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, 2013 accepted November 12, 2013
Keywors: Hippopotamus amphi- Schlüsselwörter: Hippopotamus bius; parasite, faeces, Gabon. amphibius, Parasiten, Kotproben, Gabun.
Summary Zusammenfassung 1. Oktober 2011 wurden an 46 Tagen 77 Kotproben von Flusspferden ge- Effective conservation of Parasitologische Untersuchung sammelt. Die Proben wurden in eine species requires scientific von Flusspferdekot (Hippopota- Lösung aus 15 g Natriumacetat, 20 ml evidence upon which to base mus amphibius) in Gabun Eisessig, 40 ml Formalin (37 %) und decisions. Health threats to wild- 925 ml Leitungswasser xiert. Jede life must be considered when Einleitung Probe wurde gesondert mittels Se- devising conservation strategies. Die Gefährdung von Wildtierpo- dimentation (nach der modi zierten Reference data on diseases, their pulationen auf Grund von Krank- Methode von Benedek) und Flota- spread and their consequences heitsgeschehen stellt eine wach- tion (nach der McMaster Methode) for both hosts and people are key sende und ernstzunehmende untersucht. factors in the sustainable Bedrohung dar. Wissenschaftlich management of wildlife species. fundierte Kenntnisse über Krank- Ergebnisse In this study we investigated the heiten, Krankheitserreger sowie In 70 der 77 Proben wurden Pa- possibility of extracting parasites Krankheitsverläufe und daraus fol- rasiten gefunden. 61 Proben wa- and assessing parasite type from gende Konsequenzen fungieren ren positiv für Eier von Fasciola faeces of the common hippo- als nötige Grundlagen im Rahmen spp. und in 42 Proben wurde Ei- potamus (Hippopotamus am- eines evidenzbasierenden Ent- meria gefunden. Vier Proben wa- phibius) from the central African scheidungsprozesses für nachhal- ren positiv für Larven von Stron- country of Gabon. Faecal samp- tiges Arten-Management. Diese gyliden, eine Probe beinhaltete ein les were collected in the eld, Studie befasst sich mit der Unter- deformiertes Strongyliden-Ei. xed in a formalin solution and suchung gastrointestinaler Parasi- analysed using otation and sedi- ten von Flusspferden (Hippopota- Schlussfolgerungen mentation methods. We found mus amphibius) und evaluiert die Das Fixieren von Kotproben in parasites in 70 out of 77 samples; Nutzung der angewandten Metho- einer Lösung aus Formalin, Natri- mainly comprising the genera de als Basis zur Überwachung pa- umacetat und Eisessig ermöglicht Eimeria and Fasciola. The study rasitärer Geschehen in freileben- eine zuverlässige Evaluierung von suggests that our methods are den Flusspferdpopulationen. Parasiten. Die Ergebnisse weisen suitable for screening faecal auf eine geringe parasitäre Vielfalt parasites of free-ranging hippo- Material und Methode und eine geringe Belastung der potamuses. Das Untersuchungsgebiet dieser Flusspferde im Gamba-Komplex Studie war der Gamba-Komplex im hin. Die verwendete Methode lie- Südwesten Gabuns in Zentralafrika. fert zuverlässige Daten über pa- Abbreviations: CITES = Convention Er erstreckt sich über eine Fläche rasitäre Geschehen in freileben- on International Trade in Endangered von 11.320 km2 und besteht aus ei- den Flusspferden. Ein Vergleich Species; GCPA = Gamba Complex of nem Gefüge aus Schutzgebieten mit anderen Methoden bezüglich Protected Areas; IUCN = International mit einem weitläu gen Wassersys- Sensitivität und Spezi tät sollte in Union for Conservation of Nature; WWF = World Wildlife Fund tem. Zwischen dem 14. Juni und dem Betracht gezogen werden.
66 Wiener Tierärztliche Monatsschrift – Veterinary Medicine Austria 101 (2014)
Introduction hippopotamus is fully protected throughout the country under Gabonese law (Law N° 1/82 of July The common hippopotamus (Hippopotamus 22nd 1982). Nevertheless, numbers seem to be de- amphibius L.) was once widespread across sub- clining and poaching for meat and tusks is today Saharan Africa. In the past, it occurred along the thought to constitute the biggest threat for this spe- length of the Nile River all the way to the delta and in cies in Gabon (WHITE et al., 1983; CHRISTY et al., South Africa to the Cape. The common hippo- 2008). potamus was extirpated from many of these areas in The Gamba Complex of Protected Areas (GCPA) is historic times (KINGDON, 1997). The species is reported to contain the highest density of common believed to have experienced an overall decline of hippopotamuses in Gabon (DALLMEIER et al., 2006). 7–20% between 1998 and 2008 (LEWISON and The GCPA is situated in south-western Gabon at OLIVER, 2008). As a result, it was rst listed on the latitude 1°50’-3°10’S and longitude 9°15’-10°50’E IUCN Red list in 2006 (IUCN, 2006). Major threats for (see Maps 1 and 2). The GCPA includes two of the the hippopotamus are habitat loss, habitat fragmen- thirteen national parks of Gabon, Moukalaba- tation and poaching (ELTRINGHAM, 1999; LEWISON Doudou (4,500 km2) and Loango (1,550 km2), and an and OLIVER, 2008; KLINGEL, 2013). intervening corridor (3,585 km2). Wildlife in the GCPA Today, hippopotamuses still range over much of is afforded some degree of protection by law. sub-Saharan Africa: in the west from Senegal and Hunting regulations are well de ned inside national Gambia and in the east from Sudan, Ethiopia and parks. The area has a very high biodiversity and an Somalia as far south as the Okavango River delta in extremely low human population density (<1 person Botswana, the Kunene River in Namibia and per km2) (TREBAOL and CHAILLOL, 2002; ALONSO KwaZulu Natal in South Africa. The estimated total et al., 2006). The GCPA comprises a mosaic of very population is in the order of 125,000–148,000 indivi- diverse habitat types that span altitudes at sea level duals (LEWISON and OLIVER, 2008). The common along the 200 km long pristine coast, up to about hippopotamus is still categorized as ‘vulnerable’ on 820 m a.s.l. on Mount Doudou. The equatorial climate the IUCN Red List (2013). It is also listed in Appendix is hot and humid (up to 85 % relative humidity) II of the Convention on International Trade in En- (LEMOALLE and ALBARET, 1995). The hydrologic dangered Species (CITES) of Wild Fauna and Flora landscapes in which hippopotamuses occur are due to concerns about the appearance of hippo- divided into three large basins. Together with an potamus ivory in international trade (CITES, 2013). additional network of rivers, these form a complex Parasites from free-ranging hippopotamuses were water network with wide permanently submerged rst reported during the beginning of the 20th cen- woods and mangrove forests. tury (see Tab. 1). Most samples were collected fol- Parasitological examination lowing culling operations undertaken to control po- pulation numbers in Eastern Africa. An overview of Fieldwork to sample hippopotamus faeces was the parasites found to date in the common hippo- carried out over 46 days between June 14th and potamus is shown in Table 1. Records are noticeab- October 1st 2011. Depending on accessibility and ter- ly absent from many areas in which hippopotamuses rain, surveys were performed by motorized boat, occur, including West Africa. quad, kayak or by foot. In total, surveys covered The aims of this study were threefold: I) to assess 1,500 km in distance across 12 different regions of the feasibility of parasitological screening of free the GBPA. By changing the tracks left by hippo- ranging hippopotamuses; II) to assess methods for potami after every sampling we tried to avoid extracting parasites from faeces and xing them in a collecting faeces from the same individual twice. The solution of formalin; and III) to identify diversity of ages of faeces was estimated by local guides based parasite species in the faeces of hippopotamuses on humidity, colour, smell and the impression of living in the Gamba complex. tracks next to it. We often found tracks and faeces in locations that had been sampled the previous day, Material and Methods and this increased con dence in the estimates of the age of hippopotami faeces, which were classi ed as Study Area fresh faeces deposited the previous night <24 h prior to collection; and old faeces deposited >48 h The territory of Gabon is largely (80%) covered by earlier. Each faecal sample collected took different forest. Consequently, the spatial distribution of the parts from the scat and sought to avoid contamina- hippopotamus in Gabon is restricted (MAYAUX et al., tion by sampling from parts of the scat that had the 2004). The IUCN estimates the species to number least contact with the surrounding soil. around 250 individuals in Gabon (IUCN, 2013), A total of 77 faecal samples were collected. Six of although robust information on population size these were taken from old scats, seven were taken and distribution is lacking (WWF, 2006). The from scat assessed as being between 24 and 48 hours
67 Wiener Tierärztliche Monatsschrift – Veterinary Medicine Austria 101 (2014)
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. e.g. LEIPER, 1910; NÄSMARK, 1937
Nilocotyle spp. e.g. SWART, 1961; SEY and GRABNER, 1980
Gigantocotyle spp. MCCULLY et al., 1967
Carmyerius cruciformis e.g.LEIPER, 1910; SEY and GRABER, 1979
Gigantatrium gigantoatrium NÄSMARK, 1937; CANARIS and GARDNER, 2003
Glyptamphistoma paradoxum SEY and GRABER, 1979; CANARIS and GARDNER, 2003
Gastrothylax cruciformis CANARIS and GARDNER, 2003
Platyamphistoma polycladiformae NÄSMARK,1937; CANARIS and GARDNER, 2003
Buxifrons spp. NÄSMARK, 1937; SEY and GRABER, 1979; CANARIS and GARDNER, 2003
Ugandocotyle spp. 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 LEIPER, 1910; CANARIS and GARDNER, 2003
Nematodirus hopkeni 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 GUILBRIDE et al., 1962 Rhipicephalus S. simus
Phylum Annelida
Hirudinidae Limnatis nilotica GUILBRIDE et al., 1962
Placobdelloides jaegerskioeldi OOSTHUIZEN and DAVIES, 1994
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old and 64 came from fresh faeces. The samples were xed using a solution of 15 g sodium acetate in 20 ml acetic acid, 40 ml for- malin (37%) and 925 ml tap water to enable subsequent analysis (UTZINGER et al., 2010), an established xation protocol that is used widely across the tropics (e.g. MARTIN and ESCHER, 1990). About 10–15 g of faecal material from each sample was placed in 30 ml of the diluted x a t i v e . 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- Map 1: Location of Gabon luate larvae and protozoa using a simple otation method and the parasite infesting hippopotamuses. One sample standard McMaster method (GORDON and contained a deformed egg that presumably belongs WHITLOCK, 1939; WHITLOCK, 1948), the homo- to a nematode, the taxonomy of a larva in another genized suspension of drained faeces and water sample could not be determined due to damaged was enriched with a sucrose solution (density of structures, one oocyst from Isospora was found and 1.28 g/cm ) and the sample was centrifuged at 690xg in 13 of the samples eggs of mites (Acarina) were for 8 min. Droplets from the surface were screened identi ed (see Tab. 2a and 2b). by means of a microscope at a magni cation of up to 400 x. Sedimentation was performed using the Discussion modi ed method of Benedek (BENEDEK, 1943; BORAY and PEARSON, 1960). The suspension was This study demonstrates the feasibility of deter- rst sifted through a sieve to remove plant particles. mining the prevalence and diversity of parasites In a second step, the residue in the sieve of collected in the wild from common hippopotamuses. 32 meshes/cm was washed out with water to extract The results of the present and previous studies as much of the smaller particles as possible. The (Tab. 1) show that the common hippopotamus is host resulting solution was allowed to sediment for 3 min to various species of parasite. Nevertheless, 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 samples collected. 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 has previously been described as a Map.2: The Gamba Complex of protected area in Gabon
69 Wiener Tierärztliche Monatsschrift – Veterinary Medicine Austria 101 (2014)
Tab. 2a: Prevalence of parasites found using sedimentation methods in faecal samples from common hippopotamuses collected in Gabon in 2011 Sedimentation
age of Sample Results Sample Nr. ∑ %
3, 6-14,16-22, 26-28,30-44, 46, 47, 52, 54, 59, 61, 24 h < Fasciola spp. 49 63.6 63, 68, 69, 73-77
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 evidence of disease due to parasitism in the Furthermore, the parasitic load was very low. In the hippopotamus is rare (GUILBRIDE et al., 1962; samples positive for Nematode spp. three samples ELTRINGHAM, 1999; MILLER, 2003). Some of the contained fewer than ten eggs and one sample con- parasites, including Fasciola nyanzae, Oculotrema tained only a single larva. The food mites found in six hippopotami, Schistosoma hippopotami, Schisto- different samples were most probably ingested orally soma edwardiense and the leech Placobdelloides and passed through the gastrointestinal system wit- jaegerskioeldi, are thought to be speci c to hippo- hout negative impact. The low parasitic loads might potamuses (DINNIK and DINNIK, 1961; THURSTON be linked to the low density of the hippopotamus po- and LAWS, 1965; OOSTHUIZEN and DAVIS, 1994; pulation in the GCPA region (personal observation). MORGAN et al., 2003). Previously, only three studies The apparent low parasite diversity and load could had assessed parasites from dropped faeces of also be due to the method used in this study, sug- free-ranging hippopotamuses, one of which was un- gesting the need to consider further methodological successful in extracting parasites from ‘fresh hippo- testing. To the best of the authors’ knowledge this is potamus dung samples’ (MORGAN et al., 2003). The the rst study of the parasites of the common hippo- other two studies showed a relatively low prevalence potamus from the region: previous studies have been of parasites: seven out of 30 samples and seven out con ned to Eastern or Southern Africa. A range-wide of 38 samples, respectively (DINNIK and DINNIK, comparison of parasite prevalence and diversity 1961; PITCHFORD and VISSER, 1981). Samples were seems necessary to address the problem of parasi- only xed in formalin before examination in the tism in wild hippopotamuses. second 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 Fig. 1: Extracted Fasciola egg from faeces of the common hip- Fasciola, Eimeria and in ve cases Nematode spp. popotamus
70 Wiener Tierärztliche Monatsschrift – Veterinary Medicine Austria 101 (2014)
Tab. 2b: Prevalence of parasites found using sedimentation methods in faecal samples from common hippopotamuses collected in Gabon in 2011
Flotation
age of Sample Results Sample Nr. ∑ %
17-22, 26-28, 31-37, 40-42, 45, 47, 50, 24 h < Eimeria spp. 37 48.1 54-56, 58-63, 66, 68, 74-77
24 h < deformed larva 10 1 1,3
24 h < larvae from Strogyloides 12 1 1,3
Eimeria spp.; deformed egg 24 h < 73 1 1,3 (presumably Strogyloides)
3, 6-9, 11, 13,14, 16, 30, 38,39, 43,44, 24 h < negative 24 31.2 46, 49, 51-53, 57, 64,65, 69, 70
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
larvae from Strongyloides > 48 h 4 1 1,3 (Dictyocaulus)
> 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
Conclusion
The study demonstrated the feasibility of perfor- impact, although the prevalence found in the hippo- ming a parasitological screening of free ranging potamuses in our sampling area was remarkable. common hippopotamuses through the analysis of The intriguing nding of a Dictyocaulus larva in one recovered faecal samples. The xation of faeces in a sample also suggests that there are still undescribed solution of formalin, sodium acetate, acetic acid and parasites in the common hippopotamus. tap water allowed the extraction of parasites in diffe- rent stages of development for six months after sam- Acknowledgement ple collection. The ndings suggest a low parasitic This research was partially funded by the WWF. load and diversity in the common hippopotamus in Without the permissions from the CENAREST the Gamba Complex of Protected Areas in Gabon, (National Centre of Scienti c Research of Gabon), the possibly due to the species’ low population density ANPN (National Agency for National Parks of there. Gabon), the senior warden of the national parks and The speci city and sensitivity of the method would the support in the eld from WWF Gabon and the bene t from further validation. Nevertheless, it can local staff, this survey could not have been done. be used for a reliable parasitical screening of free- Many thanks to the Institute of Parasitology of the ranging common hippopotamuses. University of Veterinary Medicine Vienna for perfor- Further research is needed to investigate which ming the examination of the faecal samples, and to species of Eimeria are present in hippopotamuses. Dr. P.K. Robbins and Dr. N. Leader-Williams for a Little is known about this parasite and its possible number of comments and suggestions.
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