Systematic and parasite-host relationship by <i>Baruscapillaria appendiculata</i> in <i>Phalacrocorax brasilianus</i> collected from Marajó Island, State of Pará, Brazil

Carvalho, Elaine Lopes de; Santana, Ricardo Luis Sousa; Gonçalves, Evonnildo Costa; Sindeaux Neto, José Ledamir; Silva, Michele Velasco Oliveira da; Giese, Elane Guerreiro

doi:10.1590/S1984-29612023043

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Revista Brasileira de Parasitologia Veterinária

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Original Article • Rev. Bras. Parasitol. Vet. 32 (3) • 2023 • https://doi.org/10.1590/S1984-29612023043 copy

Systematic and parasite-host relationship by Baruscapillaria appendiculata in Phalacrocorax brasilianus collected from Marajó Island, State of Pará, Brazil

Sistemática e relação parasito-hospedeiro por Baruscapillaria appendiculata em Phalacrocorax brasilianus da Ilha de Marajó, Estado do Pará, Brasil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

The genus Baruscapillaria Moravec, 1982 has six valid species recorded in birds Phalacrocoracidae, namely Baruscapillaria appendiculata Freitas, 1933, B. spiculata Freitas, 1933, B. carbonis (Dubinin & Dubinina, 1940), B. jaenschi (Johnston & Mawson, 1945), B. phalacrocoraxi (Borgarenko, 1975) and B. rudolphii Moravec, Scholz and Našincová, 1994. Helminthological tests carried out on cormorants of the species Phalacrocorax brasilianus (Gmelin), a migratory bird that occurs in the northeast of the State of Pará, Brazil, demonstrate B. appendiculata parasitizing the cloaca of these birds, through light microscopy, scanning electron microscopy and molecular biology. These studies allowed a redescription of males and females of this nematode in these hosts and in this geographical area through integrative taxonomy. The occurrence of lesions in the cloaca caused by this nematode parasite was registered using histological analysis. This is a new geographic report for this nematode.

Keywords:
Suliformes; Phalacrocoracidae; Capillariidae; Brazilian Amazon

	(1)	(2)	(3)	(4)	(5)	(6)	(7)	(8)	(9)	(10)	(11)	(12)	(13)	(14)	(15)	(16)	(17)	(18)	(19)
(1) Baruscapillaria appendiculata	-
(2) B. spiculata MT068209	0.010
(3) B. obsignata LC425004	0.039	0.044
(4) Aonchotheca paranalis MF621021	0.058	0.067	0.043
(5) Aonchotheca sp. LC052374	0.067	0.072	0.045	0.024
(6) A. putorii LC052356	0.063	0.070	0.040	0.021	0.016
(7) A. musimon LC052379	0.068	0.076	0.046	0.029	0.022	0.018
(8) Eucoleus sp. LC052381	0.161	0.165	0.133	0.133	0.113	0.115	0.120
(9) Eucoleus sp. LC052382	0.162	0.169	0.140	0.128	0.117	0.118	0.125	0.030
(10) E. contortus LC424996	0.171	0.176	0.145	0.152	0.134	0.132	0.143	0.046	0.047
(11) E. dispar EU004821	0.175	0.178	0.155	0.159	0.145	0.143	0.149	0.049	0.057	0.023
(12) E. aerophilus MW709573	0.188	0.196	0.161	0.163	0.146	0.144	0.152	0.048	0.048	0.020	0.019
(13) E. garfiai LC484432	0.158	0.156	0.137	0.143	0.129	0.128	0.141	0.038	0.039	0.016	0.013	0.008
(14) E. perforans LC424997	0.180	0.187	0.155	0.158	0.140	0.141	0.145	0.049	0.052	0.032	0.034	0.031	0.027
(15) Capillaria madseni LC052347	0.170	0.171	0.157	0.152	0.146	0.154	0.154	0.196	0.201	0.198	0.208	0.216	0.185	0.209
(16) C. anatis LC425001	0.169	0.170	0.145	0.149	0.143	0.144	0.152	0.180	0.190	0.187	0.198	0.196	0.171	0.196	0.096
(17) C. pudendotecta LC052339	0.216	0.219	0.185	0.190	0.169	0.181	0.187	0.213	0.222	0.215	0.237	0.228	0.209	0.241	0.144	0.113
(18) C. spinulosa LC424999	0.220	0.225	0.197	0.193	0.175	0.189	0.192	0.226	0.233	0.227	0.249	0.238	0.221	0.252	0.146	0.133	0.028
(19) C. tenuissima EU004822	0.234	0.244	0.203	0.207	0.197	0.203	0.208	0.242	0.240	0.225	0.239	0.248	0.222	0.249	0.144	0.157	0.185	0.196	-

Morphometric characterization	Baruscapillaria appendiculata		B. obsignata		B. spiculata		B. appendiculata		B. obsignata		B. obsignata		B. jaenschi		B. phalacrocoraxi		B. appendiculata
Specimen sex	Male	Female	Male	Female	Male	Female	Male	Female	Male	Female	Male	Female	Male	Female	Male	Female	Female
Host	Phalacrocorax brasilianus		chicken and turkey		P. brasilianus		P. brasilianus		Cygnus atratus		Chicken		P. sulcirostris, P. fuscescens. P. carbo, P. melanoleucas		P. pygmeus		Cyprinus carpio
Host	Phalacrocorax brasilianus		Small intestine		Cloaca		Large intestine		Small intestine		Small intestine		?		Bursa Fabricius, cloaca		Intestine
Locality	Pará, Brazil		USA		Rio de Janeiro, Brazil		Rio de Janeiro, Brazil		UK		UK		Australia		Asia		Lake Pátzcuaro, Mexico
Total body (L)^a a Measurements in milimeters.	11-16	21-29	8.60-10	10-12.70	16	28	-	22.8	12.35-14.79	16.90-20.50	6.90-12.96	8.28-17.28	9.9	7.1-27.4	9.1-13.7	19.8-24.3	21.83
Maximum body (W) ^b b Esophageal-intestinal junction. ^,^c c Measurements in micrometers.	40-70	53-82	53	-	70	100	64	88-96	46-49	56-64	42-51	49-67	36	37-41	55-66	88-90	75
Nerve-ring (L) ^c,^d d Distance from front end.	43-80	67-130	-	-	-	-	-	-	-	-	-	-	-	-	-	-	111
Muscular esophagus (L) ^c	267-370	348-523	-	-	-	-	-		-	-	-	-	-	-	-	-	399
Muscular esophagus (W) ^c	13-17	17-23	-	-	-	-	-	-	-	-	-	-	-	-	-	77	-
Total esophagus (W) ^a	4.90-6.84	5.17-7.44	-	-	6-7	6-7	-	6.3	-	-	4.23-6.00	4.94-6.70	-	-	3.9-4.3	5.6-5.9	4.78
Stichosome (W) ^a	1.97-6.34	4.68-7.21	-	-	-	-	-	-	-	-	-	-	-	-	-	-	4.39
# Stichocytes	41-52	39-46	-	-	-	-	-	-	-	-	-	-	-	-	-	-	39
Vulva (L) ^a	-	0.058-0.233 ^e e Junction of the intestinal esophagus to the vulva.	-	-	-	0.130 ^e	-	0.072 ^e	-	-	-	-	-	-	-	0.1^e	0.081^e
Eggs mature (L×W) ^c	-	43.27×21.52	-	50-62	-	40-36	-	56-32	-	42-51×22-27	-	44-56×22-29	-	48-50×18-20	-	44-45×22-23	-
Spicule (L) ^a	1.96-2.29	-	1.20	-	2.33	-	1.77	-	1.59-1.78	-	1.09-1.53	-	7	-	3.08-3.30	-	-
Spicule (W) ^d	8-12	-	-	-	-	-	-	-	-	-	-	-	-	-	22-25	-	-
ME/BL (%)	2.41	1.78	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
TE/BL (%)	39	24.30	-	-	14.5	-	-	27.6	-	-	-	-	-	-	-	-	-
# Specimen	10	10	2	3	2	2	2 fragmented	not specified	7	8	100	100	1	?	-	-	1
Reference	In this study		Graybill, 1924Graybill HW. Capillaria columbae (Rud.) from the chicken and turkey. J Parasitol 1924; 10(4): 205-207. http://dx.doi.org/10.2307/3271270. http://dx.doi.org/10.2307/3271270...		Freitas, 1933bFreitas JFT. Sur deux nouvelles espèces du genre Capillaria Zeder, 1800. Compt Rend Soc Biol Paris 1933b; 114: 962-964.		Freitas, 1933aFreitas JFT. Nouvelles espèces du genre Capillaria Zeder, 1800. Compt Rend Soc Biol Paris 1933a; 114: 1195-1196.		Wakelin, 1963Wakelin D. Capillaria obsignata Madsen, 1945 (Nematoda) from the black swan. J Helminthol 1963; 37(4): 381-386. http://dx.doi.org/10.1017/S0022149X00019982. http://dx.doi.org/10.1017/S0022149X00019...		Wakelin, 1965Wakelin D. On species of the genus Capillaria Zeder, 1800 (Nematoda) from British domestic fowl. Parasitology 1965; 55(2): 285-301. http://dx.doi.org/10.1017/S0031182000068761. PMid:14342122. http://dx.doi.org/10.1017/S0031182000068...		Johnston & Mawson, 1945Johnston TH, Mawson PM. Capillariid nematodes from South Australian fishes and birds. Trans R Soc S Aust 1945; 69(2): 243-248.		Baruš & Sergejeva, 1990aBaruš V, Sergejeva TP. A new genus of capillariids from birds, Ornithocapillaria gen. n. (Nematoda: Capillariidae). Folia Parasitol 1990a; 37(3): 237-248. PMid:2227708.		Moravec et al., 2000Moravec F, Salgado-Maldonado G, Osorio-Sarabia D. Records of the bird capillariid nematode Ornithocapillaria appendiculata (Freitas, 1933) n. comb. from freshwater fishes in Mexico, with remarks on Capillaria patzcuarensis Osorio-Sarabia et al., 1986. Syst Parasitol 2000; 45(1): 53-59. http://dx.doi.org/10.1023/A:1006233408872. PMid:10682923. http://dx.doi.org/10.1023/A:100623340887...
Morphometric characterization	*Baruscapillaria appendiculata*		B. appendiculata		B. appendiculata ^h		B. obsignata		B. obsignata		B. obsignata
Specimen sex	Male	Female	Male	Female	Male	Female	Male	Female	Male	Female	Male	Female
Host	*Phalacrocorax brasilianus*		Chirostoma estor		P. brasilianus		Chicken		Cygnus olor		Pheasant
Site of infection	Cloaca		Intestine		Cloaca/large intestine		Small intestine		Small intestine		Small intestine
Locality	Pará, Brazil		Lake Pátzcuaro, Mexico		Rio Grande do Sul, Brazil		Kagoshima, Japan		Yamaguchi, Japan		Kumamoto, Japan
Total body (L)^a	11-16	21-29	9.25^f f Fragment.	14.88-22.13	12.90-16.10	20.70-25.90	5.31-10.61	6.19-10.56	8.58-10.38	10.36-13.67	7.61-8.60	9.02-16.84
Maximum body (W) ^{b, c}	40-70	53-82	48	60-81	42-60	65-90	28-56	52-64	40-58	57-80	35-39	52-65
Nerve-ring (L) ^{c, d}	43-80	67-130	-	84-153	70-90	-	-	-	-	-	-	-
Muscular esophagus (L) ^c	267-370	348-523	-	315-435	360-477	410-530	-	-	-	-	-	-
Muscular esophagus (W) ^c	13-17	17-23	-	-	-	-	-	-	-	-	-	-
Total esophagus (W) ^a	4.90-6.84	5.17-7.44	-	4.54-6.11	4.60-5.70	4.90-7.90	3.61-6.61	3.94-5.64	4.41-5.42	4.66-5.92	4.10-4.97	4.53-5.71
Stichosome (W) ^a	1.97-6.34	4.68-7.21	-	4.21-5.79	4.60-5.70	4.40-7.50	-	-	-	-	-	-
# Stichocytes	41-52	39-46	-	40-45	45-49	43-45	-	-	-	-	-	-
Vulva (L) ^{a, f}	-	0.058-0.233^e	-	0.093-0.171^e	-	0.057-0.137^e	-	0.039-0.072^e	-	0.027-0.110 ^e	-	0.035-0.076^e
Eggs mature (L×W) ^c	-	43.27×21.52	-	57-60×27	-	49-23	-	48-59×24-31	-	-	-	48-26
Spicule (L) ^a	1.96-2.29	-	2.31	-	2.00-3.90	-	0.87-1.26	-	1.03-1.59	-	1.05-1.18	-
Spicule (W) ^c	8-12	-	0.012	-	17-30	-	-	-	-	-	-	-
ME/BL (%)	2.41	1.78	-	-	2.50-3.10	2.90-4.90	-	-	-	-	-	-
TE/BL (%)	39	24.30	-	22-41^g g Moravec 2001 book.	36.05	27.38	-	-	-	-	-	-
# Specimen	10	10	1	6	8	6	22	7	9	6	4	3
Reference	In this study		Moravec et al., 2000Moravec F, Salgado-Maldonado G, Osorio-Sarabia D. Records of the bird capillariid nematode Ornithocapillaria appendiculata (Freitas, 1933) n. comb. from freshwater fishes in Mexico, with remarks on Capillaria patzcuarensis Osorio-Sarabia et al., 1986. Syst Parasitol 2000; 45(1): 53-59. http://dx.doi.org/10.1023/A:1006233408872. PMid:10682923. http://dx.doi.org/10.1023/A:100623340887...		Monteiro, 2006Monteiro CM. Helmintofauna do biguá, Phalacrocorax brasilianus (Gmelin) (Aves, Phalacrocoracidae) do lago Guaíba, Guaíba, RS [dissertation]. Porto Alegre: Universidade Federal do Rio Grande do Sul; 2006.		Tamaru et al., 2015Tamaru M, Yamaki S, Jimenez LA, Sato H. Morphological and molecular genetic characterization of three Capillaria spp. (Capillaria anatis, Capillaria pudendotecta, and Capillaria madseni) and Baruscapillaria obsignata (Nematoda: Trichuridae: Capillariinae) in avians. Parasitol Res 2015; 114(11): 4011-4022. http://dx.doi.org/10.1007/s00436-015-4629-2. PMid:26204803. http://dx.doi.org/10.1007/s00436-015-462...				Sakaguchi et al., 2020Sakaguchi S, Yunus M, Sugi S, Sato H. Integrated taxonomic approaches to seven species of capillariid nematodes (Nematoda: Trichocephalida: Trichinelloidea) in poultry from Japan and Indonesia, with special reference to their 18S rDNA phylogenetic relationships. Parasitol Res 2020; 119(3): 957-972. http://dx.doi.org/10.1007/s00436-019-06544-y. PMid:31811424. http://dx.doi.org/10.1007/s00436-019-065...
Morphometric characterization	*Baruscapillaria appendiculata*		B. obsignata		B. obsignata		B. obsignata		B. spiculata		B. spiculata		B. kamanae
Specimen sex	Male	Male	Male	Male	Male	Female	Male	Female	Male	Female	Male	Female	Male	Female
Host	*Phalacrocorax brasilianus*		Pigeon		Goose		Turkey		P. brasilianus		P. brasilianus		Podiceps cristatus australis
Site of infection	Cloaca		Small intestine		Small intestine		Small intestine		Cloaca		Cloaca		Intestine
Locality	Pará, Brazil		Surabaya, Indonesia		Surabaya, Indonesia		Surabaya, Indonesia		Argentina ⁱ i Buenos Aires, Laguna Chis-Chis.		Argentina ^j j Buenos Aires, Laguna San Miguel del Monte.		New Zealand
Total body (L)^a	11-16	21-29	8.58-11.00	12.67-16.28	7.23-9.67	8.00-12.30	8.95-10.50	12.69-14.65	10.75-17.60	24.00-28.18	12.55-17.25	23.5-27.8	15.2-15.8	23.9-24.3
Maximum body (W) ^{b, c}	40-70	53-82	40-59	66-76	41-45	49-72	41-67	53-75	50-60	60-80	46-60	55-78	51-55	78-86
Nerve-ring (L) ^{c, d}	43-80	67-130	-	-	-	-	-	-	30-75	55-105	35-65	45-95	-	-
Muscular esophagus (L) ^c	267-370	348-523	-	-	-	-	-	-	255-560	435-670	280-580	390-630	-	-
Muscular esophagus (W) ^c	13-17	17-23	-	-	-	-	-	-	-	-	-	-	-	-
Total esophagus (W) ^a	4.90-6.84	5.17-7.44	3.96-5.24	5.22-6.95	4.48-5.15	4.21-6.20	4.65-5.27	5.19-6.31	4.25-5.95	6.35-7.98	3.85-6.05	5.80-7.50	8.4	7.5-10.3
Stichosome (W) ^a	1.97-6.34	4.68-7.21	-	-	-	-	-	-	3.85-5.64	5.90-7.12	4.27-5.61	6.10-7.32	-	-
# Stichocytes	41-52	39-46	-	-	-	-	-	-	32-46	37-48	34-44	35-45	-	-
Vulva (L) ^{a, f}	-	0.058-0.233^e	-	0-0.110^e	-	0.047-0.094^e	-	0.076-0.150^e	-	0.090-0.150^e	-	0.080-0.135^e	-	0.107-0.149
Eggs mature (L×W) ^c	-	43.27×21.52	-	45-49×23-28	-	41-49×23-29	-	42-54×25-30	-	48-55×20-27	-	50-56×20-30	-	45-53×20-24
Spicule (L) ^a	1.96-2.29	-	1.25-1.77	-	1.04-1.36	-	1.19-1.32	-	2.20-2.60	-	2.20-2.53	-	1.48-1.49	-
Spicule (W) ^c	8-12	-	-	-	-	-	-	-	-	-	-	-	-	-
ME/BL (%)	2.41	1.78	-	-	-	-	-	-	-	-	-	-	-	-
TE/BL (%)	39	24.30	-	-	-	-	-	-	32.6-39.2	24.8-29.9	28.11-43.42	25.3-30.3	53	31-43
# Specimen	10	10	6	6	4	9	6	6	10	10	8	8	6	6
Reference	In this study		Sakaguchi et al., 2020Sakaguchi S, Yunus M, Sugi S, Sato H. Integrated taxonomic approaches to seven species of capillariid nematodes (Nematoda: Trichocephalida: Trichinelloidea) in poultry from Japan and Indonesia, with special reference to their 18S rDNA phylogenetic relationships. Parasitol Res 2020; 119(3): 957-972. http://dx.doi.org/10.1007/s00436-019-06544-y. PMid:31811424. http://dx.doi.org/10.1007/s00436-019-065...						Garbin et al., 2021Garbin LE, Digiani MC, Robles MR, Montes MM, Knoff M, Fuchs D, et al. Redescription and molecular characterization of Baruscapillaria spiculata (Nematoda: Capillariidae) parasitizing the Neotropic cormorant Phalacrocorax brasilianus from two Argentinian lagoons. Parasitol Res 2021; 120(5): 1637-1648. http://dx.doi.org/10.1007/s00436-021-07112-z. PMid:33712928. http://dx.doi.org/10.1007/s00436-021-071...				Presswell & Bennett, 2022Presswell B, Bennett J. Gastrointestinal helminth parasites of the threatened Australasian crested grebe (Podiceps cristatus australis, Gould 1844) in New Zealand, with descriptions of Baruscapillaria kamanae n. sp. (Nematoda: Trichuridae) and Cryptocotyle micromorpha n. sp. (Trematoda: Opisthorchiidae). Syst Parasitol 2022; 99(2): 217-239. http://dx.doi.org/10.1007/s11230-022-10022-y. PMid:35124752. http://dx.doi.org/10.1007/s11230-022-100...

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[1] *Corresponding author: Elaine Lopes de Carvalho. E-mail: medvet.elaine@gmail.com