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Haemoparasites in Endemic and Non-Endemic Passerine Birds from Central Mexico Highlands T

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Haemoparasites in Endemic and Non-Endemic Passerine Birds from Central Mexico Highlands T IJP: Parasites and Wildlife 11 (2020) 88–92 Contents lists available at ScienceDirect IJP: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw Haemoparasites in endemic and non-endemic passerine birds from central Mexico highlands T Daphne Villalva-Pasillasa, J.P. Medinab, Edgardo Soriano-Vargasc, David Alejo Martínez-Hernándezd, Michele García-Conejoa, Karla Patricia Galindo-Sánchezb, ∗ Jessica Mariana Sánchez-Jassob, Martín Talavera-Rojasc, Celene Salgado-Mirandac, a Programa de Maestría en Ciencias Agropecuarias y Recursos Naturales, Universidad Autónoma del Estado de México, Toluca, Estado de México, Mexico b Institute for Biodiversity Research, Development and Sustainability (iBIRDS), Toluca, Estado de México, Mexico c Centro de Investigación y Estudios Avanzados en Salud Animal, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma del Estado de México, Carretera Toluca-Atlacomulco km 15.5, C. P. 50295, Toluca, Estado de México, Mexico d Profesionales en Veterinaria, Metepec, Estado de México, Mexico ARTICLE INFO ABSTRACT Keywords: Haemosporidian parasites of birds are found worldwide and include the genera Haemoproteus, Plasmodium and Haemoparasites Leucocytozoon. Infection with haemosporidian parasites can affect host physical condition and reproductive Passeriformes success. The aim of this study was to identify the blood parasites and parasitaemia in endemic and non-endemic Endemic passerine birds from central Mexico highlands. This study included 157 passerines representing 29 species from Bird 17 families. Overall, 30.6% (48/157) of the birds were infected with blood parasites. Of those, Haemoproteus spp. Mexico were found in 14.0% (n = 22), Leucocytozoon spp. 12.1% (n = 19) and microfilariae 0.6% (n = 1). Blood Haemoproteus Leucocytozoon parasites were found in 71.4% (5/7) of endemic bird species and 45.4% (10/22) of non-endemic species. Microfilariae Medium to high parasitaemia (number of parasites/number erythrocytes) was observed in birds with infections of Haemoproteus spp. and Leucocytozoon spp. Co-infections 3.8% (n = 6) were observed in two species of en- demic birds. This study contributes to the knowledge of haemoparasites in endemic and non-endemic passerine birds from central Mexico highlands. Additional investigation on the molecular identification of haemosporidian parasites, pathogenicity and health status of these birds is necessary. 1. Introduction species and species ranging farther north or south in the Americas (Peterson and Navarro-Sigüenza, 2016). Worldwide, there are ap- Parasites are organisms which live for a considerable portion of proximately 10,500 bird species, of which 1,123 to 1,150 are in Mexico; their lives in (endoparasites) or on (ectoparasites) another different from these, 194 to 212 species of birds are considered endemic kind of organism, the host. Sometimes, the parasite can cause in the (Navarro-Sigüenza et al., 2014). The first information of haemopar- host some harm. Protozoan and metazoan parasites can induce altera- asites on Mexican birds was reported in 1940 by Beltrán, he analyzed tions in host behaviour or colouration (Poulin, 2007). Parasites of the birds from bird traders (called pajareros [derived from pájaro, the Order: Haemosporida are wide-spread and infect many species of ver- Spanish word for bird]). Beltrán (1940) found 24.7% of the birds tebrates that are exposed to bites of bloodsucking dipteran insects sampled were positive to Plasmodium (11.7%), Haemoproteus (9.4%) (Order: Diptera) (Santiago-Alarcon et al., 2012). Plasmodium, Haemo- and Leucocytozoon (1.1%) with additional co-infection by Plasmodium proteus and Leucocytozoon (Phylum: Apicomplexa; and Order: Hae- with Haemoproteus (2.3%). Further analysis revealed three species of mosporida) are the three most common Haemoparasitic protozoan Plasmodium: P. relictum, P. cathemerium and P. nucleophilum in Mexican genera found in birds (Valkiūnas, 2005). Additionally, Filarioid nema- birds (Hewitt, 1940). Beltrán, 1942a also found parasites of Haemo- todes are haemoparasites; the larval microfilariae have been reported in proteus, Leucocytozoon, Plasmodium and Trypanosoma from 142 blood many organs and tissues of numerous terrestrial vertebrates, including smears of birds captured in northern Mexico, and microfilariae in birds birds (Bartlett, 2008). from northern and south-eastern Mexico (Beltrán, 1942b). More recent Mexico has a megadiverse avifauna that includes endemic bird investigations have identified a new lineage of haemosporidian ∗ Corresponding author. E-mail address: [email protected] (C. Salgado-Miranda). https://doi.org/10.1016/j.ijppaw.2019.12.007 Received 18 June 2019; Received in revised form 21 December 2019; Accepted 27 December 2019 2213-2244/ © 2020 The Author(s). Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). D. Villalva-Pasillas, et al. IJP: Parasites and Wildlife 11 (2020) 88–92 parasites unique to Columbiformes from Grey-headed dove (Leptotila (VBNPA). These locations are contained within the Natural Protected plumbeiceps)(Valkiūnas et al., 2010) and a new Haemoproteus species Area (PNA) of Central Mexico and the Transverse Neovolcanic Axis (H. paramultipigmentatus) from the Socorro Common Ground Dove (CMTNA). The NTNPA polygon (19°12′37″ N, 99°44′42″ W; 19°12′31″ (Columbina passerina socorroensis)(Valkiūnas et al., 2013). Prevalence N, 99°43′51″ W; 19°11′31″ N, 99°44′22″ W; 19°11′47″ N, 99°45′09″ W) and diversity of haemosporidians from the genera Parahaemoproteus is in the State of Mexico at 2,800 to 3,247 m above sea level (m asl). and Leucocytozoon within an individual are similar for blood, muscle Average annual temperature ranges from 18 °C (minimum 9 °C, max- and liver samples; however, Plasmodium exhibits differential detect- imum 22 °C) at low elevation and 12 °C (minimum −3 °C, maximum ability when screened from different tissue types and was more pre- 13 °C) at high elevation. The type of vegetation corresponds to a forest valent in the blood than in muscle and liver tissues (Fecchio et al., with White Cedar (Cupressus lindleyi), Tasmanian Blue Gum (Eucalyptus 2019). The aim of this study was to determine parasite genera, the globulus), Mexican White Pine (Pinus ayacahuite), Mexican Weeping proportion of blood parasites and parasitaemia in endemic and non- Pine (P. patula), and Montezuma Pine (P. montezumae)(Sánchez-Jasso endemic passerine birds from central Mexico highlands. et al., 2013). The VBNPA (19°13′25″ N, 99°57′57″ W; 19°13′26″ N, 99°13′76″ W; 19°12′31″ N, 99°57′27″ W; 19°12′39″ N, 99°56′53″ W) is 2. Materials and methods in the State of Mexico at 2,830 to 2,960 m asl. Average annual tem- perature is 13.4 °C (minimum 0.5 °C, maximum of 29.7 °C). The type of 2.1. Ethical approval vegetation corresponds to a forest with Fir (Abies spp.), Pine (Pinus spp.) and grassland at the foothill (Beltrán and Díaz de la Vega, 2010). Capture methods and sampling of animals were performed under direct supervision of a specialised ornithologist and veterinarian in 2.3. Sample collection and processing accordance with the laws and guidelines of Mexico on Animal Welfare and the specific regulations of the Mexican government. The permits At each study site, eight mist nets were set (8 × 2.5 m) to capture (SGPA/DGVS/07613/14, SGPA/DGVS/00955/16) cover all bird hand- the birds. The nets were placed at relevant points of bird activity as ling in this study and were approved by the SEMARNAT (Secretaría de previously reported (Sánchez-Jasso et al., 2013). Birds were captured Medio Ambiente y Recursos Naturales) of Mexico. from 06:00 to 15:00 h. After capture, we identified, measured, banded, took blood samples via brachial venipuncture and then released the 2.2. Study area birds. The blood was immediately smeared on two slides per bird, air dried, fixed with absolute methanol, and stained with May-Grünwald The study was conducted monthly during three-day samplings Giemsa (Piaton et al., 2015). Slides were labelled with the bird species, periods, from 21 June 2014 to 12 November 2017. The study sites bird band code, and sampling day. We examined entire smears micro- (Fig. 1) were Parque Ecológico Ejidal de Cacalomacán (PEEC) in Ne- scopically (40× and 100×) for the presence of blood parasites using a vado de Toluca Natural Protected Area (NTNPA) and Parque Ecotur- microscope Primo Star, Carl Zeiss, USA. We followed Valkiūnas (2005) ístico Corral de Piedra (PECP) in Valle de Bravo Natural Protected Area procedures for parasite identification. We took photomicrographs of Fig. 1. Location of study sites. (A) Location of the State of Mexico, (B) Location of Nevado de Toluca Natural Protected Area (NTNPA), and Valle de Bravo Natural Protected Area (VBNPA), (C) Parque Ecológico Ejidal de Cacalomacán (PEEC) and (D) Parque Ecoturístico Corral de Piedra (PECP). Datum WGS_1984_UTM Zone 14. 89 D. Villalva-Pasillas, et al. IJP: Parasites and Wildlife 11 (2020) 88–92 Fig. 2. Triple infection of Haemoproteus spp./Leucocytozoon spp./microfilaria in a Catharus occidentalis. (A). Leucocytozoon spp. ( ) and Haemoproteus spp. ( ) parasites. (B). Microfilaria (➤), Leucocytozoon spp. ( ) and Haemoproteus spp. ( ) parasites. (C). Catharus occidentalis infected. Photomicrographs. Scale-bar:10μm. parasites using a Nikon ECLIPSE 80i binocular microscope coupled to a studied, of which 45.4% (10/22 species) were infected. The prevalence Nikon DS-Fi2 digital camera. We estimated intensity of infection as a of infected birds by location (study sites) was greater for PEEC (37.6%, percentage by counting of the number of parasites per 10,000 red blood 32/85 birds) than for PECP (22.2%, 16/72 birds). Significant differ- cells (Godfrey et al., 1987). We classified blood parasite density ences (P = 0.036), were observed in infected birds and location. (number of parasites/number erythrocytes) for infections with Hae- Six birds with co-infections were observed, accounting for 3.8% (6/ moproteus (low < 0.1% erythrocytes infected; medium = 0.1–0.5%; 157) of all infected birds.
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