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Abstract
Tortoises are kept as pets in some homes and as side attraction in zoological gardens, but their usefulness could be limited by ectoparasite infestation. Ectoparasites cause harmful effects on their hosts, sometimes with high morbidity and mortality. Despite this, little attention has been paid to ectoparasite infestation in tortoises with potential extinction threat. Study was aimed at determining the presence and prevalence of tick infestation on African hinge-back tortoises (AHT) and evaluate their possible roles in the transmission of Haemogregarines, a common heamoparasites in Kinixys belliana and Kinixys homeana (African bell hinge-back and home hinge-back tortoises) obtained from major wildlife markets in Ibadan, Nigeria. In total, 120 tortoises (70 K. belliana and 50 K homeana) purchased at wildlife markets over a year during rainy and dry seasons were screened for ectoparasites but only ticks were found. Ticks were detached from tortoises, using a pair of forceps. Mean prevalence for each Kinixys belliana and Kinixys homeana group was determined and ticks were identified. The effects of sex, species, and season on parasite prevalence were evaluated using the Mann–Whitney U test and Pearson’s chi-square test. Data were quantified using correlation coefficient test. Level of significance was taken as 5%. Hard ticks Amblyomma species) were the only ectoparasites found on 54.0% of tortoises. Higher prevalence of Amblyomma was observed in Kinixys belliana (55.7%) than Kinixys homeana (52.0%). Male tortoises recorded higher prevalence (60.7%) than females (48.4%). Overall prevalence during rainy season was 55.0 and 53.3% in dry season. A comprehensive preventive health programme aimed at controlling ectoparasites such as ticks on tortoises in zoological gardens and in private facilities is hereby recommended.
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References
- Basu, A.K. Basu, M. Adesiyun, A.A. (2012). A review on ticks (Acari: Ixodidae: Ixodidae, Argasidae), associated pathogens and diseases of Trinidad and Tobago. Acarologia, 52 (1): 39–50. 10.1051/acarologia/20122034
- Cook, C.A. Netherlands, E.C. and Smit, N.J. (2015) First Hemolivia from southern Africa: reassigningchelonianHaemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) to Hemolivia (Adeleorina: Karyolysidae), African Zoology, 50: 2, 165-173. 10.1080/15627020.2015.1044467
- Cook, A.C. Lawton, P.S. Davies, J.A. and Smith, J.N. (2014). Reassignment of the land tortoise haemogregarine Haemogregarina fitzsimonsi Dias 1953 (Adeleorina: Haemogregarinidae) to the genus Hepatozoon Miller 1908 (Adeleorina: Hepatozoidae) based on parasite morphology, life cycle and phylogenetic analysis of 18S RNA sequence fragments. Parasitology, 141: 1611–1620. 10.1017/S003118201400081X
- Estrada-Pena, A., Mihalca, A.D. and Petney, T.N. 2017. Ticks of Europe and North. Africa-A Guide to Species Identification. Springer International Publishing: Cham, Switzerland. pp. 404. ISBN: 9783319637594 (alk. paper)
- Garces-Restrepro, M.F. Giraldo, A. Carr, J.L. and Brown, L.D. (2013). Turtle ectoparasites from the Pacific coastal region of Columbia. Biota Neotropica, 13: 74-79. 10.1590/S1676-06032013000300009
- Gibbon, J.W. Scot, D.E. Ryan, T.J. Bullman, K.A. Tuberville, T.D. Mett, B.S. Greene, J.L. Mills, T. Leiden, Y. Poppy, S.and Winne, C.T. (2000). The global decline of reptile’s déjà vu amphibians. Bioscience, 50: 653-666.
- Houwen, B. (2002). Blood film preparation and staining procedures. Clinics in Laboratory Medicine, 22 (1), 1-14. 10.1016/s0272-2712(03)00064-7
- Isaac, J.L. (2005). Life history and demographics of an island possum. Australian Journal of Zoology, 53: 195 – 203. 10.1071/ZO05018
- Haklova-Kocikova, B., Adriana, H., Igor, M., Karol, R., David, J. H. Gabor, F., Piotr, T. Natalia, K., Beata, M. and Majlathova, V. (2014). Morphological and molecular characterization of Karyolysus – a neglected but common parasite infecting some European lizards. Parasites and Vectors, 7:555. 10.1186/s13071-014-0555-x
- Horak, I.G. McKay, I.J. Henen, B.T. Heyne, H. Hofmeyr, M.D. and De Villiers, A.L. (2006). Parasites of domestic and wild animals in South Africa. XLVII. Ticks of tortoises and other reptiles. Onderstepoort Journal of Veterinary Research, 73(3):215–227. 10.4102/ojvr.v73i3.148
- Jacobson, E.R. (1994). Causes of Mortality and Diseases in Tortoises: A Review. Journal of Zoo and Wildlife Medicine, 25: pp. 2-17.
- Kao, N.W. Hill, N.J. Burnett, L. and Deane, E.M. (2014). Ectoparasite infestation patterns, haematology and serum biochemistry of urban-dwelling common brushtail possums. Wildlife Biology, 20: 206-216. http://www.bioone.org/doi/full/10.2981/wlb.00027
- Kar, S. Yılmazer, N. Midilli, K. Ergin, S. Alp, H. and Gargılı, A. (2011). Presence of the zoonotic Borrelia burgdorferi sl. and Rickettsia spp. in the ticks from wild tortoises and hedgehogs. Journal of Marmara University Institute of Health Sciences. 1, 166–170
- Kirecci, E. Ozer, A. Balkaya, I. Taniş, H. and Deveci, S. (2013). Identification of Ticks on Tortoises (Testudo graeca) and Investigation of Some Pathogens in these Ticks in Kahramanmaraş, Turkey. KSÜ Doğa Bilimleri Dergisi, 16 (1). 10.18016/ksujns.67594
- Knapp, C.R. Perez‐Heydrich, C. Zachariah, T.T. Schnelle, N. Buckner, S.D. Lattin, C.R. and Romero, M.L. (2019). Host sex, size, and hemoparasite infection influence the effects of ectoparasitic burdens on free‐ranging iguanas. Ecology and Evolution, 9: 1946-1956. https://doi.org/10.1002/ece3.4887
- Laghzaoui, E.M, Bouazza, A, Abbad, A, El Mouden, E.H (2022). Cross-sectional study of ticks in the vulnerable free-living spur-thighed tortoise Testudo graeca (Testudines: Testudinidae) from Morocco. International Journal of Acarology, 48(1):76–83. 10.1080/01647954.2021.2024595
- Latha, B.R and Azhahianambi P. (2013). Training manual on collection, processing and identification of ticks. Department of Veterinary Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai, India, 69 pp. bhaskaranravilatha@tanuvas.ac.in
- Luiselli, L. and Diagne, T. (2013). Kinixys homeana Bell 1827 – Home's Hinge-Back Tortoise. In A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, J. B. Iverson, & R. A. Mittermeier (Eds.), Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs (No. 5, pp. 070.1–070.10). Chelonian Research Foundation. https://doi.org/10.3854/crm.5.070.homeana.v1.2013
- McArthur, S. (2004). Problem-solving approach to common diseases of terrestrial and semi-aquatic chelonians. In: McArthur, S., Wilkinson, R., Meyer, J., Innis, C.J., Hernandez-Divers, S. (Eds.), Medicine and Surgery of Tortoises and Turtles (pp. 309-377). Blackwell Publishing, Oxford, UK. ISBN: 978-1-4051-0889-8
- Mofokeng, L.S, Netherlands, E.C, Smit, N.J and Cook, C.A. (2024) Developmental stages and molecular phylogeny of Hepatozoon fitzsimonsi (Dias 1953) (Adeleorina: Hepatozoidae) in tortoises Stigmochelys pardalis (Cryptodira: Testudinidae) and ticks of the genus Amblyomma (Acari: Ixodidae) from South Africa. Parasites and Vectors, 17(1):314. 10.1186/s13071-024- 06398-z
- Mofokeng, L. S., Smit, N. J. and Cook, C. A. (2022). Molecular detection of tick-borne bacteria from Amblyomma (Acari: Ixodidae) ticks collected from reptiles in South Africa. Microorganisms, 10 (10), 1923. 10.3390/microorganisms10101923
- Molla, S.H., Brandyopadhyay, P.K. and Gurelli, G. (2015). Description of new Haemogregarine: Haemogregarina sundarbanesisn.sp (Apicomplexa: Haemogregarinidae) from mud turtle of Sundarban Region, West Bengal, India. Turkish Journal of Parasitology, 39:131-134. 10.5152/tpd.2015.3924
- Norte, A. C. Lobata, D. N. C. Braga, E. Antonini, Y. Lacorte, G. Goncalves, M. and Ramos, J. A. (2013). Do ticks and Borrelia burgdorferi s. l. constitute a burden to birds? Parasitology Research, 112:1903–1912. 10.1007/s00436-013-3343-1
- Oduntan, O.O. Akinyemi A. Ojo, A. Ogunyode, O. and Adesina, O. (2012). Survey of Wild Animals Used in Zoo-therapy at Ibadan, Oyo State, Nigeria. International Journal of Molecular Zoology,2: (9) 70-73. 10.5376/ijmz.2012.02.0009
- Ozvegy, J. Marinkovic, D. Vucicevic, M. Gajic, B. Stevanovic, J. Krnjaic, A. and Kovacevic, S. (2015). Cytological and Molecular identification of Haemogregarina Stepanowi in blood samples of the European pond turtle (Emys Orbicularis) from Quarantine at Belgrade Zoo. Acta Veterinaria-Beograd, 65 (4), 443-453. 10.1515/acve-2015-0037
- Salkeld, D.J. and Schwarzkopf, L. (2005). Epizootiology of blood parasites in an Australian lizard: a mark-recapture study of a natural population. International Journal for Parasitology, 35: 11–18. 10.1016/j.ijpara.2004.09.005
- Segura, A. Rafael, M. Vaz-Rodrigues, R. Rodríguez, O. Gortázar, C. and de la Fuente, J. (2023). Tick infestation in spur-thighed tortoise population: a pilot study for unraveling epidemiological patterns and demographic consequences. Experimental and Applied Acarology, 91(4), 661–679. 10.1007/s10493-023-00863-7
- Stacy, N.I. Alleman, A.R. and Sayler, K.A. (2011). Diagnostic haematology of reptiles. Clin. Lab. Med. 31:87-108. 10.1016/j.cll.2010.10.006
- Tavassoli, E. Asiabi, N.R. and Tavassoli, M. (2007). Hyalomma aegyptium on Spur-thighed Tortoise (Testudo graeca) in Urmia Region West Azerbaijan, Iran. Iranian Journal of Parasitology, 2: 40-47. Corpus ID: 86748072
- Visser, M., Rehbein, S. and Wiedemann, C. (2001). Species of flea (Siphonaptera) infesting pets and hedgehogs in Germany. Journal of Veterinary Medicine Series B, 48(3), 197-202. 10.1046/j.1439-0450.2001.00445.x
- Yalew A.S. (2022). Review on Importance, Diagnosis and Control Methods of Ectoparasites. International Journal of Advanced Research in Biological Sciences, 9(9): 81-92 DOI: http://dx.doi.org/10.22192/ijarbs.2022.09.09.009
- Zhang, E.Y., Kalmath, P., Abernathy, H.A., Giandomenico, D.A., Nolan, M.S., Reiskind, M.H. and Boyce, R.M. (2024). Rickettsia africae infections in sub-Saharan Africa: A systematic literature review of epidemiological studies and summary of case reports. Tropical Medicine and International Health, 29(7), 541-583. 10.1111/tmi.14002
References
Basu, A.K. Basu, M. Adesiyun, A.A. (2012). A review on ticks (Acari: Ixodidae: Ixodidae, Argasidae), associated pathogens and diseases of Trinidad and Tobago. Acarologia, 52 (1): 39–50. 10.1051/acarologia/20122034
Cook, C.A. Netherlands, E.C. and Smit, N.J. (2015) First Hemolivia from southern Africa: reassigningchelonianHaemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) to Hemolivia (Adeleorina: Karyolysidae), African Zoology, 50: 2, 165-173. 10.1080/15627020.2015.1044467
Cook, A.C. Lawton, P.S. Davies, J.A. and Smith, J.N. (2014). Reassignment of the land tortoise haemogregarine Haemogregarina fitzsimonsi Dias 1953 (Adeleorina: Haemogregarinidae) to the genus Hepatozoon Miller 1908 (Adeleorina: Hepatozoidae) based on parasite morphology, life cycle and phylogenetic analysis of 18S RNA sequence fragments. Parasitology, 141: 1611–1620. 10.1017/S003118201400081X
Estrada-Pena, A., Mihalca, A.D. and Petney, T.N. 2017. Ticks of Europe and North. Africa-A Guide to Species Identification. Springer International Publishing: Cham, Switzerland. pp. 404. ISBN: 9783319637594 (alk. paper)
Garces-Restrepro, M.F. Giraldo, A. Carr, J.L. and Brown, L.D. (2013). Turtle ectoparasites from the Pacific coastal region of Columbia. Biota Neotropica, 13: 74-79. 10.1590/S1676-06032013000300009
Gibbon, J.W. Scot, D.E. Ryan, T.J. Bullman, K.A. Tuberville, T.D. Mett, B.S. Greene, J.L. Mills, T. Leiden, Y. Poppy, S.and Winne, C.T. (2000). The global decline of reptile’s déjà vu amphibians. Bioscience, 50: 653-666.
Houwen, B. (2002). Blood film preparation and staining procedures. Clinics in Laboratory Medicine, 22 (1), 1-14. 10.1016/s0272-2712(03)00064-7
Isaac, J.L. (2005). Life history and demographics of an island possum. Australian Journal of Zoology, 53: 195 – 203. 10.1071/ZO05018
Haklova-Kocikova, B., Adriana, H., Igor, M., Karol, R., David, J. H. Gabor, F., Piotr, T. Natalia, K., Beata, M. and Majlathova, V. (2014). Morphological and molecular characterization of Karyolysus – a neglected but common parasite infecting some European lizards. Parasites and Vectors, 7:555. 10.1186/s13071-014-0555-x
Horak, I.G. McKay, I.J. Henen, B.T. Heyne, H. Hofmeyr, M.D. and De Villiers, A.L. (2006). Parasites of domestic and wild animals in South Africa. XLVII. Ticks of tortoises and other reptiles. Onderstepoort Journal of Veterinary Research, 73(3):215–227. 10.4102/ojvr.v73i3.148
Jacobson, E.R. (1994). Causes of Mortality and Diseases in Tortoises: A Review. Journal of Zoo and Wildlife Medicine, 25: pp. 2-17.
Kao, N.W. Hill, N.J. Burnett, L. and Deane, E.M. (2014). Ectoparasite infestation patterns, haematology and serum biochemistry of urban-dwelling common brushtail possums. Wildlife Biology, 20: 206-216. http://www.bioone.org/doi/full/10.2981/wlb.00027
Kar, S. Yılmazer, N. Midilli, K. Ergin, S. Alp, H. and Gargılı, A. (2011). Presence of the zoonotic Borrelia burgdorferi sl. and Rickettsia spp. in the ticks from wild tortoises and hedgehogs. Journal of Marmara University Institute of Health Sciences. 1, 166–170
Kirecci, E. Ozer, A. Balkaya, I. Taniş, H. and Deveci, S. (2013). Identification of Ticks on Tortoises (Testudo graeca) and Investigation of Some Pathogens in these Ticks in Kahramanmaraş, Turkey. KSÜ Doğa Bilimleri Dergisi, 16 (1). 10.18016/ksujns.67594
Knapp, C.R. Perez‐Heydrich, C. Zachariah, T.T. Schnelle, N. Buckner, S.D. Lattin, C.R. and Romero, M.L. (2019). Host sex, size, and hemoparasite infection influence the effects of ectoparasitic burdens on free‐ranging iguanas. Ecology and Evolution, 9: 1946-1956. https://doi.org/10.1002/ece3.4887
Laghzaoui, E.M, Bouazza, A, Abbad, A, El Mouden, E.H (2022). Cross-sectional study of ticks in the vulnerable free-living spur-thighed tortoise Testudo graeca (Testudines: Testudinidae) from Morocco. International Journal of Acarology, 48(1):76–83. 10.1080/01647954.2021.2024595
Latha, B.R and Azhahianambi P. (2013). Training manual on collection, processing and identification of ticks. Department of Veterinary Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai, India, 69 pp. bhaskaranravilatha@tanuvas.ac.in
Luiselli, L. and Diagne, T. (2013). Kinixys homeana Bell 1827 – Home's Hinge-Back Tortoise. In A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, J. B. Iverson, & R. A. Mittermeier (Eds.), Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs (No. 5, pp. 070.1–070.10). Chelonian Research Foundation. https://doi.org/10.3854/crm.5.070.homeana.v1.2013
McArthur, S. (2004). Problem-solving approach to common diseases of terrestrial and semi-aquatic chelonians. In: McArthur, S., Wilkinson, R., Meyer, J., Innis, C.J., Hernandez-Divers, S. (Eds.), Medicine and Surgery of Tortoises and Turtles (pp. 309-377). Blackwell Publishing, Oxford, UK. ISBN: 978-1-4051-0889-8
Mofokeng, L.S, Netherlands, E.C, Smit, N.J and Cook, C.A. (2024) Developmental stages and molecular phylogeny of Hepatozoon fitzsimonsi (Dias 1953) (Adeleorina: Hepatozoidae) in tortoises Stigmochelys pardalis (Cryptodira: Testudinidae) and ticks of the genus Amblyomma (Acari: Ixodidae) from South Africa. Parasites and Vectors, 17(1):314. 10.1186/s13071-024- 06398-z
Mofokeng, L. S., Smit, N. J. and Cook, C. A. (2022). Molecular detection of tick-borne bacteria from Amblyomma (Acari: Ixodidae) ticks collected from reptiles in South Africa. Microorganisms, 10 (10), 1923. 10.3390/microorganisms10101923
Molla, S.H., Brandyopadhyay, P.K. and Gurelli, G. (2015). Description of new Haemogregarine: Haemogregarina sundarbanesisn.sp (Apicomplexa: Haemogregarinidae) from mud turtle of Sundarban Region, West Bengal, India. Turkish Journal of Parasitology, 39:131-134. 10.5152/tpd.2015.3924
Norte, A. C. Lobata, D. N. C. Braga, E. Antonini, Y. Lacorte, G. Goncalves, M. and Ramos, J. A. (2013). Do ticks and Borrelia burgdorferi s. l. constitute a burden to birds? Parasitology Research, 112:1903–1912. 10.1007/s00436-013-3343-1
Oduntan, O.O. Akinyemi A. Ojo, A. Ogunyode, O. and Adesina, O. (2012). Survey of Wild Animals Used in Zoo-therapy at Ibadan, Oyo State, Nigeria. International Journal of Molecular Zoology,2: (9) 70-73. 10.5376/ijmz.2012.02.0009
Ozvegy, J. Marinkovic, D. Vucicevic, M. Gajic, B. Stevanovic, J. Krnjaic, A. and Kovacevic, S. (2015). Cytological and Molecular identification of Haemogregarina Stepanowi in blood samples of the European pond turtle (Emys Orbicularis) from Quarantine at Belgrade Zoo. Acta Veterinaria-Beograd, 65 (4), 443-453. 10.1515/acve-2015-0037
Salkeld, D.J. and Schwarzkopf, L. (2005). Epizootiology of blood parasites in an Australian lizard: a mark-recapture study of a natural population. International Journal for Parasitology, 35: 11–18. 10.1016/j.ijpara.2004.09.005
Segura, A. Rafael, M. Vaz-Rodrigues, R. Rodríguez, O. Gortázar, C. and de la Fuente, J. (2023). Tick infestation in spur-thighed tortoise population: a pilot study for unraveling epidemiological patterns and demographic consequences. Experimental and Applied Acarology, 91(4), 661–679. 10.1007/s10493-023-00863-7
Stacy, N.I. Alleman, A.R. and Sayler, K.A. (2011). Diagnostic haematology of reptiles. Clin. Lab. Med. 31:87-108. 10.1016/j.cll.2010.10.006
Tavassoli, E. Asiabi, N.R. and Tavassoli, M. (2007). Hyalomma aegyptium on Spur-thighed Tortoise (Testudo graeca) in Urmia Region West Azerbaijan, Iran. Iranian Journal of Parasitology, 2: 40-47. Corpus ID: 86748072
Visser, M., Rehbein, S. and Wiedemann, C. (2001). Species of flea (Siphonaptera) infesting pets and hedgehogs in Germany. Journal of Veterinary Medicine Series B, 48(3), 197-202. 10.1046/j.1439-0450.2001.00445.x
Yalew A.S. (2022). Review on Importance, Diagnosis and Control Methods of Ectoparasites. International Journal of Advanced Research in Biological Sciences, 9(9): 81-92 DOI: http://dx.doi.org/10.22192/ijarbs.2022.09.09.009
Zhang, E.Y., Kalmath, P., Abernathy, H.A., Giandomenico, D.A., Nolan, M.S., Reiskind, M.H. and Boyce, R.M. (2024). Rickettsia africae infections in sub-Saharan Africa: A systematic literature review of epidemiological studies and summary of case reports. Tropical Medicine and International Health, 29(7), 541-583. 10.1111/tmi.14002
