FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Parasitol Res / Host feces, olfactory beacon guiding aggregation of intestin...
Parasitology research2022; 121(9); 2601-2613; doi: 10.1007/s00436-022-07577-6

Host feces, olfactory beacon guiding aggregation of intestinal parasites Gasterophilus pecorum (Diptera: Gasterophilidae).

Abstract: The aim of this study was to identify the aggregation sites and transmission characteristics of Gasterophilus pecorum, the dominant pathogen of endangered equines in desert steppe. Therefore, we tested with a four-arm olfactometer the olfactory response of the G. pecorum adults to the odors that have a great impact on their life cycle, and also investigated the occurrence sites of the adults in the area where the Przewalski's horse (Equus przewalskii) roam frequently during the peak period of G. pecorum infection. The results of four-directional olfactory test showed that the fresh horse feces had a stronger attraction rate on both male (50.4%) and female flies (38.2%). Stipa caucasica, the only oviposition plant where G. pecorum lay eggs, had a better attraction effect on females than that on males. And the attraction rates of S. caucasica to G. pecorum females in the early growth stage (Stipa I) and mid-growth stage (Stipa II) were 32.8% and 36.8%, respectively. In addition, the two-directional olfactory test showed that the attraction rate of males to fresh horse feces (68.90%) was higher than that to Stipa II (31.10%), and females also showed similar olfactory responses. Moreover, in our field investigation, 68.29% of G. pecorum adults were collected from around the horse feces. The results of laboratory test and field investigation implied that the location mechanism of G. pecorum aggregation for mating is related to the orientation of horse feces. The horse feces and the vicinity are the key contamination areas of G. pecorum, and it is also the areas where horses are seriously infected with G. pecorum. Those fresh feces, which gather abundant information about the host, naturally had the greatest chance of contacting with the host; G. pecorum adults create the opportunity to enter directly into the host's mouth and infect the host by laying eggs on S. caucasica, which is the most favorite plant of the host in this area. These characteristics are one of the main reasons why G. pecorum has become the dominant species under the condition of sparse vegetation in desert steppe.
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Get Full Text
Publication Date: 2022-07-05 PubMed ID: 35788769PubMed Central: 4226234DOI: 10.1007/s00436-022-07577-6Google 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.
LinkedInCopy
  • 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.

The research study focuses on the behavior and transmission characteristics of Gasterophilus pecorum, a parasite significantly impacting endangered equines in desert steppe environments. The paper notes important factors like host feces and specific plant types in driving the aggregation and mating behavior of these parasites.

Research Objectives and Methodology

  • The study aimed to understand the aggregation sites and transmission characteristics of Gasterophilus pecorum, a dominant parasite affecting endangered equines, specifically Przewalski’s horse, Equus przewalskii, in desert steppe environments.
  • The researchers performed olfactory tests using a four-arm olfactometer to study the parasite’s response to odors impacting its life cycle.
  • They examined the locations frequented by adult parasites during peak infection periods.

Findings: Role of Fresh Horse Feces

  • The study discovered that fresh horse feces had a strong attraction for both male (50.4% attraction rate) and female flies (38.2% attraction rate).
  • In a two-directional olfactory test, the attraction rate of males to fresh horse feces was 68.90% and that of females was similar.
  • Field investigations also showed that 68.29% of G. pecorum adults were collected from areas surrounding horse feces.

Findings: Role of Stipa Caucasica Plant

  • Stipa caucasica, a plant where G. pecorum lays eggs, had a stronger attraction for female flies compared to males.
  • The attraction rates for early growth (Stipa I) and mid-growth stage (Stipa II) of this plant for female G. pecorum were 32.8% and 36.8% respectively.

Conclusions and Implications

  • The study concluded that G. pecorum’s aggregation and mating behavior are heavily influenced by the odor of host feces and the presence of S. caucasica plants.
  • The areas around horse feces are key contamination areas for G. pecorum and are also where horses are most severely infected.
  • The research implies that managing the feces and surroundings could be a viable strategy for controlling the spread of this parasite.

Cite This Article

APA
Zhang K, Zhou R, Huang H, Ma W, Qi Y, Li B, Zhang D, Li K, Chu H. (2022). Host feces, olfactory beacon guiding aggregation of intestinal parasites Gasterophilus pecorum (Diptera: Gasterophilidae). Parasitol Res, 121(9), 2601-2613. https://doi.org/10.1007/s00436-022-07577-6

Publication

Parasitology research
ISSN: 1432-1955
NlmUniqueID: 8703571
Country: Germany
Language: English
Volume: 121
Issue: 9
Pages: 2601-2613

Researcher Affiliations

Zhang, Ke
  • Key Laboratory of Non-Invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, 100083, China.
  • Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Science, Xining, 810001, China.
Zhou, Ran
  • Key Laboratory of Non-Invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, 100083, China.
Huang, Heqing
  • Chongqing Academy of Environmental Science, Chongqing, 401147, China.
Ma, Wei
  • Mt. Kalamaili Ungulate Nature Reserve, Changji, Xinjiang, 831100, China.
Qi, Yingjie
  • Mt. Kalamaili Ungulate Nature Reserve, Changji, Xinjiang, 831100, China.
Li, Boling
  • China National Environment Monitoring Center, Beijing, 100012, China.
Zhang, Dong
  • Key Laboratory of Non-Invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, 100083, China.
Li, Kai
  • Key Laboratory of Non-Invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, 100083, China. jiujiu@bjfu.edu.cn.
Chu, Hongjun
  • Institute of Forest Ecology, Xinjiang Academy of Forestry, Urumqi, 830063, China. hongjunchualtai@hotmail.com.

MeSH Terms

  • Animals
  • Desert Climate
  • Diptera / physiology
  • Endangered Species
  • Feces / chemistry
  • Feces / parasitology
  • Female
  • Horse Diseases / parasitology
  • Horse Diseases / transmission
  • Horses
  • Intestinal Diseases, Parasitic / parasitology
  • Intestinal Diseases, Parasitic / transmission
  • Male
  • Parasites / growth & development
  • Parasites / isolation & purification
  • Plant Development
  • Plants

References

This article includes 58 references
  1. Albuquerque TA, Zurek L. Temporal changes in the bacterial community of animal feces and their correlation with stable fly oviposition, larval development, and adult fitness. Front Microbiol 5:590.
    doi: 10.3389/fmicb.2014.00590pubmed: 25426108pmc: 4226234google scholar: lookup
  2. Brevault T, Quilici S. Flower and fruit volatiles assist host-plant location in the Tomato fruit fly Neoceratitis cyanescens. Physiol Entomol 35:9–18.
    doi: 10.1111/j.1365-3032.2009.00704.xgoogle scholar: lookup
  3. Catts EP. Hilltop aggregation and mating behavior by Gasterophilus intestinalis (Diptera: Gasterophilidae). J Med Entomol 16:461–464.
    doi: 10.1093/jmedent/16.6.461google scholar: lookup
  4. Cheng F et al. Isolation and characterization of microsatellite loci from Gasterophilus pecorum, (Diptera: Gasterophilidae). Conserv Genet Resour 6:487–489.
    doi: 10.1007/s12686-013-0136-xgoogle scholar: lookup
  5. Chu HJ, Jiang ZG, Lan WX, Wang C, Tao YS, Jiang F. Dietary overlap among kulan Equus hemionus, goitered gazelle Gazella subgutturosa and livestock. Acta Zool Sin 54:941–954 (in Chinese with English abstract).
  6. Coapio GG, Cruz-López L, Guerenstein P, Malo EA, Rojas JC. Oviposition preference and larval performance and behavior of Trichoplusia ni (Lepidoptera: Noctuidae) on host and nonhost plants. Arthropod-Plant Inte 12:267–276.
    doi: 10.1007/s11829-017-9566-9google scholar: lookup
  7. Cogley TP, Cogley MC. Inter-relationship between Gasterophilus larvae and the horse’s gastric and duodenal wall with special reference to penetration. Vet Parasitol 86:127–142.
    doi: 10.1016/S0304-4017(99)00119-3pubmed: 10496697google scholar: lookup
  8. Cogley TP, Cogley MC. Field observations of the host-parasite relationship associated with the common horse bot fly, Gasterophilus intestinalis. Vet Parasitol 88:93–105.
    doi: 10.1016/S0304-4017(99)00191-0pubmed: 10681026google scholar: lookup
  9. Colwell DD, Hall MJR, Scholl PJ. The Oestrid flies: biology, host-parasite relationships, impact and management. Oxford University Press, London, UK pp 140–166.
    doi: 10.1079/9780851996844.0000google scholar: lookup
  10. Cope SE, Catts EP. Parahost behavior of adult Gasterophilus intestinalis (Diptera: Gasterophilidae) in Delaware. J Med Entomol 28:67–73.
    doi: 10.1093/jmedent/28.1.67pubmed: 2033621google scholar: lookup
  11. Dekker T, Geier M, Cardé RT. Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J Exp Biol 208(15):2963–2972.
    doi: 10.1242/jeb.01736pubmed: 16043601google scholar: lookup
  12. Galvez-Marroquin Z, Cruz-López L, Malo EA, Ramsey JM, Rojas JC. Behavioural and electrophysiological responses of Triatoma dimidiata nymphs to conspecific faecal volatiles. Med Vet Entomol 32:102–110.
    doi: 10.1111/mve.12271pubmed: 28892179google scholar: lookup
  13. Glasser S, Farzan S. Host-associated volatiles attract parasitoids of a native solitary bee, Osmia lignaria Say (Hymenoptera, Megachilidae). J Hymenopt Res 51:249–2560.
    doi: 10.3897/jhr.51.9727google scholar: lookup
  14. Gouinguené SP, Turlings TCJ. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296–1307.
    doi: 10.1104/pp.001941pubmed: 12114583pmc: 166523google scholar: lookup
  15. Grenacher S, Kröber T, Guerin PM, Vlimant M. Behavioural and chemoreceptor cell responses of the tick, Ixodes ricinus, to its own faeces and faecal constituents. Exp Appl Acarol 25:641–660.
    doi: 10.1023/A:1016145805759pubmed: 12171273google scholar: lookup
  16. Harris MO, Galanihe LD, Sandnayake M. Adult emergence and reproductive behavior of the leafcurling midge Dasineura mali (Diptera: Cecidomyiidae). Ann Entomol Soc Am 92:748–757.
    doi: 10.1093/aesa/92.5.748google scholar: lookup
  17. Herrebout WM, Veer J. Habitat selection in Eucarcelia rutilla Vill. (Diptera: Tachinidae). J Appl Entomol 64:55–61.
    doi: 10.1111/j.1439-0418.1967.tb02071.xgoogle scholar: lookup
  18. Hoseini SM, Zaheri BA, Adibi MA, Ronaghi H, Moshrefi AH. Histopathological study of esophageal infection with Gasterophilus pecorum (Diptera: Oestridae) in Persian Onager (Equus hemionus onager). J Arthropod Borne Dis 11(3):441–445.
    pubmed: 29322061pmc: 5758640
  19. Huang HQ, Zhang BR, Chu HJ, Zhang D, Li K. Gasterophilus (Diptera, Gasterophilidae) infection of equids in the Kalamaili Nature Reserve, China. Parasite 23:36.
    doi: 10.1051/parasite/2016036google scholar: lookup
  20. Huang HQ et al. Distribution of Gasterophilus (Diptera: Gasterophilidae) myiasis foci in arid desert steppe: a case study of Kalamaili Mountain Ungulate Nature Reserve. Sci Silvae Sin 53:142–149 (in Chinese with English abstract).
  21. Huang HQ et al. Spatial distribution of Gasterophilus pecorum (Diptera) eggs in the desert steppe of the Kalamaili Nature Reserve (Xinjiang, China). BMC Ecol Evo 21:169.
    doi: 10.1186/s12862-021-01897-4google scholar: lookup
  22. Huang HQ et al. 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.
    doi: 10.1111/1749-4877.12578pubmed: 34254452google scholar: lookup
  23. Ibrayev B, Lider L, Bauer C. Gasterophilus spp. infections in horses from northern and central Kazakhstan. Vet Parasitol 207:94–98.
    doi: 10.1016/j.vetpar.2014.11.015google scholar: lookup
  24. Jost DJ, Pitre HN. Soybean looper (Lepidoptera: Noctuidae) oviposition on cotton and soybean of different growth stages: influence of olfactory stimuli. J Econ Entomol 95:286–293.
    doi: 10.1603/0022-0493-95.2.286pubmed: 12020002google scholar: lookup
  25. Kolosova N, Gorenstein N, Kish CM, Dudareva N. Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13:2333–2347.
    doi: 10.1105/tpc.010162pubmed: 11595805pmc: 139162google scholar: lookup
  26. Krecek RC, Reinecke RK, Horak IG. Internal parasites of horses on mixed grassveld and bushveld in Transval, Republic of South Africa. Vet Parasitol 34:135–143.
    doi: 10.1016/0304-4017(89)90173-8pubmed: 2588465google scholar: lookup
  27. 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 262:56–74.
    doi: 10.1016/j.vetpar.2018.09.011pubmed: 30389013google scholar: lookup
  28. Li XY, Pape T, Zhang D. Taxonomic review of Gasterophilus (Oestridae, Gasterophilinae) of the world, with updated nomenclature, keys, biological notes and distributions. ZooKeys 891:119–156.
    doi: 10.3897/zookeys.891.38560google scholar: lookup
  29. Liu SH, Hu DF, Li K. Oviposition site selection by Gasterophilus pecorum (Diptera: Gasterophilidae) in its habitat in Kalamaili Nature Reserve, Xinjiang, China. Parasite 22:34.
    doi: 10.1051/parasite/2015034pubmed: 26621549pmc: 4664853google scholar: lookup
  30. Liu SH, Li K, Hu DF. The incidence and species composition of Gasterophilus (Diptera, Gasterophilidae) causing equine myiasis in northern Xinjiang, China. Vet Parasitol 217:36–38.
    doi: 10.1051/parasite/2015034pubmed: 26827858google scholar: lookup
  31. Lyons ET, Tolliver SC, Collins SS. Prevalence of large endoparasites at necropsy in horses infected with Population B small strongyles in a herd established in Kentucky in 1966. Parasitol Res 99:114–118.
    doi: 10.1007/s00436-005-0116-5pubmed: 16508764google scholar: lookup
  32. Mauchline AL, Osborne JL, Martin AP, Poppy GM, Powell W. The effects of non-host plant essential oil volatiles on the behaviour of the pollen beetle Meligethes aeneus. Entomol Exp Appl 114:181–188.
    doi: 10.1111/j.1570-7458.2005.00237.xgoogle scholar: lookup
  33. Moshaverinia A, Baratpour A, Abedi V, Mohammadi-Yekta M. Gasterophilosis in Turkmen horses caused by Gasterophilus pecorum (Diptera, Oestridae). Sci Parasitol 17:49–52.
  34. Mukbel R, Torgerson PR, Abo-Shehada M. Seasonal variations in the abundance of Gasterophilus spp. larvae in donkeys in northern Jordan. Trop Anim Health Prod 33:501–509.
    doi: 10.1023/A:1012732613902pubmed: 11770204google scholar: lookup
  35. Natale D, Mattiacci L, Pasqualini E, Dorn D. Apple and peach fruit volatiles and the apple constituent butyl hexanoate attract female oriental fruit moth, Cydia molesta, in the laboratory. J Appl Entomol 128(1):22–27.
    doi: 10.1046/j.1439-0418.2003.00802.xgoogle scholar: lookup
  36. Olival KJ et al. Lack of population genetic structure and host specificity in the bat fly, Cyclopodia horsfieldi, across species of Pteropus bats in Southeast Asia. Parasit Vectors 6:231.
    doi: 10.1186/1756-3305-6-231pubmed: 23924629pmc: 3750525google scholar: lookup
  37. 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 133:111–118.
    doi: 10.1016/j.vetpar.2005.05.015pubmed: 15978726google scholar: lookup
  38. Pacheco A, Blanco-Metzler H, Mora R. Modification of four-arm olfactometers to be used with the coffee borer Hypothenemus hampei Ferrari (Coleoptera: Curculionidae). Agron Costarric 6:69–78 (in Spanish with English abstract).
  39. Pawlas M, Sołtysiak Z, Nicpoń J. Existence and pathomorhological picture of gasterophilosis in horses from north-east Poland. Med Weter 63:1377–1380.
  40. Peñaflor MFGV, Erb M, Miranda LA, Werneburg AG, Bento JMS. Herbivore-induced plant volatiles can serve as host location cues for a generalist and a specialist egg parasitoid. J Chem Ecol 37:1304–1313.
    doi: 10.1007/s10886-011-0047-9pubmed: 22170346google scholar: lookup
  41. Piñero JC, Dorn S. Response of female oriental fruit moth to volatiles from apple and peach trees at three phenological stages. Entomol Exp Appl 131:67–74.
    doi: 10.1111/j.1570-7458.2009.00832.xgoogle scholar: lookup
  42. Ranjith AM. An inexpensive olfactometer and wind tunnel for Trichogramma chilonis Ishii (Trichogrammatidae: Hymenoptera). J Trop Agric 45:63–65.
  43. Rastegaev YM. Ecological characteristics of the warble and bot flies attacking horses (Diptera: Oestridae, Gasterophilidae) in the desert zone of the Caspian Region. Entomol Rev 64:35–39.
  44. Rehbein S, Visser M, Winter R. Prevalence, intensity and seasonality of gastrointestinal parasites in abattoir horses in Germany. Parasitol Res 112:407–413.
    doi: 10.1007/s00436-012-3150-0pubmed: 23052780google scholar: lookup
  45. Reshetnikov AD, Barashkova AI, Prokopyev ZS. Infestation of horses by the causative agents of gasterophilosis (Diptera: Gasterophilidae): the species composition and the north-eastern border of the area in the Republic (Sakha) of Yakutia of the Russian Federation. Life Sci J 11:587–590.
    doi: 10.7537/marslsj111114.105google scholar: lookup
  46. Robinson A et al. Responses of the putative trachoma vector, Musca sorbens, to volatile semiochemicals from human faeces. PLoS Neglected Trop Dis 14:1–15.
    doi: 10.1371/journal.pntd.0007719google scholar: lookup
  47. Salerno G, Frati F, Conti E, Peri E, Colazza S, Cusumano A. Mating status of an herbivorous stink bug female affects the emission of oviposition-induced plant volatiles exploited by an egg parasitoid. Front Physiol 10:398.
    doi: 10.3389/fphys.2019.00398pubmed: 31031636pmc: 6473057google scholar: lookup
  48. Uefune M, Shiojiri K, Takabayashi J. Oviposition of diamondback moth Plutella xylostella females is affected by herbivore-induced plant volatiles that attract the larval parasitoid Cotesia vestalis. Arthropod-Plant Inte 11:235–239.
    doi: 10.1007/s11829-016-9484-2google scholar: lookup
  49. Wang WT et al. Population genetic structure of Gasterophilus pecorum in the Kalamaili Nature Reserve, Xinjiang, based on mitochondrial cytochrome oxidase (COI) gene sequence. Med Vet Entomol 28:75–82.
    doi: 10.1111/mve.12073pubmed: 25171609google scholar: lookup
  50. Wang WT et al. Diversity and Infection of Gasterophilus spp. in Mongol-Xinjiang Region and Qinghai Tibet Region. Sci Silvae Sin 52:134–139 (in Chinese with English abstract).
  51. Wei JQ, Mo JC, Wang XJ, Lin W. Responses of housefly adults to different food. Chin J Vector Biol Control 19:12–13 (in Chinese with English abstract).
  52. Witzgall P, Stelinski L, Gut L, Thomson D. Codling moth management and chemical ecology. Annu Rev Entomol 53(1):503–522.
    doi: 10.1146/annurev.ento.53.103106.093323google scholar: lookup
  53. Zang S et al. Food patch particularity and forging strategy of reintroduced Przewalski's horse in North Xinjiang, China. Turk J Zool 41:924–930.
    doi: 10.3906/zoo-1509-9google scholar: lookup
  54. Zhang K et al. The impact of temperature on the life cycle of Gasterophilus pecorum in northwest China. Parasit Vectors 14:129.
    doi: 10.1186/s13071-021-04623-7pubmed: 33648570pmc: 7923332google scholar: lookup
  55. Zhang YJ et al. Water use patterns of sympatric Przewalski’s horse and Khulan: interspecific comparison reveals niche differences. PLoS One 10:e0132094.
    doi: 10.1371/journal.pone.0132094pubmed: 26161909pmc: 4498657google scholar: lookup
  56. Zhou R et al. Identification of volatile components from oviposition and non-oviposition plants of Gasterophilus pecorum (Diptera: Gasterophilidae). Sci Rep 10:15731.
    doi: 10.1038/s41598-020-72378-9pubmed: 32978441pmc: 7519042google scholar: lookup
  57. Zhou R et al. Analysis of volatiles from feces of released Przewalski’s horse (Equus przewalskii) in Gasterophilus pecorum (Diptera: Gasterophilidae) spawning habitat. Sci Rep 11:15671.
    doi: 10.1038/s41598-021-95162-9pubmed: 34341455pmc: 8329074google scholar: lookup
  58. Zong XL et al. Ecology of bat flies in Singapore: a study on the diversity, infestation bias and host specificity (Diptera: Nycteribiidae). Int J Parasitol-Par 12:29–33.
    doi: 10.1016/j.ijppaw.2020.04.010google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.