Growth and Coppicing Ability of the Critically Endangered Agarwood (Aquilaria Malaccensis Lam.) Tree in Monoculture and Polyculture in North East India

ABSTRACT Agarwood (Aquilaria malaccensis Lam.) (Thymelaeaceae) is valued in many cultures because of its distinctive fragrance and its use in incense, perfumery, and traditional medicine. Large-scale harvesting from natural populations caused rapid depletion of the species in the wild, and the species is now listed as “Critically Endangered” and almost extinct in the wild. The promotion of this species in agroforestry systems may pave the way for its conservation. The present study aimed to quantify the growth and coppicing ability of agarwood under monoculture and polyculture stands. Monoculture stands aged more than 20 years, and stem girth (1.37 m above ground) of 60–70 cm had the highest growth increment of 3.73 cm yr−1. Monoculture stands (>10 years old) also recorded higher number of coppicing stocks than polyculture stands. The highest coppice growth increment (4.07 cm yr−1) was recorded in the 70–80 cm stem girth in monoculture stands. Based on the results, we recommend the promotion of agarwood trees with good coppice management in forestry programs to conserve the species while also meeting the economic needs of rural communities.


Introduction
In the Indian context, all trees growing outside forest areas, irrespective of patch size' are referred to as Trees Outside Forest (TOF) (ISFR, 2019).TOF consists of trees planted in agroforestry systems, including homegardens, orchards, small woodlots, grazing lands, lands along roads and within cities, excluding all land uses that fall into the forest and other wooded lands (Das & Das, 2014;Regmi & Garforth, 2010;Singh & Chand, 2012).TOF are an integral part of Indian cultural philosophy in rural areas and have major contributions to the household economic needs, especially during periods of scarcity of resources (Nath et al., 2020;Pandey, 2008).Homegardens have been considered an important class of TOF in the rural parts of India because they supply several products and services such as food, fuel, fiber, fodder and medicines (Das & Das, 2014).In Assam, especially in the Barak valley, homegardens contain stands of agarwood (Aquilaria malaccensis), which is an economically valuable species that was found only in the wild until recently (Das & Das, 2005;Devi & Das, 2010;Nath et al., 2020).
Out of a total of 22 accepted species in the genus Aquilaria globally (The Plant List, 2013), three species (A. malaccensis, A. khasiana and A. macrophylla) are found in India.Aquilaria malaccensis produces a scented resinous wood in response to fungal infections associated with wounds made by insect borers (Lee & Mohammed, 2016;Mir et al., 2017;Nath et al., 2020;Saikia & Khan, 2013;Tabin & Shrivastava, 2014).Due to the high demand for its scented wood in Asian and European countries, prices range from US$ 100 kg −1 for low-quality to 100,000 kg −1 for high-quality resinous wood depending on the color from dark brown to blackish (Naef, 2011).Together with its perfumery value, it has also been used in traditional medicines for centuries (Mohammed et al., 2010).Due to the high demand, the species has faced overexploitation, and it is now on the brink of extinction in the wild (Ghosh, 2018).The species has been considered critically endangered in India (IUCN, 2009) and listed in Appendix II (potentially threatened species) of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES, 2010), also included in IUCN Red List in 2011.The literature suggests low natural regeneration and slow growth of agarwood trees in the wild (Paoli et al., 2001).
A. malaccensis plantations in the homegardens and community lands of Assam have been reported (Das & Das, 2005;Saikia & Khan, 2013).In the Barak valley, we could trace back the tree's introduction in homegardens to the mid 1980ʹs, nearly 30-35 years ago.It took nearly 10 years to proliferate in the study area.Agarwood trees either are found planted in monoculture stands in the extended part of the homegarden, or planted in a mixture with other tree species of economic and livelihood value (Nath et al., 2020).Cultivation of this species in homegardens has opened up a new avenue for its conservation (Das & Das, 2005;Rahman et al., 2015;Saikia & Khan, 2013).The tree also provided a new (and potentially important) source of income for local communities (Rahman et al., 2015).Cultivation ensures the survival of the species (Nath et al., 2020), directly through the expansion of the tree population and indirectly through the reduction of the extractive pressure on wild populations (Dorji et al., 2019;Hall et al., 2016).Although a few studies have been conducted on the agarwood tree population structure, its management and its socio-economic role, information on the growth ability of agarwood trees on coppicing under different stand management regimes is scanty.Studies on stand structure of agarwood can enhances our understanding of tree regeneration, recruitment and ecosystems health to inform appropriate management (Gebeyehu et al., 2019;Käber et al., 2021).Recent studies show that tree recruitment is determined by stand structure variables such as basal area, stem density, and shade casting ability rather than climate (Käber et al., 2021).Regeneration by coppicing is a key process for long-term forest dynamics, diversification of forest-based livelihoods and conservation (Matula et al., 2012;Syampungani et al., 2017).Therefore, information on the coppicing ability of trees have attracted the interest of researchers and managers aiming at developing adaptive management strategies (Syampungani et al., 2017).The present study was undertaken with the objective of quantifying the growth ability of agarwood trees after coppicing in different age groups and in different management systems.

The study area and management practices
The present study was conducted in Baghan Gaon Panchayat area of Barak Valley in Karimganj district of Assam, North East India.The study area is located between the foothills of the Himalaya and the Barak River basin (Figure 1).The district covered a total area of 1809 km 2 and bordered Cachar and Hailakandi districts in the Northeast, Mizoram, and Tripura state in the South and West.Karimganj district also shared an international trade boundary with Bangladesh in the Northwest.The annual average precipitation was 3300 mm during the study period (2016)(2017), most of which was received during the monsoon season, and the mean annual temperature was 25.8°C (NEDFCL (North Eastern Development Finance Corporation Ltd.), 2020; Table 1).Study area was dominated by sandy clay loam textured soil with pH of 4.61-5.02and SOC content of 12.7-13.6g kg −1 (Table 1).The study area was endowed with extensive agarwood tree plantations in the homegardens and their extended part. A. malaccensis now has a wide distribution in the homegardens of Barak valley.However, our study area was chosen for its particularly high concentration of agarwood trees (Nath et al., 2020).Farmers in the study area raise agarwood stands along with other economically important tree species like Areca catechu, Cocos nucifera, Artocrpus heterophyllus, Mangifera indica, etc.

Traditional management practices
Two major agarwood plantation management systems (monoculture stands and polyculture stands) were identified based on a pilot survey in the study area.Agarwood trees are managed in polyculture within the homegarden, but in monoculture in the extended part of homegarden (Nath et al., 2020).From the literature and our conversations with plantation owners, the monoculture stands and mixed stands coexist because the owners have different production objectives in each management system.Within the homegardens, the mixture of trees is based on the farmland owners' interest to derive multiple benefits from a diversity of species (Nath et al., 2020).In the monoculture stands, their objective is to maximize cash earnings from the agarwood trees (Nath et al., 2020).
Farmers raised the trees from wildings (i.e., seedlings collected from underneath mother trees) in nurseries to establish new plantations or replant in their old plantations.Loamy textured soil mixed with dry cow dung was used to prepare nursery beds.Farmers who did not develop their nursery bought seedlings from nursery owners at Rs. 5-10 per seedling (Rs. 1 = US $ 0.0134).After 6 months of seedling growth in the nurseries, they were transplanted to the field at the onset of the next monsoon season.Size of the planted field (homegarden and extended parts of it) ranged between 0.03 and 0.9 ha.During the first 2 years after planting, agarwood seedlings receive a biweekly watering in the dry periods (September-March).Application of cow dung and litters (generated within the fields) around the base of planted seedling is common management practice in the study area.Artificial injuries were mostly done around 8-12 years of the tree age when the diameter at breast height reached 8-10 cm.Iron nails were inserted across the bole's whole length to induce the production of scented resins.The traders and, in some instances, tree farmers mostly did this if natural injuries did not occur.Traders made injuries when the trees sold through an agreement between the farmer and the trader to keep it un-harvested for a minimum period of 2 years, and this was most common in the study area.The traders identified natural infested boles by checking the number of borer infestation and the depth of boring done by the insect.Infested plants (natural or artificial) were sold to the local traders who distilled and extracted the resinous oil.After felling followed sale of selected trees, farmers' practices, including management of coppice saplings from stocks, maintenance of naturally growing seedlings, and replantation, were often observed as a strategy to increase the agarwood tree density in their farms.

Selection of plot and vegetation sampling
We grouped farms into three according to the time of the introduction of agarwood tree cultivation: less than 10 years ago (<10), between 10 and 20 years (10-20), and more than 20 years ago (>20).In each age class of each plantation management, 10 random plots of 0.01 ha (10 m × 10 m) were laid (Brahma et al., 2016); a total of 60 random quadrats distributed across six selected age class (3-age class in monoculture and 3-age class in polyculture) of the study area.These 60 plots were used for assessing tree density, basal area, growth and coppicing status of the trees.All agarwood trees within the sample plots were marked with paint, counted and girth (the circumference at breast height, i.e., 1.37 m above ground) measured and each coppice stems were counted as a separate tree.The calculated tree density and basal area were extrapolated on to hectare basis (Brahma et al., 2018) by multiplying with 100 and tree density (ha −1 ) of each quadrat.Trees were identified as either intact trees or coppices by observing their location of emergence, either from the soil surface or from a stump, respectively.Initial laying of plots and vegetation sampling was conducted between November 2016 and January 2017.For estimation of the growth of trees under different management, the second measurement of vegetation was conducted between November 2017 and January 2018 in the plots established for sampling.

Statistical analysis
Data were processed in MS Excel 2007 and analyses were done with SPSS Statistics 21.All girths were converted to diameter (at 1.37 m above ground) (cm), second year girth diameter was subtracted from the previous year to assess the growth rate of the individual trees.Analysis of variance was implemented to determine the effect of management (polyculture vs monoculture) and age groups.Correlation analysis was implemented between tree size and annual diameter increment.Additionally, tree sizes were categorized into different size classes (10-20 to 70-80 cm) at 10 cm interval to evaluate size class and diameter increment relationship.Before formal analysis, normality and homogeneity of variances in the vegetation data were tested using Shapiro-Wilk and Levene's test, respectively.Statistical significance was set at 95% confidence interval.

Tree density and basal area
In the monoculture stands, the highest total tree density (4450 stems ha −1 ) was recorded in older stands (>20 years of age) and the lowest (933 stems ha −1 ) in young stands (<10 years of age).On the other hand, polyculture stands had the highest total tree density (3466 stems ha −1 ) in >20 years stands, while the lowest (2050 stems ha −1 ) was in <10 years of age (Table 2).In both monoculture and polyculture stands, total tree density and total basal area exhibited an increasing trend with the stand age.The highest basal area (48.02 m 2 ha −1 ) was recorded in stands aged >20 years in polyculture stands..

Tree growth
In the monoculture stand, diameter increment was strongly correlated (R 2 = 0.67) with DBH in the age group of >20 years (Figure 2c).In contrast, <10 years old polyculture stands exhibited a strong correlation (R 2 = 0.56) between diameter increment and DBH (Figure 2d).The annual diameter increment rate was not strongly correlated in polyculture stands of 10-20 and >20 years age (Figure 2e,f).The annual diameter increment was the highest (2.12 cm yr −1 ) in 20-30 cm size class in monoculture stands aged <10 years (Figure 3), but increment decreased with increase in tree size.Monoculture stands in the girth class of 60-70 cm at 10-20 years and >20 years age had the highest diameter increment of 3.73 cm yr −1 and 1.99 cm yr −1 , respectively.In polyculture stands aged <10 years, having the highest and the lowest diameter increment at 50-60 cm (3.18 cm yr −1 ) and 10-20 cm (0.94 cm yr −1 ) girth classes, respectively.In polyculture stands of >20 years age, the highest and the lowest increments recorded in 70-80 cm (2.93 cm yr −1 ) and 50-60 cm (1.19 cm yr −1 ) girth classes, respectively.

Coppicing ability
In monoculture and polyculture stands, coppicing was observed only in the stands of more than 10 years old.While there were no coppice trees at the age of 10-20 years in the polyculture stands, monoculture stands recorded on average two coppice stems per stock and a total of 11 coppicing trees in the plot (plot size = 100 m 2 ).Average total coppicing trees per plot were also higher in monoculture stands (33 stumps; 80% of the total stock) than polyculture stands (8 stumps; 46% of the total agarwood stumps) in the age category of >20 years.Coppicing stock per plot were more in >20 years old stands in both monoculture (15) and polyculture (5), whereas an average number of coppice saplings per plot was higher *Values are mean ± standard error.<10-≤10 years; 10-20-10-20 years; >20->20 years at 10-20 years age (Table 3).Coppice saplings, coppice trees per stock and total coppice trees per plot were more in the monoculture stands..

Discussion
Agarwood was extensively managed in the study area in monoculture stands and as polyculture in the homegardens.Cultivation of the tree was acting as a vital alternative source of livelihood to the local farmers.Initially, during the first cultivation of the tree in new farmland, the plantation was done in a scattered arrangement with space between any two trees being 1.5-2.5 m (Nath et al., 2020).As the tree matures, it becomes suitable for harvesting to extract oleoresin.Harvesting of the tree to extract agarwood and oleoresin starts around 8-10 years when the tree attains more than 8 cm diameter.In many instances, coppice shoots also grow from the stem retained after harvest.The retention of freely growing coppice shoots, natural growth of seedlings and replantation in the older stands apparently led to the increase in tree density in the >20 years old agarwood stands compared to <10 years and 10-20 years old stands.In the present study, tree density was greater than in other agroforestry systems managed in the homegarden in the region with Aquilaria trees (Das & Das, 2005;Saikia & Khan, 2013;Tangjang & Arunachalam, 2017) and without Aquilaria trees (Shimrah et al., 2018;Tynsong & Tiwari, 2017).Continuous replantation and coppice management are essential factors for higher tree density in the present study site.The reverse J-shaped distribution of size classes indicates the successful regeneration of the Aquilaria trees by managing naturally growing coppice saplings, seedlings, and replantation using nursery seedlings (Borogayary et al., 2018;Nath et al., 2020).Annual diameter increment in the monoculture stands (in ≤10 years stand age) showed an inverse J-shaped structure indicating a decreasing growth rate with the increase in size class.Comparatively, agarwood trees growing under polyculture stands showed 7% more growth increment than under monoculture stands.The diameter increment in ≤10 years of polyculture stands shows a more stable growth rate having a sigmoid-shaped increment rate with stem girth classes.The highest annual diameter increment is attributed to the presence of higher number of coppicing trees in monoculture than in the polyculture stands.Coppice shoots exhibits a faster growth rate owing to established root systems and stored reserves of nutrients (Koenig & Griffiths, 2012).The diameter increment of A. malaccensis trees in the present study was greater than other Aquilaria species planted elsewhere in the world (Hossen & Hossain, 2016;Saikia & Khan, 2013;Thapa et al., 2020) and other species managed in agroforestry systems (Das et al., 2020;Verinumbe, 2017).A. malaccensis is a fast-growing tree (Thapa et al., 2020) having the highest growth rate in the present study area.
Agarwood trees coppice readily and produce coppice shoots quickly (Ali & Kashem, 2019), which provides opportunities for increased production.In the present study, the trees produced coppice shoots within 6 months of harvest.In the monoculture stand, the coppicing stocks were more than those in the polyculture stands.This is probably because the monoculture stands experience less competition for resources necessary for producing coppice shoots than in polyculture stands (Christopher et al., 2014).An increase in coppice production with the increase in the stand age in both polyculture and monoculture stands in the present study is consistent with the earlier report by Joys et al. (2004) for different coppiced woods.The coppicing rate observed in the present study is comparatively more than reported in earlier studies (Girardclos et al., 2018;Gopikumar et al., 2002).Values are averages of all quadrats (10 m × 10 m) followed by figures within parentheses are standard errors of stands aged less than 10 years old (<10), between 10-20 years old (10-20) and more than 20 years old (>20).P values represent results of analysis of variance comparing age groups.
One of the limitations of this study is that tree growth was only calculated between two points in time 1 year apart.Having only a single year and a single interval from two data points is limited for measuring tree growth.Our results could have been more illuminating if we had a large longitudinal data.
The ability of the trees to coppice provides opportunities for increased production of agarwood and ex-situ conservation of the species on farmers' fields.Given the favorable policy environment, opportunities also exist to promote cultivation of this species.For example, the Assam Agarwood Promotion Policy of 2020 (Government of Assam Notification No. CI.127/2020/70) provides for (1) sustainable utilization of agarwood including cultivation, harvesting, processing, transit and trade, (2) encouragement of plantation of agarwood trees on farms/private lands, (3) promotion of agarwood-based industries by providing subsidies and proper market linkages, (4) support for research and development of artificial induction, sustainable harvesting and improvement in the quantity and quality of products, (5) training of local unemployed youth in plantation and nursery techniques and agarwood processing and marketing, (6) community participation in plantation of the tree processing and marketing, and (7) identification and conservation of wild agarwood population.Similarly, the Government of Tripura has also unveiled a similar policy in 2021.

Conclusions
Our findings provide evidence that Agarwood trees grown in polyculture stands have a higher annual growth rate than those in the monoculture stands.It is concluded that both monoculture and polyculture stands are successful in producing coppice stems.Therefore, the regeneration of agarwood trees by managing coppice saplings and seedlings and replantation is an essential factor for higher tree density in the study area.Our study also provides evidence for the importance of coppice management as strategy to sustaining agarwood-based livelihoods.When trees are harvested to extract agarwood and oleoresin, replanting is a common management practice in the gap created by harvesting.The ability of agarwood to coppice is advantageous because of the lower costs of reestablishment and increased tree productivity.This also provides opportunities for ex-situ conservation of the species on farmers' fields.Therefore, we recommend promotion of coppice management in agarwood plantation and social forestry programs for successful land management and conservation of this species.The challenges for extensive agarwood cultivation are the availability of the efficient induction techniques in the study area.In order to improve the induction efficiency, a farmer friendly induction technique could play a decisive role.We recommend collaboration between stakeholders (researchers, extension workers, buyers, NGOs, etc.) in knowledge sharing, farmer training, and exchange of planting materials among farmers to promote cultivation of agarwood.NGOs could play a significant role in farmer exchange and training.

Figure 1 .
Figure 1.(a) Map showing study area.(b) Photograph of different component of the study sites.amonoculture stands, b-polyculture stand, c-coppicing stock, d-first generation coppice trees, and esecond-generation coppice trees.

Table 1 .
Average annual meteorological and site data description of the study area.

Table 2 .
Total tree stand density and basal area of the differently managed Aquilaria stands.

Table 3 .
Coppicing status of Aquilaria trees in different management and age groups.