ARTICLES

Sci. Rep. Kanazawa Univ.
Vol. 63, pp. 45-58, 2019

Species composition of herbivorous insects and ants ontrees in the plantations of durian Durio zibethinus
and citrus fruits Citrus amblycarpa
in Tarakan Island of Borneo
Abdul RAHIM1, 2 * and Kyohsuke OHKAWARA1
1

Laboratory of Ecology, Division of Biological Sciences, Graduate School of Natural Science andTechnology, Kanazawa University, Kanazawa 920-1192, Japan2

Department of Agrotechnology, Agriculture Faculty, Borneo University, Tarakan,
North Kalimantan 77123, Indonesia(Received January 24, 2019 and accepted in revised form February 26, 2019)

Abstract In the tropics, the specific insect communities are observed in the fruit plantations as
one form of agroforestry systems. The information on the communities of herbivorous insects aspests and ants as pest-control agents could be useful in facilitating effective management ofplantations. Durian Durio zibethinus and citrus fruits Citrus amblycarpa are traditionally grown asagricultural products in the North Kalimantan region of Borneo, though the information on
herbivorous insects and ants remains scant. In this study, we assessed the species composition anddensities of herbivorous insects and ants inhabiting on trees in the plantations of durian and citrus
fruits in Tarakan Island of North Kalimantan. From 2016 to 2017, 55649 individuals of herbivores
comprised of 61 species and 64360 ant workers comprised of 25 species were collected by treebeating sampling on 59 durian and 63 citrus trees in three plantation sites (A-C). In citrus fruit
trees, aphid Toxoptera citridida was dominant in the herbivore communities. While, in durian trees,more than 80% of herbivores was occupied by various herbivore groups, leaf beetle, moth,
mealybug, psyllid and leafhopper. In ants, more than 60% of ants collected in each site was
occupied by three species Tapinoma melanocephalum, Technomyrmex albipes, and Oecophylla
smaragdina. NMDS analyses showed the patterns of classification in herbivorous insect and ant
communities were similar: the groups in site C could be classified, independent on the groups insite A and B. Probably, it may be caused by the environmental factors in site C. Otherwise, thecharacteristics of herbivores community are possibly affected by any interactions with ants,
resulting in the association among the structures of herbivore and ant communities. Our data could
provide useful information for the pest control activities in the plantations of durian and citrus fruitsin North Kalimantan.

Keywords.

herbivorous insects; ant; community; durian; citrus; plantation* Corresponding author

E-mail: arahim.ubt@gmail.com

46

1

Species composition of herbivorous insects and ants on durian and citrus trees

Introduction

Agroforestry systems (AF) are mixed cultivation systems that comprise crop plants and animals insome form of spatial arrangement or temporal sequence [1-3]. They offer a variety of ecosystemservices beyond food production, including recycling of nutrients, regulation of microclimates,
facilitating hydrological processes, and enabling more diverse farm activities [4-6]. Plantation
agriculture is one of form of agroforestry. In the tropics, numerous crops, such as cacao, oil palm,and some woody species have been planted and the production activities are managed by humanactivities. In the lowlands of Southeast Asia, many tropical fruits including banana, mango, andpineapple, are also cultivated through plantation farming. Such fruit production activities are someof the major agricultural services in Indonesia and Malaysia.
Agroforestry systems support a wide variety of organisms and high biodiversity [6-9]. Tropicalfruit plantations are habitats for herbivorous insects that exploit the plant resources, including
flowers, fruits, seeds, and leaves. Specific communities of herbivorous insects are frequently
observed in the plantations. However, many herbivores are regarded as fruit pests, with considerable
negative impacts on production activities. Therefore, information of herbivorous insect communities
could be critical for plantation management. In plantations of some tropical fruits in Southeast Asia,
the characteristics of herbivorous insect communities, such as species composition, densities, anddistribution have been monitored by researchers from public institutions. In addition, the plantations
are adversely affected by the presence of ants, which are one group of social insects [8, 10-11]. Ant
biomass is highest among all animals in the tropics. They influence ecosystem as predators, prey,scavengers and symbionts in both degraded and natural habitats [12]. Particularly, the predatoryrole of ants is important in plantations, where they have a negative effect on for herbivorous insect
populations [13-14]. However, some ant species exhibit mutualistic interactions with some aphids
and mealybugs by attending them on trees of some fruit species. Consequently, such interactions
could have negative effects on fruit tree species in any cases. Ants interacts with herbivorous insects
in diverse ways. Therefore, the characteristics of herbivorous insect communities in plantations
could similarly be influenced by ant communities in various ways.
Information on insect herbivore communities and ants, acting as pests and as pest control agents,
respectively, could be useful in facilitating effective management of plantations. Durian, Durio
zibethinus, and citrus fruits, Citrus amblycarpa, are traditionally grown in agroforestry plantationsin the North Kalimantan region of Borneo [15]. However, the information on herbivorous insects
and ants inhabiting the plantations in the region remains scant, though it is suggested that the largest
part of the arthropod biomass is rich [16-18]. In the present study, we assessed species compositionand densities of herbivorous insects and ants in the field with the aim of obtaining data on arboreal
insect and ant communities in durian and citrus fruit plantations.

2

Methods

Field studies were conducted in the Tarakan Island in Borneo, Indonesia (Fig. 1). Three plantationsites were selected on the island: site A at Mamburungan (3°18'15''N, 117°37'12''E), site B at East
Mamburungan (3°17'14''N, 117°38'1''E), and site C at Kampung Enam village (3°18'41''N,
117°38'1''E). All three plantations were opened 7-8 years ago. Durian D. zibethinus and citrus fruits,
C. amblycarpa were planted in that time. Citrus fruits as non native species were introduced.
Horticultural crops, including, banana, mango, maize, cabbage, and other crops were also planted in
the sites.

Abdul RAHIM and Kyohsuke OHKAWARA

47

Figure 1 Map of Tarakan island and the location of three study sites (copyright of the source of themaps: CatroGIS Services, College of Asia and the Pacific, The Australian National University).

The plantations in site A and C were established in open land including grassland and plowed
field. The densities of crop trees were low and the height of crop trees was relatively low. The
plantations in site B were adjacent to secondary forests and shrubs at hilly area. Many trees otherthan durian and citrus were present within and around the plantation. The height of crop trees was
relatively high. Although the farmers did not extensively apply pesticides in the study areas, weed
and pest management activities were sometimes carried out using herbicides and various types of
insecticides. However, such the management activities had minimal impacts on ants, since the pest
and weed management activities were not frequent.
In the plantations, we set up a study area covering 2.0 ha (200 m × 100 m), where many durian
and citrus fruits were under intense cultivation. In site A and C, we selected 66 (D. zibethinus: 44
and C. amblycarpa: 22) and 30 (D. zibethinus: 15 and C. amblycarpa: 15) trees as trees to be sampled,
respectively. In site B, only 26 citrus trees were selected. Collection of arboreal insects and ants
was carried out from March to September in 2016 and 2017. Ten branches (length: 50–80 cm,
diameter: 5–10 cm) in a tree were selected and insects and ants that were present on them werecollected by using tree beating method. In the case of insect species such as aphids, mealybugs, andfruit flies, the number of insects on 20 branches was counted. The number of ants walking on an
additional 20 branches was also counted. In site A and B, the collection and counting activities werecarried out 1-7 times, while they were carried out 1-2 times in site C. All collected samples werestored in 99% ethanol and sorted in the laboratory. Subsequently, the species of insects and ants
were identified, using identification manuals and online resources.
Frequency of species and the densities in insects and ants were compared among three sites by
calculating the average of collected number (/branch/tree/sampling time). To compare the species
composition and community structures, non-metric dimensional scaling (NMDS) analyses werecarried out. The differences in the community structures were quantified based on presence orabsence of species. The similarity matrix was then reduced to a two-dimensional ordination.
Packages vegan and MASS in R (R Core Development Team) were used for NDMS analyses.

48

3Species composition of herbivorous insects and ants on durian and citrus trees

Results

From 2016 to 2017, we collected 55649 herbivorous insect individuals, comprised of 61 species
from 60 genera, 32 families, and five orders, in three sites. They were mainly collected from thesurfaces of leaves, flowers, and fruits. To evaluate the composition of the herbivore species, weclassified the collected insects under the following 11 functional groups based on scientificclassification and foraging behavior:(1)

Leaf beetle: beetles specializing on feeding on leaves, flowers, pollen, nectar, and other plantparts, belonging to the families Chrysomelidae, Meloidae, Cerambycidae, Mordellidae, andother families in order Coleoptera(2) Weevil: beetles belonging to the superfamily Curculionidae in the order Coleoptera(3) Fruit fly: tephritid fruit flies in the family Tephritidae in the order Diptera(4) Leaf-miner fly: flies feeding on leaves belonging to the family Agromyzidae in the order
Diptera(5) Aphid: small-sucking hoppers of the family Aphididae in the order Hemiptera(6) Mealybug: scale insects in the families Pseudococcidae and Coccidae in the order Hemiptera(7) Leafhopper: small-sucking hoppers in the family Cicadellidae in the order Hemiptera(8) Psyllid: small-sucking insects in the superfamily Psylloidea superfamily in the order
Hemiptera(9) Other bugs: other sucking bugs, sap-sucking bugs, and stink bugs in the family Lygaeidae,
Corediae, Pentatomidae, and other families in the order Hemiptera(10) Moth and Butterfly: larvae and adults of lepidopterans in the order Lepidoptera(11) Thrip: thrips in the family Thripidae in the order Thysanoptera

Table 1

Species and collection number of herbivorous insects on durian trees in the two sites.

Functional Group

Order

FamilySpeciesCollection number
A

Leaf beetle

Coleoptera

C

Cantharidae

Mimopolemius sp. 1

19

1

Cerambycidae

Unknown sp. 1

1

1

Chrysomelidae

Aulacophora similis

253

10

Unknown sp. 3

111

Unknown sp. 4

15

0

Unknown sp. 5

99

2

Unknown sp. 6

14

1

Unknown sp. 7

1

1

Lema pectoralis

13

2

Menolepta bifasciata

01

Mimastra pallida

50Phratora vitellinae

134

3

Rhabdoscelus leprosus

10

2

49

Abdul RAHIM and Kyohsuke OHKAWARA

WeevilFruit flyLeaf-miner fly

Coleoptera

Diptera

DipteraMeloidae

Epicauta sp.1

320Mordellidae

Tolidopalpus nitidicoma

10

Tolidopalpus sp. 1

30

Nitidulidae

Carpophilus mutilatus

20

Tenebrionidae

Atoichus pemanoa

10Curculionidae

Alcidodes sp. 1

01

Hypomeces squamosus

79

0

Omobaris calentus

40

Sternochetus trigidus

51

Xylosandrus mongerus

13Bractocera dorsalis

58

Unknown sp. 8

121

Chromatomyia sp. 1

120

Liriomyza sp. 1

277

0

Ophiomyia sp. 1

55

0

Unknown sp. 925

4Thepritidae

Agromyzidae

Aphid

Hemiptera

Aphididae

Toxoptera citridida(Aphis tavaresi)

83

4

MealybugHemiptera

CoccidaeCoccus viridis

750

Pseudococcidae

Planococcus citri

1089

28

Cicadellidae

Idioscopus clypealis

663

372

Unknown sp. 10

21

9

Unknown sp. 11

14

3

Unknown sp. 12

14

1

Ricaniidae

Unknown sp. 13

05Leafhopper

Hemiptera

Psyllid

Hemiptera

Carsidaridae

Allocaridara malayensis

250

581

Other bugs

Hemiptera

Aleyrodidae

Leptocorisa acuta

114CoreidaePhysomerus grossipes

130

Lygaeidae

Unknown sp.14

2

2

Pentatomidae

Cappaea taprobanensis

38

3

Nezara viridula

150

Pyhrocorridae

Dysdercus sp. 1

01

Reduviidae

Sycanus sp. 1

10

TingidaeUnknown sp. 15

60

Gracillariidae

Unknown sp. 16

21

0

Unknown sp. 17

73

10

Licaenidae

Unknown sp. 18

0

5

Lymantriidae

Unknown sp. 19

10Noctuidae

Unknown sp. 20

27

0Moth and Butterfly

Lepidoptera

50Species composition of herbivorous insects and ants on durian and citrus trees

Thrip

Thysanoptera

Psychidae

Mahasena sp. 1

27

2

Pyralidae

Citripestis sagittiferella

255

19

Unknown sp. 22

91

Unknown sp. 23

32

0

Phlaeothripidae

Haplothrips sp. 1

3

3

Thripidae

Megalurothrips usitatus

56

0

0.001

0

Thrips parvispinus

Table 2

Species and collection number of herbivorous insects on citrus trees in the three sites.
Collection number

Functional group

Order

FamilySpeciesA

Leaf beetle

Coleoptera

Coleoptera

C

Cantharidae

Mimopolemius sp. 1

6

0

0

Cerambycidae

Neospondylis sp. 1

1

1

0

Unknown sp. 1

0

3

0

Unknown sp. 2

0

1

0

Aulacophora similis

26

50

2

Unknown sp. 3

1

1

0

Unknown sp. 4

5

4

0

Unknown sp. 5

10

19

2

Unknown sp. 6

4

2

0

Unknown sp. 7

25

5

0

Lema pectoralis

2

2

0

Menolepta bifasciata

1

0

0

Mimastra pallida

1

5

0

Phratora vitellinae

12

17

2

Rhabdoscelus leprosus

5

5

1

Languriidae

Languria mozardi

0

3

0

Meloidae

Epicauta sp. 1

15

21

1

Mordellidae

Tolidopalpus nitidicoma

2

0

0

Tolidopalpus sp. 1

1

0

0

Nitidulidae

Carpophilus mutilatus

31

20

0

Tenebrionidae

Atoichus Pemanoa

0

1

0

Curculionidae

Alcidodes sp.1

0

1

0

Hypomeces squamosus

48

197

0

Omobaris calentus

1

1

0

Sternochetus trigidus

5

3

0

Xylosandrus mongerus

2

1

0

Chrysomelidae

WeevilB

51

Abdul RAHIM and Kyohsuke OHKAWARA
Fruit flyLeaf-miner fly

Diptera

DipteraThepritidae

Agromyzidae

Bractocera dorsalis

14

80

5

Unknown sp. 8

2

7

0

Chromatomyia sp. 1

26

5

0

Liriomyza sp. 1

57

73

2

Ophiomyia sp. 1

15

7

0

Unknown sp. 9

4

6

8

7614

33696

3523

3

0

0

Aphid

Hemiptera

Aphididae

Toxoptera citridida(Aphis tavaresi)

MealybugHemiptera

CoccidaeCoccus viridis

Pseudococcidae

Planococcus citri

2920

1168

163

Cicadellidae

Idioscopus clypealis

11

27

12

Unknown sp. 10

7

83

1

Unknown sp. 11

0

3

0

Ricaniidae

Unknown sp. 13

0

1

1

Leafhopper

Hemiptera

Psyllid

Hemiptera

Carsidaridae

Allocaridara malayensis

2

14

103

Other bugs

Hemiptera

Aleyrodidae

Leptocorisa acuta

0

1

0

Lygaeidae

Unknown sp. 14

5

12

0

Pentatomidae

Cappaea taprobanensis

54

16

5

Nezara viridula

1

9

2

Pyhrocorridae

Dysdercus sp. 1

13

2

0

Reduviidae

Sycanus sp. 1

4

0

0

TingidaeUnknown sp. 15

2

0

0

Gracillariidae

Unknown sp. 16

1

1

0

Unknown sp. 17

1

2

1

Licaenidae

Unknown sp. 18

0

1

1

Lymantriidae

Unknown sp. 19

1

12

2

Noctuidae

Unknown sp. 20

1

2

0

PieridaeUnknown sp. 21

0

2

0

Psychidae

Mahasena sp. 1

15

9

5

Pyralidae

Citripestis sagittiferella

14

22

24

Unknown sp. 22

0

3

0

Unknown sp. 23

10

0

0

Phlaeothripidae

Haplothrips sp. 1

11

10

0

Thripidae

Megalurothrips usitatus

33

27

1

Thrips parvispinus

6

1

0

Moth and Butterfly

Thrip

Lepidoptera

Thysanoptera

Figure 2 illustrates the species composition in durian and citrus fruit trees in the three sites. The
compositions were considerably varied among the three sites and among fruit tree species (site:χ2=1961.4, P<0.01, fruits: χ2=4592.5, P<0.01, G-test). In citrus fruit trees, the aphid Toxoptera

52

Species composition of herbivorous insects and ants on durian and citrus trees

citridida a synonym of Aphis tavaresi, was dominant among the insect herbivore communities (site
A: 68.9%, site B: 94.5%, site C: 91.1%). In durian trees, more than 80% of the insect herbivores
fell under numerous functional groups, including leaf beetles, moths and butterflies, mealybugs,
psyllids, and leaf hoppers. The compositions of groups were different between site A and C. In allsites, the following nine species were dominant: leaf hopper Idioscopus clypeus, mealy bug
Planococcus citri, green weevil Hypomeces squamosus, leaf miner fly Liriomyza sp. 1, aphid T.
citridida, durian psyllid Allocarsidara malayensis, leaf beetle Aulacophora similis, stink bug
Cappaea taprobanensis, and citrus fruit borer Citripestis sagittiferella.

Figure 2 Frequency of functional groups of herbivorous insects in two fruit species at three sites. AD
and AC: durian and citrus fruit trees in site A, BC: citrus fruit trees in site B, CD and CC: durian andcitrus fruit trees in site C.

In the three sites, 64360 ant workers were collected. They were comprised of 22 species from
16 genera and five subfamilies (Table 3). Three species, including Tapinoma melanocephalum,
Technomyrmex albipes, and Oecophylla smaragdina accounted for more than 60% of all the worker
ants in each site (Fig. 3). They dominated the trees by nesting in branches and trees and building
weaver nests on trees. In addition, species composition was significantly varied among three sites(χ2=22413.2, P<0.01, G-test). In site A and B, T. melanocephalum and O. smaragdina were
dominant, while T. albipes and O. smaragdina were dominant in site C. However, ant species
composition was not substantially different between durian and citrus fruits trees.

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Abdul RAHIM and Kyohsuke OHKAWARA

Table 3Species and collection number of arboreal ants on durian and citrus trees in the three sites.
Collection number
Subfamily

Species

DurianA

CitrusC

A

BCPonerinae

Ponera sp.1

4

0

0

1

0

Dolichoderinae

Dolichoderus sp. 1

0

2

2

2

6

Iridomyrmex anceps

3101

15

670

371

49

Philidris sp.1

541

1

245

71

0

19703

3

7106

4020

42

96

30

192

45

0

Technomyrmex albipes

3945

2363

1509

383

697

Anoplolepis gracilipes

1031

0

1294

697

11

Oecophylla smaragdina

5923

578

2208

294

455

Camponotus sp. 1

49

1

8

7

0

Polyhachis sp. 1

22

5

7

47

3

Tetraponera sp. 1

281

8

44

66

0

Tetraponera sp. 2

30

0

19

1

0

Crematogaster sewardi

1314

4

807

592

14

Crematogster sp. 1

753

28

53

65

20

Crematogster sp. 2

139

0

6

14

0

Trichomyrmex destructor

2099

16

613

341

4

Monomorium sp. 1

350

0

52

0

0

Monomorium sp. 2

48

0

92

37

0

Tetramorium sp. 1

67

8

499

119

30

Tetramorium sp. 2

22

0

10

26

0

Pheidole sp. 1

16

0

0

4

0

Tapinoma melanocephalum
Tapinoma sp. 1

Formicinae

Pseudomyrmicinae

Myrmiciane

Figure 4 illustrates the classification of herbivorous insects and ant groups in fruit tree species
and sites. The patterns of classification were similar between (Fig. 4a) and ants (Fig. 4c): the groups
in site C were classified by NMDS 1 as independent of the groups in site A and B. In herbivorous
insects, 27 among 61 species had significant correlation with NMDS axes. The classifications ofgroups in site C were characterized by Idioscopus clypealis and Ricaniidae sp. (unknown sp. 13) as
leafhopper and C. sagittiferella and Gracillariidae sp. (unknown sp. 16) as moth and butterfly (Fig.
4b, Table 1 and 2). In ants, 21 among 25 species had significant correlation with NMDS axes andthe classifications of site C were characterized by T. albipes as the dominant species in the site (Fig.

54

Species composition of herbivorous insects and ants on durian and citrus trees4d). In addition, NMDS1 in the classification of herbivorous insects was significantly correlatedwith NMDS axes in the classification of ants (r2=0.47, P<0.0001), indicating that the species
composition of the herbivorous insects was associated with that of ants.

Figure 3 Frequency of ant species in two fruits at three sites. AD and AC: durian and citrus fruit
trees in site A, BC: citrus fruit trees in site B, CD and CC: durian and citrus fruit trees in site C.

4

Discussion

The species compositions of herbivorous insects in the plantations were different among fruit tree
species and sites. In citrus fruit, C. amblycarpa, the aphid T. citridida was dominant in all sites. It
is one of representative pests of citrus and vectors of the pathogenic plant virus [19]. Moreover,
the aphid is an invasive species that is widely distributed in the world, with considerable adverse
effects on the farming of citrus fruits. The results indicate pest control activities against the aphid
would be required to manage to the citrus fruit plantations in North Kalimantan. In durian, D.
zibethinus, the herbivorous insect communities were composed of more species and functionalgroups. In site A, the community was composed of many herbivore groups, while psyllid A.
malayanensis and leafhopper I. clypeus were dominant in site C. Durian has more potential
resources for various herbivorous insect groups, while citrus is mainly exploited by a specific insectgroup. In future, more extensive control strategies and techniques for various pests should be carriedout for the effective management of durian plantations.

Abdul RAHIM and Kyohsuke OHKAWARA

55

Figure 4 Classification of species composition in herbivorous insect and ant communities by NMDS.
(a) and (c) show the biplots of NMDS in herbivorous insects and ants. The symbols circle, rhombus andtriangle, mean site A, B, and C respectively. Black and white symbols mean durian and citrus trees. (b)and (d) show the ordinations of each species which had significant correlation with NMDS. In (b) and(d), the species name characterized the groups was shown.

The classification patterns derived from NMDS analyses tended to be similar for herbivorous
insect and ant communities. In particular, the species composition in site C was independent of
those of the two other sites, which was potentially because of two factors. The characteristics ofherbivorous insect and ant communities may be determined by various environmental factors in site
C, including natural and geographical conditions. In general, the community structures could begreatly influenced by environmental factors [20]. For example, the plantations in site C were
established in open land with relatively low tree densities. Such forest conditions may represent

56Species composition of herbivorous insects and ants on durian and citrus trees

unique environmental conditions, which limit the species inhabiting in the plantations, resulting inspecific communities exploiting such environments. Additionally, the characteristics of herbivore
communities could be influenced by interactions with ants. In site C, T. albipes was dominant andinfluenced the classification of ant communities. Blüthgen et al. [21] reported that T. albipes had
trophobiotic interactions with 22 leafhopper species of the family Cicadellidae in a tropicalrainforest of Borneo. Some psyllid species in the family psyllidae were also attended by some ants
[22-23]. Therefore, the attendance by T. albipes possibly increased the densities of leafhopper I.
clypealis and psyllid A. malayensis. Moreover, the densities of T. melanocephalum, which were thedominant species in the two other sites, were lower in site C. The ant is an invasive species and amajor predator of other insects and arthropods [24-25]. Low densities of T. melanocephalum may
result in high densities of any herbivorous insects, C. sagittiferella and Gracillariidae sp. (unknown
sp. 16), characterized the classification of herbivore communities in site C. Such interactions may
result in the association among the species composition of herbivore and ant communities. To test
the hypotheses, response of T. albipes and T. melanocephalum to herbivorous insects and theirinteractions should be investigated in the field.
In our study, the number of sampling and trees was smaller in site C than site A and B. The data
may be biased among the sites by such the difference of sampling efforts; the collection data in site
C is underestimated. As a possibility, herbivorous insect communities on durian trees in site C may
be composed of more various species. Additionally, in ant communities in site C, O. smaragdina
and I. anceps are more dominant. For the exact comparison of the communities among the plantationsites, more sampling efforts are needful. However, the data of our study presents basic data on
herbivorous insect communities in durian and citrus fruit plantations in North Kalimantan. In
collected insect species, it had been reported that H. squamosus, A. malayensis, and P. citri were themajor durian pests while T. citridida, C. taprobanensis, C. sagittiferella, P. citri, and H. squamosus
were the major citrus fruit pests [19, 26-27]. Effective pest control methods and techniques could
facilitate the proper management of the plantations. Furthermore, many arboreal ants haveimportant predator roles against herbivorous insects and arthropods in the plantations [28-32]. In
plantation managemant starategies, arboreal ants have been used to control herbivorus insects in theplantations [33-36]. Our study could provide useful informmation for the pest control activities
using ants in durian and citrus fruit plantations in North Kalimantan.

Acknowledgments
We are grateful to our field assistants and laboratory assistants, Muttaqien, Wisnu Ageng, Philipus
and the staffs of the Agriculture Faculty, University of Borneo Tarakan. Cordial thanks go to theowners of farmers in the studied sites of Tarakan island. We thank CartoGIS Service, College of
Asia and the Pacific for using the map data. Our study in Kanazawa University was funded by
BPPLN-RISTEKDIKTI scholarship of Indonesian Ministry of Research, Technology, and Higher
Education.

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