individuals per diameter class were collected in 20 m x 20 m square plots, while B. papyrifera sapplings were collected in 5 m x 5 m concentric square plots in 32 randomly selected locations, 16 in each site. Long horn beetle and higher parasitic plant prevalence The incidence of Idactus spinipennis and related beetles in family Cerambycidea and parasitic plants invasion and their damage was estimated on randomly selected trees within and near the plots, as some plots did not have the required number of trees in the given diameter class. Fourty trees were selected for each diameter class (<16 cm, 16 to 20 cm and > 20 cm) for each land use and at each site. Humera Tekeze/Adigoshu 295 13°42´ to 14°28´N, 36°20´ to 37°31´E 537-913 Metamorphic terrain, phyllite and quartzite Vertisols, Leptosols, Eutric cambisols, Vertic Luvisols Middle Medium Gully Totally, 480 tree were selected, 120 in each land use type in each site. Data analysis Data were analysed using excel and Minitab 16. To estimate population structure of B. papyrifera in each land use type, total number of stem for each diameter class was counted and calculated on hectare basis. Number of B. papyrifera trees infested with long horn beetle and higher parasitic plants and their intensity was expressed in percentage. Two-way Analysis of Variance and Analysis of Means (ANOVA and MONOVA) was used to see the interaction effects of land use, long horn beetle damage and parasitic plant infestation. RESULTS AND DISCUSSIONS Degradation of Boswellia dominated forest in Central Tigray and its implication The population structure of B. papyrifera shows that Boswellia is facing recruitment problems and is endangered (Figure 1). Due to this recruitment 490 Copyright © Journal of the Drylands 2016 ISSN 1817-3322 problem, the exploitation potential of this valuable forest is greatly reduced (Abreham et al 2004). Large amounts of seedlings regenerate in the rainy season, however, they disappeared and die in the dry season with very few re-emerging the next season (Negussie et al 2008). Normally, the shoots of this seedling will die back, however most are now not re-emerging. Saplings were totally absent in all plots laid to undertake this study. Trees in the diameter class ranges from 15 to 19 cm (diameter measured at breast height) are abundant. This implies that the succession of B. papyrifera is endangered (Figure 1). Similar patterns of recruitment problem and better populations in closed as opposed to open sites have been observed in other studies (Gebrehiwot et al 2003, Eshete et al 2005, Rijkers et al., 2006, Ogbazghi et al 2006b, Abiyu et al 2010, Eshete et al 2012, Groenendijk et al 2012, Tolera et al 2013). Degradation and over exploitation of natural resources are common in these forests, and the degradation of natural resources further limits local livelihood options (Tilahun et al 2007, Gebrehiwot 2003). Several studies undertaken on this valuable resource repeatedly point out that the rural poor benefit greatly from it. However, the population of this valuable tree is declining and needs immediate solutions (Gebremedhin 1997, Gebrehiwot 2003, Tilahun et al 2007, Tilahun et al 2011). Figure 1. Population structure and number of trees per diameter class of the different land uses combined for both sites (Abergelle and Tekeze). Long horned borer beetle attack B. papyrifera is also under threat as a result of infestation by Idactus spinipennis Gahan, 1890 from the family Cerambycidae, long horned borer beetles (Negussie 2008, Groenendijk et al 2012, Tolera et al 2013). The long horned beetles of the family Cerambycidea are a cosmopolitan family of beetles, typically characterized by their extremely long antennae, which are often as long as or longer than the beetle’s body (Encyclopaedia Britannica 2013). They undergo complete metamorphosis, meaning that the life stages consist of egg, larva, pupa and the winged adult. Mature larvae pupate near the surface of the wood; adults then find their way out and emerge to mate and repeat the life cycle. Many of the 30,000 species worldwide are quite large. The long white larvae bore into the stems of 491 Copyright © Journal of the Drylands 2016 ISSN 1817-3322 herbaceous plants and trees, and can be very destructive to trees. This insect is darker in colour and nocturnal. The colourful species are active during the day, while the dark ones are nocturnal (Milius 1999). The beetles attack the whole parts of the tree. In the beginning, the adult are attracted by food. Later, other relationships evolve so that the crevices and bark offer shelter and are attractive sites for laying eggs. Upon hatching, the tiny larvae bore into the wood and begin feeding, slowly carving tunnels as they bore ahead and packing frass behind them (Wang et al 1992). Their prevalence and damage caused by these beetles were documented in this study and are presented in Table 2. The use of these forests for extracting frankincense and grazing is good; however over tapping and overgrazing practices weaken these trees making them more susceptible to these attacks. Tappers collect frankincense from creating wounds; goats and cattle eat the bark during the dry season; cattle keepers defoliated its leaves for fodder when the rains start (Gebrehiwot et al 2003, Eshete et al 2005, Gebremedhin 1997). The debarked stems and damaged twigs serve as an entry point for the beetles to lay and hatch their eggs (Negussie 2008). In addition to Idactus spinipennis, termites are common and frequent problems in the area (Gebrehiwot et al 2003, Gebremedhin 1997, Eshete et al 2005). When the trees start to dry out, the combined effect of termites and beetles will hasten the end and fall of these trees. This overuse and damage is one explanation as to why the population of B. papyrifera is higher per hectare in the closed sites as compared to the open grazing areas (Figure 1). As can be seen from the study (Table 2), the less disturbed Tekeze site and lower DBH classes had significantly less infestation by the beetles. It should be noted that lower diameter classes will not be tapped, and as tapping creates entry points for the beetles, the infestation of larger diameter classes may be facilitated by tapping. This was clearly noticed in previous studies (Eshete et al 2005, Negussie 2008). Statistically, the effect of land use was not found to be significant. However, when one factors in the number of dead trees and smaller number of the trees per hectare for the open grazing sites, and the fact that other studies did find this significant (Gebrehiwot 2003, Ogbazghi et al 2006b, Abiyu et al 2010, Groenendijk et al 2012), it brings into question that site disturbance may also have an effect on the beetle infestation. Generally, this has implications for management, showing that over utilization of this valuable resource is leading to its decline and threatening its sustainability. Parasitic plants The green leaved and white pink flowered parasitic plant scientifically known as Tapinanthus globiferus subsp. bangwensis on B. papyrifera is very common in the area where this study was undertaken (Yirgu et al 2014). It has pear shaped pink or red fruits when ripe and green seeds inside with a sticky white pulp. The flower and fruit of this parasitic plant resembles with flowers and fruits of B. papyrifera. Tapinantus globiferus, and grows at the side of the branches and forms protoplasmic connections with B. papyrifera for food until it establishes well. After establishment, though, it produces chlorophyll and has the capability to photosynthesise its own food it remains dependent on the host for water and nutrients (Dörr 1987). In this study, it was observed that the infected area becomes swollen and sometimes black scares form which later harbour fungi and other insects (Negussie 2008). These parasitic plants can become numerous enough that they make up almost half of the green foliage of the tree branches, particularly on older Boswellia trees, where up to 30 individual Tapinantus globiferus plants per tree were observed. As can be seen in Table 3, the study showed that the number of parasitic plants present was significantly higher in the more disturbed Jijke site, and in the larger diameter sized trees. With these results again, the land use does not seem to have a significant effect. In the dry season, these parasitic plants remain green while the tree sheds its leaves to reduce moisture lost through transpiration. This phenomenon affects the health and physiology of the tree, and weakens the defence mechanism of the species to other insect and pest attacks (Dörr 1987). The infected branches of Boswellia often become deformed, and the flowering and fruiting delays as the parasite takes the energy and food needed to prepare flowers and fruits (Negussie 2008). 492 Copyright © Journal of the Drylands 2016 ISSN 1817-3322 Table 2. Long horn beetle damage quantification based on site, land use and tree size (DBH), ** significant at 1% using ANOVA. Sites Land Use Closed Protected Total B. papyrifera trees/Ha 513 Tekeze ** (A) Open Grazed Closed Protected 303 436 Diameter Classes Noninfested < 5% of the crown infested 5-15% of the crown infested 16- 25 % of the crown infested > 25 % of the No of crown infested infested and stem trees/ ha damaged DBH<16 ** (A) 101.25 111.91 0.00 0.00 0.00 111.91 213.16 16 >DBH< 23 ** (B) 64.52 170.11 0.00 0.00 0.00 170.11 234.63 DBH>23 ** (C) 48.31 330.32 4.14 4.14 0.00 0.00 1.38 1.38 53.83 55.21 Total 1.38 167.15 335.85 503.00 DBH<16 ** (A) 33.75 21.09 0.00 0.00 1.41 22.50 56.25 16 >DBH< 23 ** (B) 30.08 3.75 67.58 120.32 65.63 207.03 8.59 5.63 14.22 0.00 0.00 0.00 12.89 0.00 14.30 141.80 171.88 DBH>23 ** (C) Total 71.25 235.55 75.00 303.13 DBH<16 ** (A) 18.75 43.75 0.00 0.00 0.00 43.75 62.50 38.28 245.00 7.66 15.31 0.00 267.97 306.25 5.04 62.07 28.56 317.31 21.84 29.49 6.72 22.03 5.04 5.04 62.15 67.19 Total 373.87 435.94 DBH<16 ** (A) 25.11 50.23 0.00 0.00 1.93 52.16 77.27 16 >DBH< 23 ** (B) 22.87 171.49 5.72 5.72 22.87 205.79 228.65 DBH>23 ** (C) 1.58 49.55 36.27 257.98 17.35 23.06 7.89 13.60 0.00 24.80 61.50 63.08 319.45 369.00 16 >DBH< 23 ** (B) DBH>23 ** (C) Jijike** (B) Open Grazed Number of B. papyrifera trees infested with long horn beetle and intensity/ ha (based on Damaged twigs number per individual tree) 366 Total Tree per ha/ DBH class (Sources: Negussie 2008, modified) 493 Copyright © Journal of the Drylands 2016 ISSN 1817-3322 Table 3. Parasitic plants (PP) presence on B. papyrifera trees based on site, land use and tree size (DBH), ** significant at 1% using ANOVA, and Tukey’s grouping in brackets. (Sources: Negussie 2008, modified) Number of B. papyrifera trees infested with parasitic plants and intensity of infestation/ha Total B. Papyrifera Sites Land Use Diameter Classes Tree Hosts of PP Tree per ha/ each trees/Ha Non1-10 11-20 > 20 infested PP PP PP /Ha DBH class Closed Protected 503 Tekeze ** (A) Open Grazed Closed Protected 303 436 Jijike** (B) Open Grazed 366 DBH<16 (B) 213.16 0.00 0.00 0.00 0.00 213.16 16 >DBH< 23 (B) 234.63 0.00 0.00 0.00 0.00 234.63 DBH>23 ** (A) 55.21 0.00 0.00 0.00 0.00 55.21 Total 503.00 0.00 0.00 0.00 0.00 503.00 DBH<16 (B) 56.25 0.00 0.00 0.00 0.00 56.25 16 >DBH< 23 (B) 30.08 30.00 0.00 0.00 0.00 1.88 30.08 171.88 DBH>23 ** (A) 141.80 43.13 31.88 75.00 Total 241.18 60.08 0.00 1.88 61.95 303.13 DBH<16 (B) 45.31 15.63 1.56 0.00 17.19 62.50 16 >DBH< 23 (B) 99.53 199.06 7.66 0.00 206.72 306.25 DBH>23 ** (A) 8.40 48.71 6.72 3.36 58.79 67.19 Total 153.24 263.40 15.94 3.36 282.70 435.94 DBH<16 (B) 48.29 28.98 0.00 0.00 28.98 77.27 16 >DBH< 23 (B) 85.74 137.19 5.72 0.00 142.91 228.65 DBH>23 ** (A) 15.77 149.81 37.85 204.01 3.15 8.87 6.31 6.31 47.31 63.08 219.19 369.00 Total 494 Copyright © Journal of the Drylands 2016 ISSN 1817-3322 middle diameter class trees occurred in Tekeze and that of larger trees occurred in Jijike. Significantly lower mean value for infestation is observed in the middle diameter class trees in Jijike and larger diameter class trees in Tekeze. When we look at the main effect of site, we see that there is significantly higher infestation occurring in Jijike as compared to Tekeze. Looking at the main effect of diameter class, it is observed that the lower diameter class has significantly lower infestation, which agrees with previous studies (Yirgu et al. 2014) indicating that tapping aggravates the long horn beetle infestation. Interaction effects of land use, long horned beetle and parasitic plant infestation Land use did not show any significant effect on the presence of the long horn beetle and parasitic plant (Table 2 and 3). However, the study site and DBH class had an effect (Figure 2 and Figure 3). The mean infestation count for trees with DBH <16 cm was not significantly different from the overall mean (Figure 2). On the other hand, 16 ≥DBH ≤23 and DBH > 23 showed opposite situations for both sites, where significantly higher mean value for infestation of Alpha = 0,05 Interaction Effects 1 Effect 0,591 0 0 -0,591 -1 DBH_ Site 1 1 2 3 1 2 Main Effects for Site 3,326 2,983 2,641 2 Mean Mean 3 Main Effects for DBH_ 4 3 2 3,5 3,564 3,0 2,983 2,5 2,403 2,0 1 2 Site 1 2 DBH Class 3 Figure 2. Two-way Analysis of Variance (ANOVA) for beetled branches; where for site (1) is Tekeze and (2) is Jijke; and for DBH (1) < 16 cm; (2) 16 ≥DBH≤ 23; and (3) > 23 cm. In Figure 3, the interaction effect of site and DBH class for parasitic plan infestation showed that all the means are significantly different from the grand mean with trees in smaller and middle diameter classes in Tekeze. The upper diameter class in Jijke is significantly higher, while the remaining are significantly lower. This interaction analysis gives an opposite image of the main effect analysis. In the main effect analysis, for site, it shows Jijke and for the diameter class, it shows trees in the higher diameter class have significantly higher parasitic plants. What is clearly seen in this analysis and may not be clear in Table 3, is that the upper diameter class trees in both sites have significantly different number of infestation, with Tekeze being low and Jijke being high. The other two diameter classes also have significant differences with respect to the sites, and go in opposite directions. Overall, the higher diameter class in Jijike has significantly higher infestation with parasitic plans relative to the other diameter classes and the trees in Tekeze. 495 Copyright © Journal of the Drylands 2016 ISSN 1817-3322 Two-Way Analysis of Means for Parasitic Plants Alpha = 0,05 Interaction Effects Effect 2 0,501 0 -0,501 0 -2 DBH_ Site 1 1 2 3 1 2 2 Main Effects for Site Main Effects for DBH_ 4,5 2 1,890 1,6 1,310 1 0 Mean 3 Mean 3 3,0 2,092 1,6 1,108 1,5 0,0 1 2 Site 1 2 DBH_ 3 Figure 3. Two-way Analysis of Means for Parasitic Plants; where for site (1) is Tekeze; and (2) is Jijke; and for DBH (1) < 16 cm; (2) 16 ≥DBH≤ 23; and (3) > 23 cm Generally, looking at the results presented here, it is clear that B. papyrifera is facing recruitment problems and the future of the trees is under threat. The threats are multi-fold as several studies have indicated. The land use system clearly shows that there is accelerated degradation and death of the trees in the openly grazed sites. The more intensively used site of Jijike had more long horn beetle and parasitic plant infestation that again accelerate the vegetation decline. These have implications for management as they affect both production and future regeneration related issues, as the middle and upper diameter classes are the trees being tapped and are the trees producing seeds. When these diameter class trees get infested and die, both incense and seed production are in danger. Again, there is a need to stress that even if the land use did not show any significant effect, the total death and decline of trees in the openly grazed areas is a significant effect on its own. Further study is, therefore, needed to show how many trees are dying due to infestation by the long horn beetle and the parasitic plants. CONCLUSIONS Although dry land forests play an important role both in the economic and ecological wellbeing of the dryland ecosystem; their sustainability is under threat. B. papyrifera is one of the potential tree species for economic development and desertification control in arid and semi-arid areas of Ethiopia. Its distribution is restricted mainly to steep rocky lowlands where the development of the soil is young and within a limited range of rainfall. Human pressures from tapping, fire and livestock grazing on the remaining B. papyrifera dominated forest increase its habitat loss and fragility. This study revealed that there is a decline in the number of trees per hectare with a negative natural regeneration trend and a high long horn beetle and moderate parasitic plant infestation. The rapid expansion and high density of long horned beetle infestation in central Tigray where this study was undertaken is a serious problem for the future existence of B. papyrifera. This needs serious attention and further study on the control of this beetle infestatoin, in addition to improving the management and use of this valuable tree. ACKNOWLEDGMENTS Mekelle University and K.U. Leuven (Belgium) through the joint project of Forest rehabilitation through Natural Regeneration in Tigray, Northern Ethiopia provides logistic and material support during the field study and are highly acknowledged. The authors also want to acknowledge the People in Tanqua Abergelle district (Central Tigray) and KaftaHumera (Western Tigray) for their hospitality during our field stay. 496 Copyright © Journal of the Drylands 2016 ISSN 1817-3322 REFERENCES Arsema A (2008): Value Chain Analysis for Bamboo Originating from Shedem Kebele, Bale Zone. Abiyu A, Bongers F, Eshete A, Gebrehiwot K, Kindu M, Lemenih M, Moges Y, Ogbazghi W and Sterck FJ (2010): Incense Woodlands in Ethiopia and Eritrea: Regeneration Problems and Restoration Possibilities. In: Bongers F and Tennigkeit T (eds) Degraded Forests in Eastern Africa: management and resoration. London: The Earthscan Forest Library. 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