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Gastrointestinal Parasites of the Ethiopian Rock Hyrax (<i>Procavia capensis</i>, Pallas, 1766) in the North East Region of Ghana

Gastrointestinal Parasites of the Ethiopian Rock Hyrax (Procavia capensis, Pallas, 1766)... Hindawi International Journal of Zoology Volume 2023, Article ID 6008732, 8 pages https://doi.org/10.1155/2023/6008732 Research Article Gastrointestinal Parasites of the Ethiopian Rock Hyrax (Procavia capensis, Pallas, 1766) in the North East Region of Ghana 1 2 1 3 Langbong Bimi , Ato Kwamena Tetteh , Daniel Oduro , and Francis Anto Department of Animal Biology & Conservation Science, University of Ghana, P.O. Box LG. 67, Legon, Accra, Ghana Laboratory Department, Cape Coast Metropolitan Hospital, P.O. Box 174, Cape Coast, Ghana School of Public Health, College of Health Sciences, University of Ghana, Legon, Accra, Ghana Correspondence should be addressed to Langbong Bimi; lbimi@ug.edu.gh Received 2 August 2022; Revised 26 July 2023; Accepted 1 August 2023; Published 11 August 2023 Academic Editor: Edson Gandiwa Copyright © 2023 Langbong Bimi et al. Tis is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Wildlife may serve as potential reservoirs and intermediate or accidental hosts of zoonotic pathogens due to their interactions with human beings. For the frst time in Ghana, we report extempore the gastrointestinal parasites of three Ethiopian rock hyraxes captured in September 2021. Forty adult parasites (21 nematodes and 19 tapeworms) were recovered from the gastrointestinal tracts of these three game hyraxes (Procavia capensis, Pallas, 1766) from the hills of Bimbagu (near the Gambaga Scarp) in the North East Region of Ghana. Adult worms comprising 16 tapeworms and 24 nematodes were identifed. Te intestinal faecal examination detected ova of Trichuris spp., tapeworms, and hookworms. Te results are presented alongside the results of the molecular determination of the worm identities. Since wildlife has been identifed as an important source of emerging human pathogens, including helminth parasites, there is an urgent need for sufcient literature on wildlife parasites in Ghana. As the rock hyrax is hunted for its meat, there is a potential risk of transmitting these identifed helminths and other zoonotic pathogens to humans, especially involving people who handle the carcasses as the transmission is faecal-oral. A more precarious situation may arise when the eggs of cestodes are ingested by handlers of these carcasses and could result in cysticercosis/neuro-cysticercosis when these eggs cross the blood-brain barrier in the person. transmission, which originates in mammals [3, 4], or in- 1. Introduction teractions between wildlife and domestic animals [5, 6]. Te Te rock hyrax (Procavia capensis, Pallas 1760; family: majority of emerging and re-emerging human infectious Procaviidae; order: Hyracoidea), also known as rock dassies diseases (EIDs) have also been associated with zoonosis. Te or rock rabbits, are stub-tailed, rabbit-like medium-sized (3- coexistence of wildlife and humans may become more 4 kg) social terrestrial mammals native to Africa and the common because of habitat loss; however, the greater efects Middle East [1]. Rock hyraxes resemble rodents, but their of biodiversity loss may reduce the interactions. As postu- closest relatives are elephants and manatees. Tey are the lated by Cable et al. [7], the negative impacts of parasitic only member of the genus Procavia, one of only four living infections can be extreme in as much as they are ubiquitous species in the order Hyracoidea, and the hyrax species most in wildlife, livestock, and the human population. Te fre- adapted to arid environments [2]. However, farming and quent contact with wildlife through the bushmeat trade may rural hunters’ activities threaten hyraxes’ existence. also predispose people to infection with zoonotic pathogens. Human-wildlife conficts, poaching, and hunting are Pathogens transmissible to humans through bushmeat may major issues in developing countries and may contribute to include monkeypox virus, Ebola and Marburg floviruses, the extinction of some protected species. Typically, hunting anthrax, herpes viruses, hepatitis viruses, and para- of wildlife as food is associated with zoonotic disease myxoviruses [8, 9]. Despite parasitic protozoa being the 2 International Journal of Zoology Figure 1: Map of Ghana showing the location of Bimbagu in the North East Region. second most common cause of zoonotic diseases, behind [17]. We extemporaneously report on the gastrointestinal parasites of three hyraxes killed by a local hunter in viruses, helminths still play a signifcant role in disease transmission [10]. Bimbagu, North East Region of Ghana. While notable external parasites such as ticks, lice, mites, and feas have been observed in the rock hyrax, 2. Materials and Methods internal parasites, such as nematodes and cestodes, have also been recorded. Tese could also play an important role In September 2021, we encountered a local hunter spon- in hyrax mortality [11]. Hoeck [12] noted that rock and tree taneously in Bimbagu (Figure 1), a town in the Nakpanduri- hyraxes might be an important reservoir for the leishmania Bunkpurugu District, North East Region, Ghana. Te town parasite. Helminths have zoonotic potential in most in- is located at an elevation of 443 meters above sea level, and ° ° fections, although this is rare [13, 14]. Species of the its coordinates are 10 34′60″N and 0 6′0″W. Among his anoplocephalid cestode genus Inermicapsifer are very day’s games were two female and one male Ethiopian rock common in Africa, mainly in rodents and hyraxes [15]. hyraxes (Figure 2), weighing 2.32 kg, 1.73 kg, and 2.05 kg, Within the genus Inermicapsifer, I. madagascariensis is respectively. Tese were brought to the Department of widespread in animals and has been reported in humans Animal Biology and Conservation Science, University of from several African countries, including Kenya, South Ghana, for autopsy and examination of the gastrointestinal Africa, Zambia, and Zimbabwe [16]. Tese helminths have tracts for parasites. A longitudinal incision using a surgical adapted in diferent ways to the microenvironment of the blade opened the body cavity of all three animals from the vertebrate intestine since this specialised habitat afords throat to vent. Te gut contents were examined thoroughly parasites a reliable source of nutrients, a relatively ho- with a magnifying glass for adult parasites. Te various meostatic environment, and protection from predators sections of the alimentary canal were frst identifed and cut International Journal of Zoology 3 Penis (a) (b) Figure 2: Te specimen (Ethiopian rock hyraxes). of. Tese sections were removed and opened, and the 3. Results contents were washed with 0.9% saline into Petri dishes and 3.1. Identifcation of Recovered Worms. Adult worms (Fig- examined thoroughly for adult worms. All the adult worms ures3–5) and their ova/oocysts (Figure 6) were recovered found were preserved in 70% ethanol and later identifed from the GIT of all three animals. While fve nematodes according to the descriptions [18]. (hookworms and Strongyles) and three tapeworms were recovered from one of the females (Figure 2(a)), the second 2.1. Identifcation of Parasite Ova and Oocysts. After carrying female was observed to contain eight nematodes (six out the macroscopic examinations on the various segments of hookworms and two Trichuris spp.) but no tapeworms. the gastrointestinal tracts (GITs) for adult parasites, the zinc Likewise, the male specimen had eight nematodes and 16 sulphate (ZnSO ) centrifugal foatation technique [19, 20] was tapeworms from the stomach and small intestine. used for the identifcation of parasite ova (nematodes, trem- While the adult nematodes were identifed as hook- atodes, and cestodes). About 3 mg of faecal samples were mixed worms and Strongyles, the tapeworms were identifed as with 15 ml of ZnSO solution, and the resulting solutions were Inermicapsifer spp., a genus of tapeworms of the family then strained through a nylon tea strainer to remove coarse Anoplocephalidae. Some of the worm ova/eggs and larvae faecal materials. Te resultant solutions were then poured into recovered from the faecal contents of the animals are pre- the appropriate tubes and centrifuged at 1500 rpm for sented in Figure 6. 5 minutes. Te tubes were removed from the centrifuge, flled with the fotation solution to the top, and left for 10 minutes. Finally, a drop of the solution at the top was placed on a mi- 3.2. Images of Gel Electrophoresis. Te images for Strong- croscope glass slide, covered with a cover slip, and examined yloides spp. and Pinworm. are shown in Figures 7 and 8, with a 40x light microscope objective. Identifcation of hel- respectively. Te molecular weight marker, or the DNA minths, helminth eggs, and protozoan oocysts was done by ladder denoted by M (lane M), was used to detect the ap- standard parasitological criteria[21, 22]. proximate sizes of the amplicons. 2.2. DNA Amplifcation by Polymerase Chain Reaction. 4. Discussion Direct polymerase chain reaction (PCR) was used to amplify worm DNA fragments using genus-specifc primers as in- We examined the gastrointestinal tract contents of three dicated in Table 1. rock hyraxes captured from the hills of Bimbagu in Ghana. A All PCR reactions were performed in fnal volumes of total of 40 adult parasites were recovered. Tese included 25.0 μl, and the products were examined by electrophoresis hookworms, Strongyles (tapeworms), and Trichuris spp., on 2% agarose gels stained with ethidium bromide. with all three hyraxes being infested with more than one 4 International Journal of Zoology Table 1: Primer sets for the polymerase chain reaction (PCR). Pathogen Primers Primer sequence Reference F2662 5′-GGCAAAAGTCGTAACAAGGT-3′ Ascaris spp. Dorris et al. [23] R3214 5′-CTGCAATTCGCACTATTTATCG-3′ GS-forward 5′-AAAGATTAAGCCATGCATG-3′ Strongyloides spp. Ishiwata et al. [24], Marques et al. [25] GS-reverse 5′-GCCTGCTGCCTTCCTTGGA-3′ GSNC5 F 5′-GTAGGTGAACCTGCGGAAGGACATT-3′ Nematodes Newton et al. [26] GSNC2 R 5′-TTAGTTTCTTTTCCTCCGCT-3′ (a) (b) (c) Copulatory bursa (d) Figure 3: Adult hookworms with typical cylindrical bodies (a) and sharply curved heads (c). Te buccal capsule (b) and the bursae rays (d) are also very visible. (a) Whole worms (b) anterior end (c) posterior end (d) male worm with copulatory bursa. Figure 4: Adult Trichuris spp. parasite species of public health importance. As indicated by are hunted and eaten as meat. Te helminths in the hyraxes Kołodziej-Sobocinska ´ [27], the existing state of knowledge belong to the same genus that can infect people. However, on the factors afecting parasitic diseases in wild mammals we are unsure of the species present in these animals, so we shows a need for sufcient literature on parasites in wildlife. cannot say with certainty whether they can survive to infect Te reason is not only for academic purposes but also for the humans. Until we can establish their potential survival, we beneft and use in managing wild mammal species and advocate that humans avoid contact with or handle these disease control in nature. Te fndings of our current study, animals with caution. where co-infections of helminth species have been observed Although these helminths were not identifed to the in wild mammals, agree with earlier observations made in species level, the additional microscopic examination of some developed countries [28]. Also, as explained by Bimi faeces from the gastrointestinal tracts of the animals made it possible to confrm their identities. Since more than 75% of et al. [29], the fndings of parasites in wildlife should raise concerns about the possibility of zoonotic transmission of human diseases are of zoonotic origin [30], signifcant public the parasites from these animals to humans, especially if they health consideration must be given to the game we hunt for International Journal of Zoology 5 (a) (b) Figure 5: Recovered adult tapeworms presenting some of their notable features. (a) Adult tapeworms. (b) Tapeworm head/scolex with suckers. (a) (b) (c) Figure 6: Continued. 6 International Journal of Zoology (d) Figure 6: Recovered worm ova/larva presenting some of their notable features. (a) Recovered thin-shelled eggs of hookworms, taken at 40x magnifcation. (b) A flariform hookworm larva with a well-developed tail and esophagus. (c) Ova of Trichuris spp. (d) Tapeworm ovum. STRONGYLOIDES (GSF/R) &PINWORM (GSNCF/R) PRIMERS STRONGYLOIDES (GSF/R) PINWORM (GSNCF/R) NCGN PC C GPCM Figure 7: Amplifed PCR product of Strongyloides spp. and Pinworm spp. (lane M � 100 bp, lane NC � negative control, lane PC � positive control, and lane G � positive sample). ASCARIS PRIMERS (F2662/R3214) AB C D E F NC PC M Figure 8: Amplifed PCR product of Ascaris spp. (lane M � 100 bp, lane NC � negative control, lane PC � positive control, lane E � positive sample, and lanes A, B, C, D, and F � negative samples). and epidemiological data support evidence for the zoonotic food. Te recovery of these helminths in the hyraxes in this small geographic area of Ghana could be associated with potential among species of hookworm transmission to environmental conditions and interaction between wildlife, humans, which is being facilitated by increased human- domestic animals, and humans that could support the wildlife interactions. Our recent study on soil-transmitted transmission of zoonotic parasites in the area. helminthiasis in the study area found a prevalence of 19% Although the current study did not establish a direct link hookworm infestation in humans [33]. between infestations in wildlife and humans, observations are that zoonotic diseases are increasingly becoming an 5. Conclusions emerging public health threat [31], partly due to the risk of spillover incidents at the human-wildlife interface. Tere is, Tis paper has shown that there are gastrointestinal therefore, the possibility of these animals transmitting infestations of wildlife with diferent parasite species in pathogens to humans. According to Xie et al. [32], molecular the study area. Tree gastrointestinal helminths International Journal of Zoology 7 (hookworms, Strongyles, and Trichuris spp.) and ces- Acknowledgments todes (Inermicapsifer spp.) were detected in the study Te authors would like to thank the Laboratory Technicians animals. Te possibility for zoonotic helminths to es- of the Department of Animal Biology and Conservation tablish in humans and cause disease is a potential public Science for assisting in dissecting and collecting GIT con- health problem, partly due to the risk of spillover events tents for examination. at the human-wildlife interface. Tese helminths can potentially be transmitted to humans if the necessary precautions are not taken. References Furthermore, the study has demonstrated that hyraxes [1] T. Butynski, H. Hoeck, and Y. A. de Jong, “Heterohyrax could be hosts of helminths and could play a role in Brucei, Bush Hyrax,” Te IUCN Red List of Treatened transmitting the same to humans. Te infuence of these Species, 2015, https://www.inaturalist.org/taxa/43088- parasites on human health cannot be overstated and should, Heterohyrax-brucei. thus, be considered in risk assessments. [2] H. N. 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Over the years, this feat has Philosophical Transactions of the Royal Society B: Biological manifested itself grossly due to encroachment on Sciences, vol. 372, no. 1719, Article ID 20160088, 2017. their natural habitats by human dwellings and the [8] S. Friant, S. B. Paige, and T. L. Goldberg, “Drivers of bushmeat fact that they are hunted and eaten as meat. hunting and perceptions of zoonoses in Nigerian hunting communities,” PLoS Neglected Tropical Diseases, vol. 9, no. 5, (2) Te recovery of these helminths from the rock Article ID e0003792, 2015. hyrax’s intestinal tracts could indicate their ability to [9] A. O. Kamins, J. M. Rowclife, Y. Ntiamoa-Baidu, host and probably transmit the parasites into human A. A. Cunningham, J. L. N. Wood, and O. Restif, “Charac- populations. teristics and risk perceptions of Ghanaians potentially ex- (3) Tere is, therefore, an urgent need to unearth the posed to bat-borne zoonoses through bushmeat,” EcoHealth, zoonotic potential of the hyrax as a host of helminths vol. 12, no. 1, pp. 104–120, 2015. and other disease-causing organisms to lessen their [10] L. Polley, “Navigating parasite webs and parasite fow: efects. emerging and re-emerging parasitic zoonoses of wildlife or- igin,” International Journal for Parasitology, vol. 35, no. 11–12, pp. 1279–1294, 2005. Data Availability [11] V. V. Shimalov, “Helminth parasites of the Eurasian water shrew (Neomys fodiens pennant, 1771) in South-West All data used to support the fndings of this study are Belarus,” Journal of Parasitic Diseases, vol. 41, no. 2, available upon request from the corresponding author. pp. 602–604, 2017. [12] H. N. Hoeck, “Demography and competition in hyrax,” Oecologia, vol. 79, no. 3, pp. 353–360, 1989. Disclosure [13] B. A. Mathison and B. S. Pritt, “A systematic overview of zoonotic helminth infections in North America,” Laboratory Tis study was part of the authors’ employment at the Medicine, vol. 49, no. 4, pp. e61–e93, 2018. University of Ghana. Te authors’ sole responsibility was [14] M. W. Robinson and J. P. Dalton, “Zoonotic helminth in- to write, edit, seek approval, or decide to publish this fections with particular emphasis on fasciolosis and other article. trematodiases,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 364, no. 1530, pp. 2763–2776, 2009. [15] L. J. Fourie, I. G. Horak, and E. Visser, “Quantitative and Conflicts of Interest qualitative aspects of the parasite burdens of rock dassies Te authors declare that they have no conficts of interest. (Procavia capensis Pallas, 1766) in the Mountain Zebra 8 International Journal of Zoology National Park,” South African Journal of Zoology, vol. 22, ancylostomatidae), a new hookworm parasite isolated from wild giant pandas in Southwest China,” Parasites & Vectors, no. 2, pp. 101–106, 1987. [16] C. N. L. Macpherson and P. S. Craig, “Zoonotic helminths of vol. 10, p. 277, 2017. [33] L. Bimi, H. O. Addo, and F. Anto, “Prevalence of soil- wild and domestic animals in Africa,” Parasitic Helminths and Zoonoses in Africa, pp. 260–272, 1991. transmitted helminth infections in the rural North of Ghana,” Integr J Vet Biosci, vol. 4, no. 2, pp. 1–4, 2020. [17] E. G. Hayunga, “Morphological adaptations of intestinal helminths author (s): eugene G. Hayunga,” Te Journal of Parasitology, vol. 77, no. 6, pp. 865–873, 1991. [18] J. Sprent, “Studies on ascaridoid nematodes in pythons: speciation of Ophidascaris in the Oriental and Australian regions,” Parasitology, vol. 59, no. 4, pp. 937–959, 1969. [19] C. Hendrix and E. Robinson, “Common laboratory pro- cedures for diagnosing parasitism,” Diagnostic Parasitology for Veterinary Technicians, Elsevier, St. Louis, MO, USA, 4th edition, 2012. [20] K. D. Parameshwarappa, C. Chandrakanth, and B. Sunil, “Te prevalence of intestinal parasitic infestations and the evalu- ation of diferent concentration techniques of the stool ex- amination,” Journal of Clinical and Diagnostic Research, vol. 6, no. 7, pp. 1188–1191, 2012. [21] J. Hansen and B. Perry, Te Epidemiology, Diagnosis, and Control of Helminths Parasites of Ruminants, International Laboratory for Research on Animal Disease (ILRAD), Nai- robi, Kenya, 1994. [22] E. J. L. Soulsby, Helminths, Anthropods and Protozoa of Domesticated Animals, Bailliere Tindall, London, England, 7th edition, 1982. [23] M. Dorris, M. E. Viney, and M. L. Blaxter, “Molecular phylogenetic analysis of the genus Strongyloides and related nematodes,” International Journal for Parasitology, vol. 32, no. 12, pp. 1507–1517, 2002. [24] K. Ishiwata, A. Shinohara, K. Yagi, Y. Horii, K. Tsuchiya, and Y. Nawa, “Identifcation of tissue-embedded ascarid larvae by ribosomal DNA sequencing,” Parasitology Research, vol. 92, no. 1, pp. 50–52, 2004. [25] P. Marques, F. Malta, D. Meisel et al., “Diagnosis of the strongyloid nematode Strongyloides venezuelensis in experi- mentally infected rats,” Journal of Helminthology, vol. 90, no. 4, pp. 422–427, 2016. [26] L. Newton, N. Chilton, I. Beveridge, H. Hoste, P. Nansen, and R. Gasser, “Genetic markers for strongylid nematodes of livestock defned by PCR-based restriction analysis of spacer rDNA,” Acta Tropica, vol. 69, no. 1, pp. 1–15, 1998. [27] M. Kołodziej-Sobocinska, ´ “Factors afecting the spread of parasites in populations of wild European terrestrial mam- mals,” Mammal Research, vol. 64, no. 3, pp. 301–318, 2019. [28] P. Craig and C. Macpherson, Parasitic Helminths and Zoo- noses in Africa, Springer Science & Business Media, Berlin, Germany, 2012. [29] L. Bimi, F. K. Odamtten, F. Anto, and A. K. Tetteh, “Ophi- dascaris spp. in an african rock Python (Python sebae) in Ghana: a case report,” J Med Microbiol Infect Dis, vol. 9, no. 2, pp. 103–107, 2021. [30] U. Mackenstedt, D. Jenkins, and T. Romig, “Te role of wildlife in the transmission of parasitic zoonoses in peri- urban and urban areas,” Int J Parasitol Parasites Wildl, vol. 4, no. 1, pp. 71–79, 2015. [31] S. Namusisi, M. Mahero, D. Travis, K. Pelican, C. Robertson, and L. Mugisha, “A descriptive study of zoonotic disease risk at the human-wildlife interface in a biodiversity hot spot in Southwestern Uganda,” PLoS Neglected Tropical Diseases, vol. 15, no. 1, pp. 1–16, 2021. [32] Y. Xie, E. P. Hoberg, Z. Yang, J. J. Urban, and G. Yang, “Ancylostoma ailuropodae n. spp. (Nematoda: http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png International Journal of Zoology Hindawi Publishing Corporation

Gastrointestinal Parasites of the Ethiopian Rock Hyrax (<i>Procavia capensis</i>, Pallas, 1766) in the North East Region of Ghana

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Hindawi International Journal of Zoology Volume 2023, Article ID 6008732, 8 pages https://doi.org/10.1155/2023/6008732 Research Article Gastrointestinal Parasites of the Ethiopian Rock Hyrax (Procavia capensis, Pallas, 1766) in the North East Region of Ghana 1 2 1 3 Langbong Bimi , Ato Kwamena Tetteh , Daniel Oduro , and Francis Anto Department of Animal Biology & Conservation Science, University of Ghana, P.O. Box LG. 67, Legon, Accra, Ghana Laboratory Department, Cape Coast Metropolitan Hospital, P.O. Box 174, Cape Coast, Ghana School of Public Health, College of Health Sciences, University of Ghana, Legon, Accra, Ghana Correspondence should be addressed to Langbong Bimi; lbimi@ug.edu.gh Received 2 August 2022; Revised 26 July 2023; Accepted 1 August 2023; Published 11 August 2023 Academic Editor: Edson Gandiwa Copyright © 2023 Langbong Bimi et al. Tis is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Wildlife may serve as potential reservoirs and intermediate or accidental hosts of zoonotic pathogens due to their interactions with human beings. For the frst time in Ghana, we report extempore the gastrointestinal parasites of three Ethiopian rock hyraxes captured in September 2021. Forty adult parasites (21 nematodes and 19 tapeworms) were recovered from the gastrointestinal tracts of these three game hyraxes (Procavia capensis, Pallas, 1766) from the hills of Bimbagu (near the Gambaga Scarp) in the North East Region of Ghana. Adult worms comprising 16 tapeworms and 24 nematodes were identifed. Te intestinal faecal examination detected ova of Trichuris spp., tapeworms, and hookworms. Te results are presented alongside the results of the molecular determination of the worm identities. Since wildlife has been identifed as an important source of emerging human pathogens, including helminth parasites, there is an urgent need for sufcient literature on wildlife parasites in Ghana. As the rock hyrax is hunted for its meat, there is a potential risk of transmitting these identifed helminths and other zoonotic pathogens to humans, especially involving people who handle the carcasses as the transmission is faecal-oral. A more precarious situation may arise when the eggs of cestodes are ingested by handlers of these carcasses and could result in cysticercosis/neuro-cysticercosis when these eggs cross the blood-brain barrier in the person. transmission, which originates in mammals [3, 4], or in- 1. Introduction teractions between wildlife and domestic animals [5, 6]. Te Te rock hyrax (Procavia capensis, Pallas 1760; family: majority of emerging and re-emerging human infectious Procaviidae; order: Hyracoidea), also known as rock dassies diseases (EIDs) have also been associated with zoonosis. Te or rock rabbits, are stub-tailed, rabbit-like medium-sized (3- coexistence of wildlife and humans may become more 4 kg) social terrestrial mammals native to Africa and the common because of habitat loss; however, the greater efects Middle East [1]. Rock hyraxes resemble rodents, but their of biodiversity loss may reduce the interactions. As postu- closest relatives are elephants and manatees. Tey are the lated by Cable et al. [7], the negative impacts of parasitic only member of the genus Procavia, one of only four living infections can be extreme in as much as they are ubiquitous species in the order Hyracoidea, and the hyrax species most in wildlife, livestock, and the human population. Te fre- adapted to arid environments [2]. However, farming and quent contact with wildlife through the bushmeat trade may rural hunters’ activities threaten hyraxes’ existence. also predispose people to infection with zoonotic pathogens. Human-wildlife conficts, poaching, and hunting are Pathogens transmissible to humans through bushmeat may major issues in developing countries and may contribute to include monkeypox virus, Ebola and Marburg floviruses, the extinction of some protected species. Typically, hunting anthrax, herpes viruses, hepatitis viruses, and para- of wildlife as food is associated with zoonotic disease myxoviruses [8, 9]. Despite parasitic protozoa being the 2 International Journal of Zoology Figure 1: Map of Ghana showing the location of Bimbagu in the North East Region. second most common cause of zoonotic diseases, behind [17]. We extemporaneously report on the gastrointestinal parasites of three hyraxes killed by a local hunter in viruses, helminths still play a signifcant role in disease transmission [10]. Bimbagu, North East Region of Ghana. While notable external parasites such as ticks, lice, mites, and feas have been observed in the rock hyrax, 2. Materials and Methods internal parasites, such as nematodes and cestodes, have also been recorded. Tese could also play an important role In September 2021, we encountered a local hunter spon- in hyrax mortality [11]. Hoeck [12] noted that rock and tree taneously in Bimbagu (Figure 1), a town in the Nakpanduri- hyraxes might be an important reservoir for the leishmania Bunkpurugu District, North East Region, Ghana. Te town parasite. Helminths have zoonotic potential in most in- is located at an elevation of 443 meters above sea level, and ° ° fections, although this is rare [13, 14]. Species of the its coordinates are 10 34′60″N and 0 6′0″W. Among his anoplocephalid cestode genus Inermicapsifer are very day’s games were two female and one male Ethiopian rock common in Africa, mainly in rodents and hyraxes [15]. hyraxes (Figure 2), weighing 2.32 kg, 1.73 kg, and 2.05 kg, Within the genus Inermicapsifer, I. madagascariensis is respectively. Tese were brought to the Department of widespread in animals and has been reported in humans Animal Biology and Conservation Science, University of from several African countries, including Kenya, South Ghana, for autopsy and examination of the gastrointestinal Africa, Zambia, and Zimbabwe [16]. Tese helminths have tracts for parasites. A longitudinal incision using a surgical adapted in diferent ways to the microenvironment of the blade opened the body cavity of all three animals from the vertebrate intestine since this specialised habitat afords throat to vent. Te gut contents were examined thoroughly parasites a reliable source of nutrients, a relatively ho- with a magnifying glass for adult parasites. Te various meostatic environment, and protection from predators sections of the alimentary canal were frst identifed and cut International Journal of Zoology 3 Penis (a) (b) Figure 2: Te specimen (Ethiopian rock hyraxes). of. Tese sections were removed and opened, and the 3. Results contents were washed with 0.9% saline into Petri dishes and 3.1. Identifcation of Recovered Worms. Adult worms (Fig- examined thoroughly for adult worms. All the adult worms ures3–5) and their ova/oocysts (Figure 6) were recovered found were preserved in 70% ethanol and later identifed from the GIT of all three animals. While fve nematodes according to the descriptions [18]. (hookworms and Strongyles) and three tapeworms were recovered from one of the females (Figure 2(a)), the second 2.1. Identifcation of Parasite Ova and Oocysts. After carrying female was observed to contain eight nematodes (six out the macroscopic examinations on the various segments of hookworms and two Trichuris spp.) but no tapeworms. the gastrointestinal tracts (GITs) for adult parasites, the zinc Likewise, the male specimen had eight nematodes and 16 sulphate (ZnSO ) centrifugal foatation technique [19, 20] was tapeworms from the stomach and small intestine. used for the identifcation of parasite ova (nematodes, trem- While the adult nematodes were identifed as hook- atodes, and cestodes). About 3 mg of faecal samples were mixed worms and Strongyles, the tapeworms were identifed as with 15 ml of ZnSO solution, and the resulting solutions were Inermicapsifer spp., a genus of tapeworms of the family then strained through a nylon tea strainer to remove coarse Anoplocephalidae. Some of the worm ova/eggs and larvae faecal materials. Te resultant solutions were then poured into recovered from the faecal contents of the animals are pre- the appropriate tubes and centrifuged at 1500 rpm for sented in Figure 6. 5 minutes. Te tubes were removed from the centrifuge, flled with the fotation solution to the top, and left for 10 minutes. Finally, a drop of the solution at the top was placed on a mi- 3.2. Images of Gel Electrophoresis. Te images for Strong- croscope glass slide, covered with a cover slip, and examined yloides spp. and Pinworm. are shown in Figures 7 and 8, with a 40x light microscope objective. Identifcation of hel- respectively. Te molecular weight marker, or the DNA minths, helminth eggs, and protozoan oocysts was done by ladder denoted by M (lane M), was used to detect the ap- standard parasitological criteria[21, 22]. proximate sizes of the amplicons. 2.2. DNA Amplifcation by Polymerase Chain Reaction. 4. Discussion Direct polymerase chain reaction (PCR) was used to amplify worm DNA fragments using genus-specifc primers as in- We examined the gastrointestinal tract contents of three dicated in Table 1. rock hyraxes captured from the hills of Bimbagu in Ghana. A All PCR reactions were performed in fnal volumes of total of 40 adult parasites were recovered. Tese included 25.0 μl, and the products were examined by electrophoresis hookworms, Strongyles (tapeworms), and Trichuris spp., on 2% agarose gels stained with ethidium bromide. with all three hyraxes being infested with more than one 4 International Journal of Zoology Table 1: Primer sets for the polymerase chain reaction (PCR). Pathogen Primers Primer sequence Reference F2662 5′-GGCAAAAGTCGTAACAAGGT-3′ Ascaris spp. Dorris et al. [23] R3214 5′-CTGCAATTCGCACTATTTATCG-3′ GS-forward 5′-AAAGATTAAGCCATGCATG-3′ Strongyloides spp. Ishiwata et al. [24], Marques et al. [25] GS-reverse 5′-GCCTGCTGCCTTCCTTGGA-3′ GSNC5 F 5′-GTAGGTGAACCTGCGGAAGGACATT-3′ Nematodes Newton et al. [26] GSNC2 R 5′-TTAGTTTCTTTTCCTCCGCT-3′ (a) (b) (c) Copulatory bursa (d) Figure 3: Adult hookworms with typical cylindrical bodies (a) and sharply curved heads (c). Te buccal capsule (b) and the bursae rays (d) are also very visible. (a) Whole worms (b) anterior end (c) posterior end (d) male worm with copulatory bursa. Figure 4: Adult Trichuris spp. parasite species of public health importance. As indicated by are hunted and eaten as meat. Te helminths in the hyraxes Kołodziej-Sobocinska ´ [27], the existing state of knowledge belong to the same genus that can infect people. However, on the factors afecting parasitic diseases in wild mammals we are unsure of the species present in these animals, so we shows a need for sufcient literature on parasites in wildlife. cannot say with certainty whether they can survive to infect Te reason is not only for academic purposes but also for the humans. Until we can establish their potential survival, we beneft and use in managing wild mammal species and advocate that humans avoid contact with or handle these disease control in nature. Te fndings of our current study, animals with caution. where co-infections of helminth species have been observed Although these helminths were not identifed to the in wild mammals, agree with earlier observations made in species level, the additional microscopic examination of some developed countries [28]. Also, as explained by Bimi faeces from the gastrointestinal tracts of the animals made it possible to confrm their identities. Since more than 75% of et al. [29], the fndings of parasites in wildlife should raise concerns about the possibility of zoonotic transmission of human diseases are of zoonotic origin [30], signifcant public the parasites from these animals to humans, especially if they health consideration must be given to the game we hunt for International Journal of Zoology 5 (a) (b) Figure 5: Recovered adult tapeworms presenting some of their notable features. (a) Adult tapeworms. (b) Tapeworm head/scolex with suckers. (a) (b) (c) Figure 6: Continued. 6 International Journal of Zoology (d) Figure 6: Recovered worm ova/larva presenting some of their notable features. (a) Recovered thin-shelled eggs of hookworms, taken at 40x magnifcation. (b) A flariform hookworm larva with a well-developed tail and esophagus. (c) Ova of Trichuris spp. (d) Tapeworm ovum. STRONGYLOIDES (GSF/R) &PINWORM (GSNCF/R) PRIMERS STRONGYLOIDES (GSF/R) PINWORM (GSNCF/R) NCGN PC C GPCM Figure 7: Amplifed PCR product of Strongyloides spp. and Pinworm spp. (lane M � 100 bp, lane NC � negative control, lane PC � positive control, and lane G � positive sample). ASCARIS PRIMERS (F2662/R3214) AB C D E F NC PC M Figure 8: Amplifed PCR product of Ascaris spp. (lane M � 100 bp, lane NC � negative control, lane PC � positive control, lane E � positive sample, and lanes A, B, C, D, and F � negative samples). and epidemiological data support evidence for the zoonotic food. Te recovery of these helminths in the hyraxes in this small geographic area of Ghana could be associated with potential among species of hookworm transmission to environmental conditions and interaction between wildlife, humans, which is being facilitated by increased human- domestic animals, and humans that could support the wildlife interactions. Our recent study on soil-transmitted transmission of zoonotic parasites in the area. helminthiasis in the study area found a prevalence of 19% Although the current study did not establish a direct link hookworm infestation in humans [33]. between infestations in wildlife and humans, observations are that zoonotic diseases are increasingly becoming an 5. Conclusions emerging public health threat [31], partly due to the risk of spillover incidents at the human-wildlife interface. Tere is, Tis paper has shown that there are gastrointestinal therefore, the possibility of these animals transmitting infestations of wildlife with diferent parasite species in pathogens to humans. According to Xie et al. [32], molecular the study area. Tree gastrointestinal helminths International Journal of Zoology 7 (hookworms, Strongyles, and Trichuris spp.) and ces- Acknowledgments todes (Inermicapsifer spp.) were detected in the study Te authors would like to thank the Laboratory Technicians animals. 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