Characterization of a composite with enhanced attraction to savannah tsetse flies from constituents or analogues of tsetse refractory waterbuck (Kobus defassa) body odor
Savannah tsetse flies avoid flying toward tsetse fly-refractory waterbuck (Kobus defassa) mediated by a repellent blend of volatile compounds in their body odor comprised of δ-octalactone, geranyl acetone, phenols (guaiacol and carvacrol), and homologues of carboxylic acids (C5-C10) and 2-alkanones...
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Published in | PLoS neglected tropical diseases Vol. 15; no. 6; p. e0009474 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
01.06.2021
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Abstract | Savannah tsetse flies avoid flying toward tsetse fly-refractory waterbuck (Kobus defassa) mediated by a repellent blend of volatile compounds in their body odor comprised of δ-octalactone, geranyl acetone, phenols (guaiacol and carvacrol), and homologues of carboxylic acids (C5-C10) and 2-alkanones (C8-C13). However, although the blends of carboxylic acids and that of 2-alkanones contributed incrementally to the repellency of the waterbuck odor to savannah tsetse flies, some waterbuck constituents (particularly, nonanoic acid and 2-nonanone) showed significant attractive properties. In another study, increasing the ring size of δ-octalactone from six to seven membered ring changed the activity of the resulting molecule (ε-nonalactone) on the savannah tsetse flies from repellency to attraction. In the present study, we first compared the effect of blending ε-nonalactone, nonanoic acid and 2-nonanone in 1:1 binary and 1:1:1 ternary combination on responses of Glossina pallidipes and Glossina morsitans morsitans tsetse flies in a two-choice wind tunnel. The compounds showed clear synergistic effects in the blends, with the ternary blend demonstrating higher attraction than the binary blends and individual compounds. Our follow up laboratory comparisons of tsetse fly responses to ternary combinations with different relative proportions of the three components showed that the blend in 1:3:2 proportion was most attractive relative to fermented cow urine (FCU) to both tsetse species. In our field experiments at Shimba Hills game reserve in Kenya, where G. pallidipes are dominant, the pattern of tsetse catches we obtained with different proportions of the three compounds were similar to those we observed in the laboratory. Interestingly, the three-component blend in 1:3:2 proportion when released at optimized rate of 13.71mg/h was 235% more attractive to G. pallidipes than a combination of POCA (3-n-Propylphenol, 1-Octen-3-ol, 4-Cresol, and Acetone) and fermented cattle urine (FCU). This constitutes a novel finding with potential for downstream deployment in bait technologies for more effective control of G. pallidipes, G. m. morsitans, and perhaps other savannah tsetse fly species, in 'pull' and 'pull-push' tactics. |
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AbstractList | Savannah tsetse flies avoid flying toward tsetse fly-refractory waterbuck (Kobus defassa) mediated by a repellent blend of volatile compounds in their body odor comprised of [delta]-octalactone, geranyl acetone, phenols (guaiacol and carvacrol), and homologues of carboxylic acids (C.sub.5 -C.sub.10) and 2-alkanones (C.sub.8 -C.sub.13). However, although the blends of carboxylic acids and that of 2-alkanones contributed incrementally to the repellency of the waterbuck odor to savannah tsetse flies, some waterbuck constituents (particularly, nonanoic acid and 2-nonanone) showed significant attractive properties. In another study, increasing the ring size of [delta]-octalactone from six to seven membered ring changed the activity of the resulting molecule ([epsilon]-nonalactone) on the savannah tsetse flies from repellency to attraction. In the present study, we first compared the effect of blending [epsilon]-nonalactone, nonanoic acid and 2-nonanone in 1:1 binary and 1:1:1 ternary combination on responses of Glossina pallidipes and Glossina morsitans morsitans tsetse flies in a two-choice wind tunnel. The compounds showed clear synergistic effects in the blends, with the ternary blend demonstrating higher attraction than the binary blends and individual compounds. Our follow up laboratory comparisons of tsetse fly responses to ternary combinations with different relative proportions of the three components showed that the blend in 1:3:2 proportion was most attractive relative to fermented cow urine (FCU) to both tsetse species. In our field experiments at Shimba Hills game reserve in Kenya, where G. pallidipes are dominant, the pattern of tsetse catches we obtained with different proportions of the three compounds were similar to those we observed in the laboratory. Interestingly, the three-component blend in 1:3:2 proportion when released at optimized rate of 13.71mg/h was 235% more attractive to G. pallidipes than a combination of POCA (3-n-Propylphenol, 1-Octen-3-ol, 4-Cresol, and Acetone) and fermented cattle urine (FCU). This constitutes a novel finding with potential for downstream deployment in bait technologies for more effective control of G. pallidipes, G. m. morsitans, and perhaps other savannah tsetse fly species, in 'pull' and 'pull-push' tactics. Savannah tsetse flies avoid flying toward tsetse fly-refractory waterbuck (Kobus defassa) mediated by a repellent blend of volatile compounds in their body odor comprised of δ-octalactone, geranyl acetone, phenols (guaiacol and carvacrol), and homologues of carboxylic acids (C5-C10) and 2-alkanones (C8-C13). However, although the blends of carboxylic acids and that of 2-alkanones contributed incrementally to the repellency of the waterbuck odor to savannah tsetse flies, some waterbuck constituents (particularly, nonanoic acid and 2-nonanone) showed significant attractive properties. In another study, increasing the ring size of δ-octalactone from six to seven membered ring changed the activity of the resulting molecule (ε-nonalactone) on the savannah tsetse flies from repellency to attraction. In the present study, we first compared the effect of blending ε-nonalactone, nonanoic acid and 2-nonanone in 1:1 binary and 1:1:1 ternary combination on responses of Glossina pallidipes and Glossina morsitans morsitans tsetse flies in a two-choice wind tunnel. The compounds showed clear synergistic effects in the blends, with the ternary blend demonstrating higher attraction than the binary blends and individual compounds. Our follow up laboratory comparisons of tsetse fly responses to ternary combinations with different relative proportions of the three components showed that the blend in 1:3:2 proportion was most attractive relative to fermented cow urine (FCU) to both tsetse species. In our field experiments at Shimba Hills game reserve in Kenya, where G. pallidipes are dominant, the pattern of tsetse catches we obtained with different proportions of the three compounds were similar to those we observed in the laboratory. Interestingly, the three-component blend in 1:3:2 proportion when released at optimized rate of 13.71mg/h was 235% more attractive to G. pallidipes than a combination of POCA (3-n-Propylphenol, 1-Octen-3-ol, 4-Cresol, and Acetone) and fermented cattle urine (FCU). This constitutes a novel finding with potential for downstream deployment in bait technologies for more effective control of G. pallidipes, G. m. morsitans, and perhaps other savannah tsetse fly species, in ‘pull’ and ‘pull-push’ tactics. Savannah tsetse flies avoid flying toward tsetse fly-refractory waterbuck ( Kobus defassa ) mediated by a repellent blend of volatile compounds in their body odor comprised of δ-octalactone, geranyl acetone, phenols (guaiacol and carvacrol), and homologues of carboxylic acids (C 5 -C 10 ) and 2-alkanones (C 8 -C 13 ). However, although the blends of carboxylic acids and that of 2-alkanones contributed incrementally to the repellency of the waterbuck odor to savannah tsetse flies, some waterbuck constituents (particularly, nonanoic acid and 2-nonanone) showed significant attractive properties. In another study, increasing the ring size of δ-octalactone from six to seven membered ring changed the activity of the resulting molecule (ε-nonalactone) on the savannah tsetse flies from repellency to attraction. In the present study, we first compared the effect of blending ε-nonalactone, nonanoic acid and 2-nonanone in 1:1 binary and 1:1:1 ternary combination on responses of Glossina pallidipes and Glossina morsitans morsitans tsetse flies in a two-choice wind tunnel. The compounds showed clear synergistic effects in the blends, with the ternary blend demonstrating higher attraction than the binary blends and individual compounds. Our follow up laboratory comparisons of tsetse fly responses to ternary combinations with different relative proportions of the three components showed that the blend in 1:3:2 proportion was most attractive relative to fermented cow urine (FCU) to both tsetse species. In our field experiments at Shimba Hills game reserve in Kenya, where G . pallidipes are dominant, the pattern of tsetse catches we obtained with different proportions of the three compounds were similar to those we observed in the laboratory. Interestingly, the three-component blend in 1:3:2 proportion when released at optimized rate of 13.71mg/h was 235% more attractive to G . pallidipes than a combination of POCA (3- n -Propylphenol, 1-Octen-3-ol, 4-Cresol, and Acetone) and fermented cattle urine (FCU). This constitutes a novel finding with potential for downstream deployment in bait technologies for more effective control of G . pallidipes , G . m . morsitans , and perhaps other savannah tsetse fly species, in ‘pull’ and ‘pull-push’ tactics. Savannah tsetse flies avoid flying toward tsetse fly-refractory waterbuck ( Kobus defassa ) mediated by a repellent blend of volatile compounds in their body odor comprised of δ-octalactone, geranyl acetone, phenols (guaiacol and carvacrol), and homologues of carboxylic acids (C 5 -C 10 ) and 2-alkanones (C 8 -C 13 ). However, although the blends of carboxylic acids and that of 2-alkanones contributed incrementally to the repellency of the waterbuck odor to savannah tsetse flies, some waterbuck constituents (particularly, nonanoic acid and 2-nonanone) showed significant attractive properties. In another study, increasing the ring size of δ-octalactone from six to seven membered ring changed the activity of the resulting molecule (ε-nonalactone) on the savannah tsetse flies from repellency to attraction. In the present study, we first compared the effect of blending ε-nonalactone, nonanoic acid and 2-nonanone in 1:1 binary and 1:1:1 ternary combination on responses of Glossina pallidipes and Glossina morsitans morsitans tsetse flies in a two-choice wind tunnel. The compounds showed clear synergistic effects in the blends, with the ternary blend demonstrating higher attraction than the binary blends and individual compounds. Our follow up laboratory comparisons of tsetse fly responses to ternary combinations with different relative proportions of the three components showed that the blend in 1:3:2 proportion was most attractive relative to fermented cow urine (FCU) to both tsetse species. In our field experiments at Shimba Hills game reserve in Kenya, where G . pallidipes are dominant, the pattern of tsetse catches we obtained with different proportions of the three compounds were similar to those we observed in the laboratory. Interestingly, the three-component blend in 1:3:2 proportion when released at optimized rate of 13.71mg/h was 235% more attractive to G . pallidipes than a combination of POCA (3- n -Propylphenol, 1-Octen-3-ol, 4-Cresol, and Acetone) and fermented cattle urine (FCU). This constitutes a novel finding with potential for downstream deployment in bait technologies for more effective control of G . pallidipes , G . m . morsitans , and perhaps other savannah tsetse fly species, in ‘pull’ and ‘pull-push’ tactics. In our previous studies with tsetse fly-refractory waterbuck body odor, we found that certain subtle structural changes are associated with shifts in activities of some constituents from repellency to attraction. This led us to discovery of three potent tsetse attractants (ε-nonalactone, nonanoic acid and 2-nonanone). In the present study, we explored possible synergistic effects of blending of these compounds in different proportions to Glossina pallidipes and Glossina m . morsitans in the laboratory, followed by field studies with G . pallidipes . A three-component blend comprised of ε -nonalactone, nonanoic acid and 2-nonanone in 1:3:2 proportion gave 235% higher tsetse fly catches in the field compared with that of POCA and FCU. Thus, dispensing this odor blend in tsetse fly traps or insecticide treated targets is expected to suppress the tsetse flies more efficiently. It will also be interesting to see if the blend is similarly attractive to other savannah tsetse fly species. |
Audience | Academic |
Author | Kabaka, Joy M Okoth, Sylvance O Changasi, Robert Hassanali, Ahmed Wachira, Benson M Ochieng', Bernard Obore, Patrick Mireji, Paul O Murilla, Grace A Nganga, Margaret M |
AuthorAffiliation | 3 Kenya Medical Research Institute, Kilifi, Kenya 1 Kenyatta University, Nairobi, Kenya 2 Biotechnology Research Institute—Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya 4 Shimba Hills National Reserve—Kenya Wildlife Service, Kwale, Kenya University of Florida, UNITED STATES |
AuthorAffiliation_xml | – name: 4 Shimba Hills National Reserve—Kenya Wildlife Service, Kwale, Kenya – name: University of Florida, UNITED STATES – name: 1 Kenyatta University, Nairobi, Kenya – name: 2 Biotechnology Research Institute—Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya – name: 3 Kenya Medical Research Institute, Kilifi, Kenya |
Author_xml | – sequence: 1 givenname: Benson M orcidid: 0000-0002-9840-7778 surname: Wachira fullname: Wachira, Benson M organization: Biotechnology Research Institute-Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya – sequence: 2 givenname: Joy M surname: Kabaka fullname: Kabaka, Joy M organization: Kenyatta University, Nairobi, Kenya – sequence: 3 givenname: Paul O orcidid: 0000-0002-7965-2428 surname: Mireji fullname: Mireji, Paul O organization: Kenya Medical Research Institute, Kilifi, Kenya – sequence: 4 givenname: Sylvance O orcidid: 0000-0002-9959-6849 surname: Okoth fullname: Okoth, Sylvance O organization: Biotechnology Research Institute-Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya – sequence: 5 givenname: Margaret M orcidid: 0000-0002-7870-8821 surname: Nganga fullname: Nganga, Margaret M organization: Kenyatta University, Nairobi, Kenya – sequence: 6 givenname: Robert surname: Changasi fullname: Changasi, Robert organization: Biotechnology Research Institute-Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya – sequence: 7 givenname: Patrick surname: Obore fullname: Obore, Patrick organization: Biotechnology Research Institute-Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya – sequence: 8 givenname: Bernard surname: Ochieng' fullname: Ochieng', Bernard organization: Shimba Hills National Reserve-Kenya Wildlife Service, Kwale, Kenya – sequence: 9 givenname: Grace A orcidid: 0000-0002-4753-2819 surname: Murilla fullname: Murilla, Grace A organization: Biotechnology Research Institute-Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya – sequence: 10 givenname: Ahmed orcidid: 0000-0002-0654-9067 surname: Hassanali fullname: Hassanali, Ahmed organization: Kenyatta University, Nairobi, Kenya |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34061857$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_scitotenv_2023_168785 crossref_primary_10_1371_journal_pone_0273543 crossref_primary_10_1186_s13071_024_06299_1 crossref_primary_10_1371_journal_pone_0299243 crossref_primary_10_3389_fphys_2022_831618 |
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Copyright | COPYRIGHT 2021 Public Library of Science 2021 Wachira et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2021 Wachira et al 2021 Wachira et al |
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DocumentTitleAlternate | Composite with enhanced attraction of savannah tsetse |
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Notes | new_version The authors have declared that no competing interests exist. |
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References_xml | – volume: 74 start-page: 1 year: 1984 ident: pntd.0009474.ref001 article-title: Control of tsetse flies (Diptera: Glossinidae) using insecticides: a review and future prospects publication-title: Bull. Entom. Res doi: 10.1017/S0007485300009895 contributor: fullname: R. Allsopp – volume: 9 start-page: 95 year: 1988 ident: pntd.0009474.ref017 article-title: The role of 4-cresol and 3-n-propylphenol in the attraction of tsetse to buffalo urine publication-title: Insect Sci. Appl contributor: fullname: M. Owaga – volume: 146 start-page: 17 year: 2015 ident: pntd.0009474.ref020 article-title: Repellency of tsetse-refractory waterbuck (Kobus defassa) body odor to Glossina pallidipes (Diptera: Glossinidae): assessment of relative contribution of different classes and individual constituents publication-title: Acta Trop doi: 10.1016/j.actatropica.2015.02.017 contributor: fullname: M. Bett – volume: 14 start-page: 511 year: 1993 ident: pntd.0009474.ref007 article-title: The distribution of Glossina species in Africa and their natural hosts publication-title: Insect Sci. Appl contributor: fullname: S. Moloo – volume: 5 start-page: 335 year: 1984 ident: pntd.0009474.ref012 article-title: 1-Octen-3-ol: a potent olfactory stimulant and attractant for tsetse isolated from cattle odors publication-title: Insect Sci. Appl contributor: fullname: D. Hall – ident: pntd.0009474.ref018 – volume: 4 start-page: 632 year: 2010 ident: pntd.0009474.ref019 article-title: Prospects for the Development of Odor Baits to Control the Tsetse flies G. tachinoides and G. palpalis publication-title: PLoS Negl. Tropic. Dis doi: 10.1371/journal.pntd.0000632 contributor: fullname: J. Rayaisse – volume: 7 start-page: 5 year: 1986 ident: pntd.0009474.ref016 article-title: Identification of tsetse attractants from excretory products of a wild host animal, Syncerus caffer publication-title: Insect Sci. Appl contributor: fullname: A. Hassanali – volume: 29 start-page: 711 year: 1963 ident: pntd.0009474.ref006 article-title: The feeding habits of Glossina publication-title: Bull. World Health Organ contributor: fullname: B. Weitz – volume: 12 start-page: 169 year: 1998 ident: pntd.0009474.ref011 article-title: Host preferences of tsetse (Diptera: Glossinidae) based on bloodmeal identifications publication-title: Med. Vet. Entomol doi: 10.1046/j.1365-2915.1998.00097.x contributor: fullname: P. Clausen – volume: 15 start-page: 55 year: 1993 ident: pntd.0009474.ref008 article-title: Disease research in the wildlife-livestock interface in Kenya. (Review papers) publication-title: Vet. Quart doi: 10.1080/01652176.1993.9694372 contributor: fullname: J. 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Wachira – volume: 67 start-page: 635 year: 1977 ident: pntd.0009474.ref013 article-title: Feeding responses of tsetse flies (Diptera: Glossinidae) to stationary hosts publication-title: Bull. Entomol. Res doi: 10.1017/S0007485300007008 contributor: fullname: G. Vale – start-page: 209 volume-title: Insects and other Arthropods of Medical Importance year: 1973 ident: pntd.0009474.ref027 contributor: fullname: W. Potts – volume: 29 start-page: 2331 year: 2003 ident: pntd.0009474.ref010 article-title: Responses of G. m. morsitans to blends of electroantennographically active compounds in the odors of its preferred (buffalo and ox) and non-preferred (waterbuck) hosts publication-title: J. Chem. Ecol doi: 10.1023/A:1026230615877 contributor: fullname: N. Gikonyo – start-page: 412 volume-title: Principles of Instrumental Analysis year: 2014 ident: pntd.0009474.ref022 contributor: fullname: D. Skoog – volume: 34 start-page: 229 year: 1994 ident: pntd.0009474.ref003 article-title: Bait methods for tsetse fly control publication-title: Adv. Parasitol doi: 10.1016/S0065-308X(08)60140-2 contributor: fullname: C. Green – volume: 78 start-page: 31 year: 1988 ident: pntd.0009474.ref002 article-title: Odor-baited targets to control tsetse flies Glossina spp. (Diptera: Glossinidae), in Zimbabwe publication-title: Bull. Entom. Res doi: 10.1017/S0007485300016059 contributor: fullname: G. Vale – start-page: 265 volume-title: Olfaction in vector-host interactions. Ecology and Control of Vector-borne Diseases, 2 year: 2010 ident: pntd.0009474.ref005 doi: 10.3920/9789086866984_014 contributor: fullname: S. Torr – volume-title: The 1nsects of Australia year: 1991 ident: pntd.0009474.ref026 contributor: fullname: P. Cranston – volume: 63 start-page: 507 year: 1971 ident: pntd.0009474.ref023 article-title: An artificial feeding technique for Glossina publication-title: Parasitology doi: 10.1017/S0031182000080021 contributor: fullname: S. Moloo – volume: 13 start-page: 315 year: 1999 ident: pntd.0009474.ref004 article-title: The efficacy of various pyrethroid insecticides for use on odor-baited targets to control tsetse publication-title: Med. Vet. Entomol doi: 10.1046/j.1365-2915.1999.00165.x contributor: fullname: T. Mangwiro – volume: 10 start-page: 395 year: 1985 ident: pntd.0009474.ref024 article-title: ’Anemotactic’ flight paths of tsetse flies in relation to host odour: a preliminary video study in nature of the response to loss of odour publication-title: Physiological Entomology doi: 10.1111/j.1365-3032.1985.tb00061.x contributor: fullname: G Gibson – volume: 9 start-page: 95 year: 1988 ident: pntd.0009474.ref014 article-title: The role of 4-methylphenol and 3-n-propylphenol in the attraction of tsetse flies to buffalo urine publication-title: Insect Sci. Appl contributor: fullname: A. Hassanali – volume: 82 start-page: 321 year: 1992 ident: pntd.0009474.ref025 article-title: ‘Activity rhythms of tsetse flies (Glossina spp.) (Diptera: Glossinidae) at low and high temperatures in nature’ publication-title: Bull. Entomol. Res doi: 10.1017/S0007485300041092 contributor: fullname: J. Hargrove |
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Snippet | Savannah tsetse flies avoid flying toward tsetse fly-refractory waterbuck (Kobus defassa) mediated by a repellent blend of volatile compounds in their body... Savannah tsetse flies avoid flying toward tsetse fly-refractory waterbuck ( Kobus defassa ) mediated by a repellent blend of volatile compounds in their body... |
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SubjectTerms | Acetone Acids Animals Aroma compounds Attraction Baits Bioassays Biological assays Biology and Life Sciences Blending effects Body odors Carbon isotopes Carboxylic acids Carvacrol Cattle Chemotactic Factors - chemistry Chemotactic Factors - metabolism Chemotaxis Chromatography Constituents Control Cresol Cresols Deployment Disease transmission Fermentation Fermented food Field tests Flies Flight Game preserves Guaiacol Homology Insect Control Insect Repellents - chemistry Insect Repellents - metabolism Kenya Kobus ellipsiprymnus Laboratories Lactones Medicine and Health Sciences Mixtures Muscidae NMR Nonalactone Nuclear magnetic resonance Odor compounds Odorants - analysis Odors Odour Pest control Phenols Physical Sciences Prevention Repellency Repellents Ruminants - metabolism Savannahs Seabirds Social Sciences Solvents Structure-activity relationships (Biochemistry) Synergistic effect Tactics Testing Tropical diseases Tsetse Flies - physiology Tsetse-flies Urine Variance analysis Volatile compounds Volatile Organic Compounds - chemistry Volatile Organic Compounds - metabolism Wind tunnels |
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Title | Characterization of a composite with enhanced attraction to savannah tsetse flies from constituents or analogues of tsetse refractory waterbuck (Kobus defassa) body odor |
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