Charles T. Robbins

Role of Tannins in Defending Plants Against Ruminants: Reduction in Protein Availability

We tested the hypothesis that tannins defend plants against large herbivores by decreasing protein availability. Digestion trials were conducted with mule deer (Odo- coileus hemionus) and results from previous trials with white-tailed deer (O. virginianus), moose (Alces alces), caribou/reindeer (Rangifer tarandus), and elk (Cervus elaphus) were summarized to evaluate dietary factors affecting protein availability. The digestibility of plant protein in feeds with minimal tannins, such as grasses and agriculturally produced legumes and grains, was a highly predictable function of the total protein content and the amount of nondigestible, fiber-bound protein. Digestible protein in plants containing sig? nificant tannins was lower than predicted from regressions for low-tannin feeds. The re? duction in digestible protein was proportional to the protein-precipitating capacity of the plant tannins. Deciduous browse stems collected in winter had very low levels of protein- precipitating tannins and only a slightly lower protein availability than predicted. Tannins are not important in the defense of most deciduous tree and shrub stems consumed by these herbivores. Tannins in flowers and forb, tree, and shrub leaves markedly reduced protein availability. Tannins must be considered in understanding the defensive strategies of leaves and flowers. Voluntary intake of the high-phenolic forages was significantly re? duced below ingestion rates for grasses, legumes, and pelleted diets. It is hypothesized that soluble phenolics that do not inhibit digestion but are absorbed and reduce intake through their toxicity are more important in defending some plant parts against ruminants than are digestion-reducing tannins.

Role of tannins in defending plants against ruminants: reduction in dry matter digestion

Polyphenolic allelochemicals, such as tannins, are widely thought to reduce the digestibility of plants consumed by herbivores by binding to digestive enzymes and dietary proteins. While the apparent digestibility of protein and, therefore, cell solubles is reduced in mule deer (Odocoileus hemionus) and white-tailed deer (O. virginianus) consuming tanniferous forages, digestion of the plant cell wall is not reduced beyond that predicted from its content of lignin, cutin, and silica. The lack of a tannin effect on cell wall digestion in deer is in contrast to studies with domestic sheep and numerous in vitro studies. Herbivores adapted to consume tanniferous forages may defend against such allelochemicals by producing salivary proteins that bind tannins in a highly specific manner. These tannin-salivary protein complexes would reduce apparent digestibilities of protein and cell solubles and, if completely effective, would not reduce cell wall digestion. The occurrence of such proteins in ruminants is reported here for the first time. The saliva composition of mule deer (a mixed feeder that commonly consumes browse) and domestic cattle and sheep (predominant grazers) are compared, and the higher potential of the deer saliva to neutralize tannins is related to their feeding habits. Salivary proteins that preferentially bind tannins may minimize fecal nitrogen losses by maximizing the efficiency of tannin-binding per unit of protein and may reduce the absorption of hydrolyzable tannins and the potential for tannin toxicity.

The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds

We tested the competing hypotheses that (1) nitrogen discrimination in mammals and birds increases with dietary nitrogen concentration or decreasing C:N ratios and, therefore, discrimination will increase with trophic level as carnivores ingest more protein than herbivores and omnivores or (2) nitrogen discrimination increases as dietary protein quality decreases and, therefore, discrimination will decrease with trophic level as carnivores ingest higher quality protein than do herbivores. Discrimination factors were summarized for five major diet groupings and 21 different species of birds and mammals. Discrimination did not differ between mammals and birds and decreased as protein quality (expressed as biological value) increased with trophic level (i.e., herbivores to carnivores). Relationships between discrimination factors and dietary nitrogen concentration or C:N ratios were either the opposite of what was hypothesized or non-significant. Dietary protein quality accounted for 72% of the variation in discrimination factors across diet groupings. We concluded that protein quality established the baseline for discrimination between dietary groupings, while other variables, such as dietary protein intake relative to animal requirements, created within-group variation. We caution about the care needed in developing studies to understand variation in discrimination and subsequently applying those discrimination factors to estimate assimilated diets of wild animals.

Variation in Mammalian Physiological Responses to a Condensed Tannin and Its Ecological Implications

Mule deer ( Odocoileus hemionus ), domestic sheep ( Ovis aries ), and American black bears ( Ursus americanus ) were fed quebracho ( Schinopsis sp.) tannin to determine the contribution of salivary proteins to nitrogen- and fiber-digestive efficiencies and tannin metabolism. These values were compared to previously published values for laboratory rats ( Rattus rattus ) and prairie voles ( Microtus ochrogaster ). Mule deer, black bears, and laboratory rats consuming this condensed tannin produced tannin-binding salivary proteins that reduced fecal-nitrogen losses per unit of ingested tannin and reduced tannin metabolism relative to domestic sheep and prairie voles. Digestibility of the plant fiber was reduced significantly by tannins in domestic sheep, but not in mule deer. Although virtually all ingested tannin (98.3 ± 5.0%) was recovered in feces of mule deer and black bears, ca. 25% was not recovered in feces of domestic sheep and presumably was metabolized. The defensive role of tannins as digestion inhibitors or toxins is dependent upon the molecular characteristics of the tannin interacting with the physiological capability of the animal. Results from one plant-mammal interaction cannot be used to interpret others without an understanding of the characteristics of the tannins and the physiology, ecology, and evolution of the animal.

Tannin-binding proteins in saliva of deer and their absence in saliva of sheep and cattle.

A method has been developed for detecting tannin-binding proteins in the saliva of herbivores. The method is simple and requires only small quantities of crude saliva. The saliva of deer, a browsing ruminant, has been compared to that of domestic sheep and cow, which are grazing ruminants. The browser, which normally ingests dietary tannin, produces tannin-binding proteins, while the grazers do not produce such proteins. The tannin-binding protein from deer saliva is a small glycoprotein containing large amounts of proline, glycine, and glutamate/glutamine. The protein is not closely related to the proline-rich salivary proteins found in rats and other nonruminant mammals.

Nitrogen and carbon isotope fractionation between mothers, neonates, and nursing offspring

Stable isotope signatures of lactating females and their nursing offspring were measured on 11 species, including herbivores, carnivores, hibernators, and non-hibernators. We hypothesized that: (1) nursing offspring would have stable isotope signatures that were a trophic level higher than their mothers, and (2) this pattern would be species-independent. The plasma of adult females had a δ15N enrichment over their diets of 4.1±0.7‰, but offspring plasma had a mean δ15N enrichment over maternal plasma of 0.9±0.8‰ and no C enrichment (0.0±0.6‰). The trophic level enrichment did not occur between mother and offspring because milk was depleted in both δ15N (1.0±0.5‰) and δ13C (2.1±0.9‰) relative to maternal plasma. Milk to offspring plasma enrichment was relatively small (δ15N enrichment of 1.9±0.7‰ and δ13C enrichment of 1.9±0.8‰) compared to the trophic level enrichment between the adults and their diets. While some species did have significant differences between the isotope signatures of mother and offspring, the differences were not related to whether they were hibernators or non-hibernators, carnivores or herbivores. Investigators wanting to use stable isotopes to quantify weaning or other lactation processes or diets of predators when both adults and nursing offspring are consumed must first establish the parameters that apply to a particular species/environment/diet combination.

CONSTRAINTS ON FRUGIVORY BY BEARS

Bears consuming wild fruits for fall energy accumulation are constrained by several factors, including intake rate, the physiological capacity of the gastrointestinal tract, and the metabolic efficiency of gain in body mass. We measured these relationships through foraging and feeding trials using captive and wild black bears (Ursus americanus) and grizzly bears (Ursus arctos). Four fruit types covering a range of sizes and clustering were offered to captive bears to determine the effect of density, size, and presentation on intake rate. Intake rate (in grams per minute) and bite rates (in bites per minute) increased cur- vilinearly with increasing fruit density in singly spaced fruits. Maximum intakes ranged from 30 g/min for 0.5-g berries to >200 g/min for 4.2-g fruits. The highest bite rates were obtained during the initial encounter with each patch as bears consumed all visually apparent fruits on the surface. Bite rates quickly dropped by 15-20% as foraging continued within the patch. Maximum bite rates were not depressed until initial fruit density fell to 100 kg. We concluded that large bears, such as grizzlies, must depend on plants that permit large bite sizes or high bite rates through fruit clustering and bush configuration that reduce leaf-to-fruit ratios.

Role of brown bears (Ursus arctos) in the flow of marine nitrogen into a terrestrial ecosystem

Abstract We quantified the amount, spatial distribution, and importance of salmon (Oncorhynchus spp.)-derived nitrogen (N) by brown bears (Ursus arctos) on the Kenai Peninsula, Alaska. We tested and confirmed the hypothesis that the stable isotope signature (δ15N) of N in foliage of white spruce (Picea glauca) was inversely proportional to the distance from salmon-spawning streams (r=–0.99 and P<0.05 in two separate watersheds). Locations of radio-collared brown bears, relative to their distance from a stream, were highly correlated with δ15N depletion of foliage across the same gradient (r=–0.98 and –0.96 and P<0.05 in the same two separate watersheds). Mean rates of redistribution of salmon-derived N by adult female brown bears were 37.2±2.9 kg/year per bear (range 23.1–56.3), of which 96% (35.7±2.7 kg/year per bear) was excreted in urine, 3% (1.1±0.1 kg/year per bear) was excreted in feces, and <1% (0.3± 0.1 kg/year per bear) was retained in the body. On an area basis, salmon-N redistribution rates were as high as 5.1±0.7 mg/m2 per year per bear within 500 m of the stream but dropped off greatly with increasing distance. We estimated that 15.5–17.8% of the total N in spruce foliage within 500 m of the stream was derived from salmon. Of that, bears had distributed 83–84%. Thus, brown bears can be an important vector of salmon-derived N into riparian ecosystems, but their effects are highly variable spatially and a function of bear density.

Food Intake and Foraging Energetics of Elk and Mule Deer

The energetic cost of grazing was measured using indirect calorimetry with a tracheotomized elk (Cervus elaphus nelsoni). The cost of eating herbaceous forage averaged 0.32 kcal/kg body weight/ hour, an energetic increment of 26% over standing costs. Forage intake was quantified using esophageal fistulated elk and mule deer (Odocoileus hemionus hemionus). Dry matter consumption rate and mean bite size increased curvilinearly as functions of forage biomass for both species. Asymptotic grass intake rates were 2.22 and 14.04 g dry matter/minute for deer and elk, respectively. Consumption rate and bite size were greater in shrub-forb communities than on grass pastures of comparable biomass. Biting rate ranged from about 15 to 60 bites/minute and was inversely related to bite size. Rate of travel during foraging decreased exponentially with increasing forage availability. A computer model was constructed to evaluate the interaction of time and energy constraints on foraging ungulates. The effects of variation in forage quality, forage abundance, and snow cover on the ability of animals to meet daily energy requirements are discussed. J. WILDL. MANAGE. 48(4): 1285-1301 Foraging is the dominant activity of free-ranging ungulates. Wild ungulates typically devote 40-60% of each day to finding and consuming food (Craighead et al. 1973; White et al. 1975; Schwartz 1977; Belovsky and Jordan 1978; Collins et al. 1978; Owen-Smith 1979, 1982; Gates 1980; Hanley 1982). The energetic cost of these activities represents an important component of the animals energy budget (Young 1966, Osuji 1974, Chappel and Hudson 1978). However, in spite of the significance of foraging in the life strategy of wild ungulates, relatively little is known about the energetics of this behavior. The literature is replete with food habits information, but such observations are of limited value without an understanding of the efficiency with which the animal harvests the food resource and extracts energy from its environment. This study was undertaken to quantify the cost-benefit functions of foraging by captive elk and mule deer relative to food availability. Specific objectives were to: (1) determine forage intake rate as a function of the biomass of acceptable food items; (2) determine the relationship of intake rate to mean bite size and biting rate to better understand the behavioral adjustments that regulate energy intake; (3) quantify locomotion rate during foraging relative to food availability; (4) measure the energetic cost of eating as distinct from expenditures for standing and locomotion; and (5) model the effects of variation in forage quality and abundance on the ability of free-ranging cervids to meet daily energy requirements. This project was funded by the U.S. For. Serv. and Washington State Univ. We thank K. L. Parker for support and assistance in data collection and M. A. Reisenauer for the care of experimental animals. L. D. Bryant and J. W. Thomas provided facilities at the U.S. For. Serv. Range and Wildl. Habitat Lab. in La Grande, Oregon. J. Wildl. Manage. 48(4):1984 1285 This content downloaded from 157.55.39.29 on Tue, 12 Apr 2016 10:03:48 UTC All use subject to http://about.jstor.org/terms 1286 INTAKE AND FORAGING ENERGETICS OF ELK AND DEER * Wickstrom et al. METHODS AND MATERIALS Elk calves and mule deer fawns were bottle-raised and habituated to the experimental protocol. Training included acceptance of gentle restraint with a head halter, manipulation of the esophageal and tracheal cannulae, and transport in a trail-

Implications of soluble tannin-protein complexes for tannin analysis and plant defense mechanisms

Factors which establish whether tannin and protein interact to form soluble complexes or precipitates were identified. The ratio of tannin to protein in the reaction mixture influenced solubility of the tannin-protein complexes. At protein-to-tannin ratios larger than the optimum ratio, or equivalence point, soluble tannin-protein complexes apparently formed instead of insoluble complexes. Several other factors influenced the amount of protein precipitated by tannin-containing plant extracts, including the length of the reaction time and the conditions of the tannin extraction. The analytical and ecological significances of soluble complexes were considered. A titration method which allows simultaneous determination of the equivalence point and assessment of the protein-precipitating capacity of any plant extract was developed. It was postulated that in vivo, tannin and protein may not only form insoluble complexes with antinutritional effects, but may also form soluble complexes which have unknown metabolic effects.