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Stopping schistosomes from‘monkeying-around’ in chimpanzeesJ. Russell Stothard1, Lawrence Mugisha2,3 and Claire J. Standley4

1 Disease Control Strategy Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK2 College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, P.O. Box 7062, Kampala, Uganda3 Conservation and Ecosystem Health Alliance (CEHA), P.O. Box 34153, Kampala, Uganda4 Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA

Ngamba Island Chimpanzee Sanctuary (NICS) in LakeVictoria, Uganda is currently home to 44 wild-borne,semi-captive chimpanzees. Despite regular veterinaryhealth checks, it only came to light recently that manyanimals, and sanctuary staff, were naturally infectedwith Schistosoma mansoni. Indeed, local schistosometransmission appears firmly engrained for intermediatesnail hosts can be found along almost the entirety ofNgamba’s shoreline. Here, the epidemiology of infectionis a dynamic interplay between human and chimpanzeepopulations, as revealed by genetic analyses of S. man-soni. In this review, our present understanding of thiscomplex and evolving situation is discussed, alongsidegeneral disease control activities in Uganda, to highlightfuture interventions towards stopping schistosomemorbidity and transmission within this conservationsanctuary setting.

Definitive hosts of Schistosoma mansoni

Intestinal schistosomiasis caused by the trematode para-site S. mansoni is a neglected tropical disease of globalpublic health importance [1]. Although a scourge of manycommunities across sub-Saharan Africa, especially tothose living on the shoreline of Lake Victoria [2], whatis less well recognized is that this disease can be an(anthropo)zoonosis within animals other than humans,with infections potentially exhibiting similar clinical signsand symptoms [3,4]. The most well-known non-humanhosts of S. mansoni are perhaps rats, and in some partsof the world this parasite is almost completely sustained inrodent transmission cycles [5].

With our close phylogenetic proximity, however, it maycome as no surprise that given sufficient epidemiologicalopportunity, non-human primates (NHPs) can becomeinfected and sometimes act as fully competent definitivehosts; studies conducted in the 1960s and 1970s compre-hensively demonstrated that several NHPs were capable ofmaintaining transmission of schistosomiasis [6,7]. Whensampling opportunities have arisen, wild primates, partic-ularly baboons and chimpanzees, have been examinedparasitologically and sometimes found with disease[8–10]. Nonetheless, prior to the introduction of molecularDNA tools for detecting and genotyping parasites, no

studies have been able to clarify fully the levels of schisto-some population crossover, precisely striking the balancebetween zoonotic and(or) anthropozoonotic transmissioncycles [4].

Lake Victoria and intestinal schistosomiasisLake Victoria is particularly famous as the largest tropicalfreshwater water body in the world, but is also infamous inthe past half century for the extent of major ecologicalchanges it has undergone. Entirely apart from the bur-geoning human population along its shorelines, Lake Vic-toria hosted two of the most notorious human-mediatedspecies introductions in modern history: the catastrophicintroduction of Nile Perch in the 1950s [11,12], followed bythe accidental invasion of water hyacinth in the 1980s[13,14]. Both introductions and invasions have extensivelyperturbed the aquatic flora and fauna. It has been hypoth-esized, for example, that intermediate hosts of S. mansoni,freshwater snails of the genus Biomphalaria, have partic-ularly thrived and dispersed on floating vegetation matsprovided by the water hyacinth [14] and that their naturalfish predators, small cichlids which kept snail populationsin check, were decimated by Nile Perch. At the same time,the expansion of the Nile Perch fishing industry has fos-tered numerous fishing landing sites creating shanty-likehabitations and marginalized communities characterizedby both poor hygiene and sanitation. Unfortunately, intes-tinal schistosomiasis is almost universal within suchfisher-folk and associated populations [15,16].

Of the countries surrounding Lake Victoria, Uganda isperhaps the most afflicted by this disease [17,18]. In 2003,a National Control Program was launched with the inten-tion of providing mass drug administration of the anthel-mintic praziquantel to school-aged children and adultsliving within disease endemic areas, such as along theshorelines of Lakes Victoria and Albert as well as alongthe Nile itself [19,20]. During this time many of the com-munities living on the numerous islands within LakeVictoria were somewhat overlooked owing to the consider-able expenses in accessing and reaching these locations[2,21]. Moreover, certain communities on the Sesse Islandswere traditionally thought to be largely free from intestinalschistosomiasis and thus were not initially considered highpriority for control. This appraisal, however, was recentlyoverturned by targeted surveys showing there to be foci ofhyperendemic disease [22–24]; for example, at a quarter of

Review

Corresponding author: Stothard, J.R. ([email protected]).Keywords: Pan troglodytes; anthropozoonosis; intestinal schistosomiasis; LakeVictoria, Uganda.

320 1471-4922/$ – see front matter . Crown Copyright � 2012 Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2012.05.007 Trends in Parasitology, August 2012, Vol. 28, No. 8


the sites surveyed, local prevalence of infection was inexcess of 50%, although mean prevalence of intestinalschistosomiasis was 34.6% (95% confidence intervals =31.0–38.3) by stool sampling methods [23].

From additional surveying, the wide range in preva-lence or overdispersion of disease across the Sesse Islandgroup requires drug treatment regimes tailored to eachisland setting [23]. Confirmation that active transmissionwas occurring locally was later revealed by the observa-tions of high abundance of Biomphalaria as well as field-caught snails shedding S. mansoni cercariae [24]. Usingmolecular DNA methods, inspection of parasite geneticdiversity by DNA barcoding showed that previously en-countered and common genotypes were present, inclusiveof novel ones, which when taken together was consistentwith the high known genetic diversity of S. mansoni withinthis lake [1,24–26]. More broadly, the situation on theBufumira Island group demonstrated the existing chal-lenges well faced by the Ugandan National Control Pro-gram in reaching these rather remote, inaccessible andlargely itinerant populations. In addition, the local mala-cological fauna was then largely unknown with a poorlysampled and recorded freshwater snail species list. Thus,the remoteness and isolation of many of the islands in LakeVictoria have, until very recently, confounded surveyingand hampered control efforts not only for schistosomiasisbut also for other diseases such as malaria [21].

Ngamba Island and a new epidemiological opportunityWithin the above context, Ngamba Island presented itselfas somewhat of a long-term exception (Figure 1 and Box 1).This island first hosted a small fishing community duringthe 1970s and 1980s, remaining almost fully-forested, until1998 when it was taken over by the Chimpanzee Sanctuaryand Wildlife Conservation Trust (CSWCT) to become aconservation area under the auspices of the NICS. Thesanctuary was originally intended to act as a convenientoff-shore reserve with natural boundaries for holding res-cued chimpanzees and was particularly timely as theexisting sanctuary in Entebbe was becoming increasinglyoverburdened with the need to care for these animals exsitu. Upon handover, the 8000 m2 clearing left by thefishing village on its northern shore was subsequentlydivided up into a chimpanzee feeding station and animalaccommodation pens for the soon-to-arrive chimpanzees,as well as an associated island camp for NICS staff, andthen subsequently for visitors and tourists [24].

Although the remainder of the island remained a pro-tected forested area for the chimpanzees to rove and foragewithin, it was unable to sustain large numbers of animalsand was therefore partitioned from the feeding/accommo-dation station and staff camp by a tall electrified fence. Morebroadly, NICS also acts as an active conservation area andrefuge zone for other flora and fauna native to Lake Victoria;around the island there is an enforced no-fishing exclusion

Lake Victoria

Lake Victoria

50 km

10 km

Kampala

Entebbe

UGANDA(a) (c)

(d)(b)

Kimi

Ngamba

Kome Island

TRENDS in Parasitology

Figure 1. Ngamba Island Chimpanzee Sanctuary (NICS) on Lake Victoria. (a) Schematic depiction of the Ugandan shoreline of Lake Victoria illustrating the main island

groups. (b) Outline map of Ngamba and Kimi Islands. (c) Aerial photograph of Ngamba Island with the NICS camp highlighted (with white arrow). (d) Anesthetized

chimpanzee undergoing annual health check in NICS veterinary laboratory in 2011; (inset top) ultrasound image of chimpanzee liver depicting pipestem fibrosis, (inset

bottom) micrograph (�100) of egg of Schistosoma mansoni within rectal biopsy.

Review Trends in Parasitology August 2012, Vol. 28, No. 8

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zone stretching for 200 m offshore. This area is regularlyspot-patrolled by the NICS launch and island police officerwho is able to implement an onsite confiscation policy for allfishing apparatus and catches. At the inception of NICS thelocal endemicity of intestinal schistosomiasis was then un-known and information pertaining to the local presence ofintermediate snail hosts was also lacking. However, giventhe particularly high levels of wave exposure on the south-ern shoreline of NICS, it was confidently assumed to havelittle habitat potential for Biomphalaria. Indeed until late2008, intestinal schistosomiasis was not considered to be alocal threat to either NICS animals or to its staff welfare[24].

First detection of infected snails and afflictedchimpanzeesA key factor determining local transmission of S. mansoniis the presence of Biomphalaria, of which two species ofsnail in Lake Victoria were formally recognized, Biom-phalaria sudanica and Biomphalaria choanomphala [27].This appraisal has been deemed inaccurate for recentgenetic characterization and morphological studies havenow revealed that the distinctions between these two‘species’ were due to ecophenotypy of a single entity. B.choanomphala var. sudanica is an ecomorph of marshyhabitats fringing the lake, whereas B. choanomphala var.

choanomphala exists as an ecomorph in the lake proper.B. choanomphala var. choanomphala was typicallyconsidered to be abundant on submerged vegetation insheltered bay areas and not thought to be found on waveexposed shorelines and upon rocky substrates [28].

As part of a lake-wide malacological appraisal of Biom-phalaria, snail surveys penetrating into the offshoreislands of the lake took place which afforded an initialinspection of Ngamba and Kimi Islands in 2008 [22,25].This revealed the presence of B. choanomphala as well asseveral snails shedding S. mansoni cercariae patentlyinfected. This key finding then alerted NICS to the possi-bility of local transmission of intestinal schistosomiasisand focused the attentions of the chief veterinarian to theprospect that the chimpanzees could be at risk of infection.Schistosomiasis had not previously been considered withinthe diagnostic repertoire of the annual health checks. Eventhough this initial snail collection site was not accessible tothe chimpanzees (i.e., it was adjacent to the staff camp andboat docking platform), it was thought prudent to admin-ister a prophylactic dosing of praziquantel (40 mg/kg) to allanimals within their feed. Indeed, administration of pra-ziquantel in such a manner has become an annual stan-dard policy within the NICS’s disease management plan.To confirm if the animals were infected, a later detailedparasitological inspection of the animals and staff was

Box 1. Ngamba and Kimi Islands and their histories

Ngamba Island is 25 km southeast from Entebbe, accessible only

by boat, and is approximately 40 000 m2 in area, with second

generation rainforest covering the majority of the island. The island

very clearly differs from its neighbor Kimi Island, the latter hosts a

busy fish landing site with an associated itinerant fishing community

which lives in marginalized and very impoverished conditions

(Figure I).

After purchasing a long-term lease, the Ngamba Island Chimpanzee

Sanctuary (NICS) was established in October 1998 to act as a

conservation zone for the maintenance and care of orphaned and

rescued chimpanzees that are unlikely to survive reintroduction to the

wild. With 44 resident chimpanzees (http://ngambaisland.com/

chimps/chimps.html), NICS is currently working almost at full

carrying capacity. Although animals are semi-captive and return each

evening to sleeping quarters, they spend most of their day foraging

and roaming around the island. The wildlife conservation work of

NICS was featured by Mark Carwardine and Stephen Fry in the BBC

program ‘Last Chance to See’.

NICS is managed by the Chimpanzee Sanctuary and Wildlife

Conservation Trust (CSWCT) and acts in partnership with six other

organizations, inclusive of The Jane Goodall Institute. The Sanctuary

is also an active member of the Pan-African Sanctuary Alliance

(PASA) (http://pasaprimates.org/) and strongly advocates conserva-

tion of chimpanzee habitats in Uganda through community education

and political lobbying.

On Ngamba Island, there is a full-time veterinarian, with several

animal keepers, and a well-equipped veterinary laboratory. This

affords ad hoc and routine animal health checks, inclusive of more

advanced procedures (e.g., X-ray and surgery). The facility also acts

as a convenient base for medical outreach projects undertaken on

nearby islands such as on Kimi and Koome Islands in which NICS staff

actively contribute.


XX

(a) (b)

Figure I. Aerial images of the islands of (a) Ngamba and (b) Kimi very clearly showing differences in human habitation and forestation. The red cross denotes the same

island from different viewpoints.


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therefore planned, alongside a more intensive malacologi-cal inspection in an attempt to estimate the risk of infectionat key points along the NICS shoreline.

In February and March 2010, the detailed parasitologi-cal inspection took place using a variety of stool, urine andserological testing methods, inclusive of PCR detection ofschistosome DNA in stool as commonly used in routinemedical diagnosis of this disease in The Netherlands [24].A total of 39 chimpanzees and 37 CSWCT staff wereexamined for S. mansoni using both egg detection methodsand schistosome urine antigen rapid diagnostic tests basedupon circulating cathodic antigen (CCA). In addition, re-covered schistosome eggs and (or) hatched miracidia wereexamined by DNA barcoding to establish putative epide-miological crossover between humans and chimpanzees.All diagnostic methods conclusively inferred the presenceof intestinal schistosomiasis in the chimpanzees with anoverall seroprevalence of antibodies against schistosomesoluble egg antigen (SEA) by ELISA in excess of 90% [24].Three animals actively excreting schistosome eggs wereidentified and DNA barcoding analysis of miracidiahatched from chimpanzee stools revealed the presence of

three DNA barcodes commonly found in people living onthe Lake Victoria shoreline, inclusive of NICS staff, as wellas two novel DNA types at that time of schistosome sam-pling [24,26,29,30].

Although it was clear that the chimpanzees wereinfected with S. mansoni, the ability of chimpanzees tovoid schistosome eggs capable of hatching into viablemiracidia firmly suggested that these animals were capa-ble of currently maintaining a local, presumably zoonotictransmission of schistosomiasis independently of humansoutside an originally assumed anthropozoonotic cycle [24].This possibility was further enforced when the island’sperimeter was surveyed for Biomphalaria at four key sitesand not only revealed the presence of large numbers of B.choanomphala var. choanomphala, even on the wave ex-posed shoreline, but also that up to 75% of snails werecarrying pre-patent schistosome infections as ascertainedby detection of S. mansoni DNA in PCR assays (Figure 2).During these surveys the malacological collection teamwas also ambushed by chimpanzees on the water margins,although without incident, showing that the chimpanzeesregularly patrolled this shoreline along well-beaten

10 11

Chimpanzees have access to

Campsite

Number of snails

2008

(a)

(b) (c)

2010

% Uninfected % Infectedsnails

5

15

1110

9 7 5 5

59

snails

sites NG03, NG18 and NG11.

Staff water contact constrained to NG01.


Figure 2. Biomphalaria on Ngamba Island. (a) Outline map of Ngamba Island depicting four snail collecting sites in February 2010 where sampled Biomphalaria were

screened for schistosome DNA by PCR. The associated pie charts represent the prevalence of pre-patent infections at each of the four sites; snails were sampled twice (in

2008 and 2010) at the lakeshore site adjacent to the camp. (b) Photograph of wave action and large pebble substrate on the exposed shoreline on a calm day, on other days

the wave height can be upto 1 m with boat landing impossible. (c) Biomphalaria (indicated with black arrow) found clinging to the underside of a large pebble which was

taken from the background agglomeration of rocks.


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foraging tracks often in daily survey of their island terri-tory (Figure 3a).

The PCR screening of snails for schistosome DNAvery clearly revealed that snail populations were beingexposed to miracidia that could have only come fromtwo possible sources in this part of the forested areashoreline: (i) the chimpanzees themselves as they defecat-ed near or directly into the lake while exploring theselake margins; or (ii) from local fishermen who hadencroached within the 200 m no-fishing zone, presumablyat night, having used human fecal material to attract fishor had relieved themselves on dry land while the chim-panzees were in their sleeping pens. Given that chimpan-zees are normally fearful and timid of entering water, thesecond alternative was given greater credence until NICSstaff began to follow and directly observe chimpanzees onthe islands margins. It was then observed that certainanimals regularly entered the water and in so doingprobably acquired and spread their schistosome infections(Figure 3b).

Further environmental sampling and appraisalsThis initial malacological appraisal was further enforcedin June 2010, upon a more detailed microscale perimetersearch of 20 lakeshore sites, each separated by approxi-mately 75 m and noted by GPS [30]. Several other popula-tions of B. choanomphala var. choanomphala at otherlocations along the shoreline were found, including somehabitats which had hitherto been considered too wave-exposed for the presence of this snail, inclusive of otherfreshwater molluscan genera (Figure 2b) [30]. Intriguing-ly, it would appear that Biomphalaria has adapted itsbehavior to these wave-exposed shorelines by clinging tothe underside of large pebbles and small boulders, andupon more turbulent days probably penetrates even dee-per into this honeycomb structure made by these rocky

agglomerations, affording them both protection and ref-uge from the detrimental effects of wave action.

Subsequent examination of snails collected during thisand further surveys have revealed infected snails at sitesaccessible to chimpanzees. Most unexpectedly, one infectedsnail was also found to be coinfected with Schistosomarodhaini, a rodent schistosome previously found in theKenyan sector of the lake, although this Ngamba Islandpopulation was judged genetically distinctive [29]. Thisunique finding also alerts NICS researchers to the poten-tial for this schistosome to perhaps also establish withinthe chimpanzee population but has yet not been encoun-tered.

Ongoing disease surveillanceAs it stands, despite prophylactic treatments with prazi-quantel, the infection status of chimpanzees on NICSremains of concern, mainly in part due to the putativetreatment failure in several animals when given prazi-quantel tablets in their food and based upon the results ofthe parasitological surveys in the summer of 2010 [31].Together with additional surveys in March 2011, a body ofnew evidence relating to the pathological effects of long-term natural S. mansoni infection is now being gathered,courtesy of the excellent veterinary expertise and facilitieson NICS and continuing collaborations with local VectorControl Division, Ministry of Health teams as part of theactivities within the Ugandan National Control Programfor Bilharzia (Figure 1d).

As far as the authors are aware, prior to these observa-tions, no recent information was available as to the clinicalmanifestations of naturally acquired intestinal schistoso-miasis within chimpanzees [4]. Thus in March 2011, a pilotassessment of schistosome-associated morbidity was initi-ated by a team of multidisciplinary researchers by imple-menting portable ultrasonography during the annual


(a) (b)

Figure 3. Chimpanzees at the water margins of Ngamba Island. (a) Chimpanzee observed at the lakeshore after ambushing the malacological team, subsequently guarding

the metal snail scoop as a trophy that we dropped and left behind. (b) Direct water contact of chimpanzees exploring the immediate lakeshore where Biomphalaria were

also found in the submerged vegetation beds. (Inset) chimpanzee caught wading in deeper water between two lakeshore entry points.


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‘knock-down’ health check [31]. At these times animalswere lightly anesthetized for approximately 45 min andsubjected to a full veterinary investigation inclusive ofultrasound imagery and rectal snip biopsy. The findingswere particularly startling, for it was clearly shown thatseveral animals which had had a chronic history of infec-tion, were also shown to have very clear signs of liverfibrosis upon ultrasonography consistent with image pat-tern D of advanced pipestem fibrosis as classified uponconsideration of the World Health Organization (WHO)Niamey grading system (Figure 1d, insets) and calcifiedeggs were also found upon biopsies [32]. To increase theputative efficacy of praziquantel dosing, during anesthesiaanimals also received a stepped-up oral treatment at60 mg/kg dosing as delivered by a gastric tube and thiswas well-tolerated [31]. However, the performance of thisdosing and levels of putative reinfection(s) is scheduled tobe assessed in June 2012 using noninvasive parasitologicalsampling.

Can schistosomes be stopped from monkeying-around?In terms of general animal welfare on NICS, schistosomi-asis needs to be actively controlled and hopefully elimi-nated but there are several local considerations that needto be kept in mind both from short- and long-term per-spectives. First of all, general reductions in putativeanthropozoonotic potential are clearly needed, includingincreased annual coverage of preventive chemotherapy inNICS staff and in neighboring fishing communities. Thisshould help to dampen levels of schistosome egg excretioninto the environment, especially upon those occasionswhen infected people frequent the NICS margins poten-tially contaminating its shoreline. As might be expected,to more rigorously enforce the no-fishing zone and stop allencroachment of fishermen onto the island is probablyunobtainable. Moreover, a heavier handed policy mighteven become counterproductive by alienating the localhuman populace to the objectives of the NICS. Thus, toensure that a positive relationship continues, CSWCT isdeveloping strategic initiatives to promote both healthand community welfare activities within nearby fishingcommunities whilst educating the recipients to the goalsand motives of NICS (Box 1).

Further activities, specifically undertaken on NICS it-self, should involve an integrated approach requiring con-sideration of three principal factors, notwithstanding thesubtleties in adapting these to chimpanzee- and human-specific settings: (i) good sanitation, handling and disposalof all fecal waste to reduce environmental contaminationwhenever possible; (ii) disease monitoring and active treat-ment of infected individuals; and (iii) control of watercontact and aquatic exposure alongside some environmen-tal management of local populations of Biomphalaria. Ofthe above options, water supply and sanitation controlwithin the human populace on NICS is already excellentbut in the parts of the island where chimpanzees roamfreely, measures to contain their fecal input are impracti-cal due to indiscriminant defecation of these animals. Moreeffective disease surveillance is obvious but is hampered bythe need for mobilization of additional funds to synergizewith the annual health checks, which are already costly.

Better access to praziquantel with more effective adminis-tration is immediately beneficial but it would appear thatfor certain chimpanzees the dosing of 40 mg/kg in food hasbeen insufficient for cessation of egg excretion. Althoughstepped-up supervised dosing at 60 mg/kg, as delivered bya gastric tube, has been attempted it is not yet clear howeffective this has been in the short or long term and thusfurther parasitological surveillance is clearly warranted.

Of the remaining alternatives, control of snail popula-tions with chemical molluscicides, although possible, willprobably not be cost-effective in this lacustrine setting andon a shoreline which shelves steeply along with a honey-comb substrate where chemicals would probably fail to mixand penetrate. Moreover, the application of chemical con-trol agents strongly conflicts with the strict conservationethos of the sanctuary. Thus, among all alternatives,options to reduce water contact of the chimpanzees shouldbe preferentially explored. This could be done by reducingaccess in the more risky areas of the shoreline by furtherfencing off parts of this shoreline but in the short term thiswill be expensive to set up and in the long term verydifficult to maintain. It must be remembered that chim-panzees, which are particularly intelligent and resourcefulcreatures, often interfere with and potentially destroy suchfencing measures as part of their territorial enforcementand routine daily patrolling.

Concluding remarksDespite being set in a unique and carefully controlledenvironment, the situation on NICS serves as a potentexample for the opportunity for anthropozoonotic trans-mission of intestinal schistosomiasis and the pervasive-ness of risk-of-infection along a local shoreline in light of aputative zoonotic cycle. Veterinarians and conservationmanagers should be made more aware of the occurrenceof schistosomiasis, especially when wildlife is to be main-tained in ex situ settings and natural aquatic boundariesare utilized. Future disease management plans on NICSshould recognize the difficulties of care of presentlyinfected animals and maintaining long-term individualwelfare (i.e., optimization of praziquantel treatments),alongside putting in place locally appropriate measuresto mitigate other contaminating and (or) exposure enhanc-ing behaviors. Obviously, the latter is more easily targetedto the human populace rather than the chimpanzee popu-lation. Looking to the future, reducing or eventually stop-ping schistosomiasis transmission on NICS will require aconcerted long-term multidisciplinary effort in which care-ful parasitological and malacological surveillance is veryclearly needed.

AcknowledgmentsWe very warmly thank the hospitality of the CSWCT, in particular to theDirector – Lilly Ajarova – and her staff for collaboration and support;similarly to many friends and colleagues at Vector Control Division,especially Narcis Kabatereine, who have assisted with fieldwork andlogistics on Ngamba, and also to several staff at the Natural HistoryMuseum – David Rollinson – where this work originally started. Specialthanks go to Andrew ‘Fiddi’ Rugianna for all his help in snail collecting onNICS and for his extra special alertness in detecting ambushingchimpanzees. We are grateful to the support of the Uganda WildlifeAuthority (UWA) and to Dr Chris van Tulleken and other volunteerson Ngamba Island who have contributed to past endeavors. This work


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has benefited from umbrella financial support from EU-CONTRAST(J.R.S./L.M.), a Natural History Museum PhD studentship (C.J.S.) andThe Wellcome Trust–Schistosomiasis in Mothers and Infants (SIMI)project (J.R.S.).

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