Toxicity of ivermectin to estuarine and marine invertebrates

@

Marlin' PollutionBulh'tin,Vol. 36, No. 7. pp. 540-541, 1998 Pergamon

© 1998 Elsevier Science l.ld. All rights reserved Printed in Great Britain (I1125-326X/98 $ I9.(l(l+ll.0(I

PII: S0025-326X(98)00012-5

Toxicity of Ivermectin to Estuarine and Marine Invertebrates ALASTAIR GRANT and ANDREW D. BRIGGS*

School of Environmental Sciences, University of East Anglia, Norwich, NR4 7TJ, UK

The veterinary antihelminthic agent ivermectin is effective against sea-lice infections in farmed salmonid fish (Palmer et al., 1987). The treatment has recently been licensed in the UK (Anonymous, 1996; Scottish Environment Protection Agency, 1997), but there is evidence of widespread illegal use prior to approval (Siggins, 1990; Clover, 1991; Edwards, 1996; Anonymous, 1997a). There is very little published information on its toxicity or environmental effects (Roth et al., 1993; Edwards, 1996; Anonymous, 1997a; Anonymous, 1997b; and see Table 1). Salmon food containing therapeutic doses of ivermectin is acutely toxic to Crangon septemspinosa (Burridge and Haya, 1993). Ivermectin is extremely toxic to Daphnia magna, and the chemically related abamectin has a chronic toxicity threshold in the range from 0.0035 to 0.0093 ~.tg1- i for Mysidopsis bahia (Wislocki et al., 1989). Here we report the toxicity values of ivermectin for a number of marine invertebrates. These data raise further concerns about possible adverse effects in the marine environment. Toxicity testing used static tests in artificial seawater with daily renewal of toxicant and water. Artemia salina nauplii were hatched in the laboratory and other test organisms were collected from three sites in Norfolk, UK. Toxicity testing on free living nematodes followed Millward and Grant (1995). Toxicity testing of Artemia and Neomysis integer took place at 20°C. All other tests took place at 12°C. Water salinities were similar to those from which the animals were collected (3.5%0 for Palaemonetes, Gammarus, Sphaemma and Potamo-

pyrgus; 17.5%o for Carcinus, Hydrobia, Littorina, Nereis and nematodes, and 35%~ for Artemia). Ivermectin was obtained from Sigma chemicals (Poole, Dorset) and stock solutions made up in ethanol. Control mortality was always less than 10%. LCso values vary from 0.026 to more than 10000 t-tg l -I (Table 2). The most sensitive organisms are the mysid N. integer and the amphipod Gammarus spp. Toxicity thresholds for these species are as low as 0.003 t-tgl ~. These values are an order of magnitude lower than those for other species reported in the literature (Table 1), but are comparable with those reported for abamectin (Wislocki et al., 1989). Molluscs and nematodes have the highest LCs0 values, but sublethal effects on the behaviour of Littorina littorea were observed at low concentrations. Animals exposed

TABLE 2

LC~o and LCm values for species tested, calculated using probit analysis (96 h values, except where indicated). LC~ (Itg 1 i)

95% confidence interval

0.026 t 0.033 54 > 3003 348 957

0.013-0.051 0.011-0.069 44-67

Calculated LCu, (,ug I t)

Crustacea

Neomysis integer Gammarus spp. 2 Palaemonetes varians Artemia salina Sphaemma rugicauda Carcinus maenas

263-401 664-1269

0.0036 0.0033 9.4 ~3 139 88

Gastropoda TABLE 1 Summary of published information on the toxicity of ivermectin to aquatic organisms (fi-om Halley et al., 198%; Halley et al., 1989b; Burridge and Haya, 1993).

Littorina littorea Hydrobia uh,ae Potamopyrgus jenkinsii

Daphnia magna Crangon s(7)temspinosa Rainbow Trout (Salmo gairdneri) Bluegill sunfish (Lepomis macmchims)

Acute LCsu ([_lg I I) 0.025 N O E C > 21.5 3.0 4.8

*Present address: 50 St O m e r Close, Mulbarton, Norwich, NRI4 8JU, UK.

--

> 10004 > 10 000 18005

Polychaeta

Nereis divet:sk'olor Nematoda +'

Organism

> 10004 > 10 000 < 9000 7.75 > 10 000

6.7-9.1

5.4 > i0 00(Y'

I 48 h LC~<~.

2 A mixture of G. dueheni and G. zaddachi in a ratio of approximately 1 to 4. ~ 24 h LC~. 4All animals dead after 7 2 h in 10000,ttgg i. No mortality in 1000 pg g =. 5 Determined by inspection of data, rather than calculation. ~' Unselective sample of free living nematodes from a mid-estuarine site.

540

Volume 36/Number 7/July 1998 to 1.0 ~,tg 1-J w e r e u n a b l e to crawl and only r e t r a c t e d into t h e i r shells w h e n s u b j e c t e d to v i g o r o u s m e c h a n i c a l s t i m u l a t i o n . T h i s c o n c e n t r a t i o n is m o r e t h a n 1000 t i m e s l o w e r t h a n t h e LCs~. l m m o b i l i s a t i o n o f A r t e m i a o c c u r r e d at c o n c e n t r a t i o n s w h i c h a r e a f a c t o r o f 100 less t h a n a c u t e LCso values. If t h e s e e f f e c t s o c c u r r e d in t h e field, a f f e c t e d i n d i v i d u a l s w o u l d b e rapidly e a t e n by c a r n i v o r e s , so t h e low a c u t e t o ' d c i t y to m o l l u s c s a n d A r t e m i a m a s k s t h e fact t h a t a c u t e e c o l o g i c a l effects will o c c u r at 1 lag l - J for Littorina a n d at less t h a n 3 lag 1- 1 for A r t e m i a . It is c l e a r t h a t i v e r m e c t i n is e x t r e m e l y toxic to s o m e m a r i n e a n i m a l s . In v i e w o f this, m o r e d a t a a r e u r g e n t l y r e q u i r e d r e g a r d i n g its toxicity a n d p e r s i s t e n c e in t h e field. It is difficult to justify its c o n t i n u e d use until its e n v i r o n m e n t a l risks a r e u n d e r s t o o d m o r e clearly. We are grateful to Tim Benton for commenting on the manuscript. Since submission of this article, reports of toxicity of ivermectin to Neomysis integer and Arenicola marina have been published (Davies et al., 1997; Thain et al., 1998). Both species are reported as very sensitive to ivermectin, although the reported LC5¢~ for Neomysis (0.07 I-tgl- i ) is slightly higher than ours. Anonymous. Threat from new fish lice treatment. Marine Pollution Bulletin, 1996, 32, 694. Anonymous. German scare on Scottish salmon. Marine Pollution Bulh'tin, 1997, 34, 71. Anonymous. Salmon boycott. New Scientist, 1977, 154(2081 ), 16. Burridge, L. E. and Haya, K. The lethality of ivermectin, a potential agent for treatment of salmonids against sea lice, to the shrimp Crangon septemspinosa. Aquaculture, 1993, 117, 9-14.

Clover, C. (1991) Salmon shops to be tested for pesticide. The Daily Telegraph 8 July 1991. Davies, 1. M., McHenerey, J. G. and Rae, G. H. (1997) Environmental risk fi-om dissolved ivermectin to marine organisms. Aquaculture, 158, 263-275. Edwards, R. Salmon farmers win licence to kilt. New Scientist, 1996, 151(2046), 4. Halley, B. A., Jacob, T. A. and Lu, A. Y. H. The environmental impact of the use of Ivermeetin: Environmental effects and fate. ChenTosl~helv, 1989, 18, 1543-1563. Halley, B. A., Nessel, R. J. and Lu, A. Y. H. (1989b) Environmental aspects oflvermectin usage in livestock: general considerations. In lvermectin and Abamectin. ed. W. C. Campbell, pp. 162-172. Springer, New York. Millward, R, N. and Grant, A. Assessing the impact of copper on nematode communities from a chronically metal-enriched estuary using pollution induced community tolerance. Mm'ine Pollution Bulletin, 1995, 30, 701-706. Palmer, R., Rodger, H., Drinan, E., Dwyer, C. and Smith, P. R. Preliminary trials on the efficacy of ivermectin against parasitic copepods of Atlantic salmon. Bull. Eut: Ass. Fish. Pathol., 1987, 7, 47-54. Roth, M., Richards, R. H. and Somerville, C. Current practices in the chemotherapeutic control of sea lice infestations in aquaculture. A review. Journal q]" Fish Diseases, 1993, 16, 1-26. Scottish Environment Protection Agency (1997) Marine Cage Fish Farming in Scotland, Regulation and Monitoring. Scottish Environment Protection Agency, Stirling. Siggins, L. (1990) Unlicensed sea lice drug used in fish farms, h'ish Times, 22 December 1990. Thain, J. E., Davies, I. M. and Rae, G. H. (1998) Acute toxicity of ivermectin to the lugworm Arenicola marina. Aquaculture, ]59, 47-52. Wis[ocki, P. G.. Grosso, L. S. and Dybas, R. A. (1989) Environmental aspects of Abamectin use in crop protection. In lvetwTectin and Abamectin, ed. W. C. Campbell, pp. 182-200. Springer, New York.

541