Analyze Diet
Integrative zoology2021; 17(1); 128-138; doi: 10.1111/1749-4877.12578

Analysis on the relationship between winter precipitation and the annual variation of horse stomach fly community in arid desert steppe, Northwest China (2007-2019).

Abstract: Gasterophilus spp. have been found to be widespread in reintroduced Przewalski's horses in the Kalamaili Nature Reserve (Northwest China). However, data on the annual variation in Gasterophilus infections are lacking. To analyze the epidemiological features and determine the cause of the annual variation in Gasterophilus infections, we treated 110 Przewalski's horses with ivermectin and collected Gasterophilus larvae from fecal samples each winter from 2007 to 2019. All 110 Przewalski's horses studied were found to be infected by Gasterophilus spp., and a total of 141 379 larvae were collected. Six species of Gasterophilus were identified with the following prevalence: G. pecorum (100%), G. nasalis (96.36%), G. nigricornis (94.55%), G. haemorrhoidalis (56.36%), G. intestinalis (59.09%), and G. inermis (3.64%). The mean infection intensity of Gasterophilus spp. larvae in Przewalski's horses was 1285 ± 653. G. pecorum (92.96% ± 6.71%) was the most abundant species. The intensity of Gasterophilus spp. (r = -0.561, P < 0.046) was significantly correlated with winter precipitation. Our findings confirmed that, in the Kalamaili Nature Reserve, gasterophilosis is a severe parasitic disease in Przewalski's horses. Winter precipitation at the beginning of the year can indirectly affect the intensity and composition of Gasterophilus spp. in Przewalski's horses at the end of the year. Therefore, the water-related ecological regulation should be carried out to help reduce the parasite infection of Przewalski's horses.
Publication Date: 2021-08-10 PubMed ID: 34254452PubMed Central: PMC9291967DOI: 10.1111/1749-4877.12578Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article investigates the impact of winter precipitation on the variation of Gasterophilus spp. infections in Przewalski’s horses in Northwest China. The study found that the intensity of the parasite infection is significantly associated with winter precipitation, suggesting a need for water-related ecological regulation to reduce the infection rate.

Introduction

  • This research was conducted on the relationship between winter precipitation and the annual variation of Gasterophilus spp. infections in Przewalski’s horses in the Kalamaili Nature Reserve in Northwest China. The study spans over a period of twelve years from 2007 to 2019.
  • The area was selected due to the widespread prevalence of Gasterophilus spp. in the horses, but there was a lack of data available on annual variation of these infections. The researchers aim to analyze correlations between infection rates and environmental conditions to better understand the epidemiological features of the parasite and to reveal potential means for prevention.

Methodology

  • 110 Przewalski’s horses were treated with ivermectin, a medication used to treat many types of parasite infestations. Gasterophilus larvae were then collected from fecal samples each winter over the twelve-year period.
  • These horses were found to be infected by Gasterophilus spp. with a total of 141,379 larvae collected. Six species of Gasterophilus were identified, and their prevalence and intensity of infection were recorded.

Results

  • All horses were found to be infected by Gasterophilus spp., suggesting a high prevalence of this parasite in the environment. Moreover, six species of Gasterophilus were identified, with G. pecorum having the highest prevalence (100%) and G. inermis having the lowest (3.64%).
  • The mean infection intensity was 1285 ± 653 for Gasterophilus spp., with G. pecorum being the most abundant species.

Correlation with Winter Precipitation

  • The intensity of Gasterophilus spp. was significantly correlated with winter precipitation. In other words, years with increased winter precipitation saw a lower intensity of Gasterophilus spp. infections in Przewalski’s horses.
  • This finding suggests that water-related ecological regulation could help reduce the parasite infection of horses.

Conclusion

  • According to the study, gasterophilosis is a severe parasitic disease in Przewalski’s horses at the Kalamaili Nature Reserve. Winter precipitation at the beginning of the year can indirectly affect the intensity and composition of Gasterophilus spp. in these horses by year’s end.
  • The direct implication of this finding is that adjusting water-related ecological regulations such as managing precipitation or irrigation could potentially help mitigate parasite infection in Przewalski’s horses. These findings could be used to guide future conservation efforts for these animals, particularly in regions where they are reintroduced.

Cite This Article

APA
Huang H, Zhang K, Zhang B, Liu S, Chu H, Qi Y, Zhang D, Li K. (2021). Analysis on the relationship between winter precipitation and the annual variation of horse stomach fly community in arid desert steppe, Northwest China (2007-2019). Integr Zool, 17(1), 128-138. https://doi.org/10.1111/1749-4877.12578

Publication

ISSN: 1749-4877
NlmUniqueID: 101492420
Country: Australia
Language: English
Volume: 17
Issue: 1
Pages: 128-138

Researcher Affiliations

Huang, Heqing
  • Key Laboratory of Non-Invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
  • Chongqing Academy of Environmental Science, Chongqing, China.
Zhang, Ke
  • Key Laboratory of Non-Invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Zhang, Boru
  • Qinhuangdao Forestry Bureau, Qinhuangdao, China.
Liu, Shanhui
  • Office of Educational Administration, Beijing Language and Culture University, Beijing, China.
Chu, Hongjun
  • Institute of Forest Ecology, Xinjiang Academy of Forestry, Urumqi, China.
Qi, Yingjie
  • Mt. Kalamaili Ungulate Nature Reserve, Changji, Xinjiang, China.
Zhang, Dong
  • Key Laboratory of Non-Invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Li, Kai
  • Key Laboratory of Non-Invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.

MeSH Terms

  • Animals
  • Desert Climate
  • Diptera / pathogenicity
  • Horse Diseases / parasitology
  • Horses
  • Larva
  • Seasons
  • Stomach

Grant Funding

  • 31670538 / National Science Foundation of China
  • 30870463 / National Science Foundation of China
  • 2018123 / Project of Department for Wildlife and Forest Plants Protection, SFA of China

Conflict of Interest Statement

The authors declare no conflicts of interests.

References

This article includes 39 references
  1. Agneessens J, Engelen S, Debever P, Vercruysse J. Gasterophilus intestinalis infections in horses in Belgium.. Vet Parasitol 1998 Jun 15;77(2-3):199-204.
    pubmed: 9746291doi: 10.1016/s0304-4017(98)00106-xgoogle scholar: lookup
  2. Bechtel MJ, Teglas MB, Murphy PJ, Matocq MD. Parasite prevalence and community diversity in sympatric and allopatric populations of two woodrat species (Sigmodontinae: Neotoma) in central California.. J Wildl Dis 2015 Apr;51(2):419-30.
    pubmed: 25574805doi: 10.7589/2014-04-099google scholar: lookup
  3. Bello TR. Alternative antiparasitic treatment of horses with pyrantel pamoate suspension and ivermectin oral solution compared with horses treated only with ivermectin oral solution. Journal of Equine Veterinary Science 16, 106–10.
  4. CHERESHNEV NA. [Biologic properties of the gadfly Gastrophilus pecorum Fabr. (Diptera, Gastrophillidae)].. Dokl Akad Nauk SSSR 1951 Apr;77(4):765-8.
    pubmed: 14822865
  5. nCIMISS. Monthly precipitation database. .
  6. Costa AJ, Barbosa OF, Moraes FR, Acuña AH, Rocha UF, Soares VE, Paullilo AC, Sanches A. Comparative efficacy evaluation of moxidectin gel and ivermectin paste against internal parasites of equines in Brazil.. Vet Parasitol 1998 Dec 15;80(1):29-36.
    pubmed: 9877068doi: 10.1016/s0304-4017(98)00186-1google scholar: lookup
  7. Dawson K. A non-lethal method for assessment of efficacy of antiparasitics against parasites in horses such as Anoplocephala perfoliata and Gasterophilus intestinalis.. Vet Parasitol 2003 Jul 10;115(1):67-70.
    pubmed: 12860069doi: 10.1016/s0304-4017(03)00161-4google scholar: lookup
  8. Frank SA. EVOLUTION OF HOST-PARASITE DIVERSITY.. Evolution 1993 Dec;47(6):1721-1732.
  9. Getachew AM, Innocent G, Trawford AF, Reid SW, Love S. Gasterophilosis: a major cause of rectal prolapse in working donkeys in Ethiopia.. Trop Anim Health Prod 2012 Apr;44(4):757-62.
    pubmed: 21870062doi: 10.1007/s11250-011-9961-7google scholar: lookup
  10. Huang H, Zhang B, Chu H, Zhang D, Li K. Gasterophilus (Diptera, Gasterophilidae) infestation of equids in the Kalamaili Nature Reserve, China.. Parasite 2016;23:36.
    pmc: PMC5018932pubmed: 27593434doi: 10.1051/parasite/2016036google scholar: lookup
  11. Huang HQ, Zhang D, Li K. Distribution of Gasterophilus (Diptera: Gasterophilidae) myiasis foci in arid desert steppe: A case study of Kalamaili Mountain Ungulate Nature Reserve. Scientia Silvae Sinicae 53, 142–9.
  12. Ibrayev B, Lider L, Bauer C. Gasterophilus spp. infections in horses from northern and central Kazakhstan.. Vet Parasitol 2015 Jan 15;207(1-2):94-8.
    pubmed: 25522954doi: 10.1016/j.vetpar.2014.11.015google scholar: lookup
  13. Kaczensky P, Ganbaatar O, Wehrden HV, Walzer C. Resource selection by sympatric wild equids in the Mongolian Gobi. Journal Applied Ecology 45, 1762–9.
  14. Krecek RC, Reinecke RK, Horak IG. Internal parasites of horses on mixed grassveld and bushveld in Transvaal, Republic of South Africa.. Vet Parasitol 1989 Nov;34(1-2):135-43.
    pubmed: 2588465doi: 10.1016/0304-4017(89)90173-8google scholar: lookup
  15. Li XY, Chen YO, Wang QK, Li K, Pape T, Zhang D. Molecular and morphological characterization of third instar Palaearctic horse stomach bot fly larvae (Oestridae: Gasterophilinae, Gasterophilus).. Vet Parasitol 2018 Oct 15;262:56-74.
    pubmed: 30389013doi: 10.1016/j.vetpar.2018.09.011google scholar: lookup
  16. Liu SH, Hu DF, Li K. Oviposition site selection by Gasterophilus pecorum (Diptera: Gasterophilidae) in its habitat in Kalamaili Nature Reserve, Xinjiang, China.. Parasite 2015;22:34.
    pmc: PMC4664853pubmed: 26621549doi: 10.1051/parasite/2015034google scholar: lookup
  17. Liu SH, Li K, Hu DF. The incidence and species composition of Gasterophilus (Diptera, Gasterophilidae) causing equine myiasis in northern Xinjiang, China.. Vet Parasitol 2016 Feb 15;217:36-8.
    pubmed: 26827858doi: 10.1016/j.vetpar.2015.12.028google scholar: lookup
  18. Lugauer B. Differences of movement pattern between Asiatic wild ass (Equus hemionus) and Przewalski's horse (Equus ferus przewalskii) (M.S. thesis). University of Vienna, Vienna, pp. 15–6.
  19. Margolis L, Schad GA. The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68, 131–3.
  20. Mohr E. The Asiatic Wild Horse, 2nd edn. J.A. Allen & Co. Ltd, London.
  21. Moller AP. Parasitism and the regulation of host populations. In: Thomas F, Renaud F, Guégan J, eds. Parasitism and Ecosystems. Oxford University Press, Oxford, pp. 43–53.
  22. Otranto D, Milillo P, Capelli G, Colwell DD. Species composition of Gasterophilus spp. (Diptera, Oestridae) causing equine gastric myiasis in southern Italy: parasite biodiversity and risks for extinction.. Vet Parasitol 2005 Oct 10;133(1):111-8.
    pubmed: 15978726doi: 10.1016/j.vetpar.2005.05.015google scholar: lookup
  23. Özdal N, Bicek K, Orung O, Deger S. Presence of Gasterophilus species in horses in Van region. Yüzüncü yıl Üniversitesi Veteriner Fakültesi Dergisi 21, 87–90.
  24. Pandey VS, Ouhelli H, Verhulst A. Epidemiological observations on Gasterophilus intestinalis and G. nasalis in donkeys from Morocco.. Vet Parasitol 1992 Mar;41(3-4):285-92.
    pubmed: 1502790doi: 10.1016/0304-4017(92)90087-pgoogle scholar: lookup
  25. Pickles RS, Thornton D, Feldman R, Marques A, Murray DL. Predicting shifts in parasite distribution with climate change: a multitrophic level approach.. Glob Chang Biol 2013 Sep;19(9):2645-54.
    pubmed: 23666800doi: 10.1111/gcb.12255google scholar: lookup
  26. Pielou ECJ. The measurement of diversity in different types of biological collections. Journal of Theoretical Biology 13, 131–44.
  27. Pilo C, Altea A, Scala A. Gasterophilosis in horses in Sardinia (Italy): effect of meteorological variables on adult egg-laying activity and presence of larvae in the digestive tract, and update of species.. Parasitol Res 2015 May;114(5):1693-702.
    pubmed: 25663068doi: 10.1007/s00436-015-4352-zgoogle scholar: lookup
  28. Scheibe KM, Eichhorn K, Kalz B, Streich WJ, Scheibe A. Water consumption and watering behavior of Przewalski horses (Equus ferus przewalskii) in a semireserve. Zoo Biology 17, 181–92.
  29. Sequeira JL, Tostes RA, Oliveira-Sequeira TC. Prevalence and macro- and microscopic lesions produced by Gasterophilus nasalis (Diptera: Oestridae) in the Botucatu Region, SP, Brazil.. Vet Parasitol 2001 Dec 13;102(3):261-6.
    pubmed: 11777606doi: 10.1016/s0304-4017(01)00536-2google scholar: lookup
  30. Shannon CE. A mathematical theory of communication. Bell System Technical Journal 27, 623–56.
  31. Studzińska MB, Wojcieszak K. Gasterophilus sp. botfly larvae in horses from the south‐eastern part of Poland. Bulletin of the Veterinary Institute in Pulawy 53, 651–5.
  32. Wang KH, Zhang D, Li K. Developmental threshold temperature and effective accumulated temperature for pupae of Gasterophilus pecorum. Chinese Journal of Vector Biology and Control 26, 572–5.
  33. Wang W, Zhang D, Hu D, Chu H, Cao J, Ente M, Jiang G, Li K. Population genetic structure of Gasterophilus pecorum in the Kalamaili Nature Reserve, Xinjiang, based on mitochondrial cytochrome oxidase (COI) gene sequence.. Med Vet Entomol 2014 Aug;28 Suppl 1:75-82.
    pubmed: 25171609doi: 10.1111/mve.12073google scholar: lookup
  34. Watve MG, Sukumar R. Parasite abundance and diversity in mammals: correlates with host ecology.. Proc Natl Acad Sci U S A 1995 Sep 12;92(19):8945-9.
    pmc: PMC41084pubmed: 7568049doi: 10.1073/pnas.92.19.8945google scholar: lookup
  35. Wit P, Bandi N, Bouman I, van Staalduinen MA. The Przewalski's horse and its reintroduction in the steppe of Hustai National Park, Mongolia. In: Werger MJA, van Staalduinen MA, eds. Eurasian Steppes. Ecological Problems and Livelihoods in a Changing World. Springer, Dordrecht, pp. 357–68.
  36. Xue WQ, Zhao JM. Flies in China, Vol. II. Liaoning Science and Technology Press, Shenyang.
  37. Zang S, Cao Q, Alimujiang K, Liu SH, Zhang YJ, Hu DF. Food patch particularity and forging strategy of reintroduced Przewalski's horse in North Xinjiang, China. Turkish Journal of Zoology 41, 924–30.
  38. Zhang Y, Cao QS, Rubenstein DI, Zang S, Songer M, Leimgruber P, Chu H, Cao J, Li K, Hu D. Water Use Patterns of Sympatric Przewalski's Horse and Khulan: Interspecific Comparison Reveals Niche Differences.. PLoS One 2015;10(7):e0132094.
  39. Zumpt F. Morphology, biology and pathogenesis of myiasis‐producing flies in systematic order. In: Zumpt F, ed. Myiasis in Man and Animals in the Old World: A Textbook for Physicians, Veterinarians and Zoologists. Butterworths, London, pp. 110–28.

Citations

This article has been cited 7 times.
  1. Turghan MA, Jiang Z, Niu Z. An Update on Status and Conservation of the Przewalski's Horse (Equus ferus przewalskii): Captive Breeding and Reintroduction Projects. Animals (Basel) 2022 Nov 15;12(22).
    doi: 10.3390/ani12223158pubmed: 36428386google scholar: lookup
  2. Zhang K, Zhou R, Huang H, Ma W, Qi Y, Li B, Zhang D, Li K, Chu H. Host feces, olfactory beacon guiding aggregation of intestinal parasites Gasterophilus pecorum (Diptera: Gasterophilidae). Parasitol Res 2022 Sep;121(9):2601-2613.
    doi: 10.1007/s00436-022-07577-6pubmed: 35788769google scholar: lookup
  3. Rabei ȘO, Pivariu D, Cocian AI, Vaccaro D, Costache-Bobescu P, Mihalca AD. Seasonality, control, and risk factors for Gasterophilus intestinalis egg intensity in horses from Romania under field conditions. Parasitol Res 2025 Aug 6;124(8):87.
    doi: 10.1007/s00436-025-08540-xpubmed: 40767875google scholar: lookup
  4. Uakhit R, Bauer C, Smagulova A, Kiyan V. First Reported Case of Accidental Gastric Myiasis Caused by Gasterophilus Larvae in a Gray Wolf. Acta Parasitol 2025 Mar 20;70(2):72.
    doi: 10.1007/s11686-025-01012-3pubmed: 40111556google scholar: lookup
  5. Guo P, Li S, Zhu J, Lu Q. Variation in soil bacterial community characteristics inside and outside the West Ordos National Nature Reserve, northern China. Front Microbiol 2024;15:1404848.
    doi: 10.3389/fmicb.2024.1404848pubmed: 38919497google scholar: lookup
  6. Zhang Y, Liu J, Zhang K, Wang A, Sailikebieke D, Zhang Z, Ao T, Yan L, Zhang D, Li K, Huang H. Biological response to Przewalski's horse reintroduction in native desert grasslands: a case study on the spatial analysis of ticks. BMC Ecol Evol 2024 May 11;24(1):61.
    doi: 10.1186/s12862-024-02252-zpubmed: 38734637google scholar: lookup
  7. Zhang Y, Zhang K, Wang M, Wu X, Liu J, Chu H, Zhang D, Li K, Huang H. Studies on the embryonic development and larval infection potential of the stomach bot flies, Gasterophilus pecorum. Int J Parasitol Parasites Wildl 2024 Apr;23:100917.
    doi: 10.1016/j.ijppaw.2024.100917pubmed: 38419737google scholar: lookup