doi 101098rstb20110034 3246-3255366 2011 Phil Trans R Soc B

and Malcolm C PressVillanueva Owen T Lewis Christopher H C Lyal Reuben Nilus Adzley Madran Julie D Scholes Robert Bagchi Christopher D Philipson Eleanor M Slade Andy Hector Sam Phillips Jerome F dipterocarp seeds in a South East Asian rainforestImpacts of logging on density-dependent predation of

Supplementary data

ml httprstbroyalsocietypublishingorgcontentsuppl2011092336615823246DC1ht

Data Supplement

References

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This journal is copy 2011 The Royal Society

on October 18 2011rstbroyalsocietypublishingorgDownloaded from

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Phil Trans R Soc B (2011) 366 3246ndash3255

doi101098rstb20110034

Research

Autho

Electron101098

One conAsian ra

Impacts of logging on density-dependentpredation of dipterocarp seeds in a

South East Asian rainforestRobert Bagchi123 Christopher D Philipson4 Eleanor M Slade2

Andy Hector4 Sam Phillips4 Jerome F Villanueva2 Owen T Lewis2

Christopher H C Lyal5 Reuben Nilus6 Adzley Madran7

Julie D Scholes1 and Malcolm C Press8

1Department of Animal and Plant Science University of Sheffield Western Bank RoadSheffield S10 2TN UK

2Department of Zoology University of Oxford South Parks Road Oxford OX1 3PS UK3Department of Biological and Biomedical Science Durham University South Road

Durham DH1 3LE UK4Institute of Evolutionary Biology and Environmental Studies University of Zurich (Irchel )

Winterthurerstrasse 190 Zurich 8057 Switzerland5Entomology Department Natural History Museum Cromwell Road London SW7 5BD UK

6Forest Research Centre Forest Department Sepilok PO Box 1407 90715 Sandakan Sabah Malaysia7Danum Valley Field Centre PO Box 60282 91112 Lahad Datu Sabah Malaysia

8College of Life and Environmental Sciences University of Birmingham Birmingham B15 2TT UK

Much of the forest remaining in South East Asia has been selectively logged The processes promot-ing species coexistence may be the key to the recovery and maintenance of diversity in these forestsOne such process is the JanzenndashConnell mechanism where specialized natural enemies such asseed predators maintain diversity by inhibiting regeneration near conspecifics In Neotropical for-ests anthropogenic disturbance can disrupt the JanzenndashConnell mechanism but similar data areunavailable for South East Asia We investigated the effects of conspecific density (two spatialscales) and distance from fruiting trees on seed and seedling survival of the canopy tree Parashoreamalaanonan in unlogged and logged forests in Sabah Malaysia The production of mature seeds washigher in unlogged forest perhaps because high adult densities facilitate pollination or satiatepre-dispersal predators In both forest types post-dispersal survival was reduced by small-scale(1 m2) conspecific density but not by proximity to the nearest fruiting tree Large-scale conspecificdensity (seeds per fruiting tree) reduced predation probably by satiating predators Higher seed pro-duction in unlogged forest in combination with slightly higher survival meant that recruitment wasalmost entirely limited to unlogged forest Thus while logging might not affect the JanzenndashConnellmechanism at this site it may influence the recruitment of particular species

Keywords JanzenndashConnell hypothesis logging plant diversity anthropogenic disturbancepredator satiation secondary forest

1 INTRODUCTIONTropical forests are being lost and degraded at analarming rate [12] Forest loss has been particularlyrapid in South East Asia where less than half of theoriginal forest cover remains [3] While unexploitedforest is now rare in the region large areas of second-ary forest remain [45] and their importance for

r for correspondence (bagchirgmailcom)

ic supplementary material is available at httpdxdoiorgrstb20110034 or via httprstbroyalsocietypublishingorg

tribution of 16 to a Theme Issue lsquoThe future of South Eastinforests in a changing landscape and climatersquo

3246

conservation is increasingly recognized [6ndash8] Com-mercial timber extraction has inevitable dramaticimpacts on the structure diversity and communitycomposition of these secondary forests [910] butthey are still important reservoirs for biodiversity andprovide crucial ecosystem services including provisionof raw materials soil protection and sequestrating andstoring carbon [891112]

Despite the importance of secondary forests forspecies conservation the consequences of human dis-turbance for the maintenance of diversity remainpoorly understood [1314] While there is an extensiveliterature on the effects of human disturbance onspecies richness and diversity (see recent reviews in

This journal is q 2011 The Royal Society

Predation of dipterocarp seeds R Bagchi et al 3247

on October 18 2011rstbroyalsocietypublishingorgDownloaded from

[78]) the effects on the structure and organizationof ecological communities and associated ecologicalfunctions and processes have received less attention[1314] In particular for forest biodiversity to recoverand persist following disturbances such as logging it isimportant that the processes responsible for maintain-ing diversity remain intact [14] The mechanismsmaintaining tree diversity have been extensively exam-ined in the literature [15] and these mechanismscould be potentially disrupted by disturbance [14]Reductions in tree diversity could have implicationsfor diversity in other taxonomic groups because plantdiversity to some extent sets the template for diversityat higher trophic levels [1617] A particular concern isthat even when diversity is not severely reduced byexploitation itself it might decline over time if theseprocesses have been undermined

Much research has tried to understand the proces-ses involved in plant species coexistence particularlyin tropical forests [15] Among the most likely candi-dates is the JanzenndashConnell mechanism [1819]where seeds and seedlings near conspecific adults orin areas of high conspecific density suffer high mor-tality through the activity of specialized naturalenemies Consequently locally rare species have anadvantage promoting species coexistence

Support for the JanzenndashConnell mechanism mainlycomes from the Neotropics and studies from Asia andAfrica are rare [20] Of the small number of studies con-ducted in Asia several support the JanzenndashConnellmechanism [21ndash23] but others do not and sometimesshow patterns that run counter to its predictions[2425] The ecology of South East Asian forests differsin several important regards from other tropical regionsand so we need to be cautious when generalizing fromresults obtained elsewhere In particular reproductionis typically highly episodic in these forests occurring insupra-annual community-wide mast fruiting events[2627] Up to 88 per cent of canopy species can fruitat the same time and the most plausible explanationfor this phenomenon is that it evolved to satiate seed pre-dators [2728] Predator satiation decreases mortalityat the highest densities directly opposing the JanzenndashConnell mechanism Indeed Janzen [18] suggested thatmast fruiting species were unlikely to be affected by themechanism However while much of the literature onfruiting in South East Asian forests has concentrated onmast events there is some evidence of successful recruit-ment outside mast events [2529] In these partial fruitingepisodes the chance of observing density dependencemay be greater because fruiting trees are relatively iso-lated Seed predators may be attracted to these treesdecreasing the survival of seeds close to their parenttrees relative to those dispersed further away

Deforestation and hunting may reduce seed predatorpopulations which may then be unable to constrainthe recruitment of common species Converselyrestricting predators to small forest fragments couldprevent seeds of rare species from escaping in spaceremoving the rare species advantage Both scenarioswould weaken the JanzenndashConnell mechanismStudies in the Neotropics have suggested that humandisturbance disrupts the JanzenndashConnell mechanismHunting and forest fragmentation have both been

Phil Trans R Soc B (2011)

linked to reduced density dependence and conse-quently plant diversity [30ndash32] However similardata are lacking for South East Asian forests althoughforest fragmentation and logging can reduce diptero-carp recruitment because low densities of dipterocarptrees are unable to produce enough seed to satiateseed predators (which are localized in remainingforest fragments) [2633]

In this paper we assess the distance from the near-est fruiting conspecific tree (which in most cases willbe the parent) and conspecific density effects on thesurvival of Parashorea malaanonan Merr (Dipterocar-paceae) seeds and germinating seedlings in bothunlogged and logged forest in Sabah North Borneoduring a non-mast year We test the following threehypotheses

mdash seed and seedling survival will increase with dis-tance from the nearest fruiting tree (distancedependence)

mdash seed and seedling survival will decrease withincreased conspecific density (negative densitydependence)

mdash the relationship between survival and distance anddensity will be stronger in the unlogged forest thanin logged forest

2 METHODS(a) Study site

The study was conducted around the Danum ValleyField Centre in Sabah Malaysian Borneo (48580 N1188480 E) Large areas of both logged and unloggedforest lie close to the field station The Danum ValleyConservation Area (DVCA) contains 43 800 ha ofunlogged mostly lowland dipterocarp forest TheYayasan Sabah Forest Management Area (YSFMA) isa logging concession of almost 1 million ha

Logging in the YSFMA began in the mid-1970sand is ongoing The areas included in this studywere logged between 1970 and 1988 Timber wasextracted using a combination of high lead on steepslopes and traditional tractor-based methods in otherareas Most of the healthy stems greater than 60 cmdiameter at breast height (dbh) were removed Typi-cal extraction rates were about 70 m3 ha21 althoughhigher rates have been reported (see [5] for furthersite information)

(b) Study species

Parashorea malaanonan is among the commonestspecies in the YSFMA and more widely in Sabah[5] Permanent plots in the DVCA contain about186 P malaanonan stems ha21 (greater than 10 cmgirth at breast height) [34] Most of the forest in theYSFMA is classified as P malaanonan (type A)forest a category that includes much of the naturalvegetation in the upper Segama region and coastalareas of Eastern Sabah [5] Parashorea malaanonan iscommercially harvested and its timber is classed asWhite Serraya Light Hardwood (timber density052 g cm21 [3235]) It is a relatively fast-growingdipterocarp and its seedlings perform better in gapsand therefore it is considered relatively light demanding

0 10 20 30

10

20

30

40

50(a) (b)

(c)

seed

fall

(see

ds m

minus2)

0 10 20 30

10

20

30

40

50

distance (m) distance (m)

23 September 7 October 21 October 4 November 18 November

0

02

04

06

date

seed

fall

(see

ds m

minus2 d

ayminus1

)

Figure 1 The relationship between P malaanonan seedfall and distance from the nearest fruiting tree in (a) unlogged and(b) logged forest Points are the mean number of seeds falling into 1 m2 seed traps located at 2 10 20 and 30 m from 10trees in each forest type Solid lines represent the number of seeds predicted to fall at each distance by the model fitted tothe data Dotted lines represent the predictions for each of the 10 trees in each forest type (c) The majority of seeds fell in

the first six weeks of the study Points are the mean number of seeds that fell in seed traps placed 2 m away from each treeand lines are the model predictions Black line unlogged grey line logged

3248 R Bagchi et al Predation of dipterocarp seeds

on October 18 2011rstbroyalsocietypublishingorgDownloaded from

for a dipterocarp [36] However dipterocarps in generalare very shade-tolerant and overall P malaanonanhas high survival [2136] and growth rates [37] inunderstorey conditions

Parashorea malaanonan appears to fruit more oftenthan other dipterocarps at the study site and success-fully set seed in 1996 2000 and 2004 (the year of thisstudy [29]) The winged seeds are dispersed by windor gyration and mostly fall under the parent treersquoscanopy Several vertebrates and invertebrates havebeen observed attacking seeds and seedlings of Pmalaanonan including bearded pigs Sus babatus (RBagchi 2004 personal observation) rodents [38]and insect seed predators and herbivores [363940]

(c) Site selection

In August 2004 fruiting P malaanonan trees werelocated in the unlogged forest by searching alongtrails around the field station The logged forest wassurveyed from the logging roads Ten trees were ident-ified for the study in both forest types Trees wereconsidered suitable if they had a large fruit cropwere greater than 30 m away from roads and greaterthan 100 m from other fruiting trees included in thestudy A 30 m transect was established starting at thebase of each selected tree The direction of thistransect was constrained to avoid trails and otherfruiting P malaanonan trees but otherwise chosen atrandom (ie a restricted random design see electronicsupplementary material figure S1)

(d) Seedfall traps

Traps were used to establish seedfall rates soon after thefirst seedfall was observed Traps were deployed at 2

Phil Trans R Soc B (2011)

10 20 and 30 m along the transects Each 1 1 mtrap was constructed by suspending a piece of plasticmesh above the ground with string attached to suitabletrees Dipterocarp seeds are dispersed by gyration andgenerally land close to the parent tree [41ndash43] Ourexperience is that few seeds disperse further than30 m and this is supported by the data presented here(figure 1) Seeds were collected from the traps in bothforests every 4 days between 23 September and30 November 2004 In addition at each census we col-lected five seeds (if possible) from the ground at eachdistance interval but avoided the immediate vicinityof the traps and plots These seeds would have beenexposed to both pre-dispersal and post-dispersalinsect predators The collected seeds (trap andground) were brought back to the laboratory in orderto rear out insect seed predators (see sect2g)

(e) Non-manipulated plots

A 1 1 m plot was established 2 m to the right of eachseed trap Seeds found in the plot were tagged withsmall numbered flags pinned to their wings The pres-ence and status of tagged seeds were checked at thesame time as the seedfall traps and new seeds weretagged and recorded The status of each seed wasrecorded as potentially viable (intact seeds with novisible signs of fungal attack or insect exit holes)dead (decomposing or empty) germinated fungus-infected insect-predated (with exit holes) consumedby vertebrates (partially consumed seed remaining)seedling browsed by vertebrates or removed from theplot (presumed dead) Some of the removed seedswere possibly secondarily dispersed but previouswork on dipterocarp seed predation suggests that

Predation of dipterocarp seeds R Bagchi et al 3249

on October 18 2011rstbroyalsocietypublishingorgDownloaded from

most are consumed [2538] Note that these categorieswere not exclusive The plots were monitored until30 November 2004

(f) Density manipulation plots

Parashorea malaanonan seeds were collected from thevicinity of additional fruiting trees To manipulate den-sity and distance independently we established twofurther 1 1 m plots at distances of 2 and 30 m fromeach focal tree adjacent to the existing traps on9 October 2004 At each distance we assigned plots tohigh- or low-density treatments at random We placed25 (high density) or four (low density) tagged seeds ona regular grid in the plots The high-density treatment(25 seeds m22) corresponds to the highest density wefound in the naturally dispersed seed plots The low-density treatment (4 seeds m22) is at the low end ofseed densities observed naturally and provides somewithin-plot replication All naturally dispersed seedswere removed throughout the experiment These plotswere censused until 30 November 2004 at the sametime as the traps and non-manipulated plots Seedswere assigned to the same categories as those in thenon-manipulated plots (see earlier text)

(g) Insect rearing

Seeds collected from the ground and traps in differentcensuses were stored separately for rearing insects butwe pooled the seeds from each distance Any visiblesigns of insect predation were recorded and thenseeds were placed in ventilated rearing boxes linedwith damp tissue paper Seeds were examined every3 days and date of germination or emergence ofseed predators or parasitoids recorded Lepidopteranpredators were pinned on emergence and driedEmerged weevils and parasitoids were stored in90 per cent ethanol in a freezer After four monthsall seeds were dissected predation recorded and anylarvae or adults still inside the seeds stored in alcoholSpecimens were mounted and identified at the NaturalHistory Museum (London) and the Oxford UniversityMuseum of Natural History Insects were classed aspre-dispersal or post-dispersal predators on the basisof the literature [44ndash46]

(h) Statistical analysis

We used generalized linear mixed-effects models(GLMMs) [4748] for all analyses Seedfall was mod-elled as a function of forest type and distance from thenearest fruiting tree assuming a Poisson error distri-bution The intercept and effect of distance wereallowed to vary between trees as normally distributedrandom effects (random intercept and slope model)

Initial analyses suggested only small differences insurvival between seeds in the manipulated and non-manipulated plots so data were combined for ana-lyses Seeds recorded as dead removed or eaten byvertebrates were categorized as lsquodeadrsquo while seeds inother categories were regarded as survivors Notethat seeds in the lsquoinsect-predatedrsquo and lsquofungus-infectedrsquo categories were not initially counted asdead but if the seed was determined to be dead on asubsequent visit these agents were considered

Phil Trans R Soc B (2011)

responsible for their death For each plot thenumber of seeds that died or survived during eachcensus interval was recorded

We modelled seed and seedling survival usingGLMMs assuming a binomial error distribution Weexamined the effects of forest type distance to thenearest fruiting tree conspecific density at the startof the census interval and the two- and three-wayinteractions between these predictors Total seedfallat each tree over the study was included as a measureof medium-scale seed density Intercept terms for eachcensus were included in the model as normally distrib-uted random effects This allows the overall survivalrate to change over time (for example if older seedsor seedlings are less vulnerable) without makingassumptions about the form of this relationshipsimilar to Cox proportional hazard models [49]Preliminary analyses suggested that the relationshipbetween survival and time differed considerablybetween the two forest types so we included an inter-action between census and forest type as a randomeffect Intercept terms for trees and plots were includedas normally varying random effects The relationshipbetween survival and time was also allowed to varybetween plots as a random effect (random interceptand slope model)

The probability of predation by insects of seeds keptin the laboratory was modelled as a function of foresttype and the total seed crop at each tree using aGLMM with a binomial error distribution In a separ-ate model we examined the effect of distance from thenearest fruiting conspecific forest type and their inter-action using only the seeds collected from the forestfloor Predation of seeds collected in the traps willbe dominated by pre-dispersal predation and testingthe effect of distance on predation of these seedsmay therefore be inappropriate In both models separ-ate intercepts for trees were modelled as normallydistributed random effects

There is much debate about how to appropriatelytest hypotheses using GLMMs [4748] We used themethodology recommended by Gelman amp Hill [47]to construct 95 confidence intervals (CIs) for par-ameter estimates We resampled 1000 times from theposterior distribution of the parameter estimates andcalculated the 25 and 975 per cent quantiles Anapproximate two-tailed p-value was estimated as

p frac14 1 2 x

1000 05

where x is the number of samples greater than 0 Wepresent these approximate p-values and the parameterestimates on the scale of the linear predictor with their95 CI Analyses were executed in R 2111 [50]using the add-on packages lme4 0999375-34 andarm 13-05 The R-code used to fit the models is avail-able in the electronic supplementary material

3 RESULTS(a) Seedfall

Overall 353 seeds were collected from seed traps inthe unlogged forest and 174 seeds in the logged forest(figure 1ab respectively) The difference was marginally

unlogged logged

06

08

10

forest type

surv

ival

(a) (b)

0 5 10 15 2004

06

08

10

seedfall (seeds mminus2 )

surv

ival

Figure 2 (a) Survival of P malaanonan seeds and seedlings in both unlogged and logged forest Seed and seedling survival were

not significantly affected by either forest type or distance from the nearest fruiting trees Open circles 2 m filled circles 30 m(b) The effect of seed production at each tree on seed and seedling survival Data are the mean survival rates (+se) takinginto account the variation between plots and focal trees Black line unlogged grey line logged

0 5 10 15 20 2502

04

06

08

10(a) (b)

0 5 10 15 20 2502

04

06

08

10

density (seeds mminus2) density (seeds mminus2)

surv

ival

Figure 3 Survival of P malaanonan seedlings declined with conspecific seed and seedling density in both (a) unlogged and(b) logged forest Distance from nearest fruiting tree did not affect survival Points are the observed proportion of seeds that sur-

vived through 4 day census intervals in 1 m2 plots at each density at 2 and 30 m from the focal trees Lines represent theexpectations of the model fitted to the data and error bars represent the standard errors Black dashed line 2 m grey solidline 30 m

3250 R Bagchi et al Predation of dipterocarp seeds

on October 18 2011rstbroyalsocietypublishingorgDownloaded from

non-significant (parameter estimate for the effect oflogged forest blogged frac14 075 95 CIfrac14 2161ndash009p frac14 0076) and there was substantial variation betweentrees within forest types The number of seeds intraps declined sharply with distance from focal treesconsistent with local seed dispersal (figure 1bdistance frac14 0084 95 CIfrac14 2011 to 2006 p

0001) Seedfall was heavy during the first few weeks ofthe study and began to decline after the first month ofthe study Almost all seeds fell before the end of thesixth week (figure 1c)

(b) Seed survival

Over two months 332 seeds were naturally dispersedinto the non-manipulated plots (217 54 seeds m22in unlogged forest 115 29 seeds m22 in loggedforest) A further 1160 seeds were added to the 80density manipulation plots (evenly distributedbetween the two forest types) No seeds fell into 23of the non-manipulated plots so the analyses arebased on the remaining 57 non-manipulated and 80manipulated plots

Phil Trans R Soc B (2011)

Of these seeds 304 (38 of the non-manipulatedand experimental seeds combined) survived to the endof the experiment in the unlogged forest comparedwith 117 (17) in the logged forest However thisdifference was not significant (blogged frac14 029 95CIfrac14 2213ndash150 pfrac14 0746) because of the consider-able variation in seed survival among trees (figure 2a)Only seven seeds (02 seeds m22) remained in thenon-manipulated plots in logged forest at the end ofthe study compared with 75 in the unlogged forest(19 seeds m22) Total seedfall at a tree had a slight posi-tive effect on seed survival (bseedfall frac14 0026 95CIfrac14 20002ndash0053 p frac14 0072 figure 2b) There wasa strong negative relationship between small-scale den-sity and survival in both forest types (bdensity frac14 09495 CIfrac14 2131 to 2055 p 0001 figure 3) Thestrength of this relationship was unaffected by foresttype (bloggeddensity frac14 016 95 CIfrac14 2067ndash039pfrac14 0574) Distance from the nearest fruiting tree didnot affect seed survival significantly and the interactionbetween distance and density was also non-significant(figure 2)

unlogged logged0

02

04

06

08

10

forest type

prop

ortio

n of

pre

datio

n

Figure 4 The causes of mortality of P malaanonan seeds andseedlings in unlogged and logged forest Data are the mean(+se) proportion of deaths in which the mortality agent

was implicated Note that more than one agent could con-tribute to death so the proportions can add up to greaterthan 1 Open bars vertebrate predators light grey bars ver-tebrate browsers dark grey bars fungi black bars insects

Predation of dipterocarp seeds R Bagchi et al 3251

on October 18 2011rstbroyalsocietypublishingorgDownloaded from

(c) Causes of mortality

Most seed mortality appeared to be due to vertebrateseed predators with seeds either missing or found par-tially eaten in the vicinity of the plots (figure 4) A largeproportion of individuals also died soon after germi-nating and subsequently being browsed by mammalsInsects and fungi contributed little to the overall mor-tality between them This pattern was similar in bothforest types (figure 4)

(d) Insect predation

A total of 2337 seeds were collected from the traps (566seeds) and the ground (1771 seeds) and brought back tothe laboratory Insects (moths weevils or parasitoids)were reared from 210 (9) of these seeds A higherproportion of seeds in the unlogged forest were predated(blogged frac14 078 95 CIfrac14 2116 to 2 034 p

0001 figure 5a) Predation was reduced at trees withlarge seed crops (bseedfall frac14 001 95 CIfrac14 20019to 20002 p frac14 0012 figure 5a) There was no effectof distance on predation by insects of seeds collectedfrom the forest floor

The most important insect seed predators ofP malaanonan seeds were weevils of the Anthribidaeand Curculionidae (figure 5b electronic supplemen-tary material table S1) A micro-moth from theTortricidae (probably Andrioplecta shoreae KomaiK Tuck 2005 personal communication) was also animportant pre-dispersal seed predator accounting forall but two moths that emerged (see electronic sup-plementary material table S1) When the seeds weredissected at the end of the experiment several seedscontained dead larvae of weevils from the familiesCurculionidae (probably Alcidodes sp) and Anthribidae(probably Araecerus sp) However no adult Alcidodeswere successfully reared from the seeds although a fewadult Araecerus were Parasitoids were reared from 18per cent of predated seeds and were primarily of thefamilies Braconidae and Ichneumonidae (figure 5b elec-tronic supplementary material table S1) We assumedthat seeds with parasitoids must have been attacked byseed predators first and these were therefore countedas predated

Phil Trans R Soc B (2011)

There were 41 seeds from the traps that had insectexit holes on collection but no insects emerged from22 of them It is possible that these seeds had beenpredated by weevils of the family Nanophyidae suchas Nanophyes species which often leave the seedbefore it falls from the tree [51]

4 DISCUSSION(a) Effects of logging on the JanzenndashConnell

mechanism

We found strong negative effects of small-scale (1 m2)conspecific density on the survival of P malaanonanseeds and germinating seedlings in both unloggedand logged tropical forest The strength of this densitydependence was independent of logging history Thissuggests either that logging has not affected seed-predator-mediated density dependence or this processhas recovered within 15ndash35 years after logging

Similar work in the Neotropics has generally foundstrong effects of human disturbance on density depen-dence of tree survival [30ndash32] It is likely that thisdisparity with our data is due to differences in thetype of disturbance to which the forests were sub-jected While logging operations in the YSFMAextract large volumes of timber hunting pressure onwildlife is relatively low [5] The Neotropical studiescompared forests subjected to intense hunting andmissing key seed predators to relatively undisturbedones Indeed hunting was identified as the majorcause of the reduced density dependence in eachcase [30ndash32] Furthermore the Dipterocarpaceaeare mainly abiotically dispersed [42] in contrast tomany Neotropical species that will have lost dispersersas well as seed predators Because our data are the firstfrom South East Asia to compare density-dependenteffects between unlogged and logged forests it wouldbe premature to conclude that hunting pressurerather than regional differences explains the differ-ences between our results and those of previousstudies However it provides the most likely expla-nation The vertebrate faunas in many forests in theregion suffer severely from hunting [3] so data com-parable to those reported here could be collectedfrom other South-East Asian forests

While high conspecific density at very small scalesincreased mortality seed predation in the field andby insects reared in the laboratory was lower at treeswith large seed crops Such positive effects of seeddensity are unsurprising because both pre-dispersalinsect [13] and post-dispersal vertebrate [52] seed pre-dators are likely to be satiated by large amounts ofseeds One explanation for the different response ofpost-dispersal predators to density at small and largescales is that while large seed crops eventually satiatethem they concentrate their foraging in areas of theseed shadow with the largest seed density Seed preda-tion by both insects and vertebrates was independentof proximity to the nearest fruiting adult possiblybecause the disadvantages of being close to fruitingtrees are offset by the ability of large amounts ofseeds to satiate seed predators locally The indepen-dence of insect seed predation to distance mightreflect that a large proportion of the reared insects

0 5 10 15 200

005

010

015

020

seedfall (seeds mminus2)

pred

atio

n

(a) (b)

unlogged logged0

02

04

06

08

forest type

prop

ortio

n of

pre

datio

n

Figure 5 (a) Insect predation on P malaanonan seeds collected in traps or from the forest floor nearby was higher in

logged forest than unlogged forest and at trees that produced fewer seeds Lines are the predictions of the models fitted tothe data (+se) Black line unlogged grey line logged (b) The proportion of predated seeds attacked by different predatorsBars represent the mean (+se) proportion of seed predators within three different categories and the proportion of predatorsthat had been parasitized Dark grey bars moths mid-grey bars weevils light grey bars parasitoids

3252 R Bagchi et al Predation of dipterocarp seeds

on October 18 2011rstbroyalsocietypublishingorgDownloaded from

were pre-dispersal seed predators even in the seedscollected from the forest floor

While the strength of density dependence was verysimilar in unlogged and logged forests seedfall and sur-vival rates were less so Mean seedfall and survival wereboth twice as high in the unlogged forest as the loggedforest Although the differences between forest types inboth seedfall and survival were non-significant thisreflects the large amount of variation between focaltrees within forest types rather than similar averagesLogging inevitably reduces the number of adults oftimber species and this may explain reduced seed pro-duction in the logged forest Increasing the distance ofdipterocarps to the nearest flowering conspecificreduces cross-pollination and subsequently decreasesseed set [255354] Logging has been observed toreduce seed production in previous work [5354] Theseed crop in logged forest may therefore be reduced atthe scale of the individual tree by high proportions ofunpollinated and self-pollinated flowers and at thelandscape scale by a decrease in the number of adulttrees Combined with the trend for survival to be high-est at trees with large seed crops this led nearly allsurviving seeds to be in unlogged forest Only sevenseeds remained in the non-manipulated plots inlogged forest at the end of the study compared with75 seeds in the unlogged forest Thus natural regener-ation in the logged forest was practically non-existentIt should be noted that even in the unlogged forestseedling densities were very low at the end of the exper-iment (less than 2 seed m22) and may therefore makelittle contribution to the recruitment of this species

One caveat applies to all our comparisons betweenunlogged and logged forest While one of this studyrsquosstrengths is that the forest types were relatively similarin composition prior to logging [5] we consideredonly one area each of unlogged and logged forestAlthough the replicate trees within each forest typewere far from each other (greater than 100 m) andmay be considered independent samples the con-clusions of this study apply to the forests around theDVCA and YSFMA Furthermore we consideredonly one species Parashorea malaanonan is very abun-dant and is a relatively fast-growing dipterocarpmaking it an atypical species Rarer species may bebetter able to escape from their natural enemies in

Phil Trans R Soc B (2011)

space and therefore show stronger distance and den-sity dependence Further studies at other pairedareas of unlogged and logged forest and withadditional species will be necessary to establish ifthe patterns discovered here apply to unlogged andlogged forests in general

(b) Causes of mortality

Vertebrates caused the vast majority of the observedseed and germinating seedling mortality in the fieldIt has been suggested that vertebrates are unlikely tocause such density dependence because they tend tobe mobile generalists ([55] but see [56]) The mobi-lity of these seed predators did not prevent themfrom generating strong negative density dependencein P malaanonan survival Because we did not considerheterospecifics here we cannot determine if mortalityincreased with conspecific density or just density ingeneral For the JanzenndashConnell mechanism to main-tain species richness increased density of a particularspecies must increase predation of heterospecifics lessthan conspecifics [57] It is quite possible that seedsof other species would not benefit from a rare speciesadvantage if they had dispersed into plots with highdensities of P malaanonan Other work at this sitehowever suggests that small vertebrates prefer conspe-cific dipterocarp seeds to heterospecific dipterocarpseeds but large vertebrates did not discriminatebetween them [58]

Our field data probably underestimate insect preda-tion of P malaanonan A proportion of insect-predatedseeds would have been removed from the plots(assuming vertebrates did not discriminate againstthem) Such seeds would have been scored as ver-tebrate-predated causing us to underestimate therole of invertebrates While we examined seeds forsigns of insect emergence holes these can be easilymissed in the field especially because insects oftenemerge from between the wings of dipterocarp seedsThese wings are formed from the calyx andP malaanonan has two long (9ndash16 cm) and threeshort (6ndash10 cm) wings [59] The area betweenthe wings is very rough and emergence holes theremight be overlooked Emergence rates from seedskept in the laboratory provide a more realistic estimate

Predation of dipterocarp seeds R Bagchi et al 3253

on October 18 2011rstbroyalsocietypublishingorgDownloaded from

of invertebrate attack In the absence of vertebrate pre-dators insects attacked about 9 per cent of seeds lowin comparison with other studies from the region[2551] However even our laboratory data will prob-ably underestimate insect predation About 54 percent of the seeds we collected showed evidence ofinsect predation but did not produce any insects andit is likely that seed predators left a proportion ofthese seeds before we collected them Some weevilsin the Nanophyidae have been recorded to emergeprior to seed dispersal [51] Furthermore much ofthe insect-related mortality of dipterocarp seedsoccurs early on in fruit development leading to abor-tion These early losses can be substantial [51] but weonly started collecting seeds once they were matureand therefore almost certainly underestimated theimpact of insects

(c) Mast fruiting and the JanzenndashConnell

mechanism

It is generally thought that practically no diptero-carp recruitment occurs in South East Asian forestsoutside community-wide mast-fruiting events [2728]However in this study 35 per cent of seeds in theunlogged forest and 17 per cent in logged forest sur-vived until the end of two months About 8 per centof the original seedlings in the non-manipulated plots(18 individuals) were still alive in the unlogged forestsites 10 months later equivalent to 045 seedlings m22

(R Bagchi 2005 unpublished data) Therefore con-trary to the general consensus at least somedipterocarps recruited in a non-mast year albeit insmall numbers It is of course very possible that theseindividuals will die before they reach maturity or thattheir recruitment makes a negligible contribution tothe population dynamics of P malaanonan While mor-tality rates are very high during the seed and earlyseedling stage described here the seedlings that sur-vived the duration of this study will probably have tosurvive for several decades in order to reach thecanopy [42] Without comparable data from a mastyear it is difficult to determine how the density of sur-vivors in this study compares but it is likely to be muchlower than expected after a mast fruiting

Maycock et al [25] similarly reported recruitmentoutside major fruiting events of the congenericParashorea tomentella at Sepilok Forest Reserveanother lowland forest in Sabah However Maycocket al [25] also reported negligible survival of other dip-terocarp species in the same fruiting event Onepossible explanation could be that P malaanonanseeds are unpalatable However various seed preda-tors (vertebrates and invertebrates) have beenrecorded attacking P malaanonan seeds and seedlings[3840] so this seems unlikely Maycock et al [25]suggested that P tormentella satiated seed predatorsbecause a high proportion of trees fruited over alarge area Parashorea species are extremely commonin both Danum and Sepilok and this may partlyexplain its success outside community-wide mastevents However data from very abundant species atother sites suggest no such patterns Two very abun-dant dipterocarp species Shorea lamellata and Shorea

Phil Trans R Soc B (2011)

quadrinervis both failed to recruit after producingseeds in non-mast years [2760]

5 CONCLUSIONIn this study seeds and seedlings produced during anon-mast year were predated by vertebrate predatorsand to a lesser extent insects This predation wasnegatively density dependent at small spatial scales inboth forest types suggesting species diversity oflogged forests will return to pre-logging levels morerapidly than might have been expected otherwiseHowever survival increased with density at a largerspatial scale probably because predators were satiatedSeed production was much lower in logged forest andcombined with the positive effects of large-scale den-sity on survival this resulted in recruitment beingalmost completely concentrated in unlogged forestThe failure of P malaanonan to recruit in loggedforest raises concerns about the ability of some treespecies to recover from logging If similar patternswere observed during mast years this would haveserious implications for the viability of logged forestsin the region Determining whether this is the caseshould be considered a research priority

This work was funded through PhD studentships to RBand EMS (Natural Environment Research Council UK)and CDP (Swiss National Science Foundation) and aCASE studentship to EMS (Natural History MuseumLondon) We thank the Danum Valley ManagementCommittee and the Economic Planning Unit of the PrimeMinisterrsquos Department Kuala Lumpur for permission toconduct research in Malaysia We thank Kevin Tuck(Natural History Museum London) and Darren Mann(Oxford University Museum of Natural History) for helpwith the identification of insect specimens Arthur Chung(Forest Research Centre Sabah) and Glen Reynolds(Director Royal Society SEARRP) provided invaluablesupport We thank Johnny Larenus Jamil Hanapi PhilipUlok Anna Gust and Alex Karolus for their fieldassistance and Miranda Davis and two anonymous refereesfor comments on the initial manuscript This paperconstitutes Publication Number A576 of the Royal SocietySouth East Asia Rainforest Research Programme

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Gallego J Richards T amp Malingreau J-P 2002Determination of deforestation rates of the worldrsquoshumid tropical forests Science 297 999ndash1002 (doi10

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2004 Southeast Asian biodiversity an impending disas-ter Trends Ecol Evol 19 654ndash660 (doi101016jtree200409006)

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8 Dent D H amp Wright S J 2009 The future of tropicalspecies in secondary forests a quantitative review BiolConserv 142 2833ndash2843 (doi101016jbiocon200905035)

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review of mechanisms of species coexistence Oecologia130 1ndash14

16 Novotny V Drozd P Miller S E Kulfan M JandaM Basset Y amp Weiblen G D 2006 Why are there somany species of herbivorous insects in tropical rainforests

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and in rain forest trees In Dynamics of numbers inpopulations (eds P J den Boer amp G R Gradwell) pp298ndash312 Wageningen The Netherlands PUDOC

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ing the JanzenndashConnell hypothesis a review andcritique In Tropical forest community ecology (eds W PCarson amp S A Schnitzer) pp 210ndash241 Oxford UKBlackwellrsquos

21 Bagchi R Press M C amp Scholes J D 2010 Evol-

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22 Webb C O amp Peart D R 1999 Seedling densitydependence promotes coexistence of Bornean rain

forest trees Ecology 80 2006ndash2017 (doi1018900012-9658(1999)080[2006SDDPCO]20CO2)

23 Blundell A G amp Peart D R 2004 Density-dependentpopulation dynamics of a dominant rain forest canopytree Ecology 85 704ndash715 (doi10189001-4101)

Phil Trans R Soc B (2011)

24 Itoh A Yamakura T Ogino K amp Lee H S 1995Survivorship and growth of seedlings of 4 dipterocarpspecies in a tropical rainforest of Sarawak East Malaysia

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Burslem D F R P 2005 Reproduction of dipterocarpsduring low intensity masting events in a Bornean rainforest J Veg Sci 16 635ndash646 (doi101111j1654-

11032005tb02406x)26 Curran L M Caniago I Paoli G D Astianti D

Kusneti M Leighton M Nirarita C E amp HaerumanH 1999 Impact of El Nino and logging on canopy tree

recruitment in Borneo Science 286 2184ndash2188(doi101126science28654472184)

27 Curran L M amp Leighton M 2000 Vertebrateresponses to spatiotemporal variation in seed productionof mast-fruiting Dipterocarpaceae Ecol Monogr 70

101ndash128 (doi1018900012-9615(2000)070[0101VRTSVI]20CO2)

28 Janzen D H 1974 Tropical blackwater rivers animalsand mast fruiting by the Dipterocarpaceae Biotropica 669ndash103 (doi1023072989823)

29 Bagchi R 2006 Factors influencing the diversity of treesin southeast Asian rain forests PhD thesis University ofSheffield Sheffield UK

30 Wright S J Zeballos H Dominguez I Gallardo MM Moreno M C amp Ibanez R 2000 Poachers alter

mammal abundance seed dispersal and seed predationin a neotropical forest Conserv Biol 14 227ndash239(doi101046j1523-1739200098333x)

31 Wyatt J L amp Silman M R 2004 Distance-dependence

in two Amazonian palms effects of spatial and temporalvariation in seed predator communities Oecologia 14026ndash35 (doi101007s00442-004-1554-y)

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the possible consequences of contemporary defaunationIn Plantndashanimal interactions evolutionary ecology in tropicaland temperate regions (eds P W Price T M LewinsohnG W Fernandes amp W W Benson) pp 273ndash287New York NY John Wiley and Sons

33 Curran L M amp Webb C O 2000 Experimental tests ofthe spatiotemporal scale of seed predation in mast-fruitingDipterocarpaceae Ecol Monogr 70 129ndash148 (doi1018900012-9615(2000)070[0129ETOTSS]20CO2)

34 Stoll P amp Newbery D M 2005 Evidence of species-

specific neighborhood effects in the Dipterocarpaceaeof a Bornean rain forest Ecology 86 3048ndash3062(doi10189004-1540)

35 Burgess P F 1966 Timbers of Sabah Sandakan Sabah

Forest Department of Malaysia36 Bebber D P Brown N D amp Speight M R 2002

Drought and root herbivory in understorey ParashoreaKurz (Dipterocarpaceae) seedlings in Borneo J TropEcol 18 795ndash804 (doi101017S0266467402002511)

37 Philipson C D et al In press Light-based regenera-tion niches evidence from 21 dipterocarp species usingsize-specific RGRs Biotropica

38 Wells K amp Bagchi R 2005 Eat in or take awaymdashseed pre-dation and removal by rats (Muridae) during a fruiting event

in a dipterocarp rainforest Raffles B Zool 53 125ndash13039 Whitmore T C amp Brown N D 1996 Dipterocarp

seedling growth in rain forest canopy gaps during sixand a half years Phil Tran R Soc Lond B 3511195ndash1203 (doi101098rstb19960102)

40 Slade E M 2007 The effects of tropical forest manage-ment on biodiversity and ecosystem functioning PhDthesis University of Oxford Oxford UK

41 Osada N Takeda H Furukawa A amp Awang M 2001Fruit dispersal of two dipterocarp species in a Malaysian

Predation of dipterocarp seeds R Bagchi et al 3255

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rain forest J Trop Ecol 17 911ndash917 (doi101017S0266467401001687)

42 Whitmore T C 1984 Tropical rainforests of the Far East2nd edn Oxford UK Oxford University Press

43 Kettle C J Hollingsworth P M Burslem D F R PMaycock C R Khoo E amp Ghazoul J 2011 Determinantsof fine-scale spatial genetic structure in three co-occurringrain forest canopy trees in Borneo Perspect Plant EcolEvol Syst 13 47ndash56(doi101016jppees201011002)

44 Chey V K 2002 Dipterocarp seed predators MalaysianNat 55 46ndash49

45 Lyal C H C amp Curran L M 2000 Seed-feeding

beetles of the weevil tribe Mecysolobini (InsectaColeoptera Curculionidae) developing in seeds of treesin the Dipterocarpaceae J Nat Hist 34 1743ndash1847(doi10108000222930050122165)

46 Lyal C H C Robinson G D Intachat J Bupaban-

pot J amp Curran L M 2011 The Dipterocarp insectseed-predator host database See httpwwwnhmacukresearch-curationresearchprojectsdipterocarpsseed-predationindexhtml (accessed January 2011)

47 Gelman A amp Hill J 2007 Data analysis using regressionand multilevelhierarchical models New York NY Cam-bridge University Press

48 Bolker B M Brooks M E Clark C J Geange SW Poulsen J R Stevens M H H amp White J-S S2009 Generalized linear mixed models a practical

guide for ecology and evolution Trends Ecol Evol 24127ndash135 (doi101016jtree200810008)

49 Egli P amp Schmid B 2001 The analysis of complex leafsurvival data Basic Appl Ecol 2 223ndash231 (doi10

10781439-1791-00048)50 R Development Core Team 2010 R a language and

environment for statistical computing Vienna Austria RFoundation for Statistical Computing

51 Toy R J Marshall A G amp Pong T Y 1992 Fruiting

phenology and the survival of insect fruit predatorsmdashacase-study from the South-East Asian DipterocarpaceaePhil Trans R Soc Lond B 335 417ndash423 (doi101098rstb19920033)

Phil Trans R Soc B (2011)

52 Schupp E W 1992 The JanzenndashConnell model for tro-pical tree diversitymdashpopulation implications and theimportance of spatial scale Am Nat 140 526ndash530

(doi101086285426)53 Murawski D A Gunatilleke I amp Bawa K S 1994

The effects of selective logging on inbreeding in Shoreamegistophylla (Dipterocarpaceae) from Sri LankaConserv Biol 8 997ndash1002 (doi101046j1523-1739

199408040997x)54 Ghazoul J Liston K A amp Boyle T J B 1998 Disturb-

ance-induced density-dependent seed set in Shoreasiamensis (Dipterocarpaceae) a tropical forest tree

J Ecol 86 462ndash473 (doi101046j1365-2745199800270x)

55 Hammond D S amp Brown V K 1998 Disturbancephenology and life-history characteristics factors influ-encing distancedensity-dependent attack on tropical

seeds and seedlings In Dynamics of tropical communities(eds D M Newbery H H T Prins amp N D Brown)pp 51ndash78 Oxford UK Blackwellrsquos

56 Paine C E T amp Beck H 2007 Seed predation by neo-tropical rain forest mammals increases diversity in

seedling recruitment Ecology 88 3076ndash3087 (doi10189006-18351)

57 Hille R Lambers J Clark J S amp Beckage B 2002Density-dependent mortality and the latitudinal gradientin species diversity Nature 417 732ndash735 (doi101038

nature00809)58 Hautier Y Saner P Philipson P Bagchi R Ong

R C amp Hector A 2010 Effects of seed predators ofdifferent body size on seed mortality in Bornean logged

forest PLoS ONE 5 e11651 (doi101371journalpone0011651)

59 Newman M F Burgess P F amp Whitmore T C 1999Malesian Dipterocarps Foresters CD-ROM ManualEdinburgh UK Royal Botanic Garden Edinburgh

60 Blundell A G amp Peart D R 2004 Seedling recruit-ment failure following dipterocarp mast fruitingJ Trop Ecol 20 229ndash231 (doi101017S0266467403001123)