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Olfactory Sensitivity of the Turkey Vulture (Cathartes Aura) to Three Carrion-Associated Odorants

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Olfactory Sensitivity of the Turkey Vulture (Cathartes Aura) to Three Carrion-Associated Odorants OLFACTORY SENSITIVITY OF THE TURKEY VULTURE (CATHARTES AURA) TO THREE CARRION-ASSOCIATED ODORANTS STEVEN A. SMITH • AND RICHARD A. PASELK Departmentsof BiologicalSciences and Chemistry, Humboldt State University, Arcata,California 95523 USA ABSTRACT.--TheTurkey Vulture (Cathartesaura) is generally thought to rely on olfactory cuesto locate carrion. Becausevertically rising odorantsare dispersedrapidly by wind tur- bulence, we predict that Turkey Vultures should be highly sensitive to these chemicalsto detect them at foraging altitudes. Olfactory thresholdsto three by-productsof animal decomposition(1 x 10-6 M for buta- noic acid and ethanethiol, and 1 x 10-5 M for trimethylamine) were determined from heart- rate responses.These relatively high thresholds indicate that these odorantsare probably not cuesfor foraging Turkey Vultures. Odorant thresholds,food habits of Turkey Vultures, and the theoretical properties of odorant dispersion cast some doubt on the general impor- tanceof olfaction in food locationby this species.Received 23 September1985, accepted 3 March 1986. THEsensory modality by which Turkey Vul- Companydiscovered that natural gas leaks could tures (Cathartes aura) locate carrion has been be tracedby injectingethanethiol into gaslines debatedby naturalistsfor nearly 140 years(see and patrolling the lines for Turkey Vultures Stager1964 for review). Most of the controver- that, ostensibly,were attractedto the metcap- sy concernedwhether olfaction or vision was tan (Stager 1964). Stager (1964: 56) concluded the more important sense,although other the- from anatomical examinations and field tests ories included an "occult" sense (Beck 1920), that the Turkey Vulture "possessesand utilizes the noiseof carrion-eatingrodents, or the noise a well developedolfactory food locatingmech- of carrion-eatinginsects (Taber 1928, Darling- anism." ton 1930) as attractingTurkey Vultures to their If Turkey Vulturesrely on olfactorycues to prey. find food, foraging altitudes and search pat- Cathartesaura is now known to possessan terns should be a function of their ability to anatomically well-developed and physiologi- respondto concentrationgradients formed by cally functional olfactory system.Comparative carrion odorants emitted during decomposi- anatomical studies indicate that the relative size tion. Numerous mathematical models predict of the Turkey Vulture olfactory bulb is the odorant concentrationsalong Cartesian coor- eighth largestof 108 avian speciesreported by dinates downwind from the odorant source. Bang and Cobb (1968). The olfactory tubercle Most commonlyused is the Gaussiangas dis- in this speciesis scrolled and lined with an persionmodel, which assumesthat the concen- epithelium innervated by the olfactory nerve trationgradient is normally distributedin three (Bang 1960, 1971; Stager 1964). Single-unit dimensions (Strom 1976). Odorant concentra- neural responseshave been recordedfrom the tions at a given point in space decreasewith olfactory epithelial receptors (Shibuya and respect to an increase in the parameters that Tucker 1967), and heart- and respiratory-rate affect odorant dispersion.Because wind is the changesare known to occurwhen vultures are principal dispersing agent for gases released presentedwith olfactorystimuli (Wenzel 1965, into the atmosphere(Bosseft and Wilson 1963), Wenzel and Sieck 1972). In 1938 the Union Oil the model predictsthat dispersionof a given odorant concentrationis greatestin the direc- tion of the prevailing wind (x-axis). Because xPresent address: Department of Wildlife and the interaction of wind shear with the ground Fisheries Sciences,Texas A&M University, College producesturbulence, dispersion is least along Station, Texas 77843 USA. the vertical axis above the emission source (z- 586 The Auk 103:586-592. July 1986 July1986] Olfactionin theTurkey Vulture 587 axis). Bossertand Wilson (1963) applied the amine, and I x 10-8 , I x 10-7 , and I x I0 6M for Gaussianmodel to an analysisof olfactorycom- ethanethiol; these concentrations were chosen from munication in animals and provided maxima a preliminary screeningof a wide range of odorant solutionsfor the extent of odorant dispersal dilutions]. Odorant dilutions were presentedin or- along the x- and z-axesas a function of an an- der of increasingconcentration, with a control odor- ant consisting of distilled water randomly inserted imal's olfactory threshold. These solutions de- within each dilution series. A minimum of 5 rain scribe the maximum downwind distance (xm•) elapsedbetween presentations of test dilutions.All and altitude (z•) for an odorant concentration three chemicalodorants were usedduring eachtrial, that is above the threshold level of an animal with the order of presentationdetermined randomly. responding to olfactory cues. To minimize mixing the odorants,an exhaustfan was Although it is generally acceptedthat Tur- usedfor a minimum of 15 rain betweenpresentations key Vultureslocate carrion from olfactorycues, of the different chemicals. A total of 66 trials was run olfactorythresholds to carrion-associatedodor- usingeach odorant dilution series;individual sample ants have not been reported for this species. sizes for the four vultures were 15, 16, 17, and 18 trials. Presumably,their olfactory thresholdsare low Heart rateswere determinedby electrocardiogra- enough for them to detect carrion odorantsat phy (ECG).Differences in heartrate were determined foraging altitudes. Solutions for x• and z• by comparingthe number of beats in 5-s intervals provide a model that can be used to examine both before and after the odorant reached the bird the likelihood of specificcarrion odorantsserv- (0 s). Net changeswere establishedby adding the ing as olfactory cues to foraging Turkey Vul- difference in the number of beats between the time tures. intervals 0-5 s and -5 to 0 s, to the difference in We determined approximate olfactory re- the number of beats between the time intervals 5-10 sponsethresholds to three odorants (butanoic s and 0-5 s. A Kruskal-Wallisanalysis was used to acid, ethanethiol, and trimethylamine) associ- compareheart-rate changes within treatmentsto de- termine whether the data from individual birds could ated with animal decomposition.Butanoic acid has the characteristic odor of rancid fat and is be pooled.The Wilcoxontwo-sample test compared heart-ratechanges associated with eachodorant con- a by-productof protein, carbohydrate,and fat centrationagainst changes recorded during the pre- decomposition(Wells 1907).Several thioIs, in- sentationof the control.Significant (P < 0.05)changes cluding ethanethiol, are formed from the in heart rate between the control and odorant dilu- breakdown of sulfur-containing amino acids tions were interpreted as indicators of olfactory (Wells 1907)and are the compoundsused com- thresholds. mercially to give natural gas its odor. Trimeth- The Turkey Vulturesused in this studywere adults ylamine has a "fishy" odor and is releaseddur- of unknown sexand age. Three of the four had sus- ing muscletissue decomposition (Grey and Lea tained permanent wing injuries and were obtained 1969). In addition to the association of these from raptor rehabilitationcenters or other research- ers; there was no evidence that these injuries had odorants with animal decomposition, both affectedthe olfactorysense of these animals. The ethanethiol and butanoic acid are known to fourthbird wasphysically sound and had beenraised elicit olfactoryresponses in the Turkey Vulture in captivity.All four birds were maintainedon a dai- (Stager 1964, Wenzel and Sieck 1972). ly diet of meatand were weighedbiweekly to mon- itor their health. Considerabletime was spent habi- MATERIALS AND METHODS tuating the vultures to the olfactometerand the ECG EXPERIMENTAL DESIGN equipment.Test sessions always preceded daily feed- ings. Birdswere not testeduntil minimal heart rates Responsethresholds to olfactorystimuli were de- had been achieved. To minimize odorant habituation termined by continuousmonitoring of a vulture's and stress, the birds were not tested more than once heartrate before and during the presentationof three every three days. concentrationsof ethanethiol (ethyl mercaptan),tri- Olfactometer.--Theolfactometer was a modification methylamine,and butanoicacid (n-butyric acid). Our of the simple injectionolfactometer described by method was a modificationof the techniqueem- Moulton (1973).Our systemvaporized dilute odorant ployedby Wenzel(1965) and Wenzeland Sieck(1972). into an air stream to achieve the desired odorant con- Eachof four TurkeyVultures was repeatedlytested centration. Diluted odorants were drawn from 15-ml with three dilutions of each test odorant [1 x 10-7, arepulesby a peristaltic pump at 2.9 x 10-6 1/s I x 10-6, and 1 x 10-5 moles odorant/liter air (M), through0.51-ram (ID) standardpump tubing and al- calculatedat STP, for butanoicacid and trimethyl- lowedto drip ontoa glass"T" via a 20-gaugestain- 588 SMITHAND PASELK [Auk,Vol. 103 lesssteel hypodermicneedle insertedthrough a rub- ber diaphragm. The glass T was wrapped with •A nichromewire and electricallyheated to give an in- stantaneousvaporization of the odorant.A regulated and calibrated airflow (3.9 x 10 2 I/s) connected to the glassT carriedthe vaporized odorantto a mixing chamber. -5 0 5 10 The mixing chamberwas constructedfrom a glass SECONDS powder funnel attachedto a 58 x 99-mm glasstube Fig. 1. Sample ECG recordsshowing (A) no net with a perforated Plexiglasbaffle placed at the junc- changein heart rate following stimulation
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