parasitological examination of common hippopotamus ... · the common hippopotamus (hippopotamus...

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Wiener Tierärztliche Monatsschrift – Veterinary Medicine Austria 101 (2014)

From the Research Institute of Wildlife Ecology, Department of Integrative Biology and Evolution, University of Veterinary Medicine Vienna, Austria

Parasitological examination of common hippopotamus (Hippopotamus amphibius) faeces in the Gamba Complex of Protected Area in Gabon

S. RIETMANN* and C. WALZER

received August 5, 2013accepted November 12, 2013

Schlüsselwörter: Hippopotamus amphibius, Parasiten, Kotproben, Gabun.

Zusammenfassung

Parasitologische Untersuchung von Flusspferdekot (Hippopota-mus amphibius) in Gabun

EinleitungDie Gefährdung von Wildtierpo-

pulationen auf Grund von Krank-heitsgeschehen stellt eine wach-sende und ernstzunehmende Bedrohung dar. Wissenschaftlich fundierte Kenntnisse über Krank-heiten, Krankheitserreger sowie Krankheitsverläufe und daraus fol-gende Konsequenzen fungieren als nötige Grundlagen im Rahmen eines evidenzbasierenden Ent-scheidungsprozesses für nachhal-tiges Arten-Management. Diese Studie befasst sich mit der Unter-suchung gastrointestinaler Parasi-ten von Flusspferden (Hippopota-mus amphibius) und evaluiert die Nutzung der angewandten Metho-de als Basis zur Überwachung pa-rasitärer Geschehen in freileben-den Flusspferdpopulationen.

Material und MethodeDas Untersuchungsgebiet dieser

Studie war der Gamba-Komplex im Südwesten Gabuns in Zentralafrika. Er erstreckt sich über eine Fläche von 11.320 km2 und besteht aus ei-nem Gefüge aus Schutzgebieten mit einem weitläu� gen Wassersys-tem. Zwischen dem 14. Juni und dem

1. Oktober 2011 wurden an 46 Tagen 77 Kotproben von Flusspferden ge-sammelt. Die Proben wurden in eine Lösung aus 15 g Natriumacetat, 20 ml Eisessig, 40 ml Formalin (37 %) und 925 ml Leitungswasser � xiert. Jede Probe wurde gesondert mittels Se-dimentation (nach der modi� zierten Methode von Benedek) und Flota-tion (nach der McMaster Methode) untersucht.

Ergebnisse In 70 der 77 Proben wurden Pa-

rasiten gefunden. 61 Proben wa-ren positiv für Eier von Fasciola spp. und in 42 Proben wurde Ei-meria gefunden. Vier Proben wa-ren positiv für Larven von Stron-gyliden, eine Probe beinhaltete ein deformiertes Strongyliden-Ei.

SchlussfolgerungenDas Fixieren von Kotproben in

einer Lösung aus Formalin, Natri-umacetat und Eisessig ermöglicht eine zuverlässige Evaluierung von Parasiten. Die Ergebnisse weisen auf eine geringe parasitäre Vielfalt und eine geringe Belastung der Flusspferde im Gamba-Komplex hin. Die verwendete Methode lie-fert zuverlässige Daten über pa-rasitäre Geschehen in freileben-den Flusspferden. Ein Vergleich mit anderen Methoden bezüglich Sensitivität und Spezi� tät sollte in Betracht gezogen werden.

Keywors: Hippopotamus amphi-bius; parasite, faeces, Gabon.

Summary

Effective conservation ofspecies requires scientificevidence upon which to basedecisions. Health threats to wild-life must be considered whendevising conservation strategies. Reference data on diseases, their spread and their consequences for both hosts and people are key factors in the sustainablemanagement of wildlife species. In this study we investigated the possibility of extracting parasites and assessing parasite type from faeces of the common hippo-potamus (Hippopotamus am-phibius) from the central African country of Gabon. Faecal samp-les were collected in the � eld, � xed in a formalin solution and analysed using � otation and sedi-mentation methods. We found parasites in 70 out of 77 samples; mainly comprising the generaEimeria and Fasciola. The study suggests that our methods are suitable for screening faecalparasites of free-ranging hippo-potamuses.

Abbreviations: CITES = Convention on International Trade in Endangered Species; GCPA = Gamba Complex of Protected Areas; IUCN = International Union for Conservation of Nature; WWF = World Wildlife Fund

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IntroductionThe common hippopotamus (Hippopotamus

amphibius L.) was once widespread across sub-Saharan Africa. In the past, it occurred along the length of the Nile River all the way to the delta and in South Africa to the Cape. The common hippo-potamus was extirpated from many of these areas in historic times (KINGDON, 1997). The species isbelieved to have experienced an overall decline of 7–20% between 1998 and 2008 (LEWISON andOLIVER, 2008). As a result, it was � rst listed on the IUCN Red list in 2006 (IUCN, 2006). Major threats for the hippopotamus are habitat loss, habitat fragmen-tation and poaching (ELTRINGHAM, 1999; LEWISON and OLIVER, 2008; KLINGEL, 2013).

Today, hippopotamuses still range over much of sub-Saharan Africa: in the west from Senegal and Gambia and in the east from Sudan, Ethiopia and Somalia as far south as the Okavango River delta in Botswana, the Kunene River in Namibia andKwaZulu Natal in South Africa. The estimated total population is in the order of 125,000–148,000 indivi-duals (LEWISON and OLIVER, 2008). The common hippopotamus is still categorized as ‘vulnerable’ on the IUCN Red List (2013). It is also listed in Appendix II of the Convention on International Trade in En-dangered Species (CITES) of Wild Fauna and Flora due to concerns about the appearance of hippo-potamus ivory in international trade (CITES, 2013).

Parasites from free-ranging hippopotamuses were � rst reported during the beginning of the 20th cen-tury (see Tab. 1). Most samples were collected fol-lowing culling operations undertaken to control po-pulation numbers in Eastern Africa. An overview of the parasites found to date in the common hippo-potamus is shown in Table 1. Records are noticeab-ly absent from many areas in which hippopotamuses occur, including West Africa.

The aims of this study were threefold: I) to assess the feasibility of parasitological screening of free ranging hippopotamuses; II) to assess methods for extracting parasites from faeces and � xing them in a solution of formalin; and III) to identify diversity of parasite species in the faeces of hippopotamuses living in the Gamba complex.

Material and Methods

Study Area

The territory of Gabon is largely (80%) covered by forest. Consequently, the spatial distribution of the hippopotamus in Gabon is restricted (MAYAUX et al., 2004). The IUCN estimates the species to number around 250 individuals in Gabon (IUCN, 2013),although robust information on population sizeand distribution is lacking (WWF, 2006). The

hippopotamus is fully protected throughout the country under Gabonese law (Law N° 1/82 of July 22nd 1982). Nevertheless, numbers seem to be de-clining and poaching for meat and tusks is today thought to constitute the biggest threat for this spe-cies in Gabon (WHITE et al., 1983; CHRISTY et al., 2008).

The Gamba Complex of Protected Areas (GCPA) is reported to contain the highest density of common hippopotamuses in Gabon (DALLMEIER et al., 2006). The GCPA is situated in south-western Gabon atlatitude 1°50’-3°10’S and longitude 9°15’-10°50’E (see Maps 1 and 2). The GCPA includes two of the thirteen national parks of Gabon, Moukalaba-Doudou (4,500 km2) and Loango (1,550 km2), and an intervening corridor (3,585 km2). Wildlife in the GCPA is afforded some degree of protection by law.Hunting regulations are well de� ned inside national parks. The area has a very high biodiversity and an extremely low human population density (<1 person per km2) (TREBAOL and CHAILLOL, 2002; ALONSO et al., 2006). The GCPA comprises a mosaic of very diverse habitat types that span altitudes at sea level along the 200 km long pristine coast, up to about820 m a.s.l. on Mount Doudou. The equatorial climate is hot and humid (up to 85 % relative humidity)(LEMOALLE and ALBARET, 1995). The hydrologic landscapes in which hippopotamuses occur aredivided into three large basins. Together with anadditional network of rivers, these form a complex water network with wide permanently submerged woods and mangrove forests.

Parasitological examination

Fieldwork to sample hippopotamus faeces was carried out over 46 days between June 14th andOctober 1st 2011. Depending on accessibility and ter-rain, surveys were performed by motorized boat, quad, kayak or by foot. In total, surveys covered 1,500 km in distance across 12 different regions of the GBPA. By changing the tracks left by hippo-potami after every sampling we tried to avoidcollecting faeces from the same individual twice. The ages of faeces was estimated by local guides based on humidity, colour, smell and the impression of tracks next to it. We often found tracks and faeces in locations that had been sampled the previous day, and this increased con� dence in the estimates of the age of hippopotami faeces, which were classi� ed as fresh faeces deposited the previous night <24 h prior to collection; and old faeces deposited >48 hearlier. Each faecal sample collected took different parts from the scat and sought to avoid contamina-tion by sampling from parts of the scat that had the least contact with the surrounding soil.

A total of 77 faecal samples were collected. Six of these were taken from old scats, seven were taken from scat assessed as being between 24 and 48 hours

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Tab. 1: List of parasites of hippopotamuses described in the literature

Phylum Plathelminthes

Echinostomatidae Ogmocotyle spp. MCCULLY et al., 1967

Fasciolidae Fasciola nyanzae e.g. LEIPER, 1910; JACKSON, 1921

Paramphistomidae Paramphistomum spp.

Nilocotyle spp.

Gigantocotyle spp.

Carmyerius cruciformis

Gigantatrium gigantoatrium

Glyptamphistoma paradoxum

Gastrothylax cruciformis

Platyamphistoma polycladiformae

Buxifrons spp.

Ugandocotyle spp.

e.g. LEIPER, 1910; NÄSMARK, 1937

e.g. SWART, 1961; SEY and GRABNER, 1980

MCCULLY et al., 1967

e.g.LEIPER, 1910; SEY and GRABER, 1979

NÄSMARK, 1937; CANARIS and GARDNER, 2003

SEY and GRABER, 1979; CANARIS and GARDNER, 2003

CANARIS and GARDNER, 2003

NÄSMARK,1937; CANARIS and GARDNER, 2003

NÄSMARK, 1937; SEY and GRABER, 1979; CANARIS and GARDNER, 2003

e.g. SEY and GRABER, 1979; CANARIS and GARDNER, 2003

Schistosomatidae Schistosoma spp. e.g. THURSTON, 1964; MORGAN et al., 2003

Anoplocephalidae Moniezia amphibian LINSTOW, 1910; CANARIS and GARDNER, 2003

Taeniidae Echinococcus granulosus africanus MCCULLY et al,. 1967

Polystomatidae Oculotrema hippopotami STUNKARD, 1924; THURSTON, 1968a,b; DU PREEZ and MOENG, 2004

Phylum Nematoda

Trichostrongylidae Leiperiatus hopkeni

Nematodirus hopkeni

LEIPER, 1910; CANARIS and GARDNER, 2003

LEIPER, 1910

Filariidae Filaria hippopotami LEIPER, 1910

Atracitidae Cobboldina spp. e.g. OGDEN, 1967; MONDAL and MANNA, 2012

Ascarididae Ascaris hippopotami e.g. CANAVAN, 1929; MAUNG, 1975

Onchocercidae Dipetalonema hippopotami MCCULLY et al., 1967; CANARIS and GARDNER, 2003

Syngamidae Mammomonogamus hippopotami GEDOELST, 1924; CANARIS and GARDNER, 2003

Phylum: Apicomplexa

Eimeria COWAN et al., 1967; KUTTING et al., 1982a,b

Phylum Arthropoda

Amblyommidae Amblyomma tholloni Rhipicephalus S. simus

GUILBRIDE et al., 1962

Phylum Annelida

Hirudinidae Limnatis nilotica

Placobdelloides jaegerskioeldi

GUILBRIDE et al., 1962

OOSTHUIZEN and DAVIES, 1994

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Map.2: The Gamba Complex of protected area in Gabon

Map 1: Location of Gabon

old and 64 came from fresh faeces. The samples were � xed usinga solution of 15 g sodium acetate in 20 ml acetic acid, 40 ml for-malin (37%) and 925 ml tapwater to enable subsequentanalysis (UTZINGER et al., 2010), an established � xation protocol that is used widely across thetropics (e.g. MARTIN and ESCHER, 1990). About 10–15 g of faecal material from each sample was placed in 30 ml of the diluted � xative.

The samples were screened six months after collection. Each sample was analysed separately using � otation as well as sedi-mentation methods to extract the different parasitic stages. To eva-luate larvae and protozoa using a simple � otation method and the standard McMaster method (GORDON andWHITLOCK, 1939; WHITLOCK, 1948), the homo-genized suspension of drained faeces and waterwas enriched with a sucrose solution (density of1.28 g/cm3) and the sample was centrifuged at 690xg for 8 min. Droplets from the surface were screened by means of a microscope at a magni� cation of up to 400 x. Sedimentation was performed using the modi� ed method of Benedek (BENEDEK, 1943;BORAY and PEARSON, 1960). The suspension was � rst sifted through a sieve to remove plant particles. In a second step, the residue in the sieve of32 meshes/cm was washed out with water to extract as much of the smaller particles as possible. Theresulting solution was allowed to sediment for 3 min before being decanted and the sediment was screened for larvae and eggs under a microscope at a magni� cation of 25 x to 40 x.

Results

The recovered larvae and eggs showed a generally good state of preservation. We found parasites in 70 out of the 77 samplescollected. Sixty-one samples were positive for Fasciola spp. (see Fig. 1), 42 were positive for Eimeria and four contained larvae of Strongyloides, one of which belonged to the genus Dictyo-caulus. To the best of the authors’ knowledge, no representative of the genus Dictyocaulus haspreviously been described as a

parasite infesting hippopotamuses. One sample contained a deformed egg that presumably belongs to a nematode, the taxonomy of a larva in another sample could not be determined due to damaged structures, one oocyst from Isospora was found and in 13 of the samples eggs of mites (Acarina) were identi� ed (see Tab. 2a and 2b).

Discussion

This study demonstrates the feasibility of deter-mining the prevalence and diversity of parasitescollected in the wild from common hippopotamuses. The results of the present and previous studies(Tab. 1) show that the common hippopotamus is host to various species of parasite. Nevertheless,

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evidence of disease due to parasitism in thehippopotamus is rare (GUILBRIDE et al., 1962;ELTRINGHAM, 1999; MILLER, 2003). Some of the parasites, including Fasciola nyanzae, Oculotrema hippopotami, Schistosoma hippopotami, Schisto-soma edwardiense and the leech Placobdelloides jaegerskioeldi, are thought to be speci� c to hippo-potamuses (DINNIK and DINNIK, 1961; THURSTON and LAWS, 1965; OOSTHUIZEN and DAVIS, 1994; MORGAN et al., 2003). Previously, only three studies had assessed parasites from dropped faeces of free-ranging hippopotamuses, one of which was un-successful in extracting parasites from ‘fresh hippo-potamus dung samples’ (MORGAN et al., 2003). The other two studies showed a relatively low prevalence of parasites: seven out of 30 samples and seven out of 38 samples, respectively (DINNIK and DINNIK, 1961; PITCHFORD and VISSER, 1981). Samples were only � xed in formalin before examination in thesecond study. The present research shows a suc-cessful approach for extracting parasites from drop-ped faeces. A standard formalin-based solution suc-cessfully fixed parasites from common hippo-potamuses in high ambient temperatures and humi-dity and allowed a diagnostically conclusive analysis six months after sampling.

Parasitism with Fasciola seems to be fairly com-mon in wild hippopotamuses (e.g. LEIPER, 1910; JACKSON, 1921; MCCULLY et al., 1967). An infesta-tion with Eimeria has previously been described in only two individual animals (COWAN et al., 1967; KUTTING et al., 1982b).

Compared with previous studies, few species of parasites were found in Gabon. These comprised Fasciola, Eimeria and in � ve cases Nematode spp.

Furthermore, the parasitic load was very low. In the samples positive for Nematode spp. three samples contained fewer than ten eggs and one sample con-tained only a single larva. The food mites found in six different samples were most probably ingested orally and passed through the gastrointestinal system wit-hout negative impact. The low parasitic loads might be linked to the low density of the hippopotamus po-pulation in the GCPA region (personal observation).

The apparent low parasite diversity and load could also be due to the method used in this study, sug-gesting the need to consider further methodological testing. To the best of the authors’ knowledge this is the � rst study of the parasites of the common hippo-potamus from the region: previous studies have been con� ned to Eastern or Southern Africa. A range-wide comparison of parasite prevalence and diversity seems necessary to address the problem of parasi-tism in wild hippopotamuses.

Tab. 2a: Prevalence of parasites found using sedimentation methods in faecal samples from common hippopotamuses collected inGabon in 2011

Sedimentation

age of Sample Results Sample Nr. ∑ %

24 h < Fasciola spp.3, 6-14,16-22, 26-28,30-44, 46, 47, 52, 54, 59, 61, 63, 68, 69, 73-77

49 63.6

24 h < negative 45, 50, 51, 53, 55-60, 62, 64-66, 70 15 19.5

24 h - 48 h Fasciola spp. 23-25, 71,72, 29 6 7.8

24 h - 48 h negative 67 1 1.3

> 48 h Fasciola spp. 1,2, 15, 48 4 5.1

> 48 h negative 4, 5 2 2.6

Total 77 100

Total positive 59 76.6

Total negative 18 23.4

Fig. 1: Extracted Fasciola egg from faeces of the common hip-popotamus

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Conclusion

The study demonstrated the feasibility of perfor-ming a parasitological screening of free ranging common hippopotamuses through the analysis of recovered faecal samples. The � xation of faeces in a solution of formalin, sodium acetate, acetic acid and tap water allowed the extraction of parasites in diffe-rent stages of development for six months after sam-ple collection. The � ndings suggest a low parasitic load and diversity in the common hippopotamus in the Gamba Complex of Protected Areas in Gabon, possibly due to the species’ low population density there.

The speci� city and sensitivity of the method would bene� t from further validation. Nevertheless, it can be used for a reliable parasitical screening of free-ranging common hippopotamuses.

Further research is needed to investigate which species of Eimeria are present in hippopotamuses. Little is known about this parasite and its possible

impact, although the prevalence found in the hippo-potamuses in our sampling area was remarkable. The intriguing � nding of a Dictyocaulus larva in one sample also suggests that there are still undescribed parasites in the common hippopotamus.

AcknowledgementThis research was partially funded by the WWF.Without the permissions from the CENAREST(National Centre of Scienti� c Research of Gabon), the ANPN (National Agency for National Parks ofGabon), the senior warden of the national parks and the support in the � eld from WWF Gabon and the local staff, this survey could not have been done. Many thanks to the Institute of Parasitology of the University of Veterinary Medicine Vienna for perfor-ming the examination of the faecal samples, and to Dr. P.K. Robbins and Dr. N. Leader-Williams for anumber of comments and suggestions.

Tab. 2b: Prevalence of parasites found using sedimentation methods in faecal samples from common hippopotamuses collected inGabon in 2011

Flotation

age of Sample Results Sample Nr. ∑ %

24 h < Eimeria spp.17-22, 26-28, 31-37, 40-42, 45, 47, 50, 54-56, 58-63, 66, 68, 74-77

37 48.1

24 h < deformed larva 10 1 1,3

24 h < larvae from Strogyloides 12 1 1,3

24 h <Eimeria spp.; deformed egg (presumably Strogyloides)

73 1 1,3

24 h < negative3, 6-9, 11, 13,14, 16, 30, 38,39, 43,44, 46, 49, 51-53, 57, 64,65, 69, 70

24 31.2

24 h - 48 h Eimeria spp. 23, 25, 29 3 3,9

24 h - 48 h negative 24, 67, 71,72 4 5.1

> 48 h larvae from Strogyloides 5, 15 2 2.6

> 48 hlarvae from Strongyloides (Dictyocaulus)

4 1 1,3

> 48 h Eimeria spp. 48 1 1,3

> 48 h negative 1,2 2 2.6

Total 77 100

Total positive 47 61

Total negative 30 39

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*Coresponding author’s address: Sylvie Rietmann, Research Institute of Wildlife Ecology,Savoyenstraße 1, 1160 Vienna, Austria e-mail: [email protected]

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