Treatment of Gyrodactylid Infections in Fish

Vol. 86: 65–75, 2009 DISEASES OF AQUATIC ORGANISMS Published September 7 doi: 10.3354/dao02087 Dis Aquat Org

REVIEW

Treatment of gyrodactylid infections in fish

Bettina Schelkle1, Andrew P. Shinn2, Edmund Peeler3, Joanne Cable1,*

1School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK 2Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK 3Centre for Environment, Fisheries and Aquaculture Science, Barrack Road, The Nothe, Weymouth, Dorset DT4 8UB, UK

ABSTRACT: Since Norway experienced the devastating Gyrodactylus salaris (Monogenea) epi- demics in Atlantic salmon Salmo salar, there has been heightened interest in how to treat gyrodactylosis in fish. Here we summarize chemical treatments previously used against gyrodactylids and dis- cuss the main problems associated with these control measures including efficacy, host toxicity, human health concerns and application of treatments. Unfortunately, for these reasons and because of the different methodologies and different parasite and host species used in previous studies, it is difficult to recommend effective chemotherapeutic treatments. However, we suggest a method for manual removal of gyrodactylids from the host suitable for use in small-scale research facilities.

KEY WORDS: Gyrodactylus · Control treatment · Efficacy · Toxicity

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INTRODUCTION does not eradicate gyrodactylids completely (Rin- tamäki-Kinnunen & Valtonen 1996, Rowland et al. A frequently asked, but rarely addressed, question is 2006), and in some three-spined stickleback Gasteros- what is the most effective means of removing Gyro- teus aculeatus populations it is only 10% effective (J. dactylus spp. from their hosts? With increasing interest Cable pers. obs.). Due to its broad anti-parasitic prop- in this large group of ectoparasitic worms, not only as erties, formaldehyde is still commonly used in aquacul- important pathogens but also as model organisms ture, even though it is classed as a human carcinogen (reviewed by Bakke et al. 2002, 2007, Cable & Harris (IARC 2004). Mutagenic and carcinogenic effects are 2002), it seems timely to document the methods that also known for malachite green (Srivastava et al. 2004), have been used thus far to remove gyrodactylids. which like formaldehyde is widely used as an anti-parasitic treatment, but its effectiveness against Gyro- dactylus spp. has not been evaluated. Malachite green PROBLEMS WITH EXISTING TREATMENTS is now banned in food fish production in Europe and North America as it is retained in fish flesh (European Appendix 1 lists 88 compounds and treatment com- Council 1990; US Food and Drug Administration and binations that have previously been used to treat gyro- the Canadian Food Inspection Agency, cited in Srivas- dactylid infections in research facilities, aquaculture tava et al. 2004). and the hobbyist market. However, selecting the best Alternative treatments include rotenone, an indis- of these treatments is difficult, because few studies criminate ATPase inhibitor which has been used to con- have compared compounds using the same method- trol Gyrodactylus salaris in Norway by killing all poten- ologies and the majority of treatments have various tial hosts (reviewed in Bakke et al. 2007), including associated problems. Formaldehyde, for instance, was other gill-breathing organisms. This is only partially ef- found to be 100% effective at eliminating Gyrodacty- fective and has potential negative effects on human lus salaris experimentally (Buchmann & Kristensson health. Aqueous aluminium is another alternative that 2003), but under large-scale aquaculture conditions it is being tested. However, although aluminium ap-

*Corresponding author. E-mail: [email protected] © Inter-Research 2009 · www.int-res.com 66 Dis Aquat Org 86: 65–75, 2009

peared promising in laboratory studies (Soleng et al. piperazine, Fugotenil® and Neguvon®; Tojo & Santa- 1999, 2005, Poléo et al. 2004), field trials in Norway us- marina 1998), which increases the dosage needed per ing aluminium in combination with rotenone have been unit of food for efficacy. Additionally, compounds that problematic because successful treatment of the whole are partially effective as baths may not be effective if river system requires maintaining a specific concentra- administered orally (e.g. trichlorfon; Santamarina et al. tion without exceeding levels toxic to Atlantic salmon 1991, Tojo & Santamarina 1998). Moreover, resistance (P. Shave pers. comm.). Aluminium toxicity to fish in- of parasites against antihelminthics has been reported, creases under acidic water conditions (Birchall et al. with Goven & Amend (1982) and Schmahl et al. (1989) 1989, Poléo 1995, Soleng et al. 1999), and elevated en- finding resistance of gyrodactylids to dimethyl phos- vironmental aluminium levels can result in Alzheimer’s phonate and trichlorfon, respectively. Breeding para- disease (Doll 1993) and decreased agricultural and site-resistant fish or developing a vaccine against gyro- forestry productivity (Bi et al. 2001). Organophos- dactylosis would override many of the above problems phates, such as trichlorfon, are no longer in use against and bypass the potential issue of drug resistance. fish parasites as they cause irreversible effects in non- Breeding experiments with wild Atlantic salmon target species by phosphorylating acetylcholinesterase Salmo salar that show resistance against Gyrodactylus (see Kozlovskaya & Mayer 1984, Peña-Llopis et al. salaris are currently under way in Norway (R. Salte et 2003, Costa 2006). Acute and chronic toxicity to other al. unpubl.), but we are unaware of any plans for vac- aquatic organisms has also been reported for benzimi- cine development. In Norway destocking and drying of dazoles (e.g. Oh et al. 2006); however, due to their low fish farms was used successfully to eradicate G. salaris efficacy (see Appendix 1), these are not preferred over (see Mo 1994); however, this method is not suitable for broad antiparasitic treatments such as formalin. establishments which receive potentially infected fish In addition to efficacy, environmental and human on a regular basis and infected fish would still have to health issues, the main problem associated with cur- be treated. rent gyrodactylid treatments is their toxicity to the host A major problem with many of the studies presented (Schmahl & Taraschewski 1987, Santamarina et al. in Appendix 1 is that they used sub-sampling methods, 1991, Tojo et al. 1992, Scholz 1999, Ekanem et al. 2004, such as mucus scrapings (e.g. Tojo et al. 1992, Tojo & Srivastava et al. 2004). Even widely used compounds, Santamarina 1998) or partial examination of fish popu- such as formaldehyde, may significantly change the lations in field trials (e.g. Goven & Amend 1982). This host’s gill structure and epidermis (Speare et al. 1997, is a crude and unreliable estimate of parasite infection, Sanchez et al. 1998, Buchmann et al. 2004). For particularly where the gyrodactylid is not identified to instance, although zinc exposure initially stimulates species level (e.g. Tojo & Santamarina 1998, Chansue host mucus production, mucus is subsequently de- 2007) as different Gyrodactylus spp. show marked site pleted leaving the fish more susceptible to microbial specificities. Furthermore, the majority of compounds infections (McGeer et al. 2000). If these fish are subse- trialled successfully have been tested only once. For quently used for experimental infections without a suf- those with at least 2 independent studies, results have ficient recovery period, they may show an abnormal been variable probably because of different method- response to infection (see review by Bakke et al. 2007). ologies. Hence, many seemingly successful com- Host respiratory problems are also a common side pounds may not be effective when it comes to treating effect of gyrodactylid treatments due to direct interfer- a different host–parasite system. Field studies are of ence with gill function and indirectly via reduction of particular importance as they provide an indication of water quality (e.g. decrease in pH and/or dissolved how efficient treatments are on a large scale, poten- oxygen: Smith & Piper 1972, Ross et al. 1985, Rowland tially for use in the ornamental or food fish industries. et al. 2006). Toxicity in many cases is dose-dependent, However, there have only been a few such studies (see but may also be affected by one or a combination of the Appendix 1) with only Rach et al. (2000) claiming following factors: temperature, pH, salinity, mecha- 100% efficiency for the compound they tested (hydro- nism of delivery, species and exposure time (Schmahl gen peroxide). Other authors defined a treatment in & Taraschewski 1987, Schmahl et al. 1989, Scholz the field as successful if it just reduced the pathogen 1999), especially where multiple treatments are used. burden (e.g. Lewis 1967, Rintamäki-Kinnunen & Valto- Gyrodactylid treatments are applied either orally nen 1996). (with food) or topically (added to the water). Both methods usually lead to application of overly high doses to compensate for lack of control over drug MANUAL REMOVAL OF GYRODACTYLIDS administration (Scholz 1999), which may lead to environmental contamination. Oral administration of some Due to toxicity and/or difficulties in administration drugs can also reduce host food consumption (e.g. (such as the need for prolonged exposure), no treat- Schelkle et al.: Treatments of gyrodactylid infections 67

ment detailed in Table 1 is entirely satisfactory or dactylids are shed, there is no opportunity for the par- 100% effective, although several treatments indicate asites to transfer to new hosts. However, even long 100% efficacy against gyrodactylosis (e.g. formalde- periods of isolation are not always effective for certain hyde and aqueous aluminium). In laboratory trials with host–parasite combinations (see King et al. 2008) and small, hardy fish, the most effective means of removing the accompanying high maintenance is extremely time gyrodactylids (at least those that predominantly occur consuming and costly. Whatever the control method on the skin and fins) is a licensed Home Office proce- used (chemical, manual or host isolation), thorough dure in the UK which requires the host to be lightly screening is essential to ensure parasite extinction. anaesthetised (using e.g. 0.02% MS-222, chlorobu- The longer the interval between the 3 consecutive tanel) whilst the living parasites are removed manu- screens the more reliable the procedure. A single ally. Following anaesthesia, the fish is transferred to a (transparent, <1 mm long) gyrodactylid missed in an shallow dish, but kept fully immersed in dechlorinated earlier screen will have had ample time to reproduce in water and screened using a stereo-microscope with situ (as little as 24 h at 25°C) generating a larger num- fibre-optic illumination. The latter is essential to pre- ber of parasites which are less likely to be overlooked vent the host and parasites overheating during exami- on subsequent screens. nation on the microscope stage. Parasites can be most easily detected by their movement, but it is still essential to scan all surfaces of the host. Small fish, such as CONCLUSION guppies and sticklebacks, can be manipulated using a plastic disposable pipette tip. Once a parasite is Although the majority of compounds tested against detected, the worm can be removed and crushed using Gyrodactylus spp. are reportedly effective (see Appen- watchmaker’s forceps. It is essential to ensure that the dix 1), 100% efficacy has not been achieved without parasite is not released directly back into the water as toxicity to hosts. Currently, the lack of comparative even a damaged worm may re-attach to its host and data makes the selection of a drug difficult. Leaving successfully give birth. Once all parasites have been just one (hermaphrodite, viviparous) worm can be suf- removed, the same screening procedure should be ficient to initiate a new disease outbreak. For research repeated until all fish in a population have been projects, manual removal of skin gyrodactylids from screened clear of parasites on 3 consecutive occasions small fish is an option; however, this is not feasible for separated by approximately 1 wk, ideally by 2 inde- gill parasites, larger hosts or for use in aquaculture. pendent, trained researchers. If a parasite is found on Further research into different treatments and their any fish during this process, then the screening pro- application on different species of parasite and host is cess should begin again for the entire host population. necessary to combat the existing problems caused by For small fish, such as poeciliids, manual removal of Gyrodactylus spp. epizootics. parasites can be effective without any chemical inter- vention. However, for larger fish (or where gyro- Acknowledgements. This work was supported by the Natural dactylids are abundant and/or show a preference for Environment Research Council, UK (NER/J/S/2002/00706). the gills), chemical treatment prior to screening may be the only practical solution to parasite removal. In our LITERATURE CITED laboratories we use levamisole, but this is only avail- Anttila P, Kuusela J, Koski P (2007) Disinfection of Gyrodacty- able by veterinarian prescription and only reliable if lus salaris by Virkon S and heat. Poster presentation at the applied to single fish that are closely monitored for 13th International Conference of Fish and Shellfish Dis- signs of toxicity. Screening is still essential to ensure eases by the European Association of Fish Pathologists that fish are free of gyrodactylids following chemical 17–21 September 2007, Grado, Italy. EAFP Abstract Book, p 334. Available at: http://eafp.org/eafp-information/ treatment, with additional screening on subsequent 2009/2/20/grado-2007-information-archived.html occasions to ensure the experimental fish are free from Bakke TA, Harris PD, Cable J (2002) Host specificity dynam- infection. For larger fish, such as adult Atlantic salmon ics: observations on gyrodactylid monogeneans. Int J Salmo salar, sub-sampling by examining mucus scrap- Parasitol 32:281–308 ings or selected fins may be the only practical way of Bakke TA, Cable J, Harris PD (2007) The biology of gyrodactylid monogeneans: the ‘Russian-doll killers’. Adv screening, but this is not accurate. It is also stressful for Parasitol 64:161–376 the fish as it damages the fish’s epithelium, so increas- Bi SP, Yang XD, Zhang FP, Wang XL, Zou GW (2001) Analyt- ing the risk of secondary infections. An alternative or ical methodologies for aluminium speciation in environ- ideally supplementary procedure to manual removal, mental and biological samples — a review. Fresenius J Anal Chem 370:984–996 but again only suitable for small fish, is to maintain Birchall JD, Exley C, Chappell JS, Phillips MJ (1989) Acute each fish in isolation in a closed system with regular toxicity of aluminium to fish eliminated in silicon-rich acid water changes. As fish become immune and gyro- waters. Nature 338:146–148 68 Dis Aquat Org 86: 65–75, 2009

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Can J Fish Aquat Sci 55: Tojo J, Santamarina MT, Ubeira FM, Estevez J, Leiro J, San- 507–514 martin ML (1993b) Efficacy of anthelmintic drugs against Soleng A, Poléo ABS, Alstad NEW, Bakke TA (1999) Aqueous gyrodactylosis in rainbow trout (Oncorhynchus mykiss). aluminium eliminates Gyrodactylus salaris (Platyhel- Bull Eur Assoc Fish Pathol 13:45–48 70 Dis Aquat Org 86: 65–75, 2009 UK (2001), Harris et al. (2008), Caboni et al. (2004) b Tojo et al. (1993a) El-Khatib (2003) Tojo & Santamarina (1998) Tojo et al. (1993a) Tojo et al. (1993a) Tojo & Santamarina (1998) Tojo et al. (1993a) Tojo & Santamarina (1998) Tojo & Santamarina (1998) Tojo et al. (1993a) Tojo & Santamarina (1998) Tojo et al. (1993a) Pesticide Action Network –1 ) Santamarina et al. (1991) a ) Tojo et al. (1992) –1 to 1.4 –1 ) Chansue (2007) a,d,e –1 ) –1 –1 a,d,e a,b,c ) b d,e –1 ) c f e e f e f f e f e ) to 100% –1 –1 a,d,e b ) –1 from 12.6 worms fish Reduced parasite mean Steverding et al. (2005) effective (0.25 mg l Reduced parasite mean from 12.6 worm fish Not effective Not effective Not effective Not effective Not effective to 100% effective after 14 d (5.1 g l Not effective (1.7 g l and reduced prevalence by 45% (20 & 60 mg l (25 mg l Not effective Dose dependent, but none100% effective Ekanem et al. (2004) 96% effective Not effective (200 mg l Not effective Not effective Not effective 98.6% effective (4 mg l Not effective Not effective 99.6% effective Santamarina et al. (1991) ) to 100% effective ) (0.125 mg l –1 –1 ) ) ) ) ) ) ) ) to 95.5% effective ) ) ) ) ) –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 Gasterosteus aculeatus Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Carassius auratus (5 fish treatment (5 fish treatment (5 fish treatment (5 fish treatment (5 fish treatment (5 fish treatment (4–10 fish treatment Oreochromis niloticus auratus (4–10 fish treatment ) (30 ppmv) spp. Hostspp. Efficacy Source sp. sp. sp. sp. sp. sp. sp. to the water G. gasterostei G. arcuatus Gyrodactylus Gyrodactylus and/or Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus G. elegansG. salaris Carassius auratus G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss Oncorhynchus mykiss Gyrodactylus species. With the exception of orally administeredspecies. With treatments, other compounds below were applied directly on salmonids in Norwegian rivers. Kills both fish and parasites. Linked to Parkinson’s disease. G. salaris Gyrodactylus 15°C. Lab study (5 fish treatment 4 wk. Lab study 96 h. Test solution Lab study3 h. 11°C. Lab study 12 & 3 h, respectively. 3 h. 11°C. Lab study 3 h. 11°C. Lab study (10 fish treatment 3 h. 11°C. Lab. study 3 h. 15°C. Lab. study 3 h. 11°C. Lab study 3 h. 11°C. Lab study 3 h. 15°C. Lab study respectively. 18°C. Lab study 15°C. Lab study15°C. Lab study15°C. Lab study (20 fish treatment 15°C. Lab study (20 fish treatment (20 fish treatment (20 fish treatment renewed every 24 h. –1 –1 –1 –1 –1 feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 200 mg l 40 g kg 40 g kg 0.01% Tween 40 g kg 1.7, 3.4 & 5.1 g l 10, 500 & 1000 ppm Indefinite time, 2 & 1 h, ) 25 & 200 mg l ® ) 200 mg l ) 0.25 & 0.125 mg l ) 200 mg l ® ® ® extract 0.5, 1.0, 1.5 & 2 mg l ) Lab study 15°C. (20 fish treatment ) ® ) ® ® extract ® and Tween 80 0.01% Tween (probably catappa (Gabbrocol (Gabroral (Spartrix (1) Botanicals Rotenone Used extensively to treat Albendazole (Oversol (2) General chemotherapeutics Acaprin (Acaprina Aminosidine 200 mg l BenznidazoleBithionol 200 mg l Carnidazole 4, 20 & 60 mg l Chloroquine diphosphate 10 mg l Agerin Amprolium (Prolsal ChloroquineClosantel (Flukiver 40 g kg Compound DoseTea tree oil Application 3, 10 & 30 ppmv inPiper guineense 48 h. 13°C. Lab study Aminosidine 40 g kg Terminalia Appendix 1. Treatments against infections of Appendix 1. Treatments Schelkle et al.: Treatments of gyrodactylid infections 71 2008) Tojo et al. (1993b) Tojo & Santamarina (1998) Tojo et al. (1993a) Tojo et al. (1993a) Tojo et al. (1992) Tojo & Santamarina (1998) Cited in: Schmahl (1993b) Rach et al. (2000) Russo et al. (2007) Santamarina et al. (1991) Tojo et al. (1993b) Tojo et al. (1993a) b,c ) & a,d,e ) ) to Rowland et al. (2006) –1 & Tojo et al. (1992) –1 –1 b,g ) to Buchmann & ) to Schmahl (1993a) –1 –1 –1 ) to toxic Santamarina et al. (1991) a,d,e ) –1 a,c,e –1 g ) a,d,e ) : 4 trout dead –1 –1 d,e –1 b,c d,e a,b,c e f e a,e e b,c e ) –1 ) to 100% effective for 3 h) to 100% –1 h –1 Not effective (2.5 mg l 59% effective (0.025 & Santamarina et al. (1991) Not effective (0.77 mg l (decreased parasite burden);malachite green + formalin, Valtonen (1996) and/or salt not effective after 1 h, expt. terminated) Not effective Not effective Not effective Not effective Not effective 98.6% effective Not effective (2 mg l Not effective Not effective (20, 25 mg l Not effective (0–5 µg l Effective 100% effective 100% host mortality 96% effective Not effective 100% effective(20, 40 & 60 mg l Kristensson (2003) 1 h (15 µg l (0.05 & 0.5 mg l Formalin partially effective Rintamäki-Kinnunen & ) ) to host (10 mg l ) ) 0.25 mg l –1 –1 –1 –1 ) ) ) ) ) )) 25 mg l ) ) –1 –1 –1 –1 –1 –1 –1 –1 –1 trutta & S. t. lacustris Xiphophorus helleri Oncorhynchus mykiss Oncorhynchus mykiss (4–10 fish treatment (4–10 fish treatment Bidyanus bidyanys Oncorhynchus mykiss (5 fish treatment (4–10 fish treatment (5 fish treatment (5 fish treatment (5 fish treatment (5 fish treatment of water for 60 min, or 3.3 g MG in 1 l For used at Srivastava et al. (2004), –1 spp. Host Efficacy Source spp. sp. sp. sp. sp. G. salaris Salmo salar, S. trutta Appendix 1 (continued) G. aculeati Gasterosteus aculeatus G. salaris Oncorhynchus mykiss Gyrodactylus G. salaris Oncorhynchus mykiss Gyrodactylus Gyrodactylus Gyrodactylus G. salarisG. salaris Oncorhynchus mykiss G. salarisG. salaris Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss G. salaris Oncorhynchus mykiss Gyrodactylus G. arcuatusG. groschaffi Gyrodactylus Gasterosteus aculeatus G. salarisG. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss Oncorhynchus mykiss ) (5 fish treatment –1 30 min over 5 d. × 15°C. Lab study effective (>1.5 mg l 13.2–15.7°C. Field trial: sig. decrease (30, 40 mg l 3 h. 15°C. Lab study 3 h. 11°C. Lab study 3 h. 11°C. Lab study 3 h. 15°C. Lab study for 25 mg l 12 & 3 h, respectively. 24.1–26.9°C or applied to ponds 1, 2, 3 & 4 h. 3 h 3 Lab study3 h. 15°C. Lab study 3 h. 15°C. Lab study 3 h. 11°C. Lab study (51–75 fish treatment 15°C. Lab study15°C. Lab study (20 fish treatment 15°C. Lab study (5 fish treatment (20 fish treatment Field trials –1 –1 –1 & Farm study: rotation Putatively ; 1 h; 24 h. 23.5°C. –1 –1 –1 –1 of water as a prolonged immersion. Synergistic effect compounds in combination, but toxic to both parasite and host Fishdoc ( –1 –1 –1 –1 feed 10 d oral treatment. feed 10 d oral treatment. –1 –1 –1 –1 –1 –1 ; 4 g l ; 1.5–2%, of treatments –1 –1 –1 –1 –1 –1 40 g kg 40 g kg 3 & 6 mg l 40 & 60 mg l 10 mg l 0.1 mg l 11 & 16 mg l ) 2 & 10 mg l ® ) 0.5 mg l ) 25 mg l ® ) ) ® ® ® (Ivomec-F salt bath respectively (triazine derivative) 22°C. Lab study effective after 4 h (10 µg l (Panacur (Berenil (Ivomec malachite green (MG) 0.015 ml l green & formalin; 0.2 g l Diethylcarbamazine 200 mg l Formalin; malachite 0.2 g l Ivermectin 0.031 mg l Hydrogen peroxide 170, 280 & 560 mg l DimetridazoleDiminazene aceturate 200 mg l Febantel (Rintal 200 mg l Formaldehyde 2.5, 5, 10, 20, 18 h. Lab study Ivermectin + clorsulon 0.025, 0.25, 0.05 & h. 15°C. Lab study 3 Compound Dose Application FenbendazoleFlubendazole 0.77, 1.5, 6.2, 12.5 & 12 h (additionally, 3 25 & 200 mg l Formalin 20, 25, 30 & 40 mg l Formalin (For) & Recommended use in combination: 3.68 g MG 1 l For, used at 0.025 ml Ketoconazole 200 mg l HOE 092 V 0, 2, 5, 10 & 15 µg l 72 Dis Aquat Org 86: 65–75, 2009 1996), Srivastava et al. Taraschewski (1987) (2004) Tojo & Santamarina (1998) Santamarina et al. (1991) Goven & Amend (1982) Tojo & Santamarina (1998) Cited in: Schmahl (1993b) Cited in: Schmahl (1993b) Goven & Amend (1982) Tojo et al. (1993a) Liao et al. (1996) Tojo et al. (1993a) Tojo & Santamarina (1998) Tojo et al. (1993b) Santamarina et al. (1991) Schmahl & Tojo et al. (1993b) Tojo & Santamarina (1998) b e ) Santamarina et al. (1991) ) –1 a –1 a,e ) to Tojo et al. (1992) ) to Tojo et al. (1993b) ) –1 –1 –1 f b,c b,c b,c d,e f a,e f e e f d,e a,e o. Highly toxic Kou et al. (1988), Liao a,c,e , but all host g,h g,h –1 mo. Carcinogenic b,c 100% effective 100% effective Decrease of parasite Schmahl & 91% effective (0.025 mg l Reduction of parasite burden fish dead) Not effective Not effective Not effective Not 100% effective Not effective 100% effective Not effective (100 mg l Effective Effective Not effective Not effective Not effective Not effective 100% effective Not effective (100 mg l 0.2 mg l ) ) ) to 100% effective (0.05 & –1 –1 –1 )) burden ) ) ) ) )) Taraschewski (1987) ) 95% effective (25 mg l ) ) ) ) ) 100% effective (200 mg l –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 (5 fish treatment (5 fish treatment Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Carassius auratus, Astronotus ocellatus, Pterphyllum scalare, Poecela velifera & Trichogaster trichopterus (4–10 fish treatment (5 fish treatment (4–10 fish treatment (10 fish treatment (5 fish treatment (5 fish treatment (4–10 fish treatment a spp. Host Efficacy Source sp. sp. sp. sp. Appendix 1 (continued) G. aculeati Gasterosteus aculeatus G. salaris Oncorhynchus mykiss Gyrodactylus G. elegans Carassius auratus G. aculeati Gasterosteus aculeatus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus G. salarisG. elegans Oncorhynchus mykiss G. salaris Carassius auratus G. bullatarudis G. elegans Oncorhynchus mykiss G. salarisG. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss Oncorhynchus mykiss G. salarisG. salaris Oncorhynchus mykiss Oncorhynchus mykiss 15°C. Lab study (5 fish treatment 15°C. Lab study15°C. Lab study (20 fish treatment (20 fish treatment 15°C. Lab study (20 fish treatment 20°C. Lab study3 h. 15°C. Lab study 24 h. 23°C. Lab study 12 & 3 h, respectively. (10 fish treatment 24 h 24 h 3 h. 11°C. Lab study 3 h. 11°C. Lab study 3 h. 15°C. Lab study 3 h. 15°C. Lab study 20°C. Lab study3 h. 15°C. Lab study 3 h. 15°C. Lab study (10 fish treatment Tri (10 fish treatment –1 Meb & Field tests. –1 –1 –1 –1 Meb & Tri 24 h. 23°C. Lab study feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 to fish: carcinogenic, mutagenic, chromosomal fractures, teratogenicity and respiratory toxicity. Now banned in the Europe N. America for food fish. Most effective used together with formalin. ( 25 & 100 mg l 1 mg l 0.5 mg l 40 g kg 40 g kg 40 g kg 2.3 mg l 0.2 mg l 0.01 mg l 0.1 µg l )2 mg l mg )2 ) 20 mg l ) 0.025, 0.05 & 3 h. 15°C. Lab study ® ® ® ) ® ) ) ) ® ® ® ) Lab study 15°C. (20 fish treatment ® hydrochloride 100 µg l (Citarin-L (Glucantime (Flagyl (Fugotenil (Ambilhar Levamisol 0, 10, 20, 50 & 25, 30, 60, 90 & 120 min. Mebendazole (Meb)& trichlorfon (Tri) 0.1–0.4 mg l 0.46–1.8 mg l Metronidazole 200 mg l Levamisol hydrochloride 100 mg l Malachite green Recommended use: 0.5–0.8 ppm for 1 d, or 0.015 prolonged immersion. Remains in fish tissue up to m Naftalofos (Maretin Niclofolan (Bilevon Niclosamide Niridazole 6 & 1.5 mg l 100 & 200 mg l Methylene blueMetronidazole Recommendations: 8–10 ppm, bath 1 d; 2 3–5 d. Highly toxic to fish. Remains in fish tissue for up 40 g kg Netobimin (Hapasil Mebendazole 0.1 mg l Compound Dose Application Niclosamide 0, 0.05, 0.075 & 30, 60, 90 & 120 min. Meglumine 200 mg l Schelkle et al.: Treatments of gyrodactylid infections 73 Taraschewski (1987) Tojo & Santamarina (1998) Tojo & Santamarina (1998) Tojo et al. (1992) Tojo & Santamarina (1998) Lewis (1967) Tojo & Santamarina (1998) Tojo & Santamarina (1998) Santamarina et al. (1991) Santamarina et al. (1991) Santamarina et al. (1991) Tojo & Santamarina (1998) Tojo et al. (1993b) Tojo et al. (1993b) , , d,e ) to Santamarina et al. (1991) b,g ) –1 –1 , 3 h) Tojo et al. (1992) , 3 h) Tojo et al. (1992) –1 ) Tojo et al. (1993a) –1 ) to Tojo et al. (1993b) –1 –1 –1 –1 , ca. 60 s, Crigel et al. (1995) –1 f a,e a,e ) f a,e f f f a,e a,e f e e –1 d,e ) –1 b,d a,d,e a,e b,c 100% effective 99% effective (0.04 mg l Decrease in parasite Schmahl & Not effective Not effective Not effective Not effective Not effective Not effective (30 mg l Not effective Not effective (200 mg l Treatment was successful Not effective (200 mg l Not effective Not effective 98% effective Not effective 98% effective (25 mg l Effective (26 mg l time needed to anaesthetise fish) Not effective 156.25 mg l 200 mg l 12 h) 12 h) ) 100% effective (0.07, ) ) ) –1 –1 –1 –1 ) ) ) ) ) ) burden ) ) 100% effective (50 mg l ) ) to 86% effective (25 mg l ) to 91% effective (25 mg l ) ) to 100% effective (100, ) –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss (5 fish treatment (4–10 fish treatment (5 fish treatment (4–10 fish treatment (4–10 fish treatment (5 fish treatment (5 fish treatment (4–10 fish treatment Carassius auratus, Cyprinus auratus (5 fish treatment sp. spp. Host Efficacy Source sp. sp. sp. sp. sp. sp. Appendix 1 (continued) Gyrodactylus G. salaris Oncorhynchus mykiss G. aculeati Gasterosteus aculeatus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus G. salarisG. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. elegans Oncorhynchus mykiss G. salaris Notemigonus crysoleucas Oncorhynchus mykiss G. salarisG. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salarisGyrodactylus Oncorhynchus mykiss Oncorhynchus mykiss G. salaris Oncorhynchus mykiss 15°C. Lab study15°C. Lab study (5 fish treatment (5 fish treatment Lab study 15°C. Lab study15°C. Lab study0.1–0.5 acre (0.04–0.2 ha), ~3 ft (1 m) deep (20 fish treatment 15°C. Lab study15°C. Lab study (20 fish treatment (20 fish treatment 15°C. Lab study (20 fish treatment (20 fish treatment 20–22°C. Lab study 3 h. 15°C. Lab study 3 h. 15°C. Lab. study 12 & 3 h, respectively. Field trial: ponds sized 12 & 3 h, respectively. 3 h. 15°C. Lab study 3 h. 15°C. Lab study 4 h & 16 h. 20°C.3 h. 15°C. Lab study 3 h. 15°C. Lab study 3 h. 11°C. Lab study Ca. 20, 40 & 60 s. (10 fish treatment 3 h. 15°C. Lab study 15°C. Lab study –1 –1 –1 –1 –1 –1 –1 feed treatment, respectively. (20 fish treatment feed 10 d oral treatment. feed 10 d oral treatment. feedfeed 10 d oral treatment. 10 d oral treatment. feed 10 d oral treatment. –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 50 µg l 40 g kg 40 g kg 40 g kg ) 10 mg l ) 50 mg l ® ® ) ) 6.25 g kg ) ® ® ® ) ) 156.25 mg l ® ® (Distomicine (Lopatol 500 dihydrochloride (Trilombrin (Lopatol (Atabrine Nitroscanate 40, 6.25, 0.63, 10 d, 2 1 d oral Praziquantel (Droncit Parbendazole 25 & 200 mg l Nitroscanate 0.04, 0.07 & 3 h. 15°C. Lab study Oxfendazole 25 & 200 mg l Paraformaldehyde Ca. 10 g l PiperazinePiperazine citratePiperazine 200 mg l 40 g kg Praziquantel 200 mg l 0, 1, 5, 10, 20 & Pyrantel pamoate 15, 30, 60, 90, 120 min, 50 mg l Oxibendazole 25 & 200 mg l Quinacrine HCl 25, 100 & 200 mg l Compound DoseNitroxynilNitroxynil Application 30 & 50 mg l 40 g kg QuinaldineRafoxanide (Ranide 0, 26, 104 & 260 mg l 74 Dis Aquat Org 86: 65–75, 2009 Tojo & Santamarina (1998) Tojo et al. (1993a) Tojo & Santamarina (1998) Tojo et al. (1993a) Tojo et al. (1993b) Tojo et al. (1993b) Tojo & Santamarina (1998) Tojo et al. (1992) Tojo et al. (1993b) Tojo & Santamarina (1998) Tojo & Santamarina (1998) Goven & Amend (1982) Cited in: Schmahl (1993b) Schmahl & Santamarina et al. (1991) Tojo & Santamarina (1998) g a ) Buchmann & –1 ) to Schmahl & for Tojo et al. (1992) –1 –1 for 12 h) –1 f for 3 h) to 10% e d,e a,e f f e e f a,d,e e f f b,c g f –1 g ) a,b,c ) –1 –1 effective (10 d) Not effective (10, 20 mg l Not effective (5, 10 µg l Temperature dependent:119.7 min (25°C) to 9 s (40°C) Anttila et al. (2007) Not effective Not effective Not effective Not effective Not effective Not effective Time dependent: parasite Tojo & Santamarina (1998) 84% effective Not effective Not effective 95% effective Not effective Not effective (50 µg l Not effectiveNot effective Tojo et al. (1993a) Not effective 98% effective Not effective (6.2 mg l 160 mg l ) effective after 2 h Mehlhorn (1988) ) –1 –1 ) ) ) ) ) ) )) ) reduction (5 d) to 100% Taraschewski (1987) ) ) ) ) ) ) ) ) 12 h, 25 mg l –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 (5 fish treatment Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss Oncorhynchus mykiss (5 fish treatment (5 fish treatment (5 fish treatment (5 fish treatment (5 fish treatment (10 fish treatment (4–10 fish treatment (5 fish treatment ) to 100% effective (80, Kristensson (2003) spp. Host Efficacy Source sp. sp. sp. sp. sp. sp. sp. sp. Appendix 1 (continued) G. derjavinoides G. derjavini Oncorhynchus mykiss G. arcuatus Gasterosteus aculeatus Gyrodactylus G. salaris Oncorhynchus mykiss (= Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus Gyrodactylus G. salaris Oncorhynchus mykiss G. salarisG. salarisG. salaris Oncorhynchus mykiss Oncorhynchus mykiss G. salaris Oncorhynchus mykiss G. salaris Oncorhynchus mykiss Oncorhynchus mykiss G. salarisG. elegans Oncorhynchus mykiss Gyrodactylus G. aculeati Carassius auratus G. salaris Gasterosteus aculeatus G. salaris Oncorhynchus mykiss Oncorhynchus mykiss for 3 h) (5 fish treatment –1 40°C. Lab study fin clips parasite survival ranges from 15°C. Lab study (20 fish treatment 15°C. Lab study15°C. Lab study (20 fish treatment 15°C. Lab study (20 fish treatment 15°C. Lab study (20 fish treatment 15°C. Lab study (20 fish treatment 15°C. Lab study15°C. Lab study (20 fish treatment (20 fish treatment effective (25 mg l 3 h. 11°C. Lab study 3 h. 11°C. Lab study 3 h. 15°C. Lab study 3 h. 15°C. Lab study 3 h. 15°C. Lab study 3 h. 15°C. Lab study 20°C. Lab study3 h. 15°C. Lab study 24 h. 23°C. Lab study Continuous 25, 30, 60 & 90 min. 3 h. 15°C. Lab study (10–15 fish treatment 12 h (additionally, –1 –1 –1 –1 feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d oral treatment. feed 10 d & 5 oral treatment. –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 200 mg l 50 µg l 0.25 mg l 40 g kg 40 g kg 40 g kg 200 mg l 160 mg l ) 100 mg l ® ) 200 mg l ® ) ® ) ) 25 mg l ® ) ® ® sulpha-quinoxaline (Triasox (Nermafax 20 (Metrifonate)(Neguvon 20°C. Lab study (10 fish treatment (Fasinex Ronidazole 40 g kg Trichlorfon 0, 10 & 50 µg l Sodium percarbonate 10, 20, 40, 80 & 18 h. Lab study Thiabendazole 10 & 100 mg l Toltrazuril 5, 10, 20, 30 &Trichlorfon 0.3, 1, 2, 3, 4 & 6 h. Up to 2 mg l Trichlorfon Triclabendazol 200 mg l 6.2, 12.5 & 25 mg l Secnidazole 40 g kg Suramin (Naganol Tetramisole (Nemicide ThiophanateThiophanate 200 mg l 40 g kg Compound DoseSodium Application 200 mg l TriclabendazoleVirkon S + heat 40 g kg Low concentration 25, 30, 35 & Schelkle et al.: Treatments of gyrodactylid infections 75 No primary h c Carter (2003) Poléo et al. (2004) d ). b,c –1 ) to Poléo et al. (2004) ) to Poléo et al. (2004) –1 –1 g b,c Causes mortality in some or all hosts; c g d c b,c c ) ) –1 –1 b,c Mortality not indicated by author; b,d g Not effective (25 µg l Not effectiveNot effective (50 µg l Poléo et al. (2004) decrease in parasites Al-rich water: 100% effective Al-rich water: 100% effective Pettersen et al. (2006) Decrease in peak parasite Gheorgiu et al. (2005) Time dependent effect: no Soleng et al. (1998) Not effective (5–7‰) to 100% Buchmann (1997) No effect of pH, but dose- Soleng et al. (1999) Not effective (after 5 & 15 d in Carter (2003) parasite burden after 30 d Not effective Not effectiveNot effective Poléo et al. (2004) effect of Al was enhanced: 100% effective after 9 d not effective. (60 min) ) (33‰) –1 ) effective (10–20‰) –1 ) 100% effective after 3 d ) ) ) ) dependent effect. At pH 5.0 ) after 3 d. Al-poor water: ) after 8 d. Al-poor water: ) effect (5 min) to 100% effective –1 –1 –1 –1 –1 –1 –1 –1 mucus scrapings; f (fins of 6 fish Not effective (5.0‰) to 100% Soleng & Bakke (1997) others, 12 fish treatment (15 fish treatment (21–23 fish treatment pelvic fin clips, or ) (10 fish treatment e spp. Host Efficacy Source Appendix 1 (continued) G. derjavinoides) G. derjavinoides G. salaris Salmo salar G. salarisG. salaris Salmo salar Salmo salar Gyrodactylus G. salaris Salmo salar G. macronychus Phonixus phonixus G. derjavini Salmo trutta G. turnbulli Poecilia reticulata G. salarisG. derjavini(= Salmo salar Oncorhynchus mykiss G. salaris Salmo salar G. bullatarudisG. turnbulli Poecilia reticulata G. salarisG. salaris Poecilia reticulata Salmo salar Salmo salar 12°C. Lab study (15 fish treatment recovered. 8°C. Lab study8°C. Lab study (200 µg l 8°C. Lab study recovered. 8°C. Lab study until fish died/ recovered. (>50 parasites host 23°C. Lab studyuntil fish died/ recovered. (>50 parasites host 20 d trials) to decrease in (11–15 d) until fish died/ (>50 parasites host 20 & 30 d. 60 d. 23°C. Lab study Continuous exposure Continuous exposure (11–15 d) until fish died/(11–15 d) until fish died/recovered. 8°C. Lab studyrequired conc.; afterinfection continuous ex- (>50 parasites host 100% effective after 3 d (400 µg l establishment (240 µg l burden, but higher infection posure until isolated fish died/ recovered (up to29 d) 25°C. Lab study Combined effects of parasite infection & Zn exposure more detrimental to host than parasite –1 –1 –1 at Continuous exposure at Continuous –1 Infection intensity was determined by sub-sampling methods other than screening the entire fish; b –1 –1 –1 –1 –1 Infection intensity was determined 24 h post-treatment by 800 µg l control (pH 6.3) 20 & 33‰ salinity 1.4, 6 & 12°C. Lab study for 33‰ salinity; all effective after a few minutes Al-rich & Al-poor Continuous exposure. 5 µg l 8.3, 23.7, 38.1, 68.5, 1 wk pre-exposure to 33‰ salinity5–20‰ NaCl 5, 15, 30 & 60 min. 4 d. 11°C. Lab study water (pH 5.8) & 11–13°C. Lab study ( 129.5 & 260.3 µg l 200 µg l 400 µg l e,f tests included in study; (& acidification) pH 5.0, 5.2, 5.6 & 5.9 (4–30 d) 12°C. Lab study (15 fish treatment literature available Signs of host toxicity; In vitro (3) Metal salts Aluminium 25, 50, 100 & Continuous exposure IronManganeseZinc 25, 50, 100 & 200 µg l 100, 200, 400 & Continuous exposure 50, 100, 200 & Continuous exposure Copper 10, 20, 40 & 80 µg l Compound DoseAluminium 92–250 µg l Application Cadmium 5 µg l 4. Salt Salinity 5, 7.5, 10, 15,a d Continuous exposure.

Editorial responsibility: Bernd Sures, Submitted: January 19, 2009; Accepted: May 6, 2009 Essen, Germany Proofs received from author(s): September 1, 2009