Skip to main content
Log in

Cecal coccidiosis in turkeys: Comparative biology of Eimeria species in the lower intestinal tract of turkeys using genetically typed, single oocyst–derived lines

Parasitology Research Aims and scope Submit manuscript

Abstract

Differentiating the Eimeria species causing cecal coccidiosis in turkeys is challenging. To obtain benchmark biological data for Eimeria gallopavonis Hawkins 1952 and Eimeria meleagridis Tyzzer 1929 and to support the stability of the species concept for each, genetically typed, single oocyst–derived lines of E. gallopavonis Weybridge strain and E. meleagridis USAR97-01 were used to redescribe the biological, pathological, and morphological features of these parasites. Oocysts of E. meleagridis and E. gallopavonis overlap in dimensions, but oocysts of the former have a single polar granule compared with multiple in the latter. Mature first-generation meronts of E. gallopavonis were observed histologically as early as 48 h post-inoculation alongside the villi in jejunum (before and after Meckel’s diverticulum), ileum, cecal neck and rectum, but not cecal pouches. Three asexual cycles were observed suggesting that early workers apparently overlooked one asexual cycle. Examination of endogenous development of a culture labeled “Eimeria adenoeides Weybridge strain” suggested that this strain (found in a number of publications as a large oocyst strain of “Eimeria adenoeides”) matched the species description of E. gallopavonis and so has been renamed herein. Macroscopic lesions induced by E. gallopavonis consisted of caseous material distally from posterior of the yolk stalk through the remaining intestinal tract, excluding the cecal pouches. For E. meleagridis, only the first asexual generation was observed outside of the cecal pouches within the jejunum around the yolk stalk. Second- and 3rd-generation asexual stages developed almost exclusively in the cecal pouches (but not cecal necks). Macroscopic lesions described for E. meleagridis were similar to those of E. adenoeides. Marked corrugation of the cecal serosal surface was observed. Cecal pouches contained creamy colored, caseous material varying from loose material to granular. Distinguishing features of the Eimeria species infecting the lower part of the small intestine are summarized in the present study, and new type specimens were designated for E. gallopavonis and E. meleagridis to provide a stable reference for future work with these parasites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig.7
Fig. 8
Fig. 9

References

  • Chapman HD (2008) Coccidiosis in the turkey. Avian Pathol 37:205–223

    Article  CAS  PubMed  Google Scholar 

  • Clarkson MJ (1958) Life history and pathogenicity of Eimeria adenoeides Moore & Brown, 1951, in the turkey poult. Parasitology 48:70–88

    Article  CAS  PubMed  Google Scholar 

  • Clarkson MJ (1959) The life history and pathogenicity of Eimeria meleagridis Tyzzer, 1927, in the turkey poult. Parasitology 49:519–528

    Article  CAS  PubMed  Google Scholar 

  • Clarkson MJ (1960) The coccidia of the turkey. Ann Trop Med Parasitol 54:253–257

    Article  CAS  PubMed  Google Scholar 

  • Cook SM, Higuchi DS, McGowan AL, Schrader JS, Withanage GS, Francis MJ (2010) Polymerase chain reaction-based identity assay for pathogenic turkey Eimeria. Avian Dis 54:1152–1156

    Article  PubMed  Google Scholar 

  • Doran DJ, Augustine PC (1977) Eimeria dispersa and Eimeria gallopavonis: infectivity, survival, and development in primary chicken and turkey kidney cell cultures. J Protozool 24:172–176

    Article  CAS  PubMed  Google Scholar 

  • El-Sherry S, Ogedengbe ME, Hafeez MA, Barta JR (2013) Divergent nuclear 18S rDNA paralogs in a turkey coccidium, Eimeria meleagrimitis, complicate molecular systematics and identification. Int J Parasitol 43:679–685

    Article  CAS  PubMed  Google Scholar 

  • El-Sherry S, Rathinam T, Hafeez MA, Ogedengbe ME, Chapman HD, Barta JR (2014a) Biological re-description of a genetically typed, single oocyst line of the turkey coccidium, Eimeria meleagrimitis Tyzzer 1929. Parasitol Res 113:1135–1146

    Article  CAS  PubMed  Google Scholar 

  • El-Sherry S, Ogedengbe ME, Hafeez MA, Sayf-Al-Din M, Gad N, Barta JR (2014b) Re-description of a genetically typed, single oocyst line of the turkey coccidium, Eimeria adenoeides Moore and Brown, 1951. Parasitol Res 113:1–12

    Article  Google Scholar 

  • El-Sherry S, Ogedengbe ME, Hafeez MA, Sayf-Al-Din M, Gad N, Barta JR (2015) Sequence-based genotyping clarifies conflicting historical morphometric and biological data for 5 Eimeria species infecting turkeys. Poult Sci 94:262–272

    Article  CAS  PubMed  Google Scholar 

  • Farr MM (1964) Life cycle of Eimeria gallopavonis Hawkins in the turkey. J Parasitol 50(3 Section 2, Suppl):52

    Google Scholar 

  • Farr M, Wehr E, Shalkop W (1961) Pathogenicity of Eimeria gallopavonis. V J Sci 12:150–151

    Google Scholar 

  • Hammond DM, Bowman GW, Davis LR, Simms B (1946) The endogenous phase of the life cycle of Eimeria bovis. Parasitology 32:409–427

    Article  CAS  Google Scholar 

  • Hawkins PA (1952) Coccidiosis in turkey. Technical Bulletin 226. Michigan State College Agricultural Experiment Station, East Lansing, MI

  • Hein H (1969) Eimeria adenoeides and E. meleagrimitis: pathogenic effect in turkey poults. Exp Parasitol 24:163–170

    Article  CAS  PubMed  Google Scholar 

  • Joyner LP, Norton CC (1972) The drug sensitivity of recently isolated strains of Eimeria meleagrimitis and a laboratory strain of Eimeria adenoeides in turkeys to robenidene. Res Vet Sci 13:279–281

    Article  CAS  PubMed  Google Scholar 

  • Matsler PL, Chapman HD (2006) Characterization of a strain of Eimeria meleagridis from the turkey. Avian Dis 50:599–604

    Article  CAS  PubMed  Google Scholar 

  • McDougald LR, Fitz-Coy SH (2003) Coccidiosis. In: Saif YM, Fadly AA, Glisson JR, McDougald LR, Nolan L, Swayne DE (eds) Diseases of poultry, 12th edn. ISU, Ames, pp 1080–1083

    Google Scholar 

  • Miska KB, Schwarz RS, Jenkins MC, Rathinam T, Chapman HD (2010) Molecular characterization and phylogenetic analysis of Eimeria from turkeys and game birds: implications for evolutionary relationships in Galliform birds. J Parasitol 96:982–986. https://doi.org/10.1645/GE-2344.1

    Article  CAS  PubMed  Google Scholar 

  • Moore EN, Brown JA (1951) A new coccidium pathogenic for turkeys, Eimeria adenoeides n. sp. (Protozoa: Eimeriidae). Cornell Vet 41:124–135

    CAS  PubMed  Google Scholar 

  • Ogedengbe ME, El-Sherry S, Whale J, Barta JR (2014) Complete mitochondrial genome sequences from five Eimeria species (Apicomplexa; Coccidia; Eimeriidae) infecting domestic turkeys. Parasit Vectors 7:335. https://doi.org/10.1186/1756-3305-7-335

    Article  PubMed  PubMed Central  Google Scholar 

  • Poplstein M, Vrba V (2011) Description of the two strains of turkey coccidia Eimeria adenoeides with remarkable morphological variability. Parasitology 138:1211–1216

    Article  CAS  PubMed  Google Scholar 

  • Rampin T, Manarolla G, Recordati C, Sironi G (2006) Caecal coccidiosis in commercial male turkeys. Ital J Anim Sci 5:315–317

    Article  Google Scholar 

  • Remmler O, McGregor JK (1964) A method to facilitate isolation of single coccidial oocysts. J Parasitol 50:294

    Article  CAS  PubMed  Google Scholar 

  • Trees AJ (2002) Parasitic diseases. In: Jordan FTW (ed) Poultry diseases. Baillière Tindal, London, p p413

    Google Scholar 

  • Tyzzer EE (1929) Coccidiosis in gallinaceous birds. Am J Hyg 10:269–383

    Google Scholar 

  • Tyzzer EE, Theiler H, Jones EE (1932) Coccidiosis in gallinaceous birds. II. A comparative study of species of Eimeria of the chicken. Am J Hyg 15:319–393

  • Vrba V, Pakandl M (2014) Coccidia of turkey: from isolation, characterisation and comparison to molecular phylogeny and molecular diagnostics. Int J Parasitol 44(13):985–1000. https://doi.org/10.1016/j.ijpara.2014.06.004

    Article  CAS  PubMed  Google Scholar 

  • Wehr EE, Farr MM, Shalkop WT (1962) Studies on pathogenicity of Eimeria gallopavonis to turkeys. J Protozool 9:8–9

    Google Scholar 

  • Williams RB (2010) The correct date of the original description and availability of the coccidian name Eimeria meleagridis Tyzzer (Apicomplexa: Eimeriorina: Eimeriidae). Syst Parasitol 76:77–79

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Julie Cobean and Julia Whale are thanked for their skilled technical assistance. Staff members of the CAF Animal Isolation Facility at the University of Guelph are thanked for their skilled care of experimental animals used in this study.

Funding

This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC, DG 400566); from the Ontario Ministry of Agriculture, Food, and Rural Affairs (OMAFRA, Tier II 200331); and from the Federal Economic Development Agency for Southern Ontario (FedDev) to J.R.B. Scholarship support was provided by the Ministry of Higher Education and Research (MOHE), Egypt, to S.E.S. administered through the Bureau of Cultural and Educational Affairs (BCEA) of Egypt in Canada; scholarship support was provided to M.E.O. by the Ontario Veterinary College (OVC PhD Scholarship).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. R. Barta.

Ethics declarations

All experimental manipulations were reviewed and approved by the University of Guelph’s Animal Care Committee and complied with the Canadian Council on Animal Care’s Guide to the Care and Use of Experimental Animals (2nd edition).

Conflict of interest statement

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Bill Chobotar

Ogedengbe and Hafeez contributed equally

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El-Sherry, S., Ogedengbe, M.E., Hafeez, M.A. et al. Cecal coccidiosis in turkeys: Comparative biology of Eimeria species in the lower intestinal tract of turkeys using genetically typed, single oocyst–derived lines. Parasitol Res 118, 583–598 (2019). https://doi.org/10.1007/s00436-018-6147-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-018-6147-5

Keywords

Navigation