complete review of bison research · bison bonasus anthrax growth and development bison in parks...

Complete Review of Bison Research

For the National Bison Association

May 7, 2018

Gerald B. Huntington, Ph.D.

Professor Emeritus

Department of Animal Science

North Carolina State University

Raleigh, NC 27695

[email protected]

mailto:[email protected]

Executive Summary

I began the project with broad literature searches, to cast a wide net. The key words, “bison” and “buffalo”

turned out to be just that; the (inter)net brought in information about cities in New York, all kinds of animals

from around the world, a productive researcher in health medicine name Bison, and insight into nuclear

physics, that among other things has bison particles. Subsequent cross-searches between databases, and

independent key work searches on authors and content of garnered publications created a database of

approximately 2,000 entries, with high confidence that I haven’t missed something significant.

I used the software EndNote to organize and categorize the database. Information or publications that were

not available to me via on-line, internet searches were obtained by interlibrary loan and personal visits to the

libraries of North Carolina State University. Dr. Murray Woodbury and Vern Anderson provided material from

their personal digital libraries.

Table One. EndNote Groups and sub-Groups

Group Sub groups Group Sub groups

Physiology Management

Anatomy Bison in parks

Blood chemistry Management practices

Body and tissue composition General overview

Digestive tract General overview

Growth and Development Theses and Dissertations

Homeostasis and metabolism Reproduction

Genetics Reproduction female

Genetics and growth Reproduction male

Genetics general background Reproductive behavior

Genetics phylogeny Feeding and Nutrition

Molecular genetics Digestion and metabolism

Energy, protein and minerals

Diseases and health management General feeding and nutrition

Anaplasma Intake, digestion and metabolism

Anthrax Grazing behavior and selection

Brucellosis Miscellaneous and other

Diseases unclassified Anthropology, archaeology and phylogeny

General disease reviews Bison bonasus

Malignant Catarrhal Fever Grasslands

Mycobacterium bovis Meat and other products

Mycoplasma Other

Parasites Behaviour

Paratuberculosis/ Johne’s disease

Bison and other animals

Pasturella Management practices

Pasturella

Viral diseases

The EndNote database has the advantages of popularity, versatility, and availability. I believe free versions can

be downloaded and operated on any computer connected to the internet. The EndNote file is compatible with

a spectrum of other software packages, including Microsoft Word and Excel. All entries have some keywords to

allow users to search on topics of interest. I gathered pdf copies of practically all the entries, allowing quick

access to the publications. The database is transferable by internet, including pdf files. The EndNote database

is categorized in the several ‘groups’, Endnote’s way of facilitating searches, and allowing individual

publications to be classified in multiple categories. I also created an internal classification that should allow

broad categorical searches on any platform.

Table Two. Categories within the dataset

Anatomy Diseases Grasslands Anthropology, archaeology and Phylogeny

Anaplasma Grazing behavior selection

Bison bonasus Anthrax Growth and development Bison in parks Brucellosis Homeostasis and metabolism Bison and other animals Diseases unclassified Management Blood chemistry General disease reviews Meat and other products Body tissue composition Reproduction female Digestive tract Malignant Catarrhal Fever Reproduction male Feedstuffs and nutrition Mycobacterium bovis Reproduction behavior General behavior Mycoplasma Theses and dissertations General overview Parasites genetics Paratuberculosis/ Johne’s

disease

Pasteurella Viral diseases

Almost all entries have specific information on author, title, source (year, volume, issue, pages), and a pdf file

copy. Transcription of the EndNote file to other software with similar goals and features should retain all of

this information. I can provide pdf copies of publications separately, identified by author, year, and source (not

titles).

The bulk of published work in the general topic of bison falls into 4 categories: archaeology, anthropology;

diseases and health management; behavior, including social, grazing, reproductive behavior; and publications

from industry magazines over the past 30 years. These categories contain recent publications and application

of state-of-the-art research tools and technologies. Categories with lesser activity include: physiology (other

than reproductive); genetics; growth and development; work that focuses on European bison; meat and other

bison products; and nutrition. I allowed the sources of information to guide and shape this report, with the

following exceptions. First, I decided not to explore archaeology and anthropology in detail. Secondly, I have

omitted description and discussion of work done with European bison, except where I thought it was relevant

to the subject at hand, mostly in the area of diseases. Third, although I perceive management of private herds

to be a topic of high interest, I decided that interested parties could and should go to the information in the

industry magazines for specific topics rather than simply copying them into a final report. Further, most of that

information was published over 15 years ago, and may or may not be relevant today.

The final report is written in the form of a scientific article, with references and literature cited at the end of

each section. I have summarized and presented information in tables and figures to provide analysis, and

interpretation. I made a conscious effort to avoid jargon, and to provide explanations or descriptions that

would allow a non-scientist, a.k.a. a normal person, to read with some comprehension.

Key take-home points from my perspective are 1) we have a good understanding of the basic reproductive,

digestive, and growth physiology, metabolism, and behavior of bison; 2) we have profited, and will continue to

profit, from application of molecular biological techniques to improve understanding and application of the

genetic background and future of bison today; 3) in terms of breeding and feeding, they are similar enough to

cattle that application of concepts and techniques from cattle by in large will work, or at least will not cause

damage. Advances in understanding nutrition and metabolic systems will come from new and innovative ways

to obtain samples and metabolic information from bison without causing artifacts from stress caused by

interaction with humans. Statistical confidence in research results will come from well-designed, replicated

experiments with adequate animal numbers.

Gerald Huntington

Table of Contents Page

I. Intake, digestion, metabolism, nutrition 1

Grazing behavior and selection 1 Digestion and metabolism 5 Gut anatomy and physiology 5 Microbiology 5 Summary of digestion studies 8 Intake and weight gain in feedlot studies 9 Blood chemistry 11 Literature cited 13 II. Growth and development 18

Fetal growth 18 Growth curves 18 Growth information from domestic bison 19 Indirect measures of growth 20 Literature cited 21 III. Reproduction 23

Males 23 Females 25 Reproductive behavior 27 Literature cited 29 IV. Genetics 35

Advances in molecular genetics and genomics 35 Introgression of cattle genes 37 Genetic diversity 37 Literature cited 38 V. Diseases 44

Anthrax 44 Brucellosis 44 Paratuberculosis, or Johne’s disease 45 Mycoplasma 45 Tuberculosis 45 Malignant catarrhal fever 46 Parasitic diseases 46 Other viral diseases 47 Other diseases and treatment 47 Literature cited 48 VI. Grasslands 58

Literature cited 61 VII. Meat and other products 65

Literature cited 66 VIII. Management 67

Literature cited 68 IX. Theses and dissertations 69

Literature cited 69 X. Anthropology, archaeology, phylogeny 70

XI. Bison in parks 70

XII. Bison Bonasus 70

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I. Intake, digestion, metabolism, nutrition

Summary

Available biomass and nutritive value, not capacity to eat, will limit acquisition of needed nutrition by grazing bison. The two main approaches, quantity-driven and quality-driven selection, are not mutually exclusive, and likely interact in response to other factors, like landscape, weather, predators, season of year, social interactions, and previous experience

Kansas researchers interpret results of their studies of rumen microbiology to say that any putative advantage in fiber fermentation capacity in bison vs cattle does not appear to be due to ruminal microbial populations. An elegant series of experiments in Canada show the mixtures of rumen fluid from bison and cattle have superior fermentative capacity than either rumen fluid source by itself.

In vivo digestion trials with bison have been interpreted to show that bison have greater digestibility coefficients than cattle, but the comparison is compromised by relatively low intake of the animals during sample collection. Feedlot bison show the expected depression in intake and weight gain during winter months. Feedlot bison gain about 750 grams per day, and convert feed to gain at 9 % efficiency.

Although it is not emphasized in this review, the majority of studies on bison blood chemistry had explicit or implicit comparison to similar values, conditions, and situations in domestic cattle. By in large, the data show that values and responses for the two species are similar. An exception is serum glucose concentrations that may be unphysiologically high for bison, ostensibly in response to stress anxiety in the bison at or before sampling time.

Introduction

These topics seemed to link for me, so I have included them in one section. Most of the grazing behavior studies were done with conservation herds, but I’m assuming that all grazing bison have similar traits. The largest single contribution to this general topic has been in the area of microbiology and rumen function, especially the recent Canadian work with rumen fluid from bison. I have compiled summary tables and figures where I could to provide reference information for future work.

Grazing behavior and selection

The data of Hudson and Frank (1987), Bergman et al. (2000), Bergman et al. (2001) and Fortin et al. (2002) show how intake per unit of time increases at a decreasing rate as biomass, available forage dry matter (DM) on offer increases.

The calcuations are based on short-term (1 to 5 min) grazing episodes, and represent the phyiological maximum, the fastest a bison can eat. Yearling bison in Bergman et al. (2001), about 220 kg body weight (BW), consumed DM equal to 2.5% of (BW) and minimized daily foraging time (150 min) on a patch providing at least 2790 kg DM/ha. A mature cow, 500 kg, consuming DM at the same proportion of BW would need 185 min at her maximal rate to ingest 12.5 kg of DM (Hudson and Frank, 1987). This time is much less than the 8 to 12 hr of grazing time observed by Hudson and Frank, indicating ample time opportunity. Similary, yearling bison grazed seeded pastures (2775 kg DM/ha), from 6.5 to 9.5 hr, far above the minimal 150 min (Rutley and Hudson, 2001). The model of Belovsky (1986) predicts that a mature adult (636 kg) would graze at 64.5 g/min, thereby needing 197 min to consume DM equal to 2% of BW. These examples indicate that bison likely do not eat as fast as they can all the time; the lines in Figure 1. show that half of maximal capacity is reached between 800 and 1400 kg DM/ha.

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In the studies cited above the researchers recorded data on bite mass and bite rate, then calcuated mass/min. Bite mass and bite rate are inversely related (Hudson and Frank, 1987), forage biomass and maturity (as the growing season proceeds) are directly related, eating rate and increased digestibility and energy content are directly related, but nutritive value and biomass/digestibilty are inversely related; for example in vitro digestibility decreased from about 70 to 60 % of DM from June through August as biomass increased from 500 to at least 2500 kg/ha, and maximal eating rate increased as depicted in Figure 1. (Bergman et al., 2001), all in concert to maintain, or perhaps increase, the daily nutrient supply, as long as the bison’s physical limit to eat (gut fill) is not in play. Digestible DM intake at low biomass in the example above was 3.85 kg/d; the bison would need to eat about 1 kg more DM daily at the end of August to supply the same amount of digestible DM, or eat at a maximal 55 g DM/min for another 18 min. Table 1 shows calculations for relatively low forage biomass with digestibility constant.

Gut fill limitation may require some time for digestion to make room for more forage. One can conclude from this scenario that available biomass and nutritive value, not capacity to eat, will limit acquisition of needed nutrition by grazing bison.

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0 1000 2000 3000 4000 5000 6000 7000 8000 9000 10000

Figure 1. Eating rate, g/min vs. biomass, kg/ha

Bergman et al., 2000 Hudson and Frank, 1987

Fortin et al., 2002 summer Fortin et al., 2002 winter

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Table 1. Effects of intake and biomass on grazing time and space

Biomass, kg M/ha

Gut fill, kg/d

Area grazed, m2

hours to gut fill

Gut fill, kg/d

Area grazed, m2

hours to gut fill

100 12.5 1250 27.1 10 1000 21.7

200 12.5 625 15.1 10 500 12.1

300 12.5 417 11.1 10 333 8.9

400 12.5 313 9.1 10 250 7.3

500 12.5 250 7.9 10 200 6.3

600 12.5 208 7.1 10 167 5.7

700 12.5 179 6.5 10 143 5.2

800 12.5 156 6.1 10 125 4.9

900 12.5 139 5.8 10 111 4.6

1000 12.5 125 5.5 10 100 4.4

Hours to gut fill calculated with equation from (Hudson and Frank, 1987).

Figure 2 arguably oversimplifies a complicated process that make bison graze as they do, but it does cover major points of this review. Situations 3 and 4 are addressed in Figure 1; There may or may not be enough time in day based on availability especially at 200 kg DM/ha or less. Larter and Gates (1991) contend that forage availability is the main factor in habitat selection. While effect of negative factors, like alkaloid content, and positive factors, like leafiness and nutritive value (with N content as a popular marker for quality), basically bison, like other grazers, select for amount, not quality (Reynolds, 1978; Waggoner and Hinkes, 1986; Wallace et al., 1995; Babin et al., 2011; Merkle et al., 2014; Merkle et al., 2015; Merkle et al., 2016; Zielke, 2017). Fecal seed profiles indicate a wide range of non-graminoid plants are consumed (Rosas et al., 2008). Others contend that factors like sward plant composition and/or nutritive value play a role in selection (Figure 3).

Figure 2. Rubric to evaluated foraging decisions (adapted from Fortin et al., 2002)

Daily intake not limited by digestive constraints

Daily intake limited by digestive constraints

Daily intake not limited by biomass availability Foraging situation I Foraging situation III

Daily intake limited by biomass availability Foraging situation II Foraging situation IV

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While Figure 3 shows proportions of biomass on offer and consumed, it does not show biomass available, which may affect selection; reported values for available biomass ranged from 1440 to 1800 kg DM/ha ((Plumb and Dodd, 1993; Abaturov et al., 2017); no data from Peden (1976)). The three studies show that bison select from biomass available, and, at least in a prairie habitat, show preference for warm-season (C4) grasses. They consume other plants, varying with prevalence in the sward and time of year. Canadian bison don’t prefer C4 grasses, because by in large, they are not available; Again, in response to biomass availability and plants on offer, Canadian bison prefer Carex spp. (sedges), and will consume other cool-season (C3) grasses, forbs, and shrubs if available (Figure 4). Biomass available for the Prince Albert National Park bison in the study of (Fortin et al., 2002) ranged from about 1000 to 5000 kg DM/ha.

Bulls (prefer to) eat more C4 grasses than females or juveniles (Post et al., 2001; Rosas et al., 2005; Berini and Badgley, 2017). Bison select forage that is greater than forage on offer in N and predicted digestible energy (DE), and lesser in acid-detergent fiber (ADF) and lignin (Peden, 1974; Belovsky, 1986; Plumb and Dodd, 1993; Singer, 1995; Coppedge et al., 1998b; Rutley and Hudson, 2001; Courant and Fortin, 2010). Bison preference for regrowth after fires under patch grazing or lawn grazing behaviors is consistent with the concept of selection for greater nutritive value on a short-term or long-term basis (Biondini et al., 1999; Green and Detling, 2000), assuming sufficient biomass availability and DM intake.

The two approaches, quantity-driven and quality-driven selection, are not mutually exclusive, and likely interact in response to other factors, like landscape, weather, predators, season of year, social interactions, and previous experience (Borowski and Kossak, 1972; Larter and Gates, 1991; Plumb and Dodd, 1993; Fortin et al., 2002; Fortin, 2003; Courant and Fortin, 2010; Courant and Fortin, 2012).

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20%

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100%

Offer Cons Offer Cons Offer Cons Offer Cons Offer Cons Offer Cons Offer Cons Offer Cons Offer Cons

June August March June August March June August

Heavily grazed Lightly grazed

Plumb and Dodd, 1993 Peden et al., 1976 Abaturov etal., 2016

Figure 3. Biomass on offer and consumed

C3 C4 Forbs Browse

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Digestion and metabolism

Gut anatomy and physiology

Krause (1981) and Hofmann et al. (2008) provide information on bison Brunner’s glands and salivary glands, respectively. The location frequency, and intensity of ruminoreticular contractions in bison, necessary for mixing and passage of digesta, have been described (Dziuk, 1965).

In 4 male European bison, gut tissue accounted for from 3.1 to 5% of body mass (Gil, 1968). Total gut weight, tissue plus digesta was from 7 to 13% of BW, and from 1/3 to 2/3 of digesta was in the rumen. Rumen volume in American bison was 57.2 L (DeLiberto, 1993).

Clauss et al. (2009)collected viscera from 10 Bison at a commercial slaughter, and compared bison gross anatomy to similar tissues from other wild ruminants - red deer, addax and moose. General morphology shows many large, flattened papillae in the central rumen, small ones in the dorsal rumen wall and intermediate in the ventral rumen wall (similar to those in deer and addax), with the moose having large papillae everywhere. Dry matter in the ruminoreticulum was ranked moose < red deer < bison < addax. Mean particle size in bison digesta decreased from 9.1 mm in the dorsal rumen, 8.6 mm in the ventral rumen, 6.6 mm in reticulum, to 1.2 mm in omasum. In the rumen mean particle size of floating and sedimenting particles was 9 and 8 mm, respectively. Corresponding values in the omasum were 1.4 floating and 0.8 sedimenting particles. Digesta DM increases with passage through the gut from 5% or less in the ruminoreticulum, to 18.2% for European bison (600 kg BW) in a forest habitat and 17.8% in American bison (600 kg BW) in a savanna habit (Clauss, 2004 ).

Microbiology

Several researchers have isolated and identified bacteria from the gut of bison, including strains of Clostridia, Enterococci, and E. coli (Kopečný et al., 1996; Rieu-Lesme et al., 1996; Lauková et al., 2001; Štyriak et al., 2002; Kudva and Stasko, 2013). The focus of some of the studies cited was potential resistance to antibiotics; for example, enterococci in fecal samples from European bison were susceptible to rifampicin, and nicin, but resistant to kanamycin, gentamicin, novabiocin, bacitracin and tetracycline (Štyriak et al., 2002; Lauková et al., 2003).

The application of molecular genetics techniques to gut microflora has generated volumes of information on bison. Bergmann (2017) collected digesta from forage-finished cows (3 cows, 4-14 yr old, from Nebraska,

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Offer Cons Offer Cons Offer Cons Offer Cons Offer Cons Offer Cons

1/5- 2/16 2/17-4/4 5/23-6/19 6/20-7/12 7/13-8/7 8/8-9/3

Figure 4. Biomass on offer and consumed in Prince Albert National Park (Fortin et al., 2002)

Carex spp Scolochioa festucacea Calamagrostis inexpansa Other C3 other

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Population A) and grain-finished (60:40 corn:roughage) bulls from Colorado (4 bulls 2-3 yr old, Population B). At slaughter, gut was sectioned into esophagus, reticulum, rumen, omasum, abomasum, duodenum, jejunum, ileum, cecum, ascending colon, transverse colon, descending colon, and rectum. 16S rRNA was isolated and amplified, and then computerized bioinformatics programs identified genera of bacteria. There were over 25,000 operational taxonomic units across all sections, which indicates at most there were that many species of bacteria in the gut. As in other mammals, Bacteroidetes (lowest in small intestine) and Firmicutes (most abundant in small intestine) are the dominant bacterial phyla. There was statistically significant diversity between the ileum and other gut sections in Population A, and significant differences among various sections in Population B. Bacteroidetes bacteroidales was abundant in the foregut of both groups, B. Paraprevotellaceae was abundant in the colon of Population A and more distal gut sections of Population B. Firmicutes Peptostreptococcaceae was more abundant in the ileum and cecum of Population A, more abundant in the more distal jejunum and ileum of B. Author points out that fecal samples may provide insight into bacterial profiles in the cecum, but would not represent the distinct profiles of the foregut, the rumen, reticulum, and omasum. The relatively small biomass in the small intestine reflects the low pH, especially in the duodenum, and relatively rapid transit of digesta. Firmicutes, gram +, thick cell wall, are better to that environment than other genera. Changes in relative abundance of bacteria in the foregut of Population B vs A are consistent with known changes in substrate, fermentation products, and acidity with high-forage and high=grain diets fed to ruminants. For both Populations A and B, diversity is least in the ileum, with greater diversity proximal or distal, and there are distinctions between Populations A and B on which bacteria create diversity in the distad sections; there are relatively more Ruminococcaceae and Bacteriodaceae and fewer other general in A than in B.

Weese et al. (2014) collected fecal samples from 40 bison, then used rDNA and bioinformatics to characterize their gut bacteria. Group A was assigned to 7 males less than 3 yr old, group B to 20 adult females, and group C to 13 adult males over 3 yr old. All fed a common hay diet for one month before sampling. Bacteria were classified in two groups that had sources from all 3 animal groups, therefore not related to location, age, or gender. Fecal group A had greater proportions of Actinobacteria and Firimcutes phyla, and lesser proportion of Chloroflexi, Deferibacteres, and Proteobacteria than fecal group B. The authors state that the clinical relevance of their data is unclear, and that there are other published reports that propose causes associated with prevalence of Proteobacteria, as seen in group B, and Firmicutes in group A.

Pearson (1967) reported bacterial counts of 5.88 to 8.52 X 109 and protozoal counts of 580 X 103 /ml rumen fluid) in 7 bison killed in a hunt in Utah, numbers that are in general agreement with those cited below.

Researchers at Kansas State University completed a series of experiments designed to describe rumen function in bison and to compare bison to cattle and sheep. (Towne et al., 1988a) characterized rumen ciliated protozoa found in 81 Bison rumens at slaughter. Before slaughter the animals were grazing pasture or hay (21 bison), forage plus grain supplement (45 bison), or a silage:concentrate diet in a feedlot (15 bison). The Bison came from KS, CO, NE, ND, OK, SD and TX. No protozoal species were found that haven’t been found in cattle. They claimed first report of Microcetus lappus in North American ruminants; that species had been found previously in European cattle. Population types had a greater influence on protozoal populations than diet. Type A populations contain Polyplastron multivesiculatum, Ophryoscolex species, and Metadinium affine; and type B contain Epidinium ecaudatum, Eudiplodinium maggii, and Eudiplodinium bovis (Eremoplastron bursa). If types A and B are mixed, type A will prey upon and eliminate protozoa uniquely classified as type B and create at type A-B. Type O populations are found in feedlot ruminants who usually have ruminal pH that is lethal for some protozoa, and contain only Entodinium species or holotrichs or both. Type B populations were evident in 30 bison, type A-B were in 38 bison and type A were 12 bison. One feedlot bison had Type O population. Based on the history and source of the bison in the study, they concluded that bison have a type B population unless they are exposed to animals whose rumens contain Polyplastron multivesiculatum. Other wild species are categorized as type B populations. In the highly competitive rumen environment, protozoal species change size as a defense against their predatory neighbors. Towne et al. (1988b) fed 2 ruminally fistulated bison (265 kg, about 2 yr old) and 2 Hereford steers (457 kg, 2.5 yr old) prairie hay (4.5% crude protein (CP), 70% neutral

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detergent fiber (NDF)) 2 times a day. Bison had greater populations of Dasytricha, Eudiplodinium bursa, and Epidinium than cattle, indicative of a type B population. Bison also had greater total protozoal number (328 vs 157 X 103 cells /g of rumen fluid) and volume (407 vs 162 X 108 µm3/g of rumen fluid) than cattle. Two ruminally cannulated bison (375 kg) fed twice a day ad lib ate less alfalfa (22 % CP 34% NDF), but similar amounts of prairie hay (4.4% CP, 70 % NDF) as two 567 kg steers (Towne and Nagaraja, 1989). Bison had great bacterial counts of xylanolytic (90 vs 61 X 10 9/g rumen fluid) and total anaerobic bacteria (78 vs 45 X 10 9/g rumen fluid) than cattle when fed alfalfa hay, but not when fed prairie hay. Authors interpret their results to say that any putative advantage in fiber fermentation capacity in bison vs cattle does not appear to be due to ruminal microbial populations. Towne and Nagaraja (1990) Studied ruminal and omasal protozoal profiles in samples collected at slaughter for cattle, 15 bison, and sheep. As in the other ruminants, bison had greater protozoal numbers (1748 vs 304 X 103 cells /g fluid) and volume (897 vs 142 X 108 µm3/g of fluid) in the rumen vs the omasum. Authors speculate that omasal protozoa play key role in repopulating defaunated rumens.

The research team at Agriculture and Agri-Food Canada, Lethbridge, AB, Canada used a semi-continuous in vitro rumen fermentation simulation technique (Rusitec) to substantiate and quantify the assertion that bison have greater capacity than cattle to digest roughage (Oss et al., 2016). The Rusitec fermenters are noted for their capacity to control input and outflow rates, and to sustain valid fermentations for days and weeks rather than the more limited hours or days of closed in vitro systems. Rusitec allows time for adaptation after changes in inoculum or feed supply. They inoculated 8 fermenters with cattle:bison rumen fluid ratios of 0:100, 33:67, 67:33, 100:0. Rumen fluid from 32 bison fed and 75:25 barley silage and oats diet came from an abattoir, and cattle rumen fluid came from 16 cannulated animals fed the same diet as the fermenters, a 70:30 barley straw (5.8% CP, 73% NDF) and concentrate (35.2% CP, 31% NDF) diet. The Rusitec system in conjunction with 15N and molecular genetic techniques provided information on microbial populations, digestion of the straw and concentrate feed separately, and digestion of the mixed diet. As the proportion of bison rumen fluid increased, protozoal numbers and mass increased. As proportion of bison rumen fluid increased, proportions of F. succinogenes increased quadratically, R. albus decreased linearly, and R. flavefaciens tended to decrease. The proportions of cattle:bison rumen fluid did not affect total bacterial populations (based on 16S rRNA copies), or the proportions of S. ruminantium or P. bryantii. These changes in microbial populations as the proportion of bison rumen fluid increased were associated with a linear increase in N disappearance from the mixed diet and the concentrate portion of the diet, a quadratic increase in DM and NDF digestion of the straw, the concentrate, and the mixed diet, indicating that a mixture of cattle and bison rumen fluid supported more digestion than rumen fluid for single sources. It also was associated with increased production of ammonia, total VFA, and individual volatile fatty acids except propionate. Production of methane and microbial N were not different among proportions of cattle:bison rumen fluid inoculations. Another study similar again saw a quadratic increase in DM digestion of barley straw, and a linear decrease of the same components in alfalfa hay and wheat distiller’s grains with solubles as level of Bison rumen fluid increased (He et al., 2016).

The Lethridge researchers (Ribeiro et al., 2017) followed the Rusitec studies with in vivo studies in cannulated beef heifers that received transfer of bison rumen fluid collected at an abattoir, to create a 30:70 cattle:bison rumen fluid ratio in the rumens of the cannulated heifers fed the same 70:30 barley straw:concentrate diet used in the earlier studies Rusitec. The rumen fluid transfer was repeated 14 d later. Bison rumen fluid from the two transfers had more protozoa (344 and 282 X 103/ g rumen fluid) than heifers before the transfers (134 X 103 / g rumen fluid). Bison rumen fluid had higher % Isotricha, eudiplodinium, and lower % Entodinium and Ostracodinium than heifer rumen fluid. Bison rumen fluid transfer had no effect on ruminal solids or fluid turnover, but it decreased transit time of fluids through the total tract (from 11.2 to 8.5 h before appearance of marker in feces), tended to decrease solid transit time, and increased total DM in gut from 2.68 to 3.01 % of BW. After the transfers, heifers ate more DM, OM, and digested more NDF daily than they did before the transfers, but total tract apparent digestibility (% of DM Intake) of DM, organic matter (OM), NDF, ADF were not affected by the transfers; however, apparent N digestibility increased from 63.3 to 66.5 % of N intake. After transfers, rumen pH was lower and ruminal ammonia N concentration was greater 6 hr after feeding. Inoculation did not affect eating, ruminating, and chewing time per day, but chewing time as a percentage of DMI decreased because they ate more. After inoculation the heifers ate more, defecated and urinated more

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often, and retained more N per day. After inoculation there were more total purine derivatives, allantoin and microbial purines in urine (indicating greater intestinal absorption of digestion products from microbial biomass), but there was no change in microbial N flow from the rumen per kg of BW.

The third study by the Lethridge group (Griffith et al., 2017)again used rumen fluid transfers from bison at slaughter. The diet again was 70:30 barley straw: concentrate, and this time the concentrate was pelleted and the amount of concentrate fed regularly adjusted to fit the straw intake of the cannulated heifers. Before and after transfer for bison rumen fluid, In situ digestion of barley straw (4.9% CP, 78 % NDF), canola straw (6.0 % CP, 74 % NDF), alfalfa hay (16.9% CP, 48 % NDF), and timothy hay (8.5 % CP, 769 % NDF) were measured intermittently up to 120 h in the rumen. The results provide rates of disappearance for the four substrates, before and after transfer of bison rumen fluid. They found no differences in rate of digestion after vs before transfer, and the tested forages varied in digestion rates as might be expected from difference in NDF content, canola straw < barley straw < timothy hay < alfalfa hay. The extent of degradations at 24 and 48 hr, comparable to other studies at those in situ incubation times, showed greater digestion before vs. after transfer. The authors acknowledge that the pore size in the nylon incubation bags, 50 µm, may have precluded access to samples by larger protozoal species that may exist in bison rumens, thereby limiting digestion of fiber after transfer.

Varel and Dehority (1989) evaluated rumen fluid from bison and Hereford steers fed alfalfa:corn ratios of 100:0 (13.4 %CP, 62% NDF), 75:25 (18.2 % CP, 41% NDF), or 50:50 (15.0 % CP, 34% NDF). As the portion of alfalfa hay decreased, numbers of total bacteria increased (3.02 to 5.44 X 109 / ml rumen fluid) while cellulolytic bacteria decreased (10.9 to 6.6 X 107 / ml rumen fluid). Proportions of Butyrivibrios spp., Ruminoccocus. albus and unclassified bacteria increased, and proportions of R. flavefaciens, and B. succinogenes decreased. In Hereford steers, similar response in bacterial numbers were evident, and proportions of R. albus, R. flavefaciens, and B. succinogenes decreased. Genera of protozoa were similar among animals and diets, as were total protozoal numbers (249 X 103 /ml rumen fluid), but Hereford steers had proportionately more Entodinium and less Epidinium spp., Diplodiniinae and Dasytricha spp. than cattle. When diets containing corn were fed, Entodinium spp decreased to 1% or less compared with 51% in the steers. And Diplodiniinae increased in bison (81%) more than the steers (20%). Except for concentrations of isovalerate, Bison fed 50:50 alfalfa:corn had greater VFA concentrations than steers fed that diet (103 mM vs. 66 mM total VFA), which could be attributed less ruminal fluid in bison, not determined in this study. Otherwise, ruminal VFA concentrations were similar for bison and steers fed the other diets. 48-hr in vitro digestibility of NDF (28%), Hemicellulose (38%), and Cellulose (31%) was not affected by animal species across diets, and in general increased as the proportion of alfalfa in the diet decreased.

Summary of digestion studies

Table 2 summarizes information available from 60 bison of various BW on DMI, and in vivo apparent digestibility DM, energy, CP, NDF (plant cell walls), and components of NDF, hemicellulose (H-C) and ADF. Two points to be made from the information in the table are 1) DM intake is less than one would expect in production conditions, with only one set of observations greater than 19 g/kg BW; and 2) the standard deviations are large, greater than 15% of the average except for H-C, which is a calculation based on NDF minus ADF. Data from other ruminants indicates a population standard deviation of 10 % of the average or less for these types of variables. Again, based on other ruminants (cattle, sheep, and goats), one would expect less variation (a smaller standard deviation as percentage of the average) as intake decreases below production-level intakes. I conclude from these data that it is likely that the bison felt distressed, which would negatively affect voluntary intake, rate of passage of digesta through the digestive tract, and likely water intake. Stanton et al. (1996) fed diets ranging from 30% to 90% concentrate and expressed apparent digestibility on an organic matter basis rather than DM, ostensibly to correct for soil/dirt consumption in a feedlot situation, and reported organic matter apparent digestibilities for 24 to 64 g/ 100 g OM, CP apparent digestibilities from 19 to 53% of OM intake, and ADF apparent digestibilities from 27 to 53 % of OM intake. Organic matter and CP apparent digestibilities increased as percentage concentrate in the diet increases, as one would expect, and ADF apparent digestibility was not affected by diet.

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Table 2. Body weight (BW), dry matter intake (DMI), diet DM and apparent digestibility of various diets

Table 2 Apparent digestibility, g/100 intake

Diet BW, kg

DMI, kg/d

DMI, g/kg BW DM Energy CP NDF H-C ADF Cite

Sedge Hay 177 1.6 9.0 64.2 _ 54.2 69 76.5 62.8 1 Sedge Hay 244 3.9 16.0 51.6 51.2 35.8 52.3 63.8 45 2 Sedge Hay 314 5.0 16.0 51.1 50.1 41.4 57.6 71 49.4 2 Grass Hay 170 1.9 11.0 74.0 _ 70 79.2 79.25 67.2 1 Grass Hay 230 4.9 21.3 59.9 _ _ _ _ _ 3 Grass Hay 154 2.2 14.3 67.1 _ _ _ _ _ 3 80% Straw 241 3.4 14.0 47.1 _ 53.2 51.5 _ 49.1 4 Brome/alfalfa 279 4.8 17.1 50.1 49.3 67 _ _ 5 Alfalfa hay 187 2.4 13.0 77.5 _ 84.8 76.5 76.5 65 1 Alfalfa hay 250 4.9 19.6 70.1 68.2 71.7 66.2 57.2 _ 6 Alf:Corn 75:25 275 5.6 20.4 69.3 67.1 76.2 65.2 65.2 _ 6 Alf:Corn 50:50 320 7.0 21.9 71.3 69.5 74.1 59.3 63 _ 6

Average 236.8 4.0 16.1 62.8 59.2 62.8 64.1 69.1 56.4 Std Dev 55.4 1.7 4.1 10.5 9.9 16.0 9.8 7.9 9.6

1 Richmond et al., 1977, n = 4; 2 Hawley et al., 1981 n= 5 or 6; 3 Rutley and Hudson, 2000, n = 10; 4 DeLiberto et al., 1993, n=3; 5 Schaefer et al., 1978, n= 2; 6 Koch et al., 1995, n = 4

Intake and weight gain in feedlot studies

Table 3 provides a summary of feedlot studies from over 1300 bison, over 43 yr (Peters, 1958; Christopherson et al., 1978; Koch et al., 1995; Miller and Anderson, 1996; Stanton, 1996; Anderson and Miller, 1997; Church et al., 1999; Anderson and Bock, 2001). I calculated dietary content of total digestible nutrients (TDN) and CP from feedstuffs and tabular values when the publication did not provide those data, and I calculated initial and final weights when those were not explicit in the publications. With the exception of the 2 bison fed by Christopherson et al. (1978) the feeding trials fed diets that contained between 74 to 90% TDN (average was 77% TDN), indicating a grain, or concentrate, concentration that was about 50% of diet DM and a hay, or roughage, content of 25% or less of DM. Dietary concentrate level did not affect intake or gain in studies designed to identify such as response (Anderson, Stanton) Dietary content of CP was 12% of DM, and with the exception of Anderson and Bock (2001) exceeded 10%. Anderson showed a statistically significant response to dietary CP in younger, lighter bison bulls that suggested maximal daily gain was attained between 11.6 and 13.9% of DM.

There are four main points to be derived from the table. First, the most recent study was published 17 yr ago. Second, the data show the effect of season, the ‘winter slump’ in reduced voluntary intake and weight gain compared with other seasons of the year. The data of Anderson and Miller (1997) show a statistically significant response to season of the year, and other data of Stanton (1996) not presented in table, show weight loss during the month of December. Third, the weighted average of voluntary intake was 25 g of dry matter/kg of BW, a reasonable baseline estimate of intake, and the same as that measured in grazing bison (Bergman et al., 2001). Fourth, the weighted average daily gain was 730 g/d, which is about twice the rate for grazing bison or hay-fed bison described in the section on growth and development. The increased gain of confined bison likely reflects the greater energy content of the diet, and less energy expended in locomotion than by free-ranging, grazing animals. When data were restricted to bulls, other than winter, average gain was 773 g/d, and feed efficiency was 0.091 kg gain/kg intake, or 11 kg feed/kg gain. Anderson and Sexhus (1996) reported an average gain of 740 g/d in North Dakota feedlots, and a range in gain from 454 to 1000 g/d.

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Table 3. Season of year, diet composition, body weight (BW), days on feed, average daily gain (ADG), and dry matter intake (DMI) of bison in confinement feeding

Source, Season, Diet Year Animal n Diet, % TDN

Diet, % CP

Initial BW, kg

Final BW, kg Days ADG

DMI, kg/d

DMI, g/kg BW

Peters 1958

January-May bull 9 74 12.3 156 279 196 0.63 4.8 22

January-May bull 8 74 12.3 171 269 196 0.50 4.3 20

January-May female 8 74 12.3 150 249 197 0.50 5.3 27

January-May female 11 74 12.3 166 247 197 0.41 4.3 21

Christopherson et al 1978

Winter ? 2 53 12.3 118 158 96 0.42 3.25 24

Koch et al 1995

March -June castrate 10 79 9.7 185 253 112 0.60 5.25 25

July - October castrate 10 79 9.7 253 357 112 0.93 6.34 23

Stanton et al 1996

June - October

30% concentrate bulls 44 68 12.0 235 335 141 0.71 7.70 21.8




January - March



70% concentrate, 10% CP bulls 42 78 10.0 360 394 69 0.50 7.68 30.7


Miller and Anderson 1996

Summer bull 80 82 10.8 274 341 80 0.84 8.9 29

Fall bull 80 82 10.8 341 412 80 0.89 10.3 27

Winter bull 80 82 10.8 412 448 80 0.45 8.3 18

Spring bull 80 82 10.8 448 498 80 0.60 8 18

Anderson and Miller 1997

Spring bull 78 77 15.0 245 302 80 0.78a 8 33

Summer bull 78 77 15.0 302 361 80 0.63a 8.4 28

Fall bull 78 77 14.0 361 397 80 0.80a 11.4 32

Winter bull 78 77 14.0 397 411 80 0.17b 11.2 28

Church et al., 1999

1992 Winter bull 28 78 11.0 317 395 90 0.87 8.7 24

1992 Winter bull 15 78 11.0 317 370 90 0.59 6.3 18

1993 Summer bull 24 78 11.0 448 538 90 1.01 10.1 20

1993 Summer bull 15 78 11.0 406 557 90 1.68 13.8 29

1993 Winter bull 11 78 11.2 317 386 90 0.77 10.2 29

1993 Winter bull 23 78 11.2 317 369 90 0.58 12.3 36

1994 Summer bull 19 78 11.2 432 515 90 0.92 10.9 23

1994 Summer bull 21 78 11.2 404 490 90 0.95 12.4 28

Anderson and Bock 2001

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January - April

9.4% CP bull 20 76 9.4 287 353 90 0.73a 6.1 19

11.6% CP bull 20 76 11.6 289 356 90 0.74a 6.2 19

13.9% CP bull 20 76 13.9 286 364 90 0.87b 6.2 19

16.0% CP bull 20 76 16.0 286 361 90 0.83ab 6.3 19

April - September

9.4% CP bull 20 76 9.4 353 423 90 0.78 9.1 23

11.6% CP bull 20 76 11.6 356 423 90 0.75 8.9 23

13.9% CP bull 20 76 13.9 364 437 90 0.81 9.0 22

16.0% CP bull 20 76 16.0 361 429 90 0.76 8.96 23

ab For Anderson and Miller (1996) and Anderson et al. (2001), ADG with different letters differ (P < 0.05).

Blood chemistry

Blood samples are difficult to obtain from bison and other wild animals, especially without alteration of blood parameters due to the sampling process. Techniques used include jugular venipuncture, tail vein venipuncture, and post-mortem samples obtained from freshly killed animals. Whole blood, blood plasma or blood serum samples from bison are used to assess nutrient status, physiological status, immune status, metabolic disorders, stress and/or trauma, and genetic information.

Hemoglobin (Hb) and blood type and genetics

The primary interest in blood typing and blood proteins centered on genetics, or relatedness, of bison and cattle (Suzuki et al., 1979; Nagi and Babiuk, 1989). Braend and coworkers isolated proteins from such animals to show similarities and distinctions among hybrids and their parent lines. They showed Hb similarities between European bison (Eb) and North American bison (Bb) , and Hb types that are shared with cattle (Braend and Stormont, 1963; Braend and Gasparski, 1967; Braend et al., 1969). Sartore et al. (1969), Leary (1978), and Peden and Kraay (1979) isolated carbonic anhydrase from erythrocytes to demonstrate relatedness among and within bovine and bison. Harris et al. (1973) added further clarification on Hb types, including amino acid sequences.

Brzuski et al. (2010) compared ranched Bb in Poland with Bb. They sampled 9 calves, 6 cows, and 1 bull and found that Polish Bb had greater concentration of BUN, bilirubin, alkaline phosphatase, P, and AST, and lower values for glucose, creatinine, total protein, albumin, Na, and Cl-.

Histology

Nutritional Status

The main goal of the studies of Hawley and Peden (1982) was to compare bison in feedlot setting to cattle, and cattle differed from bison in 13 of the 21 blood parameters. Bison were fed diets containing combination of high protein (11 to 13% CP) or low crude protein (7 to 9%CP) factored with high energy (3.5 Mcal DE/kg or 80% TDN) or low energy (2.5 Mcal/kg DM or 57% TDN). Serum BUN concentration were greater for high protein than low protein in winter, not in summer. Otherwise, there were no marked effects of diet or season on histology, or serum enzyme activity. In a separate study, bison from Elk Island National Park, ostensibly Bb, had greater values than those from Wood Buffalo National Park, ostensibly Ba. for CPK, AST, Hb and PCV, and lesser values for BUN and mean corpuscular hemoglobin (Hawley and Peden, 1982). Compared with adult bison, younger bison had greater values for P and alkaline phosphatase, red and white cell counts, Hb and mean corpuscular cell volume, and plasma and serum protein.

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Keith et al. (1978) had 6 adult bison that had been in close human contact for months, fed grass hay (6% CP) or grass hay plus a supplement containing 15% CP. They were sampled December 1. and again March 1. Few animals precludes statistical analysis; bison fed supplement had numerically greater serum urea N, Ca and P.

Sikarskie (1989) sampled Michigan ranched bison and bison from Badlands National Park in South Dakota; at the Park serum was obtained from 20 sedated adults. Average ± SD Selenium values for the Michigan bison, who are in a region recognized as Se-deficient, were 0.026 ±0.009 µg/mL serum, lower than Park bison, living in a Se-adequate region, which were 0.099±0.019 µg/mL. Authors noted that the Michigan bison were offered a Se source in a mineral block and/or Se injections, and that 0.1 µg/mL was recommended as a normal serum concentration for bison. Clemens et al. (1987) reported 0.30 µg Se/mL in whole blood from adult bison in Nebraska. In their survey of blood samples from 13 domestic herds in 11 states, Stoltenow and Dyer (2001) characterized serum selenium in 3 categories: 1) no supplemental Se, 157 samples, 0.06 ± 0.012 µg Se/mL serum; 2) supplemental Se, 208 samples, 0.24 ± 0.073 µg Se/mL serum; and 3) grazing areas recognized for high levels of Se, 30 samples, 0.62 ± 0.132 µg Se/mL serum. The bison in the last group showed no obvious signs of Se toxicity. They also reported serum values from 360 samples for Cu, 0.079 ± 0.25 µg /mL, and Fe, 1.49 ± 0.44 µg /mL.

Age and gender

Mehrer (1976) collected post-mortem samples as well. with the intent of detecting gender or age differences in histology indicative of disease or other immune challenge. Statistical analyses of blood parameters from 5 conservation herds, 163 bison in total, found no significant differences among age, gender or location, except for increased hematocrit, erythrocytes, and Hb in older vs younger bulls. Sikarskie et al. (1990) compared Michigan ranched bison to bison in the Badlands National Park in South Dakota. Young bison (< 185 kg) had greater P, RBC and Total Protein than older bison (> 185 kg). Older bison had greater eosinophil and neutrophil counts with lesser lymphocytes, which authors say indicates more immune stress for older bison. Calves had neutrophil:lymphocyte ratio commonly seen in bovine. Vestweber et al. (1991) studied 3 age groups, 40 bison in all, from the Konza Prairie in Kansas. MCV, MCHb, neutrophil and eosinophil counts, total protein, globulin, creatinine and urea N increased with age, SDH, AlK, glucose, Na, Ca, and P decreased. Marler (1975) measured blood histology, metabolites, and enzymes 2 groups of bison, one from 9 mo to 2 yr of age, the other group 2 yr old and older. The 25 older bison had lesser AST and AP activity than the 12 younger bison.

Immune status and stress

Yearling bison, both male and female, 106 in total, showed no change in blood chemistry of histology in a controlled experiment in which exposure to Mycobacterium bovis was evaluated (Miller et al., 1989). Zaugg et al. (1993) obtained blood samples from 149 of 257 bison from Yellowstone National Park after they were killed in compliance with a Montana Livestock Department’s order. They were interested in identifying clinical markers to determine internal parasite burden in bison. They did not find low blood urea N values or leukopenia associated with high parasite burdens; fecal samples showed moderate parasite infestation. Glucose values were unreasonably high and WBC values were low, likely due post-mortem sampling. Grain-fed bison were allocated to groups designed to alter duration and form of stress associated with handling before slaughter (McCorkell et al., 2013). Serum levels of glucose, cortisol, corticosterone, and enzymes were consistent with accepted concepts on effects of stress on these parameters.

Other

Plasma progesterone ranged from 0.9 to 2.8 ng/ml in 3 barren bison 2 to 5 yr old, 4.1 ng ml in an 8-yr-old pregnant female and 10.5 ng/ml in a 2 yr old pregnant female (Kirkpatrick et al., 1992). The main goal of this study was to validate use of urine samples to follow progesterone and pregnancy, much as Mooring et al. (2006) used fecal steroid hormone levels with dominance rank in bison bulls.

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Table 4 shows number of bison, weighted means and SD for blood histology, and serum samples from several studies (Marler, 1975; Mehrer, 1976; Hawley and Peden, 1982; Miller et al., 1989; Vestweber et al., 1991; Zaugg et al., 1993; Stoltenow and Dyer, 2001).

Table 4. Blood histology and serum values for bison

Component n Mean SD Component n Mean SD

PCV, % 871 48 9.0 Total protein, /dl 306 7.84 0.93 RBC x 106 775 8.0 3.4 Albumin, g/dl 305 3.76 2.3 Hb, g/dl 851 17.4 1.7 Globulin, g/dl 249 3.71 0.81 MCV, µm3 511 52.9 6.5 Creatinine, mg/dl 693 2.66 .60 MCHb, pg 517 19.0 2.4 Urea N, mg/dl 763 16.2 5.9 MCV, g/dl 517 35.8 2.6 Glucose, mg/dl 670 145 97 WBC x 103 810 6.48 3.06 Na, mM 578 145 10 Neutrophils x 106 427 3.0 2.0 K, mM 579 7.2 3.6 Lymphocytes x 106 427 2.4 1.5 Cl, mM 218 104 10 Monocytes x 106 427 0.24 0.24 Ca, mg/dl 709 9.9 .6 Eosinophils x 106 427 0.24 0.26 Mg, mg/dl 420 2.20 .36 Basophils x 106 427 0.01 0.03 P, mg/dl 755 6.6 2.2 Lymphocytes, % 335 21.0 26.6 Fe, µg/dl 479 138 42 Neutrophils, % 295 27.2 30.0 Sorbital DH, IU 104 17 11 Eosinophils, % 295 2.1 3.6 AP, U/L 362 54 25 Monocytes, % 295 3.1 3.9 AST IU/L 304 97 45

GGT, IU/L 553 20 25

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Merkle, J. A., D. Fortin, and J. M. Morales. 2014. A memory-based foraging tactic reveals an adaptive mechanism for restricted space use. Ecol Lett 17(8):924-931. doi: 10.1111/ele.12294

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II. Growth and development

Summary

Bison show distinct sexual dimorphism from birth through maturity. Mature body size appears to be latitude specific, with smaller body size as latitude decreases in North America. Other factors such as ambient temperature and rainfall may affect food supply on a long-term basis, hence body size. Rates of weight gain for young animals, up to 2 years of age, range from 0.30 to 0.50 kg/d for females and males, respectively. Greater gains can be expected in pen-fed animals fed diets containing adequate nutrition to support gains up to 1.0 kg/d or more. Domestic herds show variation in body weight, and weight gain in response to location and health status. The ‘winter slump’ indicated by observation of body condition in conservation herds is confirmed in pen-fed animals, indicating that management of domestic herds should take that seasonal phenomenom into consideration

Introduction

To define growth characteristics, starting with fetal growth and continuing past physiological maturity, researchers have developed growth curves from data on age and size for almost all domestic species and many wild species, including bison. Size usually is defined as body weight, or some function thereof. During growth in young bison and after maturity, there is an annual cycle, or wave of fluctuation in body weight, concurrent with winter weather; during this ‘winter slump’, voluntary intake decreases, digesta transit rates from the rumen and post-ruminal sections of the gut decrease, body weight (or weight gain for young animals) decreases, and metabolic rate decreases, when days are short and temperatures fall (Price, 1985; Hudson, 1985 ; Stanton, 1996; Agabriel et al., 1998; Rutley and Hudson, 2000). It is not clear whether decreased appetite and feed intake cause the physiologic and metabolic changes or vice versa.

There are few studies with confined, or penned, bison to provide measures of weight and age, on individuals or even small groups of bison. There are many more data on weight and age from conservation herds in national parks and preserves.

Fetal growth

Gogan et al. (2005) collected fetal weights and a morphometric measure, crown-to-rump length, from 300 bison fetuses from Yellowstone National Park over several years. They used these measures to create fetal growth curves and to estimate time of gestation for fetuses. From these they estimated birth weights of 22.5 kg for females and 27 kg for males. They validated their calculations with available data on live calving dates; so, stage of gestation can be predicted based on weight and crown-rump length.

Growth Curves

Licht (2016) summarized animal weight and age data accumulated between 1983 and 2014 at three sites, The Badlands National Park and Wind Cave National Park in South Dakota, and Theodore Roosevelt National Park in North Dakota. Growth curves from the Badlands for males and females fit a rising logistic equation (y = a (1- e-kt ), where y = body weight, a = mature body weight, k is a rate constant, and t = time in years). That equation fits rate of growth until maturity, and then predicts maximal mature weight. On average, females gain 0.37 kg/d for the first 2.5 yr and reach a mature weight, about 508 kg, at about 6.5 yr of age. Males gain 0.41 kg/d for the first 3.5 yr and reach mature weight, about 870 kg, at 11.5 yr of age. Similar data from the National Bison Reserve in Montana (Berger and Peacock, 1988), Fort Niobrara in Nebraska (Berger and Peacock, 1988) and Wind Cave National Park and Ordway Prairie, South Dakota (Green and Rothstein, 1991a; Craine et al., 2015b) show almost the same initial rates of gain and mature body size. However, data from Kansas and Oklahoma indicates slower initial rates of gain, 0.24 kg/d for females and 0.21 - 0.33 kg/d for males, and lighter mature weights, 400 and 450 kg for females, 700 to 750 kg for males (Halloran, 1968; Towne, 1999; Craine et al., 2015a). The limited information on indirect (Haigh and Gates, 1995) and direct measures of age and weight of Bison bison athabasca (Price, 1985; McCorkell et al., 2013) indicates that Bison bison athabasca and Bison

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bison bison (Licht, 2016) have similar mature weights, and body weights of 10 female Bison bison athabasca, 2.5 yr old and 280-350 kg are comparable to data of Licht (2016).

Nutritive value and quantity of food supply could compromise rate of gain, and climate (warmer ambient temperatures) might affect mature size. Variation in growth rates and mature weights also indicates response to genetics and environment. In the large dataset of Licht (2016), mean weight of weaned female calves is 147 kg, and the coefficient of variation is 20%, which means that the weight of 2/3 of all 1,142 calves ranges from 117 to 177 kg. The mean ± the coefficient of variation for male calves is 153 kg ±25%, 307 kg ± 16% for yearling females, 325 kg ± 16% for yearling bulls, 449 kg ± 8% for mature cows, and 641 kg ± 12% for mature bulls.

Licht (2016) found correlations (R2= .36 to .45) between calf and yearling weights of 275 females and 200 males at Badlands National Park, and weaker correlations (R2 = .07 to .19) for the same comparisons at Wind Cave National Park. There were weak correlations between calf weight and adult cow weight at the two locations (R2 = 0.02 to 0.06), indicating that the linear relations of age and juvenile growth phase did not persist in mature cows, because other factors, like feed supply, disease, and calving affect cow body weight. As expected, there was no correlation between age and mature body weight in either sex (Lott and Galland, 1987). Plots of body weight, and ostensibly, body condition, of mature cows typically show a ‘wave’ pattern, in response to pregnancies, nutritive quality of feed supply, seasons of the year (including the end of altered metabolic rates in the winter associated with new plant growth in the spring) and ambient conditions (Berger and Peacock, 1988; Towne, 1999; Craine, 2013; Craine et al., 2015a)

Growth information from domestic bison

Intake and gain of 8 yearling females weighing 218 kg and fed in confinement were measured for 138 d from September to May (Agabriel et al., 1998). Average daily gain (ADG) on pasture before the study began was 0.34 kg/d. They were fed hay whose dry matter (DM) was 57 to 68% digestible, contained 10 to 15% CP, and 7.3 MJ ME/kg DM. During the ’winter slump’, DM intake and ADG decreased from 5.75 to 4.9 kg/d and 0.52 to -.01 kg/d, then recovered to 5.4 kg/d and 0.28 kg/d during the spring months. During the fall and spring, ADG was linearly related to energy supply, but not during the winter; the heifers’ apparent energy efficiency was reduced during the winter. Similarly, ’winter slump’ was evident in 178 Canadian bison bulls pen-fed diets ranging from 30 to 90% concentrate in Colorado (Stanton, 1996). Initial weight was 235 kg, indicating the bulls were about 1 yr old. From June until December they ate from 7.8 to 8.6 kg DM/d, and gained from 0.74 to 0.96 kg/d, then from December until March they ate from 6.8 to 7.7 kg/d, and gained from 0.29 to 0.43 kg/d. In December, the bulls lost weight, 0.03 to 0.25 kg/d. The authors point out that deer and elk demonstrate a similar depression in feed intake and metabolism during the winter. Ten castrated males (initial body weight = 185 kg) fed a corn silage-based, 33 % concentrate diet ate 6.34 kg/d of DM and gained 0.77 kg/d over 224 d during late winter and spring in Nebraska (Koch et al., 1995). They also fed 4 castrated males (initial body weight = 248 kg), fed diets ranging from alfalfa hay to alfalfa hay:corn grain 3:1 or 1:1, ate 6.46 kg DM/d and gained from 0.00 (alfalfa hay in late winter) to 0.60 kg/d on other diets in spring and summer, a total of 336 days for the experiment). Although the alfalfa diet contained less energy than alfalfa:corn diets, lack of gain in December is similar to results seen by Stanton et al. (1995) in December, supporting the conclusion that ‘winter slump’ precluded any gain from alfalfa hay.

Rutley et al. (1997) completed a 3-yr study of 3,329 bison from 16 private herds in Peace county Alberta, Canada. Bison ranged in age from birth to 15 yr. Location, or herd, year, and gender affected calf weights. Males of 1,486 calves weaned in the fall at 8 to 10 mo of age were heavier (196 kg) than females (187 kg). Males from a pool of 944 calves weaned in the fall at 8 to 10 mo old were heavier (209 kg) than females (197 kg). At 12 mo old, males weighed more (217 kg) than females (197 kg). Males calves gained more weight (0.50 kg/d) than females (0.42 kg/d). Average yearling weight for 905 bison was heavier for winter-weaned males (310 kg) than females (299 kg). Yearling weight for 136 spring-weaned bison (345 kg) was not different for males vs females. The weight differential returned at 2 yr of age in 47 bison weighed in the winter, 467 kg for males vs 413 kg for females. Average winter weight for 458 adult bison was 594 kg for males and 448 kg for

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females, was not significantly different for gender, due to the large range in weight for males (416 to 887 kg) and females (294 to 594 kg, with half weighing more than 500 kg). Year-to-year ambient conditions, prevalence of treated health problems, and location usually affected bison weights. They also found that winter supplemental feeding lessened the usual ‘winter slump, spring recovery’ metabolic scheme and growth pattern of bison; supplemental feeding also reduced the gain response (compared to unsupplemented bison) to spring pasture growth, presuming adequate grazing supply and composition to meet the nutrient requirements for gain. These growth results fit well with the growth curves of Licht (2016), giving confidence to the ability to use information obtained on conservation herds to private herds.

,

Figure 1. Observed data of Rutley et al (1997) and predicted growth curves of Licht (2016)

A grazing study designed to assess energy requirements of 12 yearling bison reported comparable rates of gain in the summer and early fall, 0.55 kg/d, and weight loss in December, -1.3 kg/d, that was reduced to -0.42 kg/d with hay supplementation (Rutley and Hudson, 2000).

Indirect measures of growth

Other, often less confining, ways to assess growth have been adapted to bison, including shoulder height, chest girth, body length, head length and width, horn shape and size, with correlations among measures or with body weight ranging from about 0.7 to 0.9 (Halloran, 1968; Haynes, 1984; Berger and Peacock, 1988; Kimball and Wolfe, 1989; Green and Rothstein, 1991c, b, 1993; Komers et al., 1994). Scrotal circumference is correlated with age, r2 = 0.26 (Keen et al., 1999). (Kelsall, 1978) and Berger and Peacock (1988) found that

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chest girth was more strongly correlated with body weight in males (r = 0.77 to 0.82) than females (r = 0.58 0.61). Tooth replacement and wear are reliable indicators of age (Fuller, 1959; Novakowski, 1965; Haynes, 1984; Christianson et al., 2005).

Literature Cited

Agabriel, J., J. Bony, and J. Lassalas. 1998. American buffalo husbandry. Point Veterinaire 29(190):218-226. Berger, J., and M. Peacock. 1988. Variability in size-weight relationships of Bison bison. J. Mammalogy

69(3):618-624. Christianson, D. A., P. J. P. Gogan, K. M. Podruzny, and E. M. Olexa. 2005. Incisor wear and age in Yellowstone

bison. Wildlife Society Bulletin 33(2):669-676. Craine, J. M. 2013. Long-term climate sensitivity of grazer performance: a cross-site study. PLoS One

8(6):e67065. doi: 10.1371/journal.pone.0067065 Craine, J. M., E. G. Towne, and A. Elmore. 2015a. Intra-annual bison body mass trajectories in a tallgrass

prairie. Mammal Research 60(3):263-270. doi: 10.1007/s13364-015-0227-z Craine, J. M., E. G. Towne, M. Miller, and N. Fierer. 2015b. Climatic warming and the future of bison as grazers.

Sci Rep 5:16738. doi: 10.1038/srep16738 Fuller, W. A. 1959. The Horns and Teeth as Indicators of Age in Bison. Journal of Wildlife Management

23(3):342-344. Gogan, P. J. P., K. M. Podruzny, E. M. Olexa, H. I. Pac, and K. L. Frey. 2005. Yellowstone bison fetal development

and phenology of parturition. Journal of Wildlife Management 69(4):1716-1730. doi: 10.2193/0022-541X(2005)69[1716:YBFDAP]2.0.CO;2

Green, W. C., and A. Rothstein. 1991a. Trade-offs between growth and reproduction in female bison. Oecologia 86(4):521-527. doi: 10.1007/BF00318318

Green, W. C. H., and A. Rothstein. 1991b. Sex bias or equal opportunity? Patterns of maternal investment in bison. Behavioral Ecology and Sociobiology 29(5):373-384. doi: 10.1007/BF00165963

Green, W. C. H., and A. Rothstein. 1991c. Trade-offs between growth and reproduction in female bison. Oecologia 86(4):521-527. doi: 10.1007/BF00318318

Green, W. C. H., and A. Rothstein. 1993. Persistent influences of birth date on dominance, growth and reproductive success in bison. Journal of zoology 230(2):177-186.

Haigh, J. C., and C. C. Gates. 1995. Capture of wood bison (Bison bison athabascae) using carfentanil-based mixtures. Journal of wildlife diseases 31(1):37-42.

Halloran, A. F. 1968. Bison (Bovidae) Productivity on the Wichita Mountains Wildlife Refuge, Oklahoma. Southwestern Naturalist 13(1):23-26.

Haynes, G. 1984. Tooth Wear Rate in Northern Bison. Journal of mammalogy 65(3):487-491. Hudson, R. J. C., R. J. 1985 Chapter 6. Maintenance Metabolism. In: R. J. W. Hudson, R. G., editor, Bioenergetics

of Wild Herbivores,. CRC Press, Boca Raton, FL. p. 121-142. Keen, J. E., G. P. Rupp, P. A. Wittenberg, and R. E. Walker. 1999. Breeding soundness examination of North

American bison bulls. Journal of the American Veterinary Medical Association 214(8):1212-1217. Kelsall, J. P. T., Edmund S.; Kingsley,Michael 1978. Relationship of Bison Weight to Chest Girth. Journal of

Wildlife Management 42(3):659-661. Kimball, J. R., and M. L. Wolfe. 1989. Bison studies siza, teeth age Buffalo! No. 17. p 28-29. Koch, R. M., H. G. Jung, J. D. Crouse, V. H. Varel, and L. V. Cundiff. 1995. Growth, digestive capability, carcass,

and meat characteristics of Bison bison, Bos taurus, and Bos x Bison. Journal of animal science 73(5):1271-1281.

Komers, P. E., F. Messier, and C. C. Gates. 1994. Plasticity of reproductive behaviour in wood bison bulls: When subadults are given a chance. Ethology Ecology and Evolution 6(3):313-330.

Licht, D. S. 2016. Bison Weights From National Parks in the Northern Great Plains Rangelands No. 38. p 138-144.

Lott, D. F., and J. C. Galland. 1987. Body Mass as a Factor Influencing Dominance Status in American Bison Cows. Journal of mammalogy 68(3):683-685.

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Novakowski, N. S. 1965. Cemental Deposition as an Age Criterion in Bison, and the Relation of Incisor Wear, Eye-Lens Weight, and Dressed Bison Carcass Weight to Age. Can J Zool 43:173-178.

Price, M. A. W., R.G. 1985. Chapter 9. Growth and Development. In: R. J. W. Hudson, R. G., editor, Bioenergetics of Wild Herbivores. CRC prese, Boca Raton, FL. p. 183-213.

Rutley, B. D., and R. J. Hudson. 2000. Seasonal energetic parameters of free-grazing bison (Bison bison). Canadian Journal of Animal Science 80(4):663-671.

Rutley, B. D., C. M. Jahn, and R. J. Hudson. 1997. Management, gain and productivity of Peace Country bison (Bison bison). Canadian Journal of Animal Science 77(3):347-353.

Stanton, T. L. S., D.; McFarlane, W.; Seedig, R.; Stewart, D. 1996. Concentrate level in bison finishing rations on feedlot performance. Professional Animal Scientist 12:6-11.

Towne, E. G. 1999. Bison performance and productivity on tallgrass prairie. Southwestern Naturalist 44(3):361-366.

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III. Reproduction

Summary

The Darwinian drive to survive is fully evident in bison; their homeorhetic mechanisms and controls evolved to fit their climate, terrain, ambience and food supply and to synchronize cost/benefit ratios that determine survival of the species. Breeding season in early summer is a manifestation of all that biological synchrony. Successful conception restarts the cycle of life and early summer is the best time to do it. The risks and challenges are serious and severe; 50 to 75 % of pregnant females might wean a calf the following spring; younger females, or females that overcame short food supply, severe winter weather or trauma from disease or combat often forgo consecutive calvings, not from conscious effort but as a result of those homeorhetic controls that sent the message, “Not this time.” More successful females combine genetic capacity, and experience that somehow result in more offspring, a greater contribution to the gene pool than less successful herd mates, a process the often requires aggressive behavior to accomplish that goal. Life is simpler for males, and the probability of a bull making a contribution comparable to that of the average female is low; ‘survival of the fittest’ has a direct physical effect on the bison bulls’ success or no success in terms of affecting the gene pool. Of course, there are other contributions made by bison, in the give and take of operation of the ecosystem, eat, the alterations to the landscape, the plants that they and the organisms that eat them when they die. This section will discuss how research and application of results have improved human understanding and application of bison biology.

Introduction

Reproduction is a progression of dramatic events from calving, nursing and social interactions of newborns to the violent interaction of bulls vying for the privilege of breeding during the rut. The calm interlude of fall, winter and spring obscures events that proceed behind the scenes to potentiate recurrence of the main events next year. Calves are prima facia evidence of a renewable resource. Economic and conservation interests encourage better understanding of reproductive biology and behavior, to take full advantage of fecundity to create marketable products of recreation, tourism, bison meat, hide hair, and skulls, or to create a better, more balanced, natural environment.

Males

When are young bulls ready to breed? Helbig et al. (2007b) evaluated prepubertal testicular development and semen quality in bison ranging from 13 to 24 mo of age and weighing 263 to 475 kg. They also collected fecal samples from the bulls to measure changes in testosterone levels. The bulls reached puberty at 16.5 ±2.5 mo, with age being the most significant factor affecting puberty. They conclude that 2-yr old bulls should be ready for a breeding soundness examination, and that younger bulls that failed the exam should be given a second chance when they are 2 yr old. In general, larger testicles and therefore scrotal circumference are positively correlated. Scrotal circumference is useful indicator of reproductive competence in terms of semen production, spermatozoa motility and morphology. In bison 28 to 30 mo of age, scrotal circumference ranged from 22.0 to 37.0 cm and averaged 28.9 cm (Keen et al., 1999); based on their data, they recommended a minimal ‘satisfactory’ rating was 29 cm. Scrotal circumference increased from 32.4 to 40.7 cm, as age increased from 1 yr to over 6 yr (Komers et al., 1994a). As with other aspects of bison’s annual cycle of biological and behavior activities, male reproductive potential ebbs and flows with the time of year. (Helbig et al., 2007a) collected data from testicles from 288 bulls that were commercially slaughtered monthly over one year. Semen and feces were collected from 21 bison, 2.5 to 6 yr old. Carcass and testes weights were correlated, but the major factor affecting weight and morphology of testicular tissues was season of the year, with significantly greater testicular weights, seminiferous tubule and lumen diameter, and epithelial thickness in summer than in other times of the year. Sperm percentages, and motility, fecal testosterone, and body weight were greater in June, before breeding, than at other times of year. The live bulls gained weight in spring and summer, and lost weight in fall and winter. They conclude that bull evaluation should be done as close to breeding season as possible, when bulls are their biological best.

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Cryopreserved and thawed epidydimal sperm had significantly greater post-thaw motility (36 Vs 31%) and in vitro fertilization rate (30 vs 14%) from 61 bulls killed in July to September than 61 bulls killed in January to March (Krishnakumar et al., 2015). Recent work from the same group found an association between season of the year and ability of two key seminal fluid proteins, BSPS and TIMP-2, to modulate sperm function in a manner consistent with increase potency during the breeding season of bison bulls (Krishnakumar et al., 2017).

Expression of connexin43, an intercellular communication protein associated with testicular development, was relatively greater in reproductive tissues from European bison bulls as they entered puberty (Hejmej et al., 2009). These researchers also noted that Connexin43 activity was markedly reduced or absent in bulls that had impaired spermatogenesis, and suggested a potential link to homozygosity, or inbreeding. The potential adverse effects of inbreeding are a concern for those studying European bison, and potentially, American bison as well. A study of 461 bulls over 5 decades found that the prevalence of cryptorchidism was positively correlated with the coefficient of inbreeding (Czykier et al., 2016). They reported 18 cases overall, with more cases in the earlier decades, when inbreeding was greater.

In bison as well as in other animals, artificial insemination is an attractive way to accelerate genetic change and perhaps reduce risk of disease. As in other animals, a major challenge to is store, or preserve semen at very low temperature, then thaw it in preparation of insemination, without losing sperm viability. McHugh and Rutledge (1998) described how in vitro fertilization could be used to evaluate semen from bison. Pegge et al. (2011) used such a technique to show that semen from 5 age-matched bulls was equally potent in in vitro fertilization (83%).

Perez-Garnelo et al. (2006) collected semen from a mature European bison bull and used it to show that semen extended with Trialdyl® or a synthetic product. Other than acrosome integrity, which was significantly greater for Trialdyl® (57 vs 43%), other measures, e.g., motility (87%), viability (80%) and in vitro oocyte zona penetration assay (53%) were similar for the two extenders.

Lessard et al. (2009) collected semen by electroejaculation from 5 bulls, and post-mortem from the epididymis of 7 bulls, and cryopreserved samples in commercially available extenders (Trialdyl® and Andromed®). Sperm motility decreased from 50 to 80% before cryopreservation to 15 to 30% after cryopreservation and thawing, with significantly greater motility for samples extended in Trialdyl® vs. Andromed®. They noted that post-thawing motility in epidydimal samples extended with Andromed® (15%) was significantly greater than motility electro ejaculated samples with the same extender. Krishnakumar et al. (2011) reported on similar research with epidydimal sperm from 11 bulls that showed no difference in motility (34%), viability (37%), acrosome integrity (76%) and in vitro fertilization (20 % blastocysts) in samples extended with Trialdyl® or Andromed®.

Kozdrowski et al. (2011) collected epidydimal spermatozoa post-mortem from two mature European bison bulls, treated samples with two custom-made and one commercially available extender (BioXcel®), cooled the diluted semen to 5° C, then stored the samples in liquid N. spermatozoa motility decreased for 60 to 70% (before treatment) to 11 and 13% (after thawing). Two of 39 female cattle (Bos Taurus) became pregnant after artificial insemination. Hussain et al. (2011) compared the effects on sperm viability of commercially available extender (Triladyl ®) with custom made tris-citric acid compared at 3 freeze rates. They found that either extender could be used for bison semen, and that freezing at -40°C/h is needed to improve post-thaw semen quality. Subsequently, this same group searched for ways to improve post-thaw quality by pretreatment with extender (Triladyl ®) before cryopreservation, and found that cholesterol-loaded cyclodextrin, but not reduced glutathione, zwitterion-based extenders Tes-Tris or HEPES-Tris, or various temperatures of glycerol addition (Hussain et al, 2013). Chilling semen from 14 bulls for at least 48 hr before cryopreservation maintained sperm motility after thawing (Krishnakumar et al., 2013) but in vitro fertilization assay indicated variation among bulls in potency after the cryopreservation procedures. Results of Aurini et al. (2009) and Vilela et al. (2017)support the concept that epidydimal sperm can be maintained, or preserved at 5° C up to 48 hr prior to cryopreservation without appreciable loss of sperm viability bases in vitro fertilization assay.

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Reproduction – female

Most of the research effort in female reproductive function borrows from work done with domestic farm animals that establishes the time frames around estrous cycles, length of gestation, maternal behavior around calving and nursing, and then rebreeding. Bison females become sexually competent by 2 yr of age (and calve at 3 yr of age), but they may calve at 2 yr of age (McHugh, 1958; Halloran, 1968; Lott, 1979; Lott and Galland, 1987; Kirkpatrick, 1993; Berger, 1994). Fecundity is highest between 3 and 13 yr of age; A 5-yr study in one conservation herd found that 75% of 10- to 11-yr olds produced a calf annually; fewer than 30% of females older than 13 yr and 4% of 2-yr-old females produced young. Bison are seasonally polyestrous, with 21-d cycles that have been reported to vary between 19 and 26 d (Kirkpatrick, 1993; Vervaecke and Schwarzenberger, 2006). However, females may calve any time of year depending on nutritional status, climate, and management protocol (Green and Rothstein, 1993a),

Females are in ‘heat’, or estrus, for 1 to 2 d that include copulation (Vervaecke and Schwarzenberger, 2006). In conservation herds, females are fertile for one or two cycles in the spring, resulting in a synchronized calving that allows one-half of the calves to be born within 27 d, and 80% to be born within 70 d (Rutberg, 1984; Green and Berger, 1990; Berger, 1992; Green and Rothstein, 1993a; Berger, 1994; Berger and Cain, 1999; Gogan et al., 2005). Other herds have shown less synchrony, with calving seasons that last over 90 d for 80% of the calves (Wolff, 1998; Wolfe et al., 1999). Transrectal sonography of ovaries of females at 2.5 yr confirmed regular and synchronous follicular development that coincided with FSH concentrations in blood (McCorkell et al., 2013). Their results also support absence of ovulation in January and February.

Gestation ranges from 262 to 293 d with a putative average of 275 d (Haugen, 1974; Berger, 1994; Vervaecke and Schwarzenberger, 2006). Factors like body condition, feed availability and weather can cause both breeding season and gestation length to vary (Berger, 1992; Berger, 1994; Gogan et al., 2005; Vervaecke and Schwarzenberger, 2006). With the exception of two sets of twins (McHugh, 1958; Halloran, 1968), multiparous births are unreported (Lott and Galland, 1985; Rutberg, 1986b; Green and Rothstein, 1991a; Berger and Cunningham, 1994; Wolfe et al., 1999).

Calf sex ratio did not vary significantly from 1:1 in 256 births over 7 yr in a conservation herd (Towne, 1999); in one year the ratio was 21:40 male:female. Shaw and Carter (1989) and (Green and Rothstein, 1991b) likewise reported essentially 1:1 ratios; Others found ratios in embryos and unborn fetuses that favored males over females (Haugen, 1974; Rutberg, 1986b).

Green and Rothstein (1993b) concluded that most calves were weaned within 3 mo of calving; however, nursing behavior may continue from 17 to 21 mo for nonpregnant females and 9 – 12 mo for pregnant females (Green, 1990). In her review of bison (Meagher, 1986) reported that most calves are weaned on or before 12 mo after calving. Calf mortality rates are less than 5% (Green and Rothstein, 1991c; Berger, 1994).

Overall productivity, or generation of the next generation, can be measured by pregnancy rates, calving rates, and by ratio of adult animals:calves in a herd. Pregnancy rate or calving rate (percentage of females diagnosed as pregnant after breeding or having a live calf at the time of data recording) averaged 46 % over a 10-yr period (Wolfe et al., 1999), 88 % over 3 yr (Rutberg, 1986b), 63% over 7 yr (van Vuren, 1986), and 72% over 8 yr (Shaw and Carter, 1989). (Larter et al., 2000) reported annual calving percentages over 14 yr that ranged from 24 to 53% annually, reflecting relatively more negative pressure from the environment and predators in Canada than in the U.S. Fecundity, or ability to produce calves, increases as females reach 4 yr, and maintains a high level, greater than 70%, until females age reach their ‘teens’, and then gradually decreases (Halloran, 1968; Shaw and Carter, 1989). Berger and Cunningham (1994) collected data on 58 females over 5 yr and found that 17% had no offspring, 4% had one calf, 46% and 2 or 3 calves, 9% had 4 calves, and 26% had a calf every year (numbers do not sum to 100 due to rounding).

Adult:calf ratio in two conservation herds ranging from 216 to 3,376 animals per year over 7 yr ranged from 0.14 to 0.31 (Fuller et al., 2007). They found that snow cover and, for one herd, drought index, correlated with adult:calf ratio in a logical manner; adverse weather and climatic conditions reduce fecundity in bison herds.

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(Pyne et al., 2010) collected 1,154 observations from females over 7 yr from a conservation herd and found that the probability of pregnancy in females 1.5 to 3.5 yr old was 0.8, the probability of pregnancy in females that had not calved the previous year was 0.68 for females 4.5 to 12.5 yr old, then decreased to 0.2 for females 13.5 yr old and older. For lactating females the probability of pregnancy the following year was 0.2 for females 4.5 to 12.5 yr old, then decreased to 0.17 for females 13.5 yr old and older. The cow:calf ratio ranged from 0.32 to 0.60, and male:female sex ratio for calves in the study was 0.99

The comprehensive study of (Kirkpatrick et al., 1996) that included over 3,000 females in a 3-yr study of two conservation herds provides the following time line: Approximately 85% of cows were in estrus, 76% of the females had ovulations. Nonlactating females (ostensibly did not raise a calf that year) accounted for 78% of detected fall pregnancies. Greater than 80% of all pregnancies were in females 4 yr old or older, and 100% of all pregnant, lactating females were 5 yr old or older. We can conclude that the number of live calves and the pregnancy rate are lesser for lactating vs. nonlactating cows, due mainly to lack of ovulation in lactating females, primarily caused by ovulation failure, and lactating females that successfully reproduce (females that will have calves two years in a row) are 5 yr old or older. In a prior study, Kirkpatrick et al (1993) showed that about 85% of mature but only 15% of lactating females had calves on alternate years. Their data indicate that anovulatory lactation explained the lesser rate.

Techniques and technologies designed to enhance or preserve the quantity or genetic quality of offspring have been evaluated for application in bison. Estrous synchronization, superovulation, artificial insemination, aspiration and cryopreservation of embryos has been investigated in bison (Matuszewska, 1996; Thundathil and Whiteside, 2007; Thundathil et al., 2007; Palomino et al., 2013; Palomino et al., 2014a; Palomino et al., 2014b; Palomino et al., 2015; Palomino et al., 2016; Palomino et al., 2017a; Palomino et al., 2017b). Results indicated that the strategy has merit, and they also indicate that while embryo and follicles can be produced and recovered during the anovulatory season of year, the response is inferior to that in the ovulatory season, again emphasizing the genetic and behavior proclivity of bison to conceive calves once a year, in the spring. Similarly, (Krishnakumar et al., 2015) found that oocytes from females during breeding season performed better in in vitro transfers and manipulations that oocytes collected during the non-breeding season. Toosi et al. (2013) synchronized ovulation in 20 bison to evaluate method of synchronization and subsequent embryo transfer. They found that a single dose of follicle stimulating hormone provide more ova and embryos than two doses. They collected embryos from 5 donor females that were transferred to bison recipients and ultimately produced live offspring. Rasmussen et al. (2005) fertilized bovine oocytes in vitro with bison semen to study the pattern of secretion of embryonic signaling molecule interferon tau

A key piece of management information is determination of ovarian activity (in anticipation of natural or artificial insemination) or pregnancy. Bison females can be evaluated by techniques used with bovine, uterine manual palpation or ultrasonic imaging via the rectum, which requires animal restraint. Evaluation can be based on hormone levels in blood plasma or serum, again requiring animal restraint for blood sampling. (Love et al., 2017) used as commercial BioPRYN® ELISA designed for detection of pregnancy in bovine and found that the assay completely recognized bison pregnancy- specific protein- B and accurately predicted pregnancy in 45 of 49 bison. Haigh et al. (1991) likewise found pregnancy- specific protein- B to be and effective tool to monitor pregnancy in females. Alternatively, evaluation of fecal or urinary concentrations of hormones, derivative of hormones, or other metabolic markers can provide non-invasive, restraint-free information. Ovulation was detected by increased urinary pregnanediol-3-delta (PdG) or increased fecal progesterone concentrations (Kirkpatrick et al., 1992). Both PdG and fecal total estrogens (TE) were 100% accurate in predicting pregnancy in the 18 females in the study. A prior study with 5 females also showed 100% accurate pregnancy prediction with increased urinary PdG concentrations (Kirkpatrick et al., 1991).

In contrast to a desire for increased population numbers, some situations, like limited feed resources and potential control of disease, prompt interest in birth control in bison. Gonadotropin releasing hormone vaccination, and porcine zona pellucida vaccine (with appropriate adjuvants) are two successful methods in

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several species (Kirkpatrick et al., 2011). Authors expressed some concern that the aftermath of a porcine zona pellucida vaccination might cause a positive test to tuberculosis. A single dose of gonadotropin releasing hormone will prevent pregnancy in bison for up to one year (Miller et al., 2004).

Interest in understanding the very first steps in reproductive biology led to experiments with interspecies somatic cell nuclear transfer between oocytes from bovine and bison. Embryo development up to the 8-16 cell stage did not differ significantly between interspecies somatic cell nuclear transfer of ooplasm from the two species. Nor were any negative effects observed as a result of the manipulation (Gonzalez-Grajales et al., 2016a). Subsequently studies with oocytes of Bos Taurus, American bison and European bison found some developmental differences after interspecies somatic cell nuclear transfer manipulations, but did not clarify mechanisms for the molecular changes observed (Gonzalez-Grajales et al., 2016b).

Reproductive behavior

Studies of reproductive behavior center around two major annual events, breeding (the rut), and parturition and subsequent care of offspring. Researchers have developed protocols, or descriptions of behavior in order to quantify, objectify, and share information. Individual animal identification, date, time, location, identification of the human observers, or type of equipment are essential. Other information on weather, terrain, other animals is useful, sometimes essential, but less frequently recorded. The observer and accoutrements should not interfere with the animals’ behavior. For example, Maher and Byers (1987) quantified and statistically evaluated when bulls’ interactions were chin, jump away, mount, move away, run away, spar (greater in younger bulls than older), back up, chase, clash, displace from cow, fight, head nod, lower head, move toward, parallel stand, push heads, run toward, swing head, turn head away, walk away (greater in older bulls than younger). Green and Berger (1990) quantified cow-calf interactions by recording duration of nursing/bout (minutes), interbout interval (hours), nursing time (minutes/hour), rejected suckling attempts/nursing minute, % of bouts ended by calf, interruptions by mother/bout, interruptions by calf/bout, duration of calf’s pauses (seconds), % bout interruptions by mother, mother’s reactions to calf’s bunting/bout, contact initiated by mother/hour, contact initiated by calf/hour, and % contact initiated by mother. The time investment by the researchers is almost unimaginable. Clearly, the researchers agreed beforehand on definitions of terms, and likely trained beforehand to synchronize numerical scoring among themselves.

Bull calves become sexually competent at about 12 -16 mo (Haugen, 1974; Helbig et al., 2007b); a putative weight would be 300 kg. Competition for breeding rights during the rut will come when they are 5 to 6 yr old (Maher and Byers, 1987), and weigh about 800 kg (Wyman et al., 2012). In the meantime, they are weaned and begin their social association with other males and interact with their contemporary female herd mates (Jezierski et al., 1989; Rothstein and Griswold, 1991). Between ruts, older bulls segregate from herds, living alone or in small groups (Komers et al., 1993; Komers et al., 1994a; Mooring et al., 2006b). Although it is not certain, most likely the rut begins when bulls detect products of reproductive cycling activity in females’ urine. Bulls change their daily activities routine by spending less time eating, drinking, ruminating, self-grooming, and more time walking, wallowing, scent marking exhibiting flemen response, vocalizing, and increasing agonistic behavior against other bulls (McHugh, 1958; Berger, 1994; Mooring et al., 2006a; Mooring et al., 2006b;

Bowyer et al., 2007; Wyman et al., 2008; Wyman et al., 2012). Mature bulls lose a minimum of 10% of their

body weight during the rut owing to a combination of sharply reduced feeding and sharply increased,

energy-costly social interactions (Lott, 1979). Concentrations of the androgens (Mooring et al., 2006b) and corticoids (Mooring et al,2006a) in blood increase (as measured in increased concentrations in urine and feces) as the stress of the rut grows. Bulls bellow in agonistic behavior against other bulls, not to affect female estrus (Berger and Cunningham, 1991); and the frequency of the vocalizations is linked to breeding success (louder and more frequent bellows from aspirants vs. achievers, Berger and Cunningham, 1994; Wyman et al., 2008;2012). A bull tends cows that are perceived as likely mates, fends off other bulls, and finally mounts the cow, copulates and ejaculates in a brief (seconds) end to the process (Maher and Byers, 1987). The positioning of the cow’s tail through mating is distinctive, and is used by researchers as a key indicator of copulation (Lott, 1981; Berger, 1989; Komers et al., 1992; Wolff, 1998). He may continue to tend the cow for a while (Lott, 1981;

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Wolff, 1998), or move to another prospect. As the cow’s estrous cycle terminates with a pregnancy or no pregnancy, she no longer sends the signals that attracted the bull in the first place.

(Lott, 1979) reported that in a group of 26 bulls, neither age nor body weight were correlated with high social status, and the bull’s social status, his ‘rung on the ladder’, is positively related to his breeding activity. He also noted that 88% of bull/bull interactions during rut were ‘won’ by the initiator. Others have reported bulls highest in social order, ostensibly by ‘winning interactions’, have the greatest breeding success (Berger and Cunningham, 1994; Wolff, 1998). As bulls age beyond 5 yr they become more solitary, eat less and walk more between ruts, are more aggressive against other males, and more attentive to cows than they used to be (Komers et al., 1992; Berger, 1994; Komers et al., 1994a; Komers et al., 1994b). The bulls ostensibly leave groups to recover from the rut more than to search for more females. Therefore, winning aggressive interactions does more to determine mating success than head size, body mass (weight and height), or travel distance (Berger and Cunningham, 1994). It is also relevant to note that dominance in aggressive interactions is temporal; a given bull may not win future interactions at different times and locations. After the rut, bulls’ head hair, beard and pantaloons (hair on the lower forelegs) regresses, ostensibly in response to changes in hormonal status (Lott, 1979.

Females show dominance in herds, and that dominance appears to be more associated with age (keeping in mind the close, but not absolute, positive relation between age and weight) than weight by itself (McHugh, 1958; Rutberg, 1983; Rutberg, 1986a; Berger, 1994). After statistically accounting for age (Green and Rothstein, 1993b) found correlation between dominance and reproductive success, but Berger and Cunningham (1994) did not. Apparently, other factors have effect here, including level of confinement or freedom of range for the herd (Lott and Galland, 1985; Lott and Galland, 1987). A common theme among data sources is that females that were born early in the calving season maintain a reproductive advantage throughout their maternal careers through items like good body condition, shorter gestations and relatively high social status (Green and Rothstein, 1993a, b).

Literally and metaphorically, female bison bear the brunt of time and effort expended in parenting during their 3- to 18-yr careers as mothers; they are responsible for gestation, parturition, and nursing offspring. Reports of parturition (calving) vary in specifics and rationale, e.g., calving within or apart from other bison, in the open, in the trees, in response to putative predators or not. Consistent among reports (for example, Lott and Galland, 1985; Berger and Cunningham, 1994) is that parturition is quick, neonates are standing and nursing within minutes of birth, and are quickly able to travel. No reports of pre-term abortions or still-birth were found in publish literature. Calves gradually transition from nursers to grazers and from close maternal contact to integration into the herd during the first 3 mo of life (Green, 1992b, a; Haßpacher and Sambraus, 2005). Older cows spend more time nursing than do younger cows (Green, 1986).

“Weaning” is a gradual, complicated process that involves cessation of suckling(nursing) and complex, often aggressive interactions between mothers and their calves (Green et al., 1993). For male calves, that effort ceases at weaning, but contact between mothers and daughters may continue until daughters are sexually mature (McHugh, 1958; Green et al., 1989; Green and Berger, 1990; Green et al., 1993). Bison cows have been found to weigh more when barren than after calving, suggesting that the former are in better body condition and ostensibly more likely to be fertile. ((Green and Rothstein, 1991c; Craine et al., 2015). Daughters do not appear to retain and special relation with their mothers after daughters reach maturity (Lott and Minta, 1983).

A chronology of the rut demonstrates interactions between male and female sexual behavior (Berger, 1989). The period covered was July 5 to August 10, 1985, during which 164 females were deemed to have exhibited estrus by virtue of observed tending by a bull, copulation and/or ‘tail up’ behavior. Females, chronologically first to last were barren females (previously had a calf, but none in 1985), females with daughters, females with sons, and nulliparous females (at least 3 yr old, never had a calf). The curve of estrous behavior was skewed to the right, with a plateau of about 15% in estrous until July 25, a quick increase to about 35% in estrous on July 30, followed by a decline to none in estrous by August 10. Concomitant flehmen activity by bull followed the same sequence: early interest in barren females, followed by attention to lactating females,

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ending with attention to nulliparous females at the end of the rut. Older bulls, 31 bulls at least 6 yr old, were active early in the rut, with breeding activity essentially over just after the peak prevalence of estrus, where about ½ of the females had shown estrous behavior. Younger bulls, 21 bulls 2 to 5 yr old, had three bursts of activity, from d 9 to 12, d15-18 and d27-30 of the rut. The results fit the teleological rationale that allow dominant, older bulls to breed the most fertile females, with the younger bulls looking for opportunities. That is followed by younger bulls breeding younger, lighter females, with both sexes representing the latest version of the gene pool. The time frame allows for more than one estrous cycle, which can explain the discrepancies between copulations and conceptions discussed below.

Two problems, or apparent contradictions, exist in interpretation of reproductive behavior data. First, estrous (biological active ovaries) and fertility are not synonymous, and second, copulation and conception are not synonymous. Additionally, scientific reports based on well-intentioned, but limited observations due to time or the size of the bison population studied, may lead to spurious conclusions or generalizations. A case in point is reported variation in length of gestation. Because measures of gestation length are a function of observed copulations in most studies, it is possible (and likely) that much of the reported variation in gestation is in fact the observed copulation did not result in conception, and there was another 21-d estrous cycle and subsequent copulation that resulted in conception. Green and her colleagues studied from 300 to 775 animals for 5 yr in one conservation herd and from 300 to 400 animals for 8 yr in another herd. Berger and Cunningham (1994) and their cohorts spent 8750 hours (there are 8760 hours in one year) over 5 yr observing one of the same herds as Green. Wilson et al. (2002) used DNA techniques to establish paternity in 253 calves and maternity in 295 bison calves over 4 yr of study; there were animals in the herd that avoided annual roundups. (Mooring and Penedo, 2014) studied a conservation herd containing from 101 – 125 breeding age bulls and from 112-150 breeding age females for 7 yr. Green and Berger (1990)reported that 10% of the males accounted for 50% of the copulations, and Berger and Cunningham (1994) reported that 10% of the males accounted for 50% of the copulations. Mooring and Penedo (2014) established parentage through DNA techniques, and found that 56% of copulations represented conceptions, and 40% of conceptions (live calves) accurately predicted the sire identified by observation. On average across years, about 8% of bulls observed to copulate sired no calves, and about 16% of sires were never observed to copulate. The authors note that, despite dawn-to-dusk observations in nearly ideal conditions, over the course of their study they did not observe 60% of the copulations.

Over 4 yr, from 35 to 40% of bulls sired at least one calf each year, and at least 60% of the mature bulls sampled sired at least one calf (Wilson et al., 2002). In the same study, from 50 to 70% of females delivered a calf each year, and at least 81% of the females delivered at least one calf over 4 yr. Of females observed to copulate or exhibiting tail-up behavior by Mooring and Penedo (2014), 56% became pregnant and delivered a calf. On a smaller scale, 4 small, private herds (from 19 to 45 females) had cow:bull ratios ranging from 5:1 to 11:1, and from 2 to 5 bulls per herd (Roden et al., 2003). They established parentage through DNA techniques and found that in each herd, one bull sired from 75 to 84 % calves born. They analyzed data from four other small, private herds from 6 to 14 cows and found one bull sired 82% of calves (14 cows, 0 calves, 4 bulls) 89% of the calves (14 cows, 10 calves 2 bulls), or all the calves (6 cows, two bulls, or 6 cows, 3 bulls)

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IV. Genetics

Summary

The American bison and European bison narrowly escaped extinction, and both are re-established in numbers sufficient to obviate that fate. Advances in molecular and population genetics, application of techniques that reveal the intricacies of the genetic code, and advent of powerful computers to sort and make sense of huge databases will allow human custodians to minimize the genetic damage wreaked on bison. Further, information derived from this effort can and will be used to the benefit of other species on earth.

Introduction

Halbert et al. (2007), Hedrick (2009), Giglio et al. (2016) and many others have summarized the history of the genetic bottleneck and conservation efforts to first, avoid extinctions of bison, and second, to restore them, at least in part , to their role in grassland ecosystems. The chromosome diploid number in bison is 60; there are 29 pairs of autosomes and one pair of sex chromosomes (Basrur and Moon, 1967; Bhambhani and Kuspira, 1969). Except for differences in the Y chromosome, (Bonfiglio et al., 2012), this array is similar to that of cattle (Bos taurus). Blood types of bison and cattle also are very similar (Owen, 1958; Stormont, 1961). Twenty of the 29 autosomal pairs and the sex chromosome of Bison bison bison (Bb) and Bison bison athabasca (Ba) are homologous (the same); the remaining 9 autosomes were not characterized (Ying and Peden, 1977). More advanced cytogenetic techniques detailed the differences among species of the subfamily Bovinae, including Bb and European bison (Eb) ((Treus, 1997). Contrary to progeny of cattle and Bb, progeny of Bb and Eb are fertile (Verkaar et al., 2004). Phenotypic variation in Bb and Ba populations in Canada was described by van Zyll De Jong et al. (1995) and this presentation will subscribe to the conclusion of Cronin et al. (2013) that Ba and Bb are not phylogenetically distinct.

Advances in molecular genetics and genomics

The door was opened by the ability to determine the amino acid sequence of proteins, and the breaking of the genetic code. Those advances describe how sequences of DNA and RNA, small sets of nucleic acids in chromosomes and ribosomes code for specific amino acids; amino acids join to make proteins to sustain life as we know it today. Those advances were followed by development of techniques to enzymatically chop strings or DNA or RNA into pieces, to copy those pieces many times to build up sample volume, to use electric current through a starch gel and high-speed centrifuges to separate fragments, all followed by automated analysis of the nucleic acid sequences in the fragments. The key to successful application of all these laboratory procedures is the computer, the machine that stores, statistically analyzes, and shares literally tons of information, if you were to print it on paper. All that information allows those interested to find nucleotide sequences that correspond to a given amino acid sequence, which in turn reveals the gene, or genes, associated by manufacture of that protein. Molecular geneticists exploited the use proteins of known composition to search for DNA sequences, genes, and variations of genes, on DNA located in the nucleus (chromosomes) or mitochondria of almost all the cells in an organism’s body. That molecular variation points to the time course of parentage, from the current generation to generations of ancient animals far up the evolutionary chain. Imagine yelling, “Who’s your daddy?” or “Who’s your momma?” into a large echo chamber or large canyon, and getting an answer from each echo. Following is by in large a chronology of research in this area that pertains to bison.

Ribonuclease A was isolated from bison pancreas (Stewart and Stevenson, 1973). Bison have two Hb phenotypes, initially thought to be products of two, nonallelic structural genes and their alleles (Harris et al., 1973). That was clarified by Scaloni et al. (1998). Carleer et al. (1978)Identified cell culture lines in the American Type Culture Collection with enzymatic polymorphisms distinctive for bison. These proteins could be used as genetic markers. Similarly, amylase isoforms that could be used as genetic markers were defined (Steklenev and Rozhkov Iu, 1990). A polymorphism of kappa-casein is linked to DNA sequences and alleles specific for several (Cronin and Cockett, 1993; Ward et al., 1997; Woollard and Dentine, 1999). Bos and Bison genera each have a distinct gene, and they share a gene.

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Cotinot et al. (1991) catalogued Y-chromosome DNA probes, and found two that are specific for Y chromosome for Bos and Bison genera. These probes could be used for sex determination of cultured cells. The SRY gene (sex determination on Y chromosome) was cloned and showed similar structure among bison and other ungulate species (Payen and Cotinot, 1994). Sequences of mitochondrial DNA (mtDNA) were isolated, including mitochondrial D-loop variations from bison, cattle, and other ungulates (Miyamoto, 1989; Murray et al., 1995). Perret et al. (1990) isolated polymorphic satellite sequences of the bovine Y chromosome, and starch-gel electrophoresis of bison DNA was used to identify DNA sequences known to code for specific proteins (McClenaghan Jr et al., 1990).

Polymerase chain reaction (PCR) primers specific for the bovine lymphocyte antigen gene were amplified, and showed that bison and cattle genes are similar (Morris et al., 1994). PCR and fluorescent in situ hybridization (FISH) of Zinc finger protein gene showed its amplification in Bos but not Bb or Eb, buffalo, sheep or goats (Chalony et al., 1996). Gallagher Jr et al. (1999) used a color-banding technique, FISH, and distribution of nucleolar organizing regions (NOR) to clarify evolution of the X chromosome in Bovinae species. Nucleotide sequence of the mitochondrial cytochrome b gene in several species was used to detail the phylogeny of Bovidae (Hassanin and Douzery, 1999). Telomeric markers were developed to create DNA ‘fingerprints’ that help clarify interspecies relations (Semenova et al., 1999; Semenova et al., 2000; Vasil'ev et al., 2002).

Chromosome mapping of microsatellite sequences was used to study early embryonic development (Piedrahita et al., 1997), and parentage of bison (Mommens et al., 1998). PCR, random amplified polymorphic DNA (RAPD), and gene sequencing technology identified species-specific and intraspecific genetic markers for Bb and Ba; ((Glazko, 1999; Wilson and Strobeck, 1999; Wilson, 1999; Schnabel et al., 2000; Nijman and Lenstra, 2001; Modi et al., 2004).

Molecular cloning and cDNA expression described genes associated with production of cytochrome P450 17 alpha from sheep, goats, and bison (Gilep et al., 2003) and CD18, a leukocyte receptor associated with the disease Mannheimia haemolytica (Shanthalingam et al., 2010). Verkaar et al. (2003) used established techniques, PCR-restriction polymorphism and competitive PCR assays, to elucidate the Y-chromosome of cattle, Bb and Ba. (Schnabel et al., 2003) developed a Quantitative Trait Loci (QTL) map, or library, for bison.

Microarray chip and single-nucleotide polymorphisms (SNP) were used to characterized genes associated with milk protein synthesis within and among species (Kaminski et al., 2005). Variation in gene expression revealed the toll-like receptor 4 (TLR4) in bison, a gene involved in cellular immune response to several diseases (Wilson et al., 2005), and evolution of cattle and bison from an ancient common ancestor (MacEachern et al., 2009a; MacEachern et al., 2009b; MacEachern et al., 2009c; Pertoldi et al., 2009a; Pertoldi et al., 2009b). Mikko et al. (1997), Traul et al. (2005)and Takeshima et al. (2008) used immunogenetic assays to describe polymorphisms of the major histocompatibility complex (MHC) as a way to clarify evolution of species of cattle and bison.

Random amplified polymorphic DNA (RAPD), fluorescent in situ hybridization (FISH) and DNA sequencing were used to identify new, bovine-male DNA sequences on the Y chromosome (Alves et al., 2006).

The growth hormone gene has been defined for bison (Varvio et al., 2008). It would be an attractive quantitative trait loci, a candidate gene, for traits affecting milk yield and milk composition. However, (Musani et al., 2006) was not able to show statistically significant relationships among 60 microsatellite genetic loci and herd location, sex, and age of 1,316 bison sampled from 4 conservation herds. They did show that the herds had ancestral connections and that the interaction between the trait loci and ancestry were statistically associated with phenotypes.

The value of population genomics as a tool for wildlife management was demonstrated by (Gompert, 2012), using bighorn sheep as an example; genomics improved understanding of male gene flow which will change estimates of biparently and maternally inherited markers (Hedrick et al., 2013), Two genes associated with function of the zona pellucida, specifically in controlling sperm access are shared by Bos and Bison species, partially explaining the capacity for cattle and bison to interbreed (Chen et al., 2011).

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(Suzuki et al., 1979) used the enzyme 6PGD as a species marker that showed differences between bison and cattle. Use of reference genomes in cattle, swine, sheep, goat, water buffalo and bison allowed completion of gene maps of other mammalian species, and to identify variation associated with disease (Kalbfleisch and Heaton, 2014). However, (Taylor et al., 2016) expressed some reservations and cautions in development and application of whole-genome sequences.

Gene maps were used to trace strains of B. abortus and then the process of brucellosis infection among cattle and bison in the Greater Yellowstone Ecosystem (O'Brien et al., 2017). Differences in detection of the prion protein gene in cattle and bison provides evidence of an association between this protein and prevalence of Brucella spp antibodies in bison, as a component of bison’s natural resistance to brucellosis infection (Seabury et al., 2005). The nucleotide sequence for bovine A3 genes, associated with resistance to lentivirus has been described. This gene is found in several bovine species, including bison (Yamada et al., 2016).

We may be able to use artificial oligonucleotides separated by electrochemical impedance spectroscopy (EIS) and scanning electrochemical microscopy (SECM) to detect differences among cattle, Bb and Ba (Shamsi and Kraatz, 2011).

Introgression of cattle genes

Because of crossbreeding of bison and cattle during the late 19th and early 29th century, cattle mitochondrial DNA (mtDNA) and autosomal DNA are detectable in most bison (Hedrick, 2009, 2010). The decreased frequency of mtDNA versus autosomal cattle genes perhaps is due to bison bull X domestic cow crosses, and the fact all surviving progeny are females. Bovine mtDNA exists in several North American bison populations(Polziehn et al., 1995; Polziehn et al., 1996). Polziehn et al. also compared mtDNA from Bb and Ba and concluded that the potential gain in genetic diversity by moving individual bison among herds was not likely to improve genetic diversity, and may cause problems through disease transfer or other unintended consequences. Similarly, (Ward et al., 1999) found bovine mtDNA in 30 of 572 Bb and Ba tested. Subsequently, Halbert, Derr and other researchers at Texas A &M university began a series of investigations to describe and quantify the extent of inbreeding and introgression of cattle DNA in living bison. They found that Texas State Bison are extremely inbred (homozygous, with high calf mortality) (Halbert et al., 2004). This herd has one allele not found in other bison or domestic cattle. The herd contains 13 idealized individuals, which falls below the short-term minimum of 50 idealized individuals. Halbert et al. (2005) used linked microsatellite markers to search for domestic cattle chromosomal segments in 14 bison populations. Cattle nuclear introgression was found in 5 populations, and 6 populations were free of mitochondrial or nuclear introgression. Halbert and Derr (2007)looked for nuclear or mitochondrial introgression in 11 conservation herds. One population had mtDNA introgression. Nuclear introgression was found in 7 of 11 herds. Introgression confirmed historical accounts of transfers among herds. Neither nuclear or mtDNA was found in several herds, but Wind Cave National Park and Yellowstone National Park were only herds to meet 90% statistical confidence limits. The Texas A&M researchers estimated that 3.7 % of living bison carry cattle mtDNA (Douglas et al., 2011).

There likely is a measurable effect of introgression of bovine genetics on bison growth and size. Derr et al. (2012) collected data from the bison herd on Catalina Island in order to quantify body weight effects of introgression of cattle genes on bison phenotype. Bovine mtDNA was found in 48% of the Catalina Island bison herd, a herd that was established over 90 yr ago, and survives with limited feed resources (Vogel et al., 2007). Both females (194 head) and males and females combined (329 head) with bison mtDNA weighed about 10% more than animals with cattle mtDNA. Derr et al. (2012) also compared body weights of 618 bison males (about 10% had bovine mtDNA, the oldest were about 2 yr old) in a Montana feedlot (with free choice feed supply) with or without bovine mtDNA and found that those without bovine mtDNA consistently weighed about 10% less at each of 9 weighings over about 800 d.

Genetic diversity

Halbert and Derr (2008) Used a panel of 51 nuclear markers to evaluate genetic variation among 2,379 samples from 11 conservation herds, or about 1/3 of individual bison in those herds. They collected

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approximately equal samples from males and females. Despite the historic bottleneck, they found genetic diversity comparable to some breeds of domestic cattle. Why? They speculated that geographic dispersal at time of the bottleneck, and rapid increase in population growth after the bottleneck would have reduced potential for genetic drift and inbreeding, and (albeit unlikely) introgression as result of interbreeding with cattle. Why did they find as much genetic diversity among herds as they did? They point out differences in herd size and culling criteria, and that success of use of translocation to increase diversity depends on mating success of translocated individuals. To that last point, Berger and Cunningham (1995) talked about ‘wimpy bulls’ that were translocated from Nebraska to South Dakota, and failed to sire any calves. As result of their analysis, the Texas A&M researchers identify three conservation herds, the Nation Bison Range, Wind Cave and Yellowstone National Park herds, as critical, or important, germplasm resources because of their relatively high allelic richness and diversity of genes. These same herds are among those in which there is no detected introgression of cattle genes. They also recommend translocations among Fort Niobrara, Theodore Roosevelt South, and Theodore Roosevelt North herds; all are free of infectious diseases, and contain cattle introgression for the same source.

Halbert et al. (2012) analyzed samples from 661 bison that were culled from Yellowstone National Park between 1999 and 2003. Bison in the park divide genetically and geographically into two subpopulations, or clusters, that differ in genetic diversity and allelic distributions. One cluster had 6 private alleles, and the other had 14.; These alleles are present in other bison conservation herds with no known associated with Yellowstone populations. They found evidence of genetic overlap between the clusters, indicating movement, or association of individuals between the clusters. From a genetic perspective the herds look like populations that have been distinct in location and reproduction for over 40 years (5 generation intervals for bison). Similar evidence of genetic diversity in ostensibly related bison populations was recently reported by Ball et al. (2016).

Ranglack et al. (2015) found less heterozygosity and allelic diversity in a conservation herd than is found in other conservation herds (herds under the management of the U.S. Department of Interior, Halbert et al 2008), but Ungerer et al. (2013) measured similar heterozygosity and greater allelic diversity than that reported for the U.S. Department of Interior herds.

Cronin and Leesburg (2016) used variation and differentiation in DNA from 587 cattle representing 4 breeds and 188 bison from 3 locations to conclude that genetic variation that has been lost to bottlenecks or inbreeding can be recovered by astute breeding management. Similarly Giglio et al. (2016) compared three methods of management strategies to maintain genome variation and recommended measuring a suite of variable loci (mean allele frequency), measuring mean kinship as well as information of sex and age of a population (demographic stability). This work supports the earlier work from Texas A&M data on variability despite the bottleneck.

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V. Diseases

Summary

Information published in the past 16 years is the focus of this section, showing that main interests in bison contagious diseases continue to be parasites, brucellosis, tuberculosis, and malignant catarrhal fever.

General overview

The base for this summary is the review of bison diseases prepared by Dr. Murray Woodbury about 16 years ago (http://www.usask.ca/wcvm/herdmed/specialstock/bison/bisondis.html) and the comprehensive review of Haigh (2002). The summary will synopsize published information since those reviews. A common advance, or progress, involves the use of molecular technology to elucidate and clarify details of a given disease, for example, Kramsky et al. (2003) and Sausker and Dyer (2002).

Most of the reviews since 2002 have addressed problems linked to parasitism, and authors highlight this area as the most important, or most rapidly growing, area of concern (Demiaszkiewicz, 2014; Jolles et al., 2015). The role of infectious diseases in wildlife relative to domesticated species was reviewed (Nolen, 2004; Heisey et al., 2006). Shury et al. (2015) and Jolles et al. (2015) reviewed challenges and strategies associated with management of brucellosis and tuberculosis in bison. Taxis (2016) reviewed the potential of probiotics in herd health management.

Published work describes remote drug delivery systems (Benischek, 2006; Denisov et al., 2010; Falconer et al., 2016) and drug clearance and pathogen resistance to antibiotics (Štyriak et al., 2002; Boison et al., 2016).

Anthrax

Eleven publications generally chronicle outbreaks of the disease in conservation herds ((Dragon et al., 2005; Shury et al., 2009; Stratilo and Bader, 2012; Salb et al., 2014; New et al., 2017), and private herds (Himsworth and Argue, 2008; Mongoh et al., 2008; Blackburn et al., 2014). Lewis (2006) prepared a review of the disease published in Smoke Signals. A review of outbreaks between and 2012 in the Woods National Forest herd indicated a decrease in antibody titers over time (New et al., 2017). A similar historical perspective in the Wood Buffalo National Park and the Slave River Lowlands (SRL), Northwest Territories, found that the number of dead animals per outbreak declined over 4 decades. (Salb et al., 2014). This report also provides insight into the effects of time of year, length of outbreaks, and gender on outbreaks of anthrax. The potential role of predators and scavengers and local dissemination of B. anthracis spores has been elucidated (Dragon and Elkin, 2001; Blackburn et al., 2014).

Lee et al. (2007) established that B. anthracis produces biofilms that enhance the pathogen’s resistance to antibiotics. Phylogeny and characterization of B. anthracis types answered, and posed, questions about fine-scale typing of the pathogen (Stratilo and Bader, 2012).

Brucellosis

Twenty-nine publications focus on Yellowstone National Park, the prevalence of the disease, transmission among other species, and the controversy among conservationist, park managers, and private livestock owners and ranchers in the surrounding area. Many of these chronicle use and results obtained from molecular biological techniques to identify and clarify aspects of the disease, and its vectors

Reports have focused on presence of antibodies in bison and other wild species (Nymo et al., 2016). Bison appear to be more susceptible to the disease than cattle (Olsen and Johnson, 2011). A single nucleotide polymorphism in the bison genome I linked to natural resistance to brucellosis infection (Seabury et al., 2005).

Brucella exposure may be detectable with a breath test (Bayn et al., 2013). A single dose of GnRH vaccine is effective as a contraceptive, and therefore presents a potential avenue to control transmission of the disease by female bison (Miller et al., 2004).

http://www.usask.ca/wcvm/herdmed/specialstock/bison/bisondis.html

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Protocol and efficacy of vaccination with B. abortus strain RB51 to produce resistance or immunity (Olsen and Holland, 2003; Olsen et al., 2003; Olsen, 2010; Olsen and Johnson, 2012a; Olsen and Johnson, 2012b; Olsen et al., 2015). Salmakov et al. (2010) tested several live brucellosis vaccines and found some strains that were more effective than RB51 in prevention of the disease. Encapsulation of S19 or SB51 strains enhanced the potency of vaccine given orally or subcutaneously to red deer (Arenas-Gamboa et al., 2009a; Arenas-Gamboa et al., 2009b)

Paratuberculosis, or Johne’s disease

Improved laboratory techniques to detect the (Thornton et al., 2002; Ellingson et al., 2005; Huntley et al., 2005). Narnaware et al. (2016) found evidence of or Johne’s disease in 8.7% of 404 castrated male bison. Use molecular techniques have sharpened the ability to distinguish strains of M. avium subsp. Paratuberculosis and the animal species associated with specific strains (Sevilla et al., 2005; Motiwala et al., 2006; Sevilla et al., 2007; Sibley et al., 2007; Paustian et al., 2008; Sevilla et al., 2008; Herthnek, 2009; Abendano et al., 2012; Ahlstrom et al., 2016a; Ahlstrom et al., 2016b). However, Pruvot et al. (2013) pointed out limitations in using assays in species other than those used in development of the assay.

Response to strains of M.avium varies between bison and cattle (Stabel et al., 2003), and strains associated with bison have been detected in cattle (Kaur et al., 2010; Sohal et al., 2014; Ahlstrom et al., 2015). Forde et al. (2013) used analysis of bacterial strains in fecal samples to substantiate translocation of M. avium subsp. paratuberculosis among animal species and locations.

Mycoplasma

The disease caused by Mycobacterium bovis has been identified in feedlot bison (Dyer et al., 2008), cows between 5 and 10 yr old (Janardhan et al., 2010), various location in the U.S. (Dyer et al., 2013; Suleman et al., 2016a) herds of bison producers in Canada (Bras et al., 2016; Bras et al., 2017a; Bras et al., 2017b) and European bison (Krzysiak et al., 2014; Dudek et al., 2015). It also was reported in bison as a result of infection by M. caprae in a European zoo (Pate et al., 2006). (Jacob et al., 2006) found M. haemophilium in an American bison.

Enzyme-linked immunosorbent assays (ELISA) indicated detectable differences between samples from bison and cattle, but it is not clear that they are genetically distinct strains (Register et al., 2013; Register et al., 2015; Suleman et al., 2016a; Suleman et al., 2016b) and other molecular techniques link M. bovis to placentitis and abortion in bison (Register et al., 2013).

Tuberculosis

Study of archaeological evidence indicates that the disease evolved in animals before transmission to humans. (Lee et al., 2012). A review of the disease’s status in Canadian wildlife was completed by (Wobeser, 2009).

Miller and Sweeney (2013) proposed 1) commingling of infected cattle with susceptible wildlife, (2) supplemental feeding of wildlife, (3) inadequate surveillance of at-risk wildlife, and (4) unrecognized emergence of alternate wildlife species as successful maintenance hosts as the major risks factors for transmission of the disease from domesticated to wild species. The disease has been identified in several species of free-living and farmed animals in Europe (Macháčková et al., 2004; Welz et al., 2005; Schmidbauer et al., 2007) and in several animal species in Brazil (Zimpel et al., 2017). Mycobacterium bovis and B. abortus are endemic in Wood Buffalo National Park (Joly and Messier, 2004, 2005), Riding Mountain National Park (Nishi et al., 2006) Hook Lake Wood Bison Recovery (Himsworth et al., 2010a; Himsworth et al., 2010b) and Northwest Territories (Lutze-Wallace et al., 2006) in Canada. Shury et al. (2015) recommended a multistakeholder, collaborative-management approach to address the prevalence and negative consequences of the disease.

Leid et al. (2002) developed monoclonal antibodies that reacted to samples from animals known to be exposed to M. bovis and M. paratuberculosis. Harrington et al. (2007) described a whole-blood assay specific for elk,

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and suggest similar assays could be developed for other species. A definitive comparison between skin-fold tests and serological assays for the disease was not found by Chapinal et al. (2012); further comparison by the same group concluded that the skin-fold test with an animal-side serologic test increases sensitivity of disease detection (Chapinal et al., 2015).

Malignant Catarrhal Fever

Over 16 years, at least 20 studies have shown that malignant catarrhal fever in bison requires exposure to ovine herpesvirus 2. Li et al. (2014)and O'Toole and Li (2014) wrote recent reviews of progress and challenges associated with control or prevention of the disease.

There is a direct relationship between temporal and spatial interaction, contact between sheep and bison that subsequently develop the disease (Berezowski et al., 2005; Li et al., 2006a; Li et al., 2006b; Li et al., 2006c; Li et al., 2008). Although the mortality may exceed 50% of the bison exposed (Li et al., 2006a), about 23% of infected bison do not exhibit symptoms (Berezowski et al., 2005). The disease damages its victims through alterations in the victims’ immune response system (Anderson et al., 2007); susceptibility may be linked to genetic differences among bisons’ major histocompatibility system (Traul et al., 2007a; Traul et al., 2007b).

The work of Thonur et al. (2006) provides important information on how ovine herpesvirus 2 is expressed in reservoir animals (sheep) and susceptible animal species, and points to potential development of a vaccine to control or prevent malignant catarrhal fever. (AlHajri et al., 2017) provide mechanistic explanations of the structure and functions of viral glycoproteins of Ovine herpesvirus 2; that insight will contribute to eventual creation of a strategy to thwart the virus’ capacity to cause damage to host tissues.

Parasitic diseases

The bulk of the research and reports on parasites come the work with Bison bison bonasus in Europe. During the last century the recorded parasite fauna of Bison bonasus includes 88 species. These are 22 species of protozoa, 4 trematode species, 4 cestode species, 43 nematode species, 7 mites, 4 Ixodidae ticks, 1 Mallophaga species, 1 Anoplura, and 2 Hippoboscidae flies (Karbowiak et al., 2014). There are few monoxenous parasites, the majority of parasites are typical for other Bovidae and Cervidae species and many are newly acquired from Cervidae. Demiaszkiewicz (2014) concluded in their review that the relationship between bison bonasus and cervidae is a good model for studies on the influence of migration and introduction of new species on the helminthofauna of wild ruminants and the occurrence of new parasitoses.

Anaplasma

Work since 2002 has focused on use of molecular biological techniques to confirm communality among disease vectors (Anaplasma marginale and its parasitic transmitters) in bison and cattle in North America, and establish presence of A. phagocytophilum in European areas used by Bison bison bonasus (Eb). Grzeszczuk et al. (2004) used molecular techniques to constitute the first molecular evidence of infection of wild Eb and may indicate the role of these largest mammals living in a primeval forest as a natural reservoir of these bacteria. Reintroduced Eb infected with A. phagocytophilium in northern Poland (Karbowiak et al., 2016), and Eb were shown to be infected with A. phagocytophilium (Dziegiel et al., 2015). Although (Matsumoto et al., 2009) did not isolate neither A. phagocytophilum nor Rickettsia raoultii, their results confirmed the presence of A. phagocytophilum and R. raoultii in the Bialowieza Primeval Forest ecosystem and increased the list of pathogens identified in the forest.

In North America, A. marginale is biologically vectored by hard ticks (Acari: Ixodidae), Dermacentor variabilis and D. andersoni (Yunik et al., 2016). Biting flies, particularly horse flies (Diptera: Tabanidae), can also act as mechanical vectors. An outbreak of bovine anaplasmosis, consisting of 14 herds, was detected in southern Manitoba in 2008. This outbreak survived multiple rounds of testing and culling before eradication in 2011, suggesting the pathogen was being maintained locally. The researchers applied novel approaches to examine the vector ecology of this disease in this region. They did not detect A. marginale by screening of 2056 D. variabilis in 2011 and 2012 or 520 horse flies in 2011 using molecular analytical techniques. St. Maries, the

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Idaho strain of A. marginale is transmitted by Rocky Mountain wood tick to bison in U.S. and Canada (Scoles et al., 2006).

Kocan et al. (2004) used a major surface protein from A. marginale to show that isolates obtained from bison were similar to those from naturally infected bovine. 9 isolates of A. marginale from bison had the characteristic surface protein called MSP 1a. Isolates of A. marginale from North American cattle and bison were found to be similar (De La Fuente, 2003), but New world strains of Anaplasma marginale are phylogenically different than Spanish strains (De La Fuente et al., 2004). Al-Adhami et al. (2011) found serological cross-reactivity between A. marginale and Ehrlichia spp in cattle. This cross-reactivity reduces the value of serological tests for anaplasma when Ehrlichia ssp. Are present.

Nematodes

Sixteen publications since 2002 describe research into the identification and description of nematode parasites in bison. Examples of that work include Kolodziej-Sobocinska et al. (2016b), Kołodziej-Sobocińska et al. (2016a), Woodbury et al. (2012), Woodbury et al. (2014), Kuznetsov (2010), and Weiss et al. (2008). In general, the work shows extensive parasitism, particularly in animals in smaller, more concentrated environments. Anthelmintics used in other herbivores appear to be effective in bison (Woodbury and Lewis, 2011; Eljaki et al., 2016; Yamada et al., 2016).

Protozoic diseases

The etiology and prevalence of protozoal parasites of bison have been described and clarified in 21 publications since 2002. Example publications include Geurden et al. (2009), Paziewska et al. (2007), Rosenthal et al. (2008), and a series of research by Pyziel et al (Pyziel et al., 2011; Pyziel, 2012; Pyziel, 2014; Pyziel and Demiaszkiewicz, 2015). As with nematodes, there are common and prevalent, and can be spread by biting insects like horse flies. They can be treated with proper application of medicines like potassium dichromate.

Other parasites

Since 2002, there have been research reports describing disease associated with tick-borne encephalitis virus (Biernat and Karbowiak, 2014; Biernat et al., 2016), Lyme borreliosis (Bhide et al., 2005; Gutierrez-Exposito et al., 2012; Adaszek et al., 2014) enterococci (Anderson et al., 2008), and skin mites (Izdebska, 2006) ticks (Mierzejewska et al., 2015), biting midges, (Pfannenstiel and Ruder, 2015) liver flukes (Walker et al., 2013; Januszkiewicz et al., 2015) and fungus (Morrow, 2006).

Other viral diseases

Shiratori and Chase (2002)concluded from their investigations that bison are susceptible to several viral diseases common in cattle, including: bovine herpesvirus 1 (BHV-1), bovine respiratory syncytial virus (BRSV), cytopathic (CP) and noncytopathic (NCP.) bovine viral diarrhea virus (BVDV) type I and type II, and bluetongue virus (BTV). Deregt et al. (2005) isolated BVDV type I and II from bison tissues. Viruses identified in bison tissues in bovine lentiviruses (Yamada et al., 2016), bovine papillomaviruses (Literak et al., 2006; Corteggio et al., 2013) coronaviruses (Chung et al., 2011), hemorrhagic disease virus (Nol et al., 2010; Bachtold et al., 2015; Krzysiak et al., 2017) bluetongue virus (Bachtold et al., 2015; Niedbalski, 2015), foot and mouth disease (Rhyan et al., 2008) and bovine rhinotracheitis (Borchers et al., 2002). Schmallenberg virus (Tarlinton et al., 2013; Larska et al., 2014; Bachtold et al., 2015; Krzysiak et al., 2017) and BVDV (Giangaspero et al., 2006) have been isolated from bison bonasus tissues in Europe. Hepatitis E virus was not in samples from Eb (Larska et al., 2014) or found at low levels, 3 of 65 samples (Dong et al., 2011).

Other diseases and treatment

Descriptions of cases of other diseases include those related to the bacteria Trueperella pyogenes (Rzewuska et al., 2012; Rzewuska et al., 2016) and Francisella tulacensis (Bachtold et al., 2015; Krzysiak et al., 2017), and Histophilis somni (Corbeil, 2007; Zekarias et al., 2011; O'Toole and Sondgeroth, 2016). Zhao et al. (2015) and Seabury et al. (2004) reported their work on the prion protein gene. There were publications related to bovine

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spongiform encephalopathy (mad cow disease) (Hauer, 2003), malignant Schwannoma (Cho et al., 2006), posthitis or balanoposthitis in Eb (Kita et al., 2003; Lehnen et al., 2006; Anusz et al., 2007; Olenski et al., 2015), repair of a cleft palate (Minter et al., 2010), and hepatic lipidosis in bison (Palmer and Olsen, 2002).

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Stabel, J. R., M. V. Palmer, and R. H. Whitlock. 2003. Immune responses after oral inoculation of weanling bison or beef calves with a bison or cattle isolate of mycobacterium avium subsp. paratuberculosis. Journal of wildlife diseases 39(3):545-555.

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VI. Grasslands

Summary

The grasslands, or Tallgrass Prairie ecosystem is an intricate interchange among plants, animals, soil, water, fire, and air. Bison have played a key role in that ecosystem for a long time, and whether in conservation herds of domestic herds, they should be considered as a serious component of future responses to climate change.

Introduction

The reviews of Knapp et al. (1999) and Truett (2003) provide a comprehensive overview of the history and interactions of bison and the Tallgrass Prairie, elucidating plant and soil ecology in response to grazing behavior, wallowing, and death of bison. Reviews of Fuhlendorf (2001)and Truett (2003) focus on the role of bison in (re)establishment ecological diversity on grasslands. Frelich (2003) details the effects of ranching on “problem” animals, truncation of the food web, fencing, roads and fragmentation, exotic weeds and herbicides, alteration of fire regimes, and effects to water supplies and riparian areas. These authors recommend a holistic approach as conservations and ranchers work to address these issues. There have been two main thrusts, or interests in this area – the first is restoration, preservation of the Great Plains of North America, and the second is anticipation and expectations of the effect of global warming on that process.

Status of the grasslands

(Allred et al., 2013)) pointed out that in North America, bison are considered to be livestock, the vast majority of bison are privately owned, and about 90% of the former grasslands is now privately-owned rangeland, used for livestock production, cattle, sheep, goats, horses, and bison. They used The Nature Conservancy Tallgrass Prairie in Oklahoma to compare effects and responses of two main herbivores, bison and cattle. They found that bison differ from cattle in their preference for recently burned areas, for water, and for woody areas; bison will remain in the open and away from water sources longer that cattle as ambient temperatures increase, and bison prefer woody areas more than cattle. They conclude that those differences may be useful for management of future earth warming. Similarly, Bork et al. (2013) reported that wild ungulates in Canada, including bison, have a greater negative effect on aspen saplings than cattle; more damage from bison emanates from preferring wooded habitat. Reclamation of forest clear cut may provide adequate forage for bison in the summer, but not during the winter (Redburn et al., 2008). Kohl (2013) compared cattle (from the Weiderrick and Barnard ranches) with bison from the American Prairie Reserve and Grasslands National Park, in Montana and Saskatchewan, Canada; these areas are adjacent except for Grasslands NP. They Used GPS collars on female bison and cattle to track movements and location. Bison spend from 26 to 28% of the day grazing, 15 to18% standing, 46% lying, 8 to 11% moving, and 2% on other things. Cattle spend more time grazing and moving, and less time lying. The Stocking rates, measured in animal units per month, were 0.09 – 0.49 AUM/ha for cattle, and 0.11 – 0.25 AUM/ha for bison. Bison move further from water than cattle. Bison move faster than cattle. Bison spend less time grazing than cattle, in agreement with Plumb and Dodd (1993). Due to species differences in herbage selection, Plumb and Dodd (1993) and Steuter and Hidinger (1999) describe differences between bison and cattle in grazing behavior and recommend that both cattle and bison may play positive roles in future prairie management. A summary of 10 yr of research showed cover by the grass little bluestem decreased in bison pastures, and big bluestem cover increased in cattle pastures in tallgrass pastures grazed by bison vs cattle in a system that balanced annual stocking rate of 1.7 AU/ha, and included an ungrazed control that included annual burnings Towne et al. (2005). They also noted an increase in plant species richness and a dramatic increase in cover of Missouri goldenrod and annual forbs. Similarly, Van Vuren (1984) and van Vuren and Bray (1993) noted similar grazing selection by bison and cattle, but increased prevalence of forbs in pastures grazed by bison vs cattle. There is little difference in plant composition in grazed and ungrazed locations in Yellowstone National Park (Singer, 1995). Comparison of nutritional values, percentage of dry matter (DM), of grazed and ungrazed grasses found increased crude protein (9.1 vs 7.6 % of DM) and ash (1.17 vs 1.94% of DM) in grazed grasses, and no effect of grazing on in vitro digestibility (62%) or neutral detergent fiber (70% of DM).

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Among many factors affecting grassland ecology, fire and grazing are powerful partners in the effort to restore grasslands (Fuhlendorf et al., 2009). Burning, and mechanical removal of brush complement effects of grazing on rangeland quality by bison or other herbivores (Ranglack and du Toit, 2015; Ranglack et al., 2015; Raynor, 2015; Raynor et al., 2016; Raynor et al., 2017). Bison prefer to graze recently burned areas, ostensibly because the plant profile in those areas has greater nutritive value (Shaw and Carter, 1990; Wallace and Crosthwaite, 2005; Schuler et al., 2006). Burning prairie annually or every 4 yr provides a reference to ungrazed prairie in scientific assessment of fire and grazing on plant profiles and diversity (Hartnett, 1996). Grazing by bison increased frequency of indiangrass and switchgrass, but did not affect big bluestem. In both burn schedules, grazing decreased ground cover from big bluestem, and indiangrass, switchgrass and rough dropseed. Concomitantly, grazing increased cover from sideoats grama, Kentucky bluegrass and western wheatgrass. Authors conclude that the increased diversity in response to burning or grazing increases the resistance of the grassland ecosystem to stressors, like drought. Pfeiffer and Steuter (1994) studied the effect of fire and bison grazing on the plant profile for 2 yr at Niobrara Valley Preserve in the Nebraska sandhills (42.78° N, 100.03° W), and concluded that lack of burning sustained bunchgrasses, so grazing and burning reduced bunchgrass standing crop to the advantage of rhizomatous grass and forbs. That change may increase forage supply for bison, but it also increases the risk of wind erosion, and complete loss of herbage in severely affected ‘blowouts’. Introduction of bison to the Nature Conservancy Konza Prairie Biological Station (KPBS, 3,487 Ha, 39◦05’N, 96◦35’ W) stocked with 225 bison) increased plant species diversity (Collins et al., 1998) and increased total tree density (Briggs, 2002). Veach et al. (2014) concurred that fire alone will not prevent encroachment of woody vegetation. Wildfire in Alaska increased grazing area and increased availability of sedges for bison at the expense of woody shrubs and trees (Campbell, 1983). Fire also affects plant diversity, but not at the same scale as grazing by bison; bison can ‘patch graze’, exert heavy grazing pressure on an area that burned recently, thereby causing longer-term changes in quantity and nutritional quality of herbage regrowth which varies according to burning frequency, and is associated with bison preferentially grazing regrowth on burned areas (Vinton and Hartnett, 1992; Vinton, 1993; Nellis, 1997). An analysis of 22 yr of data from the KPBS showed that the effects of fire and grazing on grasslands are distinct (Spasojevic et al., 2010); grazing promoted more plant diversity than burning. Annual burning favored C4 grasses, whereas grazing promoted C3 grasses. Intermediate burning and grazing promoted relative abundance of annual C4 grasses. The authors point out the fire can be seen as a non-selective herbivore, and burning annually versus quadrennially exacerbated the negative effects of fire on plant diversity. Over a period of 8 yr, bison grazing in KPBS enhanced plant species diversity at least in part by increasing access to sunlight, access to water, and increasing N availability for some plants (Fahnestock and Knapp, 1993, 1994; Bakker, 2003). A one-year study on effects of burn frequency and five forb species showed interactions among species, burn status, and grazed/not grazed by bison (Damhoureyeh and Hartnett, 1997). The frequency and time of year of defoliation by manually clipping (to simulate grazing) affected relative growth rates and plant anatomy of 2 perennial forbs and a C4 (warm season) grass (Damhoureyeh, 2002). Regrowth of little bluestem after burning makes it preferable to big bluestem for bison, the opposite of preference in unburned areas (Pfeiffer and Hartnett, 1995).

(Coppedge et al., 1998a) completed a two-year comprehensive study of factors affecting grassland diversity on the Nature Conservancy Tallgrass Prairie Preserve (TPP) in Oklahoma (15, 342 ha, 36◦50’N, 96◦25’ W). During the study it was stocked with 300 Bison at 6 – 7 ha per bison. The relative composition of the grassland, tallgrasses (C4), little bluestem (C4), annual grasses sedges and rushes (C3), forbs, and legumes varied with burn date (fall, spring, summer), soil and topography (upland, run-in, lowland), sampling year, and sampling date (June or August). Perennial grass abundance was not affected by any of these factors. The amount of forbs increased as Bison grazing intensity increased. Conversely, the amount forb decreased as number of growing season since last burned increased; the amount of tallgrasses and sedges and rushes increased as burn interval increased (Coppedge et al., 1998b). On a dry herbage mass basis, grasses contributed most of the dry herbage mass, 38 to 87% across years and season, with sedges and forbs contributing the rest Bison selected almost all grasses (that’s what was available), particularly little bluestem, but preferred sedges and avoided forbs (Coppedge and Shaw, 1998). Bull groups selected burn sites for grazing in 4% and avoided them in 46% of the observations, selected unburned areas in 29% and avoided them in 14% of the observations.

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Mixed groups of bison selected burn sites 23% and avoided them 13% of the observations, and avoided unburned areas in 63% of the observations. Wintering bison in Yellowstone National Park preferentially grazed previously burned areas as well (Pearson et al., 1995).

As in other grasslands and herbivores across the world, bison do not graze indiscriminately; grazing patches and establishment of grazing lawns are caused by bison grazing behavior (England and Devos, 1969; Knapp, 1998) and from ant, badger and gopher mounds, prairies lowlands and ‘potholes’, bison wallows (now mostly historical artifacts, (Umbanhowar Jr, 1992), animal carcasses, and prairie dog towns (Cid et al., 1991). These effects, along with fire, cause short-term and longer-term effects on plant heterogeneity and relative abundance in grasslands, that emanate from concomitant changes in topoedaphy (terrain, soil hydration, mineralization, fungus, earthworms), physical changes to plants and soil surface, plant physiology (leaf area, root growth, CO2 sequestration, urination by bison, and N and P cycles (Gibson, 1989; Larson and Murdock, 1989; Day and Detling, 1990a, 1990b; James, 1992; Coppedge and Shaw, 1997; Frank and Evans, 1997; Knapp, 1998; Crockett and Engle, 1999; Knapp et al., 1999; McMillan et al., 2000; Towne, 2000; Kemp and Dodds, 2001; Steinauer, 2001; McMillan et al., 2011; Eby et al., 2014; Klodd et al., 2016). Bison will browse, eat woody plants, including tree bark, rather than starve (Waggoner and Hinkes, 1986; Zielke, 2017)

Regrowth of graminoids in the wet meadows of Mackenzie Bison Sanctuary (582,900 ha, 61° 30' N - 116° W) depends on accumulation of dead plant material in ungrazed areas (Smith and La Roi, 2005). Moderate grazing by Bison, or simulated grazing by manual clipping, promoted regrowth in some areas, but in others. Recovery of Bison populations in northern Canada depends on regrowth of graminoids in wet and dry meadows to provide sufficient food supply over the winter (Strong and Gates, 2009).

The array of size of herbivores and their predators affects the plant community because of selection differences are associated with animal sizes; modeling predictions indicate that a diverse predator community promotes a positive cycle by promoting high-quality plants in the long run. (Ruifrok et al., 2015).

Adaptation to climate change

Application of DNA technology, to distinguish plants eaten based on plant residues in feces, illustrates how climate affects grazing habits of bison (Craine, 2013; Craine et al., 2015). Compared with bison from Montana (47° 19′ N and 114° 13′ W), Bison from Kansas (39° 05′ N and 96° 35′ W) are 129 kg lighter, ostensibly due to the quantity and quality of ingested herbage. Over a 3-yr study, as a percentage of plant species in feces, the Kansas bison profile was 8% cool-season graminoids (C3 plants), 31% warm-season graminoids (C4 plants), 18% from non-N2-fixing forbs and 42% were from N-fixing species. The South Dakota bison profile was contained greater proportions of C3 grasses, lower proportion of N2-fixing species, and similar proportions of C4 grass and forbs. The authors conclude that the fecal profiles reflect the plant communities, and the warmer Kansas climate has a different community that yields bison that weigh less. They further predict that this serves as a harbinger of future climate changes associated with global warming. In Manitoba (12, 500 ha, 51◦47’N, 100◦30’ W, stocked with350 bison) fecal profiles of similar DNA analysis indicated 44.3% grass, 37.7% forb, 16.3% brows and the remainder sedge and rush (Leonard et al., 2017). Available forage was 51.2% grass, 28% forb. 11.0% sedge and 7,6% rush. The proportion of grass and forb shifted, however, during June, July, and August, indicating that selection of grass, forb, and rush changed during the summer in ways that reflect difference for plant composition in response to senescence or ambient conditions. The authors point out that changing preferences for plants may be to spatial limitations; bison don’t migrate or range as they did in the past, but they will choose a diet from available herbage. The diet selected by bison bulls contains more C4 plants than diets of cow or calves (Post et al., 2001; Rosas et al., 2005) so the sex ratio in herds of grazing bison could affect the grassland plant profile, at least in areas occupied by one sex or the other.

Eastman et al. (2001) flip over the scenario, and show how grazing, removal of plant material from the soil surface, changes soil temperatures and hydrology, ambient temperatures, and ultimately, regional climate conditions.

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Wilsey et al. (1997) studied effects of elevated atmospheric CO2 on grasses. They found no effect on C4 species, and small effects on C3 grasses. Increased CO2 decreased N content of Yellowstone National Park grasses. Clipping grasses responded to increased CO2 the same as unclipped grasses. Authors conclude that herbivores will affect plants through nutrient cycling rather than through direct defoliation and subsequent effects on photosynthetic capacity. Yellowstone grasses have a natural ‘rest period’ before and after summer grazing. The bottom line is no large, dramatic effects. Cotton et al. (2016) used δ13C in Cenozoic-era bison and mammoth tissues as a proxy for C4 plant contribution to their diets and concluded that atmospheric CO2 levels did not play a major role in evolution of C4 plants. After reviewing several years’ data from various locations, Craine et al (2009, 2013a, b) noted the effects of climate change, ambient temperatures and rainfall on the nutritive value of grasslands and concomitant reduction in weight gain of bison.

The grasslands, or Tallgrass Prairie ecosystem is an intricate interchange among plants, animals, soil, water, fire, and air. Bison have played a key role in that ecosystem for a long time, and whether in conservation herds or domestic herds, they should be considered as a serious component of future responses to climate change.

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Damhoureyeh, S. A. H., David C. . 2002. Variation in Grazing Tolerance among Three Tallgrass Prairie Plant Species. American Journal of Botany 89(10):1634-1643.

Day, T. A., and J. K. Detling. 1990a. Grassland patch dynamics and herbivore grazing preference following urine deposition. Ecology 71(1):180-188.

Day, T. A., and J. K. Detling. 1990b. Changes in grass leaf water relations following bison urine deposition. American Midland Naturalist 123(1):171-178.

Eastman, J. L., M. B. Coughenour, and R. A. Pielke Sr. 2001. Does grazing affect regional climate? Journal of Hydrometeorology 2(3):243-253. doi: 10.1175/1525-7541(2001)002<0243:DGARC>2.0.CO;2

Eby, S., D. E. Burkepile, R. W. Fynn, C. E. Burns, N. Govender, N. Hagenah, S. E. Koerner, K. J. Matchett, D. I. Thompson, K. R. Wilcox, S. L. Collins, K. P. Kirkman, A. K. Knapp, and M. D. Smith. 2014. Loss of a large grazer impacts savanna grassland plant communities similarly in North America and South Africa. Oecologia 175(1):293-303. doi: 10.1007/s00442-014-2895-9

England, R. E., and A. Devos. 1969. Influence of Animals on Pristine Conditions on the Canadian Grasslands. Journal of Range Management 22(2):87-94.

Fahnestock, J. T., and A. K. Knapp. 1993. Water relations and growth of tallgrass prairie forbs in response to selective grass herbivory by bison. International journal of plant sciences 154(3):432-440. doi: 10.1086/297126

Fahnestock, J. T., and A. K. Knapp. 1994. Plant responses to selective grazing by bison: Interactions between light, herbivory and water stress. Vegetatio 115(2):123-131.

Frank, D. A., and R. Evans. 1997. Effects of native grazers on grassland N cycling in Yellowstone National Park. Ecology 78(7):2238-2248.

Frelich, J. E. E., John M.; Duda, Jeffrey J.; Reeeman, D. Carl', Cafaro, Philip J. 2003. Ecological Effects of Ranching: A Six-Point Critique. Bioscience 53(8):759-765. (Journal artice)

Fuhlendorf, S. D., D. M. Engle, J. Kerby, and R. Hamilton. 2009. Pyric herbivory: rewilding landscapes through the recoupling of fire and grazing. Conservation Biology 23(3):588-598. doi: 10.1111/j.1523-1739.2008.01139.x

Fuhlendorf, S. D. E., David M. 2001. Restoring Heterogeneity on Rangelands: Ecosystem Management Based on Evolutionary Grazing Patterns We propose a paradigm that enhances heterogeneity instead of homogeneity to promote biological diversity and wildlife habitat on rangelands grazed by livestock. Bioscience 51(8):625-632.

Gibson, D. J. 1989. Effects of animal disturbance on tallgrass prairie vegetation. American Midland Naturalist 121(1):144-154.

Hartnett, D. C. H., Karen R.; Fischer Walter, Laura E. 1996. Effects of bison grazing, fire, and topography on floristic diversity in taligrass prairie. Journal of Range Management 49(5):413-420.

James, S. W. 1992. Localized dynamics of earthworm populations in relation to bison dung in north American tallgrass prairie. Soil Biology and Biochemistry 24(12):1471-1476.

Kemp, M. J., and W. K. Dodds. 2001. Spatial and temporal patterns of nitrogen concentrations in pristine and agriculturally-influenced prairie streams. Biogeochemistry 53(2):125-141. doi: 10.1023/A:1010707632340

Klodd, A. E., J. B. Nippert, Z. Ratajczak, H. Waring, and G. K. Phoenix. 2016. Tight coupling of leaf area index to canopy nitrogen and phosphorus across heterogeneous tallgrass prairie communities. Oecologia 182(3):889-898. doi: 10.1007/s00442-016-3713-3

Knapp, A. K., J. M. Blair, J. M. Briggs, S. L. Collins, D. C. Hartnett, L. C. Johnson, and E. G. Towne. 1999. The keystone role of bison in North American tallgrass prairie. Bioscience 49(1):39-50.

Knapp, A. K. C., Shawn L.;, Blair, John M. 1998. Determinants of Soil CO2 Flux from a Sub-Humid Grassland: Effect of Fire and Fire History. Ecological Applications 8(3):760-770.

Kohl, M. T. K., Paul R.; Kunkel, Kyran; Williams, David M. 2013. Bison Versus Cattle: Are They Ecologically Synonymous? Rangeland Ecology and Management 66(6):721-723.

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Larson, D. L., and G. K. Murdock. 1989. Small Bison Herd Utilization of Tallgrass Prairie Proc. 11th N. Amer. Prairie Conf (Conference Proceedings)

Leonard, J. L., L. B. Perkins, D. J. Lammers, and J. A. Jenks. 2017. Are Bison Intermediate Feeders? Unveiling Summer Diet Selection at the Northern Fringe of Historical Distribution. Rangeland Ecology & Management 70(4):405-410. doi: 10.1016/j.rama.2017.01.005

McMillan, B. R., M. R. Cottam, and D. W. Kaufman. 2000. Wallowing behavior of American bison (Bos bison) in tallgrass prairie: An examination of alternate explanations. American Midland Naturalist 144(1):159-167.

McMillan, B. R., K. A. Pfeiffer, and D. W. Kaufman. 2011. Vegetation Responses to an Animal-generated Disturbance (Bison Wallows) in Tallgrass Prairie. American Midland Naturalist 165(1):60-73.

Nellis, M. D. B., John M. 1997. Modeling Spatial Dimensions of Bison Preferences on the Konza Prairie Landscape Ecology: An Overview. Transactions Kansas Academy Science 100(1-2):3-9.

Pearson, S. M., M. G. Turner, L. L. Wallace, and W. H. Romme. 1995. Winter habitat use by large ungulates following fire in northern Yellowstone National Park. Ecological Applications 5(3):744-755.

Pfeiffer, K. E., and D. C. Hartnett. 1995. Bison selectivity and grazing response of little bluestem in tallgrass prairie. Journal of Range Management 48(1; 1):26-31.

Pfeiffer, K. E., and A. A. Steuter. 1994. Preliminary response of sandhills prairie to fire and bison grazing. Journal of Range Management 47(5):395-397.

Plumb, G. E., and J. L. Dodd. 1993. Foraging ecology of bison and cattle on a mixed prairie: implications for natural area management. Ecological applications : a publication of the Ecological Society of America 3(4; 4):631-643.

Post, D. M., T. S. Armbrust, E. A. Horne, and J. R. Goheen. 2001. Sexual segregation results in differences in content and quality of bison (Bos bison) diets. Journal of mammalogy 82(2):407-413. doi: 10.1644/1545-1542(2001)082<0407:SSRIDI>2.0.CO;2

Ranglack, D. H., and J. T. du Toit. 2015. Wild bison as ecological indicators of the effectiveness of management practices to increase forage quality on open rangeland. Ecological Indicators 56:145-151. doi: 10.1016/j.ecolind.2015.04.009

Ranglack, D. H., S. Durham, and J. T. du Toit. 2015. Competition on the range: science vs. perception in a bison-cattle conflict in the western USA. J Appl Ecol 52(2):467-474. doi: 10.1111/1365-2664.12386

Raynor, E. J., H. L. Beyer, J. M. Briggs, and A. Joern. 2017. Complex variation in habitat selection strategies among individuals driven by extrinsic factors. Ecological Applications 7(6):1802-1822. doi: 10.1002/ece3.2764

Raynor, E. J., A. Joern, J. B. Nippert, and J. M. Briggs. 2016. Foraging decisions underlying restricted space use: effects of fire and forage maturation on large herbivore nutrient uptake. Ecological Applications 6(16):5843-5853. doi: 10.1002/ece3.2304

Raynor, E. J. J., Anthony; Briggs, John M. 2015. Bison foraging responds to fire frequency in nutritionally heterogeneous grassland. Ecology 96(6):1586-1597.

Redburn, M. J., W. L. Strong, and C. C. Gates. 2008. Suitability of boreal mixedwood clearcuts as wood bison (Bison bison athabascae) foraging habitat in north-central Alberta, Canada. Forest Ecology and Management 255(7):2225-2235. doi: 10.1016/j.foreco.2007.12.033

Rosas, C. A., D. M. Engle, and J. H. Shaw. 2005. Potential ecological impact of diet selectivity and bison herd composition. Great Plains Research 15(1):3-13.

Schuler, K. L., D. M. Leslie Jr, J. H. Shaw, and E. J. Maichak. 2006. Temporal-spatial distribution of American bison (Bison bison) in a tallgrass prairie fire mosaic. Journal of mammalogy 87(3):539-544. doi: 10.1644/05-MAMM-A-115R2.1

Shaw, J. H., and T. S. Carter. 1990. Bison movements in relation to fire and seasonality. Wildlife Society Bulletin 18(4):426-430.

Singer, F. J. 1995. Effects of grazing by ungulates on upland bunchgrass communities of the northern winter range of Yellowstone National Park. Northwest Science 69(3):191-203.

Smith, D. L., and G. H. La Roi. 2005. The response of subhumid mid-boreal graminoids to grazing by wood bison. Community Ecology 6(1):39-47. doi: 10.1556/ComEc.6.2005.1.5

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Spasojevic, M. J., R. J. Aicher, G. R. Koch, E. S. Marquardt, N. Mirotchnick, T. G. Troxler, and S. L. Collins. 2010. Fire and grazing in a mesic tallgrass prairie: impacts on plant species and functional traits. Ecology 91(6):1651-1659.

Steinauer, E. M. C., Scott L. 2001. Feedback Loops in Ecological Hierarchies Following Urine Deposition in Tallgrass Prairie. Ecology 82(5):1319-1329.

Steuter, A. A., and L. Hidinger. 1999. Comparative ecology of bison and cattle on mixed-grass prairie. Great Plains Research 9(2):329-342.

Strong, W. L., and C. C. Gates. 2009. Wood bison population recovery and forage availability in northwestern Canada. Journal of environmental management 90(1):434-440.

Towne, E. G. 2000. Prairie vegetation and soil nutrient responses to ungulate carcasses. Oecologia 122(2):232-239. doi: 10.1007/PL00008851

Towne, E. G., D. C. Hartnett, and R. C. Cochran. 2005. Vegetation trends in tallgrass prairie from bison and cattle grazing. Ecological Applications 15(5):1550-1559.

Truett, J. C. 2003. Migrations of grassland communities and grazing philosophies in the Great Plains: A review and implications for management. Great Plains Research 13(1):3-26.

Umbanhowar Jr, C. E. 1992. Abundance, vegetation, and environment of four patch types in a northern mixed prairie. Canadian Journal of Botany 70(2):277-284.

Van Vuren, D. H. 1984. Summer Diets of Bison and Cattle in Southern Utah. Journal of Range Management 37(3):260-261. (Journal Article)

van Vuren, D. H., and M. P. Bray. 1993. Diets of Bison and Cattle on a Seeded Range in Southern Utah. Journal of Range Management 36(4):499-500. (Journal Article)

Veach, A. M., W. K. Dodds, and A. Skibbe. 2014. Fire and grazing influences on rates of riparian woody plant expansion along grassland streams. PLoS One 9(9):e106922. doi: 10.1371/journal.pone.0106922

Vinton, M. A., and D. C. Hartnett. 1992. Effects of bison grazing on Andropogon gerardii and Panicum virgatum in burned and unburned tallgrass paririe. Oecologia 90(3):374-382. doi: 10.1007/BF00317694

Vinton, M. A. D. C. H., David C.; Finck, Elmer J.; Briggs, John M. 1993. Interactive Effects of Fire, Bison (Bison bison) Grazing and Plant Community Composition in Tallgrass Prairie. American Midland Naturalist 29(1):10-18.

Waggoner, V., and M. Hinkes. 1986. Summer and fall browse utilization by an Alaskan bison herd. Journal of Wildlife Management 50(2):322-324.

Wallace, L. L., and K. A. Crosthwaite. 2005. The effect of fire spatial scale on Bison grazing intensity. Landscape Ecology 20(3):337-349. doi: 10.1007/s10980-005-5648-7

Wilsey, B. J., J. S. Coleman, and S. J. McNaughton. 1997. Effects of elevated CO2 and defoliation on grasses: A comparative ecosystem approach. Ecological Applications 7(3):844-853.

Zielke, L. W.-M., Nicole ; Müller, Jürgen. 2017. Seasonal preferences in diet selection of semi-free ranging European bison (Bison bonasus). European Bison Conservation Newsletter 10:61-70.

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VII. Meat and other products

Slightly over 100 publications are available on the topic of bison meat and other products. Over half were on topic of carcass traits (22%) and meat quality and composition (35%). Marketing was the topic for 16% of the publications, and human health benefits or risk 14%. Hides and fiber (hair) and cooking and meat preparation accounted for 9% and 4%, respectively. Carcass yield and value were discussed by Throlson (1985), Hawley (1986), Koch et al. (1995), Patterson (2003), Gill et al. (2000), and Gill and Badoni (2010). Nutrient composition bison meat has been quantified, with attention to amino acids, vitamins and lipid fractions (Wilbur, 1955; Koch et al., 1995; Lakritz et al., 1998; Helbig and Galbraith, 2005; Helbig, 2006; Woodbury, 2006; Kerr et al., 2013; Galbraith et al., 2014; Turner et al., 2014). Food safety has been discussed from the consumer perspective (Li et al., 2004; Helbig and Galbraith, 2005; Li and Logue, 2005; Helbig, 2006; Li et al., 2006; Li et al., 2007a, b; Oloya et al., 2007; Reinstein et al., 2007; Oloya et al., 2009; Galbraith et al., 2014), as have cooking techniques with an eye to acceptability and preferences of consumers (Deerthardt, 1980; Dhanda et al., 2002). Quinto et al. (2016b) explains use of DNA coding to verify meat source; there is a technical correction to that paper (Quinto et al., 2016a). Buffalo hides are an important product (Warren, 2004) as well as skulls (Anonymous, 1990) and bison fur (Grant, 1986). Finally aspects of marketing have been discussed by Torok et al. (1998) and Yang and Woods (2013).

Literature Cited

Anonymous. 1990. Skull cleaning Buffalo! No. 18. Deerthardt, D. 1980. The Best of Bison Cooking recipes The Best of Bison. Dhanda, J. S., R. B. Pegg, J. A. M. Janz, J. L. Aalhus, and P. J. Shand. 2002. Palatability of bison

semimembranosus and effects of marination. Meat Science 62(1):19-26. doi: 10.1016/S0309-1740(01)00222-4

Galbraith, J., A. Rodas-Gonzalez, O. Lopez-Campos, M. Juarez, and J. Aalhus. 2014. Bison meat: Characteristics, challenges, and opportunities. Animal Frontiers 4(4):68-73. doi: 10.2527/af.2014-0036

Gill, C. O., and M. Badoni. 2010. Effects of experience with swabbing procedures on the numbers of bacteria recovered from carcasses by swabbing with sponges. J Food Prot 73(4):747-751.

Gill, C. O., T. Jones, J. Bryant, and D. A. Brereton. 2000. The microbiological conditions of the carcasses of six species after dressing at a small abattoir. Food Microbiology 17(2):233-239. doi: 10.1006/fmic.1999.0303

Grant, D. 1986. Prairie Cashmere - buffalo fur Buffalo! No. 14. p 8. Helbig, L. 2006. Establishing nutrient composition for Organ Meats of Elk and Bison. Smoke Signals (Fall):32-33. Helbig, L., and J. Galbraith. 2005. Nutrient Composition of Retail Cuts of Bison Smoke Signals. p 14-15. S.G.

Bennett, Winnipeg, MB. Kerr, K. R., A. N. Beloshapka, C. L. Morris, C. M. Parsons, S. L. Burke, P. L. Utterback, and K. S. Swanson. 2013.

Evaluation of four raw meat diets using domestic cats, captive exotic felids, and cecectomized roosters. J Anim Sci 91(1):225-237. doi: 10.2527/jas.2011-4835

Koch, R. M., H. G. Jung, J. D. Crouse, V. H. Varel, and L. V. Cundiff. 1995. Growth, digestive capability, carcass, and meat characteristics of Bison bison, Bos taurus, and Bos x Bison. Journal of animal science 73(5):1271-1281.

Lakritz, L., J. B. Fox, and D. W. Thayer. 1998. Thiamin, riboflavin, and α-tocopherol content of exotic meats and loss due to gamma radiation. Journal of food protection 61(12):1681-1683.

Li, Q., and C. M. Logue. 2005. The growth and survival of Escherichia coli O157:H7 on minced bison and pieces of bison meat stored at 5 and 10°C. Food Microbiology 22:415-421.

Li, Q., J. S. Sherwood, and C. M. Logue. 2004. The prevalence of Listeria, Salmonella, Escherichia coli and E. coli O157:H7 on bison carcasses during processing. Food Microbiology 21:791-799.

Li, Q., J. S. Sherwood, and C. M. Logue. 2007a. Antimicrobial resistance of Listeria spp. recovered from processed bison. Letters in applied microbiology 44(1):86-91. doi: 10.1111/j.1472-765X.2006.02027.x

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Li, Q., J. S. Sherwood, and C. M. Logue. 2007b. Characterization of antimicrobial resistant Escherichia coli isolated from processed bison carcasses. Journal of applied microbiology 103(6):2361-2369. doi: 10.1111/j.1365-2672.2007.03470.x

Li, Q., J. A. Skyberg, M. K. Fakhr, J. S. Sherwood, L. K. Nolan, and C. M. Logue. 2006. Antimicrobial susceptibility and characterization of Salmonella isolates from processed bison carcasses. Appl Environ Microbiol 72(4):3046-3049. doi: 10.1128/AEM.72.4.3046-3049.2006

Oloya, J., D. Doetkott, and M. L. Khaitsa. 2009. Antimicrobial drug resistance and molecular characterization of salmonella isolated from domestic animals, humans, and meat products. Foodborne Pathogens and Disease 6(3):273-284. doi: 10.1089/fpd.2008.0134

Oloya, J., M. Theis, D. Doetkott, N. Dyer, P. Gibbs, and M. L. Khaitsa. 2007. Evaluation of Salmonella occurrence in domestic animals and humans in North Dakota (2000-2005). Foodborne Pathogens and Disease 4(4):551-563. doi: 10.1089/fpd.2007.0014

Patterson, M. 2003. Estimated Revenue From a Prime Bison Bull Carcass SaskBISONews. p 5-6. Saskatchewan Bison Association, Regina, SK.

Quinto, C. A., R. Tinoco, and R. S. Hellberg. 2016a. Corrigendum to “DNA barcoding reveals mislabeling of game meat species on the U.S. commercial market” [Food Control 59 (2015) 386–392]. Food Control 63doi: 10.1016/j.foodcont.2015.12.005

Quinto, C. A., R. Tinoco, and R. S. Hellberg. 2016b. DNA barcoding reveals mislabeling of game meat species on the U.S. commercial market. Food Control 59:386-392. doi: 10.1016/j.foodcont.2015.05.043

Reinstein, S., J. T. Fox, X. Shi, M. J. Alam, and T. G. Nagaraja. 2007. Prevalence of Escherichia coli O157:H7 in the American bison (Bison bison). Journal of food protection 70(11):2555-2560.

Throlson, K. 1985. Doc Ken's Korner carcasses Buffalo! No. 14. p 20. Torok, S. J., K. Tatsch, E. Bradley, J. Mittelstaedt, and G. J. May. 1998. Identification of bison consumer

characteristic dimensions and restaurant marketing strategies. Agribusiness : an international journal 14(1; 1):33-48.

Turner, T. D., J. L. Pilfold, J. Jensen, D. Prema, K. K. Donkor, J. D. Van Hamme, B. Cinel, J. K. Galbraith, and J. S. Church. 2014. Fatty Acid Profiles of Western Canadian Bison (Bison bison) Meat. Journal of Food Research 3(6)doi: 10.5539/jfr.v3n6p146

Warren, J. 2004. Hide front Smoke Signals. Wilbur, C. G. a. G., Theodore W. . 1955. The lipids in Bison bison. Journal of mammalogy 36(2):305-305.

(Journal article ) Woodbury, M. 2006. Forage Diets Produce Healthier Meat Smoke Signals. p 32-33. S.G. Bennet Marketing

Services, Winnipeg, MB. Yang, J. C., and T. A. Woods. 2013. Assessing Consumer Willingness to Pay for Ground Bison Given Nutrition

Information. In: Southern Agricultural Economics Association Annual Meeting, Orlando, FL

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VIII. Management

Of the 284 publications that dealt with management, 63 addressed diseases (Nishi et al., 2002; Olsen et al., 2002; Lewis, 2003; Nishi et al., 2006; Woerner, 2011; Woodbury, 2012; Shury et al., 2015; Taxis, 2016; Woodbury, 2017), 27 discussed feeding and nutrition (Hauer, 1999; Feist, 2000a; Hauer, 2001, 2002b; Anderson, 2006; Klein, 2009; Klemm, 2009; Patterson, 2012, 2015), 26 addressed genetics, breeding and reproduction (Anonymous, 1985; Reynolds, 1985; Maher and Byers, 1987; Throlson, 1987; Brown, 2001; Hauer, 2002a; Mooring et al., 2006), and 9 addressed animal welfare or animal care (Bornett-Gauci et al., 2006; Lewis, 2010). Other topics include fencing (Anonymous, 1986; Cummings, 1986; Duvall, 1988; Lee, 1990; Scott, 1992; Boos, 1999; Anonymous, 2013, 2014; Kossler, 2015), animal handling equipment (Harasawa, 1985; Patterson, 2001, 2002, 2003; Johnson, 2011; Woerner, 2012), annual activity calendars (Hauer, 2000; Lewis, 2000), and descriptions of bison farms (Errington, 1985; Anonymous, 1988; Lee, 1988; Dawson and Dawson, 1989; Shepherd et al., 1989).

About 60% of management publications came from trade magazines, like Smoke Signals, the Tracker, SaskBISONews, Buffalo! or Bison World, or experiment station research updates and reports. Thirty-five were published in the last 5 years, and 58 since 2010. The reviews of Woodbury (2002) of health care and of Anderson (2000) and Feist (Feist, 2000b, a) of feeding management are relevant to today’s production systems. Although the dollar values numbers are outdated, Metzger (2000) and Metzger (2001) have valid rationale and procedures for economic analysis of bison production that can be applied using current dollar values.

Literature Cited

Woodbury, M. 2000 Diseases of Bison. Available at (http://www.usask.ca/wcvm/herdmed/specialstock/bison/bisondis.html)

Anderson, V. 2000. Perspectives on Nutritional Management of Bison Bulls Fed for Meat, NDSU, Carrington Research Extension Center.

Anderson, V., Feist, M. 2006. Feeding systems Smoke Signals. Anonymous. 1985. Breeding for maximum profits Buffalo! No. 13. Anonymous. 1986. <Tensilewirefencing.pdf> Buffalo! No. 14. p 29. Anonymous. 1988. Ranch Review: Durham Ranches, Inc. Buffalo! No. 16. p 8-10. Anonymous. 2013. A long-lasting fence begins with proper installation Bison World No. Oct Nov Dec. Anonymous. 2014. A long-lasting fence begins with proper installation - Part II Bison World No. Jan Feb March. Boos, R. 1999. how-build-better-fence Smoke Signals. p 88-89. Bornett-Gauci, H. L. I., J. E. Martin, and D. R. Arney. 2006. The welfare of low-volume farm animals during

transport and at slaughter: A review of current knowledge and recommendations for future research. Animal Welfare 15(3):299-308.

Brown, D. O. 2001. Breeding Soundness Evaluation The Tracker No. 5. p 80. Tracker Publications Inc, Alder Flats, AB.

Cummings, J. 1986. "Hevy" Fences Buffalo! No. 14. p 18-20. Dawson, W., and R. Dawson. 1989. Randh Review: Thistlewood Farm Buffalo! No. 17. p 6-7. Duvall, M. 1988. Buffalo beliefs and behaviors Buffalo! 16(4):9-11. Errington, J. 1985. How we manage 88 sections and 3000 head of buffalo Buffalo! No. 13. p 15-17. Feist, M. 2000a. Basic nutrition of bison Part 2 Smoke Signals No. XI. Feist, M. 2000b. Basic nutrition Part 1 Smoke Signals No. IX. Harasawa, R. 1985. Deciding what type of equiment to put into the corral. Buffalo! 13(4):6-7. Hauer, G. 1999. Selenium The Tracker No. 3. p 6 & 8. Cat Tail Publishing Ltd., Sylvan Lake, AB. Hauer, G. 2000. Bison Calendar The Tracker No. 4. p 6 & 8. Cat Tail Publishing Ltd., Sylvan Lake, AB. Hauer, G. 2001. Winter Feeding for Bison The Tracker No. 5. p 8-9. Tracker Publications Inc, Alder Flats, AB. Hauer, G. 2002a. Feeding Fertility The Tracker No. 6. p 23-24. Tracker Publications, Regina, SK. Hauer, G. 2002b. Nitrate Poisoning The Tracker No. 6. p 38-39. Tracker Publications, Regina, SK.

http://www.usask.ca/wcvm/herdmed/specialstock/bison/bisondis.html

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Johnson, J. 2011. Bison management tip Bison World No. Jan Feb Mar. Klein, L. 2009. Bale Grazing- Can it work with Bison? Smoke Signals. p 30-31. S.G. Bennet Marketing Services,

Winnipeg, MB. Klemm, K. 2009. Finishing bison with grass Bison World No. Jan Feb Mar. Kossler, J. R., J.; Handyside, P. 2015. Fencing for livestock and wildlife on Blue Valley Ranch Bison World No.

Apr May June. Lee, P. F. 1988. Ranch Reviews: Lee Buffalo Farms. Buffalo! 16(4):30-31. Lee, P. F. 1990. High Tensile Fencing Buffalo! No. 18. p 27-30. Lewis, R. 2000. Bison production calendar Smoke Signals. Lewis, R. 2003. Are We Processing & Vaccinating Bison (Buffalo) Too Much? Smoke Signals No. 9. p 29-30.

Canadian Bison Association, Morden, MB. Lewis, R. 2010. New scoop on bison poop parasite control Smoke Signals. Maher, C. R., and J. A. Byers. 1987. Age-related changes in reproductive effort of male bison. Behavioral

Ecology and Sociobiology 21(2):91-96. doi: 10.1007/BF00553178 Metzger, S. 2000. Bison for Fun or Profit?, NDSU, Carrington Research Extension Center Metzger, S. 2001. Bison Cow-Calf Cash Flow Projections, North Dakota State University, Carrington Research

Extension Center. Mooring, M. S., M. L. Patton, D. D. Reisig, E. R. Osborne, A. L. Kanallakan, and S. M. Aubery. 2006. Sexually

dimorphic grooming in bison: the influence of body size, activity budget and androgens. Animal Behaviour 72(3):737-745. doi: 10.1016/j.anbehav.2006.02.006

Nishi, J. S., D. C. Dragon, B. T. Elkin, J. Mitchell, T. R. Ellsworth, and M. E. Hugh-Jones. 2002. Emergency response planning for anthrax outbreaks in bison herds of northern Canada: A balance between policy and science No. 969. p 245-250.

Nishi, J. S., T. Shury, and B. T. Elkin. 2006. Wildlife reservoirs for bovine tuberculosis (Mycobacterium bovis) in Canada: Strategies for management and research. Veterinary Microbiology 112(2-4 SPEC. ISS.):325-338. doi: 10.1016/j.vetmic.2005.11.013

Olsen, S. C., T. J. Kreeger, and W. Schultz. 2002. Immune responses of bison to ballistic or hand vaccination with Brucella abortus strain RB51. Journal of wildlife diseases 38(4):738-745.

Patterson, M. 2001. Bison Behavioral Management and Handling Facilites Design SaskBISONews. p 5-7. Saskatchewan Bison Association, Regina, SK.

Patterson, M. 2002. Bison Behavioral Management and Handling Facilities Design- Part 3 SaskBISONews. p 6-7. Saskatchewan Bison Association, Regina, SK.

Patterson, M. 2003. Bison Behavioral Management and Handling Facilities Design- Part 5 SaskBISONews. p 3-4 & 9-11. Saskatchewan Bison Association, Regina, SK.

Patterson, M. 2012. Nutritional preparation for weaning - Part IV Bison World No. July Aug Sept. Patterson, M. 2015. Minimize winter feed cost Bison World No. Apr May June. Reynolds, D. 1985. Opportunities in managing closed herds Buffalo! No. 13. p 17. Scott, M. D. 1992. Buck-and-Pole Fence Crossings by 4 Ungulate Species. Wildlife Society Bulletin 20(2):204-

210. Shepherd, D., J. Shepherd, j. Shepherd, and E. Shepherd. 1989. Ranch review: Shepherd Farms Buffalo! No. 17.

p 20-21. Shury, T. K., J. S. Nishi, B. T. Elkin, and G. A. Wobeser. 2015. Tuberculosis and Brucellosis in Wood Bison (Bison

Bison Athabascae) in Northern Canada: A Renewed Need to Develop Options for Future Management. Journal of wildlife diseases 51(3):543-554. doi: 10.7589/2014-06-167

Taxis, T. 2016. Might probiotics for bison be around the corner? Bison World No. Oct Nov Dec. Throlson, K. 1987. Buffalo bulls: Part 1 - Inbreeding Buffalo! No. 15. p 19. Woerner, D. 2011. How to develop a biosecurity plan for the bison operation Bison World No. Oct Nov Dec. Woerner, D. 2012. The bison lifestyle Bison World No. Oct Nov Dec. Woodbury, M. 2012. Tropical parasites Bison World No. July Aug Sep. Woodbury, M. 2017. The real dirt on diatomaceous earth Bison World No. Jan Feb March.

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IX. Theses and dissertations

The database contains 23 theses or dissertations of students investigating various aspects of bison. Subjects studied include archaeology and phylogeny (Leyden, 2007; Sutton, 2007), feeding and management(Rutley, 1998; Bergman, 2016) , grasslands and grazing behavior (Kerby, 2000; Connacher, 2012; Raynor, 2015), reproductive biology and behavior (Olthen, 1997; Helbig, 2005; Klein, 2016), establishment and management of herds (Fuller, 2006; Ecoffey, 2009; Raymond, 2010), disease (Berezowski, 2003; Seabury, 2004; Herman, 2016), and bison meat (Heitschmidt, 2012).

Much of the information in these documents has been published in scientific journal or trade magazines. The value of perusing these students’ graduate work is to gain insight into the rationale of the work, and more detail on interpretation and application of what the students found in their research.

Literature Cited

Berezowski, J. A. 2003. The Epidemiology of Malignant Catarrhal Fever Viruses in Bison, University of Saskatchewan.

Bergman, G. T. 2016. Diet, gut microbiota, and management of American bison (Bison bison) in conservaton and commercial hers of the great plains, University of Colorado

Connacher. 2012. The effects of grazing (bison and elk) and burning on biodiveristy of hemiptera (Heteroptera: Homoptera: Auchenorrhyncha) at Prairie State Park, Missouri, University of Central Missouri.

Ecoffey, T. 2009. Reintroduction of Bison (Bison bison) on Reservations in South Dakota: Four Cases, South Dakota State University.

Fuller, J. A. 2006. Populationdemography of the Yellowstone National Park bison herds, MONTANA STATE UNIVERSITY.

Heitschmidt. 2012. Quality attributes of ready-to-eat bison meat snack during 40° C accelerated storage KANSAS STATE UNIVERSITY.

Helbig, L. 2005. Onset of Puberty and Seasonal Fertility in Bison Bulls, University of Saskatchewan. Herman. 2016. Genetic natural resistance to burcellosis in Yellowstone National Park bison (Bison bison): a

preliminary assessment, Colorado State University. Kerby, J. 2000. Patch-level foraging behavior of bison and cattle on tallgrass prairie, Oregon State University. Klein, K. 2016. Maternal expenditure in American bison (Bison bison) : The influence of population density and

offspring sex, Hoftstra. Leyden, J. J. 2007. Paleoecology of Southeastern Saskatchewan Bison : Changes in Diet and Environment as

Inferred Through Stable Isotope Analysis. MS(Web Page) Olthen. 1997. Reproductive endocrinology of wood bison during estrus synchronization, supovulation and

pregnancy, The University of Guelph. Raymond, R. 2010. Montana bison: controversy in Yellowstone National Park, Humboldt State University. Raynor, E. J. 2015. Ecological hierarchy of foraging in a large hervivoe: the plains bison perspective in tallgrass

prairie, KANSAS STATE UNIVERSITY. Rutley, B. D. 1998. Management, growth and performance of bison (Bison bison) on seasonal pastures,

University of Alberta. Seabury, C. M. 2004. GENETIC EVALUATION OF THE OVINE AND BOVINE PRION PROTEIN GENES (PRNP), Texas

A&M. Sutton, H. A. 2007. Faunal Analysis of the Tongue River Bison Kill Site (24RB2135) in Southeastern Montana.

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X. Anthropology, Archaeology, and Phylogeny

Of the slightly fewer than 200 publications in this category, 20% were published since 2010, 50% dealt with some aspect of phylogeny (origin and derivation of bison species), and 32% focused human interaction in prehistoric times up to the 1800’s.

XI. Bison in Parks

Almost all of these 113 citations have been cited elsewhere, except for a few that have a political or ecological theme, dealing with the politics of national parks and their users and neighbors.

XII. Bison Bonasus

There are 246 publications in this category, some of which have been cited in relevant areas to provide contrast or otherwise unavailable information. Two things that stand out for me in this section are 1) the bison appear to be particularly afflicted by diseases and inbreeding, and 2) many of the publication lack scientific merit due to treatment of animals, or lack of robust experimental design and analysis. However, few if any researchers have spent more time and effort than Januz Gill on understanding the biology of bison.

complete review of bison research · bison bonasus anthrax growth and development bison in parks...

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