Biodiversity of parasites found in the trahira, <i>Hoplias malabaricus</i> (Bloch, 1794), collected in the Batalha River, Tietê-Batalha drainage basin, SP, Brazil

GIÃO, THAYANA; PELEGRINI, LARISSA S.; AZEVEDO, RODNEY K. DE; ABDALLAH, VANESSA D.

doi:10.1590/0001-3765202020180610

THAYANA GIÃO

Universidade do Sagrado Coração/USC, Pró-reitoria de Pesquisa e Pós-graduação, Laboratório de Ictioparasitologia, Rua Irmã Arminda, 10-50, Jardim Brasil, 17011-160 Bauru, SP, Brazil

http://orcid.org/0000-0002-9655-5603

LARISSA S. PELEGRINI

Universidade Estadual Paulista/UNESP, Instituto de Biociências de Botucatu, Rua Prof. Dr. Antônio Celso Wagner Zanin, 250, Distrito de Rubião Júnior, 18618-970 Botucatu, SP, Brazil

http://orcid.org/0000-0001-8435-994X

RODNEY K. DE AZEVEDO

Universidade do Sagrado Coração/USC, Pró-reitoria de Pesquisa e Pós-graduação, Laboratório de Ictioparasitologia, Rua Irmã Arminda, 10-50, Jardim Brasil, 17011-160 Bauru, SP, Brazil

http://orcid.org/0000-0002-0471-6079

VANESSA D. ABDALLAH

Universidade do Sagrado Coração/USC, Pró-reitoria de Pesquisa e Pós-graduação, Laboratório de Ictioparasitologia, Rua Irmã Arminda, 10-50, Jardim Brasil, 17011-160 Bauru, SP, Brazil

http://orcid.org/0000-0001-6539-6091

Correspondence to: Vanessa Doro Abdallah E-mail: vanessaabdallahusc@gmail.com

AUTHOR CONTRIBUTIONS

Thayana Gião had a substantial contribution in the concept and study design. She contributed to data collection, data analysis and interpretation, in the manuscript preparation, in the critical revision and adding intellectual content. Larissa Sbeghen Pelegrini contributed to data collection, data analysis and interpretation, in the manuscript preparation, in the critical revision and adding intellectual content. Rodney Kozlowiski de Azevedo contributed to data collection, in the critical revision, adding intellectual content. Vanessa Doro Abdallah had a substantial contribution in the concept and study design. She contributed to data analysis and interpretation, in the critical revision and adding intellectual content.

Parasite	Location	Reference
Monogenea
Anacanthorus sp.	Paraná River, Brazil	Graça et al. (2013)
	Eastern Amazon basin, Brazil	Ferreira et al. (2017)
	Paraná River, Brazil	Graça et al. (2018)
Cosmetocleithrum bulbocirrus Kristsky, Thatcher and Boeger, 1986	Paraná River, Brazil	Graça et al. (2013)
Dactilogyridae gen. sp.	Mogi-Guassu River, Brazil	Kohn et al. (1985)
	Brazil	Rosim et al. (2011)
	Paraná River, Brazil	Graça et al. (2013)
	Eastern Amazon basin, Brazil	Ferreira et al. (2017)
Dactylogyrus spp.	Paraíba State, Brazil	Bernadino et al. (2016)
Gyrodactilus trairae Boeger and Popazoglo 1995	Eastern Amazon basin, Brazil	Ferreira et al. (2017)
Monogenea gen. sp.	Paraná River, Brazil	Takemoto et al. (2009)
	Paraná, Brazil	Kohn et al. (2011)
	Amazônia Ocidental, Brazil	Malacarne & Godoi (2012)
	Maranhão State, Brazil	Rodrigues et al. (2017)
Vancleaveus janauacaensis Kristsky, Thatcher and Boeger, 1986	Paraná River, Brazil	Graça et al. (2013)
Urocleidoides brasiliensis Rosim, Mendoza-Franco and Luque, 2011	Brazil	Rosim et al. (2011)
	Paraná River, Brazil	Graça et al. (2013)
	Eastern Amazon basin, Brazil	Ferreira et al. (2017)
Urocleidoides cuiabai Rosim, Mendoza-Franco and Luque, 2011	Brazil	Rosim et al. (2011)
	Paraná River, Brazil	Graça et al. (2013)
	Paraná River, Brazil	Gasques et al. (2015)
	Eastern Amazon basin, Brazil	Ferreira et al. (2017)
Urocleidoides eremitus Kristsky, Thatcher and Boeger, 1986	Perú, Brazil	Iannacone & Luque (1993)
	Brazil	Rosim et al. (2011)
	Paraná River, Brazil	Graça et al. (2013)
	Amapá, Brazil	Gonçalvez et al. (2016)
	Eastern Amazon basin, Brazil	Ferreira et al. (2017)
	Amapá, Brazil	Alcântara & Tavares-Dias (2015)
Urocleidoides malabaricusi Rosim, Mendoza-Franco and Luque 2011	Brazil	Rosim et al. (2011)
	Paraná River, Brazil	Graça et al. (2013)
	Paraná River, Brazil	Gasques et al. (2015)
Urocleidoides naris Rosim, Mendoza-Franco and Luque, 2011	Brazil	Rosim et al. (2011)
Urocleidoides naris Rosim, Mendoza-Franco and Luque, 2011	Eastern Amazon basin, Brazil	Ferreira et al. (2017)
Digenea
Austrodiplostomum compactum (Lutz, 1928)	Paraná River, Brazil	Machado et al. (2005)
	Tietê River, Brazil	Paes et al. (2010)
	Paraná River, Brazil	Santos et al. (2012)
	Doce River, Brazil	Belei et al. (2013)
	Paranapanema River, Brazil	Ramos et al. (2013)
Austrodiplostomum sp.	São Francisco River, Brazil	Corrêa et al. (2014)
Austrodiplostomum sp.	São Francisco River, Brazil	Costa et al. (2015)
Clinostomum complanatum Rudolphi, 1814	Paraná River, Brazil	Dias et al. (2003)
Clinostomum marginatum (Rudolphi, 1819)	Amapá, Brazil	Gonçalvez et al. (2016)
Clinostomum marginatum (Rudolphi, 1819)	Amapá, Brazil	Alcântara & Tavares-Dias (2015)
Clinostomatopsis sorbens (Braun, 1899) Dollfus1932	Marajó Island, Brazil	Benigno et al. (2014)
Dendrorchis neivai Travassos, 1926	Amapá, Brazil	Gonçalvez et al. (2016)
Dendrochis sp.	Santa Maria, Brazil	Weiblen & Brandão (1992)
Digenea gen. sp.	Paraná River, brazil	Takemoto et al. (2009)
Diplostomidae gen. sp.	Paraná, Brazil	Kohn et al. (2011)
Genarchella genarchella Kohn & Fernandes, 1988	Amapá, Brazil	Gonçalvez et al. (2016)
Genarchella sp.	Quebrada Juan Grande, Brazil	Choudhury et al. (2016)
Ithyoclinostomum dimorphum (Diesing,1850) Witenberg, 1926	Chaco Province, Argentina	Szidat (1969)
	Santa Maria, Brazil	Weiblen & Brandão (1992)
	Rio Grande do Sul State, Brazil	Gallio et al (2007)
	Lajes Reserve, Brazil	Paraguassú & Luque (2007)
	Doce River, Brazil	Belei et al (2013)
	Marajó Island, Brazil	Benigno et al. (2014)
Ithyoclinostomum sp.	São Francisco River, Brazil	Costa et al. (2015)
Phyllodistomum spatula Odhner, 1902	São Francisco River, Brazil	Costa et al. (2015)
Posthodiplostomum sp.	Amapá, Brazil	Gonçalvez et al. (2016)
Pseudosellacotyla lutzi (Freitas, ١٩٤١)	Mogi Guaçu River, Brazil	Kohn et al. (1985)
	Mogi Guaçu River, Brazil	Kohn & Fernandes (1987)
	Parana River, Brazil	Fernandes & Kohn (2001)
	Chocó, Colômbia	Perez-Caicedo et al. (2010)
	Paraná, Brazil	Kohn et al. (2011)
	São Francisco River, Brazil	Costa et al. (2015)
	Argentina	Núñez et al. (2017)
Sphincterodiplostomum musculosum (Dubois, 1936)	Chaco Province, Argentina	Szidat (1969)
Thometrema overstreeti(Brooks et al., ١٩٧٩)	Perú, Brazil	Iannacone & Luque (1993)
Tylodelphylus s Province1 (Szidat, 1969)	Chaco Province, Argentina	Szidat (1969)
Tylodelphylus s Province1 (Szidat, 1969)	Santa Maria, Brazil	Weiblen & Brandão (1992)
Nematoda
Amplicaecum sp.	Mogi Guaçu River, Brazil	Kohn & Fernandes (1987)
Brevimulticaecum sp.	Pantanal, Brazil	Vieira et al. (2010)
Contracaecum sp.	Uruguai	Lent & Teixeira de Freitas (1948)
	Iguaçú River, Brazil	Kohn et al. (1988)
	Santa Maria, Brazil	Weiblen & Brandão (1992)
	Barinas State, Venezuela	Moravec et al. (1997)
	Jaguari River, Brazil	Madi & Silva (2005)
	Maranhão State, Brazil	Martins et al. (2005)
	Lajes Reserve, Brazil	Paraguassú & Luque (2007)
	Córdoba	Pardo et al (2008)
	Cuiabá River, Brazil	Barros et al. (2008)
	Cuiabá River, Brazil	Barros et al. (2009)
	Paraná, Brazil	Kohn et al. (2011)
	Marajó Island, Brazil	Benigno et al. (2012)
	Pirassununga, Brazil	Corrêa et al. (2013)
	Dique Channel, Colombia	Olivero-Verbel & Caballero - Gallardo (2013)
	Argentina	Mancini et al. (2014)
	São Francisco River, Brazil	Corrêa et al. (2015)
	Trinidad	Suepaul et al. (2015)
	Amapá, Brazil	Gonçalvez et al. (2016)
	Dr. João Penido Dam, Brazil	Carvalho et al. (2017)
	Amapá, Brazil	Baia et al. (2018)
	Amapá, Brazil	Alcântara & Tavares-Dias (2015)
Contracaecum multipapillatum (von Drasche, 1882)	Cuiabá River, Brazil	Fontenelle et al. (2017)
Cystidicoloides sp.	Amapá, Brazil	Gonçalvez et al. (2016)
Eustrongylides ignotus Jäegerskiold, 1909	Dr. João Penido Dam, Brazil	Carvalho et al. (2017)
Eustrongylides sp.	Paraná River, Brazil	Martins et al. (2009)
	Rondonia, Brazil	Meneguetti et al. (2013)
	Trinidad	Suepaul et al. (2015)
Guyanema baudi Petter & Dlouhy (1985)	Santa Maria, Brazil	Weiblen & Brandão (1992)
Guyanema raphiodoni Moravec, Kohn and Fernandes, 1993	Paraná, Brazil	Kohn et al. (2011)
Nematoda	Mato Grosso State, Brazil	Barros et al. (2007)
Nematoda	Paraná River, Brazil	Takemoto et al. (2009)
Paracappilaria piscicola Travassos, Artigas & Pereria, 1928	Santa Maria, Brazil	Weiblen & Brandão (1992)
Parasseuratum soaresi	Santa Maria, Brazil	Weiblen & Brandão (1992)
Physalopteridae gen. sp.	Uruguai	Lent & Freitas (1948)
Procamallanus (Spirocamallanus) inopinatus Travassos, Artigas and Pereira, 1928	Mogi Guaçu River, Brazil	Kohn & Fernandes (1987)
	Amazonas River, Brazil	Baia et al. (2018)
	Amapá, Brazil	Gonçalvez et al. (2016)
	Amapa	Alcântara & Tavares-Dias (2015)
Procamallanus (Spirocamallanus) ihering Travassos, Artigas and Pereira, 1928	Mogi Guaçu River, Brazil	Kohn & Fernandes (1987)
Procamallanus (Spirocamallanus) hilarii Vaz and Pereira, 1934	Santa Maria, Brazil	Weiblen & Brandão (1992)
	Santiago del Estero, Argentina	Ramallo (1997)
	Dr. João Penido Dam, Brazil	Carvalho et al. (2017)
Procamallanus (Procamallanus) peraccuratus Pinto et al. 1976	Santa Maria, Brazil	Weiblen & Brandão (1992)
Hirudinea
Glossiphonidae gen. sp.	Amapá, Brazil	Gonçalvez et al. (2016)
Glossiphonidae gen. sp.	Lajes Reserve, Brazil	Paraguassú & Luque (2007)
Mizobdella platensis (Cordero, 1933)	Santa Fé Province, Argentina	Cordero (1933)
Mizobdella platensis (Cordero, 1933)		Lopretto (1995)

Species	Point 1			Point 2
	P (%)	MA ± SE	MI ± SE	P (%)	MA ± SE	MI ± SE
Monogenea
Urocleidoides sp.	2.3	0.02 ± 0.02	1	-	-	-
Urocleidoides margolisi Molnar, Hanek and Fernando, 1974	4.5	0.1 ± 0.1	2.5 ± 2.1	-	-	-
Urocleidoides aimarai Moreira, Scholz and Luque, 2015	2.3	0.02 ± 0.02	1	2.7	0.03 ± 0.03	1
Urocleidoides cuiabai	38.6	3.0 ±1.05	7.7 ± 2.3	37.8	2.0 ± 0.5	5.3 ± 0.8
Urocleidoides malabaricusi	22.7	2.0 ± 0.7	8.7 ± 2.5	10.8	0.4 ± 0.2	3.5 ± 0.6
Urocleidoides eremitus	15.9	1.6 ± 0.7	9.8 ± 3.2	-	-	-
Jainus leporini Abdallah, Azevedo and Luque, 2012	2.3	0.02 ± 0.02	1	8.1	0.1 ± 0.3	1.7 ± 0.3
Sciadicleithrum sp.	2.3	0.02 ± 0.02	1	5.4	0.1 ± 0.1	1.5 ± 0.5
Scleroductus sp.	6.8	0.2 ± 0.14	3 ± 1.5	2.7	0.1 ± 0.1	3
Anacanthorus sp.	6.8	0.3 ± 0.2	4.3 ± 0.7	8.1	0.6 ± 0.5	7.3 ± 5.4
Dactylogyridae gen. sp.	6.8	0.8 ± 0.5	11.3 ± 5.5	-	-	-
Gyrodactilus trairae	2.3	0.1 ± 0.2	1	2.7	0.4 ± 0.4	15
Nothogyrodactylus sp.	2.3	0.04 ± 0.04	1	-	-	-
Digenea
Ithyoclinostomum dimorphum	2.2	0.02 ± 0.03	1	27	0.3 ± 0.1	1.1 ± 0.1
Austrodiplostomum compactum	31.8	1 ± 0.40	3.1 ± 1	21.6	0.3 ± 0.1	1.4 ± 0.2
Austrodiplostomum mordax (Szidat and Nani, 1951)	-	-	-	5.4	0.1 ± 0.1	2.5 ± 0.5
Phyllodistomum rhandiae (Amato and Amato, 1993)	29.5	1.4 ± 0.5	4.8 ± 1.3	2.7	0.2 ± 0.2	6
Tylodelphys sp.	65.9	36.7 ± 9.3	55.6 ± 12.8	37.8	10.8 ± 5.7	28.6 ± 14.1
Clinostomum sp.	4.5	0.04 ± 0.03	1	-	-	-
Bucephalidae gen. sp.	27.2	1.2 ± 0.5	4.6 ± 1.3	8.1	0.2 ± 0.1	2.6 ± 1.2
Nematoda
Goezia brasiliensis Moravec, Kohn and Fernandes, 1994	-	-	-	10.8	1.0 ± 0.6	9.0 ± 3.8
Contracaecum sp.	38.6	1.06 ± 0.4	2.6 ± 0.7	70.2	7.4 ± 1.5	10.6 ± 1.8
Spirox contortus (Rudolphi, 1819)	-	-	-	2.7	0.03 ± 0.03	1
Procamallanus (Spirocamallanus) inopinnatus Travassos, Artigas and Pereira, 1928	13.6	0.1 ± 0.07	1.3 ± 0.3	5.4	0.1 ± 0.1	1.5 ± 0.5
Guyanema baudi Petter and Dloughy, 1985	-	-	-	2.7	0.03 ± 0.03	1
Spinitectus rodolphihering Vaz and Pereira, 1934	4.5	0.1 ± 0.1	2.5 ± 1.5	2.7	0.05 ± 0.05	2
Eustrongylides sp.	-	-	-	2.7	0.03 ± 0.03	1
Hirudinea
Placobdella sp.	2.2	0.06 ± 0.07	3	5.4	0.08 ± 0.5	1.5 ± 0.5
Helobdella sp.	4.5	0.09 ± 0.07	2 ± 1.5	-	-	-

Species	Point 1		Point 2
	DF (%)	RD	DF (%)	RD
Monogenea
Urocleidoides sp.	0	0	0	0
Urocleidoides margolisi	0	0	0	0
Urocleidoides aimarai	0	0	0	0.001
Urocleidoides cuiabai	6.8	0.06	2.7	0.08
Urocleidoides malabaricusi	6.8	0.04	2.7	0.01
Urocleidoides eremitus	2.3	0	0	0
Jainus leporini	0	0.002	0	0.005
Sciadicleithrum sp.	0	0.03	0	0.003
Scleroductus sp.	0	0.004	0	0.003
Anacanthorus sp.	0	0.005	0	0.02
Dactylogyridae gen. sp.	0	0.01	0	0
Gyrodactilus trairae	0	0.003	0	0.02
Nothogyrodactylus sp.	0	0	0	0
Digenea
Ithyoclinostomum dimorphum	0	0	0	0.01
Austrodiplostomum compactum	4.5	0.02	0	0.01
Austrodiplostomum mordax	0	0.03	0	0.005
Phyllodistomum rhandiae	4.5	0	0	0.006
Tylodelphys sp.	47.7	0.7	19	0.4
Clinostomum sp.	0	0	0	0
Bucephalidae gen. sp.	0	0.02	0	0.008
Nematoda
Goezia brasiliensis	0	0	0	0.04
Contracaecum sp.	9.1	0.02	54	0.30
Spirox contortus	0	0	0	0.001
Procamallanus (Spirocamallanus) inopinnatus	0	0.003	0	0.003
Guyanema baudi	0	0	0	0.001
Spinitectus rodolphihering	0	0.002	0	0.002
Eustrongylides sp.	0	0	0	0.001
Hirudinea
Placobdella sp.	0	0.001	0	0.003
Helobdella sp.	0	0.001	0	0

Species	Point 1			Point 2
	DI	d	GI	DI	d	GI
Urocleidoides cuiabai	16.31	37.32	0.35	5.11	10.78	0.11
Urocleidoides malabaricusi	12.19	32.2	0.26	3.57	7.63	0.07
Urocleidoides eremitus	15.01	35.81	0.32	-	-	-
Austrodiplostomum compactum	6.13	22.77	0.11	1.28	1.20	0.007
Phyllodistomum rhandiae	7.74	25.63	0.15	-	-	-
Tylodelphys sp.	104.09	94.56	2.39	111.41	22.63	3.06
Bucephalidae gen. sp.	7.85	25.8	0.15	-	-	-
Ithyoclinostomum dimorphum	-	-	-	0.90	-0.36	0
Contracaecum sp.	5.46	21.47	0.10	10.77	19.44	0.27
Goezia brasiliensis	-	-	-	13.38	22.63	0.34
Procamallanus (Spirocamallanus) inopinnatus	1.60	11.36	0.01	-	-	-

Species	Point 1				Point 2
	Abundance x SL		Abundance x W		Abundance x SL		Abundance x W
	rs	(p)	rs	(p)	rs	(p)	rs	(p)
Urocleidoides cuiabai	-0.15	0.90	-0.21	0.18	0.37	0.02*	0.43	0.01*
Urocleidoides malabaricusi	-0.15	0.34	-0.21	0.18	0.10	0.54	0.13	0.45
Urocleidoides eremitus	-0.14	0.37	-0.22	0.15	-	-	-	-
Austrodiplostomum compactum	-0.01	0.96	0.11	0.47	0.18	0.28	0.25	0.13
Phyllodistomum rhandiae	0.25	0.09	0.25	0.11	-	-	-	-
Tylodelphys sp.	0.02	0.90	0.10	0.52	0.25	0.13	0.29	0.08
Bucephalidae gen. sp.	0.27	0.08	0.30	0.04*	-	-	-	-
Ithyoclinostomum dimorphum	-	-	-	-	0.00	0.99	0.01	0.97
Contracaecum sp.	0.04	0.78	0.02	0.90	-0.55	< 0.0001*	-0.73	< 0.0001*
Goezia brasiliensis	-	-	-	-	-0.20	0.23	-0.18	0.30
Procamallanus (Spirocamallanus) inopinnatus	-0.05	0.77	0.03	0.85	-	-	-	-

Species	Point 1		Point 2
	Z (U)	p	Z (U)	p
Urocleidoides cuiabai	0.73	0.22	13.4	0.09
Urocleidoides malabaricusi	0.46	0.31	0.51	0.31
Urocleidoides eremitus	0.15	0.43	-	-
Austrodiplostomum compactum	0.49	0.31	0.39	0.35
Phyllodistomum rhandiae	0.1	0.45	-	-
Ithyoclinostomum dimorphum	-	-	0.15	0.43
Tylodelphys sp.	0.12	0.44	0.39	0.35
Bucephalidae gen. sp.	0.55	0.29	-	-
Goezia brasiliensis	-	-	10.4	0.15
Contracaecum sp.	0.43	0.33	0.19	0.42
Procamallanus (Spirocamallanus) inopinnatus	10.44	0.14	-	-

	Point 1	Point 2
D	0.75 ± 0.59	0.68 ± 0.48
H	0.54 ± 0.45	0.50 ± 0.34
J’	0.51 ± 0.35	0.59 ± 0.33
H/M	0.93	0.70

[1] Correspondence to: Vanessa Doro Abdallah E-mail: vanessaabdallahusc@gmail.com

Brasil

Brasil

Biodiversity of parasites found in the trahira, Hoplias malabaricus (Bloch, 1794), collected in the Batalha River, Tietê-Batalha drainage basin, SP, Brazil

Abstract