Cross-sectional study of ticks in the vulnerable free-living spur-thighed tortoise Testudo graeca (Testudines: Testudinidae) from Morocco

References

• Akveran GA, Karasartova D, Keskin A, Comba A, Celebi B, Mumcuoglu KY, Taylan-ozkan A. 2020. Bacterial and protozoan agents found in Hyalomma aegyptium (L., 1758) (Ixodida: ixodidae) Collected from Testudo graeca L., 1758 (Reptilia: testudines) in Corum province of Turkey. Ticks and Tick-borne Diseases. 11:101458.
   PubMed Web of Science ®Google Scholar
• Amo L, Fargallo JA, Martínez-Padilla J, Millán J, López P, Martín J. 2005. Prevalence and intensity of blood and intestinal parasites in a field population of a Mediterranean lizard, Lacerta lepida. Parasitology Research. 96:413–417.
   PubMed Web of Science ®Google Scholar
• Amo L, López P, Martín J. 2004. Prevalence and intensity of haemogregarinid blood parasites in a population of the Iberian rock lizard, Lacerta monticola. Parasitology Research. 94:290–293.
   PubMed Web of Science ®Google Scholar
• Auliya M, Altherr S, Ariano-Sanchez D, Baard EH, Brown C, Brown RM, Cantu JC, Gentile G, Gildenhuys P, Henningheim E, et al. 2016. Trade in live reptiles, its impact on wild populations, and the role of the European market. Biological Conservation. 204:103–119.
   Web of Science ®Google Scholar
• Bailly-Choumara H, Morel PC, Rageau J. 1976. Sommaire des données actuelles sur les tiques du Maroc (Acari, ixodoidea). Bulletin de l’Institut Scientifique. 1:101–117.
   Google Scholar
• Barnard S, Durden L. 2000. A veterinary guide to the parasites of reptiles. vol. 2, Arhropods (Excluding Mites). Malabar (Florida): Krieger Publishing Company. p. 1–298.
   Google Scholar
• Bayley JR, Highfield AC. 1996. Observations on ecological changes threatening a population of Testudo graeca graeca in the Souss Valley, Southern Morocco. Chelonian Conservation and Biology. 2:36–42.
   Google Scholar
• Ben Kaddour K, El Mouden EH, Slimani T, Bonnet X, Lagarde F. 2008. Sexual dimorphism in the Greek Tortoise: a test of the body shape hypothesis. Chelonian Conservation and Biology. 7:21–27.
   Web of Science ®Google Scholar
• Ben Kaddour K, Mouden EH EL, Slimani T, Lagarde F, Bonnet X. 2005. Dimorphisme sexuel et cinétique de croissance et de maturation chez Testudo g. graeca, dans les Jbilets Centrales, Maroc. Revue d’Ecologie (Terre Vie). 60:265–278.
   Google Scholar
• Ben Kaddour K, Slimani T, El Mouden EH, Lagarde F, Bonnet X. 2006. Population structure, population density and individual catchability of Testudo graeca in the central Jbilets (Morocco). Vie et Milieu. 56:49–54.
   Web of Science ®Google Scholar
• Bergin D, Nijman V. 2014. Open, unregulated trade in wildlife in Morocco’s markets. Traffic Bulletin. 26:65–70.
   Google Scholar
• Bitam I, Kernif T, Harrat Z, Parola P, Raoult D. 2009. First detection of Rickettsia aeschlimannii in Hyalomma aegyptium from Algeria. Clinical Microbiology and Infection. 15:253–254.
   PubMed Web of Science ®Google Scholar
• Brianti E, F D-T, Giannetto S, Risitano A, Brucato G, Gaglio G, Otranto D. 2010. Risk for the introduction of exotic ticks and pathogens into Italy through the illegal importation of tortoises, Testudo graeca. Medical and Veterinary Entomology. 24:336–339.
   PubMed Web of Science ®Google Scholar
• Bull CM, Burzacott DA. 2006. The influence of parasites on the retention of long-term partnerships in the Australian sleepy lizard, Tiliqua rugosa. Oecologia. 146:675–680.
   PubMed Web of Science ®Google Scholar
• Chergui B, Rodríguez-Caro RC, Graciá E, Fahd S, Santos X. 2019. Population density of the spur-thighed tortoise Testudo graeca declines after fire in North-western Africa. PLoS One. 14:1–12.
   Web of Science ®Google Scholar
• Comas M. 2019. Body condition, sex and elevation in relation to mite parasitism in a high mountain gecko. Journal of Zoology 310:298–305.
   Web of Science ®Google Scholar
• David P, Heeb P. 2009. Parasites and sexual selection. Ecology and evolution of parasitism. Oxford: Oxford University Press; p. 31–47.
   Google Scholar
• Day MJ. 2011. One health: the importance of companion animal vector-borne diseases. Parasites and Vectors. 4:1–6.
   PubMed Web of Science ®Google Scholar
• de La Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE. 2008. Overview: ticks as vectors of pathogens that cause disease in humans and animals. Frontiers in Bioscience. 13:6938–6946.
   PubMed Web of Science ®Google Scholar
• Diaz-Paniagua C, Keller C, Andreu AC. 2001. Long-term demographic fluctuations of the spur-thighed tortoise Testudo graeca in SW Spain. Ecography. 24:707–721.
   Web of Science ®Google Scholar
• Domingos A, Antunes S, Borges L, Do Rosário VE. 2013. Approaches towards tick and tick-borne diseases control. Revista da Sociedade Brasileira de Medicina Tropical. 46:265–269.
   PubMed Web of Science ®Google Scholar
• Ehman KD, Scott ME. 2002. Female mice mate preferentially with non-parasitized males. Parasitology. 125:461–466.
   PubMed Web of Science ®Google Scholar
• El Mouden EH, Laghzaoui E-M, Elbahi AA, Abbad A. 2020. A case of massive infestation of a female Spurthighed tortoise Testudo graeca by blood-sucking ticks Hyalomma aegyptium (Acari: ixodidae). International Journal of Acarology. 46:63–65.
   Web of Science ®Google Scholar
• El Mouden EH, Slimani T, Ben Kaddour K, Lagarde F, Ouhammou A, Bonnet X. 2006. Testudo graeca graeca feeding ecology in an arid and overgrazed zone in Morocco. Journal of Arid Environments. 64:422–435.
   Web of Science ®Google Scholar
• Estrada-Peña A, Ayllón N, De La Fuente J. 2012. Impact of climate trends on tick-borne pathogen transmission. Frontiers in Physiology. 3:1–12.
   PubMed Web of Science ®Google Scholar
• Fritz U, Harris DJ, Fahd S, Rouag R, Martínez EG, Casalduero AG, Široký P, Kalboussi M, Jdeidi TB, Hundsdörfer AK. 2009. Mitochondrial phylogeography of Testudo graeca in the Western Mediterranean: old complex divergence in North Africa and recent arrival in Europe. Amphibia Reptilia. 30:63–80.
   Web of Science ®Google Scholar
• Gemel R, Horweg C. 2011. Ticks in the Spur-thighed Tortoise Testudo graeca LINNAEUS, 1758, and their significance as vectors. A literature survey including own observations (Testudines: testudinidae). Herpetozoa. 23:21–30.
   Web of Science ®Google Scholar
• Gharbi M, Rjeibi MR, Rouatbi M, Mabrouk M, Mhadhbi M, Amairia S, Amdouni Y, Boussaadoun MA. 2015. Infestation of the spur-thighed tortoise (Testudo graeca) by Hyalomma aegyptium in Tunisia. Ticks and Tick-borne Diseases. 6:352–355.
   PubMed Web of Science ®Google Scholar
• Godfrey SS, Moore JA, Nelson NJ, Bull CM. 2010. Unravelling causality from correlations: revealing the impacts of endemic ectoparasites on a protected species (tuatara). Parasitology. 137:275–286.
   PubMed Web of Science ®Google Scholar
• Graciá E, Vargas-Ramírez M, Delfino M, Anadón JD, Giménez A, Fahd S, Corti C, Jdeidi TB, Fritz U. 2017. Expansion after expansion: dissecting the phylogeography of the widely distributed spur-thighed tortoise. Biological Journal of the Linnean Society. 121:641–654.
   Web of Science ®Google Scholar
• Hamilton WD, Zuk M. 1982. Heritable true fitness and bright birds: a role for parasites? Science. 218:384–387.
   PubMed Web of Science ®Google Scholar
• Hedley J. 2013. A review of gastrointestinal parasites in tortoises. Testudo. 7:1–11.
   Google Scholar
• Hedley J, Eatwell K, Shaw DJ. 2013. Gastrointestinal parasitic burdens in UK tortoises: a survey of tortoise owners and potential risk factors. Veterinary Record. 173:525–532.
   PubMed Web of Science ®Google Scholar
• Herzog H. 2011. The impact of pets on human health and psychological well-being: fact, fiction, or hypothesis? Current Directions in Psychological Science. 20:236–239.
   Web of Science ®Google Scholar
• Hichami N, Znari M, Naimi M, Namous S. 2016. Clutch, egg and hatchling characteristics in the Souss Valley tortoises, Testudo graeca soussensis Pieh, 2001 (Testudines: testudinidae) from an arid steppe-land of west-central Morocco. African Journal of Herpetology. 65:21–32.
   Web of Science ®Google Scholar
• Hidalgo-Vila J, Díaz-Paniagua C, Ribas A, Florencio M, Pérez-Santigosa N, Casanova JC. 2009. Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in southwestern Spain: transmission from native turtles. Research in Veterinary Science. 86:463–465.
   PubMed Web of Science ®Google Scholar
• Hoogstraal H. 1956. African Ixodoidea. voI. I. Ticks of the Sudan (with special reference to Equatoria province and with preliminary reviews of the genera Boophilus, Margaropus, and Hyalomma). The American Journal of Tropical Medicine and Hygiene 6:767-769.
   Google Scholar
• Jacobson ER. 1994. Causes of mortality and diseases in Tortoises. Journal of Zoo and Wildlife Medicine. 25:2–17.
   Web of Science ®Google Scholar
• Javanbakht H, Široký P, Mikulíček P, Sharifi M. 2015. Distribution and abundance of Hemolivia mauritanica (Apicomplexa: Haemogregarinidae) and its vector Hyalomma aegyptium in tortoises of Iran. Biologia. 70:229–234.
   Web of Science ®Google Scholar
• Jongejan F, Uilenberg G. 2016. Ticks and control methods. Revue Scientifique Et Technique de l’OIE. 13:1201–1226.
   Web of Science ®Google Scholar
• Kalmár Z, Cozma V, Sprong H, Jahfari S, D’Amico G, Mărcutan DI, Ionică AM, Magdaş C, Modrý D, Mihalca AD. 2015. Transstadial transmission of Borrelia turcica in Hyalomma aegyptium ticks. PLoS One. 10:1–9.
   Web of Science ®Google Scholar
• Kar S, Rodriguez SE, Akyildiz G, Cajimat MNB, Bircan R, Mears MC, Bente DA, Keles AG. 2020. Crimean ‑ Congo hemorrhagic fever virus in tortoises and Hyalomma aegyptium ticks in East Thrace, Turkey : potential of a cryptic transmission cycle. Parasites & Vectors. 13:1–13.
   PubMed Web of Science ®Google Scholar
• Kautman M, Tiar G, Papa A, Široký P. 2016. AP92-like Crimean-Congo Hemorrhagic fever virus in Hyalomma aegyptium ticks, Algeria. Emerging Infectious Diseases. 22:354–356.
   PubMed Web of Science ®Google Scholar
• Kruse H, Kirkemo AM, Handeland K. 2004. Wildlife as source of zoonotic infections. Emerging Infectious Diseases. 10:2067–2072.
   PubMed Web of Science ®Google Scholar
• Lagarde F, Bonnet X, Nagy K, Henen B, Corbin J, Naulleau G. 2002. A short spring before a long jump: the ecological challenge to the steppe tortoise (Testudo horsfieldi). Canadian Journal of Zoology. 80:493–502.
   Web of Science ®Google Scholar
• Lagarde F, Guillon M, Dubroca L, Bonnet X, Ben KK, Slimani T, El Mouden EH. 2008. Slowness and acceleration: a new method to quantify the activity budget of chelonians. Animal Behaviour. 75:319–329.
   Web of Science ®Google Scholar
• Lagarde F, Louzizi T, Slimani T, El Mouden H, Ben Kaddour K, Moulherat S, Bonnet X. 2012. Bushes protect tortoises from lethal overheating in arid areas of Morocco. Environmental Conservation. 39:172–182.
   Web of Science ®Google Scholar
• Laghzaoui E-M, Elbahi A, Kasrati A, Abbad A, El Mouden EH. 2019. Toxicity of essential oils obtained from Juniperus thurifera var. africana and Mentha suaveolens subsp. timija chemotypes against pre-adult stages of Hyalomma aegyptium tick (Acari : ixodidae). Natural Product Research 17:1–6.
   Google Scholar
• Laghzaoui E-M, Kasrati A, Abbad A, Leach D, Spooner-Hart R, El Mouden EH. 2018. Acaricidal properties of essential oils from Moroccan plants against immature ticks of Hyalomma aegyptium (Linnaeus, 1758); an external parasite of the spur-thighed tortoise (Testudo graeca). International Journal of Acarology. 44:315–321.
   Web of Science ®Google Scholar
• Lambert MRK. 1983. Some factors influencing the Moroccan distribution of the western Mediterranean spur-thighed tortoise, Testudo graeca graeca L., and those precluding its survival in NW Europe. Zoological Journal Ofthe Linnean Society. 79:149–179.
   Web of Science ®Google Scholar
• Longo AV, Rodriguez-Gomez CA, Zegarra JP, Monzon O, Claudio-Hernandez HJ, Joglar RL, Zamudio KR, Burrowes PA, Lopez-Torres AL. 2020. Tick parasitism as a cost of sexual selection and male parental care in a Neotropical frog. Ecosphere. 11:1–13.
   Web of Science ®Google Scholar
• Matei IA, Kalmár Z, Lupşe M, D’Amico G, Ionică AM, Dumitrache MO, Gherman CM, Mihalca AD. 2017. The risk of exposure to rickettsial infections and human granulocytic anaplasmosis associated with Ixodes ricinus tick bites in humans in Romania: a multiannual study. Ticks and Tick-borne Diseases. 8:375–378.
   PubMed Web of Science ®Google Scholar
• Meddour-Bouderda K, Meddour A. 2006. Clés d’identification des Ixodina (Acarina) d’Algerie. Sciences & Technologie. 24:32–42.
   Google Scholar
• Megía-Palma R, Paranjpe D, Reguera S, Martínez J, Cooper RD, Blaimont P, Merino S, Sinervo B. 2018. Multiple color patches and parasites in Sceloporus occidentalis: differential relationships by sex and infection. Current Zoology. 64:703–711.
   PubMed Web of Science ®Google Scholar
• Moulherat S, Delmas V, Slimani T, El Mouden EH, Louzizi T, Lagarde F, Bonnet X. 2014. How far can a tortoise walk in open habitat before overheating? Implications for conservation. Journal for Nature Conservation. 22:186–192.
   Web of Science ®Google Scholar
• Moutou F. 2015. Rôle des animaux vertébrés dans l’épidémiologie des zoonoses. Revue Francophone des Laboratoires. 2015:25–33.
   PubMedGoogle Scholar
• Najjar C, Kaabi B, Younsi H, Petretto M, Riordan P, Zhioua E. 2020. Ticks parasitizing the Spur-thighed tortoise (Testudo graeca) population of Tunisia. Journal of Wildlife Diseases. 56:5–12.
   Web of Science ®Google Scholar
• Nijman V, Bergin D. 2017. Trade in spur-thighed tortoises Testudo graeca in Morocco: volumes, value and variation between markets. Amphibia Reptilia. 38:275–287.
   Web of Science ®Google Scholar
• Paperna I. 2006. Hemolivia mauritanica (Haemogregarinidae: apicomplexa) infection in the tortoise Testudo graeca in the Near East with data on sporogonous development in the tick vector Hyalomna aegyptium. Parasite. 13:267–273.
   PubMed Web of Science ®Google Scholar
• Parola P, Raoult D. 2001. Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clinical Infectious Diseases. 32:897–928.
   PubMed Web of Science ®Google Scholar
• Paștiu AI, Matei IA, Mihalca AD, D’Amico G, Dumitrache MO, Kalmár Z, Sándor AD, Lefkaditis M, Gherman CM, Cozma V. 2012. Zoonotic pathogens associated with Hyalomma aegyptium in endangered tortoises: evidence for host-switching behaviour in ticks? Parasites & Vectors. 5:1–6.
   PubMed Web of Science ®Google Scholar
• Petney TN, Al-Yaman F. 1985. Attachment sites of the Tortoise tick Hyalomma aegyptium in relation to tick density and physical condition of the host. The Journal of Parasitology. 71:287–289.
   Web of Science ®Google Scholar
• Plath M. 2004. Cave molly females (Poecilia mexicana) avoid parasitised males. Acta Ethologica. 6:47–51.
   Google Scholar
• Quinn G, Keough M. 2002. Experimental design and data analysis for biologists. Cambridge: Cambridge University Press.
   Google Scholar
• R Core Team. 2020. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/
   Google Scholar
• Rouag R, Benyacoub S, Luiselli L, El Mouden EH, Tiar G, Ferrah C. 2007. Population structure and demography of an Algerian population of the Moorish tortoise, Testudo graeca. Animal Biology. 57:267–279.
   Web of Science ®Google Scholar
• Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ. 2005. Restitution of mass size residuals: validating body condition indices. Ecology. 86:155–163.
   Web of Science ®Google Scholar
• Segura A, Delibes-Mateos M, Acevedo P. 2020. Implications for conservation of collection of Mediterranean Spur-Thighed Tortoise as Pets in Morocco: residents’ perceptions, habits, and knowledge. Animals. 10:1–16.
   Web of Science ®Google Scholar
• Segura A, Rodríguez O, Ruiz-fons F, Acevedo P. 2019. Tick parasitism in the Mediterranean spur-thighed tortoise in the Maamora. Ticks and Tick-borne Diseases. 10:286–289.
   PubMed Web of Science ®Google Scholar
• Sereau M, Lagarde F, Bonnet X, El Mouden EH, Slimani T, Dubroca L, Trouvé C, Dano S, Lacroix A. 2010. Does testosterone influence activity budget in the male Greek tortoise (Testudo graeca graeca)? General and Comparative Endocrinology. 167:181–189.
   PubMed Web of Science ®Google Scholar
• Široký P, Erhart J, Petrzelkova KJ, Kamler M. 2011. Life cycle of tortoise tick Hyalomma aegyptium under laboratory conditions. Experimental and Applied Acarology. 54:277–284.
   PubMed Web of Science ®Google Scholar
• Široký P, Mikulíček P, Jandzík D, Kami H, Mihalca AD, Rouag R, Kamler M, Schneider C, Záruba M, Modrý D. 2009. Co-distribution pattern of a Haemogregarine Hemolivia mauritanica (Apicomplexa: haemogregarinidae) and Its Vector Hyalomma aegyptium (Metastigmata: ixodidae). Journal of Parasitology. 95:728–733.
   PubMed Web of Science ®Google Scholar
• Široký P, Petrzelkova KJ, Kamler M, Mihalca AD, Modry D. 2006. Hyalomma aegyptium as dominant tick in tortoises of the genus Testudo in Balkan countries, with notes on its host preferences. Experimental and Applied Acarology. 40:279–290.
   PubMed Web of Science ®Google Scholar
• Smallridge CJ, Bull CM. 2000. Prevalence and intensity of the blood parasite Hemolivia mariae in a field population of the skink Tiliqua rugosa. Parasitology Research. 86:655–660.
   PubMed Web of Science ®Google Scholar
• Soghigian J, Valsdottir LR, Livdahl TP. 2017. A parasite’s modification of host behavior reduces predation on its host. Ecology and Evolution. 7:1453–1461.
   PubMed Web of Science ®Google Scholar
• Stull JW, Brophy J, Weese JS. 2015. Reducing the risk of pet-associated zoonotic infections. Canadian Medical Association Journal. 187:715–716.
   Web of Science ®Google Scholar
• Tiar G, Saadi MT, Benyacoub S, Rouag R, Široký P. 2016. The dependence of Hyalomma aegyptium on its tortoise host Testudo graeca in Algeria. Medical and Veterinary Entomology. 30:351–359.
   PubMed Web of Science ®Google Scholar
• Traversa D, Capelli G, Iorio R, Bouamer S, Cameli A, Giangaspero A. 2005. Epidemiology and biology of nematodofauna affecting Testudo hermanni, Testudo graeca and Testudo marginata in Italy. Parasitology Research. 98:14–20.
   PubMed Web of Science ®Google Scholar
• Wajnberg É, Ris N. 2002. Parasitisme et lutte biologique. Biology. 257–300.
   Google Scholar
• Walker AR, Bouattour A, Camicas J-L, Estrada-Peña A, Horak IG, Latif AA, Pegram RG, Preston PM. 2004. Ticks of domestic animals in africa: a guide to identification of species. Edinburgh, UK: Bioscience Reports; 221 pp.
   Google Scholar
• Wolf D, Vrhovec MG, Failing K, Rossier C, Hermosilla C, Pantchev N. 2014. Diagnosis of gastrointestinal parasites in reptiles: comparison of two coprological methods. Acta Veterinaria Scandinavica. 56:1–13.
   PubMed Web of Science ®Google Scholar
• Zlatanova VD. 1991. Ixodid ticks (Parasitiformes, Ixodidae) of tortoises (Reptilia, Testudinidae) in Bulgaria. Acta Zoologica Bulgarica. 41:77–79.
   Google Scholar
• Znari M, Germano DJ, Macé J-C. 2005. Growth and population structure of the Moorish Tortoise (Testudo graeca graeca) in Westcentral Morocco: possible effects of over-collecting for the tourist trade. Journal of Arid Environments. 62:55–74.
   Web of Science ®Google Scholar
• Znari M, Hichami N. 2018. Biology, life history traits and conservation of the vulnerable Souss Valley tortoise in arid areas of West Central Morocco. Reptiles and Amphibians. 118–137.
   Google Scholar