COCCIDIA IN PASSERINES FROM THE LA
LOMA SANTA MARIA PROTECTED NATURAL
AREA, MICHOACAN, MEXICO
COCCIDIAS EN PASSERIFORMES DEL ÁREA NATURAL
PROTEGIDA LA LOMA DE SANTA MARÍA,
MICHOACÁN, MÉXICO
Claudia Guzmán-Lara
Universidad Michoacana de San Nicolás de Hidalgo, México
Alejandro Villaseñor Alvarez
Universidad Michoacana de San Nicolás de Hidalgo, México
Rufino Osorio Marquez
Universidad Michoacana de San Nicolás de Hidalgo, México
pág. 1367
DOI: https://doi.org/10.37811/cl_rcm.v8i4.12381
Coccidia in Passerines from the la Loma Santa Maria Protected Natural
Area, Michoacan, Mexico
Claudia Guzmán-Lara1
claudia.guzman@umich.mx
https://orcid.org/0000-0002-5903-0584
Departamento de Parasitología
Facultad de Medicina Veterinaria y Zootecnia
Universidad Michoacana de San Nicolás de
Hidalgo
México
Alejandro Villaseñor Alvarez
alejandro.villaseñor@umich.mx
https://orcid.org/0009-0000-2990-7050
Departamento de Parasitología
Facultad de Medicina Veterinaria y Zootecnia
Universidad Michoacana de San Nicolás de
Hidalgo
México
Rufino Osorio Marquez
rufino.osorio@umich.mx
https://orcid.org/0000-0002-2044-9484
Departamento de Parasitología
Facultad de Medicina Veterinaria y Zootecnia
Universidad Michoacana de San Nicolás de
Hidalgo
México
ABSTRACT
The objective of the present study was to find the presence of coccidia in passerine birds in the La
Loma de Santa María Protected Natural Area, Michoacán, Mexico. Non-sporulated coccidial oocysts
were found in passerine birds in that locality. A total of 61 birds were captured during three field
surveys from December 2022 to April 2023, obtaining fecal samples that were examined. A total of
39 samples examined were positive for non-sporulated coccidial oocysts. The bird species sampled
were: Red Warbler (Cardellina rubra)1 Russet Ruisset Thrush (Catharus occidentalis)1; Cordilleran
Flycatcher (Empidonax occidentalis)2; Yellow-throated euponia (Euphonia hirundinacea)1; common
finch (Haemorhous mexicanus)1; Nashville Warbler (Leiothlypis ruficapilla)1; Blue mockingbird
(Melanotis caerulescens)6; Lincoln's sparrow (Melospiza lincolnii)4; Rusty-crowned ground sparrow
(Melozone kieneri)1; Black and white warbler (Mniotilta varia)3; Brown-backed Solitaire (Myadestes
occidentalis)1; Slate-colored Solitaire (Myadestes unicolor)2; Yellow-tailed grackle (Quiscalus
mexicanus)7; Yellow-rumped Warbler (Setophaga coronata)1; Plumbeous Vireo (Vireo plumbeus);1.
This is the first study to examine passerine birds from Michoacán.
Keywords: coccidia, Mexico, passerines
1
Autor principal
Correspondencia: claudia.guzman@umich.mx
pág. 1368
Coccidias en Passeriformes del Área Natural Protegida la Loma de Santa
María, Michoacán, México
RESUMEN
El objetivo del presente estudio fue encontrar la presencia de coccidias en aves paseriformes, en el
Área Natural Protegida La Loma de Santa María, Michoacán, México. Se encontraron ooquistes de
coccidios no esporulados en aves paseriformes, en esa localidad. Se capturaron un total de 61 aves
durante tres muestreos de campo desde diciembre de 2022 hasta abril de 2023, obteniendo muestras
de heces que fueron examinadas. Un total de muestras examinadas fueron 39 positivas a ooquistes de
coccidios no esporulados. Las especies de aves muestreadas fueron: Reinita Roja (Cardellina rubra)1
Zorzal Ruisset Russet (Catharus occidentalis)1; Papamoscas Cordillerano (Empidonax occidentalis)2;
Eufonía de garganta amarilla (Euphonia hirundinacea)1; Pinzón común (Haemorhous mexicanus)1;
Reinita de Nashville (Leiothlypis ruficapilla)1; Sinsonte azul (Melanotis caerulescens)6; Gorrión de
Lincoln (Melospiza lincolnii)4; Gorrión de tierra corona oxidada (Melozone kieneri)1; Reinita blanca y
negra (Mniotilta varia )3; Solitario de lomo marrón (Myadestes occidentalis)1; Solitario de color
pizarra (Myadestes unicolor)2; Zanate de cola amarilla (Quiscalus mexicanus)7; Reinita rabadilla
amarilla (Setophaga coronata)1; Vireo plomizo (Vireo plumbeus); )1. Este es el primer estudio que
examina aves paseriformes de Michoacán.
Palabras clave: coccidios, México, paseriformes
Artículo recibido 27 junio 2024
Aceptado para publicación: 30 julio 2024
pág. 1369
INTRODUCTION
Protozoa parasites of the genera Eimeria or Isospora infect avian species. In diseased birds, signs may
include diarrhea, fever, inappetence, weight loss and emaciation (SEMARNAT 2016; Villaseñor
2005). Nevertheless, many infections are subclinical (Constable 2014). Other vertebrates can be
parasitized with coccidia, being Isospora Schneider 1881, considered the genus most important,
before the genus Eimeria Schneider 1875 (Pereira et al. 2011).
The passerine order contains more than half of the world’s birds, considered the most diversified
group of vertebrates with more than 5,700 identified in 110 families of this taxonomic order (Ohlson
et al. 2013) 46 families with 533 species a total at distribute in Mexico (Berlanga et al. 2020). La
Loma de Santa María Protected Natural Area Michoacan, Mexico 23 families including been
registered 97 species of passerines (iNaturalist 2017; Shivaprasad 2014).
There is almost no research on the presence of coccidia in wild birds from Mexico (Pereira and Lopes
2013) and nothing from the state of Michoacan. The presence of coccidia in passerine birds at
Michoacan State are unknown. Hence the aim this present study was the identification of the presence
of coccidia oocysts in passerines birds from the La Loma de Santa Maria Protected Natural Area,
Michoacan, Mexico.
METHODOLOGY
Sixty-two passerines were caught with six mist nets (19°40´41´´ N; 101°10´23´´ W), on and
longitudinal gradient ranging from 1,920 to 2,390 (m a.l.s.) (Chávez, 1993) from October 2022 to
April 2023, the mist nets were placed in the first 7 hours after dawn for three days followed for visit,
with sufficient distance between them so as not to interfere with the capture and in its manipulation.
The birds were withdrawing from the nets and placed in cotton bags designed for this activity, after
defecation were released, the stool samples, were processed by the technique of direct observation,
with an ocular microscope in 10X and 40X objetives. The activity was carried out with the scientific
collection permit number 08964 granted by the secretary of environment and natural resources
(Gobierno Constitucional del Estado de Michoacán de Ocampo 2009; Fair et al. 2010; NOM-059-
SEMARNAT-2010; Ralph and Sauer 1995; SEMARNAT 2016).
pág. 1370
RESULTS
The 62 stool samples, were processed periodically according to corresponding field sampling within
12 hours after the collection (Ralph and Sauer 1995). Positive results to unsporulated coccidia oocysts
were found in 39 samples, however they were all kept refrigerated at 7°C, and processed again (all at
the same time) to confirm their absolute positivity (Rodríguez and Cob 2005). The second processing
of the samples was carried out in Centro de Investigación y Estudios Avanzados en Salud Animal
(CIESA). A total of 39 of them positive to unsporulated coccidia oocysts; Red Warbler (Cardellina
rubra) (1); Russet Nightingale-Thrush (Catharus occidentalis) (1); Cordilleran Flycatcher
(Empidonax occidentalis) (2); Yellow-throated Euphonia (Euphonia hirundinacea) (1); House Finch
(Haemorhous mexicanus) (1); Nashville Warbler (Leiothlypis ruficapilla (1); Blue Mockingbird
(Melanotis caerulescens) (6); Lincoln’s Sparrow (Melospiza lincolnii) (4); Rusty-crowned Ground-
Sparrow (Melozone kieneri) (1); Black and White Warbler (Mniotilta varia) (3); Brown-backed
Solitaire (Myadestes occidentalis) (1); State-colored Solitaire (M. unicolor) (2); House Sparrow
(Passer domesticus) (1); Hepatic Tanager (Piranga flava) (1); Great-tailed Grackle (Quiscalus
mexicanus) (7); Yellow-rumped Warbler (Setophaga coronata) (1); Curve-billed Trasher (Toxostoma
curvirostre) (3); Warbling Vireo (Vireo gilvus) (1) and Plumbeous Vireo (V. plumbeus) (1),that
represent the 62% of positivity of the total simples obtained in that period.
DISCUSSION
63% of the birds studied were positive to unsporulated coccidia oocysts, significant results because of
61 birds captured, 39 were positive, representing more than 50% of parasitized passerine birds of the
presence of these unicellular parasites in four endemic birds; Red Warbler (Cardellina rubra); Russet
Nightingale-Thrush (Catharus occidentalis); Blue Mockingbird (Melanotis caerulescens); Rusty-
crowned Ground-Sparrow (Melozone kieneri) (Berlanga et al. 2020). The difficult to detect and study
in protected areas being important to confirm its biological value and reinforce the arguments for its
protection. More studies are needed to better understand the coccidias that infect passerines birds,
considering that the information on this parasitic disease in wild birds is insufficient to generate
research that strongly documents what is happening with these apicomplexan parasites and their
impact on the health of wild birds. Afterwards, we performed an extensive search of the following
pág. 1371
keywords (in Spanish, English, and Latin): coccidia, coccidiosis, oocyst, oocysts, oocisto, oocistos,
Eimeria, Isospora, ave, aves, pájaro, pájaros, bird, birds, passerine, Passeriformes, Mexico, in the
most popular databases (e.g. Web of Knowledge, PubMed, Searchable Ornithological Research
Archive, Scopus, SciELO, Redalyc). Some studies were found on the presence of coccidia in
passerines in the State of Mexico, which was useful to strengthen the present study. A publication on
coccidia in wild passerines from the Americas was also found but did not show records for Mexico
(Pereira and Lopes 2013). Therefore, our study appears to provide the first evidence of the presence of
coccidia in passerine birds in the west of the country.
CONCLUSIONS
The resistance of the coccidia oocyst in the environment and the immune conditions of the hosts make
them susceptible to suffering from coccidia. Let us remember that it was only in a limited area, with
the possibility that the negative processed samples could be false negatives.
Acknowledgements
We acknowledge the Comite of Protected Areas in Michoacan for the facilities provided to carry out
this study, to the parasitology area of the FMVZ-UMSNH for immediate sample processing, to the
Benito Juárez de Michoacan zoological park for their support in the field work, to CIESA-FMVZ-
UAEM project 5000/2020CIB and Consejo Nacional de Ciencia y Tecnología (CONACYT), we also
acknowledge the iBird International.
REFERENCES
1. Berlanga, H., Gómez de Silva, H., Vargas-Canales, V.M., Rodríguez-Contreras, V., Chávez
Hernández, A. (1993). Decreto Área Natural protegida, con el carácter de zona sujeta a
conservación ecológica la loma de Santa María y depresiones aledañas en el municipio de
Morelia, Michoacán México, Diario Oficial de la Federación 2‒3.
2. Constable P.D., Winter, A., Abuelo, A., Allen D.G., Porter, R., Brutlag, A., Carter K.K.
(2014). The Merck Manual of Diagnosis and Therapy. Harvard University Press, Cambridge,
USA 498 pp.
pág. 1372
3. Fair J.M., Paul E, Jones J., Barrett C.A., Davi C., Kaiser G. (2010) Guía para la utilización de
aves silvestres en investigación. 3th ed. Consejo de Ornitología Washington, DC. USA, 51‒62
pp.
4. Gobierno Constitucional del Estado de Michoacán de Ocampo. (2009) Decreto por el que se
declara como zona de restauración y protección ambiental La Loma de Santa María y
depresiones aledañas, del municipio de Morelia. Periódico Oficial del Gobierno
Constitucional del Estado de Michoacán de Ocampo. Web electronic publication
https://en15dias.com/wp-content/uploads/2023/05/DECRETO-LOMA-DE-SANTA-MARIA-
2009.pdf. 8/23.
5. iNaturalist-Aves de México. (2017). National Geographic, California Academy of Sciences.
Web electronic publication https://www.inaturalist.org/projects/aves-de-la-loma-de-santa-
maria-y-depresiones-aledanas-morelia-michoacan. 3/21.
6. Norma Oficial Mexicana NOM-059-SEMARNAT-2010. (2010). Protección Ambiental
Especies nativas de México de flora, fauna y silvestres. Categorías de riesgo. Estados Unidos
Mexicanos. Diario Oficial de la Federación.
7. Ohlson L.I., Irestedt M., Ericson P.G.P., Fjeldså J. (2013). Phylogeny and classification of the
New World suboscines (Aves, Passeriformes). Zootaxa, 3613,001‒035.
8. Pereira Berto, B. and Gomes Lopes, C.W. (2013). Distribution and dispersion of coccidia in
wild passerines of the Americas in Birds Evolution and behavior breeding strategies migration
and spread of disease. Nova Science Publishers, Inc, New York. 47‒65.
9. Pereira Berto, B., Gomes Lopes, W., McIntosh, D., Teixeira-Filho, W.L. and Lopes Carlos,
W.G. (2011). Coccidia of the New World passerine birds (Aves: Passeriformes) a review of
Eimeria Schneider, 1875 and Isospora Schneider,1981 (Apicomplexa: Eimeriidae).
Systematic Parasitology, 80,159‒204.
10. Ralph C.J., Sauer J.R., Droege, S. (1995). Monitoring Bird Populations by Point Counts. Gen.
Tech. Rep. PSW-GTR-149. Albany, CA Pacific Southwest Research Station Forest Service,
U.S editors Department of Agriculture, USA, 187‒217 pp.
pág. 1373
11. Rodríguez V.R.I and Cob G.L.A. (2005) Técnicas diagnósticas en parasitología veterinaria
México. Universidad Autónoma de Yucatán, México, 20‒24 pp.
12. Sánchez-González, L.A. Ortega-Álvarez, R y Calderón-Parra, R. (2021). Aves de México
Lista actualizada de especies y nombres comunes. CONABIO, xico, DF. Web electronic
publication, https://www.gob.mx/conabio. 6/20
13. SEMARNAT (Secretaria de Medio Ambiente y Recursos Naturales). (2016). Licencia de
colecta científica con propósitos de enseñanza en materia de vida silvestre. Gobierno de
México. Web electronic publication https://www.gob.mx/tramites/ficha/licencia-de-colecta-
cientifica-con-propositos-de-ensenanza-en-materia-de-vida-silvestre/SEMARNAT442. 10/20.
14. Shivaprasad H.L. (2014) Bird pathology. California Animal Health y Food Safety Laboratory
System, School of Veterinary Medicine, University of Southern California University. Press
USC, USA, 289‒291 pp.
15. Villaseñor G. (2005) La biodiversidad en Michoacán. Estudio de Estado Comisión Nacional
para el Conocimiento y Uso de la Biodiversidad. Secretaría de Urbanismo y Medio Ambiente.
Universidad Michoacana de San Nicolás de Hidalgo, México 101‒103 pp.