Histopathological evaluation of formalin toxicity in <i>Arapaima gigas</i> (Arapaimidae), the giant fish from Amazon

Andrade-Porto, Sanny M.; Ramos, Cleverson A.; Roque, Rosemary; Affonso, Elizabeth G.; Barcellos, José F.M.; Queiroz, Marieta N.; Araújo, Cleusa S.O.; Tavares-Dias, Marcos

doi:10.1590/1678-5150-PVB-5106

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LIVESTOCK DISEASES • Pesq. Vet. Bras. 38 (06) • June 2018 • https://doi.org/10.1590/1678-5150-PVB-5106 copy

Histopathological evaluation of formalin toxicity in Arapaima gigas (Arapaimidae), the giant fish from Amazon

Avaliação histopatológica da toxicidade da formalina em Arapaima gigas (Arapaimidae), o peixe gigante da Amazônia

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT:

This study aimed to determine the lethal concentration and the structural and ultra-structural effects caused by the formalin exposure on juveniles of Arapaima gigas. Ninety fish (60.1± 2.5g and 20.2±0.9cm) were exposed to 0, 22, 44, 66, 88 and 110mg L^-1 in order to determine the lethal concentration (LC_50-96h) that was 36.4mg L^-1 of formalin. Sublethal effects were evaluated using histopathological analysis on the gills and assessment of behavioral alterations and clinical signs. The LC₅₀ of formalin for 24, 48 and 72h was 88.3, 64.7 and 56.8mg L^-1 respectively. Clinical signs and behavioral changes were found: erratic swimming, lethargy, crowding on the water surface, loss of hydrodynamic equilibrium, spasms and agonistic confrontation, which were observed only at 88 and 110mg L^-1. The histological alteration index (HAI) showed that 66, 88 and 100mg L^-1 presented significant difference (p<0.05) in relation to unexposed fish, indicating that moderate damage to the gills of fish exposed to formalin had occurred. The mean values of alteration (MVA) for 22, 44, 66, 88 and 110mg L^-1 were 1.14, 1.29, 1.51, 1.53 and 1.60 respectively, and differences in this index were only observed with 110 mgL^-1 of formalin. It is therefore possible to conclude that sublethal concentrations of formalin (22.0mg L^-1) did not compromise the health of juveniles of A. gigas. Finally, concentrations greater than to LC_50-96h may be carefully used for short-term exposure, since the MVA for all concentrations tested only indicated localized lesions that did not compromise gills functionality of exposed fish.

INDEX TERMS:
Formalin; toxicity; Arapaima gigas; Arapaimidae; freshwater fish; pirarucu; treatment; histopathology; toxicoses

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[1] *Corresponding author: marcos.tavares@embrapa.br

Formalin concentrations (mg L^-1)
Parameters	0	22	44	66	88	110
DO	7.0±0.3^a	6.8±0.3^a	6.9±0.4^a	6.9±0.4^a	7.1±0.1^a	7.2±0.1^a
Temp	25.8±0.4^a	25.1±0.3^a	25.0±0.3^a	25.5±0.2^a	25.7±0.5^a	25.3±0.4^a
pH	6.2±0.2^a	6.1±0.6_a	6.2±0.4^a	5.8±0.9^a	5.8±0.0^a	6.2±0.0^a
EC	21.7±1.7^a	22.2±2.9^a	22.7±3.7^a	23.2±3.3^a	23.5±1.7^a	23.9±2.4^a
TA	1.2±0.9^a	1.3±0.7^a	1.3±0.8^a	1.3±0.7^a	1.4 ± 0.8^a	1.5±0.03^a
NO₂	0.005±0.0004^a	0.005±0.0008^a	0.005±0.0^a	0.06±0.0^a	0.005±0.0^a	0.005±0.0^a
NO₃	0.05±0.0^a	0.05±0.0^a	0.05±0.0^a	0.05±0.0^a	0.05±0.0^a	0.05±0.0^a
Alkal	11.2±4.8^a	10.4±5.8^a	11.1±4.6^a	10.1±1.2^a	11.3±0.0^a	11.6±0.0^a

Concentration (mg L^-1)	Exposure time (h)
Concentration (mg L^-1)	24	48	72	96
0	0	0	0	0
22	0	0	0	6.6
44	0	20.0	20.0	26.6
66	6.6	40.0	53.4	-
88	33.4	66.6	-	-
110	100	-	-	-

Behavioral alterations	Formalin concentrations (mg L^-1)
Behavioral alterations	0	22	44	66	88	110
Erratic swimming	0^a	0^a	0^a	0^a	4±^b	13±1^b
Lethargy	0^a	0^a	0^a	0^a	1±^a	10±2^b
Concentration at the water surface	0^a	0^a	0^a	0^a	0±0^a	12±1^b
Loss of hydrodynamic balance	0^a	0^a	0^a	0^a	4±^a	14±1^b
Spasms	0^a	0^a	0^a	0^a	0±0^a	8±2^b
Agonistic confrontation	0^a	0^a	0^a	0^a	0±0^a	8±2^b

Clinical signs	Formalin concentrations (mg L^-1)
Clinical signs	0	22	44	66	88	110
Corneal opacity	0^a	0^a	0^a	0^a	1±0^a	6±1^b
Opaque gill	0^a	0^a	0^a	0^a	2±^a	12±2^b
Hyperemia with hemorrhage in the caudal peduncle	0^a	0^a	0^a	0^a	0±^a	2±0^a
Friable gill	0^a	0^a	0^a	0^a	0±^a	12±2^b
Excess mucous on the skin and gill	0^a	0^a	0^a	0^a	3±^a	15±1^b

Alteration	Formalin concentrations (mg L^-1)
Alteration	Stage	0	22	44	66	88	110
Lamellar epithelium hypertrophy	I	0	0	0	0	+	+
Lamellar epithelium hyperplasia	I	0	0	0+	+	++	+++
Proliferation of mucus cells	I	0	0+	+	++	+++	+++
Proliferation of mitochondria-rich cells (MRCs)	I	0	0+	+	++	+++	+++
Constriction of the system of pillar cells	I	0	0	0	0	0	0+
Partial fusion of the lamellae	I	0	0	0	+	+	++
Total fusion of several lamellae	I	0	0	0	++	++	+++
Dilation of the marginal channel	I	0	0	0	+	+	++
Mucus secretion	I	0	0	0	0+	0+	+
Epithelial detachment	I	0	0	0	0+	+	+
Edema	I	0	0	0	+	++	++
Capillary constriction	I	0	0	0	0+	+	++
Lamellar aneurism	II	0	0	0	0+	+	++
Epithelial rupture (hemorrhage)	II	0	0	0	+	+	++

Fish species	LC_50-96h (mg L^-1)	Stage of life	References
Morone saxatilis Walbaum, 1792	7.3	Larva	Wellborn (1969)Wellborn Junior T.L. 1969. The toxicity of nine therapeutic and herbicidal compounds to striped. Progr. Fish-Cult. 31(1):27-32. http://dx.doi.org/10.1577/1548-8640(1969)31[27:TTONTA]2.0.CO;2. https://doi.org/10.1577/1548-8640(1969)3...
	10.0	Larva	Hughes (1973)Hughes G.M. 1973. Respiratory responses to hypoxia in fish. Am. Zool. 13(2):475-489. http://dx.doi.org/10.1093/icb/13.2.475. https://doi.org/10.1093/icb/13.2.475...
	15.0	Juvenile	Hughes (1975)Hughes G.M. 1975. Coughing in the rainbow trout (Salmo gairner) and the influence of pollutants. Rev. Suisse Zool. 82(1):47-64. http://dx.doi.org/10.5962/bhl.part.78257. PMid:1182042. https://doi.org/10.5962/bhl.part.78257...
Hoplias lacerdae Ribeiro, 1908	7.5	Larva	Cruz et al. (2005)Cruz C., Fujimoto R.Y., Luz R.K., Portella M.C. & Martins M.L. 2005. Toxicidade aguda e histopatologia do fígado de larvas de trairão Hoplias lacerdae expostas à solução aquosa de formaldeído a 10%. Pesticidas, Revta Ecotoxicol. Meio Amb. 15:21-28.
Ictalurus punctatus Rafinesque, 1818	14.1	Fingerling	Howe et al. (1995)Howe G.E., Marking L.L., Bills T.D. & Schreier T.M. 1995. Efficacy and toxicity of formalin solutions containing paraformaldehyde for fish and egg treatments. Progr. Fish Cult. 57(2):147-152. http://dx.doi.org/10.1577/1548-8640(1995)057<0147:EATOFS>2.3.CO;2. https://doi.org/10.1577/1548-8640(1995)0...
Mugil platanus Günther, 1880	20.7	Juvenile	Pahor-Filho et al. (2012)Pahor-Filho E., Miranda-Filho K.C. & Pereira-Júnior J. 2012. Parasitology of juvenile mullet (Mugil liza) and effect of formaldehyde on parasites and host. Aquaculture 354:111-116. http://dx.doi.org/10.1016/j.aquaculture.2012.03.032. https://doi.org/10.1016/j.aquaculture.20...
Pimephales promelas Rafinesque, 1820	24.1	Juvenile	Geiger et al. (1990)Geiger D.L., Brooke L.T. & Call D.J. 1990. Acute toxicities of organic chemicals to fathead minnows Pimephales promelas. University of Wisconsin, Madison, Wisconsin. 23p.
Ameiurus melas Rafinesque, 1820	25.1	Fingerling	Bills et al. (1977)Bills T.D., Marking L.L. & Chandler J.H. 1977. Investigation in fish control. Formalin: its toxicity to no target aquatic organisms, persistence, and counteraction. Fish Wildl. Serv. 73:1-7.
Salvelinus namaycush Walbaum, 1792	40.3	Juvenile	Bills et al. (1977)Bills T.D., Marking L.L. & Chandler J.H. 1977. Investigation in fish control. Formalin: its toxicity to no target aquatic organisms, persistence, and counteraction. Fish Wildl. Serv. 73:1-7.
Oncorhynchus mykiss Walbaum, 1792	48.8	Fingerling	Howeet et al. (1995)Howe G.E., Marking L.L., Bills T.D. & Schreier T.M. 1995. Efficacy and toxicity of formalin solutions containing paraformaldehyde for fish and egg treatments. Progr. Fish Cult. 57(2):147-152. http://dx.doi.org/10.1577/1548-8640(1995)057<0147:EATOFS>2.3.CO;2. https://doi.org/10.1577/1548-8640(1995)0...
Corydoras melanistius Regan, 1912	50.7	Adult	Santos et al. (2012)Santos R.F.B., Dias H.M. & Fujimoto R.Y. 2012. Acute toxicity and histopathology in ornamental fish amazon blue spotted corydora Corydoras melanistius exposed to formalin. An. Acad. Brasi. Ciênc. 84(4):1001-1007. PMid:23207704.
Micropterus salmoides Lacepéde, 1802	54.9	Fingerling	Bills et al. (1977)Bills T.D., Marking L.L. & Chandler J.H. 1977. Investigation in fish control. Formalin: its toxicity to no target aquatic organisms, persistence, and counteraction. Fish Wildl. Serv. 73:1-7.
Micropterus dolomieu Lacepéde, 1802	57.7	Fingerling	Bills et al. (1977)Bills T.D., Marking L.L. & Chandler J.H. 1977. Investigation in fish control. Formalin: its toxicity to no target aquatic organisms, persistence, and counteraction. Fish Wildl. Serv. 73:1-7.
Lepomis cyanellus Rafinesque, 1819	69.8	Fingerling	Bills et al. (1977)Bills T.D., Marking L.L. & Chandler J.H. 1977. Investigation in fish control. Formalin: its toxicity to no target aquatic organisms, persistence, and counteraction. Fish Wildl. Serv. 73:1-7.
Salmos alar Linnaeus, 1758	69.8	-	Bills et al. (1977)Bills T.D., Marking L.L. & Chandler J.H. 1977. Investigation in fish control. Formalin: its toxicity to no target aquatic organisms, persistence, and counteraction. Fish Wildl. Serv. 73:1-7.
Clarias gariepinus Burchell, 1822	112.2	Juvenile	Ayuba et al. (2013)Ayuba V.O., Iyakwari S.P. & Oyeniyi M.E. 2013. Acute toxicity of formalin on Clarias gariepinus juveniles. Prod. Agricult. Technol. 9:21-28.
Arapaima gigas Schinz, 1822	36.4	Juvenile	Present study