Use of predator odors as repellents to reduce feeding damage by herbivores

The effectiveness of predator odors (fecal, urine, and anal scent gland) in suppressing feeding damage by snowshoe hares was investigated in pen bioassays at the University of British Columbia Research Forest, Maple Ridge, British Columbia, Canada. A total of 28 bioassay trials tested the effects of these odors on hare consumption of willow browse and coniferous seedlings. Lynx and bobcat feces, weasel anal gland secretion, and lynx, bobcat, wolf, coyote, fox, and wolverine urines resulted in the most effective suppression of hare feeding damage. Novel odors of domestic dog urine and 2-methylbutyric acid did not reduce feeding. A field bioassay with lodgepole pine seedlings and weasel scent provided significant results comparable to the pen bioassays. The short-term (up to seven days) effectiveness of these treatments was more likely due to evaporative loss of the active repellent components of a given odor than habituation of hares to the stimulus. Predator odors as repellents have a biological basis compared with the anthropomorphic origins of commercial repellents. When encapsulated in weather-proof controlled-release devices, these odors could provide long-term protection for forestry plantations and agricultural crops which experience hare/rabbit feeding damage.     

Germacrone defends labrador tea from browsing by snowshoe hares

Labrador tea (Ledum groenlandicum), a slow-growing late successional evergreen, is highly unpalatable to snowshoe hares (Lepus americanus). Germacrone, a sesquiterpene that is the major component of the essential oil ofL. groenlandicum, was shown by bioassay to be a potent antifeedant to hares. Its concentrations in leaves and intemodes of the plant are high enough to defendL. groenlandicum from hares. This chemical defense of Labrador tea from herbivory is consistent with the resource availability theory of antiherbivore defense.     

Influence of the plant antifeedant,pinosylvin, on suppression of feeding by snowshoe hares

This study investigated the influence of the plant antifeedants, pinosylvin and pinosylvin methyl ether (PME), on suppression of feeding by snowshoe hares (Lepus americanus). Screening bioassays showed clearly that pinosylvin suppressed feeding by hares when sprayed directly on coniferous tree seedlings. Pinosylvin odor, when associated with food (but not mixed with it), also significantly reduced consumption of rabbit chow by hares. Large pen bioassays indicated that both pinosylvin and PME significantly reduced feeding on tree seedlings by hares when the antifeedants were sprayed directly on trees. In field bioassays near Prince George, British Columbia, Canada, pinosylvin sprayed on trees and encapsulated in controlled-release devices of PVC plastic, with an internal wire as a twist-tie for attachment to tree, significantly reduced feeding by hares. Thus, pinosylvin will generate an avoidance response in terms of feeding by snowshoe hares. This response is likely triggered by an olfactory pathway based on positive results with controlledrelease devices attached to seedlings. Our study reports the first practical utilization of plant antifeedants for forest crop protection and wildlife management.     

Camphor from juvenile white spruce as an antifeedant for snowshoe hares

One theory in plant antiherbivore defense predicts that slow growing late succession plants like white spruce (Picea glauca) make large investments in antiherbivore defenses. Juvenile stages of white spruce in the Yukon, Canada, are rarely browsed by snowshoe hares (Lepus americanus), an abundant herbivore, but mature spruce is a highly preferred food. The hexane-soluble fractions of the methanol extracts from juvenile and mature white spruce contain camphor and bomyl acetate. There is four times as much camphor in juvenile spruce as in mature spruce from GC analysis. Plant extracts were added to rabbit chow. Pairs of extracts were offered to hares in choice tests. These tests demonstrated that camphor in the juvenile spruce extracts deterred feeding. Bornyl acetate did not have a clear antifeeding effect.On leave from the Department of Chemistry, University of South Pacific, Fiji.     

Effects of birch phenolics on a grazing and a browsing mammal: A comparison of hares

Mountain hares (Lepus timidus L.) commonly have high proportions of birch (Betula spp.) in their winter diets, whereas European hares (Lepus europaeus) do not. The effects of a birch extract added to laboratory diets offered to mountain hares and European hares on the digestibility and sodium balance were measured. The extract added contained total phenolics equivalent in amount to that occurring in diets containing 0, 40, 60 and 80% dry matter of birch twigs. Increasing dietary phenolic concentration led to reduced voluntary food intake and apparent protein digestibility in both hare species. No effects on apparent dry matter digestibility were observed. The highest concentration of birch extract caused severe sodium losses via the urine by European hares but not by mountain hares. The effects of the birch extract within the digestive system appear to be similar in the two hare species, whereas the mountain hare appears to be better adapted to the toxic effects that disrupted sodium balance in the European hare. These preliminary results suggest that detoxification rather than digestive abilityper se may contribute to different mammalian herbivores' feeding strategies.     

Bark consumption by voles in relation to mineral contents

Recent field experiments with impregnated wooden sticks have demonstrated a pronounced use by small rodents of mineral supplies, especially sodium, and such findings seemed related to vole damage to forestry seedlings. Consumption of the bark of experimentally introduced aspen twigs and of sodium-impregnated sticks by voles (mainly or onlyMicrotus agrestis) correlated significantly on clear-cuts but not on unmanipulated abandoned fields. Such a correlation appeared when abandoned fields were cut continuously in summer. At vole peak densities, bark of pine seedlings experimentally fertilized with sodium was consumed but not bark of seedlings fertilized with calcium or control seedlings. Field pine seedlings attacked by voles had significantly higher levels of calcium, sodium, and phosphorus than the nearest untouched seedling. However, sodium and phosphorus contents correlated strongly. Sodium and calcium supply to voles in laboratory feeding trials did not diminish the moderate interest in pine bark. Such conditions are, however, assumed to mimic a situation of bark sampling in low-density populations. Sodium, and possibly also calcium, requirements are concluded to be partial determinants of the destructive bark consumption by voles at the peaks of their multiannual population cycles.     

Role of phenolics of coniferous trees as deterrents against debarking behavior of meadow voles (Microtus pennsylvanicus)

Preferences of meadow voles (Microtus pennsylvanicus) toward various coniferous species were tested under winter conditions. Cafeteria tests showed preferences for Norway spruce (Picea abies) and Norway pine (Pinus resinosa) and rejection of white pine (Pinus strobus) and white spruce (Picea glauca). When phenolic extracts of these species were prepared and added to a low 8% protein diet, food intake of voles and preferences by rank followed the same patterns. Determination of the concentration of phenolics in branch samples using the Singleton and Rossi procedure showed that Norway pines contained the smallest amount (2.15%/g dry matter) while spruces yielded the most (2.76%/g dry matter). These experiments lead us to expect high losses of Norway pine and Norway spruce in habitats harboring high vole densities.     

Feeding responses of snowshoe hares (Lepus americanus) to volatile constituents of red fox (Vulpes vulpes) urine

This study investigated the influence of the volatile constituents of red fox (Vulpes vulpes) urine in suppressing feeding by snowshoe hares (Lepus americanus) on coniferous tree seedlings. Pen and field bioassays indicated that the odor of fox urine and its principal component, 3-methyl-3-butenyl methyl sulfide, had a negative effect on feeding behavior of hares. The other sulfur-containing compounds, 2-phenylethyl methyl sulfide and 3-methylbutyl methyl sulfide, as well as six other constituents, were not effective. Synthetic urine mixtures composed of eight and nine volatile constituents, respectively, did not suppress feeding in pen bioassays. However, the mixture of eight compounds in a field bioassay did result in significantly fewer seedlings being eaten by hares than in the control. 3-Methyl-3-butenyl methyl sulfide may act as an interspecific chemical signal which induces a fear or avoidance response in hares. Additional work is required to determine the optimum concentration and release system for 3-methyl-3-butenyl methyl sulfide to be used as a mammalian semiochemical in crop protection.     

Chemical defense ofPopulus balsamifera: A Clarification

A previous report that the relative payabilities of juvenile versus maturePopulus balsamifera towards browsing snowshoe hares is due to the presence of 2,4,6-trihydroxydihydrochalcone in the juvenile growth form has been shown to be incorrect. Specifically, 2,4,6-trihydroxydihydrochalcone is present in internodes ofPopulus balsamifera in exceedingly low concentrations (<0.02% wet wt) and its concentrations are not elevated in internodes of the juvenile developmental stage. Its high levels in the buds (20–25% wet wt) ofPopulus balsamifera, however, probably makes it a deterrent substance for herbivores that cannot remove buds from twigs during foraging.     

Behavioral and electrophysiological responses of Arhopalus tristis to burnt pine and other stimuli

The exotic longhorn beetle Arhopalus tristisis a pest of pines, particularly those damaged by fire, and a major export quarantine issue in New Zealand. Actinograph recordings of caged individuals showed that males and females were most active from dusk to midnight. Olfactometer experiments indicated that females moved upwind toward odors from burnt pine (80%, N= 75), compared to unburnt pine (20%). Oviposition choice tests showed that eggs were predominantly laid on burnt logs (79%, N= 20), compared to unburnt logs. Beetles were trapped by funnel traps baited with burnt (mean catch per trap 7.8) and unburnt (mean catch 4.1 per trap) pine bark from inside a screen cage (4 × 3 m), while unbaited traps had a mean catch 0.1 beetles (N= 8 replicates). The treatment of burnt pine bark with a 1:1:2 mixture of green leaf volatiles (E)-2-hexen-1-ol and (E)-2-hexenal) in mineral oil as a repellent reduced trap catch by fivefold in a similar experiment (mean catches of 1.2 beetles per trap to burnt pine bark plus repellent treatment and 6.2 beetles per trap to burnt pine bark alone). The treatment of burnt pine bark with this solution also reduced oviposition by 98.5% (mean eggs per log of 11.1 on burnt pine and 0.3 on burnt pine plus repellent), indicating that oviposition cues have the potential to be significantly disrupted. The electrophysiological responses of adult beetles were recorded to a range of odorants. Normalized responses to monoterpenes known to occur in Pinus radiataranged from about 20 to about 150, with -terpineol giving the greatest responses in both sexes. Green leaf volatiles also gave high responses. The potential exists to improve the management of this insect using chemical cues in various ways.     

Lespedeza phenolics andPenstemon alkaloids: Effects on digestion efficiencies and growth of voles

Lespedeza cuneata contains high levels of phenolics and is a common food plant of the meadow vole (Microtus pennsylvanicus);Penstemon digitalis contains substantial quantities of alkaloids and is a common food plant of meadow voles and prairie voles (M. ochrogaster). We investigated the palatability of these plants and the effects of their secondary compounds on the digestion efficiencies and growth of both species of voles. Voles ate very little of either plant when alternative food was present. Phenolics and alkaloids were extracted from the plants, incorporated into separate artificial diets, and fed to weanling voles for three weeks.Lespedeza phenolics reduced the growth of meadow voles but not prairie voles throughout the feeding trial. These compounds disrupted digestion, reducing protein digestibility by more than half.Penstemon alkaloids lowered only the initial growth rates of prairie voles and had no significant effect on meadow voles. Prairie voles tended to increase food consumption rates on bothLespedeza andPenstemon diets. This response offset some of the decrease in digested protein intake in the first case, and offset the increased metabolic cost of processing the diet in the latter case. Our results indicate that althoughLespedeza phenolics andPenstemon alkaloids do influence consumption and digestibility of artificial diets, they do not greatly reduce the performance (i.e., growth or survival) of voles when consumed at levels generally observed for wild voles. However, these compounds probably do place an upper limit on the amount of freshLespedeza andPenstemon that can be consumed and contribute to the generalist feeding strategy of voles.     

Pine Weevil (Hylobius abietis) Antifeedants from Lodgepole Pine (Pinus contorta)

Pine weevils (Hylobius abietis) fed less on bark of lodgepole pine (Pinus contorta) than on bark of Scots pine (P. sylvestris). Two pine weevil antifeedants, ethyl trans-cinnamate and ethyl 2,3-dibromo-3-phenyl-propanoate, were isolated from bark of lodgepole pine. These two compounds significantly reduced pine weevil feeding in a laboratory bioassay. In field assays, the second compound significantly decreased pine weevil damage on planted seedlings. Ethyl 2,3-dibromo-3-phenylpropanoate has not previously been reported as a natural product.     

Effect of experience with pine (Pituophis melanoleucus) and king (Lampropeltis getulus) snake odors on Y-maze behavior of pine snake hatchlings

The abilities of hatchling pine snakes (Pituophis melanoleucus) and king snakes (Lampropeltis getulus) to discriminate the chemical trails of pine and king snakes was investigated inY-maze experiments. Pine snakes were housed for 17 days either with shavings impregnated with pine snake odor, king snake odor, or no odor to test for the effect of experience on choice. Both pine and king snake hatchlings entered the arm with the pine snake odor and did not enter the arm with the king snake odor. The data support the hypothesis that hatchlings of both species can distinguish conspecific odors from other odors and that our manipulation of previous experience was without effect for pine snake hatchlings.     

Cover and efficacy of predator-based repellents for Townsend's voleMicrotus townsendii

Predator-based repellents have been used experimentally to control wildlife damage in both agriculture and forestry, but they have not always been effective. We examined the relative importance of cover and predator odors in forage patch selection by Townsend's vole,Microtus townsendii, and its behavior related to cover and predator cues. Experiments were conducted in which forage patch and area choices were related to available habitat alternatives. Outdoor enclosures were divided into halves: one side was treated and the other used as a control. Treatments consisting of cover, repellent, and cover plus repellent were compared to controls (no cover, no repellent). In the absence of cover, voles preferred to feed on the side without repellents. When cover was present, voles preferred to feed on the side with cover, regardless of whether or not repellents were present. Voles visited more feeding stations on the side without cover when repellents and cover were present than they visited during cover-only treatments. These additional feeding stations, visited outside of cover, were used only lightly as food sources. The amounts of oats eaten by voles decreased with increasing distance from cover. This inverse relationship had a steeper slope in coveronly treatments compared to cover plus repellent treatments. A selection model based on forage patch selection and a habitat preference hierarchy is proposed. We conclude that predator odors are effective as repellents, but their efficacy depends on habitat conditions. Managers intending to use predator-based repellents must ensure that alternative sites available to pests are better quality habitat than in areas to be protected.     

Influence of mustelid scent-gland compounds on suppression of feeding by snowshoe hares (Lepus americanus)

This study investigated the influence of mustelid anal-gland compounds in suppressing feeding by snowshoe hares on coniferous tree seedlings. Pen and field bioassays indicated that 3-propyl-1,2-dithiolane from the stoat (Mustela erminea), and secondarily, 2,2-dimethylthietane from the mink (M. vison) had a very negative effect on feeding behavior of hares. The major component of stoat anal gland secretions, 2-propylthietane, and the related compounds, thietane and 2-methylthietane, were not effective. 3,3-Dimethyl-1,2-dithiolane from the least weasel (M. nivalis) and ferret (M. putorius) and di-n-propyldisulfide (acyclic analog of 3-propyl-1,2-dithiolane) similarly did not affect hare feeding. 3-Propyl-1,2-dithiolane and 2,2-dimethylthietane (also found inM. erminea) may act as interspecific chemical signals which induce a fear or avoidance response in hares. Such compounds have outstanding potential as area repellents to reduce crop and livestock depredations. Our study reports one of the first practical utilizations of mammalian semiochemicals in crop protection and wildlife management.     

Sheep food repellents: Efficacy of various products,habituation, and social facilitation

The study of food repulsion in ungulates is of practical importance for controlling browsing damage to forest trees and agricultural crops. Experiments with domestic sheep assessed the repulsive value of three natural and two synthetic products, using a food-choice situation. Animals were individually presented with two troughs, each containing 30 g of maize, one treated with a chemical product, and the other a control. The odor of domestic dog feces appeared to be highly repulsive, as none of the treated food was eaten, whereas 3 g ±9 and 6 g ±10 were eaten, respectively, of food treated with fetal fluids from sheep and odor of pig feces. Synthetic odors of lion feces and a commercial deer repellent were less efficient as repellents with 11 g ±13 and 14 g ±15 of food eaten, respectively. Habituation to three of the repellents was tested for a minimum of seven successive days. With dog feces, no habituation to the odor was observed. On the contrary, significant habituation (P < 0.05) was observed as early as the third trial for sheep fetal fluids and the fourth trial for the commercial repellent. To test for the effects of social facilitation, groups of four sheep including no, one, or two anosmic animals were presented with food treated with the odor of dog feces. No social facilitation was observed as none of the intact sheep ate any of the food, although the anosmic animals actively ate it throughout the test. In individual food choice tests, the odor of dog feces appeared to be an especially efficient repellent when compared with the other natural or synthetic products. Such repulsion was nearly complete, and neither habituation nor social facilitation could be observed.     

Inhibition of Snowshoe Hare Succinate Dehydrogenase Activity as a Mechanism of Deterrence for Papyriferic Acid in Birch

The plant secondary metabolite papyriferic acid (PA) deters browsing by snowshoe hares (Lepus americanus) on the juvenile developmental stage of the Alaska paper birch (Betula neoalaskana). However, the physiological mechanism that reduces browsing remains unknown. We used pharmacological assays and molecular modeling to test the hypothesis that inhibition of succinate dehydrogenase (SDH) is a mode of action (MOA) of toxicity of PA in snowshoe hares. We tested this hypothesis by measuring the effect of PA on the activity of SDH in liver mitochondria isolated from wild hares. In addition, we used molecular modeling to determine the specific binding site of PA on SDH. We found that PA inhibits SDH from hares by an uncompetitive mechanism in a dose-dependent manner. Molecular modeling suggests that inhibition of SDH is a result of binding of PA at the ubiquinone binding sites in complex II. Our results provide a MOA for toxicity that may be responsible for the concentration-dependent anti-feedant effects of PA. We propose that snowshoe hares reduce the dose-dependent toxic consequences of PA by relying on efflux transporters and metabolizing enzymes that lower systemic exposure to dietary PA.     

Effects of pine-produced chemicals on selected understory species in aPinus ponderosa community

Pinus ponderosa accounted for more than 98% of all tree and shrub stratum stems in a climax community with low herb coverage and aboveground biomass, 35% and 60 g/m², respectively. Because of our previous report that nitrification and nitrifying bacteria in the same community were allelopathically inhibited, we speculated that the pine-produced allelochemics might also directly influence the development and growth of the herb stratum. In most cases decaying needles, needle leachate, and field soils significantly reduced germination and radicle growth ofAndropogon gerardii andA. scoparius, pine-associated herbaceous species. Additionally, growth ofAndropogon scoparius seedling radicles was reduced 28–56% by pine needle extracts, 33% by pine bark extracts, and 67% by soil hydrolysate extracts.Andropogon seed germination was reduced 20–25% by pine needles and soil. Phytotoxins identified in various plant parts and associated soils were caffeic acid, chlorogenic acid, quercetin, and condensed tannins. Pine needle water and soil hydrolysate extracts were most inhibitory to the radicle growth of the test species. Thus it appears that the limited growth of the herbaceous stratum in the pine community may be accounted for, in part, by allelopathy. Such allelopathic interactions may have an adaptive ecological significance in various forest and other plant communities.     

A comparison of the effectiveness of predator odor and plant antifeedant in deterring small mammal feeding damage on lodgepole pine seedlings

The influence of mustelid (weasel) anal-gland compounds (semiochemicals) and a plant antifeedant (pinosylvin) on snowshoe hare (Lepus americanus) and meadow vole (Microtus pennsylvanicus) feeding damage was investigated. This study has shown conclusively that when applied to spring-planted lodgepole pine seedlings, pinosylvin is effective in significantly reducing feeding damage. Seedlings treated with pinosylvin suffered damage levels of 2.3% and 21.2% compared to the controls with damage levels of 24.5% and 41.0%. Weasel scent was found to reduce damage levels, but the reduction was not statistically significant in all blocks.     

The effects of chronic tannic acid intake on prairie vole (Microtus ochrogaster) reproduction

The hypothesis was tested that the reproductive performance of voles would be reduced when fed diets containing tannins either because of increased metabolic rates, decreased intake, or decreased digestive efficiency. We fed a ration containing 4% tannic acid (TA) (dry mass basis) to 24 pair of prairie voles (Microtus ochrogaster) and compared reproductive performance (litter size, birth weights, body mass of the young until weaning, and mass changes in the dams) to that of 24 pair of prairie vole fed a control ration. We also compared the intake rates, digestive efficiency, and metabolic rates [as measured by Vo₂ consumption (cm³/hr)] of dams and young fed both rations. Voles consuming 4% TA diets produced litters of similar size and mass as did voles fed the control ration. Furthermore, the mass of the young of dams fed the tannic acid ration were similar to the young of dams consuming the control ration through day 19 postpartum. However, dams consuming the tannic acid ration lost mass throughout lactation while the control dams maintained mass. Because the Vo₂ rates of both treated and control dams and litters were similar, we conclude increased metabolic costs were not the reason for the observed mass loss but, rather, reduced digestive efficiency, reduced intake of digestible dry mass, and apparent digestible nitrogen.