William B. Collins

Summer dietary nitrogen availability as a potential bottom‐up constraint on moose in south‐central Alaska

Recent studies suggest that the growth and fecundity of northern ungulates may be coupled to their summer nutrition. Here, we compare summer dietary nitrogen availability of the five major browse plants (comprising approximately 79% of the diet) of moose (Alces alces) in Denali National Park and Nelchina Basin, Alaska, USA. In recent years the productivity of Denali moose has been significantly higher than that of Nelchina moose, prompting this comparison. We examined the phenological progression of leaf nitrogen concentration, tannin-protein precipitation capacity, and digestible protein over three summers in both regions. We then modeled the potential nutritional consequences for a cow moose consuming representative diets on each range, predicting both net protein intake (NPI) and lean body mass accumulation each year. We found that leaf nitrogen and digestible protein decreased, while tannin-protein precipitation capacity increased throughout the summer for all forages. There was 23% more digestible protein in Denali leaves than Nelchina leaves on average, and this difference was significant in all three years. Tannins accounted for a large (mean = 46%) reduction in protein availability, suggesting a key role of these secondary compounds in the nitrogen balance of moose in these regions. Finally, our NPI model predicted that Denali cows were in positive protein balance 17 days longer than Nelchina cows and accumulated 18 kg more lean body mass over the summer, on average. We conclude that summer dietary nitrogen availability may act as a nutritional constraint on moose and suggest that more emphasis be placed on elucidating its role in population dynamics and conservation of northern ungulates.

Differential passage of fluids and different-sized particles in fistulated oxen (Bos primigenius f. taurus), muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces): Rumen particle size discrimination is independent from contents stratification

Ruminant species differ in the degree that their rumen contents are stratified but are similar insofar that only very fine particles are passed from the forestomach to the lower digestive tract. We investigated the passage kinetics of fluid and particle markers (2, 10 and 20 mm) in fistulated cattle (Bos primigenius f. taurus), muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces) on different diets. The distribution of dry matter in the rumen and the viscosity of rumen fluids suggested that the rumen contents were more stratified in muskoxen than moose. Correspondingly, as in previous studies, the species differed in the ratio of mean retention times of small particles to fluids in the reticulorumen, which was highest in cattle (2.03) and muskoxen (1.97-1.98), intermediate in reindeer (1.70) and lowest in moose (0.98-1.29). However, the ratio of large to small particle retention did not differ between the species, indicating similarity in the efficiency of the particle sorting mechanism. Passage kinetics of the two largest particle classes did not differ, indicating that particle retention is not a continuous function of particle size but rather threshold-dependent. Overall, the results suggest that fluid flow through the forestomach differs between ruminant species. A lower relative fluid passage, such as in moose, might limit species to a browse-based dietary niche, whereas a higher relative fluid passage broadens the dietary niche options and facilitates the inclusion of, or specialization on, grass. The function of fluid flow in the ruminant forestomach should be further investigated.

Simulating the influences of various fire regimes on caribou winter habitat

Caribou are an integral component of high-latitude ecosystems and represent a major subsistence food source for many northern people. The availability and quality of winter habitat is critical to sustain these caribou populations. Caribou commonly use older spruce woodlands with adequate terrestrial lichen, a preferred winter forage, in the understory. Changes in climate and fire regime pose a significant threat to the long-term sustainability of this important winter habitat. Computer simulations performed with a spatially explicit vegetation succession model (ALFRESCO) indicate that changes in the frequency and extent of fire in interior Alaska may substantially impact the abundance and quality of winter habitat for caribou. We modeled four different fire scenarios and tracked the frequency, extent, and spatial distribution of the simulated fires and associated changes to vegetation composition and distribution. Our results suggest that shorter fire frequencies (i.e., less time between recurring fires) on the winter range of the Nelchina caribou herd in eastern interior Alaska will result in large decreases of available winter habitat, relative to that currently available, in both the short and long term. A 30% shortening of the fire frequency resulted in a 3.5-fold increase in the area burned annually and an associated 41% decrease in the amount of spruce-lichen forest found on the landscape. More importantly, simulations with more frequent fires produced a relatively immature forest age structure, compared to that which currently exists, with few stands older than 100 years. This age structure is at the lower limits of stand age classes preferred by caribou from the Nelchina herd. Projected changes in fire regime due to climate warming and/or additional prescribed burning could substantially alter the winter habitat of caribou in interior Alaska and lead to changes in winter range use and/or population dynamics.

New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11

Ruminants have co-evolved with their gastrointestinal microbial communities that digest plant materials to provide energy for the host. Some arctic and boreal ruminants have already shown to be vulnerable to dietary shifts caused by changing climate, yet we know little about the metabolic capacity of the ruminant microbiome in these animals. Here, we use meta-omics approaches to sample rumen fluid microbial communities from Alaskan moose foraging along a seasonal lignocellulose gradient. Winter diets with increased hemicellulose and lignin strongly enriched for BS11, a Bacteroidetes family lacking cultivated or genomically sampled representatives. We show that BS11 are cosmopolitan host-associated bacteria prevalent in gastrointestinal tracts of ruminants and other mammals. Metagenomic reconstruction yielded the first four BS11 genomes; phylogenetically resolving two genera within this previously taxonomically undefined family. Genome-enabled metabolic analyses uncovered multiple pathways for fermenting hemicellulose monomeric sugars to short-chain fatty acids (SCFA), metabolites vital for ruminant energy. Active hemicellulosic sugar fermentation and SCFA production was validated by shotgun proteomics and rumen metabolites, illuminating the role BS11 have in carbon transformations within the rumen. Our results also highlight the currently unknown metabolic potential residing in the rumen that may be vital for sustaining host energy in response to a changing vegetative environment.

Stochastic and Compensatory Effects Limit Persistence of Variation in Body Mass of Young Caribou

Abstract Nutritional restriction during growth can have short- and long-term effects on fitness; however, animals inhabiting uncertain environments may exhibit adaptations to cope with variation in food availability. We examined changes in body mass in free-ranging female caribou (Rangifer tarandus) by measuring mass at birth and at 4, 11, and 16 months of age to evaluate the relative importance of seasonal nutrition to growth, the persistence of cohort-specific variation in body mass through time, and compensatory growth of individuals. Relative mean body mass of cohorts did not persist through time. Compensatory growth of smaller individuals was not observed in summer; however, small calves exhibited more positive change in body mass than did large calves. Compensation occurred during periods of nutritional restriction (winter) rather than during periods of rapid growth (summer) thus differing from the conventional view of compensatory growth.

A Modified Method for Determining Tannin–Protein Precipitation Capacity Using Accelerated Solvent Extraction (ASE) and Microplate Gel Filtration

The protein precipitation assay used by Robbins et al., (1987) Ecology 68:98–107 has been shown to predict successfully the reduction in protein availability to some ruminants due to tannins. The procedure, however, is expensive and laborious, which limits its utility, especially for quantitative ecological or nutritional applications where large numbers of assays may be required. We have modified the method to decrease its cost and increase laboratory efficiency by: (1) automating the extraction by using Accelerated Solvent Extraction (ASE); and (2) by scaling and automating the precipitation reaction, chromatography, and spectrometry with microplate gel filtration and an automated UV–VIS microplate spectrometer. ASE extraction is shown to be as effective at extracting tannins as the hot methanol technique. Additionally, the microplate assay is sensitive and precise. We show that the results from the new technique correspond in a nearly 1:1 relationship to the results of the previous technique. Hence, this method could reliably replace the older method with no loss in relevance to herbivore protein digestion. Moreover, the ASE extraction technique should be applicable to other tannin–protein precipitation assays and possibly other phenolic assays.

Fire, Grazing History, Lichen Abundance, and Winter Distribution of Caribou in Alaska's Taiga

ABSTRACT In the early 1990s the Nelchina Caribou (Rangifer tarandus) Herd (NCH) began a dramatic shift to its current winter range, migrating at least an additional 100 km beyond its historic range. We evaluated the impacts of fire and grazing history on lichen abundance and subsequent use and distribution by the NCH. Historic (prior to 1990) and current (2002) winter ranges of the NCH had similar vascular vegetation, lichen cover (P = 0.491), and fire histories (P = 0.535), but the former range had significantly less forage lichen biomass as a result of grazing by caribou. Biomass of forage lichens was twice as great overall (P = 0.031) and 4 times greater in caribou selected sites on the current range than in the historic range, greatly increasing availability to caribou. Caribou on the current range selected for stands with >20% lichen cover (P < 0.001), greater than 1,250 kg/ha (P < 0.001) forage lichen biomass and stands older than 80 yr postfire (P < 0.001). After fires, forage lichen cover and biomass seldom recovered sufficiently to attract caribou grazing until after ≥60 yr, and, as a group, primary forage lichen species did not reach maximum abundance until 180 yr postfire. Recovery following overgrazing can occur much more quickly because lichen cover, albeit mostly fragments, and organic substrates remain present. Our results provide benchmarks for wildlife managers assessing condition of caribou winter range and predicting effects of fires on lichen abundance and caribou distribution. Of our measurements of cover and biomass by species, densities and heights of trees, elevation, slope and aspect, only percentage cover by Cladonia amaurocraea, Cladina rangiferina, Flavocetraria cuculata, and lowbush cranberry (Vaccinium vitis-idaea) were necessary for predicting caribou use of winter range.

White sweetclover (Melilotus albus) and narrowleaf hawksbeard (Crepis tectorum) seed germination after passing through moose.

Abstract White sweetclover and narrowleaf hawksbeard are nonindigenous invasive plant species in Alaska that are rapidly spreading, including into areas that are otherwise free of nonindigenous plants. There has been concern that native moose could be dispersing germinable seed from these plants after ingestion. To address this concern, a study was conducted involving tame moose at the University of Alaska Fairbanks Agriculture and Forestry Experiment Station, Matanuska Experiment Farm, Palmer, AK. Objectives were to determine if seeds from these two plant species could survive mastication and digestive passage through moose, whether this passage impacted seed germination, and whether seed passage rates were the same as similar sized Cr-mordanted fiber. In this study, narrowleaf hawksbeard seed rarely survived mastication and digestion with only five seedlings recovered from 42,000 germinable seed fed to the moose. About 16% of germinable white sweetclover seed (3,595 of 22,000) fed to the moose produced seedlings. Most of the sweetclover seedlings came from feces produced 2 and 3 d after feeding. In two moose, sweetclover seedlings were grown from fecal material that was passed 11 d after feeding, raising the possibility that seeds could be transported long distances after ingestion. Cr-mordanted fiber passage did not closely follow seedling producing seed, possibly because time in the rumen might reduce seed germination. Once roadsides in Alaska become infested with white sweetclover, moose can then serve as a transport vector of these weeds into river channels and floodplains, which are distant from roads. This information will impact white sweetclover management programs and alert land managers to the potential for other instances of wildlife-mediated seed dispersal. Nomenclature: Narrowleaf hawksbeard, Crepis tectorum L.; white sweetclover, Melilotus albus Desr.; moose, Alces alces L.

Relationship of dietary browse to intake in captive muskoxen.

The effect of dietary browse (Salix bebbiana Sarg.) on intake and activity of muskoxen (Ovibos moschatus Zimmermann) pastured in south-central Alaska was compared to animals on grass pasture only. In previous work, intake increased in penned animals fed increasing browse: hay rations, which presumably allowed for increased weight gain and wool fiber (qiviut) growth. Eight mature steers were divided into 2 treatments: 8 hours daily ad libitum access to browse plus pasture grass (Bromus inermis Leyss., Poa pratensis L. mix) or pasture grass only. Animals were placed in adaptation enclosures 10 days before each trial. Bundles of browse were tied to perimeter fences. Trials were conducted 3 times during the 1992 growing season. For the trials, animals of like treatment were placed in each of four 0.33 ha trial enclosures for 8 hours, every other day, for 6 days (3 trial days). Activity budgets were calculated using scan sampling. Hand-harvested simulated bites were weighed to determine bite size, an bite rate was calculated using focal sampling techniques. Intake was calculated as a function of bite size, bite rate, and time spent foraging. Intake was greater (P = 0.064) for animals with access to browse. Digestive physiology of mukoxen may have favored higher intake of a mixed grass-browse diet over grass alone. Previous data suggest that elevated intake increases weight gain and qiviut growth.

Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem

Because of their agricultural value, there is a great body of research dedicated to understanding the microorganisms responsible for rumen carbon degradation. However, we lack a holistic view of the microbial food web responsible for carbon processing in this ecosystem. Here, we sampled rumen-fistulated moose, allowing access to rumen microbial communities actively degrading woody plant biomass in real time. We resolved 1,193 viral contigs and 77 unique, near-complete microbial metagenome-assembled genomes, many of which lacked previous metabolic insights. Plant-derived metabolites were measured with NMR and carbohydrate microarrays to quantify the carbon nutrient landscape. Network analyses directly linked measured metabolites to expressed proteins from these unique metagenome-assembled genomes, revealing a genome-resolved three-tiered carbohydrate-fuelled trophic system. This provided a glimpse into microbial specialization into functional guilds defined by specific metabolites. To validate our proteomic inferences, the catalytic activity of a polysaccharide utilization locus from a highly connected metabolic hub genome was confirmed using heterologous gene expression. Viral detected proteins and linkages to microbial hosts demonstrated that phage are active controllers of rumen ecosystem function. Our findings elucidate the microbial and viral members, as well as their metabolic interdependencies, that support in situ carbon degradation in the rumen ecosystem.A combination of proteomics, metagenome-assembled genomes and heterologous gene expression experiments reveals a trophic system for carbon utilization in the moose rumen microbiome and provides insights into phage dynamics in this ecosystem.