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Research Article
Rumen metabolites serve ticks to exploit large mammals
Gérard Donzé, Conor McMahon, Patrick M. Guerin
Journal of Experimental Biology 2004 207: 4283-4289; doi: 10.1242/jeb.01241
Gérard Donzé
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Conor McMahon
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Patrick M. Guerin
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Article Figures & Tables

Figures

  • Table 1.

    Responses of adults of five hard tick species to odour being released from rumen fluid

    Amblyomma variegatum b Amblyomma hebraeumIxodes scapularisIxodes persulcatusIxodes ricinus
    N 1815201316
    Attraction (%)a+44***+26***+21***+13*+4**
    Change in speed (%)+23**+5+1+28**+4*
    • ↵a Median % change compared with control

    • ↵* P<0.05

    • ↵** P<0.01

    • ↵*** P<0.001; Wilcoxon signed rank test

    • ↵b Eight of the 18 A. variegatum adults tested undertook significant local search behaviours (see Fig. 1) upon removal of rumen odour from the air stream (Fisher exact test, P<0.01, two-tailed)

  • Fig. 1.
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    Fig. 1.

    Attraction of A. variegatum to rumen fluid odour. Polar plots of the mean walking direction of 18 A. variegatum adults presented in three successive 1 min intervals with (A) a control air stream (0°), (B) rumen fluid odour in the air stream and (C) the control air stream (without rumen fluid) again. Ticks that spent more time walking in the cone delimited by 60° either side of upwind (in red) after presentation of the rumen odour were considered to be attracted. (D) A track described by an A. variegatum adult in the same experiment; the track started (filled circle) with the tick walking down or across wind in the control period; the arrows on the track indicate stimulus on and off; the bar represents a displacement of 20 cm. Note the local search behaviour induced in A. variegatum by withdrawal of the rumen odour from the air stream. Open arrow at bottom indicates airstream direction (0°) for A,B,C and D.

  • Table 2.

    Responses of adult A. variegatum to entrained rumen odour and to individual chemostimulants of the rumen fluid odour and their mixtures

    TreatmentTicks tested (N)Source dose% Attraction1% Change in speed1
    Entrained rumen fluid odour171/10 dilution+42***,a+4e,f
    Single components
       Butanoic acid1610 ng+34***,a,b–34**,f,g
       Isobutanoic acid2910 ng–1 μg+32***,a,b–9*,e,f
       4-Methylphenol1110 ng+24**,b,c–2e
       3-Methylindole2010 ng+12*,b,c–7e,f
       Acetic acid141 μg+15*,b,c+3e
       Propanoic acid2010 ng+22***,a,b–12***,f
    Mixtures
       Butanoic acid:isobutanoic acid:4-methylphenol: 3-methylindole181 μg:100 ng:10 ng:10 ng+25***,a,b–3e,f
       Butanoic acid:isobutanoic acid:4-methylphenol: 3-methylindole111 μg:10 ng:10 ng:10 ng+3c–5e,f
       Butanoic acid:isobutanoic acid:4-methylphenol: 3-methylindole2010 ng:10 ng:10 ng:10 ng+2c+6e
       2Methane1370 ppm+1c–6e,f
    • ↵1 Median % change compared with control

    • ↵* P<0.05

    • ↵** P<0.01

    • ↵*** P<0.001; Wilcoxon signed rank test. Treatments sharing the same letter are not significantly different; (P>0.05; Wilcoxon–Mann–Whitney test

    • ↵2 Estimated concentration in the air stream

  • Fig. 2.
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    Fig. 2.

    Identification of rumen volatiles that stimulate olfactory receptor cells of ticks. Cattle rumen volatiles were analysed after collection on a porous polymer by gas chromatography coupled with electrophysiology recordings from olfactory receptor cells in wall-pore olfactory sensilla on the first leg tarsus of Amblyomma variegatum and Ixodes ricinus. (A) Flame ionisation detector (FID) response of the gas chromatograph to the separated rumen volatiles. (B) Enlarged sections of A where butanoic (A1), isopentanoic (A2), pentanoic (A3) and hexanoic (A4) acids, 2-nitrophenol (P1), 4-methyl-2-nitrophenol (P2), 4-methylphenol (P3), indole (I1) and 3-methylindole (I2) eluted and induced electrophysiological (EL) responses from olfactory receptor cells of A. variegatum and I. ricinus (trace for A. variegatum presented). The receptor cell response profiles in B were generated by summing the frequencies of the action potentials of the responding sensory cells (frequency to voltage conversion). U indicates an unidentified stimulus. (C,D) The spike trains generated in responding (from the arrows) A. variegatum (C) and I. ricinus (D) receptor cells to 4-methylphenol, butanoic acid and indole eluting from the gas chromatographic column. Receptor cells from both tick species also responded to acetic acid, propionic acid, phenol and 2-methylphenol (data not presented). The same carboxylic acid and phenolic volatiles identified in rumen odour of cattle were also recovered in the odour of roe deer rumen. Sensillum identity (DI and DII types) is according to a classification by Hess and Vlimant (1982).

  • Fig. 3.
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    Fig. 3.

    Microbial production of volatile rumen products perceived by ticks.

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Research Article
Rumen metabolites serve ticks to exploit large mammals
Gérard Donzé, Conor McMahon, Patrick M. Guerin
Journal of Experimental Biology 2004 207: 4283-4289; doi: 10.1242/jeb.01241
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Research Article
Rumen metabolites serve ticks to exploit large mammals
Gérard Donzé, Conor McMahon, Patrick M. Guerin
Journal of Experimental Biology 2004 207: 4283-4289; doi: 10.1242/jeb.01241

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