American Journal of Primatology 73:9–24 (2011)

RESEARCH ARTICLE

Primate Seed Dispersers as Umbrella Species: A Case Study From KibaleNational Park, Uganda, With Implications for Afrotropical Forest Conservation

JOANNA E. LAMBERT�

Department of Ecological Anthropology, The University of Texas at San Antonio, One UTSA Circle, San Antonio, Texas

Almost half of the world’s extant primate species are of conservation concern [IUCN, InternationalUnion for the Conservation of Nature Red List of Threatened Species, 2008]. Primates are also effectiveseed dispersers. The implications of and interactions between these two facts are increasinglyunderstood, and data demonstrating the consequences of losing primates for forest ecology are nowavailable from throughout the tropics. However, a reality is that not all species—and the mutualismsamong them—can be protected. Conservation managers must make difficult decisions and useshortcuts in the implementation of conservation tactics. Using taxa as ‘‘umbrellas’’ is one suchshortcut, although a lack of an operational definition of what an umbrella species is and how to chooseone has made implementing this tactic difficult. In this study, I discuss primates as umbrellas bydefining a selection index in terms of richness/co-occurrence, rarity, and sensitivity to anthropogenicdisturbance. I evaluate the anthropoid assemblage of Kibale National Park, Uganda, in light of theselection index and determine that Cercopithecus is the genus best fitting the criteria for umbrellastatus. I then evaluate the functional significance—in terms of seed dispersal—of using Cercopithecusmonkeys (guenons) as umbrellas. Results from 1,047 hr of observation of focal fruiting trees in Kibaleindicate that Cercopithecus ascanius was the most commonly observed frugivore visitor (July2001–June 2002). These data corroborate earlier data collected in Kibale demonstrating that guenonsare highly effective seed dispersers. Patterns of richness/co-occurrence, rarity, and sensitivity observedin Kibale are reflected in Afrotropical forests more generally, with the genus Cercopithecus tending toexhibit greatest richness/co-occurrence with taxonomically similar species, to be neither extremely rarenor ubiquitous, and also to be moderately sensitive to human disturbance. Moreover, in all availableevaluations of frugivory in Afrotropical forests, guenons emerge as among the most important seeddispersers relative to other taxa. Am. J. Primatol. 73:9–24, 2011. r 2010 Wiley-Liss, Inc.

Key words: Cercopithecus; Lophocebus; Procolobus; Colobus; Pan; Uvariopsis; Celtis; Ficus;conservation; frugivory; abundance; sensitivity; logging; rarity

INTRODUCTION

Almost half of the world’s extant primate speciesare of conservation concern [IUCN Red List, 2008].Primates are also highly effective seed dispersers inall habitats in which they are found [Chapman, 1995;Gross-Camp et al., 2009; Lambert & Garber, 1998;Stoner et al., 2007a; Vulinec et al., 2006]. Theimplications of—and interactions between—thesetwo facts regarding primates are increasingly under-stood; indeed, data demonstrating the consequencesof losing primates for plant species diversity, demo-graphy and recruitment are now available fromthroughout the tropics [Asquith et al., 1999; Brodieet al., 2009; Chapman & Chapman, 1995; Chapman& Onderdonk, 1998; Dirzo & Miranda, 1991;Guariguata et al., 2000; Gutierrez-Granados &Dirzo, 2010; Holbrook & Loiselle, 2009; Nunez-Iturriet al., 2008; Pacheco & Simonetti, 2000; Pannell,1989; Peres & Palacios, 2007; Stoner et al., 2007a,b;Vanthomme et al., 2010; Wang et al., 2007; Wright,

2003; Wright et al., 2000, 2007a,b]. In short, the lagtime between local primate population decline andits impact on forest ecology is closing.

A concurrent reality is that not all plant andanimal species (and the important mutualismsamong them) can be protected. Limited funds, time,and inventory data mean conservation managersalmost inevitably confront ‘‘conservation triage’’[sensu Marris, 2007] in their efforts to conserve

Published online 13 September 2010 in Wiley Online Library(wileyonlinelibrary.com).

DOI 10.1002/ajp.20879

Received 13 August 2009; revised 25 July 2010; revision accepted25 July 2010

Contract grant sponsors: McCauley Foundation; University ofOregon.

�Correspondence to: Joanna E. Lambert, Department of Ecolo-gical Anthropology, The University of Texas at San Antonio, OneUTSA Circle, San Antonio, TX. E-mail: joanna.lambert@utsa.edu

rr 2010 Wiley-Liss, Inc.

biodiversity. In a system dealing with resourceconstraints, the prioritization of a conservation unit(alleles, populations, species, genera, mutualisms,habitats, ecosystems, etc.) is a necessary shortcut inthe implementation of conservation tactics [Bifolchi& Lode, 2005; Caro & O’Doherty, 1998].

Using taxa as ‘‘umbrellas’’ is one such conserva-tion shortcut. This tactic is most appropriate insituations where managers need to prioritize an areafor protection on the basis of species richness. Usinga subset of a taxonomic group is typically more costefficient than surveying all members of that groupand thus appealing because of the promise ofmaximal data yield from minimum time and finan-cial commitment [Fleishman et al., 2000; Leader-Williams & Dublin, 2000; Terborgh, 1999].

However, umbrella tactics have not been withoutcontroversy. The lack of an operational definition ofwhat an umbrella species actually is, how to choseone, and thereby how to advance the umbrellaconcept from a theoretical construct to a useful toolhave all contributed to the contention over the utilityof an umbrella approach [Fleishman et al., 2000;Frankel & Soule, 1981; Leader-Williams & Dublin,2000; Roberge & Angelstam, 2003; Simberloff, 1998;Wilcox, 1984]. Terms such as ‘‘umbrella’’, ‘‘flagship’’,‘‘indicator’’, and ‘‘keystone’’ are often used inter-changeably and are easily conflated. In fact, whilebeing an indicator, flagship or keystone species doesnot preclude a species from serving as an umbrella(e.g. northern spotted owl, Strix occidentalis 5

flagship1umbrella), it is not a prerequisite charac-teristic [Dunk et al., 2006; Leader-Williams & Dublin,2000; Simberloff, 1998].

Among the most recent definitions of umbrellaspecies has been offered by Roberge and Angelstam[2003] who define umbrella species as: ‘‘specieswhose conservation confers protection to a largenumber of naturally co-occurring species’’ (p 77).I used this definition in this article adding: ‘‘yandthe important mutualisms among them’’ [see Sabo,2007; Table I).

However, even with a definition of what anumbrella species is, decisions regarding which taxonin a community has the greatest potential to serve asone is a challenging first step [Fleishman et al., 2000,2001]. The facts that primates are endangered andimportant seed dispersers whose removal has cascad-ing effects on forest ecology provide reasonable apriori justification for their selection broadly speak-ing (i.e. at the taxonomic level of Order). Butidentifying candidates at the genus, species, orsubspecies level with the greatest potential to serveas an umbrella for other taxa requires an explicit andoperationally defined formula.

Although investigations into the roles of primatesas seed dispersers have been undertaken since the1970s [e.g. Lieberman et al., 1979], there is a notablelack of explicit discussion regarding primates as

umbrellas; indeed, a database search using ‘‘pri-mates’’ and ‘‘umbrella’’ as search terms revealed onlya handful of references [e.g. Gippoliti & Sousa, 2004;Martins & Valladres-Padua, 2005]. Why this is thecase is not clear, although a lack of detailed naturalhistory data and few details regarding abundance anddistribution for many species are certainly implicated[Chapman & Peres, 2001; Cowlishaw & Dunbar,2000; Harcourt, 1998, 2006; Mittermeier et al., 2007;Struhsaker, 1999]. Thus, my overarching aim in thisreview was to explore primate seed dispersal in lightof recent discussion of umbrella species. Afteroperationally defining a method by which to select aprimate umbrella taxon, I integrated case study datafrom Kibale National Park, Uganda, with a broader

TABLE I. Definitions of Umbrella Species andSelection Variables (Richness/Co-occurrence, Rarity,and Sensitivity); After Roberge and Angelstam [2003],Cowlishaw and Dunbar [2000], Skorupa [1986], andHarcourt [1998]

Terms related toumbrellasspecies and taxonselection variables Definition

Umbrella species Species whose conservation confersprotection to a large number ofnaturally co-occurring speciesand the important mutualismsamong them [after Roberge &Angelstam, 2003]

Species richness andco-occurrence

Total number of species within agenus in a community ofsympatric primate species(assemblage)

Rarity When the abundance (]indvs/genus/km2) of a genus fallswithin the lower 25% of thefrequency distribution for allgenera within a primateassemblage [after Cowlishaw &Dunbar, 2000]

Common: when the abundance ofthat genus falls within the top25% of the frequencydistribution

Neither common nor rare: whenthe abundance of that genus fallsbetween 25 and 75% of thefrequency distribution for allgenera in a primate community

Sensitivity Index of response(sensitivity) 5 species density inanthropogenically disturbedforest: species density in primaryforest in the same site [afterSkorupa, 1986]

Sensitive: o0.5Not sensitive: >0.5 [after Harcourt,

1998]

Am. J. Primatol.

10 / Lambert

discussion of primates as umbrellas and seed dis-persers in Afrotropical forests. More specifically, mygoals in this article are to:

1. Discuss African primate species as umbrellas bydefining a selection index based on speciesrichness and co-occurrence, rarity, and sensitivityto anthropogenic disturbance.

2. Evaluate the anthropoid assemblage of KibaleNational Park, Uganda, in light of umbrellaselection criteria and determine which taxon inthis assemblage is the best candidate for umbrellastatus.

3. Present data from Kibale on the functional (interms of seed dispersal) significance of usingCercopithecus species as an umbrella taxon.

4. Consider the applicability and implications of datafrom Kibale for Afrotropical forests more generally.

HOW TO CHOOSE? UMBRELLA SPECIESSELECTION

In response to the lack of an operationaldefinition for selecting an umbrella species in anarea under consideration for protection, Fleishmanet al. [2000, 2001] have proposed and tested an indexbased on Great Basin butterfly species’ richness,co-occurrence with congenerics, rarity, and sensitivityto disturbance. These authors suggest explicitly thatthe selection must be carried out within a taxonomicgroup; congenerics have more similar ecologicalrequirements than phylogenetically distinct species[e.g. Fleagle & Reed, 1999] and hence are more likelyto encapsulate the ecological requirements of relatedspecies [Roberge & Angelstam, 2003]. From theiranalysis, Fleishman et al. [2000] conclude that toserve as an effective umbrella, a taxon must (withinan assemblage): (1) exhibit greatest richness and co-occurrence with taxonomically similar species; (2) beneither extremely rare nor extremely common; (3) bemoderately sensitive to human disturbance—i.e.neither completely extirpated nor able to exploitheavily human-modified landscapes.

There is a considerable merit in the use of all thethree variables (i.e. richness/co-occurrence, rarity,and sensitivity) in umbrella species selection. Rarityand sensitivity to anthropogenic impact are com-monly employed variables in umbrella strategies[Cowlishaw & Dunbar, 2000; Groom et al., 2006;Harcourt, 2006; Rodriguez & Rojas-Suarez, 1996].Yet these variables used in the isolation of considera-tion of other variables—e.g. richness/co-occurrence—may not result in the best taxon choice. For example,rare or sensitive species may not exhibit high levelsof co-occurrence with other species. Nor is choosing ataxon just on the basis of its rarity or commonness agood strategy. Species may be rare for many intrinsicand extrinsic reasons (e.g. body size, trophic level,

temporal/spatial patchiness of foods) other thananthropogenic disturbance. Very rare species aregenerally poor umbrellas and difficult to managebecause of their highly restricted distribution; con-versely, ubiquitous taxa are not useful for trackinganthropogenic impact [Fleishman et al., 2000].

Thus, in this article, I followed Fleishman et al.[2000] in their usage of all the three variables.Of these variables, species richness and their co-occurrence with congenerics is the most straightfor-ward to define. Fleishman et al. [2000] definerichness and co-occurrence by ranking a speciesaccording to their mean percentage of co-occurringspecies (PCS), averaging the number (n�1) ofbutterfly species in each microhabitat, and dividingthe average maximum possible number of co-occur-ring species in the total habitat. Using this method,the authors were able to identify the numbers ofbutterfly taxa by microhabitat in a region. Thisapproach is appropriate with butterflies (and otherinsects) that exhibit fine-grain microhabitat specia-lization and co-evolved relationships with a small setof plant species or—in some cases—a single planttaxon [Howe & Westley, 1988; Speight et al., 2008].However, such fine-scale assessment is difficult toapply to orders of magnitude larger-bodied, moregeneralist species such as primates whose homeranges (indeed daily paths) subsume multiple micro-habitat types. Another important consideration isthe taxon level of choice. ‘‘Species’’ is an unstabletaxonomic unit in primates [Groves, 2001; Harcourt,2006; Isaac & Purvis, 2004; Strier, 2006, 2007].Moreover, as suggested by Harcourt [2006] ‘‘deepertaxa carry a stronger historical signature than doshallower taxa and therefore might be more usefulthan species for detecting any evolutionary influ-ences on macroecological relationships’’ (p 2078).Thus, in this analysis, richness/co-occurrence isdefined as the total number of species within a genusin a community of sympatric primate species(Table I).

Ideally, an umbrella taxon should be neitherextremely rare nor extremely common. Measuringrarity in itself can be challenging, and indeed thevariable has been defined in multiple ways overthe years [Cowlishaw & Dunbar, 2000; Gaston,1994; Groom et al., 2006; Harcourt, 2000, 2006;Rabinowitz, 1981]. Fleishman et al. [2000] assessedrarity of butterfly species by calculating the propor-tional occurrence (Pj) of each species j across studymicrohabitats (canyons) and dividing by n; rarity(Qj) was then calculated as 1�Pj. Similar to richness/co-occurrence, this fine-grain definition is difficult touse with large, generalist species. For primates, mostauthors [e.g. see Cowlishaw & Dunbar, 2000;Harcourt, 2006] define rarity in terms of either lowpopulation density or small geographic range, orboth. Cowlishaw and Dunbar [2000] suggest thatrarity is most useful when defined in terms of a

Am. J. Primatol.

Primate Seed Dispersers as Umbrella Species / 11

threshold; they thus define a taxon as rare when itsabundance or range falls into the lower 25% of thefrequency distribution for that group. A group can bedefined in many ways, including taxon, phylogeny,ecosystem, geopolitical area, etc. In this study, I usedgenus as the taxon of interest and primate assem-blage (community) as the group and defined rarity asbeing when the abundance (]indvs/genus/km2) of agenus falls within the lower 25% of the frequencydistribution for all genera within a primate assem-blage. A taxon is ‘‘common’’ when the abundance ofthat genus falls within the top 25% of the frequencydistribution and ‘‘neither common nor rare’’ whenthe abundance of that genus falls between 25 and 75%of the frequency distribution for all genera in aprimate community (Table I). There can be (and are,see next section) extreme differences among generaor species in their abundance or biomass; underthese circumstances means are not the most infor-mative measure of central tendency. Thus, I usedmedian values.

Sensitivity is an extremely difficult variable toassess regardless of taxon (i.e. butterflies, primates,etc.) [Cowlishaw & Dunbar, 2000; Harcourt, 1998;Isaac & Cowlishaw, 2004; Johns & Skorupa, 1987].Fleishman et al. [2000] evaluated butterfly sensitiv-ity in terms of a disturbance-sensitivity index (DSI)based on life-history parameters deemed sensitive toanthropogenic impact (e.g. larval host-plant specifi-city, riparian habitat dependency). Proposing such aDSI requires simplifying intraspecific variation; themore plastic a species is, the more difficult suchsimplification becomes. Primates are noted for theirbehavioral and ecological flexibility with high levelsof intraspecific variance in response to shifts inextrinsic factors [Chapman et al., 2002; Cowlishaw &Dunbar, 2000; Strier, 2006, 2007, 2009; Struhsaker,2008]. For example, in an analysis of 28 species fromthree continents, after controlling for phylogeny,Harcourt [1998] found that only home range size andlatitude were correlated with sensitivity to logging,and concluded a general ecological model for pre-dicting risk is still lacking.

Nonetheless, assessing sensitivity must be acentral feature of identifying umbrella candidates.In this study, I assessed sensitivity through casestudies in which researchers evaluated the impact ofdisturbance on primate abundance; those speciesexhibiting the greatest response to human distur-bance were identified as the most sensitive, and viceversa. Such evaluations are valid only at the samesite because of the confounding effects of biotic andabiotic differences among forests. As noted by severalauthors [e.g. Chapman et al., 1999, 2010; Chapman& Peres, 2001; Harcourt 1998; Johns & Skorupa,1987; Struhsaker, 1997], there are extremely fewdata evaluating the impact of hunting and/or habitatloss on primate abundance. These data are alsohighly susceptible to sampling error. One of the

earliest and most thorough case studies comes fromSkorupa [1986] on the impact of selective logging(light logging, heavy logging, no logging) on primateabundance in Kibale National Park, Uganda. In thisstudy, I followed Skorupa [1986] and definedsensitivity via an index of response (sensitivity) 5

species density in anthropogenically disturbed forest:species density in primary forest in the same site.Because of the potentially considerable impact ofsampling error, following Harcourt [1998] taxa areconsidered ‘‘sensitive’’ if the index is less than orequal to 0.5 and ‘‘not sensitive’’ if the index is greaterthan 0.5 [see Harcourt, 1998, for discussion regard-ing application of this index; Table I].

In the next section, I evaluate the case study ofKibale National Park, Uganda, with the specific goalof identifying which of Kibale’s 13 primate speciesis the most appropriate umbrella taxon. I then evaluatethe functional significance—in terms of seed dispersal—of using the Cercopithecus taxon as an umbrella, andwhether patterns of richness/co-occurrence, rarity,and sensitivity of primates across Africa support thetaxon selection based on Kibale.

PRIMATE RICHNESS/CO-OCCURRENCE,RARITY AND SENSITIVITY

Kibale National Park, Uganda, As a Case Study

Kibale National Park, Uganda (01130�01190Nand 301190–301320E), covers an area of 766 km2 at anelevation ranging from approximately 1,200 to1,500 m [Struhsaker, 1975, 1997]. Roughly 60% ofthe park comprises primary and regenerating forest,ranging from medium-altitude moist evergreen tomedium-altitude semi-deciduous forest; the remain-ing 40% is occupied by grassland and swampcommunities, abandoned farms, and wetlands[Chapman & Lambert, 2000]. Because of its historyas a Forest Reserve (Kibale was gazetted as aNational Park in 1993), the forest was historicallyparceled into compartments that underwent varyingregimes of logging disturbance. Three of thesecompartments have received particular attentionwith regard to anthropogenic impact on primates:K-15, K-14, and K-30 [Chapman et al., 2000, 2010;Skorupa, 1988; Struhsaker, 1975, 1997]. K-15 is a347-ha section of forest that experienced heavyselective felling from September 1968 through April1969; approximately 50% of all trees in this compart-ment were destroyed by logging and incidentaldamage [Struhsaker, 1997]. Forestry compartmentK-14, a 405-ha forest block, was lightly and selec-tively harvested from May through December 1969;approximately 25% of all trees in this compartmentwere destroyed by logging and incidental damage[Skorupa, 1988; Struhsaker, 1997]. K-30 is a 282-haarea that has not been commercially harvested; thiscompartment is viewed as having intact forest

Am. J. Primatol.

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structure and species composition [Skorupa, 1988;Struhsaker, 1997; Skorupa & Kasenene, 1984].

The Kibale primate community is among therichest and most abundant in the world [Chapmanet al., 1999; Struhsaker, 1997] (Table II). Intensiveand long-term research on the abundance andbiomass of the primate community has been under-taken in Kibale since the early 1970s [Chapmanet al., 2000, 2010; also, see Chapman et al., 2005,for history of research in Kibale; Skorupa, 1986;Struhsaker, 1975, 1997, 2010]. I used Chapman et al.[2000, 2010], Skorupa [1986], and Struhsaker [1975,1997] as primary sources of data and informationregarding primate density/abundance, biomass, rar-ity and sensitivity.

All African Catarrhini and Prosimii subfamiliesare represented in Kibale: Colobinae, Cercopitheci-nae, Pongidae, Galaginae, and Lorisinae. Withregard to community richness and co-occurrence,evaluations at the family level (Galagidae (threespecies), Cercopithecidae (eight species), Pongidae(one species) suggest that monkeys are the richesttaxon. Patterns at the subfamily reveal that mostmonkey taxonomic richness is among Cercopitheci-nae (six of eight species), with three of theserepresented by the genus Cercopithecus.

Evaluations of rarity and sensitivity rely onabundance data. Although Chapman et al. [2010]report primate abundance data collected in K-30,K-14, and K-15 between 1970 and 2006, thesenumbers are presented as group density/km2.Because rarity in this article is defined in terms ofindividual density, I evaluated the data reported byStruhsaker [1997] who provides information regard-ing individuals/km2 in unlogged (K-30) and logged(K-14 and K-15) compartments.

In Kibale, primate species differ in occurrenceand sensitivity (Table II). In both logged andunlogged forest compartments, Procolobus rufomi-tratus is the least rare, and Pan troglodytes the mostrare. That the one ape in the sample is also the most

rare species is not a surprise; regression analysis hasdemonstrated that in general, large-bodied primates(e.g. apes) tend to be found at lower densities thansmaller-bodied primates [Clutton-Brock & Harvey,1977; Harcourt, 2006].

Following Harcourt [1998] and his use ofSkorupa’s [1986] index of sensitivity (density indisturbed forest over the density in primary forest inthe same site; r0.5 5 ‘‘sensitive’’; Z0.5 5 ‘‘not sen-sitive’’), in Kibale, all species (Table II) were‘‘sensitive’’ except for Colobus guereza. In otherevaluations of levels of Kibale species’ sensitivity tologging [Skorupa, 1986, 1988; Struhsaker, 1997],anthropoids were classified in terms of sub-guilds ofsensitivity; these sub-guilds reveal a more complexpattern of response. Skorupa [1986, 1988], forexample, classified Lophocebus albigena, Cercopithe-cus lhoesti, Procolobus rufomitratus, and Pan troglo-dytes as belonging to a ‘‘mature-forest core primatespecies’’ sub-guild and sensitive to anthropogenicimpact. Cercopithecus mitis, C. ascanius, and Colo-bus guereza were placed into a sub-guild less obligateto mature forest, and hence less sensitive to logging[Skorupa, 1986, 1988; Struhsaker, 1997]. As such, allKibale primate species were sensitive to logging withthe exception of Colobus guereza, which is ubiquitousand capable of tolerating a moderate amount oflogging [Chapman et al., 2000, 2010; Oates, 1996;Skorupa, 1986, 1988; Struhsaker, 1997].

In summary, in Kibale National Park, Cerco-pithecus emerges as the best candidate for umbrellastatus in that it (1) exhibits greatest richness and co-occurrence with taxonomically similar species and(2) is neither extremely rare nor ubiquitous. Aswould be expected given the diversity of primateresponses to disturbance [Cowlishaw & Dunbar,2000; Isaac & Cowlishaw, 2004], Cercopithecusspecies are more complicated in terms of sensitivity,with one species (C. lhoesti) obviously sensitive byany index; however, overall, this genus exhibits asensitivity pattern that is (3) moderately sensitive to

TABLE II. Primate Density of Diurnal Anthropoids in Logged (K-12, K-14, K-15, K-17, K-28, and K-29) andUnlogged (K-30) Forestry Compartments of Kibale National Park, Uganda

Family SpeciesDensity in logged

forestry compartmentsDensity in unlogged

compartment Sensitivity index

Colobinae Procolobus rufomitratus 109 (159) 300 0.36Colobus guereza 34.2 (26) 12.3–100 [mean 5 56] 0.34–2.78 [mean 5 0.61]

Cercopithecinae Cercopithecus ascanius 53.7 (184) 158 0.34Cercopithecus mitis 28 (6.0) 44.5 0.63Cercopithecus l’hoesti 0.7 (5.0) 13.8 0.05Average Cercopithecus 27.6 72 0.38Lophocebus albigena 1.66 (45) 10.3 0.16Papio anubis – – –

Pongidae Pan troglodytes 0.18 (3.0) 1.98 0.09

Data from Struhsaker [1997] (note that logged forest density numbers in parentheses are those reported in Chapman and Lambert [2000], and included inthis study for comparison).

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Primate Seed Dispersers as Umbrella Species / 13

human disturbance—i.e. neither completely extir-pated nor unable to exploit heavily human-modifiedlandscapes.

FUNCTIONAL SIGNIFICANCE OFCERCOPITHECUS AS AN UMBRELLASPECIES

Primate Seed Dispersal in Kibale NationalPark, Uganda

In this section, I explore the functional implica-tion of using Cercopithecus monkeys (guenons) as anumbrella; in this case, ‘‘functional implication’’ isdefined in terms of the degree to which various taxaserve as seed dispersers in a forest and thusumbrellas for important plant–animal mutualisms.My underpinning rationale for evaluating seeddispersal mutualisms within a discussion of umbrellaspecies stems from research indicating that theremoval of frugivorous, seed-dispersing primateshas consequences for plant diversity, recruitment,and population genetics. Although primates aregenerally demonstrated to be highly effective seeddispersers in all habitats and continents in whichthey are found, assessments of their impact are oftenmade in the absence of consideration of their relativeimpact. By estimating the number of seeds dispersedby a taxon (e.g. Cercopithecus species) and thequality of that dispersal relative to other taxa (e.g.primate or otherwise), it is possible to substantiateclaims of their utility as an umbrella for importantplant–animal mutualisms.

In this study, I present new data from KibaleNational Park, Uganda, documenting patterns ofvisits by frugivores (primates, birds, and arborealmammals) to common zoochorous tree species in thestudy area. In undertaking this research I compliedwith the protocols approved by the University ofOregon Animal Care and Use Committee andadhered to policy outlined by the Ugandan NationalCouncil for Science and Technology and theAmerican Society of Primatology’s policy on theethical treatment of nonhuman primates.

With the assistance of three field assistants(Agaba Erimosi, John Rusegwe, and PatrickKataramu), I monitored all frugivore visitors to 42individual trees (of three species) in Kibale’s K-14and K-15 compartments for a total of 1,047 hr for 12days/month over a 12-month period (July 2001–June2002). The tree species sample included Ficusexasperata (Moraceae, Vahl), Uvariopsis congensis(Annonaceae, Robbins & Chesquiere), and Celtisdurandii (Ulmaceae, Engl.; Table III). The focal treespecies are neither rare nor endangered; they werechosen because they occur commonly in the studyarea and elsewhere in Kibale, exhibit a diversity ofzoochorous fruit types, and had a fruiting pheno-phase during the study period. In terms of stem T

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Am. J. Primatol.

14 / Lambert

density (]indv/ha >10 cm DBH), Uvariopsis congen-sis is the most abundant tree in the study area, Celtisdurandii the third, and Ficus exasperata the mostcommon fig [Chapman & Chapman, 1997; Chapmanet al., 2005; Howard, 1991]. The choice of specifictrees was determined by 1 day/month of reconnais-sance of logged (K-14) and unlogged (K-30) forestrycompartments. Previously established trails werewalked and trees non-randomly selected on the basisof (1) whether the crown of the tree was readilyobserved and not visually obstructed by canopycover, (2) whether they were actively producingfruit, and (3) whether they had DBH greater than20 cm (Table III).

Focal trees were observed from 0800 to 1730 hr.All vertebrate frugivore visitors to the focal trees wererecorded, but only if they were observed to feed;animals using trees for roosting or as a travel pathwere not recorded. Numbers of individual feedingfrugivores in a tree’s crown were recorded every15 min to allow for fine-scale monitoring of animalentry and exit; this resulted in four 15-min intervals/hrand an average of thirty-six 15-min intervals/tree/day.To avoid repeated measures, if an animal was in a tree>one 15-min interval, it was not re-counted; only newarrivals to a tree were used in the summing of totalfrequency of visitors.

The vertebrate sample included four cercopithe-cine species (Cercopithecus mitis, C. mitis, C. lhoesti,Lophocebus albigena), two colobine species (Procolobusrufomitratus tephrosceles, Colobus guereza), and oneape (Pan troglodytes) (Table II). In addition toprimates, visitation and frugivory of diurnal frugivor-ous birds (Families: Columbidae, Musophagida,Bucerotidae, Sturnidae, Psittacidae) and squirrels

were also monitored (Table IV). Although squirrelsand parrots are known seed predators, similar tocolobines, they can also serve as seed dispersers [Forget& Wenny, 2005; Norconk et al., 1998]. Elephants(Loxodonta africana)—known to disperse seeds inKibale [Chapman et al., 1992; Cochrane & Reef,2003]—did not range within the study area duringthis year. It is important to note that nocturnalfrugivores, including primates (e.g. Perodicticus potto)and bats (e.g. Hypsignathus monstrosus) werenot monitored. Moreover, the sampling hours(0800–1730 hr) do not include approximately 2 hrof daylight during which diurnal frugivores mayhave visited trees. Without data from a 24-hrsampling period, our understanding of fruit removalis incomplete.

A total of 1,047 hr of direct observation of the 42focal tree species resulted in 4,186 15-min intervalsduring which all frugivore visits were recorded(Table V–VII). Summed across species and individualtrees, 952 of 4,186 intervals (23%) had recordsof feeding frugivores, 725 (76%) of which wereprimates. Cercopithecus ascanius accounted forthe largest fraction of visits across primates(275/952 5 29%; Tables VI and VII). There wereclear differences in the number of—and which—species were observed in focal trees (Table V–VII).Undoubtedly, this is partially due to sampling bias,with a greater number of observational hoursdevoted to Ficus exasperata. Nonetheless, it isnoteworthy that, similar to the results reported byChapman and Chapman [1996] (in which n 5 12 focaltrees), in over 230 hr of direct observation ofUvariopsis congensis and Celtis durandii there wasno bird visitation.

TABLE IV. Frugivores Observed in Focal Trees, K-14 and K-30 Forestry Compartments, Kibale National Park,Uganda, 2001–2002

Class Family Genus species Common name

Aves Columbidae (Doves and Pigeons) Aplopelia larvata Lemon DoveColumba arquatrix Olive PigeonColumba unicincta Afep PigeonStreptopelia semitorquata Red Eyed DoveTurtur tympanistria Tambourine DoveTreron australis Green Pigeon

Psittacidae (Parrots) Psittacus erithacus African Grey ParrotMusophagidae (Turacos) Corythaeola cristata Great Blue TuracoBucerotidae (Hornbills) Bycanistes subcylindricus Black & White Casqued HornbillSturnidae (Starlings) Cinnyricinclus leucogaster Violet-backed Starling

Lamprotornis purpureiceps Purple-headed Glossy StarlingLamprotornis splendidus Splendid Glossy StarlingOnychognathus fulgidus Chestnut-winged StarlingPoeoptera stuhlmanni Stuhlmann’s Starling

Mammalia Sciuridae (Squirrels) Heliosciurus rufobrachium Red-legged Sun SquirrelFunisciurus sp.a Thomas’s Tree Squirrel (F. anerythus)

Cuvier’s Tree Squirrel (F. pyrrhopus)Protoxerus stangeri Giant Forest Squirrel

aUnable to positively identify which of two Funisciurus species was observed; note that some authors view these as one species [Haltenorth & Diller, 1980].

Am. J. Primatol.

Primate Seed Dispersers as Umbrella Species / 15

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Am. J. Primatol.

16 / Lambert

Data on seed handling (i.e. spit, drop, swallow, ordestroy) and feeding rates were difficult to collectbecause of observation conditions. However, resultsfrom previous work [Lambert, 1997, 1998, 1999;unpub] can be recruited here (Table VIII). Overall,seed handling behaviors of a given fruit speciesare highly consistent within a frugivore species[Lambert, 1997, 1999, 2005]. Squirrels, parrots, andcolobines generally are seed predators, althoughoccasionally seeds escape mastication and are defe-cated or regurgitated intact. Sturnids, columbids,Corythaeola cristata, and Bycanistes subcylindricusare all known to be effective seed dispersers viaeither swallowing and defecating, or by mandibulat-ing and regurgitation. Cercopithecines (Cercopithe-cus, Lophocebus) spit out a majority of the seeds fromfruit they consume [Lambert, 1997, 1998]. Althoughthey can be seed predators as well, this is not the casefor the three tree species reported here. Pantroglodytes is almost invariably a seed swallower,and defecates seeds intact.

In summary, in this case study evaluation,Cercopithecus was the taxon that was most com-monly observed feeding in the study tree species,both in the logged and unlogged forest compart-ments. Of note is that cercopithecines have histori-cally been overlooked as seed dispersers, especially in

comparison with apes, perhaps because cercopithe-cines tend to be seed spitters rather than seedswallowers. For example, Wrangham et al. [1994]suggested that Pan troglodytes may be a moreimportant seed disperser than their low densitywould suggest. They based this assessment on thenumber of seeds defecated by chimpanzees versusmonkeys. Using primate density and numbers ofseeds in dung, they calculated that an individualchimpanzee disperses 147 seeds/km2/day, while anindividual monkey disperses 2.48 seeds/km2/day. Theauthors implicitly argue that the relative importanceof seed dispersal by chimpanzees is greater than therelative dispersal of seeds by monkeys.

However, in other work [Lambert, 1997, 1999,2001], I have demonstrated that Cercopithecusdisperses more seeds than any other primate taxonin the study areas of Kibale. Of 216 species of foresttrees, more than a third (77/216–37%) have seedsthat are dispersed by the frugivorous diurnalanthropoids of Kibale [Howard 1991; Lambert,1997, 1999]. Data on feeding rates, feeding boutduration, and population density indicate that in, ina single day, two Cercopithecus species (C. ascaniusand C. mitis) can move (via either spitting orswallowing then defecating) upwards of 33,840fruits/km2 in comparison with chimpanzee move-ment of seeds (via swallowing and defecation) of1,398 fruits/km2. These seeds are effectively [sensuSchupp, 1993] moved into safe sites [Kaplin &Lambert, 2002; Lambert, 2001, 2002]. Althoughsimilar to most tropical tree species there is a highmortality of primate-dispersed seeds in Kibale[Lambert, 2002], many seeds do escape predationand fungal attack and recruit effectively. From seedfate data [Lambert, 1997, 2000; Lambert & Chapman,2005], it is not unreasonable to expect about 1.0%survivorship of seeds moved by guenons and Pantroglodytes in Kibale Forest. If the daily removalnumbers are extrapolated to an annual removalnumber, and assuming that only 1.0% survives (andalso assuming that there is only one seed/fruit), then123,177 of the seeds that cercopithecines dispersesurvive versus 5,088 survivorship of seeds dispersedby Pan troglodytes, a 24-fold difference. Chapman andChapman [1996] have reported crop sizes for several

TABLE VI. Total Primate, Bird, and Squirrel Visitsto Study Trees, Kibale National Park, Uganda,2001–2002

Species visiting focal treesTotal visits (focal trees

and species pooled)

Total primate visits 725/952 (76%)Total Cercopithecinae visits 605/725 (83%)Total Colobinae visits 68/725 (9%)Pan troglodytes visits 52/725 (7%)

Total bird visits 195/952 (20.5%)Total Columbidae visits 49/195 (25%)Total Sturnidae visits 31/195 (16%)Total Corythaeola cristata visits 64/195 (33%)Total Bycanistes subcylindricusvisits

16/195 (8%)

Total squirrel 32/952 (3%)

Focal trees and species pooled.

TABLE VII. Most Common Visitors to Study Species, Kibale National Park, Uganda, 2001–2002

Frugivore species Celtis durandii Ficus exasperata Uvariopsis congensis

Total observation hours: 81.5 hr Total observation hours: 813 hr Total observation hours: 152 hr

Total intervals: 326 Total intervals: 3,252 Total intervals: 608

Intervals with visitors: 39 Intervals with visitors: 829 Intervals with visitors: 84

Cercopithecus ascanius 17/39 (44%) 224/ 829 (27%) 41/84 (49%)Cercopithecus mitis 12/39 (31%) 166/829 (20%) 17/84 (20%)Lophocebus albigena 10/39 (27%) 108/829 (13%) 24/84 (29%)Corythaeola cristata – 74/829 (9%) –Pan troglodytes – 50/829 (6%) 2/84 (2%)

Am. J. Primatol.

Primate Seed Dispersers as Umbrella Species / 17

Kibale trees, including Uvariopsis congensis. Thespecies average crop size for U. congensis is 925/indv.U. congensis trees occur at an average density of4,470 indv/km2, for a total average fruit availabilityof 4,134,750/km2. Assuming that all the individualsof a fruiting tree population have ripe fruit, and alsoassuming that the primates consume only one fruitspecies in a day, then in one square kilometer,monkeys remove approximately 0.8% of availableripe U. congensis fruit, and apes 0.03%. Thesenumbers support the argument that, in Kibale,guenons play absolutely and relatively importantroles in seed dispersal via spitting.

In addition to high-quantity of seed dispersal,Cercopithecus monkeys also provide high quality ofseed dispersal—the other component of seed dis-persal effectiveness [Schupp, 1993]. For example, theimpact of Cercopithecus seed processing and hand-ling can dramatically improve the germination ofStrychnos mitis [Lambert, 2001]. I have found thatCercopithecus ascanius spat out cleaned seeds ofStrychnos mitis in a majority of fruit-feeding records(477/542; 88%); seeds were occasionally swallowedwhole, but only when pulp was unripe (69/542; 12%).I monitored the fate of these spat seeds to gauge theimpact of monkey fruit processing and found that83% of spat seeds germinated, while only 12% ofunprocessed seeds survived to germination. Of theprocessed seeds that germinated, 60% survived togermination and seedling establishment, while only5% of unprocessed seeds survived to seedling estab-lishment. Unprocessed seeds were also significantlymore likely to be attacked by seed predators andfungal pathogens. Although I would not generalizethese results to other C. ascanius–plant interactions,these data do demonstrate highly effective seeddispersal similar to seed cleaning by myrmecochor-ous ants in the Neotropics [Oliveira et al., 1995].

APPICABILITY OF KIBALE CASE STUDY

As discussed at the outset, my incentive forevaluating seed dispersal mutualisms within a dis-cussion of umbrella species derives from datademonstrating that primate population decline hasdemonstrable consequences for forest ecology. In thisstudy, I evaluate the degree to which patternsobserved in Kibale are reflected in Afrotropicalforests more broadly. That is: (1) does Cercopithecusemerge elsewhere as an umbrella candidate on thebasis of richness/co-occurrence, rarity, and sensitiv-ity, and (2) what is the evidence that Cercopithecusspecies are effective and important seed dispersers inother forests in Africa?

Richness and Co-occurrence, Rarity, andSensitivity in Afrotropical Forests

The patterns of richness and co-occurrenceobserved in Kibale are mirrored elsewhere inT

AB

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Am. J. Primatol.

18 / Lambert

Africa—both across the continent and withinassemblage. Africa is home to a diversity of primatespecies (15 prosimians, 46 Cercopithecoids, and 3apes) [Chapman et al., 1999; Oates, 1996]. Of themonkeys, 39 species are classified within the Cerco-pithecinae, and seven within Colobinae. WithinCercopithecinae, 54% (21 spp) are in the genusCercopithecus. Cercopithecus also stands out as thetaxon with the greatest number of co-occurringcongenerics.

At the community level, there are few assem-blages for which detailed data on abundance areavailable (see Table II in Chapman et al. [1999]). Inan exhaustive review of the richness and abundanceof African primate fauna, Chapman et al. [1999]described Afrotropical primate communities as beingrich in cercopithecines, with the greatest abundanceamong colobines. As these authors note, at ninewell-studied sites in Africa (Tiwai, Sierra Leone;Tai National Park, Cote d’Ivoire; Douala-Edea,Cameroon; Lope, Gabon, Foret des Abielles, Gabon;Makokou, Gabon; Botsima, DR Congo; Ituri, DRCongo, Kibale National Park, Uganda, and Budongo,Uganda), it is the genus Cercopithecus that exhibitsthe richest co-occurrence with an average of 3.7species of Cercopithecus living sympatrically. Theleast Cercopithecus-rich community (two species;Botsima, Salonga National Park, DRC) (Table IX) isalso the least rich primate community overall amongthe comparative communities. Other well-studiedsites (e.g. Kakamega Forest, Kenya) show similarpatterns of richness [Table IX; Fashing & Cords,2000]. Thus, as with the Kibale case study, on averagethe genus Cercopithecus exhibits greatest richnessand species co-occurrence in Afrotropical forest.

In contrast to Kibale, where decades of datacollection using similar techniques have been used,assessing and generalizing rarity and sensitivity toanthropogenic impact across Africa is extremelydifficult for numerous reasons, including complexand diverse species responses to disturbance, extra-ordinary diversity in habitat type and biogeographyacross the continent, and limited data. A lack ofbaseline data is exacerbated by the fact thatthroughout Africa, primate populations are beingdecimated by an illegal commercial bush meat trade,logging, and habitat conversion before informationon rarity and sensitivity can be collected [Butynski,2002; Chapman & Peres, 2001; Cowlishaw &Dunbar, 2000; Harcourt, 1998; Mittermeier et al.,2007; Oates, 1999; Oates et al., 2000; Struhsaker,1999, 2005; Ukizintambara & Thebaud, 2002; Wilkieet al., 1992]. Even if abundance and distribution dataare collected in an area, they often are obsoletebefore they are incorporated into local conservationsolutions.

This is not to say that evaluations of rarity andsensitivity have not been undertaken. For example,using data from White [1994], Cowlishaw and

TABLE IX. Diurnal Primate Genera and Number ofSpecies Across Afrotropical Forests, in Well-StudiedSites Where Density Data Have Been Collected; AfterChapman et al. [1999], with data from Fashing andCords [2000]

Site Anthropoid community

Tiwai Island, Procolobus (2 species)Sierra-Leone Colobus (1 species)

Cercopithecus (4 species)Cercocebus (1 species)Pan (1 species)

Tai National Park, Procolobus (1 species)Cote d’Ivoire Colobus (2 species)

Cercopithecus (4 species)Cercocebus (1 species)Pan (1 species)

Forest des Abeilles, Procolobus (2 species)Gabon Colobus (1 species)

Cercopithecus (4 species)Lophocebus (1 species)Mandrillus (1 species)Cercocebus (1 species)Pan (1 species)Gorilla (1 species)

Lope Reserve, Gabon Colobus (1 species)Cercopithecus (3 species)Lophocebus (1 species)Mandrillus (1 species)Pan (1 species)Gorilla (1 species)

Makokou, Gabon Colobus (1 species)Cercopithecus (4 species)Miopithecus (1 species)Lophocebus (1 species)Mandrillus (1 species)Cercocebus (1 species)Pan (1 species)Gorilla (1 species)

Ituri Forest, Democratic Procolobus (1 species)Republic of Congo Colobus (2 species)

Cercopithecus (6 species)Miopithecus (1 species)Lophocebus (1 species)Mandrillus (1 species)Cercocebus (1 species)Papio (1 species)Pan (1 species)

Kibale National Park, Procolobus (1 species)Uganda Colobus (1 species)

Cercopithecus (3 species)Lophocebus (1 species)Papio (1 species)Pan (1 species)

Budongo Forest Reserve, Colobus (1 species)Uganda Cercopithecus (3 species)

Papio (1 species)Pan (1 species)

Kakamega Forest, Kenya Colobus (1 species)Cercopithecus (3 species)Papio (1 species)

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Dunbar [2000] found that at five sites in Gabon,primate species tended to either be common or rare,regardless of the site. Harcourt [1998] evaluatedprimate sensitivity to disturbance by selective log-ging (in Kibale, Budongo Forest (Uganda), and IturiForest, DRC). He determined that of eight Cerco-pithecus species, two were vulnerable, one (Cerco-pithecus ascanius) variably vulnerable or safe, andfive safe. Lophocebus was found to be both safe andvulnerable depending on site, Procolobus was vulner-able in all sites where abundance estimates areavailable, and Colobus sometimes safe and some-times vulnerable. In a meta-analysis of primateresponse to forestry, hunting, and agriculture, Isaacand Cowlishaw [2004] found that a species’ responseto one threat type is not predictive of its response toothers. In the most exhaustive evaluation of Cerco-pithecus sensitivity to date, Ukizintambara andThebaud [2002] analyzed the relationships amongtraits of 19 Cercopithecus species and extrinsicfactors, such as deforestation, hunting, war, humanpopulation density, gross national product, andprotection level. They found that the smallest-bodiedCercopithecus species with restricted distributionand ecological specialization were the most threa-tened. These results stand in contrast to Harcourt’s[1998] analysis suggesting that neither dietarybreadth nor geographic range correlated with Afri-can primate vulnerability to logging.

Thus, a highly complicated pattern of bothsensitivity and rarity emerges across the continent.Without further data, generalizations cannot bemade; yet, time and resources, among other variables(civil strife) preclude the collection of such data. Thisonly strengthens the argument for the use of anumbrella, and the proposition that Cercopithecuscould be useful is not contradicted by data fromoutside Kibale.

Primate Seed Dispersal in Afrotropical Forests

As with assessing species sensitivity, assessingand generalizing patterns of primate seed dispersalacross the continent is difficult for many reasonsincluding a lack of data. Very few studies havequantified the role of various frugivores in seeddispersal relative to other taxa. However, all avail-able data are consistent with the argument thatCercopithecus monkeys are important seed disper-sers relative to other taxa. For example, in NyungweNational Park, Rwanda, Gross-Camp et al. [2009]found that cercopithecines were most predictive ofeffective seed dispersal. Nyungwe is home to ninecercopithecine species, seven of which belong to thegenus Cercopithecus. The authors suggested Cerco-pithecus had the highest potential for seed dispersal(PSD) because they spend so much time in focal treesthat they tend to overlap with the greatest number ofspecies across all frugivore assemblages.

Poulsen et al. [2002] evaluated whether themajor seed dispersers (hornbills and primates) in theDja Reserve, Cameroon, have high fruit diet overlap.They tested the hypothesis that these taxa may beredundant seed dispersers, and that the loss of onetaxon may be compensated for by another. Five yearsof diet and seed removal data demonstrated thatprimates and hornbills have low dietary overlap andthat these taxa are not redundant as seed dispersers.The authors also determined that species could beclustered into dietary guilds and sub-guilds. Of these,the sub-guild comprising three Cercopithecus speciesemerged as having the greatest potential for disper-sing seeds [Poulsen et al., 2002].

Cercopithecus species may be the primarydispersers of a specific subset of Afrotropical trees.Data from several studies of frugivores in NyungweNational Park suggest that two forest tree specieswith relatively large seeds are not visited by turacos,understory birds, or chimpanzees, but are regularlyvisited by Cercopithecus monkeys [Kaplin & Lambert2002]. Similar findings come from studies conductedelsewhere. In Malawi, tree censuses over 16 monthsdemonstrated that of 134 fruiting tree species, fruitsof five species were visited by only Cercopithecusspecies [Dowsett-Lemaire, 1988]. In the BudongoForest, Uganda, Cercopithecus monkeys are the onlyfrugivores known to visit and disperse the seeds ofsix important tree species [Kaplin & Lambert, 2002;Plumptre et al., 1997].

CONCLUSIONS

Within the logged and unlogged forestry com-partments of Kibale National Park, the taxon bestfitting the selection criteria for an umbrella taxon isCercopithecus. Comparative data are too few andconfounded by biotic and abiotic variance to evaluateand compare broad patterns of rarity and sensitivityat a continental scale to that of Kibale. However,data from Kibale on primate richness/co-occurrenceare corroborated by (or, at least not contradicted by)data from throughout Afrotropical forests. Moreover,Cercopithecus is an important seed disperser, both inKibale and among Afrotropical forests across thecontinent. This is not to say that Cercopithecusmonkeys do not consume seeds; indeed, they areknown to be seed predators of some seed species,during some seasons, and in some habitats [Gautier-Hion et al., 1993; Kaplin & Moermond, 1998]. But inall research, Cercopithecus monkeys are predomi-nantly seed dispersers rather than predators [e.g.Gautier-Hion, 1984; Gautier-Hion et al., 1993;Kaplin & Moermond, 1998; Lambert, 1998; Rowell& Mitchell, 1991], and in all case studies whererelative contribution of seed dispersal is assessed,Cercopithecus species emerge as among the mostimportant as a function of high levels of frugivoryand—in some species—relatively high biomass [e.g.

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Dowsett-Lemaire, 1988; Gross-Camp et al., 2009;Plumptre et al., 1997; Poulsen et al., 2002]. Thesepatterns are consistent with the proposition that if ataxon-focused conservation approach were adopted,Cercopithecus would result in a reasonable umbrellastrategy that conserves co-occurring species, area,species interactions, and the dispersal requirementsof important canopy tree species.

However, the sobering reality is that 26% ofCercopithecus species are threatened with extinction,some critically so (e.g. Cercopithecus diana roloway isone of the world’s top 25 most endangered primates)[Butynski, 2002; Mittermeier et al., 2007; Oates,1999; Struhsaker, 2010]. Unless immediate anddramatic conservation action is undertaken at allscales of governance, using a Cercopithecus umbrellatactic may become obsolete. Using Cercopithecus asan umbrella does not preclude a strategy of umbrella1

flagship [Dunk et al., 2006; Simberloff, 1998].Cercopithecus monkeys themselves are charismaticand attractive forest species of interest to the public,and thus could serve as a flagship1umbrella species.Moreover, Gorilla gorilla and Pan troglodytes—species with proven success in flagship tactics—arealmost invariably found in sympatry with one ormore Cercopithecus monkeys. A strategy of targetingone taxon (Cercopithecus) as an umbrella, whileusing another species (Pan, Gorilla) as a flagshipcould be an alternative mixed strategy.

In closing, it is important to reiterate that thenew data presented in this study were collected for asingle year only. Moreover, the visits by nocturnalspecies (e.g. prosimians and bats) were not recorded;until all frugivore activity (24 h) is monitored, acomplete picture of fruit removal and seed dispersalcannot be known. As such, these results and analysisshould be viewed as preliminary and offered in thespirit of linking important sets of data: indicators ofprimate population decline and the cascading effectsof their removal on plant–animal mutualisms.

ACKNOWLEDGMENTS

I thank Sue Boinski and Marilyn Norconk forcritical feedback and for inviting me to contribute totheir important symposium. This article was greatlyimproved by thoughtful feedback from Paul Garber,Marina Cords, Jerry K. Jacka, and two anonymousreviewers. Research permission was granted by theOffice of the President, Uganda, and the UgandaWildlife Authority. Research assistance was providedby Agaba Erimosi, John Rusegwe, and PatrickKataramu; project oversight was facilitated by TomGillespie. The research complied with protocolsapproved by the University of Oregon Animal Careand Use Committee and adhered to policy outlinedby the Ugandan National Council for Science andTechnology and the American Society of Primatol-ogy’s policy on the ethical treatment of nonhuman

primates. I dedicate this article to my esteemedcolleagues Drs Thomas T. Struhsaker and Colin A.Chapman. Without their support, friendship, knowl-edge, and decades of dedication to the plight ofKibale, this research simply could not have beenundertaken.

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