Research Proposal

Decomposer biodiversity and decomposition processes: the functional consequences of chemical and natural anthelmintics

Introduction

The intensification of agriculture over the last 50 years in the UK has been associated with substantial losses of biodiversity (Woodcock et al., 2006). While of considerable intrinsic value, diverse communities within agricultural systems play a number of essential functional roles, such as pollination, pest control, seed dispersal and decomposition. The presence and successful activity of these communities are critical to effective ecosystem function.

Decomposition is an ecosystem function of particular importance, as the timely decay of plant and animal remains is essential to carbon and nitrogen cycles, soil fertility and population dynamics of a wide range of inter-linked species. In many agroecosystems, the cycling of organic matter through herbivore dung into the soil, plays an important role in helping to maintain pasture fertility and productivity (Lumaret and Kadiri 1995; Stevenson and Dindal 1987). The healthier the dung decomposer community, the higher the rate at which dung is broken down and removed from pastures, a fact that is of great importance to farmers. It has been estimated that dung beetle activity staves the loss of $380 million to the US cattle industry per year (Losey & Vaughan, 2006). The activity of the invertebrates that contribute to dung decomposition can, however be disrupted by a range of agricultural practices, particularly the treatment of livestock with insecticides and anthelmintics. Endectocides, or macrocyclic lactones, are a class of veterinary pharmaceuticals that have a broad spectrum of activity against nematodes and arthropods, are convenient to use, and have low mammalian toxicity. For these reasons, they have achieved global popularity since the introduction of ivermectin in the early 1980s.

Anthelmintics are excreted primarily in the faeces of the treated animal where they may continue to exert an insecticidal effect (Fisher & Mrozik, 1992; Floate, 1998). Therefore, the application of anthelmintics to reduce numbers of internal parasites of livestock can also reduce numbers of insects in their dung (Floate et al., 2005 and references therein). Only a small percentage of insects associated with cattle dung are pests and reductions in non-pest species may have undesired consequences. Firstly, reduced levels of insect feeding and tunnelling can slow dung degradation (Holter, 1979). This prolongs pats as feeding sites for pest flies and helminth parasites, reduces available grazing area, and reduces soil nitrogen in pastures: the activity of dung beetles effectively recycles tons of nitrogen that would normally be lost to the atmosphere (references in Fincher, 1981). Secondly, parasitic and predaceous insects of the cattle dung community help maintain pest species at low levels, but have been shown to be more sensitive to endectocide residues than their hosts (Floate & Fox, 1999). Indirect effects of ivermectin have also been shown to alter host quality, and hence sublethal effects may influence parasitoid activity and success in controlling prey numbers (Floate & Fox, 1999). Thirdly, insects breeding in dung may provide a significant source of food for endangered populations of bats (Jones, 1990), as well as farmland birds, which have been experiencing a severe decline over the last three decades, probably as a result of agricultural intensification (Chamberlain et al., 2000).

The importance of an appropriate dung-decomposer insect community was perhaps most clearly demonstrated in Australia, where the native dung beetles, which feed preferentially on dry marsupial dung, were unable to feed on the wetter dung of introduced large herbivores such as cattle and horses. The result of this was extensive pasture pollution and increased pest fly populations, necessitating a major programme to introduce exotic dung-burying beetles (Bornemissza, 1976).

Natural wormers, based on herbal formulations are gradually becoming available as alternatives to these chemical treatments. However, there have been no published studies of the impact of natural cattle worming practices on dung insect populations and dung decomposition, or direct comparisons of impacts of natural compared to chemical wormers on dung insects. Along with the major global shift towards more extensive farming practices, a growing number of producers are turning towards the organic sector. Currently, what discourages more farmers from converting is the question of how to tackle their worm problems without the use of chemical wormers, not allowed under Soil Association organic ruling. In addition to this, the increasing problem of parasite resistance to ivermectin and related drugs (Xu et al., 1998) is increasing the need to find and use alternative methods of control. As yet, there are mixed reports on the success of natural wormers at controlling intestinal parasites. But an unpublished ovicidal effectivity test using the natural wormer Verm-X has been shown to reduce larval hatching by 91%. It is also often claimed that natural wormers exert less of a toxic effect on dung beetles than chemical wormers; however it is not acceptable to assume that natural wormers would have any less of an impact on dung invertebrates without comprehensive research to back it up.

Aims

1. To assess the effect of faecal drug residues on the natural assemblage of insects developing in the dung of cattle treated with oral doses of chemical and natural wormers.

2. To assess the effects of these products on the degradation rate of dung from treated cattle to relate dung community composition and diversity to decomposition function (e.g. Lee & Wall, 2006a,b).

3. To use standard laboratory tests for toxicity in order to assess toxicity of these products to Scarabaeidae.

4. To investigate the relationship between diversity and decomposition through experimental field manipulations: altering community structure, by addition or exclusion of specific invertebrate groups.

5. To assess the effect of test products on the growth of pasture herbage and underlying soil aeration and nitrogen incorporation facilitated by Scarabaeidae.

Materials and methods

Location: Pembrokeshire. The effects of faecal dung residues following the oral administration of ivermectin, fenbendazole, moxidectin (cydectin), Verm-X, Wormwood and a control on dung-colonising Coleoptera, Diptera and Hymenoptera will be reported.

Following standard methodology, groups of matched grass-fed beef cattle from farms across Pembrokeshire will be treated with different wormers (Strong et al., 1996). Dung will be collected from each group of cattle prior to treatment and at standard intervals after treatment to enable toxicity levels over time and dung decomposition rates to be assessed (Floate et al., 2002). At the study site, artificial dung pats will be formed from each treatment group at each time interval after worming and randomly distributed in a grid and collected in at standard time intervals after pat preparation (Lee & Wall, 2006a; Strong et al., 1996). Adult stages of Coleoptera, Diptera and Hymenoptera will be identified to species. Immatures and other invertebrate groups will be sorted to the family level (morpho-species where possible), before everything is counted. Taxonomic assistance has been agreed with D.J. Mann (Oxford University Museum of Natural History). Pats will also be assessed for decomposer activity and success of matter breakdown by measuring water content, ash-free organic matter content and dry weight during the trial (Lee & Wall, 2006a). Standard dung-baited pitfall trapping (Newton & Peck, 1975) will be carried out at the study site using dung from each treatment group in order to assess dung attractiveness, and adult Scarabaeidae will be sorted to the species level and counted. Species richness, diversity, beta diversity and abundance distributions will be calculated.

In order to assess the function of species that may be differentially affected by anthelmintics, standardised insect exclusion experiments (Lee & Wall, 2006a) will be used. This enables the effect of exclusion of the early insect colonisers on the subsequent patterns of colonisation and degradation of cattle dung pats in the field to be considered. It will be possible to determine the impact of various key species in simplified communities on the rates of decomposition. It is feasible that dung decomposition is unaffected by an impoverished dung decomposer community, provided that keystone species, such as Aphodius species, are present, the loss of which may greatly retard decomposition rate (Slade et al., 2007). In addition, the standard laboratory test for toxicity, developed by the Dung Organism Toxicity Testing Standardisation (DOTTS) will be performed for each treatment, using the standard test organisms. Brood and beetle counts, brood emergence, brood survival and juvenile development time will all be assessed. Facilities have been arranged with Huntingdon Life Sciences allowing the comparison of laboratory and field studies. Pasture herbage, soil aeration and soil nitrogen incorporation will be tested with each treatment using standard field and greenhouse methodology (Bang et al., 2005).

Project advisors and contributors

Dr Owen Lewis (University of Oxford, Ecology Research Group) has agreed to supervise the project. This study will fit in well with the Group's interests of insect community processes and interactions. Dr Owen Lewis is currently supervising a PhD student studying dung beetle ecosystem functioning. There is great taxonomic expertise in Oxford: agreed taxonomic advisor D. J. Mann (OUMNH) is the dung beetle National Recorder, and a key worker in the field. As a resident of Pembrokeshire, and having worked closely with farmers in the county, access to cattle groups will provide no difficulties. Ten farmers have agreed to hold on-farm trials. Further details are available on request. The following have agreed to assist with the project: Earth Science Partnership Ltd. (advice), Paddocks Farm Ltd (supplying Verm-X natural wormer and advice), Professor Richard Field (Nottingham University) and Professor Richard Wall (University of Bristol), Dr Leeann Reaney (Queen Mary, University of London), Jean-Pierre Lumaret (Universite Paul Valery-Montpellier 3), Dr Keith Wardhaugh (DOTTS), Huntingdon Life Sciences (laboratory space, equipment and assistance), Dr Rob Davies WWBIC (mapping software and advice), Dr Ann Humble (Tir Gofal National Co-ordinator), Farming and Wildlife Advisory Group FWAG, The Soil Association and Organic Centre Wales. William Scale (2006 Nuffield Scholar), Roger Mathias (agri-environment award winner), The Grazing Animals Project, The Welsh Black Cattle Society and Welsh Black Cattle Society Organic Club, Fenton Veterinary Practice.

References

Bang, H.S., Lee, J.H., Kwon, O.S., Na, Y.E., Jang, Y.S. & Kim, W.H. (2005) Effects of paracoprid dung beetles (Coleoptera: Scarabaeidae) on the growth of pasture herbage and on the underlying soil. Applied Soil Ecology 29(2), 165-171.

Bornemissza, G. F. (1976) The Australian Dung Beetle Project, 1965-1975. Aust Meat Res Comm. Rev 30,1-30.

Chamberlain, D.E., Fuller, R.J., Bunce, R.G.H., Duckworth, J.C. & Shrubb, M. (2000) Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. Journal of Applied Ecology 37(5), 771-788.

Fincher, G.T. (1981) The potential value of dung beetles in pasture ecosystems. Journal of the Georgia Entomological Society 16, 301-316.

Fisher, M.H. & Mrozik, H. (1992) The chemistry and pharmacology of avermectins. Annual Review of Pharmacological Toxicology 32, 537-553.

Floate, K.D. (1998) Off-target effects of ivermectin on insects and on dung degradation in southern Alberta, Canada. Bulletin of Entomological Research 88, 25-35.

Floate, K.D., & Fox, A.S. (1999) Indirect affects of ivermectin residues across trophic levels: Musca domestica (Diptera: Muscidae) and Muscidifurax zaraptor (Hymenoptera: Pteromalidae). Bulletin of Entomological Research 89, 225-229.

Floate, K.D., Wardhaugh, K.G., Boxall, A.B.A., Sherratt, T.N. (2005). Fecal residues of veterinary parasiticides: nontarget effects in the pasture environment. Annual Review of Entomology, 50, 153-179.

Holter, P. (1979) Effect of dung beetles (Aphodius Spp.) and earthworms on the disappearance of cattle dung. Oikos 32, 393-402.

Jones, G. (1990) Prey selection by the greater horseshoe bat (Rhinolophus ferrumequinum): optimal foraging by echolocation? Journal of Animal Ecology 59, 587-602.

Lee, C.M. & Wall, R. (2006a) Cow-dung colonization and decomposition following insect exclusion. Bulletin of Entomological Research 96, 315-322.

Lee, C.M. & Wall, R. (2006b) Distribution and abundance of insects colonizing cattle dung. Journal of Natural History 40, 1167-1177.

Losey, J.E. & Vaughan, M. (2006) The economic value of ecological services provided by insects. Bioscience 56(4), 311-323.

Lumaret, J.P. & N. Kadiri (1995) The influence of the first wave of colonizing insects on cattle dung dispersal. Pedobiologia 39, 506-517.

Newton, A. & Peck, S.B. (1975) Baited pitfall traps for beetles. The Coleopterist's Bulletin 29 (1), 45-46.

Slade, E.M., Mann, D.J., Villanueva, J.F. & Lewis, O.T (2007) Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. Journal of Animal Ecology 76, 1094-1104.

Strong, L., Wall, R., Woolford, A. & Djeddour, D. (1996) The effect of faecally excreted ivermectin and fenbendazole on the insect colonisation of cattle dung following the oral administration of sustained-release boluses . Veterinary Parasitology 62, 253-266.

Stevenson, B.G. & D.L. Dindal (1987) Insect effects on decomposition of cow dung in microcosms. Pedobiologia 30, 81-92.

Woodcock, B.A., Potts, S.G., Pilgrim, E., Ramsay, A.J., Tscheulin, T., Parkinson, A., Smith, R.E.N., Gundrey, A.L., Brown, V.K. & Tallowin, J.R. (2007) The potential of grass field margin management for enhancing beetle diversity in intensive livestock farms. Journal of Applied Ecology 44 (1), 60-69.

Xu, M., Molento M., Blackhall, W., Ribeiro, P., Beech, R. & Prichard, R. (1998) Ivermectin resistance in nematodes may be caused by alteration of P-glycoprotein homolog. Molecular and Biochemical Parasitology 91(2), 327-335.

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