Pankaj S. Shah

Taxon-specific differences in responsiveness to capsaicin and several analogues: correlates between chemical structure and behavioral aversiveness

The present set of experiments was designed to explore avian insensitivity to capsaicin. Based upon a molecular model of avian chemosensory repellency, we hypothesized that structural modifications of the basic capsaicin molecule, which is itself not aversive to birds, might produce aversive analogues. To this end, European starlings (Sturnus vulgaris) and Norway rats (Rattus norvegicus) were given varied concentrations of synthetic capsaicin and four analogues (methyl capsaicin, veratryl amine, veratryl acetamide, vanillyl acetamide) in feeding and drinking tests. The results agreed with a model that we are developing to describe the chemical nature of avian repellents. Synthetic capsaicin and vanillyl acetamide were not repellent to birds, owing to the presence of an acidic phenolic OH group. Conversely, veratryl acetamide was aversive, due to the basic nature of this compound. For rats, repellent effectiveness among compounds was reversed: synthetic capsaicin was the best repellent while veratryl acetamide was the worst. We speculate that this taxonomic reversal may reflect basic differences in trigeminal chemoreception. In any case, it is clear that chemical correlates of mammalian repellents are opposite to those that predict avian repellency.

Ortho-Aminoacetophenone Repellency to Birds: Similarities to Methyl Anthranilate

Methyl anthranilate is an effective bird repellent at concentrations ≥1.0% (g/g). Ortho-aminoacetophenone (OAP) has an odor similar to that of methyl anthranilate and is chemically (structurally) similar. Coincidentally, OAP is present in the scent gland secretions of mustelid species that prey on birds. For these reasons, we chose to test the bird repellency of this material and 3 isomers to European starlings (Sturnus vulgaris). Ortho-aminoacetophenone was repellent at concentrations ≤0.01% in both choice and no-choice feeding tests. The other structural isomers (meta-, para-, alpha-) were less effective

Avian Repellency of Coniferyl and Cinnamyl Derivatives

Phenylpropanoids, a class of common phenolic compounds in plants, may potentially be useful as pest repellents. We investigated the relationship between the chemical structure of coniferyl benzoate and its repellency to birds by comparing coniferyl benzoate to two analogous natural esters, corresponding alcohols, and benzoic acid. The absolute and relative feeding repellency of these compounds were assessed in choice (two-cup) and no-choice (one-cup) tests using European Starlings (Sturnus vulgaris). In addition, benzoin Siam (= gum benzoin Siam) was compared to coniferyl benzoate to ascertain if phenolics that naturally occur with coniferyl benzoate in benzoin Siam enhance its repellency. Two-cup tests suggested that coniferyl alcohol was the most repellent compound followed by 3,4-dimethoxycinnamyl alcohol, 3,4-dimethoxycinnamyl benzoate, cinnamyl alcohol, cinnamyl benzoate, coniferyl benzoate, and benzoic acid. The repellency of most alcohols relative to their corresponding ester reversed in the one-cup tests. One-cup tests suggested that 3,4-dimethoxycinnamyl benzoate was the most repellent substance followed by cinnamyl benzoate, benzoin Siam, 3,4-dimethoxycinnamylalcohol, cinnamyl alcohol, coniferyl alcohol, coniferyl benzoate, and benzoic acid. Three conclusions on structure-activity relationships were inferred from these data. First, benzoate esters are more repellent than their corresponding alcohols.Second, repellency is increased by electron-donating groups. Third, acidic functions decrease repellency. We suggest that one function of naturally occurring coniferyl and cinnamyl derivatives may be chemical defense. Genetically engineering agricultural crops to produce analogs of coniferyl alcohol, as an inherent defense against pests and pathogens, may be possible.

Tests and refinements of a general structure-activity model for avian repellents

We tested the robustness of a structure-activity model for avian trigeminal chemoirritants. Fourteen benzoates and acetophenones were tested using European starlingsSturnus vulgaris as a bioassay. In general, the previously proposed model was a reasonable predictor of repellency (i.e., irritant potency). We found that the presence of a phenyl ring was critical to repellency. Basicity of the molecule is the next most critical feature influencing repellency. The presence of an acidic function within the electron-withdrawing functionality seriously detracts from repellency. The presence or absence of an electron-withdrawing or -donating group may potentiate repellent effects, but its presence is not critical, so long as the phenyl ring is electron rich. Our data suggest that there is ano-aminoacetophenone/methyl anthranilate trigeminal chemoreceptor in birds analogous to the mammalian capsaicin receptor. Both receptors contain a benzene site. However, birds seem to lack the associated thiol/hydrogen-bonding site present in mammals which is needed to activate the benzene site. Rather, birds may possess an associated exposed charged site that in turn may interact with the stimulus to activate the benzene site. These differences may explain the differential sensitivity of birds and mammals to aromatic irritants.

Prediction of avian repellency from chemical structure: The aversiveness of vanillin, vanillyl alcohol, and veratryl alcohol

Abstract The effectiveness of bird repellents is associated with the presence of an electron-withdrawing group (carbonyl or carboxyl) and an electron-donating group in resonance on a phenyl ring. The present experiments were designed to examine the relative importance of these structural features. European starlings (Sturnus vulgaris) were presented with vanillin, vanillyl alcohol, and veratryl alcohol in two-cup and one-cup feeding trials and in one-bottle drinking tests. In feeding trials, veratryl alcohol was significantly more aversive than the other two chemicals. In drinking tests, veratryl alcohol was repellent only at the highest concentration (0.5% ml/ml), and was lethal at that concentration and at 0.1 and 0.05% ml/ml. Together, the findings have several implications. From a basic perspective, the data emphasize the importance of electron-donating groups on the phenyl ring of repellent chemicals. From the practical perspective, the data suggest veratryl alcohol as an avian toxicant, and warn against generalization from feeding to drinking tests. We propose that avian repellents must be tailored to the specialized settings in which they are used.

CHEMICAL BIRD REPELLENTS: POSSIBLE USE IN CYANIDE PONDS

Regulatory agencies are pressuring the mining industry to protect wildlife from mortality associated with the consumption of dump leachate pond water containing cyanide. Using European starlings (Sturnus vulgaris) as an avian model, we tested the effectiveness of 5 chemical bird repellents at reducing consumption of pond water containing cyanide. The repellents, which were previously shown to be good bird repellents, were: o-aminoacetophenone (OAP), 2-amino-4,5-dimethoxyacetophenone (2A45DAP), methyl anthranilate (MA), 4-ketobenztriazine (4KBT), and veratryl amine (VA). Despite the high pH (10.6) and presence of chelating metals, conditions which we hypothesized might destroy the activity of repellents, each of the additives reduced pond water intake relative to controls for up to 5 weeks. The rank order (from best to worst) of repellents was: OAP, 2A45DAP, VA, MA and 4KBT, although only OAP and 4KBT differed at the P < 0.05 level. These candidate repellents hold promise as a strategy to reduce bird losses at cyanide ponds and should be tested in the field.

Taxonomic Differences between Birds and Mammals in Their Responses to Chemical Irritants

Ninety-five products are registered with the U.S. Environmental Protection Agency as bird damage control chemicals, but 38 (40%) are nonlethal chemical repellents (Eschen and Schafer, 1986). Of these products, the active ingredients in 27 (71%) are methiocarb (a physiologic repellent that acts through food avoidance learning) or polybutene (a tactile repellent). In general, chemical repellents are effective either because of aversive sensory effects (irritation), or because of post-ingestional malaise (sickness). If the former, then chemicals are usually stimulants of trigeminal pain receptors (i.e., undifferentiated free nerve endings) in the nose, mouth, and eyes (Mason and Otis, 1990). Although many birds possess adequate olfactory and gustatory capabilities (e.g., Berkhoudt, 1985, Kare and Mason, 1986) smell and taste, per se, are rarely of consequence for bird damage control. Here, we address chemosensory repellents only.

Information Content of Prey Odor Plumes: What Do Foraging Leach’s Storm Petrels Know?

Electrophysiological responses to odor have been recorded for concentrations as low as 0.01 ppm for Manx Shearwaters Puffinus puffinus and Black-footed Albatrosses Diomedea niaripes indicating that relative to most birds, procellariiforms have a keen sense of smell (Wenzel and Sieck 1972, cf. Clark 1991; Clark and Smeraski 1990; Clark and Mason 1989). Such acuity is not unexpected, given the extensive development of the olfactory anatomy of these species (Bang and Wenze 1986). Field observations indicate that Procellariiformes use their sense of smell to locate food (Grubb 1972; Hutchison and Wenzel 1980; Lequette, Verheyden and Jouventin 1989). However, it is not known how far from the source petrels can detect odors. This information would improve our understanding of procellariiform foraging ecology and engender a broader appreciation of the selective forces involved in shaping the evolution of the sensory anatomy of this group (Healy and Guilford 1990). Herein, we report preliminary observations on the odor sensitivity of Leach’s Storm Petrel Oceanodroma leucorhoa to the major components of natural prey items. The detection data are used to generate a first order estimate of the odor active space for free ranging petrels.

Avian Chemical Repellency: A Structure-Activity Approach and Implications

Until recently, the discovery of avian sensory repellents has been empirical (Mason, Adams and Clark 1989). However, recent studies in our laboratory have shown that many avian repellents have similar perceptual and structural properties (Mason et al. 1989; Mason Clark and Shah 1991; Clark and Shah 1991; Clark, Shah and Mason 1991; Shah, Clark and Mason 1991). For example, methyl anthranilate, which has a grapy odor, is repellent to birds (Kare and Pick, 1960). Ortho-aminoacetophenone has an odor and structure similar to that of methyl anthranilate, differing only in the substitution of a ketone for an ester group (Mason et al. 1991). Behavioral tests of this aminoacetophenone isomer showed that it is at least an order of magnitude more repellent to birds than methyl anthranilate (Clark and Shah 1991). These similarities in structure and function prompted us to undertake a series of studies to elucidate a predictive model of chemical structure-activity (Clark and Shah 1991; Clark et al 1991; Shah et al. 1991). As a consequence of these studies we hypothesize a model where the following structural features appear to be important: (1) A phenyl ring with an electron donating or a basic group is central to repellency; (2) An electron withdrawing group in resonance with a basic group decreases the repellency (as well as the toxicity) of a substance. These effects are pronounced when the groups are ortho to one another; (3) The presence of an acidic group decreases repellency; (4) The presence of an H-bonded ring or a covalently bonded fused ring that possesses the required features (e.g., electron donating and withdrawing groups ortho to each other) can enhance repellency, but is not essential; (5) Steric hinderance can overpower the features described above, and can weaken the effectiveness of potentially aversive substances.