Abstracts

Introduction

In North America, a relatively large range of exotic gallinaceous birds have been introduced and domesticated in certain areas specifically for hunting. Differently, some of these gallinaceous birds have been reared in South America exclusively for meat. The most popular exotic meat birds belong to the family Phasianidae Horsfield, 1821, which includes species of pheasants, partridges, quails, ducks, geese and doves. The chukar partridge, Alectoris chukar Gray, 1930, is a short, round, greyish-brown Eurasian upland bird that has been introduced into many countries and is well established in the United States, Canada and New Zealand for game purposes (WOODARD, 2002Woodard AE. Raising chukar partridge [online]. Okland: University of California; 2002. vol. 21321e [cited 2003 Jan 10]. Available from http://anrcatalog.ucdavis.edu/
http://anrcatalog.ucdavis.edu/... ). It has been introduced into Brazil because of its fast growth rate. Likewise, the common grey quail, Coturnix coturnix Linnaeus, 1758, is marketed in Brazil exclusively for meat, because it is slightly larger than the domestic Japanese quail (Coturnix japonica), which is used as an egg-layer. The grey quail originated in Asia Minor and was first domesticated in Europe, but it can be found around the world except in the Americas (BIGLAND et al., 1965Bigland CH, Da Massa AJ, Woodard AE. Diseases of Japanese quail (Coturnix coturnix japonica) – A flock survey and experimental transmission of selected avian pathogens. Avian Dis 1965; 9(2): 212-219. http://dx.doi.org/10.2307/1588003.
http://dx.doi.org/10.2307/1588003... ). The exotic meat bird industry in Latin America is small and the majority of its flock is located in the state of Santa Catarina in southern Brazil.

It is common knowledge that the parasite with the most negative impact on the economic avian industry worldwide is Eimeria. In North America, it is a major limitation to the production and marketing of bobwhite quails, ring-neck pheasants and chukar partridges (DUSZYNSKI & GUTIÉRREZ, 1981Duszynski DW, Gutiérrez RJ. The coccidia of quail in the United States. J Wildl Dis 1981; 17(3): 371-379. http://dx.doi.org/10.7589/0090-3558-17.3.371. PMid:7310946
http://dx.doi.org/10.7589/0090-3558-17.3... ; KEENE & SCHWARTZ, 1984Keene OD, Schwartz LD. Prevalent diseases and medications most frequently used by the game bird industry, Results of a national survey. Poult Sci 1984; 63(1): 70.; RUFF, 1985Ruff MD. Life cycle and biology of sp. n. (Protozoa: Eimeriidae) from the northern bobwhite, (L.). Eimeria lettyae Colinus virginianusJ Wildl Dis 1985; 21(4): 361-370. http://dx.doi.org/10.7589/0090-3558-21.4.361. PMid:4078970
http://dx.doi.org/10.7589/0090-3558-21.4... ). Virtually no research has been conducted on the causative agents of diseases of grey quails and chukar partridges in South America, including coccidia. The aim of this work was to make preliminary observations on Eimeria spp. from exotic gallinaceous meat birds marketed in Brazil.

Materials and Methods

This study was conducted on commercial farms integrated with or belonging to BRF S.A., the largest poultry company and the only one raising exotic meat birds in Brazil. The average production was around 50,000 chukar and 510,000 quails, slaughtered weekly at the company’s abattoir located in Videira, Santa Catarina.

There was a single chukar farm with a flock separated into categories: three sheds for mothers consisting of wired cages for rearing birds from the age of twelve weeks onwards; and seven sheds for meat birds in which they were reared on the floor in wood shavings between the ages of 1 and 77 days. There were three quail farms, which were also separated into categories: four sheds for mothers, containing caged birds from the age of six weeks onwards and seven sheds for meat birds in which they were kept on bed litter between the ages of 1 and 35 days. All the sheds of all the chukar and quail flocks were studied. While prophylactic anticoccidial treatments were provided by the company to both chukar and quails, the regimen, type of drugs and doses used were not revealed.

Fecal samples from the meat sheds were collected from different points in the bed litter (n = 20). In the mothers’ sheds, samples were collected from each cage. A total of 11 sheds on the chukar farm and 33 sheds on the quail farms were sampled. All the samples were kept in plastic bags under refrigeration for transportation purposes. Four birds from each shed were randomly selected to be necropsied for lesion scoring and to collect tissue samples from the duodenum, jejunum, ileum and caeca. The tissue samples were fixed in 10% buffered formalin.

The fecal samples were sieved and stored at room temperature for sporulation in a thin layer of 2.5% w/v potassium dichromate. Oocysts were recovered from the feces after seven days of sporulation, by means of centrifugation in Sheather’s solution. The oocysts were photographed for morphological analysis, under an Olympus BX 51 microscope coupled with an Olympus DP71 camera, using the Image-Pro Express 6 software for measurements (CARVALHO et al., 2011Carvalho FS, Wenceslau AA, Teixeira M, Matos Carneiro JA, Melo ADB, Albuquerque GR. Diagnosis of Eimeria species using traditional and molecular methods in field studies. Vet Parasitol 2011; 176(2-3): 95-100. http://dx.doi.org/10.1016/j.vetpar.2010.11.015. PMid:21167646
http://dx.doi.org/10.1016/j.vetpar.2010.... ). Morphological identification was performed using oocyst length, width, shape index and inner features (DUSZYNSKI & WILBER, 1997Duszynski DW, Wilber PG. A guideline for the preparation of species descriptions in the Eimeriidae. J Parasitol 1997; 83(2): 333-336. http://dx.doi.org/10.2307/3284470. PMid:9105325
http://dx.doi.org/10.2307/3284470... ). To study the endogenous stages using optical microscopy, tissue samples were prepared in Histosec® (Merck), sectioned at a thickness of 5 μm and stained with periodic acid-Schiff.

Results

All the fecal samples from chukar partridges were negative for Eimeria oocysts. This result was confirmed by means of gross and microscopic examination, which showed that lesions or endogenous stages of Eimeria were absent from the tissue samples. These findings, together with the flock history and lack of clinical signs, suggest that chukar partridges reared in Santa Catarina do not have any visible coccidial infection. The fecal samples from all the quail farms were positive for Eimeria, but the oocyst numbers were very low. According to the morphological characteristics of the oocysts found (Table 1), two Eimeria species that had previously been described were identified in the quail samples (Figure 1). The most prevalent of these was E. bateri Bathia, Pandey & Pande, 1965 (80.31%), followed by E. tsunodai Tsutsumi, 1972 (9.69%). No specific macro and microscopic lesions were observed in the tissues from the quails. Endogenous stages were observed mostly in sections from the upper and descending small intestine of quails. The parasites were located at the base of the villi, towards the glands. Occasional mature schizonts (mean size 8.7 × 7 µ) were observed within the duodenum and ileum sections of young meat quails (23 days of age). They were generally located above the nucleus of the host cell. Gametocytes occurred throughout the small intestine but were more concentrated in the jejune of meat quails. Mature macrogametocytes (mean size 20.5 × 11 µ) were more numerous than microgametocytes (mean size 19.8 × 12 µ). No schizonts or gametocytes were observed in the sections from the intestine of adult caged quails.

Figure 1
Sporulated oocysts of (a) Eimeria bateri and (b) E. tsunodai in Sheater’s solution (scale bar = 10µm).

Discussion

The prevalence and identity of the coccidia of exotic meat birds in the Brazilian poultry industry has never been assessed. Coccidiosis is the most frequent parasitic disease of the poultry industry worldwide and it is uncommon to find Eimeria-free flocks (RUFF et al., 1984Ruff MD, Fagan JM, Dick JW. Pathogenicity of coccidia in Japanese quail (Coturnix coturnix japonica). Poult Sci 1984; 63(1): 55-60. http://dx.doi.org/10.3382/ps.0630055. PMid:6701143
http://dx.doi.org/10.3382/ps.0630055... ). However, according to the data presented here, coccidiosis is very well controlled in both the chukar and the quail farms in Santa Catarina, Brazil. The absence of infection in the chukar partridges could be due to the fact that these birds were introduced through egg importation from Europe. Consequently, no infected birds were introduced into Brazil. Moreover, egg hatching takes place under restricted conditions without any presence of circulating Eimeria species that might be able to infect these birds. This is probably due to host specificity (BIGLAND et al., 1965Bigland CH, Da Massa AJ, Woodard AE. Diseases of Japanese quail (Coturnix coturnix japonica) – A flock survey and experimental transmission of selected avian pathogens. Avian Dis 1965; 9(2): 212-219. http://dx.doi.org/10.2307/1588003.
http://dx.doi.org/10.2307/1588003... ; EDGAR et al., 1964Edgar SA, Waggoner R, Flanagan C. Susceptibility of quail to certain disease producing agents common to poultry. CoturnixPoult Sci 1964; 43(5): 1315.; SHAH & JOHNSON, 1971Shah HL, Johnson CA. Bhatia, Pandey and Pande, 1965 from the Hungarian quail in the United States and its attempted transmission to the chicken. Eimeria bateri Coturnix c. coturnixJ Protozool 1971; 18(2): 219-220. http://dx.doi.org/10.1111/j.1550-7408.1971.tb03310.x. PMid:5104608
http://dx.doi.org/10.1111/j.1550-7408.19... ; LONG & MILLARD, 1979Long PL, Millard BJ. Rejection of by foreign hosts. EimeriaParasitology 1979; 78(2): 239-247. http://dx.doi.org/10.1017/S0031182000049271. PMid:471537
http://dx.doi.org/10.1017/S0031182000049... ; FAYER, 1980Fayer R. Epidemiology of protozoan infections: the coccidia. Vet Parasitol 1980; 6(1-3): 75-103. http://dx.doi.org/10.1016/0304-4017(80)90039-4.
http://dx.doi.org/10.1016/0304-4017(80)9... ; LONG & JOYNER, 1984Long PL, Joyner LP. Problems in the identification of species of . EimeriaJ Protozool 1984; 31(4): 535-541. http://dx.doi.org/10.1111/j.1550-7408.1984.tb05498.x. PMid:6392531
http://dx.doi.org/10.1111/j.1550-7408.19... ). Furthermore, prophylactic use of anticoccidial drugs and biosecurity measures may also have strengthened the limitation of infection among these chukar partridges.

Making a morphological diagnosis of Eimeria is often difficult because of similarities in oocyst morphology and infection sites. According to Ruff (1986)Ruff MD. Coccidiosis in gallinaceous gamebirds. In: MacDougald LR, Joyner LP, Long PL, editors. Research in Avian Coccidiosis. Athens: University of Georgia; 1986. p. 107-115., the taxonomic status of game bird coccidia is still in disarray, because different hosts may harbor different Eimeria species and cross-infections may not be entirely ruled out. This problem might be reduced through development of novel diagnostic methods (KUCERA & REZNICKY, 1991Kucera J, Reznický M. Differentiation of species of from the fowl using a computerized image-analysis system. EimeriaFolia Parasitol (Praha) 1991; 38(2): 107-113. PMid:1937268.; DAUGSCHIES et al., 1999Daugschies A, Imarom S, Bollwahn W. Differentiation of porcine Eimeria spp. by morphologic algorithms. Vet Parasitol 1999; 81(3): 201-210. http://dx.doi.org/10.1016/S0304-4017(98)00246-5. PMid:10190864
http://dx.doi.org/10.1016/S0304-4017(98)... ). However, application of molecular diagnostic techniques depends on construction of PCR primers for detecting and distinguishing Eimeria spp. This technology remains unavailable for most exotic birds (GERHOLD et al., 2011Gerhold RW, McDougald LR, Beckstead RB. Construction of PCR primers to detect and distinguish Eimeria spp. in northern bobwhites and a survey of Eimeria on gamebird farms in the United States. J Parasitol 2011; 97(5): 892-895. http://dx.doi.org/10.1645/GE-2816.1. PMid:21612414
http://dx.doi.org/10.1645/GE-2816.1... ). Thus, morphological differentiation in association with assessment of host specificity is still useful in characterizing Eimeria.

In Coturnix quails, six Eimeria species are known (Table 1) and three have been reported in Brazil (TEIXEIRA et al., 2004Teixeira M, Teixeira Filho WL, Lopes CWG. Coccidiosis in Japanese Quails (. Coturnix japonica): Characterization of a naturally occurring infection in a commercial rearing farmBraz J Poult Sci 2004; 6(2): 129-134.; BERTO et al., 2013Berto BP, Borba HR, Lima VM, Flausino W, Teixeira-Filho WL, Lopes CWG. Eimeria spp. from Japanese quails (): new characteristic features and diagnostic tools. Coturnix japonicaPesqui Vet Bras 2013; 33(12): 1441-1447. http://dx.doi.org/10.1590/S0100-736X2013001200008.
http://dx.doi.org/10.1590/S0100-736X2013... ). Eimeria bateri, a parasite originally described from Indian quails, seems to be well distributed worldwide (SHAH & JOHNSON, 1971Shah HL, Johnson CA. Bhatia, Pandey and Pande, 1965 from the Hungarian quail in the United States and its attempted transmission to the chicken. Eimeria bateri Coturnix c. coturnixJ Protozool 1971; 18(2): 219-220. http://dx.doi.org/10.1111/j.1550-7408.1971.tb03310.x. PMid:5104608
http://dx.doi.org/10.1111/j.1550-7408.19... ). This species was found to be able to infect and develop its entire life cycle in Japanese quails (NORTON & PEIRCE, 1971Norton CC, Peirce MA. The life cycle of (Protozoa, Eimeriidae) in the Japanese quail . Eimeria bateri Coturnix coturnix japonicumJ Protozool 1971; 18(1): 57-62. http://dx.doi.org/10.1111/j.1550-7408.1971.tb03280.x. PMid:5552705
http://dx.doi.org/10.1111/j.1550-7408.19... ). However, there are very few acceptable records of transmission of Eimeria species from one host genus to complete development in another, with the exception of situations that may reflect a close systematic relationship between two hosts (DORAN, 1978Doran DJ. The life cycle of Tyzzer 1929 from the turkey in gallinaceous birds. Eimeria dispersaJ Parasitol 1978; 64(5): 882-885. http://dx.doi.org/10.2307/3279523. PMid:722458
http://dx.doi.org/10.2307/3279523... ; LONG & JOYNER, 1984Long PL, Joyner LP. Problems in the identification of species of . EimeriaJ Protozool 1984; 31(4): 535-541. http://dx.doi.org/10.1111/j.1550-7408.1984.tb05498.x. PMid:6392531
http://dx.doi.org/10.1111/j.1550-7408.19... ). In a similar situation, Japanese quails were infected in a laboratory with E. dispersa, which is known to be a parasite of partridges and grey quails, but not of chickens or turkeys (EDGAR et al., 1964Edgar SA, Waggoner R, Flanagan C. Susceptibility of quail to certain disease producing agents common to poultry. CoturnixPoult Sci 1964; 43(5): 1315.). Because Coturnix coturnix and Coturnix japonica are phylogenetically related birds, E. bateri and E. tsunodai may infect both hosts.

The other four species that have been described in Coturnix quails have oocysts that differ from those reported here. The oocysts of E. dispersa are slightly larger, have no polar granule and have a single wall. Those of E. coturnicis are considerably larger and contain sporocysts in which the sporozoites lie at opposite poles along the transverse axis and residuum is present. Oocysts of E. uzura, E. tahamensis and E. taldykurganica also differ in size, shape and shape index from those described here.

The presence of endogenous stages within the small intestine of young quails seen in our study was concordant with the form and location described in previous life cycle studies (NORTON & PEIRCE, 1971Norton CC, Peirce MA. The life cycle of (Protozoa, Eimeriidae) in the Japanese quail . Eimeria bateri Coturnix coturnix japonicumJ Protozool 1971; 18(1): 57-62. http://dx.doi.org/10.1111/j.1550-7408.1971.tb03280.x. PMid:5552705
http://dx.doi.org/10.1111/j.1550-7408.19... ; TSUTSUMI, 1972Tsutsumi Y. Eimeria tsunodai sp. nov. (protozoa; Eimeriidae). A caecal coccidium of Japanese quails (). Coturnix coturnix japonicaNippon Juigaku Zasshi 1972; 34(1): 1-9. http://dx.doi.org/10.1292/jvms1939.34.1. PMid:5063025
http://dx.doi.org/10.1292/jvms1939.34.1... ). This also suggests that young quails reared on the floor are more susceptible to infection. Even in situations of mild infection, constant monitoring of Eimeria incidence is necessary, particularly in younger categories, since this represents a threat to the livestock business if left unchecked.

Acknowledgements

The authors would like to thank to Walter Leira Teixeira Filho and Fabiana Lessa Silva for the preparation of histologic sessions of this study. This research project was conducted under the supervision of and was fully sponsored by the National Research Council (CNPQ) and the Research Support Foundation of the State of Bahia (FAPESB), in Brazil.

References

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