Caracterização morfológica e molecular de <i>Haemoproteus coatneyi</i> e <i>Haemoproteus erythrogravidus</i> (Haemosporida: Haemoproteidae) em Passeriformes da Mata Atlântica, Brasil

Oliveira, Luísa de; Barino, Glauber Thiago Martins; Rossi, Mariana Fonseca; D’Agosto, Marta; Dias, Roberto Júnio Pedroso; Santos, Huarrisson Azevedo

Luísa de Oliveira

Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Juiz de Fora, MG, Brasil

Glauber Thiago Martins Barino

Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Juiz de Fora, MG, Brasil

Mariana Fonseca Rossi

Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Juiz de Fora, MG, Brasil

Marta D’Agosto

Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Juiz de Fora, MG, Brasil

Roberto Júnio Pedroso Dias

Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Juiz de Fora, MG, Brasil

Huarrisson Azevedo Santos ^**Corresponding author: Huarrisson Azevedo Santos. E-mail: huarrisson@yahoo.com.br

Departamento de Epidemiologia e Saúde Pública, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro – UFRRJ Seropédica, RJ, Brasil

http://orcid.org/0000-0002-8218-3626

*Corresponding author: Huarrisson Azevedo Santos. E-mail: huarrisson@yahoo.com.br

Figuras (6)
Tabelas (1)

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Figure 1
Haemoproteus coatneyi in the blood of Tangara sayaca (lineage TSJB01). Young and growing gametocytes (a – d); macrogametocytes (e – k); microgametocytes (l – p). Arrowheads indicate the pigment granules. Arrows indicate the nucleus of the parasites. Bar = 12 µm.

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Figure 2
Haemoproteus erythrogravidus in the blood of Zonotrichia capensis (lineage ZCSB01). Young gametocytes (a – d); macrogametocytes (e – j); microgametocytes (k – p). Black arrowheads indicate pigment granules. Black arrow indicates the parasite’s nucleus. White arrowheads indicate attenuation in the central part of the gametocytes. Black arrows with open heads indicate vacuoles. White arrows indicate protrusions formed in the infected erythrocytes. Bar = 11 µm.

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Figure 3
Haemoproteus erythrogravidus in the blood of Zonotrichia capensis (lineage ZCSB02). Young gametocytes (a – d); macrogametocytes (e – j); microgametocytes (k – p). White arrowheads indicate attenuation in the central part of the gametocytes. Black arrow indicates the parasite’s nucleus. Black arrows with open heads indicate vacuoles. Black arrow heads indicate pigment granules. White arrows indicate protrusions formed in the infected erythrocytes. Bar = 11 µm.

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Figure 4
Bayesian Inference (BI) based on 479 bp fragments of the mitochondrial cytb gene. The sequences used in the analysis were obtained from the MalAvi and GenBank databases, whose access numbers are in parentheses. The sequences of H. coatneyi and H. erythrogravidus were gathered in four groups (Clades I - IV), one of them being formed by sequences of these two species (Clade II a-b). The sequences of the present study are given in bold font inside the gray frame. Leucocytozoon buteonis was used as outgroup.

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Figure 5
Genetic divergence based on 479 bp fragments of the mitochondrial cytb gene between Haemoproteus coatneyi and Haemoproteus erythrogravidus lineages used in phylogenetic analyses. The lineages of the present study are given in bold font.

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Figure 6
Hosts and geographical distribution of Haemoproteus coatneyi and Haemoproteus erythrogravidus lineages.

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Table 1
Comparative morphometry of the gametocytes of Haemoproteus coatneyi in Tangara sayaca and Haemoproteus erythrogravidus in Zonotrichia capensis.

Characteristic	*H. coatneyi* ^a a All measurements are provided in minimum and maximum values. The averages are in parentheses together with the standard deviation;	*H. coatneyi*	H. erythrogravidus ^a	*H. erythrogravidus*
Characteristic	(This study)	Burry-Caines & Bennett (1992) Burry-Caines JR, Bennett GF. The Haemoproteidae (Apicomplexa: Haemosporina) of the avian families Fringillidae and Emberizidae s.I. Can J Zool 1992; 70(6): 1149-1160. http://dx.doi.org/10.1139/z92-161. http://dx.doi.org/10.1139/z92-161...	(This study)	Mantilla et al. (2016) Mantilla JS, González AD, Lotta IA, Moens M, Pacheco MA, Escalante AA, et al. Haemoproteus erythrogravidus n. sp. (Haemosporida, Haemoproteidae): description and molecular characterization of a widespread blood parasite of birds in South America. Acta Trop 2016; 159: 83-94. http://dx.doi.org/10.1016/j.actatropica.2016.02.025. PMid:26995696. http://dx.doi.org/10.1016/j.actatropica....
Uninfected erythrocytes	n = 21	n = 135	n = 21	n = 25
Length	10.9–13 (11.9 ± 0.5)	11.9 (0.8)	10.1–11.9 (11 ± 0.5)	10.3-11.7 (10.9 ± 0.4)
Width	6–7.1 (6.3 ±0.3)	6.2 (0.6)	5.6–6.7 (6.2 ± 0.3)	5.8-6.5 (6.1 ± 0.2)
Area	53.6–71.6 (60.9 ± 3.8)	59.2 (7.4)	46.7–60.6 (55.2 ± 3.7)	41.8-56.3 (47.9 ± 3.7)

Nucleus of uninfected erythrocytes
Length	5.3–6.4 (5.8 ± 0.3)	5.5 (0.5)	5.1–6.1 (5.6 ± 0.3)	4.7-5.6 (5.1 ± 0.1)
Width	2.3–3.1 (2.6 ± 0.2)	2.4 (0.3)	2.4–3.1 (2.7 ± 0.2)	1.9-2.4 (2.1 ± 0.1)
Area	11.6–15.3 (13.4 ± 1)	11.0 (1.8)	11.6–14.2 (13.1 ± 0.8)	7.5-9.1 (8.2 ± 0.5)

Macrogametocytes	n = 21	n = 150	n = 21	n = 25
Infected erythrocytes
Length	11.2–13.3 (12.4 ± 0.5)	12.3 (0.9)	11–13 (11.8 ± 0.5)	10.3-11.7 (11.1 ± 0.5)
Width	4.7–7.1 (5,9 ± 0.6)	6.2 (0.7)	5–7.4 (6.4 ± 0.7)	5.4-7.2 (6.4 ± 0.7)
Area	54.1–74.1 (63.4 ± 6.1)	63.4 (8.7)	52.7–72.1 (64.2 ± 5.2)	49.6-56.7 (52.7 ± 2.1)
Nucleus of infected erythrocytes
Length	4.4–5.7 (5.1 ± 0.3)	5.4 (0.5)	5.1–6.1 (5.6 ± 0.3)	4.1-5 (4.6 ± 0.2)
Width	1.7–2.7 (2.3 ± 0.2)	2.3 (0.4)	2.3–3.6 (2.7 ± 0.3)	2-2.2 (2.1 ± 0.05)
Area	9.1–12.8 (10.4 ± 1.1)	10.6 (2.1)	10.5–17 (12.8 ± 1.3)	6.4-8 (7.4 ± 0.5)

Gametocytes	n = 21	n = 150	n = 21	n = 25
Length	11.4–15 (13.1 ±1.1)	16.5 (3.4)	11.4–14.1 (12.9 ± 0.7)	10.3-12 (11.1 ± 0.6)
Width	1.5–3.2 (2.1 ± 0.4)	2.0 (0.9)	0.9–2.1 (1.4 ± 0.3)	2.3-7.2 (4.1 ± 1.7)
Area	30.8–50.6 (36.8 ± 5.9)	39.4 (7.9)	26.3–37.8 (31.7 ± 3.8)	34.3-40 (36.9 ± 1.8)
Nucleus of Gametocytes
Length	1.3–3.3 (2.2 ± 0.5)	2.4 (0.6)	1.3–3 (2.2 ± 0.4)	1.4-3.1 (2.2 ± 0.4)
Width	0.7–2.0 (1.2 ± 0.3)	2.1 (0.5)	0.8–1.9 (1.4 ± 0.3)	1-2.2 (1.6 ± 0.39)
Area	1.4–4.9 (2.8 ± 0.9)	4.4 (1.6)	1.5–4.1 (2.8 ± 0.8)	2.3-4.5 (3.6 ± 0.7)
No. Pigment granules	9–17 (13 ± 2.7)	11.6 (2.9)	8–14 (11 ± 1.6)	12-17 (13.5 ± 1.6)
NDR^b	0.4–1 (0.8 ± 0.2)	0.8 (0.2)	0.8–1.3 (1 ± 0.1)	0.5-0.8 (0.6 ± 0.1)

Microgametocytes	n = 21	—	n = 21	n = 11
Infected erythrocytes
Length	11.7–13.4 (12.6 ± 0.5)	—	11.1–12.9 (12 ± 0.5)	13.8 -16.9 (15.3 ± 1)
Width	5.1–7.7 (6.4 ± 0.8)	—	6–7.7 (6.8 ± 0.4)	6.8-8.4 (7.6 ± 0.6)
Area	52.5–78.9 (67.4 ± 7.5)	—	56.6–74 (65.8 ± 4.2)	36.7-45.9(40.6 ± 2.9)
Nucleus of infected erythrocytes
Length	5.1–6 (5.5 ± 0.3)	—	5.2–6.1 (5.7 ± 0.3)	6.2-8.2 (6.9 ± 0.6)
Width	2.1–3 (2.5 ± 0.2)	—	2.5–3.7 (2.9 ±0.3)	2.2 – 3.1 (2.6 ± 0.3)
Area	10.9–13.7 (12.3 ± 0.7)	—	11.1–16.9 (13.7 ± 1.5)	15.4 - 21.7(18 ± 2.1)

Gametocytes	n = 21	—	n = 21	n = 11
Length	12.3–14.9 (13.4 ± 0.8)	—	12.9–15.4 (14.2 ± 0.9)	8.4 -12.1 (10.4 ± 1.2)
Width	1.7–4.3 (2.9 ± 0.8)	—	2.5–3.7 (2.9 ± 0.3)	0.7- 3.3 (2.1 ± 0.7)
Area	31.1–54 (43.9 ± 6.6)	—	30–44.1 (36.5 ± 3.9)	21.3-30.6 (27.4 ± 2.7)
Nucleus of Gametocytes	—	—	—	—
Length	—	—	—	—
Width	—	—	—	—
Area	—	—	—	—
Number of Pigment granules	9–16 (12.2 ± 2.1)	—	7–13 (9.7 ± 1.8)	8-15(10 ± 1.2)
NDR^b b Range of variation and the average value of the nuclear displacement ratio (NDR) of infected erythrocytes which is calculated according to the formula: NDR = 2x/(x+y) Bennett & Campbell (1972).	0–0.9 (0.4 ± 0.2)	—	0.7–1.2 (0.9 ± 0.1)	0.7-1.2 (0.9 ± 0.1)

[1] *Corresponding author: Huarrisson Azevedo Santos. E-mail: huarrisson@yahoo.com.br

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Caracterização morfológica e molecular de Haemoproteus coatneyi e Haemoproteus erythrogravidus (Haemosporida: Haemoproteidae) em Passeriformes da Mata Atlântica, Brasil

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