Abstract
Several Cryptosporidium species that infect reptiles, especially squamates, are well described, but there is limited data about Cryptosporidium species infecting crocodilians. In this study, we assess the occurrence of intestinal parasites using traditional microscopic examination and describe the prevalence and Cryptosporidium species in the captive-bred Chinese alligators (Alligator sinensis) in eastern China using molecular methods. The results of microscopic examination showed that no intestinal parasites were detected among the 491 fecal samples examined from the Chinese alligators. The overall prevalence for Cryptosporidium was 0.41% (2/491) by PCR detection using the SSU rRNA locus. Sequence and phylogenetic analysis of the SSU rRNA, COWP, and actin genes revealed the presence of Cryptosporidium testudinis, which has been isolated primarily from chelonians. This is the first detection of the specific DNA of C. testudinis in the feces of the Chinese alligator. This study expands our knowledge of the Cryptosporidium species involved in crocodiles, and more extensive studies are necessary to confirm the validity of C. testudinis in crocodiles.
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References
Alves M, Xiao L, Lemos V, Zhou L, Cama V, da Cunha MB, Matos O, Antunes F (2005) Occurrence and molecular characterization of Cryptosporidium spp. in mammals and reptiles at the Lisbon Zoo. Parasitol Res 97:108–112
Enabulele EE, Ozemoka HJ, Awharitoma AO, Aisien MS (2013) Parasitic infections of the African dwarf crocodile (Osteolaemus tetraspis) and the ornate Nile monitor (Varanus ornatus) from Nigeria. Acta Parasitol 58:191–197
Griffin C, Reavill DR, Stacy BA, Childress AL, Wellehan JF Jr (2010) Cryptosporidiosis caused by two distinct species in Russian tortoises and a pancake tortoise. Vet Parasitol 170:14–19
Huchzermeyer FW (2003) Crocodiles: biology, husbandry and diseases. Crocodiles Biol Husb Dis 74:98–138
Jezkova J, Horcickova M, Hlaskova L, Sak B, Kvetonova D, Novak J, Hofmannova L, McEvoy J, Kvac M (2016) Cryptosporidium testudinis sp. n., Cryptosporidium ducismarci Traversa, 2010 and Cryptosporidium tortoise genotype III (Apicomplexa: Cryptosporidiidae) in tortoises. Folia Parasitol (Praha) 14:63
Kváč M, Havrdová N, Hlásková L, Daňková T, Kanděra J, Ježková J, Vítovec J, Sak B, Ortega Y, Xiao L, Modrý D, Chelladurai JR, Prantlová V, McEvoy J (2016) Cryptosporidium proliferans n. sp. (Apicomplexa: Cryptosporidiidae): molecular and biological evidence of cryptic species within gastric Cryptosporidium of mammals. PLoS One 11:e0147090
Pedraza-Diaz S, Ortega-Mora LM, Carrion BA, Navarro V, Gomez-Bautista M (2009) Molecular characterization of Cryptosporidium isolates from pet reptiles. Vet Parasitol 160:204–210
Richter B, Rasim R, Vrhovec MG, Nedorost N, Pantchev N (2012) Cryptosporidiosis outbreak in captive chelonians (Testudo hermanni) with identification of two Cryptosporidium genotypes. J Vet Diagn Investig 24:591–595
Sulaiman IM, Lal AA, Xiao L (2002) Molecular phylogeny and evolutionary relationships of Cryptosporidium parasites at the actin locus. J Parasitol 88:388–394
Tang KY, Wang ZW, Wan QH, Fang SG (2019) Metagenomics reveals seasonal functional adaptation of the gut microbiome to host feeding and fasting in the Chinese alligator. Front Microbiol 10:2409
Traversa D, Iorio R, Otranto D, Modrý D, Šlapeta J (2008) Cryptosporidium from tortoises: genetic characterisation, phylogeny and zoonotic implications. Mol Cell Probes 22:122–128
Wang Q, Huang DC, Yang GY, Jiang B, Niu LL, Zhao B, Yu MX, Deng JB, Chen WG (2007) Investigation on parasitic infection in reptiles at a zoo in Chengdu, Sichuan. J Zool 26:451–453
Xiao L, Escalante L, Yang C, Sulaiman I, Escalante AA, Montali RJ, Fayer R, Lal AA (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small subunit ribosomal RNA gene locus. Appl Environ Microbiol 65:1578–1583
Xiao L, Sulaiman IM, Ryan UM, Zhou L, Atwill ER, Tischler ML, Zhang X, Fayer R, Lal AA (2002) Host adaptation and host-parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. Int J Parasitol 32:1773–1785
Xiao L, Ryan UM, Graczyk TK, Limor J, Li L, Kombert M, Junge R, Sulaiman IM, Zhou L, Arrowood MJ, Koudela B, Modrý D, Lal AA (2004) Genetic diversity of Cryptosporidium spp. in captive reptiles. Appl Environ Microbiol 70:891–899
Yang W, Chen P, Villegas EN, Landy RB, Kanetsky C, Cama V, Dearen T, Schultz CL, Orndorff KG, Prelewicz GJ, Brown MH, Young KR, Xiao L (2008) Cryptosporidium source tracking in the Potomac River watershed. Appl Environ Microbiol 74:6495–6504
Zhao J, Zhou Y, Wang S, Tu G, Tang X, Wu X (2015) Preliminary report on the intestinal parasites and their diversity in captive Chinese alligators. Nutr Hosp 31:813–819
Acknowledgments
We thank the Chinese alligator raisers from the Anhui Chinese Alligator National Natural Reserve Administration, for providing technical assistance during our sample collection. We thank Janine Miller, PhD, and Amanda Guthrie, DVM, from Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.
Funding
This work was supported by the Anhui Provincial Natural Science Foundation (1808085MC84 and 1908085QC116), the school-level talent project of Anhui Science and Technology University (dkwd201702), and the Key Discipline Construction Program of Anhui Science and Technology University (AKZDXK2015A04).
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This study was carried out with permission from the State Forestry Administration of China (Forest Conservation Permission Document (2014) 1545). The fecal samples were obtained from Chinese alligators at the Anhui Chinese Alligator National Natural Reserve according to the guidelines and approval of the Animal Care and Welfare Committee of Anhui Science and Technology University (AHSTU-2010-16).
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Supplementary Fig. 1
The Chinese alligators and their feces in the playground. (PNG 1951 kb)
Supplementary Fig. 2
Neighbor-joining trees based on partial actin gene sequences from different Cryptosporidium species. The actin sequence of C. testudinis isolate obtained in this study (indicated by asterisks) were located on the C. testudinis branches (PNG 828 kb)
Supplementary Fig. 3
Neighbor-joining trees based on partial COWP gene sequences from different Cryptosporidium species. The sequence from this study is indicated by asterisks. (PNG 591 kb)
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Huang, Jm., Chen, Hl., Zhou, Yk. et al. The first report of Cryptosporidium testudinis in Chinese alligators (Alligator sinensis) in China. Parasitol Res 119, 2359–2362 (2020). https://doi.org/10.1007/s00436-020-06733-0
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DOI: https://doi.org/10.1007/s00436-020-06733-0