Cestodes of the family Anoplocephalidae parasitize a wide range of usually herbivorous hosts including e.g. rodents, ungulates, primates, elephants and hyraxes. While in some hosts, the epidemiology of the infection is well studied, information is lacking in others. In this study of mountain gorillas in the Virunga Massif, an extensive sample set comprising adult cestodes collected via necropsies, proglottids shed in feces, and finally, fecal samples from both night nests and identified individuals were analysed. Anoplocephala gorillae was the dominant cestode species detected in night nest samples and individually known gorillas, of which only 1 individual hosted a Bertiella sp. It was shown that the 2 species can be distinguished through microscopy based on egg morphology and polymerase chain reaction (PCR) assays for diagnostics of both species were provided. Sequences of mitochondrial (cox 1) and nuclear (ITS1, 18S rDNA, 28S rDNA) markers were used to evaluate the phylogenetic position of the 2 cestodes detected in mountain gorillas. Both types of fecal samples, from night nests and from identified individuals, provided comparable information about the prevalence of anoplocephalid cestodes, although the analysis of samples collected from identified gorilla individuals showed significant intra-individual fluctuation of A. gorillae egg shedding within a short period. Therefore, multiple samples should be examined to obtain reliable data for wildlife health management programmes, especially when application of anthelmintic treatment is considered. However, while A. gorillae is apparently a common symbiont of mountain gorillas, it does not seem to impair the health of its host.

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Pathology and Parasitology Faculty of Veterinary Sciences University of Veterinary Sciences Brno Brno Czech Republic

Department of Physical Geography and Geoecology Faculty of Science Charles University Prague Czech Republic

Department of Veterinary Sciences Faculty of Agrobiology Food and Natural Resources CINeZ Czech University of Life Sciences Prague Prague Czech Republic

Dian Fossey Gorilla Fund Musanze Rwanda

Gorilla Doctors Davis CA USA

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

Liberec Zoo Liberec Czech Republic

Rwanda Development Board Kigali Rwanda

Sydney School of Veterinary Science Faculty of Science University of Sydney Sydney Australia

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Altschul SF, Gish W, Miller W, Myers EW and Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Anisimova M, Gil M, Dufayard JF, Dessimoz C and Gascuel O (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Systematic Biology 60, 685–699. doi: 10.1093/sysbio/syr041. PubMed DOI PMC

Appleton CC, Krecek RC, Verster A, Bruorton MR and Lawes MJ (1994) Gastrointestinal parasites of the Samango monkey, Cercopithecus mitis, in Natal, South Africa. Journal of Medical Primatology 23, 52–55. doi: 10.1111/j.1600-0684.1994.tb00096.x. PubMed DOI

Ashford RW, Reid GDF and Butynski TM (1990) The intestinal faunas of man and mountain gorillas in a shared habitat. Annals of Tropical Medicine and Parasitology 84, 337–340. doi: 10.1080/00034983.1990.11812477. PubMed DOI

Ashford RW, Lawson H, Butynski TM and Reid GDF (1996) Patterns of intestinal parasitism in the mountain gorilla Gorilla gorilla in the Bwindi-Impenetrable Forest, Uganda. Journal of Zoology 239, 507–514. doi: 10.1111/j.1469-7998.1996.tb05939.x. DOI

Ashford RW, Reid GDF and Wrangham RW (2000) Intestinal parasites of the chimpanzee Pan troglodytes in Kibale Forest, Uganda. Annals of Tropical Medicine and Parasitology 94, 173–179. doi: 10.1080/00034983.2000.11813526. PubMed DOI

Back H, Nyman A and Osterman Lind E (2013) The association between Anoplocephala perfoliata and colic in Swedish horses- – a case control study. Veterinary Parasitology 197, 580–585. doi: 10.1016/j.vetpar.2013.07.020. PubMed DOI

Baer JG (1927) Monographie des Cestodes de la famille des Anoplocephalidae. Bulletin biologique de France et de Belgique, Supplément 10, 1–241.

Beveridge I (1985a) The genus Bertiella (Cestoda: Anoplocephalidae) from Australasian mammals: new species, new records and redescriptions. Systematic Parasitology 7, 241–289. doi: 10.1007/BF00009995. DOI

Beveridge I (1985b) Three new species of Progamotaenia (Cestoda: Anoplocephalidae) from Australasian marsupials. Systematic Parasitology 7, 91–102. doi: 10.1007/BF00009812. DOI

Beveridge I (1994) Family Anoplocephalidae Cholodkovsky, 1902. In Khalil LF, Jones A and Bray RA (eds), Keys to the Cestode Parasites of Vertebrates. Oxfordshire, UK: CAB International, pp. 315–366.

Beveridge I, Shamsi S, Hu M, Chilton and NB and Gasser RB (2007) Genetic variation in the mitochondrial cytochrome c oxidase subunit 1 within Progamotaenia festiva (Cestoda: Anoplocephalidae) from macropodid marsupials. Parasitology 134, 1465–1476. doi: 10.1017/S0031182007002752. PubMed DOI

Bohórquez A, Meana A, Pato NF and Luzón M (2014) Coprologically diagnosing Anoplocephala perfoliata in the presence of A. magna. Veterinary Parasitology 204, 396–401. doi: 10.1016/j.vetpar.2014.04.023. PubMed DOI

Burgunder J, Pafčo B, Petrželková KJ, Modrý D, Hashimoto C and MacIntosh AJJ (2017) Complexity in behavioural organization and strongylid infection among wild chimpanzees. Animal Behaviour 129, 257–268. doi: 10.1016/j.anbehav.2017.06.002. DOI

Bush GK, Ikirezi M, Daconto G, Gray M and Fawcett K (2010) Assessing impacts from community conservation interventions around Parc National des Volcans, Rwanda. Technical Report, Dian Fossey Gorilla Fund International. 131 pp.

Chapman CA, Speirs ML, Gillespie TR, Holland T and Austad KM (2006) Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups. American Journal of Primatology 68, 397–409. doi: 10.1002/ajp.20233. PubMed DOI

Conn BC (1985) Scanning electron microscopy and histochemistry of embryonic envelopes of the porcupine tapeworm, Monoecocestus americanus (Cyclophyllidea: Anoplocephalidae). Canadian Journal of Zoology 63, 1194–1198.

Deplazes P, Eckert J, Mathis A, von Samson-Himmelstjerna G and Zahner H (eds) (2016) Parasitology in Veterinary Medicine. Wageningen, Netherlands: Wageningen Academic Publishers, p. 650.

Doležalová J (2018) Anoplocephalid tapeworms. In Modrý D, Pafčo B, Petrželková KJ and Hasegawa H (eds), Parasites of Apes an Atlas of Coproscopic Diagnostics. Frankfurt am Main, Germany: Edition Chimaira, pp. 126–129.

Doležalová J, Vallo P, Petrželková KJ, Foitová I, Nurcahyo W, Mudakikwa A, Hashimoto C, Jirků M, Lukeš J, Scholz T and Modrý D (2015) Molecular phylogeny of anoplocephalid tapeworms (Cestoda: Anoplocephalidae) infecting humans and non-human primates. Parasitology 142, 1278–1289. doi: 10.1017/S003118201500058X. PubMed DOI

Doležalová J, Pafčo B, Modrý D and Jirků-Pomajbíková K (2018) Parasite quantification. In Modrý D, Pafčo B, Petrželková KJ and Hasegawa H (eds), Parasites of Apes an Atlas of Coproscopic Diagnostics. Frankfurt am Main, Germany: Edition Chimaira, pp. 34–37.

Drakulovski P, Bertout S, Locatelli S, Butel C, Pion S, Mpoudi-Ngole E, Delaporte E, Peeters M and Mallieé M (2014) Assessment of gastrointestinal parasites in wild chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon. Parasitology Research 113, 2541–2550. doi: 10.1007/s00436-014-3904-y. PubMed DOI PMC

Drogemuller M, Beelitz P, Pfister K, Schnieder T and von Samson-Himmelstjerna G (2004) Amplification of ribosomal DNA of Anoplocephalidae: Anoplocephala perfoliata diagnosis by PCR as a pssible alternative to coprological methods. Veterinary Parasitology 124, 205–215. doi: 10.1016/j.vetpar.2004.07.012. PubMed DOI

Galán-Puchades MT, Vicent Fuentes M and Mas-Coma S (2000) Morphology of Bertiella studeri (Blanchard, 1891) sensu Stunkard (1940) (Cestoda: Anoplocephalidae) of human origin and a proposal of criteria for the specific diagnosis of bertiellosis. Folia Parasitologica 47, 23–28. doi: 10.14411/fp.2000.005. PubMed DOI

Gilardi KV, Gillespie TR, Leendertz FH, Macfie EJ, Travis DA, Whittier CA and Williamson EA (2015) Best Practice Guidelines for Health Monitoring and Disease Control in Great Ape Populations. Gland, Switzerland: UCN/SSC Primate Specialist Group. doi:10.2305/IUCN.CH.2015.SSC-OP.56.en. DOI

Gillespie TR, Greiner EC and Chapman CA (2004) Gastrointestinal parasites of the guenons of Western Uganda. Journal of Parasitology 90, 1356–1360. doi: 10.1645/GE-311R. PubMed DOI

Gillespie TR, Greiner EC and Chapman CA (2005) Gastrointestinal parasites of the colobus monkeys of Uganda. Journal of Parasitology 91, 569–573. doi: 10.1645/GE-434R. PubMed DOI

Hardman, LM, Haukisalmi V and Beveridge, I (2012) Phylogenetic relationships of the anoplocephaline cestodes of Australasian marsupials and resurrection of the genus Wallabicestus Schmidt, 1975. Systematic Parasitology 82, 49–63. doi: 10.1007/s11230-012-9346-y. PubMed DOI

Hastings BE, Gibbons LM and Williams JE (1992) Parasites of free ranging mountain gorillas: Survey and epidemiological factors. American Association of Zoo Veterinarians and American Association of Wildlife Veterinarians Annual Proceedings, pp. 301–302.

Haukisalmi V and Henttonen H (2000) Description and morphometric variability of Paranoplocephala serrata n. sp. (Cestoda: Anoplocephalidae) in collared lemmings (Dicrostonyx spp., Arvicolinae) from Arctic Siberia and North America. Systematic Parasitology 45, 219–231. doi: 10.1023/A:1006244331243. PubMed DOI

Haukisalmi V, Wickström LM, Hantula J and Henttonen H (2001) Taxonomy, genetic differentiation and Holarctic biogeography of Paranoplocephala spp. (Cestoda: Anoplocephalidae) in collared lemmings (Dicrostonyx; Arvicolinae). Biological Journal of the Linnean Society 74, 171–196. doi: 10.1006/bijl.2001.0570. DOI

Haukisalmi V, Wickström LM, Henttonen H, Hantula J and Gubány A (2004) Molecular and morphological evidence of multiple species within Paranoplocephala omphalodes (Cestoda: Anoplocephalidae) in Microtus voles (Arvicolinae). Zoologica Scripta 33, 277–290. doi: 10.1111/j.0300-3256.2004.00148.x. DOI

Haukisalmi V, Hardman LM, Hardman M, Rausch RL and Henttonen H (2008) Molecular systematics of the Holarctic Anoplocephaloides variabilis (Douthitt, 1915) complex, with the proposal of Microcephaloides n.g. (Cestoda: Anoplocephalidae). Systematic Parasitology 70, 15–26. doi: 10.1007/s11230-008-9129-7. PubMed DOI

Haukisalmi V, Henttonen H, Hardman LM, Hardman M, Laakkonen J, Murueva G, Niemimaa J, Shulunov S and Vapalahti O (2009) Review of tapeworms of rodents in the Republic of Buryatia, with emphasis on anoplocephalid cestodes. Zookeys 8, 1–18. doi: 10.3897/zookeys.8.58. DOI

Hickey JR, Granjon AC, Vigilant L, Eckardt W, Gilardi KV, Cranfield M, Musana A, Masozera AB, Babaasa D, Ruzigandekwe F and Robbins MM (2019) Virunga 2015-2016 Surveys: monitoring mountain gorillas, other select mammals, and illegal activities. GVTC, IGCP & partners, Kigali, Rwanda. 45 pp. Available at https://igcp.org/content/uploads/2020/09/Virunga-Census-2015-2016-Final-Report-2019-with-French-summary-2019_04_24.pdf.

Huffman MA, Gotoh S, Turner LA, Hamai M and Yoshida K (1997) Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38, 111–125. doi: 10.1007/BF02382002. DOI

Jirků-Pomajbíková K and Hůzová Z (2018) Coproscopic examination techniques. In Modrý D, Pafčo B, Petrželková KJ and Hasegawa H (eds), Parasites of Apes an Atlas of Coproscopic Diagnostics. Frankfurt am Main, Germany: Edition Chimaira, pp. 22–28.

Kalema-Zikusoka G, Rothman JM and Fox MT (2005) Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Primates 46, 59–63. doi: 10.1007/s10329-004-0103-y. PubMed DOI

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A and Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Kooriyama T, Hasegawa H, Shimozuru M, Tsubota T, Nishida T and Iwaki T (2012) Parasitology of five primates in Mahale Mountains National Park, Tanzania. Primates 53, 365–375. doi: 10.1007/s10329-012-0311-9. PubMed DOI

Krief S, Huffman MA, Sévenet T, Guillot J, Bories C, Hladik CM and Wrangham RW (2005) Noninvasive monitoring of the health of Pan troglodytes schweinfurthii in the Kibale National Park, Uganda. International Journal of Primatology 26, 467–490. doi: 10.1007/s10764-005-2934-9. DOI

Letunic I and Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49, W293–W296. doi: 10.1093/nar/gkab301. PubMed DOI PMC

Lilly AA, Mehlman PT and Doran D (2002) Intestinal parasites in gorilla, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 23, 555–573. doi: 10.1023/A:1014969617036. DOI

Masi S, Chauffour S, Bain O, Todd A, Guillot J and Krief S (2012) Seasonal effects on great ape health: a case study of wild chimpanzees and western gorillas. PLoS ONE 7, e49805. doi: 10.1371/journal.pone.0049805. PubMed DOI PMC

McLennan MR and Huffman MA (2012) High frequency of leaf swallowing and its relationship to intestinal parasite expulsion in “village” chimpanzees at Bulindi, Uganda. American Journal of Primatology 74, 642–650. doi: 10.1002/ajp.22017. PubMed DOI

McLennan MR, Hasegawa H, Bardi M and Huffman MA (2017) Gastrointestinal parasite infections and self-medication in wild chimpanzees surviving in degraded forest fragments within an agricultural landscape mosaic in Uganda. PLoS ONE 12, e0180431. doi: 10.1371/journal.pone.0180431. PubMed DOI PMC

Meana A, Pato NF, Martín R, Mateos A, Pérez-García J and Luzón M (2005) Epidemiological studies on equine cestodes in Central Spain: infection pattern and population dynamics. Veterinary Parasitology 130, 233–240. doi: 10.1016/j.vetpar.2005.03.040. PubMed DOI

Mezerova J, Koudela B and Vojtkova M (2007) Equine colic caused by tape worms – 5 clinical case reports. Praktische Tierarzt 88, 26–27.

Minh BQ, Nguyen MAT and von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30, 1188–1195. doi: 10.1093/molbev/mst024. PubMed DOI PMC

Mudakikwa AB, Cranfield MR, Sleeman JM and Eilenberger U (2001) Clinical medicine, preventive health care and research on mountain gorillas in the Virunga Volcanoes region. In Robbins MM, Sicotte P and Stewart KJ (eds), Mountain Gorillas. Cambridge, UK: Cambridge University Press, pp. 341–360. doi: 10.1017/CBO9780511661631.014. DOI

Muehlenbein MP (2005) Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. American Journal of Primatology 65, 167–179. doi: 10.1002/ajp.20106. PubMed DOI

Muhangi D, Gardiner CH, Ojok L, Cranfield MR, Gilardi KVK, Mudakikwa AB and Lowenstine LJ (2021) Pathological lesions of the digestive tract in free-ranging mountain gorillas (Gorilla beringei beringei). American Journal of Primatology 83, e23290. doi: 10.1002/ajp.23290. PubMed DOI

Mul IF, Paembonan W, Singleton I, Wich SA and van Bolhuis HG (2007) Intestinal parasites of free-ranging, semicaptive and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology 28, 407–420. doi: 10.1007/s10764-007-9119-7. DOI

Naz S, Arooj S, Ali Z and Farooq Z (2021) Potential consequences of captivity and environmental pollution in endoparasitic prevalence in different antelopes kept at wildlife parks. Environmental Science and Pollution Research 28, 16308–16313. doi: 10.1007/s11356-020-11561-x. PubMed DOI

Nielsen MK, Mittel L, Grice A, Erskine M, Graves E, Vaala W, Tully RC, French DD, Bowman R and Kaplan RM (2019) AAEP Internal Parasite Control Guidelines. American Association of Equine Practitioners. Available at https://aaep.org/document/internal-parasite-control-guidelines (accessed 17 April 2023).

Nybelin O (1927) Anoplocephala gorillae n. sp. Arkiv Zoologie 19B, 1–3.

Owiunji I, Nkuutu D, Kujirakwinja D, Liengola I, Plumptre A, Nsanzurwimo A, Fawcett K, Gray M and Mcneilage A (2005) The biodiversity of the Virunga Volcanoes. Technical Report, Wildlife Conservation Society, New York. 97 pp. Available at https://library.wcs.org/doi/ctl/view/mid/33065/pubid/DMX1163000000.aspx

Pafčo B (2018) Parasites of Gorillas. In Modrý D, Pafčo B, Petrželková KJ and Hasegawa H (eds), Parasites of Apes an Atlas of Coproscopic Diagnostics. Frankfurt am Main, Germany: Edition Chimaira, pp. 64–70.

Pafčo B, Benavides JA, Pšenková-Profousová I, Modrý D, Červená B, Shutt KA, Hasegawa H, Fuh T, Todd AF and Petrželková KJ (2017) Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas? Parasitology Research 116, 3401–3410. doi: 10.1007/s00436-017-5667-8. PubMed DOI

Petrželková KJ, Uwamahoro C, Pafčo B, Červená B, Samaš P, Mudakikwa A, Muvunyi R, Uwingeli P, Gilardi K, Nziza J, Noheri JB, Eckardt W, Ndagijimana F, Ssebide B, Okwirokello R, Nizeyimana F, Syaluha EK, Nzayisenga G, Girón LF, Bahizi M, Ntwari EA, Lukusa J-P, Tumushime JC, Mangura D, Mapilanga J, Kalonji A, Aruho R, Stryková A, Tehlarová Z, Cameira R, Lowenstine L, Šlapeta J, Romportl D, Ferrari N, Cranfield M and Modrý D (2021) Heterogeneity in patterns of helminth infections across populations of mountain gorillas (Gorilla beringei beringei). Scientific Reports 11, 10869. doi: 10.1038/s41598-021-89283-4. PubMed DOI PMC

Petrželková KJ, Samaš P, Romportl D, Uwamahoro C, Červená B, Pafčo B, Prokopová T, Cameira R, Granjon AC, Shapiro A, Bahizi M, Nziza J, Noheri JB, Syaluha EK, Eckardt W, Ndagijimana F, Šlapeta J, Modrý D, Gilardi K, Muvunyi R, Uwingeli P, Mudakikwa A, Mapilanga J, Kalonji A, Hickey JR and Cranfield M (2022) Ecological drivers of helminth infection patterns in the Virunga Massif mountain gorilla population. International Journal for Parasitology: Parasites and Wildlife 17, 174–184. doi: 10.1016/j.ijppaw.2022.01.007. PubMed DOI PMC

Rasambainarivo FT, Junge RE and Lewis RJ (2014) Biomedical evaluation of Verreaux's sifaka (Propithecus verreauxi) from Kirindi Mitea National Park in Madagascar. Journal of Zoo and Wildlife Medicine 45, 247–255. doi: 10.1638/2013-0038R1.1. PubMed DOI

Redmond I (1983) Summary of parasitological research, November 1976 to April 1978. In Fossey D (ed), Gorillas in the Mist. London, UK: Hodder and Stoughton, pp. 271–286.

Rijsman LH, Monkelbaan JF and Kusters JG (2016) Clinical consequences of polymerase chain reaction-based diagnosis of intestinal parasitic infections: PCR-based diagnosis of enteric protozoa. Journal of Gastroenterology and Hepatology 31, 1808–1815. 10.1111/jgh.13412 PubMed DOI

Rothman JM, Pell AN and Bowman DD (2008) Host-parasite ecology of the helminths in mountain gorillas. The Journal of Parasitology 94, 834–840. doi: 10.1645/GE-1454.1. PubMed DOI

Sá RM, Petrášová J, Pomajbíková K, Profousová I, Petrželková KJ, Sousa C, Cable J, Bruford MW and Modrý D (2013) Gastrointestinal symbionts of chimpanzees in Cantanhez National Park, Guinea-Bissau with respect to habitat fragmentation. American Journal of Primatology 75, 1032–1041. doi: 10.1002/ajp.22170. PubMed DOI

Sapp SGH and Bradbury RS (2020) The forgotten exotic tapeworms: a review of uncommon zoonotic Cyclophyllidea. Parasitology 147, 533–558. doi: 10.1017/S003118202000013X. PubMed DOI PMC

Schuster R (1991) [Morphometric analysis of an Anoplocephala perfoliata population]. Angewandte Parasitologie 32, 105–111. PubMed

Servián A, Zonta ML, Cociancic P, Falcone A, Ruybal P, Capasso S and Navone GT (2020) Morphological and molecular characterization of Bertiella sp. (Cestoda, Anoplocephalidae) infection in a human and howler monkeys in Argentina. Parasitology Research 119, 1291–1300. doi: 10.1007/s00436-020-06615-5. PubMed DOI

Sharma S, Lyngdoh D, Roy B and Tandon V (2016) Molecular phylogeny of Cyclophyllidea (Cestoda: Eucestoda): an in-silico analysis based on mtCOI gene. Parasitology Research 115, 3329–3335. doi: 10.1007/s00436-016-5092-4. PubMed DOI

Shaw DJ, Grenfell BT and Dobson AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610. doi: 10.1017/S0031182098003448. PubMed DOI

Sinayitutse E, Modry D, Slapeta J, Nyiramana A, Mudakikwa A, Muvunyi R and Eckardt W (2021) Daily defecation outputs of mountain gorillas (Gorilla beringei beringei) in the Volcanoes National Park, Rwanda. Primates 62, 311–320. doi: 10.1007/s10329-020-00874-7. PubMed DOI

Sleeman JM, Meader LL, Mudakikwa AB, Foster JW and Patton S (2000) Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National Des Volcans, Rwanda. Journal of Zoo and Wildlife Medicine 31, 322–328. doi: 10.1638/1042-7260(2000)031[0322:GPOMGG]2.0.CO;2. PubMed DOI

Stunkard WH (1962) The organization, ontogeny, and orientation of the Cestoda. The Quarterly Review of Biology 37, 23–34. doi: 10.1086/403568. DOI

Tenora F, Koubková B and Feliu C (2002) Redescription of Andrya cuniculi (Blanchard, 1891) (Cestoda: Anoplocephalidae), a parasite of Oryctolagus cuniculus (Lagomorpha) in Spain. Folia Parasitologica 49, 50–54. doi: 10.14411/fp.2002.011. PubMed DOI

Tomczuk K, Kostro K, Szczepaniak KO, Grzybek M, Studzińska M, Demkowska-Kutrzepa M and Roczeń-Karczmarz M (2014) Comparison of the sensitivity of coprological methods in detecting Anoplocephala perfoliata invasions. Parasitology Research 113, 2401–2406. doi: 10.1007/s00436-014-3919-4. PubMed DOI PMC

Traversa D, Fichi G, Campigli M, Rondolotti A, Iorio R, Proudman CJ, Pellegrini D and Perrucci SA (2008) Comparison of coprological, serological and molecular methods for the diagnosis of horse infection with Anoplocephala perfoliata (Cestoda, Cyclophyllidea). Veterinary Parasitology 152, 271–277. doi: 10.1016/j.vetpar.2007.12.032. PubMed DOI

Trifinopoulos J, Nguyen LT, von Haeseler A and Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44, W232–W235. doi: 10.1093/nar/gkw256. PubMed DOI PMC

Vimalraj PG and Jayathangaraj MG (2015) Endoparasitic infections in free-ranging Asiatic elephants of Mudumalai and Anamalai Wildlife Sanctuary. Journal of Parasitic Diseases 39, 474–476. doi: 10.1007/s12639-013-0375-5. PubMed DOI PMC

Vlčková K, Pafčo B, Petrželková KJ, Modrý D, Todd A, Yeoman CJ, Torralba M, Wilson BA, Stumpf RM, White BA, Nelson KE, Leigh SR and Gomez A (2018) Relationships between gastrointestinal parasite infections and the faecal microbiome in free-ranging western lowland gorillas. Frontiers in Microbiology 9, 1202. doi: 10.3389/fmicb.2018.01202. PubMed DOI PMC

Wickström LM, Haukisalmi V, Varis S, Hantula J and Henttonen H (2005) Molecular phylogeny and systematics of anoplocephaline cestodes in rodents and lagomorphs. Systematic Parasitology 62, 83–99. doi: 10.1007/s11230-005-5488-5. PubMed DOI

Williamson R, Beveridge I and Gasser R (1998) Coprological methods for the diagnosis of Anoplocephala perfoliata infection of the horse. Australian Veterinary Journal 76, 618–621. doi: 10.1111/j.1751-0813.1998.tb10242.x. PubMed DOI

Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Read AF and Skorping A (2001) Heterogeneities in macroparasite infections: patterns and processes. In Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H and Dobson AP (eds), The Ecology of Wildlife Diseases. Oxford, UK: Oxford University Press, pp. 6–44.

Wong SS, Fung KS, Chau S, Poon RW, Wong SC and Yuen KY (2014) Molecular diagnosis in clinical parasitology: when and why? Experimental Biology and Medicine 239, 1443–1460. doi: 10.1177/1535370214523880. PubMed DOI

Wrangham RW (1995) Relationship of chimpanzee leaf-swallowing to a tapeworm infection. American Journal of Primatology 37, 297–303. doi: 10.1002/ajp.1350370404. PubMed DOI