Global distribution patterns of <i>Caligus</i> Müller, 1785 (Copepoda: Caligidae) associated to teleost fishes, with physiological and histopathological data and description of treatment strategies

TAVARES-DIAS, MARCOS; OLIVEIRA, MARCOS S.B.

doi:10.1590/0001-3765202320220281

MARCOS TAVARES-DIAS

Conception, elaboration and redaction

Embrapa Amapá, Rodovia Josmar Chaves Pinto, 2600, Universidade, 68903-419 Macapá, AP, Brazil

Universidade Federal do Amapá (UNIFAP), Programa de Pós-Graduação em Biodiversidade Tropical (PPGBio), Rodovia Josmar Chaves Pinto, s/n, Universidade, 68903-419 Macapá, AP, Brazil

https://orcid.org/0000-0002-8376-1846

MARCOS S.B. OLIVEIRA

Confection of Maps and statistical analyses

Universidade Federal do Amapá (UNIFAP), Programa de Pós-Graduação em Biodiversidade Tropical (PPGBio), Rodovia Josmar Chaves Pinto, s/n, Universidade, 68903-419 Macapá, AP, Brazil

https://orcid.org/0000-0002-4421-9608

Correspondence to: Marcos Tavares-Dias E-mail: marcos.tavares@embrapa.br

Host order	Host family	Host species number	Parasite species richness
Acanthuriformes	Acanthuridae	4	5
	Chaetodontidae	1	1
	Drepaneidae	1	1
	Ephippidae	2	4
	Leiognathidae	1	1
	Lobotidae	2	4
	Pomacanthidae	3	3
	Scatophagidae	2	4
	Siganidae	3	5
Acropomatiformes	Lateolabracidae	1	1
Albuliformes	Albulidae	1	1
Atheriniformes	Atherinopsidae	2	5
	Atherinidae	1	1
Aulopiformes	Synodontidae	2	2
Beloniformes	Belonidae	6	9
	Hemiramphidae	2	2
Blenniiformes	Blenniidae	3	2
	Clinidae	2	1
	Tripterygiidae	1	1
Carangiformes	Carangidae	35	35
	Centropomidae	4	5
	Coryphaenidae	3	7
	Echeneidae	1	1
	Latidae	2	9
	Nematistiidae	1	1
	Polynemidae	3	3
	Sphyraenidae	4	6
Centrarchiformes	Girellidae	1	2
	Kyphosidae	4	6
	Scorpididae	1	1
	Terapontidae	1	2
Cichliformes	Cichlidae	3	5
Clupeiformes	Chirocentridae	1	1
	Clupeidae	3	3
	Engraulidae	2	2
Cypriniformes	Leuciscidae	1	1
	Cyprinidae	1	1
Dactylopteriformes	Dactylopteridae	1	1
Gadiformes	Gadidae	8	4
	Merlucciidae	2	3
Gobiesociformes	Gobiesocidae	1	1
Gobiiformes	Gobiidae	4	1
Gonorynchiformes	Chanidae	1	1
Labriformes	Pomacentridae	8	6
Lophiiformes	Lophiidae	1	1
Mugiliformes	Mugilidae	14	20
Mulliformes	Mullidae	5	5
Orectolobiformes	Hemiscylliidae	1	1
Perciformes	Cyclopteridae	1	1
	Eleginopidae	1	5
	Embiotocidae	1	1
	Gasterosteidae	1	1
	Gerreidae	5	7
	Haemulidae	11	12
	Hexagrammidae	1	1
	Labridae	16	8
	Lethrinidae	3	2
	Lutjanidae	19	23
	Malacanthidae	1	3
	Moronidae	1	9
	Nemipteridae	6	3
	Nototheniidae	1	1
	Odacidae	2	1
	Pinguipedidae	2	2
	Platycephalidae	1	1
	Pomacentridae	2	1
	Priacanthidae	5	5
	Scaridae	4	9
	Sciaenidae	14	7
	Scorpaenidae	1	1
	Sebastidae	1	1
	Serranidae	19	15
	Sillaginidae	5	6
	Sparidae	29	37
	Triglidae	8	6
Pleuronectiformes	Bothidae	1	1
	Paralichthyidae	5	5
	Pleuronectidae	4	5
	Soleidae	5	4
Salmoniformes	Salmonidae	9	8
Scombriformes	Arripidae	3	4
	Polynemidae	1	1
	Pomatomidae	1	7
	Scombridae	28	25
	Stromateidae	1	1
	Trichiuridae	3	5
Siluriformes	Ariidae	10	8
	Plotosidae	1	1
Syngnathiformes	Aulostomidae	1	3
	Fistulariidae	1	1
Tetraodontiformes	Balistidae	4	5
	Diodontidae	1	1
	Monacanthidae	5	6
	Ostraciidae	2	3
	Tetraodontidae	7	8
	Triacanthidae	2	2
Zeiformes	Zeidae	1	1

Fish species	Parasite species	Organs	Tissue alterations	References
Mugil cephalus	Caligus curtus	Skin	Focal desquamation of the most superficial layer of the epidermis. Areas of vacuolar degeneration with multiple bulla formations were noticed in the skin of most examined cases. Ulcerated areas displayed edema which overdistended the scale pockets. The dermis showed congested blood vessels as well as infiltration, with numerous leukocytes, mainly lymphocytes and macrophages, together with melanomacrophage cells. Numerous melanin-carrying cells were seen in the tunica compacta. The underlying muscles showed sarcoplasmolysis, myophagia, and migration of sarcolemmal nuclei, especially in the ulcerated areas.	Easa & El-Wafa (1995)EASA MES & EL-WAFA AA. 1995. Pathological studies on an epidemic of Caligus curtus (Copepoda) among captive Mugil and Sparus in Egypt with reference to malathion control. J Appl Aquacul 5: 25-29. doi:10.1300/J028v05n02_02.
Mugil cephalus	Caligus curtus	Skin	The skin of fish showed hyperplasia of club cells of the epidermis, congested and hemorrhagic dermis with excessive aggregation of round cells, melanomacrophage cell and edema of the dermis	El-Atta & El-Ekiaby (2012)EL-ATTA MEA & EL-EKIABY WT. 2012. Prevalence of bacterial infection associated with Caligus infestation in cultured Mugil cephalus with trial to control. Abbassa Int J Aqua 5: 415-440.
Salmo salar	Caligus elongatus	Skin	Chalimus larvae were anchored to the host scales by a frontal filament that penetrates through the epidermis and anchors into the basement membrane around the scale. Larval stages remain in one place feeding on the mucus and epidermal cells. The tissue surrounding the third- and fourth stage chalimus larvae showed no tissue changes due to the presence of the filament or any evidence of damage caused by the initial attachment by the second antennae of the copepodid. The feeding of the larvae resulted in excavation of a hole in the epidermis of fish, down to the basement membrane, with detachment of the epidermal layer from the basement membrane in the area surrounding the hole in the majority of samples examined. Necrotic cells line the hole formed by the larva, and some samples of chalimus IV larvae showed evidence of slight hyperplasia around the excavated area.	Mackinnon (1993)MACKINNON BM. 1993. Host response of Atlantic salmon (Salmo salar) to infection by sea lice (Caligus elongatus). Can Fish Aquat Sci 50: 789-792.
Dicentrarchus labrax	Caligus minimus	Skin	Ulceration of the epidermis with marked inflammatory, mainly mononuclear cellular infiltration of the dermis as a result of the attachment and feeding activity of the parasites. The attachment was achieved by means of second pair of the antennae which were inserted into the host epidermal tissue. A marked reactive epidermal hyperplasia was observed at those areas as well as at the periphery of ulcerated lesions. Many epidermal cells around the damaged area showed signs of necrosis, the vacuolar degeneration of basal cells was prominent and epidermis was also characterized by diffuse areas of spongiosis. In many cases, increased fibroplasia and spongiosis was noticed within dermal collagenous connective tissue	Ragias et al. (2004)RAGIAS V, TONTIS D & ATHANASSOPOULOU F. 2004. Incidence of an intense Caligus minimus Otto 1821, C. pageti Russel, 1925, C. mugilis Brian, 1935 and C. apodus Brian, 1924 infection in lagoon cultured sea bass (Dicentrarchus labrax L.) in Greece. Aquaculture 242: 727-733.
Oncorhynchus mykiss	Caligus rogercresseyi	Skin	Analyses revealed differences between the epidermis of the control and infected fish. In particular, attachment sites were characterized by varying degrees of epithelium erosion and disorganization, no epidermal hyperplasia was observed. Lesions extended into the underlying dermis, showing hyperplasia, inflammation of the stratum compactum connective tissue, disorganization of collagen fiber arrangement, and an increased number of melanophores. Furthermore, an increased quantity of goblet cells was interspersed between epithelial cells. The ultra-structural analysis of the skin from infected fish also showed collagen fiber disruption and an evident increase in subdermal melanophores.	Rojas et al. (2018)ROJAS V, SÁNCHEZ D, GALLARDO JA & MERCADO L. 2018. Histopathological changes induced by Caligus rogercresseyi in rainbow trout (Oncorhynchus mykiss). Lat Am J Aquat Res 46: 843-848. doi:10.3856/vol46-issue4-fulltext-23.
Acanthopagrus australis	Caligus epidemicus	Skin	Copepodids eroded the epidermis and usually attached their frontal filament to the basement membrane on the inter-ray region of fins, as well as the fin rays or scales. The most extensive tissue response was associated with the redundant frontal filament, and was characterized by infiltrating macrophages, multinucleated giant cells, and epidermal and fibroblast proliferation.	Roubal (1994)ROUBAL FR. 1994. Histopathology caused by Caligus epidemicus Hewitt (Copepoda: Caligidae) on captive Acanthopagrus australis (Gunther) (Pisces: Sparidae). J Fish Dis 17: 631-640.
Dicentrarchu labrax	Caligus clemensi	Gills	Partial or complete sloughing of their lamellar epithelium which results in denuded filaments. Sometimes hyperplastic secondary lamellar epithelium in the adjacent area which led to fusion of the filaments were encountered thickened filaments by numerous inflammatory cells and edema beside dilated capillaries were observed. Fragments from the parasite were detected between primary filaments with ulceration and distortion of the adjacent filaments. Sometimes, heavy parasitic infestation with atrophy, distortion and blunting of the gill filaments could be seen. The base of primary filaments was covered by sheath from hyperplastic lamellar epithelium. The gill arch contained congested blood vessels beside edema, hemorrhage and inflammatory cells infiltration mainly eosinophil, granular cells in their necrotic muscles.	Abdelkalek et al. (2021)ABDELKALEK N, MAGED RAE, ALI H & SATOUR N. 2021. Identification of Caligus parasites infesting Morone labrax and its impact on fish health status and pathological alteration. MVMJ 22: 7-12. 10.35943/mvmj.2021.56334.1023.
Mugil cephalus	Caligus curtus	Gills	Parasites induced severe congestion of brachial blood vessels, telangiectasia, and also sloughing of secondary lamellae and desquamation of secondary lamellar epithelium	El-Atta & El-Ekiaby (2012)EL-ATTA MEA & EL-EKIABY WT. 2012. Prevalence of bacterial infection associated with Caligus infestation in cultured Mugil cephalus with trial to control. Abbassa Int J Aqua 5: 415-440.
Mugil cephalus	Caligus sp.	Gills	Many branchial lesions showed severe inflammatory reactions to advanced degenerative and hyperplastic changes. The inflammatory changes were mainly observed in gill arch and congestion of lamellar blood vessels and adhesion of most gill filaments and lamellae	El-Deen et al. (2012)EL-DEEN NAE, ABDEL HOK, SHALABY SI & ZAKI MS. 2012. Field studies on Caligus disease among cultured Mugil cephalus in brackish water fish farms. Life Sci J 9: 733-737.
Dicentrarchus labra x	Caligus elongatus	Gills	Variety of circulatory, degenerative and proliferative changes evident in tissues of infected fish. Severe congestion of lamellar blood vessels was common among pathological findings. Diffuse hyperplasia at the base of the secondary lamellae as well as lamellar fusion was frequently denoted. Increase in the activity of goblet cells was characteristic. In some other cases, gill arch demonstrated edema, hemorrhages together with some eosinophilic granular cell aggregations	Elgendy et al. (2015)ELGENDY MY, ABDELSALAM M, MOUSTAFA M, KENAWY AM & SEIDA A. 2015. Caligus elongatus and Photobacterium damselae subsp piscicida concomitant infections affecting broodstock European seabass, Dicentrarchus labrax, with special reference to histopathological responses. J Aquac Res Development 6: 346. doi:10.4172/2155-9546.1000346.
Oncorhynchus mykiss	Caligus rogercresseyi	Gills	The secondary lamellae showed evidence of hyperplasia, base and tip thickening, and complete or partial lamellar fusion. The gills presented ordered organization, with numerous parallel threadlike secondary lamellae arranged at nearly right angles to the primary lamellae. Moreover, at the primary lamellae of the infected fish, the connective tissue showed an increased quantity of MCs/EGCs, macrophages, and lymphocytes). Increase in mucus-secreting or goblet cells in the epithelium of secondary lamellae and the distal tip of the gill filaments	Rojas et al. (2018)ROJAS V, SÁNCHEZ D, GALLARDO JA & MERCADO L. 2018. Histopathological changes induced by Caligus rogercresseyi in rainbow trout (Oncorhynchus mykiss). Lat Am J Aquat Res 46: 843-848. doi:10.3856/vol46-issue4-fulltext-23.

Fish species	Parasite species	Alterations	References
Salmo salar	Caligus rogercresseyi	Increase in plasma glucose and decrease in osmolality in 1day post infestation, with decrease in glucose and increase in osmolality in 16day post infestation, and decrease in triglycerides levels	González et al. (2015)GONZÁLEZ MP, MARÍN SL & VARGAS-CHACOFF L. 2015. Effects of Caligus rogercresseyi (Boxshall and Bravo, 2000) infestation on physiological response of host Salmo salar (Linnaeus 1758): establishing physiological thresholds. Aquaculture 438: 47-54. http://dx.doi.org/ 10.1016/j.aquaculture.2014.12.039. https://doi.org/ 10.1016/j.aquaculture.2...

Salmo salar	Caligus rogercresseyi	Decrease in plasma glucose, pCO₂ and hematocrit, and increase in hemoglobin and lymphocytes	González et al. (2016a)GONZÁLEZ MP, MUÑOZ JLP, VALERIO V & VARGAS-CHACOFF L. 2016a. Effects of the ectoparasite Caligus rogercresseyi on Salmo salar blood parameters under farm conditions. Aquaculture 457: 29-34. http://dx.doi.org/10.1016/j.aquaculture.2016.01.027. https://doi.org/10.1016/j.aquaculture.20...

Salmo salar	Caligus rogercresseyi	Increase in plasma cortisol levels, and decrease in plasma level of glucose and triglycerides	González et al. (2016b)GONZÁLEZ MP, VARGAS-CHACOFF L & MARÍN SL. 2016b. Stress response of Salmo salar (Linnaeus 1758) when heavily infested by Caligus rogercresseyi (Boxshall & Bravo 2000) copepodid. Fish Physiol Biochem 42: 263-274. doi: 10.1007/s10695-015-0134-x.

Salmo salar	Caligus rogercresseyi	Increase in plasma cortisol and glucose levels	González et al. (2020)GONZÁLEZ MP, MARÍN SL, MANCILLA M, CAÑON-JONES H & VARGAS-CHACOFF L. 2020. Fin erosion of Salmo salar (Linnaeus 1758) Infested with the parasite Caligus rogercresseyi (Boxshall & Bravo 2000). Animals 10: 1166. doi:10.3390/ani10071166.
Thunnus maccoyii	Caligus chiastos	Increase in plasma cortisol and glucose levels	Hayward et al. (2010)HAYWARD CJ, ELLIS D, FOOTEC D, WILKINSON RJ, CROSBIE PBB, BOTT NJ & NOWAK BF. 2010. Concurrent epizootic hyperinfections of sea lice (predominantly Caligus chiastos) and blood flukes (Cardicola forsteri) in ranched southern bluefin tuna. Vet Parasitol 173: 107-115. doi:10.1016/j.vetpar.2010.06.007.
Netuma bilineata	Calugus sp.	Decrease in hematocrit, hemoglobin and total erythrocytes	Jori & Mohamad (2008)JORI MM & MOHAMAD ET. 2008. The effect of Hamatopeduncularia sp. and Caligus sp. on some blood parameters of Arius bilineatus (Val., 1840). Mar Meso 23: 269-277.
Eleginops maclovinus	Caligus rogercresseyi	Decrease in hematocrit, total erythrocytes and monocytes, and increase in hemoglobin, MCV, MCHC, leukocytes and lymphocytes	Peña-Rehbein et al. (2013)PEÑA-REHBEIN P, RUIZ K, ORTLOFF A, PIZARRO MI & NAVARRETE C. 2013. Hematological changes in Eleginops maclovinus during an experimental Caligus rogercresseyi infestation. Rev Bras Parasitol Vet 22: 402-406. https://doi.org/10.1590/S1984-29612013000300014. https://doi.org/10.1590/S1984-2961201300...

Salmo salar	Caligus rogercresseyi	Decrease in plasma glucose and plasma total α-amino acids levels	Vargas-Chacoff et al. (2016)VARGAS-CHACOFF L ET AL. 2016. Atlantic salmon (Salmo salar) and Coho salmon (Oncorhynchus kisutch) display differential metabolic changes in response to infestation by the ectoparasite Caligus rogercresseyi. Aquaculture 464: 469-479. http://dx.doi.org/10.1016/j.aquaculture.2016.07.029. https://doi.org/10.1016/j.aquaculture.20...
Oncorhynchus kisutch	Caligus rogercresseyi	Increase in plasma glucose, triglycerides and total protein levels, and decrease in plasma total α-amino acids levels	Vargas-Chacoff et al. (2016)VARGAS-CHACOFF L ET AL. 2016. Atlantic salmon (Salmo salar) and Coho salmon (Oncorhynchus kisutch) display differential metabolic changes in response to infestation by the ectoparasite Caligus rogercresseyi. Aquaculture 464: 469-479. http://dx.doi.org/10.1016/j.aquaculture.2016.07.029. https://doi.org/10.1016/j.aquaculture.20...
Salmo salar	Caligus rogercresseyi	Increase in plasm a lactate dehydrogenase levels	Vargas-Chacoff et al. (2017)VARGAS-CHACOFF L ET AL. 2017. Ectoparasite Caligus rogercresseyi modifies the lactate response in Atlantic salmon (Salmo salar) and Coho salmon (Oncorhynchus kisutch). Vet Parasitol 243: 6-11. http://dx.doi.org/10.1016/j.vetpar.2017.05.031. https://doi.org/10.1016/j.vetpar.2017.05...
Oncorhynchus kisutch	Caligus rogercresseyi	Increase in plasm a lactate dehydrogenase levels	Vargas-Chacoff et al. (2017)VARGAS-CHACOFF L ET AL. 2017. Ectoparasite Caligus rogercresseyi modifies the lactate response in Atlantic salmon (Salmo salar) and Coho salmon (Oncorhynchus kisutch). Vet Parasitol 243: 6-11. http://dx.doi.org/10.1016/j.vetpar.2017.05.031. https://doi.org/10.1016/j.vetpar.2017.05...

Parasite species	Products	Concentrations	Results	References
Caligus rogercresseyi	Cypermethrin	15 μg/L	High efficacy	Agusti et al. (2016)AGUSTI C, BRAVO S, CONTRERAS G, BAKKE MJ, HELGESEN KO, WINKLER C, SILVA MT, MENDOZA J & HORSBER TE. 2016. Sensitivity assessment of Caligus rogercresseyi to anti-louse chemicals in relation to treatment efficacy in Chilean salmonid farms. Aquaculture 458: 195-205.
Caligus rogercresseyi	Cypermethrin	0.4 mg/L	High efficacy	González-Gómez et al. (2019)GONZÁLEZ-GÓMEZ MP, OVALLE L, MENANTEAU M, SPINETTO C, OYARZÚN R, RIVAS M & OYARZO C. 2019. Susceptibility of Caligus rogercresseyi collected from the native fish species Eleginops maclovinus (Cuvier) to antiparasitics applied by immersion. J Fish Dis 42: 1143-1149. https://doi.org/10.1111/jfd.13020. https://doi.org/10.1111/jfd.13020...
Caligus rogercresseyi	Cypermethrin	15 ppb	Inefficacy	Marín et al. (2015)MARÍN SL, MARTIN R & LEWIS R. 2015. Effects of Caligus rogercresseyi (Boxshall & Bravo 2000) chalimus stage condition (dead, moribund, live) on the estimates of Cypermethrin BETAMAX® efficacy. Aquac Res 46(Suppl. 1): 30-36 doi:10.1111/are.12460.
Caligus elongatus	Cypermethrin	5 μg/L	High efficacy	Treasurer & Wadsworth (2004)TREASURER JW & WADSWORTH SL. 2004. Interspecific comparison of experimental and natural routes of Lepeophtheirus salmonis and Caligus elongatus challenge and consequences for distribution of chalimus on salmonids and therapeutant screening. Aquacul Res 35: 773-783. doi:10.1111/j.1365-2109.2004.01100.x.
Caligus rogercresseyi	Deltamethrin	3 μg/L	High efficacy	Agusti et al. (2016)AGUSTI C, BRAVO S, CONTRERAS G, BAKKE MJ, HELGESEN KO, WINKLER C, SILVA MT, MENDOZA J & HORSBER TE. 2016. Sensitivity assessment of Caligus rogercresseyi to anti-louse chemicals in relation to treatment efficacy in Chilean salmonid farms. Aquaculture 458: 195-205.
Caligus rogercresseyi	Deltamethrin	0.003 mg/L	Moderate efficacy	Bravo et al. (2013)BRAVO S, NUÑEZ M & SILVA MT. 2013. Efficacy of the treatments used for the control of Caligus rogercresseyi infecting Atlantic salmon, Salmo salar L., in a new fish-farming location in Region XI, Chile. J Fish Dis 36: 221-228. doi:10.1111/jfd.12023.
Caligus rogercresseyi	Deltamethrin	2 μg/L	High efficacy	Bravo et al. (2014b)BRAVO S, SILVA MT & TREASURER J. 2014a. Factors affecting the abundance of Caligus rogercresseyi (Boxshall and Bravo) on farmed salmonids in Chile in the period 2006–2007. Aquaculture 434: 456-461. http://dx.doi.org/10.1016/j.aquaculture.2014.09.009. https://doi.org/10.1016/j.aquaculture.20...
Caligus rogercresseyi	Deltamethrin	0.08 mg/L	High efficacy	González-Gómez et al. (2019)GONZÁLEZ-GÓMEZ MP, OVALLE L, MENANTEAU M, SPINETTO C, OYARZÚN R, RIVAS M & OYARZO C. 2019. Susceptibility of Caligus rogercresseyi collected from the native fish species Eleginops maclovinus (Cuvier) to antiparasitics applied by immersion. J Fish Dis 42: 1143-1149. https://doi.org/10.1111/jfd.13020. https://doi.org/10.1111/jfd.13020...
Caligus_rotundigenitalis	Deltamethrin	12.5 mg/L	High efficacy	Solanki et al. (2016)SOLANKI HG, PATIL PK, VANZA JG, PATEL P, SETHI S & GOPAL C. 2016. Sea lice, Caligus rotundigenitalis infestations and its management in pond cultured pearlspot, Etroplus suratensis in Gujarat: a case study. J Parasit Dis 40: 565-567. doi:10.1007/s12639-014-0539-y.
Caligus rogercresseyi	Azamethiphos	100 μg/L	High efficacy	Agusti et al. (2016)AGUSTI C, BRAVO S, CONTRERAS G, BAKKE MJ, HELGESEN KO, WINKLER C, SILVA MT, MENDOZA J & HORSBER TE. 2016. Sensitivity assessment of Caligus rogercresseyi to anti-louse chemicals in relation to treatment efficacy in Chilean salmonid farms. Aquaculture 458: 195-205.
Caligus rogercresseyi	Azamethiphos	0.9 mg/L	High efficacy	González-Gómez et al. (2019)GONZÁLEZ-GÓMEZ MP, OVALLE L, MENANTEAU M, SPINETTO C, OYARZÚN R, RIVAS M & OYARZO C. 2019. Susceptibility of Caligus rogercresseyi collected from the native fish species Eleginops maclovinus (Cuvier) to antiparasitics applied by immersion. J Fish Dis 42: 1143-1149. https://doi.org/10.1111/jfd.13020. https://doi.org/10.1111/jfd.13020...
Caligus rogercresseyi	Azamethiphos	100 mg/m³	High efficacy	Jimenez et al. (2018)JIMENEZ DF, IBARRA R, ARTACHO P, PRIMUS AE & TELLO A. 2018. Prolonging Azamethiphos bath increases the effectiveness of field treatments against Caligus rogercresseyi in Atlantic salmon in Chile (Salmo salar). Aquaculture 493: 186-191. https://doi.org/10.1016/j.aquaculture.2018.04.034. https://doi.org/10.1016/j.aquaculture.20...
Caligus elongatus	Azamethiphos	0.2 mg/L	High efficacy	Roth et al. (1996)ROTH M, RICHARDS RH, DOBSON DP & RAE GH. 1996. Field trials on the efficacy of the organophosphorus compound azamethiphos for the control of sea lice (Copepoda: Caligidael infestations of farmed Atlantic salmon (Salmo salar). Aquaculture 140: 217-239.
Caligus elongatus	Ivermectin	0.2 mg/kg	High efficacy	Palmer et al. (1987)PALMER R, RODGER H, DRINAN E, DWYER C & SMITH PR. 1987. Preliminary trials on the ivermectin efficacy of against parasitic copepods of Atlantic salmon. Bull Eur Ass Fish Pathol 7(2): 47-54.
Caligus teres	Neguvon	0.25 mg/L	High efficacy	Reyes & Bravo (1983)REYES XP & BRAVO S. 1983. Nota sobre una copepodosis en salmones de cultivo. Invest Mar Valparaíso 1: 55-57.
Caligus rogercresseyi	Emamectin benzoate	50 μg/kg	High efficacy	Agusti et al. (2016)AGUSTI C, BRAVO S, CONTRERAS G, BAKKE MJ, HELGESEN KO, WINKLER C, SILVA MT, MENDOZA J & HORSBER TE. 2016. Sensitivity assessment of Caligus rogercresseyi to anti-louse chemicals in relation to treatment efficacy in Chilean salmonid farms. Aquaculture 458: 195-205.
Caligus rogercresseyi	Emamectin benzoate	50-100 μg/kg	Inefficacy	Bravo et al. (2012)BRAVO S, SILVA MT & MONTI G. 2012. Efficacy of emamectin benzoate in the control of Caligus rogercresseyi on farmed Atlantic salmon (Salmo salar L.) in Chile from 2006 to 2007. Aquaculture 364-365: 61-66. http://dx.doi.org/10.1016/j.aquaculture.2012.07.036. https://doi.org/10.1016/j.aquaculture.20...
Caligus rogercresseyi	Emamectin benzoate	70 μg/kg	Inefficacy	Bravo et al. (2013)BRAVO S, NUÑEZ M & SILVA MT. 2013. Efficacy of the treatments used for the control of Caligus rogercresseyi infecting Atlantic salmon, Salmo salar L., in a new fish-farming location in Region XI, Chile. J Fish Dis 36: 221-228. doi:10.1111/jfd.12023.
Caligus curtus	Emamectin benzoate	50 μg/kg	High efficacy	Hamre et al. (2011)HAMRE LA, LUNESTAD BT, HANNISDAL R & SAMUELSEN OB. 2011. An evaluation of the duration of efficacy of emamectin benzoate in the control of Caligus curtus Müller infestations in Atlantic cod, Gadus morhua L. J Fish Dis 34: 453-457. doi:10.1111/j.1365-2761.2011.01256.x.
Caligus clemensi	Emamectin benzoate	-	High efficacy	Byrne et al. (2018)BYRNE AA, PEARCE CM, CROSS SF, JONES SRM, ROBINSON SMC, HUTCHINSON MJ, MILLER MR, HADDAD CA & JOHSON DL. 2018. Planktonic and parasitic stages of sea lice (Lepeophtheirus salmonis and Caligus clemensi) at a commercial Atlantic salmon (Salmo salar) farm in British Columbia, Canada. Aquaculture 486: 130-138. https://doi.org/10.1016/j.aquaculture.2017.12.009. https://doi.org/10.1016/j.aquaculture.20...
Caligus elongatus	Emamectin benzoate	50 μg/kg	High efficacy	Stone et al. (2000)STONE J, SUTHERLAND IH, SOMMERVILLE C, RICHARDS RH & VARMA KJ. 2000. Field trials to evaluate the efficacy of emamectin benzoate in the control of sea lice, Lepeophtheirus salmonis (Kroyer) and Caligus elongatus Nordmann, infestations in Atlantic salmon Salmo salar L. Aquaculture 186: 205-219.
Caligus rogercresseyi	Hydrogen peroxide	1.5 g/L	Inefficacy	Bravo et al. (2010)BRAVO S, TREASURER J, SEPULVEDA M & LAGOS C. 2010. Effectiveness of hydrogen peroxide in the control of Caligus rogercresseyi in Chile and implications for sea louse management. Aquaculture 303: 22-27. doi:10.1016/j.aquaculture.2010.03.007.
Caligus rogercresseyi	Hydrogen peroxide	2.0 g/L	High efficacy	Chávez-Mardones et al. (2017)CHÁVEZ-MARDONES J, ASENCIO G, LATUZ S & GALLARDO-ESCÁRATE C. 2017. Hydrogen peroxide modulates antioxidant system transcription, evidencing sex-dependent responses in Caligus rogercresseyi. Aquac Res 48: 969-978 doi:10.1111/are.12939.
Caligus rogercresseyi	Hydrogen peroxide	825 mg/L	High efficacy	Marín et al. (2018)MARÍN SL, GONZÁLEZ MP, MADARIAGA ST, MANCILLA M & MANCILLA J. 2018. Response of Caligus rogercresseyi (Boxshall & Bravo, 2000) to treatment with hydrogen peroxide: recovery of parasites, fish infestation and egg viability under experimental conditions. J Fish Dis 41: 861-873. https://doi.org/10.1111/jfd.12691. https://doi.org/10.1111/jfd.12691...
Caligus elongatus	Hydrogen peroxide	15.0-20.0 mg/L	High efficacy	El- Deen et al. (2013)
Caligus rogercresseyi	Hydrogen peroxide	1200 mg/L	High efficacy	Valenzuela-Muñoz et al. (2020)VALENZUELA-MUÑOZ V, GALLARDO-ESCÁRATE A, SÁEZ-VERA C, GARCÉS F, BONFATTI J & GALLARDO-ESCÁRATE C. 2020. More than bubbles: In vivo assessment and transcriptome modulation of Caligus rogercresseyi and Atlantic salmon exposed to hydrogen peroxide (Paramove®). Aquaculture 522: 735170. https://doi.org/10.1016/j.aquaculture.2020.735170. https://doi.org/10.1016/j.aquaculture.20...
Caligus rogercresseyi	Freshwater	-	Inefficacy	Bravo et al. (2015b)BRAVO S, SILVA MT, AGUSTI C, SAMBRA K & HORSBERG TE. 2015a. The effect of chemotherapeutic drugs used to control sea lice on the hatching viability of egg strings from Caligus rogercresseyi. Aquaculture 443: 77-83. http://dx.doi.org/10.1016/j.aquaculture. 2015.03.011. https://doi.org/10.1016/j.aquaculture...
Caligus curtus	Freshwater	-	High efficacy	El-Atta & El-Ekiaby (2012)EL-ATTA MEA & EL-EKIABY WT. 2012. Prevalence of bacterial infection associated with Caligus infestation in cultured Mugil cephalus with trial to control. Abbassa Int J Aqua 5: 415-440.
Caligus sp.	Freshwater	-	High efficacy	El-Deen et al. (2012)EL-DEEN NAE, ABDEL HOK, SHALABY SI & ZAKI MS. 2012. Field studies on Caligus disease among cultured Mugil cephalus in brackish water fish farms. Life Sci J 9: 733-737.
Caligus elongatus	Freshwater	-	High efficacy	El-Deen et al. (2013)EL-DEEN AIEN, MAHMOUD E & HASSAN HM. 2013. Field Studies of Caligus parasitic Infections among cultured seabass (Dicentrarchus labrax) and Mullet (Mugil cephalus) in marine fish farms with emphasis on treatment trials. Global Vet 11(5): 511-520. doi:10.5829/idosi.gv.2013.11.5.76168.
Caligus elongatus	Freshwater	-	High efficacy	Landsberg et al. (1991)LANDSBERG JH, VERMEER GK & RICHARDS SA. 1991. Control of the parasitic copepod Caligus elongatus on pond-reared red drum. J Aquat Anim Health 3: 206-209. doi: 10.1577/1548-8667(1991)003<0206:COTPCC>2.3.CO;2.
Caligus orientalis	Freshwater	-	Inefficacy	Urawa & Kato (1991)URAWA S & KATO T. 1991. Heavy Infections of Caligus orientalis (Copepoda: Caligidae) on caged rainbow trout Oncorhynchus mykiss in Brackish Water. Gyobyo Keokyug 26(3): 161-162.
Caligus curtus	Malathion	0.02 mg/L	High efficacy	Easa & El-Wafa (1995)EASA MES & EL-WAFA AA. 1995. Pathological studies on an epidemic of Caligus curtus (Copepoda) among captive Mugil and Sparus in Egypt with reference to malathion control. J Appl Aquacul 5: 25-29. doi:10.1300/J028v05n02_02.
Caligus elongatus	Malathion	0.15-0.20 mg/L	High efficacy	El-Deen et al. (2013)EL-DEEN AIEN, MAHMOUD E & HASSAN HM. 2013. Field Studies of Caligus parasitic Infections among cultured seabass (Dicentrarchus labrax) and Mullet (Mugil cephalus) in marine fish farms with emphasis on treatment trials. Global Vet 11(5): 511-520. doi:10.5829/idosi.gv.2013.11.5.76168.
Caligus sp.	Trichlorfon	20.0-30.0 mg/L	High efficacy	El-Deen et al. (2012)EL-DEEN NAE, ABDEL HOK, SHALABY SI & ZAKI MS. 2012. Field studies on Caligus disease among cultured Mugil cephalus in brackish water fish farms. Life Sci J 9: 733-737.
Caligus elongatus	Trichlorfon	20.0-30.0 mg/L	High efficacy	El-Deen et al. (2013)EL-DEEN AIEN, MAHMOUD E & HASSAN HM. 2013. Field Studies of Caligus parasitic Infections among cultured seabass (Dicentrarchus labrax) and Mullet (Mugil cephalus) in marine fish farms with emphasis on treatment trials. Global Vet 11(5): 511-520. doi:10.5829/idosi.gv.2013.11.5.76168.
Caligus elongatus	Trichlorfon	0.25 mg/L	Inefficacy	Landsberg et al. (1991)LANDSBERG JH, VERMEER GK & RICHARDS SA. 1991. Control of the parasitic copepod Caligus elongatus on pond-reared red drum. J Aquat Anim Health 3: 206-209. doi: 10.1577/1548-8667(1991)003<0206:COTPCC>2.3.CO;2.
Caligus elongatus	Formalin	250 mg/L	Inefficacy	Landsberg et al. (1991)LANDSBERG JH, VERMEER GK & RICHARDS SA. 1991. Control of the parasitic copepod Caligus elongatus on pond-reared red drum. J Aquat Anim Health 3: 206-209. doi: 10.1577/1548-8667(1991)003<0206:COTPCC>2.3.CO;2.
Caligus platytarsis	Formalin	0.02%	High efficacy	Chatterji et al. (1982)CHATTERJI A, INGOLE BS & PARULEKAR AH. 1982. Effectiveness of formaldehyde in Caligus infection of laboratory reared grey mullet, Mugil cephalus (L). Indian J Marine Sci 11: 344-346.
Caligus elongatus	Potassium permanganate	5.0-10.0 mg/L	High efficacy	El-Deen et al. (2013)EL-DEEN AIEN, MAHMOUD E & HASSAN HM. 2013. Field Studies of Caligus parasitic Infections among cultured seabass (Dicentrarchus labrax) and Mullet (Mugil cephalus) in marine fish farms with emphasis on treatment trials. Global Vet 11(5): 511-520. doi:10.5829/idosi.gv.2013.11.5.76168.
Caligus sp.	Potassium permanganate	5.0-10.0 mg/L	High efficacy	El-Deen et al. (2012)EL-DEEN NAE, ABDEL HOK, SHALABY SI & ZAKI MS. 2012. Field studies on Caligus disease among cultured Mugil cephalus in brackish water fish farms. Life Sci J 9: 733-737.
Caligus elongatus	Copper	150 mg/L	Inefficacy	Landsberg et al. (1991)LANDSBERG JH, VERMEER GK & RICHARDS SA. 1991. Control of the parasitic copepod Caligus elongatus on pond-reared red drum. J Aquat Anim Health 3: 206-209. doi: 10.1577/1548-8667(1991)003<0206:COTPCC>2.3.CO;2.

[1] Correspondence to: Marcos Tavares-Dias E-mail: marcos.tavares@embrapa.br

Brasil

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Global distribution patterns of Caligus Müller, 1785 (Copepoda: Caligidae) associated to teleost fishes, with physiological and histopathological data and description of treatment strategies

Abstract