The Effects of Macrocyclic Lactones^§ on Dung Insects – Myths and Realities

In 1998, a detailed review of the effects of macrocyclic lactones (ML’s) on dung beetles and other dung-eating Insects has been carried out by the then National Registration Authority for Agricultural and Veterinary Chemicals (the NRA). The NRA is now called the Australian Pesticides and Veterinary Medicines Authority (the APVMA). This special review¹ of most of the information available at the time is available on line (http://www.apvma.gov.au/chemrev/maclac.pdf) or can be obtained by contacting the APVMA or your ANCARE representative. The document is 94 pages long and rests on the examination of no less than 96 bibliographic references and studies. The present ANCARE document is essentially a summary of the main findings of the review.

INTRODUCTION

The principal focus of this review is the dung-eating insect fauna of cattle dung in Australia, which by comparison with Europe contains an impoverished fauna and is used primarily by several species of abundant flies and 20 or so purposely introduced dung beetles together with a few native dung beetle species which have adapted successfully to utilising the dung of introduced livestock.

Commencing in 1968, the CSIRO Dung Beetle Program imported 52 species of dung beetles from southern Africa and Europe of which a total of 42 species was released and 22 of these had established breeding populations in the field by 1991 (See Tables on page 2).

A dung beetle (Onthophagus gazella)²

Wherever the exotic species have become established in Australia there has been a significant increase in cattle dung dispersal through burial and shredding. Dung beetles only have a minor role in decomposition of sheep dung under Australian conditions although they undoubtedly use it as a feed resource.

MYTH 1 – Moxidectin is completely safe for all species of dung beetles

Moxidectin residues in cattle dung are considered non-toxic to egg-laying adults and developing larvae.

No data are available on the effects of moxidectin residues in cattle dung on mortality of newly emerged adult dung beetles or their reproductive development. Slower rates of excretion in faeces presumably contribute to the lack of toxic effects on larval development but there has been no examination of possible sublethal effects on beetle populations arising from the longer-term excretion pattern of moxidectin in cattle dung.

Moxidectin residues excreted in sheep dung during the first two days after oral treatment inhibit larval development in the one species of dung beetle tested. This is consistent with the high residue levels in faeces at that time and suggests that other species may be similarly affected.

Moxidectin residues in sheep dung 2 days after oral drenching caused a 46% reduction in emergence of Aphodius constans larvae. The genus Aphodius is prevalent in Australia.

This beetle genus was introduced accidentally c1850 from South America and is established on Dividing Range from Victoria to northern New South Wales⁸.

An Aphodius spp dung beetle⁵

These observations, together with the protracted excretion profile for moxidectin residues in sheep dung, indicate the need to evaluate possible sub-lethal effects on larvae and immature adults of the more important Australian species to assess the risk exposure to dung beetle populations of moxidectin drenching of sheep.

A 1997 observation, not mentioned in the 1998 NRA review, and only recently reported by two CSIRO scientists (Steel & Wardhaugh, 2002)⁶, also showed that moxidectin administered subcutaneously to cattle reduced the fecundity of the dung beetle species Euoniticellus fulvus feeding on the dung of treated cattle.

An Euoniticellus spp dung beetle⁹

MYTH 2 – There are no moxidectin residues in dung

Macrocyclic lactones are almost entirely excreted in faeces but the rate differs considerably between the various commercial compounds […]. Following subcutaneous or pour-on dosing, ivermectin levels in cattle faeces peak within 2-6 days and negligible or very low levels persist beyond 14 days. Doramectin is excreted at a similar rate to ivermectin. Moxidectin residues are excreted more slowly and persist in cattle faeces for more than 28 days.

In cattle by 28 days only trace amounts of ivermectin metabolites continue to be excreted in bile [and then in faeces] whereas 40 ppb of moxidectin residues are present at this time. Similar patterns are evident in sheep: removal of ivermectin residues from sheep tissues is substantially faster than for moxidectin.

Excretion of moxidectin residues in faeces continues for more than 28 days at which time the cumulative excretion totals 58% of the dose, whereas cumulative excretion of ivermectin residues is 62% of the dose at 7 days.

Pour-on administration of ivermectin at 500 mg/kg resulted in higher initial concentrations in faeces (9 ppm dry matter) but by 5 days these were similar (2.8 ppm dry matter) to those following subcutaneous treatment. By contrast, pour-on treatment of cattle with moxidectin results in substantially lower faecal residue concentrations than after subcutaneous dosing and peak levels were not attained until 11 days.

MYTH 3 – All macrocyclic lactones have the same activity on Insects

Ivermectin residues in cattle faeces following subcutaneous treatment are highly toxic to the development of the larvae of the horn fly, Haematobia irritans, with mortalities of 100% initially and impaired development being evident in faeces collected for up to 8 weeks. Faeces of moxidectin-treated cattle exhibited lower toxicity against this species for a considerably shorter period of 3 days, with maximum mortality of approximately 75% on day 1.

Against the closely related buffalo fly, Haematobia irritans exigua, whereas abamectin levels of 4 ppb or greater caused 100% mortality there were no toxic effects of moxidectin until levels exceeded 64 ppb.

When given subcutaneously to cattle, ivermectin reduces larval development of the fly Musca spp. in dung for at least 2 weeks and up to 7 weeks after treatment. Of particular interest in the Australian context is the impact on the bushfly M. vetustissima which exhibits reduced larval development for at least 4-5 weeks when eggs are laid in dung of cattle treated with ivermectin or abamectin. By contrast there was no effect on development of M. domestica [the house fly] and M. vetustissima [the bushfly] larvae on dung collected as early as 3 days after subcutaneous treatment of cattle with moxidectin.

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These observations are consistent with the fact that ivermectin has a >99% efficacy on bots (Gasterophilus spp) in horses, whereas moxidectin efficacy is variable⁷.

MYTH 4 – Ivermectin and Abamectin deplete dung beetle populations

Neither ivermectin nor abamectin is toxic to mature egg-laying adults at concentration likely to be found in [cattle] dung. However, there is increased mortality and impaired development of larvae with sub-lethal effects on the morphology of some species in dung voided within 2-3 weeks of treatment, and increased mortality and delayed reproductive development in newly emerged adults of some species feeding on dung voided within 1 to 2 weeks of treatment.

In Europe, there is no evidence for long-term adverse effects of ivermectin or abamectin residues on the degradation of dung pats or on the accumulation of dung on pasture, despite initial reductions in insect larvae and dung disappearance rate.

Under Australian conditions, it has been shown that adult native and introduced species of dung beetles actively colonise the dung of treated cattle and that short-term increases occur in burial rates of dung containing avermectin residues.

Studies in Spain (Lumaret et al., 1993) 3 and Australia (Wardhaugh & Mahon, 1991)⁴ have given results that contrast with the Northern European observations of the impact of ivermectin and abamectin on adult dung beetles; increased numbers of adult Coleoptera were recovered in pats prepared from faeces deposited up to 17 days after subcutaneous treatment, which suggests that dung containing avermectin residues may be more attractive to the particular Scarabaeid species of dung beetles present in these environments.

[In the Australian study] dung collected 3 days after treatment with abamectin attracted more beetles than dung from untreated animals and this effect was still evident with day 25 but not day 35 dung.

MYTH 5 – Dung degradation is adversely affected by macrocyclic lactone treatments

The review has studied 13 experiments, which examined ivermectin or abamectin and one experiment, which examined doramectin effects on the degradation of artificial or naturally voided cattle dung pats. No experiments have been reported on the degradation of dung from cattle treated with moxidectin.

Experiments in Germany, France, England and Scotland were generally unable to detect any significant change in degradation rate or in the long-term accumulation of dung on the paddock following subcutaneous, topical or bolus treatment with ivermectin. In one experiment there was no long-term effect of abamectin given subcutaneously on degradation of dung collected 3 days after treatment despite an initial reduction in the rate of disappearance.

Under field conditions in Zimbabwe freshly deposited dung is rapidly buried by onthophagine and oniticelline dung beetles and may largely disappear within 24 hours. The lack of effect on dung degradation in this study is therefore consistent with the absence of effect on adult beetle mortality of ivermectin residues in dung. Similarly, in Australia the increased rate of burial of cattle dung collected shortly after abamectin treatment was consistent with the observed increases in adult beetle populations and their tunnelling activity.

Only one investigation has been reported of the effects of macrocyclic lactone treatment of sheep on the degradation of dung deposited on pasture under Australian conditions. In this study the accumulation of dung was measured on paddocks which grazed sheep during and for 140 days following treatment with ivermectin released from an intraruminal capsule at 1.6 mg/day for 100 days. No significant differences were found at any sampling time throughout the 240 days in the dry weight of dung collected at multiple sites on each paddock between the ivermectin treatment, albendazole treatment at 32.5 mg/day for 100 days using a similar capsule or the untreated control group.

CONCLUSION

These observations illustrate the complexity of interpreting changes in the abundance of dung beetle fauna associated with avermectin treatment. Without a more complex analysis of dung beetle population dynamics taking into account many factors including climatic effects, mobility, regional differences in species abundance and diversity, frequency of actual usage of macrocyclic lactones in different classes of cattle, proportion of the population exposed at particular stages of the life cycle and the relative impact of the various compounds on the different species, it is not possible to quantify potential impact on overall fitness of these beetle populations.

There are substantially more published papers in scientific journals on ivermectin and abamectin effects on dung insects and dung degradation than for moxidectin and there are none on doramectin.

Based on the findings of the detailed review, it is concluded that there is no clear evidence to demonstrate that any of the macrocyclic lactone products have a long-term detrimental effect on dung beetle populations or dung disappearance rates in the field in Australian conditions.

REFERENCES

1. NRA Special Review of MACROCYCLIC LACTONES, NRA Special Review Series 98.3 by the Chemical Review Section, National Registration Authority, Canberra, AUSTRALIA, May 1998
2. Photograph of Dung Beetle (Onthophagus gazella) from Department of Entomology, Texas A&M University: http://entowww.tamu.edu/images/insects/common/images/b-txt/bimg147.html
3. Lumaret JP, Galante E, Lumberas C, Mena J, Bertrand M, Bernal JL, Cooper JF, Kadiri N & Crowe D, 1993. Field effects of ivermectin residues on dung beetles. Journal of Applied Ecology, 30, 428-436.
4. Wardhaugh KG & Mahon RJ, 1991. Avermectin residues in sheep and cattle dung and their effects on dung-beetle (Coleoptera: Scarabaeidae) colonization and dung burial. Bulletin of Entomological Research, 81, 333-339.
5. Photograph of Dung Beetle (Aphodius fimetarius) from Olaf Wolfram http://www.koleopterologie.de/gallery/fhl08/aphodius-fimetarius-foto-wolfram.html
6. Steel JW and Wardhaugh KG – Ecological Impact of Macrocyclic Lactones on Dung Fauna, p. 149 in Vercruysse J and Rew RS (eds) – Macrocyclic Lactones in Antiparasitic Therapy – CABI Publishing, Oxon, New York, 2002 (ISBN 0 85199 617 5)
7. Monahan CM and Klei TR – The Use of Macrocyclic Lactones to Control Parasites of Horses, p. 327 in Vercruysse J and Rew RS (eds) – Macrocyclic Lactones in Antiparasitic Therapy – CABI Publishing, Oxon, New York, 2002 (ISBN 0 85199 617 5)
8. The Australian Museum: http://www.austmus.gov.au/biodiversity/dungbeetle/index.htm
9. Photograph of Dung Beetle (Euoniticellus intermedius) © Rebecca Harris, The Australian Museum

GENESIS TM TAPE
contains 1 g/L abamectin and 18.8 g/L praziquantel

§ Macrocyclic lactones registered for use in large animals in Australia comprise the avermectins (ivermectin, abamectin, eprinomectin and doramectin) and the milbemycins (moxidectin).