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RESEARCH ARTICLE
Contents Vol 45(6)

Effects of ivermectin on soil nutrient cycling, plant biomass, and dung beetle abundance

Shiva Torabian https://orcid.org/0000-0001-8235-8847 A * , A. Joshua Leffler A and Lora Perkins A
+ Author Affiliations
- Author Affiliations

A Department of Natural Resource Management, South Dakota State University, Brookings, SD, USA.

* Correspondence to: shiva_torabian@yahoo.com

The Rangeland Journal 45(6) 224-234 https://doi.org/10.1071/RJ24009
Submitted: 20 March 2024  Accepted: 22 May 2024  Published: 6 June 2024

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the Australian Rangeland Society.

Abstract

Ivermectin, a commonly used parasiticide, is known to affect dung beetle abundance when present in cattle dung. In this experimental study, we explicitly manipulated ivermectin concentrations in dung pats to examine its effects on dung beetle abundance, soil properties, and plant growth throughout the growing seasons of spring and summer in a western South Dakota grassland. Dung pats containing zero, low (2 mg/kg), and high (10 mg/kg) concentrations of ivermectin were strategically placed in the grassland in summer 2019 and spring 2021. Over a period of 63 days, we monitored changes in the nitrogen content of dung, soil, plants, as well as the abundance of dung beetles, and plant biomass. Our findings indicated that beetle abundance was 50% greater in dung pats without ivermectin, especially when the dung was fresh. However, ivermectin concentrations did not significantly alter the nitrogen content in dung and plants across both seasons, nor was there a discernible effect on plant biomass, despite the pronounced impact on dung beetle abundance.

Keywords: dung, Grassland, inorganic nitrogen, inorganic phosphorus, parasiticide, plant growth.

References

Adler N, Bachmann J, Blanckenhorn WU, Floate KD, Jensen J, Römbke J (2016) Effects of ivermectin application on the diversity and function of dung and soil fauna: regulatory and scientific background information. Environmental Toxicology and Chemistry 35(8), 1914-1923.
| Crossref | Google Scholar | PubMed |

Ajiboye B, Akinremi OO, Racz GJ (2004) Laboratory characterization of phosphorus in fresh and oven‐dried organic amendments. Journal of Environmental Quality 33(3), 1062-1069.
| Crossref | Google Scholar | PubMed |

Bang HS, Lee JH, Kwon OS, Na YE, Jang YS, Kim WH (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.
| Crossref | Google Scholar |

Baykov AA, Evtushenko OA, Avaeva SM (1988) A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Analytical Biochemistry 171(2), 266-270.
| Crossref | Google Scholar | PubMed |

Bicknell JE, Phelps SP, Davies RG, Mann DJ, Struebig MJ, Davies ZG (2014) Dung beetles as indicators for rapid impact assessments: evaluating best practice forestry in the neotropics. Ecological Indicators 43, 154-161.
| Crossref | Google Scholar |

Bishop TR, Robertson MP, Van Rensburg BJ, Parr CL (2017) Coping with the cold: minimum temperatures and thermal tolerances dominate the ecology of mountain ants. Ecological Entomology 42(2), 105-114.
| Crossref | Google Scholar |

Bloor JM (2015) Additive effects of dung amendment and plant species identity on soil processes and soil inorganic nitrogen in grass monocultures. Plant and Soil 396, 189-200.
| Crossref | Google Scholar |

Bornemissza GF, Williams CH (1970) An effect of dung beetle activity on plant yield. Pedobiologia 10, 1-7.
| Crossref | Google Scholar |

Brown J, Scholtz CH, Janeau JL, Grellier S, Podwojewski P (2010) Dung beetles (Coleoptera: Scarabaeidae) can improve soil hydrological properties. Applied Soil Ecology 46(1), 9-16.
| Crossref | Google Scholar |

Campbell WC, Fisher MH, Stapley EO, Albers-Schönberg G, Jacob TA (1983) Ivermectin: a potent new antiparasitic agent. Science 221(4613), 823-828.
| Crossref | Google Scholar | PubMed |

Carter MR, Gregorich EG (Eds) (2007) ‘Soil sampling and methods of analysis.’ (CRC Press)

Cerkvenik V, Doganoc DZ, Skubic V, Beek WM, Keukens HJ (2001) Thermal and long-term freezing stability of ivermectin residues in sheep milk. European Food Research and Technology 213, 72-76.
| Crossref | Google Scholar |

Choate PM (1999) Introduction to the identification of beetles (Coleoptera). In ‘Dichotomous keys to some families of Florida Coleoptera’. pp. 23–33. Available at http://entnemdept.ufl.edu/choate/beetles.pdf.

Correa CM, Braga RF, Louzada J, Menéndez R (2019) Dung beetle diversity and functions suggest no major impacts of cattle grazing in the Brazilian Pantanal wetlands. Ecological Entomology 44(4), 524-533.
| Crossref | Google Scholar |

Correa CM, Ferreira KR, Abot AR, Louzada J, Vaz‐de‐Mello FZ (2022) Ivermectin impacts on dung beetle diversity and their ecological functions in two distinct Brazilian ecosystems. Ecological Entomology 47(5), 736-748.
| Crossref | Google Scholar |

Costa C, Oliveira VHF, Maciel R, Beiroz W, Korasaki V, Louzada J (2017) Variegated tropical landscapes conserve diverse dung beetle communities. PeerJ 5, e3125.
| Crossref | Google Scholar | PubMed |

deCastro‐Arrazola I, Andrew NR, Berg MP, Curtsdotter A, Lumaret JP, Menéndez R, et al. (2023) A trait‐based framework for dung beetle functional ecology. Journal of Animal Ecology 92(1), 44-65.
| Crossref | Google Scholar | PubMed |

Delgado JA (2002) Quantifying the loss mechanisms of nitrogen. Journal of Soil and Water Conservation 57(6), 389-398.
| Google Scholar |

Doube BM (2018) Ecosystem services provided by dung beetles in Australia. Basic and Applied Ecology 26, 35-49.
| Crossref | Google Scholar |

Du Z, Wang X, Xiang J, Wu Y, Zhang B, Yan Y, et al. (2021) Yak dung pat fragmentation affects its carbon and nitrogen leaching in northern Tibet, China. Agriculture, Ecosystems & Environment 310, 107301.
| Crossref | Google Scholar |

Evans KS, Mamo M, Wingeyer A, Schacht WH, Eskridge KM, Bradshaw J, Ginting D (2019) Soil fauna accelerate dung pat decomposition and nutrient cycling into grassland soil. Rangeland Ecology & Management 72(4), 667-677.
| Crossref | Google Scholar |

Ghasemi A, Zahediasl S (2012) Normality tests for statistical analysis: a guide for non-statisticians. International Journal of Endocrinology and Metabolism 10(2), 486-489.
| Crossref | Google Scholar | PubMed |

Gotcha N, Machekano H, Cuthbert RN, Nyamukondiwa C (2021) Low‐temperature tolerance in coprophagic beetle species (Coleoptera: Scarabaeidae): implications for ecological services. Ecological Entomology 46(5), 1101-1112.
| Crossref | Google Scholar |

Holter P (2004) Dung feeding in hydrophilid, geotrupid and scarabaeid beetles: examples of parallel evolution. European Journal of Entomology 101(3), 365-372.
| Crossref | Google Scholar |

Holter P, Scholtz CH (2007) What do dung beetles eat? Ecological Entomology 32(6), 690-697.
| Crossref | Google Scholar |

Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S, Hothorn MT (2016) ‘Package ‘multcomp’. Simultaneous inference in general parametric models.’ (Project for Statistical Computing: Vienna, Austria)

Iglesias LE, Saumell CA, Fernández AS, Fusé LA, Lifschitz AL, Rodríguez EM, et al. (2006) Environmental impact of ivermectin excreted by cattle treated in autumn on dung fauna and degradation of faeces on pasture. Parasitology Research 100, 93-102.
| Crossref | Google Scholar | PubMed |

Iglesias LE, Fusé LA, Lifschitz AL, Rodríguez EM, Sagüés MF, Saumell CA (2011) Environmental monitoring of ivermectin excreted in spring climatic conditions by treated cattle on dung fauna and degradation of faeces on pasture. Parasitology Research 108, 1185-1191.
| Crossref | Google Scholar | PubMed |

Jensen J, Scott-Fordsmand JJ (2012) Ecotoxicity of the veterinary pharmaceutical ivermectin tested in a soil multi-species (SMS) system. Environmental Pollution 171, 133-139.
| Crossref | Google Scholar | PubMed |

Kabir SMH, Howlader AJ, Begum J (1985) Effect of dung beetle activities on the growth and yield of wheat plants. Bangladesh Journal of Agriculture 10, 49-55.
| Google Scholar |

Keeney DR, Nelson DW (1982) Nitrogen—inorganic forms. In ‘Methods of soil analysis: Part 2 chemical and microbiological properties. Vol. 9’. (Eds AL Page, RH Miller, DR Keeney​) pp. 643 – 693. (American Society of Agronomy: Madison, WI, USA)

Lenth R, Singmann H, Love J, Buerkner P, Herve (2019) Package ‘lsmeans’. The American Statistician 34(4), 216-221.
| Google Scholar |

Liu J, Veith TL, Collick AS, Kleinman PJA, Beegle DB, Bryant RB (2017) Seasonal manure application timing and storage effects on field‐and watershed‐level phosphorus losses. Journal of Environmental Quality 46(6), 1403-1412.
| Crossref | Google Scholar | PubMed |

Lovell RD, Jarvis SC (1996) Effect of cattle dung on soil microbial biomass C and N in a permanent pasture soil. Soil Biology and Biochemistry 28(3), 291-299.
| Crossref | Google Scholar |

Lumaret JP, Galante E, Lumbreras 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(3), 428-436.
| Crossref | Google Scholar |

Luo Y, & Zhou X (2006) Chapter 2: Importance and roles of soil respiration. In ‘Soil Respiration and the Environment’. pp. 17–32. (Academic Press, Elsevier: San Diego, CA, USA)

Macqueen A, Beirne BP (1975) Effects of cattle dung and dung beetle activity on growth of beardless wheatgrass in British Columbia. Canadian Journal of Plant Science 55(4), 961-967.
| Crossref | Google Scholar |

Maldaner ME, Sobral-Souza T, Prasniewski VM, Vaz-de-Mello FZ (2021) Effects of climate change on the distribution of key native dung beetles in South American grasslands. Agronomy 11(10), 2033.
| Crossref | Google Scholar |

Maldonado MB, Aranibar JN, Serrano AM, Chacoff NP, Vázquez DP (2019) Dung beetles and nutrient cycling in a dryland environment. Catena 179, 66-73.
| Crossref | Google Scholar |

Manning P, Slade EM, Beynon SA, Lewis OT (2016) Functionally rich dung beetle assemblages are required to provide multiple ecosystem services. Agriculture, Ecosystems & Environment 218, 87-94.
| Crossref | Google Scholar |

Menéndez R, Webb P, Orwin KH (2016) Complementarity of dung beetle species with different functional behaviours influence dung–soil carbon cycling. Soil Biology and Biochemistry 92, 142-148.
| Crossref | Google Scholar |

Miranda KM, Paolocci N, Katori T, Thomas DD, Ford E, Bartberger MD, et al. (2003) A biochemical rationale for the discrete behavior of nitroxyl and nitric oxide in the cardiovascular system. Proceedings of the National Academy of Sciences 100(16), 9196-9201.
| Crossref | Google Scholar | PubMed |

Morugán-Coronado A, García-Orenes F, McMillan M, Pereg L (2019) The effect of moisture on soil microbial properties and nitrogen cyclers in Mediterranean sweet orange orchards under organic and inorganic fertilization. Science of The Total Environment 655, 158-167.
| Crossref | Google Scholar | PubMed |

Nervo B, Caprio E, Celi L, Lonati M, Lombardi G, Falsone G, et al. (2017) Ecological functions provided by dung beetles are interlinked across space and time: evidence from 15N isotope tracing. Ecology 98(2), 433-446.
| Crossref | Google Scholar | PubMed |

Newman A (1996) Review of Methods in Applied Soil Microbiology and Biochemistry. Biological Agriculture and Horticulture 13(3), 304-305.
| Google Scholar |

Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME, Network TSR (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation 141(6), 1461-1474.
| Crossref | Google Scholar |

Õmura S (2008) Ivermectin: 25 years and still going strong. International Journal of Antimicrobial Agents 31(2), 91-98.
| Crossref | Google Scholar | PubMed |

Õmura S, Crump A (2004) The life and times of ivermectin — a success story. Nature Reviews Microbiology 2(12), 984-989.
| Crossref | Google Scholar | PubMed |

Otronen M, Hanski I (1983) Movement patterns in Sphaeridium: differences between species, sexes, and feeding and breeding individuals. The Journal of Animal Ecology 52, 663-680.
| Crossref | Google Scholar |

Pegan SD, Tian Y, Sershon V, Mesecar AD (2010) A universal, fully automated high throughput screening assay for pyrophosphate and phosphate release from enzymatic reactions. Combinatorial Chemistry & High Throughput Screening 13(1), 27-38.
| Crossref | Google Scholar | PubMed |

Penttilä A, Slade EM, Simojoki A, Riutta T, Minkkinen K, Roslin T (2013) Quantifying beetle-mediated effects on gas fluxes from dung pats. PLoS One 8(8), e71454.
| Crossref | Google Scholar | PubMed |

Peterson RA (2021) Finding Optimal Normalizing Transformations via bestNormalize. R Journal 13(1), 310-329.
| Crossref | Google Scholar |

Peterson RA, Cavanaugh JE (2020) Ordered quantile normalization: a semiparametric transformation built for the cross-validation era. Journal of Applied Statistics 47, 2312-2327.
| Crossref | Google Scholar | PubMed |

Ridout M, Demétrio CG, Hinde J (1998) Models for count data with many zeros. In ‘Proceedings of the XIXth international biometric conference. Vol. 19’. pp. 179–192. (International Biometric Society Invited Papers: Cape Town, South Africa)

Ripley B, Venables B, Bates DM, Hornik K, Gebhardt A, Firth D, Ripley MB (2013) Package ‘mass’. Cran r 538, 113-120.
| Google Scholar |

Römbke J, Coors A, Fernández ÁA, Förster B, Fernández C, Jensen J, et al. (2010) Effects of the parasiticide ivermectin on the structure and function of dung and soil invertebrate communities in the field (Madrid, Spain). Applied Soil Ecology 45(3), 284-292.
| Crossref | Google Scholar |

Römbke J, Scheffczyk A, Lumaret J-P, Tixier T, Blanckenhorn W, Lahr J, Floate K (2017) Comparison of dung and soil fauna from pastures treated with and without ivermectin as an example of the effects of a veterinary pharmaceutical ((UBA-FB) 002155/E). Umweltbundesamt. Available at https://www.umweltbundesamt.de/en/publikationen/comparison-of-dung-soil-fauna-from-pastures-treated

Rouphael Y, Cardarelli M, Schwarz D, Franken P, Colla G (2012) Effects of drought on nutrient uptake and assimilation in vegetable crops. In ‘Plant responses to drought stress: from morphological to molecular features’. pp. 171–195. (Springer)

Sands B, Wall R (2017) Dung beetles reduce livestock gastrointestinal parasite availability on pasture. Journal of Applied Ecology 54(4), 1180-1189.
| Crossref | Google Scholar |

Schick BD, Guretzky JA, Schacht WH, Mamo M (2019) Dietary nutritive value, dung quality, decomposition, and nutrient movement into soil in smooth bromegrass pastures. Crop Science 59(3), 1294-1308.
| Crossref | Google Scholar |

Slade EM, Roslin T, Santalahti M, Bell T (2016) Disentangling the ‘brown world’ faecal–detritus interaction web: dung beetle effects on soil microbial properties. Oikos 125(5), 629-635.
| Crossref | Google Scholar |

Stark JM, Firestone MK (1995) Mechanisms for soil moisture effects on activity of nitrifying bacteria. Applied and Environmental Microbiology 61(1), 218-221.
| Crossref | Google Scholar | PubMed |

Tixier T, Blanckenhorn WU, Lahr J, Floate K, Scheffczyk A, Düring RA, et al. (2016) A four‐country ring test of nontarget effects of ivermectin residues on the function of coprophilous communities of arthropods in breaking down livestock dung. Environmental Toxicology and Chemistry 35(8), 1953-1958.
| Crossref | Google Scholar | PubMed |

Torabian S, Leffler AJ, Perkins L (2024) Importance of restoration of dung beetles in the maintenance of ecosystem services. Ecological Solutions and Evidence 5(1), e12297.
| Crossref | Google Scholar |

Ulrich-Schad JD, Li S, Leffler AJ, Gu W, Schoon L, Perkins L (2021) What and why: South Dakota rangeland livestock producers’ usage of parasiticides. Rangeland Ecology & Management 79, 190-200.
| Crossref | Google Scholar |

Vadas PA, Good LW, Jokela WE, Karthikeyan KG, Arriaga FJ, Stock M (2017) Quantifying the impact of seasonal and short‐term manure application decisions on phosphorus loss in surface runoff. Journal of Environmental Quality 46(6), 1395-1402.
| Crossref | Google Scholar | PubMed |

Verdú JR, Lobo JM, Sánchez-Piñero F, Gallego B, Numa C, Lumaret JP, et al. (2018) Ivermectin residues disrupt dung beetle diversity, soil properties and ecosystem functioning: an interdisciplinary field study. Science of The Total Environment 618, 219-228.
| Crossref | Google Scholar | PubMed |

Wachendorf C, Taube F, Wachendorf M (2005) Nitrogen leaching from 15N labelled cow urine and dung applied to grassland on a sandy soil. Nutrient Cycling in Agroecosystems 73, 89-100.
| Crossref | Google Scholar |

Wardhaugh KG, Rodriguez‐Menendez H (1988) The effects of the antiparasitic drug, ivermectin, on the development and survival of the dung‐breeding fly, Orthelia cornicina (F.) and the scarabaeine dung beetles, Copris hispanus L., Bubas bubalus (Oliver) and Onitis belial F. Journal of Applied Entomology 106(1–5), 381-389.
| Crossref | Google Scholar |

Yamada D, Imura O, Shi K, Shibuya T (2007) Effect of tunneler dung beetles on cattle dung decomposition, soil nutrients and herbage growth. Grassland Science 53(2), 121-129.
| Crossref | Google Scholar |

Yoshihara Y, Sato S (2015) The relationship between dung beetle species richness and ecosystem functioning. Applied Soil Ecology 88, 21-25.
| Crossref | Google Scholar |