Complementary seed dispersal by three avian frugivores in a fragmented Afromontane forest

Complementary seed dispersal by three avian frugivores in a fragmented

Afromontane forest

Lehouck, V.1,2�

; Spanhove, T.1,2,3

; Demeter, S.4; Groot, N. E.

5& Lens, L.

1,6

1Terrestrial Ecology Unit, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium; 2Ornithology Section,

Zoology Department, National Museums of Kenya, P.O. Box 40658, 00100, Nairobi, Kenya; 3E-mail ToonSpanhove

@hotmail.com; 4Behavioural Ecology and Conservation Group, Biodiversity Research Centre, Universite catholique

de Louvain, Croix du Sud 4, 1348 Louvain-la-Neuve, Belgium; Email [email protected]; 5Resource Ecology

Group, Wageningen University, Droevendaalsesteeg 3a, 6708 Wageningen, The Netherlands; Email [email protected];[email protected];

�Corresponding author; Fax 132 926 48794; E-mail [email protected]

Abstract

Questions: To what extent does species-specific variationin gut passage time (GPT), habitat use and mobility ofthree key avian frugivores synergistically affect the dis-tribution of Xymalos monospora seeds within and amongisolated forest fragments?

Location: Three fragments of a severely fragmented cloudforest, Taita Hills, southeast Kenya.

Methods: We experimentally determined GPTs of X.monospora seeds and recorded movements and habitatuse by Turdus helleri, Andropadus milanjensis and Tauracohartlaubi through radiotelemetry, and combined thesedata to generate species-specific seed dispersal patterns.

Results:Differences in mobility and habitat use among thethree frugivores caused significant complementarity inseed dispersal, despite the fact that gut transit times werehighly comparable. While the most sedentary and forest-dependent species mainly led to short-distance dispersalaway from parent trees, two more mobile species dispersedseeds further away from the source trees, both withinindigenous forest patches and towards exotic plantationsand isolated fruiting trees in the landscape matrix. A.milanjensis inhabiting a very small forest fragment spentsignificantly more time in the landscape matrix thanconspecifics residing in the two larger fragments.

Conclusions: By varying distances over which seeds arecarried away from parent trees and the habitat types inwhich they are ultimately deposited, avian frugivoresaffect the spatial distribution of seeds and early plantrecruits in a distinct and complementary manner. Becauselandscape properties are expected to lead to differentconstraints on avian mobility for habitat specialists andfor generalists, ecosystem processes such as avian seeddispersal are shaped by complex interactions betweendisperser behaviour and the environment.

Keywords: Africa; Birds; Cupressus; Eucalyptus; Exoticplantation; Fragmentation; Frugivores; Pinus; Taita Hills.

Nomenclature: Gill et al. (2009), International PlantNames Index (2008).

Introduction

Fleshy fruits are typically consumed by a widearray of frugivorous species that vary in the numberof seeds that they disperse and in their putative ef-fects on seed germination, and seedling growth andsurvival through handling, dispersal and depositionof seeds (Schupp 1993; Jordano & Schupp 2000).The cumulative seed dispersal pattern, i.e. the spa-tial distribution of seeds resulting from dispersal byfrugivorous species that differ in feeding habits,mobility or physiology, may affect the colonizationpotential of fleshy-fruited plants and shape theirpopulation dynamics, genetic structure, communitycomposition and diversity (Nathan & Muller-Land-au 2000; Wang & Smith 2002; Levin et al. 2003).Frugivores are therefore regarded as key drivers ofvegetation structure and dynamics (Herrera et al.1994; Nathan & Muller-Landau 2000; Levin et al.2003), especially in tropical rain forests that aredominated by fleshy-fruited trees (Fleming et al.1987; Estrada et al. 1993) and are characterized bypervasive seed limitation (Clark et al. 1999; Hubbellet al. 1999).

Dispersal of animal-dispersed seeds is typicallyinfluenced by multiple biotic and abiotic factorsthat may either act separately or in concert, and cantherefore be expected to be context-dependent. Forinstance, gut passage or regurgitation rates depend

Journal of Vegetation Science 20: 1110–1120, 2009& 2009 International Association for Vegetation Science

on the behaviour, morphology and physiology ofthe frugivores, as well as on properties of seeds,such as size, pulp-to-seed ratio and the presence ofsecondary compounds (Murray et al. 1994; Trave-set 1998). Mobility and habitat use of frugivores, inturn, not only depend on their behaviour and mor-phology (e.g. Jordano et al. 2007; Martınez et al.2008), but may also vary with season (e.g. Gehring& Swihart 2004; Bowen et al. 2007), time of the day(Westcott et al. 2005), landscape structure (Belisleet al. 2001; Revilla et al. 2004; Castellon & Sieving2006; Levey et al. 2008) and/or the spatiotemporaldistribution of critical resources such as food andwater (e.g. Morales & Carlo 2006; Thies et al. 2006;Lehouck et al. 2009c). Species-specific gut passageor regurgitation times of swallowed seeds, in combi-nation with the movement behaviour of frugivoreswhile seeds are carried, determine the primary dis-persal distance of animal-dispersed seeds (e.g.Murray 1988; Schupp 1993). This, in turn, mayshape patterns of plant recruitment at multiplespatial scales (Jordano et al. 2007; Spiegel &Nathan 2007). At a local scale, seed dispersal mayreduce density- or distance-dependent mortality asa result of decreased host-specific pathogen loading,seed predation, herbivory or sibling competitionaway from the parent tree (Janzen 1970; Connell1971; Augspurger & Kelly 1984). At a larger (land-scape-wide) scale, long-distance dispersal of seedsfacilitates the colonization of new habitats byplants, which may affect their (meta)populationsurvival and reproduction under directional habitator climate change (Johst et al. 2002; Pearson &Dawson 2005; Trakhtenbrot et al. 2005; Nathan2006).

Frugivores may vary in their effectiveness asseed dispersers both in terms of quantity, i.e. in thenumber of seeds dispersed, and quality, i.e. in sur-vival and recruitment rates of seeds after dispersal(Schupp 1993). Whereas quantitative variation inseed dispersal has been well documented in tempe-rate and tropical ecosystems, qualitative variationin dispersal effectiveness has long been ignored.Nevertheless, frugivores may strongly vary in theirimpact on plant recruitment, e.g. through differ-ential ability to move among isolated habitatpatches during gut passage of swallowed seeds oruse of (micro)habitats that are favourable for seedgermination and growth. When habitat patches areheterogeneously distributed across landscapes,movements of some seed dispersers, but not others,may become spatially constrained (e.g. Kremenet al. 2007). For example, in an Israeli desertecosystem, yellow-vented bulbuls (Pycnonotus bar-

batus) distributed seeds within natural forestpatches around wadis, while larger-sized, sympatricTristam’s starlings (Onychognathus tristramii) didso among isolated wadis (Spiegel & Nathan 2007).Similarly, in a temperate secondary forest in north-west Spain, rates of seed removal, dispersal anddeposition by five related Turdus species of com-parable size and physiology varied significantlywith their level of gregariousness (Martınez et al.2008). Based on such evidence, Jordano et al. (2007)and Spiegel & Nathan (2007) proposed to expandthe concept of ‘seed disperser effectiveness’ by im-plicitly incorporating effects of dispersal distanceand habitat use. Complementary seed dispersal byfrugivores, here defined as their differential con-tribution to the spatial distribution of seeds andseedlings, may hence arise from interspecific varia-tion in number of seeds dispersed, seed handlingbehaviour, movement patterns and habitat use. Inheterogenous landscapes, effectiveness of seed dis-persal likely varies among habitat patches, bothdirectly through variation in the composition offrugivore guilds, and indirectly through environ-mental effects on frugivore behaviour andperformance. This, in turn, may affect the level ofcomplementarity of seed dispersal and, hence, plantpopulation dynamics, genetic structure, communitycomposition and diversity (Nathan & Muller-Landau 2000; Wang & Smith 2002; Levin et al.2003).

Despite the potential implications for popula-tion ecology and conservation biology of fleshy-fruited plants, especially in heterogeneous land-scapes, variation in complementary seed dispersaland its effects on the spatial distributions of seedsdispersed from single plants (seed shadows sensuNathan & Muller-Landau 2000) remain poorly un-derstood. To fill this gap, we studied variation inseed dispersal of Xymalos monospora (Harv.) Warb.(Monimiaceae) by three sympatric avian frugivoresinhabiting a severely fragmented cloud forest insoutheast Kenya. Together, the three species dis-perse over 80% of all X. monospora seeds in thestudy area (Lehouck et al. 2009b), and 7 years ofcapture-recapture data (Lens et al. 2002) in combi-nation with 3 years of visual observations (V.Lehouck, unpubl. data) suggest interspecific varia-tion in mobility and tolerance to forest disturbance.To understand the behavioural and ecological dri-vers of dispersal of X. monospora seeds within afragmented forest ecosystem, we quantified species-specific gut passage times (GPTs) and movementcharacteristics of the three key avian frugivores, andstudied if, and to what extent, variation in these

- Complementary seed dispersal in a fragmented forest - 1111

traits affect dispersal of X. monospora seeds in threeisolated forest fragments.

Methods

Study area

The study was conducted in the Taita Hills for-est of southeast Kenya (031200S, 381150E, alt 1200-2208m), a severely fragmented cloud forest locatedat the northernmost edge of the Eastern Arc Moun-tains biodiversity hotspot (Burgess et al. 2007). Theregional climate is dominated by heavy rains duringthe cold season (March-May/June) and short rainsduring the warm season (October-December). Soilsare composed of a high-humic A-horizon overlayinga pinkish, acid sandy loam (Beentje 1988). Majorloss and fragmentation of the Taita forest started ca.200 years ago, and currently only 2% of the originalcloud forest cover is retained in three larger frag-ments (90, 133 and 179 ha), nine small ones (2-8 ha)and several tiny patches (o2 ha) (Beentje 1988;Appendix S1). Indigenous forest vegetation is clas-sified as moist montane forest, and comprises treespecies such as Strombosia scheffleri, Newtoniabuchananii, Chrysophyllum sp., Albizia gummifera,Cola greenwayi, Macaranga conglomerata, Syzygiumsclerophyllum, X. monospora, Tabernaemontanastapfiana and Phoenix reclinata (Beentje 1988). Mostindigenous forest fragments are bordered by exoticstands of Eucalyptus saligna, Cupressus lusitanicaand Pinus spp. planted for timber during the 1950-1980s (Beentje 1988; Mbuthia 2003), and are onaverage 5497 ( � 654)m apart from neighbouringforest fragments, embedded within a mosaic of hu-man settlements and smallholder cultivation plots(Beentje 1988). Despite significant loss, fragmenta-tion and deterioration of indigenous forest over thelast decades, the Taita forest continues to harbour ahighly diverse flora and fauna, including several en-demic bird, amphibian, reptile and plant species(Beentje 1988; Burgess et al. 2007).

Tree and bird species

X. monospora (Harv.) Warb. (Monimiaceae) is a6-20-m tall, dioecious tree, with small, cream-green-ish flowers that are arranged in unisexual panicles orracemes and fleshy, ovoid, yellow to reddish, single-seeded fruits (Verdcourt 1968). Average dimensionsof 120 fruits/seeds collected from 12 trees were: fruitlength (11.8 � 0.4mm), fruit width (9.4 � 0.3mm),seed length (9.6 � 0.2mm), seed width (7.3 �

0.4mm). In the Taita Hills, trees produce fruit dur-ing April-November (peaking in June to August),and fruits are mainly dispersed by birds (Lehoucket al. 2009b), with no evidence of secondary seeddispersal over long distances (J. Decoene andV. Lehouck, unpubl. data).

Within the study area, three forest specialistbirds, i.e. occurring almost exclusively in un-disturbed forest where they exclusively breed(Bennun et al. 1996), are responsible for dispersingover 80% of all X. monospora fruits (Lehouck et al.2009b). These are (i) Andropadus milanjensis (stripe-cheeked greenbul), a medium-sized passerine (36-54 g, gape width ca. 10mm) that lives in pairs orsmall groups and mainly forages on fruits in themiddle stratum and canopy, but occasionally at-tends ant swarms to feed on insects. In the TaitaHills, this species is abundant in the larger forestfragments and occurs at lower densities in most ofthe smaller fragments; (ii) Turdus helleri (Taitathrush), a medium-sized passerine (47-85 g, gapewidth ca. 12mm) that feeds on fruits and ar-thropods. It is endemic to the Taita Hills, where itonly survives in the three largest fragments and inone medium-sized fragment; (iii) Tauraco hartlaubi(Hartlaub’s turaco), a larger species (195-275 g, gapewidth ca. 12.5mm) that lives in pairs or small groupsand is nearly strictly frugivorous (Fry et al. 1988). Inthe Taita Hills, it occurs in low densities in largerforest fragments and only rarely visits the smallestones. Ingestion of X. monospora seeds by each of thethree frugivorous species significantly increasedtheir probability and rate of germination as com-pared to non-ingested control seeds, and similarresults were obtained for seeds of sympatric plantspecies (V. Lehouck et al., unpubl. data).

Bird movements

Movement behaviour of the three study specieswas examined in one small forest fragment (MAC,3 ha indigenous forest/25 ha including exoticstands), one intermediate-size fragment (CHA, 90/95 ha) and one large fragment (NGA, 133/161 ha)(see Appendix S1 for the landscape configurationaround these fragments). Individuals were capturedwith standard mist-nets between July-September2005 and July-September 2006, i.e. during the fruit-ing season of X. monospora. Upon capture, eachindividual was weighed, measured and banded witha steel numbered band and a unique combination ofcolour bands. A total of 30 adultA. milanjensis (fourin CHA, 12 in MAC, 14 in NGA) and nine adultT. helleri (one in CHA, eight in NGA) were fitted

1112 Lehouck, V. et al.

with lightweight Pip radio transmitters (BiotrackLtd, Dorset, UK) glued to their interscapulars.Two T. hartlaubi (one in MAC, one in NGA) wereprovided with a tail-mounted TW-4 transmitter(Biotrack Ltd.) sewn to their rectrices (methodolo-gical details in Sykes et al. 1990; Kenward 2001).Each transmitter weighed o2.5% of the species’mean body mass, which is less than half the thresh-old value proposed by Kenward (2001). Apart froma temporary increase in preening behaviour im-mediately after release, tagged individuals behaved,flew and fed normally, and recaptured individualswere in normal body condition. Following a 24-hhabituation period, individuals were tracked withportable TR-4 receivers (Telonics, Mesa, AZ, USA)and three-element flexible Yaggi antennas (BiotrackLtd.). To increase accuracy of mapping and to en-hance behavioural observations, individuals wereapproached up to 10m without interfering withtheir natural behaviour (homing-method sensuMillspaugh & Marzluff 2000), and GPS location(Garmin 60CSX; accuracy 5-15m), habitat type(indigenous forest, exotic plantation, farmland) andbehaviour (resting, preening, feeding, moving) wererecorded every fifth minute. Both in 2005 and 2006,individual birds were tracked for an average of 30 hover 20 days (06:30 to 18:30), with tracking sessionsrandomized according to forest fragment and timeof day.

Seed dispersal

To assess species-specific time windows duringwhich X. monospora seeds can be dispersed by thestudy species, we captured 90 adult A. milanjensisand 27 adult T. hartlaubi and fed each individualwith bananas to clear their guts (Denslow et al.1987). If during two subsequent defecations, noseeds were present in the faeces, each individual wasforce-fed three to five X. monospora fruits during asingle feeding session, and time intervals betweenswallowing and defecating were recorded as a mea-sure of GPT. To minimize stress during GPTexperiments, birds were individually held in cleancotton bags in situ and were checked every 5minuntil all seeds were defecated (in rare cases, birdswere released earlier). Birds were released at theirsite of capture within 3 h. Since we failed to catch arepresentative number of T. hartlaubi in the field, weperformed 31 feeding experiments on five captiveindividuals belonging to four Tauraco species (simi-lar in size and weight to T. hartlaubi; Appendix S2)in Antwerp Zoo (Belgium). As GPT is mainly afunction of body mass (Traveset & Verdu 2002) and

is generally comparable among congeners (Izhaki& Safriel 1990; Charalambidou et al. 2003), theseindividuals were considered valid proxies forT. hartlaubi. After a seedless diet mainly consistingof bananas and pellets (see also Denslow et al. 1987),each Tauraco was fed five ripe, intact X. monosporafruits that had been collected in the Taita Hills andwere stored at 51C. On average 96% (A. milanjensis),94% (T. helleri) and 99% (Tauraco spp.) of all seedsfed were subsequently retrieved in faeces. As o5%of seeds were regurgitated, these data were not usedin further analysis.

Throughout this paper, we assume that theaverage distance flown by a frugivore within a timeinterval equal to its median GPT, reflects the aver-age distance over which seeds are dispersed by thespecies. To obtain species-specific flying distances,movements of tagged individuals were recorded forat least 1 h and for up to 12 h in a single trackingsession, either immediately following the observedintake of a X. monospora fruit, or starting at a ran-dom point in time. For each tracking session, birdmovements recorded during time intervals that co-incided with median seed retention times were usedfor analysis of seed movement. Because presumeddispersal distances following the intake of aX. monospora fruit did not statistically differ fromthose covered during random sessions (A. mi-lanjensis: F1, 554 5 3.51, P5 0.06; T. hartlaubi andT. helleri P40.20), nor among tracking sessions be-fore 11.00, between 11.00 and 15.00 or after 15.00(A. milanjensis: F2, 574 5 1.40, P5 0.25; T. hartlaubi:F2, 134 5 1.97, P5 0.14; T. helleri: F2, 332 5 1.31,P5 0.27), data were pooled in all analyses.

Statistical analysis

Differences in mean GPT values among specieswere tested with non-parametric Mann-Whitney U-tests, averaging values per feeding session to ac-count for individual variance (Charalambidou et al.2003). Differences in movement distances amongspecies were tested with linear mixed models (PROCMixed) after log-transformation of the data. Differ-ences in proportion of time spent in different habitattypes (insufficient data available for T. helleri andT. hartlaubi) were tested with a binomial distribu-tion model (PROC Glimmix). To account forindividual variation in movement behaviour, factor‘individual’ was included as a random effect in all ofthe statistical tests. As among-individual variationin movement distances during median GPTs waslow (o10% of the total variation), tracking sessions

- Complementary seed dispersal in a fragmented forest - 1113

of all individuals were pooled. All analyses wereperformed with SAS v. 9.1.3 (SAS Inc. 2004).

Results

Median GPT values of X. monospora seeds wereof the same order of magnitude in the threestudy species (A. milanjensis 33min, 24-54min;T. hartlaubi 40min, 30-47min; T. helleri 34min, 26-57min; median and 25th and 75th percentiles, re-spectively) and did not significantly differ amongspecies (w22 5 0.62, P5 0.73; Fig. 1a-c). Presumeddispersal distances of X. monospora seeds varied be-tween 5 and 194m and significantly differed amongbird species (Table 1; F2, 26.7 5 5.19, P5 0.01). Inpairwise post hoc comparisons, values significantlydiffered between T. hartlaubi and T. helleri only(Tukey-Kramer t23.6 5 3.07, P5 0.01; other com-

parisons P40.05), with the largest average distancesand the longest distribution tails recorded in T. har-tlaubi, followed by A. milanjensis and T. helleri(Table 1, Fig. 1d-f). The percentage of movementsbeyond 150m during median GPTs was particularlylow in T. helleri (3%) but higher in A. milanjensis(12%) and T. hartlaubi (16% and 38% in each of thetwo individuals, respectively; Fig. 1d-i). Distancesmoved by A. milanjensis during median GPTs didnot significantly differ among fragments (F2, 22.7 5

1.05, P5 0.37; no comparison for other species).More than half of the 30 tagged A. milanjensis

visited plantations or scattered trees in farmland atleast once during tracking, thereby moving up to600m away from indigenous forest edges. In-dividuals inhabiting the smallest fragment (MAC)spent significantly more of their time outside in-digenous forest compared to individuals inhabitingthe two larger fragments (F2, 290 5 5.41, P5 0.005;

(a) (d)

(f)

Distance (m)

05

101520253035

T. hellerin = 337 (9)

0 100 200 300 400 500 60005

101520253035

A. milanjensisn = 30 (593)

freq

uenc

y (%

)

05

101520253035

T. hartlaubin = 141 (2)

(e)

(g)

0 1 2 3 4 5 60

100

200

300

400

500A. milanjensisn = 30

Delta time (h)

0

100

200

300

400

500T. hellerin = 9

Dis

plac

emen

t (m

)

0

100

200

300

400

500T. hartlaubin = 2

(h)

(i)

Fre

quen

cy (

%)

0

5

10

15

20

25

30T. hartlaubin = 31

0 20 40 60 80 100 120 140

0 100 200 300 400 500 600 0 1 2 3 4 5 60 20 40 60 80 100 120 140

0 100 200 300 400 500 600 0 1 2 3 4 5 60 20 40 60 80 100 120 140

0

5

10

15

20

25

30A. milanjensisn = 114

Time (min)

0

5

10

15

20

25

30T. hellerin = 26

(b)

(c)

Journal of Vegetation Science

Fig. 1. (a-c) Distribution of gut passage times of X. monospora seeds in A. milanjensis, T. hartlaubi and T. helleri; (d-f) dis-tribution of presumed displacement distances of X. monospora seeds away from source trees after median gut passage time;(g-i) distribution of displacement distances in time for each frugivore species (mean � SE). Black vertical lines and dark andlight grey areas indicate median, 25-75 percentile and minimum-maximum gut passage times, respectively (a-c and g-i).n5 number of individuals (a-c) or number of radio-telemetry sessions (g-i, d-f; number of individuals between brackets). ForT. hartlaubi, frequency distribution of movements (e) and displacements (h) are depicted per individual.

1114 Lehouck, V. et al.

CHA-MAC: t290 5 � 2.72, P5 0.02; NGA-MAC:t290 5 2.53, P5 0.03; CHA-NGA: t290 5 � 1.29,P5 0.4; Table 2). One A. milanjensis individual in-habiting fragment MAC spent 96.8% of its time inplantations and farmland. During tracking, both T.hartlaubi spent nearly half of their time in exoticplantations bordering indigenous forest fragmentsor in isolated trees in farmland (% time spent � SE:exotic plantation 15.37 � 8.29; trees in farmland30.39 � 0.94; indigenous fragment 54.24 � 7.35)and wandered up to 460m away from indigenousforest boundaries. In contrast to A. milanjensis andT. hartlaubi, all nine tagged T. helleri consistentlyrestricted foraging and movements to within the in-digenous boundaries of a single forest fragment.

Discussion

While transit times of ingested X. monosporaseeds were comparable among the three frugivorousbirds of a severely fragmented African cloud forest,species-specific differences in mobility and degree offorest dependency caused strong complementarityin seed dispersal. The highly sedentary and strictlyforest-dependent T. helleri mainly caused short-dis-tance dispersal away from parent trees, i.e. morethan 85% of the seeds were dispersed over 10m ormore. Such short-distance movements are widelyassumed to reduce density- or distance-dependentseed mortality through a decrease in sibling compe-tition or local pathogen infestation (Augspurger1983; Augspurger & Kelly 1984), which is supportedby a significant increase in seed germination andseedling survival of X. monospora with distancefrom the parental tree (Lehouck et al. 2009a). A.milanjensis and T. hartlaubi, in contrast, dispersedseeds over longer distances, both within indigenousforest patches and across forest boundaries to exoticplantations and small patches of fruiting trees with-in the landscape matrix. These mobile species maytherefore facilitate the colonization of new habitat

patches by X. monospora trees and other fleshy-fruited species with similar transit times (Higginset al. 2003; Levin et al. 2003). Fitness advantages forplants of the observed complementarity in dispersalof their seeds are mainly related to risk spreading:seeds that are deposited at short distances from theparent tree have a high probability of ending up in(micro)habitats that are suitable for germinationand growth, while seeds dispersed over longer dis-tances have a high probability of colonizing newhabitats, however, at the potential cost of facingless favourable environmental conditions (Harper1977). Due to the more frequent use of the landscapematrix by A. milanjensis that reside in small forestfragments, seeds from trees growing in such frag-ments may have a higher probability of movingthrough the landscape than those from conspecifictrees in larger fragments. Whether, and to what ex-tent, such asymmetrical seed dispersal additionallyaffects the genetic signature of forest fragmentation,requires further study.

Habitat use by animals is often asymmetrical,and their preference for particular microhabitatsmay influence movement directions and/or dispersaldistances depending on the spatial pattern of fa-voured microhabitats (e.g. Levey et al. 2005; Carlo& Morales 2008). In this study, the probability thatseeds were deposited into the landscape matrix wascontext-dependent, in that it varied between differ-ent-sized forest fragments. Earlier studies comparedvariation in dispersal distances and habitat use dur-ing seed deposition at higher taxonomic levels (e.g.mammals versus birds; Galindo-Gonzalez et al.2000; Jordano et al. 2007), or in relation to inter-specific variation in body size (Jetz et al. 2004;Jordano et al. 2007; Spiegel & Nathan 2007) andsocial behaviour (Martınez et al. 2008). While ourstudy was restricted to three avian frugivore speciesand three forest patches only, our results suggestthat interspecific variation in body size, and in mo-bility and degree of forest dependency in particular,may cause complementarity of seed dispersal in acontext-dependent way, i.e. depending on the inter-

Table 1. Distances moved by three avian frugivoresduring median and maximum gut passage times (GPT) ofX. monospora seeds (mean � SE and highest value).

Species DisplacementduringmedianGPT (m)

DisplacementduringmaximumGPT (m)

Highestdisplacementvalue duringmaximumGPT (m)

A. milanjensis 61.0 � 5.2 127.3 � 30.6 419.8T. hartlaubi 114.9 � 51.5 255.2 � 48.6 653.0T. helleri 44.7 � 3.7 86.5 � 17.7 373.0

Table 2. Proportion of time spent in three different habi-tat types by radio-tagged A. milanjensis originating fromthree different-sized indigenous forest fragments: MAC(3 ha), CHA (90 ha), NGA (133 ha).

Forest fragment % of time (mean � SE)

Indigenous Farmland Plantation

MAC 74.6 � 8.1 15.2 � 7.5 10.2 � 2.7CHA 99.3 � 0.5 0.5 � 0.6 0.2 � 0.3NGA 91.2 � 3.5 7.3 � 3.2 1.6 � 0.8

- Complementary seed dispersal in a fragmented forest - 1115

action between the behaviour of seed dispersal vec-tors and the environment.

While complementary seed dispersal may be acommon phenomenon in spatially structured popu-lations, it may be absent when the landscape matrixhampers mobility of all dispersal vectors. Althoughour design did not allow us to replicate fragmentsize, results from our study suggest that species thatare capable of exploring the landscape matrix do somore frequently when inhabiting smaller forestfragments, probably as a result of temporal foodshortages. The hypothesis of asymmetrical use ofthe landscape matrix around different-sized forestfragments by forest birds may have important con-servation implications, yet needs to be tested withmore species, more different-sized forest fragmentsand in different landscape contexts.

Apart from direct positive or negative effects ofgut passage on seed germination (Traveset 1998;Traveset & Verdu 2002), seed dispersal by frugivoresmay indirectly shape plant dynamics, e.g. by seeddeposition at different distances from the parenttrees (Jordano et al. 2007; Spiegel & Nathan 2007)or in different microhabitats that differ in suitabilityfor seed germination and seedling establishment(Schupp 1993; Jordano & Schupp 2000). Despite thefact that retention times of X. monospora seeds didnot vary among the three bird species, seed dispersaldistance by the large-bodied and strictly frugivorousT. hartlaubi was estimated to be twice that of thesmaller-bodied and partly frugivorousA. milanjensisand T. helleri. More than 60% of the dispersed X.monospora seeds were estimated to be depositedwithin 60m of parental trees (see also Howe et al.1985; Clark et al. 1999, 2005), while dispersal over150m (often referred to as ‘long distance dispersal’;see Levey et al. 2008) was rare. As GPTs for seeds ofother Afromontane tree species were broadly similarto those of X. monospora (V. Lehouck et al., sub-mitted), and dispersal distances tended to level-offwithin the gut retention range ofXymalos seeds (Fig.1), dispersal distances estimated for X. monosporaseeds likely apply to a wide range of species, includ-ing those with longer GPTs. Such a rapid levelling-off of distances moved by birds through time iscommonly reported in the literature and results inbroadly similar dispersal seeds of plant species dis-persed by the same frugivore community (Westcott& Graham 2000; Weir & Corlett 2007). Even whendisregarding the variation in distance over whichseeds were carried by the frugivorous species (i.e.difference between T. helleri and T. hartlaubi only),interspecific variation in habitat use still causedstrong complementarity in seed dispersal.

Quantitative knowledge of dispersal distances isparticularly important in patchy environmentswhere seeds may be distributed among isolated ha-bitat blocks with different probabilities (Nathan &Muller-Landau 2000; Bohrer et al. 2005). Despitebeing considered a true forest specialist (Bennunet al. 1996),A. milanjensis regularly dwelled in exoticplantations and surrounding farmland, especiallyindividuals that inhabited the smallest forest rem-nant. Such behaviour may explain why average seeddispersal distances were not significantly shorter inthis fragment compared to the larger fragments, aswould be expected if movements were constrainedwithin indigenous forest boundaries (e.g. Serio-Silva& Rico-Gray 2002). T. hartlaubi also regularly ven-tured into farmland or mixed indigenous-exoticpatches, independently of the size of the indigenousforest fragment. Excursions into the matrix weremainly directed towards isolated, fleshy-fruited treesor shrubs of indigenous (Ficus sp., Prunus africana,P. reclinata, Maesa lanceolata) as well as thoseof exotic (Maesopsis eminii, Cinnamom camphora,Lantana camara) origin, on which they foraged(Spanhove & Lehouck 2008; V. Lehouck et al., un-publ. data). Unless seeds consistently end up inunsuitable habitats for germination or seedling sur-vival, such excursions may eventually lead to thecolonization of new habitats by the trees. Results ofthis study further provide evidence that trees insmall and isolated forest remnants or in pastures(so-called outlier assemblages) may comprise im-portant sources of extraneous pollen and seeds,form nuclei for new populations and serve as inter-population bridges for pathogens and herbivores(Levin 1995). Whereas the majority of X. monosporaseeds from large forest fragments remained withinthe specific fragment boundaries, seeds from trees insmall and isolated fragments had a higher chance ofending up in other forest patches (see above), someof which may be unoccupied by this species. As ger-mination and survival rates of X. monospora seedsand seedlings in Eucalyptus, Pinus and Cupressusequalled those in indigenous forest (Lehouck et al.2009a), exotic plantation plots may also act as re-cruitment nuclei (Guevara & Laborde 1993;Parrotta 1995; Zahwai & Augspurger 2006). Be-cause isolated trees were earlier shown to enrich andintegrate population gene pools (Levin 1995; Al-drich & Hamrick 1998), the importance of small,isolated habitat patches for maintaining metapopu-lation integrity cannot be overestimated.

Forest fragmentation may affect fruit-frugivoremutualisms in several ways. For example, reduceddensities of quantitatively efficient dispersers (sensu

1116 Lehouck, V. et al.

Schupp 1993) may result in reduced seed removal(Cordeiro & Howe 2003), while local extinction oflong-distance dispersers (Kattan et al. 1994) and re-striction of bird movements among isolated forestremnants (Castellon & Sieving 2006) may hampercolonization of new habitats by plants. Such seeddispersal limitation may affect (meta)populationsurvival and reproduction under directional habitator climate change (Johst et al. 2002; Pearson &Dawson 2005). At community level, variation inseed dispersal may affect species coexistence andspecies richness through altering competitive bal-ances among plant species (Hurtt & Pacala 1995;Condit et al. 2002; but see Webb & Peart 2001). Forinstance, failure of seeds of dominant species toreach suitable microsites may facilitate local recruit-ment of less competitive species, hence increasingbeta-diversity (‘winning-by-forfeit’, Hurtt & Pacala1995). An earlier study in the Taita Hills revealedreduced removal rates of X. monospora seeds insmall and disturbed forest fragments (Lehouck et al.2009b), while over 700 h of radio-tracking (thisstudy) only revealed two movement events betweenneighbouring forest fragments (ca. 760m apart),albeit over a time-span of two consecutive days,and hence beyond the time window for dispersal ofviable X. monospora seeds. While direct evidence forseed dispersal between isolated forest fragments inour study area is therefore lacking, other sympatricfrugivores such as Ceratogymna brevis (silvery-cheeked hornbill) and Onychognathus morio (eed-winged starling) are known to make uninterruptedmovements beyond inter-fragment distances (Cor-deiro et al. 2004; pers. obs.). Whether or not theserare and unpredictable long-distance dispersalevents allow (meta)populations to persist in the longterm, remains unclear (Johst et al. 2002; Trakhten-brot et al. 2005). Action within forest fragments tomaximize local survival of frugivores, and acrosslandscapes to maximize their long-distance mobi-lity, may be advisable to enhance such long-distancedispersal.

Acknowledgements. We are grateful to the Kenyan Minis-

try of Education, Science and Technology for granting

research permission 13/001/33C306/2. We also wish to

thank M. Chovu, J. Decoene, D. Gitau, T. Imboma, N.

Mkombola, J. Mwadime, A. Mwaumba, M. Nyeri, H.

Parmentier and E.Wiersma for field assistance, the staff of

Antwerp Zoo for granting permission to conduct feeding

experiments, and B. Pellegroms for help with data man-

agement. Comments of N. Cordeiro on an earlier version

greatly improved this manuscript. VL and TS are research

assistants of the Research Foundation Flanders (FWO).

This study was made possible through FWO research

projects G.0210.04 and G.0055.08 to LL.

References

Aldrich, P.R. & Hamrick, J.L. 1998. Reproductive

dominance of pasture trees in a fragmented tropical

forest mosaic. Science 281: 103–105.

Augspurger, C.K. 1983. Seed dispersal of the tropical

tree, Platypodium elegans, and the escape of its

seedlings from fungal pathogens. Journal of Ecology

71: 759–771.

Augspurger, C.K. &Kelly, C.K. 1984. Pathogenmortality

of tropical tree seedlings: experimental studies of the

effects of dispersal distance, seedling density and light

conditions. Oecologia 61: 211–217.

Beentje, H. (ed.)., 1988. An ecological and floristic study

of the forests of the Taita Hills, Kenya. Utafiti 1: 23–

66.

Belisle, M., Desrochers, A. & Fortin, M.J. 2001. Influence

of forest cover on the movements of forest birds: a

homing experiment. Ecology 82: 1893–1904.

Bennun, L., Dranzoa, C. & Pomeroy, D. 1996. The forest

birds of Kenya and Uganda. Journal of East African

Natural History 85: 23–48.

Bohrer, G., Nathan, R. & Volis, S. 2005. Effects of long-

distance dispersal for metapopulation survival and

genetic structure at ecological time and spatial scales.

Journal of Ecology 93: 1029–1040.

Bowen, L.T., Moorman, C.E. & Kilgo, J.C. 2007.

Seasonal bird use of canopy gaps in a bottomland

forest. Wilson Journal of Ornithology 119: 77–88.

Burgess, N.D., Butynski, T.M., Cordeiro, N.J., Doggart,

N.H., Fjeldsa, J., Howell, K.M., Kilahama, F.B.,

Loader, S.P., Lovett, J.C., Mbilinyi, B., Menegon,

M., Moyer, D.C., Nashanda, E., Perkin, A.,

Rovero, F., Stanley, W.T. & Stuart, S.N. 2007. The

biological importance of the Eastern Arc mountains of

Tanzania and Kenya. Biological Conservation 134:

209–231.

Carlo, T.A. & Morales, J.M. 2008. Inequalities in fruit-

removal and seed dispersal: consequences of bird

behaviour, neighbourhood density and landscape

aggregation. Journal of Ecology 96: 609–618.

Castellon, T.D. & Sieving, K.E. 2006. An experimental

test of matrix permeability and corridor use by an

endemic understory bird. Conservation Biology 20:

135–145.

Charalambidou, I., Santamaria, L. & Langevoord, O.

2003. Effect of ingestion by five avian dispersers on

the retention time, retrieval and germination ofRuppia

maritima seeds. Functional Ecology 17: 747–753.

Clark, C.J., Poulsen, J.R., Bolker, B.M., Connor, E.F. &

Parker, V.T. 2005. Comparative seed shadows of

bird-, monkey-, and wind-dispersed trees. Ecology 86:

2684–2694.

- Complementary seed dispersal in a fragmented forest - 1117

Clark, J.S., Silman, M., Kern, R., Macklin, E. &

Hillerislambers, J. 1999. Seed dispersal near and far:

patterns across temperate and tropical forests. Ecology

80: 1475–1494.

Condit, R., Pitman, N., Leigh, E.G., Chave, J., Terborgh,

J., Foster, R.B., Nunez, P., Aguilar, S., Valencia, R.,

Villa, G., Muller-Landau, H.C., Losos, E. & Hubbell,

S.P. 2002. Beta-diversity in tropical forest trees.

Science 295: 666–669.

Connell, J.H. 1971. On the role of natural enemies in

preventing competitive exclusion in some marine

animals and in rain forest trees. In: den Boer, P.J. &

Gradwell, G.R. (eds.) Dynamics of populations. pp.

298–312. Center for Agricultural Publication and

Documentation, Wageningen, NL.

Cordeiro, N.J. & Howe, H.F. 2003. Forest fragmentation

severs mutualism between seed dispersers and an

endemic African tree. Proceedings of the National

Academy of Sciences of the United States of America

100: 14052–14056.

Cordeiro, N.J., Patrick, D.A.G., Munisi, B. & Gupta, V.

2004. Role of dispersal in the invasion of an exotic tree

in an East African submontane forest. Journal of

Tropical Ecology 20: 449–457.

Denslow, J.S., Levey, D.J., Moermond, T.C. &

Wentworth, B.C. 1987. A synthetic diet for fruit-

eating birds.Wilson Bulletin 99: 131–135.

Estrada, A., Coatesestrada, R., Meritt, D., Montiel, S. &

Curiel, D. 1993. Patterns of frugivore species richness

and abundance in forest islands and in agricultural

habitats at Los-Tuxtlas,Mexico.Vegetatio 108: 245–257.

Fleming, T.H., Breitwisch, R. & Whitesides, G.H. 1987.

Patterns of tropical vertebrate frugivore diversity.

Annual Review of Ecology and Systematics 18: 91–109.

Fry, C.H., Keith, S. & Urban, E.K. (eds)., 1988. The birds

of Africa. Vol. 3: parrots to woodpeckers. Academic

Press, London, UK.

Galindo-Gonzalez, J., Guevara, S. & Sosa, V.J. 2000. Bat-

and bird-generated seed rains at isolated trees in

pastures in a tropical rainforest. Conservation Biology

14: 1693–1703.

Gehring, T.M. & Swihart, R.K. 2004. Home range and

movements of long-tailed weasels in a landscape

fragmented by agriculture. Journal of Mammalogy 85:

79–86.

Gill, F., Wright, M. & Donsker, D. 2009. IOC World

Bird Names (Version 2.2). Available at http://www.

worldbirdnames.org

Guevara, S. & Laborde, J. 1993. Monitoring seed

dispersal at isolated standing trees in tropical pastures

– consequences for local species availability. Vegetatio

108: 319–338.

Harper, J.L. 1977. Population biology of plants. Academic

Press, London, UK.

Herrera, C.M., Jordano, P., Lopezsoria, L. & Amat, J.A.

1994. Recruitment of a mast-fruiting, bird-dispersed

tree-bridging frugivore activity and seedling establish-

ment. Ecological Monographs 64: 315–344.

Higgins, S.I., Lavorel, S. & Revilla, E. 2003. Estimating

plant migration rates under habitat loss and

fragmentation. Oikos 101: 354–366.

Howe, H.F., Schupp, E.W. & Westley, L.C. 1985. Early

consequences of seed dispersal for a Neotropical tree

(Virola surinamensis). Ecology 66: 781–791.

Hubbell, S.P., Foster, R.B., O’brien, S.T., Harms, K.E.,

Condit, R., Wechsler, B., Wright, S.J. & De Lao, S.L.

1999. Light-gap disturbances, recruitment limitation,

and tree diversity in a Neotropical forest. Science 283:

554–557.

Hurtt, G.C. & Pacala, S.W. 1995. The consequences of

recruitment limitation – reconciling chance, history

and competitive differences between plants. Journal of

Theoretical Biology 176: 1–12.

International Plant Names Index 2008. Available at

http://www.ipni.org

Izhaki, I. & Safriel, U.N. 1990. The effect of some

Mediterranean scrubland frugivores upon germina-

tion patterns. Journal of Ecology 78: 56–65.

Janzen, D.H. 1970. Herbivores and number of tree species

in tropical forests. American Naturalist 104: 501–527.

Jetz, W., Carbone, C., Fulford, J. & Brown, J.H. 2004.

The scaling of animal space use. Science 306: 266–268.

Johst, K., Brandl, R. & Eber, S. 2002. Metapopulation

persistence in dynamic landscapes: the role of dispersal

distance. Oikos 98: 263–270.

Jordano, P. & Schupp, E.W. 2000. Seed disperser

effectiveness: the quantity component and patterns of

seed rain for Prunus mahaleb. Ecological Monographs

70: 591–615.

Jordano, P., Garcia, C., Godoy, J.A. & Garcia-Castano,

J.L. 2007. Differential contribution of frugivores to

complex seed dispersal patterns. Proceedings of the

National Academy of Sciences of the United States of

America 104: 3278–3282.

Kattan, G.H., Alvarezlopez, H. & Giraldo, M. 1994.

Forest fragmentation and bird extinctions – San-

Antonio 80 years later. Conservation Biology 8: 138–

146.

Kenward, R.E. 2001. A manual for wildlife radio tagging.

Academic Press, London, UK.

Kremen, C., Williams, N.M., Aizen, M.A., Gemmill-

Herren, B., Lebuhn, G., Minckley, R., Packer, L.,

Potts, S.G., Roulston, T., Steffan-Dewenter, I.,

Vazquez, D.P., Winfree, R., Adams, L., Crone, E.E.,

Greenleaf, S.S., Keitt, T.H., Klein, A.M., Regetz, J. &

Ricketts, T.H. 2007. Pollination and other ecosystem

services produced by mobile organisms: a conceptual

framework for the effects of land-use change. Ecology

Letters 10: 299–314.

Lehouck, V., Spanhove, T., Gonsamu, A., Cordeiro, N.J.

& Lens, L. 2009a. Spatial and temporal effects on

recruitment of an Afromontane forest tree in a

threatened fragmented ecosystem. Biological

Conservation 142: 518–528.

Lehouck, V., Spanhove, T., Colson, L., Adringa-Davis,

A., Cordeiro, N.J. & Lens, L. 2009b. Habitat

1118 Lehouck, V. et al.

disturbance reduces seed dispersal of a forest interior

tree in a fragmented African cloud forest. Oikos 118:

1023–1034.

Lehouck, V., Spanhove, T., Vangestel, C., Cordeiro, N.J.

& Lens, L. 2009c. Does landscape structure affect

resource tracking by avian frugivores in a fragmented

Afrotropical forest? Ecography 32: 789–799.

Lens, L., Van Dongen, S., Norris, K., Githiru, M. &

Matthysen, E. 2002. Avian persistence in fragmented

rainforest. Science 298: 1236–1238.

Levey, D.J., Bolker, B.M., Tewksbury, J.J., Sargent, S.

& Haddad, N.M. 2005. Effects of landscape cor-

ridors on seed dispersal by birds. Science 309:

146–148.

Levey, D.J., Tewksbury, J.J. & Bolker, B.M. 2008.

Modelling long-distance seed dispersal in hetero-

geneous landscapes. Journal of Ecology 96: 599–608.

Levin, D.A. 1995. Plant outliers – an ecogenetic

perspective. American Naturalist 145: 109–118.

Levin, S.A., Muller-Landau, H.C., Nathan, R. & Chave,

J. 2003. The ecology and evolution of seed dispersal: a

theoretical perspective. Annual Review of Ecology

Evolution and Systematics 34: 575–604.

Martınez, I., Garcia, D. & Obeso, J.R. 2008. Differential

seed dispersal patterns generated by a common

assemblage of vertebrate frugivores in three fleshy-

fruited trees. Ecoscience 15: 189–199.

Mbuthia, K.W. 2003. Ecological and ethnobotanical

analyses for forest restoration in the Taita Hills,

Kenya. PhD Dissertation. Miami University Oxford,

Oh, US.

Millspaugh, J. & Marzluff, J. 2000. Radio tracking and

animal populations. Academic Press, San Diego, CA,

US.

Morales, J.M. & Carlo, T. 2006. The effects of plant

distribution and frugivore density on the scale and

shape of dispersal kernels. Ecology 87: 1489–1496.

Murray, K.G. 1988. Avian seed dispersal of 3 Neotropical

gap-dependent plants. Ecological Monographs 58:

271–298.

Murray, K.G., Russell, S., Picone, C.M., Winnettmurray,

K., Sherwood, W. & Kuhlmann, M.L. 1994. Fruit

laxatives and seed passage rates in frugivores –

consequences for plant reproductive success. Ecology

75: 989–994.

Nathan, R. 2006. Long-distance dispersal of plants.

Science 313: 786–788.

Nathan, R. &Muller-Landau, H.C. 2000. Spatial patterns

of seed dispersal, their determinants and consequences

for recruitment. Trends in Ecology and Evolution 15:

278–285.

Parrotta, J.A. 1995. Influence of overstory composition on

understory colonization by native species in

plantations on a degraded tropical site. Journal of

Vegetation Science 6: 627–636.

Pearson, R.G. & Dawson, T.P. 2005. Long-distance plant

dispersal and habitat fragmentation: identifying

conservation targets for spatial landscape planning

under climate change. Biological Conservation 123:

389–401.

Revilla, E., Wiegand, T., Palomares, F., Ferreras, P. &

Delibes, M. 2004. Effects of matrix heterogeneity on

animal dispersal: from individual behavior to

metapopulation-level parameters. American Naturalist

164: 130–153.

Schupp, E.W. 1993. Quantity, quality and the effective-

ness of seed dispersal by animals. Vegetatio 108: 15–

29.

Serio-Silva, J.C. & Rico-Gray, V. 2002. Interacting effects

of forest fragmentation and Howler monkey foraging

on germination and dispersal of fig seeds. Oryx 36:

266–271.

Spanhove, T. & Lehouck, V. 2008. Don’t miss the

invasives!. Journal of East African Natural History 97:

255–256.

Spiegel, O. & Nathan, R. 2007. Incorporating dispersal

distance into the disperser effectiveness framework:

frugivorous birds provide complementary dispersal to

plants in a patchy environment. Ecology Letters 10:

718–728.

Sykes, P.W., Carpenter, J.W., Holzman, S. & Geissler,

P.H. 1990. Evaluation of 3 miniature radio transmitter

attachment methods for small passerines. Wildlife

Society Bulletin 18: 41–48.

Thies, W., Kalko, E.K.V. & Schnitzler, H.U. 2006.

Influence of environment and resource availability on

activity patterns of Carollia castanea (Phyllostomidae)

in Panama. Journal of Mammalogy 87: 331–338.

Trakhtenbrot, A., Nathan, R., Perry, G. & Richardson,

D.M. 2005. The importance of long-distance dispersal

in biodiversity conservation. Diversity and Distribu-

tions 11: 173–181.

Traveset, A. 1998. Effect of seed passage through

vertebrate frugivores’ guts on germination: a review.

Perspectives in Plant Ecology, Evolution and

Systematics 1: 151–190.

Traveset, A. & Verdu, M. 2002. A meta-analysis of the

effect of gut treatment on seed germination. In: Levey,

D.J., Silva, W.R. & Galetti, M. (eds.) Seed dispersal

and frugivory: ecology, evolution and conservation. pp.

339–351. CABI Publishing, Wallingford, UK.

Verdcourt, B. 1968. Monimiaceae. In: Milne-Redhead, E.

& Polhill, R.M. (eds.) Flora of tropical East Africa.

Crown agents for oversea governments and

administrations, pp. 1–3. Royal Botanical Gardens,

Kew, London, UK.

Wang, B.C. & Smith, T.B. 2002. Closing the seed dispersal

loop. Trends in Ecology and Evolution 17: 379–385.

Webb, C.O. & Peart, D.R. 2001. High seed dispersal

rates in faunally intact tropical rain forest: theoretical

and conservation implications. Ecology Letters 4: 491–

499.

Weir, J.E.S. & Corlett, R.T. 2007. How far do birds

disperse seeds in the degraded tropical landscape

of Hong Kong, China? Landscape Ecology 22:

131–140.

- Complementary seed dispersal in a fragmented forest - 1119

Westcott, D.A. & Graham, D.L. 2000. Patterns of

movement and seed dispersal of a tropical frugivore.

Oecologia 122: 249–257.

Westcott, D.A., Bentrupperbaumer, J., Bradford, M.G. &

Mckeown, A. 2005. Incorporating patterns of

disperser behaviour into models of seed dispersal and

its effects on estimated dispersal curves.Oecologia 146:

57–67.

Zahwai, R.A. & Augspurger, C.K. 2006. Tropical forest

restoration: tree islands as recruitment foci in

degraded lands of Honduras. Ecological Applications

16: 464–478.

Supporting Information

Additional supporting information may befound in the online version of this article:

Appendix S1. Map of the study area above1200m altitude (forest–shrubland boundary) with

indication of the forest fragments CHA, MAC andNGA. Black polygons: indigenous forest fragments;grey polygons: plantations and isolated tree patches;white: settlements and smallholder cultivation plots(mainly bean, cabbage, maize, banana).

Appendix S2.Gut passage time of X. monosporaseeds in five captive-held Tauraco species.Nindividual5

number of individuals; Ntrial 5 number of feedingtrials, each consisting of five X. monospora fruits.

Please note: Wiley-Blackwell is not responsiblefor the content or functionality of any supportingmaterials supplied by the authors. Any queries(other than missing material) should be directed tothe corresponding author for the article.

Received 5 April 2009;

Accepted 8 June 2009.

Co-ordinating Editor: B. Collins.

1120 Lehouck, V. et al.