ISSN: 1412-033X E-ISSN: 2085-4722 Journal of Biological Diversity Volume 16 – Number 1 – April 2015
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Society for Indonesia Sebelas Maret University Biodiversity Surakarta BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 1-9 DOI: 10.13057/biodiv/d160101
Effects of timber harvest on structural diversity and species composition in hardwood forests
FARZAM TAVANKAR1,♥, AMIR ESLAM BONYAD2 1Department of Forestry, Khalkhal Branch, Islamic Azad University, Khalkhal, Iran. P.O. Box 56817-31367, Tel.: +98 4532451220-2, Fax: +98 42549050452, ♥email: [email protected] 2Department of Forestry, Faculty of Natural Resources, University of Guilan, Somehsara, Iran.
Manuscript received: 13 August 2014. Revision accepted: 10 September 2014.
Abstract. Tavankar F, Bonyad AE. 2015. Effects of timber harvest on structural diversity and species composition in hardwood forests. Biodiversitas 16: 1-9. Forest management leads to changes in structure and species composition of stands. In this research vertical and horizontal structure and species composition were compared in two harvested and protected stands in the Caspian forest of Iran. The results indicated the tree and seedling density, total basal area and stand volume was significantly (P < 0.01) higher in the protected stand. The Fagus orientalis L. had the most density and basal area in the both stands. Species importance value (SIV) of Fagus orientalis in the protected stand (92.5) was higher than in the harvested stand (88.5). While, the SIV of shade-intolerant tree species such as Acer insigne, Acer cappadocicum and Alnus subcordata was higher in the harvested stand. The density of trees and seedling of rare tree species, such as Ulmus glabra, Tilia begonifolia, Zelkova carpinifolia and Fraxinus coriarifolia, was also higher in the protected stand. The Shannon-Wiener diversity index in the protected stand (0.84) was significantly higher (P < 0.01) than in the harvested stand (0.72). The highest diversity value in the harvested stand was observed in DBH of 10-40 cm class, while DBH of 40-70 cm had the highest diversity value in the protected stand.
Key words: Beech stands, Shannon-Wiener index, stand structure, uneven aged management.
INTRODUCTION maintained by managing the structural diversity of stands is a common argument among researchers (Buongiorno et al. One main principle of biodiversity protection in multiple 1994; Lindenmayer and Franklin 1997; Sullivan et al. management of national forest is the protection of stands 2001; Franklin et al. 2002; Kant 2002; Varga et al. 2005). structure composition (Eyre et al. 2010; Sohrabi et al. Some silvicultural practices can enhance biological 2011). In forest science, stand structure refers to the within- diversity in managed forests, such as retaining old trees stand distribution of trees and other plants characteristics (Seymour and Hunter 1999), maintaining adequate levels such as size, age, vertical and horizontal arrangement, or of dead wood (Sturtevant 1997), establishing mixed stands species composition (Powelson and Martin 2001). (Palik and Engstrom 1999) or extending rotation lengths Structural diversity is a straightforward indicator of (Ferris et al. 2000). potential biodiversity in forest landscapes because a diverse The Caspian natural forests of Iran also called Hyrcanian stand structure provides better habitat for forest-dwelling forests, are located on the southern border of the Caspian organisms. Broadly accepted, a structurally diverse stand Sea and cover an area of 2 million hectares. The stands in provides living space for a number of organisms. this area are the most valuable and economical. The main Increasing and maintaining structural diversity in forest benefits of these forests are essentially two-fold: on the one stands, also has become an important forest management hand there is its wood production while on the other hand strategy for adapting climate change. Conservation of there are various physical and social effects frequently forests biodiversity is one of important objective in termed as forest influence. In many instances, the latter sustainable forest management (Burton et al. 1992; transcends is the significance of forests as producers of Brockerhoff et al. 2008). It is common opinion in forest wood (Bonyad et al. 2012). The current forest harvesting ecology that different management practices are a major method in these forests is mainly selective cutting. The determinant of forest diversity and that a more complex main goal of selection cutting management is uneven aged forest structure is linked to a high diversity of plant and and mixed stands that are close to nature. Selection cutting animal species (Pretzsch 1997; Boncina 2000; Shimatani is the silvicultural practice of harvesting a proportion of the 2001). Forest management leads to changes in horizontal trees in a stand (Pourmajidian and Rahmani 2009). In and vertical structure (Kuuluvainen et al. 1996; North et al. selective cutting, each tree must be individually assessed to 1999) and in the species composition (Nagaike Hayashi decide whether it should be cut or left. In reality, this 2004; Uuttera et al. 1997). The idea that biodiversity can be method is the practice of removing mature timber or 2 BIODIVERSITAS 16 (1): 1-9, April 2015 thinning to improve the timber stand. Selection cutting The physiographical characteristics of these compartments improves the health of the stand and releases space for are almost similar. The elevation of these compartments young trees to grow. In the selection system, regeneration, ranges from 850 m to 1,100 m asl. The climate is temperate tending, and harvesting all take place concurrently (Marvie on based Demarton climate classification, with a mean Mohadjer 2006). Selection cutting may include opening up annual temperature of 9.1°C and mean annual precipitation areas to allow tree species that require greater light of 950 mm for along with the 1990 to 2008 years. intensity to grow but that are not large enough to meet the Vegetation period maintains for 7 months in average. The legal definition of a clear cut (Nyland 1998; Anderson et al. original vegetation of this area is an uneven-aged mixed 2000; Webster and Lorimer 2002; Pourmajidian and forest dominated by Fagus orientalis and Carpinus betulus, Rahmani 2009). Selection cutting is appropriate for forests with the companion species Alnus subcordata, Acer composed of trees of different sizes and ages. Selection platanoides, Acer cappadocicum, Ulmus glabra and Tilia cutting does not have a visual impact on landscapes rubra. The soil type is forest brown soil and the soil texture because only some of trees are removed, a factor that is varies between sandy clay loam to clay loam. This study much appreciated by forest users. Uneven-aged was carried out in two areas, harvested and protected management is one alternative that could generate compartments in the Nav forest area of Iran (Nav Forest sustainable harvests while maintaining continuous forest Management Plan 1998). cover and protecting stands diversity (Guldin 1996). A planned program of silvicultural treatments ensures Data collection the conservation and maintenance of biological diversity Data were collected by circular sample plots with an and richness for sustainable forestry (Torras and Saura area of 0.1 hectare. The sample plots were located on the 2008; Schumann et al. 2003; Battles and Fahey 2000; study area through systematic grid (100 m × 100 m) with a Simila et al. 2006). The uneven-aged management can be random start point. Diameter at breast height (DBH) of all economically viable while preserving forest stand diversity trees (DBH ≥ 7.5 cm) was measured by diameter tape. (Buongiorno et al. 1994, Schulte and Buongiorno 1998, Individuals of trees with DBH < 7.5 cm were counted by Volin and Buongiorno 1996). species as seedling. Height was measured to the nearest m Beech (Fagus orientalis Lipsky) is the most industrial using Suunto clinometer. commercial tree species among more than 80 broad-leaved trees and shrubs. Many studies have been carried out on Data analysis plant biodiversity in Beech stands in Iran and around the Species importance value (SIV) for each specious was world (Sohrabi et al. 2011; Pourmajidian et al. 2009; calculated by (Ganesh et al. 1996; Krebs 1999; Pourbabaei Brunet et al. 2010; Sefidi et al. 2011; Pourbabaei et al. et al. 2013; Rezaei Taleshi 2014): SIV= Relative density 2013). The study of forest structure especially in virgin (RD) + relative frequency (RF) + relative dominance (RD). forests is very important and gives us comprehensive Basal area was considered for dominancy and relative information about the condition in forest for programming. dominance (RD) calculated by: RD = (basal area of a The selection cutting, such as other forestry practices, can species × 100) / total basal area of all species. The species leads to changes in stand structure and tree compositions. diversity index was computed using the Shannon-Wiener The stand structural diversity can be characterized information function (Krebs 1999; Sharma et al. 2009; horizontally, i.e. the spatial distribution of trees, and Abedi and Pourbabaei 2010; Pourbabaei et al. 2012) as: vertically in their height differentiation (Zenner and Hibbs H'=-Σni/n log2 ni/n, where: ni = denote to the SIV of a 2000). In this research, stand volume and structure, tree and species and n= denote to the sum of total SIV of all species. seedling density, and species composition were compared The species evenness index was computed using the in the harvested and protected Beech dominated stands. Pielou’s evenness index (J) as: J = H' / ln S, where ln is The objective of this study was effects of timber harvesting Natural logarithm, S is the total species number in each on structural diversity and species composition in oriental plot. Also species richness (S) was number of species per Beech stands in the Iranian Caspian forests. plot. After checking for normality (Kolmogorov-Smirnov test) and homogeneity of variance (Levene’s test), the means of stand characteristics (tree and seedling density, MATERIALS AND METHODS basal area, stand volume) in two compartments (harvested and protected) were compared using independent samples t Study area test. The means of biodiversity indices (diversity, evenness The study area is Iranian Caspian forests. These forests and richness) in two compartments were also compared are suitable habitats for a variety of hardwood species and using independent samples t test. The means of biodiversity include various forest types. Approximately 60% of these indices in DBH classes compared using a one-way forests are used for commercial purposes and the rest of ANOVA. Multiple comparisons were made by Tukey’s test them are more or less degraded (Marvie Mohadjer 2006). (significance at α < 0.05). Regression analysis was applied This study was conducted in Nav forests (latitude 37° 38' to test the relations between DBH and stand volume, tree 34" to 37° 42' 21" N, longitude 48° 48' 44" to 48° 52' 30" density and tree height. SPSS 19.0 software was used for E) in Guilan province, north of Iran. Two adjacent statistical analysis; also the results of the analysis were compartments of 123 (protected) and 112 (harvested) with presented using descriptive statistics. areas of 43 and 63 ha were selected for collection of data. TAVANKAR & BONYAD – Effects of timber harvest on hardwood forests 3
A
Harvested
Protected
B C
Figure 3. Study site map of Nav-forest, northern Iran. A. Guilan Province, Iran, B. Nav-forest within study site, near Nav ( ), Asalem, Talesh, Guilan, Iran, C. Detailed site of forest sampling.
RESULTS AND DISCUSSION stem.ha-1 or 29%. Also the basal area of Aceraceae species in the harvested stand was 4.8 m2.ha-1 or 27.6%, while in Results the protected stand was 6.3 m2.ha-1 or 25.3%. However, the The stand parameters in two studied compartments are family of Rosaceae had the most number of tree species, shown in table 1. The results indicated the tree and seedling but these trees had the minimum density and basal area in density in the protected stand was significantly higher (P < two stands. The Rosaceae species include Mespilus 0.01) than the harvested stand. The total basal area and germanica, Cerasus avium, Pyrus communis, Prunus stand volume in the protected stand was also significantly divaricata and Sorbus torminalis. higher (P < 0.01) than the harvested stand (Table 1). Species Importance Value (SIV) of different tree A total of 16 tree species from 8 families were observed species in the harvested and protected stands is shown in in the sample plots (Table 2). The Fagus orientalis had the Figure 1. The SIV of Fagus orientalis in the protected most density and basal area in the both stands. Density of stand (92.5) was higher than the harvested stand (88.5). Beech trees in the harvested stand was 66.8 stem.ha-1 While, the SIV of Carpinus betulus, Acer insigne, Acer (28.7%), while in the protected stand was 89.1 stem.ha-1 cappadocicum and Alnus subcordata in the harvested stand (25.9%). Basal area of Beech trees in the harvested stand was higher than in the protected stand. Also, the SIV of was 5.1 m2.ha-1 (29.3%), while in the protected stand was Acer platanoides, Quercus castaneifolia, Tilia begonifolia, 7.9 m2.ha-1 (31.7%). Indeed, the density percentage of Ulmus glabra and Zelkova carpinifolia in the protected Oriental Beech trees was higher in the harvested stand, stand was the higher than the harvested stand. The SIV of while the basal area percentage of Oriental Beech trees was other tree species (Fraxinus coriarifolia, Mespilus higher in the protected stand. After the Oriental Beech germanica, Cerasus avium, Pyrus communis, Prunus trees, Carpinus betulus had the most density in the divaricata and Sorbus torminalis was almost equal in the harvested (32.6 stem.ha-1 or 14%) and in the protected harvested and protected stands (Figure 1). Volume of (54.7 stem.ha-1 or 15.9%) stands. In addition, the density different tree species in the harvested and protected stands percentage of Carpinus betulus was higher in the protected is shown in Figure 2. The volume of all tree species in the stand, but the basal area percentage of Carpinus betulus protected stand was higher than in the harvested stand. The was higher in the harvested stand (16.1% vs. 13.6%). The volume of Fagus orientalis in harvested and protected family of Aceraceae had three species (A. insigne, A. stands was 51.5 and 74.5 m3.ha-1. Seedling of different tree cappadocicum and A. platanoides) in these stands. The species in harvested and protected stands are shown in density of Aceraceae species in harvested stand was 77.3 Figure 3. The seedling density of all tree species, except of stem.ha-1 or 33.2%, while in the protected stand was 99 Carpinus betulus, in the protected stand was higher than in 4 BIODIVERSITAS 16 (1): 1-9, April 2015 the harvested stand. The multiple regression analyses the harvested stand was observed in DBH of 10-40 cm applied to test the relations between DBH and tree height in class, while DBH of 40-70 cm had the highest diversity the harvested and protected stands that were statistically value in the protected stand. The highest evenness value in significant (P < 0.001) and the result are shown in Figure 4. the harvested stand was observed in DBH of 70-100 cm, The regression analysis between DBH and tree density in while DBH of > 100 cm had the highest evenness value in the harvested and protected stands was also statistically the protected stand. The highest richness value was significant (P < 0.001) and the results are shown in Figure observed in DBH of 10-40 cm in the both of harvested and 5. The regression analyses applied to test the relations protected stands. between DBH and stand volume in the harvested and The results of t test showed were not significant protected stands that were statistically significant (P < difference between the values of diversity index in two 0.001) and the result are shown in Figure 6. stands in the DBH class of 10-40 cm (Table 5). While, the Biodiversity indices in harvested and protected stands values of diversity index in the DBH classes of 40-70, 70- are shown in table 3. The value of diversity index in the 100 and > 100 cm in the protected stand were significantly protected stand (0.84) was significantly higher (P < 0.01) higher than harvested stand (Table 5). The value of than harvested stand (0.72). The value of evenness and evenness index was significantly higher in the protected richness indices in the protected stand were also higher (P stand than the harvested stand only in the DBH class of > < 0.01) than in the harvested stand. ANOVA tests showed 100 cm (Table 5). The values of richness index in the all of the DBH classes had significantly affect (P < 0.01) on the DBH classes in the protected stand were significantly means of biodiversity indices in the harvested and higher than the harvested stand (Table 5). protected stands (Table 4). The highest diversity value in
Table 1. Stand parameters (mean ± standard deviation) in the study sites.
Parameter Harvested Protected T-Value Tree density (stem.ha-1) 232.7 ± 57.7 344.1 ± 41.3 11.14** Basal area (m2.ha-1) 17.4 ± 2.3 24.9 ± 5.2 8.59** Volume (m3.ha-1) 154.3 ± 14.2 257.3 ± 17.3 31.05** Seedling density (stem.ha-1) 350.4 ± 18.1 486.8 ± 68.5 10.87** Note: **: P < 0.01.
Table 2. Frequency and basal area of tree species in the study sites.
Density (stem.ha-1) Basal area (m2.ha-1) Tree species Family Harvested Protected Harvested Protected Fagus orientalis Lipsky Fagaceae 66.8 89.1 5.1 7.9 Carpinus betulus L. Corylaceae 32.6 54.7 2.8 3.4 Acer insigne Boiss. Aceraceae 28.1 38.0 2.3 2.6 Acer cappadocicum Gled. Aceraceae 26.5 32.6 1.8 2.3 Alnus subcordata C.A.M. Betulaceae 25.0 30.1 1.1 1.7 Acer platanoides L. Aceraceae 23.3 28.4 0.7 1.4 Quercus castaneifolia Gled. Fagaceae 9.6 20.5 0.9 1.6 Tilia begonifolia Stev. Tiliaceae 5.2 20.3 0.7 1.8 Ulmus glabra Huds. Ulmaceae 3.3 10.8 0.6 1.4 Zelkova carpinifolia Diopp Ulmaceae 2.8 8.5 0.5 1.0 Fraxinus coriarifolia Scheel Oleaceae 2.2 4.1 0.3 0.6 Mespilus germanica L. Rosaceae 2.0 2.4 0.1 0.2 Cerasus avium L. Rosaceae 1.7 2.0 0.1 0.2 Pyrus communis L. Rosaceae 1.2 1.8 0.1 0.1 Prunus divaricata Ledeb. Rosaceae 1.0 1.5 0.1 0.1 Sorbus torminalis L. Rosaceae 0.5 0.8 0.1 0.1
Table 3. Biodiversity indices (mean ± standard deviation) in DBH classes.
Diversity* Evenness Richness DBH (cm) Harvested Protected Harvested Protected Harvested Protected 10-40 0.78 ± 0.18a 0.70 ± 0.13b 0.51 ± 0.14b 0.46 ± 0.18b 4.96 ± 1.50a 6.80 ± 1.54b 40-70 0.55 ± 0.16b 0.91 ± 0.19a 0.60 ± 0.17a 0.53 ± 0.12b 4.51 ± 1.45ab 6.21 ± 1.53ab 70-100 0.44 ± 0.15c 0.81 ± 0.20a 0.66 ± 0.15a 0.71 ± 0.16a 3.88 ± 1.38b 5.65 ± 1.58a > 100 0.40 ± 0.10c 0.55 ± 0.13c 0.53 ± 0.14b 0.76 ± 0.19a 3.20 ± 1.25c 4.31 ± 1.62a All trees 0.72 ± 0.15 0.84 ± 0.09 0.61 ± 0.08 0.70 ± 0.07 3.77 ± 1.09 4.79 ± 1.08 Note: *: Different letters in each column indicated significant difference at α = 0.05. TAVANKAR & BONYAD – Effects of timber harvest on hardwood forests 5
Table 4. ANOVA results for means of biodiversity indices in DBH class.
Indices Sites SS df MS F P-Value Diversity Harvested 3.307 3 1.102 182.05 0.000 Protected 3.839 3 1.279 201.38 0.000 Evenness Harvested 2.736 3 0.912 112.45 0.000 Protected 3.263 3 1.088 131.52 0.000 Richness Harvested 49.293 3 16.431 28.760 0.000 Protected 64.72 3 21.573 30.536 0.000
Table 5. Results of t test for comparing means of biodiversity indices in harvested and protected stands according DBH class.
DBH (cm) Diversity Evenness Richness 10-40 1.678N.S 1.982N.S 5.528** 40-70 2.543* 2.104N.S 3.371** 70-100 4.659** 2.001N.S 4.580** > 100 2.324* 3.064** 5.051** All trees 5.032** 6.058** 4.584** Note: N.S: Not significance, *: P < 0.05, **: P < 0.01
Figure 1. SIV of tree species in the harvested and protected stands.
Figure 2. Volume of tree species in the harvested and protected stands. 6 BIODIVERSITAS 16 (1): 1-9, April 2015
Figure 3. Seedling density of tree species in the harvested and protected stands.
Figure 4. Relation between DBH and tree height in the harvested and protected stands.
Figure 5. Relation between DBH and tree density in the harvested and protected stands. TAVANKAR & BONYAD – Effects of timber harvest on hardwood forests 7
Figure 6. Relation between DBH and stand volume in the harvested and protected stands.
Discussion Our results indicated the species importance value Understanding the effects of forest management (SIV) of shade-intolerant species such as Acer insigne, practices on plant species diversity is important for Acer cappadocicum and Alnus subcordata in the harvested achieving ecologically sustainable forest management stand were higher than protected stand. The diversity of a (Banda et al. 2006; Nagaike et al. 2006; Liang et al. 2007; forest stand may not be sufficiently described by tree Sefidi et al. 2011). The results of this study indicated the species diversity alone. Forest ecologically management tree and seedling density, total basal area and stand volume include forest ecosystem, wood production and non timber in the protected stand was higher than in the harvested values (Lindenmayer et al. 2000; Pourbabaei and stand. Managing the forest for periodic income from the Pourrahmati 2009). The forest biodiversity guidelines focus sale of trees as raw material for forest products depends on on how best to conserve and enhance biodiversity in being able to regenerate the forest successfully. Forests are forests, through appropriate planning, conservation and the most species rich of all terrestrial ecosystems and management. Tavankar et al. (2011) investigated effects of provide essential benefits to society. Forest management selection cutting on species diversity of trees and plan should describe both short and long term management regeneration at a 10 years period in the Caspian forests. goals and how to maintain forest productivity. Qiu et al. Their results indicated species diversity of tree and (2006) investigated effects of selection cutting on the forest regeneration were slightly increased after 10 years from structure and species diversity of evergreen broad-leaved cutting since. Also the researchers reported the species forest in northern Fujian, China. They reported selection importance value (SIV) of Beech and Hornbeam trees were cutting of low and medium intensities caused to little decreased, but SIV of Maple and Alder trees were variation in the stand structure, while high intensity of increased at the end of period. selection cutting caused to significantly changing in the The structural attributes of forest stands are increasingly stand structure. Sohrabi et al. (2011) studied structural recognized as being of theoretical and practical importance diversity of Beech stands in northern Iran and reported the in the understanding and management of forest ecosystems most diversity of trees is in low height and diameter classes. (Franklin et al. 2002). The structural diversity can be The results of this study indicated the density of trees characterized by diameter variation of trees in a forest and seedling of rare tree species, for example, Ulmus stand. The regression analysis of relation between DBH glabra, Tilia begonifolia, Zelkova carpinifolia and and tree height showed the height of trees with DBH of > Fraxinus coriarifolia, in the protected stand was higher 30 cm in protected stand were higher than in the harvested than in the harvested stand. It is widely demonstrated that stand. Pourmajidian and Rahmani (2009) compared stand more species contribute to greater ecosystem stability. structure after 12 years in a Beech stand. They reported the Nowadays, forest management practices increasingly stand volume was not significantly changed, but density promote conservation and enhancement of biodiversity. and basal area of trees significantly increased after 12 Forest management typically has a marked affect on plant years. Structural diversity is an important property of forest species diversity, which is an important ecological stands. Diameter diversity is the most straightforward way indicator (Lindenmayer et al. 2000). Poor forest for quantifying vertical structure (canopy layering) of a management practices contribute to decline or loss of forest stand because diameter is strongly associated with biodiversity. The conservation of biodiversity has become a tree height and crown width (Neumann and Starlinger major concern for resource managers and conservationists 2001). The regression analysis of relation between DBH worldwide and it is one of the foundation principles of and tree density showed the density of trees in the protected ecologically sustainable forestry (Carey and Curtis 1996; stand were higher than in the harvested stand in the all Hunter 1999). DBH classes. Villela et al. (2006) studied effect of 8 BIODIVERSITAS 16 (1): 1-9, April 2015 selective logging on stand structure in Brazil forests and species that are high density. Diversity of species is reported did not differ in stem density and total basal area correlated to the diversity of their habitats. Marking for in logged and unlogged stands, but unlogged stand had trees selection should not be only for harvesting of the more density of large diameter trees and greater mean of wood, but also it should consider the uneven aged canopy height. structure, keeping the seed trees and their regeneration and Forest managers have been seeking a feasible way to the diversity of wood species. The conservation of integrate biodiversity issues into management plans. To biological diversity is one of the goals of ecologically control forest stand structure may be the most practical way sustainable forestry (Lindenmayer et al. 2000). Fully to manage biodiversity in forest ecosystems. The regression protected areas are often assumed to be the best way to analysis of relation between DBH and stand volume conserve plant diversity and maintain intact forest showed the trees with DBH of almost 80 cm have the most composition and structure (Banda et al. 2006). Forest stand volume in the both harvested and protected stands. protection should aim at ensuring that forests continue to Kia-Daliri et al. (2011) investigated how to marking of perform all their productive, socio-economic and trees that will be harvested during selection cutting and its environmental functions in the future. Forest structure is impact on stand structure in a mixed Beech stand in the important feature in management of forest ecosystems Caspian forest. They reported the most marked and (Zenner and Hibbs 2000; Tavankar 2013). harvested trees were large diameter (DBH > 60 cm), high quality and Beech specimen. It is now widely accepted that forests should be REFERENCES managed in an ecologically sustainable fashion (Kohm and Franklin 1997; Lindenmayer et al. 2000). Biodiversity is an Abedi R, Pourbabaei H. 2010. Plant diversity in natural forest of Guilan essential case for life continuance, economical affairs and Rural Heritage Museum in Iran. 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Effect of Alnus subcordata, Acer insigne and Sequoia sempervirens plantations on plant diversity in Hyrcanian forest of Iran
FATEMEH GHEIBI, MOSLEM AKBARINIA♥, YAHYA KOOCH Faculty of Natural Resources and Marine Sciences, Tarbiat Modares University, 46417-76489, Noor, Mazandaran, Iran. Tel: + 98-122-6253101 (-3), Fax: + 98-122-6253499, ♥email: [email protected].
Manuscript received: 19 June 2014. Revision accepted: 27 September 2014.
Abstract. Gheibi F, Akbarinia M, Kooch Y. 2015. Effect of Alnus subcordata, Acer insigne and Sequoia sempervirens plantations on plant diversity in Hyrcanian forest of Iran. Biodiversitas 16: 10-15. Forest plantation is a common action in order to restore the degraded forests in Hyrcanian forests of Iran. This study compares the plant biodiversity in four 25-year-old stands of plantation, adjacent understorey of alder (Alnus subcordata C. A. Mey.), maple (Acer insigne Boiss.), sequoia or red wood (Sequoia sempervirens (D. Don) Endl.) and mixed stand (maple and sequoia), located in Salmanshahr of Mazandaran Province, northern Iran. Research carried out in, 10 sample plots with 20m × 20m area which taken by systematic-random in each plantation. All understorey species were identified, recorded and then the biodiversity indices (diversity, richness and evenness) were calculated. Our findings show that the planted species had significant effects on understorey diversity. Statistical comparisons revealed that the highest and lowest diversity (Simpson and Shanon-Winer) and richness (Margalef and Menhinic) indices occurred in sequoia and alder stands, respectively. The evenness indices (Camargo and Smith-Wilson) were significantly greater in maple, sequoia and mixed stands compared with the alder type. As a conclusion, floristic change trends were different according to the planted tree species. A good understanding of the complexity of vegetation processes requires long-term monitoring of vegetation change.
Key words: diversity, evenness, richness, sequoia, understorey.
INTRODUCTION Hyrcanian forests (Takhtajan 1974; Kooch et al. 2014a,b). These forests cover 1.8 million hectares of land area. Biodiversity is necessary for mankind life duration, Approximately 60 percent of these forests are used for economical issues and for ecosystem stability and function commercial purposes and the rest of them are degraded. (Singh 2002). Biodiversity is declining at an unprecedented They are suitable habitats for a variety of hardwood species rate and on a global scale. Indeed, loss of ecosystem such as beech, hornbeam, oak, maple, alder, and functions and services associated with such declines has encompass various forest types including 80woody species generated international debate (Zhou et al. 2006). Several (Marvie Mohadjer 2005). Today, the Caspian forests of causes have been identified to explain such loss, including Iran are depleting rapidly due to population growth, and increased land use by an expanding human population associated socio-economic problems, industrial (Lambin and Geist 2006) and global climate change development and urbanism (Poorzady and Bakhtiari 2009). (Thuiller 2007). Biodiversity is often used to compare the Forest plantation is a common action in order to restore the forest ecosystems the ecological status of forest ecosystems degraded forests in the Caspian region (Kooch et al. 2012; and evaluate the forest communities and ecosystems Mohammadnezhad Kiasari et al. 2013). (Esmailzadeh and Hosseini 2008). Forests support about Forest plantations are being established at an increasing 65% of the world’s terrestrial taxa (Lindenmayer et al. rate throughout much of the world, and now account for 2006) and have the highest species diversity for many 5% of global forest cover (FAO 2001). Plantations can taxonomic groups including birds, invertebrates and buffer edges between natural forests and non-forest lands, microbes (Lindenmayer et al. 2006). High species diversity and improve connectivity among forest patches, which in ecosystems led to high food chain and more complex might be important for some populations (Cullen et al. network environment (Lindenmayer et al. 2003). The 2004). The primary aim of almost all plantations is the layers of vegetation in a forest ecosystem support desirable production of large quantities of woodland fiber (e.g. for habitats for these taxonomic groups. So forests in the world timber and pulp production). However, there are often have the most contribution to biodiversity in terrestrial important opportunities for biodiversity conservation ecosystems. Loss of native species or alteration and within plantations (Hartley 2002). Various studies have introduction of invasive species through habitat destruction found that plantations of native or exotic timber species can is considerable because of vicinity of forest ecosystems to increase biodiversity by promoting woody understorey human population centers (Pilehvar et al. 2010). regeneration (Carnevale and Montagnini 2002). Plantations Caspian forests of Iran are located in the north of Iran promote understorey regeneration by shading out grasses, and south coast of Caspian Sea, also known as the increasing nutrient status of topsoil (through litter fall), and GHEIBI et al. – Effect of commercial trees plantations on plant diversity 11 facilitating the influx of site-sensitive tree species (Cusack stands were located at an altitude of 250 m above sea level and Montagnini 2006). and with gentle slope (0-5%). Annual rainfall averages Numerous studies have shown that the establishment of 1300 mm, with wetter months occurring between plantations or restoration plantings on degraded lands can September and February. In the dry season from April to ameliorate unfavorable microclimatic and soil conditions, August, monthly rainfall usually averages less than 40 mm and provide habitat for seed-dispersing wildlife, there by for four months. The soils have textures of loam and clay greatly accelerating natural forest regeneration (Carnus et loam with an acidic pH in the top layers; in the deep layers, al. 2006). Previous studies investigated the effect of soil textures were clay and silty clay and soil pH was less different land use and also cover on plant biodiversity with acidic. Previously this area was dominated by degraded different condition (Nagaike 2002; Esmailzadeh and natural forests containing native tree species such as Hosseini 2008; Pilehvar et al. 2010, Taleshi and Akbarinia Quercus castaneifolia, Zelkova carpinifolia, Parrotia 2011; Mohammadnejad Kiasari et al. 2013). Here we persica, Carpinus betulus, Diospyros lotus and Buxus designed to investigate and compare the plant diversity in hyrcana. While 25 years ago after clear cutting (in small the stands of 25-year-old plantation (sequoia, maple, alder areas in degraded natural forests), reforestations have been and sequoia-maple mixed). The results of this study can be established (within 3×3 m spaces) in this area with some useful for forest plantation and conservation of biodiversity native species including alder (Alnus subcordata C. A. in degraded lands located in northern forests of Iran and Mey.), maple (Acer insigne Boiss.), as well as exotic same situation. This information also can be used as the species of sequoia or red wood (Sequoia sempervirens (D. database for further research. Don) Endl.) and mixed stand (maple and sequoia).
Data collection and diversity measures MATERIALS AND METHODS Research done in, 10 sample plots with 400 m2 (20m×20m) areas taken by systematic-random in each Site characteristics plantation. The entire understorey species were identified, The study area is located at the Tilekenar district of recorded and then the values of diversity (Simpson and Salmanshahr in Mazandaran Province, in the north of Iran, Shanon-Wiener indices), richness (Margalef and Menhinic between 36°39'36″N-36°40'01″N and 51°09'55″ E- indices) and evenness indices (Camargo and Smith-Wilson 51°10'18″ E at the coast of Caspian sea (Figure 1). Study indices) were calculated by using PAST and Ecological Methodology software's as follow (Mesdaghi 2001, 2005):
50o 0’0”
Sequoia sempervirens Mixed stand Caspian Sea Alnus subcordata Acer insigne
Figure 1. Site locations of study area in Mazandaran Province, north of Iran. 12 BIODIVERSITAS 16 (1): 10-15, April 2015
RESULTS AND DISCUSSION
...... (1) A total number of 47 plant species were identified in the studied stands (Table 1).Our findings show that the Where, S is Simpson index; s is the number of species; planted species had significant effects on understorey ni is the number of ith species in sample; N is the number diversity (Table 2). Statistical comparisons revealed that of all species. the highest and lowest diversity (Simpson and Shanon- Winer) and richness (Margalef and Menhinic) indices occurred in sequoia and alder stands, respectively (Figure ...... (2) 2a, b , c, d). The evenness indices (Camargo and Smith- Wilson) were significantly greater in pure maple and Where, H is Shannon-Wiener index; s is the number of sequoia as well as mixed stands compared with the alder species; PI is the proportion of individuals found in the ith type (Figure 2 e,f). species. In the early stages after clear cutting due to high intensity light herbaceous plant diversity rapidly increased and sometimes invasive species are dominant (Humphery ...... (3) et al. 2003). Diversity index is the combination of species richness and evenness that have both the species richness Where, R is Margalef index; s is the number of species; and evenness in a quantity collects (Brockway et al. 1998). N is the number of all species. Biodiversity in a plantation area increase when trees are cut down to grow seedlings during planting seedlings in a change of fluctuate...... (4) In the present study, the most dominant species in all stands belongs to those after the destruction of the natural area expand sand shows the breakdown of natural Where, R is Menhinic index; s is the number of species; ecosystem of the destroyed area (Marvie Mohadjer 2005). N is the number of all species. Initially, study area was in the natural forest and slowly become dilapidated due to human influences, and to preventing the process of destruction and human poaching into forest plantation of exotic and native species has been ...... (5) suggested. The destruction of the ecosystem stops and with time recover and return to the natural ecosystem would be Where, E is Camargo species evenness indexes; Pi is require a lot of time finally what is visible the plantation the ratio of ith species to all species; Pj is the ratio of jth was able to stop the destruction. Various species richness species to all species; S is the number of species. shows that the numbers of plant species in an area are achieved. So far, a large number of species richness, which was invented by the index counts the total number of species (Maguran 1988), as is most celebrated for species richness (Kent and Coker 1992). Our findings showed that the number of species in the stands of sequoia and mixed ..(6) are more than others, as shown in Figure 3, by the Margalef index. The simple stand most common criterion for assessing species richness of habitats and plant Where, Evar is Smith and Wilson index; ni is the number of ith species in sample; nj is the number of jth species in communities is the number of species (Humphrey et al. sample; S is the number of all species. 1996). The broken branches in sequoias stand were more detected than other stands that cause more light to penetrate into the stand and may cause a higher diversity in sequoia Statistical analysis stand. Dense canopy of alder and maple perhaps is one The normality of the variables was checked by the reason for the low number of species on the forest cover Kolmogorov-Smirnov test, while Levene’s test was used to plantation compared to sequoia stand. The result of examine the equality of the variances. Differences in Fallahchai and Hashemi (2012) research showed that biodiversity indices (diversity, richness and evenness) Shanon-Winer diversity index had greater amounts in the among afforested stands were tested with ANOVA One- Pinus taeda stand than to the other broad-leaved stands. As way analysis. Duncan’s test was used to separate the shown indifferent researches that planting of tree species in averages of the dependent variables which were a plantation canopy over time, that larger trees are also significantly affected by treatment. Significant differences wider and it would reduce the variation in stand plantation. among treatment averages for different parameters were Plant diversity will be reduced with closing of canopy tested at P ≤ 0.05. cover gradually (Kuksina and Ulanova 2000).Since the sequoia stand that is a species of conifers, its soils are more GHEIBI et al. – Effect of commercial trees plantations on plant diversity 13 acidic than other sand presence of higher percentage of stand can also reduce biodiversity. The numerical value of ferns can be a reason for the higher diversity and richness the indices was not too different, because after 25 years of the stand. since plantation the plantation covers of different stands Barbier et al. (2008) in their review study on the effect become similar to each other. of tree on herbaceous species diversity and the mechanisms affecting boreal forests also concluded that presence of Table 2. ANOVA for biodiversity indices in the studied stands acidic friendly (Acidophilus) under a canopy of conifers species diversity in these populations will increase. Also, Biodiversity indices F-value Sig. the effect of these have on the soil and encourage more Diversity Simpson 7.161 .000** Shannon-Wiener 5.426 .001** herbaceous plants that are more oriented toward acidic soils Richness Margalef 3.374 .019** to increase some parameters in this stand (Humphery et al. Menhinic 9.812 .000** 2002). As alder species belong to those that leaves earlier Evenness Camargo 11.011 .000** and shed it after other therefore over the years a massive Smith and Wilson 9.331 .000** canopy will be emerge which with the high humidity of the Note: **Different is significant at the 0.01 level.
Table 1. Average percentage of floor coverings in the studied stands.
Scientific name Sequoia Maple Alder Mixed Brachypodium pinnatum (L.) P.Beauv. 0.1 0.14 0 0.06 Carex sylvatica L. 1.53 1.76 2.57 1.34 Conyza bonariensis (L.) Cronq. 0 0.18 0 0 Oxalis corniculata L. 0 0.08 0 0 Oplismenus undulatifolius (Ard.) P. Beauv. 14.94 15.68 51.7 20.64 Calystegia sepium (L.) R.Br. 0 0.2 0.64 0.23 Cyclamen coum Miller. 0 0.1 0 0 Primula heterochroma Stapf. 0 0.12 0.24 0 Parietaria officinalis L. 0 0.54 0 0 Pteris cretica L. 5.26 0.44 0.82 11.54 Urtica dioica L. 0 0.06 0 0.04 Scutellaria tournefortii Benth. 0 0.04 0.12 0 Viola alba L. 1.78 1.26 1.06 1.31 Fragaria vesca L. 0.12 0.04 0 0.04 Geum urbanum L. 0 0 0.42 0 Prunella vulgaris L. 0 0 0.88 0 Hypericum androsaemum L. 0.02 0 0.04 0 Polystichum aculeatum (L.) Roth 1.9 0 0.56 1.7 Clinopodium vulgare L. 0 0 0.38 0 Solanum nigrum L. 0 0 0.1 0 Stellaria media (L.) Cyr. 0 0 0.1 0 Cardamine impatiens L. 0 0 0.06 0 Phytolacca aquatica L. 0 0 0.13 0 Plantago major L. 0.02 0 0 0 Hedera pastuchovii Woron. 0.14 0 0 0.08 Danae racemosa (L.) Moench 0 0 0 0.06 Phyllitis scolopendrium (L.) Newm. 0.04 0.04 0 0.44 Lamium album L. 0 0 0.26 0 Sanicula europaea L. 0.38 0 0 0.04 Smilax excelsa L. 0.38 0.24 0.36 0.36 Pteris dentate Forssk 0.1 0 0 0 Mentha aquatica L. 0.2 0 0 0 Microstegium vimineum (Trin.) A. Camus. 0.62 0.39 0.51 2.08 Carpesium cernuum L. 0.24 0 0 0.2 Pimpinella affinis Ledeb 0.22 0 0 0 Ajuga reptans L. 0.26 0 0 0.3 Potentilla reptans L. 0.16 0 0 0.12 Tamus communis L. 0.04 0 0 0.09 Athyrium filix-femina (L.) Roth 3.66 0 0.2 1.6 Setaria viridis (L.) P. Beauv. 0.1 0 0 0 Mercurialis perennis L. 0.06 0 0 0.44 Ruscus hyrcanus Woron. 0.76 0.78 1.26 0.7 Sambucus nigra L. 0.06 0 0.58 1.5 Rubus persicus Bioss. 0.08 0.04 0.06 0.4 Melissa officinalis L. 0 0 0 0.04 Ilex spinigera (Loes) Loes 0 0 0 0.6 Unknown 0 0 0 0.4 14 BIODIVERSITAS 16 (1): 10-15, April 2015
A B
C D
E F
Figure 2. Average values of Simpson (A) and Shanon-Wiener (B) Margalef (C) and Menhinic (D) Camargo (E) and Smith-Wilson (F) indices for understorey.
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Plant species diversity among ecological species groups in the Caspian Sea coastal sand dune; Case study: Guilan Province, North of Iran
MOKARRAM RAVANBAKHSH1,♥, TAYYEBEH AMINI2, SAYED MOHSEN NASSAJ HOSSEINI1 1Environmental Research Institute, Academic Center for Education, Cultural Research (ACECR), Rasht, Iran, Tel. 0098-131-3232413, Fax. 0098-131-3242006, ♥email: [email protected] 2Agricultural and Natural Resources Research Center of Mazandaran (RCANRM), Noshahr, Iran
Manuscript received: 3 August 2014. Revision accepted: 30 September 2014.
Abstract. Ravanbakhsh M, Amini T, Hosseini SMN. 2015. Plant species diversity among ecological species groups in the Caspian Sea coastal sand dune; Case study: Guilan Province, North of Iran. Biodiversitas 16: 16-21. Biodiversity is often discussed in terms of species diversity is concentrated. Species diversity is one of the important characteristics of biological communities and its as a function of the number and size represent populations of species in a special geographic region.The aim of this study was to identification of ecological species groups and investigates the diversity among ecological species groups. The research area comprises a coastal dune system in northern of Guilan Province, Iran. Vegetation sampling was carried out along 22 shore perpendicular transects, approximately 500-m long. A total of 62 plot of 25 square meters were taken in transects. In each sampled plot, the cover percentage value of each species was estimated using Bran-Blanquet scales. Vegetation classified using Two-Way Indicator Species Analysis (TWINSPAN). The comparison of diversity indices among groups were performed with ANOVA test. The results revealed that there were 232 plant taxa and 8 ecological species group in the region. Results of analysis of variance in species diversity indices showed significant differences among the groups in terms of biodiversity indices. The survey of variation in the groups showed that groups 5 and 6 had the highest and groups 1, 2, 3, and 7 had the lowest indices. Checking of the group's position with high diversity in comparison with other groups in this coastal area indicates that the group settled on the coastal land with stabilized soil and proper distance from the sea had higher diversity indices.
Key words: Coastal sand dune, ecological species groups, plant species diversity, Guilan, Iran.
INTRODUCTION individual indicator species, in that once vegetation- environment relationships are established the abundance of Iran is one of the centers of plant diversity is considered multiple species of a group may strongly indicate old world so that nearly 22 percent of the 8000 plant environmental site conditions than the abundance of species of flora are the endemic (Ghahreman 1975). individual species (Bergeron and Bouchard 1984; Spies Despite to endangered state of coastal vegetation in Iran, and Barnes 1985). some fragmented sandy areas are still natural. Some of This study was carried out to evaluate the significance these separated sandy patches often constitute parts of of coastal dune habitats for biodiversity conservation. In Caspian coastal ecosystems designed in Ramsar checklist order to achieve this gold, the vegetation of the nearly of International Wetlands (Alagol, Ulmagol and Ajigol unaltered coastal sand dune between Roodsar and Astara, Lakes, Amirkelayeh Lake, Anzali Mordab (Talab) complex on the southern Caspian Sea, was described by means of MR., Bujagh National Park, Gomishan Lagoon, Miankaleh ecological species groups and quantitative analysis of the Peninsula, Gorgan Bay and Lapoo-Zaghmarz Ab-bandan) vegetation by diversity indices. and others are considered as part of protected areas, no hunting areas, wildlife refuges, biosphere reserves (Naqinezhad 2012b; Ramsar 2014). MATERIALS AND METHODS During the last decades, a few studies were conducted on the Flora, identification of vegetation groups and Study area ecological characters in these ecosystems. Most of these The research area comprises a coastal dune system in studies concentrated in the wetlands on the southern beach northern Guilan Province, Iran, between 48° 52´ 44´´ - 50° of the Caspian Sea (Riazi 1996; Asri and Eftekhari 2002; 35´ 59´´ E and 36° 56´ 4´´-38° 26´ 55´´ N. The study area Ejtehadi et al. 2003; Asri and Moradi 2004, 2006; Shokri et was delimited using a Landsat 7ETM satellite image (Path al. 2004; Asri et al. 2007; Sharifnia et al. 2007; Khodadadi 166/ Row 34) (Figure 1).The Caspian Sea constitutes the et al. 2009). Rarely floristic and vegetation grouping southern limit of the study area. The climate is humid and studies were carried out on the southern coastal area of the very humid with cool winter according to Eumberger Caspian Sea (Frey 1974; Amini 2001; Akhani 2003; climate classification (Abedi and Pourbabaei 2010). Guilan Ghahreman et al. 2004; Sobh Zahedi et al. 2005, 2007; has a humid subtropical climate with by a large margin the Naqinezhad 2012b). Ecological species groups differ from heaviest rainfall in Iran reaching as high as 1,900 mm in RAVANBAKHSH et al. – Plant diversity in the Caspian Sea coastal sand dune 17 the southwestern coast and generally around1, 400 mm. determined using nested plot sampling and species/area Rainfall is heaviest between September and December curve (Muller-Dombois and Ellenberg 1974). A total of 62 because the onshore winds from the Siberian High are sampling areas were selected in stands of vegetation that strongest, but it occurs throughout the year though least were homogeneous to the eye in floristic composition and abundantly from April to July. Humidity is very high structure (Monserrat et al. 2012). In each sampled plot, the because of the marshy character of the coastal plains and cover percentage value of each species was estimated using can reach 90 percent in summer for wet bulb temperatures Braun-Blanquet scale (Braun-Blaunquet 1964, Muller- of over 26°C (Zarekar et al. 2012). Mean annual Dombois and Ellenberg 1974). temperature is 15.8˚C and precipitation is 1506 mm. Maximum and minimum temperature is 27.8°C in August Data analysis and 4.1°C in February, respectively. The Alborz range Vegetation analysis method provides further diversity to the land in addition to the The floristic data matrix consists of 62 plots and 116 Caspian coasts ( Zarekar et al. 2012). species. To classify vegetation types present in the study area, the vegetation data were analyzed using two-way Sampling methods indicator species analysis (TWINSPAN) using PC-ORD Data collection was performed from May 2011 to May version 4.14 (Mc Cune and Mefford 1999).This analysis 2012. Voucher specimens were submitted in Guilan was used to produce a divisive classification of the stations University Herbarium (GUH). Prior to the commencement and plant species matrix (Murphy et al., 2003). This of fieldwork a short reconnaissance survey was undertaken method is a commonly employed program in ecological to get an overview of the area (Mashwani et al. 2011). A studies for the classification of vegetation types according total of 22 site were selected and one transect was to their floristic similarity (Kent and Coker, established in each site. For detailed data collection line 1992).Classification was stopped at the fifth level, so that transect survey was selected which is a very popular the result in groups would contain sufficient number of vegetation survey technique (Kent and Coker ,1992). samples to characterize each vegetation groups Vegetation sampling was carried out along 22 shore (Vogiatzakis et al. 2003; Khaznadar et al. 2009). The perpendicular transects between 100-500-m long (Figure names of identified vegetation types were derived from the 1). The length of transects was variable depended on the dendrogram and importance of more frequent species into strip of the natural vegetation. Size of sampling plots was each group of plots (Abedi et al. 2011).
Figure 1. Location of Guilan Province in Iran and vegetation sampling in coastal sand dune. 18 BIODIVERSITAS 16 (1): 16-21, April 2015
Measuring plant diversity Comparison of plant diversity To quantify the diversity of the plant species, The Normality of the data distribution was checked by Shannon-Wiener’s (H'), Simpson index (1-D), Margalef ’s Kolmogorov -Smirnov test, and Levene’s test was used to richness index (DMg) and Pielou ’s evenness index (E1) examine the equality of the variances. One -way analyses were used. The formulas are as follows. (ANOVA) of variance were used to compare groups with normal distribution data. Duncan test was used to test for s ni significant differences in the species richness, diversity and 1 D P 2 Pi i N evenness indices among the groups. This analysis was i1 conducted using SPSS 16.0. S 1 DMg LnN RESULTS AND DISCUSSION
s s Vegetation groups H Pi ln Pi (Pi) (log pi) The application of TWINSPAN analysis led to identify i1 i1 vegetation groups associated with the distribution of these plants in the region (Figure 2). The classification was stopped at fifth level of division, leaving only groups with a sufficient number of samples to characterize the vegetation communities. Thus, 62 sampling plots were classified into eight groups. In the first level, 62 sampling H' = Shannon-Wiener's diversity index, D = Simpson's plots were divided into two groups (Eigenvalue = 0.536). The indicator species which have been seen on the left side index, DMg = Margalef 's richness, E1 = Pielou's evenness, th Pi = relative frequency of i species, S = number of included: Alnus subcordata, Oxalis corniculata and species, N = Total individual of species (Ludwig and Scutellaria tournefortii. The indicator species on the right Reynolds 1988). side were Crypsis schoenoides and Argusia sibirica. In
Aln sub (1.9) Cry sch (22.5) Oxa cor (0.8) Are sib (12.0) Scu tou (0.7)
Con arv (2.0) Oxa cor (8.0) Phy nod (2,5)
Cen asi (5.0) Con per (7.0) Cry sch (15.1) Pun gra (1,9) Jun acu (3.0) Oxa cor (7,1) Eri cau (3.4) Scu tou (3.0)
Are sib (11.0) Cry sch (15.1) Era bar (0.3) Rub san (0.4) Sil lat (1.3) Tor lep (0.4)
Arg sib (9.2) Cry sch (3.10) Cen ibe (1,6)
Figure 2. Classification of ecological species groups by using TWINSPAN analysis. Note: Aln sub = Alnus subcordata, Oxa cor = Oxalis corniculata, Scu tou = Scutellaria tournefortii, Cry sch = Crypsis schoenoides, Arg sib = Argusia sibirica, Con arv = Convolvulus arvensis , Phy nod = Phyla nodiflora, Con per = Convolvulus persicus, Cen asi = Centella asiatica, Pun gra = Punica granatum, Ery cau = Eryngium caucasicum, Jun acu = Juncus acutus, Era bra = Eragrostis barrelieri, Sil lat = Silene latifolia, Rub san = Rubus sanctus, Tor lep = Torilis leptophylla, Cen ibe = Centaurea iberica. RAVANBAKHSH et al. – Plant diversity in the Caspian Sea coastal sand dune 19
Table1 1. ANOVA results of diversity indices among groups and mean and standard error of diversity indices.
Diversity index F P Mean square df Mean and standard error Shanon diversity index 3.756 .003* .606 7 1.491±0.662 Simpson diversity index 3.074 .010* .068 7 0.6572±0.236 Margalef richness index 2.769 .018* 1.872 7 2.070±0.285 Pielou 's evenness index 2.679 .021* .051 7 0.6572±0.236
the second level, 35 sampling plots were divided into two diversity index is in group 6. While there were not groups (Eigenvalue = 0.523) with Convolvulus arvensis significant differences among groups of 5 and 6. The (group 1) on the left side as indicator species. Also, on the lowest value of Shannon-Wiener's diversity index is in right side, there was not any indicator species. In this level, group 3. There were not significant differences among 27 sampling plots were divided into two groups groups of 1, 2, 3, 7 also between groups of 4 and 8. Figure (Eigenvalue = 0.585) with Phyla nodiflora and Oxalis 4 shows the changes of Simpson's diversity index among corniculata on the left and right side, respectively, as ecological groups. Group 6 had the highest value of indicator species. Simpson's diversity index. The lowest value of Simpson's In the third level, 33 sampling plots were divided into diversity index was in group 3.In this index there were not two groups (Eigenvalue = 0.499); the indicator species on significant differences among groups of 1, 2, and 7 also the left side was Convolvulus persicus (group 2) and there between groups of 4 and 8. was not any indicator species on the right side. In this level, Figure 5 shows the changes of Margalef's richness 18 sampling plots were divided into two groups index among groups. The highest value of Margalef's (Eigenvalue = 0.586). The indicator species on the left side richness was in group 5.and group 1 had the lowest value included: Centella asiatica, Crypsis schoenoides and of Margalef 's richness index. Figure 6 shows the changes Oxalis corniculata. The indicator species on the left side of Pielou's evenness index among ecological groups. The were Punica granatum and Eryngium caucasicum (group highest value of Pielou's evenness index was in group 3). Also, in this level, 9 sampling plots were divided into 5.and group 3 had the lowest value of this richness index. two groups (Eigenvalue = 0.791). The indicator species on Altogether Duncan's tests showed that among the eight the left side were Juncus acutus and Scutellaria tournefortii ecological groups, Group 5 and 6 had the highest and (group 4) while on the right side, there was not any Group 1 and 3 had the lowest values in groups. indicator species. In the fourth level, 26 sampling plots were divided into Discussion two groups (Eigenvalue = 0.527); the indicator species on In the present study, TWINSPAN analysis was the left side were Argusia sibirica and Crypsis schoenoides performed to identify plant species groups. Results showed and those on the right side included: Eragrostis barrelieri, that eight ecological species groups were found in the Silene latifolia (group 5). In this level, 12 sampling plots southwestern coastal sand dune of the Caspian Sea. The were divided into two groups (Eigenvalue = 0.616); the vegetation groups in the Caspian coastal regions have been indicator species were Rubus sanctus × hyrcanus and analyzed by different methods such as physiognomic, Torilis leptophylla (group 6) on the right side while there Braun-Blanquet and multivariate methods led to the was not any indicator species on the left side. In the fifth identification of these communities and types: Juncus, level, 21 sampling plots were divided into two groups Rubus, sand dune, halophyte, hydrophyte (Shokri et al. (Eigenvalue = 0.540) that those indicator species on the left 2004); Plantago indica-Carex nutans, pure Punica, and right side were Argusia sibirica (group7), and Crypsis Punica-Rubus, Punica-Juncus, Juncus-Rubus, Frankenia schoenoides and Centaurea iberica (group8), respectively. hirsuta-Plantago coronopus (Ejtehadi et al. 2005); Convolvulus persicus-Cakile maritima, Juncus acutus, Species diversity among groups Trifolium repens-Centaurea iberica, Tamarix ramosissima, First of all, based on Kolmogorov-Smirnov test it Ruppia maritima, Typha latifolia-Phragmites australis, should be approved that the data are normal. .For analyzing Schoenoplectus litoralis, Nelumbium caspicum, the diversity among the groups, one-way Analysis of Ceratophyllum demersum-Myriophyllum spicatum variance (ANOVA) was used. ANOVA results of diversity (Naqinezhad 2012a), Potamogeton pectinatus, indices among groups and mean and standard error of Ceratophyllum demersum-Azolla filiculoides, Nymphaea diversity indices were listed in Table 1. ANOVA showed alba, Nelumbium nuciferum, Phragmites australis, that there were significant differences among groups in Hydrocotyle ranunculoides, Typha latifolia, Cladium terms of biodiversity indices (P<0.05). mariscus, Sparganium neglectum, Cyperus sp., Paspalum Duncan's test of groups showed in figure of 3- 6. Figure distichum, Cerastium dichotomum (Asri and Moradi 2006); 3 shows the changes of Shannon-Wiener's diversity index Frankenia hirsuta, Juncus acutus, Juncus maritimus, among ecological groups. Maximum of Shannon-Wiener's J u n c u s littoralis , J u n c u s l i t t o ra l i s - T a m a r i x 20 BIODIVERSITAS 16 (1): 16-21, April 2015
arceuthoides, Salicornia europaea, Tamarix ramosissima, Artemisia tschernieviana, Convolvulus persicus, Tournefortia sibirica, Filaginella sp., Juncus maritimus- Rubus sanctus, Juncus littoralis-Punica granatum, Juncus littoralis-Rubus sanctus, Mespilus germanica-Punica granatum, Punica granatum, Rhamnus pallasii-Punica granatum, Rubus sanctus-Punica granatum, Saccharum griffithii, Saccharum kajkaiense, Sambucus ebulus, Phragmites australis, Phragmites australis-Juncus acutus, Scirpus lacustris, Typha laxmannii, Typha laxmannii- Phragmites australis (Asri et al. 2007). Figure 3. Changes in Shannon-Wiener’s diversity index among These groups, types and communities indicated that ecological groups. some of them belong to Freshwater or marginal freshwater ecosystems those were plentifully found in the wetlands and southern coastal area of the Caspian Sea. Our study showed that the vegetation types included: Convolvulus persicus, Juncus acutus, Punica granatum and Rubus sanctus have been reported in the other studies (Shokri et al. 2004; Ejtehadi et al. 2005; Asri et al. 2007; Naqinezhad 2012a). The following ecological species groups were reported firstly from Iran containing: Convolvulus arvensis, Eragrostis barrelieri-Silene latifolia, Argusia sibirica and Crypsis schoenoides-Centaurea iberica. As was mentioned in the results, the goal of this research was to investigate diversity indices among ecological groups. The results of the ANOVA and the Duncan's tests showed that the groups differed significantly Figure 4. Changes in Simpson's diversity index among ecological in terms of biodiversity indices. Checking of the 3-6 groups. Figures indicated that groups 5 and 6, and 1, 2, 3 and 7 had the highest and lowest level of the indices, respectively. The reason of high diversity in groups 5 and 6 can be interpreted that these groups belong to coastal pasture grass including helliophyta species. Also, the group 6 was a marginal sea shrub cover consisting of some sciophyta species in the under layer of canopy cover and helliophyta species in the open space between shrubs. Also, these two groups were grown on the stabilized soil with appropriate distance from the sea. In contrast, the reasons of the low species diversity in the groups 1, 2 and 7 were perhaps growing in don’t fixed sand dunes and being closely to the sea. In conclusion, diversity is one of the main factors of sustainable management. Identifying plants species of a Figure 5. Changes in Margalef's richness index among ecological region and their biodiversity is very effective way to groups. identify disturbance factors and develop recovery plans. It is also essential to maintain a high proportion of native species, create protection programs and preserve the area against human and livestock disturbances. Our knowledge about plant biodiversity of the southern Caspian coast is fragmentary and requires in-depth studies to reveal all of its components. The southern Caspian coast and their sand dune went through extensive man-made changes during the past decades. The growth of population followed by the land usage changing for agriculture and urban utilizing, has affected on the biodiversity. The loss of genetic and species diversity by the destruction of natural habitats would need to restore many years. It is necessary to establish certain laws and regulations in order to protect all plants species and ecosystems. Figure 6. Changes in Pielou's evenness index among ecological groups. RAVANBAKHSH et al. – Plant diversity in the Caspian Sea coastal sand dune 21
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Importance of Vegetation Studies in National Conference on Watershed Management and Soil and Water Conservation of Wildlife: A Case Study in Miankaleh Wildlife Resources Management, Irrigation and Water Engineering Society of Refuge, Mazandaran Province, Iran. Environ Sci 9: 53-58. Iran, Kerman, Iran, 22-23 February 2005. Frey W, Probst W. 1974. Vegetations analytische Untersuchungen im Spies TA, Barnes BV. 1985. A multifactor ecological classification of the Dünengebiet bei Babolsar (Kaspisches Meer, Iran). Bot Jahrb Syst 94: northern hardwood and conifer ecosystems of Sylvania Recreation 96-113. Area, Upper Peninsula, Michigan. Can J For Res 15, 949-960. Ghahreman A. 1975. The Species Eliminated from the Native Vegetation Vogiatzakis IN, Griffiths GH, Mannion AM. 2003. Environmental factors of Iran; Proceeding of First seminar on problems of the Natural and vegetation composition. Glob Ecol Biogeogr 12, 131-146. vegetation of Iran.Tehran, June 29-July 2 1975. [Iran] Zarekar A, Vahidi H, Kazemi Zamani B, Ghorbani S, Jafari H. 2012. Ghahreman, A, Naqinezhad AR, Attar F. 2004. Habitats and Flora of the Forest fire hazard mapping using fuzzy Ahp and GIS study area: Chamkhaleh-Jirbagh Coastline and Amirkelayeh Wetland. J Environ Gilan Province of Iran. Intl J Tech Phys Probl Eng 4 (3): 47-55. Stud 33 (1): 46-67. BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 22-26 DOI: 10.13057/biodiv/d160104
Short Communication: Note on Excoecaria indica (Willd.) Muell.-Arg, 1863 (Euphorbiaceae), from the Andaman and Nicobar Islands, India; a data deficient species
PADISAMY RAGAVAN1,♥, K. RAVICHANDRAN2, P.M. MOHAN3, ALOK SXAENA4, R.S. PRASANTH1, R.S.C. JAYARAJ5, S. SARAVANAN1 1Institute of Forest Genetics and Tree Breeding, R.S.Puram, P.B. No 1061, Coimbatore 641002, Tamil Nadu, India. Tel. +91-422-2484100, Fax. +91-422-2430549, ♥email: [email protected]. 2Department of Environment and Forest, Andaman and Nicobar Administration, Port Blair, A & N Islands, India. 3Department of Ocean studies and marine Biology, Pondicherry University, Brookshabad Campus, Port Blair, A & N Islands, India. 4Indira Gandhi National Forest Academy, Dehradun, Uttarakhand, India. 5Department of Environment and Forest, Arunachal Pradesh, India.
Manuscript received: 1 October 2014. Revision accepted: 27 October 2014.
Abstract. Ragavan P, Ravichandran K, Mohan PM, Sxaena A, Prasanth RS, Jayaraj RSJ, Saravanan S. 2015. Note on Excoecaria indica (Willd.) Muell.-Arg, 1863 (Euphorbiaceae), from the Andaman and Nicobar Islands, India; a data deficient species. Biodiversitas 16: 22-26. Excoecaria indica (Wild.) Muell.-Arg was recorded from Middle Andaman and Great Nicobar Island representing a new addition to the mangrove flora of the, Andaman and Nicobar islands. This species is characterized by its thorny trunk, crenulate- lanceolate leaves and cherry-sized green fruits containing three seeds. Information about E. indica is inadequate, and it is recognized as data deficient species. Further studies and conservation measures are imperative for managing the mangrove diversity of the islands with regards to this species.
Key words: Andaman and Nicobar Islands, Excoecaria, India, new records.
INTRODUCTION from related genera by a combination of characters including dioecious condition, axillary inflorescences, male Mangrove forests are unique plant communities of the flowers with 3 stamens, and the absence of a caruncle from critical interface between terrestrial, estuarine, and near- the seed (Tomlinson 1986). The genus includes up to 40 shore marine ecosystems in tropical and subtropical regions species in the Indo-west pacific region, from tropical (Polidoro et al. 2010; Hanum et al. 2013). Despite its Africa and Asia to the western pacific. Two species occur ecological and economical values, globally mangrove areas in mangroves, including Excoecaria indica (Wild.) Muell.- are disappearing at the rate of approximately 1% per year Arg and Excoecaria agallocha L. In India E. indica is rare, (FAO 2003, 2007). The mangroves of Andaman and classified as critically endangered (Kathiresan 2008) and Nicobar (A & N) Islands are probably the best in India in known to occur only in Sundarban and Kerala (Kathiresan terms of its density and growth (Mandel and Naskar 2008, 2008). E. indica is categorized by the IUCN as data Dagar et al. 1991). According to the latest estimate by the deficient (Polidoro et al. 2010), due to lack of adequate Forest Survey of India (Anon. 2013), the total mangrove information. In contrast, E. agallocha is abundant, known area is about 4,628 km2 in India, out of which, 604 km2 to occur on both east and west coasts of India except occur in A & N Islands. Out of this 601 km2 is in Andaman Gujarat and it is among the mangrove species which is and only 3 km2 found in Nicobar Islands. Total 13 km2 area considered to be in the IUCN category of lesser risk of mangrove stands has degraded as a consequence of (Kathiresan 2008). Though Goel and Chakrabarthy (1990) massive earthquake and subsequent tsunami of 2004 in reported the occurrence of E. indica from Andaman Andaman Islands in comparison with 2011 (Anon. 2013). Islands, its occurrence was not reliable as other authors like However, after the tsunami distribution of some mangrove Dagar et al. (1991) and Kathiresan (2008) reported that E. species, not recorded earlier in ANI, are reported (Dam indica was not found in ANI. Moreover, authentic Roy et al 2009; Nehru and Balasubramanian 2012; herbariums are not available for the occurrence of E. indica Goutham-Bharathi et al. 2012; Ragavan et al. 2014). The in ANI. Recent floristic surveys revealed the occurrence of present study also adds the new distributional record of Excoecaria indica from Middle Andaman and Great Excoecaria indica (Wild.) Muell.-Arg from this island. Nicobar Island, which we report herein as a new The tropical indo-pacific genus Excoecaria L. belongs distribution record in the ANI along with a detailed to the family Euphorbiaceae Juss., and includes several taxonomical description as follows. mangrove representatives (Duke 2006). It is distinguished RAGAVAN et al. – Excoecaria indica of the Andaman and Nicobar Islands 23
TAXONOMIC TREATMENT muddy soil, along the tidal creek on the landward margin of mangroves in association with Heritiera littoralis, Key to Excoecaria species in ANI Sonneratia griffithii and Dolichandrone spathacea. 1. Leaf margin serrated, bark smooth, trunk with thrones, monoecious, fruits rounded with three seeds ...... …. E. Indica Excoecaria agallocha L. 2. Leaf margin entire to wavy, bark fine fissured with lenticels, Excoecaria agallocha L.; Linnaeus, C. von, Systema dioecious, fruits three lobed ...... ….. E. agallocha Naturae ed. 10: 1288 (1759). Type: Tropical Asia, Malaya and Pacific Islands. Ng, P.K.L and Sivasothi, N. eds. A Description Guide to the Mangroves of Singapore. Volume 1 The Ecosystem and Plant Diversity. Singapore Science Centre, Excoecaria indica (Willd.) Muell.-Arg. Singapore, 160 pp (1999). (Figure 2) Excoecaria indica (Willd.) Muell.-Arg, Airy Shaw, Tree up to 10-15m high, columnar or spreading, mutli- H.K., The Euphorbiaceae of Borneo. Kew Bulletin stemmed, dioecious, deciduous; bark grey, rough, fissured Additional Series IV, Her Majesty’s Stationaery Office, on maturity, pustular with lenticels. Stem simple, London, 245 pp. (1975); Aksornkoae, S. Ecology and occasionally slight buttresses. Root above ground, Management of Mangroves. IUCN Wetlands Programme. serpentine like. Leaves simple, alternate, elliptic, green, IUCN, Bangkok, Thailand, 176 pp. (1993); Heyne, K. De apex acute to acuminate, base cuneate, margin variably Nuttige Planten van Indonesië. Publishers W. vanHoeve, serrate to entire, 5-15cm L, 2-6cm W, L/W ratio is >2; TheHague/Bandung, 2 volumes, 1660 pp. & CCXLI. petiole green, terete 1-3.5cm L, 0.2cm W. Inflorescences (1950); Ng, P.K.L and Sivasothi, N. eds. A guide to the axillary; male inflorescence 5-10cm L, flowers arranged Mangroves of Singapore. Volume 1. The Ecosystem and spirally with bract, calyx lobes 3; stamens 3, yellow, 0.3- Plant Diversity. Singapore Science Centre, Singapore, 160 0.5cm L, pistillode absent ; Female inflorescence 2-4cm L, pp. (1999); Tomlinson, P.B. The Botany of Mangroves. peduncle 0.5cm L, bract glandular, basal bracteoles 2, Cambridge University Press, Cambridge, U.K., 419 pp. calyx lobes 3, staminodes absent, ovary tri-locular; styles 3, (1986). (Figure 1). 0.3cm L. Fruit 3-lobed capsule, 1-1.5cm W, green Tree 10-15m, high with upright branches and more or becoming brown on maturity, three seeded; seeds are less drooping twigs; thorny trunk without buttress; bark rounded, black or dark brown, streaked, up to 0.5cm W. fissured; greyish brown in colour; no above ground roots. Distribution. Occurs in the Asian tropics, from India Leaves simple, alternate, elliptic or lanceolate, 7-14 x 3-4 and Sri Lanka throughout Southeast Asia, to southern cm, base obtuse, margins conspicuously serrate, apex sub- China, Taiwan, Southern Japan, Australia and the west acuminate to acuminate with two small glands at the base Pacific. Except Gujarat it was known to occur in other of the blade; lateral veins 18-24; petiole 7-20 mm long and places. In ANI it was recorded from both Andaman Islands reddish. Inflorescences solitary, raceme-like, to 10 cm, axis and Nicobar islands. pilose, petal absent ; flowers unisexual, male or staminate Habitat and Ecology. It is commonly found on the flowers are numerous with 3 prominent stamens; stamen landward margin of mangroves but in Andaman Islands filaments 0.5-0.6 mm at anthesis, nearly absent in bud; this species was observed from downstream to upstream anthers 0.4-0.5 mm; female or pistillate flowers are 1or 2; estuarine position and mid and high intertidal regions. Like solitary with 3 long styles; styles ca. 1.5 mm; stigmas 4-6 other common mangrove species this is also flooded by mm. Fruit is a round, woody capsule, 2.5-3 cm in diameter, tidal fluctuations. green ; black when dries, 3-seeded. Fruit stalk 8-22mm. Phenology. Flowering: June to August; Fruiting: Seeds 11-13 by 7-8.5 mm, keeled on the back, medium to September to November. pale brown, not spotted, without caruncle. Specimen examined. India, Middle Andaman, Rangat, o o Distribution. From south and east India throughout Betapur (92 57’39.7” E, 12 34’31.3”N) 6/9/2013 Southeast Asia to the Solomon Islands. In Southeast Asia P.Ragavan (s n 30935 & 30936PBL). so far not (yet) recorded in the Philippines. In India it was known from west Bengal and Kerala In this study it was Discussion recorded first from ANI at Panchwati and Campbell bay. Both E. indica and E. agallocha are characterized with Habitat and ecology. The distribution and habitat simple leaves, absences of petals, trilocular ovary with 1 ecology of E. indica is poorly known. Generally it is ovule per loculus, inarticulate laticifers with white latex, known to occur in primary Nypa forest in sea water, tidal and biglandular bracts on the inflorescences (Tomlinson river banks and sea shores (Giesen et al. 2006) and in 1986). However, E. indica is distinguished from E. primary and advanced secondary forests of swampy and agallocha by its thorny trunk, crenulate-lanceolate leaves seasonally inundated places (Esser 1999). Also occurs in and green fruits the size of cherry with three seed (Duke freshwater swamp forests, along rivers and in evergreen 2006) and most importantly E. indica is monoecious lowland forest up to an altitude of 250 m. whereas E. agallocha is dioecious (Table 1). Though it is Phenology. Flowering: March to June; Fruiting: July to native to India, Biswas et al. (2007) categorized it as a October. weed with potential environmental impacts to the Specimen examined. India, Middle Andaman, Rangat, Sundarbans because it accumulates allelopathic toxins in Betapur (92o57’39.7” E, 12o34’31.3”N) 6/9/2013 the soil, affecting biota, including poisoning of animals. P.Ragavan (s n 30758PBL). 16 trees were observed in the The present record of E. indica from Andaman and Nicobar 24 BIODIVERSITAS 16 (1): 22-26, April 2015
A B C \ \
D E F \ \ \ F \
G H I \ \
Figure 1. Excoecaria indica. A. Habitat, B. Lanceolate leaves with serrated margin, C. Characteristic thorny trunk, D. Cat-kin like inflorescences, E. Male flowers, F. Female flower, G. Small green globose fruit, H. Mature fruit black in color, I. Cross section of fruit showing three locus arrangement. RAGAVAN et al. – Excoecaria indica of the Andaman and Nicobar Islands 25
A B \ \
C D E \ \ \
F G H I \ \
Figure 2. Excoecaria agallocha. A. Habit, B. Leafy rosette, C. Male inflorescences, D. Young male inflorescences, E. Male flowers with three stamens, F. Female inflorescences, G. Female flowers with three style, H. Three lobed fruits, I. Bark. 26 BIODIVERSITAS 16 (1): 22-26, April 2015
Table 1. Key diagnostic characters of Excoecaria spp in ANI
Characters E. agallocha E. indica Leaf shape Broadly elliptic to lanceolate Lanceolate Leaf apex Acute to acuminate Acuminate Leaf base Attenuate Cuneate Leaf margin Variably serrate to entire Serrated Bark Pale grey, finely fissured, trunk smooth Grayish brown, fissured, trunk with prominent thrones Inflorescences Axillary, Male and female inflorescences on Axillary, male and female flowers on same different individual inflorescences Male inflorescence Long, flowers with three long stamens Numerous with three long stamens Female inflorescence Small, flowers with three style One or two at the base of inflorescences with prominent style. Fruits Three lobed, three seeded Rounded, three seeded
Islands represents a new addition to the mangrove flora of Dam Roy S, Krishnan P, George G, Kaliyamoorthy M, Goutham Bharathi the islands, and highlightens its floristic affinities with MP. 2009. Mangroves of Andaman and Nicobar Islands. CARI, Port Blair Southeast Asian countries. Further, it suggests the need for Duke NC. 2006. Australia’s Mangroves: the Authoritative Guide to periodical floristic survey to update information on the Australia’s Mangrove Plants. The University of Queensland and extent and status of mangroves in the Andaman and Norman C. Duke, Brisbane. Nicobar Islands. Since E. indica is categorized as data Esser HJ. 1999. A partial revision of the Hippomaneae (Euphorbiaceae) in Malesia. Blumea 44: 149-215 deficient, immediate efforts should be taken to generate FAO. 2003. Status and trends in mangrove area extent worldwide. In: information about its habitat ecology, distribution and Wilkie ML, Fortuna S, eds; Forest Resources Assessment Working conservation. Paper No. 63. Rome: Forest Resources Division, FAO. FAO. 2007. The World’s Mangroves 1980-2005, FAO Forestry Paper 153. Forest Resources Division, FAO, Rome. Giesen W, Wulffraat S, Zieren M, Scholten L.2006. Mangrove Guidebook ACKNOWLEDGEMENTS for Southeast Asia. FAO and Wetlands International. RAP Publication, Bankok, Thailand. Goel AK, Chakrabarty T. 1990. Excoecaria indica new record We are highly indebted to Director General, Indian Euphorbiaceae new for Andaman Islands India. J Econ Tax Bot 14 Council for Forestry Research and Education for providing (3): 738. necessary support under NFRP. Extremely Grateful to the Goutham-Bharathi MP, Kaliyamoorthy M, Dam Roy S, Krishnan P, Principal Chief Conservator of Forests, Andaman and Grinson George, Murugan C. 2012. Sonneratia ovata Nicobar Islands for his guidance and ensuring necessary (Sonneratiaceae)－A new distributional record for India from Andaman and Nicobar Islands. Taiwania 57(4): 406–409 support from field. Appreciate the cooperation and support Hanum F, Latiff A, Hakeem KL, Ozturk. M (eds.). 2013. Mangrove provided by the CCF (Research and Working Plan), CCF, Ecosystems of Asia. Springer, Berlin. Territorial Circle and all the Divisional Forest Officers and Kathiresan K. 2008. Biodiversity of Mangrove Ecosystems. Proceedings their staff in the Department of Environment and Forests, of Mangrove Workshop. GEER Foundation, Gujarat, India. Mandal RN, Naskar KR. 2008. Diversity and classification of Indian Andaman and Nicobar Administration. Thanks are due to mangroves: a review. Trop Ecol 49: 131-146 Dr. N. Krishnakumar, IFS, Director, Institute of Forest Nehru P, Balasubramanian P. 2012. Sonneratia ovata Backer Genetics and Tree Breeding, Coimbatore for his support (Lythraceae): status and distribution of a Near Threatened mangrove and encouragement. Special thanks are extended to DFO species in tsunami impacted mangrove habitats of Nicobar Islands, India. Journal of Threatened Taxa 4(15): 3395–3400. Campbell Bay for constant support. Polidoro BA, Carpenter KE, Collins L, Duke NC, Ellison AM, Ellision JC, Farnsworth EJ, Fernando ES, Kathiresan K,. Koedam NE, Livingstone SR, Miyagi T, Moore GE, Vien Ngoc Nam, Ong JE,. Primavera JH, Salmo SG, Sanciangco JC, Sukardjo S, Wang Y, Yong REFERENCES JWH. 2010. The loss of species: Mangrove extinction risk and geographic areas of global concern. PLoS ONE 5 (4): 1-10. Anon. 2013. Status of forest report. Forest Survey of India (FSI), Dehra Ragavan P, Ravichandran K, Mohan PM, Sxaena A, Prasanth R S, Jayarai Dun. RSC, Saravanan S. 2014. New distributional records of Sonneratia Biswas SR, Choudhury JK, Nishat A, Matiur Rahman Md. 2007. Do spp. from Andaman and Nicobar Islands, India. Biodiversitas 15: 250- invasive plants threaten the Sundarbans mangrove forest of 259 Bangladesh?. For Ecol Manag 245 (1-3): 1-9. Tomlinson BP. 1986. The Botany of Mangroves. Cambridge Univ. Press, Dagar JC, Mongia AD, Bandhyopadhyay AK. 1991. Mangroves of Cambridge. Andaman and Nicobar Islands, Oxford and IBH, New Delhi. BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 27-43 DOI: 10.13057/biodiv/d160105
Ferns and fern allies of District Shopian, Kashmir Valley, India
SHAKOOR A. MIR1,♥, ANAND K. MISHRA1, SHAUKET AHMAD PALA2, ZAFAR A. RESHI2, M.P. SHARMA1 1Department of Botany, Jamia Hamdard, Hamdard Nagar, New Delhi-110062, India. Tel: +91-9968172445; ♥email: [email protected]. 2 Department of Botany, University of Kashmir, Hazratbal, Srinagar-190006, Jammu and Kashmir, India
Manuscript received: 11 November 2014. Revision accepted: 9 December 2014.
Abstract. Mir SA, Mishra AK, Pala SA, Reshi ZA, Sharma MP. Ferns and fern allies of District Shopian, Kashmir Valley, India Biodiversitas 16: 27-43. Shopian, recently created hilly district of Kashmir valley, Jammu and Kashmir is surrounded by the lofty mountains of Pir-Panjal range. More than half area of district is occupied by different forests, subalpine, alpine and mountainous zones. Great altitudinal variation, adequate rainfall, high forest cover, large number of streams, springs and topographic variations render the district worthy for supporting rich fern flora. Therefore, the current study was aimed to undertake in-depth systematic survey of different habitats of Shopian for the collection of diversity of pteridophytes. Specimens were collected during 2010, 2011 and 2012 growing seasons from June to November. A total 81 species of ferns and fern allies belonging 27 genera and 11 families were reported. The dominant families of the region are Dryopteridaceae (25 species) followed by Woodsiaceae (16 species), Aspleniaceae (13 species) and Pteridaceae (12 species). Similarly, the dominant genera collected from here are Dryopteris (14 species), Asplenium (13), Polystichum (11 species) and Athyrium (6 species). A list of the fern and fern allies, along with update nomenclature, their selected Synonym, diagnostic features, distributional and ecological notes have been provided here.
Key words: distribution, diversity, ferns, Kashmir valley, lycophytes, Shopian, survey.
INTRODUCTION plants; many species are distinct from those in the rest of the country and are endemic to this region. However, the Pteridophytes comprise a group of seedless but spore published literature on the flora of Kashmir reveals that producing plants, formed by two lineages, lycophytes- only the Phanerogams have been well documented. The fronds with no leaf gap in the stem stele (Lycophylls) and cryptogams, particularly pteridophytes have met little Monilophytes or ferns- fronds with leaf gap in the stem attention in the past with regards to their survey and stele (Euphylls) (Pryer et al. 2001, 2004; Smith et al. 2006). inventorization (Dar et al. 2002). They constitute an important component of earth’s flora for The valley has been occasionally explored in the past millions of years (Pryer et al. 2001). Presently there are for pteridophyte diversity by Clarke (1880), Beddome about 300 genera of pteridophytes containing (1883, 1992) and Hope (1899-1904). Some isolated fern approximately 9600 ferns and about 1400 lycophytes collections have also been made in this region by the worldwide (Smith et al. 2006, 2008), with highest diversity botanists of botanical survey of India, like R.B. in the tropics (Jacobsen and Jacobsen 1989; Kornas 1993; Keshavanand, T.A. Rao, P.K. Hajra, U.C. Bhattacharayya, Linder 2001). The current revised treatment of fern and B.M. Wadhwa, M.V. Vishwanathan, etc. (Wani et al. 2012) fern allies from India revealed 1150 species (Fraser-Jenkins The other studies particularly relevant to the pteridophytic 2008; Fraser-Jenkins and Benniamin 2010). The west flora of Kashmir are of Stewart (1945, 1951, 1957 1972, Himalayas is the fourth richest area for pteridophytes in 1984); Javeid (1965), Kaul and Zutshi (1966, 1967), Kapur India after the east Indo-Himalayas, the Manipur-Khasi and Sarin (1977), Dhir (1980), Kapur (1985), Khullar range and south India, and harbours about 402 species, (1984, 1994, 2000), Razdan et al. (1986); Khullar and which constitute 40%, over one-third of pteridoflora of Sharma (1987), Fraser-Jenkins (1989, 1991, 1992, 1993, whole country (Kumari et al. 2010). Kashmir Himalaya, a 1997, 2008) and Singh and Pande (2002). Recently, an up- picturesque south Asian region, is unique biospheric unit to-date account of fern and fern allies has been published located in the northwestern extreme of the Himalayan collectively for Kashmir valley, Gurez (Kishanganag biodiversity hotspot (Rodgers and Panwar 1988). valley) and Ladakh by Wani et al. (2012) yet representing One of the main features contributing to the worldwide only 106 taxa of fern and fern allies. The present authors fame of Kashmir is the rich biodiversity that decorates its have, therefore, undertaken to explore in-depth captivating landscape (Lawrence 1895). Owing to the vast pteridophytic wealth and possibility of new records in the variety of edapho-climatic and physiographic heterogeneity Kashmir valley, and have restricted their study to district and diverse habitats including lakes, springs, swamps, Shopian, which possesses the majority of topographical marshes, rivers, cultivated fields, orchards, subalpine and features of the large expanse of valley. alpine meadows, mountain slopes and terraces, permanent glaciers, etc., the valley harbors almost all groups of land 28 BIODIVERSITAS 16 (1): 27-43, April 2015
MATERIAL AND METHODS region is deciduous type. The low land zone is mostly under cultivation and habitation, supporting crop fields- Shopian, one of the ten districts of Kashmir division of kharief crop fields, orchards, kitchen gardens and natural Jammu and Kashmir State (Figure 1) is located in the south fields- roadsides, pastures, grasslands, graveyards, rocky and south-west extremity of Kashmir valley within the meadows, streams, waste-lands, ponds, small ditches and coordinates of 330 20′ and 340 54′ North latitude and 730 spring sites. Mountain zone which is the maximum portion 35′ and 750 35′ East longitude. The district has been created of the district includes broad-leaved deciduous forests, in 2006. Total area of the region is 812.70 km2, of which mixed conifer forest, kail forests, scrub forests, meadows more than half about 442.98 km2 is occupied by alpine and bare snow laden mountains. Each of these habitats has zone with a considerable portion under meadowlands and a peculiar type of vegetation, thus making the whole glaciers. The forest cover of different forests viz, deodar, district biologically diverse. All these remarked features kail, fir and broad leaved forests is approximately 316.60 support a rich flora of cryptogams, particularly km2. The temperature ranges from an average daily pteridophytes. However, during the last decades the floras maximum of 31ºC and minimum of 15ºC during summer to published from this region including Flora of Pulwama an average daily maximum of 4ºC and minimum of – 4ºC (Kashmir) (Navchoo and Kachroo 1995) reported only during winter (Bhat et al. 2012). The long and cold winter flowering plants and therefore, no keen interest has been season is dominated by the western atmospheric laid on Pteridophytic flora and as such no published depressions called Western Disturbances (Jeelani et al. pterido-flora is available from this district. 2010), which cause snowfall and rainfall. The annual Diverse habitats such as plains, streams, rivulets, rivers, precipitation of is about 1,050 mm; by and large in the small valleys, dense forests, meadows, sub-alpine, alpine, form of snow during the winter months and rain during the mountains etc. of study area were surveyed for the late winter and early spring (Raza et al. 1978). According collection of fern diversity during the years 2010 – 2012. to Raza et al. (1978) the district possesses rich soil The major research sites are shown in Figure 1. Each diversity, having three major categories of soils namely hill specimen was photographed, numbered as it was collected soils, alluvial soils and Karewa soils. With the gradual and the detailed notes were entered in the notebook. The ascending slope from its north and north-eastern sides and collected specimens were pressed and dried in the standard loft Pir Panjal mountain range falling on its south and way and described and identified with the relevant south-west periphery, the district has most of its areas of literature (Beddome 1976, 1983; Clarke 1880; Fraser- hilly character with the altitudinal range varying from 1600 Jenkins 1989; Khulllar 1994, 2000; Ghosh et al. 2004). The to 4562 meters. Most of the vegetation met in this identity of specimens was authenticated from Botanical
1
9 8 10 7 INDIA 11 16 6 13 12 15 14 15 4 3 2
KASHMIR
Figure 1. Research sites in district Shopian of Jammu and Kashmir State, India. 1. Zainapora; 2. Kaunsernag; 3. Huran; 4. Secjan; 5. Reshi Nagar; 6. D. K. Pora; 7. Narwani; 8. Imamsahib; 9. Rambi Ara; 10. Rambi Ara; 11. Heerpur; 12. Sedow; 13. Dubjan; 14. Peergali; 15. Aharbal; 16. Lahanthoor. MIR et al. – Pterydophytes of Shopian, Kashmir Valley 29
Survey of India, Northern Circle, Dehradun. One set of growing luxuriously between 1600-2500; 18 were reported voucher specimens are deposited in Department of Botany, within the range of 2500-3200 m; and 12 were found Jamia Hamdard and another in the Herbarium, Centre for within the altitudinal range of 3300-4100 m. However, Biodiversity and Plant Taxonomy, University of Kashmir Adiantum venustum, Asplenium adiantum-nigrum, A. (KASH). The identified plants are listed according to the trichomanes, Athyrium mackinnoni, Cystopteris fragilis classification system of Smith et al. (2008), followed by and Equisetum arvense were collected throughout the selected Synonym, habitat and taxonomic notes, range of ranges of altitudes and were numerically the most abundant distribution and Specimen examined and wide-spread species among all pteridophytes recorded from the region. The species Asplenium viride, Cryptogramma brunoniana, C. stelleri, Lepisorus RESULTS AND DISCUSSION clathratus, Polystichum lachenense, P. shensiense and Woodsia alpina were rarest and restricted to higher An interesting feature of the Shopian is occurrence of altitudes in alpine meadows and rocky mountains. varying topography and great altitudinal range that As per the distribution of pteridophyte species recorded develops immense habitat variation, that facilitated by Dixit (1984), Chandra (2000) and Khullar (1994, 2000), luxurious growth of pteridophyte flora and therefore, as out of 81 species, 61 (75%) are common with the list of many as 81 pteridophyte species belonging to 27 genera, 11 fern and fern allies of Jammu and 67 species (82%) are families, 4 orders and 2 classes were collected from here. common with fern flora of Himachal Pradesh. 59 species The richest fern families of this area are Dryopteridaceae (72%) are common with the Garhwal region, 41 species sharing 25 species followed by Woodsiaceae (15 species), (50%) with Dehradun and 42 species (52%) with Sikkim. Aspleniaceae (13 species) and Pteridaceae (12 species). Summing up, 71 species (87%) and 52 species (64%) Besides these, the families Thelypteridaceae and resemble with pteridoflora of Western Himalaya (Almora, Equisetaceae have 5 and 3 species, respectively; Chamoli, Dehradun, Garhwal, Himachal Pradesh, Jammu, Marsileaceae and Osmundaceae are represented by 1 Kinnaur, Kumaun, Nanital, Pithogarh, Shimla, Uttar species each and Dennstaedtiaceae, Polypodiaceae and Pradsh) and Eastern Himalaya (Arunachal Pradesh, Assam, Salviniaceae with 2 species each. Similarly, the dominant Darjeeling hills, Meghalaya, Mizoram, Nagaland, Sikkim, genera reported from here are Dryopteris (14 species), West Bengal), respectively. 16 species (19%) ferns of this Asplenium (13 species) and Polystichum (11 species). region resemble those met within the South India. The collected species also showed a range of ecological The fern species collected in this region are ethnically distribution varying from aquatic (Marsilea, Azolla) to insignificant. The crosiers of two ferns, Diplazium terrestrial (Athyrium, Dryopteris) to lithophytic (Lepisorus, allantodioides and Pteridium aquilinum are used as some species of Asplenium); and from low-land to forests vegetable by the tribal people. Few others such as to sub-alpine to alpine zones. Except for some lowland Adiantum capillus-veneris, Adiantum venustum, Asplenium ferns, namely Dryopteris filix-mas and D. pulvinulifera that adiantum-nigrum, Asplenium pseudofontanum, Asplenium mature fairly earlier, the appropriate time of maturation is trichomanes, Athyrium wallichianum, Deparia from mid-June to ending October. Within these 3-4 allantodioides, Equisetum arvense, Pteridium aquilinum months, the ferns produce sori and complete their life have various medicinal uses. cycle. However, Equisetum arvense produce cone i.e. Out of 81 species, eight have been recently added by reproductive stage earlier than the vegetative stage from authors to the pteridoflora of Kashmir Valley as new earlier April to mid-May. records. These are Dryopteris caroli-hopei Fraser-Jenk., Based on personal observation and data available from Dryopteris blanfordii subsp. nigrosquamosa (Ching) literature (Stewart 1972; Khullar 1994, 2000; Wani et al. Fraser-Jenk., Dryopteris pulvinulifera (Bedd.) Kuntze and 2012), a rough estimate of status of collected taxa has also Polystichum Nepalense (Spreng) C. Ch (Mir et al. 2014a); been figured. The most common species of the area are Hypolepis polypodioides (Blume) Hook., Pteris Adiantum venustum, Asplenium trichomanes, A. stenophylla Wall. ex Hook. & Grev., Dryopteris pseudofontanum, Athyrium attenuatum, A. mackinnoni, subimpressa Loyal and Dryopteris wallichiana (Spreng.) Deparia allantodioides, Equisetum arvense, Polystichum Hylander (Mir et al. 2014b). prescottianum, Pseudophegopteris levingei. On the Two species Asplenium punjabense Bir & Fraser-Jenk. contrary, Adiantum pedatum, Asplenium viride, Athyrium (Figure 2) and Pseudophegopteris pyrrhorachis (Kunze) strigillosum, Cyclosorus erubescens, Cryptogramma Ching, subsp. distans (Mett.) Fraser-Jenk. (Figure 3) stelleri, Lepisorus clathratus, L. stewartii, Onychium reported here has been recorded first time from the plumosum, Pellaea nitidula, Polystichum lonchitis and Kashmir valley. There are no earlier reports of their Woodsia alpina have been reported only with 1-3 collection from the valley, but have been collected from specimens, whereas other species range in status from Jammu division of J & K State. Asplenium punjabense occasional to frequent. Out of 81 taxa, 29 taxa were differs from its closely related species Asplenium ceterach recorded to be rare and just only 3 taxa, namely Adiantum in having long stipes (more than 3 cm) with sparse scaly venustum, Asplenium trichomanes, and Equisetum arvense lamina on abaxial surface which do not fringe the edges of were abundant in this region. lamina; whereas the later has short stipes (less than 3 cm) The pteridophyte species were reported within the with dense scaly lamina on abaxial surface and fringing the altitudinal range of 1600 to 4100 m. 51 species were found edges of lamina. The P. pyrrhorachis subsp. distans 30 BIODIVERSITAS 16 (1): 27-43, April 2015 contrasts from its close relatives, P. pyrrhorachis subsp. Specimen examined: Huran (SAM 840), 3350, laterepens in having long rhizome, castaneous stipe and 15/072011; Dubjan (SAM 876), 23/07/2011, 3150 m. pinnules with acute apex, whereas the later has rhizome short, stipe stramineous with very base brownish and Salviniaceae Martynov pinnules with rounded apex. 5. Salvinia natans (L) All., Fl. Pedem 2: 289 (1785). Synonym: Marsilea natans L. Enumeration of species Aquatic, free floating small fern, stem dichotomously branched, leaves in whorls of three: 2 floating green entire Equisetaceae Michx. Ex De Candolle and one submerged finely dissected into linear root-like 1. Equisetum arvense L., Sp. Pl. 2: 1061 (1753). structure, common in water bodies with altitudinal range Synonym: Equisetum calderi B. Boivin; E. saxicola from 1700-2000 m. Suksd. Distribution: Africa, Asia, China, Europe, Thailand, Terrestrial, medium sized fern ally, grows along the Vietnam, India (Kashmir. moist stream banks, shady marshes and fields, stem erect, Specimen examined: Zainapora (SAM 902), dimorphic, fertile stem unbranched, sterile stem branched, 10/09/2012, 1630 m. abundant with altitudinal range of 1650-3500 m. 6. Azolla cristata Kaulf., Enum. Fil.: 274 (1824). Distribution: America, Bhutan, Canada, Iran, Turkey, (Previously mis-identified as Azolla pinnata R. Br., Japan, Korea, Mongolia, Nepal, Russia, Europe, North Prodr. Fl. Nov. Holland. 167 (1810). America, India (Northern India). Very small aquatic fern, polygonal in outline, stem Specimen examined: D. K. Pora (SAM 801), pseudodichotomously branched bearing long feathery 20/07/2011, 1750 m; Aharbal (SAM 817), 02/08/2011, roots, leaves minute, overlapping, bilobed; dorsal lobe 2350 m; Heerpur (SAM 929), 15/04/2012, 2650 m. brown-green or reddish, ventral lobe translucent 2. Equisetum diffusum D. Don, Prodr. Fl. Nepal. 19 submerged, fairly common in rice fields and ponds from (1825). 1700-2000 m altitude. Synonym: Equisetum diffusum var. paucidentatum C.N. Distribution: India (Kashmir) Page; E. mekongense C.N. Page Specimen examined: 10/09/2012, 1630 m. Medium size fern ally occurring along road in thickets or in semi-shaded places usually on wet ground in lowland, Marsileaceae Mirb. monomorphic, stem much branched bearing 6-12 ridges, 7. Marsilea quadrifolia L. Sp. pl. 2: 1099 (1753) occasional from 1700-2500 m altitude. Medium size aquatic/terrestrial fern bearing long, Distribution: Bhutan, Japan, Myanmar, Nepal, Pakistan, slender, creeping and branched rhizome, leaves with 4 Vietnam, India (Jammu and Kashmir, Assam, Sikkim, triangular leaflets in cross-shape; common in rice fields and Himalayan Mountains from Shimla to Tibet, Meghalaya, ponds from 1600-2200 m altitude. South India). Distribution: China, Europe, Japan, Korea, North Specimen examined: Narwani (SAM 821), 20/08/2011, America, India (Kashmir, Tamil Nadu). 1740 m. Specimen examined: Herman (SAM 918), 20/06/2011, 3. Equisetum palustre L, Sp. Pl. 2: 1061 (1753). 1800 m; Narwani (SAM 824), 01/07/2011, 1750 m. Synonym: Equisetum palustre var. polystachion Weigel; E. palustre var. szechuanense C. N. Page. Polypodiaceae J. Presl Medium size fern-ally growing in marshes, amongst 8. Lepisorus clathratus (C. B. Clarke) Ching, Bull. Fan sand and boulders of river valleys, under bushes, aerial Mem. Inst. Biol. Bot. 4: 71 (1933). stems monomorphic, green, branched, hollow center, Synonym: Lepisorus nepalensis K. Iwats.; Pleopeltis sheath tubes long, teeth dark, 5-9, teeth margins white, clathrata (C.B. Clarke) Bedd.; Polypodium clathratum scarious, rare from 2000-3600 m altitude. C.B. Clarke Distribution: Bhutan, China, Japan, Korea, Nepal, Lithophytic small fern having long creeping rhizome, North America, Russia, Pakistan, Tibet, India (Kashmir). stipe straw colored, lamina lanceolate, widest at or below Specimen examined: Rambi Ara (SAM 942), middle, costa raised on both sides, veins visible, 17/09/2012, 1950 m. anastomosing to form areolae; rare growing from 2000- 4300 m altitude. Osmundaceae Martinov Distribution: Bhutan, China, Japan, Nepal India 4. Osmunda claytoniana L, Sp. Pl. 2: 1066 (1753). (Kashmir). Synonym: Osmundastrum claytonianum (L.) Tagawa Specimen examined: Huran (SAM 864), 15/07/2011, Terrestrial, large, thick textured, hemi-dimorphic fern, 3455 m; Kongwatan (SAM 940), 20/09/2012, 2650 m. naturally growing in open sunny and rocky slopes in 9. Lepisorus stewartii Ching, in Acta Bot. Austro populations, occasional from 2600-3800 m altitude. Sinica, 1: 23 (1983). Distribution: Bhutan, China, Japan, Korea, Nepal, Lithophytic small fern appearing in colonies on large North America, Russia, Pakistan, Siberia, Tibet, India rocks along streams, stipe very short, green, lamina (Assam, Himachal Pradesh, Kashmir, Sikkim, Meghalaya, narrowly linear, pale green, margin revolute, veins obscure, Dehradun, Garhwal, West Bengal). midrib raised abaxially, rare with altitudinal range 2200- 4000 m. MIR et al. – Pterydophytes of Shopian, Kashmir Valley 31
Distribution: India (West Himalaya). sessile, pinnules linear-oblong, incised into small round Specimen examined: Aharbal (SAM 895), 06/09/2011, bead-like segments, occasional with altitudinal range of 2500 m. 1700-2500 m. Pteridaceae E. D. M. Kirchn. Distribution: Afghanistan, Asia, Europe, Iran, Italia, 10. Adiantum capillus-veneris L., Sp. Pl. 2: 1096 Pakistan, Persia, Turkey, Tibet, India (Kashmir Himachal (1753). Pradesh). Synonym: Adiantum formosum R. Br.; A. michelii H. Specimen examined: Lahanthoor (SAM 887) Christ; A. modestum Underw.; A. remyanum Esp. Bustos; 15/08/2011, 2000 m. A. schaffneri E. Fourn.; A. wattii Baker 14. Coniogramme affinis Wall ex Hieron. Hedwigia, Lithophytic medium size fern occurring on moist walls 57: 279 (1916). and rocks, rhizome long-creeping, stipe castaneous black, Synonym: C. affinis var. pilosa H. S. Kung; C. polished, pinnules or ultimate lobes fan shaped or rhombic, argutiserrata Ching & K. H. Shing. Grammitis affinis sori covered with false, yellow or yellowish brown, Wall.; Gymnogramma affinis C. Presl; G. javanica sensu narrowly reniform or orbicular- reniform indusia, Hook.; Syngramme fraxinea (D. Don) Bedd. occasional with altitudinal range of 1700-2800 m. Terrestrial, medium size fern naturally growing in Distribution: China, Japan, Vietnam, widely distributed rocky meadows, rhizome long-creeping, scaly, lamina in temperate and tropical regions in Africa, America, Asia, thinly herbaceous, pinnae linear to lanceolate, base sub- Europe, Oceania, India (throughout India). cunate to rotundate, margin with sharp teeth, Sori Specimen examined: Munad SAM (841), 14/07/2011, exindusiate extending from costa up to near margin, 1760 m; Zainapora SAM (943), 20/08/2012, 1630 m. frequently distributed from 2000- 3500 m altitude. 11. Adiantum pedatum L. Sp. Pl. 2: 1095 (1753). Distribution: China, Myanmar, Nepal, Tibet, India Synonym: Adiantum boreale C. Presl; A. pedatum var. (Jammu and Kashmir, Himachal Pradesh, Garhwal, aleuticum Rupr.; A. pedatum subsp. aleuticum (Rupr.) Kumaun, Meghalaya). Calder & Roy L. Taylor; A. pedatum f. billingsae Kittr.; A. Specimen examined: Secjan (SAM 891), 16/09/2011, pedatum var. glaucinum C. Chr.; A. pedatum var. 2500 m; Kund (SAM 924), 02/09/202, 2050 m; Kongwatan kamtschaticum Rupr.; A. pedatum f. laciniatum Weath. (SAM 941), 20/10/2012, 2360 m. Lithophytic medium sized fern growing on moist, cool, 14. Cryptogramma brunoniana Wall. ex Hook. & shaded areas, fronds clustered, herb green, fan shaped, Grev. Icon. Fil: t. 158 (1829) dichotomously branching from end of the stipe, with 4-6 Synonym: Cryptogramma crispa Bedd.; C. crispa var. lateral pinnae, veins multi-dichotomously forked, rare from brunoniana (Wall. ex Hook. & Grev.) Hook. & Baker; C. 1750-3000 m altitude among rocky seeps. crispa f. indica Hook.; Phorolobus brunonianus (Wall. ex Distribution: Bhutan, Canada, China, Japan, Korea, Hook. & Grev.) Fee; C. emeiensis Ching & K. H. Shing; C. Nepal, North America, India (Jammu and Kashmir, shensiensis Ching. Himachal Pradesh, Garhwal, Kumaun, Sikkim). Lithophytic small size plants occurring at higher Specimen examined: Secjan (SAM 898), 09/09/2011, altitudes in rock crevices or under rocks in areas with late- 2520 m; Kund (SAM 946), 14/08/2012, 2260 m. lying snow, fronds dimorphic; sterile tufted, many and 12. Adiantum venustum D. Don, Prod. Fil. Nepal 17 short, fertile fronds one or two with longer stipes, (1825). occasional with altitudinal range of 3000-4000 m. Synonym: Adiantum fimbriatum, A. venustum var. Distribution: Afghanistan, Bhutan, China, Japan, Nepal, wuliangense Ching & Y. X. Lin. Pakistan, Siberia, Taiwan, India (Kashmir, Himachal Terrestrial or lithophytic growing on moist shady Pradesh, Garhwal, Kumaun, Sikkim, Andaman & Nicobar). humus rich but well drained soils, rock crevices, stipes Specimen examined: Dubjan (SAM 863), 10/07/2011, dark-purple to nearly black, glossy, lamina triangular, light- 3560 m, Huran (SAM 915), 12/08/2012, 3220 m. green, pinnules wedge shaped, margin regularly toothed, 16. Cryptogramma stelleri (S. G. Gmel.) Prantl in Bot. fertile lobes with 2-3 notches, each notch bearing a sorus, Jahrb. Syst. 3: 413 (1882). abundant having wide altitudinal range from 2000-3300 m. Synonym: Allosorus gracilis (Michx.) C. Presl; A. Distribution: Afghanistan, Bhutan, Myanmar, Nepal, minutus Turcz. ex Trautv.; A. stelleri (S.G. Gmel.) Rupr.; Pakistan, Tibet, China, India (Jammu and Kashmir, Cheilanthes gracilis (Michx.) Kaulf.; Pellaea gracilis Himachal Pradesh, Garhwal, Arunachal Pradesh, West (Michx.) Hook.; P. stelleri (S.G. Gmel.) Baker; Pteris Bengal, Assam, Meghalaya, Uttar Pradesh). gracilis Michx.; P. stelleri S.G. Gmel. Specimen examined: Aharbal (SAM 805), 14/07/2011, Lithophytic high altitudinal small size fern grows on 1900 m; Dubjan (SAM 838), 28/08/20111, 3410 m; cool moist and shady calcareous rocks, rock lodges and Heerpur (SAM 892), 02/09/2011, 2420 m. cliffs, fronds remote, dimorphic, sterile shorter than fertile 13. Cheilanthes persica (Bory) Mett. ex Kuhn, Fil. Afr. ones, sori elongate, submarginal indusiate, indusium false, 73 (1868). pale-green, occasional from 2700-4000 m altitude. Synonym: Notholaena persica Bory; Cheilanthes Distribution: Afghanistan, China, Japan, Nepal, Russia, szovitsii Fish. & Meyer North America, India (Kashmir, Kumaun). Lithophytic small size fern occurring in rock crevices, Specimen examined: Dubjan (SAM 867); 10/07/2011; fronds clustered, stipe erect, ebenous, shiny, hairy, lamina 3550 m. Huran (914), 12/08/2012, 3120 m. with abaxial dense white hairs, pinnae triangular to deltate, 32 BIODIVERSITAS 16 (1): 27-43, April 2015
17. Onychium contiguum Wall. ex Hope, Journ. backwards, fertile fronds with longer and stronger stipes, Bombay Nat. Hist. Soc., 13: 444 (1901). lamina imparipinnate, herbaceous-sub-coriaceous, pinnae Synonym: Cheilanthes contiguum Wall.; Onychium lanceolate, margin spinulose-serrate, sori continuous, sub- cryptogrammoides H. Christ; O. japonicum var. intermedia marginal covered by false indusium of reflexed pinnae C. B. Clarke; O. japonicum var. multisecta C.B. Clarke margin, common from 1800-3000 m altitude. Terrestrial medium size fern growing in open rocky Distribution: Afghanistan, Australia, Africa, Europe, meadows along stream banks, stipe long, base black, straw Iran, Bhutan, Burma, China, Nepal, Sri Lanka, Pakistan, colored distally, lamina finely dissected 4 pinnate- Philippines, Korea, Taiwan, Thailand, Japan, India pinnatifid or more; sterile ultimate lobes linear with acute (Kashmir, Himachal Pradesh, Garhwal, Kumaun, West apex, entire margin, fertile ultimate lobes broader than Bengal, Assam, Nagaland, Madhya Pradesh, Tamil Nadu, sterile ones, frequent with altitudinal range of 1800-2700 m Kerala). altitude. Specimen examined: Secjan (SAM 830), 15/07/2011, Distribution: Bhutan, China, Cambodia, Laos, 2400 m; Aharbal (SAM 913), 17/08/2012, 2270 m; Myanmar, Nepal, Thailand, Vietnam, Pakistan, Taiwan, Heerpur (SAM 942), 29/09/2012, 2520 m. Tibet, India (Jammu and Kashmir, Himachal Pradesh, 21. Pteris stenophylla Wall. ex Hook. et Grev., Icon. Garhwal, Sikkim, West Bengal). Filic., t. 130 (1829). Specimen examined: Secjan (SAM 822), 15/07/2011, Synonym: Pteris cretica L. var. stenophylla (Wall. ex 2430 m; Aharbal (SAM 831), 19/07/2011, 2340 m; Hook. & Grev.) Baker; P. digitata Wall.; P. pellucid C. Kongwatan (SAM 871), 13/09/2011, 2360 m. Presl. var. stenophylla (Wall. ex Hook. & Grev.) C. B. 18. Onychium japonicum (Thunb.) Kunze Bot. Zeitung Clarke. (Berlin) 6: 507 (1848). Terrestrial fern growing amongst dry rocks in open Synonym: Caenopteris japonica (Thunb.) Thunb.; forests, pinnae 3-5 clustered at stipe apex, fronds Cryptogramma japonica (Thunb.) Prantl; Trichomanes dimorphic, apex of sterile pinnae small and coarsely japonicum Thunb. dentate-serrate, fertile pinnae longer and narrower than Medium size fern growing on open rocky meadows sterile, rare with altitudinal range of 2500-3000 m. near streams, rhizome long-creeping, branched, fronds Distribution: Bhutan, Nepal, Philippines, India (Jammu slightly dimorphic (fertile fronds more coarsely divided and Kashmir, Himachal Pradesh, Garhwal, Sikkim, West than sterile), stipes similar in length or shorter than the Bengal, Dehra Dun). lamina, lamina 3-4 pinnate, deltate-oblong, olive-green, Specimen examined: Kellar (SAM 820); 28/08/2011; papery when dry, rarely occurring from 1700-2500 m 2230 m. altitude. Distribution: Bhutan, China, Indonesia, Japan, Korea, Dennstaedtiaceae Lotsy Myanmar, Nepal, Pakistan, Philippines, Thailand, Vietnam; 22. Pteridium revolutum (Blume) Nakai, Bot. Mag. Pacific islands, India (Jammu and Kashmir, Himachal (Tokyo) 39: 109 (1925). Pradesh, Uttarakhand, West Bengal, Meghalaya, Assam, (Previously mis-identified as Pteridium aquilinum (L.) Nagaland). Kuhn., Bot. Ost-Afrika 3: 11 (1879). Specimen examined: Kund (SAM 909), 27/09/2012, Synonym: Pteridium aquilinum subsp. wightianum (J. 2300 m. Agardh) W.C. Shieh; Pteridium aquilinum var. wightianum 19. Pellaea nitidula Wall. ex Hope, Journ. Bombay (J. Agardh) R.M. Tryon; Pteridium capense var. densa Nat. Hist. Soc., 13: 444 (1901). Nakai; Pteris recurvata var. wightiana J. Agardh; Pteris Synonym: Allosorus nitidulus C. Presl; Cheilanthes revoluta Blume. nitidula Hook.; Mildella henryi (H. Christ) Hall & Terrestrial large fern grows in open, sunny slopes, Lellinger; Pellaea henryi H. Christ; P. nitidula Wall. ex forest floor and edges, rhizome subterranean, lamina hairy, Hope; Pteris nitidula Wall. nectaries on the underside at the base of pinnae and costae, Small terrestrial fern growing amongst large boulders, sori continuous along margins, covered with double stipes dark-brown, shinny, covered with reddish-brown indusium, outer made of reflexed margin, inner obsolete, hairs, lamina brownish-green, ultimate segments linear to membranous, common with altitudinal range of 1800-2700 lanceolate, simple, indusiate false, continuous, brown, m. membranous with irregularly dentate margin, rare with Distribution: North-Australia, tropical and subtropical altitudinal range from 1700-2500 m. regions of Asia including Bangladesh, Bhutan, China, Distribution: China, Nepal, Pakistan, Taiwan, Tibet, Taiwan, Indonesia, Malaysia, Philippines, Thailand, Viet India (Kashmir, Himachal Pradesh, Garhwal, Kumaun). Nam, Nepal, Pakistan, Sri Lanka, India (Himachal Pradesh, Specimen examined: Kund (SAM 905), 20/17/2011, Jammu and Kashmir, Kumaun, Assam, Meghalaya, Tamil 2017 m. Nadu, Kerala, Sikkim, Arunachal Pradesh, Manipur). 20. Pteris cretica L., Mant. Pl. 1: 130 (1767). Specimen examined: Aharbal (SAM 814), 05/06/2011, Synonym: Pteris serraria Sw.; P. treacheriana Baker; 2225 m; Secjan (SAM 832), 14/07/2011, 2400 m; Heerpur P. trifoliata Fee.; P. triphylla M. Martens & Galeotti; P. (SAM 930), 05/09/2012, 2540 m. nervosa thumb.; Pycnodoria cretica (L.) Small. 23. Hypolepis polypodioides (Blume) Hook., Sp. Fil. 2: Commonly occur in open rocky meadows having 63 (1852). dimorphic fronds, sterile fronds usually small and bending Synonym: Cheilanthes polypodioides Blume MIR et al. – Pterydophytes of Shopian, Kashmir Valley 33
Large fern occurring on wet sandy slopes and open 26. Pseudophegopteris pyrrhorachis (Kunze) Ching, rocky areas near streams, rhizome long-creeping, hairy, subsp. distans (Mett.) Fraser-Jenk., New Sp. Synder. stipes very long 50 cm or more, eglandular hairy, lamina Indian Pterid.: 214 (1997) (Figure 3). hairy on both surfaces, sori exindusiate, round, Synonym: Phegopteris distans (D. Don) Mett. intramarginal, partially protected by marginal reflexed Large fern growing in rocky meadows alongside teeth, rare growing from 1650-2200 m altitude. streams, rhizome thin, long-creeping, stipe base red Distribution: Bangladesh, Burma, China, Indonesia, castaneous, hairy, rachis blackish-brown, densely hairy, Laos, Malaysia, Myanmar, Nepal, Philippines, Taiwan, lamina abaxially hairy, pinnules narrow, lanceolate, rare Thailand, Vietnam, India (Arunachal Pradesh, Himachal from 2000-2800 m altitude. Pradesh, Manipur, Sikkim, South India, Uttar Pradesh, Distribution: China, Malaysia, Philippines, Taiwan, Uttarakhand). Polynesia, Sri Lanka, Vietnam, India (Jammu and Kashmir, Specimen examined: Kund (SAM 907), 27/09/2011; Himachal Pradesh, Uttarakhand, Sikkim, Darjeeling hills, 2025 m. south India). Specimen examined: Secjan (SAM 897), 15/09/2012, Thelypteridaceae Pichi Sermolli 2450. 24. Phegopteris connectilis (Michx.) Watt., Canad. 27. Pseudophegopteris pyrrhorachis (Kunze) Ching, Nat. 29 (1866). subsp. laterepens (Trotter in Hope) Fraser-Jenk.; New Sp. Synonym: Aspidium Phegopteris (L.) Baumg.; Synder. Indian Pterid. 215 (1997). Dryopteris phegopteris (L.) C. Chr.; Gymnocarpium Synonym: Polypodium Laterepens Trotter in Hope; phegopteris (L.) Newman; Lastrea phegopteris (L.) Bory; Dryopteris Laterepens (Trotter) C. Chr.; Thelypteris Nephrodium phegopteris (L.) Prantl; N. phegopteris (L.) laterepens (Trotter) R. Stewart. Baumg. ex Diels; Phegopteris phegopteris (L.) Keyserl.; P. Very large fern occurring in forest under-stories near vulgaris Mett.; P. polypodioides Fee; Polypodium streams, rhizome shot-creeping, thick, stipe long with connectile Michx.; P. phegopteris L.; Polystichum sparse scales, rachis stramineous, hairy, lower pinnae phegopteris (L.) Roth; Thelypteris phegopteris (L.) Sloss. distant, pinnules wide, deeply lobed, occasional from 2000- ex Rydb. 2700 m altitude. Medium size fern growing on cool moist cliffs and Distribution: Pakistan, India (Kashmir). woods along stream banks, rhizome black, stipe clothed Specimen examined: Kund (SAM 925), 10/09/2012, with unicellular white hairs, rachis winged, lamina 2400 m. triangular, hairy, hairs transparent, needle-like, pinnae 28. Cyclosorus erubescens (Wall. ex Hook.) C. M. adnate to the rachis, lowest pair drooping down and out, Kuo, Taiwania 47: 171 (2002). frequent with distributional range from 2700-3100 m Synonym: Asplenium glanduliferum Wall., nom. nud.; altitude. Christella erubescens (Wall. ex Hook.) H. Leveille; Distribution: China, Caucasus, Europe, Japan, Siberia, Dryopteris braineoides (Baker) C. Chr.; D. erubescens Pakistan, India (Kashmir, Himachal Pradesh, Garhwal, (Wall. ex Hook.) C. Chr.; Glaphyropteridopsis erubescens Uttar Pradesh, Kumaun, Sikkim). (Wall. ex Hook.) Ching; Glaphyropteris erubescens (Wall. Specimen examined: Dubjan (SAM 834), 27/07/2011, ex Hook.) Fee; Lastrea erubescens (Wall. ex Hook.) 3000 m; Kund (SAM 877), 07/09/2011, 2450 m. Copeland; Nephrodium braineoides Diels; N. erubescens 25. Pseudophegopteris levingei (C.B. Clarke) Ching, Diels; Phegopteris erubescens (Wall. ex Hook.) J. Sm.; Acta Phytotax. Sin. 8: 314 (1963). Polypodium braineoides Baker; P. erubescens Wall. ex Synonym: D. levingei (C. B. Clarke) C. Chr.; D. Hook.; Thelypteris erubescens (Wall. ex Hook.) Ching. purdomii C. Chr.; Gymnogramma aurita var. levingei C. B. Terrestrial large fern growing amongst boulders along Clarke; G. levingei (C. B. Clarke) Baker; Leptogramma stream banks, rhizomes erect, woody, stipe ribbed, rachis aurita var. levingei (C. B. Clarke) Bedd.; L. levingei (C. B. rectangular abaxially hairy, basal pinnae deflexed and Clarke) Bedd.; Phegopteris levingei (C. B. Clarke) forward, margin lobed, basal pair of lobes touching the Tagawa; Thelypteris levingei (C. B. Clarke) Ching; Lastrea corresponding lobes above and below; rare from 2000- levingei (C.B. Clarke) Copel. 3600 m altitude. Medium size fern growing along streams in thickets, Distribution: Bhutan, China, Indonesia, Malaysia, forests amongst boulders, rhizome thin, fronds remote, Taiwan, Japan, Myanmar, Nepal, Pakistan, Philippines, green, delicate, lamina lanceolate or oblong-lanceolate, Vietnam, India (Jammu and Kashmir, Himachal Pradesh, herbaceous, base gradually tapering, apex acuminate, Uttarakhand, Kumaun, Sikkim, West Bengal, Meghalaya, pinnae sessile, alternate, common from 2100-3000 m Tamil Nadu). altitude. Specimen examined: Kund (SAM 906), 27/09/2011, Distribution: Afghanistan, Bhutan, China, Pakistan, 2050 m. Tibet, India (Jammu and Kashmir, Himachal Pradesh, Uttarakhand, Sikkim, Darjeeling hills). Aspleniaceae Newman Specimen examined: Dubjan (SAM 807), 16/06/2011, 29. Asplenium adiantum-nigrum L. Sp. Pl. 2: 1081 1950 m; Aharbal (SAM 828), 01/07/2011, 2180 m; (1753). Heerpur (SAM 853), 11/07/2011, 2550 m. Synonym: Asplenium andrewsii A. Nelson; A. chihuahuense J. G. Baker; A. dubiosum Davenport 34 BIODIVERSITAS 16 (1): 27-43, April 2015
Lithophytic medium size fern growing on rocky woods, 33. Asplenium kukkonenii Viane & Reichstein, hedge banks, shady walls and rocks bearing evergreen Pteridol. New Mellenium, 18 (2003). fronds, stipes clustered, lustrous, lamina 2-3 pinnate, dark- Very small fern grows on moist shady rocks on forest green, glossy, thick, coriaceous, margins acutely dentate to floor, lamina broadest below the middle, apex acute, serrate, frequent with distributional range of 1700-3000 m bipinnate at base, pinnae triangular-ovate, pinnules rounded altitude. with acute teeth, lowest acroscopic pinnule the largest, rare Distribution: Africa, Afghanistan, Europe, Japan, Iran, with 2100-3300 m. Java, Nepal, Taiwan, Turkey, Pakistan, North America, Distribution: Nepal, India (Jammu and Kashmir, India (Kashmir, Himachal Pradesh, Garhwal, Kumaun). Himachal Pradesh, Uttar Pradesh). Specimen examined: Secjan (SAM 815), 25/06/2011, Specimen examined: Aharbal (SAM 886), 37/08/2011, 2600 m; Kellar (SAM 854), 16/08/2011, 2150 m. Narwani 2600 m. (SAM 889), 19/09/2011, 1720 m. 34. Asplenium pseudofontanum Kossinsky, Notulae 30. Asplenium x alternifolium Wulfen, Jacq. Misc. Syst. Hort. Bot. Petrop. 3: 122 (1922). Austr. Bot. 2: 51 (1781). Synonym: Athyrium fontanum (L.) Roth; A. halleri Synonym: Asplenium x breynii Retz; Asplenium x Roth.; Aspidium fontanum (L.) Sw.; A. halleri (Roth) germanicum Hope Willd.; Asplenium fontanum (L.) Bernh. subsp. Small lithophytic fern growing among rock crevices, a pseudofontanum; A. lanceolatum subsp. fontanum (L.) P. cross product of Asplenium septentrionale and A. Fourn.; A. halleri (Roth) DC.; A. leptophyllum Lag. trichomanes, lamina pinnate, up to 2x1 cm, lanceolate, Lithophytic small ferns commonly occur in rock pinnae alternate, petiolate, oblanceolate-cuneiform, base crevices in forests, fronds clustered, evergreen, lamina cunate, apex toothed; sori indusiate, linear, rare from 2200- finely dissected, widest above the middle, narrowed 3300 m altitude. towards the both ends, rare with distributional range of Distribution: Europe, India (Kashmir, Himachal 1800-3000 m altitude. Pradesh). Distribution: Afghanistan, Pakistan, India (Jammu and Specimen examined: Huran (SAM 869), 14/08/2011, Kashmir, Himachal Pradesh, Kumaun, Garhwal, West 3100 m. Bengal). 31. Asplenium ceterach L., Sp. Pl. 2: 1080 (1753) Specimen examined: Aharbal (SAM 810), 11/07/2011, Synonym: Asplenium ceterach L; Ceterach officinarum 2350 m, Secjan (SAM 829), 21/07/2011, 2400 m; Willd.; Scolopendrium ceterach Symons; Vittaria ceterach Kongwatan (SAM 899), 14/09/2011, 2650 m. Bernh.; Grammitis ceterach Sw.; Gymnogramme ceterach 35. Asplenium punjabense Bir, Fraser-Jenk. & Lovis, Spring; Hemidictyum ceterach (L.) Bedd. Fern Gaz. 13: 53-63 (1985) (Figure 2) Small lithophytic fern growing in relatively dry Lithophytic fern growing in open rocky meadows, conditions, stipes short, brown, densely covered with lamina brownish-green, thick, nearly pinnate with deep brown, concolorous scales, lamina leathery, abaxially deep rounded grooves, adaxially glabrous, abaxially scaly, scales green, glabrous and adaxially dense scaly, margin slightly not dense, sori with rudimentary indusia, rare from 1650- bending upwards revealing the scales, alternately lobed, 2100 m altitude. frequent from 1700-2600 m altitude. Distribution: Afghanistan, Pakistan, India (Himachal Distribution: Afghanistan, Australia, Brazil, Scotland, Pradesh, Jammu and Kashmir). Siberia, Tibet, Ireland, Pakistan, Africa, Europe, India Specimen examined: Kund (SAM 903), 24/09/2012; (Kashmir, Himachal Pradesh, Uttarakhand). 2020 m. Specimen examined: Kund (SAM 896), 27/09/2011, 36. Asplenium ruta-muraria L. Sp. Pl. 2: 1081 (1753) 1930 m. Synonym: Acrostichum ruta-muraria Lam.; Phyllitis 32. Asplenium dalhousiae Hook. Icon. Pl. 2: pl. 105 ruta-muraria Moench; Amesium ruta-muraria Newmann; (1837). Tarachia ruta-muraria C. Presl; Asplenium murale Bernh.; Synonym: Asplenium alternans Wall.; A. rupium A. cryptolepis Fernald; A. cryptolepis Fernald var. ohionis Goodd.; Ceterach alternans Kuhn; Ceterach dalhousiae Fernald; A. ruta-muraria var. cryptolepis (Fernald) (Hook.) C. Chr. Wherry. Terrestrial small fern occurring in rocky meadows, stipe Small lithophytic fern growing in open sites in rick brown, indumenta of scales throughout, lamina deeply crevices, pinnae imparipinnate triangular, pinnules lateral, pinnatifid, subcoriaceous, gradually narrowed towards obovate or rhomboid, apex sub-rounded, margins base, lobes alternate, spreading, lower distant, rare from irregularly sharp dentate, base cuneate, sori born along 1700-2700 m. veins, rare from 2000-4000 m altitude. Distribution: Afghanistan, Africa, Bhutan, Ethiopia, Distribution: Afghanistan, China, Iran, Japan, Nepal, Pakistan, Africa, North America, India (Jammu and Kazakhstan, Korea, Nepal, Pakistan, Russia, Tajikistan; Kashmir, Himachal Pradesh, Garhwal, Arunachal Pradesh, NW Africa, SW Asia, Europe, North America, India Kumaun, Sikkim, West Bengal, Meghalaya, Manipur, (Kashmir, Kumaun, Arunachal Pradesh). Rajasthan). Specimen examined: Secjan (SAM 855), 20/08/2011, Specimen examined: Kund (SAM 904), 27/09/2012, 2400 m; Dubjan (SAM 888), 06/09/2011. 1900 m. Zainapora (SAM 931), 15/05/2012, 1630 m. 37. Asplenium septentrionale (L.) Hoffman, Deutschl. Fl. 2: 12 (1795). MIR et al. – Pterydophytes of Shopian, Kashmir Valley 35
Synonym: Acrostichum septentrionale L.; Amesium Distribution: Afghanistan, Bhutan, Burma, China, sasaki Hayata; Scolopendrium septentroinal Reth; Belvisia Hawaii, Japan, Korea, Sri Lanka, Philippines, Nepal, septentrionalis Mirb.; Acropteris septentrioonalis Link; Vietnam, Africa, Taiwan, Thailand, India (Kashmir, Blahnum septentrionale Wall.; Amesium septentrionale Himachal Pradesh, Uttarakhand, Sikkim, West Bengal, Newm.; Asplenium septentrional var. sasakii (Hayata) C. Assam, Meghalaya, Tamil Nadu). Chr. Specimen examined: Aharbal (SAM 923), 05/09/2012, Lithophytic fern grows higher altitudes in open sites in 2190 m. rocks crevices and cliffs in light forest; rhizome much 41. Asplenium viride Hudson, Fl. Angl. 385 (1762). branched to produce dense many stemmed, tufts or mats Synonym: Asplenium ramosum L.; A. trichomanes- bearing numerous crowded leaves, lamina dichotomously 2 ramosum L. or 3 partite, sori confluent at maturity covering the entire High altitudinal fern that grows on limestone rock surface, frequent from 2200-3500 m altitude. crevices, fronds evergreen, stipe reddish-brown at base, Distribution: Afghanistan, China, Kazakhstan, green distally, lustrous, shallowly grooved on abaxial Kyrgyzstan, W Mongolia, Nepal, Pakistan, Russia, surface, rare from 2800-4200 m altitude. Tajikistan; Africa, Europe, North America, India (Kashmir, Distribution: Afghanistan, Japan, Nepal, Pakistan, Himachal Pradesh, Garhwal, Kumaun, Shimla). Russia, Europe, North America, India (Jammu and Specimen examined: Aharbal (SAM 811), 10/07/2011, Kashmir, Himachal Pradesh, Uttar Pradesh). 2400 m; Secjan (SAM 823), 28/07/2011, 2350 m; Dubjan Specimen examined: Kaunsernag (SAM 921), (SAM 843), 11/08/2011, 2800 m. 28/08/2012, 3500 m. 38. Asplenium tenuicaule Hayata, Icon. Pl. Formosan. 4: 228 (1914). Woodsiaceae Herter Synonym: Gymnogramma fauriei Christ, Asplenium 42. Athyrium atkinsonii Bedd. Ferns Brit. Ind., Suppl. subvarians Ching, A. shiobarensse Koidz 11. t. 359 (1876). Small fern growing on moist shady rocks on forest Synonym: Aspidium senanense Franch. & Sav.; floor, lamina bipinnate, 1 cm broad, oblong-lanceolate, Asplenium atkinsonii (Bedd.) C.B. Clarke; A. lastreoides pinnules alternate, born on thin delicate stalks, fan shaped Baker; Athyrium lastreoides (Baker) Diels; A. microsorum to rounded-ovate, rare with altitudinal range from 2000- Makino; A. monticola Rosenst.; A. senanense (Franch. & 3600 m. Sav.) Koidz. & Tagawa; Cystopteris grandis C. Chr. in H. Distribution: Bhutan, China, Japan, Korea, Nepal, Lev.; Davallia athyriifolia Baker; Dryopteris senanensis Pakistan, Philippines, Russia, Thailand; Africa, Pacific (Franch. & Sav.) C. Chr.; Pseudocystopteris atkinsonii islands (Hawaii) India (Kashmir, Himachal Pradesh, (Bedd.) Ching Garhwal, Kumaun). Middle size fern commonly grows on moist areas above Specimen examined: Aharbal (SAM 922), 05/09/2012, tree line, Fronds single, lamina 3-pinnate-pinnatifid, 2600 m. broadly ovate or triangular, shortly acuminate or almost 39. Asplenium trichomanes L. Sp. Pl. 2: 1080 (1753). acute; pinnae distant, petiolate; frequent from 2500-3500 m Synonym: Asplenium melanocaulon Will.; A. altitude. trichomanoides Houtt.; A. minus Bl.; A. pusillum Bl.; A. Distribution: Bhutan, Burma China, Taiwan, Nepal, densum Brack.; A. melaolepis Col. Chamaefilix Japan, Pakistan, Tibet, Taiwan, Korea India (Kashmir, trichomanes (L.) Farw. Trichomanes crenatm Gilib.; Himachal Pradesh, Uttarakhand, Sikkim, Darjeeling hills, Pylilitis rotundifolia Moench. Arunachal Pradesh). Lithophytic fern occurring in open moist areas, fronds Specimen examined: Dubjan (SAM 875), 23/07/2011, clustered, evergreen, stipes brown- black to coppery, 3200 m. lustrous, brittle, lamina deep green, linear, abundant from 43. Athyrium attenuatum (Wall. ex C. B. Clarke) 1650-3200 m altitude. Tagawa, Acta. Phytotax. Geobot. 16: 177 (1956). Distribution: worldwide in all temperate zones, in Synonym: Asplenium filix-femina (L.) Bernh. var. tropics on high mountains, India (Kashmir, Himachal attenuatum Wallich ex C. B. Clarke, Athyrium contigens Pradesh, Uttarakhand, Uttar Pradesh, Sikkim, Assam, Ching & Wu. Meghalaya, Arunachal Pradesh, Manipur, Rajasthan, Tamil Terrestrial large fern growing on meadows and gentle Nadu). mountain slopes, rhizome short-erect, covered with Specimen examined: Aharbal (SAM 808); 25/06/2011; persistent leaf bases, stipe upward, stramineous, rachis 2250 m; Secjan (SAM 839), 22/08/2011, 2400 m; Narwani succulent, sparsely scaly, lamina tapering at both ends, (SAM 872), 28/09/2011, 1780 m. pinnae higher up congested, pinnule margin serrate, 40. Asplenium varians Wall. ex Hook. & Grev. con. common from 2200-3500 m altitude. Filic. 2: 172 (1830). Distribution: Afghanistan, Bhutan, China, Nepal, Synonym: Asplenium lankongense Ching Pakistan, India (Jammu and Kashmir, Himachal Pradesh, Small fern grows on moss covered shady rocks on Uttarakhand). forest floor, fronds erect or arching, lamina bipinnate, Specimen examined: Aharbal (SAM 826), 15/06/2011, lanceolate, pinnae extremely short stalked, triangular-ovate, 2400 m; Secjan (SAM 835), 27/06/2011, 2300 m; Dubjan pinnules obovate, sharply dentate on the outer margin, rare (SAM 900), 27/08/2012, 3460 m; Huran (SAM 932), with altitudinal range of 1700-2900 m. 19/09/2012, 3340 m. 36 BIODIVERSITAS 16 (1): 27-43, April 2015
44. Athyrium distans (D. Don.) T. Moore, Index Filic.: pinnules round, margin serrate, duplicato-dentate, teeth 152 (1859). triangular, common from 3300-4600 m altitude. Synonym: Asplenium distans D. Don., Athyrium Distribution: Bhutan, Myanmar, Nepal, Pakistan, India imbricatum Christ, A. fangii Ching, A. sikkimense Ching; (Kashmir, Himachal Pradesh, Dehra Dun, Garhwal, A. decorum Ching; A. nanyueense Ching in Ching & Hsieh Kumaun, Sikkim, Arunachal Pradesh). Medium size fern grows on forest floor near water, Specimen examined: Dubjan (SAM 836), 16/08/2011, rhizomes apex densely scaly, stipes long, purplish red to 3500 m; Huran (SAM 890), 10/08/2012, 3360 m. greenish stramineous, lamina 2-pinnate-pinnatisect, grass- 48. Cystopteris dickieana R. Sim, Gard. Farmers J. 2: green, widest just above the base, pinnules distant, base 308 (1848). asymmetrical, occasional from 1700-2500 m altitude. Synonym: Cystopteris fragilis (L.) Bernh. f. granulos Distribution: China, Nepal, Japan, India (Kashmir, Bir & Trikha; C. fragilis (L.) Bernh. subsp. dickieana Himachal Pradesh, Uttarakhand, Sikkim, Darjeeling hills, (Sim) Hook.; C. fragilis (L.) Bernh. var. dickieana (Sim) T. Meghalaya). Moore; C. sikkimensis Ching ex Bir Specimen examined: Aharbal (SAM 874), 18/07/2011, Distribution: Afghanistan, China, Nepal, Pakistan, 2200 m. Japan, Iran, Africa, Europe, North America, Pakistan, 45. Athyrium mackinnonii (Hope) C. Chr., Index Filic. Taiwan, India (Jammu and Kashmir, Himachal Pradesh, Fasc. 3: 143 (1905). Uttarakhand). Synonym: Asplenium mackinnonii Hope, Athyrium Small fern growing in open slopes, forest floors and nigrips sensu Bedd., A. caudipinnum Ching edges of forests, rhizome short- creeping, internodes beset Medium size fern grows on forest floor, rhizomes with old petiole bases, stipes fragile, sori indusiate, round, covered with persistent leaf bases, densely scaly; scales indusium forming a hood over the sorus, spore exine bicolorous, blackish-brown in central part, brown at rugose or verrucose, occasional with altitudinal range of margin, stipes pinkish, lamina pale green, pinnae lowest 1800-2800 m. pair deflexed and opposite, rest alternate, ascending, veins Specimen examined: Aharbal (SAM 806), 15/06/2011, visible on both surfaces, common from 1700-2700 m 2250 m; Secjan (SAM 852), 17/08/2011, 2350 m. altitude. 49. Cystopteris fragilis (L.) Bernh. Schrad. Neues J. Distribution: Afghanistan, Myanmar, Nepal, Pakistan, Bot. 1: 26 (1805). Thailand, Vietnam, India (Jammu and Kashmir, Himachal Synonym: Aspidium dentatum Sw.; A. fragile (L.) Sw.; Pradesh, Garhwal, Dehra Dun, Uttar Pradesh A. viridulum Desv.; A. dentatum (Sw.) Gray; A. fragile (L.) Specimen examined: D. K. Pora (SAM 802), Spreng.; A. fumarioides C. Presl; Cyathea anthriscifolia 10/06/2011, 1800 m; Aharbal (SAM 845), 10/07/2011, (Hoffm.) Roth; C. cynapifolia (Hoffm.) Roth; C. fragilis 2300 m; Heerpur (SAM 850), 15/07/2011, 2400 m. (L.) J. Sm.; Cystea angustata (Hoffm.) Sm.; C. dentata 46. Athyrium strigillosum (T. Moore ex E. J. Lowe) (Dicks.) Sm.; C. fragilis (L.) Sm.; Cystopteris acuta Fee.; Salomon, Nom. Gefasskrypt, 112 (1883). C. baenitzii Dorfl.; C. canariensis C. Presl.; C. dentata Synonym: Allantodia denticulate Wall.; Asplenium (Sw.) Desv. denticulatum Wall. ex. J. Sm.; A. setudosum Wall. ex. J. Morphologically similar to Cystopteris dickieana Sm.; A. strigillosum T. Moore ex E.J. Lowe; A. tenuifrons except in spore ornamentation, spore exine is echinate not Wall. ex Hope; Athyrium proliferum T. Moore; A. rugose or verrucose, common from 1800-2800 m altitude. viviparum Christ Distribution: Afghanistan, China, Nepal, Russia, Medium size fern growing on stream sides in valleys, Pakistan, Japan, Iran, Africa, Europe, North America, stipe stramineous, thin, lamina 2-pinnate, triangular- Pakistan, Taiwan, Korea India (Jammu and Kashmir, lanceolate, base hardly narrowed, apex acuminate, pinnules Himachal Pradesh, Uttarakhand, Nagaland ascending, approximate, apex toothed, margin lobed, lobes Specimen examined: Sedow (SAM 837), 05/08/2011, serrate-dentate, rare from 1700-2500 m. 2350, m; Aharbal (SAM 851), 25/08/2011, 2250 m; Distribution: Bhutan, Japan, Myanmar, Nepal, India Heerpur (SAM 865), 15/09/2011, 2400 m. (Kashmir). 50. Deparia acuta (Ching) Fraser-Jenk., New Sp. Specimen examined: Saangran (SAM 927), 20/08/2012, Syndrome Indian Pterid.: 104 (1997) 2150 m. Synonym: Lunathyrium acutum Ching 47. Athyrium wallichianum Ching. Bull. Fan Mem. Medium size fern growing in open rocky meadow and Inst. Biol., Bot. 8: 497 (1938). mountain slopes, rhizome short-erect, scaly at apex, scales Synonym: Aspidium brunonianum Wall.; A. red-brown, stipe and rachis densely hairy, lamina much brunonianum Wall. ex Mett.; Lastrea brunoniana Wall. ex reduced towards base, apex acuminate, pinnae sessile, C. Presl.; L. brunoniana (Wall. ex Mett.) Bedd. L. slightly ascending, frequent from 2300-3800 m altitude. brunoniana C. Presl; Dryopteris brunoniana (Wall. ex Distribution: China, Pakistan, India (Kashmir, Mett.) Kuntz; Nephrodium brunonianum (Wall. ex Mett.) Himachal Pradesh, Uttarakhand). Hook. Specimen examined: Secjan (SAM 842), 03/07/2011, Medium size growing in alpine shrub meadows, 2400 m; Huran (SAM 849), 10/08/2011, 2900 m. rhizome thick, black, covered with brown scales, fronds 51. Deparia allantodioides (Bedd.) M. Kato, J. Fac. green, clustered, rachis scaly and fibrillose, lamina thick, Sci. Univ. Tokyo, Sect. 3, Bot. 13: 393 (1984). abruptly narrowed at the apex, pinnae crowded, sessile, MIR et al. – Pterydophytes of Shopian, Kashmir Valley 37
Synonym: Asplenium thelypteroide sensu Clark, ex Nyland; Allantodia crenata (Sommerf) Ching; Athyrium allantodioides Bedd, A. thelypteroides sunsu Cystopteris crenata Fries; Dipazium sommerfeldtii Love & Bedd., Deparia sikkimensis (Ching) Nakaike & Malk, Love Lunathyrium allantodioides (Bedd.) Ching, L. mackinnonii Medium size fern growing on steep forest ravines, Ching, L. sikkimensis Ching rhizome slender, long-creeping, black, stipe longer than Large fern growing on forest floor with higher levels of lamina, lamina triangular, costae and veins below hairy; moisture, stipe brown, hairy, rachis fibrillose, hairy, pinnae basal sori paired back to back on the same vein, others alternate, sessile, lower pinnae reduced, sometimes up to singular; frequent with 2300-2800 m. auricles, deflexed downwards, deeply lobed, lobes Distribution: China, Japan, Korea, Russia, Europe, connected by a narrow wing, basal basiscopic pinnule Nepal, Siberia, India (Kashmir, Himachal Pradesh, outwards; common from 1900-3700 m altitude. Uttarakhand). Distribution: Bhutan, China, Nepal, Tibet, Pakistan, Specimen examined: Dubjan (SAM 885), 28/07/2011, India (Jammu and Kashmir, Himachal Pradesh, 2600 m. Uttarakhand, Sikkim, Arunachal Pradesh, West Bengal). 55. Gymnocarpium dryopteris (L.) Newman, Specimen examined: Aharbal (SAM 812), 25/06/2011, Phytologist 4: 371 (1851). 2450 m; Dubjan (SAM 819); 12/08/2011, 2500 m; Secjan Synonym: Aspidium dryopteris (L.) Baumgarten; (SAM 934), 25/09/2012, 2400 m. Carpogymnia dryopteris (L.) A. Love & D. Love; 52. Deparia macdonellii (Bedd.) M. Kato, J. Fac. Sci. Currania dryopteris (L.) Wherry; Dryopteris dryopteris Univ. Tokyo, Sect. 3, Bot. 13: 391 (1984). Britton; D. pulchella (Salisb.) Hayek; D. linnaeana (L.) C. Synonym: Asplenium macdonellii Bedd.; Athyrium Chr.; D. pumila V.I. Krecz.; Filix pumila Gilib.; Lastrea macdonellii Bedd.; Cornopteris macdonellii (Bedd.) dryopteris (L.) Bory.; Nephrodium dryopteris (L.) Michx.; Tardieu; Deparia pterorachis (Christ) kato; Dryoathyrium Phegopteris dryopteris Fee; Polypodium dryopteris L.; P. macdonellii (Bedd.) Morton; Lunathyrium macdonellii pulchellum Salisb.; Polystichum dryopteris (L.) Roth; (Bedd.) Khullar; L. macdonellii (Bedd.) Ching Thelypteris dryopteris (L.) Sloss Very large fern growing on forest slopes along Medium size fern growing on damp areas and among streamlets, rhizome long-creeping, lamina basal pinnae rock crevices near moisture in forests, rhizomes long- triangular and opposite, deeply lobed near to the costa; creeping, black-brown, apex densely scaly, stipe base lobes connected by a very narrow wing, sinus wide and purplish, above stramineous, lamina pentagonal-ovate, cunate, apex rounded with sharp teeth, margin crenate- veins visible abaxially, sori exindusiate, frequent from serrate, occasional having altitudinal range of 1800-2700 m 2000-2900 m altitude. altitude. Distribution: Japan, China, Tibet, Nepal, Korea, Distribution: Japan, Pakistan, Japan, China, India Europe, North America, Pakistan, India (Jammu and (Kashmir, Himachal Pradesh). Kashmir, Himachal Pradesh, Uttarakhand, Sikkim). Specimen examined: Dubjan (SAM 911), 02/08/2012, Specimen examined: Aharbal (SAM 804), 23/06/2011, 2500 m. 2400 m; Kongwatan (SAM 816), 20/07/2011, 2450 m; 53. Diplazium maximum (D. Don) C. Chr. Index Filic. Heerpur (SAM 827); 12/08/2011, 2300 m fasc. 1: 235 (1905). 56. Woodsia alpine (Bolton) Gray, Nat. Arr. Brit. Pl. 2: Synonym: Allantodia maxima (D. Don) Ching; 17 (1821). Asplenium maximum D. Don; A. frondosum Wall.; Synonym: Acrostichum alpinum Bolton; Woodsia Diplazium flaccidum Christ; Diplazium giganteum (Bak.) alpina var. bellii G. Lawson; W. bellii (Lawson) A.E. Ching in C. Chr.; Gymnogramma gigantae Baker; Porsild; W. hyperboreum R. Br.; W. himalaica Ching & S. Diplazium frondosum (Clark) Christ.; Diplazium K.Wu.; W. ilvensis var. alpina Watt; W. ilvensis subsp. polymorphum Wall. ex Mett. alpina Asch. Terrestrial fern occurring amongst large boulders along Small fern occurring among rock crevices and screes at streamlets and ravines, rhizome ascending with dense loose high altitudes, rhizome compact with cluster of persistent scales at apex, scales brown or chestnut, frond large, up to stipe bases, stipe lustrous, fibrillose and hairy, lamina 180x90 cm, pinnules sessile, rounded apex, margin pinnate to pinnatifid, hairy along the margin, indusia hairy, shallowly crenate, sori linear, diplazoid, common from rare from 2500-3800 m altitude. 1800-2500 m altitude. Distribution: Afghanistan, Iran, Tibet, Europe, N Asia, Distribution: Bhutan, China, Myanmar, Nepal, Pakistan, India (Kashmir, Himachal Pradesh, Uttarakhand). Pakistan, Polynesia, Vietnam, India (Jammu and Kashmir, Specimen examined: Huran (SAM 868), 20/07/2011, Himachal Pradesh, Uttarakhand, Sikkim, West Bengal, 3200 m. Assam, Meghalaya). Specimen examined: Secjan (SAM 848), 05/08/2011, Dryopteridaceae Herter 2400 m; Kund (SAM 908), 20/08/2012, 2100 m; 57. Dryopteris barbigera (T. Moore ex Hook.) Kuntze, Kongwatan (SAM 947), 28/09/2012, 2450 m. Revis. Gen. Pl. 2: 812 (1891). 54. Diplazium sibiricum (Turcz. ex Kunze) Kurata in Synonym: Aspidium barbigerum (T. Moore ex Hook.) Namegata and Kurata Enum. Jap. Pterid. 292: 340 (1961). H. Christ; Dryopteris falconeri (Hook.) Kuntze; Lastrea Synonym: Asplenium sibiricum Turcz. ex Kunze; A. barbigera (Hook.) T. Moore ex Bedd.; L. falconeri (Hook.) crenatum Sommerf; Athyrium crenatum (Sommerf) Ruper Bedd.; Nephrodium barbigerum Hook.; N. falconeri Hook. 38 BIODIVERSITAS 16 (1): 27-43, April 2015
Terrestrial fern growing in birch forests, stipe, rachis Synonym: Aspidium depastum Schkuhr; A. erosum and lamina densely scaly and fibrillose; scales reddish- Schkuhr; A. expansum D. Dietr.; A. filix-mas (L.) Sw.; A. brown, lamina thickly herbaceous, pinnule lobes rounded mildeanum Gopp.; A. nemorale (Salisb.) Gray; A. opizii with serrate and prominent acute teeth, occasional from Wierzb.; A. umbilicatum (Poir.) Desv.; A. veselskii Hazsl. 2800-4700 m altitude. ex Domin; Dryopteris patagonica Diem; Filix-mas filix- Distribution: Bhutan, Pakistan, China, Tibet, Taiwan, mas Farwell; Lastrea filix-mas (L.) C. Presl; Nephrodium Nepal, India (Jammu and Kashmir, Himachal Pradesh, crenatum Stokes; N. filix-mas (L.) Rich.; Polypodium filix- Uttarakhand, Assam, Sikkim, West Bengal). mas L.; P. heleopteris Borkh.; P. nemorale Salisb.; P. Specimen examined: Peergali (SAM 918), 18/08/2012, umbilicatum Poir.; Polystichum filix-mas (L.) Roth; P. 3100 m; Dubjan (SAM 934), 16/09/2012. polysorum Tod.; Tectaria filix-mas Cav.; Thelypteris filix- 58. Dryopteris blanfordii subsp. blanfordii (Hope) C. mas Nieuwl. Chr.; Ind. Fil. 254 (1905). Terrestrial fern growing under shade near moisture, Synonym: Dryopteris gongboensis Ching; Nephrodium rhizome long-erect, stipe grooved, scaly and fibrillose, blanfordii Hope lamina pale to mid-green above, pinnae shortly petiolate, Terrestrial fern growing on forest floor, stipes with pinnules lobed, lobe ending in an acute tooth, sori crowded, dark-brown base, fibrillose and scaly, scales ovate to upper part of the lamina fertile, rare from 1700-3200 m lanceolate, brown, concolorous, glossy, margin fimbriate, altitude. lamina ca. 50x17 cm, pinnules slightly lobed or sometimes Distribution: Africa, China, Argentina, Afghanistan, without lobes, segment apex with 2-3 sharp serratures, Russia, Greenland, Malaya, Peru, Mexico, Kazakhstan, frequent from 1800-3500 m altitude. Pakistan, Russia, Iran, Jamaica, Europe, North America, Distribution: Afghanistan, China, Tibet, Pakistan, India (Kashmir, Uttarakhand). Nepal, India (Kashmir, Himachal Pradesh, Uttarakhand). Specimen examined: Narwani (SAM 879), 25/07/2011, Specimen examined: Aharbal (SAM 893), 08/09/2011, 1775 m. 2300 m 62. Dryopteris juxtaposita H. Christ, Bull. Acad. Int. 59. Dryopteris blanfordii subsp. nigrosquamosa Geogr. Bot. 17: 138 (1907) (Ching) Fraser-Jenk., Bull. Brit. Mus. (Nat. Hist.), Bot. 18: Synonym: Aspidium filix-mas var. normale (C. B. 388 (1989). Clarke) H. Christ; Dryopteris odontoloma (Bedd.) C. Chr.; Synonym: Dryopteris gushaingensis Ching; Dryopteris Lastrea odontoloma Bedd.; L. odontoloma T. Moore; nigrosquamosa Ching Nephrodium filix-mas var. normale C. B. Clarke. Terrestrial fern growing in steep abies forests, stipes Medium size fern growing on forest floor near water, densely fibrillose and scaly, scales broadly ovate, fuscous- rhizome scaly, scales brown, fronds caespitose, lamina brown, concolorous, crinkled, margins with filamentous subcoriaceous, upper surface blue-green, lower surface projections, lamina ca. 40x12 cm, pinnules lobed, segment whitish-green, sori round, mostly upper part of lamina apex rarely sharply serrate, rare with 2600-3400 m. fertile, indusia brown, rounded-reniform, occasional from Distribution: SE Tibet, W. China, Nepal, India 2200-3700 m altitude. (Kashmir). Distribution: Afghanistan, Burma, Bhutan, Japan, Specimen examined: Dubjan (SAM 847), 05/07/2011, Nepal, Tibet, Vietnam, China, Nepal, Thailand, India 2750 m. (Kashmir, Himachal Pradesh, Uttarakhand, Sikkim, West 60. Dryopteris caroli-hopei Fraser-Jenk., Bull. Brit. Bengal, Assam, Nagaland, Manipur, Meghalaya, Tamil Mus. Nat. Hist. Bot. 18: 422 (1989). Nadu). Synonym: Aspidium dilatatum var. patuloides H. Specimen examined: Heerpur (SAM 883), 28/07/2011, Christ, Dryopteris pseudomarginata Ching; D. 2715 m; Secjan (SAM 910), 05/09/2012. pseudomarginata Ching; D. marginata sensu auct. West 63. Dryopteris nigropaleacea Fraser-Jenk., Bol. Soc. Himalaya, non (Wall. ex C. B. Clarke) Christ; Nephrodium Brot., ser. 2, 55: 238 (1982). marginarum sensu Hope Synonym: Dryopteris pallida Subsp. nigropaleacea Large fern growing near stream banks under shade, Fraser-Jenk.; Nephrodium filix-mas Rich. var. normalis C. rhizome thick, stipe base densely scaly, scales pale-brown, B. Clarke broad ovate, lamina pale-green, 2-3-pinnate, elongated Medium size fern growing near small streams banks, ovate-lanceolate, pinnules deeply lobed to the costa stipe very base scaly and fibrillose, lamina elongate, (sometimes becoming pinnate), apex bluntly acuminate, triangular-lanceolate, crispaceous, abaxially glaucous, occasional from 1700-2300 m altitude. adaxially blue-green, matt, glabrous; pinnae lobes Distribution: Bhutan, China, Nepal, Tibet, Yunnan, rectangular with rounded-truncate and toothed apices, India (Jammu and Kashmir, Arunachal Pradesh, Manipur, frequent from 1700-2800 m altitude. Meghalaya, Nagaland, Himachal Pradesh, Uttarakhand). Distribution: Afghanistan, Bhutan, Burma, Nepal, Specimen examined: Imamsahib (SAM 844), Pakistan, India (Jammu and Kashmir, Himachal Pradesh, 15/07/2011, 1866 m; D. K. Pora (SAM 860), 29/07/2011, Uttarakhand, Sikkim, West Bengal, Nagaland). 1800 m. Specimen examined: Dubjan (SAM 857), 27/07/2011, 61. Dryopteris filix-mas (L.) Schott, Gen. Fil. , sub pl. 9 2700 m; Heerpur (SAM 884), 18/08/2011, 2600 m. 1834. 64. Dryopteris pulvinulifera (Bedd.) Kuntz, Revis. Gen. Pl. 2: 813 (1891). MIR et al. – Pterydophytes of Shopian, Kashmir Valley 39
Synonym: Dryopteris harae H. Ito; D. reholttumii M. Synonym: Dryopteris lancipinnula Ching; D. Price; Lastrea pulvinulifera Bedd.; L. sparsa var. zeylanica submarginata Loyal; D. subodontoloma Loyal Bedd.; L. pulvinulifera var. zeylanica Bedd.; Nephrodium Medium size fern growing on small streams banks, pulvinuliferum (Bedd.) Baker; N. sparsum var. rhizome long-ascending, stipe long, base scaly, scales pale squamulosum C. B. Clarke brown, lamina deltoid-lanceolate, pale green, thinly Plants growing on steep forest floor under shade, leathery, basal pinnae pair largest, basal basiscopic pinnule rhizome thin, stipe base with densely scaly, scales bright of lowest pinnae largest, rare from 1800-2700 m altitude. golden, narrow, linear, lamina dark-green, deltoid- Distribution: Bhutan, Nepal, China, India (Kashmir, lanceolate, lower part 4-pinnate, upper part 3-pinnate, Himachal Pradesh, Kumaun, Uttarakhand, Sikkim, West pinnules pinnate, apices acute ending in few small acute Bengal). teeth, pinnulets overlapping, occasional from 1700-2800 m Specimen examined: D.K. Pora (SAM 856), altitude. 06/07/2011, 1830 m Distribution: Bhutan, China, Nepal, Sri Lanka, 69. Dryopteris wallichiana (Spreng.) Hylander, Bot. Philippines, India (Kashmir, Sikkim, West Bengal, Assam, Notis: 352 (1953). Meghalaya, Nagaland). Synonym: Aspidium donianum Spreng.; A. paleaceum Specimen examined: Heerpur (SAM 813), 08/07/2011, Lag. ex Sw.; A. paleaceum (T. Moore) Dalla Torre & 2600 m; Dubjan (SAM 858), 28/08/2011, 2800 m. Sarnth.; A. parallelogrammum Kunze; A. patentissimum 65. Dryopteris ramosa (Hope) C. Chr., Index Filic. Wall. ex Kunze; A. Wallichianum Spreng.; Dichasium fasc. 5: 287 (1905). parallelogrammum (Kunze) Fee; D. patentissimum (Wall. Synonym: Nephrodium ramosum Hope ex Kunze) Fee; Dryopteris cyrtolepis Hayata; D. doiana Terrestrial large fern growing on forest floor, rhizome Tagawa; D. doniana (Spreng.) Ching; D. himalaica (Ching densely scaly and surrounded by stipe bases, lamina 3- & S.K. Wu) S.G. Lu; D. pachyphylla Hayata; D. paleacea pinnate, deltate, apex acuminate, pale-green, pinnae distant, (T. Moore) Hand. Mazz.; D. parallelogramma (Kunze) frequent with the altitudinal range of 2000-4000 m altitude. Alston; D. patentissima (Wall. ex Kunze) N.C. Nair; D. Distribution: Afghanistan, Bhutan, California, quatanensis Ching; D. ursipes Hayata; D. Walliachiana Caucasus, Tibet, Europe, Nepal, Pakistan, India (Kashmir, var. himalaica Ching & S.K. Wu; Lastrea paleacea (Lag. Himachal Pradesh, Uttarakhand). ex Sw.) T. Moore; L. parallelogramma (Kunze) Liebm.; L. Specimen examined: Dubjan (SAM 846), 18/07/2011, patentissima C. Presl; L. patentissima (Wall. ex Kunze) J. 2700 m. Sm.; Nephrodium parallelogrammum (Kunze) Hope; N. 66. Dryopteris redactopinnata S.K. Basu & Panigrahi, patentissimum (Wall. ex Kunze) C.B. Clarke Indian J. Forest. 3: 270 (1980). Very large fern growing on forest floor, rhizome Synonym: Dryopteris pseudofibrillosa Ching; D. massive, stipe very densely scaly, scales at stipe base tsangpoensis Ching blackish mixed with pale ones, scales upwards along with Medium size fern growing on forest floor, stipe densely rachis light-brown to paler, mixed with few blackish ones, clothed with scales, scales light to mid-brown, concolorous, scale base usually dark, rachis densely scaly and fibrillose; not glossy, lamina ca. 30x13 cm, glossy on upper surface, lamina green to deep-green, large, ca. 70x22 cm, sori upper part of lamina fertile, indusia with brown center and indusiate, round, 2/3rd of frond is fertile, indusia dark- pale brown margin, frequent from 2400-3800 m altitude. brown, reniform falling off at maturity, frequent from Distribution: Bhutan, China, Tibet, Taiwan, Nepal, 2300-3500 m altitude. Pakistan, India (Jammu and Kashmir, Himachal Pradesh, Distribution: Argentina, Bhutan, Borneo, Burma, Uttarakhand, Sikkim, West Bengal). China, Malaysia, Myanmar, Nepal, Jamaica, Cuba, Brazil, Specimen examined: Dubjan (SAM 878); 05/08/2011; Tibet, Nepal, Taiwan, Japan, Mexico, Vietnam, 3320 m. Philippines, Java, India (Kashmir, Himachal Pradesh, 67. Dryopteris stewartii Fraser-Jenk., Kalikasan Philip. Uttarakhand, Sikkim, Meghalaya, Arunachal Pradesh, J. Biol. 7: 272 (1979). Nilgiri hills). Synonym: Dryopteris odontoloma (Bedd) C. Chr. f. Specimen examined: Dubjan (SAM 929); 27/07/2011; brevifolia Mehra & Khullar 2725 m. Medium size fern growing on small stream banks, stipe 70. Dryopteris xanthomelas (H. Christ) C. Chr., Index base densely scaly, scales blackish-brown to brown, glossy, Filic., Suppl. 1: 41 (1913). sometimes bicolorous, margin serrate, apex acuminate, Synonym: Aspidium xanthomelas Christ; Dryopteris lamina widest above the base, mid-green adaxially, green discrete Ching & S. K. Wu; D. omeicola Ching; D. abaxially, frequent with altitudinal range of 1800-3100 m. canaliculata Ching in C. Y. Wu; D. centrochinensis R. C. Distribution: Afghanistan, Pakistan, Nepal, India Ching; D. chingii Nair; D. fibrillosa (C. B. Clarke) Hand. (Kashmir, Himachal Pradesh, Uttarakhand). Mazz; D. fibrillosissima Ching in C. Y. Wu; D. hupehensis Specimen examined: D. K. Pora (SAM 856); Ching; D. pulcherrima Ching; D. qandoensis Ching in C. 23/07/2011, 1850 m; Heerpur (SAM 870), 08/08/2011, Y. Wu; D. rosthornii (Diels) C. Chr.; D. rosthornii sensu 2550 m; Aharbal (SAM 895), 05/07/2012, 2400 m. Stewart; D. sinofibrillosa Ching; Nephrodium rosthornii 68. Dryopteris subimpressa Loyal, Nova Hedwigia 16: Diels 467 (1968). Large fern growing on forest floor and scrub zone, stipe black, base densely scaly and fibrillose, scales black, 40 BIODIVERSITAS 16 (1): 27-43, April 2015 broadly lanceolate, glossy, apex acuminate, upper part Bengal, Meghalaya, Bihar, Tamil Nadu, Sikkim, Manipur, together with rachis clothed with linear-lanceolate and Arunachal Pradesh). linear, dentate scales, lamina ca. 30x10 cm, sori indusiate, Specimen examined: Narwani (SAM 881), 25/07/2011, upper part of lamina fertile, indusia brown, rounded- 1775 m; Kund (SAM 945), 24/09/2012, 2350 m. reniform, frequent from 2400-3800 m altitude. 74. Polystichum lachenense (Hook.) Bedd, Ferns Brit. Distribution: Bhutan, Nepal, Pakistan, Tibet, Taiwan, India, pl. 32 (1865). India (Kashmir, Himachal Pradesh, Arunachal Pradesh, Synonym: Aspidium lachenense Hook.; Polystichum Uttarakhand, Sikkim, West Bengal). aleuticum C. Chr. ex Holten; P. tsuchuense Ching in C. Y. Specimen examined: Dubjan (SAM 880), 27/07/2011, Wu; P. sinkiangense Ching ex Chang Y. Yang; P. 3320 m; Huran (SAM 945), 25/09/2012, 3450. xinjiangense Ching ex C.Y. Yang. 71. Polystichum bakerianum (Atk. ex C.B. Clarke) Small fern growing under rocks, stipe dark brown to Diels, Nat. Pflanzen fam. 1: 191 (1899). blackish-purple, glossy, rachis scaly and fibrillose, lamina Synonym: Aspidium bakerianum (Atk. ex C. B. Clarke) fragile, abaxially fibrillose, pinnae deltoid-ovate, distant, Atk. ex Baker; A. prescottianum var. bakerianum Atk. ex lobed, lobes ending in acute tooth, upper half of frond C. B. Clarke; Polystichum prescottianum var. bakerianum fertile; rare from 3000-4200 m altitude. (Atk. ex C. B. Clarke) Bedd. Distribution: Burma, China, Japan, Bhutan, Myanmar, Large fern growing on steep and open bushy areas at Nepal, Taiwan, Pakistan, Tibet, India, Kashmir, Himachal higher altitudes, stipe and rachis densely scaly and Pradesh, Uttarakhand, Sikkim). fibrillose, lamina abaxially scaly and fibrillose, pinnule Specimen examined: Huran (SAM 866), 10/07/2011, margin lobed, lobes ending in a sharp long and curved 3550 m; Kaunsernag (SAM 920), 28/08/2012, 3450 m; tooth, frequent from 3000-3900 m altitude. Dubjan (SAM 937), 20/09/2012, 3260 m. Distribution: Afghanistan, Bhutan, China, Nepal, 75. Polystichum lonchitis (L.) Roth. Tent. Fl. Germ. 3: Pakistan, India (Kashmir, Himachal Pradesh, Uttarakhand, 71 (1799). Sikkim, Arunachal Pradesh). Synonym: Aetopteron lonchitis House; Aspidium Specimen examined: Peergali (SAM 917), 18/08/2012; lonchitis (L.) Sw.; Dryopteris lonchitis (L.) O. Kuntze; 3250 m. Hypopeltis lonchitis Tod.; Polypodium lonchitis L.; 72. Polystichum castaneum (C. B. Clarke) B. K. Nayar Polystichum asperum Bubani & S. Kaur, Comp. Bedd. Handb. Ferns Brit. India, 50 Lithophytic fern growing at higher altitudes in alpine (1974). and subalpine regions, lamina linear to linear-lanceolate, Synonym: Aspidium prescottianum Wallich ex base narrowed, drooping at tip, glossy, pinnae edges with Mettenius var. castaneum C. B. Clarke; Polystichum spiny teeth, auricled at anterior and cunate at posterior prescottianum (Wallich ex Mettenius) T. Moore var. bases, rare from 2700-4000 m altitude. castaneum (C. B. Clarke) Beddome Distribution: Afghanistan, N. America, Iran, Ireland, Medium size fern growing in alpine meadows, stipes China, Japan, Europe, Pakistan, India (Kashmir). and rachis very densely scaly and fibrillose, scales usually Specimen examined: Huran (SAM 862), 10/07/2011, light-brown with few dark streaks mixed with blackish- 3550 m; Dubjan (SAM 938), 20/09/2012, 3330 m. brown, pinnae basal pairs slightly distant and reduced, 76. Polystichum luctuosum (Kunze) T. Moore Index margin serrate and spinulose, occasional from 3200-4600 Fil. 95 (1858). m altitude. Synonym: Aspidium tsus-simense Hook.; A. luctuosum Distribution: China, Myanmar, India (Jammu and Kunze; A. aculeatum var. pallescens Franch.; Polystichum Kashmir, Himachal Pradesh, Garhwal, Sikkim, West monotis Christ; P. falcilobum Ching; P. tsus-simense var. Bengal). pallescens Franch. P. mayebarae Tagawa Specimen examined: Dubjan (SAM 919), 10/08/2012, Terrestrial fern growing in shady areas along streams 3300 m with partial to no sun exposure, rhizome scaly, scales 73. Polystichum discretum (D. Don) J. Smith, J. Bot. 3: brown with blackish apex, lower pinnae bending forward 413 (1841). and downward, pinnules auriculate, ovate-trapezoid, rare Synonym: Aspidium discretum D. Don; Polystichum from 1700-2500 m altitude. discretum (D. Don) Diels; P. fuscopaleaceum Alston; P. Distribution: Japan, China, Korea, Madagascar, Nepal, indicum Khullar & S. C. Gupta; P. kathmanduense Pakistan, Africa, Tibet, Taiwan, India (Jammu and Nakaike; P. nigropaleaceum (H. Christ) Diels Kashmir, Uttarakhand, Arunachal Pradesh). Large fern growing at shaded and humus rich areas, Specimen examined: Kund (SAM 926), 16/09/2012, stipe densely fibrillose, scaly, scales dark-brown to almost 1900 m. black, lamina abaxially fibrillose, adaxially shiny, lowest 77. Polystichum nepalense (Spreng) C. Chr., Index pinnae pair deflexed forward and downwards, pinnule apex Filic. 1: 84 (1905). acute with prominent teeth curved towards pinna apex, Synonym: Aspidium auriculatum var. marginatum C. B. occasional from 1700–2700 m altitude. Clarke; A. marginatum Wall.; A. nepalense Spreng; Distribution: Africa, Burma, China, Japan, Malaya, Sri Polystichum atroviridissimum Hayata; P. auriculatum var. Lanka, Bhutan, Myanmar, Nepal, Pakistan, Thailand, marginatum Bedd. India, Kashmir, Himachal Pradesh, Uttarakhand, West Medium size fern growing in rocky meadows near stream, Stipes scaly and fibrillose, lamina pinnate, MIR et al. – Pterydophytes of Shopian, Kashmir Valley 41 narrowly lanceolate, slightly narrowed below, margin Distribution: Bhutan, China, Taiwan, Tibet, Nepal, irregularly more or less entire or slightly serrate with pale Pakistan, India (Kashmir, Uttarakhand, Himachal Pradesh). colored teeth, rare from 2000-3200 m altitude. Specimen examined: Kaunsernag (SAM 816), Distribution: Afghanistan, Bhutan, Burma, china, 15/07/2012, 3450 m; Dubjan (SAM 936), 26/09/2012, 3350 Japan, Myanmar, Nepal, Philippines, Sri Lanka, Tibet, m. Vietnam, Yunnan, India (Arunachal Pradesh, Darjeeling 81. Polystichum yunnanense H. Christ, Notul. Syst. hill, Himachal Pradesh, Manipur, Meghalaya, Mizoram, (Paris) 1: 34 (1909). Nagaland, Sikkim, Uttarakhand). Synonym: Polystichum gyirongense Ching; P. Specimen examined: Secjan (SAM 928), 08/09/2012, jizhushanense Ching; P. yunnanense var. submuticum C. 2400 m. Chr.; P. makino sensu Frase-Jenkins & Khullar 78. Polystichum piceopaleaceum Tagawa in Acta Large fern growing on forest floor, stipes long brown, Phytotax. Geobot. 5: 255 (1936). stipe base scaly, rachis densely fibrillose, scaly, lamina Synonym: Aspidium angular sensu Hope; Polystichum broadly lanceolate, dark bluish-green upper surface with aculeatum var. fargesii H. Christ; P. bicolor Ching & S.K. little depressions opposite the sorus, basal acroscopic Wu; P. doianum Tagawa; P. setiferum var. fargesii (H. pinnule largest, margin deeply lobed, lowest lobe largest Christ) C. Chr.; P. yunnanense var. fargesii (H. Christ) C. and parallel to the costa facing towards apex, margin with Chr. sharp teeth, frequent from 2000-3200 m altitude. Terrestrial fern growing on forest floor, rocky Distribution: Afghanistan, China, Tibet, Burma, meadows, lamina bipinnate, abaxially scaly and fibrillose, Bhutan, Myanmar, Nepal, Pakistan, India (Jammu and apex acuminate, lower pinnae pairs deflexed downwards; Kashmir, Himachal Pradesh, Uttarakhand, Tamil Nadu, pinnules rhomboidal-ovate, frequent from 1800-3200 m Sikkim, Arunachal Pradesh, Meghalaya, Manipur, altitude. Darjeeling hills). Distribution: Afghanistan, Bhutan, Burma, China, Specimen examined: Aharbal (SAM 873), 23/07/2011, Japan, Myanmar, Nepal, Pakistan, Sri Lanka, Taiwan, India 2250 m; Kund (SAM 912), 16/09/2012, 2120 m. (Jammu and Kashmir, Himachal Pradesh, Arunachal Pradesh, Uttarakhand, Assam, Manipur, Meghalaya, Nilgiri hills, Nagaland). Botanical study of flora of particular area is an Specimen examined: Aharbal (SAM 825) 05/07/2011, important aspect as it forms baseline information for the 2650 m; Heerpur (SAM 933), 24/07/2011, 2500 m; Secjan distribution of plant species or communities and their (SAM 894), 06/08/2012, 2450 m. relation with physical environment. This paper gives a 79. Polystichum prescottianum (Wall. ex Mett.) T. broad outlook about the pteridophytes of Shopian. About Moore. Ind. Fill.: 101 (1858). 81 species of ferns and fern allies have been collected in Synonym: Aspidium mouoinense Franch.; Aspidium the course of the study for three consecutive years, 2010- prescottianum Wall. ex Mett.; Polystichum erinaceum 2012; indicating that agro-climatic conditions of the study Ching & S.K. Wu.; P. mouoinense (Franchet) Bedd. area are favorable for the growth and development of Large fern forming colonies in open meadows above pteridophytes. The pteridophytes form a vital element of the tree line, fronds clustered, stipe base dark-blue, densely the ecosystem and most of them being forest dwellers that scaly and fibrillose, lamina densely fibrillose, pinnae can be taken as good indicators of the extent of problems margin deeply lobed, lobes/pinnules serrate with each lobe like deforestation and habitat destruction. Botanical ending in an awn or spine, upper part of the frond fertile, explorations should increase in the under-explored common from 2800-3900 m altitude. botanically rich areas for documenting the diversity and Distribution: Afghanistan, Bhutan, China, Pakistan, ecological characteristics of pteridophytes. Taxonomic Taiwan, Nepal; India (Kashmir, Himachal Pradesh, reinvestigations in such areas should take place to avoid the Uttarakhand, Sikkim, West Bengal). confusions with new species and existing species. Specimen examined: Huran (SAM 861), 08/07/2011, 3200 m; Dubjan (SAM 939), 10/08/2012, 3300 m. 80. Polystichum shensiense Christ, Bull. Acad. Geogr. ACKNOWLEDGEMENTS Bot. Mans. 16: 113 (1906). Synonym: Dryopteris lichiangensis (Wright) C. Chr.; The first author is thankful to University Grants Nephrodium lichiangense C.H. Wright; Polystichum Commission (UGC), New Delhi, India for providing lichiangense (Wright) Ching ex H.S. Kung; P. financial assistance to carry out the research work. Authors obtusipinnum Ching & H.S. Kung; P. prescottianum var. are also thankful to Late Dr. H. C. Pande (Sci.-'D') and shensiense (H. Christ) C. Chr. Brijesh Kumar, Botanical Survey of India, Dehradun; Dr. Terrestrial fern growing above tree line, stipe and rachis Shweta Singh, Guru Gobind Singh Indraprastha University, scaly and fibrillose, scales light-brown, broad-ovate New Delhi; and Prof. S. P. Khullar, Chandigarh for their intermixed with lanceolate ones, pinnae sessile, alternate, help in the identification of plants and rendering me triangular-lanceolate, margin deeply segmented or necessary literature facilities. becoming pinnate, segments small with few marginal teeth, rare with the range of 3200-4500 m altitude. 42 BIODIVERSITAS 16 (1): 27-43, April 2015
Figure 2. Asplenium punjabense Bir, Fraser-Jenk. & Lovis.
Figure 3. Pseudophegopteris pyrrhorachis (Kunze) Ching, subsp. distans (Mett.) Fraser-Jenk. MIR et al. – Pterydophytes of Shopian, Kashmir Valley 43
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Vegetation of Kashmir University Campus, Pakistan & Kashmir In: Nasir E, Ali SI (eds). Flora of West Pakistan. Srinagar. J Ind Bot Soc 45: 354 364. – Fakhri Press, Pakistan. Kaul V, Zutshi DP. 1967. A study of aquatic and marshland vegetation in Stewart RR. 1984. Remarks on North–West Himalayan Ferns. Indian Fern Srinagar. Proc Nat Inst Sci India 33: 111 127. – J 1: 41-46. Khullar SP, Sharma SS. 1987. The ferns of Western Himalaya excluding Wani MH, Shah, MY, Naqshi AR. 2012. The ferns of Kashmir-an update Uttarakhand. In: Pangtey YPS, Joshi SC (eds). Western Himalaya, account. Indian fern J 29: 100-136. BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 44-54 DOI: 10.13057/biodiv/d160106
Local knowledge of medicinal plants in sub-ethnic Batak Simalungun of North Sumatra, Indonesia
MARINA SILALAHI1,3,♥, JATNA SUPRIATNA1, EKO BAROTO WALUJO2, NISYAWATI1 1Departement of Biology, Faculty of Mathematics and Natural Science, Universitas Indonesia, Depok, 16424, Indonesia 2Division of Botany, The Indonesian Institute of Sciences, Cibinong, Bogor, 16911, Indonesia 3Departement of Biology Education, Faculty of Education and Teacher Training, Universitas Kristen Indonesia, Jakarta. Jl. Mayjen Sutoyo, No. 2 Cawang, Jakarta 13630. Tel. +62-21-8009190, 8092425. Fax. +62-21-80886882. ♥email: [email protected]
Manuscript received: 29 October 2014. Revision accepted: 12 Desember 2014.
Abstract. Silalahi M, Supriatna J, Walujo EB, Nisyawati. 2015. Local knowledge of medicinal plants in sub-ethnic Batak Simalungun of North Sumatra, Indonesia. Biodiversitas 16: 44-54. Research on the local knowledge of medicinal plants by sub-ethnic Batak Simalungun of North Sumatra was conducted, using an ethnobotanical approach. The sample consisted of 8 key informants and 32 general respondents, who were grouped into two, namely those who were 30-50 years old and >50 years old. Data were analyzed both qualitatively by descriptive statistics and quantitatively by calculating the index of cultural significance (ICS) and the use value (UVs). It was found that 239 species (170 genera, 70 families) of medicinal plants were used to cure 18 kinds of natural diseases and 2 kinds of supra natural diseases. Almost half of those plants (119 species) had leaves used as medicines. Among the diseases, gastrointestinal disorders had the highest number of medicinal plants used (72 species), followed by fever (64 species), and fractures (41 species). It seemed that younger generation had lost their knowledge in the medicinal plants because their knowledge of medicinal plants (48.19 ± 8.35 species) was lower than the that of older generation (170.19 ± 18.38 species), while our key informants had the highest knowledge of medicinal plants among respondents (202.00 ± 12.32 species).
Keywords: local knowledge, medicinal plants, North Sumatra, sub-ethnic Batak Simalungun.
INTRODUCTION proved through scientific approach (ethic approach) (Walujo 2009). Man is known to have utilized plants as a source of The traditional medicine is related to cultural diversity, drugs for thousand years. The World Health Organization ethnic diversity, and biodiversity of plants. Indonesia has (WHO) estimated that about 60-80% of the world more than 300 ethnics, one of which is Batak, which population still relies on the traditional medicine derived consists of five sub-ethnics or tribes often referred to as from plants (Joy et al. 1998), and Indonesian population sub-ethnics, namely Karo, Phakpak, Simalungun, Toba, (60%) relies on traditional medicinal plants for their health and Angkola-Mandailing (Bangun 2010). Researches on care. Medicinal plants are species known to have efficacy the usage of plants by local communities or ethnic groups to help maintain the health or to cure a disease. Medicinal in Sumatra have been carried out, among others: Batak plants are grouped into three: traditional, modern, and Toba (Simbolon 1994), Rejang (Darnaedi 1999), Malay potential medicinal plants. (Setyowati and Siagian 2004; Setyowati and Wardah 2007; The local knowledge of medicinal plants is inherited Sunesi and Wiryono 2007; Rahayu et al. 2007; Hariyadi orally or in written in ancient manuscripts. The main and Ticktin 2011. Those studies show that the diversity of obstacle encountered in recovering local knowledge the medicinal plants used by local communities depends on through ancient manuscripts is the difficulty in reading, the ethnicity, locality, age of respondent, and number of because some parts of many manuscripts have been lost or respondents. damaged (Nawangningrum et al. 2004). To overcome this, It is really unfortunate that high deforestation in it is necessary to look for more efficient alternative Indonesia that causes the loss of many plant species and methods to recover the local knowledge. Ethnomedicine is understanding of local knowledge will hamper our efforts an alternative that has been used because it may use both to find new drugs. The high rate of erosion of the local ethnology and medicinal science (Martin 1995). knowledge has been found everywhere in the world Ethnomedicine is the study of perception and including Indonesia (Hoang et al. 2008). At the same time, conception of local communities in understanding health or our local knowledge of medicinal plants are kept only by research that studies the traditional ethnic medical system. the older people (>50 years old) and shamans (Darnaedi The high effectiveness of ethnomedicine research is due to 1999). While the rate of species loss is also similar to the reduction of time and costs in finding new chemical rate loss of local knowledge (Hoang et al. 2008). compounds used as drugs (Fabricant and Farnsworth 2001). Meanwhile, researches on the local knowledge of sub- Ethnomedicinal study is done through a community ethnic in Sumatra have not been intensively carried out. For perspective approach (emic approach), which is then that purpose, we have done our research on the SILALAHI et al. – Medicinal plants of Batak Simalungun, Indonesia 45 ethnomedicine of sub-ethnic Batak Simalungun. This Data analysis research had two objectives: (i) to understand the local Data were analyzed using qualitative and quantitative knowledge of medicinal plants in sub-ethnic Batak methods. Qualitative analysis was done by grouping plants Simalungun; (ii) to understand and preserve the value and based upon usage category. Quantitative analysis was done cultural heritage of the medicinal plants. by determining UVs, ICS, and calculating the differences of those parameters in statistical analysis, using Anova. The results consisted of: (i) Index of cultural significance MATERIALS AND METHODS (ICS), calculated using the formula of Turner (1988), (ii) use value (UVs) of each species was based on Prance et al. Study area 1987, and Anova was calculated using software SPSS version 17. Our study site is located in Nagori Simbou Baru, Raya Sub-district, Simalungun District, North Sumatra, Indonesia. The total area of those villages is 2002.96 RESULTS AND DISCUSSION hectares, within the altitude of 650-700 m above sea level. Simbou Baru village is geographically located at N The concept of “disease” in Sub-ethnic Batak 2o57’05’’ and E 98o57’84’’ (Figure 1). Simalungun The local knowledge of sub-ethnic Batak Simalungun Data Collection in making use of plants as medicine is related to the To obtain the local knowledge on medicinal plants in concept of diseases. The diseases are grouped into natural sub-ethnic Batak Simalungun, interviews were conducted and supra natural diseases. Natural diseases are those with ethnobotanical approach (Martin 1995; Alexiades caused by the malfunctioning of the body such as, fever, 1996). It was conducted through semi-structured and in- toothache, ulcers, and diarrhea. Sub-ethnic Batak depth interviews. The interviews were conducted with 8 Simalungun has known as many as 18 kinds of natural key informants (healers, ethnic chiefs), 32 general diseases (Table 1). The medicinal plants which have been respondents with two age groups: the first group was 30-50 used to cure diseases vary in number and species. The years old and the second group above 50 years old with a highest number of medicinal plants used were those to cure ratio of 1:1. gastrointestinal disorders (72 species), followed by fever (64 species), and fractures (41 species).
Figure 1. Study site of Nagori Simbou Baru, Raya Sub-district, Simalungun District, North Sumatra, Indonesia. 46 BIODIVERSITAS 16 (1): 44-54, April 2015
Table 1. Number of medicinal plants species used to cure the catechins, ᵝ-citosterol which serves as antipyretic and “diseases” in sub-ethnic Batak Simalungun of North Sumatra. analgesic. The local knowledge of curing fractures has presumably Number of Characteristics Name of diseases been adopted from the behavior of a bird called siburuk. species They have learned from siburuk bird that when their chicks Natural disease Hypertension 15 are fractured and hurt by communities, the mother will Cough 10 Asthma 24 bring the herbs. There were 41 species of plants used to Diarrhea 22 cure fractures. To cure fractures, those plants have to be Gastrointestinal disorders 72 cooked using coconot oil. The examples of plants used for Stomach ache 12 curing fractures were jengkol (Pithecolobium lobatum), Fractures 41 sibaguri (Sida ungulata), ompu-ompu (Crinum asiaticum), Rheumatism 6 kelapa (Cocos nucifera), and baru (Hibiscus similis). The Itch 8 ompu-ompu leaves contain alkaloids, glycosides, Ulcer 12 triterpenes, coumarins which can serve as an analgesic Kidney disease 25 Diabetes mellitus 21 (Asmawi et al. 2011) and anti-inflamantory (Rahman et al. Aphrodisiac 13 2013). Injury 39 Supra natural diseases are those caused by supra natural Fever 64 spirits, bad person, and curse (karma) such as busung (liver Eye infection 6 disease) and alogo-alogo (“malnutrition”). Local Thrush 4 communities believed that busung disease only occurs to Toothache 5 people who commit a theft. Busung disease will be treated Supranatural Busung (liver disease) 23 by shaman, through a series of rituals. Those plants used to disease Alogo-alogo (“malnutrition”) 18 treat busung have been identified as: kelapa (Cocos Traditional Tinuktuk tawar 117 (“mashed nucifera), jarango (Acorus calamus), utte mungkur (Citrus concoction concoction” to maintain stamina) Tinuktuk paranggetek (“mashed 11 hystrix), silinjuang (Cordyline fruticosa), bagot (Arenga concotion” to maternity) pinnata), and demban (Piper betle). Alogo-alogo (alogo means wind) disease affects the children. Local communities believe that the alogo-alogo The high frequency of gastrointestinal disorder is disease is caused by sin of their ancestors. The patients are caused by poor sanitation in their houses and in the characterized by thin body, pale face, bloated abdomen, surrounding villages, which may force local communities and fever at night. Plants used to cure alogo-alogo disease to explore any medicinal plants to cure the diseases. were, among others, demban (Piper betle), jarango (Acorus Medicinal plants which have bitter taste such as: jambu calamus), and lada (Piper nigrum). Those plants are able to batu (Psidium guajava), horis kotala (Eurycoma warm the body, so they can expedite the blood circulation, longifolia), ratusan (Ageratum conyzoides), and andor because Acorus calamus contains high potassium, which golat (Mikania cordata) have been used to cure can be used to cure fever (Motley 1994). gastrointestinal disorders. The bitter taste in those plants is Sub-ethnic Batak Simalungun has traditional due to its chemical contents, namely tannin and flavonoid. concoction called tinuktuk (tuntuk = mashed). It is called The tannin has been proven to cure the diarrhea (de Padua tinuktuk because of the producing process, namely by et al. 1999). Tannin is able to form a thin layer on the mashing a variety of medicinal plants. The local lumen, therefore reducing irritation (Munim and Hanani communities can distinguish two different kinds of 2011). Those plants can also prevent water secretion and tinuktuk: tinuktuk tawar (to maintain stamina) and tinuktuk also kill microbes (Achmad et al. 2008). Furthermore, paranggetek (concoction for maternity). The plants that Munim and Hanani (2011) say that the tannin causes the have been used to cure tinuktuk tawar were 117 species denaturation of protein whereas flavonoid causes the while for tinuktuk paranggetek were 11 species. destruction of cell wall of bacteria. The extract of Psidium To cure Tinuktuk concoction, the roots, leaves, and guajava leaves prevents the growth of Escherichia coli tuber of 117 species of plants have been used. Roots of 7 (Voravuthikunchai et al. 2004), Staphylococcus aureus, species of bamboo (Poaceae), 7 species of palms Bacillus subtilis, and Pseudomonas aeruginosa (Arecaceae), 7 species of rattan (Arecaceae), and 7 species (Abdelrahim 2002). of Citrus (Rutaceae) were among the listed plants. While A large number of plants species have been used to cure tubers that have been used were from ground orchid fever, a symptom caused by some deseases such as chicken (Orchidaceae). The roots to be used were firstly cut into pox, cough, and wounds. Those plants were identified as small pieces, dried, and crushed. The materials of leaves follows: bunga raya (Hibiscus rosa-sinensis), habu-habu were mashed until fine and then squeezed to get the water (Ceiba pentandra), silundad (Impatiens platypetala), out. The water resulted from squeezed materials was used rampas binei (Drymaria cordata), jarango (Acorus to boil the roots until all the water evaporated and the calamus), and horis kotala (Eurycoma longifolia). The material became dry and salt was used as preservative. ability of plants to reduce fever is related to the content of Tuber of Orchidaceae such as: salembar satahun (Nervillia bioactive compounds. Buenz et al. (2005) state that Ceiba plicata), salembar sabulan (Nervilia aragoana), and pentandra has a chemical compound that serves as gadong harangan (Goodyera rubicunda) have been used. SILALAHI et al. – Medicinal plants of Batak Simalungun, Indonesia 47
Whereas rattan from both genus Daemonorops and sabulan (Nervilia aragoana), salembar satahun (Nervilia Calamus, have been utilized more often. Other tribes such plicata), and gadong harangan (Goodyera rubicunda). as Anak Dalam tribe in Jambi have used Daemonorops to Tuber of orchids can be used to make traditional cure wounds and headache (Sulasmi et al. 2012). concoction (tinuktuk), which is to enhance stamina. In the process of producing tinuktuk, some local communities (7-10 people) cooperate because they have to find plants from the forests, farms, and plantations. Due to difficulties in finding the plants, the young generation (<50 years old) tend to ignore this kind of treatment and consider those practices are out of date.
Diversity of medicinal plants The sub-ethnic Batak Simalungun has used as many as 239 species (170 genera, 70 families) of medicinal plants. Those plant species which have been used by local communities were spermatophyta (230), pterydophyta (8) and lichens (1). Figure 2 shows that the main families of medicinal plants that have been used consisted of Arecaceae (20 species), followed by Poaceae (16 species), Rutaceae (13 species) and Zingiberaceae (12 species). The highest number of genera was found in Arecaceae (13 genera), followed by Euphorbiaceae (12 genera), Poaceae (11 genera), Fabaceae and Asteraceae (10 genera). At least 20 species of Arecaceae have been used as Figure 2. Composition of species and family used for medicinal medicinal plants by sub-etnis Simalungun, , most of which plants by sub-ethnic Batak Simalungun. were rattans and palms. Some of the palms mainly used for medicines were kelapa (Cocos nucifera), bagot (Arenga pinnata), and pining (Areca catechu). Cocos nucifera was used to cure fever, fractures and as a component of tinuktuk concoction because it has anti bacterial, anti fungal, anti- viral, immunostimulant, antioxidant, and hypoglycemia (Debmandal and Mandal 2011). It was found that 18 spesies of medicinal plants belong to Poaceae, especially bamboo. Most parts of bamboo both leaves and roots have been used as medicinal plants. The leaves of bamboo have been used to cure injury and fever. The same usage of bamboo leaves is found in Chinese medicines (Wang et al. 2012). Utte bunga (Citrus aurantium), utte mungkur (Citrus hystrix), and tuba (Zanthoxylum acanthopodium) belong to Rutaceae and they were commomly used. Out of 15 spesies of Rutaceae, 13 spesies are from genus Citrus and 2 more Figure 3. Parts of medicinal plants used as medicines in sub- spesies are from other genera. The number of species of ethnic Batak Simalungun, North Sumatra. Rutaceae was relatively small in comparation to the other families, however, the frequency of species used was relatively high. Simalungun and Karo Districts are the centers of Citrus cultivation in North Sumatra. Sub-ethnic Batak Simalungun used eight species of Lamiaceae as medicinal plants, some of those were sibabi dalu (Paraphlomis javanica), silanglang kabungan (Coleus scutellarioides), simarihur-ihur niasu (Pogostemon auricularius), and terbangun (Coleus amboinicus) which have been known to be rich in essential oils, so they can be used to cure gastrointestinal disorders and fever. Solanaceae has been used to cure fractures latting (Solanum verbascifolium), and injury timbaho (Solanum nicotiana). In Brazil, Solanum nigrum have been used to cure anti depression (Giorgetti and Negri 2011). Our research also found that orchids (Orchidaceae) Figure 4. The corelation between age of respondents and means have been used for medicinal plants such as, salembar of medicinal plants known. 48 BIODIVERSITAS 16 (1): 44-54, April 2015
Table 2. Local and scientific names of medicinal plants in sub-ethnic Batak Simalungun of North Sumatra, Indonesia.
UVs Part 30-50 > 50 Key Family Scientific name Local name Use* ICS used years years infor- old old mants Acanthaceae Clinacanthus nutans Siborutiktik Leaves Gas, Fev 6.0 - 1.2 1.5 Graptophyllum pictum Silastom Leaves Ulc, Kid 36.0 1.0 1.2 1.5 Justicia gendarussa Sangke sempilit Leaves Fev, Bus 30.0 0.8 1.0 1.0 Parastrobilanthes Andalotung Leaves Gas, Fev 6.0 0.6 1.6 2.0 parabolica Psedeanthemum Topu arang Leaves Ash, Aph, Fev, Tt 36.0 - 2.2 2.8 acumiinatisimun Strobilanthes crispus Kecibeling Leaves Gas, Kid, Tt 30.0 0.8 1.0 0.8 Strobilanthes sp.1 Pijor holing Leaves Ash, Kid 42.0 0.6 1.4 1.5 Strobilanthes sp.2 Topu ringring Leaves Kid 33.0 - 0.6 0.8 Actinidiaceae Saurauia vulcani Sopsopan Leaves Dia, Gas, Inj, Tt 12.0 - 1.8 2.5 Amaranthaceae Celosia cristata Rudang Leaves Fev, Bus, Alg 13.5 - 1.4 2.0 Amaryllidaceae Crinum asiaticum Ompu-ompu Tuber Fra, Fev 45.0 1.2 1,6 1.8 Annonaceae Cyathocalyx virgatus Paet tandang Leaves Gas, Inj 9.0 - 0.4 0.5 Apiaceae Centella asiatica Papaga Leaves Gas, Kid, Inj 45.0 1.2 2.0 2.5 Apocynaceae Alstonia pneumatophora Rahu Bark Dia, DM 24.0 0.8 1.2 1.3 Araceae Acorus calamus Jarango Stem Fev, Bus, Alg 30.0 1.0 1.8 2.0 Colocasia esculenta Suhat sabah Stem Fev 6.0 0.8 0.4 0.8 Colocasia sp.1 Hau sangggir Tuber Fev 12.0 - 0.6 0.8 Arecaceae Areca catechu Pining Fruit Fra, Bus, Tt, 60.0 1.0 1.6 1.6 Arenga pinnata Bagot Root Fra, DM, Tt 30.0 0.4 0.8 2.0 Calamus caecius Malno Root Tt 9.0 - 0.8 0.8 Calamus cf. javensis Hotang pulogos Root Fra, Tt 6.0 - 0.8 1.0 Calamus sp.1 Hotang aek Root Tt 6.0 0.6 0.6 1.0 Calamus sp.2 Hotang kiskisan Root Fra, Tt 6.0 - 0.8 1.0 Calamus sp.3 Hotang rusrus Root Tt 6.0 - 0.8 0.8 Caryota cf. maxima Riman Root Tt 24.0 0.6 0.6 1.0 Caryota cf. mistis Andudur Root Tt 24.0 0.2 1.0 1.0 Cocos nucifera Kelapa Root, Fra, DM, Bus, Tt 60.0 1.8 1.6 2.0 fruit Cyrtostachys lakka Simarpining- Root Ash, Kid, Fev 4.5 - 1.6 1.3 pining Daemonorops sp.1 Hotang rutti Root Tt 6.0 - 0.8 0.8 Daemanorops sp.2 Boar-boar Root Tt 24.0 - 1.0 0.8 Korthalsia junghuhnii Hotang Root Fra, Tt 6.0 - 1.6 0.8 dadahanan Livistona sp.1 Baluhur Root Tt 24.0 - 0.8 1.0 Livistona sp.2 Biruh Root Tt 12.0 - 0.8 1.0 Nypa fruticans Nipah Root DM, Tt 24.0 - 0.6 1.0 Plectocomia cf. elongata Hotang Boar-boar Root Tt 6.0 - 0.8 1.0 Oncosperma filamentosum Libung Root Fra, Tt 15.0 1.0 1.4 1.5 Salacca zalacca Salak Fruit Gas 18.0 0.8 1.0 0.8 Asclepiadaceae Hoya sp.1 Simanisia Leaves Fra, Kid, Aph, Tt 12.0 - 0.4 2.0 Hoya sp.2 Tukkok matua Leaves Ash, Fra, Aph, Tt 109.0 1.6 2.0 3.3 sabungan Hoya sp.3 Tukkot matua Leaves Ash, Aph, Tt 93.0 - 2.4 2.8 boru-boru Asteraceae Ageratum conyzoides Ratusan Leaves Ulc, DM, Inj 24.0 2.2 1.8 2.3 Blumea balsamifera Galunggung Leaves Gas, Inj, Bus 24.0 1.2 1.6 2.0 Clibadium surinamense Longa begu Leaves Dia, Gas, DM, 45.0 1.6 2.4 2.5 somarittop Fev Chromolaena odorata Sihampir safari Leaves, Hyp, Dia, Gas, 106.0 - 4.8 6.0 fruit Ulc, Fev, Inj, Tt Chromolaena sp.1 Suwawa Leaves Gas, Fra, Rhe 45.0 3.0 1.8 2.5 Elephantopus scaber Malehan Leaves Inj 3.0 - 0.8 1.0 Eupatorium inulifolium Longa bengu Leaves Dia, Gas, DM 45.0 1.8 1.8 2.5 marittop Gynura crepidioides Payon baru Leaves Gas, Kid, Inj, Fev 45.0 1.6 1.8 2.5 Gynura sp.1 Sihorhor Leaves Gas, Fev 42.0 2.0 2.0 2.0 Mikania cordata Andor golat Leaves Dia, Gas 55.0 2.4 2.2 2.5 Spilanthes iabadicensis Sihampir Leaves Too 9.0 0.6 0.8 0.8 Balsaminaseae Impatiens platypetala Silundad Leaves Fev 9.0 0.8 0.8 1.0 Blechnaceae Blechnum orientale Padung-padung Leaves Fra, Fev 9.0 - 1.0 1.5 Blechnum sp.1 Pahu lipan Leaves Gas, Kid, Fev 6.0 - 1.2 1.8 SILALAHI et al. – Medicinal plants of Batak Simalungun, Indonesia 49
Bombacaceae Ceiba pentandra Habu-habu Leaves Fev 24.0 - 1.0 1.0 Ceiba sp.1 Kabu-kabu Leaves Fev 24.0 0.6 0.6 1.0 Durio zibethinus Durian Bark Gas 6.0 0.6 0.8 0.8 Caricaceae Carica papaya Botik Leaves Dia, Gas, Fev 54.0 1.2 1.8 2.0 Caryophyllaceae Drymaria cordata Rampas binei Whole Fev 18.0 0.4 0.6 1.0 Convolvulaceae Ipomoea batatas Gadong suwawa Leaves Gas, Ulc, Tt 99.0 1.0 3.0 3.0 Ipomoea sp.1 Hanawi Leaves Gas, Tt 3.0 - 0.6 1.0 Costaceae Costus speciosus Sibalik humosing Rhizome Aph 30.0 0.4 0.6 1.0 Costus sp.1 Tabar-tabar Rhizome Fev 9.0 - 0.8 1.0 Crassulaceae Kalanchoe pinnata Hatengget Leaves Ulc, Fev 18.0 - 1.8 1.5 Cucurbitaceae Benincasa hispida Gundur Fruit Gas, Sto 24.0 1.2 1.6 2.0 Cucumis sativus Ancimun Fruit Hyp 24.0 1.0 1.0 1.0 Lagenaria siceraria Tatabu Fruit Ash, Dia, Fra, Inj 9.0 0.8 1.4 1.8 Cyatheaceae Cyathea sp.1 Tanggiang Leaves Fev, Inj 24.0 0.8 1.0 1.5 Cyperaceae Cyperus rotundus Sitomu dalan Root Hyp, Ash, Kid 9.0 - 1.4 1.8 Dilleniaceae Tetracera scandens Pastulan Stem Eye 9.0 0.6 0.8 1.0 Euphorbiaceae Aleurites moluccana Gambiri Seed Dia, Gas, Sto, 129.0 2.2 3.2 4.5 Kid, Fev, Tt Bischofia javanica Sinkam Root, Dia, Gas, Sto, 102.0 2.0 2.2 3.8 bark DM, Inj Claoxylon indicum Topu hayu Leaves Ash, Alg, Tt 36.0 1.2 1.4 2.3 Euphorbia heterophylla Katemas Sap Gas 6.0 - 0.8 0.8 Homalanthus populneus Andulpak Leaves Fev, Bus 4.5 - 0.8 1.0 Jatropha curcas Dulang jawa Leaves Gas, Fev, Too 18.0 - 2.4 2.5 Mallotus philippinensis Sira lada Leaves Tt 4.5 - 0.6 0.5 Manihot utilissima Gadong hau Leaves Inj 6.0 0.6 0.8 0.8 Phyllanthus urinaria Tanduk erbuah Whole Hyp, Kid 24.0 - 1.6 1.5 Pimeleodendron Sibunbun Leaves Fra, Fev 3.0 - 0.4 0.8 griffithianum Ricinus communis Dulang bajora Leaves Gas, Fev 18.0 1.4 2.0 2.0 Sauropus androgynus Nasi-nasi Leaves Gas, Fev 36.0 1.0 1.8 1.8 Fabaceae Cassia alata Galinggang Leaves Itc 15.0 0.6 0.6 1.0 Cassia juncea Simarabal-abal Leaves Fra, Inj, Fev, Tt 90.0 - 1.8 2.3 Leucaena leucocephala Palia moka Leaves, Itc 4.5 - 0,6 0.8 seed Mimosa pudica Podom-podom Root Fra, Kid 15.0 - 1.4 1.4 Mimosa sp.1 Sihirput Root Cou, DM 1.5 0.8 1.2 1.8 Parkia speciosa Palia Bark, Gas, Itc 13.5 0.6 1.2 1.5 leaves Pithecolobium lobatum Jengkol Root, Gas, Fra 15.0 - 1.6 1.5 leaves Pterocarpus indicus Sona Sap Fev, Too 4.5 - 0.8 1.0 Psophocarpus Borong Leaves Inj, Tt, Tp 9.0 - 2.2 2.5 tetragonolobus Uraria lagopodioides Sibalince Leaves Fev 4.5 - 0.4 0.8 Vigna unguiculata Kacang safari Leaves Tt 30.0 0.8 1.0 1.0 Gesneriaceae Aeschynanthus cf. Hariari sendok Leaves Fev 9.0 - 0.4 0.8 horsfieldii Cyrtandra sp.1 Dilah swara Leaves Fra, Tt 18.0 - 0.8 0.8 Aeschynanthus sumatranus Simarhappilis Leaves Bus, Tt 24.0 - 1.4 2.0 Guttiferae Garcinia atroviridis Galugur Fruit Gas 24.0 - 0.6 1.0 Lamiaceae Coleus amboinicus Terbangun Leaves Ash, Gas, Inj, Tt, 45.0 2.4 2.6 2.8 Tp Coleus scutellarioides Silanlang Leaves Gas, Inj, Fev, Tt 66.0 - 3.2 3.3 kabungan Ocimum americanum Ruhu-ruhu Root Cou, Rhe 24.0 - 1.2 1.8 Paraphlomis javanica Sibabi dalu Root Aph, Tt 30.0 - 1.0 2.0 Pogostemon cablin Nilam Leaves Inj 12.0 0.8 1.0 1.0 Pogostemon auricularius Simarihur-ihur Leaves Fra, Fev, Alg, Tt 24.0 1.2 1.4 2.3 niasu Orthosiphon stamineus Kumis kucing Leaves Kid 30.0 1.0 0.6 1.0 Lauraceae Cinnamomum burmanii Kulit manis Leaves, Alg 24.0 0.4 0.8 1.0 Bark Cinnamomun cassia Sabal Bark Kid 24.0 - 1.0 1.0 Persea gratissima Pokat Leaves Kid 6.0 - 1.0 1.0 Liliaceae Allium cepa Bawang merah Tuber Cou, Dia, Gas, 96.0 2.2 3.6 8.0 Rhe, Ulc, Inj, Fev, Bus, Alg, Tt Allium chinense Hosaya Tuber Hyp, Dia, Gas, Itc, 90.0 3.8 4.8 6.0 Ulc, DM, Fev, Tt Allium sativum Bawang putih Tuber Hyp, Dia, Bus Tt 90.0 2.6 2.4 3.0 50 BIODIVERSITAS 16 (1): 44-54, April 2015
Cordyline fruticosa Silinjuang Leaves Hyp, Fev, Alg, 45.0 1.2 2.0 2.5 Bus Lomariopsidaceae Bolbitis heteroclite Pahu sayu Leaves Tt 18.0 - 0.6 0.8 Loranthaceae Loranthus sp.1 Sarindan kopi Leaves Kid, DM 36.0 0.8 0.8 1.3 Lycopodiaceae Lycopodium proliferum Limut-limut Whole App, Tt 9.0 - 1.8 1.3 mangolu Lythraceae Lawsonia inermis Hatirongga hau Leaves Gas 3.0 0.6 0.8 1.0 Malvaceae Abelmoschus moschatus Purba jolma Root, Fra, Tt 18.0 - 0.8 1.0 bark Hibiscus rosa-sinensis Bunga-bunga Leaves Fev, Tt 57.0 1.0 1.6 2.0 Hibiscus similis Baru Root Fra, Tt 18.0 0,8 1.6 2.0 Sida rhombifolia Sibaguri safari Root Fra, Inj 30.0 - 1.6 2.0 Sida ungulata Sibaguri Root Fra, Inj 39.0 1.6 1.8 2.0 Urena lobata Sampelulut Root, Fra 9.0 0.8 1.0 1.0 leaves Maranthaceae Donax cannaeformis Banban Leaves Ulc, Fev 12.0 0.4 1.4 1.5 Marattiaceae Angiopteris evecta Ingol Leaves Ulc 9.0 - 0.6 1.0 Melastomataceae Clidemia hirta Sanduduk Leaves Gas, Inj 36.0 1.0 1.6 2.0 Melastoma malabathricum Sanduduk Root, Gas, Inj 36.0 - 1.6 1.8 leaves Melastoma sylvaticum Sanduduk Leaves Gas, Inj 24.0 - 1.4 1.8 harangan Meliaceae Lansium domesticum Langsat Root, Gas 9.0 0.6 0.8 1.0 bark Menispermaceae Cyclea barbata Lakkup-lakkup Leaves Gas, Kid, Inj, Tt 15.0 1.2 1.4 1.8 Cycles sp.1 Andor hondali Leaves Fra, Tt 24.0 0.4 0.8 1.0 Tinospora crispa Raja panawar Stem Ash, Gas, Fra, 54.0 1.0 1.8 2.3 DM, Tt Tinospora sp.1 Siraja enus Leaves Gas 30.0 - 0.8 1.0 Moraceae Artocarpus communis Sukun Bark Hyp, Ash, Gas 72.0 1.0 1.4 2.5 Artocarpus elastica Torop Bark Dia, Gas, DM, Inj 36.0 1.4 2.4 2.5 Artocarpus heterophyllus Pinasa Fruit Gas 6.0 - 1.0 1.0 Ficus cf. deltoidea Siraja landong Leaves Ash, Tt 30.0 0.6 2.0 2.0 Musaseae Musa paradisiaca Pisang sitabar Stem Fev, Gas 38.0 1.2 1.4 1.4 Myrtaceae Eugenia aromatica Bunga lawang Flower Cou, Tp 39.0 1.6 1.6 2.0 Eugenia polyantha Salam Leaves Gas, Sto, Fev, DM 30.0 - 1.2 2.0 Eugenia sp.1 Murak Leaves Gas, Tt 45.0 1.4 0.8 1.5 Myristica fragrans Pala Seed Tt, Tp 36.0 1.4 1.2 1.8 Psidium guajava Jambu batu Leaves Gas, Sto, DM 42.0 1.4 1.4 2.0 Syzygium aromaticum Cengkeh Flower Cou, Ash, Alg, Tt 56.0 3.2 4.0 4.0 Myrsinaceae Ardisia sp.1 Gompang batu Leaves Eye 6.0 - 0.6 1.0 Nepentheceae Nepenthes garcilis Takkul-takkul Leaves Too 9.0 0.6 1.0 1.0 Ophioglossaseae Ophioglossum Sonduk-sonduk Whole Hyp, Fev, Tt 30.0 - 1.2 1.8 pedunculosum Orchidaceae Anoectochilus reinwardtii Suratan ilik Whole Hyp, Ash, Aph, 96.0 1.8 3.6 3.3 Bus, Tt Macodes sp.1 Suratan ilik Whole Tt 96.0 1.8 3.6 3.3 Goodyera rubicunda Gadong harangan Tuber Dia, Tt 54.0 - 1.4 2.0 Nervilia aragoana Salembar sabulan Tuber Tt 35.0 - 0.6 1.0 Nervilia plicata Salembar satahun Tuber Ash, Tt 30.0 - 1.4 2.0 Phaius callosus Sukkit katari Tuber Hyp, Ash, Tt 18.0 - 1.6 2.8 Oxalidaceae Oxalis corniculata Saripitpit gawang Whole Cou, Fev, Thr, Tt 12.0 - 1.8 2.8
Oxalis sp.1 Saripitpit Whole Kid, Fev, Alg, Tt 30.0 - 1.8 2.5 Phyllataceae Breynia cerma Podom-podom Whole Fev 3.0 - 0.6 0.6 Piperaceae Piper betle Demban Leaves Itc, Inj, Fev, Eye, 120.0 - 2.6 4.8 Thr, Bus Piper crocatum Demban siangir Leaves Itc, Inj, Eye, Bus 24.0 - 1.4 2.0 Piper nigrum Lada Seed Rhe, Fev, Bus, Tt, 120.0 1.0 2.4 3.5 Tp Piper umbellatum Gombalayo Leaves Bus, Tt 24.0 0.6 0.8 0.8 Piper sp.1 Dilah horbo Leaves Fra, Tt 24.0 - 0.8 0.8 Piper sp.2 Bursik horbo Leaves Fra, Tt 24.0 - 0.8 1.0 Plassifloraceae Adenia cordifolia Ancimen riris Whole Hyp 9.0 0.4 1.0 0.8 Poaceae Andropogon nardus Sangge-sangge Stem Fev 24.0 - 0.8 0.8 dipar Bambusa horsfieldii Bulu bolon Root DM, Tt 18.0 0.2 1.8 1.8 Bambusa spinosa Bulu duri Root Fra, Bus, Tt 18.0 0.4 1.6 2.0 Cymbopogon citratus Sangge-sangge Stem Alg, Tt, Tp 45.0 1.8 1.6 2.5 Dendrocalamus asper Bulu sonduk Root Tt 9.0 - 0.8 0.8 Lophatherum gracile Sidayok jagur Root Tt 30.0 - 0.4 0.8 SILALAHI et al. – Medicinal plants of Batak Simalungun, Indonesia 51
Paspalum conjugatum Sarang buaya Leaves Inj 12.0 0.8 0.8 1.0 Scleria laevis Bonang sawi Leaves Tt 9.0 - 0.8 0.8 Schizostachyum blumei Bulu hayan Root DM, Tt 18.0 - 1.6 2.0 Schizosstachyum Bulu suling Root Tt 9.0 0.6 1.0 1.0 brachycladum Schizostachyum sp.1 Bulu laga Root DM, Tt 18.0 - 1.6 2.0 Schizostachyum sp.2 Bulu lomang Root Tt 18.0 0.4 1.0 1.0 Schizostachyum sp.3 Bulu balakki Root Fra, Tt 9.0 0.6 1.0 1.0 Scleria purpurascens Ria-ria Leaves Fra, Kid, Tt 1.5 - 0.8 1.8 Scleria sp.1 Oma-oma Leaves Inj, Tt 6.0 - 1.2 1.3 Thysanolaena sp. Bulu moria Root Fra, Tt 18.0 - 1.8 2.0 Polypodiaceae Pyrrosia sphaerotrichia Pandukkap Leaves Tt 30.0 - 0.6 1.0 naburuk Platycerium coronarium Raja pinayungan Leaves Bus, Tt 3.0 - 0.6 1.0 Primulaceae Ardisia japonica Sibukkar Leaves Tt 3.0 - 0.6 0.8 Rosaceae Robus moluccanus Hupi-hupi Leaves Dia, Gas, Sto, Tt 54.0 - 2.0 2.5 Rubiaceae Morinda citrifolia Mengkudu Fruit DM 9.0 0.6 0.6 0.8 Neonauclea calycina Algit Leaves Fra, Kid 33.0 0.2 1.4 1.3 Paederia verticillata Salaun bulung Leaves Fev 9.0 0.6 0.6 0.5 Uncaria gambir Gambir Leaves Dia, Gas, Sto, Bus 96.0 1.6 1.2 3.0 Rutaceae Citrus aurantium Utte bunga Root, Fra, Fev, Tt 36.0 1.6 2.4 1.8 fruit Citrus hystrix Utte mungkur Root, Fra, Bus, Alg, Tt 90.0 2.0 2.8 2.8 fruit Citrus maxima Utte bolon Root, Fra, Tt 18.0 - 1.4 1.5 fruit Citrus medica Utte gawang Root, Fra, Tt 12.0 - 1.0 1.0 fruit Citrus mitis Utte kasturi Root, Fra, Fev, Bus, Tt 9.0 - 1.6 1.5 fruit Citrus nobilis Utte puraga Root, Tt 9.0 - 0.8 1.0 fruit Citrus sp.1 Utte begu Root, Fra, Bus, Tt 18.0 - 1.2 2.0 fruit Citrus sp.2 Utte hajor Root, Tt 12.0 - 0.8 1.5 fruit Citrus sp.3 Utte hayu Root, Fra, Tt 9.0 - 1.0 1.5 fruit Citrus sp.4 Utte kejaren Root, Fra, Tt 9.0 - 0.8 1.0 fruit Citrus sp.5 Utte rihit Root, Tt 9.0 - 0.8 0.8 fruit Ruta angustifolia Soriangin Leves Gas, Fev 9.0 0.8 1.2 1.0 Zanthoxylum Tuba Fruit Cou, Tt 60.0 1.4 2.0 2.0 acanthopodium Sapindaceae Nephelium lappaceum Rambutan Leaves, Gas, Fev 9.0 - 1.2 1.8 bark Sapotaceae Achas zapota Sawo Fruit Gas 6.0 0.6 0.6 1.0 Schisandraceae Kadsura scandens Sibau sira Leaves Gas, Fra, Inj 4.5 - 0.6 1.0 Kadsura sp.1 Lendir sidarih Leaves Fev 12.0 - 0.6 1.0 Scrolphulariaceae Lindernia crustacea Simaragong- Leaves Inj, Fev, Thr, Alg 24.0 - 2.2 1.3 angong Lndernia liman Siang-siang Whole Fev 9.0 - 1.2 1.0 Lindernia viscosa Pogu ni tano Leaves Gas, Kid, Alg 24.0 - 2.2 2.2 Simaroubaceae Eurycoma longifolia Horis kotala Whole Ash, Fra, Aph, 72.0 - 2.6 3.3 Fev, Tt Smilaceae Smilax sp.1 Udut tulan Whole Ash, Aph 72.0 - 1.0 1.0 Solanaceae Capsicum frutescens Lasina Leaves Ulc 24.0 0.8 1.0 1.0 Solanum lycopersicum Tomat Leaves, Hyp, Inj, Fev 18.0 1.4 1.2 2.3 fruit Physalis angulata Pultak-pultak Whole Fev 30.0 1.4 1.6 1.8 Solanum nicotiana Timbaho Leaves Inj, Too, Bus 60.0 0.8 1.6 2.0 Solanum schiffnerianum Saur paet Fruit Gas, Inj, Fev 24.0 1.2 1.0 2.0 Solanum torvum Rimbang Leaves, Ulc, Eye 36.0 - 1.8 2.0 fruit Solanum verbascifolium Latting Leaves, Gas, Fra, Tt 72.0 2.0 2.4 2.8 fruit Theaceae Eurya japonica Samoja Leaves Tt 12.0 - 0.6 1.0 Eurya sp.1 Raru Bark Gas, DM 45.0 - 1.4 1.8 Urticaceae Elatostema strigosum Sisik naga Leaves, Hyp, Ash, Gas Inj, 30.0 0.4 2.8 3.3 fruit Fev 52 BIODIVERSITAS 16 (1): 44-54, April 2015
Elatostema sp.1 Sihip Root Kid, Alg, Tt 18.0 - 1.8 1.8 Leucosyke capitellata Simarhambing- Leaves Kid, Alg, Tt 30.0 1.0 1.2 1.5 hambing Usneaceae Usnea barbata Tois alogo Whole Alg, Tt 12.0 - 0.8 1.5 Verbenaceae Clerodendrum calamitosum Simarbakkudu Leaves Ash, Gas, Fev, 9.0 - 1.6 2.3 Alg, Thr Clerodendrum fragrans Burta-burta Leaves Cou, Gas, Itc, Inj 30.0 - 3.0 3.3 Stachytarpheta indica Odor-odor Leaves Fev 4.5 - 0.8 0.8 Vitex trifolia Sialagundi Leaves Hyp, Gas, Kid 33.0 - 2.2 2.0 Vitaceae Ampelocissus thyrsiflora Sibalik kortas Leaves Ash, Gas, Sto, 45.0 - 2.0 4.0 Aph, Tt Pterisanthes polita Siporgis laga Leaves Aph, Fev, Tt 30.0 - 1.8 2.5 Zingiberaceae Alpinia galanga Halaos Rhizome Fev, Itc, Dia, Gas, 56.0 2.2 2.8 3.8 Rhe, Tt, Tp Alpinia sp.1 Laja Rhizome Dia, Gas, Tt 112.0 - 2.6 2.8 Boesenbergia pandurata Sitomu hursi Rhizom, Fev, Gas, Tt, Tp 30.0 1.2 1.4 2.3 leaves Curcuma domestica Hunik Rhizome Dia, Gas, Sto, Inj, 142.0 3.2 2.6 4.0 Fev, Eye, Alg, Tt, Tp Curcuma xanthorrhiza Tomulawak Rhizome Ash, Sto, DM, 108.0 3.6 3.6 4.8 Fev, Inj, Tt Etlingera eliator Rias Leaves, Cou, Ulc, Tt, Tp 54.0 1.2 1.4 2.0 stem Etlingera sp.1 Sihala Rhizom, Ash, Tt 30.0 2.6 4.0 3.8 stem Etlingera sp.2 Kambing bajar Rhizome Tt 30.0 - 0.6 1.0 Kaempferia galanga Hasohor Rhizome Cou, Ash, Gas, 90.0 1.6 3.2 5.8 Sto, Rhe, Aph, Fev, Alg, Tt Zingiber americanus Lampuyang Rhizome Dia, Gas, Tt 18.0 1.6 2.2 2.8 Zingiber officinale Pege Rhizome Gas, Sto, Inj, Fev, 112.0 2.2 2.6 4.6 Aph, Tt, Tp Zingiber purpureum Bungle Rhizome Dia, Gas, Tt 114.0 2.2 1.8 2.5
Note: Alg (Alogo-alogo), Aph(Aphrodisiac), Ash (Ashma), Bus (Busung), Cou (Cough), Dia (Diarrhea), DM (Diabetes mellitus), Eye (Eye infection), Fev (Fever), Fra (Bone fractures), Gas (Gastrointestinal disorders), Hyp (Hypertension), Inj (Injury), Itc (Itchy), Kid (Kidney disease), Rhe (Rheumatism), Sto (Stomach ache), Thr (Thrush), Too (Toothache), (Tp) Tinuktuk paranggetek, Tt (Tinuktuk tawar), Ulc (Ulcer).
Plant parts used as medicinal umbellatum), and salam (Eugenia polyantha). Leaves have Parts of the plants used as medicinal plants were the been used as medicines for injuries (Ageratum conyzoides, leaves, stems, roots, bark, sap, flowers, fruits, seeds, and Centella asiatica), gastrointestinal disorders (Blumea whole sections. The species composition consisted of balsamifera, Coleus ambonicus, Eugenia polyantha), and leaves (119) and roots (54), flowers and the sap (2), as it is kidney diseases (Strobilanthes crispus, Orthosiphon shown in Figure 3. Bioactive compounds used as medicinal stamineus). The medicinal plants used by local plants are produced and stored in leaves, stems, roots, communities to cure kidney diseases and injuries were flowers, and seeds. For example, asiaticoside of Centella those whose leaves have rough-surface. Those leaves have asiatica utilized as anti-inflammantory is stored in the been identified to be able to destroy kidney stones and stop leaves, whereas ajmalicine of Catharanthus roseus used as bleeding in injuries. Flanol of leaves of Ageratum antihypertensive medicine is stored in the roots (Joy et al. conyzoides has been known to cure injuries (de Padua 1998). 1999). The usage of medicinal plant parts depends on the The number of medicinal plants whose whole parts purpose of curing. It seemed that the local communities were used, were relatively fewer than those whose only knew exactly the efficacy of every part of plants. For some parts (leaves, roots, or fruits) are utilized. Factors that example: flowers and leaves of sampelulut (Urena lobata) encourage the use of whole plants parts were the relatively were used to cure fever, while the root was used as a small size of the plants (Anoectochilus reinwardtii, medicine for fractures. One of the bioactive compound of Ophioglossum pedunculosum) and the difficulty in Urena lobata leaves is acetic acid which serves as separating the parts of plant organs (Phyllanthus urinaria). analgesic (Islam et al. 2012), so that it can be used as a The utilization of whole plant has resulted in the death of fever medicine. the plants, so that some of these medicinal plants, for There were 119 species or about 50% of the medicinal example suratan ilik (Anoectochilus reinwardtii) and plants whoseleaves were used, such as: galunggung sonduk-sonduk (Ophioglossum pedunculosum) have been (Blumea balsamifera), ratusan (Ageratum conyzoides), hard to find in the wild. papaga (Centella asiatica), gombalayo (Piper SILALAHI et al. – Medicinal plants of Batak Simalungun, Indonesia 53
There were 11 species of medicinal plants whose medicinal plants with the highest value of ICS (142.0) was rhizomes were used as medicines, and 9 species whose hunik (Curcuma domestica) and the lowest value (1.5) tubers were used as medicines. Medicinal rhizomes were were ria-ria (Scleria purpurascens) and sihirput (Mimosa derived mainly from Zingiberaceae (Boesenbergia sp.). Medicinal plants that show high value on ICS are pandurata, Curcuma xanthorrhiza, Curcuma domestica, those which have many usages and are utilized frequently Zingiber officinale), while the tubers from Orchidaceae by local communities, while those having low value on ICS (Nervilia aragoana, Nervilia plicata) and Liliaceae (Allium have fewer usage and are rarely used. cepa, Allium sativum). The rhizomes of Zingiber officinale The plants with medium ICS value were, among others, contain gingerol, shagaol, and gingerdion that has strong garlic (Allium sativum), ompu-ompu (Crinum asiaticum), effect to cure gastrointestinal disorder (Achmad et al. 2008). and poyon baru (Gynura crepidioides). The value of ICS The local communities know the growth of medicinal on sub-ethnic Batak Simalungun was higher than that of plants in nature. For example, Nervilia aragoana is plant in ethnic Malays (Susiarti et al. 2005), but lower than that of the local languange called salembar sabulan (has only one sub-ethnic Batak Karo (Silalahi et al. 2013). The usage of piece of leaf in a month), while Nervilia plicata is called medicinal plants is strongly influenced by culture, spiritual salembar satahun (has only one piece of leaf in a year). beliefs of local communities (Cocks and Dold 2006), and Naturaly both of the orchids grow very slowly; therefore geography (Pieroni 2001). utilization of these plants may lead to their extinction. IUCN (2010) noted that Nervillia plicata and Nervillia Correlation between age and utilization aragona have been categorized as protected plant. One of the approaches used to determine usage value of The roots of horis kotala (Eurycoma longifolia), sinkam medicinal plants is carried out by calculating the use value (Bischofia javanica), andudur (Caryota cf. mitis), and (UVs). The UVs depends on the number of medicinal pining (Areca catechu) grow above ground. Those species plants used and known by respondents or the local have only one main root; therefore taking their roots kills communities. Age structure seemed to influence on the them. This kind of harvesting accelerates the extinction of sub-ethnic Batak Simalungun UVs of the medicinal plants, Eurycoma longifolia. In sub-ethnic Batak Simalungun roots the younger (30-50 years old) having lower value than the of Eurycoma longifolia were used as medicines for fever older age group (>50 years old). For example, the UVs of and aphrodisiac. Bioassay of root extract of Eurycoma Allium cepa was 2.2 in the younger group, 3.6 in the older longifolia improves sexual activity in mice and make their group, and 8.0 for key informants (Table 2). The coitus longer. That makes this plant appropriate to be used differences of UVs (Table 2) shows the degradation of the as aphrodisiac (Ang and Ngai 2001). local knowledge in terms of traditional medicines. There were 14 species of plants whose bark was used as Beside having lower Uvs, the younger group knew medicines, such as raru (Eurya sp.), kulit manis significantly (P=0.05 on Anova) fewer species of medicinal (Cinnamomum burmanii), and sinkam (Bischofia javanica). plants (48.19 ± 8.35 species) than the older (170.19 ± 18.38 Raru and Sinkam have been used primary as medicines for species), and key informants (202. 00 ± 12.32 species) as diabetes mellitus. The usage of raru as medicine for shown in Figure 4. diabetes mellitus has been derived from the custom of local The number of medicinal plants species known by the communities habit of drinking tuak (traditional beverage of younger group was only 28.31% of those by the older sub-ethnic Batak). After having dinner they will drink tuak group and only 23.85% of those by the key informants. with seasoning made from the bark of Sinkam. Tuak is sap Therefore, it is clear that local knowledge of the usage of of Arenga pinnata, which is mixed with the bark of raru. It medicinal plants has declined and has not been passed into is believed to decrease blood sugar level. To prove the the younger generation. This degradation is due to: (1) medicinal effect of Bischofia javanica and Eurya sp., difficulty in passing this information through oral ways to phytochemistry and bioassay analysis need to be the young generation (2) Changes in cultural value, (3) the conducted. Over exploitation of the plants, especially their availability of modern medical system. That the younger bark harvested directly from the forest may cause age had less interest in local knowledge on medicinal extinctions. plants was also found by Caniago and Siebert (1998), Voeks (2007), Guimbo et al. (2011).. The documentation of Index of Cultural Significance (ICS) and Use Value local knowledge in a written form is considered to be the (UVs) of medicinal plants best alternatives to avoid the degradation of the local The ICS of medicinal plants is a quantitative method knowledge and as a first step for the conservation of used by ethnobotanists to determine the cultural value of medicinal plants (Suryadharma 2010). plants. Based on their uses, the plants were grouped into 5 A total of 239 species of medicinal plants (170 genera, categories, namely: >200 (very high), 100-199 (high), 20- 70 families) were used by sub-ethnic Batak Simalungun of 99 (medium), 5-19 (low), and <5 (very low) (modified North Sumatra, to cure 20 diseases (18 natural disease, 2 from Pieroni 2011). The medicinal plants with medium supra natural disease) and to make 2 kinds of traditional values of ICS had the highest number of species (113), and concoction. The local knowledge of medicinal plants was followed by low categories (98), very low categories (16), lower in the younger generation (between 30-50 years old) and high categories (11) (Tabel 2). than that of the older group (>50 years old) and key The value of medicinal plants in the sub ethnic Batak informants (mostly shamans) both in number of known Simalungun varied between 1.5 to 142.0 (Table 2). The species and use 54 BIODIVERSITAS 16 (1): 44-54, April 2015
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Screening and analysis of the Islam MT, Ibrahim M, Ahsan MQ, Chowdhury MMU, Hossain MA, potential bioactive components in rabbit plasma after oral Rashid MA. 2012. Phytochemical and pharmacological investigations administration of hot-water extracts from leaves of Bambusa textilis McClure. Molecules 17: 8872-8885. BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 55-61 DOI: 10.13057/biodiv/d160107
DNA barcoding and phylogenetic reconstruction of shark species landed in Muncar fisheries landing site in comparison with Southern Java fishing port
PREHADI1, ANDRIANUS SEMBIRING2, EKA MAYA KURNIASIH1,2, RAHMAD1, DONDY ARAFAT1, BEGINER SUBHAN1, HAWIS H. MADDUPPA1,♥ 1Department of Marine Science and Technology, Faculty of Fisheries and Marine Science, Bogor Agricultural University (IPB), Jl. Darmaga Raya, Bogor 16680, West Java, Indonesia. Telp/Fax +62 85693558653, ♥email: [email protected] 2Indonesian Biodiversity Research Center, Jl. Raya Sesetan Gg. Markisa No. 6, Denpasar 80223, Bali, Indonesia.
Manuscript received: 31 October 2014. Revision accepted: 4 Desember 2014.
Abstract. Prehadi, Sembiring A, Kurniasih EM, Arafat D, Subhan B, Madduppa HH. 2015. DNA barcoding and phylogenetic reconstruction of shark species landed in Muncar fisheries landing site in comparison with Southern Java fishing port. Biodiversitas 16: 55-61. Sharks are one of main fisheries commodity that are currently exploited on a large scale because of their high economic value. The identification of sharks has been a difficult one due to the specimen’s similarity in morphology and mostly have had key diagnostic features removed. This study aimed to identify and to review the status of sharks, and also to reconstruct the shark species that were landed at South Java fishing port using molecular approaches. The DNA amplification was using cytochrome oxidase I mitochondrial of locus and 600-700 basepairs. A total of seven species from 59 individuals was identified including Alopias pelagicus, Carcharhinus falciformis, C. sorrah, C. amblyrhynchos, Galeocerdo cuvier, Atelomycterus marmoratus, and Spyrna lewini. The diversity of shark species landed in Muncar during the last 2 years has been decreased. The identified sharks species in this study sites were about 18% of all Indonesian sharks. The result of this study is expected help the Government to manage shark fisheries in Indonesia.
Keywords: DNA barcoding, Muncar, phylogenetic, sharks, southern Java.
INTRODUCTION Cilacap of Central Java and Palabuhanratu in West Java (White et al. 2006). Sharks has been greatly exploited in various countries The identification of sharks has been a difficult one due across the globe, including Indonesia, which ranked first in to the specimen’s similarity in morphology and mostly the list of the 20 biggest shark fishing countries above have had key diagnostic features removed. In recent years, India, Spain, Taiwan and Argentina between 2002-2011 molecular approach has been able to give solutions in (Mundy et al. 2013). During that period, Indonesia has identifying shark species, especially when the taxonomy been exporting 10,762 tons of shark fins or 13% of the total method is impossible to conduct due to insufficient world exports (Mundy et al. 2013). morphological information such as ones that has been The biological characters of shark are making them implemented on shark fin and fillet (Smith et al. 2001). vulnerable to exploitation. In their natural habitat, sharks Hebert et al (2003) introduced DNA barcode method with are known to be slow in reaching maturity stage (8-13 mitochondrial marker for all animal species, for one chain years) and also low reproduction level (Camhi et al. 1998). of gene is claimed to be enough for distinguishing one The effect from shark fisheries is damaging and hence the species to another. DNA barcoding method uses primer in fast decreasing population of shark in the wild as proved by PCR (Polymerase Chain Reaction) process to amplify the a number of studies in Northwest Atlantic, Southeast DNA until around 600-700 bp on cytochrome oxidase I Australia, Gulf of Mexico, South Africa and Australian (COI) locus of mitochondrial. DNA barcoding method has Great Barrier Reef (Holden 1973; Casey and Myers 1998; been used to identify over 207 species of fish in Australia Graham et al. 2001; Baum and Myers 2004; Baum et al. including 143 species of teleostean, 61 species of shark and 2005; Dudley and Simpfendorfer 2006; Robbins et al. stingrays, and 3 species of chimaerid (Ward et al. 2008). 2006; Burgess et al. 2005). Population decline occurred as There are around 35 species of sharks that has been an effect from intensive and continuous fishing due to fished in Indonesia based on DNA barcoding analysis unmanaged and unregulated fisheries (Dharmadi and (Sembiring et al. 2014). As many as 10 species of shark has Fahmi 2005). The main problem is that the data given from been recorded in Cilacap and 6 others in Palabuhanratu the port is only the volume of total production without through DNA barcoding method (Sembiring et al. 2014). describing the shark species and the total individuals Phylogenetic is a description of relationship based on DNA caught, for example in Muncar fish landing site (UPPPP sequence composition or protein which resembles to that of Muncar 2013). Muncar is one of the ports that plays an a tree to estimate the past evolution process (Baldauf important role in shark fishing in Southern Java, aside from 2003). Phylogenetic reconstruction is able to analyze the 56 BIODIVERSITAS 16 (1): 55-61, April 2015 gene distance through DNA variation with Neighbor Joining I (COI) gene was amplified by polymerase chain reaction Tree method (Saitou and Nei 1987) that is capable on (PCR) using the forward primer fish-BCL (5' TCA ACY calculating the distance which is shown with bootstrap value. AAT CAY AAA GAT ATY GGC AC '3) and reverse The current study was conducted to identify shark primer fish-BCH (5'ACT TCY GGG TGR CCR AAR AAT species landed in Muncar, Banyuwangi, East Java in 2013, CA '3) (Baldwin et al. 2009). PCR amplifications were and to reconstruct phylogenetic tree between species found performed in 26 µL reaction mixture containing 2 µL 25 in Muncar compared with Cilacap and Palabuhanratu mM MgCl2, 2.5 µL 8μM dNTPs ; 1.25 µL each primer pair which previously has been analyzed through DNA 10 mM; 0,125 µL Taq DNA polymerase, 2.5 µL 10xPCR barcoding (Kurniasih 2013; Rahmad 2013). Buffer, 2 µL DNA template, 14.5 µL deionize water (ddH2O). Cycling parameters were an initial denaturation at 95°C for 2 min followed by 35 cycles of denaturation MATERIALS AND METHODS (94°C for 30 s), annealing (50 °C for 30 s), and extension (72°C for 45 s) with the final extension step at 72°C for 2 Sample collection min. PCR-amplified DNAs were visualized on 1% agarose The tissue sample of shark were collected from three gels. Prior to sequencing, excess dNTPs and fisheries landing site in Java Island (Indonesia), i.e.: oligonucleotides were eliminated from the PCR product Muncar, Palabuhanratu and Cilacap (Figure 1). A total of using shrimp alkaline phosphatase and exonuclease I (Exo- 59 samples were collected in Muncar in July 2013. The SAP-IT kit; Affymetrix, Santa Clara CA, U.S.A.) following tissue sample was stored in 95% ethanol. In 2012, the manufacturer’s protocol. Sequence reactions were samplings were done in 2 days covering all warehouses in performed in both directions using the BigDye terminator Muncar, while the recent research was done within 30 days v3.1 cycle sequencing kit (Applied Biosystems), 8-10 μL when all the catch is landed from ships. purified PCR product, and 4-5 μL of either primer (3 μM) per reaction. Sequence-reaction products were loaded into PCR extraction, amplification, and sequencing an ABI 3130xl automated sequencer (Applied Biosystems) DNA was extracted using 10% chelex (Walsh 1991). at the Berkeley Sequencing Facility located in the United The DNA extracts were stored at -30°C until required for States (Sanger et al. 1997). laboratory analyses. The mitochondrial cytochrome oxidase
Figure 1. Sampling location in three main fisheries landing site in Indonesia (Muncar, Palabuhanratu, and Cilacap), located in Jawa Island (blue circle). PREHADI et al. – DNA barcoding of sharks 57
Data analysis species are not evaluated by CITES, but Sphyrna lewini is Forward and reverse sequences were proofread, aligned included Appendix II. and edited using MEGA 5.2 (Tamura et al. 2011). Edited sequences were deposited in GENBANK Shark species landed in Muncar in 2012 and 2013 (http://www.ncbi.nlm.nih.gov/). The nucleotide sequence Table 2 describes sharks species landed in Muncar for data will be matched with the data contained in GenBank at the last 2 years and were identified using DNA barcoding. the NCBI (National Center for Biotechnology Information) C. falciformis was the most collected species within two for species identification by using BLAST (Basic Local sampling period. There was a slight different in species Alignment Search Tool) in website address identified between two period of sampling (2012 and http://blast.ncbi.nlm.nih.gov/Blast.cgi. A neighbor joining 2013). Low number of species was recorded in 2013 (7 phylogenetic trees was reconstructed in MEGA 5.2 species) compared with in 2012 (11 species), even though (Tamura et al. 2011) using Kimura-2-parameter models sampling duration was longer in 2013 (30 days) than in (Kimura 1980) with 1000 of bootstrap value. Samples that 2012 (2 days). have been analyzed is then compared with samples from The huge differences of duration of the sampling and Palabuhanratu and Cilacap (39 and 35 samples, the number of species observed might be indication in respectively). Furthermore, the data from July 2013 from declining shark population in the wild. However, many Muncar will be compared to catch from August 2012. A factors could influence on status of exploited species, such review of the conservation status was determine with IUCN as type of gear, location fished, biological characters of (2014), and the trade status was determine in CITES shark as migratory species (Lynch et al. 2011). (2014). The near threatened species are the population that The number of shark species being exploited in Muncar is in danger of declining in the near future if nothing can be reached 14 species or around 18% of the entire shark done to prevent it. Vulnerable species are those who have a species found in Indonesia (White et al. 2006). That high risk of extinction in the wild (IUCN-SSC 2001). number can be considered as huge in shark fishing, as sharks greatly varied in terms of maturing and young being produced (Castro and Mejuto 1995). Based on these facts, RESULTS AND DICUSSION it is inevitable that proper shark fishing management is urgent to be implemented in Muncar, Banyuwangi, East Java. DNA barcoding, conservation status, and trading status A total of seven species from 59 tissue samples belongs Table 2. The number of individual of identified shark species to four different families (Alopiidae, Carcharhinidae, landed in Muncar between two period sampling (2012 and 2013) Scyliorhinidae, and Sphyrnidae) has been successfully through DNA barcoding identified (Table 1). Family of Carcharhinidae is the most common family found in Muncar with four species with a Species 2012 2013 total of 46 individuals. 41 of those belong to species of Carcharhinus falciformis 6 41 Carcharhinus falciformis (Silky shark). Carcharhinidae Carcharhinus brevipinna 5 - Family is the most commonly caught might be due to their Carcharhinus limbatus 1 - diversified habitat or fishing gear used by fishermen. The Carcharhinus sorrah 2 2 number of Sphyrnidae Family found in Muncar is 11 Galeocerdo cuvier 1 2 individuals which consist of a single species, Sphyrna Hemitriakis indroyonoi 4 - Mustelus lenticulatus 6 - lewini or scalloped hammerhead. Alopias pelagicus 3 1 All sharks identified in Muncar have been assessed by Alopias superciliosus 1 - IUCN: one species is categorized as Threatened (Sphyrna Isurus oxyrinchus 1 - lewini), five species categorized as near threatened Prionace glauca 1 - (Carcharhinus, C. amblyrhynchos, C. sorrah, Galeocerdo Carcharhinus amblyrhynchos - 1 cuvier, and Atelomycterus marmoratus) and 1 other species Sphyrna lewini - 11 is categorized as vulnerable (Alopias pelagicus). Most Atelomycterus marmoratus - 1
Table 1. Identified shark species landed in Muncar using BLAST program, along with IUCN and CITES status
Max. No. of Red List Status CITES status Family BLAST analysis Common name Similarity indivi- (2014) (2014) (%) dual Alopiidae Alopias pelagicus Pelagic Thresher 100 1 Vulnerable Not evaluated Carcharhinidae Carcharhinus falciformis Silky Shark 100 41 Near threatened Not evaluated Carcharhinus amblyrhynchos Grey Reef Shark 99 1 Near threatened Not evaluated Carcharhinus sorrah Spot-tail Shark 100 2 Near threatened Not evaluated Galeocerdo cuvier Tiger shark 100 2 Near threatened Not evaluated Scyliorhinidae Atelomycterus marmoratus Coral catshark 99 1 Near threatened Not evaluated Sphyrnidae Sphyrna lewini Scalloped Hammerhead 100 11 Endangered Appendix II 58 BIODIVERSITAS 16 (1): 55-61, April 2015
Phylogenetic reconstruction Figure 3 describes phylogenetic reconstruction of C. A total of seven clades with a bootstrap value of 100 falciformis from 3 locations and formed 2 different clades which means they possess close kinship between with both bootstrap value of 65 therefore not really strong individuals (Figure 2). The large group consists of species to hold the position if added by another individuals, but such as Carcharhinus falciformis, C. sorrah, C. these two clades will still be different nevertheless. There is amblyrhynchos, Galeocerdo cuvier, Alopias pelagicus, one clade which the individual is a C. falciformis from Sphyrna lewini, and Atelomycterus marmoratus. Palabuhanratu, but on the other side there is one other Cladogram could be used to show that in every family there clade. It indicates that there are two different genetic are species which is located very close. This indicates that groups of C. falciformis in Palabuhanratu, which means the study on a species of one particular family could be that they come from two different populations (Zhao et al. described through phylogenetic reconstruction (Zuazo and 2013) in Southern Java and proved how wide the Agnarson 2010). distribution of this species, from Southern Java to Bali Sea (White et al. 2006).
Figure 2. The Neighbour-joining tree based on COI sequence data using Kimura-2-parameter substitution model with 1000 bootstrap, from shark species landed in Muncar in 2013. PREHADI et al. – DNA barcoding of sharks 59
Phylogenetic reconstruction of Carcharhinus on 2006, C. limbatus can be found throughout Southern brevipinna landed in Muncar was divided into two clades Java Sea until South China Sea. Sphyrna lewini was with bootstrap value of 88-89 (Figure 4.A). Differences divided into two different clades between Muncar and between these two branches are pretty strong (100% Cilacap (Figure 4.C). This indicates that the aggregate bootstrap value) and indicate these individuals might come location of this species is separated between Southern Java from different population. The distribution of this species and Northern Java, because according to their behavior, covers the central sea areas of Indonesia (White et al. this species is likely to seek the same shelter with their own 2006). The species of Carcharhinus limbatus consists of groups, usually in underwater valley basin of sea two different clades between from data pooled of mountains (Klimley et al. 1983). S. lewini is a species that Palabuhanratu and Muncar (Figure 4.B). It could be seen could be found widely distributed throughout Indonesian from the cladogarm that each of species grouped according Seas. However, it was unclear where and how fishermen to the locations respectively. Based on White experiment catch this species.
Figure 3. Phylogenetic reconstruction of Carcharhinus falciformis landed in landed in Ports in Southern Java for location, using the Neighbour-joining tree based on COI sequence data using Kimura-2-parameter substitution model with 1000 bootstrap. 60 BIODIVERSITAS 16 (1): 55-61, April 2015
A
B
C
Figure 4. Phylogenetic reconstruction of pooled data of Carcharhinus brevipinna (A), Carcharhinus limbatus (B), and Carcharhinus limbatus (C) landed in three ports in Southern Java. PREHADI et al. – DNA barcoding of sharks 61
The diversity of shark species landed in Muncar during Holden MJ. 1973. Are long-term sustainable fisheries for elasmobranchs the last two years has been decreased, even though possible? In: Parish BB (ed) Fish stocks and recruitment. ICES Rapp Proc Verb 164: 360-367. sampling efforts was prolonged in 2013. The identified IUCN [International Union for Conservation of Nature and Natural sharks species in this study sites were about 18% of all Resources]. 2014. The IUCN Red List of Threatened Species. Version Indonesian sharks. The phylogenetic reconstruction of 2014.3.
The diversity of non-methanogenic bacteria involved in biogas production from tofu-processing wastewater
SUNARTO, HANNI TSAAQIFAH, CAHYADI PURWOKO, ARTINI PANGASTUTI Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University. Jl. Ir. Sutami 36A Surakarta 57126, Central Java, Indonesia. Tel./Fax. +62-271-663375, email: [email protected]
Manuscript received: 29 November 2014. Revision accepted: 22 December 2014.
Abstract. Sunarto, Tsaaqifah H, Purwoko C, Pangastuti A. 2014. The diversity of non-methanogenic bacteria involved in biogas production from tofu-processing wastewater. Biodiversitas 16: 62-68. The energy crisis is an important current issue, so diversification of energy is needed to solve the problem. Biogas from tofu-processing wastewater is one potential alternative energy to be developed because it has high organic matter content. The amount of methane formed by methanogens is also influenced by the presence of bacteria, so it is necessary to do research on the diversity of non-methanogenic bacterial communities. This study aimed to determine the diversity of non-methanogenic bacteria in anaerobic fermentation using ARDRA (Amplified Ribosomal DNA Restriction Analysis) method. Tofu-processing wastewater was anaerobically fermented, followed by DNA extraction, amplification of 16S rRNA marker gene, and cloning. Then, restriction was done using MspI and AluI restriction enzymes, followed by sequencing of different patterns. The data were analyzed to know the diversity of non-methanogenic bacteria and the relative importance of each phylotype in the community using Shannon-Wiener index of diversity (H’) and evenness (E).The results showed that there were 38 positive clones of 16S rRNA genes clones. The sequencing using BLASTn analysis showed the presence of 10 species of non-methanogenic bacteria. There were four sequences with 97% similarity, indicating that the bacteria belong to species from GeneBank data. There were 6 sequences that had 96% similarity with the closest relative in the database, indicating that these bacteria are new species. The Shanon- Wiener index was 1.291, categorized as low and the evenness was 0.561, categorized as low because there was dominance of a species.
Keywords: ARDRA, biogas, non-methanogenic bacteria, wastewater, 16S rRNA.
INTRODUCTION anaerobic fermentation, consisting of four stages of decomposition, namely hydrolysis, acidogenesis, Enery is essential for every living creature. Global acetogenesis and methanogenesis (Briones et al. 2007). energy demand increases along with the increasing human Each stage involves a group of different microbes which population and activities. The Ministry of Energy and work synergically with each other, so they form microbial Mineral Resources of Indonesia reported that energy consortia (Griffin et al. 1998). The consortia are classified consumption per capita in Indonesia increases with the as non-methanogenic and archaic bacteria. The non- growing rate of more than 5% (MEMR 2009). Ironically, methanogenic bacteria play important roles in organic the increasing demand for energy is not balanced with its waste degradation, namely in liquefaction or hydrolysis supply, so the energy stocks, especially the fossil fuels are stage and the production of acid which provides substrate depleted. According to Sun et al. (2013), 88% of global for the archaic bacteria (Madigan et al. 2009). enery consumption comes from fossil fuels, which lead to Because the information of the diversity of non- energy crisis, because fossil fuels are non renewable, which methanogenic bacteria involved in the processing of biogas may be gone within 50-100 years. from tofu-processing wastewater is limited, studies are Many governments in the world, including Indonesian needed. In general, studies on morphology, cell structure government, have realized the threat of energy crisis. The and biochemistry of bacteria are conducted through utilization of alternative energy sources is the appropriate isolation and characterization using culture (Reeve 1994). measure to overcome the energy problem. Biogas is one the However, there is a problem because not all microbes, most considered alternative sources of energy. Biogass including the major bacteria group, can be cultured refers to the mixture of methane, carbondioxide and other (Suwanto 1994). Therefore, it is necessary to choose a gasses produced by decomposition of organic waste, such method which can be used to study the structure of all as domestic waste and manure by methanogenic bacteria bacteria, namely ARDRA (Amplified Ribosomal DNA (Ntengwe et al. 2010). Restriction Analysis). This method can be used to analyze In Indonesia one potential source of organic waste for population of bacteria and the predicted genetic changes biogas is tofu-processing wastewater. There are 84.000 tofu within a period of time. The objective of this study was to production units in Indonesia with a total production of know the diversity of non-methanogenic bacteria involved 2.56 million tons per day (Sadzali 2010). Tofu-processing in the processing of biogas from tofu-processing waste- wastewater can be processed to make biogas through water. SUNARTO et al. – The diversity of non-methanogenic bacteria 63
MATERIALS AND METHODS denaturation at 94oC for 30 seconds, annealing at 55oC for 30 seconds, extension at 72oC for 30 seconds (35 cycles The materials for biogas production were substrate each), post extension 1 cycle at 72oC for 7 minutes, and it namely tofu-processing wastewater and inoculum in the was ended with storing at 4oC. Then, the PCR product was form of active sludge of tofu. The substrate and inoculum processed in electrophoresis at 0.8% agarose gel; then it were then fermented in anaerobic condition for 20 days in a was purified with GeneJETTM Gel Extraction Kit digester. Then, the molecular research was started with the (Fermentas, MA, USA). extraction of digester samples using UltraClean Soil DNA Kit (MoBio, Carlsbad, CA, USA). The result of extraction Cloning of 16S rRNA of PCR Product was genomic DNA of non-methanogenic bacteria. Then the The PCR products were cloned in accordance with 16S rRNA gene was amplified using PCR cycle, using procedures recommended in InsTAcloneTM PCR Cloning primers 63F and 1387R. The result of amplification was Kit (Fermentas, Waltham, MA, USA). Clone selection was subsequently purified with GeneJetTM Gel Extraction Kit done in LB agar medium added with 50 mg/mL Ampicillin (Fermentas c.q. Thermo Fisher Scientific Inc., Waltham, and X-Gal substrate. Then, the white clone was picked and MA, USA). The product of purification was litigated with grown in LB agar added with 50 mg/mL Ampisilin at 37 vector pTZ57R/T (Fermentas, MA, USA) which was then °C, shaken for 3-5 hours. This cell-containing medium was cloned using InsTAcloneTM PCR Cloning Kit (Fermentas, used as a template for insert amplification using primer Waltham, MA, USA). The transformant cell culture was M13 with mixed reactant composed of 10% culture, 0.8 grown in Luria Bertani (LB) agar medium with the addition of ampicillin, X-gal and IPTG. Then, Blue- white selection mM dNTP, 1μM of each primer, 0.1 U/μL Taq DNA Polymerase, bufferred 1x. The PCR condition consisted of was conducted. The positive clones were digested using 3 cycles at 94 °C for 70 seconds, at 56 °C for 45 seconds, restriction enzymes, AluI and MspI. at 72 °C for 90 seconds; 23 cycles at 90 °C for 15 seconds, 56 °C for 30 seconds, 72°C for 1 second; 1 cycle at 72 °C The making of biogas for 10 minutes, and it was ended at 4 °C. Fifty clones First, inoculum was put into digester with concentration which positively contained insert were randomly selected of 20% of 264 mL of the digester working volume or to be used for the subsequent analyses. equivalent to 52.8 mL. Then, 211.2 mL (or 80% of 264 mL) of the substrate was poured into the digester. Then the ARDRA (Amplified Ribosomal DNA Restriction digester was closed tight. The fermentation took place for Analysis) 20 days until biogas was produced, which was Inserts were digested using restriction enzymes, MspI subsequently channeled through a small tube into a water- and AluI, in a mixture reaction with the following filled gas collecting tank (a drinking water bottle, 330 mL). composition: 0.2 µL of enzymes, 2 µL of tango buffer, 10 The gas pushed the water out of the bottle. The volume of µL of DNA, and 7.8 µL of ddH O. The mixture was then water spilled out the bottle was equal to the volume of gas 2 incubated at 37 °C for one night. Then, the DNA resulted filling the bottle. from the digestion was processed in electrophoresis at 2% The samples for molecular study were taken on the 20th agarose gel, at a voltage of 70 V, for 2 hours. The number day. According to Sunarto et al. (2013), usually the of inserts having different restriction patterns was counted production of biogas has taken place optimally on the 20th in percentage of the total analyzed clones. Then, the 16S day, so all stages of anaerobic fermentation have occurred. rRNA marker genes of the clones were sequenced for identification. Extraction of DNA samples After 20 days of incubation, the sludge from the Sequencing and identification of the16S rRNA marker digester was sampled for DNA extraction using UltraClean genes Soil DNA kit (MoBio, CA, USA), following the procedure The resulted clones were run in PCR again for recommended by the manufacturer. The result of extraction sequencing by 1st Base Sequencing Services (Axil was genomic DNA of non methanogenic bacteria as the Scientific Pte. Ltd., Singapore through PT. Genetika DNA templates in PCR process. Science Indonesia, Jakarta). Identification was done by comparing the sequences of the16S rRNA marker gene, Amplification of 16S rRNA Gene for ARDRA about 1300 bp in size, with the database using the Program The genomic DNA of non-methanogenic bacteria was BLAST (Basic Local Alignment Search Tool) in the web then amplified. PCR reaction was made by mixing 0.5 μL site of National Center for Biotechnology Information of DNA samples, 17.5 μL of ddH2O, 2.5 μL of dNTP, 2.5 (http://www.ncbi.nlm.gov/BLAST). mM 2.5 μL of Buffer Taq, 0.2 μL of DNA Taq Polimerase enzyme, and 1 μL of primer. The DNA amplification used Data analyses primer 63F (5’ CAG GCC TAA CAC ATG CAA GTC 3’) The diversity index of Shannon-Wiener (H’) and the 5 pmol pairing with 1387R (5’ GGG CGG WGT GTA evenness index (E) were determined to show the diversity CAA GGC 3’) 5 pmol (Marchesi et al. 1998). The PCR of bacteria community and the relative importance value of program consisted of 1 cycle of pre denaturation at a each phylotype in the community. temperature of 95oC for 5 minutes, followed by 64 BIODIVERSITAS 16 (1): 62-68, April 2015
The diversity index: (Yimer and Sahu 2014).
Extraction of DNA and amplification of 16S rRNA genes Extraction of non-methanogenic bacteria DNA was done to get genomic DNA as a template for PCR process. H’ = Diversity index UltraClean Soil DNA Kit (MoBio, CA, USA) was used for S = number of species the extraction of genomic DNA of non-methanogenic Pi = Ni/N = proportion of Species i bacteria from the tofu sludge, following the procedures in Ni = number individuals of species i the manual kit. The genomic DNA of non-methanogenic N = number of individuals of all species bacteria resulted from the extraction was then amplified. The amplification of 16S rRNA genes used the PCR cycle The criteria used to interpret the diversity index: which was the result of optimizing in the research of H’ < 1: low diversity Sunarto et al. (2013). The primers used were 63F and 1-3: medium diversity 1387R, the universal primers for amplification of 16S >3: high diversity rRNA gene of bacteria with an amplicon target of 1.300 bp (Marchesi et al. 1998). Primer is an important component Relative importance value: in PCR reaction because it will determine the region of targeted genome which will be amplified (Rafsanjani 2011). The amplified DNA was separated with 0.8% agarose gel electrophoresis and then visualized using coloring agent of ethidium bromide and detected with UV E = Evenness; H’ = Diversity index; Hmax = ln S light. The result of electrophoresis of amplification of PCR product of non-methanogenic bacteria 16S rRNA is shown in Figure 1. RESULTS AND DISCUSSION The electropherogram shows that the size of region of 16S rRNA of non-methanogenic bacteria was 1300 bp, and The production of biogas from tofu-processing it also shows single band indicating that the primer pair wastewater used was specific and attached to targeted area. The single The sludge from tofu-processing wastewater digestion, band contained collection of 16S rRNA genes from many after 20 days of anaerobic fermentation, was sampled for bacteria present in tofu waste sludge from the digester. The molecular analyses. The measurements of pH and temperature thickness of the band indicates the quantity of the amplified were done in day 0 and day 20. The pH in day 0 was 7, and DNA templates. The electropherogram in this study was in day 20 was 7.87. The temperature in day 0 and day 20 clearly visible and thick, indicating that the concentration was the same, which was 30 oC. The increase of pH in day of molecules separated in this region was high. The 20 was influenced by the archaic methanogenic bacteria amplicon was then amplified using GeneJetTM Gel activities. According to Fulford (1988), at the early phase Extraction Kit (Fermentas, MA, USA). Purification is of biogas processing, the acid-producing non-methanogenic needed because the cloning stage requires clean gene bacteria are active, so the pH of digester becomes low. inserts, free from contaminant such as oligonucleotide Then, the archaic methanogenic bacteria use the acid as which is not used in PCR process, the residues of buffers, substrate, so the pH increases. The pH in the 20th day in and dNTP. The contaminant must be removed, because if this study was 7,87 which is tolerable by archaic the residue of dNTP combines with residue of DNA methanogenic and non-methanogenic bacteria (NAS 1981). polymerase, it will disturb the methods designed for Concentration of methane measured using amplified DNA during cloning stage (Sanger et al. 1977). chromatography was 655.82 ppm (R. Setioningsih, pers. comm.). The flame test showed that the production of gas Cloning of 16S rRNA genes was not sufficient to be lit. The biogas production refers to The product of purification was litigated with plasmid the reaction and interaction between the methanogenic vector pTZ57R/T (Fermentas, MA, USA), catalyzed with microbes and the non-methanogenic ones (Gunnerson and T4 ligase enzyme to get plasmid recombinant. The Stuckey 1986). The non-methanogenic bacteria are litigation product was then transformed into E. coli JM107, categorized into three groups, namely hydrolitic, using InsTAcloneTM PCR Cloning Kit (Fermentas, acidogenic, and acetogenic. These non-methanogenic Waltham, MA, USA) following the procedures bacteria groups play roles in fermentation of acid, in which recommended by the manufacturer. Transformant cell they convert complex compounds into simple ones. The culture was grown in LB agar medium with the addition of compounds resulted from fermentation are then used by X-gal by spreading it using L rod and then incubated for 16 archaic methanogenic bacteria in methanogenic hours at 37°C. The result of E. coli JM 107 transformation fermentation and converted into methane (Sunarto et al. showed the formation of blue-white colonies. The white 2013). Generally, biogas is composed of methane 55-65%, colonies were estimated to contain fragments of insert carbon dioxide 30-40%, H2O 2-7%, H2S 2-3%, NH3 0- genes, whereas blue colonies were estimated not to have 0.05%, Nitrogen 0-2%, oxygen 0-2%, and 0-1% hydrogen fragments of insert genes. SUNARTO et al. – The diversity of non-methanogenic bacteria 65
The formation of blue white colonies was caused by the fragments from the 6 phylotype sequences and those in the presence of selection marker at vector pTZ57R. The GeneBank indicated that the identified bacteria had close selection marker in vector pTZ57R was gene resistant to kinship, but not from the same species, with those in the ampicillin and additional selection marker was LacZ gene. GeneBank. The absence of 97% similarity between 16S This ampicillin-resistant gene is the marker of -lactamase rRNA fragments and those registered in the GeneBank enzyme, which will degrade the ampicillin, so when the indicated that the identified bacteria were partial sequences cells carrying recombinant plasmid are grown in of the new strains of those in the GeneBank. ampicillin-containing media, the cells will grow while the The compared sequences were partial sequences cells which do not carry recombinant plasmid will die. Lac resulted from the sequencing and each restriction pattern Z gene is the marker for -galactosidase enzyme which produced different sequences. The results of phylotype will hydrolyze X-Gal into galactoside and its derivative identification indicated that there were at least 10 species compounds, namely the blue 5-bromo-4-chloro-indoxyl of non-methanogenic bacteria, the composition of which is (Susanti and Ariani 2003). If there is a fragment of inserted presented in Table 2. gene in the plasmid, the synthesis of -peptide which will serve as an activator for -galactosidase enzyme will be 1 kb DNA impeded, so the blue color will not appear (Brown and ladder Brown 1991). The white colonies formed in selection media were then amplified with PCR and confirmed with electrophoresis. The PCR of colonies was started with the selection of separated colonies in selection media. Previously, a number was assigned to each colony. Then, with sterile toothpicks the colonies were duplicated in selection media which had been divided into several regions. The positive white clones which were estimated to contain fragments of inserted genes were subsequently grown in LB media added with 50 mg/mL of ampicillin and X-Gal substrate. The clones were used as templates for amplification of inserts using primer M13. The electropherogram of insert amplicon from cloning is presented in Figure 2. The insert amplicon was digested with MspI and AluI restriction enzymes which cut with high frequency, which resulted in 10 different restriction patterns. The restriction patterns of DNA of non-methanogenic bacteria 16S rRNA marker genes are presented in Figure 3. Figure 1. Electropherogram of amplicon of genomic DNA of non-methanogenic bacteria 16S rRNA marker gene. Sequencing and identification of 16S rRNA marker genes The results of PCR amplification were sent to 1st Base 1 kb DNA Sequencing Services Singapore (via PT. Genetika Science ladder Indonesia, Jakarta) to be sequenced using ABI Big Dye Terminator Kit (Applied Biosystems® c.q. Thermo Fisher Scientific Inc., Waltham, MA, USA). The results of sequencing were then compared with the sequences in the GeneBank database, using Basic Local Alignment Search Tool (BLAST) on-line in website: www.ncbi.nlm.nih.gov. All ten phylotypes were identified based on the 16S rRNA marker gene and compared with the database and using BLASTn analyses. Based on the results of BLASTn analyses, there were 4 phylotype sequences of non-methanogenic bacteria from the fermentation of tofu-processing wastewater which had partial sequences similar to those in the database of the GeneBank with percent similarity 97%. This indicated that the bacteria were of the same species with the isolates which had been identified (Larsen et al. 1993). There were 6 phylotype sequences with percent similarity <97%, meaning that those were new species Figure 2. The electropherogram of insert amplicon resulted from whose data were not available in the GeneBank. The high cloning of 16S rRNA gene from tofu-processing wastewater percentage of <97% similarity between 16S rRNA gene samples. 66 BIODIVERSITAS 16 (1): 62-68, April 2015
100 bp DNA 1 kb DNA 1 kb DNA ladder ladder ladder
A
1 kb DNA 1 kb DNA 1 kb DNA ladder ladder ladder
B
Figure 3. Restriction patterns of DNA of non-methanogenic bacteria 16S rRNA marker gene with MspI phylotype 1-10 restriction enzymes. A. 100 bp DNA ladder, B. 1 kb DNA ladder.
Table 1. The persentage of similarity between non-methanogenic bacteria DNA in the biogas production process from tofu-processing wastewater and the sequences in the GeneBank.
Restriction % Closest kin No Access pattern codes Similarity Type 1 Chelatococcus daeguensis strain TAD1 HM000004.1 94 Type 2 Uncultured bacterium clone NBBP10309_58 JQ072591.1 98 Type 3 Brevundimonas diminuta strain R057 KC252887.1 99 Type 4 Ochrobactrum anthropi strain YZ-1 JN248785.1 94 Type 5 Devosia albogilva strain IPL15 NR_044212.1 96 Type 6 Acinetobacter junii strain J14N JX490072.1 95 Type 7 Ochrobactrum oryzae strain CK1711 KC955129.1 97 Type 8 Olsenella umbonata FN178463.2 94 Type 9 Defluvibacter lusatiensis strain S1 NR_025312.1 97 Type 10 Rhizobium borbori strain DN365 GU356639.1 94 SUNARTO et al. – The diversity of non-methanogenic bacteria 67
Table 2. The composition persentage of non-methanogenic bacteria of biogas production from tofu-processing wastewater.
Restriction pattern % Composition of non-methanogenic Closest kin codes bacteria Type 1 Chelatococcus daeguensis strain TAD1 5.26% Type 2 Uncultured bacterium clone NBBP10309_58 2.63% Type 3 Brevundimonas diminuta strain R057 68.42% Type 4 Ochrobactrum anthropi strain YZ-1 2.63% Type 5 Devosia albogilva strain IPL15 5.26% Type 6 Acinetobacter junii strain J14N 2.63% Type 7 Ochrobactrum oryzae strain CK1711 5.26% Type 8 Olsenella umbonata 2.63% Type 9 Defluvibacter lusatiensis strain S1 2.63% Type 10 Rhizobium borbori strain DN365 2.63%
The non-methanogenic bacterium with the highest nitrogen. According to Sterling et al. (2001) nitrogen percentage in this study was Brevundimonas diminuta, sources are important as nutrient for microbes to produce which was 68.42% with 26 clones out of the total of 38 biogas. clones. Chelatococcus daeguensis, Devosia albogilva, and In this study, seven out of ten phylotypes were aerobic Ochrobactrum oryzae had the same percentage, namely which had close kinship with Ochrobactrum oryzae, 5.26%, each having two clones. Several bacteria which had Defluvibacter lusatiensis, Devosia albogilva, Rhizobium the smallest percentage, only 2.63%, were uncultured borbori, Chelatococcus daeguensis, Brevundimonas bacterium, Ochrobactrum anthropi, Acinetobacter junii, diminuta and Ochrobactrum anthropi. The presence of Olsenella umbonata, Defluvibacter lusatiensis, and aerobic bacteria in the fermented sludge indicated the Rhizobium borbori, each having only 1 clone. presence of oxygen in the digester, so the biogas Uncultured bacterium clone NBBP10309_58 referred to production was not maximal. The high concentration of bacterium that had not been cultured and identified because oxygen in the digester impedes archaic methanogenic it had such low metabolism activities that its similarity to bacteria in producing methane gases. or difference from other bacteria was not known. Based on The presence of oxygen in the digester in this study the results of BLASTn, this phylotype was considered to might be caused by the use of simple, laboratory-scale have close kinship with phylum Firmicutes they had 92% digester. The initial condition of digester was not similarity. According to Sun et al. (2013) the important role anaerobic, so the aerobic bacteria still survived. This of phylum Firmicutes in biogas production is its ability to condition was correlated with the low biogas production, hydrolyze organic substrate. especially the CH4. So far there has been no sufficient information about non-methanogenic bacteria which play role in the Analyses of non-methanogenic bacteria hydrolysis and fermentation of substrate from tofu- The analyses of non-methanogenic bacteria were based processing wastewater. The only available information is on the calculation of the number of clones. Species richness limited to general species of non-methanogenic bacteria (S) was the number of clones recorded, which was 10. The responsible for hydrolysis and fermentation processes, Shannon-Wiener index was 1.291, indicating the low including facultative and obligate anaerobic bacteria such diversity in the tofu-processing wastewater processed into as Actinomyces, Bacteroides, Bifidobacterium spp., biogas. According to Krebs (1989), the classification of H’ Clostridium spp, Corynebacterium spp., Desulfovibrio spp., are as follows: low diversity (H’ = 0-2.302), medium Escherichia coli, Lactobacillus, Peptococcus anaerobius, diversity (H’ = 2.302-6.907), and high diversity (H’ > Staphylococcus and Streptococcus (Tchobanoglous et al. 6.09). 2002; Madigan et al. 2009). The Evenness index (E) indicates evenness of a Based on the available information, there are 6 community. The evenness index in the tofu-processing phylotypes of non-methanogenic bacteria considered to wastewater processed into biogas was 0.561, categorized as play role in biogas production. Uncultured bacterium clone low. According to Krebs (1985), the value of E ranges from considered to have close kinship with Firmicutes plays role 0 to 1. If E approaches 0, the evenness of community is low in hydrolysis stage because it is able to hydrolyze organic and the abundance of species is not uniform, and the substrate (Sun et al. 2013). Brevundimonas diminuta plays community is dominated by certain species. If E role in acidogenesis stage because it is able to produce approaches 1, the evenness is high, meaning that there is no acetic acid (Kohyama et al. 2006). Olsenella umbonata also dominant species, or the abundance of species is uniform. plays role in acidogenesis stage because it can convert The low diversity in this study was caused by the glucose into acetic acid and formic acid (Isolauri et al. dominance of Brevundimonas diminuta. The plausible 2004; Wilson 2005). 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Infraspecific morphological and genome size variations in Linum glaucum in Iran
SEYED MEHDI TALEBI1,♥, MASOUD SHEIDAI2, MORTEZA ATRI3, FARIBA SHARIFNIA4, ZAHRA NOORMOHAMMADI5 1Department of Biology, Faculty of Sciences, Arak University, Arak, 38156-8-8349 Iran. Tel. +98-863-4173317. ♥email:[email protected]. 2Shahid Beheshti University, GC, Faculty of Biological Sciences, Tehran, Iran. 3Bu-Ali Sina Hamedan University, Hamedan, Iran. 4Department of Biology, North Tehran Branch, Islamic Azad University, Tehran Iran. 5Department of Biology, School of Sciences, Tehran Science and Research Branch, Islamic Azad University, Tehran, Iran
Manuscript received: 27 December 2014. Revision accepted: 20 January 2015.
Abstract. Talebi SM, Sheidai M, Atri M, Sharifnia F, Noormohammadi Z. 2015. Infraspecific morphological and genome size variations in Linum glaucum in Iran. Biodiversitas 16: 69-78. There are many discussions about taxonomic position of Linum glaucum in different Flora. In this study, the morphological traits associated with the nuclear genome size were used for identification of infraspecific variations in the nine populations of L. glaucum. Twenty three qualitative and quantitative morphological characteristics were investigated. The Analysis of variance tests showed significant difference for some morphological features. The Canonical Correspondence Analysis of habitat ecological factors showed that each of the habitats had prominent characteristics, and also Pearson’s coefficient of correlation confirmed the significant correlations between the morphological features in relation to ecological factors. In the morphological Unweighted Paired Group using Average method tree, populations were separated from each other, so that population No. 4 was separated from others. In the flow cytometery investigations, variation of about 1.19 times was presented between the maximum and minimum averages of the genome sizes in the populations. Minimum amount of genome size was found in populations No. 4. Significant correlations occurred between the nuclear genome size with habitat elevation as well as some of the quantitative morphological features. The mentioned variations caused to difference between the populations and lead to creation of ecotype and ecophene in the studied populations.
Key words: Ecology, genome size, morphology, population.
INTRODUCTION strile (Rechinger 1974). In 1967, Davis named it as L. austriacum L. subsp. glaucescens, following Rechinger Biodiversity is mostly investigated at the species level (1974) recognized this taxon as a synonym of L. glaucum. as well as higher taxonomic ranks. However, the basis for Therefore there are three different synonyms for L. biodiversity and organic evolution is the genetic difference glaucum in different Flora such as Flora Iranica (Rechinger within species (Ramel 1998). Linhart and Grant (1996) 1974) and Flora of Iran (Sharifnia and Assadi 2001). suggested that Comparable developmental variation Although L. glaucum is morphologically very similar to presents between different populations of a species L. austriacum, the other member of this section, but in (intraspecific), which likely resounds verifications to different taxonomical treatments such as palynology different natural environments and it is the source of plant (Talebi et al. 2012a), seed micromorphology (Talebi et al. species differentiation. Therefore, humans have used these 2012b), anatomy (Rashnou-Taei 2014) and also molecular infraspecefic variations for the domestication and genetic investigation (ISSR) (Talebi 2013) these species placed improvement of many of plant species (Diamond 2002). separately. The obtained results of these studies showed Linum glaucum Boiss. & Nöe belongs to section Linum that L. glaucum and L. austriacum are separate species. of the genus Linum L. This species is an Irano-Turanian In addition to morphological characteristics, variation element which naturally spread in the slops of the Zagrous between populations can be investigated with using 2C- Mountains in the different provinces of Iran such as value or nuclear genome size. One of the most important Kurdistan, Kermanshah, Zanjan, Hamadan, Lurestan as features of all living organisms is nuclear DNA amount. well as Markazi. In addition this species are found in the Swift (1950) definite C-value as DNA content in the neighboring countries as Iraq and Turkey (Rechinger 1974; unreplicated haploid nucleus. Nuclear DNA amount is Mobayen 1996; Sharifnia and Assadi 2001). positively related to the number of cellular traits such as: There are many discussions about taxonomic position time of mitotic cell cycle, nuclear DNA synthesis rate, the of L. glaucum. This taxon was described for the first time size of cell and its nuclear, through to the whole plant traits as L. alpinum Jacq, var. glaucescens Boiss. in Flora such as minimum generation time and geographic Orientalis (Boissier 1867), then Stapf recognized it as L. distribution (Bennett 1972, 1987; Kidd et al. 1987). Studies 70 BIODIVERSITAS 16 (1): 69-78, April 2015 confirmed that infraspecific variation in nuclear genome measured in picograms (pg) and the nuclei status described size amount is most significant for plant taxonomy as an in terms of ‘C’ value (Doležel et al. 2007). Both of the C- indicator of taxonomic heterogeneity (Murray 2005). value as well as the genome size can be expressed either in Because, the lacks of previously infraspecific study for DNA picograms (=10-9 g) or mega base pairs (1 pg = 978 L. glaucum in Iran as well as the world, we have used for Mbp). The nuclear DNA amount of the studied samples the first time in the present work morphological calculated on the basis of the values of the G1/G2 peak characteristics as well as nuclear genome size for means (Doležel and Bartoš 2005). identification and determining kind and level of infraspecific variations between the nine populations of this species in Iran.
Ecological factors MATERIAL AND METHODS In order to compare the effect of different environmental factors on the nuclear genome size and Plant material morphological characteristics of L. glaucum populations, Nine populations of L. glaucum were randomly five factors were examined for each population’s habitat, collected from western regions of Iran during spring 2011 such as: longitude (E˚), latitude (N˚), altitude (in meters), (Table 1). Plant samples were identified based on the average of annual minimum and maximum temperature (in descriptions provided in accessible references such as Flora C˚). Longitude, latitude and altitude were calculated with Iranica (Rechinger 1974) and Flora of Iran (Sharifnia and Garmin GPS map76CSx, and the averages annual Assadi 2001). The voucher specimens were deposited in minimum and maximum temperature for each population the herbarium of Shahid Beheshti University (HSBU). were taken from the web site of the meteorological From each population four samples were selected randomly organization of Iran. and then examined for their nuclear DNA content and morphological features. Statistical analysis The mean and standard deviation of the studied Morphometry morphological characteristics were determined. In order to Twenty three quantitative and qualitative morphological group the studied populations on the basis of characteristics from the both of vegetative and reproductive morphological features, data were standardized (mean = 0, organs of this species were examined. The studied variance = 1) and used for multivariate analyses including morphological characteristics include: stem lengths and its Unweighted Paired Group using Average method branch number, stem diameter, shape, length and width of (UPGMA) as well as Principal Coordinate Analysis basal and floral leaves, the shape of apex, margin and base (PCoA) (Podani 2000). Analysis of variance (ANOVA) test of basal and floral leaf blade, basal leaf diameter, calyx was employed to assess the significant quantitative dimensions as well as corolla color and dimensions. Four morphological characteristics difference among the studied replications were used for quantitative characters populations, and Pearson’s coefficient of correlation was measurements and the used terminologies for qualitative used to determine significant correlations of nuclear morphological traits were on the basis of descriptive genome size and quantitative morphological traits in terminology provided by Stearn (1983). relation to ecological factors, as well as, longitude, latitude, altitude, average of annual minimum and maximum Flow cytometry temperature, so as to show possible relationship between In order to preparation of nuclei suspensions, small populations. The multivariate method, Canonical amounts of mature fresh leaf tissue together with an equal Correspondence Analysis (CCA), was used to elucidate the weight of mature leaf tissue of the standard reference were relationship between the studied populations and their used. In this study Allium cepa L. was used as standard environmental factors. NTSYS ver. 2 (1998) and SPSS ver. references, which has a 2C DNA value of 33.5 pg 9 (1998) softwares were used for statistical analyses. (Greilhuber and Ebert 1994). For preparation of the nuclear suspension two-stepped method was employed. Plant materials were chopped with RESULTS AND DISCUSSION a sharp scalpel with adding 400 μl nuclei isolation buffer in the plastic Petri dish at room temperature. For staining the Morphometry extracted nuclei, 1600 μl DNA fluorochrome or 4´, 6- In present study, in order to compare the effect of Diamidino-2-phenylindole (DAPI) added and the different environmental factors on the phenotype of L. suspensions were filtered through a 50 μm nylon mesh into glaucum populations, twenty three traits of the both a labeled sample tube. Then the suspensions of stained vegetative and reproductive organs were selected and nuclei were analyzed with a Partec PI Flow Cytometer examined between nine natural populations. The mean and (Partec Germany). In the obtained histograms, some flow standard deviations of the studied characteristics are cytometric statistics such as: coefficient of variation (CV), presented in Table 2. Qualitative characteristics such as: the mode, mean and the number of counted cells were shape of blade and also its margin, apex and basis of the investigated. The obtained nuclear DNA amounts were TALEBI et al. – Intraspecific variations in Linum glaucum 71
Table 1 .Locality and herbarium voucher number of the studied populations.
No. Population Habitat address Collector Herbarium nos. 1 Kurdistan, road of Sanandaj to Hasan Abad, 1684 m. Talebi HSBU2011353 2 Kurdistan, Sanandaj, Darbandeh village, 1559 m. Talebi HSBU2011354 3 Kurdistan, Sanandaj, Kani Moshkan village, 1678 m. Talebi HSBU2011355 4 Kurdistan, Sanandaj, Kilaneh village, 1471 m. Talebi HSBU2011356 5 Kurdistan, Sanandaj, Abidar Mountain, 1585 m. Talebi HSBU2011358 6 Kurdistan, road of Saqqez to Baneh, 1546 m. Talebi HSBU2011360 7 Kurdistan, 25 km Baneh to Saqqez, 1623 m. Talebi HSBU2011361 8 Kurdistan, Saqqez, 1570 m. Talebi HSBU2011362 9 Kurdistan, road of Saqqez to Divandareh, 1617 m. Talebi HSBU2011363
Table 2. Selected morphological traits of the studied population of L. glaucum (all values are in cm, details of each population are given in Table 1).
Basal Basal Floral Floral Stem Stem Basal leaf Floral leaf Calyx Calyx Pedicle Sepal Sepal Petal Petal Populations leaf leaf leaf leaf length ramification shape shape width length length length width length width length width length width 1 Mean 49.12 10.50 1.77 0.19 Linear- 0.87 0.09 Linear- 0.37 0.45 0.10 0.20 0.10 1.55 1.20 N 4 4 4 4 Lanceolate 4 4 Lanceolate 4 4 4 4 4 4 4 SD 9.54 2.64 0.10 0.10 0.15 0.02 0.05 0.06 0.00 0.00 0.00 0.33 0.14 2 Mean 60.37 8.75 1.96 0.25 Linear- 0.87 0.11 Linear- 0.35 0.45 0.09 0.18 0.10 1.72 1.25 N 4 4 4 4 Lanceolate 4 4 Lanceolate 4 4 4 4 4 4 4 SD 6.75 1.25 0.49 0.04 0.09 0.02 0.05 0.05 0.00 0.02 0.00 0.22 0.05 3 Mean 55.37 10.25 1.67 0.21 Linear 1.07 0.12 Linear- 0.38 0.40 0.10 0.23 0.10 1.55 1.22 N 4 4 4 4 4 4 Lanceolate 4 4 4 4 4 4 4 SD 6.79 4.78 0.38 0.06 0.12 0.05 0.02 0.00 0.00 .04 0.00 0.38 0.17 4 Mean 40.25 8.00 1.27 0.15 Linear 1.04 0.31 Lanceolate 0.37 0.47 0.10 0.27 0.10 2.32 1.60 N 4 4 4 4 4 4 4 4 4 4 4 4 4 SD 5.17 3.65 0.17 0.00 0.13 0.45 0.05 0.05 0.00 0.05 0.01 0.37 0.31 5 Mean 49.75 6.50 1.50 0.22 Lanceolate 0.80 0.09 Linear- 0.33 0.42 0.07 0.22 0.12 1.65 1.27 N 4 4 4 4 4 4 Lanceolate 4 4 4 4 4 4 4 SD 6.65 1.73 0.11 0.05 0.18 0.00 0.04 0.05 0.02 0.02 0.05 0.51 0.15 6 Mean 47.75 16.75 1.57 0.35 Linear- 1.05 0.16 Lanceolate 0.37 0.42 0.10 0.22 0.10 1.62 1.35 N 4 4 4 4 Lanceolate 4 4 4 4 4 4 4 4 4 SD 8.46 3.09 0.26 0.05 0.23 0.04 0.05 0.05 0.00 0.05 0.00 0.15 0.17 7 Mean 53.87 15.00 1.87 0.18 Linear- 1.37 .17 Lanceolate 0.45 0.47 0.10 0.22 0.12 1.97 1.82 N 4 4 4 4 Lanceolate 4 4 4 4 4 4 4 4 4 SD 7.37 6.78 0.26 0.04 0.12 0.05 0.05 0.05 0.00 0.02 0.05 0.17 0.17 8 Mean 55.25 8.75 1.47 0.15 Linear 1.12 .10 Linear .38 .45 .10 .25 .13 1.82 1.35 N 4 4 4 4 4 4 4 4 4 4 4 4 4 SD 4.85 1.70 .37 0.03 0.25 0.00 0.06 0.05 0.00 0.05 0.04 0.22 0.23 9 Mean 59.00 4.50 1.60 0.23 Lanceolate 1.02 0.24 Lanceolate 0.36 0.52 0.09 0.23 0.10 2.00 1.65 N 4 4 4 4 4 4 4 4 4 4 4 4 4 SD 8.36 0.57 0.14 0.02 0.12 0.24 0.04 0.05 0.02 0.04 0.00 0.08 0.12
both of basal and floral leaf as well as petal color were such as: stem height and diameter, branch number, basal examined between the populations. Basal and floral leaf leaf width and thickness, floral leaf length, petal length and shape varied between populations and presented in the width (Table 3). shape of linear, lanceolate or linear-lanceolate. In spite of Highest and smallest stems lengths being recorded in variations in blades shape in the basal and floral leaf, blade populations No. 2 (62.16 cm) and No. 4 (40.25 cm), apex, margin and base shapes were stable between respectively. Stem branch number was between 5 populations and were in the shape of acute, entire and (population No. 9) to 17 (population No. 6). Biggest basal cuneate respectively, furthermore the petal colors were leaf (1.57×0.35 cm) occurred in population No. 6, while stable inter-populations and presented as blue. population No. 4 had smallest basal leaf (1.27×0.15 cm). The performed ANOVA test on the quantitative Widest floral leaf (0.31 cm) registered in population No. 4 morphological traits between the studied populations and narrowest (0.1 cm) belonged to population No. 1. showed significant difference (p<0.05) in characteristics Biggest calyx (0.45×0.45 cm) recorded in population No. 7, 72 BIODIVERSITAS 16 (1): 69-78, April 2015
Table 3. Results on the ANOVA analysis to assess for differences in the quantitative morphological traits in L. glaucum populations.
Characters Sum of Squares df Mean Square F Significant Stem height Between Groups 1252.889 8 156.611 2.977 .016 Within Groups 1420.250 27 52.602 Total 2673.139 35 Stem ramification Between Groups 481.556 8 60.194 5.079 .001 Within Groups 320.000 27 11.852 Total 801.556 35 Basal leaf length Between Groups 1.457 8 .182 2.082 .074 Within Groups 2.362 27 .087 Total 3.819 35 Basal leaf width Between Groups .118 8 .015 8.910 .000 Within Groups .045 27 .002 Total .163 35 Floral leaf length Between Groups .926 8 .116 4.184 .002 Within Groups .747 27 .028 Total 1.674 35 Floral leaf width Between Groups .184 8 .023 .748 .649 Within Groups .832 27 .031 Total 1.016 35 Calyx width Between Groups .032 8 .004 1.554 .186 Within Groups .070 27 .003 Total .102 35 Calyx length Between Groups .042 8 .005 2.040 .079 Within Groups .070 27 .003 Total .112 35 Pedicle Between Groups .002 8 .000 1.294 .288 Within Groups .005 27 .000 Total .007 35 Sepal length Between Groups .021 8 .003 1.552 .186 Within Groups .046 27 .002 Total .066 35 Sepal width Between Groups .005 8 .001 .838 .578 Within Groups .022 27 .001 Total .028 35 Petal length Between Groups 2.122 8 .265 2.879 .019 Within Groups 2.488 27 .092 Total 4.610 35 Petal width Between Groups 1.581 8 .198 5.783 .000 Within Groups .922 27 .034 Total 2.503 35 Leaf thickness Between Groups .062 8 .008 3.111 .013 Within Groups .067 27 .002 Total .130 35 Stem diameter Between Groups .137 8 .017 4.974 .001 Within Groups .093 27 .003 Total .230 35
while smallest calyx (0.35×0.4 cm) was seen in population No. 5 rested in eastern regions (Figure 1). CCA biplot of No. 2. Largest (0.27 cm) and smallest sepal (0.1 cm) were morphological traits and environmental factors showed that found in populations No. 4 and 6, respectively. Biggest and the mentioned parameters had strong effect on the plant smallest corolla (2.32×1.6 cm) were registered in populations phenotype. For example, branch number and also basal leaf No. 4 and 1, respectively. Thickest basal leaf (0.2 mm) and shape were varied along annual minimum temperature and stem (0.33 cm) were found in populations No. 2 and 3, also variations in floral leaf length, petal width and floral respectively. Slimmest basal leaf (0.1 mm) and stem (0.13 leaf width were parallel with northern distribution of cm) occurred in populations No. 7 and 4, respectively. populations; furthermore, annual maximum temperature Five geographic and climatic factors of population’s had strong effect on floral leaf shape (Figure 2). habitat were examined. CCA analysis showed that these In addition, Pearson’s coefficient of correlations were factors varied between habitat, and each of them had a determined between the quantitative morphological features prominent environmental feature. For example, populations in relation to environmental factors of habitat, including No. 6 and 7 placed at coldest environments or population longitude, latitude, altitude and average of annual minimum TALEBI et al. – Intraspecific variations in Linum glaucum 73 and maximum temperature, showed significant minimum average value (1.73 pg) being registered in negative/positive correlations. For example, floral leaf population No. 4, showing variation of about 1.19 times. length had a significant negative correlation (p<0.05, r=- A significant negative correlation (p<0.05, r=-0.73) 0.65) with maximum temperature of year, but this feature occurred between genome size with habitat altitude. This had significant positive correlations (p<0.05) with means that, L. glaucum populations that grow in higher minimum temperature of year (r=-0.65) and northern altitude possess smaller nuclear DNA amounts, while the distribution (r= 0.69) of populations. A significant negative populations found in lower had larger nuclear DNA correlation (p<0.001, r=-0.94) occurred between calyx amounts. Not only significant correlation occurred between width with annual maximum temperature, while this trait nuclear genome sizes in relation to environmental factors had a significant positive correlation (p<0.05, r= 0.72) with of habitat, but also morphological traits of the studied northern distribution of populations. populations had significant correlations with 2c-value The studied populations were separated in the UPGMA amount of plants. For example, nuclear genome size had tree of morphological features (Figure 3). In the mentioned significant negative correlations (p<0.05) with floral leaf diagram two main branches were seen, one of these had one width (r=-0.67) and also with petal length (r=-0.72). A population, namely population No. 4, which arranged significant positive correlation (p<0.05, r=0.67) found separately far from others. The rest of populations placed in between nuclear DNA amount with stem height. another branch. This branch had two sub branches; populations No. 7 and 6 became detached from others and Table 4. Nuclear genome size of the studied populations (details placed in one sub branch. As seen in the box and whisker of each population are given in Table 1). plots (Figure 4), each of the studied populations had distinct Genome size morphological trait (s). Population 2C DNA amount (mega base nos. (picograms) pairs) Genome size 1 1.99 1946.22 Nuclear DNA amounts of the studied populations were 2 2.05 2004.9 calculated with flow cytometer apparatus (Table 4). In the 3 1.99 1946.22 analyzed samples, most of the leaf nuclei of the both L. 4 1.73 1691.94 glaucum and standard references were at the G1 phase of the 5 2.06 2014.68 cell division and thus represented the 2C DNA amount. The 6 1.96 1916.88 average of nuclear genome size differed between 7 1.94 1897.32 populations. Maximum average of genome size was 8 2.02 1975.56 recorded in population No. 5 with about 2.06 pg, while the 9 2.01 1965.78
Figure 1. CCA plot of the ecological factors of L. glaucum populations. Abbreviations, minte: average of annual minimum temperature, maxtem: average of annual maximum temperature, north: latitude, altit: altitude, east: Longitude (details of each population are given in Table 1). 74 BIODIVERSITAS 16 (1): 69-78, April 2015
Figure 2. CCA biplot of morphological traits with ecological factors of the studied populations. Abbreviations, minte: average of annual minimum temperature, maxtem: average of annual maximum temperature, north: latitude, altit: altitude, east: Longitude, balesh: basal leaf shape, flesh: floral leaf shape, fllewi: floral leaf width, fllele: floral leaf length, leadi: basal leaf dimentions, petwi: petal width, balewi: basal leaf width, bra: branch number (details of each population are given in Table 1).
Figure 3. Morphological UPGMA tree of the L. glaucum populations (details of each population are given in Table 1). TALEBI et al. – Intraspecific variations in Linum glaucum 75 leaf length leaf Basal leaf length leaf Basal width leaf Basal Floral width leaf Floral length Calyx width Calyx Pedicle length Sepal width Sepal length Petal width Petal size Genome
Figure 4. Box and whisker plot of some important characteristics of the studied populations (details of each population are given in Table 1).
Mixoploidy Discussion In mixoploidy condition, the plant body consisting of Alonso-Blanco et al. (2005) suggested that plant diploid and polyploid cells. Genome size of all cells diversity has fascinated man all over history, primarily due undergoes cyclic changes. In the resting (G0 phase) and to the great difference that presents in nature for pre-replicative stages of cells (G1 phase), each cell has 2C morphological and other developmental features. of nuclear DNA amount, but synthesis of new DNA occurs According to Cronk (2001), the effects of fitness of such during S phase of cell cycle, resulting in doubled (4C) naturally occurring variation exist in the different nuclear DNA content. In the post-replicative period of cell populations of a species (infraspecific) have driven plant growth (G2 phase), the DNA content is maintained at 4C macroevolution by means of natural selection, this level. In population No. 1, in addition to peak of G1 phase developmental diversity being the principle of plant nuclei (2C= 1.99 pg), the peak of G2 phase nuclei were seen classification and phylogeny. and represented the 4C (DNA4C = 4.11 pg). So mixoploids In the present study, in addition to morphological can be identified in flow cytometry histograms by the characters, nuclear genome size was used for identification presence of two peaks of Linum in the histogram (Figure 5). of infraspecific variations in the L. glaucum populations. Not only quantitative morphological traits differed between populations and ANOVA test showed significant difference for some of them, but also qualitative features such as floral as well as basal leaf shape varied among the studied samples. In the UPGMA tree of morphological features, populations were detached, not only population No. 4 placed in separated branch but also populations No. 6 and 7 separated from the rest. This subject confirmed high morphological variations between the populations. The individuals of the mentioned populations had distinct morphological characteristics, for example population No.4 had smallest stem, basal leaf and sepal and also biggest corolla with widest floral leaf in comparison to other populations. Therefore, these traits differentiated these populations from others. Different morphological studies on the populations of this species confirmed the obtained Figure 5. Flow cytometry histogram of mixoploidy in L. glaucum results of the present study. For example morphological population (peak 2: L. glaucum 2c value amount, peak 3: L. characters of long-styled and short-styled plant populations glaucum 4c value amount and peak 4: standard reference). 76 BIODIVERSITAS 16 (1): 69-78, April 2015 in L. glaucum were investigated by Talebi et al. (2012c). In size can alter phenotypic features at the population scale their study, T-test analysis of morphological characters (but see Lavergne et al. 2010). between long-styled and short-styled plant populations, The obtained results showed that, in addition to showed significant difference (p<0.05) for some characters morphological features, nuclear genome size showed such as basal leaf length, calyx width and length. variations of about 1.19 times between populations. These Understanding the sources of morphological variation in variations are widespread phenomenon in this genus. organisms such as plants is central to the understanding of ANOVA test revealed a significant variation in genome natural variation and the responses of organisms to their size among the Iranian populations of Linum austriacum L. environment. Morphological traits variability expression (Sheidai et al. 2014a) as well as Linum album (Sheidai et can show differentiation of plant populations in a particular al. 2014b). Some of Linum species are known as a good habitat (Schlichting 1986). example of plastic genome in plant (Evans et al. 1966; The observed variations between the studied Evans 1968a, b; Durrant and Jones 1971; Joarder et al. populations can be caused by two main factors: it may be 1975), for example different cultivars of L. sativum related to ecological factors of the population’s habitat or Hasselq. had a 10 % difference in genome size. Some variations in genetic structures of populations. Most of the degree of chromosomal variation within populations such existing relationships between the morphological features as duplications and deletions, spontaneous aneuploidy or with environmental factors were significant; this subject polyploidy, heterochromatic segments, B-chromosomes showed that variation in phenotypical characteristics is and sex chromosomes will naturally cause some inter- predictable and had significant correlations with individual DNA content variation (Greilhuber 1998). environmental variations. Referring again to the mentioned Results of this study showed that nuclear genome size above populations, it can see that both of the populations had strong effect on morphological characteristics of the No. 4 and 6 were found in habitats which had salient studied populations, and significant positive/negative characteristic (s), for example population No.4 found in the correlations recorded between morphological highest altitude (1741 m), conversely population No. 6 was characteristics with 2c-value amounts. Furthermore, seen in the lowest elevation habitat (1546 m), with population’s arrangements in the morphological UPGMA variation about 200 m. These conditions were true about tree were coinciding with 2c-value amounts of the other ecological factors of habitats such as annual populations. Population No. 4 which separated of others minimum and maximum temperatures and also had smallest amount of nuclear genome size. This geographical latitude and altitude. Furthermore, significant condition was true about populations No. 6 and 7. These positive or negative correlations found between populations placed together and approximately had equal environmental factors with morphological characteristics of nuclear genome size. Quantitative differences in nuclear populations individuals. For example, increase in habitat DNA contents within a species result in changes in cell temperature shortens the length of floral leaf or northern cycle and cell size in many plant species such as Zea mays populations have more elongated floral leaf. Different L. (McMurphy and Rayburn 1992), Festuca arundinacea studies on the other species, either of the genus Linum or Schreb. (Minelli et al. 1996) and Poa annua L. (Mowforth other genus/ families confirmed this condition. For and Grime 1989). These changes at the cellular level have example, Morphological characteristics of twenty one multitudinous effects on various phenotypic traits through populations of Linum album Kotschy ex Boiss. were allometric effects of the changes in cell dimension survived (Talebi et al. 2014a). The results of the study have (Cavalier-Smith 1985). DNA is effected growth and shown that the different populations of L. album were development of each organism in two ways, directly adapted to their habitat and the ranges of phenotype through its informational and gene content, and indirectly plasticity were high between populations which led to by the physical-mechanical effects of nuclear DNA mass. creation of ecomorphs (Talebi et al. 2014a). Furthermore, Although the amount of nuclear DNA does not involve Talebi et al. (2014b) investigated morphological traits of expression and regulation of single genes, it has great different populations of Stachys inflata Benth. in Iran. The effects on cellular metabolic processes (Cavalier-Smith results of this study showed that different populations of 1985). same species that grow under different ecological The term ‘nucleotype’ was used to describe those conditions, altered their morphological features for conditions of the nucleus, which affect the phenotype adaptation with their habitat condition. (Bennett 1972). The infraspecific changes in genome size, The relationships between nuclear DNA mounts and being therefore subject to natural selection is naturally phenotypic features have been discussed in different related with those leading to the divergence and evolution studies at different levels, for example effect of genome of species. Therefore, a thorough appraisal of such changes size on cell size and stomatal density in angiosperms is required for the application of genome size data to (Beaulieu et al. 2008), effect of genome size on phenotypic demarcate infrageneric taxa and in microsystematics. traits at the cellular level i.e. guard cell length and In the studied populations, habitat ecological factors epidermal cell area (Knight and Beaulieu 2008); influenced nuclear genome size, as significant negative relationship between genome size and production of above- correlations occurred between genome sizes with habitat ground biomass, seedling establishment success as well as altitude. Different studies confirmed this condition for seed weight and seed dormancy (Munzbergova 2009), but other Linum species. For example, various genotrophs of L. few studies have studied how and whether nuclear genome usitatissimum L. created by a process of environmentally TALEBI et al. – Intraspecific variations in Linum glaucum 77 induced changes in genomes structure (Cullis et al. 1999). distinguished between the studied populations. Population The mentioned heritable alternations are due to specific No. 4 had distinct morphological characteristics with least rearrangements at prominent positions of the genome, nuclear DNA amount, which with these traits adapted to its furthermore Cullis et al. (1999) stated that some changes in habitat, so this population could be definite as ecotype. genome structure such as highly repetitive, middle- Creation of ecotype is very important because this type of repetitive, as well as low-copy-number sequences are variation had adaptive value for each species and increase involved in the polymorphisms detected, and sequence biodiversity in occurring ecosystem. Matching ecotypes to alterations of specific subsets of 5SrDNA have been local conditions increases restoration success. A practical distinct, in addition different varieties of L. usitatissimum value of recognizing ecotypic variation in grasses is in which grew in different environmental conditions for allowing recognition of the most suitable ecotypes for example: high nitrogen concentrations or high temperatures conservation, restoration, renovation, landscaping, and increased 10% in nuclear DNA amounts (Evans 1966). bioremediation (Gibson 2009). Price et al. (1981) studied DNA contents of 222 plant Other interpopulation variation was phenotypic samples of Microseris douglasii (DC.) Sch. Bip. plasticity (accommodation ecophene) which found between representing geographically, ecologically and the studied populations, for instance populations No. 7 and morphologically diverse populations in California which 6 that morphologically separated from others, because no showed a 14% variation between population means, with appreciable difference registered in nuclear DNA amount those having higher and lower DNA amounts restricted to between these in comparison with other populations. The mesic and xeric sites, respectively. Similarly, Ceccarelli et ability of plant to alter its morphology in response to al. (1992, 1993) recorded a 32.3 % difference covering 35 changes in environments can be regarded as phenotypic natural populations of hexaploid Festuca arundinacea was plasticity or accommodation ecophene (Bradshaw 1965; positively correlated with mean temperature during the Schlichting 1986). 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Afr J Biotechnol 11 (94): 16040-16054. Podani J. 2000. Introduction to the exploration of multivariate biological Talebi SM. 2013. Biosystematics and genecology study of the genus data. Backhuys Publishers, Leiden. Linum in Iran. [Dissertation]. Shahid Beheshti University, Tehran. Price HJ, Chambers KL, Bachmann K. 1981. Geographic and ecological [Persian]. distribution of genomic DNA content in Microseris douglasii Thompson JD. 1991. Phenotypic plasticity as a component of evolutionary (Asteraceae). Bot Gaz 142: 415-429. change. Trends Ecol Evol 6: 246-249. Ramel C. 1998. Biodiversity and intraspecific genetic variation. Pure Appl Chem 70 (11): 2079-2084. BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 79-83 DOI: 10.13057/biodiv/d160110
Short Communication: Occurrence of leaf spot diseases on Aloe vera (L.) Burm.f. caused by Curvularia species from Madhya Pradesh, India
SHUBHI AVASTHI1, AJAY KUMAR GAUTAM2, REKHA BHADAURIA1,♥ 1Mycology and Plant Pathology Laboratory, School of Studies in Botany, Jiwaji University, Gwalior 474011, Madhya Pradesh, India, ♥email:[email protected] 2Faculty of Agriculture, Abhilashi University, Mandi 175045, Himachal Pradesh, India
Manuscript received: 8 January 2015 Revision accepted: 31 January 2015.
Abstract. Avasthi S, GautamAK, Bhadauria R. 2015. Occurrence of leaf spot diseases on Aloe vera (L.) Burm.f. caused by Curvularia species from Madhya Pradesh, India. Biodiversitas 16: 79-83. During 2010-2011, occurrence of leaf spot diseases was observed on Aloe vera plants grown in various nurseries of Gwalior, Madhya Pradesh, India. The typical disease symptoms were observed on the abaxial surface, tips and spiny margins of leaves. Disease spots were sunken, dry, necrotic, dark maroon to dark brown in color. On the basis of morphological and microscopic characteristics of the fungus, two species of Curvularia i.e. Curvularia lunata and Curvularia ovoidea, were found to be associated with the leaf spot diseases. Koch’s postulate was applied to confirm the causal organisms of the diseases. According to the literature, this is the first report of leaf spot disease on A. vera caused by Curvularia lunata from Madhya Pradesh, and the first report of Curvularia ovoidea from India.
Key words: Aloe vera, Curvularia lunata, Curvularia ovoidea, leaf spot, India
INTRODUCTION agent of leaf spot symptoms on A. vera.
Aloe vera (L.) Burm.f. belongs to family Aloeaceae, is a perennial, succulent, monocotyledonous plant with an MATERIALS AND METHODS average height of 60-100 cm. There are about 400 species of Aloe, but the most commercially cultivated species is A. Sample collection and study of symptoms vera. It is a native of warm tropical regions, especially Various nurseries in Gwalior, India were surveyed for North Africa, the Mediterranean region of southern Europe the presence of leaf spot diseases on A. vera during the and the Canary Islands. This species was first described by rainy and winter seasons of 2010 and 2011. Ten infected Carl Linnaeus in 1753. Aloe vera belongs to a large group leaves were collected randomly from each nursery, placed of plants known as Xeroids because of its ability to close into labeled zip lock bags, and brought into the laboratory. its stomata completely to avoid loss of water and help in The morphology of the symptoms was studied with the retaining a large amount of water in its tissues (Akinyele help of hand lens and dissecting microscope. and Odiyi 2007). It is commonly referred as a “miracle plant” and has a long history of economic and medicinal Isolation and purification of pathogen from diseased uses that spans thousands of years (Daodu 2000). More leaves than 200 chemical components have been identified from Diseased leaves of A. vera were taken into the the leaf pulp and exudates of A. vera (Reynolds and Dweck laboratory and washed thoroughly with running tap water 1999; Choi and Chang 2003; Ni et al. 2004). Its gel is to remove the surface dirt. The leaves were cut into small widely used for the treatment of sores, wounds, skin pieces using sterile scalpel blades. These small pieces were cancer, cold, constipation, asthma, ulcer, diabetes and then surface sterilized with 2% sodium hypochlorite fungal infection (Joseph and Justin 2010). The leaf pulp solution (NaOCl) for 2 mins and then washed three-four exhibited inhibition of AIDS virus by accemannan and times in sterile distilled water. These surface sterilized inhibition of the prostaglandin synthesis by anthraquinone- pieces were then placed between blotting papers and type compound (Hassannuzzaman et al. 2008). In the aseptically inoculated onto petridishes containing Potato cosmetic industries A. vera is used in the production of Dextrose Agar media. The plates were incubated at 25±2 soap, shampoo, toothpaste and body lotions (Daodu 2000). °C for 5 to 6 days, and the growth of fungal colonies were Despite its therapeutic and antimicrobial potential, A. recorded every day. vera is susceptible to various fungal diseases. Leaf spot is an important disease that not only affect the leaf texture but Characterization and identification of the pathogens also reduce the quality and quantity of mucilaginous gel The isolated fungal species were identified on the basis used for medicinal and commercial purposes. Therefore, it of morphological and cultural characteristics as described was the objective of this study to identify the causal by Ellis (1971) and Gilman (2012). Identification of 80 BIODIVERSITAS 16 (1): 79-83, April 2015 pathogens was further confirmed at the Indian Type Identification of fungal pathogens Culture Collection (ITCC), IARI, New Delhi and the The fungal colony isolated from diseased tissue was National Fungal Culture Collection of India (NFCCI), subfloccose, dark olive-gray in color and on the reverse Agharkar Research Institute, Pune, Maharashtra, India. side was greyish black on PDA. Hyphae septate, branched, 3.0-3.6 µm in diameter. Conidiophores were erect, long Pathogenicity test of the pathogens and unbranched. Conidia borne more or less in whorl at the Pathogenicity test was carried out in vitro on the tip of conidiophores, curved and brown in color. Generally healthy leaves of A. vera, according to the method conidia have four transverse septa and 18-29 × 10-8 µm in described by Kamalakannan et al. (2008). The isolated size. The central cell is typically darker and larger as fungal species were cultured on Potato Dextrose Agar compared to the end cells (Figure 1C & D). Based on (PDA) medium at 25±2°C for 8-10 days in an incubator. morphological and cultural characteristics the fungus was Conidial concentration was subsequently adjusted to 1×109 identified as C. lunata (Walker) Boedijin (# ITCC - per ml by using hemocytometer to make a spore 8185.11). suspension. Healthy leaves were surface sterilized for 1 The growth of another fungal colony on PDA was min with 2% sodium hypochlorite solution (NaOCl). initially light grey and circular, becoming velvety, pale Artificial pricks approximately 2 mm deep on the abaxial brown to dark brown in color. The reverse side of the PDA surface of leaves were made by sterilized needle. Spore turned into black color. Conidiophores were pale brown, suspension of the test organisms was delivered through a straight, cylindrical and multiseptate. Conidia were ovoid, sprayer and lined with moist blotting paper. Leaves sprayed three septate, straight or curved, 16-29 × 10-17 µm, brown with sterile distilled water served as control. Leaves were with paler end cells (Figure 2C-D). Based on incubated at 25±2 °C for 8-10 days. morphological and cultural characteristics the fungus was identified as C. ovoidea (Hiroe & N. Watan.) Munt.-Cvetk. (# NFCCI-3053). RESULTS AND DISCUSSION Pathogenicity test Results of the survey revealed that all the nurseries Curvularia lunata and C. ovoidea were pathogenic cultivated only a single species of Aloe, i.e. A. vera and under in vitro conditions. The symptoms of leaf spot none of the nursery was found free from leaf spot diseases. diseases recorded during the pathogenicity test were almost Microscopic and cultural analysis of the isolated fungi similar to the natural symptoms. Symptoms of leaf spot indicates the association of two Curvularia species, infection appeared on fourth day of infestation. Initially, Curvularia lunata and Curvularia ovoidea. Isolation result round, water soaked lesions were appeared on the abaxial indicates that C. lunata and C. ovoidea were isolated from surface of leaves. As the infection progressed, spots all the infected leaf samples. Minor differences were became sunken and reddish maroon in color. On the observed in disease symptoms caused by both fungi. The thirteenth day, the lesions become necrotic and turned into disease symptoms and microscopic characteristics of the dark brown in color. The fungi were re-isolated from the pathogens are described as follows. infected leaves and were compared with the original culture of C. lunata and C. ovoidea. Symptoms of leaf spot diseases Leaf spot disease caused by C. lunata began in the form Discussion of circular, water soaked lesions on the tip and abaxial Curvularia is a filamentous fungus reported to cause surface of the leaves. Gradually the size of the lesions various diseases on different plant hosts. Leaf spot disease expands and became light red in color bordered by water caused by C. lunata and C. ovoidea affects the quality and soaked tissues. As the disease progressed, the lesions were quantity of A. vera leaf gel. Jat et al. (2013) reported severe sunken, maroon color with an average size of 0.5-1.4 × 0.4- form of leaf spot disease on A. vera caused by C. lunata 1.0 cm. In later stages, lesions became dry, necrotic and and its management from Jaipur. Curvularia lunata has turned into dark maroon in color (Figure 1A & B). The been found to cause leaf spot disease on Amaranthus disease was observed during both the rainy and winter spinosus (Sharma et al. 2011), Clerodendrum indicum seasons. (Mukherjee et al. 2013), Grewia optiva (Gautam et al. Symptoms of leaf spot disease caused by C. ovoidea 2011), Hordeum vulgare (Kumar and Singh 2002), appeared as elongated, water soaked lesions, generally Nelumbo nucifera (Cui and Sun 2012) and Zea mays occurred on the spiny margins and abaxial surface of the (Akinbode 2010). Similarly, C. ovoidea has been reported leaves. Progressively, these lesions became sunken and as a leaf spot pathogen on Capsicum annuum (Singh and light brown in color. Later, these lesions were enlarged, Tondon 1970) and Psophocarpus tetragonolobus (Awurum centre of the lesions dark brown in color with maroon red and Emechebe 2001). Other pathogenic fungi have also margins, and measured about 0.7-1.7 × 0.6-1.3 cm in size. been reported to cause leaf spot diseases on A. vera, such In severe infection, the spiny margin of the leaves was as Alternaria alternata (Kamalakannan et al. 2008), twisted inside due to necrosis of the tissues (Figure 2A & Colletotrichum gloeosporioides (Avasthi et al. 2011), B). Interestingly, the disease was observed only in the Nigrospora oryzae (Zhai et al. 2013) and Phoma betae winter season. (Avasthi et al. 2013). Although, C. lunata has already been reported from Jaipur, India, there are no reports available AVASTHI et al. – Leaf spot diseases on Aloe vera caused by Curvularia species 81 for C. ovoidea. To the best of our knowledge, this is the lunata from Madhya Pradesh, while by C. ovoidea from first report of leaf spot disease on A. vera caused by C. India.
A B
C D
Figure 1. Leaf spot disease on A. vera caused by Curvularia lunata. A. Initiation of disease symptoms, B. Mature symptoms, C. Ten days old colony of C. lunata incubated at 25±2 °C on PDA, D. Conidia of C. lunata 82 BIODIVERSITAS 16 (1): 79-83, April 2015
A B
C D
Figure 2. Leaf spot disease on A. vera caused by Curvularia ovoidea. A. Initiation of disease symptoms, B. Mature symptoms, C. Ten days old colony of C. ovoidea incubated at 25±2 °C on PDA, D. Conidia of C. ovoidea
ACKNOWLEDGMENTS REFERENCES
The authors are thankful to Head, School of Studies in Akinbode OA. 2010. Evaluation of antifungal efficacy of some plant Botany, Jiwaji University Gwalior, Madhya Pradesh, India extracts on Curvularia lunata, the causal organism of maize leafspot. African J Environ Sci Technol 4: 797-800. for providing essential laboratory facilities and support to conduct this research work successfully. AVASTHI et al. – Leaf spot diseases on Aloe vera caused by Curvularia species 83
Akinyele BO, Odiyi AC. 2007. Comparative study of the vegetative Aloe vera as affected by organic manure in pot culture. Aust J Crop morphology and the existing taxonomic status of Aloe vera L. J Pl Sci Sci 2: 158-163. 2: 558-563. Jat RN, Jat RG, Nitharwal M. 2013. Management of leaf spot of Indian Avasthi S, Gautam AK, Bhadauria R. 2011. First report of anthracnose Aloe (Aloe barbadensis Mill.) caused by Curvularia lunata (Wakker) disease of Aloe vera caused by Colletotrichum gloeosporioides. J Res Boedijn. J Pl Sci Res 29: 89. Biol 5: 408-410. Joseph B, Justin RS. 2010. Pharmacognostic and phytochemical properties Avasthi S, Gautam AK, Bhadauria R. 2013. First report of Phoma betae of Aloe vera Linn. - An overview. Int J Pharm Sci Rev Res 2: 106- on Aloe vera in India. Arch Phytopathol Pl Prot 46: 1508-1511. 110 Awurum AN, Emechebe AM. 2001. The effects of leaf spot diseases and Kamalakannan A, Gopalakrishanan C, Renuka R, Kalpana K, Lakshmi staking on yield and yield attribute of winded bean Psophocarpus LD, Valluvaparidasan V. 2008. First report of Alternaria alternata tetragonolobus (L.Dc.). J Appl Chem Agric Res 7: 42-47. causing leaf spot on Aloe barbadensis in India. Aust Pl Dis Notes 3: Choi S, Chung MH. 2003. A review on the relationship between Aloe vera 110-111. components and their biological effect. Seminars in Integrative Kumar K, Singh RN. 2002. Leaf spot of barley by Curvularia lunata. Medicines 1: 53-62. Indian Phytopathol 55: 532-533. Cui RQ, Sun XT. 2012. First Report of Curvularia lunata causing leaf Mukherjee A, Bandhyopadhyay A, Dutta S. 2013. New report of leaf spot spot on Lotus in China. Plant Dis 96: 1068. disease of Clerodendrum indicum caused by curvularia lunata. Intl J Daodu T. 2000. Aloe vera, the miracle healing plant. Health Field Pharm Bio Sci 4: 808. Corporation, Lagos. Ni Y, Turner D, Yates KM, Tizard IR. 2004. Isolation and Ellis MB. 1971. Dematiaceous Hyphomycetes. Ist Ed. Kew, characterization of structural components of Aloe vera L. leaf pulp. Commonwealth Mycological Institute, Kew, Surrey, United Intl Immunopharmacol 4 : 1745-1755. Kingdom. Reynolds T, Dweck AC. 1999. Aloe vera leaf gel: A review update. J Gautam AK, Avasthi S, Ashok D. 2011. Leaf spot disease on Grewia Ethnopharmacol 68: 3-37. optiva caused by Curvularia lunata recorded from India. In: Denchev Sharma P, Singh N, Verma OP. 2011. First Report of Curvularia CM (ed.). New records of fungi, fungus-like organisms, and slime lunata Associated with leaf spot of Amaranthus spinosus. Asian J Pl moulds from Europe and Asia: 28-29. Mycologia Balcanica 8:173- Pathol 5:100-101. 174. Singh BP, Tandon RN. 1970. Nutritional studies on two species of Gilman JC. 2012. A Manual of Soil Fungi. Biotech Books, New Delhi, Curvularia causing leaf spot diseases. II. Utilization of various India. sources of sulphur. Proc Nat Acad Sci India 49: 276-280. Hassannuzzaman M, Ahmed KU, Khilequzzaman KM, Shamsuzzaman Zhai LF, Liu J, Zhang MX, Hong N, Wang GP, Wang LP. 2013. The first AMM, Nahr K. 2008. Plant characteristics, growth and leaf yield of report of leaf spots in Aloe vera caused by Nigrospora oryzae in China. Plant Dis 97: 1256. BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 84-88 DOI: 10.13057/biodiv/d160111
The interaction between diversity of herbaceous species and history of planting, Masal’s plantations, Guilan Province, Iran
1, 1 1 2 HASSAN POURBABAEI ♥, MASOUMEH ESKANDARI , MEHRDAD GHODSKHAH DARYAEI , MEHDI HEYDARI 1Department of Forestry, Faculty of Natural Resources, University of Guilan, Somehsara, Guilan, Iran. P.O. Box 1144, Tel.: +98-182-3220895, Fax.: +98-182-3223600, ♥email: [email protected] 2Faculty of Agriculture and Natural Resources, Ilam University, Ilam, Iran.
Manuscript received: 6 November 2014. Revision accepted: 2 February 2014.
Abstract. Pourbabaei H, Eskandari M, Daryaei MG, Heydari M. 2015. The interaction between diversity of herbaceous species and history of planting, Masal’s forests, Guilan Province, Iran. Biodiversitas 16: 84-88. The purpose of this study was to determine the relationship between the plantation age and diversity of herbaceous species. The study area is located in the Masal’s plantations of Guilan in north of Iran. For this purpose, 60 plots were sampled by a randomized-systematic method throughout the study area in order to record the herbaceous species, the Whitaker′s nested plot was applied and the minimal area was obtained 64 m2 (8 × 8 m). In order to evaluate the plant diversity, some indices including Shannon-Wiener’s diversity (H′), species richness (S) and Smith-Wilson’s evenness (Evar) were utilized. Results indicated that 31 herbaceous species were found in two plantations. There were significant differences between two sites regarding H′ and Evar. Whereas, there was no significant difference in view of species richness between two sites. In addition, results revealed that older plantation has not caused to increase richness and evenness of species.
Keywords: Age, diversity, herbaceous species, plantation, Masal’s plantations.
INTRODUCTION which are at risk (Brockerhoff et al. 2003). Plantations can promote regeneration of understorey by shading out There is a very close relation between plants and other grasses, increasing soil nutrients, improving micro-climate, living organisms in an ecosystem. Observing appearance of and generally increasing the chance for seed germination land’s plants shows that these species choose their habitat and establishment, which is difficult in highly degraded according to their intrinsic ecological needs (Heydari and sites (Senbeta and Teketay 2001). Mahdavi 2009). Plants with more complicated structure Plantations can make an important contribution to the than climate and soil become stable in lands and waters and conservation of native biodiversity, but not if their have a major role on life of living things, preserving nature establishment involves the replacement of native natural or and balance of ecosystem as a resources of local system. semi-natural ecosystems. While a plantation stand will Therefore, vegetation is always as an integral part of usually support fewer native species than a native forest at ecosystem. Although forests have covered only 30% of the the same site, plantations are increasingly replacing other land, but current process of destruction and subversion of human-modified ecosystems (e.g., degraded pasture) and forest is worried (Mosaddegh 1994). On the other hand, will almost always support a greater diversity of native regarding increased population and daily increasing species. In addition, plantations can play an important role requirements of wood products and other services of forest, in sustaining native biodiversity in production landscapes developing forests through afforestation is inevitable in and indeed be an opportunity for biodiversity (Brockerhoff present and future (Shabanian et al. 2009). In other words, et al. 2008). Stand age is one of the most important factors destruction and declining natural forests have made it is that affects on plant species diversity (Nagaike et al. 2010, necessary to afforest in order to reconstruct and develop 2003; Li et al. 2014). In areas where primary or old-growth forests. Plantation forests, or planted forests, are cultivated forests have already disappeared or diminished forest ecosystems established by planting or seeding in the considerably, long rotation plantations are thought to process of afforestation and reforestation, primarily not mitigate the detrimental effects on biological diversity only for wood biomass production but also for soil and (Ratcliffe and Peterken 1995). With increasing rotation age water conservation or wind protection (Carnus et al. 2006). in plantations allows to restore old-growth habitats, which Presently, the objectives of plantations not only for the can be cause structural and biological diversity (Ferris et al. production of lumber and wood products but also include 2000; Humphrey et al. 2000; Peterson and McCune 2001). the provision a habitat for wildlife and non-commercial The plantations also have an important role in ecological plants and the conservation of biological diversity (Nagaike reconstruction and create various environmental services. et al. 2003). Plant species diversity in plantations has a Therefore, a comprehensive study about plantation effect prominent role in order to preserve genetic resources, on all part of ecosystems (living and non-living) is assessing ecological succession and identifying species necessary. Today, survey in biodiversity is crucial in POURBABAEI et al. – The interaction between species diversity and history of planting 85 terrestrial ecosystems due to extinction of plant species and Data collection reduction of their population (Pourbabaei et al. 2004). The study design was a random-systematic method with The purpose of the study was to determine floristic list grid dimension of 150 m × 200 m and 60 sample plots were and to compare herbaceous species diversity in two taken from the two sites. The size of the sample plot was different age plantations with the same species. obtained 68 m2 using Whitaker′s nested plots and species/area curve. The factors such as percentage of canopy cover, herbaceous species and light, litter depth MATERIALS AND METHODS were recorded in each sample plot. The herbaceous species were identified in herbarium of Faculty of Natural Study area Resources, Guilan University, Iran. The study area is located in west of Guilan Province and in Talesh mountain range, Iran (Figure 1). The mean Data analysis annual precipitation and temperature are 989.7 mm and To measure diversity, Shannon-Wiener index (Shannon 16oC, respectively. The climate is very humid with cool and Weaver 1949) was used, which is computed as winters based on Emberger method. Soil of the region is following equation: brown calcic along with brown calcimorphic soil (FRWO s 2008). General altitude of the region is 150-200 m asl. and H'Pi lnpi the average slop is from 20 to 25 percent. i1 Two plantations areas (i.e., Ahaklan and Tabarsa) with th an area 100 ha and located in Masal City, 55 kilometers Pi is relative frequency of i species. from the center of Guilan Province were selected. The two To measure richness Margalef’s index (Clifford and Stephenson 1975) was used, which is computed as sites have the same conditions in terms of physiographic factors and dominated species were as follows: Alnus following equation: subcordata C.A. Mey, Acer insigne Boiss, Fraxinus R S 1 excelsior L., Quercus castaneifolia C.A. Mey, Populus 1 ln N deltoids Marsh., Robinia pseudoacacia L. The Ahaklan and Tabarsa sites had 9 and 22 years old, respectively. S is total number of species and N is total population in sample plot.
Figure 1. Study areas location in Masal City, Guilan Province, Iran. 86 BIODIVERSITAS 16 (1): 84-88, April 2015
To measure evenness, Smith-Wilson’s index (Smith and RESULTS AND DISCUSSION Wilson 1996) was used, which is computed as following equation: Our findings revealed that there are significant differences in percentage of canopy cover and herbaceous species (P<0.05), so that percentage of canopy cover, and 2 light were higher in 22 years than in 9 years old plantation. E var s s However, percentage of herbaceous species was more in 9 arcton log (ni) log (nj) / s) 2 / S e e years old than in 22 years old plantation. i1 j 1 In 9 years old plantation, species which had percentage of cover more than 10% are as follow: Rubus hyrcanus 20.38, Asplenium adiantum-nigrum (14.72), Carex Where, ni is population of species i in sample plot, nj is sylvatica (13.83), Microstegium vimineum (11.75), population of species j in sample and S is numbers of Potentilla reptans (11.54), Sambucus ebulus (11 ) and species in all samples. Mentioned indices computed by Calystegia sepium (10). In addition, in 22 years old Ecological Methodology software for Windows version 6.0 plantation species which had percentage of cover more than (Krebs 1989). 10% are as follow: Oplismenus undulatifolius (16.58), To compare structural characteristics and averages of Carex sylvatica (15), Viola alba (13.09), Sambucus ebulus diversity and evenness in the two sites, student t-test was (12.5), Microstegium vimineum (11.67). Totally, there were used. Before doing the test, Kolmogorov-Smirnov test was 31 species belonging to 26 families in the two plantations. used to be certain about the normality of data. These The 21 species were common in the both sites, 4 species statistical analyses were done using SPSS 16.0. were only in Ahaklan (9 years old) and 6 species were found only in Tabarsa (12 years old) as well as 4 species had 1% or less coverage the in both sites (Table 1).
Table 1. List of species [(-) herbaceous absence; (+): presence]
Family name Scientific name F.* F. P.C.** P.C. Plantation age (year) 22 9 22 9 22 9 Aspleniaceae Asplenium adiantum-nigrum L. 22 18 9.83 14.72 + + Euphorbiaceae Acalypha australis L. 17 4 9.5 7.5 + + Convolvulaceae Calystegia sepium L. 4 1 2.75 10 + + Cyperaceae Carex divulsa L. 26 30 4.7 4.6 + + Cyperaceae Carex sylvatica L. 26 30 15 13.83 + + Asteraceae Conyza bonariensis L. 7 8 1.86 2.84 + + Umbelliferae Eryngium caucasicum Trautv. - 10 - 5.5 - + Geraniceae Geranium robertianum L. - 8 - 6.87 - + Asteraceae Helianthus tuberosus L. - 2 - 1 - + Hypericaceae Hypericum androsaemum L. 13 21 4.31 4.69 + + Hypericaceae Hypericum perforatum L. 3 - 1 - + - Asteraceae Inula caspica Bium. 2 1 0.25 5 + + Lamiaceae Lamium album L. 3 - 3.5 - + - Lamiaceae Mentha aquatica L. 21 17 11.67 5.29 + + Poaceae Microstegium vimineum Trin. 21 20 11.67 11.75 + + Poaceae Oplismenus undulatifolius (Ard.) P.Beauv. 19 17 16.58 9.7 + + Oxalidaceae Oxalis acetosella Boiss. 12 8 3.89 4 + + Plantaginaceae Plantago major L. 2 - 0.75 - + - Aspleniaceae Phyllitis scolopendrium (L.) Scop. 3 - 5 - + - Polygonaceae Polygonum hydropiper L. 6 6 9.25 6.67 + + Rosaceae Potentilla reptans L. 9 13 6.11 11.54 + + Asclepiadaceae Periploca graeca L. - 2 - 1 - + Pteridiaceae Pteris cretica L. 19 18 9.76 7.51 + + Rosaceae Rubus hyrcanus Juz. 5 13 0.5 20.38 + + Caprifoliaceae Sambucus ebulus L. 6 10 12.5 11 + + Lamiaceae Satureja hortensis L. 2 2 7.62 3 + + Asparaginaceae Smilax excelsa L. 17 24 6.94 5.83 + + Solanaceae Solanum nigrum L. - 1 - 1 - + Caryophyllaceae Stellaria media (L.) Cyr. 3 - 6.67 - + - Asteraceae Taraxacum syriacum Boiss. - 2 - 3 - + Violaceae Viola alba L. 21 23 13 7.83 + + Note: *F.: Frequency, **P.C.: Percent Coverage. POURBABAEI et al. – The interaction between species diversity and history of planting 87
Table 2. Diversity indices in herbaceous layer in view of richness. In spite of, richness mean was a few more in Tabarsa site. Nagaike et al. (2003) in three Plantation age Sig. different ages of a plantation concluded that plantation with Indices 9 22 higher age had less diversity and richness than younger H´ 3.01 2.63 0.03 plantation and opening canopy, obtaining much light and E 0.66 0.51 0.04 Var pruning weeds are reasons for high diversity in younger R 2.09 1.88 0.20 1 plantation. The results of Nagaike’s studies indicated that the relationship between stand age and plant species diversity and richness of forest floor plants have been Table 3. Relationships between the herbaceous diversity indices varied in plantations. Several studies have shown a positive and environmental factors in 9 and 22 years old stands correlation between plant species diversity and plantation age (Kirby 1988; Kiyono 1990), whereas Hill and Jones Age Index Pearson Litter Light Canopy (1978) and Sykes et al. (1989) demonstrated that the
9 R1 r 0.10 -0.10 0.01 richness of herbaceous species in Picea sitchensis, P. abies, P 0.57 0.58 0.95 and Tsuga heterophylla plantations decreased with H´ r 0.18 0.01 -0.12 increasing stand age. Peterken and Game (1984) found that P 0.33 0.93 0.52 the richness of herbaceous species was not correlated with EVar r 0.17 0.10 -0.17 plantations age that were planted between 1600 and 1947 P 0.35 0.59 0.34 in England (Nagaike et al. 2003). 22 R1 r -0.10 0.37 -0.4 The result showed that there was significant positive P 0.56 0.04 0.03 correlation between Shannon-Wiener and richness indices H´ r -0.15 0.42 -0.39 with light in 22 years stand. On other hand, Shannon- P 0.41 0.03 0.02 Wiener and richness indices had negative correlation with EVar r -0.15 -0.17 -0.07 canopy cover. There were not any correlations between P 0.40 0.36 0.68 diversity indices with canopy, light and litter depth in 9 years old stand. Canopy cover values are closely related to Plant diversity understorey light levels (Machado and Reich 1999) and Regarding to diversity and evenness, there were they are effective on net primary productivity and nitrogen significant differences between the two sites (P<0.05), but cycling rates (Reich et al. 2001). Higher light availability in there was not any significant difference in view of richness younger plantation is favorable for the growth of (P>0.05). Average cover herbaceous was higher in species heliophytes; lower light availability in older plantation is such as Plantago major and Microstegium vimineum in 9 more favorable for neutrophilous or shade-tolerant plants years of plantation, but Oplismenus undulatifolius had the (Christian et al. 1994). most average cover in 22 years of plantation (Table 2). It seems light availability in 22-year-old stand was more favorable for plant species diversity. This result can be justified because the light in young plantation is intense Relationships between the herbaceous diversity indices and direct. Light is commonly considered to be the major and canopy cover, light and litter depth limiting factor of forest vegetation cover and (or) richness The result showed that there were significant positive (Barbier et al. 2008). correlations between Shannon-Wiener and richness indices Higher opening canopy cover provides condition for a with light in 22 years stand. In other hand, Shannon- higher abundance of Rubus hyrcanus in 9 years old site Wiener and richness indices had negative correlation with where had significant difference with 22 years old site in canopy cover. There were not any correlations between view of percentage of canopy cover of Rubus hyrcanus. If diversity indices with canopy cover, light and litter depth in the salvage cutting does not apply until canopy is closed, 9 years stand. Also, there was not any significant tree regeneration is disturbed and shadows destroyed it. correlation between the herbaceous diversity indices and Also, Asplenium adiantum is found wherever light is very litter in the both stands (Table 3). much so it creates a competitive condition for other species and it is more successful in this competition. In addition, Discussion Calystegia sepium and Potentilla reptans were more in 9 Our findings in the studied sites showed that percentage years old site which is due to high light requirement these of herbaceous species in 9 years old plantation was species. There were six species (Eryngium caucasicum, significantly more than 22 years old. This is probably due Geranium robertianum, Helianthus tuberosus, Periploca to opening canopy of 9 years old site. On the other hand, graeca, Solanum nigrum and Taraxacum syriacum) which opening canopy cover creates situation to enter more light they only found in nine years old plantation. On the other in the environment so that it is a suitable environment for hand, Oplismenus undulatifolius had a high percentage in herbaceous species. Rees and Juday (2002) stated that 22 years old plantation and this species is indicating high richness of plant species in forests is affected by open or compacted soil. This is due to presence of wild and closed canopy of overstorey. Also, there was significant domestic animals of adjacent regions come to this area of difference in diversity and evenness between two sites and plantation and cause a compacted soil. In addition, the these values were more in 9 years old plantation. However, other reason for less percentage of vegetation in 22 years there is not significant difference between two plantations 88 BIODIVERSITAS 16 (1): 84-88, April 2015 old plantation than 9 years old site is closed canopy cover FRWO [Forests, Range and Watershed Management Organization]. 2008. and shortage of light and higher regeneration of Buxus Forestry plan. General Depatrment of Natural Resources of Guilan Province, Someahsara. hyrcana species in this site. Since Buxus hyrcana is a shade Heydari M, Mahdavi A. 2009. Patterns of plant species diversity related to tolerant species, consequently it prevents to establish shade physiographic factors in Melah Gavan protected area, Iran. Asian J intolerant herbaceous species and it is decreased percentage Biol Sci 2: 21-28. of vegetation. Also, Pourbabaei et al. (2004), stated the Hill MO, Jones EW. 1978. Vegetation changes resulting from afforestation of rough grazings in Caeo forest, south Wales. J Ecol 66: same reason for low percentage cover of some species in 433-456. the Tanian region in Somesara city. Veinotte et al. (1998) Humphrey JW, Newton AC, Peace AJ, Hilden E. 2000. The importance of and Humphrey et al. (2000), found that plant diversity in conifer plantations in northern Britain as a habitat for native fungi. plantation increases rapidly in early ages of plantation due Biol Conserv 96: 241-252. Kirby KJ. 1988. A woodland survey handbook. Nature Conservation to intensity of light and sometimes invasive species become Council, Peterborough, UK. dominant species. When the age of plantation is increased Kiyono Y. 1990. Dynamics and control of understories in Chamaecyparis and the light intensity decreased, as a result it causes to obtusa plantations Bull For Prod Res Dev Inst 359: 1-122. decrease herbaceous diversity. Kuksina and Ulanova Krebs CJ. 1989. Ecological Methodology. Harper Collins, New York. Kryshen AM. 2000. Dynamics of vascular plant diversity at the initial (2000) stated that when canopy cover is closed in stases of reforestation after clear cutting of secondary spruce stand. plantations, plant species diversity declines. Proceding of Reforestation and Management of Biodiversity. Kohmo, Kryshen (2000) found about 90% vascular species in a Findland. August 21-25. Aspen plantation during 1 to 2 first years, but 3 to 4 years Kuksina N, Ulanova G. 2000. Plant species diversity in spruce forest after clear cutting disturbance: 16 year monitoring in Russian Taja. after planting when canopy cover was closed, presence of Proceding of Reforestation and Management of Biodiversity. Kohmo, vascular plant declined to 58% and annual plants declined Findland. August 21-25. to 40%. In general, plantations in a long-term help to Li Y, Chen X, Xie Y, Li X, Li F, Hou Z. 2014. Effects of young poplar maintaining ecological processes in ecosystems. Also, plantations on understory plant diversity in the Dongting Lake wetlands, China. Sci Rep 4: 6339. different managements have major effects on diversity of Machado JL, Reich PB. 1999. Evaluation of several measures of canopy plant species in forest ecosystems (Nagaike et al. 2003). openness as predictors of photo-synthetic photon flux density in Regarding to the aim of plantation whether is for deeply shaded conifer-dominated forest understory. Canadian J For restoration or economic exploitation; we should achieve Res 29: 1438-1444. Mosaddegh A. 1994. Geoghraphy of world forests, publications university our purposes using different managements in different of Tehran, Tehran. plantations. Regarding that this research has conducted in Nagaike T, Hayashi A, Abe M, Arai N. 2003. Differences in plant species two sites with different plantation ages, it is recommended diversity in Larix kaempferi plantations of different ages in central that such studies which conducted in consecutive years Japan. For Ecol Manag 183: 177-193. Nagaike T, Hayashi A, Kubo M. 2010. Diversity of naturally regenerating with pure and mixed species being compared and surveyed. tree species in the overstorey layer of Larix kaempferi plantations and abandoned broadleaf coppice stands in central Japan. Forestry 83: 285-291. Peterken GF, Game M. 1984. Historical factors affecting the number and ACKNOWLEDGEMENTS distribution of vascular plant species in the woodlands of central Lincolnshire. J Ecol 72: 155-182. We hereby offer our profound thanks and appreciation Peterson EB, McCune B. 2001. Diversity and succession of epiphytic to all dears who were cooperated us in different stages of macrolichen communities in low-elevation managed conifer forests in Western Oregon. J Veg Sci 12: 511-524. this research. Pourbabaei H. Shadram S, Khorasani M. 2004. comparison plan diversity between plantation Alnus subcordata and mixed plantation Fraxinus excelsior-Acer insigne in region Tanian of Somesara. Iranian J Biol REFERENCES 17: 357. Ratcliffe PR, Peterken GF. 1995. The potential for biodiversity in British upland spruce forests. For Ecol Manag 79: 153-160. Barbier S, Gosselin F, Balandier P. 2008. Influence of tree species on Rees DC, Juday GP. 2002. Plant species diversity on logged versus understory vegetation diversity and mechanisms involved—A critical burned sites in central Alaska. For Ecol Manag 155: 291-302. review for temperate and boreal forests. For Ecol Manag 254: 1-15. Reich PB, Peterson DW, Wedin DA, Wrage K. 2001. Fire and vegetation Brockerhoff EG, Ecroyd CE, Leckie AC. 2003. 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BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 89-94 DOI: 10.13057/biodiv/d160112
Feeding habit and length weight relationship of keureling fish, Tor tambra Valenciennes, 1842 (Cyprinidae) from the western region of Aceh Province, Indonesia
ZAINAL A. MUCHLISIN1,♥, AGUNG S. BATUBARA1, MOHD N. SITI-AZIZAH2, MUHAMMAD ADLIM3, AFRIZAL HENDRI4, NUR FADLI1, ABDULLAH A. MUHAMMADAR1, SUGIANTO SUGIANTO4 1Department of Aquaculture, Faculty of Fishery and Marine Sciences, Syiah Kuala University, Banda Aceh 23111, Tel. +62-651-7411323, Fax. +62-651- 7552370 Indonesia. ♥email: [email protected] 2School of Biological Sciences, Universiti Sains Malaysia, 11800 Penang, Malaysia. 3Department of Chemistry, Faculty of Education and Teacher Training, Syiah Kuala University, Banda Aceh 23111, Indonesia. 4Faculty of Fisheries and Marine Sciences, Teuku Umar University, Meulaboh, Indonesia 5Faculty of Agriculture, Syiah Kuala University, Banda Aceh 23111, Indonesia
Manuscript received: 8 December 2014. Revision accepted: 5 February 2015.
Abstract. Muchlisin ZA, Batubara AS, Siti-Azizah MN, Adlim M, Hendri A, Fadli N, Muhammadar AA, Sugianto S. 20015. Feeding habit and length weight relationship of keureling fish, Tor tambra Valenciennes, 1842 (Cyprinidae) from the western region of Aceh Province, Indonesia. Biodiversitas 16: 89-94. The objective of the present study was to describe the aspects of feeding habit and length- weight relationship of keureling fish Tor tambra, this information is crucial to plan a conservation startegy for this species. A series of samples were taken between June and September 2012 and February 2014 in the two main rivers of western Aceh i.e. the Sikundo and Nagan Rivers. A total of 48 and 38 fish were caught during the study in Nagan and Sikundo Rivers, respectively. Stomach content analysis suggested that freshwater green algae and earthworms were the main food items for T. tambra, indicating an omnivorous feeding habit. In addition, the length-weight relationship revealed that T. tambra has an allometric negative growth pattern from all populations, and the condition factors indicate the rivers are still in good condition and support fish life.
Key words: Allometric, LWS, green algae, threatened, proponderance
INTRODUCTION tambra (Muchlisin et al. 2009) and presumed one other species of T. douronensis was also occurred in Aceh waters The Aceh Province Indonesia has many aquatic (Muchlisin et al. 2014). Of these four species, T. tambra is resources including coastal waters, marshes, rivers and is the most abundant and the most highly target fish due to lakes and rain forests in the Leuser and Ulu Masen its good taste and higher price of upto USD35-kg. ecosystems (Muchlisin et al. 2012). According to The keureling is one of the largest freshwater fishes in Muchlisin and Siti-Azizah (2009) there are at least 114 Aceh, reaching upto 30-45 kg. Therefore, this species has freshwater fishes in Aceh waters Indonesia, of these 14 always been the predominant target of local fishermen species have high economical value. In addition, a total of using various fishing gears, including destructive fishing 73 species were recorded in the Tripa peat swamp forest in gears, such as electric fishing, poison and dynamite. This the western coast of Aceh Province where 46 species are has resulted in declining wild population over the last ten categorized as fish consumption and 17 have potential for years (Personal communication with local fishermen). aquaculture, for example Tor tambra, Anabas testudineus, According to local fishermen, it is very difficult to catch Anguilla bicolor, Channa spp., Clarias spp., Anematichthys large wild mahseer any more. Presently, T. tambra is repasson, Cyclocheilichthys spp., Osteochilus spp., Oxyele- currently listed as endangered in the IUCN red list (IUCN tris sp., and Barbonymus sp. (Muchlisin et al. 2015). In 1990). According to Kottelat et al. (1993) and Singh (2007) particular, the Genus Tor or locally know as keureling, it is the Genus Tor is threatened by over-explotation, pollution belonging to the family Cyprinidae, forms the basis of a and ecological perturbation. This is supported by Decamps wild fishery and has high potency for aquaculture industry (2011) who stated that most large freshwater fish species (Muchlisin 2013). This genus is an important group of are threatened by overfishing and habitat degradation on a freshwater cyprinids in Indonesia and Malaysia which global scale. inhabits fast flowing stream throughout the trans- Fishing keureling in the wild should be reduced and Himalayan and South-east Asian regions (Ambak et al. possibly be prohibited in the future to protect this species; 2007). There are 20 species of Tor in Asia (Kiat 2004) and hence the fishermen have to shift their business to at least four (T. soro, T. tambra, T. douronensis dan T. aquaculture. For this purpose, breeding and feeding tambroides) are found Indonesian (Haryono 2006), three of technologies need to be developed. Therefore, information these were recorded in Aceh; T. soro, T. tambroides and T. on biological aspects such as feeding, reproduction and 90 BIODIVERSITAS 16 (1): 89-94, April 2015 growth are crucially important to support these programs. Indonesia. The first location was Nagan River, Nagan Raya Information of feeding habit of fish in their natural habitat District at seven sampling sites: (1) 040.14’.34,9”N, is crucial in order to support the domestication process and 960.29’.36,7”E; (2) 040.14’.39,6” N, 960.30’.44,1” E; (3) to develop feeding practices and breeding technologies to 040.14’.40,20”N, 960.30’.24,20”E; (4) 040.14’.44,3”N, support the aquaculture industry and to plan an effective 960.31’.00,1” E; (5) 040.16’. 50,7” N, 960.26’. 0”E; (6) conservation strategy. Indonesia is known as a mega 040.16’.34,2” N, 960.27’.13,7”E; (7) 040.16’.19,4”N, biodiversity country second in fish species richness only to 960.27’.42,6” E, and the second location was Sikundo Brazil (Muchlisin and Siti-Azizah, 2009); however, there is River, Aceh Barat Distric at two sampling sites: (8) 040. very limited information on the biology and ecology of 28’.36,5”N, 960.21’.52,1”E; (9) 040.13’.29,6”N, fishes in particular threatened species from Aceh waters for 960.10’.24,4”E. Site selection was based on information by example within genus Tor. To date only two threatened local residents. Gillnets (mesh size of 0.75, 1, 2 and 3 inch- species of Rasbora tawarensis and Poropuntius tawarensis normally metric), hooks and casting nets (mesh size of 1, 2 from this region have been studied comprehensively and 3 inch) were used to collect the fish samples. (Muchlisin et al. 2010a; 2010b; 2011b). Hence, the The collected fishes were counted, rinsed and objective of the present study was to desribe important anesthetized in a solution of tricaine methanesulfonate (MS aspects of the biology of T. tambra in particular, diet and 222), prepared by dissolving 4 g of MS 222 in 5L tap growth pattern from western region of Aceh Province, water, then preserved in 10% formalin in a plastic bag with Indonesia. which was tagged with the location, date and habitat characteristics. The fish samples longer than 10 cm in total length were injected with absolute formalin in their body MATERIALS AND METHODS cavity prior to preservation in 10% formalin to unsure that internal organs (gonad and alementary organs) did not Study site and sampling decay. Fishes were identified based on Kottelat et al. The study was conducted for four months between June (1993). Samples were transported to the laboratory for and September 2012 plus February 2014 at two different further evaluation. locations in western region of Aceh Province, Sumatra,
8
6 5 7 1 3 2 2 4 9
Figure 1. Map of Aceh Barat and Nagan Raya Districts of Aceh Province showing sampling sites MUCHLISIN et al. – Tor tambra of the western Aceh 91
Diet analysis same fish as calculated from a composite of length-weight The specimens were abdominal dissected by using a regression throughout the range of the species: Ws = aLb. surgical scissors, and then their stomachs were taken and The Fulton condition coefficient (K) was determined weighed nearest to 0.01 g. The stomachs were dissected according to Okgerman (2005) as follows: and the contents emptied into a petri-dish. The larger foods K = WL-3 x 100 were isolated, counted and weighed. The food items were where K is the condition factor, W is weight (g), L is observed by the nake eye. length (mm), and -3 is coefficient of length to ensure that the K value tend to one. Food occurrence The occurrence of each food item was scored and then converted to a percentage by multiplying the ratio of the RESULTS AND DISCUSSION number of times an item occurred to the total number of stomachs analyzed by a hundred. The percentage Diets abundance of each food item was also computed by A total of 48 and 38 keureling fish were caught from multiplying the ratio of the number of a particular item in Nagan and Sikundo Rivers, respectively, of these stomach the stomach to the total number of items in the stomach by content was examined for 45 and 35 fishes. The stomach a hundred. contents of fish from Nagan containing 69.6% of earthworms, 27.8% of green algae, 2.1% of leafage and Index of proponderance 0.5% of sands. The keureling from Sikundo has stomach Index of preponderance is a combination of volumetric contents of green algae (77.60%) and earthworms (22.4%) and frequency of occurrence methods, and it is used to (Table 1). The analysis of food occurance showed that identify the most important food items eaten by fish. The earthworms found in 80.8% and 81.3% of the fish samples index proponderance of fish was calculated based on from Nagan River and Sikundo, respectively. While, green Biswas (1993) as follow: algea was found in 73.1% and 93.8% of fish samples from Nagan and Sikundo, respectively (Table 2). However, the preponderance index analysis showed that green algae was the most important food item for keureling fish from both populations (Table 3). Where Ii= Index of preponderance, Vi = Percentage of Th results revealed that the younger fish prefer volume of each food item, Oi = percentage of occurence of earthworms, but this shifted to green algae after the fish each food item, ∑Vi is total percentage of occurence of reached bigger size (Table 4). Change in feeding habit was food items, ∑Oi is total percentage of volume for all food associated with an increase in the length of the alimentary items. tract. For example, fish 100-175 mm in lenght (137.5 mm average) had an alimentary tract length of157 mm (1.2 Dietary shifts times of alimentary tract). This increased to 377 mm with To evaluate the ontogenic shift in dietary preference, an average total length of 288 mm (1.3 times of alimentary the sampled fishes were divided into three length classes tract). i.e. 100-175 mm, 176-250 mm, and 251-325 mm. The food Our results showed that the T. tambra eat both plants compositions of each class were evaluated and compared. and aquatic animal, indicating an omnivorous diet. Further evidence in support of omnivory is the fact that their Lenght weight relationship and condition factor alimentary tract length was slightly longer than the body The Linear Allometric Model (LAM) was used to length (1.25 times of the total length). According to Smith estimate the parameters a and b by log-transformed weight (1989),omnivorous fish have a digestive tract 1.5 to 2 times and length measurements. A correction for bias attributable their total body length. Haryono (2006) studied the feeding to the back-transformation of mean weights from habit of T. tambroides from the Barito River, Central logarithmic units was applied to predict weight at length Kalimantan, Indonesia and the alimentary tract of this from parameters fitted to the allometric equation following species was 1.5 times of the total body length. Green algae De-robertis and William (2008): and earthworms were the foremost food items for mahseer W = e0.56 (aLb) in Sikundo and Nagan Rivers, Western Aceh, Indonesia. where W is the weight (g), L is the length (mm), a the According to local fishermen, in addition to green algae intercept of the regression, b the regression coefficient and mahseer also eats figs, small crabs and mollusks. In e is the variance of the residuals from the LAM regression. addition, the local fishermen in Sikundo River frequently 0.56 is the correction factor of the data sets. use chopped cassava for catching mahseer. The diet of the keureling fish also changed with ontogeny where smaller The relative weight (Wr) and Fulton condition coefficient (K) were used to evaluate the condition factor fish fed preferentially on earthworms, and this changed to a diet of mainly green algae above 175 mm body length. of T. tambra. Relative weight (Wr) was determined according to Rypel and Richter (2008) as follows: According to Kolkovski (2001) and Mai (2005) that at early life of fish, the alimentary tract is rudimentary and Wr = (W/Ws) x 100 insufficient digestive enzyme capacity so they are unable to where Wr is relative weight, W the weight of a digest algae. However, in several marine fishes the particular fish and Ws the predicted standard weight for the 92 BIODIVERSITAS 16 (1): 89-94, April 2015 alimentary tract has been present at first day hatching Table 1. Volume of food items consumed by keureling fish (T. larvae, but not well developed (Infante and Cahu 2001; tambra) in Nagan and Sikundo Rivers, Aceh Province, Indonesia. Putra et al 2012). Nagan River Sikundo River Food items n=45 n=35 Length weight relationship and condition factors Total Volume The total lengths ranged between 117 mm to 194 mm volume (%) (%) (mL) (mean 149.89±19.33 mm) and 120 mm to 505 mm (mean (mL) 228.32±99.66 mm) for Nagan and Sikundo population, Green algae 5.3 27.8 20.1 77.6 respectively. There were no fish greater than 200 mm Earthworm 13.3 69.6 5.8 22.4 lengthin Nagan River. The relative weight condition factors Leafage 0.4 2.1 - - were closed to 100, while the Fulton’s condition factor Sand 0.1 0.50 - - ranged from 1.75 to 2.67. Total 19.1 100 25.9 100 The length weight relationship showed that the tambra has b value between 2.34 to 2.84 (Table 5). Growth is considered isometric when b value is equal to 3 or Table 2. Food items occurance in keureling fish (T. tambra) stomach from Nagan and Sikundo Rivers, Aceh Province, allometric if otherwise (positive allometric if b>3 and Indonesia. negative allometric if b<3). However, generally exponent b values lie between 2.5 to 3.5 (Froese 2006). The exponent Nagan River Sikundo River b values irrespective populations were lower than 3 (b<3). Foo items n= 45 n=35 Thus, both populations could be categorized as displaying Occurance % Occurance % allometric negative growth. The allometric negative growth Green algea 19 73.1 15 93.8 pattern has been observed in several freshwater fish species Earthworm 21 80.8 13 81.3 in Southeast Asia for example; Garra cambodgiensis from Leafage 3 11.5 - - Ulu Dungun, Malaysia (Mazlan et al. 2007), Rasbora sand 1 3.9 - - sumatrana in Bukit Rengit, Malaysia (Shukor et al. 2008), R. tawarensis and Poropuntius tawarensis (Muchlisin et al. 2010b). On the other hand, Mystacoleucus marginatus Table 3. Index preponderance of keureling fish (T. tambra) fish (Mazlan et al. 2007) displayed allometric positive growth from western region of Aceh Province (Nagan and Sikundo pattern. In contrast, isometric growth pattern was observed Rivers). in Leiognathus jonesi and L. decorus sampled from the coastal waters of Pulau Sibu-Tinggi, Malaysia (Mazlan and Food item Vi Ii Food item occurance Vi × Oi Seah 2006) and serandang (Channa pleurophthalmus) in (%) Musi River, Indonesia (Said 2007). mL % Occur. % The predicted growth was relatively similar to actual Green algea 20.1 77.6 15 93.8 7275.94 78 growth trend (Figure 2), indicate the fish is growing in Earthworm 5.8 22.4 13 81.3 1819.19 22 optimum performance in both Sikudo and Nagan Rivers. Total 25.9 100 - - 9095.13 100 However, unfortunately, no large mahseer were caught, suggesting the species is overfished in these rivers. In general, population b values are dependent on Table 4. Dietary shift of the keureling fish (T. tambra) according physiological growth condition such as gonad development to the length classes and food availability (Jenning and Kaiser 2001), biological and environmental conditions, geographical, temporal and Length of Food occurance alimentary tract sampling factors (Froese 2006). According to Shukor et al. Fish size Erath- Green recorded in this study where the Sikundo and Geumpang (mm) Others Range Average worm algae Rivers have higher speed of water flow compared to Nagan (%) (mm) (mm) (2008) fast flowing streams result in lower b value as (%) (%) 100 - 175 81.25 75 12.5 118-214 157 River resulted in lower in b values relatively. Besides the 176 - 250 100 100 - 190-294 273 above stated factors, it is speculated that the b value is also 251 - 325 33.3 100 - 312-396 377
Table 5. Lenght weight relationship and condition factors of two populations of keureling fish (T. tambra) from western region of Aceh Population Parameter Nagan River (n=48) Sikundo River (n= 38) Total lenght, TL (mm) 117.0 - 194.0 (149.9±19.3) 120.0 - 505.0 (228.3±99.7) Measured weight, W (g) 17.4 - 70.9 (33.4±13.2) 28.0 - 1390.0 (201.7±340.4) Predicted weight, Ws (g) 15.7 - 66.1 (33.2±12.4) 22.8 - 1000.1 (177.0±243.6) Relative weight, Wr (g) 74.5 - 123.9 (100.6±10.9) 55.9 - 139.0 (102.3±20.8) Fulton condition factor, K 2.5 - 2.9 (2.7±0.1) 2.7 - 3.1 (3.0±0.1) b value 2.84 2.63 MUCHLISIN et al. – Tor tambra of the western Aceh 93
average size reported elsewhere (Asih and Setijaningsih 2011; Sarkar et al. 2012; Haryono 2006). According to the local fishermen of Nagan Raya and Aceh Barat districts it is very difficult to find larger fish over the last decade, suggesting the keureling fish has been over exploited and is highly threatened in Nagan and Sikundo Rivers. This finding is in agreement with Haryono and Subagja (Haryono and Subagja 2008) who studied the T. tambroides in Muller Mountains, Central Kalimantan where the the population were dominated by juvenile fish. Similarly, Ogale (2002) reported that the mahseer (Genus Tor) population in India has been declining in number and size and is in serious danger of extinction due to indiscriminate fishing of brood and juvenile fish and the adverse effect on the habitat of of the river valley Figure 2. Comparison between observed and predicted growth for development projects. Clearly, the mahseer has a number keureling fish (T. tambra) catches in Nagan and Sikunod Rivers of life history traits that make if vulnerable to overfishing (growth curve of predicted, y= 0.723x-71.50, R2= 0.983 and and accordingly much more information on the ecology observed growth, y= 0.648x-63.86, R2=0.906) and biology of these species are required to ensure the sustainability of the resource. The stomach content analysis indicated that earthworms affected by fish behaviour, for example active swimming and freshwater green algae were the most important food fish (mostly pelagic fishes) have lower b value compared to for keureling T. tambra in western Aceh region, indicates passive swimming fishes (mostly demersal fishes). This is an omnivorous feeding habit. In addition T. tambra had an related to the energy allocation for movement and growth allometric negative growth pattern, both relative weight (Muchlisin et al. 2010b). Our results suggest that T. tambra index and Fultons condition factor showed that the rivers is an active fish. can still support the presence of T. tambra. The relative weight condition factors were closed to 100 indicating the population is stabile with sufficient food and a lack of predation. The condition factor is regularly ACKNOWLEDGEMENTS calculated to assess the overall health, productivity and physiology of fish population (Richter 2007; Blackwell et The work reported in this paper was supported by a al. 2000). It reflects the fish physiological characteristic grant from the Directorate General of Higher Education such as body morphology, lipid content and growth rate (DGHE), Republic of Indonesia (Project No. (Bister et al. 2000; Rypel and Richter 2008; Stevenson and 139/UN11/A.01/APBN-P2T/2012). We express appreciate Woods, 2006). The b value and condition factor of T. to anonymous reviewers for their critical comments and tambra from Sikundo River were relatively lower than suggestions. The technical assistance by all members of those Nagan River (Table x). According to Anderson and Aquaculture Research Group of Syiah Kuala University, Neumann (1996), values of Relative Weight (Wr condition Banda Aceh, Indonesia are also acknowledged. factor) falling below 100 for an individual or population suggest problems such as low prey availability or high predatory density, whereas values above 100 indicate prey REFERENCES surplus or low predatory density. In addition, Porath et al. (2003) stated that changes in body condition could be Ambak MA, Ashraf AH, Budin S. 2007. Conservation of the Malaysian interpreted as a measure of predation success i.e. fish of mahseer in Nenggiri basin through community action . 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Comparison of woody species diversity between managed and unmanaged forests considering vertical structure in Hyrcanian forests, Iran
ZAHRA NOURI♥, MAHMOUD ZOBEIRI, JAHANGIR FEGHHI, GHAVAMALDIN ZAHEDI AMIRI, MOHAMMAD REZA MARVIE MOHADJER Tehran University, Faculty of Natural Resources, department of Forestry and Forest economics, Shahid Chamran Blvd., Karaj, Elborz Province, Iran. Tel.: +989111584369, Fax: +982632249312, ♥email: [email protected]
Manuscript received: 27 January 2015. Revision accepted: 13 March 2014.
Abstract. Nouri Z, Zobeiri M, Feghhi J, Amiri GZ, Marvie Mohadjer MR. 2015. Comparison of woody species diversity between managed and unmanaged forests considering vertical structure in Hyrcanian forests, Iran. Biodiversitas 16: 95-101. Biodiversity conservation is increasingly considered a key to sustainable forest management and understanding biodiversity in forest ecosystems is essential to reveal forest dynamics, so this study aims to compare tree and shrub species diversity and vertical species distribution between two managed and unmanaged forest stands. The study area was consisted of two adjacent districts in which two different management practices were implemented. In 1000 m2 circular plots, type of species and diameter at breast height (D.B.H) of all trees larger than 2.5 cm as well as type of species of all shrubs and vertical distribution of tree species were recorded. In addition to richness, evenness and heterogeneity indices were calculated for whole tree and shrub species and also for each tree layer. The results showed that tree species diversity indices were significantly greater in the unmanaged area, whereas richness and heterogeneity indices of shrubs were greater in the managed area. Comparing the biodiversity indices indicated that richness index had the greatest value in the understorey and heterogeneity indices were greatest in the middle storey in both regions. Greater amounts of evenness were detected in the middle- and over storey of unmanaged and managed areas, respectively. As forestry operations result in change in various forest characteristics such as species diversity, it is essential to assess and monitor the effect of logging operations on forest diversity Hyrcanian forests of Iran.
Keywords: Forest stories, heterogeneity indices, Iran, species richness, sustainable management.
INTRODUCTION geomorphological, hydrological, ecological stability in forest ecosystems (Noss 1999). Loss of habitat resulting Sustainable management of forest is one of the recent from human land-use practices is the single largest factor expressions of sustainability in forestry. It adopts an causing the decline of biodiversity (Millennium Ecosystem ecosystem approach to forest management, while operating Assessment 2005; Mönkkönen et al. 2014). Various in an interdisciplinary context (Hahn and Knoke 2010). ecosystem functions might be affected negatively by One of the comprehensive definitions of sustainable forest biodiversity loss, and long term reduction of species management is managing forest stands in such a way that numbers may lead to a decrease of the ecosystem’s ability their productivity, regeneration, vitality and biodiversity is to confront with disturbances (Ishii et al. 2004). As a preserved in accordance with ecological, economic and consequence, any sustainable forest management should be social functions in local, national and global levels, in accordance with environmental policies including currently and in the future (Bernasconi 1996). Nowadays, it biodiversity conservation. is increasingly acknowledged that biodiversity, as a main Biodiversity of forest ecosystems encompasses many aspect of ecosystem structure and functioning as well as a different aspects, such as species diversity, ecosystem key issue of sustainable forest management, needs to be diversity and genetic diversity. Species composition can considered in forest management plans in conjunction with alter ecosystem properties through functional traits and other environmental and economic criteria (Bertomeu and interactions (Hooper et al. 2005; Schmidt et al. 2015). At Romero 2001). Biodiversity has a substantial role in forest the stand level, species diversity is often associated with ecosystems for the preservation of ecosystem functioning stand structural complexity (e.g. vertical and horizontal (Bengtsson et al. 2000). Indeed biologically diverse structure and other spatial components), as an appropriate systems serve a variety of human needs; it provides us with indicator of habitat diversity (Ishii et al. 2004), and has a wealth of products and services. There is concern that the been reported to be a major factor determining forest loss of biodiversity within forests is jeopardizing these vegetation (Cardinale et al. 2012). services (Aerts and Honnay 2011). Forest structure is directly related to the habitat of many It is also related to the delivery of many ecosystems different animal and plant species (Kint 2000) and the services (Balvanera et al. 2006), and results in alterations in forest structure through the intervention of 96 BIODIVERSITAS 16 (1): 95-101, April 2015 man and natural disturbances can affect the conditions Mountain, and extend from the Northwest to the Northeast needed for the survival of many species (Guner 2002). of Iran with a total area of about 1.9 million hectares. Most Moreover, natural and human disturbances influence parts of the forests within this range are managed for different components of biodiversity in many communities timber production as these forests are the only source of by their direct impact on species and stand structural wood production in Iran and the main revenue of forest diversity (Huston 1994; Robert and Gilliam 1995; Lindgren management plans is the income of logging (Forest and and Sullivan 2001). Species diversity as well as its vertical Rangelands Organization of Iran 1997). We hypothesize differentiation within stands may thus be used as indicators that the intensive logging in Hyrcanian forests has of disturbances regime in forest ecosystems (Larsson and considerably decreased the species diversity in managed Danell 2001). stands compared to natural forest relicts. Therefore this Over the last 300 years, the world population has study aims at analyzing tree and shrub species diversity and increased considerably. This rapid development brings comparing vertical species distribution between two increased, widened and varied demands for timber and managed and unmanaged forests using different diversity non-timber products (Baskent 2000). Timber extraction is indices. one of the most important disturbances occurring in forests throughout the world, and there is an increasing debate over the global effect of forest management for timber MATERIALS AND METHODS production on biodiversity (Siitonen 2001). At the local scale, unmanaged forests in general are said to contain Study area more species than managed forests (Okland et al. 2003), This research was conducted in the Kheyrud Forest but the results of some studies failed to confirm this idea Research Station of University of Tehran (KFR), an 8000 for particular taxa (Graae and Heskjaer 1997; Bobiec hectare forest which is a portion of Hyrcanian uneven-aged 1998). Hyrcanian (Caspian) forests located in the north of forest, located approximately 7 km east of Nowshahr (or Iran comprise a narrow band of temperate deciduous Noshahr) (51°32ʹN, 36°27ʹE), Mazandaran Province, forests and are contiguous to a larger forest block within the Elborz mountain range, northern Iran (Figure 1). extending across eastern Turkey and Caucasia. These forests cover the north-facing slopes of the Elborz
A
B C
Figure 1. Study site in the Kheyrud Forest Research Station of University of Tehran (KFR) (C), east of Nowshahr (B), Mazandaran Province, northern Iran (A). NOURI et al. – Woody species diversity considering structure 97
The elevation in the region ranges from 50 to 2200 m s n (n 1) D ( i i ) above sea level, composed of mostly broadleaved species. N(N 1) The climate of the area, according to the Emberge climate i1 system, is wet with cold winters. The mean annual temperature is 15.9ͦC, the highest mean monthly Where n is the number of individuals in the ith species temperature of 29 ͦ C occurs in June and July and the lowest i and N the total number of individuals. When D increases, of 7.1 ͦC in February. The mean annual precipitation is diversity decreases and therefore Simpson’s index is 1354.5 mm, with maximum and minimum amounts in -1 -1 September and June, respectively. KFR is divided into 7 usually expressed as 1.D this expression (i.e. 1.D ) was districts; however, only the first district, Patom, was also used in this study. Two indices of evenness, Smith and surveyed. After field inspection, two adjacent areas Wilson and Simpson’s (E), were used. The Simpson’s characterized by the same soil type, plant community and evenness index (E) is calculated as the ratio of the site quality were selected. The southern area which is a Simpson’s diversity index D to the maximum possible protected forest has never been harvested and characterized index of diversity, given S species and N individuals. as a reference forest for sustainable forest management, Smith and Wilson (1996) proposed an index of whereas in the northern area, logging is performed. evenness based on the variance in abundance of the species. According to Smith and Wilson, this is the best index of evenness because it is independent of species Procedures richness and is sensitive to both rare and common species Using systematic random sampling method, 40 0.1 ha in the community, the index calculated as: circular sampling plots were laid out in each study area. Within each plot, D.B.H of all trees larger than 2.5 cm and the crown cover of all shrubs were recorded. 2 Considering that Hyrcanian forests consist of three s s loge ni loge n j / S stories (understorey, middle storey and overstorey), vertical 2 i1 j1 EVar 1 arctan layers were determined by visual estimation. Slope, altitude S and aspect were measured for each plot using a clinometer, altimeter and compass, respectively.
Data analysis Many different indices have been proposed for the Where, Evar= Smith and Wilson’s index of evenness evaluation of species diversity. During their historical ni= Number of individuals in species i in sample (i = 1, development, the indices have been separated into three 2, ..., s) categories: indices of (i) species richness: the oldest and the nj= Number of individuals in species j in sample (j = 1, simplest understanding of species diversity expressed as a 2, ..., s) number of species in an ecosystem, (ii) species evenness: a S = Number of species in entire sample measure of the equality in species composition in a community, and (iii) species heterogeneity: a characteristic The indices were calculated for tree and shrub species encompassing both species richness and evenness (Ludwig separately, as well as for vertical tree layers within each and Reynolds 1988; Krebs 1989). In this study, species plot. If the number of trees N is used, the size of the tree is richness S is the number of species recorded at each neglected for calculating species diversity indices, while sampled plot (Magurran 1988). For species heterogeneity using the basal area, the tree size is taken into account Shannon (Shannon 1949) and Simpson (Simpson 1949) through its diameter, or more precisely by the square of its diversity indices were used, as these are successful tools for diameter (Merganic and Smelko 2004). The sum of basal the evaluation and quantification of plant diversity (Dale et area of all individuals for each species in sample plots was al. 1994). used instead of species number in calculating evenness and Shannon’s index was calculated as: heterogeneity indices of trees. Ecological Methodology software package was employed for calculating diversity s indices. The normality of calculated indices for shrub and H ( pi )(log2 pi ) tree species was examined by using Kolmogorov-Smirnov i1 test. Since some geomorphological features like elevation, aspect and slope were different between the two studied Where pi is the relative abundance of species i. areas and might influence the diversity indices, these features were considered as covariates and an Analysis of Covariance (ANCOVA) was applied for removing their Simpson’s index (D), a diversity index heavily effects and then comparing indices between logged and weighted towards the most abundant species in the sample unlogged areas and also among vertical layers. Significant while being less sensitive to species richness, was differences among treatment averages for different calculated as: parameters were tested at p ≤ 0.05. 98 BIODIVERSITAS 16 (1): 95-101, April 2015
RESULTS AND DISCUSSION Evenness indices Both evenness indices showed significant differences There were only a few shrub species and 15 tree species between the areas, with higher values for unlogged area. in this study area. Among the species, four tree species and Evenness indices calculated for the overstorey were higher one shrub species were only found in the unlogged area. in unlogged area (Table 4), but these differences were not Carpinus betulus L., Diospyros lotus L., Parrotia persica significant. In the middle- and the understorey, evenness (Dc.) C.A.M., Acer velutinum Boiss., Fagus orientalis indices were significantly higher in the logged area (Table Lipsky, Quercus castaneifolia C.A.M., Acer cappadocicum 4). Highest values in the logged region were observed in Gled., Alnus subcordata C.A.M., Ulmus glabra Huds., the middle storey (p < 0.05), but in unlogged area evenness Cerasus avium (L). Moench, Rhamnus frangula and Tilia values were the highest in the overstorey (p < 0.05). begonifolia Stev., Ulmus carpinifolia Borkh., Ficus carica L., and Sorbus torminalis (L.) Crantz were only recorded in Table 2. Stem density of observed shrub species in the managed the unlogged area. Tree species, stem density and basal and unmanaged areas. area were common species in both areas, whereas of all tree species in both areas are presented in Table 1. Shrub species Stem density (per ha) Crataegus microphylla C. Koch and Mespilus germanica Managed Unmanaged L. were common shrub species in both forest sand Prunus area area divaricata Ledeb was only observed in the logged area Crataegus monophylla 145 8 (Table 2). Mespilus germanica 57 6 Comparison of indices between two areas and among Prunus divaricata 3 - tree layers using ANCOVA showed that diversity indices were not significantly influenced by geomorphological features. The p-values related to covariates in all tests Table 3. Mean values ± standard error of richness index and result of statistical tests in both study areas were 0.05 . Since community, climatic and edaphic conditions were similar in two regions and Unlogged Logged area p-value geomorphological characteristics did not show significant area influence on diversity indices, it seems the difference Total tree species 3.923 ± 1.156 1.156 ± 0.925 0.000 between diversity indices of two areas were the output of Overstorey 0.911 ± 2.100 1.196 ±2.575 0.077 management practices. Middle storey 0.811 ± 2.020 1.500±3.575 0.000 Understorey 0.811 ± 2.600 1.500 ± 3.950 0.000 Tree species diversity indices Species richness The comparison between both study areas showed that Table 6. Mean values of diversity indices of shrubs species richness of trees was significantly higher in Managed Unmanaged unlogged area (Table 3). Species richness values calculated Diversity indices for vertical layers were also greater in unlogged area, but area area the difference was only significant in the middle- and Richness S 2.143 1.307 Evenness Simpson 0.771 0.799 understorey (Table 3). Species richness indicated Smith and Wilson 0.689 0.708 significant difference among layers, and the highest species Hetero- Simpson 0.408 0.332 richness was found in the understorey in both areas (p < geneity Shannon 0.911 0.705 0.05).
Table 1. Stem density and basal area of observed tree species in the managed and unmanaged areas.
Managed area Unmanaged area Tree species Stem density (per ha) Basal area (m2.ha -1) Stem density (per ha) Basal area (m2.ha -1) Carpinus betulus 167 26.23 153 11.29 Diospyros lotus 51 0.50 51 0.72 Parrotia persica 42 2.30 490 11.30 Acer velutinum 14 2.04 3 2.50 Fagus orientalis 8 0.94 7 0.90 Quercus castaneifolia 4 1.86 57 6.62 Acer cappadocicum 4 0.45 29 1.79 Alnus subcordata 3 0.28 1 <0.01 Ulmus glabra 3 <0.01 5 0.11 Rhamnus frangula 1 <0.01 1 <0.01 Tilia begonifolia 1 <0.01 17 1.26 Prunus avium - - 4 0.13 Ulmus carpinifolia - - 1 <0.01 Ficus carica - - 1 <0.01 Sorbus torminalis - - 1 <0.01 NOURI et al. – Woody species diversity considering structure 99
Table 4. Mean values ± standard error of evenness indices and result of statistical tests in both study areas
Managed area Unmanaged area p-value Smith and Smith and Smith and Simpson Simpson Simpson Wilson Wilson Wilson Total tree species 0.438 ± 0.162 0.228 ± 0.215 0.501 ± 0.098 0.236 ± 0.168 0.020 0.000 Overstorey 0.141±0.650 0.538 ± 0.230 0.687 ± 0.141 0.633 ± 0.202 0.147 0.096 Middle storey 0.721 ± 0.164 2.568 ± 0.980 0.167 ± 0.611 0.488± 1.919 0.006 0.007 Understorey 0.175 ± 0.533 0.262 ± 0.350 0.179± 0.424 0.230 ± 0.264 0.004 0.093
Table 5. Mean values ± standard error of heterogeneity indices and result of statistical tests in both study areas
Managed area Unmanaged area p-value Simpson Shannon Simpson Shannon Simpson Shannon Total tree species 0.338 ± 0.186 0.842 ± 0.446 0.628 ± 0.104 1.727 ± 0.406 0.000 0.000 Overstorey 0.181 ± 0.331 0.422 ± 0.809 0.196 ± 0.450 0.528 ± 1.143 0.021 0.010 Middle storey 0.387 ± 0.151 0.899 ± 0.348 0.173 ± 0.482 0.523 ±1.263 0.023 0.003 Understorey 0.174 ± 0.284 0.705 ± 0.390 0.178 ± 0.298 0.441 ± 0.804 0.748 0.331
Shannon’s diversity index decreases species diversity; independent of how many The Shannon diversity index for all tree species was years ago clear cutting or selective cutting were done. significantly higher in unlogged area (Table 5). The same is Forest utilization by logging may result in better conditions observed for tree layers, but the difference was not for invasive species (Drake et al. 1989) and poses a threat significant in understorey (Table 5). Regarding to vertical to biodiversity by possibly displacing native plants or structure, this index had the highest value for middle reducing their diversity. Even though logging might reduce storey, but the difference was only significant difference competition, it increases light by creating gaps in canopy between layers in unlogged area (p < 0.05). and increases the chance of soil contact for incoming propagates (Robert and Dong 1993), in long term managed Simpson’s diversity index forests do not retrieve their primary tree species diversity. The Simpson diversity index for tree species showed Other studies showed a positive effect of management on significant differences between both areas with higher the total species richness of vascular plants (Schmidt diversity value for unlogged area (Table 5). The same holds 2005), which could be a specific response to the for all tree layers, but only in the upper and middle storey disturbance that causes an increment in species diversity. In the differences were significant (Table 5). Regarding to fact, the increase in diversity in some harvested forests has vertical structure, this index had the highest value in middle been related to a short-term response of the system to storey but only in the unlogged area a significant difference disturbance (Pitkanen 2000; Peltzer et al. 2000; Roberts was found between layers (p < 0.05). and Zhu 2002). Some studies showed that in the first 20 years of management practices, species richness was higher Shrub diversity indices in managed than to unmanaged forests; after the 20-year Since shrub species were recorded in 35 sample plots in cutoff, higher species richness is observed in unmanaged logged area and only in 3 sample plots in unlogged area, forests (Paillet et al. 2010). the difference of diversity indices of shrub species between Regarding to tree structural diversity, the results also two areas were obvious. As presented in Table 6, in indicated that all diversity indices in the overstorey were contrary to tree species, richness and heterogeneity greater in unlogged area, whereas in the middle- and (Simpson and Shannon) indices of shrubs were greater in understorey only species richness and heterogeneity were the logged area but evenness indices values were greater in higher in the unlogged area, but evenness values were unlogged area. greater in the logged area. In most sample plots in unlogged area the middle storey consisted of semi shade Discussion tolerant species such as Carpinus betulus and Parrotia Considering overall tree species diversity indices, all persica, which hindered presence of other species and species richness, evenness and heterogeneity indices resulted in uneven distribution of species in these layers. In showed significant differences between unlogged and analyzing tree structural diversity it was observed that logged areas with greater values for unlogged area. This species richness decreased from understorey to overstorey difference is most probably related to management in the unlogged area. It seems in parallel with tree differences between both regions and selective logging. individual’s diameter and height increment and transition These findings are in accordance with Brown and to higher layers, some species were outcompeted because Gurevitch (2004) who reported that logging operation of competition for ecological conditions like light, moisture, nutrients, etc. In contrary, the trend of species 100 BIODIVERSITAS 16 (1): 95-101, April 2015 richness changes was different in the managed area; it effect of management programs like logging operations on decreased from understorey to middle storey and then forest diversity is essential. increased to overstorey, in other words this index had its highest value in the top layer. 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Ludwig JA, Reynolds JF. 1988. Statistical ecology: A Primer on Methods Pitkanen S. 2000. Classification of vegetation diversity in managed boreal and Computing. John Wiley & Sons, New York. forests in eastern Finland. Plant Ecol 146: 11-28. Magurran AE. 1988. Ecological Diversity and its Measurement. Princeton Ratcliffe S, Holzwarth F, Nadrowski K, Levick S, Wirth C. 2015. Tree University Press, New Jersey. neighborhood matters - Tree species composition drives diversity- Merganic J, Smelko S. 2004. Quantification of tree species diversity in productivity patterns in a near-natural beech forest, For Ecol Manag forest stands - model BIODIVERSS. Eur J For Res 123: 157-165. 335: 225-234. Millennium Ecosystem Assessment. 2005. Ecosystems and Human Well- Roberts MR, Gilliam FS. 1995. Patterns and mechanisms of plant being: Biodiversity Synthesis. World Resources Institute, diversity in forested ecosystems: implications for forest management. Washington, DC. Ecol Appl 5: 969-977. Mönkkönen M, Juutinen A, Mazziotta A, Miettinen K, Podkopaev D, Roberts MR, Zhu L. 2002. Early response of the herbaceous layer to Reunanen P, Salminen H, Tikkanen O. 2014. Spatially dynamic forest harvesting in a mixed coniferous-deciduous forest in New Brunswick, management to sustain biodiversity and economic returns, J Environ Canada. For Ecol Manag 155: 17-31. Manag 134: 80-89. Schmidt M, Veldkamp E, Corre MD. 2015. Tree species diversity effects Noss RF. 1999. Assessing and monitoring forest biodiversity: A suggested on productivity, soil nutrient availability and nutrient response framework and indicators. For Ecol Manag 115: 135-146. efficiency in a temperate deciduous forest. For Ecol Manag 338: 114- Okland T, Rydgren K, Okland R, Storaunet HKO, Rolstad J. 2003. 123. Variation in environmental conditions, understorey species number, Schmidt W. 2005. Herb layer species as indicators of biodiversity of abundance and composition among natural and managed Picea-Abies Managed and unmanaged beech forests. For Snow Landsc Res 79: forest stands. For Ecol Manag 177: 17-37. 111-125. Paillet Y, Bergès L, Hjältén J, Ódor P, Avon C, Bernhardt-Römermann M, Shannon CE. 1949. The mathematical theory of communication. In: Bijlsma RJ, De Bruyn L, Fuhr M, Grandin U, Kanka R, Lundin L, Shannon CE, Weaver W (eds). The Mathematical Theory of Luque S, Magura T, Matesanz S, Mészáros I, Sebastià MT, Schmidt Communication. University of Illinois Press, Urbana, IL. W, Standovár T, Tóthmérész B, Uotila A, Valladares F, Vellak K, Siitonen J. 2001. Forest management, coarse woody debris and saproxylic Virtanen R. 2010. Biodiversity differences between managed and organisms: Fennoscandian boreal forests as an example. Ecol Bull 49: unmanaged forests: meta-analysis of species richness in Europe. 11-41. Conserv Biol 24 (1): 101-112. Simpson EH. 1949. Measurement of diversity. Nature 163: 688-688. Peltzer DA, Bast ML, Wilson SD, Gerry AK. 2000. Plant diversity and tree responses following contrasting disturbances in boreal forest. For Ecol Manag 127: 191-203. BIODIVERSITAS ISSN: 1412-033X Volume 16, Number 1, April 2015 E-ISSN: 2085-4722 Pages: 102-107 DOI: 10.13057/biodiv/d160114
Nest temperatures of the Piai and Sayang Islands green turtle (Chelonia mydas) rookeries, Raja Ampat Papua, Indonesia: Implications for hatchling sex ratios
RICARDO F. TAPILATU1,2,♥, FERDIEL BALLAMU3 1Marine Science Laboratory and Department, University of Papua (UNIPA). Marine and Fisheries Hall Room Ikn-4, Jl. Gunung Salju, Amban, Manokwari 98314, Papua Barat, Indonesia. Tel./Fax.: +62-986-212156/211455, ♥email: [email protected] 2Pacific Marine Resources Research Center, University of Papua (UNIPA). Manokwari 98314, Papua Barat, Indonesia 3Papua Sea Turtle Foundation, Sorong 98413, Papua Barat, Indonesia
Manuscript received: 25 January 2015. Revision accepted: 31 March 2015.
Abstract. Tapilatu RF, Ballamu F. 2015. Nest temperatures of the Piai and Sayang Islands green turtle (Chelonia mydas) rookeries, Raja Ampat Papua, Indonesia: Implications for hatchling sex ratios. Biodiversitas 16: 102-107. Sex determination and hatching success in sea turtles is temperature dependent. Warmer sand temperatures may skew sea turtle population sex ratios towards predominantly females and high sand temperatures may also decrease hatching success. Therefore, understanding nest temperatures is important for conservation programs, including the evaluation of the potential impact of global climate change. Nest temperatures were monitored during the 2013 nesting season of the green sea turtle, Chelonia mydas, at Piai and Sayang Islands, Raja Ampat, West Papua, Indonesia. Nest temperatures increased from 29oC early in the incubation to 34-36oC in the middle, before decreasing again. Monitored nest temperatures were similar across all beaches. Nest temperatures increased 2-4oC during the middle third of incubation due to metabolic heating. Hatchling sex ratio inferred from nest temperature profiles indicated a strong female bias. This finding is consistent with the relatively warm thermal profiles of the majority of the nesting beaches. This also included some extremely warm nest temperatures that were associated with lower hatching success. Information from this study provides a foundation for developing conservation strategies for enhancing hatchling production with optimal sex ratios at the most important nesting beaches for the western Pacific green sea turtle. This study is the first comprehensive assessment of sex ratios for green sea turtles in Raja Ampat and represents the initiation of a long- term database that can be used at a local level to develop strategies that could potentially offset the impact of long-term climate change on the western Pacific green sea turtle.
Keywords: Chelonia mydas, hatching success, Piai, Sayang, sex determination.
INTRODUCTION of protein for local villagers. Further, the expansion of the Balinese turtle fishery towards eastern Indonesia in the mid Sea turtle populations, globally, are experiencing 1970s caused the depletion of populations in Green turtle dramatic population decline. This is due, primarily, to rookeries in Sulawesi, Maluku and Irian Jaya (Polunin and nesting habitat destruction and disturbance, the incidence Nuitja 1982). Hunting for subsistence and poaching for of commercial fishing by-catch, hunting, shell marketing commercial benefit are most likely to occur during the and raiding of nests by villagers in subsistence economies. nesting season abundance. Reviews of the status of sea turtle populations in Southeast Like all sea turtles, the green turtle possesses Asia by Limpus (1994; 1997) determined that all marine temperature-dependent sex determination (TSD). turtle populations in the Indo Pacific region, outside Incubation temperature determines the sex of hatchling sea Australia, are severely depleted through overharvesting and turtles during the middle third of embryonic development, excessive incidental mortality. Limpus (1997) further with low temperatures producing males, and high estimated that the rate of turtle harvest exceeds the temperatures producing females (Yntema and Mrosovsky replacement capacity of existing populations in the entire 1982). Because the environmental conditions at the nest Pacific region. Raja Ampat is a unique site, located on the site are a major determinant of nest temperature, it may be northwestern side of West Papua province, Indonesia. The expected that females choose their nest site carefully. archipelago contains a full range of marine and coastal However, even within a rookery there must be some habitats that are important for the breeding, foraging and variation in nest temperature in order to maintain migration of several species of sea turtles. Similar to other phenotypic diversity. As such, it is of interest to evaluate areas in the Indo Pacific region, the commercial harvest is naturally occurring sex ratios in green turtle populations. In identified as one of the major threats to turtle populations this study, nest temperature profiles were reported from in Raja Ampat. Exploitation of sea turtles for both green turtle rookeries on Piai and Sayang Islands of Raja subsistence and commercial purposes is a long-standing Ampat. Nest temperature profiles were also used to predict practice in Raja Ampat. Sea turtles have long been a source the sex ratio of turtles emerging from nests. Documenting TAPILATU & BALLAMU – Nest temperature of green turtle 103 variation in nest temperatures within a rookery is the first Sayang island is the largest island with approximately 9km step toward a detailed understanding of how incubation of beaches, which are fragmented by karsts. A large temperature influences sea turtle populations. The results number of nests were found on the western beach. Piai provide insight on spatial and temporal dynamics of nest island, which is much smaller than Pulau Sayang, is also an temperatures and predicted hatchlings sex ratios produced important rookery for Green turtles. Sandy beaches, with on the primary nesting beaches for the western Pacific an approximate length of 3km, are situated on the northern green turtles at Raja Ampat. These data provide an initial and southern parts of the island. Nest temperatures below step in establishing a long-term database of hatchling sex the surface were monitored every hour at two sites on Piai ratios for assessing the ecological and conservation and Sayang islands at two different beach zones, open area implications of TSD in this population, including the and under vegetation with temperature data loggers from potential impact of global climate change. This type of January to April 2013. In general, the topography of the information can prove valuable when attempting to beaches includes an intertidal zone, then a gently sloping understand the reproductive ecology of sea turtles and zone, followed by a vegetative zone. Most of the nesting when developing conservation strategies for enhancing the typically occurs well above the high tide line on the gently recovery of threatened and endangered populations (Coyne sloping zone of the beach. Due to logistical difficulties et al. 2007; Wibbels 2007). related to placing and retrieving data loggers, they were used primarily during the main nesting season (i.e. the austral summer, January to April). A type of temperature MATERIALS AND METHODS data loggers (HOBO Pendants, Onset Computer Corporation, Pocassete, MA) was used to record sand and This study took place on Piai and Sayang Islands nest temperatures. The datalogger accurately records (Figure 1) of Raja Ampat, West Papua, Indonesia during temperatures to approximately ± 0.3-0.4°C. the 2013 green turtle (Chelonia mydas) nesting season.
Figure 1. Map of study area in the Piai and Sayang Islands, Raja Ampat, West Papua, Indonesia
104 BIODIVERSITAS 16 (1): 102-107, April 2015
A B
Figure 2. Nest temperature traces. A. Nests constructed in the open beach section. B. Nests constructed close and or under vegetation zones
predicted from incubation temperature, knowing that incubation at a constant temperature of 26oC produces 100% males, incubation at a constant temperature of 29oC produces 100% females, and assuming a linear transition from all males to all females within this temperature range (Booth and Astill 2001; Miller and Limpus 1981). Further, to evaluate the effect of nest temperature on hatchling sex ratio accurately, the mean nest temperature during the middle third of incubation was calculated for each nest. The middle third of development for each nest was estimated from the model of embryonic growth to determine the TSP duration. Hatchling sex ratio was estimated by the mean temperature, weighted by embryonic Figure 3. Nests temperatures (Mean±SE) during middle third of growth, during the middle third of development for each development in nests that were monitored with dataloggers at nest. The mean nest temperature during the middle third in open and vegetation zones at Piai and Sayang Islands each nest was compared to available pivotal temperature
for western Pacific green turtle population. Previous studies
indicate that mean nest temperature during the middle third
Nesting females were located during the night and the of incubation represents an accurate method for predicting nests were excavated after nesting had finished. Eggs were sex ratio in nest that do not experience large daily removed and counted and a temperature data logger was fluctuations in temperature (Georges et al. 2004; Georges positioned in the centre of the egg mass during egg et al. 1994). No direct validation of the sex predictions at replacement. The nest was reburied and the eggs incubated this reporting period was made because this would have naturally without further interference. Temperature data involved sacrificing the hatchlings for dissection to loggers were used to record incubation temperatures during determine their sex. incubation period of in situ nests. Three nests and four nests were opportunistically selected from open beach zones and under/close to vegetation zones respectively for RESULTS AND DISCUSSION data logger placement. Nests were excavated after hatching when hatchlings hatched from eggs and dug upwards to Results retrieve the data logger. The data loggers were The profiles of nest temperatures could be divided into programmed in the laboratory to record temperature every three distinct phases: early, heating, and cooling (Figure 2). hour. The hour measurements were averaged over 24 h to During the January-April period, nest temperatures at nests obtain a single daily temperature. laid both open and vegetation zones are likely to track the Nest temperature traces from the time of oviposition to sand temperature at 60 cm for the early portion of o the time of emergence were used to model the thermal incubation and then increased to be 2-4 C above sand reaction norm of embryonic development using the R temperature at middle portion (Figure 2A-B). The climb in package, embryo growth (5.2, http://cran.r-project.org) nest temperatures was relatively smooth with temperature o (Girondot and Kaska 2014). Hatchling sex ratios were fluctuations within any given week being less than 0.9 C.
TAPILATU & BALLAMU – Nest temperature of green turtle 105
Fluctuations in nest temperatures over a period of a few temperatures for green turtles have been estimated to days probably due to rainfall events. Nest temperature cluster at 28oC in Costa Rica (Morreale et al. 1982) and at increased slightly so that at the time of middle incubation 29oC in Mediterranean (Kaska et al. 1998). The simple period, nest temperatures were 2-4oC distinctively warmer method predicted that all successfully monitored nests than sand temperature. An increase in nest temperature during the January-April 2013 period should produce above surrounding sand temperature during middle portion female hatchlings, even in a nest (YPP-20) that initiated of incubation is commonly reported in sea turtle nests incubation temperature at 27oC. The overall prediction (Bustard 1972; Booth and Astill 2001; Broderick et al. from monitored nests was an extreme female bias. In 2001; Godley et al. 2002), and is caused by the metabolic addition, all nests monitored with dataloggers, mean heat produced by developing embryos which increases temperatures were above the pivotal temperature (Figure 3) greatly during the final stages of incubation. suggesting female biased sex ratios. Thus, collectively The patterns of nest temperature profiles early nesting these results support the hypothesis that female-biased season 2013 were consistent across two monitoring zones. hatchling sex ratios may predominate on the green turtles Nest temperatures for nests laid at open beach zones are nesting beaches of Piai and Sayang Islands. This female relatively similar with zones close to vegetation with the biased hatching ratio is similar with reports of green turtle exception of Nest with YPP-09 datalogger. During the nests on Heron Island (Limpus et al. 1983; Booth and Astill early phase, nest temperatures of this nest tracked the beach 2001), but the bias found in this current study is more temperatures at 27oC while majority of nests initiated at extreme than reported in Heron Island. This difference 29oC. Furthermore, mean nest temperatures recorded in the might be attributed to a warmer than average nesting current study were typically above the pivotal temperature season in 2002-2003on Heron island. There is a trend for a (PT, Figure 3) that had been reported for green turtles in female hatchling bias from sea turtle rookeries worldwide Costa Rica, 28oC (Morreale et al. 1982), in Mediteranean, (Spotila et al. 1987; Mrosovsky 1994; Broderick et al. 29oC (Kaska et al. 1998), and tend to cluster at 29oC 2001; Godley et al. 2001, 2002). The evolutionary (Mrosovsky 1988) in all sea turtles. reason(s) for the apparent strong female hatchling bias in An extreme female-biased sex ratio was predicted by most sea turtle rookeries remain unexplained (Mrosovsky the mean temperature during the middle third of 1994). development regardless of whether temperatures were In an evolutionary context, a female visiting a particular weighted by embryonic growth or time. However, the mean rookery has the potential to influence the sex ratio of her temperature of nests during the TSP weighted by offspring by varying her nest timing, nesting beach and embryonic growth was higher ( = 32.14°C±0.69) than nest depth. Given the importance of nest temperature in when weighted by time ( = 31.71°C±0.59). In addition, a determining hatchling attributes, a prediction might be that female-biased sex ratio was also predicted for all but one once ashore females use cues to choose nest sites of nest when TSP length in this study was compared to TSP optimal thermal characteristics. Studies investigating the length where hatchling sex ratios were known (Miller and role of thermal cues in nest site choice have not been done Limpus 1981). It is possible that a few intersex individuals for green turtles from Piai and Sayang, but green turtles may have been produced in these nests (Miller and Limpus nesting at Tortugero, Costa Rica do not actively select nest 1981); however, the overall sex ratio would remain sites based on temperature (Bjorndal and Bolten 1992). strongly female biased. Global climate change (IPCC 2013) could have a significant impact on reptiles with TSD (Janzen 1994; Mitchell and Janzen 2010) including sea turtles (Hawkes et al. 2007; Chaloupka et al. 2008; Poloczanska et al. 2009; Discussion Fuentes et al. 2009, 2010; Hays et al. 2010; Witt et al. It has been suggested that numerous factors affect nest 2010; Patino-Martinez et al. 2012). It has been suggested temperatures (Binckley et al. 1998). These vary from large that increases in sand temperature associated with climate scale annual and seasonal differences in climate (patterns change will affect both leatherback sex ratios (Binckley et of precipitation and air temperature) during nesting seasons al. 1998; Hulin et al. 2009; Patino-Martinez et al. 2012) to mesoscale factors such as nest placement on a beach and hatchling fitness (Mickelson and Downie 2010). These (sun versus shade, distance to high tide) or sand color changes are predicted to increase the proportion of female (black versus white) down to factors at the individual nest leatherback hatchlings and reduce hatching success and such as depth, egg position (bottom versus top) and fitness primarily at sites already experiencing biases toward metabolic heat generated by developing embryos (Godfrey female-producing temperatures (Binckley et al. 1998; et al. 1997; Binckley et al. 1998; Mickelson and Downie Mickelson and Downie 2010; Patino-Martinez et al. 2012). 2010). On Piai and Sayang islands, nest temperatures may indicate Sexual differentiation in sea turtles is strongly the production of a range of sex ratios but with an overall influenced by ambient incubation temperature or TSD female bias. This could potentially pose a problem if future (Standora and Spotila 1985; Mrosovsky 1994). temperatures increase due to global climate change. Specifically, the sustained temperature to which the Considering that green sea turtles on these islands are embryo is exposed during the middle trimester of already producing a female biased hatchling sex ratio and incubation determines the eventual gonadal differentiation that some nest temperatures reach as high as 35oC, the and sex of the hatchling (Wibbels 2003). The pivotal temperature may vary with species and locale. The pivotal
106 BIODIVERSITAS 16 (1): 102-107, April 2015 projected increases (IPCC 2013) could result in extreme Dr. Mark Erdmann who provided advices in obtaining female biases and potentially impact hatching success. WFF grant. This initial study suggested that the potential of hatchling sex ratio produced on Piai and Sayang is female- biased and the finding adds to the general paradigm REFERENCES emerging for sea turtles that female biases are prevalent (Mrosovsky 1994; Wibbels 2003). There are several Binckley CA, Spotila JR, Wilson KS, Paladino FV. 1998. Sex implications for the conservation of the western Pacific sea determination and sex ratios of Pacific leatherback turtles, Dermochelys coriacea. Copeia 2: 291-300. turtle population at Bird’s Head since this population has Bjorndal KA, Bolten AB. 1992. Spatial distribution of green turtle significantly declined due to over-harvesting (Hitipeuw (Chelonia mydas) nests at Tortuguero, Costa Rica. Copeia 1: 45-53. 2003). It is plausible that possessing TSD and producing Booth DT, Astill K. 2001. Incubation temperature, energy expenditure and female-biased sex ratios from Piai and Sayang islands hatchling size in the green turtle (Chelonia mydas), a species with temperature-sensitive sex determination. Australian J Zool 49: 389- could be advantageous to the recovery of the Raja Ampat 396. green sea turtle population. It has been proposed that biased Broderick AC, Godley BJ, Hays GC. 2001. Metabolic heating and the sex ratios could significantly impact the recovery of sea prediction of sex ratios for green turtles (Chelonia mydas). Physiol turtle populations in both positive and negative ways (Vogt Biochem Zool 74: 161-170. Bustard R. 1972. Sea turtles: natural history and conservation. Collins, 1994; Mrosovsky and Godfrey 1995; Wibbels 2003; Coyne London. et al. 2007; Wibbels 2007). Coyne (2007) provides a model Chaloupka M, Kamezaki N, Limpus C. 2008. Is climate change affecting showing that female-biased sex ratios could potentially the population dynamics of the endangered Pacific loggerhead sea increase recovery rates, since increasing the number of turtle? J Exp Mar Biol Ecol 356: 136-143. Chan EH, Liew HC. 1991. Sea turtles. In: Kiew R (ed). The State of females will increase the egg (and therefore juvenile) Nature. Conservation in Malaysia. Malayan Nature Society, KL. production in future years. As an example, the recovery Coyne M, Landry Jr AM, Plotkin PT. 2007. Population sex ratios, and its rate of the Kemp’s ridley turtle may have been accelerated impact on population models. Biology and conservation of Ridley sea by the artificial skewing of sex ratios (Wibbels 2007). turtles. Johns Hopkins University Press, Baltimore, MD. Fuentes M, Limpus CJ, Hamann M. 2010. Vulnerability of sea turtle However, these projections are based upon the assumption nesting grounds to climate change. Global Change Biol 17: 140-153. that lack of males does not become a limiting factor as the Fuentes M, Maynard JA, Guinea M, Bell IP, Werdell PJ, Hamann M. proportion of females increases. 2009. Proxy indicators of sand temperature help project impacts of The concept of manipulating sex ratios has drawn some global warming on sea turtles in northern Australian Endang Sp Res 9: 33-40. controversies (Vogt 1994; Mrosovsky and Godfrey 1995). Georges A, Doody S, Beggs K, Young J. 2004. Thermal models of TSD In particular the impact of biased sex ratios on the under laboratory and field conditions. Temperature-dependent sex reproductive ecology of sea turtles is not well understood determination in vertebrates. Smithsonian Books, Washington, DC. and it is plausible that extreme biases could have a negative Georges A, Limpus C, Stoutjesdijk R. 1994. Hatchling sex in the marine turtle Caretta caretta is determined by proportion of development at a impact (Mrosovsky and Godfrey 1995). Extreme biases temperature, not daily duration of exposure. J Exp Zool 270: 432-444. could potentially affect reproduction in regards to fertility, Girondot M, Kaska Y. 2014. A model to predict the thermal reaction norm probability of nesting, and multiple paternities (Wood and for the embryo growth rate from field data. J Thermal Biol 45: 96- Wood 1980; Harry and Briscoe 1988; Chan and Liew 102. Godfrey MH, Barreto R, Mrosovsky N. 1997. Metabolically-generated 1991). It is plausible that an extreme female bias could lead heat of developing eggs and its potential effect on sex ratio of sea to the Allee effect due to reduction in number of males. For turtle hatchlings. J Herpetol 31 (4): 616-619. example, it has been suggested that low hatch rates of Godley BJ, Broderick AC, Glen F, Hays GC. 2002. Temperature- leatherback in Malaysia could have related to insufficient dependent sex determination of Ascension Island green turtles. Mar Ecol Prog Ser 226: 115-124. number of males to fertilize clutches (Chan and Liew Godley BJ, Broderick AC, Mrosovsky N. 2001. Estimating hatchling sex 1991). However, it has been suggested that the Allee effect ratios of loggerhead turtles in Cyprus from incubation durations. Mar may not impede the recovery of relatively small population Ecol Prog Ser 210: 195-201. of sea turtles (Hays 2004). Harry JL, Briscoe DA. 1988. Multiple paternity in the loggerhead turtle (Caretta caretta). J Heredity 79: 96-99. Hawkes LA, Broderick AC, Godfrey MH, Godley BJ. 2007. Investigating the potential impacts of climate change on a marine turtle population. ACKNOWLEDGEMENTS Global Change Biol 13: 923-932. Hays GC. 2004. Good news for sea turtles. Trends Ecol Evol 19: 349-351. Hays GC, Fossette S, Katselidis KA, Schofield G, Gravenor MB. 2010. Our sincere thanks and appreciation are to sea turtle Breeding periodicity for male sea turtles, operational sex ratios, and patrollers from villages of Salio and Selpele of Waigeo implications in the face of climate change. Conserv Biol 24: 1636- Sub-District who assisted in the experiment and gave 1643. access to use dataloggers in nests of green for this study at Hitipeuw C. 2003. Status of Sea Turtle Populations in the Raja Ampat Islands. Report on a rapid ecological assessment of the Raja Ampat Piai and Sayang Islands. Taylor Roberge and Dr. Thane Islands, Papua, Eastern Indonesia held October 30-November 22, Wibbels of Biology Department University of Alabama at 2002. Birmingham (UAB)-USA assisted in data analysis and Hulin V, Delmas V, Girondot M, Godfrey MH, Guillon JM. 2009. Petrus Dimara of University of Papua (UNIPA) assisted Temperature-dependent sex determination and global change: are some species at greater risk? Oecologia 160: 493-506. with graphic. We also thank the anonymous reviewers for IPCC. 2013. Intergovernmental Panel for Climate Change: Climate their insightful comments. Laure Katz and Debbie Jacobs Change 2013: The physical Science Basis. Summary for of Conservation International Indonesia Program who Policymakers. Cambridge University Press, Cambridge. solicited the Walton Family Fund (WFF) grant application, Janzen FJ. 1994. Climate change and temperature-dependent sex determination in reptiles. Proc Natl Acad Sci USA 91: 7487-7490.
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Kaska Y, Downie R, Tippett R, Furness RW. 1998. Natural temperature Patino-Martinez J, Marco A, Quiñones L, Hawkes L. 2012. A potential regimes for loggerhead and green turtle nests in the eastern tool to mitigate the impacts of climate change to the caribbean Mediterranean. Canadian Journal of Zoology 76: 723-729. leatherback sea turtle. Global Change Biol 18 (2): 401-411. Limpus CJ. 1994. Current declines in South East Asian turtle populations, Poloczanska ES, Limpus CJ, Hays GC. 2009. Chapter 2 Vulnerability of In Proceedings of the 13th Annual Symposium on Sea Turtle Biology Marine Turtles to Climate Change, In: David WS (ed.). Advances in and Conservation. pp. 89-91. NOAA Technical Memorandum NMFS Marine Biology. Academic Press, London. SEFSC-341, USA. Polunin NVC, Nuitja NS. 1982. Sea turtle populations of Indonesia and Limpus CJ. 1997. Marine turtle populations of Southeast Asia and the Thailand. In: Bjorndal KA (ed.). Biology and Conservation of Sea western Pacific Region: distribution and status. Wetlands Turtles.. Smithsonian Institution Press, Washington, D.C. International - Indonesia Program, Indonesia. Spotila JR, Standora EA, Morreale SJ, Ruiz GJ. 1987. Temperature Limpus CJ, Parmenter CJ, Baker V, Fleay A. 1983. The Crab Island sea dependent sex determination in the green turtle (Chelonia mydas): turtle rookery in the north-eastern Gulf of Carpentaria. Wildlife Res effects on the sex ratio on a natural nesting beach. Herpetologica 43: 10: 173-184. 74-81. Mickelson LE, Downie JR. 2010. Influence of incubation temperature on Standora EA, Spotila JR. 1985. Temperature dependent sex determination morphology and locomotion performance of Leatherback in sea turtles. Copeia 3: 711-722. (Dermochelys coriacea) hatchlings. Canadian J Zool 88: 359-368. Vogt RC. 1994. Temperature controlled sex determination as a tool for Miller JD, Limpus CJ. 1981. Incubation period and sexual differentiation turtle conservation. Chelonian Conserv Biol 1: 159-162. in the green turtle Chelonia mydas L, In Melbourne Herpetological Wibbels T. 2003. Critical approaches to sex determination in sea turtles. Symposium. Zoological Board of Victoria, Parkville, Victoria, Biol Sea Turtles 2: 103-134. Australia. Wibbels T. 2007. Sex determination and sex ratios in Ridley Turtles. In Mitchell NJ, Janzen FJ. 2010. Temperature-dependent sex determination Plotkin P. (ed.). Biology and Conservation of Ridley Sea Turtles. and contemporary climate change. Sexual Dev 4: 129-140. Johns Hopkins University Press, Baltimore, MD. Morreale SJ, Ruiz GJ, Spotila JR, Standora EA. 1982. Temperature- Witt MJ, Hawkes LA, Godfrey MH, Godley BJ, Broderick AC. 2010. dependent sex determination: current practices threaten conservation Predicting the impacts of climate change on a globally distributed of sea turtles. Science 216: 1245-1247. species: the case of the loggerhead turtle. J Exp Biol 213: 901-911. Mrosovsky N. 1988. Pivotal temperatures for loggerhead turtles (Caretta Wood JR, Wood FE. 1980. Reproductive biology of captive green sea caretta) from northern and southern nesting beaches. Canadian J Zool turtles Chelonia mydas. American Zoologist 20: 499-505. 66: 661-669. Yntema CL, Mrosovsky N. 1982. Critical periods and pivotal Mrosovsky N. 1994. Sex ratios of sea turtles. J Exp Zool 270: 16-27. temperatures for sexual differentiation in loggerhead sea turtles. Mrosovsky N, Godfrey MH. 1995. Manipulating sex ratios: turtle speed Canadian J Zool 60: 1012-1016. ahead. Chelonian Conserv Biol 1: 238-240.
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Effects of timber harvest on structural diversity and species composition in hardwood 1-9 forests FARZAM TAVANKAR, AMIR ESLAM BONYAD Effect of Alnus subcordata, Acer insigne and Sequoia sempervirens plantations on plant 10-15 diversity in Hyrcanian forest of Iran FATEMEH GHEIBI, MOSLEM AKBARINIA, YAHYA KOOCH Plant species diversity among ecological species groups in the Caspian Sea coastal sand 16-21 dune; Case study: Guilan Province, North of Iran MOKARRAM RAVANBAKHSH, TAYYEBEH AMINI, SAYED MOHSEN NASSAJ HOSSEINI Short Communication: Note on Excoecaria indica (Willd.) Muell.-Arg, (Euphorbiaceae), 22-26 from the Andaman and Nicobar Islands, India; a data deficient species PADISAMY RAGAVAN, K. RAVICHANDRAN, P.M. MOHAN, ALOK SXAENA, R.S. PRASANTH, R.S.C. JAYARAJ, S. SARAVANAN Ferns and fern allies of District Shopian, Kashmir Valley, India 27-43 SHAKOOR A. MIR, ANAND K. MISHRA, SHAUKET AHMAD PALA, ZAFAR A. RESHI, M.P. SHARMA Local knowledge of medicinal plants in sub-ethnic Batak Simalungun of North Sumatra, 44-54 Indonesia MARINA SILALAHI,, JATNA SUPRIATNA, EKO BAROTO WALUJO, NISYAWATI DNA barcoding and phylogenetic reconstruction of shark species landed in Muncar 55-61 fisheries landing site in comparison with Southern Java fishing port PREHADI, ANDRIANUS SEMBIRING, EKA MAYA KURNIASIH,, RAHMAD, DONDY ARAFAT, BEGINER SUBHAN, HAWIS H. MADDUPPA The diversity of non-methanogenic bacteria involved in biogas production from tofu- 62-68 processing wastewater SUNARTO, HANNI TSAAQIFAH, CAHYADI PURWOKO, ARTINI PANGASTUTI Infraspecific morphological and genome size variations in Linum glaucum in Iran 69-78 SEYED MEHDI TALEBI, MASOUD SHEIDAI, MORTEZA ATRI, FARIBA SHARIFNIA, ZAHRA NOORMOHAMMADI Short Communication: Occurrence of leaf spot diseases on Aloe vera (L.) Burm.f. caused 79-83 by Curvularia species from Madhya Pradesh, India SHUBHI AVASTHI, AJAY KUMAR GAUTAM, REKHA BHADAURIA The interaction between diversity of herbaceous species and history of planting, Masal’s 84-88 plantations, Guilan Province, Iran HASSAN POURBABAEI, MASOUMEH ESKANDARI, MEHRDAD GHODSKHAH DARYAEI, MEHDI HEYDARI Feeding habit and length weight relationship of keureling fish, Tor tambra Valenciennes, 89-94 (Cyprinidae) from the western region of Aceh Province, Indonesia ZAINAL A. MUCHLISIN, AGUNG S. BATUBARA, MOHD N. SITI-AZIZAH, MUHAMMAD ADLIM, AFRIZAL HENDRI, NUR FADLI, ABDULLAH A. MUHAMMADAR, SUGIANTO SUGIANTO Comparison of woody species diversity between managed and unmanaged forests 95-101 considering vertical structure in Hyrcanian forests, Iran ZAHRA NOURI, MAHMOUD ZOBEIRI, JAHANGIR FEGHHI, GHAVAMALDIN ZAHEDI AMIRI, MOHAMMAD REZA MARVIE MOHADJER Nest temperatures of the Piai and Sayang Islands green turtle (Chelonia mydas) rookeries, 102-107 Raja Ampat Papua, Indonesia: Implications for hatchling sex ratios RICARDO F. TAPILATU,, FERDIEL BALLAMU GUIDANCE FOR AUTHORS
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