Research ArticleDiversity of Wild Bees along Elevational Gradient inan Agricultural Area in Central Java Indonesia

Imam Widhiono Eming Sudiana and Darsono Darsono

Faculty of Biology Jenderal Soedirman University Jl Dr Soeparno no 63 Purwokerto Central Java 53122 Indonesia

Correspondence should be addressed to ImamWidhiono imamwidhionoyahoocom

Received 6 December 2016 Accepted 12 January 2017 Published 31 January 2017

Academic Editor Jacques Hubert Charles Delabie

Copyright copy 2017 ImamWidhiono et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Increases in mean temperature affect the diversity and abundance of wild bees in agricultural ecosystems Pollinator communitycomposition is expected to change along an elevational gradient due to differences in the daily ambient temperature This studyinvestigated the diversity and abundance of wild bees in an agricultural area along an elevational gradient in Central Java IndonesiaWild bees were collected using a sweep net in 40 green bean (Phaseolus vulgaris) cultivation sampling locations at seven differentelevations (8 108 224 424 644 893 and 1017m above sea level) Species diversity was determined using the ShannonndashWienerdiversity indexWe identified 932 individuals from8 species of wild bee belonging to 3 familiesThe familyApidaewas predominantwith 6 species while only 1 species was found from each of Megachilidae and Halictidae Across the study sites diversity increasedwith increasing elevation ((1198671015840) = 14 (119863) = 025 and (119864) = 078 at low elevation to (1198671015840) = 204 119863 = 013 and 119864 = 096 at highelevation) and higher numbers of species were found at middle and high elevations Species richness and abundance increasedlinearly with increasing elevation and species diversity was highest at middle elevations

1 Introduction

Wild bees (order Hymenoptera Apoidea) represent the mostimportant group of pollinator insects because they play akey role in agriculture pollinating almost all crop varietiesHowever they are increasingly at risk of local and even globalextinction due to climate change [1] which can disrupt theoverlap of flower production and pollinator flight activity[2] The major characteristic of climate change is an increasein the mean global temperature Elevated temperatures areknown to influence the foraging activity body size at matu-rity and individual lifespan [3] of wild beesThe physiologicalimpacts of climate warming might not have negative effectson individual insect pollinators in fact some could evenhave positive effects Increases in mean temperature affectthe diversity and abundance of wild bees in agriculturalecosystems

Elevational gradients can be used as model systems forclimatic change to analyse the role of environmental filteringeffects on animal communities [4] Comparative studies of

species ecology along elevational gradients can provide cluesto the likely response of both species and communities inthe study of the effects of increasing temperature on thediversity and abundance of pollinator insects However thereare significant differences among the characteristics of typicalelevational gradients Pollinator community composition isexpected to change along an elevational gradient due todifferences in ambient daily temperature Due to the harsherenvironmental conditions the number of pollinator speciestends to decrease with increasing elevation [5] The relativeabundance of Hymenoptera has been negatively correlatedwith increasing elevation [6] However some studies havefound that Hymenoptera especially wild bees are the mostabundant floral visitor at high elevations at least for someplant species [7] Total pollinator richness [8] and abundance[9] have been found to decrease with increasing elevationwith plants becoming more ecologically specialised at higherelevations [10] However to the best of our knowledgethe wild bee diversity and abundance along an elevationalgradient in agricultural areas has not previously been studied

HindawiPsycheVolume 2017 Article ID 2968414 5 pageshttpsdoiorg10115520172968414

2 Psyche

Elevation

0

2

4

6

8

10Sp

ecie

s ric

hnes

s

8m

asl

108

m as

l

224

m as

l

424

m as

l

644

m as

l

893

m as

l

1017

m as

l

(a)

0

50

100

150

200

250

Abun

danc

e

Elevation

8m

asl

108

m as

l

224

m as

l

424

m as

l

644

m as

l

893

m as

l

1017

m as

l

(b)

Figure 1 Species richness (a) and abundance (b) of wild bees among elevation

in Java In this study we investigated the diversity andabundance of wild bees in an agricultural area along anelevational gradient to test the hypothesis that elevation isa significant factor underlying the species composition andabundance of wild bees

2 Materials and Methods

21 Study Area The study was conducted in areas of greenbean (Phaseolus vulgaris) cultivation at seven locations alongan elevational gradient Lomanis Cilacap Regency (7∘411015840063210158401015840N 109∘01101584012 2410158401015840E 8m above sea level (asl)) GunungTugel Purwokerto (7∘28101584003 9210158401015840N 109∘14101584006 3510158401015840E 106m asl)Banteran Sikapat and Banyumas Regency (7∘20101584000 4310158401015840N109∘16101584029 4910158401015840N 224 and 442m asl resp) Limpakuwus andTuwel Tegal Regency (7∘09101584046 3810158401015840N 109∘09101584006 6610158401015840E 664and 887m asl) and Serang Pubalingga Regency (7∘141015840484110158401015840E 109∘17101584028 9110158401015840N 1077m asl) In the regions green beanis a minor vegetable crop that extensive planting is usuallyvery small and located on land planted with other types ofvegetables such as long bean but as for research purposesthis plant was chosen because it was found at all altitudes

22 Sampling of Bee Diversity and Identification The sevenlong bean plantations were sampled twice each month fromApril to June 2014 We collected 100 plant individuals ateach site using the standard sweep net procedures describedby Brosi et al [11] (2008) to sample the bees During eachsampling session 14 members of the field team (two personsper location) aerially netted bees over 30min periods Beesboth on flowers and in flight were collected individuallywith the sweep net Sampling was performed in the morning(0700ndash0900 local time) on fine days Bee species wereidentified by the Indonesian Institute of Science BogorVoucher specimens are held at the Entomology LaboratoryFaculty of Biology Jenderal SoedirmanUniversity Indonesia

23 Statistical Analyses The species richness and abundanceof wild bees recorded in the seven plots were analysedA general linear model was applied using SPSS ver 180software The dependent variables were wild bee speciesrichness and abundance and the categorical variables wereelevation and daily temperature Raw data from the field wereused to reveal species richness species diversity (ShannonndashWeiner index) component of dominance (Simpson domi-nance index) and relative abundance of different species ateach sampling site [12] Comparisons of species compositionaccording to location were performed using single linkagecluster analysis based on BrayndashCurtis similarity All diversityparameters were analysed using Biodiversity Pro software[13]

3 Results and Discussion

31 Species Composition In total 932 individual wild beesbelonging to 8 species 5 genera and 3 families were collectedduring the study period Apidae was themost dominant fam-ily with 6 species (Xylocopa latipes X confusa X caeruleaApis cerana A dorsata andAmegilla cingulata) and two fam-ilies (Megachilidae and Halictidae) were represented by onespecies eachThe composition of wild bee species found at theseven elevations varied with the largest number of species(8) at the middle-to-high elevations (442ndash1017m asl) andthe lowest species richness at the lowest elevation (8m asl)with only 3 species Xylocopa latipes X confusa Apis ceranaand Megachile relative were observed at most elevationsApis dorsata and Xylocopa caerulea were found only at themiddle and high elevations (Figure 1(a)) Species richnessdiffered significantly among elevations (analysis of variance(ANOVA) F649 = 5445 p = 0000223 lt 005) Increasing ele-vation increased wild bee species richness up to 893m asl (R2= 084) and then decreased species richness above 1017m asl(Table 1)

Psyche 3

Table 1 Species composition abundance and diversity of wild bees and seven different elevations

Species Elevation m above sea level (asl) Abundance Relative ()8 108 224 424 644 893 1017Xylocopa latipes 18 26 25 27 26 22 16 160 1716Xylocopa confusa 15 14 19 44 26 19 23 160 1716Xylocopa caerulea 0 0 0 15 29 31 22 97 104Apis cerana 20 23 37 44 38 27 0 189 202Apis dorsata 0 0 0 21 26 16 11 74 79Amegilla cingulata 1 4 11 8 22 13 17 76 81Megachile relativa 9 10 11 16 20 18 19 103 1105Lasioglossum malachurum 0 7 13 12 14 13 14 73 78Abundance 63 84 116 187 201 159 122 932Relative () 67 901 1244 2006 2156 1706 1309Mean temperature ∘C 343 325 312 304 298 29 287Shannon H 1408 1622 1684 193 2045 2035 1919Simpson 1-D 0740 0778 07944 08361 08665 08634 08498Evenness eandHS 0817 0843 0897 0860 0966 0956 0973

32 Abundance In total 932 individual wild bees belongingto 8 species 5 genera and 3 families were recorded Site 1supported 4 species with 63 individuals (58 of all indi-viduals) Site 2 5 species and 84 individuals (901) Site 35 species and 116 individuals (1244) Site 4 7 species and187 individuals (2006) Site 5 8 species and 201 individuals(215) Site 6 8 species and 169 individuals (1706) and Site7 7 species and 122 individuals (1309) (Figure 1(b))

Wild bee abundance differed significantly among sites(ANOVA F649 = 3478 p = 0006 lt 005)Themost abundantspecies was Apis cerana with 189 individuals (202) fol-lowed by X confusa and X latipes each with 160 individuals(1716)M relativawith 103 individuals (1105)X caeruleawith 97 individuals (104) A cingulata with 76 individuals(81) and A dorsata with 74 individuals (79) and theleast abundant was Lmalachurumwith 73 individuals (78)Comparing the wild bee abundance among sampling eventsat all elevations the highest abundance was from samplingnumber 2 with 199 individuals (213) followed by samplingnumber 1 with 172 individuals (184) sampling number 4with 157 individuals (168) sampling number 3 with 148individuals (158) sampling number 5 with 136 individu-als (145) and the lowest abundance was from samplingnumber 6 with 120 individuals (128) However statisticalanalysis revealed no significant differences among samplingevents (ANOVA F542 = 101800 119901 = 0419 gt 005)

Across the study sites diversity increased with increasingelevation (ShannonndashWiener index (1198671015840)= 14 dominance (119863)= 025 and evenness (119864) = 078 at low elevation to (1198671015840) =204 119863 = 013 and 119864 = 096 at high elevation) and highernumbers of species were found atmiddle and high elevationsThe distribution of wild bees among the sites was significantlyinfluenced by elevation The richness abundance diversityand evenness of wild bees at different sites are presented inTable 1

Analysis of community structure similarity among eleva-tions showed that the three sites categorised as low elevation(8ndash224m asl) had high similarity (8453) the two middle-elevation sites (424ndash644m asl) had 8350 similarity and

8m asl108m asl224m asl424m asl644 m asl893m asl1017m asl

0 50 100

similarity

BrayndashCurtis cluster analysis (single link)

Figure 2 Similarity (BrayndashCurtis) single linkage of wild bee inseven different elevations

the two high-elevation sites (893mndash1017m asl) had 797similarity However the highest species similarity (872)was found between Site 5 (644m asl) and site 6 (893m asl)(Figure 2)

4 Discussion

The number of wild bee species and the species compositionrecorded in this study were similar to those reported inprevious studies in various regions Hoiss et al [14] observed10 species of wild bees atVigna unguiculata in Ghana belong-ing to the families Apidae (Xylocopa Apis and Amegilla)Megachilidae (Megachile eurymera) and Halictidae (Nomiasp) Kwapong et al [15] reported that the main insectsobserved on cowpea flowers were bees such as Apis melliferaCeratina sp Megachile sp Xylocopa calens Xylocopa imita-tor Braussepis sp Lipotriches sp Melecta sp and Amegillasp Kingha et al [16] reported Apis mellifera as the mostabundant insect species visiting P vulgaris flowers in Kenyafollowed by Xylocopa calens and X inconstans The flowers oflong bean attract wild bee pollinators from Apidae probablybecause themembers of this family have sufficient strength toopen the flower to collect pollen and nectar [17] However tothe best of our knowledge to date there have been no studieson insect pollinator diversity in green bean cultivation areas

4 Psyche

in Indonesia for comparison purposes In Sukabumi WestJava in mustard (Brasica rapus) at an elevation of approx-imately 854m asl Aouar-Sadli et al [18] observed insectpollinators from the order Hymenoptera family Apidaesubfamily Apinae consisting of the species Apis cerana Apisdorsata and Trigona sp from the subfamily Xylocopinae thespecies Xylocopa caerulea X confusa X latipes and Ceratinasp from the family Colletidae subfamily Hylaeinae Hylaeussp from the family Halictidae subfamily Nomiinae Nomiasp and from the family Scoliidae Compsomeris lindenniOur study findings indicate that the species composition ofinsect pollinators on agricultural land is dominated by wildbees

Elevation strongly influenced the diversity and abun-dance of wild bee communities Species richness and abun-dance increased linearly with increasing elevation andspecies diversity was highest at middle elevations Theseresults are inconsistent with those of Gottlieb et al [19]who reported that the diversity and abundance of wildbees decreased linearly with increasing elevation from 60 to2000m asl This difference may be due to differences in thegeographical region climate zone and range of elevationalgradient A commonly reported pattern in species richnessalong elevational gradients is a unimodal distribution with amid-elevation peak [20] In our study peak species diversityoccurred at middle elevations due to the presence of twospecies (Apis dorsata and Xylocopa caerulea) that began toappear above 442m asl The presence of the giant honeybee (A dorsata) at mid-to-high elevations may be due tohabitat suitability rather than elevation effects because thesebees require a forested habitat with high trees whereas bluecarpenter bees tend to be abundant in cool environmentsLarge carpenter bees (genusXylocopa) are wood-nesting gen-eralist pollinators of broad geographical distribution Theirforaging is characterised by a wide range of food plants longseason of activity tolerance of high temperatures and activityunder low illumination levels [21] Carpenter bees toleratehigh ambient temperatures during foraging andmost speciesare inactive at low temperatures and these bees were foundin all of our study sites All of the sites from the lowest tohighest elevation had daily temperature ranges appropriatefor wild bees Generally the genus Xylocopa is able to movearound well in a daily temperature range of 25ndash35∘C [22]This heat tolerance suggests efficient heat regulation abilityin carpenter bees possibly controlled by a thermoregulatorycentre in the prothorax [23] In contrast Apis cerana has atendency to forage in conditions of warm temperatures [24]The presence of the three speciesMegachile relativa Amegillacingulata and Lasioglossum malachurum almost evenly atall elevations studied indicates that these species are able tomove around in the range of temperatures that occur at theseelevations

5 Conclusion

Eight species of wild bees from four families of the orderHymenoptera were recorded in green bean cultivation areasat seven different elevations in Central Java IndonesiaSpecies richness and abundance increased linearly with

increasing elevation and species diversity was highest atmiddle elevations

Disclosure

TheEnglish in this document has been checked by at least twoprofessional editors both native speakers of English For acertificate please see httpwwwtextcheckcomcertificateA8au11

Competing Interests

The authors declare that they have no competing interests

Acknowledgments

The authors are grateful to Yulia Arnitasari Tutut KusumaWahyuni Ismayanti Pangalinan Riadiana Sulistyaningrumand Ganesha Rifky Rinaldi for assistance with data collectionand their encouragement of this study from its inceptionThisstudy was a part of a larger research programme funded byJenderal Soedirman University They also thank the heads ofthe Institute of Research and Community Services JenderalSoedirman University for their support

References

[1] J C Biesmeijer S P M Roberts M Reemer et al ldquoParalleldeclines in pollinators and insect-pollinated plants in Britainand the Netherlandsrdquo Science vol 313 no 5785 pp 351ndash3542006

[2] M A Wall M Timmerman-Erskine and R S Boyd ldquoCon-servation impact of climatic variability on pollination of thefederally endangered plant Clematis socialis (Ranunculaceae)rdquoSoutheastern Naturalist vol 2 no 1 pp 11ndash24 2003

[3] V L Scaven and N E Rafferty ldquoPhysiological effects ofclimate warming on flowering plants and insect pollinators andpotential consequences for their interactionsrdquo Current Zoologyvol 59 no 3 pp 418ndash426 2013

[4] WKarunaratne and J Edirisinghe ldquoDiversity of bees at differentaltitudes in the knuckles forest reserverdquo Ceylon Journal ofScience (Biological Sciences) vol 37 no 1 pp 61ndash72 2009

[5] M Devoto D Medan and N H Montaldo ldquoPatterns of inter-action between plants and pollinators along an environmentalgradientrdquo Oikos vol 109 no 3 pp 461ndash472 2005

[6] I D Hodkinson ldquoTerrestrial insects along elevation gradi-ents species and community responses to altituderdquo BiologicalReviews vol 80 no 3 pp 489ndash513 2005

[7] Y L Dupont D M Hansen and J M Olesen ldquoStructure ofa plant-flower-visitor network in the high-altitude sub-alpinedesert of Tenerife Canary Islandsrdquo Ecography vol 26 no 3 pp301ndash310 2003

[8] S Kimball ldquoLinks between floralmorphology and floral visitorsalong an elevational gradient in a Penstemon hybrid zonerdquoOikos vol 117 no 7 pp 1064ndash1074 2008

[9] Oslash Totland ldquoEnvironment-dependent pollen limitation andselection on floral traits in an alpine speciesrdquo Ecology vol 82no 8 pp 2233ndash2244 2001

Psyche 3

Table 1 Species composition abundance and diversity of wild bees and seven different elevations

Species Elevation m above sea level (asl) Abundance Relative ()8 108 224 424 644 893 1017Xylocopa latipes 18 26 25 27 26 22 16 160 1716Xylocopa confusa 15 14 19 44 26 19 23 160 1716Xylocopa caerulea 0 0 0 15 29 31 22 97 104Apis cerana 20 23 37 44 38 27 0 189 202Apis dorsata 0 0 0 21 26 16 11 74 79Amegilla cingulata 1 4 11 8 22 13 17 76 81Megachile relativa 9 10 11 16 20 18 19 103 1105Lasioglossum malachurum 0 7 13 12 14 13 14 73 78Abundance 63 84 116 187 201 159 122 932Relative () 67 901 1244 2006 2156 1706 1309Mean temperature ∘C 343 325 312 304 298 29 287Shannon H 1408 1622 1684 193 2045 2035 1919Simpson 1-D 0740 0778 07944 08361 08665 08634 08498Evenness eandHS 0817 0843 0897 0860 0966 0956 0973

32 Abundance In total 932 individual wild bees belongingto 8 species 5 genera and 3 families were recorded Site 1supported 4 species with 63 individuals (58 of all indi-viduals) Site 2 5 species and 84 individuals (901) Site 35 species and 116 individuals (1244) Site 4 7 species and187 individuals (2006) Site 5 8 species and 201 individuals(215) Site 6 8 species and 169 individuals (1706) and Site7 7 species and 122 individuals (1309) (Figure 1(b))

Wild bee abundance differed significantly among sites(ANOVA F649 = 3478 p = 0006 lt 005)Themost abundantspecies was Apis cerana with 189 individuals (202) fol-lowed by X confusa and X latipes each with 160 individuals(1716)M relativawith 103 individuals (1105)X caeruleawith 97 individuals (104) A cingulata with 76 individuals(81) and A dorsata with 74 individuals (79) and theleast abundant was Lmalachurumwith 73 individuals (78)Comparing the wild bee abundance among sampling eventsat all elevations the highest abundance was from samplingnumber 2 with 199 individuals (213) followed by samplingnumber 1 with 172 individuals (184) sampling number 4with 157 individuals (168) sampling number 3 with 148individuals (158) sampling number 5 with 136 individu-als (145) and the lowest abundance was from samplingnumber 6 with 120 individuals (128) However statisticalanalysis revealed no significant differences among samplingevents (ANOVA F542 = 101800 119901 = 0419 gt 005)

Across the study sites diversity increased with increasingelevation (ShannonndashWiener index (1198671015840)= 14 dominance (119863)= 025 and evenness (119864) = 078 at low elevation to (1198671015840) =204 119863 = 013 and 119864 = 096 at high elevation) and highernumbers of species were found atmiddle and high elevationsThe distribution of wild bees among the sites was significantlyinfluenced by elevation The richness abundance diversityand evenness of wild bees at different sites are presented inTable 1

Analysis of community structure similarity among eleva-tions showed that the three sites categorised as low elevation(8ndash224m asl) had high similarity (8453) the two middle-elevation sites (424ndash644m asl) had 8350 similarity and

8m asl108m asl224m asl424m asl644 m asl893m asl1017m asl

0 50 100

similarity

BrayndashCurtis cluster analysis (single link)

Figure 2 Similarity (BrayndashCurtis) single linkage of wild bee inseven different elevations

the two high-elevation sites (893mndash1017m asl) had 797similarity However the highest species similarity (872)was found between Site 5 (644m asl) and site 6 (893m asl)(Figure 2)

4 Discussion

The number of wild bee species and the species compositionrecorded in this study were similar to those reported inprevious studies in various regions Hoiss et al [14] observed10 species of wild bees atVigna unguiculata in Ghana belong-ing to the families Apidae (Xylocopa Apis and Amegilla)Megachilidae (Megachile eurymera) and Halictidae (Nomiasp) Kwapong et al [15] reported that the main insectsobserved on cowpea flowers were bees such as Apis melliferaCeratina sp Megachile sp Xylocopa calens Xylocopa imita-tor Braussepis sp Lipotriches sp Melecta sp and Amegillasp Kingha et al [16] reported Apis mellifera as the mostabundant insect species visiting P vulgaris flowers in Kenyafollowed by Xylocopa calens and X inconstans The flowers oflong bean attract wild bee pollinators from Apidae probablybecause themembers of this family have sufficient strength toopen the flower to collect pollen and nectar [17] However tothe best of our knowledge to date there have been no studieson insect pollinator diversity in green bean cultivation areas

4 Psyche

in Indonesia for comparison purposes In Sukabumi WestJava in mustard (Brasica rapus) at an elevation of approx-imately 854m asl Aouar-Sadli et al [18] observed insectpollinators from the order Hymenoptera family Apidaesubfamily Apinae consisting of the species Apis cerana Apisdorsata and Trigona sp from the subfamily Xylocopinae thespecies Xylocopa caerulea X confusa X latipes and Ceratinasp from the family Colletidae subfamily Hylaeinae Hylaeussp from the family Halictidae subfamily Nomiinae Nomiasp and from the family Scoliidae Compsomeris lindenniOur study findings indicate that the species composition ofinsect pollinators on agricultural land is dominated by wildbees

Elevation strongly influenced the diversity and abun-dance of wild bee communities Species richness and abun-dance increased linearly with increasing elevation andspecies diversity was highest at middle elevations Theseresults are inconsistent with those of Gottlieb et al [19]who reported that the diversity and abundance of wildbees decreased linearly with increasing elevation from 60 to2000m asl This difference may be due to differences in thegeographical region climate zone and range of elevationalgradient A commonly reported pattern in species richnessalong elevational gradients is a unimodal distribution with amid-elevation peak [20] In our study peak species diversityoccurred at middle elevations due to the presence of twospecies (Apis dorsata and Xylocopa caerulea) that began toappear above 442m asl The presence of the giant honeybee (A dorsata) at mid-to-high elevations may be due tohabitat suitability rather than elevation effects because thesebees require a forested habitat with high trees whereas bluecarpenter bees tend to be abundant in cool environmentsLarge carpenter bees (genusXylocopa) are wood-nesting gen-eralist pollinators of broad geographical distribution Theirforaging is characterised by a wide range of food plants longseason of activity tolerance of high temperatures and activityunder low illumination levels [21] Carpenter bees toleratehigh ambient temperatures during foraging andmost speciesare inactive at low temperatures and these bees were foundin all of our study sites All of the sites from the lowest tohighest elevation had daily temperature ranges appropriatefor wild bees Generally the genus Xylocopa is able to movearound well in a daily temperature range of 25ndash35∘C [22]This heat tolerance suggests efficient heat regulation abilityin carpenter bees possibly controlled by a thermoregulatorycentre in the prothorax [23] In contrast Apis cerana has atendency to forage in conditions of warm temperatures [24]The presence of the three speciesMegachile relativa Amegillacingulata and Lasioglossum malachurum almost evenly atall elevations studied indicates that these species are able tomove around in the range of temperatures that occur at theseelevations

5 Conclusion

Eight species of wild bees from four families of the orderHymenoptera were recorded in green bean cultivation areasat seven different elevations in Central Java IndonesiaSpecies richness and abundance increased linearly with

increasing elevation and species diversity was highest atmiddle elevations

Disclosure

TheEnglish in this document has been checked by at least twoprofessional editors both native speakers of English For acertificate please see httpwwwtextcheckcomcertificateA8au11

Competing Interests

The authors declare that they have no competing interests

Acknowledgments

The authors are grateful to Yulia Arnitasari Tutut KusumaWahyuni Ismayanti Pangalinan Riadiana Sulistyaningrumand Ganesha Rifky Rinaldi for assistance with data collectionand their encouragement of this study from its inceptionThisstudy was a part of a larger research programme funded byJenderal Soedirman University They also thank the heads ofthe Institute of Research and Community Services JenderalSoedirman University for their support

References

[1] J C Biesmeijer S P M Roberts M Reemer et al ldquoParalleldeclines in pollinators and insect-pollinated plants in Britainand the Netherlandsrdquo Science vol 313 no 5785 pp 351ndash3542006

[2] M A Wall M Timmerman-Erskine and R S Boyd ldquoCon-servation impact of climatic variability on pollination of thefederally endangered plant Clematis socialis (Ranunculaceae)rdquoSoutheastern Naturalist vol 2 no 1 pp 11ndash24 2003

[3] V L Scaven and N E Rafferty ldquoPhysiological effects ofclimate warming on flowering plants and insect pollinators andpotential consequences for their interactionsrdquo Current Zoologyvol 59 no 3 pp 418ndash426 2013

[4] WKarunaratne and J Edirisinghe ldquoDiversity of bees at differentaltitudes in the knuckles forest reserverdquo Ceylon Journal ofScience (Biological Sciences) vol 37 no 1 pp 61ndash72 2009

[5] M Devoto D Medan and N H Montaldo ldquoPatterns of inter-action between plants and pollinators along an environmentalgradientrdquo Oikos vol 109 no 3 pp 461ndash472 2005

[6] I D Hodkinson ldquoTerrestrial insects along elevation gradi-ents species and community responses to altituderdquo BiologicalReviews vol 80 no 3 pp 489ndash513 2005

[7] Y L Dupont D M Hansen and J M Olesen ldquoStructure ofa plant-flower-visitor network in the high-altitude sub-alpinedesert of Tenerife Canary Islandsrdquo Ecography vol 26 no 3 pp301ndash310 2003

[8] S Kimball ldquoLinks between floralmorphology and floral visitorsalong an elevational gradient in a Penstemon hybrid zonerdquoOikos vol 117 no 7 pp 1064ndash1074 2008

[9] Oslash Totland ldquoEnvironment-dependent pollen limitation andselection on floral traits in an alpine speciesrdquo Ecology vol 82no 8 pp 2233ndash2244 2001

4 Psyche

in Indonesia for comparison purposes In Sukabumi WestJava in mustard (Brasica rapus) at an elevation of approx-imately 854m asl Aouar-Sadli et al [18] observed insectpollinators from the order Hymenoptera family Apidaesubfamily Apinae consisting of the species Apis cerana Apisdorsata and Trigona sp from the subfamily Xylocopinae thespecies Xylocopa caerulea X confusa X latipes and Ceratinasp from the family Colletidae subfamily Hylaeinae Hylaeussp from the family Halictidae subfamily Nomiinae Nomiasp and from the family Scoliidae Compsomeris lindenniOur study findings indicate that the species composition ofinsect pollinators on agricultural land is dominated by wildbees

Elevation strongly influenced the diversity and abun-dance of wild bee communities Species richness and abun-dance increased linearly with increasing elevation andspecies diversity was highest at middle elevations Theseresults are inconsistent with those of Gottlieb et al [19]who reported that the diversity and abundance of wildbees decreased linearly with increasing elevation from 60 to2000m asl This difference may be due to differences in thegeographical region climate zone and range of elevationalgradient A commonly reported pattern in species richnessalong elevational gradients is a unimodal distribution with amid-elevation peak [20] In our study peak species diversityoccurred at middle elevations due to the presence of twospecies (Apis dorsata and Xylocopa caerulea) that began toappear above 442m asl The presence of the giant honeybee (A dorsata) at mid-to-high elevations may be due tohabitat suitability rather than elevation effects because thesebees require a forested habitat with high trees whereas bluecarpenter bees tend to be abundant in cool environmentsLarge carpenter bees (genusXylocopa) are wood-nesting gen-eralist pollinators of broad geographical distribution Theirforaging is characterised by a wide range of food plants longseason of activity tolerance of high temperatures and activityunder low illumination levels [21] Carpenter bees toleratehigh ambient temperatures during foraging andmost speciesare inactive at low temperatures and these bees were foundin all of our study sites All of the sites from the lowest tohighest elevation had daily temperature ranges appropriatefor wild bees Generally the genus Xylocopa is able to movearound well in a daily temperature range of 25ndash35∘C [22]This heat tolerance suggests efficient heat regulation abilityin carpenter bees possibly controlled by a thermoregulatorycentre in the prothorax [23] In contrast Apis cerana has atendency to forage in conditions of warm temperatures [24]The presence of the three speciesMegachile relativa Amegillacingulata and Lasioglossum malachurum almost evenly atall elevations studied indicates that these species are able tomove around in the range of temperatures that occur at theseelevations

5 Conclusion

Eight species of wild bees from four families of the orderHymenoptera were recorded in green bean cultivation areasat seven different elevations in Central Java IndonesiaSpecies richness and abundance increased linearly with

increasing elevation and species diversity was highest atmiddle elevations

Disclosure

TheEnglish in this document has been checked by at least twoprofessional editors both native speakers of English For acertificate please see httpwwwtextcheckcomcertificateA8au11

Competing Interests

The authors declare that they have no competing interests

Acknowledgments

The authors are grateful to Yulia Arnitasari Tutut KusumaWahyuni Ismayanti Pangalinan Riadiana Sulistyaningrumand Ganesha Rifky Rinaldi for assistance with data collectionand their encouragement of this study from its inceptionThisstudy was a part of a larger research programme funded byJenderal Soedirman University They also thank the heads ofthe Institute of Research and Community Services JenderalSoedirman University for their support

References

[1] J C Biesmeijer S P M Roberts M Reemer et al ldquoParalleldeclines in pollinators and insect-pollinated plants in Britainand the Netherlandsrdquo Science vol 313 no 5785 pp 351ndash3542006

[2] M A Wall M Timmerman-Erskine and R S Boyd ldquoCon-servation impact of climatic variability on pollination of thefederally endangered plant Clematis socialis (Ranunculaceae)rdquoSoutheastern Naturalist vol 2 no 1 pp 11ndash24 2003

[3] V L Scaven and N E Rafferty ldquoPhysiological effects ofclimate warming on flowering plants and insect pollinators andpotential consequences for their interactionsrdquo Current Zoologyvol 59 no 3 pp 418ndash426 2013

[4] WKarunaratne and J Edirisinghe ldquoDiversity of bees at differentaltitudes in the knuckles forest reserverdquo Ceylon Journal ofScience (Biological Sciences) vol 37 no 1 pp 61ndash72 2009

[5] M Devoto D Medan and N H Montaldo ldquoPatterns of inter-action between plants and pollinators along an environmentalgradientrdquo Oikos vol 109 no 3 pp 461ndash472 2005

[6] I D Hodkinson ldquoTerrestrial insects along elevation gradi-ents species and community responses to altituderdquo BiologicalReviews vol 80 no 3 pp 489ndash513 2005

[7] Y L Dupont D M Hansen and J M Olesen ldquoStructure ofa plant-flower-visitor network in the high-altitude sub-alpinedesert of Tenerife Canary Islandsrdquo Ecography vol 26 no 3 pp301ndash310 2003

[8] S Kimball ldquoLinks between floralmorphology and floral visitorsalong an elevational gradient in a Penstemon hybrid zonerdquoOikos vol 117 no 7 pp 1064ndash1074 2008

[9] Oslash Totland ldquoEnvironment-dependent pollen limitation andselection on floral traits in an alpine speciesrdquo Ecology vol 82no 8 pp 2233ndash2244 2001

Psyche 5

[10] J M Olesen and P Jordano ldquoGeographic patterns in plant-pollinator mutualistic networksrdquo Ecology vol 83 no 9 pp2416ndash2424 2002

[11] B J Brosi G CDaily TM Shih F Oviedo andGDuran ldquoTheeffects of forest fragmentation on bee communities in tropicalcountrysiderdquo Journal of Applied Ecology vol 45 no 3 pp 773ndash783 2008

[12] A E Magurran Ecological Diversity and Its MeasurementChapman and Hall London UK 1st edition 1988

[13] N McAleece P J D Lambshead and G L J PatersonBiodiversity Pro The Natural History Museum London UK1997

[14] B Hoiss J Krauss S G Potts S Roberts and I Steffan-Dewenter ldquoAltitude acts as an environmental filter on phylo-genetic composition traits and diversity in bee communitiesrdquoProceedings of the Royal Society B Biological Sciences vol 279no 1746 pp 4447ndash4456 2012

[15] P K Kwapong P O A Danquah and A T Asare ldquoInsect floralvisitors of cowpea (Vigna unguiculata L)rdquo Annals of BiologicalResearch vol 4 no 4 pp 12ndash18 2013

[16] B M T Kingha F N T Fohouo A Ngakou and DBruckner ldquoForaging and pollination activities of Xylocopa oli-vacea (Hymenoptera Apidae) on Phaseolus vulgaris (Fabaceae)flowers at Dang (Ngaoundere-Cameroon)rdquo Journal of Agricul-tural Extension and Rural Development vol 4 no 6 pp 330ndash339 2012

[17] T Atmowidi D Buchori S Manuwoto B Suryobroto and PHidayat ldquoDiversity of pollinator insects in relation to seed setof mustard (Brassica rapus L Cruciferae)rdquo HAYATI Journal ofBiosciences vol 14 no 4 pp 155ndash161 2007

[18] M Aouar-Sadli K Louadi and S E Doumandji ldquoPollinationof the broad bean (Vicia faba Lvar major)(Fabaceae) by wildbees and honey bees (Hymenoptera Apoidea) and its impact onthe seed production in the Tizi-Ouzou area (Algeria)rdquo AfricanJournal of Agricultural Research vol 3 no 4 pp 266ndash272 2008

[19] D Gottlieb T Keasar A Shmida and U Motro ldquoPossibleforaging benefits of bimodal daily activity inProxylocopa olivieri(Lepeletier) (Hymenoptera Anthophoridae)rdquo EnvironmentalEntomology vol 34 no 2 pp 417ndash424 2005

[20] S VolynchikM Plotkin N Y Ermakov D J Bergman and J SIshay ldquoPresence of a thermoregulatory hot spot in the prothoraxof the large carpenter bee and the bumble beerdquo MicroscopyResearch and Technique vol 69 no 11 pp 903ndash912 2006

[21] T Keasar ldquoLarge carpenter bees as agricultural pollinatorsrdquoPsyche vol 2010 Article ID 927463 7 pages 2010

[22] T Keasar A Sadeh M Shilo and Y Ziv ldquoSocial organiza-tion and pollination efficiency in the carpenter bee Xylocopapubescens (Hymenoptera Apidae Anthophorinae)rdquoEntomolo-gia Generalis vol 29 no 2ndash4 pp 225ndash236 2007

[23] K Tan S Yang Z-W Wang S E Radloff and B P OldroydldquoDifferences in foraging and broodnest temperature in thehoney beesApis cerana andA melliferardquoApidologie vol 43 no6 pp 618ndash623 2012

[24] D Goulson ldquoEffects of introduced bees on native ecosystemsrdquoAnnual Review of Ecology Evolution and Systematics vol 34no 1 pp 1ndash26 2003

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology