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Prevalence of parasites in selected captive bird species

Prevalência de parasitas em espécies de pássaros em cativeiro selecionados

Abstract

Blood and fecal samples of chukar partridge (Alectoris chukar), albino pheasant (Phasianus colchicus), silver pheasant (Lophura nycthemera), rose-ringed parakeet (Psittacula krameri) and turkeys (Meleagris gallopavo) were analyzed to check parasitic prevalence. To record parasites these five avian species were placed kept in separate cages at Avian Conservation and Research Center, Department of Wildlife an Ecology, University of Veterinary and Animal Sciences, Lahore, Pakistan. 100 fecal and 100 blood samples for each bird species were inspected to analyze internal parasites. During present study, 17 species of endoparasites 14 from fecal samples and three from blood were examined. Two species of ectoparasites i.e. mite Dermanyssus gallinae 42% and fowl ticks Args persicus 41%were studied. Blood parasites included Plasmodium juxtanucleare 50%, Leucoctoyzoon simond having parasitic prevalence 40%, and Aegyptinella pullorum having parasitic prevalence of 40%. Parasitic species recorded from fecal samples included 6 species of nematodes viz. Allodpa suctoria 2%. Syngamus trachea with parasitic prevalence of 60%, Capillaria annulata 37.5%, Ascardia galli 24%, Capillaria anatis 40% and Heterakis gallinarum 28.3%. Similarly, two species of trematodes viz. Prosthogonimus ovatus having parasitic prevalence of 50% and Prosthogonimus macrorchis 21% were also documented from fecal avian samples . Single cestode species Raillietina echinobothrida having parasitic prevalence of 72% and 3 protozoan species i.e. Eimeria maxima having parasitic prevalence of 21%, Giardia lamblia 41% and Histomonas meleagridis 18% were documented during corpological analysis. In our recommendation, proper sanitation, medication and vaccination of bird’s enclousres are suggested to avoid parasites.

Keywords:
ACRC UVAS; Giardia lamblia; Histomonas meleagridis; Capillaria annulata; Dermanyssus gallinae

RESUMO

Amostras de sangue e fezes de perdiz chukar (Alectoris chukar), faisão-albino (Phasianus colchicus), faisão-prateado (Lophura nycthemera), periquito-de-rosa (Psittacula krameri) e perus (Meleagris gallopavo) foram analisadas para verificar a prevalência de parasitas. Para registrar os parasitas, essas cinco espécies de aves foram colocadas em gaiolas separadas no Centro de Conservação e Pesquisa de Aves, Departamento de Vida Selvagem e Ecologia, Universidade de Veterinária e Ciências Animais, Lahore, Paquistão. Cem amostras fecais e 100 amostras de sangue para cada espécie de ave foram inspecionadas para analisar os parasitas internos. Durante o presente estudo, foram examinadas 17 espécies de endoparasitas, 14 de amostras fecais e 3 de sangue. Foram estudadas duas espécies de ectoparasitas, ou seja, o ácaro Dermanyssus gallinae 42% e o carrapato aviário Args persicus 41%. Os parasitas sanguíneos incluíram Plasmodium juxtanucleare 50%, Leucoctoyzoon simond com prevalência parasitária de 40% e Aegyptinella pullorum com prevalência parasitária de 40%. As espécies parasitas registradas em amostras fecais incluíram 6 espécies de nematoides viz. Allodpa suctoria 2%, Syngamus traqueia com prevalência parasitária de 60%, Capillaria annulata 37,5%, Ascardia galli 24%, Capillaria anatis 40% e Heterakis gallinarum 28,3%. Da mesma forma, duas espécies de trematódeos viz. Prosthogonimus ovatus com prevalência parasitária de 50% e Prosthogonimus macrorchis 21% também foram documentados em amostras fecais de aves. Espécies de cestoide único Raillietina echinobothrida com prevalência parasitária de 72% e 3 espécies de protozoários, isto é, Eimeria maxima com prevalência parasitária de 21%, Giardia lamblia 41% e Histomonas meleagridis 18% foram documentadas durante a análise corpológica. Em nossa recomendação, o saneamento adequado, medicação e vacinação de invólucros de pássaros são sugeridos para evitar parasitas.

Palavras-chave:
ACRC UVAS; Giardia lamblia; Histomonas meleagridis; Capillaria annulata; Dermanyssus gallinae

1. Introduction

Parasitic prevalence in birds varies among species, age, gender and ecological conditions (Valkiūnas et al., 2005VALKIŪNAS, G., SEHGAL, R.N.M., IEZHOVA, T.A. and SMITH, T.B., 2005. Further observations on the blood parasites of birds in Uganda. Journal of Wildlife Diseases, vol. 41, no. 3, pp. 580-587. http://dx.doi.org/10.7589/0090-3558-41.3.580. PMid:16244068.
http://dx.doi.org/10.7589/0090-3558-41.3...
). Even closely related species may differ significantly in blood parasitic prevalence. Higher prevalence of parasites in juvenile birds than in adults is well documented. These blood parasites affect plumage coloration, reproductive rates, survival and community structure of their hosts (Fokidis et al., 2008FOKIDIS, H.B., GREINER, E.C. and DEVICHE, P., 2008. Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. Journal of Avian Biology, vol. 39, no. 3, pp. 300-310. http://dx.doi.org/10.1111/j.0908-8857.2008.04248.x.
http://dx.doi.org/10.1111/j.0908-8857.20...
). Birds interact with their natural environments in numerous ways and can respond to changes in their ambient environment such as resistance against parasites and changing climate (Wood et al., 2007WOOD, M.J., COSGROVE, C.L., WILKIN, T.A., KNOWLES, S.C.L., DAY, K.P. and SHELDON, B.C., 2007. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology, vol. 16, no. 15, pp. 3263-3273. http://dx.doi.org/10.1111/j.1365-294X.2007.03362.x. PMid:17651202.
http://dx.doi.org/10.1111/j.1365-294X.20...
; Loiseau et al., 2010LOISEAU, C., IEZHOVA, T., VALKIUNAS, G., CHASAR, A., HUTCHINSON, A., BUERMANN, W., SMITH, T.B. and SEHGAL, R.N., 2010. Spatial variation of haemosporidian parasite infection in African rain forest bird species. The Journal of Parasitology, vol. 96, no. 1, pp. 21-29. http://dx.doi.org/10.1645/GE-2123.1. PMid:19860532.
http://dx.doi.org/10.1645/GE-2123.1...
; Wood et al., 2007WOOD, M.J., COSGROVE, C.L., WILKIN, T.A., KNOWLES, S.C.L., DAY, K.P. and SHELDON, B.C., 2007. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology, vol. 16, no. 15, pp. 3263-3273. http://dx.doi.org/10.1111/j.1365-294X.2007.03362.x. PMid:17651202.
http://dx.doi.org/10.1111/j.1365-294X.20...
). However, these interactions are not fully understood and need exploration (Forsman et al., 2008FORSMAN, J.T., HJERNQUIST, M.B., TAIPALE, J. and GUSTAFSSON, L., 2008. Competitor density cues for habitat quality facilitating habitat selection and investment decisions. Behavioural Ecology, vol. 19, no. 3, pp. 539-545. http://dx.doi.org/10.1093/beheco/arn005.
http://dx.doi.org/10.1093/beheco/arn005...
). To rear the birds on ground in aviaries is a common practice in many countries and such settings negatively affect the health of birds. Pavo cristatus are amongst highly diverse peafowl species and usually suffer from parasitic infections due to sanitary issues affecting wild populations. Infected birds mostly show subclinical conditions that may lead to death (Freitas et al., 2002FREITAS, M.F.L., OLIVERIA, J.B., CAVALCANTI, M.D.B., LEITI, A.S., MAGALHAES, V.S., OLIVERIA, R.A. and EVENCIO-SOBRINO, A., 2002. Gastrointestinal parasites of captive wild birds in Pernambuco state, Brazil. Parasitología Latinoamericana, vol. 57, pp. 50-54.). However, disease pathology in peafowls especially in case of parasitic diseases is less known, but it is an accepted fact that most diseases look like the ones faced by turkeys. Similarly, pheasant farming has lot of potential for raising livelihoods of the people from developing countries through enhancing hunting, game reserves and tourism. In addition, the pheasants can be used to monitor ecosystem health as they are considered excellent bio-indicators (Dzugan et al., 2010DZUGAN, M., SZOSTEK, M. and PIENIAZEK, M., 2010. Using of pheasants (Phasianus colchicus L.) in biomonitoring of soil environment [in Polish]. Scientific Papers of Polish Ecological Engineering and Polish Soil Science Society, vol. 13, pp. 49-50.). Ring-necked pheasant (Phasianus colchicus) is a common bird of woodland habitats, modified to largely cultivated farmlands near bushy areas or woodland edges. Wild pheasants have suffered rigorous population decline over the last 30 years. Major pathogens of pheasants include roundworms (Heterakis isolonche, Syngamus trachea, Ascaridia spp. and Capillaria spp.) and coccidia (Eimeria spp.), which are widespread in reared and wild game birds and may reduce breeding rates (Edosomwan and Igetei, 2018EDOSOMWAN, E.U. and IGETEI, E.J., 2018. Ecto-and endo-parasites of domestic birds in Owan west, east and Akoko-Edo in Edo state of Nigeria. International Journal of Zoology Studies, vol. 3, pp. 28-35.). Ostrich farming has been started where these birds did not exist previously. Ostrich parasites and diseases reported in Africa include tapeworm, nematodes, anthrax, ophthalmia, ticks and lices. Health problems and mortality diagnosed mainly in juveniles and chicks include intestinal obstruction, leg abnormalities, starvation, malnutrition and coliform infections (Huchzermeyer, 1997HUCHZERMEYER, F.W., 1997. Public health risks of ostrich and crocodile meat. Revue Scientifique et Technique, vol. 16, no. 2, pp. 599-604. http://dx.doi.org/10.20506/rst.16.2.1051. PMid:9501374.
http://dx.doi.org/10.20506/rst.16.2.1051...
). Investigations in ducks and chickens managed under parallel conditions like pigeons have exposed high prevalence of gastrointestinal helminths (Muhairwa et al., 2007MUHAIRWA, A.P., MAOFFE, P.L., RAMADHANI, S., MOLLEL, E.L., MTAMBO, M.M. and KASSUKU, A.A., 2007. Prevalence of gastro-intestinal helminthes in free –range ducks in Morogoro Municipality, Tanzania. The Indian Veterinary Journal, vol. 1, pp. 1-5.) which impairs health and production of these birds (Adriano and Cordeiro, 2001ADRIANO, E.A. and CORDEIRO, N.S., 2001. Prevalence and intensity ofHaemoproteus columbaein three species of wild doves from Brazil. Memorias do Instituto Oswaldo Cruz, vol. 96, no. 2, pp. 175-178. http://dx.doi.org/10.1590/S0074-02762001000200007. PMid:11285493.
http://dx.doi.org/10.1590/S0074-02762001...
). Characterization of pathogenic microbes and parasites from avian species has become mandatory to improve flock health (Roto et al., 2015ROTO, S.M., RUBINELLI, P.M. and RICKE, S.C., 2015. An introduction to the avian gut microbiota and the effects of yeast-based prebiotic-type compounds as potential feed additives. Frontiers in Veterinary Science, vol. 2, pp. 28. http://dx.doi.org/10.3389/fvets.2015.00028. PMid:26664957.
http://dx.doi.org/10.3389/fvets.2015.000...
; Gilbert et al., 2016GILBERT, J.A., QUINN, R.A., DEBELIUS, J., XU, Z.Z., MORTON, J., GARG, N., JANSSON, J.K., DORRESTEIN, P.C. and KNIGHT, R., 2016. Microbiome-wide association studies link dynamic microbial consortia to disease. Nature, vol. 535, no. 7610, pp. 94-103. http://dx.doi.org/10.1038/nature18850. PMid:27383984.
http://dx.doi.org/10.1038/nature18850...
). Changes in peoples’ lifestyles and closer contacts with animals have accelerated parasitic and bacterial infections. It is perhaps due to closer interaction with adopted small animals, which are accepted and treated as a family member in communities. In addition, the microbes may also have zoonotic importance and can affect the attendants and farmers (Best et al., 2017BEST, A.A., PORTER, A.L., FRALEY, S.M. and FRALEY, G.S., 2017. Characterization of gut microbiome dynamics in developing pekin ducks and impact of management system. Frontiers in Microbiology, vol. 7, pp. 2125. http://dx.doi.org/10.3389/fmicb.2016.02125. PMid:28101086.
http://dx.doi.org/10.3389/fmicb.2016.021...
). Present study is therefore planned to find out interspecific variations in ectoparasites and endoparasitic prevalence in selected avian species in captivity.

2. Materials and Methods

Selected captive avian species including chukar partridge (Alectoris chukar), albino pheasant (Phasianus colchicus), silver pheasant (Lophura nycthemera), rose-ringed parakeet (Psittacula krameri) and turkey (Meleagris gallopavo) (Figure 1) were maintained at Avian Conservation and Research Center, Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Ravi Campus (31.044398, 73.874542) (Figure 2) for parasitic analysis. At least ten mature birds (5♂ & 5 ♀) of each species were maintained at different cages. Each cage was provided with separate feeding and water facilities. Birds were vaccinated for chronic respiratory disease fowl cholera and Newcastle disease.

Figure 1
Selected captive avian species including A: Chukar partridge (Alectoris chukar) B: Albino pheasant (Phasianus colchicus C: Silver pheasant (Lophura nycthemera) D: Turkey (Meleagris gallopavo) and E: Rose-ringed parakeet (Psittacula krameri).
Figure 2
Avian Conservation and Research Center, Department of Wildlife and Ecology, UVAS , Ravi Campus.

2.1. Ectoparasite analysis

To ascertain ectoparasites, the experimental birds viz. chukar partridge (Alectoris chukar), albino pheasant (Phasianus colchicus), silver pheasant (Lophura nycthemera), rose-ringed parakeet (Psittacula krameri) and turkeys (Meleagris gallopavo), at least ten birds of each species were visually inspected and their whole body was fully examined on weekly basis. The parasites were collected using forceps, and were observed under stereo microscope and identified (Fokidis et al., 2008FOKIDIS, H.B., GREINER, E.C. and DEVICHE, P., 2008. Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. Journal of Avian Biology, vol. 39, no. 3, pp. 300-310. http://dx.doi.org/10.1111/j.0908-8857.2008.04248.x.
http://dx.doi.org/10.1111/j.0908-8857.20...
).

2.2. Fecal sampling and parasite analysis

Fresh fecal droppings of chukar partridge (Alectoris chukar), albino pheasant (Phasianus colchicus), silver pheasant (Lophura nycthemera), rose-ringed parakeet (Psittacula krameri) and turkeys (Meleagris gallopavo) were collected and brought to the Postgraduate Lab, Department of Wildlife an Ecology, University of Veterinary and Animal Sciences, Lahore, Pakistan for corpological examination. The samples were examined by direct fecal smear method, simple floatation and sedimentation techniques to detect parasitic oocytes and/or egg. Later on, quantitative fecal sample examination, in term of oocysts per gram of feces was conducted using Macmaster’s egg counting technique. The oocytes were repeatedly examined for micrometery (Soulsby, 2005SOULSBY, E.J.L., 2005. Helminths, arthropods and protozoa of domesticated animals. 7th ed. London: Baillière, pp. 763-778.). The species identification action was based on morphology of oocysts and eggs (Fokidis et al., 2008FOKIDIS, H.B., GREINER, E.C. and DEVICHE, P., 2008. Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. Journal of Avian Biology, vol. 39, no. 3, pp. 300-310. http://dx.doi.org/10.1111/j.0908-8857.2008.04248.x.
http://dx.doi.org/10.1111/j.0908-8857.20...
).

2.3. Blood sampling and parasitic analysis

For collection and identification of endoparsaites, the blood samples of chukar partridge (Alectoris chukar), albino pheasant (Phasianus colchicus), silver pheasant (Lophura nycthemera), rose-ringed parakeet (Psittacula krameri) and turkeys (Meleagris gallopavo) were collected on fortnightly basis for a period of one year. Blood was collected directly from brachial vein; a drop was placed on a clean microscopic slide and blood smears was prepared. The smear was then fixed with methyl alcohol and stained with Giemsa's stain for 10 to 15 minutes. The slides were washed with distilled water, dried and examined under microscope for blood parasites. Parasites were identified by using taxonomic key (Fokidis et al., 2008FOKIDIS, H.B., GREINER, E.C. and DEVICHE, P., 2008. Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. Journal of Avian Biology, vol. 39, no. 3, pp. 300-310. http://dx.doi.org/10.1111/j.0908-8857.2008.04248.x.
http://dx.doi.org/10.1111/j.0908-8857.20...
).

3. Result and Discussion

Spatial and temporal dissimilarities are well documented in parasitic prevalence and these differences are recognized with intermediate hosts (Cooper, 2005COOPER, J.E., 2005. Birds of prey. Health and disease. 3rd ed. Oxford: Blackwell Publishing, 120 p.). In Asia, Helminth species are greatly distributed and are highly diverse (Bagust, 1994BAGUST, T.J., 1994. Improving health for poultry production in Asia: a development perspective. Avian Pathology, vol. 23, no. 3, pp. 395-404. http://dx.doi.org/10.1080/03079459408419011. PMid:18671108.
http://dx.doi.org/10.1080/03079459408419...
). During present study, nine helminthes species were recorded including six of nematodes C. anatis, Ascardia galli, Syngamus trachea, Capillaria annulata, , Heterakis gallinarum and Allodopa suctoria, two species of trematodes P. macrorchis, Prosthogonimus ovatus, and one species of cestode Raillietina echinobothrida. Heterakis gallinarum, Ascardia galli and Capillaria annulata are main parasitic species of poultry. Important helminthic diseases of poultry are cestodiosis and ascariodiosis (Fatihu et al., 1991FATIHU, M.Y., OGBOGU, V.C., NIOKU, C.O. and SAROR, D.I., 1991. Comparative studies of gastrointestinal helminthes of poultry in Zaria, Nigeria. Revue D’Elelevage et de Medecin Veterinaire des Pays Troicaux, vol. 44, pp. 175-177.). One hundred helminth species have been identified from wild and domesticated avian species. Parasitic infections may result in stunted growth and egg laying in bird (Card and Neshein, 1972CARD, E.L. and NESHEIN, R., 1972. Poultry production. Philadelphia: Lea and Febiger. ). Nematodes cause serious infection of digestive tract in bird (Gylstorff and Grimm, 1998GYLSTORFF, I. and GRIMM, F., 1998. Vogelkrankheiten. 2nd ed. Stuttgart: Verlag Eugen Ulmer.).

Blood and fecal samples of chukar partridge (Alectoris chukar), albino pheasant (Phasianus colchicus), silver pheasant (Lophura nycthemera), rose-ringed parakeet (Psittacula krameri) and turkeys (Meleagris gallopavo) were analyzed to check parasitic prevalence in these birds (Table 1). To record parasites these five avian species were placed kept in separate cages. 100 fecal and 100 blood samples for each bird species were inspected to analyze internal parasites. During present study, 17 species of endoparasites 14 from fecal samples and three from blood were examined. Two species of ectoparasites i.e. mite Dermanyssus gallinae 42% and fowl ticks Args persicus 41%were studied (Table 2 and 3). Blood parasites included Plasmodium juxtanucleare 50%, Leucoctoyzoon simond having parasitic prevalence 40%, and Aegyptinella pullorum having parasitic prevalence of 40%. Parasitic species recorded from fecal samples included 6 species of nematodes viz. Allodpa suctoria 2%. Syngamus trachea with parasitic prevalence of 60%, Capillaria annulata 37.5%, Ascardia galli 24%, Capillaria anatis 40% and Heterakis gallinarum 28.3%. Similarly, two species of trematodes viz. Prosthogonimus ovatus having parasitic prevalence of 50% and Prosthogonimus macrorchis 21% were also documented from fecal avian samples. Single cestode species Raillietina echinobothrida having parasitic prevalence of 72% and 3 protozoan species i.e. Eimeria maxima having parasitic prevalence of 21%, Giardia lamblia 41% and Histomonas meleagridis 18% were documented during corpological analysis (Table 4).

Table 1
Fecal parasites of different captive avian species their prediction site, morphology, life cycle, clinical diagnosis and control measure.
Table 2
Blood parasites, their prediction sites, morphology, life cycle and clinical diagnosis.
Table 3
Ectoparasites, their prediction sites, morphology, life cycle and clinical diagnosis.
Table 4
Identification of parasites in different captive avian species during present study.

4. Conclusions and Recommendations

During present investigation, two species of ectoparasites and 17 endoparasitic species; 14 from fecal samples and 3 from blood were identified. Proper sanitation, medication and vaccination of bird’s enclousres are suggested to avoid parasites.

References

  • ADRIANO, E.A. and CORDEIRO, N.S., 2001. Prevalence and intensity ofHaemoproteus columbaein three species of wild doves from Brazil. Memorias do Instituto Oswaldo Cruz, vol. 96, no. 2, pp. 175-178. http://dx.doi.org/10.1590/S0074-02762001000200007 PMid:11285493.
    » http://dx.doi.org/10.1590/S0074-02762001000200007
  • BAGUST, T.J., 1994. Improving health for poultry production in Asia: a development perspective. Avian Pathology, vol. 23, no. 3, pp. 395-404. http://dx.doi.org/10.1080/03079459408419011 PMid:18671108.
    » http://dx.doi.org/10.1080/03079459408419011
  • BEST, A.A., PORTER, A.L., FRALEY, S.M. and FRALEY, G.S., 2017. Characterization of gut microbiome dynamics in developing pekin ducks and impact of management system. Frontiers in Microbiology, vol. 7, pp. 2125. http://dx.doi.org/10.3389/fmicb.2016.02125 PMid:28101086.
    » http://dx.doi.org/10.3389/fmicb.2016.02125
  • CARD, E.L. and NESHEIN, R., 1972. Poultry production Philadelphia: Lea and Febiger.
  • COOPER, J.E., 2005. Birds of prey. Health and disease 3rd ed. Oxford: Blackwell Publishing, 120 p.
  • DZUGAN, M., SZOSTEK, M. and PIENIAZEK, M., 2010. Using of pheasants (Phasianus colchicus L.) in biomonitoring of soil environment [in Polish]. Scientific Papers of Polish Ecological Engineering and Polish Soil Science Society, vol. 13, pp. 49-50.
  • EDOSOMWAN, E.U. and IGETEI, E.J., 2018. Ecto-and endo-parasites of domestic birds in Owan west, east and Akoko-Edo in Edo state of Nigeria. International Journal of Zoology Studies, vol. 3, pp. 28-35.
  • FATIHU, M.Y., OGBOGU, V.C., NIOKU, C.O. and SAROR, D.I., 1991. Comparative studies of gastrointestinal helminthes of poultry in Zaria, Nigeria. Revue D’Elelevage et de Medecin Veterinaire des Pays Troicaux, vol. 44, pp. 175-177.
  • FOKIDIS, H.B., GREINER, E.C. and DEVICHE, P., 2008. Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. Journal of Avian Biology, vol. 39, no. 3, pp. 300-310. http://dx.doi.org/10.1111/j.0908-8857.2008.04248.x
    » http://dx.doi.org/10.1111/j.0908-8857.2008.04248.x
  • FORSMAN, J.T., HJERNQUIST, M.B., TAIPALE, J. and GUSTAFSSON, L., 2008. Competitor density cues for habitat quality facilitating habitat selection and investment decisions. Behavioural Ecology, vol. 19, no. 3, pp. 539-545. http://dx.doi.org/10.1093/beheco/arn005
    » http://dx.doi.org/10.1093/beheco/arn005
  • FREITAS, M.F.L., OLIVERIA, J.B., CAVALCANTI, M.D.B., LEITI, A.S., MAGALHAES, V.S., OLIVERIA, R.A. and EVENCIO-SOBRINO, A., 2002. Gastrointestinal parasites of captive wild birds in Pernambuco state, Brazil. Parasitología Latinoamericana, vol. 57, pp. 50-54.
  • GILBERT, J.A., QUINN, R.A., DEBELIUS, J., XU, Z.Z., MORTON, J., GARG, N., JANSSON, J.K., DORRESTEIN, P.C. and KNIGHT, R., 2016. Microbiome-wide association studies link dynamic microbial consortia to disease. Nature, vol. 535, no. 7610, pp. 94-103. http://dx.doi.org/10.1038/nature18850 PMid:27383984.
    » http://dx.doi.org/10.1038/nature18850
  • GYLSTORFF, I. and GRIMM, F., 1998. Vogelkrankheiten. 2nd ed. Stuttgart: Verlag Eugen Ulmer.
  • HUCHZERMEYER, F.W., 1997. Public health risks of ostrich and crocodile meat. Revue Scientifique et Technique, vol. 16, no. 2, pp. 599-604. http://dx.doi.org/10.20506/rst.16.2.1051 PMid:9501374.
    » http://dx.doi.org/10.20506/rst.16.2.1051
  • LOISEAU, C., IEZHOVA, T., VALKIUNAS, G., CHASAR, A., HUTCHINSON, A., BUERMANN, W., SMITH, T.B. and SEHGAL, R.N., 2010. Spatial variation of haemosporidian parasite infection in African rain forest bird species. The Journal of Parasitology, vol. 96, no. 1, pp. 21-29. http://dx.doi.org/10.1645/GE-2123.1 PMid:19860532.
    » http://dx.doi.org/10.1645/GE-2123.1
  • MUHAIRWA, A.P., MAOFFE, P.L., RAMADHANI, S., MOLLEL, E.L., MTAMBO, M.M. and KASSUKU, A.A., 2007. Prevalence of gastro-intestinal helminthes in free –range ducks in Morogoro Municipality, Tanzania. The Indian Veterinary Journal, vol. 1, pp. 1-5.
  • ROTO, S.M., RUBINELLI, P.M. and RICKE, S.C., 2015. An introduction to the avian gut microbiota and the effects of yeast-based prebiotic-type compounds as potential feed additives. Frontiers in Veterinary Science, vol. 2, pp. 28. http://dx.doi.org/10.3389/fvets.2015.00028 PMid:26664957.
    » http://dx.doi.org/10.3389/fvets.2015.00028
  • SOULSBY, E.J.L., 2005. Helminths, arthropods and protozoa of domesticated animals. 7th ed. London: Baillière, pp. 763-778.
  • VALKIŪNAS, G., SEHGAL, R.N.M., IEZHOVA, T.A. and SMITH, T.B., 2005. Further observations on the blood parasites of birds in Uganda. Journal of Wildlife Diseases, vol. 41, no. 3, pp. 580-587. http://dx.doi.org/10.7589/0090-3558-41.3.580 PMid:16244068.
    » http://dx.doi.org/10.7589/0090-3558-41.3.580
  • WOOD, M.J., COSGROVE, C.L., WILKIN, T.A., KNOWLES, S.C.L., DAY, K.P. and SHELDON, B.C., 2007. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology, vol. 16, no. 15, pp. 3263-3273. http://dx.doi.org/10.1111/j.1365-294X.2007.03362.x PMid:17651202.
    » http://dx.doi.org/10.1111/j.1365-294X.2007.03362.x

Publication Dates

  • Publication in this collection
    26 Nov 2021
  • Date of issue
    2024

History

  • Received
    14 July 2021
  • Accepted
    31 Aug 2021
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
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