7/29/2021 Researcch article: Potential risk of tree regeneration failure-AGUS SUSATYA - [email protected] - Email Universitas Bengkulu
898 Researcch a icle: Potential risk of tree regeneration failure-A
Agus Susatya
Dear editors.
Attached files are my research article intended to be published in BIODIVERSITAS. First file consists of cover letter and main manuscript. Second file contains supplements (list of species 1
hopefully, it will be published on BIODIVERSITAS.
best regard
Agus Susatya Head of ecology and conservation div. Dept of Forestry UNIB. mobile; +62 85236506354
2 Lampiran
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Agus Susatya
Fwd: edited tree regeneration article 3 pesan
Managing Editor
Please, find attached file for comment. Kindly use "CLEAN/without track change" file to improve the mss. The improved mss is awaited.
Thank you, Regards,
Ahmad Dwi Setyawan
Managing Editor, - Biodiversitas, Journal of Biological Diversity (biodiversitas.mipa.uns.ac.id) (SCOPUS, DOAJ) - Nusantara Bioscience (biosains.mipa.uns.ac.id/N/index.htm) (Web of Science (ESCI), DOAJ)
--- Chairman/Co-Chairman - National Seminar & International Conference on Biodiversity, http://biodiversitas.mipa.uns.ac.id/snmbi.html
--- Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University, Jl. Ir. Sutami 36A Solo 57126, Central Java, Indonesia, Tel. & Fax. +62-271-663375, e-mail: [email protected]
------Forwarded message ------From: ...... Date: 2018-08-18 0:04 GMT+07:00 Subject: edited tree regeneration article To: Managing Editor
Yth Pak Ahmad:
Assalamu'alaikum wr wb.
Terlampir artikel tree regeneration yang sudah saya edit.
Catatan artikel tree regeneration:
1. Artikel ini bagus sekali, pembahasannya komprehensif, menyitir banyak hasil studi lainnya, menunjukkan kepakaran penulisnya. Selain itu, artikel ini menawarkan ide, perlunya menambahkan satutus konservasi secara lokal pada IUCN Redlist.
......
2. Dalam Results and Discussion, sebagian besar hasil penelitian disajikan dalam present tense. Tense tsb saya ubah ke dalam past tense karena hasil tersebut bersifat spesifik untuk saat https://mail.google.com/mail/u/0?ik=c367ee2064&view=pt&search=all&permthid=thread-f%3A1609085673601529393&simpl=msg-f%3A16090856736… 1/3 7/29/2021 Email Universitas Bengkulu - Fwd: edited tree regeneration article penelitian berlangsung, yang keadaan bisa berubah dalam perjalanan waktu. Hasil study yang disitir dan teori tetap saya pertahankan dalam bentuk present tense dengan asumsi bahwa yang disampaikan sudah dianggap sebagai kebenaran umum. Jika kita menyajikan hasil penelitian dalam present tense maka kita bersumsi bhw hasil penelitian tersebut bersifat umum. Secara etika, lebih baik kita menyajikan hasil penelitian spesifik kita dalam bentuk past tense (kecuali untuk fakta yang memang berlaku umum atau interpretasi atas data yang akan dibuat generalisasi).
3. Frasa declining its population (baris 261 file asli) saya ganti dengan the population ... is dwindling, dan pada baris 327 frasa declining population saya ubah menjadi dwindling population. Dalam demografi, istilah populasi itu berarti jumlah penduduk, sedangkan dalam ekologi istilah populasi berarti sekelompok individu sejenis. Namun seringkali istilah populasi dalam arti demografi digunakan untuk menunjukkan jumlah individu, misalnya populasi gajah Sumatera menurun (yang dimaksud adalah jumlah gajah Sumatera menurun). Dalam ekologi, untuk menggambarkan jumlah individu dalam populasi bisa digunakan istilah population size (jika jumlah individunya banyak berarti populasinya besar, dan sebaliknya), atau bisa juga population density (jumlah individu per satuan luas banyak berarti kepadatannya tinggi dan sebaliknya). Secara ekologi frasa populasi gajah Sumatera menurun lebih baik diganti dengan kepadatan populasi gajah Sumatera menurun, atau ukuran populasi gajah Sumatera mengecil. Sejalan dengan itu, frasa maintain population (Results and discussion, baris 121, dan 234 file asli) saya ubah jadi maintain its population density.
4. Kata fruits (jamak), di baris 155, saya ubah jadi fruit (tunggal) jika yang dimaksud adalah jumlah buahnya. Kata fruit adalah uncountable jika menyangkut jumlahnya, tapi countable jika menyangkut jenisnya. Fruits berarti buah dari berbagai jenis tumbuhan.
5. Dalam artikel ini banyak digunakan istilah such as (sebagai contoh) untuk merinci suatu kategori. Penggunaan istilah tersebut kurang tepat karena semua item disebutkan dalam rinciannya, maka istilah tersebut saya ganti dengan namely (yaitu). Jika rincian itu belum pasti menyebutkan semua item, maka istilah such as tidak saya ubah.
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2 lampiran 03-AUG-WER-edited with track changes The potential risk of tree regeneration.doc 456K 03-aug-wer-edited without track changes.doc 424K
Agus Susatya
dear editor
attached file is corrected file according to edited comments.
best regard
agus susatya dept of forestry unib [Kutipan teks disembunyikan]
https://mail.google.com/mail/u/0?ik=c367ee2064&view=pt&search=all&permthid=thread-f%3A1609085673601529393&simpl=msg-f%3A16090856736… 2/3 7/29/2021 Email Universitas Bengkulu - Fwd: edited tree regeneration article corrected article forest tree regeneration agus susatya.doc 393K
Managing Editor
Thank you, Regards,
Ahmad Dwi Setyawan
Managing Editor, - Biodiversitas, Journal of Biological Diversity (biodiversitas.mipa.uns.ac.id) (SCOPUS, DOAJ) - Nusantara Bioscience (biosains.mipa.uns.ac.id/N/index.htm) (Web of Science (ESCI), DOAJ)
--- Chairman/Co-Chairman - National Seminar & International Conference on Biodiversity, http://biodiversitas.mipa.uns.ac.id/snmbi.html
--- Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University, Jl. Ir. Sutami 36A Solo 57126, Central Java, Indonesia, Tel. & Fax. +62-271-663375, e-mail: [email protected]
[Kutipan teks disembunyikan]
https://mail.google.com/mail/u/0?ik=c367ee2064&view=pt&search=all&permthid=thread-f%3A1609085673601529393&simpl=msg-f%3A16090856736… 3/3 1 The potential risk of tree regeneration failure in species-rich Taba 2 Penanjung lowland rain forest, Bengkulu, Indonesia
3 AGUS SUSATYA 4 Department of Foresty, University of Bengkulu, Indonesia. Jl. WR Supratman, Bengkulu, Indonesia. Email: [email protected] 5 6 Abstract. Tropical lowland rain forest is recognized by its high species richness with very few trees per species. It is also known for 7 having tendency to out crossing of its species with different floral sexualities, which requires the synchronization between flowering of 8 its trees and the presence of pollinators. Such ecological attributes raise possible constraints for the forest trees to regenerate. The 9 objective of the study is was to develop assess the potential risk of failed regeneration for each tree species of the forest. Each of species 10 with dbh of more than 5 cm in a one- ha plot was collected, identified, and further determined its ecological criteria, including rarity, 11 floral sexuality, seed size, and flowering phenology were determined. The potential risk of the failure of regeneration was calculated by 12 summing all scores from Analytical Hierarchical Process of the criteria. The results indicated that the forest consists consisted of 118 13 species belonging to 69 genera and 37 families. Rare species accounted to 52.10% of the total species. Of the 118 species, the 14 potential medium risk category contributed to 38.14 %, and more than 33% one third tree species arewere grouped into very high and 15 high risk or are were more prone to the failed regeneration in the future. All rare dioecious species were categorized into very high and 16 high risks. Only 21 species (17.79%) are listed in 2017’s IUCN red list. Among unevaluated species, 22 and 13 species are were 17 respectively included into very high and high potential risk categories. The results revealed more detailed the potential risk of failed 18 regeneration of tree species, and can serve as basic information to develop proper conservation managements.
19 Keywords: Bengkulu, dioeciousdioecy, hermaphrodite, phenology, rarity, rain forest, risk regeneration.
20 Running title: Risk of tree regeneration failure on in tropical forest
21 INTRODUCTION
22 The presence of tropical rain forests and theirs intangible functions are growing getting more important in the recent 23 years due to their vital roles in providing life-supporting and ecological services such as carbon reserves sequestration, and 24 water resources provision, and as well as in fighting prevention of global warming and its negative impacts. However, 25 their existences are constantly being threatened by economic as well as human population pressures. Indonesian lowland 26 rain forests especially in Sumatra and Kalimantan Islands, have been undergoing rapid deforestration and degradation as 27 the results of conversions into mainly oil palm tree plantations as well as into much simpler tree stand structures of the 28 industrial plantation forests plantationswhich have simpler stand structure. In addition to those external factors, the forests 29 inherently have their own ecological attributes that potentially become constrains constrain their abilities to regenerate. In 30 species-rich tropical rain forests, each of its their tree species generally consists of very few individual trees (Whitmore 31 1984; Sakai et al. 1999; Sakai 2001). 32 Susatya (2007, 2010) studying three different tropical rain forests discovered the similarity of their structural patterns, 33 where namely, they were composed by of many species, but with very few individual trees. The very low density of tree 34 species appears to be more prevalent to the climax tree species than the pioneer species ones (Susatya 2011). Furthermore, 35 unlike pioneer species that have good capabilities to explore wide ecological ranges, the climax tree species have been 36 known to adapt to more limited ecological ranges as well as more stable environments, and have difficulties to grow under 37 warmer and drier environments (Whitmore 1983). Therefore, rapid environmental changes induced by both climate 38 change and forest degradation will pose constraints for climax tree species to regenerate. Moreover, according to floral 39 sexuality, Ng (1983) shows that dioecy is common among tropical tree species, which requires at least two different 40 individual trees to perform sexual regeneration. 41 In the tropical forest, even hermaphrodite species, they tend to be self incompatible, and consequently have to do out 42 crossing (Bawa et al.1985). Both phenomena require flower synchronization among trees of the same species in order to 43 that pollination process to can occur. Even, if this takes place, then pollination process is still difficult, because different 44 flowering trees can be distant to from each other (Whitmore 1983; Chave 2008). In the tropical rain forest of Malaysia 45 Peninsular, for example, it requires 32 ha to find two trees of the same species (Poore 1968). Therefore tropical trees must 46 either may suffer to adapt and be threatened bymust adapt to the rapid environmental alterations; or otherwise, they may be 47 threatened by those changes and may face difficulties in regeneration because of their own reproductive biologiesbiology. 48 The focus of the study is was to determine the potential risk of failed regeneration of tree species based on their floral 49 sexualities, tree density, flowering patterns, and seed sizes. 50 MATERIALS AND METHODS
51 The Research research site was located at Bukit Daun lowland rain Protected forestForest Area. The This lowland rain 52 forest was well protected and minor illegal logging in the form of cutting small pole (< 10 cm dbh) for social purposes was 53 infrequently occurred. Records at Talang Pauh climate station showed that in the last of decade, Taba Penanjung area 54 received the annual rain fall around 2848 mm, with no monthly rainfall less than 100 mm. November, December, and 55 January respectively received, 533, 420, 304 mm rainfall, and were higher monthly rainfalls than those that of the other 56 months. August was known to receive the lowest monthly rainfall (BPS Kab. Bengkulu Tengah 2012). Unusual low 57 monthly rainfall occurred in 1991 and 1994, when September and October got only 3 mm. The monthly relative humidity 58 was 83%, and reached as high as 87.7%, but dropped as low as 75.96%. The average of monthly temperature was 26.2 0C, 59 and reached its respective maximum and minimum at 29 0C in August, and 23 0C in October (Susatya 2007). Basic 60 floristic data were collected from a one- hectar plot in 2015. All trees with dbh of > 5 cm, were tagged, measured their 61 diameters measured, and collected their herbarium specimens collected. Species identification was carried out in the 62 Herbarium of Universitas Bengkulu (HUB). Species nomenclature followed Turner (1995). In the case of the absence of 63 tree’s reproductive aspects such as floral sexuality, flowering phenology, and seed size for each species, I relied on the 64 available secondary information including Plant Resources of South East Asia (PROSEA) No 5.(1) Timber trees: Major 65 commercial timbers (Soerianegara and Lemmens 1994), PROSEA No 5 (2) Timber trees: Minor commercial timbers 66 (Lemmens et al. 1995), PROSEA No 5 (3): Timber trees: Lesser-known species. (Sosef et al. 1998), and Plants of 67 Southeast Asia. www.asianplant.net to collect those data. 68 To determine the potential risk of failed regeneration (PRR), I applied Analytic Hierarchy Process (AHP) developed 69 by Saaty (1994), and adopted a similar approach from Oktariadi (2009), who used AHP to develop the risk ranking of 70 tsunami in Southern Java. The use method of AHP was selected because PRR was calculated by summing the score of 71 different criteria or biological aspects such as density, floral sexuality, flowering phenology, and seed size. AHP was is 72 widely used for selecting alternatives from different criteria in different hiearchies. AHP tranformed tranforms qualitative 73 data into the quantitative data ones through pairwise comparisons by experts (Saaty, 1980). Each comparison was 74 conducted to assign a value between two criteria according to their relative importances (Table 1) . 75 For the purpose of the study, it was established two hiearchies were established. The first hiearchy consisted of main 76 criteria such as species sexuality (Si), flowering phenology (Pi), seed size (Zi), and rarity (Ri) or the number of individual 77 trees per species per ha. Meanwhile, the second hierarchy was subcriteria within sexuality, phenology, seed size, and 78 rarity. Subcriteria of floral sexuality (Sj) included hermaphrodite (S1), monoecious (S2), dioecious (S3), while subcriteria 79 of the flowering phenology ( P j ) consisted of once (P1), twice (P2), throughout year (P3), and supra annual (P4). We 80 defined supra annual category as tree species that performs flowering every more than 1 year, while throughout year was 81 tree species that flowers more or less continued continuously within a year. The subcriteria of seed size (Z j ) was 82 categorized and developed following Chacon et al. (1998). It consisted of very small (0-4 mm), small (4-8 mm), medium 83 (8-12 mm), large (12-16 mm), and very large (> 16 mm), and was respectively coded as Z1, Z2, Z3, Z4, and Z5 . 84 Subcriteria of the rarity (R j ) consisted of R1, R2, R3, R4, R5, R6, and R7, which was defined by species with 1, 2, 3, 4, 85 5-6, > 7 trees per ha, respectively. Three senior ecologists within the Department of Forestry, University of Bengkulu 86 were selected as experts to carry out pairwise comparisons between two criteria or subcriteria. The results of pairwise 87 comparisons were used to construct the matrix of the value judgements, which was further analyzed to find the matrix of 88 the priority rank (eigenvalue). Each eigenvalue of criteria or subcritearia reflected the score of their relative importances 89 in determining the potential risk of failed regeneration. 90 At each hierachy level, the consistencies of all scores were checked their consistencies by comparing their calculated 91 consistency ratios with Saaty’s consistency ratio table. If there were inconsistencies in their judgements, all proseses of 92 pairwise comparison and analysis would bewere repeated (Saaty 1980, Saaty 2008). Potential risk of failed regeneration, 93 then, was calculated by summing the score of criteria and subcriteria of each species i (Si Sj + P i Pj + Z i Zj +R i Rj) x 94 100. Five categories of the potential risks consisting of very high, high, medium, low, and very low were developed. A 95 species was included to in either very high, high, medium, low or very low risks, if it had respectively a total score of PRR 96 between 30.93-36.44, 25.42-30.93, 19.91-25.42, 14.41-19.92, and 8.89-14.40. Potential risk was developed to indicate the 97 relative sensitivity of a species to regeneration failure. 98 It was aimed to extend the interpretation of species threats and the modifications of the systems in determining 99 extinction risk in IUCN at local level. A species with very high risk category implied implies that over the time frame, this 100 species was is expected to have be more sensitive to the regeneration failure than those of in lower risk categories. Any 101 species with very high and high risks will have respectively very high and high probability of the regeneration failure in 102 the near future. 103 104 Table 1: Assigned values of pair-wise comparisons 105 Assigned Definition Explanation judgment value 1 Equally important Two criteria or subcriteria are equally important to influence the potential risk of regeneration failure.
3 Moderately more important One criterion or subcriterion is moderately more important to influence the potential risk of regeneration failure. 5 Much more important One criterion or subcriterion is much more important to influence the potential risk of regeneration failure. 7 Very much more important One criterion or subcriterion is very more important to influence the potential risk of regeneration failure. 9 Extremly more important One criterion or subcriterion is extremely more important to influence the potential risk of regeneration failure. 2,4,6,8 Intermediate judment value values between two consecutive judgments 106
107 RESULTS AND DISCUSSION
108 Taba Penanjung lowland rain forest consists consisted of 118 species belonging to 69 genera and 37 families 109 (Supplement). The forest structure is was dominated composed mostly by of species with a single tree per ha that 110 contributed to 60 species or 52.10 % of the total species (Figure. 1). Only four species, consisting ofnamely Microcos 111 laurifolia, Croton argyratus, Elateriospernum tapos, and Endospermum diadenum, that have had more than 10 trees/ha. 112 Elateriospernum tapos (Euphorbiaceae) has had the highest density per ha with 31 trees. Following to Ng’s category 113 (1979) on species rarity, who defined that any species with a single tree is categorized as rare species, then the forest 114 structure is unproportionally dominated bycomposed of rare species. This rarity e species is was also shown at both genus 115 and family levels , wherein that 8 families or 21.62 % of the total families and 20 genera or 28.98 % of the total are were 116 respectively represented by a single tree. Therefore, any loss of an individual tree of the rare species can result in the loss 117 of species, genus, and family. The unproportional number of rare species composing forest structure appears to be 118 common in Bengkulu such as in Tambang Sawah lower montane forest of Kerinci-Seblat National Park (Susatya 2010), 119 and Talang Tais secondary lowland rain forest (Susatya 2007). Euphorbiaeae is was the most diverse family with 11 120 genera and 23 species, and followed subsequently by Moraceae with 3 genera and 13 species, and Miliaceae Meliaceae 121 with 3 genera and 10 species. It seems that the abundant species of Euphorbiaceae is one of the characters of the floristic 122 composition of Sumatra lowland forest. This is also observed elsewhere in West Sumatra (Hadi et al. 2009, Kohyama et 123 al. 1989). Interestingly, the rare species is was also common among the most diverse families. Among 23 species of 124 Euphorbiaceae, 11 species (47.82 %) are were rare species. Meanwhile the families of Moraceae and Meliaceae 125 respectively have had 33.33% and 40 % of its their species categorized as rare species. Species characterized by very few 126 individual trees per ha potentially faces more difficulty to maintain its population. 127 128
70 60 60 Number of species 50.85 50 % of the total species 40 (a) 30 18 16 20 15.25 13 13.56 11.02 7 5.93 10 4 3.39 0 1 2 3 4 5--6 >7 Tree /ha 60 49 50 41.53 39 40 33.05 30 (b) 30 25.42 20 10 0 Hermaphrodite Dioecious Monoecious
60 54
50 45.38 41 (c) 40 34.45
30
20 12 10.08 11 9.24 10
0 Once Twice Throughout Supra annual Figure 1: The structure of Taba Penanjung lowland rain forest according to tree density (a), floral sexuality (b) and flower phenology (c) of 129 its species. 130 131 132 According to floral sexuality, hermaphrodite species are were the most prevalent, and contribute contributing to 41.53 133 % of the total species (49 species). Meanwhile, monoecious and dioecious species respectively consisted of 33.05 % (39 134 species), and 25.42% ( 30 species) (Figure 1b) . Monoecious and dioecious species generally account to 4% and 6 % 135 (Renner and Ricklefs 1995), but the later appears to be more prevalent in the tropics than that of in temperate regions 136 (Renner 2014). The number of monoecious and dioecious species of Taba Penanjung lowland rain faorest is was higher 137 than that of Costa Rica wet premontana wet forest (Breanne 2017) as well as of Central Kalimantan, Indonesia (Brearley 138 et al 2007). Both monoecious Monoecious dan and dioecious species of Costa Rica premontana respectively come 139 account to 13.10 % and 13.70 % (Breanne 2017), while the similar categories of Central Kalimantan respectively 140 contribute to 14.70% and 23.49 % of the total species (Brearley et al. 2007). Special to dioecious species, its number 141 appears to be almost more similar than those found at both Sarawak (Ashton 1969) and Pasoh forests (Kochummen et al. 142 1991). Dioecious species at both sites respectively account to 26 % and 28 %. The number of monoecieous and 143 dioecious species of the site altogether accounts accounted up to 58,47 % of the total species (69 species). This shows 144 that more than half of the total species have to perform out crossing in order to that pollination to can occur. Such a 145 process requires both the synchronization of flowering phenology and the presence of pollinators, which could lead to 146 uncertainty on seed production and tree regeneration. The uncertainty is even greater because the sex ratio of dioecious 147 species is male biased (Queenborough et al 2009; Gao et al 2012) , and male flowers opens earlier than their female 148 counterparts at certain species (Queenborough et al 2013). 149 With regard to tree regeneration, dioecious species have advantages because they tend to produce large seeds, and 150 containing more energy energyreserved seed (Varmosi et al. 2008), which increase the probability of seedling 151 survivorship. However, dioecious species also face the most difficult regeneration, because they have only half of their 152 mature trees to produce seeds (Renner 2014). Dioecious tree species also tend to produce high seed density around their 153 female parent trees, which further attract lead to seed predation. It was is speculated that the more distance distant the 154 individual dioecious trees are located from their female parent trees, the individual dioecious trees have higher probability 155 of seed survivorship and, and arethe better seedling recruitment they have due to predation avoidance (Abbebe 2008). 156 Taba Penanjung lowland rain forest has diverse tree species based on flowering phenology. According to flowering 157 phenology, the majority of species of Taba Penanjung rain forest performs either throughout or once flowering phenology
158 (Fig 1c). Flowering phenology shows to the incidence of reproductive efforts of the species, which reflects and will 159 determine the probability of the reproductive success. The throughout flowering species has relatively higher probability 160 to ensure seed production and tree regeneration in the future compared tothan the supra annual category, simply because 161 the former produces more frequent flowers and fruits than that of the later, which only produces flower and fruit once for 162 every two to five years. Flowering phenology becomeis an important aspectsfactor on in tree regeneration, because the 163 duration, timing of flowering and fruiting coupled with seasons will determine seed production, survival, seedling 164 establishment and growth (Augspurger 1981). The role of environments becomes a pivot point on in tree regeneration 165 because the flowering phenology shows a strong correlation with climate, rain fall and humidity, drought and temperature 166 (Kushwaha et al 2011; Sulistyawati et al. 2012). Species with throughout flowering contributes contributed to 45.38 % of 167 the total species (54 species), while thosespecies with once flowering a year accounts accounted to 34.45 % (41 species). 168 The number of species with twice a year and supra annual flowering patterns is was not as much many as both throughout 169 and once flowering phenologies. Both patterns respectively accounted to 10.08 % (13 species) and 9.14 % (11 species). 170 The number of species with supra annual flowering in the site are was far lessmuch lower than that of Central Kalimantan 171 (Brearley et al. 2007), and of Lambir hill of Sarawak (Sakai et al. 1999). The supra annual flowering species at those two 172 last sites respectively account to 75 %, and 54 %. Both forests were are dominated by species of Dipterocarpaceae 173 (Brearley et al. 2007; Sakai et al. 1999), which were are well known to perform mass flowering or supra annual flowering 174 (Whitmore 1984). Meanwhile Taba Penanjung rain forest is dominated by species of Euphorbiacae and Moraceae, which 175 are recorded to have throughout flowering patterns (Whitmore 1984). 176 Most of species falls falled into medium risk category, and contributes contributing to 38.14 % of the total species. 177 Species with this medium risk indicate that they do not face an immediate risk which may further threaten their 178 regeneration. Other categories such asnamely very high, low, and high risks have had almost similar values, ranging from 179 19.49 %, 18.64%, to 17.80 %. (Figure 2) Both very high and high risk categories altogether accounted to 37.29 %, and 180 showindicating that more than one third of the species will face more serious threat to their tree regenerations in the near 181 future. 182 183
184 185 186 Figure 2: The potential risk of regeneration failure of trees of Taba Penanjung lowland rain forest. 187 188 189 190 Twenty three species from five families are were included into very high risk category, consisting of species from 191 Euphorbiaceae, Myristicaceae, Lauraceae, Flaucourticaeae, Moraceae, and Rubiaceae. Each of these families respectively 192 contributes contributed to 52.17 % (12 species), 21.74 % (5 species), 13.04 % (3 species), and 4.3% (1 species). Of these 193 families, all species of Myristicaeae, namely such as Knema globularia, Knema glauca, Horsfieldia polyspherula, 194 Horsfieldia costulata, and Gymnacranthera forbesii, awere included into this category. The very high risk category is was 195 dominated by dioecious species (22 of 23 species). The only monoecious included toin this category is was Artocarpus 196 kemando (Moraceae). Artocarpus kemando iwas characterized by a single tree per species per ha, large seed category, and 197 supra annual flowering. The combination of these biological characters makes this species becoming have very high risk. 198 A Nnote of this species is that, the incident of supra annual flowering is relatively longer compared tothat of the other 199 supra annual flowering species. It has been recorded to produce no flowers within 7 years (Sosef et al. 1998). The Very 200 very high risk category does not all consisted by not only of species with a single tree;, in fact, 7 of them have had more 201 than one tree per ha, such asnamely Aporosa accuminatisima (2), Actinodaphne peduncularis (2 trees), Drypetes 202 longifolia (2 trees), Hydnocarpus curtisi (3 trees), Horsfieldia costulata (2 trees), and Knema globularia (3 trees) (3 trees). 203 All of these species have similar characters such as dioecious, and extra large speciesseeds, and with various flowering 204 phenology. Among these species, Aporosa. accuminatisima and Actinodaphne peduncularis are recorded to have
205 ecological disadvantages, where in that the former has been reported for its low regeneration, and the later has been known 206 for its restricted distribution (Sosef et al. 1998). It appears that the extra large seed category, and the species density of 207 more than one tree per ha will put the dioecious species into very high risk regardless of their flowering phenologies. The 208 extra large- size of seeds is generally recalcitrant, which has very fast germination, the low capability of dormancy, and the 209 high sensitivity to drought (Marcos-Filho 2005). Water content within seeds for of this type determines germination 210 success, and it varies according to species and habitat quality. For example the seeds of Shorea roxburghii, which has 211 habitat with less little rainfall, will beis tolerant to low water content and still be able to germinate when the water content 212 of its seeds reaches as low as 35 %. Meanwhile, the seeds of other species such as S. almon, and S. robusta can not 213 germinate with when the water content is less than 40 %. Recalcitrant seeds generally are not able to germinate if the 214 water content reaches as low as 20%-30% (Davies & Ashton 1999). 215 This is the is reason shows thatwhy the species with large seeds prefer to growing and becoming become common in 216 the moist condition under canopy trees, but hardly survive in open canopy, or a drierdry, warmer, and disturbed habitat. 217 Davies & Ashton (1999) raise the issues on the disadvantages for large- seed species. A Large large seed tends to have 218 lower fecundity, and is can hardly to thrive at a forest gap habitat. On the other hand, a large seed has the advantages for 219 of being having more energy reserved in its cotyledon. In the righta good-quality environmental quality, the large seed 220 will rapid germinationgerminates and, fast growthgrows rapidly, and perform has high seedling survivorship due to the 221 large energy stored in cotyledon (Arunachalam et al. 2003). In On the contrary, the smaller small-size seed size is 222 generally more tolerant to decreasing water contents ( Chin et al. 1989). Small- size seeds are categories categorized as 223 orthodox seed which generally tolerate to drought, and are well known to have long dormancy. Therefore, species with 224 small seeds are able to wait until suitable environments become avaiable for their germination. The presence of gap 225 generating more light intensity, drier and less moist conditions triggers small seeds to germinate and dominate the open 226 habitat (Marcos-Filho 2005). Furthermore, a small seed has many ecological advantages of having , where it 227 increaseswider dispersal, and isbeing able to select suitable microclimates, and performs having high fecundity (Davies & 228 Ashton 1999). 229 The majority of the very high risk category has had throughout flowering (12 species), followed by once flowering 230 phenology type (6), and while supra annual flowering only contribute toconsisted of 3 species. This flowering phenology 231 variation shows that the phenology does not determine the very high risk category. Furthermore, the very high risk also 232 contains comprised 8 and 7 species that are respectively characterized by extra large and small seed categories. Similar to 233 the phenology, seed size does not also determine the very high risk category either. Therefore, In in general, if a species 234 is dioecious and rare, then the species is likely to belongs to very high category regardless of seed size and flowering 235 phenology. Dioecious species generally fall into very high risk category, because of the complexity of reproduction 236 biology. To carry out reproduction efforts, they require flowering synchronization and the presence of 237 pollinationpollinators. Dioecious species show more limited reproduction capacity than the those having other flower 238 sexuality types, simply due tobecause it they has have only half of their mature trees contributing to seed production. 239 Their flowering and fruiting successes are also influenced by both the distance between male and female trees and the 240 pollinator movement from male to female trees (Renner 2014). During pollination process, pollinators travel a certain 241 distance which further add up to the uncertainty of fruit production. The longer the distance between mature male and 242 female trees, the more uncertain pollination process to occur. It was estimated that the closest distance between the same 243 tree species could reach up to 131 m, and the distance between female and male trees could be even farther (Abebbe, 244 2008). The difficulty of the regeneration of dioecious species is even greater due to the fact that the microclimates beneath 245 male mature trees play a determinant determining factor role in regeneration. It has been known that seedling and sapling 246 recruitments tend to be greater beneath the male trees than those ofthe female trees (Arai & Kamitani 2005) 247 A Rare rare species are is expected to face the regeneration problem due to its difficulty to maintain its population 248 density. A Rare rare or single-tree per ha species easier is more likely to experiences failed regeneration, simply because 249 rare species or single tree per hait statistically has a lower chance to regenerate than those of more than one tree per ha. 250 Forest structure dominated by species having very few individual trees species appears a common ecological attribute of 251 species-rich Southeast Asia rainforest (Susatya 2010) and Nigerian rain forest (Adekunle et al. 2013). For From the forest 252 tree regeneration perspective, it this attribute has been worsened by the fact that even hermaphrodite species tends to be 253 self incompatible, and has to perform outcrossing (Bawa 1979; Bawa et al. 1989). However, in this research, a species 254 with a single tree alone do not necessarily determine whether the species belongs to either to very high or high risk 255 categories. In fact, 55 % of the total of rare species are classified into either medium risk (27 species) or low risk (5 256 species) category. Only rare species with either dioecious dioecy or monoecious monoecy are most likely to belong to 257 either very high or high risk category. Rare species with high and very high risk categoris accounted up to 12 species and 258 16 species, respectively. Moreover, rare hermaphrodite species will fall into medium risk category regardless of seed size 259 and flowering phenology. However, rare hermaphrodite species with both small seed category and throughout phenology 260 such as Bhesa paniculata (Celastraceae) Astronia macrophylla (Melastomaceae), Neolamarckia cadamba (Rubiaceae), 261 Micromelum minutum (Rutaceae), and Rinorea anguifera (Violaceae) are were included to in low risk category. These 262 combined criteria make these five species are have a better change chance to have better reproductive success as well as 263 better seedling survivorship than those ofthe monoecious and dioecious species. This pattern shows that the being 264 dioecious or monoecious have is more influential on in determining very high and high risks than being rare species. As
265 long as a rare species does not belong to dioecious and monoecious categories, it will not be included into either very high 266 and or high risk categoriescategory. 267 The high risk category is was composed of 21 species of 10 families, where of which family of Meliaceae contributed 268 most with 7 species, while the other nine families only contributed ranging from one species to 4 four species. High risk 269 category composes comprised various species with all types of the flower sexuality. Monoecious species contributes 270 contributed most with 13 species (61.90 %), followed by diocious species (6 species). Meanwhile, hermaphrodite species 271 only accounts accounted to 2 species. Interestingly, of the 48 hermaphrodite species generally belonging to either 272 medium or very low risk, two of them arewere included within high risk category, . These high risk hermaphrodite species 273 includenamely Shorea ovalis and Palaquium hexandrum, both of which both are characterized by extra large seed and 274 supra annual flowering phenology. The combination between of extra large seed and the less frequent incidence of 275 flowering and fruiting makes those two species classified into high risk category. In addition to these biological aspects, 276 an external factor in the form of timber harvesting becomes an eminent threat to these two species. The population of 277 Shorea ovalis, the member of commercial light Red Meranti group, is also declining dwindling its population due to 278 logging (Soerianegara & Lemmens 1994). Like other species of Palaquium, Palaquium hexandrum faces a reproductive 279 problem, because its flowers hardly reach maturity due to insect predation. If they pass through fruit development, then it 280 their fruits suffer high predation by bats, birds, and squirrels (Soerianegara & Lemmens 1994). Furthermore, a special 281 attention has to be made for a rare species of Diospyros sumatrana which has been classified into high risk category. The 282 species appears to face fruit a development problem, because it needs long period of time to reach fruit ripening (Lemmens 283 et al. 1995). Such a long period could result to in being more vulnerable to fruit predation, which could further lead to 284 lower its regeneration capability. 285 Not all the Monoecious monoecious species does not all fall into a single category. Most of the monoecious species 286 falls falled into medium risk (18 species), subsequently followed by high risk (13 species), low risk (6 species), and very 287 high and very lows risk categories which respectively consistedtribute to of only 1 species. Monoecious species with one 288 to two trees per ha, large and extra large seed categories, and once flowering pattern will fall into high risk category. 289 Meanwhile similar monoecious species with very small seed and throughout phenology (12 species) will belong to 290 medium risks category. Interestingly, monoecious species with 3-4 trees but with once and supra annual flower will also 291 belong to medium risk category regardless of seed size. It appears that whether a monoecious species will fall into a 292 certain category is not solely defined by its rareness, but also by the seed size and flowering phenology. 293 Species belonging into medium risk category should not face immediate threats for their regeneration. However, 294 timber harvesting will potentially jeopardize their futures. Among the medium risk category (45 species), 26.27 % (12 295 species) of them are either included into major or minor commercial timbers (Soerianegara & Lemmens 1994; Lemmens et 296 al. 1995). This indicates that these species are likely to become a target for logging in the near future. In addition to a 297 timber harvesting factor, their ecological attributes could potentially increase the risks a special attention should be made 298 for of several medium risk species because their ecological attributes could potentially increase their risks. For example, 299 the tree population of Alstonia angustiloba has been locally depleted due to logging (Soerianegara & Lemmens 1994), 300 while Baccaurea racemosa has been recorded as uncommon species at the lower strata of the Southeast Asia rain forest ( 301 Sosef et al. 1998). Furthermore, Endospernum diadenum faces a high predation of its seeds, and is known to have low 302 seed viability (Soerianegara & Lemmens 1994). Three species of Polyalthia, P. hookeriana, P. michaelii, and P. rumphii 303 are noted to have scattered distribution, and their seedlings are sensitive to drought (Sosef et al. 1998). 304 The Hermaphrodite hermaphrodite species were included to in various categories from medium to very low risk. Rare 305 hermaphrodite species are likely to fall into medium risk, if they have medium to extra large seeds, regardless of their 306 flowering phenologies. However, if rare hermaphrodite species with small to very small seed categories and throughout 307 flowering pattern will fall into low risks. Furthermore, hermaphrodite species with more than one tree are mostly likely 308 to belong to low and very low risk categories. Hermaphrodite species with more than 4 trees will come up into two 309 different categories depending to on their seed sizes. Those with small and medium sizes will end up to very low risk 310 category, while those with large and extra large seeds will fall into low category. The former consists of Shorea 311 platyclados, Barringtonia lanceolata, and Syzygium rostrata, while the later are Geunsia hexandra, Dillenia excelsa, 312 Strombosia javanica, Neonauclea gigantea, Microcos laurifolia, Euonymus javanicus, and Cratoxylum sumatrana. 313 Of the 118 tree species, only 21 species (17.79%) are listed in 2017’s IUCN red list. The other species are listed as not 314 assessed species, meaning the conservation statutes of these species has have not been evaluated their conservation statues 315 according to IUCN’s criteria. The tree species listed at IUCN consists of 2, 1, 3, and 15 tree species respectively 316 categorized into endangered (E), Vulnerable (V), near threatened (NT), and least concerned (LC). Furthermore, Of of the 317 23 species with very high risk category, only three tree species, namely including Litsea spathacea, Knema glauca, K. 318 globularia have been included into least concerned. Of the 21 species with high risk category, seven tree species are 319 categorized into four different IUCN’s conservation status. Two species, namely such as Aglaia speciosa and Sterculia 320 oblongata, are classified as endangered, while Sterculia parvifolia is included as vulnerable. Furthermore, three species of 321 Meliaceae, namely such as Aglaia odoratissima, A. ologophylla, and A. rubiginosa, are grouped into near threatened. 322 Species of Knema glauca, K. globularia, Litsea spathacea, Aglaia tomentosa , Sterculia parviflora, Archidendron 323 ellipticum, Magnolia sumatrana, Microcos laurifolia, , Alstonia angustiloba, , Bhesa paniculata,, Euonymus javanicus, , 324 Payena maingayi, P. lanceolata, Polyalthia hookeriana, and Prunus arborea, are categorized as the least concerned
325 species. Comparing between the IUCN redlist and the results of the potential risk analysis, it comes up withresulted in 326 interesting results. Among the 15 species listed as least concerned by IUCN, nine species are classified into medium to 327 low risk catagories, which is almost similar to least concerned category, while the other six species, namely such as 328 Knema glauca, K. globularia Aglaia tomentosa, Archidendron ellipticum, Knema, Litsea spathacea, and sterculia 329 obolongata are either included into high risk or very high risk category. The first two are were very high risk species 330 characterized by dioecious species with supra annual flowering phenology, while the rest are were high risk monoecious 331 species with large seed category. Sterculia oblongata, vulnerable species by IUCN, is was classified into high risk. Both 332 seem to be comparable status, where both indicate that in the near future, the species will face difficulty to maintain its 333 population density in order to avoid local extinction. Interestingly, Shorea platiclados that has long been classified as 334 endangered species (Ashton 1998), does did fall into low risk. Low risk category of this species indicates that it relatively 335 does not face immediate threat on its tree regeneration locally, and is considered to be able to ensure its future 336 regeneration. The number of tree per ha (4 trees) becomes becomed the main reasons for the species to be classified as 337 low risk category. Moreover, among the 97 species unevaluated whose conservation statuses species have not been 338 evaluated by IUCN, 22 and 13 species arewere respectively included into very high and high potential risk categories. 339 The conservastion statuses of Most most of the very high and high risk tree species have not eventually been evaluated 340 their conservation status according to IUCN’s criteria. IUCN is aware that there is a need to for more detailed evaluation 341 for conservation status at local level due tobecause differences between global and local threats is are very important for 342 conservation management. It further indicates that a species that which has been globally categorized into endangered 343 could be the least concerned category due to stable and healthy population at a local level. On the other hand, species with 344 least concern species status can turn into endangered category due to its small and locally declining dwindling population 345 (IUCN 2012). The results of the this research make more detailed ecological information concerning the potential risk of 346 the failure of tree regeneration available, which is not always provided by IUCN red list documents. The results are very 347 important to serve as both substitutes and guidances at local level for conservation purposes in the absence of conservation 348 status of IUCN of the tree species.
349 ACKNOWLEDGEMENTS
350 The author is indebted to members of WARISAN, who helped in the field works, and also grateful to Astri W. Utami, 351 Sequoia MS Rhomadhon, and Magnolia GR. Satriorini, who supported logistics during the field work.
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435 Table S1 (Supplement): Tree species of Taba Penanjung Lowland Rain forest and their potential risks of the regeneration failure 436 No Species Family Rarity Floral sexuality Seed size Flowering phenology Total Score PRR tree/ha Score Type Score Type Score type Score 1 Actinodaphne peduncularis L Lauraceae 2 0.238 Dio 0.581 Exl 0.3260 Onc 0.281 34.1826 VH 2 Aglaia affinis Merr Meliaceae 2 0.238 Mon 0.309 Med 0.1770 Onc 0.281 25.6374 H 3 Aglaia faveolata Pannell Meliaceae 1 0.286 Mon 0.309 Med 0.1770 Onc 0.281 27.8982 H 4 Aglaia odoratissima Blume Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H 5 Aglaia oligophylla Miq Meliaceae 3 0.19 Mon 0.309 Exl 0.3260 Onc 0.281 24.9858 M 6 Aglaia rubiginosa (Hiern.) Pannell1 Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H 7 Aglaia speciosa Blume Meliaceae 2 0.238 Mon 0.309 Lrg 0.2960 Onc 0.281 26.9226 H 8 Aglaia tomentosa Teijm ex Binn Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H 9 Alstonia angustiloba Miq. Apocynaceae 1 0.286 Hmp 0.11 Vsm 0.087 San 0.412 24.0132 M 10 Antidesma brachybotrys Airy Shaw Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 11 Antidesma griffithii Hoof. F Euphorbiaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH 12 Antidesma leucocladon Hook.f Euphorbiaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH 13 Antidesma montanum Blume Euphorbiaceae 2 0.238 Dio 0.581 Vsm 0.087 Thr 0.116 28.8789 H 14 Antidesma velutinosum Blume Euphorbiaceae 3 0.19 Dio 0.581 Sml 0.114 Thr 0.116 26.9097 H 15 Aporosa accuminatisima Merr Euphorbiaceae 2 0.238 Dio 0.581 Sml 0.114 Onc 0.281 31.8930 VH 16 Archidendron ellipticum (Blume) Nielsen Leguminosae 1 0.286 Mon 0.309 Exl 0.3260 Thr 0.116 26.7849 H 17 Artocarpus anisophyllus Miq. Moraceae 4 0.143 Mon 0.309 Lrg 0.2960 San 0.412 24.6096 M 18 Artocarpus elasticus Reinw. ex Blume Moraceae 4 0.143 Mon 0.309 Exl 0.3260 Onc 0.281 22.7721 M 19 Artocarpus kemando Miq Moraceae 1 0.286 Mon 0.309 Lrg 0.2960 San 0.412 31.3449 VH 20 Astronia macrophylla Blume Melastomaceae 1 0.286 Hmp 0.11 Sml 0.114 Thr 0.116 19.4208 L 21 Baccaurea bracteata Mull. Arg Euphorbiaceae 1 0.286 Dio 0.581 Med 0.1770 Thr 0.116 32.1117 VH 22 Baccaurea edulis Merr Euphorbiaceae 1 0.286 Dio 0.581 Exl 0.3260 Onc 0.281 36.4434 VH 23 Baccaurea racemosa (Reinw. ex Blume) Mull. Arg. Euphorbiaceae 6 0.095 Dio 0.581 Lrg 0.2960 Thr 0.116 24.4008 M 24 Baccaurea sumatrana (Miq.) Mull. Arg. Euphorbiaceae 3 0.19 Dio 0.581 Med 0.1770 Thr 0.116 27.5901 H 25 Barringtonia lanceolata (Ridl.) Payen Lecythidaceae 4 0.143 Hmp 0.11 Exl 0.3260 Thr 0.116 14.9751 L 26 Bhesa paniculata Arn Celastraceae 1 0.286 Hmp 0.11 Sml 0.114 Thr 0.116 19.4208 L 27 Bridelia insulana Hance Euphorbiaceae 3 0.19 Mon 0.309 Sml 0.114 Thr 0.116 19.9737 M 28 Campnosperma auriculatum (Blume) Hook.f Anarcadiaceae 1 0.286 Mon 0.309 Med 0.1770 Thr 0.116 25.1757 M 29 Casearia capitellata Blume Flacourtiaceae 1 0.286 Hmp 0.11 Exl 0.3260 Thr 0.116 21.7104 M 30 Casearia clarkei King var. kunstleri (King) Ridl. Flacourtiaceae 1 0.286 Hmp 0.11 Exl 0.3260 Thr 0.116 21.7104 M 31 Castanopsis inermis (Lindl.) Benth. ex Hook. F Faagaceae 4 0.143 Mon 0.309 Lrg 0.2960 Onc 0.281 22.4481 M 32 Chionanthus pluriflorus (Knob) Kew Oleaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Thr 0.116 19.1256 L 33 Chionanthus spicata Blume Oleaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M 34 Commersonia bartramia (L) Merr. Sterculiaceae 2 0.238 Mon 0.309 Sml 0.114 Thr 0.116 22.2345 M 35 Cratoxylum sumatrana (Jack.) Blume Hypericaceae 6 0.095 Hmp. 0.11 Sml 0.114 Onc 0.281 13.1472 VL 36 Croton argyratus Blume Euphorbiaceae 15 0.048 Mon 0.309 Med 0.1770 Thr 0.116 13.9659 VL 37 Dacryodes rugosa (Blume) H. J. Lam Burseraceae 3 0.19 Dio 0.581 Exl 0.3260 Thr 0.116 29.1993 H 38 Dillenia excelsa (Jack.) Gilg Dilleniaceae 6 0.095 Hmp 0.11 Sml 0.114 Onc 0.281 13.1472 VL 39 Diospyros sumatrana Miq Ebenaceae 1 0.286 Mon 0.309 Sml 0.114 Onc 0.281 27.2178 H 40 Drypetes longifolia (Blume) Pax ex. K. Hoffm Euphorbiaceae 2 0.238 Dio 0.581 Exl 0.3260 Onc 0.281 34.1826 VH 41 Durio zibethinus L Bombacaceae 1 0.286 Hmp 0.11 Exl 0.3260 Twi 0.191 22.9479 M 42 Dysoxylum arborescens (Blume) Miq Meliaceae 2 0.238 Mon 0.309 Exl 0.3260 Onc 0.281 27.2466 H 43 Dysoxylum densiflorum (Blume) Miq. Meliaceae 4 0.143 Mon 0.309 Sml 0.114 Onc 0.281 20.4825 M 44 Dysoxylum excelsum Blume Meliaceae 4 0.143 Mon 0.309 Exl 0.3260 Onc 0.281 22.7721 M 45 Elaeocarpus nitidus Jack Elaeocarpaceae 1 0.286 Hmp 0.11 Med 0.1770 Onc 0.281 22.8237 M 46 Elateriospernum tapos Blume Euphorbiaceae 31 0.048 Mon 0.309 Exl 0.3260 Thr 0.116 15.5751 L 47 Endospermum diadenum (Miq.) Airy Shaw Euphorbiaceae 12 0.048 Dio 0.581 Vsm 0.087 Thr 0.116 19.9299 M 48 Erismanthus obliquus Wall ex. Mull. Arg. Euphorbiaceae 1 0.286 Mon 0.309 Sml 0.114 Thr 0.116 24.4953 M 49 Euonymus javanicus Blume Celastraceae 3 0.19 Hmp. 0.11 Lrg 0.2960 Onc 0.281 19.5873 L 50 Ficus benjamina L Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M 51 Ficus depressa Blume Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M 52 Ficus fistulosa Reinw. ex. Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M 53 Ficus fulva Reinw. ex. Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M 54 Ficus heteropleura Blume Moraceae 3 0.19 Mon 0.309 Vsm 0.087 Thr 0.116 19.6821 L 55 Ficus lepicarpa Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M 56 Ficus ribes Reinw. ex Blume Moraceae 3 0.19 Mon 0.309 Vsm 0.087 Thr 0.116 19.6821 L 57 Ficus sundaica Blume Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M 58 Ficus variegata Blume Moraceae 4 0.143 Mon 0.309 Vsm 0.087 Thr 0.116 17.4684 L 59 Flacourtia rukam Zoll. et. Moritzi Flaucourtiaceae 3 0.19 Hmp 0.11 Sml 0.114 Onc 0.281 17.6217 L 60 Geunsia hexandra (Teijsm. et. Binn) Koord Verbenaceae 4 0.143 Hmp 0.11 Sml 0.114 Thr 0.116 12.6855 VL 61 Gironniera subaequalis Planch Ulmaceae 5 0.095 Mon 0.309 Sml 0.114 Thr 0.116 15.4992 L 62 Gordonia maingayi Dyer Theaceae 1 0.286 Hmp 0.11 Exl 0.3260 Twi 0.191 22.9479 M 63 Gordonia multinervis King Theaceae 3 0.19 Hmp 0.11 Exl 0.3260 Twi 0.191 18.4263 L 64 Gymnacranthera forbesii (King) Ward Myristicaceae 1 0.286 Dio 0.581 Exl 0.3260 Twi 0.191 34.9584 VH 65 Horsfieldia costulata Warb Myristicaceae 2 0.238 Dio 0.581 Exl 0.3260 Thr 0.116 31.4601 VH 66 Horsfieldia polyspherula (Hook. F) J. Sinclair Myristicaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH 67 Hydnocarpus curtisii King Flacourtiaceae 3 0.19 Dio 0.581 Exl 0.3260 Onc 0.281 31.9218 VH 68 Knema glauca (Blume) Petermann Myristicaceae 4 0.143 Dio 0.581 Exl 0.3260 San 0.412 31.8696 VH 69 Knema globularia ( Lam.) Warb. Myristicaceae 3 0.19 Dio 0.581 Exl 0.3260 San 0.412 34.0833 VH 70 Lansium domesticum Corra Sapindaceae 1 0.286 Mon 0.309 Exl 0.3260 Onc 0.281 29.5074 H 71 Litsea cubeba (Laur.) Pers Lauraceae 4 0.143 Dio 0.581 Lrg 0.2960 Onc 0.281 29.3841 H 72 Litsea sessilis Boerl. Lauraceae 1 0.286 Dio 0.581 Med 0.1770 Onc 0.281 34.8342 VH 73 Litsea spathacea Gamble Lauraceae 1 0.286 Dio 0.581 Med 0.1770 Onc 0.281 34.8342 VH 74 Macaranga hosei King ex Hook Euphorbiaceae 1 0.286 Dio 0.581 Vsm 0.087 Thr 0.116 31.1397 VH 75 Macaranga hulletii King ex Hook. F. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 76 Macaranga triloba (Blume) Mull. Arg. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 77 Magnolia uvariifolia Dandy ex Noot 2 Magnoliaceae 1 0.286 Hmp 0.11 Med 0.1770 Onc 0.281 22.8237 M 78 Mallatus leptophyllus Pax et C.K. Hoffm. Euphorbiaceae 2 0.238 Hmp 0.11 Vsm 0.087 Onc 0.281 19.5909 M 79 Mallotus auriculatus Merr Euphorbiaceae 3 0.19 Dio 0.581 Sml 0.114 Thr 0.116 26.9097 H 80 Mallotus montanus (Mull. Arg) Airy Shaw Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 81 Mallotus peltatus (Geisel.) Mull. Arg. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 82 Microcos laurifolia (Hook et Mast) Burret Tiliaceae 14 0.048 Hmp 0.11 Med 0.1770 Thr 0.116 8.8914 VL 83 Micromelum minutum (G. Forst.) Wright and Arn. Rutaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L 84 Naphelium lappaceum L Sapindaceae 1 0.286 Hmp 0.11 Exl 0.3260 Onc 0.281 24.4329 M 85 Neolamarckia cadamba (Roxb) Basser Rubiaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L 86 Neonauclea excelsa Merr Rubiaceae 1 0.286 Hmp 0.11 Med 0.1770 Thr 0.116 20.1012 M 87 Neonauclea gigantea Merr Rubiaceae 6 0.095 Hmp 0.11 Med 0.1770 Thr 0.116 11.1051 VL 88 Ochanostachys amentacea Mast Olacaceae 2 0.238 Mon 0.309 Lrg 0.2960 Thr 0.116 24.2001 M 89 Palaquium hexandrum (Griff.) Baill Sapotaceae 1 0.286 Hmp 0.11 Exl 0.3260 San. 0.412 26.5944 H 90 Payena lanceolata Ridl. Sapotaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M
91 Payena maingayi Clarke Sapotaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M 92 Pittosporum ferrugineum W.T. Aiton Pittosporaceae 3 0.19 Hmp 0.11 Vsm 0.087 Thr 0.116 14.6076 L 93 Polyalthia hookeriana King Annonaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Twi 0.191 22.6239 M 94 Polyalthia michaelii C.T. White Annonaceae 1 0.286 Hmp 0.11 Med 0.1770 Twi 0.191 21.3387 M 95 Polyalthia rumphii (Blume) Merr. Annonaceae 1 0.286 Hmp 0.11 Med 0.1770 Twi 0.191 21.3387 M 96 Pometia pinnata J.R. Forst et G. Frost Sapindaceae 1 0.286 Mon 0.309 Exl 0.3260 Onc 0.281 29.5074 H 97 Prainea limpato (Miq.) Beumee Moraceae 4 0.143 Mon 0.309 Vsm 0.087 Onc 0.281 20.1909 M 98 Prunus arborea (Blume) Kalkman Rosaceae 1 0.286 Hmp 0.11 Sml 0.114 Onc 0.281 22.1433 M 99 Prunus lamponga (Miq.) Kalkman Rosaceae 3 0.19 Hmp 0.11 Sml 0.114 Onc 0.281 17.6217 L 100 Quercus argentata Korth Fagaceae 7 0.048 Mon 0.309 Exl 0.3260 Onc 0.281 18.2976 L 101 Rhodamnia cinerea Jack Myrtaceae 1 0.286 Hmp 0.11 Med 0.1770 Thr 0.116 20.1012 M 102 Rinorea anguifera (Lour.) Kuntze Violaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L 103 Shorea ovalis (Korth.) Blume Dipterocarpaceae 1 0.286 Hmp 0.11 Exl 0.3260 San 0.412 26.5944 H 104 Shorea parvifolia Dyer Dipterocarpaceae 3 0.19 Hmp 0.11 Med 0.1770 San 0.412 20.4636 M 105 Shorea platyclados Slooten ex. Fox Dipterocarpaceae 4 0.143 Hmp 0.11 Lrg 0.2960 San 0.412 19.5351 L 106 Sterculia oblongata R. Br. Sterculiaceae 1 0.286 Mon 0.309 Sml 0.114 San 0.412 29.3793 H 107 Sterculia parviflora Roxb. ex. G. Don Sterculiaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H 108 Strombosia javanica Blume Olacaceae 6 0.095 Hmp 0.11 Med 0.1770 Onc 0.281 13.8276 VL 109 Symplocos crassipes C. B. Clarke Symplocaceae 2 0.238 Hmp 0.11 Sml 0.114 Twi 0.191 18.3975 L 110 Syzygium flosculiferum (M. R. Hensd.) Sreek Myrtaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Twi 0.191 20.3631 M 111 Syzygium kunstleri (King). Bahadur et R.C. Gour Myrtaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Twi 0.191 22.6239 M 112 Syzygium lineatum (DC) Merr. ex L. M. Terry Myrtaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Onc 0.281 24.1089 M 113 Syzygium politum (King). I.M. Turner Myrtaceae 1 0.286 Hmp 0.11 Sml 0.114 Twi 0.191 20.6583 M 114 Syzygium rostrata Blume Myrtaceae 4 0.143 Hmp 0.11 Lrg 0.2960 Twi 0.191 15.8886 L 115 Urophyllum macrophyllum Korth Rubiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 116 Vitex vestita Wall. ex Schauer Verbenaceae 1 0.286 Hmp 0.11 Sml 0.114 Onc 0.281 22.1433 M 117 Xylopia caudata Maingay ex. Hook. F. et Thomson Annonaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Onc 0.281 21.8481 M 118 Xylopia elliptica Hook.f and Thomson Annonaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Onc 0.281 24.1089 M 437 Note : Floral sexuality code; Dioecious (Dio), Monoecious (Mon), Hermaphrodite (Hmp). Seed size code; Extra large (Exl), Large (Lrg), Medium (Med), Small (Sml), Very small (Vsm). 438 Flowering phenology code ; Once (Onc), Twice (Twi), Throughout (Thr), Supra annual (San). PRR refers to the potential risk of regeneration failure. PRR code: Very high risk (VH), High risk 439 (H), Medium risk (M),Low risk (L), and Very low (VL). 440
1 The potential risk of tree regeneration failure in species-rich Taba 2 Penanjung lowland rain forest, Bengkulu, Indonesia
3 AGUS SUSATYA 4 Department of Foresty, University of Bengkulu, Indonesia. Jl. WR Supratman, Bengkulu, Indonesia. Email: [email protected] 5 6 Abstract. Tropical lowland rain forest is recognized by its high species richness with very few trees per species. It is also known for 7 having tendency to out crossing of its species with different floral sexualities, which requires the synchronization between flowering of 8 its trees and the presence of pollinators. Such ecological attributes raise possible constraints for the forest trees to regenerate. The 9 objective of the study was to assess the potential risk of failed regeneration for each tree species of the forest. Each of species with dbh 10 of more than 5 cm in a one-ha plot was collected, identified, and its ecological criteria, including rarity, floral sexuality, seed size, and 11 flowering phenology were determined. The potential risk of the failure of regeneration was calculated by summing all scores from 12 Analytical Hierarchical Process of the criteria. The results indicated that the forest consisted of 118 species belonging to 69 genera and 13 37 families. Rare species accounted to 52.10% of the total species. Of the 118 species, the potential medium risk category contributed 14 to 38.14 %, and more than 33% were grouped into very high and high risk or were more prone to failed regeneration in the future. All 15 rare dioecious species were categorized into very high and high risks. Only 21 species (17.79%) are listed in 2017’s IUCN red list. 16 Among unevaluated species, 22 and 13 species were respectively included in very high and high potential risk categories. The results 17 revealed more detailed potential risk of failed regeneration of tree species, and can serve as basic information to develop proper 18 conservation management.
19 Keywords: Bengkulu, dioecy, hermaphrodite, phenology, rarity, rain forest, risk regeneration.
20 Running title: Risk of tree regeneration failure in tropical forest
21 INTRODUCTION
22 Tropical rain forests and their intangible functions are getting more important in recent years due to their vital roles in 23 providing life-support and ecological services such as carbon sequestration, water provision, and prevention of global 24 warming and its negative effects. However, their existences are constantly being threatened by economic as well as 25 human population pressures. Indonesian lowland rain forests especially in Sumatra and Kalimantan Islands, have been 26 undergoing rapid deforestration and degradation as the results of conversions into mainly oil palm plantations as well as 27 into industrial plantation forests which have simpler stand structure. In addition to those external factors, the forests 28 inherently have their own ecological attributes that potentially constrain their abilities to regenerate. In species-rich 29 tropical rain forests, each of their tree species generally consists of very few individual trees (Whitmore 1983; Sakai et al. 30 1999; Sakai 2001). 31 Susatya (2007, 2010) studying three different tropical rain forests discovered the similarity of their structural patterns, 32 namely, they were composed of many species, but with very few individual trees. The very low density of tree species 33 appears to be more prevalent to the climax tree species than the pioneer ones (Susatya 2010). Furthermore, unlike pioneer 34 species that have good capabilities to explore wide ecological ranges, the climax tree species have been known to adapt to 35 more limited ecological ranges as well as more stable environments, and have difficulty to grow under warmer and drier 36 environments (Whitmore 1983). Therefore, rapid environmental changes induced by both climate change and forest 37 degradation will pose constraints for climax tree species to regenerate. Moreover, according to floral sexuality, Ng (1983) 38 shows that dioecy is common among tropical tree species, which requires at least two different individual trees to perform 39 sexual regeneration. 40 In the tropical forest, even hermaphrodite species tend to be not self compatible, and consequently have to do out 41 crossing (Bawa et al.1985). Both phenomena require flower synchronization among trees of the same species in order that 42 pollination process can occur. Even if this takes place, then pollination process is still difficult, because different 43 flowering trees can be distant from each other (Whitmore 1983). In the tropical rain forest of Malaysia Peninsular, for 44 example, it requires 32 ha to find two trees of the same species (Poore 1968). Therefore tropical trees must adapt to the 45 rapid environmental alterations; otherwise, they may be threatened by those changes and may face difficulties in 46 regeneration because of their own reproductive biology. The focus of the study was to determine the potential risk of failed 47 regeneration of tree species based on their floral sexualities, tree density, flowering patterns, and seed sizes. 48 MATERIALS AND METHODS
49 The research site was located at Bukit Daun Protected Forest Area. This lowland rain forest was well protected and 50 minor illegal logging in the form of cutting small pole (< 10 cm dbh) for social purposes infrequently occurred. Records at 51 Talang Pauh climate station showed that in the last decade, Taba Penanjung area received the annual rain fall around 52 2848 mm, with no monthly rainfall less than 100 mm. November, December, and January respectively received, 533, 53 420, 304 mm rainfall, higher than that of the other months. August was known to receive the lowest monthly rainfall (BPS 54 Kab. Bengkulu Tengah 2012). Unusual low monthly rainfall occurred in 1991 and 1994, when September and October got 55 only 3 mm. The monthly relative humidity was 83%, and reached as high as 87.7%, but dropped as low as 75.96%. The 56 average of monthly temperature was 26.2 0C, and reached its respective maximum and minimum at 29 0C in August, and 57 23 0C in October (Susatya 2007). Basic floristic data were collected from a one-hectar plot in 2015. All trees with dbh of 58 > 5 cm were tagged, their diameters measured, and their herbarium specimens collected. Species identification was carried 59 out in the Herbarium of Universitas Bengkulu (HUB). Species nomenclature followed Turner (1995). In the case of the 60 absence of tree’s reproductive aspects such as floral sexuality, flowering phenology, and seed size for each species, I 61 relied on the available secondary information including Plant Resources of South East Asia (PROSEA) No 5.(1) Timber 62 trees: Major commercial timbers (Soerianegara and Lemmens 1994), PROSEA No 5 (2) Timber trees: Minor commercial 63 timbers (Lemmens et al. 1995), PROSEA No 5 (3): Timber trees: Lesser-known species. (Sosef et al. 1998), and Plants of 64 Southeast Asia (www.asianplant.net) to collect those data. 65 To determine the potential risk of failed regeneration (PRR), I applied Analytic Hierarchy Process (AHP) developed 66 by Saaty (1980), and adopted a similar approach from Oktariadi (2009), who used AHP to develop the risk ranking of 67 tsunami in Southern Java. The method of AHP was selected because PRR was calculated by summing the score of 68 different criteria or biological aspects such as density, floral sexuality, flowering phenology, and seed size. AHP is widely 69 used for selecting alternatives from different criteria in different hiearchies. AHP tranforms qualitative data into the 70 quantitative ones through pairwise comparisons by experts (Saaty, 1980). Each comparison was conducted to assign a 71 value between two criteria according to their relative importances (Table 1) . 72 For the purpose of the study, two hiearchies were established. The first hiearchy consisted of main criteria such as 73 species sexuality (Si), flowering phenology (Pi), seed size (Zi), and rarity (Ri) or the number of individual trees per 74 species per ha. Meanwhile, the second hierarchy was subcriteria within sexuality, phenology, seed size, and rarity. 75 Subcriteria of floral sexuality (Sj) included hermaphrodite (S1), monoecious (S2), dioecious (S3), while subcriteria of the 76 flowering phenology ( P j ) consisted of once (P1), twice (P2), throughout year (P3), and supra annual (P4). We defined 77 supra annual category as tree species that performs flowering every more than 1 year, while throughout year was tree 78 species that flowers more or less continuously within a year. The subcriteria of seed size (Z j ) was categorized and 79 developed following Chacon et al. (1998). It consisted of very small (0-4 mm), small (4-8 mm), medium (8-12 mm), 80 large (12-16 mm), and very large (> 16 mm), and was respectively coded as Z1, Z2, Z3, Z4, and Z5 . Subcriteria of the 81 rarity (R j ) consisted of R1, R2, R3, R4, R5, R6, and R7, which was defined by species with 1, 2, 3, 4, 5-6, > 7 trees per ha, 82 respectively. Three senior ecologists within the Department of Forestry, University of Bengkulu were selected as experts 83 to carry out pairwise comparisons between two criteria or subcriteria. The results of pairwise comparisons were used to 84 construct the matrix of the value judgements, which was further analyzed to find the matrix of the priority rank 85 (eigenvalue). Each eigenvalue of criteria or subcritearia reflected the score of their relative importances in determining 86 the potential risk of failed regeneration. 87 At each hierachy level, the consistencies of all scores were checked by comparing their calculated consistency ratios 88 with Saaty’s consistency ratio table. If there were inconsistencies in their judgements, all proseses of pairwise comparison 89 and analysis were repeated (Saaty 1980, Saaty 2008). Potential risk of failed regeneration, then, was calculated by 90 summing the score of criteria and subcriteria of each species i (Si Sj + P i Pj + Z i Zj +R i Rj) x 100. Five categories of the 91 potential risks consisting of very high, high, medium, low, and very low were developed. A species was included in either 92 very high, high, medium, low or very low risks, if it had respectively a total score of PRR between 30.93-36.44, 25.42- 93 30.93, 19.91-25.42, 14.41-19.92, and 8.89-14.40. Potential risk was developed to indicate the relative sensitivity of a 94 species to regeneration failure. It was aimed to extend the interpretation of species threats and the modifications of the 95 systems in determining extinction risk in IUCN at local level. A species with very high risk category implies that over the 96 time, this species is expected to be more sensitive to the regeneration failure than those in lower risk categories. Any 97 species with very high and high risks will have respectively very high and high probability of regeneration failure in the 98 near future. 99 100 101 102 103 104 105 106
107 Table 1: Assigned values of pair-wise comparisons 108 Assigned Definition Explanation judgment value 1 Equally important Two criteria or subcriteria are equally important to influence the potential risk of regeneration failure. 3 Moderately more important One criterion or subcriterion is moderately more important to influence the potential risk of regeneration failure. 5 Much more important One criterion or subcriterion is much more important to influence the potential risk of regeneration failure. 7 Very much more important One criterion or subcriterion is very more important to influence the potential risk of regeneration failure. 9 Extremly more important One criterion or subcriterion is extremely more important to influence the potential risk of regeneration failure. 2,4,6,8 Intermediate judment value values between two consecutive judgments 109
110 RESULTS AND DISCUSSION
111 Taba Penanjung lowland rain forest consisted of 118 species belonging to 69 genera and 37 families (Supplement). 112 The forest structure was composed mostly of species with a single tree per ha that contributed to 60 species or 50.85 % of 113 the total species (Figure. 1a). Only four species, namely Microcos laurifolia, Croton argyratus, Elateriospernum tapos, 114 and Endospermum diadenum, had more than 10 trees/ha. Elateriospernum tapos (Euphorbiaceae) had the highest density 115 per ha with 31 trees. Following to Ng’s category (1978) on species rarity, who defined that any species with a single tree 116 is categorized as rare species, then the forest structure is unproportionally composed of rare species. This rarity was also 117 shown at both genus and family levels in that 8 families or 21.62 % of the total families and 20 genera or 28.98 % of the 118 total were respectively represented by a single tree. Therefore, any loss of an individual tree of the rare species can result 119 in the loss of species, genus, and family. The unproportional number of rare species composing forest structure appears 120 to be common in Bengkulu such as in Tambang Sawah lower montane forest of Kerinci-Seblat National Park (Susatya 121 2010), and Talang Tais secondary lowland rain forest (Susatya 2007). Euphorbiaeae was the most diverse family with 11 122 genera and 23 species, followed subsequently by Moraceae with 3 genera and 13 species, and Meliaceae with 3 genera 123 and 10 species. It seems that the abundant species of Euphorbiaceae is one of the characters of the floristic composition 124 of Sumatra lowland forest. This is also observed elsewhere in West Sumatra (Hadi et al. 2009, Kohyama et al. 1989). 125 Interestingly, the rare species was also common among the most diverse families. Among 23 species of Euphorbiaceae, 126 11 species (47.82 %) were rare species. Meanwhile the families of Moraceae and Meliaceae respectively had 33.33% and 127 40 % of their species categorized as rare. Species characterized by very few individual trees per ha potentially faces more 128 difficulty to maintain its population. 129 130
70 60 60 Number of species 50.85 50 % of the total species 40 (a) 30 18 16 20 15.25 13 13.56 11.02 7 5.93 10 4 3.39 0 1 2 3 4 5--6 >7 Tree /ha 60 49 50 41.53 39 40 33.05 30 (b) 30 25.42 20 10 0 Hermaphrodite Dioecious Monoecious
60 54
50 45.38 41 (c) 40 34.45
30
20 12 10.08 11 9.24 10
0 Once Twice Throughout Supra annual Figure 1: The structure of Taba Penanjung lowland rain forest according to tree density (a), floral sexuality (b) and flower phenology (c) of 131 its species. 132 133 134 According to floral sexuality, hermaphrodite species were the most prevalent, contributing to 41.53 % of the total 135 species (49 species). Meanwhile, monoecious and dioecious species respectively consisted of 33.05 % (39 species), and 136 25.42% ( 30 species) (Figure 1b). Monoecious and dioecious species generally account to 4% and 6 % respectively, but 137 the later appears to be more prevalent in the tropics than in temperate regions (Renner 2014). The number of monoecious 138 and dioecious species of Taba Penanjung lowland rain forest was higher than that of Costa Rica wet premontana forest 139 (Breanne 2017) as well as of Central Kalimantan, Indonesia (Brearley et al 2007). Monoecious and dioecious species of 140 Costa Rica premontana respectively account to 13.10 % and 13.70 % (Breanne 2017), while the similar categories of 141 Central Kalimantan respectively contribute to 14.70% and 23.49 % of the total species (Brearley et al. 2007). Special to 142 dioecious species, its number appears to be more similar than those found at both Sarawak (Ashton 1969) and Pasoh 143 forests (Kochummen et al. 1991). Dioecious species at both sites respectively account to 26 % and 28 %. The number 144 of monoecieous and dioecious species of the site altogether accounted up to 58,47 % of the total species (69 species). 145 This shows that more than half of the total species have to perform out crossing in order that pollination can occur. Such 146 a process requires both the synchronization of flowering phenology and the presence of pollinators, which could lead to 147 uncertainty on seed production and tree regeneration. The uncertainty is even greater because the sex ratio of dioecious 148 species is male favoured (Queenborough et al 2009; Gao et al 2012) , and male flowers bloom earlier than their female 149 opposites at certain species (Queenborough et al 2013). 150 With regard to tree regeneration, dioecious species have advantages because they tend to yield large seeds, containing 151 more energy (Varmosi et al. 2008), which increase the probability of seedling survivorship. However, dioecious species 152 also face the difficult regeneration, because they have only half of their adult trees to produce seeds (Renner 2014). 153 Dioecious tree species also tend to generate high seed density around their female parent trees, which further lead to high 154 seed predation. It is speculated that the more distant the individual dioecious trees grow from their female parent trees, the 155 higher probability of their seed survivorships and the better seedling recruitment they have due to predation avoidance 156 (Abebbe 2008). 157 Taba Penanjung lowland rain forest has diverse tree species based on flowering phenology. According to flowering 158 phenology, the majority of species of Taba Penanjung rain forest perform either throughout or once flowering phenology 159 (Fig 1c). Flowering phenology shows the incidence of reproductive efforts of the species, which reflects and will
160 determine the probability of the reproductive success. The throughout flowering species has relatively higher probability 161 to ensure seed production and tree regeneration in the future than the supra annual category, simply because the former 162 produces more frequent flowers and fruit than the later, which only produces flower and fruit once for every two to five 163 years. Flowering phenology is an important factor in tree regeneration, because the length, timing of flowering and 164 fruiting coupled with seasons will determine seed production, seedling mortality, establishment and growth (Augspurger 165 1981). Furthermore, the role of environments becomes a pivot point in tree regeneration because the flowering phenology 166 shows a strong correlation with climate, rainfall and humidity, drought and temperature (Kushwaha et al 2011; 167 Sulistyawati et al. 2012). Species with throughout flowering contributed to 45.38 % of the total species (54 species), 168 while those with once flowering a year accounted to 34.45 % (41 species). The number of species with twice a year and 169 supra annual flowering patterns was not as many as both throughout and once flowering phenologies. Both patterns 170 respectively accounted to 10.08 % (13 species) and 9.14 % (11 species). The number of species with supra annual 171 flowering in the site was much lower than that of Central Kalimantan (Brearley et al. 2007), and of Lambir hill of 172 Sarawak (Sakai et al. 1999). The supra annual flowering species at those two last sites respectively account to 75 %, and 173 54 %. Both forests are dominated by species of Dipterocarpaceae (Brearley et al. 2007; Sakai et al. 1999), which are 174 well known to perform mass flowering or supra annual flowering (Whitmore 1983). Meanwhile, Taba Penanjung rain 175 forest is dominated by species of Euphorbiacae and Moraceae, which are recorded to have throughout flowering patterns 176 (Whitmore 1983). 177 Most of species falled into medium risk category, contributing to 38.14 % of the total species. Species with this 178 medium risk indicate that they do not face an immediate risk which may further threaten their regeneration. Other 179 categories namely very high, low, and high risks had almost similar values, ranging from 19.49 %, 18.64%, to 17.80 %. 180 (Figure 2) Both very high and high risk categories altogether accounted to 37.29 %, indicating that more than one third of 181 the species will face more serious threat to their tree regenerations in the near future. 182 183
184 185 186 Figure 2: The potential risk of regeneration failure of trees of Taba Penanjung lowland rain forest. 187 188 189 190 Twenty three species (Fig. 2) from five families were included in very high risk category, consisting of species from 191 Euphorbiaceae, Myristicaceae, Lauraceae, Flaucourticaeae, Moraceae, and Rubiaceae. Each of these families respectively 192 contributed to 52.17 % (12 species), 21.74 % (5 species), 13.04 % (3 species), and 4.3% (1 species). Of these families, all 193 species of Myristicaeae, namely Knema globularia, Knema glauca, Horsfieldia polyspherula, Horsfieldia costulata, and 194 Gymnacranthera forbesii, were included in this category. The very high risk category was dominated by dioecious species 195 (22 of 23 species). The only monoecious included in this category was Artocarpus kemando (Moraceae). Artocarpus 196 kemando was characterized by a single tree per species per ha, large seed category, and supra annual flowering. The 197 combination of these biological characters makes this species have very high risk. A note of this species is that the 198 incident of supra annual flowering is relatively longer that of the other supra annual flowering species. It has been 199 recorded to not produce flowers within 7 years (Sosef et al. 1998). The very high risk category consisted not only of 200 species with a single tree; in fact, 7 of them had more than one tree per ha, namely Aporosa accuminatisima (2), 201 Actinodaphne peduncularis (2 trees), Drypetes longifolia (2 trees), Hydnocarpus curtisi (3 trees), Horsfieldia costulata (2 202 trees), and Knema globularia (3 trees). All of these species have similar characters such as dioecious and extra large 203 seeds, with various flowering phenology. Among these species, Aporosa accuminatisima and Actinodaphne peduncularis 204 are recorded to have ecological disadvantages, where the former has been reported for its low regeneration, and the later 205 has been known for its restricted distribution (Sosef et al. 1998). It appears that the extra large seed category, and the 206 species density of more than one tree per ha will put the dioecious species into very high risk regardless of their flowering
207 phenologies. The extra large-size seed is generally recalcitrant, which has very fast germination, low capability of 208 dormancy, and high sensitivity to drought (Marcos-Filho 2005). Water content within seeds of this type determines 209 germination success, and varies according to species and habitat quality. For example the seed of Shorea roxburghii, 210 which has habitat with low rainfall, is tolerant to low water content and still be able to germinate when the water content 211 reaches as low as 35 %. Meanwhile, the seeds of other species such as S. almon, and S. robusta can not germinate when 212 the water content is less than 40 %. Recalcitrant seeds generally are not able to germinate if the water content reaches as 213 low as 20%-30% (Davies & Ashton 1999). This is the reason why the species with large seeds prefer to grow and become 214 common in the moist condition under canopy trees, but hardly survive in open canopy, or a dry, warm, and disturbed 215 habitat. 216 Davies & Ashton (1999) raise the issues on the disadvantages for large-seed species. A large seed tends to have lower 217 fecundity and can hardly thrive at a forest gap habitat. On the other hand, a large seed has the advantages of having 218 more energy reserved in its cotyledon. In a good-quality environment, the large seed germinates and grows rapidly, and 219 has high seedling survivorship due to the large energy stored in cotyledon (Arunachalam et al. 2003). On the contrary, 220 the small-size seed size is generally more tolerant to decreasing water contents (Chin et al. 1989). Small-size seeds are 221 categorized as orthodox which generally tolerate drought, and are well known to have long dormancy. Therefore, species 222 with small seeds are able to wait until suitable environments become avaiable for their germination. The presence of gap 223 generating more light intensity, drier and less moist conditions triggers small seeds to germinate and dominate the open 224 habitat (Marcos-Filho 2005). Furthermore, a small seed has many ecological advantages of having wider dispersal, being 225 able to select suitable microclimates, and having high fecundity (Davies & Ashton 1999). 226 The majority of the very high risk category had throughout flowering (12 species), followed by once flowering 227 phenology type (6), while supra annual flowering only consisted of 3 species. This flowering phenology variation shows 228 that the phenology does not determine the very high risk category. Furthermore, the very high risk comprised 8 and 7 229 species respectively characterized by extra large and small seed categories. Similar to the phenology, seed size does not 230 determine the very high risk category either. Therefore, in general, if a species is dioecious and rare, then the species is 231 likely to belong to very high category regardless of seed size and flowering phenology. Dioecious species generally fall 232 into very high risk category, because of the complexity of reproduction biology. To carry out reproduction efforts, they 233 require flowering synchronization and the presence of pollinators. Dioecious species also show more limited reproduction 234 capacity than those having other flower sexuality types, simply because they have only half of their mature trees 235 contributing to seed production. Their flowering and fruiting successes are also influenced by both the distance between 236 male and female trees and the pollinator movement from male to female trees (Renner 2014). During pollination process, 237 pollinators travel a certain distance which further add up to the uncertainty of fruit production. The farther the distance 238 between mature male and female trees, the more uncertain pollination process to occur. It was estimated that the closest 239 distance between the same tree species could reach up to 131 m, and the distance between female and male trees could be 240 even farther (Abebbe, 2008). The difficulty of the regeneration of dioecious species is even greater due to the fact that the 241 microclimates beneath male mature trees play a determining role in regeneration. It has been known that seedling and 242 sapling recruitments tend to be greater under the male trees than the female trees (Arai & Kamitani 2005) 243 A rare species is expected to face the regeneration problem due to its difficulty to maintain its population density. A 244 rare or single-tree per ha species is more likely to experience failed regeneration simply because it statistically has a lower 245 chance to regenerate than those of more than one tree per ha. Forest structure dominated by species having very few 246 individual trees appears a common ecological attribute of species-rich Southeast Asia rainforest (Susatya 2010) and 247 Nigerian rain forest (Adekunle et al. 2013). From the forest tree regeneration perspective, this attribute has been worsened 248 by the fact that even hermaphrodite species tends to be not self compatible (Bawa 1979; Bawa et al. 1989). However, in 249 this research, a species with a single tree alone do not necessarily determine whether the species belongs to either very 250 high or high risk categories. In fact, 55 % of the total of rare species are classified into either medium risk (27 species) or 251 low risk (5 species) category. Only rare species with either dioecy or monoecy are most likely to belong to either very 252 high or high risk category. Rare species with high and very high risk categories accounted up to 12 species and 16 species, 253 respectively. Moreover, rare hermaphrodite species will fall into medium risk category regardless of seed size and 254 flowering phenology. However, rare hermaphrodite species with both small seed category and throughout phenology such 255 as Bhesa paniculata (Celastraceae), Astronia macrophylla (Melastomaceae), Neolamarckia cadamba (Rubiaceae), 256 Micromelum minutum (Rutaceae), and Rinorea anguifera (Violaceae) were included in low risk category. These 257 combined criteria make these five species have better reproductive success as well as better seedling survivorship than the 258 monoecious and dioecious species. This pattern shows that being dioecious or monoecious is more influential in 259 determining very high and high risks than being rare species. As long as a rare species does not belong to dioecious and 260 monoecious categories, it will not be included in either very high or high risk category. 261 The high risk category was composed of 21 species of 10 families (Fig 2), of which family of Meliaceae contributed 262 most with 7 species, while the other nine families only contributed from one to four species. High risk category comprised 263 various species with all types of the flower sexuality. Monoecious species contributed most with 13 species (61.90 %), 264 followed by diocious species (6 species). Meanwhile, hermaphrodite species only accounted to 2 species. Interestingly, 265 of the 48 hermaphrodite species generally belonging to either medium or very low risk, two were included in high risk 266 category, namely Shorea ovalis and Palaquium hexandrum, both of which are characterized by extra large seed and supra
267 annual flowering phenology. The combination of extra large seed and less frequent incidence of flowering and fruiting 268 makes those two species classified into high risk category. In addition to these biological aspects, an external factor in the 269 form of timber harvesting becomes an eminent threat to these two species. The population of Shorea ovalis, the member 270 of commercial light Red Meranti group, is also dwindling due to logging (Soerianegara & Lemmens 1994). Like other 271 species of Palaquium, Palaquium hexandrum faces a reproductive problem, because its flowers hardly reach maturity due 272 to insect predation. If they pass through fruit development, then their fruit suffer high predation by bats, birds, and 273 squirrels (Soerianegara & Lemmens 1994). Furthermore, a special attention has to be made for a rare species of 274 Diospyros sumatrana which has been classified into high risk category. The species appears to face fruit development 275 problem, because it needs long period of time to reach fruit ripening (Lemmens et al. 1995). Such a long period could 276 result in being more vulnerable to fruit predation, which could further lead to lower its regeneration capability. 277 Not all of the monoecious species fall into a single category. Most of the monoecious species falled into medium risk 278 (18 species), subsequently followed by high risk (13 species), low risk (6 species), and very high and very lows risk 279 categories which respectively consisted of only 1 species. Monoecious species with one to two trees per ha, large and 280 extra large seed categories, and once flowering pattern will fall into high risk category. Meanwhile similar monoecious 281 species with very small seed and throughout phenology (12 species) will belong to medium risks category. Interestingly, 282 monoecious species with 3-4 trees but with once and supra annual flower will also belong to medium risk category 283 regardless of seed size. It appears that whether a monoecious species will fall into a certain category is not solely defined 284 by its rareness, but also by the seed size and flowering phenology. 285 Species belonging to medium risk category should not face immediate threats for their regeneration. However, timber 286 harvesting will potentially jeopardize their future. Among the medium risk category (45 species), 26.27 % (12 species) 287 are either included into major or minor commercial timbers (Soerianegara & Lemmens 1994; Lemmens et al. 1995). This 288 indicates that these species are likely to become a target for logging in the near future. In addition to a timber harvesting 289 factor, their ecological attributes could potentially increase the risks of several medium risk species. For example, the tree 290 population of Alstonia angustiloba has been locally depleted due to logging (Soerianegara & Lemmens 1994), while 291 Baccaurea racemosa has been recorded as uncommon species at the lower strata of the Southeast Asia rain forest ( Sosef 292 et al. 1998). Furthermore, Endospernum diadenum faces a high predation of its seeds, and is known to have low seed 293 viability (Soerianegara & Lemmens 1994). Three species of Polyalthia, P. hookeriana, P. michaelii, and P. rumphii are 294 noted to have scattered distribution, and their seedlings are sensitive to drought (Sosef et al. 1998). 295 The hermaphrodite species were included in various categories from medium to very low risk. Rare hermaphrodite 296 species are likely to fall into medium risk, if they have medium to extra large seeds, regardless of their flowering 297 phenologies. However, rare hermaphrodite species with small to very small seed categories and throughout flowering 298 pattern will fall into low risks. Furthermore, hermaphrodite species with more than one tree are most likely to belong to 299 low and very low risk categories. Hermaphrodite species with more than 4 trees will come up into two different categories 300 depending on their seed sizes. Those with small and medium sizes will end up to very low risk category, while those with 301 large and extra large seeds will fall into low category. The former consists of Shorea platyclados, Barringtonia 302 lanceolata, and Syzygium rostrata, while the later are Geunsia hexandra, Dillenia excelsa, Strombosia javanica, 303 Neonauclea gigantea, Microcos laurifolia, Euonymus javanicus, and Cratoxylum sumatrana. 304 Of the 118 tree species, only 21 species (17.79%) are listed in 2017’s IUCN red list. The other species are listed as not 305 assessed species, meaning the conservation statutes of these species have not been evaluated according to IUCN’s criteria. 306 The tree species listed at IUCN consists of 2, 1, 3, and 15 tree species respectively categorized into endangered (E), 307 Vulnerable (V), near threatened (NT), and least concerned (LC). Furthermore, of the 23 species with very high risk 308 category, only three tree species, namely Litsea spathacea, Knema glauca, K. globularia have been included into least 309 concerned. Of the 21 species with high risk category, seven are categorized into four different IUCN’s conservation status. 310 Two species, namely Aglaia speciosa and Sterculia oblongata, are classified as endangered, while Sterculia parvifolia is 311 included as vulnerable. Furthermore, three species of Meliaceae, namely Aglaia odoratissima, A. oligophylla, and A. 312 rubiginosa, are grouped into near threatened. Species of Knema glauca, K. globularia, Litsea spathacea, Aglaia 313 tomentosa, Sterculia parviflora, Archidendron ellipticum, Magnolia sumatrana, Microcos laurifolia, Alstonia angustiloba, 314 Bhesa paniculata, Euonymus javanicus, Payena maingayi, P. lanceolata, Polyalthia hookeriana, and Prunus arborea, are 315 categorized as the least concerned species. Comparing the IUCN redlist and the results of the potential risk analysis 316 resulted in interesting outcomes. Among the 15 species listed as least concerned by IUCN, nine are classified into 317 medium to low risk catagories, which is almost similar to least concerned category, while the other six species, namely 318 Knema glauca, K. globularia Aglaia tomentosa, Archidendron ellipticum, Litsea spathacea, and Sterculia obolongata are 319 either included in high risk or very high risk category. The first two were very high risk species characterized by dioecious 320 species with supra annual flowering phenology, while the rest were high risk monoecious species with large seed category. 321 Sterculia oblongata, vulnerable species by IUCN, was classified into high risk. Both seem to be comparable status, where 322 both indicate that in the near future, the species will face difficulty to maintain its population density in order to avoid local 323 extinction. Interestingly, Shorea platiclados that has long been classified as endangered species (Ashton 1998), did fall 324 into low risk. Low risk category of this species indicates that it relatively does not face immediate threat on its tree 325 regeneration locally, and is considered to be able to ensure its future regeneration. The number of tree per ha (4 trees) 326 becomed the main reason for the species to be classified as low risk category. Moreover, among the 97 species whose
327 conservation statuses have not been evaluated by IUCN, 22 and 13 were respectively included in very high and high 328 potential risk categories. 329 The conservastion statuses of most of the very high and high risk tree species have not been evaluated according to 330 IUCN’s criteria. IUCN is aware that there is a need for more detailed evaluation for conservation status at local level 331 because differences between global and local threats are very important for determining the status. It further indicates that 332 a species which has been globally categorized into endangered could be the least concerned category due to steady 333 population at a local level. On the other hand, species with least concern status can turn into endangered category due to 334 its small and locally dwindling population (IUCN 2012). The results of this research make more detailed ecological 335 information concerning the potential risk of the failure of tree regeneration available, which is not always provided by 336 IUCN red list documents. The results are very important to serve as both substitutes and guidances at local level for 337 conservation purposes in the absence of conservation status of IUCN of the tree species.
338 ACKNOWLEDGEMENTS
339 The author is indebted to members of WARISAN, who helped in the field works, and also grateful to Astri W. Utami, 340 Sequoia MS Rhomadhon, and Magnolia GR. Satriorini, who supported logistics during the field work.
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423 Table S1 (Supplement): Tree species of Taba Penanjung Lowland Rain forest and their potential risks of the regeneration failure 424 No Species Family Rarity Floral sexuality Seed size Flowering phenology Total Score PRR tree/ha Score Type Score Type Score type Score 1 Actinodaphne peduncularis L Lauraceae 2 0.238 Dio 0.581 Exl 0.3260 Onc 0.281 34.1826 VH 2 Aglaia affinis Merr Meliaceae 2 0.238 Mon 0.309 Med 0.1770 Onc 0.281 25.6374 H 3 Aglaia faveolata Pannell Meliaceae 1 0.286 Mon 0.309 Med 0.1770 Onc 0.281 27.8982 H 4 Aglaia odoratissima Blume Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H 5 Aglaia oligophylla Miq Meliaceae 3 0.19 Mon 0.309 Exl 0.3260 Onc 0.281 24.9858 M 6 Aglaia rubiginosa (Hiern.) Pannell1 Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H 7 Aglaia speciosa Blume Meliaceae 2 0.238 Mon 0.309 Lrg 0.2960 Onc 0.281 26.9226 H 8 Aglaia tomentosa Teijm ex Binn Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H 9 Alstonia angustiloba Miq. Apocynaceae 1 0.286 Hmp 0.11 Vsm 0.087 San 0.412 24.0132 M 10 Antidesma brachybotrys Airy Shaw Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 11 Antidesma griffithii Hoof. F Euphorbiaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH 12 Antidesma leucocladon Hook.f Euphorbiaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH 13 Antidesma montanum Blume Euphorbiaceae 2 0.238 Dio 0.581 Vsm 0.087 Thr 0.116 28.8789 H 14 Antidesma velutinosum Blume Euphorbiaceae 3 0.19 Dio 0.581 Sml 0.114 Thr 0.116 26.9097 H 15 Aporosa accuminatisima Merr Euphorbiaceae 2 0.238 Dio 0.581 Sml 0.114 Onc 0.281 31.8930 VH 16 Archidendron ellipticum (Blume) Nielsen Leguminosae 1 0.286 Mon 0.309 Exl 0.3260 Thr 0.116 26.7849 H 17 Artocarpus anisophyllus Miq. Moraceae 4 0.143 Mon 0.309 Lrg 0.2960 San 0.412 24.6096 M 18 Artocarpus elasticus Reinw. ex Blume Moraceae 4 0.143 Mon 0.309 Exl 0.3260 Onc 0.281 22.7721 M 19 Artocarpus kemando Miq Moraceae 1 0.286 Mon 0.309 Lrg 0.2960 San 0.412 31.3449 VH 20 Astronia macrophylla Blume Melastomaceae 1 0.286 Hmp 0.11 Sml 0.114 Thr 0.116 19.4208 L 21 Baccaurea bracteata Mull. Arg Euphorbiaceae 1 0.286 Dio 0.581 Med 0.1770 Thr 0.116 32.1117 VH 22 Baccaurea edulis Merr Euphorbiaceae 1 0.286 Dio 0.581 Exl 0.3260 Onc 0.281 36.4434 VH 23 Baccaurea racemosa (Reinw. ex Blume) Mull. Arg. Euphorbiaceae 6 0.095 Dio 0.581 Lrg 0.2960 Thr 0.116 24.4008 M 24 Baccaurea sumatrana (Miq.) Mull. Arg. Euphorbiaceae 3 0.19 Dio 0.581 Med 0.1770 Thr 0.116 27.5901 H 25 Barringtonia lanceolata (Ridl.) Payen Lecythidaceae 4 0.143 Hmp 0.11 Exl 0.3260 Thr 0.116 14.9751 L 26 Bhesa paniculata Arn Celastraceae 1 0.286 Hmp 0.11 Sml 0.114 Thr 0.116 19.4208 L 27 Bridelia insulana Hance Euphorbiaceae 3 0.19 Mon 0.309 Sml 0.114 Thr 0.116 19.9737 M 28 Campnosperma auriculatum (Blume) Hook.f Anarcadiaceae 1 0.286 Mon 0.309 Med 0.1770 Thr 0.116 25.1757 M 29 Casearia capitellata Blume Flacourtiaceae 1 0.286 Hmp 0.11 Exl 0.3260 Thr 0.116 21.7104 M 30 Casearia clarkei King var. kunstleri (King) Ridl. Flacourtiaceae 1 0.286 Hmp 0.11 Exl 0.3260 Thr 0.116 21.7104 M 31 Castanopsis inermis (Lindl.) Benth. ex Hook. F Faagaceae 4 0.143 Mon 0.309 Lrg 0.2960 Onc 0.281 22.4481 M 32 Chionanthus pluriflorus (Knob) Kew Oleaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Thr 0.116 19.1256 L 33 Chionanthus spicata Blume Oleaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M 34 Commersonia bartramia (L) Merr. Sterculiaceae 2 0.238 Mon 0.309 Sml 0.114 Thr 0.116 22.2345 M 35 Cratoxylum sumatrana (Jack.) Blume Hypericaceae 6 0.095 Hmp. 0.11 Sml 0.114 Onc 0.281 13.1472 VL 36 Croton argyratus Blume Euphorbiaceae 15 0.048 Mon 0.309 Med 0.1770 Thr 0.116 13.9659 VL 37 Dacryodes rugosa (Blume) H. J. Lam Burseraceae 3 0.19 Dio 0.581 Exl 0.3260 Thr 0.116 29.1993 H 38 Dillenia excelsa (Jack.) Gilg Dilleniaceae 6 0.095 Hmp 0.11 Sml 0.114 Onc 0.281 13.1472 VL 39 Diospyros sumatrana Miq Ebenaceae 1 0.286 Mon 0.309 Sml 0.114 Onc 0.281 27.2178 H 40 Drypetes longifolia (Blume) Pax ex. K. Hoffm Euphorbiaceae 2 0.238 Dio 0.581 Exl 0.3260 Onc 0.281 34.1826 VH 41 Durio zibethinus L Bombacaceae 1 0.286 Hmp 0.11 Exl 0.3260 Twi 0.191 22.9479 M 42 Dysoxylum arborescens (Blume) Miq Meliaceae 2 0.238 Mon 0.309 Exl 0.3260 Onc 0.281 27.2466 H 43 Dysoxylum densiflorum (Blume) Miq. Meliaceae 4 0.143 Mon 0.309 Sml 0.114 Onc 0.281 20.4825 M 44 Dysoxylum excelsum Blume Meliaceae 4 0.143 Mon 0.309 Exl 0.3260 Onc 0.281 22.7721 M 45 Elaeocarpus nitidus Jack Elaeocarpaceae 1 0.286 Hmp 0.11 Med 0.1770 Onc 0.281 22.8237 M 46 Elateriospernum tapos Blume Euphorbiaceae 31 0.048 Mon 0.309 Exl 0.3260 Thr 0.116 15.5751 L 47 Endospermum diadenum (Miq.) Airy Shaw Euphorbiaceae 12 0.048 Dio 0.581 Vsm 0.087 Thr 0.116 19.9299 M 48 Erismanthus obliquus Wall ex. Mull. Arg. Euphorbiaceae 1 0.286 Mon 0.309 Sml 0.114 Thr 0.116 24.4953 M 49 Euonymus javanicus Blume Celastraceae 3 0.19 Hmp. 0.11 Lrg 0.2960 Onc 0.281 19.5873 L 50 Ficus benjamina L Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M 51 Ficus depressa Blume Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M 52 Ficus fistulosa Reinw. ex. Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M 53 Ficus fulva Reinw. ex. Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M 54 Ficus heteropleura Blume Moraceae 3 0.19 Mon 0.309 Vsm 0.087 Thr 0.116 19.6821 L 55 Ficus lepicarpa Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M 56 Ficus ribes Reinw. ex Blume Moraceae 3 0.19 Mon 0.309 Vsm 0.087 Thr 0.116 19.6821 L 57 Ficus sundaica Blume Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M 58 Ficus variegata Blume Moraceae 4 0.143 Mon 0.309 Vsm 0.087 Thr 0.116 17.4684 L 59 Flacourtia rukam Zoll. et. Moritzi Flaucourtiaceae 3 0.19 Hmp 0.11 Sml 0.114 Onc 0.281 17.6217 L 60 Geunsia hexandra (Teijsm. et. Binn) Koord Verbenaceae 4 0.143 Hmp 0.11 Sml 0.114 Thr 0.116 12.6855 VL 61 Gironniera subaequalis Planch Ulmaceae 5 0.095 Mon 0.309 Sml 0.114 Thr 0.116 15.4992 L 62 Gordonia maingayi Dyer Theaceae 1 0.286 Hmp 0.11 Exl 0.3260 Twi 0.191 22.9479 M 63 Gordonia multinervis King Theaceae 3 0.19 Hmp 0.11 Exl 0.3260 Twi 0.191 18.4263 L 64 Gymnacranthera forbesii (King) Ward Myristicaceae 1 0.286 Dio 0.581 Exl 0.3260 Twi 0.191 34.9584 VH 65 Horsfieldia costulata Warb Myristicaceae 2 0.238 Dio 0.581 Exl 0.3260 Thr 0.116 31.4601 VH 66 Horsfieldia polyspherula (Hook. F) J. Sinclair Myristicaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH 67 Hydnocarpus curtisii King Flacourtiaceae 3 0.19 Dio 0.581 Exl 0.3260 Onc 0.281 31.9218 VH 68 Knema glauca (Blume) Petermann Myristicaceae 4 0.143 Dio 0.581 Exl 0.3260 San 0.412 31.8696 VH 69 Knema globularia ( Lam.) Warb. Myristicaceae 3 0.19 Dio 0.581 Exl 0.3260 San 0.412 34.0833 VH 70 Lansium domesticum Corra Sapindaceae 1 0.286 Mon 0.309 Exl 0.3260 Onc 0.281 29.5074 H 71 Litsea cubeba (Laur.) Pers Lauraceae 4 0.143 Dio 0.581 Lrg 0.2960 Onc 0.281 29.3841 H 72 Litsea sessilis Boerl. Lauraceae 1 0.286 Dio 0.581 Med 0.1770 Onc 0.281 34.8342 VH 73 Litsea spathacea Gamble Lauraceae 1 0.286 Dio 0.581 Med 0.1770 Onc 0.281 34.8342 VH 74 Macaranga hosei King ex Hook Euphorbiaceae 1 0.286 Dio 0.581 Vsm 0.087 Thr 0.116 31.1397 VH 75 Macaranga hulletii King ex Hook. F. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 76 Macaranga triloba (Blume) Mull. Arg. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 77 Magnolia uvariifolia Dandy ex Noot 2 Magnoliaceae 1 0.286 Hmp 0.11 Med 0.1770 Onc 0.281 22.8237 M 78 Mallatus leptophyllus Pax et C.K. Hoffm. Euphorbiaceae 2 0.238 Hmp 0.11 Vsm 0.087 Onc 0.281 19.5909 M 79 Mallotus auriculatus Merr Euphorbiaceae 3 0.19 Dio 0.581 Sml 0.114 Thr 0.116 26.9097 H 80 Mallotus montanus (Mull. Arg) Airy Shaw Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 81 Mallotus peltatus (Geisel.) Mull. Arg. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 82 Microcos laurifolia (Hook et Mast) Burret Tiliaceae 14 0.048 Hmp 0.11 Med 0.1770 Thr 0.116 8.8914 VL 83 Micromelum minutum (G. Forst.) Wright and Arn. Rutaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L 84 Naphelium lappaceum L Sapindaceae 1 0.286 Hmp 0.11 Exl 0.3260 Onc 0.281 24.4329 M 85 Neolamarckia cadamba (Roxb) Basser Rubiaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L 86 Neonauclea excelsa Merr Rubiaceae 1 0.286 Hmp 0.11 Med 0.1770 Thr 0.116 20.1012 M 87 Neonauclea gigantea Merr Rubiaceae 6 0.095 Hmp 0.11 Med 0.1770 Thr 0.116 11.1051 VL 88 Ochanostachys amentacea Mast Olacaceae 2 0.238 Mon 0.309 Lrg 0.2960 Thr 0.116 24.2001 M 89 Palaquium hexandrum (Griff.) Baill Sapotaceae 1 0.286 Hmp 0.11 Exl 0.3260 San. 0.412 26.5944 H 90 Payena lanceolata Ridl. Sapotaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M
91 Payena maingayi Clarke Sapotaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M 92 Pittosporum ferrugineum W.T. Aiton Pittosporaceae 3 0.19 Hmp 0.11 Vsm 0.087 Thr 0.116 14.6076 L 93 Polyalthia hookeriana King Annonaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Twi 0.191 22.6239 M 94 Polyalthia michaelii C.T. White Annonaceae 1 0.286 Hmp 0.11 Med 0.1770 Twi 0.191 21.3387 M 95 Polyalthia rumphii (Blume) Merr. Annonaceae 1 0.286 Hmp 0.11 Med 0.1770 Twi 0.191 21.3387 M 96 Pometia pinnata J.R. Forst et G. Frost Sapindaceae 1 0.286 Mon 0.309 Exl 0.3260 Onc 0.281 29.5074 H 97 Prainea limpato (Miq.) Beumee Moraceae 4 0.143 Mon 0.309 Vsm 0.087 Onc 0.281 20.1909 M 98 Prunus arborea (Blume) Kalkman Rosaceae 1 0.286 Hmp 0.11 Sml 0.114 Onc 0.281 22.1433 M 99 Prunus lamponga (Miq.) Kalkman Rosaceae 3 0.19 Hmp 0.11 Sml 0.114 Onc 0.281 17.6217 L 100 Quercus argentata Korth Fagaceae 7 0.048 Mon 0.309 Exl 0.3260 Onc 0.281 18.2976 L 101 Rhodamnia cinerea Jack Myrtaceae 1 0.286 Hmp 0.11 Med 0.1770 Thr 0.116 20.1012 M 102 Rinorea anguifera (Lour.) Kuntze Violaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L 103 Shorea ovalis (Korth.) Blume Dipterocarpaceae 1 0.286 Hmp 0.11 Exl 0.3260 San 0.412 26.5944 H 104 Shorea parvifolia Dyer Dipterocarpaceae 3 0.19 Hmp 0.11 Med 0.1770 San 0.412 20.4636 M 105 Shorea platyclados Slooten ex. Fox Dipterocarpaceae 4 0.143 Hmp 0.11 Lrg 0.2960 San 0.412 19.5351 L 106 Sterculia oblongata R. Br. Sterculiaceae 1 0.286 Mon 0.309 Sml 0.114 San 0.412 29.3793 H 107 Sterculia parviflora Roxb. ex. G. Don Sterculiaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H 108 Strombosia javanica Blume Olacaceae 6 0.095 Hmp 0.11 Med 0.1770 Onc 0.281 13.8276 VL 109 Symplocos crassipes C. B. Clarke Symplocaceae 2 0.238 Hmp 0.11 Sml 0.114 Twi 0.191 18.3975 L 110 Syzygium flosculiferum (M. R. Hensd.) Sreek Myrtaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Twi 0.191 20.3631 M 111 Syzygium kunstleri (King). Bahadur et R.C. Gour Myrtaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Twi 0.191 22.6239 M 112 Syzygium lineatum (DC) Merr. ex L. M. Terry Myrtaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Onc 0.281 24.1089 M 113 Syzygium politum (King). I.M. Turner Myrtaceae 1 0.286 Hmp 0.11 Sml 0.114 Twi 0.191 20.6583 M 114 Syzygium rostrata Blume Myrtaceae 4 0.143 Hmp 0.11 Lrg 0.2960 Twi 0.191 15.8886 L 115 Urophyllum macrophyllum Korth Rubiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH 116 Vitex vestita Wall. ex Schauer Verbenaceae 1 0.286 Hmp 0.11 Sml 0.114 Onc 0.281 22.1433 M 117 Xylopia caudata Maingay ex. Hook. F. et Thomson Annonaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Onc 0.281 21.8481 M 118 Xylopia elliptica Hook.f and Thomson Annonaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Onc 0.281 24.1089 M 425 Note : Floral sexuality code; Dioecious (Dio), Monoecious (Mon), Hermaphrodite (Hmp). Seed size code; Extra large (Exl), Large (Lrg), Medium (Med), Small (Sml), Very small (Vsm). 426 Flowering phenology code ; Once (Onc), Twice (Twi), Throughout (Thr), Supra annual (San). PRR refers to the potential risk of regeneration failure. PRR code: Very high risk (VH), High risk 427 (H), Medium risk (M),Low risk (L), and Very low (VL). 428 429
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https://mail.google.com/mail/u/0/?tab=rm&ogbl#search/unsjournals%40gmail.com/FMfcgxvzKbNpsmvFNPCcgMswMwccCWhS 1/1 BIODIVERSITAS ISSN: 1412-033X Volume 19, Number 5, September 2018 E-ISSN: 2085-4722 Pages: xxxx DOI: 10.13057/biodiv/d1905xx
The potential risk of tree regeneration failure in species-rich Taba Comment [a1]: Need a map Penanjung lowland rainforest, Bengkulu, Indonesia Comment [u2]: I PUT IT AT THE AFTER REFERENCE, MARKED As. Figure 1. PLEASE AGUS SUSATYA REARRANGE IN THE MAIN ARTICLE Department of Forestry, Faculty of Agriculture, Universitas Bengkulu. Jl. WR Supratman, Kota Bengkulu 38371A, Bengkulu, Indonesia. Tel./fax. +62- 736-21170, email: [email protected]
Manuscript received: 28 May 2018. Revision accepted: xxx September 2018.
Abstract. Susatya A. 2018. The potential risk of tree regeneration failure in species-rich Taba Penanjung lowland rainforest, Bengkulu, Indonesia. Biodiversitas 19: xxxx. Tropical lowland rain forest is recognized by its high species richness with very few trees per species. It is also known for having tendency to outcrossing of its species with different floral sexualities, which requires the synchronization between flowering of its trees and the presence of pollinators. Such ecological attributes raise possible constraints for the forest trees to regenerate. The objective of the study was to assess the potential risk of failed regeneration for each tree species of the forest. Each of species with dbh of more than 5 cm in a one-ha plot was collected, identified, and its ecological criteria, including rarity, floral sexuality, seed size, and flowering phenology were determined. The potential risk of the failure of regeneration was calculated by summing all scores from Analytical Hierarchical Process of the criteria. The results indicated that the forest consisted of 118 species belonging to 69 genera and 37 families. Rare species accounted to 52.10% of the total species. Of the 118 species, the potential medium risk category contributed to 38.14%, and more than 33% were grouped into very high and high risk or were more prone to failed regeneration in the future. All rare dioecious species were categorized into very high and high risks. Only 21 species (17.79%) are listed in 2017’s IUCN red list. Among unevaluated species, 22 and 13 species were respectively included in very high and high potential risk categories. The results revealed more detailed potential risk of failed regeneration of tree species, and can serve as basic information to develop proper conservation management.
Keywords: Bengkulu, dioecy, hermaphrodite, phenology, rarity, rainforest, risk regeneration
INTRODUCTION difficulty to grow under warmer and drier environments (Whitmore 1983). Therefore, rapid environmental changes Tropical rainforests and their intangible functions are induced by both climate change and forest degradation will getting more important in recent years due to their vital pose constraints for climax tree species to regenerate. roles in providing life-support and ecological services such Moreover, according to floral sexuality, Bawa et al. (1985) as carbon sequestration, water provision, and prevention of shows that dioecy is common among tropical tree species, global warming and its negative effects. However, their which requires at least two different individual trees to existences are constantly being threatened by economic as perform sexual regeneration. well as human population pressures. Indonesian lowland In the tropical forest, even hermaphrodite species tend rain forests especially in Sumatra and Kalimantan Islands, to be not self-compatible, and consequently have to do have been undergoing rapid deforestation and degradation outcrossing (Bawa et al.1985). Both phenomena require as the results of conversions into mainly oil palm flower synchronization among trees of the same species in plantations as well as into industrial plantation forests order that pollination process can occur. Even if this takes which have simpler stand structure. In addition to those place, then pollination process is still difficult, because external factors, the forests inherently have their own different flowering trees can be distant from each other ecological attributes that potentially constrain their abilities (Whitmore 1983). In the tropical rainforest of Malaysia to regenerate. In species-rich tropical rain forests, each of Peninsular, for example, it requires 32 ha to find two trees their tree species generally consists of very few individual of the same species (Poore 1968). Therefore tropical trees trees (Whitmore 1983; Sakai et al. 1999; Sakai 2001). must adapt to the rapid environmental alterations; Susatya (2007, 2010) studying three different tropical otherwise, they may be threatened by those changes and rainforests discovered the similarity of their structural may face difficulties in regeneration because of their own patterns, namely, they were composed of many species, but reproductive biology. The focus of the study was to with very few individual trees. The very low density of tree determine the potential risk of failed regeneration of tree species appears to be more prevalent to the climax tree species based on their floral sexualities, tree density, species than the pioneer ones (Susatya 2010). Furthermore, flowering patterns, and seed sizes. unlike pioneer species that have good capabilities to explore wide ecological ranges, the climax tree species have been known to adapt to more limited ecological ranges as well as more stable environments, and have 2 BIODIVERSITAS 19 (5): xxx, September 2018
MATERIALS AND METHODS density, floral sexuality, flowering phenology, and seed size. AHP is widely used for selecting alternatives from The research site was located at Taba Penanjung Area different criteria in different hierarchies. AHP transforms within Bukit Daun Protection Forest, Bengkulu Province, qualitative data into the quantitative ones through pairwise Indonesia. This lowland rainforest was well protected and comparisons by experts (Saaty, 1980). Each comparison Comment [a3]: Check this location and give a minor illegal logging in the form of cutting small pole (< was conducted to assign a value between two criteria map 10 cm dbh) for social purposes infrequently occurred. according to their relative importance (Table 1). Comment [u4R3]: I added complete locaation Records at Talang Pauh climate station showed that in the For the purpose of the study, two hierarchies were last decade, Taba Penanjung area received the annual established. The first hierarchy consisted of main criteria Comment [a5]: Add maps rainfall around 2848 mm, with no monthly rainfall less than such as species sexuality (Si), flowering phenology (Pi), 100 mm. November, December, and January respectively seed size (Zi), and rarity (Ri) or the number of individual Comment [u6]: I added map. SEE IN THE EN received, 533, 420, 304 mm rainfall, higher than that of the trees per species per ha. Meanwhile, the second hierarchy OF ARTICLE FOR THE MAP other months. August was known to receive the lowest was subcriteria within sexuality, phenology, seed size, and AND PLEASE REARRANGE OF THE ARTICLE IT WILL BE Figure 1. monthly rainfall (BPS Kab. Bengkulu Tengah 2012). rarity. Subcriteria of floral sexuality (Sj) included Unusual low monthly rainfall occurred in 1991 and 1994, hermaphrodite (S1), monoecious (S2), dioecious (S3), while when September and October got only 3 mm. The monthly subcriteria of the flowering phenology (P j ) consisted of relative humidity was 83%, and reached as high as 87.7%, once (P1), twice (P2), throughout year (P3), and supra but dropped as low as 75.96%. The average monthly annual (P4). We defined supra annual category as tree temperature was 26.2 0C, and reached its respective species that performs flowering every more than 1 year, maximum and minimum at 29 0C in August, and 23 0C in while throughout year was tree species that flowers more or October (Susatya 2007). Basic floristic data were collected less continuously within a year. The subcriteria of seed size from a one-hectare plot in 2015. All trees with dbh of > 5 (Z j ) was categorized and developed following Chacon et cm were tagged, their diameters measured, and their al. (1998). It consisted of very small (0-4 mm), small (4-8 herbarium specimens collected. Species identification was mm), medium (8-12 mm), large (12-16 mm), and very carried out in the Herbarium of Universitas Bengkulu large (> 16 mm), and was respectively coded as Z1, Z2, Z3, (HUB). Species nomenclature followed by Turner (1995). Z4, and Z5. Subcriteria of the rarity (R j ) consisted of R1, In the case of the absence of tree’s reproductive aspects R2, R3, R4, R5, R6, and R7, which was defined by species such as floral sexuality, flowering phenology, and seed size with 1, 2, 3, 4, 5-6, > 7 trees per ha, respectively. Three for each species, I relied on the available secondary senior ecologists within the Department of Forestry, information including Soerianegara and Lemmens (1994), University of Bengkulu were selected as experts to carry Lemmens et al. (1995), Sosef et al. (1998), and Plants of out pairwise comparisons between two criteria or Southeast Asia (www.asianplant.net) to collect those data. subcriteria. The results of pairwise comparisons were used To determine the potential risk of failed regeneration to construct the matrix of the value judgments, which was (PRR), I applied Analytic Hierarchy Process (AHP) further analyzed to find the matrix of the priority rank developed by Saaty (1980), and adopted a similar approach (eigenvalue). Each eigenvalue of criteria or subcriteria from Oktariadi (2009), who used AHP to develop the risk reflected the score of their relative importance in ranking of tsunami in Southern Java. The method of AHP determining the potential risk of failed regeneration. was selected because PRR was calculated by summing the score of different criteria or biological aspects such as
Table 1. Assigned values of pair-wise comparisons
Assigned Definition Explanation judgment value
1 Equally important Two criteria or subcriteria are equally important to influence the potential risk of regeneration failure. 3 Moderately more important One criterion or subcriterion is moderately more important to influence the potential risk of regeneration failure. 5 Much more important One criterion or subcriterion is much more important to influence the potential risk of regeneration failure. 7 Very much more important One criterion or subcriterion is very more important to influence the potential risk of regeneration failure. 9 Extremely more important One criterion or subcriterion is extremely more important to influence the potential risk of regeneration failure. 2,4,6,8 Intermediate judgment values between two consecutive judgments value
SUSATYA – Risk of tree regeneration failure in tropical forest 3
At each hierarchy level, the consistencies of all scores species of Euphorbiaceae, 11 species (47.82%) were rare were checked by comparing their calculated consistency species. Meanwhile, the families of Moraceae and ratios with Saaty’s consistency ratio table. If there were Meliaceae respectively had 33.33% and 40% of their inconsistencies in their judgments, all processes of pairwise species categorized as rare. Species characterized by very comparison and analysis were repeated (Saaty 1980, Saaty few individual trees per ha potentially faces more difficult 2008). Potential risk of failed regeneration, then, was to maintain its population. calculated by summing the score of criteria and subcriteria According to floral sexuality, hermaphrodite species of each species i (Si Sj + Pi Pj + Zi Zj +Ri Rj) x 100. Five were the most prevalent, contributing to 41.53% of the total categories of the potential risks consisting of very high, species (49 species). Meanwhile, monoecious and high, medium, low, and very low were developed. A dioecious species respectively consisted of 33.05% (39 species was included in either very high, high, medium, species), and 25.42% (30 species) (Figure 2.B). low or very low risks, if it had respectively a total score of Monoecious and dioecious species generally account to 4% PRR between 30.93-36.44, 25.42-30.93, 19.91-25.42, and 6% respectively, but the later appears to be more 14.41-19.92, and 8.89-14.40. Potential risk was developed prevalent in the tropics than in temperate regions (Renner to indicate the relative sensitivity of a species to 2014). The number of monoecious and dioecious species of regeneration failure. It was aimed to extend the Taba Penanjung lowland rain forest was higher than that of interpretation of species threats and the modifications of Costa Rica wet premontane forest (Breanne 2017) as well the systems in determining extinction risk in IUCN at local as of Central Kalimantan, Indonesia (Brearley et al. 2007). level. A species with very high-risk category implies that Monoecious and dioecious species of Costa Rica over the time, this species is expected to be more sensitive premontane respectively account to 13.10% and 13.70% to the regeneration failure than those in lower risk (Breanne 2017), while the similar categories of Central categories. Any species with very high and high risks will Kalimantan respectively contribute to 14.70% and 23.49% have respectively very high and high probability of of the total species (Brearley et al. 2007). Special to regeneration failure in the near future. dioecious species, its number appears to be more similar than those found at both Sarawak (Ashton 1969) and Pasoh forests (Kochummen et al. 1991). RESULTS AND DISCUSSION
Taba Penanjung lowland rainforest consisted of 118 70 A 60 species belonging to 69 genera and 37 families 60 Number of species (Supplement). The forest structure was composed mostly of 50.85 50 % of the total species species with a single tree per ha that contributed to 60 40 species or 50.85% of the total species (Figure 2.A). Only 30 four species, namely Microcos laurifolia, Croton 18 16 20 15.25 13 argyratus, Elateriospernum tapos, and Endospermum 13.56 11.02 7 5.93 diadenum, had more than 10 trees/ha. Elateriospernum 10 4 3.39 tapos (Euphorbiaceae) had the highest density per ha with 0 1 2 3 4 5--6 >7 31 trees. Tree /ha Following to Ng’s category (1978) on species 60 rarity, who defined that any species with a single tree is B 49 50 41.53 categorized as rare species, then the forest structure is 39 40 33.05 unproportionally composed of rare species. This rarity was 30 also shown at both genus and family levels in that 8 30 25.42 families or 21.62% of the total families and 20 genera or 20 28.98% of the total were respectively represented by a 10 single tree. Therefore, any loss of an individual tree of the 0 rare species can result in the loss of species, genus, and Hermaphrodite Dioecious Monoecious family. The unproportional number of rare species composing forest structure appears to be common in 60 C 54 Bengkulu such as in Tambang Sawah lower montane forest 50 45.38 of Kerinci-Seblat National Park (Susatya 2010), and Talang 41 Tais secondary lowland rainforest (Susatya 2007). 40 34.45 Euphorbiaceae was the most diverse family with 11 genera 30 and 23 species, followed subsequently by Moraceae with 3 20 12 genera and 13 species, and Meliaceae with 3 genera and 10 10.08 11 9.24 species. It seems that the abundant species of 10 Euphorbiaceae is one of the characters of the floristic 0 composition of Sumatra lowland forest. This is also Once Twice Throughout Supra annual observed elsewhere in West Sumatra (Hadi et al. 2009, Kohyama et al. 1989). Interestingly, the rare species was Figure 2. The structure of Taba Penanjung Lowland rainforest also common among the most diverse families. Among 23 according to: A. Tree density, B. Floral sexuality, C. Flower phenology of its species
4 BIODIVERSITAS 19 (5): xxx, September 2018
Dioecious species at both sites respectively account to forests are dominated by species of Dipterocarpaceae 26% and 28%. The number of monoecious and dioecious (Brearley et al. 2007; Sakai et al. 1999), which are well species of the site altogether accounted up to 58,47% of the known to perform mass flowering or supra annual total species (69 species). This shows that more than half of flowering (Whitmore 1983). Meanwhile, Taba Penanjung the total species have to perform outcrossing in order that rainforest is dominated by species of Euphorbiaceae and pollination can occur. Such a process requires both the Moraceae, which are recorded to have throughout synchronization of flowering phenology and the presence flowering patterns (Whitmore 1983). of pollinators, which could lead to uncertainty on seed Most of species fallen into medium risk category, production and tree regeneration. The uncertainty is even contributing to 38.14% of the total species. Species with greater because the sex ratio of dioecious species is male- this medium risk indicate that they do not face an favored (Queenborough et al. 2009; Gao et al. 2012), and immediate risk which may further threaten their male flowers bloom earlier than their female opposites at regeneration. Other categories namely very high, low, and certain species (Queenborough et al. 2013). high risks had almost similar values, ranging from 19.49%, With regard to tree regeneration, dioecious species have 18.64%, to 17.80% (Figure 3). Both very high and high- advantages because they tend to yield large seeds, risk categories altogether accounted to 37.29%, indicating containing more energy (Varmosi et al. 2008), which that more than one-third of the species will face more increase the probability of seedling survivorship. However, serious threat to their tree regenerations in the near dioecious species also face the difficult regeneration, future. because they have only half of their adult trees to produce Twenty three species (Figure 3) from five families were seeds (Renner 2014). Dioecious tree species also tend to included in very high-risk category, consisting of species generate high seed density around their female parent trees, from Euphorbiaceae, Myristicaceae, Lauraceae, which further lead to high seed predation. It is speculated Flaucourticaeae, Moraceae, and Rubiaceae. Each of these that the more distant the individual dioecious trees grow families respectively contributed to 52.17% (12 species), from their female parent trees, the higher probability of 21.74% (5 species), 13.04% (3 species), and 4.3% (1 their seed survivorships and the better seedling recruitment species). Of these families, all species of Myristicaeae, they have due to predation avoidance (Abebbe 2008). namely Knema globularia, Knema glauca, Horsfieldia Taba Penanjung lowland rainforest has diverse tree polyspherula, Horsfieldia costulata, and Gymnacranthera species based on flowering phenology. According to forbesii, were included in this category. The very highrisk flowering phenology, the majority of species of Taba category was dominated by dioecious species (22 of 23 Penanjung rain forest perform either throughout or once species). The only monoecious included in this category flowering phenology (Figure 2.C). Flowering phenology was Artocarpus kemando (Moraceae). Artocarpus kemando shows the incidence of reproductive efforts of the species, was characterized by a single tree per species per ha, large which reflects and will determine the probability of the seed category, and supra annual flowering. The reproductive success. The throughout flowering species has combination of these biological characters makes this relatively higher probability to ensure seed production and species have very highrisk. A note of this species is that the tree regeneration in the future than the supra annual incident of supra annual flowering is relatively longer that category, simply because the former produces more of the other supra annual flowering species. It has been frequent flowers and fruit than the later, which only recorded to not produce flowers within 7 years (Sosef et al. produces flower and fruit once for every two to five years. 1998). The very high risk category consisted not only of Flowering phenology is an important factor in tree species with a single tree; in fact, 7 of them had more than regeneration, because the length, timing of flowering and one tree per ha, namely Aporosa accuminatisima (2), fruiting coupled with seasons will determine seed Actinodaphne peduncularis (2 trees), Drypetes longifolia (2 production, seedling mortality, establishment, and growth trees), Hydnocarpus curtisi (3 trees), Horsfieldia costulata (Augspurger 1981). Furthermore, the role of environments (2 trees), and Knema globularia (3 trees). becomes a pivot point in tree regeneration because the flowering phenology shows a strong correlation with climate, rainfall, and humidity, drought and temperature (Kushwaha et al. 2011; Sulistyawati et al. 2012). Species with throughout flowering contributed to 45.38% of the total species (54 species), while those with once flowering a year accounted to 34.45% (41 species). The number of species with twice a year and supra annual flowering patterns was not as many as both throughout and once flowering phenologies. Both patterns respectively accounted to 10.08% (13 species) and 9.14% (11 species). The number of species with supra annual flowering in the site was much lower than that of Central Kalimantan (Brearley et al. 2007), and of Lambir hill of Sarawak (Sakai et al. 1999). The supra annual flowering species at those two last sites respectively account to 75%, and 54%. Both
SUSATYA – Risk of tree regeneration failure in tropical forest 5
Figure 3. The potential risk of regeneration failure of trees of very high category regardless of seed size and flowering Taba Penanjung lowland rainforest phenology. Dioecious species generally fall into very high- Comment [u7]: I CHANGE TO FIGURE 3, All of these species have similar characters such as risk category, because of the complexity of reproduction INSTEAD OF FIG 2) dioecious and extra large seeds, with various flowering FIGURE 3 EXPLANATION SHOULD NOT BE biology. To carry out reproduction efforts, they require SEPARATED FROM THE FIGURE phenology. Among these species, Aporosa accuminatisima flowering synchronization and the presence of pollinators. and Actinodaphne peduncularis are recorded to have Dioecious species also show more limited reproduction ecological disadvantages, where the former has been capacity than those having other flower sexuality types, reported for its low regeneration, and the later has been simply because they have only half of their mature trees known for its restricted distribution (Sosef et al. 1998). It contributing to seed production. Their flowering and appears that the extra large seed category, and the species fruiting successes are also influenced by both the distance density of more than one tree per ha will put the dioecious between male and female trees and the pollinator species into very high risk regardless of their flowering movement from male to female trees (Renner 2014). phenologies. The extra large-size seed is generally During pollination process, pollinators travel a certain recalcitrant, which has very fast germination, low distance which further adds up to the uncertainty of fruit capability of dormancy, and high sensitivity to drought production. The farther the distance between mature male (Marcos-Filho 2005). Water content within seeds of this and female trees, the more uncertain pollination process to type determines germination success, and varies according occur. It was estimated that the closest distance between to species and habitat quality. For example, the seed of the same tree species could reach up to 131 m, and the Shorea roxburghii, which has habitat with low rainfall, is distance between female and male trees could be even tolerant to low water content and still be able to germinate farther (Abebbe, 2008). The difficulty of the regeneration when the water content reaches as low as 35%. Meanwhile, of dioecious species is even greater due to the fact that the the seeds of other species such as S. almon, and S. robusta microclimates beneath male mature trees play a can not germinate when the water content is less than 40%. determining role in regeneration. It has been known that Recalcitrant seeds generally are not able to germinate if the seedling and sapling recruitments tend to be greater under water content reaches as low as 20%-30% (Davies and the male trees than the female trees (Arai and Kamitani Ashton 1999). This is the reason why the species with large 2005). seeds prefer to grow and become common in the moist A rare species is expected to face the regeneration condition under canopy trees, but hardly survive in open problem due to its difficulty to maintain its population canopy, or a dry, warm, and disturbed habitat. density. A rare or single-tree per ha species is more likely Davies and Ashton (1999) raise the issues on the to experience failed regeneration simply because it disadvantages for large-seed species. A large seed tends to statistically has a lower chance to regenerate than those of have lower fecundity and can hardly thrive at a forest gap more than one tree per ha. Forest structure dominated by habitat. On the other hand, a large seed has the advantages species having very few individual trees appears a common of having more energy reserved in its cotyledon. In a good- ecological attribute of species-rich Southeast Asia quality environment, the large seed germinates and grows rainforest (Susatya 2010) and Nigerian rain forest rapidly, and has high seedling survivorship due to the large (Adekunle et al. 2013). From the forest tree regeneration energy stored in cotyledon (Arunachalam et al. 2003). On perspective, this attribute has been worsened by the fact the contrary, the small-size seed size is generally more that even hermaphrodite species tend to be not self- tolerant to decreasing water contents (Chin et al. 1989). compatible (Bawa 1979; Bawa et al. 1989). However, in Small-size seeds are categorized as orthodox which this research, a species with a single tree alone does not generally tolerate drought, and are well known to have long necessarily determine whether the species belongs to either dormancy. Therefore, species with small seeds are able to very high or high-risk categories. In fact, 55% of the total wait until suitable environments become available for their of rare species are classified into either medium risk (27 germination. The presence of gap generating more light species) or low risk (5 species) category. Only rare species intensity, drier and less moist conditions triggers small with either dioecy or monoecy are most likely to belong to seeds to germinate and dominate the open habitat (Marcos- either very high or high-risk category. Rare species with Filho 2005). Furthermore, a small seed has many high and very high-risk categories accounted up to 12 ecological advantages of having wider dispersal, being able species and 16 species, respectively. to select suitable microclimates, and having high fecundity Moreover, rare hermaphrodite species will fall into (Davies and Ashton 1999). medium risk category regardless of seed size and flowering The majority of the very high-risk category had phenology. However, rare hermaphrodite species with both throughout flowering (12 species), followed by once small seed category and throughout phenology such as flowering phenology type (6), while supra annual flowering Bhesa paniculata (Celastraceae), Astronia macrophylla only consisted of 3 species. This flowering phenology (Melastomaceae), Neolamarckia cadamba (Rubiaceae), variation shows that the phenology does not determine the Micromelum minutum (Rutaceae), and Rinorea anguifera very high-risk category. Furthermore, the very high risk (Violaceae) were included in low-risk category. These comprised 8 and 7 species respectively characterized by combined criteria make these five species have better extra large and small seed categories. Similar to the reproductive success as well as better seedling survivorship phenology, seed size does not determine the very high-risk than the monoecious and dioecious species. This pattern category either. Therefore, in general, if a species is shows that being dioecious or monoecious is more dioecious and rare, then the species is likely to belong to
6 BIODIVERSITAS 19 (5): xxx, September 2018 influential in determining very high and high risks than Lemmens et al. 1995). This indicates that these species are being rare species. As long as a rare species does not likely to become a target for logging in the near future. In belong to dioecious and monoecious categories, it will not addition to a timber harvesting factor, their ecological be included in either very high or high-risk category. attributes could potentially increase the risks of several The high-risk category was composed of 21 species of medium risk species. For example, the tree population of 10 families (Figure 3), of which family of Meliaceae Alstonia angustiloba has been locally depleted due to contributed most with 7 species, while the other nine logging (Soerianegara and Lemmens 1994), while families only contributed from one to four species. High- Baccaurea racemosa has been recorded as uncommon risk category comprised various species with all types of species at the lower strata of the Southeast Asia rain forest the flower sexuality. Monoecious species contributed most (Sosef et al. 1998). Furthermore, Endospernum diadenum with 13 species (61.90%), followed by dioecious species (6 faces a high predation of its seeds and is known to have species). Meanwhile, hermaphrodite species only low seed viability (Soerianegara and Lemmens 1994). accounted to 2 species. Interestingly, of the 48 Three species of Polyalthia, P. hookeriana, P. michaelii, hermaphrodite species generally belonging to either and P. rumphii are noted to have scattered distribution, and medium or very low risk, two were included in high-risk their seedlings are sensitive to drought (Sosef et al. 1998). category, namely Shorea ovalis and Palaquium hexandrum, The hermaphrodite species were included in various both of which are characterized by extra large seed and categories from medium to very low risk. Rare supra annual flowering phenology. The combination of hermaphrodite species are likely to fall into medium risk, if extra large seed and less frequent incidence of flowering they have medium to extra large seeds, regardless of their and fruiting makes those two species classified into high- flowering phenologies. However, rare hermaphrodite risk category. In addition to these biological aspects, an species with small to very small seed categories and external factor in the form of timber harvesting becomes an throughout flowering pattern will fall into low risks. imminent threat to these two species. The population of Furthermore, hermaphrodite species with more than one Shorea ovalis, the member of commercial light Red tree are most likely to belong to low and very low-risk Meranti group, is also dwindling due to logging. Like other categories. Hermaphrodite species with more than 4 trees species of Palaquium, Palaquium hexandrum faces a will come up into two different categories depending on reproductive problem, because its flowers hardly reach their seed sizes. Those with small and medium sizes will maturity due to insect predation. If they pass through fruit end up to very low-risk category, while those with large development, then their fruit suffer high predation by bats, and extra large seeds will fall into low category. The birds, and squirrels (Soerianegara and Lemmens 1994). former consists of Shorea platyclados, Barringtonia Furthermore, a special attention has to be made for a rare lanceolata, and Syzygium rostrata, while the later are species of Diospyros sumatrana which has been classified Geunsia hexandra, Dillenia excelsa, Strombosia javanica, into high-risk category. The species appears to face fruit Neonauclea gigantea, Microcos laurifolia, Euonymus development problem, because it needs long period of time javanicus, and Cratoxylum sumatrana. to reach fruit ripening (Lemmens et al. 1995). Such a long Of the 118 tree species, only 21 species (17.79%) are period could result in being more vulnerable to fruit listed in 2017’s IUCN red list. The other species are listed predation, which could further lead to lower its as not assessed species, meaning the conservation statutes regeneration capability. of these species have not been evaluated according to Not all of the monoecious species fall into a single IUCN’s criteria. The tree species listed at IUCN consists of category. Most of the monoecious species fallen into 2, 1, 3, and 15 tree species respectively categorized into medium risk (18 species), subsequently followed by high endangered (E), Vulnerable (V), near threatened (NT), and risk (13 species), low risk (6 species), and very high and least concerned (LC). Furthermore, of the 23 species with very lows risk categories which respectively consisted of very high-risk category, only three tree species, namely only 1 species. Monoecious species with one to two trees Litsea spathacea, Knema glauca, K. globularia have been per ha, large and extra large seed categories, and once included into least concerned. Of the 21 species with high- flowering pattern will fall into high-risk category. risk category, seven are categorized into four different Meanwhile, similar monoecious species with very small IUCN's conservation status. Two species, namely Aglaia seed and throughout phenology (12 species) will belong to speciosa and Sterculia oblongata, are classified as medium risks category. Interestingly, monoecious species endangered, while Sterculia parvifolia is included as with 3-4 trees but with once and supra annual flower will vulnerable. Furthermore, three species of Meliaceae, also belong to medium risk category regardless of seed namely Aglaia odoratissima, A. oligophylla, and A. size. It appears that whether a monoecious species will fall rubiginosa, are grouped into near threatened. Species of K. into a certain category is not solely defined by its rareness, glauca, K. globularia, Litsea spathacea, Aglaia tomentosa, but also by the seed size and flowering phenology. Sterculia parviflora, Archidendron ellipticum, Magnolia Species belonging to medium risk category should not sumatrana, Microcos laurifolia, Alstonia angustiloba, face immediate threats for their regeneration. However, Bhesa paniculata, Euonymus javanicus, Payena maingayi, timber harvesting will potentially jeopardize their future. P. lanceolata, Polyalthia hookeriana, and Prunus arborea, Among the medium risk category (45 species), 26.27% (12 are categorized as the least concerned species. Comparing species) are either included into major or minor the IUCN RedList and the results of the potential risk commercial timbers (Soerianegara and Lemmens 1994; analysis resulted in interesting outcomes. Among the 15
SUSATYA – Risk of tree regeneration failure in tropical forest 7 species listed as least concerned by IUCN, nine are Adekunle VAJ, Olagoke AO, Akindale SO. 2013. Tree species diversity classified into medium to low risk categories, which is and structure of a Nigerian strict nature reserve. Trop Ecol 54 (3). 275-289. almost similar to least concerned category, while the other Arai N, Kamitani T. 2005. Seedrain and seeding establishment if the six species, namely K. glauca, K. globularia, Aglaia dioecious trees Neolitsea sericea (Lauraceae). Effect of tree sexs and tomentosa, Archidendron ellipticum, Litsea spathacea, and density on invasion into confiner plantation in central Japan. Sterculia obolongata are either included in high risk or Canadian J Bot: 83 (9) 7144-1150 Arunachalam A, Khan ML, Singh ND. 2003. Germination, growth and very high-risk category. The first two were very high-risk biomass allocation as influenced by seed size in Mesua ferrea. L. species characterized by dioecious species with supra Turk J Bot 27: 345-348. annual flowering phenology, while the rest were high-risk Ashton P. 1998. Shorea platyclados. The IUCN Red List of Threatened monoecious species with large seed category. S. oblongata, Species 1998: e.T33136A9761412. DOI: 10.2305/IUCN.UK.1998.RLTS.T33136A9761412.en vulnerable species by IUCN, was classified into high risk. Ashton PS.. 1969. Speciation among tropical forest trees: some Both seem to be comparable status, where both indicate deductions in the light of recent evidence. Biol J Linn Soc 1: 155- that in the near future, the species will face difficulty to 196 maintain its population density in order to avoid local Augspurger C. 1981. Reproduction synchronization of a tropical shrub: experimental studies on effects of pollinator and seed predation in extinction. Interestingly, Shorea platiclados that has long Hybanthus pruniformis (Violaceae). Ecology 61: 775-788. been classified as endangered species (Ashton 1998), did Bawa KS. 1979.. Breeding systems of trees in a tropical wet forest. N Z J fall into low risk. Low-risk category of this species Bot. 17 (521-524). indicates that it relatively does not face immediate threat on Bawa KS, Ashton PS, Primack RB, Terborgh J, Nor SM, Ng FSP, Hadley M. 1989. Reproductive ecology of tropical forest plants. IUBS its tree regeneration locally, and is considered to be able to Special issue-21. International Union Biological Sciences, Paris, ensure its future regeneration. The number of tree per ha (4 France. trees) became the main reason for the species to be Bawa KS, Perry DR, Beach JH. 1985. Reproductive biology of tropical classified as low-risk category. Moreover, among the 97 lowland rainforest trees I. Sexual systems and incompatibility mechanism. Amer J Bot 73: 331-480 species whose conservation statuses have not been BPS Kab. Bengkulu Tengah. 2012. Kabupaten Bengkulu Tengah Dalam evaluated by IUCN, 22 and 13 were respectively included Angka Tahun 2012. BPS Kab. Bengkulu Tengah. [Indonesian] in very high and high potential risk categories. Breanne H. 2017. Ecological Correlates with Dioecy in the Flora of a The conservation statuses of most of the very high and Tropical Premontane Wet Forest in Costa Rica. Distinction Papers 53. Otterbein University, Westerville, OH high-risk tree species have not been evaluated according to Brearley FQ, Proctor J, Suriantata, Nagi, J, Dalrymple G, Voyse, BC. IUCN's criteria. IUCN is aware that there is a need for 2007. Reproductive phenology over a 20 year period in a lowland more detailed evaluation for conservation status at local evergreen rainforest old central Borneo. Ecology 95: 828-839. level because differences between global and local threats Chacon P, Bustamante R, Henriquez C. 1998. The effect of seed size on germination and seedling growth of Cryptocarya alba in Chile. are very important for determining the status. It further Revista Chilena de Historia Natural 71: 189-197. indicates that a species which has been globally categorized Chin HF, Krishnapillay B, Stanwood PC. 1989. Seed Moisture: into endangered could be the least concerned category due Recalcitrant vs. Orthodox Seeds. SSA Special Publication no. 14. to steady population at a local level. On the other hand, USDA. Madison, WI, USA. Davies SJ, Ashton PS. 1999. Phenology and fecundity in 11 sympatric species with least concern status can turn into endangered pioneer species of Macaranga (Euphorbiaceae) in Borneo. Amer J category due to its small and locally dwindling population Bot 86 (12): 1786-1792. (IUCN 2012). The results of this research make more Gao J, Queenborough SA, Chai JP.2012. Flowering sex ratios and spatial detailed ecological information concerning the potential distribution of dioecious trees in a South-East Asian seasonal tropical forest. J Trop For Sci 24 (4): 517-527. risk of the failure of tree regeneration available, which is Hadi S, Ziegler T, Waltert M, Hodges JK. 2009. Tree diversity and forest not always provided by IUCN red list documents. The structure in Northern Siberut. Mentawai Island, Indonesia. J Trop results are very important to serve as both substitutes and Ecol 50 (2): 315-327. guidance at local level for conservation purposes in the IUCN. 2012. IUCN red list categories and criteria. Version 3.1. Second Edition. IUCN, Gland. absence of conservation status of IUCN of the tree Kochummen KM, LaFrankie JV, Manokaran N. 1991. Floristic species. composition of Pasoh Forest Reserve, a lowland rain forest in Peninsular Malaysia. J Trop For Sci 3: 1-13. Kohyama T, Hotta M, Ogino K, Syahbudin, Mukhtar E. 1989. Structure and dynamics of forest stand in Gunung Gadut, West Sumatra. In: ACKNOWLEDGEMENTS Hotta M (ed.). Diversity and plant-animal interaction in equatorial rainforest: report of 1987-1988 Sumatra Research. Kagoshima The author is indebted to members of WARISAN, who University, Kagoshima. Kushwaha SP, Tripathi SK, Triphati BD, Sing KP. 2011. Pattern of tree helped in the field works, and also grateful to Astri W. phenology diversity in dry forest. Act Ecol Sin 13: 179-185 Utami, Sequoia MS Rhomadhon, and Magnolia GR. Lemmens RHMJ, Soerianegara I, Wong WC. 1995. Plant resources of Satriorini, who supported logistics during the field work. South-East Asia No 5 (2). Timber trees: Minor commercial timbers. Prosea Foundation, Bogor, Indonesia. Marcos-Filho J. 2005. Fisiologia de sementes de plantas cultivadas (Seed physiology of cultivated plants). FEALQ, Piracicaba. REFERENCES Ng FSP. 1978. Tree flora of Malaya: A Manual for Forester. vol 3&4. Longman Malaysia Sdn. Bhd., Kuala Lumpur. Abebbe GT. 2008. Ecology of regeneration and phenology of seven Oktariadi O. 2009. Penentuan peringkat bahaya Tsunami dengan method indigenous species in a dry tropical afromontana forest, Southern analytical hierarchy process. (studi kasus: wilayah Pesisir Kabupaten Ethiopia. [Dissertation]. Addis Abeba Universiy, Ethiopia. Sukabumi). Junal Geologi Indonesia 4 (2): 103-106. [Indonesian] Poore MED. 1968. Studies in Malaysian rain forest I. The forest on the Triassic sediments in Jengka Forest Reserve. J Ecol 56: 213-216.
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Queenborough SA, Mazer SJ, Vamosi SM, Garwood NC, Valencia R, and Susatya A. 2007. The ecology and taxonomy of Rafflesias in Bengkulu. Freckleton RP. 2009. Seed mass, abundance and breeding system [Dissertation]. Faculty of Science and Technology, National among tropical forest species: do dioecious species exhibit University of Malaysia (UKM), Selangor. compensatory reproduction or abundances?. J Ecol 97: 555-566. Susatya A. 2010. The diversity and richness of tree species of Tambang Queenborough SA, Humphreys AM, Valencia R. 2013. Sex-specific Sawah Forest, Kerinci-Seblat National Park. Sumatra Indonesia. Berk flowering patterns and demography of the understorey rainforest tree Penel Hayati 16: 63-67. Iryanthera hostmannii (Myristicaceae). Trop Conserv Sci 6 (5): 637- Turner IM. 1995. A catalogue of the vascular plants of Malaya. Gard Bull 652. Sing 47: 1-757. Renner SS. 2014. The relative and absolute frequency of angiosperm Varmosi SM, Mazer SJ, Cornejo F. 2008. Breeding systems and seed size sexual systems, Dioecy, monoecy, ynodiocy, and update online in a neotropical flora. Testing evolutionary hypothesis. Ecology 89 database. Amer J Bot 101 (10): 1588-1596. (9): 61-72 Saaty T. 1980. The Analytic Hierarchy Process. McGraw Hill, New York. Whitmore TC.1983. An introduction for tropical rainforest in Far East Saaty T. 2008. Decision making with the analytic hierarchy process. Intl J Asia. Clarendon Press, Cambridge. Serv Sci 1 (1): 83-98. Sakai S, Momose K, Yumoto T, Nagamitsu T, Nagamasu H, Hamid AA, Nakashizuka T. 1999. Plant reproductive phenology in a lowland Dipterocarp forest, Sarawak. Malaysia. Amer J Bot 86: 1414-1436. Sakai S. 2001. Phenological diversity in tropical forest. Popul Ecol 43: 77- 86. Soerianegara I, Lemmens RHM. 1994. Plant resources of South-East Asia No 5 (2). Timber trees: Major commercial timbers. Prosea Foundation, Bogor, Indonesia. Sosef MSM, Hong LT, Prawirohatmodjo S. 1998. Plant resources of South-East Asia No 5 (3). Timber trees: Lesser-known timbers. Backhuys, Leiden. Sulistyawati E, Mashita N, Setiawan NN, Choesin DN, Suryana P. 2012. Flowering and fruiting phenology of tree species in Mount Papandayan Nature Reserve, West Java, Indonesia. Trop Life Sci Res 23(2): 81-95.
Figure 1. Taba Penanjung Research site, Bengkulu Province, Indonesia
BIODIVERSITAS ISSN: 1412-033X Volume 19, Number 5, September 2018 E-ISSN: 2085-4722 Pages: xxxx DOI: 10.13057/biodiv/d1905xx
Table S1. Tree species of Taba Penanjung Lowland Rainforest and their potential risks of the regeneration failure
Rarity Floral sexuality Seed size Flowering phenology Species Family Total score PRR tree/ha Score Type Score Type Score Type Score Actinodaphne peduncularis L Lauraceae 2 0.238 Dio 0.581 Exl 0.3260 Onc 0.281 34.1826 VH Aglaia affinis Merr Meliaceae 2 0.238 Mon 0.309 Med 0.1770 Onc 0.281 25.6374 H Aglaia faveolata Pannell Meliaceae 1 0.286 Mon 0.309 Med 0.1770 Onc 0.281 27.8982 H Aglaia odoratissima Blume Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H Aglaia oligophylla Miq Meliaceae 3 0.19 Mon 0.309 Exl 0.3260 Onc 0.281 24.9858 M Aglaia rubiginosa (Hiern.) Pannell1 Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H Aglaia speciosa Blume Meliaceae 2 0.238 Mon 0.309 Lrg 0.2960 Onc 0.281 26.9226 H Aglaia tomentosa Teijm ex Binn Meliaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H Alstonia angustiloba Miq. Apocynaceae 1 0.286 Hmp 0.11 Vsm 0.087 San 0.412 24.0132 M Antidesma brachybotrys Airy Shaw Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH Antidesma griffithii Hoof. F Euphorbiaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH Antidesma leucocladon Hook.f Euphorbiaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH Antidesma montanum Blume Euphorbiaceae 2 0.238 Dio 0.581 Vsm 0.087 Thr 0.116 28.8789 H Antidesma velutinosum Blume Euphorbiaceae 3 0.19 Dio 0.581 Sml 0.114 Thr 0.116 26.9097 H Aporosa accuminatisima Merr Euphorbiaceae 2 0.238 Dio 0.581 Sml 0.114 Onc 0.281 31.8930 VH Archidendron ellipticum (Blume) Nielsen Leguminosae 1 0.286 Mon 0.309 Exl 0.3260 Thr 0.116 26.7849 H Artocarpus anisophyllus Miq. Moraceae 4 0.143 Mon 0.309 Lrg 0.2960 San 0.412 24.6096 M Artocarpus elasticus Reinw. ex Blume Moraceae 4 0.143 Mon 0.309 Exl 0.3260 Onc 0.281 22.7721 M Artocarpus kemando Miq Moraceae 1 0.286 Mon 0.309 Lrg 0.2960 San 0.412 31.3449 VH Astronia macrophylla Blume Melastomaceae 1 0.286 Hmp 0.11 Sml 0.114 Thr 0.116 19.4208 L Baccaurea bracteata Mull. Arg Euphorbiaceae 1 0.286 Dio 0.581 Med 0.1770 Thr 0.116 32.1117 VH Baccaurea edulis Merr Euphorbiaceae 1 0.286 Dio 0.581 Exl 0.3260 Onc 0.281 36.4434 VH Baccaurea racemosa (Reinw. ex Blume) Mull. Arg. Euphorbiaceae 6 0.095 Dio 0.581 Lrg 0.2960 Thr 0.116 24.4008 M Baccaurea sumatrana (Miq.) Mull. Arg. Euphorbiaceae 3 0.19 Dio 0.581 Med 0.1770 Thr 0.116 27.5901 H Barringtonia lanceolata (Ridl.) Payen Lecythidaceae 4 0.143 Hmp 0.11 Exl 0.3260 Thr 0.116 14.9751 L Bhesa paniculata Arn Celastraceae 1 0.286 Hmp 0.11 Sml 0.114 Thr 0.116 19.4208 L Bridelia insulana Hance Euphorbiaceae 3 0.19 Mon 0.309 Sml 0.114 Thr 0.116 19.9737 M Campnosperma auriculatum (Blume) Hook.f Anarcadiaceae 1 0.286 Mon 0.309 Med 0.1770 Thr 0.116 25.1757 M Casearia capitellata Blume Flacourtiaceae 1 0.286 Hmp 0.11 Exl 0.3260 Thr 0.116 21.7104 M Casearia clarkei King var. kunstleri (King) Ridl. Flacourtiaceae 1 0.286 Hmp 0.11 Exl 0.3260 Thr 0.116 21.7104 M Castanopsis inermis (Lindl.) Benth. ex Hook. F Fagaceae 4 0.143 Mon 0.309 Lrg 0.2960 Onc 0.281 22.4481 M Chionanthus pluriflorus (Knob) Kew Oleaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Thr 0.116 19.1256 L Chionanthus spicata Blume Oleaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M Commersonia bartramia (L) Merr. Sterculiaceae 2 0.238 Mon 0.309 Sml 0.114 Thr 0.116 22.2345 M Cratoxylum sumatrana (Jack.) Blume Hypericaceae 6 0.095 Hmp. 0.11 Sml 0.114 Onc 0.281 13.1472 VL Croton argyratus Blume Euphorbiaceae 15 0.048 Mon 0.309 Med 0.1770 Thr 0.116 13.9659 VL Dacryodes rugosa (Blume) H. J. Lam Burseraceae 3 0.19 Dio 0.581 Exl 0.3260 Thr 0.116 29.1993 H Dillenia excelsa (Jack.) Gilg Dilleniaceae 6 0.095 Hmp 0.11 Sml 0.114 Onc 0.281 13.1472 VL 10 BIODIVERSITAS 19 (5): xxx, September 2018 Diospyros sumatrana Miq Ebenaceae 1 0.286 Mon 0.309 Sml 0.114 Onc 0.281 27.2178 H Drypetes longifolia (Blume) Pax ex. K. Hoffm Euphorbiaceae 2 0.238 Dio 0.581 Exl 0.3260 Onc 0.281 34.1826 VH Durio zibethinus L Bombacaceae 1 0.286 Hmp 0.11 Exl 0.3260 Twi 0.191 22.9479 M Dysoxylum arborescens (Blume) Miq Meliaceae 2 0.238 Mon 0.309 Exl 0.3260 Onc 0.281 27.2466 H Dysoxylum densiflorum (Blume) Miq. Meliaceae 4 0.143 Mon 0.309 Sml 0.114 Onc 0.281 20.4825 M Dysoxylum excelsum Blume Meliaceae 4 0.143 Mon 0.309 Exl 0.3260 Onc 0.281 22.7721 M Elaeocarpus nitidus Jack Elaeocarpaceae 1 0.286 Hmp 0.11 Med 0.1770 Onc 0.281 22.8237 M Elateriospernum tapos Blume Euphorbiaceae 31 0.048 Mon 0.309 Exl 0.3260 Thr 0.116 15.5751 L Endospermum diadenum (Miq.) Airy Shaw Euphorbiaceae 12 0.048 Dio 0.581 Vsm 0.087 Thr 0.116 19.9299 M Erismanthus obliquus Wall ex. Mull. Arg. Euphorbiaceae 1 0.286 Mon 0.309 Sml 0.114 Thr 0.116 24.4953 M Euonymus javanicus Blume Celastraceae 3 0.19 Hmp. 0.11 Lrg 0.2960 Onc 0.281 19.5873 L Ficus benjamina L Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M Ficus depressa Blume Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M Ficus fistulosa Reinw. ex. Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M Ficus fulva Reinw. ex. Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M Ficus heteropleura Blume Moraceae 3 0.19 Mon 0.309 Vsm 0.087 Thr 0.116 19.6821 L Ficus lepicarpa Blume Moraceae 2 0.238 Mon 0.309 Vsm 0.087 Thr 0.116 21.9429 M Ficus ribes Reinw. ex Blume Moraceae 3 0.19 Mon 0.309 Vsm 0.087 Thr 0.116 19.6821 L Ficus sundaica Blume Moraceae 1 0.286 Mon 0.309 Vsm 0.087 Thr 0.116 24.2037 M Ficus variegata Blume Moraceae 4 0.143 Mon 0.309 Vsm 0.087 Thr 0.116 17.4684 L Flacourtia rukam Zoll. et. Moritzi Flaucourtiaceae 3 0.19 Hmp 0.11 Sml 0.114 Onc 0.281 17.6217 L Geunsia hexandra (Teijsm. et. Binn) Koord Verbenaceae 4 0.143 Hmp 0.11 Sml 0.114 Thr 0.116 12.6855 VL Gironniera subaequalis Planch Ulmaceae 5 0.095 Mon 0.309 Sml 0.114 Thr 0.116 15.4992 L Gordonia maingayi Dyer Theaceae 1 0.286 Hmp 0.11 Exl 0.3260 Twi 0.191 22.9479 M Gordonia multinervis King Theaceae 3 0.19 Hmp 0.11 Exl 0.3260 Twi 0.191 18.4263 L Gymnacranthera forbesii (King) Ward Myristicaceae 1 0.286 Dio 0.581 Exl 0.3260 Twi 0.191 34.9584 VH Horsfieldia costulata Warb Myristicaceae 2 0.238 Dio 0.581 Exl 0.3260 Thr 0.116 31.4601 VH Horsfieldia polyspherula (Hook. F) J. Sinclair Myristicaceae 1 0.286 Dio 0.581 Lrg 0.2960 Thr 0.116 33.3969 VH Hydnocarpus curtisii King Flacourtiaceae 3 0.19 Dio 0.581 Exl 0.3260 Onc 0.281 31.9218 VH Knema glauca (Blume) Petermann Myristicaceae 4 0.143 Dio 0.581 Exl 0.3260 San 0.412 31.8696 VH Knema globularia (Lam.) Warb. Myristicaceae 3 0.19 Dio 0.581 Exl 0.3260 San 0.412 34.0833 VH Lansium domesticum Corra Sapindaceae 1 0.286 Mon 0.309 Exl 0.3260 Onc 0.281 29.5074 H Litsea cubeba (Laur.) Pers Lauraceae 4 0.143 Dio 0.581 Lrg 0.2960 Onc 0.281 29.3841 H Litsea sessilis Boerl. Lauraceae 1 0.286 Dio 0.581 Med 0.1770 Onc 0.281 34.8342 VH Litsea spathacea Gamble Lauraceae 1 0.286 Dio 0.581 Med 0.1770 Onc 0.281 34.8342 VH Macaranga hosei King ex Hook Euphorbiaceae 1 0.286 Dio 0.581 Vsm 0.087 Thr 0.116 31.1397 VH Macaranga hulletii King ex Hook. F. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH Macaranga triloba (Blume) Mull. Arg. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH Magnolia uvariifolia Dandy ex Noot 2 Magnoliaceae 1 0.286 Hmp 0.11 Med 0.1770 Onc 0.281 22.8237 M Mallatus leptophyllus Pax et C.K. Hoffm. Euphorbiaceae 2 0.238 Hmp 0.11 Vsm 0.087 Onc 0.281 19.5909 M Mallotus auriculatus Merr Euphorbiaceae 3 0.19 Dio 0.581 Sml 0.114 Thr 0.116 26.9097 H Mallotus montanus (Mull. Arg) Airy Shaw Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH Mallotus peltatus (Geisel.) Mull. Arg. Euphorbiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH Microcos laurifolia (Hook et Mast) Burret Tiliaceae 14 0.048 Hmp 0.11 Med 0.1770 Thr 0.116 8.8914 VL Micromelum minutum (G. Forst.) Wright and Arn. Rutaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L
SUSATYA – Risk of tree regeneration failure in tropical forest 11 Naphelium lappaceum L Sapindaceae 1 0.286 Hmp 0.11 Exl 0.3260 Onc 0.281 24.4329 M Neolamarckia cadamba (Roxb) Basser Rubiaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L Neonauclea excelsa Merr Rubiaceae 1 0.286 Hmp 0.11 Med 0.1770 Thr 0.116 20.1012 M Neonauclea gigantea Merr Rubiaceae 6 0.095 Hmp 0.11 Med 0.1770 Thr 0.116 11.1051 VL Ochanostachys amentacea Mast Olacaceae 2 0.238 Mon 0.309 Lrg 0.2960 Thr 0.116 24.2001 M Palaquium hexandrum (Griff.) Baill Sapotaceae 1 0.286 Hmp 0.11 Exl 0.3260 San. 0.412 26.5944 H Payena lanceolata Ridl. Sapotaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M Payena maingayi Clarke Sapotaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Thr 0.116 21.3864 M Pittosporum ferrugineum W.T. Aiton Pittosporaceae 3 0.19 Hmp 0.11 Vsm 0.087 Thr 0.116 14.6076 L Polyalthia hookeriana King Annonaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Twi 0.191 22.6239 M Polyalthia michaelii C.T. White Annonaceae 1 0.286 Hmp 0.11 Med 0.1770 Twi 0.191 21.3387 M Polyalthia rumphii (Blume) Merr. Annonaceae 1 0.286 Hmp 0.11 Med 0.1770 Twi 0.191 21.3387 M Pometia pinnata J.R. Forst et G. Frost Sapindaceae 1 0.286 Mon 0.309 Exl 0.3260 Onc 0.281 29.5074 H Prainea limpato (Miq.) Beumee Moraceae 4 0.143 Mon 0.309 Vsm 0.087 Onc 0.281 20.1909 M Prunus arborea (Blume) Kalkman Rosaceae 1 0.286 Hmp 0.11 Sml 0.114 Onc 0.281 22.1433 M Prunus lamponga (Miq.) Kalkman Rosaceae 3 0.19 Hmp 0.11 Sml 0.114 Onc 0.281 17.6217 L Quercus argentata Korth Fagaceae 7 0.048 Mon 0.309 Exl 0.3260 Onc 0.281 18.2976 L Rhodamnia cinerea Jack Myrtaceae 1 0.286 Hmp 0.11 Med 0.1770 Thr 0.116 20.1012 M Rinorea anguifera (Lour.) Kuntze Violaceae 1 0.286 Hmp 0.11 Vsm 0.087 Thr 0.116 19.1292 L Shorea ovalis (Korth.) Blume Dipterocarpaceae 1 0.286 Hmp 0.11 Exl 0.3260 San 0.412 26.5944 H Shorea parvifolia Dyer Dipterocarpaceae 3 0.19 Hmp 0.11 Med 0.1770 San 0.412 20.4636 M Shorea platyclados Slooten ex. Fox Dipterocarpaceae 4 0.143 Hmp 0.11 Lrg 0.2960 San 0.412 19.5351 L Sterculia oblongata R. Br. Sterculiaceae 1 0.286 Mon 0.309 Sml 0.114 San 0.412 29.3793 H Sterculia parviflora Roxb. ex. G. Don Sterculiaceae 1 0.286 Mon 0.309 Lrg 0.2960 Onc 0.281 29.1834 H Strombosia javanica Blume Olacaceae 6 0.095 Hmp 0.11 Med 0.1770 Onc 0.281 13.8276 VL Symplocos crassipes C. B. Clarke Symplocaceae 2 0.238 Hmp 0.11 Sml 0.114 Twi 0.191 18.3975 L Syzygium flosculiferum (M. R. Hensd.) Sreek Myrtaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Twi 0.191 20.3631 M Syzygium kunstleri (King). Bahadur et R.C. Gour Myrtaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Twi 0.191 22.6239 M Syzygium lineatum (DC) Merr. ex L. M. Terry Myrtaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Onc 0.281 24.1089 M Syzygium politum (King). I.M. Turner Myrtaceae 1 0.286 Hmp 0.11 Sml 0.114 Twi 0.191 20.6583 M Syzygium rostrata Blume Myrtaceae 4 0.143 Hmp 0.11 Lrg 0.2960 Twi 0.191 15.8886 L Urophyllum macrophyllum Korth Rubiaceae 1 0.286 Dio 0.581 Sml 0.114 Thr 0.116 31.4313 VH Vitex vestita Wall. ex Schauer Verbenaceae 1 0.286 Hmp 0.11 Sml 0.114 Onc 0.281 22.1433 M Xylopia caudata Maingay ex. Hook. F. et Thomson Annonaceae 2 0.238 Hmp 0.11 Lrg 0.2960 Onc 0.281 21.8481 M Xylopia elliptica Hook.f and Thomson Annonaceae 1 0.286 Hmp 0.11 Lrg 0.2960 Onc 0.281 24.1089 M Note: Floral sexuality code; Dioecious (Dio), Monoecious (Mon), Hermaphrodite (Hmp). Seed size code; Extra large (Exl), Large (Lrg), Medium (Med), Small (Sml), Very small (Vsm). Flowering phenology code; Once (Onc), Twice (Twi), Throughout (Thr), Supra annual (San). PRR refers to the potential risk of regeneration failure. PRR code: Very high risk (VH), High risk (H), Medium risk (M),Low risk (L), and Very low (VL).
BIODIVERSITAS ISSN: 1412-033X Volume 19, Number 5, September 2018 E-ISSN: 2085-4722 Pages: xxxx DOI: 10.13057/biodiv/d1905xx